**The Importance of Large Trees in Shrine Forests for the Conservation of Epiphytic Bryophytes in Urban Areas**

Yoshitaka Oishi and Keizo Tabata

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59074

## **1. Introduction**

### **1.1. Shrine forests**

Shrines in Japan are often surrounded by forests known as *chinju-no-mori* (shrine forests; Figure 1). Previous studies have shown that shrine forests contribute to the conservation of biodiver‐ sity, particularly in urban areas where green area is severely limited, although these forests are often fragmented by the city matrix. For example, shrine forests promote the diversity of birds [1, 2], trees [3], grasses [4], and ferns [5]. These forests can thus be regarded as important for biodiversity in urban areas.

### **1.2. Bryophytes in shrine forests**

Shrine forests are also important habitats for bryophytes in urban areas [6-10]. Oishi [8] found approximately 30–60 epiphytic bryophyte species, including endangered species, on tree bark in several shrine forests.

Bryophytes are unique among plants in that they lack vascular bundles and cuticle layers on their leaves (Figure 2); they absorb water and nutrients through their leaf surfaces instead of through roots [11]. This character allows bryophytes to grow on tree bark where soils are scarce; some bryophytes strongly prefer to grow on tree bark [10]. Thus, tree bark is an important habitat for bryophytes.

© 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2014 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and eproduction in any medium, provided the original work is properly cited.

**in Urban Areas**

Japan

Japan

**Introduction Shrine forests**

in urban areas.

**Bryophytes in shrine forests**

important habitat for bryophytes.

Right: Enlarged view of the shrine forest

List of authors and their affiliations

Yoshitaka Oishi1 and Keizo Tabata2

<sup>2</sup> Faculty of Agriculture, Kinki University

1Department of Forest Science, Faculty of Agriculture, Shinshu University

**The Importance of Large Trees in Shrine Forests for the Conservation of Epiphytic Bryophytes**

Shrines in Japan are often surrounded by forests known as *chinju-no-mori* (shrine forests; Figure 1). Previous studies have shown that shrine forests contribute to the conservation of biodiversity, particularly in urban areas where green area is severely limited, although these forests are often fragmented by the city matrix. For example, shrine forests promote the diversity of birds [1, 2], trees [3], grasses [4], and ferns [5]. These forests can thus be regarded as important for biodiversity

Shrine forests are also important habitats for bryophytes in urban areas [6-10]. Oishi [8] found approximately 30–60

Bryophytes are unique among plants in that they lack vascular bundles and cuticle layers on their leaves (Figure 2); they

grow on tree bark where soils are scarce; some bryophytes strongly prefer to grow on tree bark [10]. Thus, tree bark is an

epiphytic bryophyte species, including endangered species, on tree bark in several shrine forests.

Figure 1. Shrine forests Left: Nakaragi shrine and its shrine forest, Kyoto prefecture **Figure 1.** Shrine forests: Left: Nakaragi shrine and its shrine forest, Kyoto prefecture; Right: Enlarged view of the shrine forest

As the leaf section shows, the body structure of bryophytes is very simple and lacks vascular bundles. **Figure 2.** *Plagiomnium actum* (left) and a leaf section (right). As the leaf section shows, the body structure of bryophytes is very simple and lacks vascular bundles.

species richness in fragmented forests is strongly affected by patch size and maintenance. In fragmented forests, the forest

#### Several studies have examined epiphytic bryophytes in fragmented forests, including shrine forests. Oishi [8] showed that **1.3. Environmental factors for bryophytes in shrine forests**

Figure 2. *Plagiomnium actum* (left) and a leaf section (right)

**Environmental factors for bryophytes in shrine forests**

**Objective**

**Methods Study site**

edge dries more quickly because of its greater exposure to strong wind and light intensity (edge effects); therefore, patch size is closely connected with drought stress [12-13], which impacts bryophyte diversity [8]. This drought stress causes severe damage to species vulnerable to desiccation, such as bryophytes on tree bases [8-9]. In another study, Hylander et al. [14] found that bryophytes on convex forms (e.g., logs, tree bases, and mesic ground) are more vulnerable to desiccation than those on concave forms. Conversely, some bryophytes prefer to grow at sunny sites. For these species, maintenance such as tree cutting or trimming is necessary to increase light intensity in the forest interior [8]. Previous studies [6-10] have partly revealed the effects of environmental conditions on bryophytes; however, the effects of forest structure on these species have not been sufficiently addressed. Several studies have examined epiphytic bryophytes in fragmented forests, including shrine forests. Oishi [8] showed that species richness in fragmented forests is strongly affected by patch size and maintenance. In fragmented forests, the forest edge dries more quickly because of its greater exposure to strong wind and light intensity (edge effects); therefore, patch size is closely connected with drought stress [12-13], which impacts bryophyte diversity [8]. This drought stress causes severe damage to species vulnerable to desiccation, such as bryophytes on tree bases [8-9]. In another study, Hylander et al. [14] found that bryophytes on convex forms (e.g., logs, tree bases, and mesic ground) are more vulnerable to desiccation than those on concave forms.

To understand the relationship between forest structure and bryophyte diversity, we focused on the diameter at breast height (DBH) of trees in shrine forests for the following reasons. First, large trees in shrine forests are often regarded as sacred and are preferentially preserved. Second, DBH is deeply related to bryophyte diversity because the nature of tree Conversely, some bryophytes prefer to grow at sunny sites. For these species, maintenance such as tree cutting or trimming is necessary to increase light intensity in the forest interior [8]. Previous studies [6-10] have partly revealed the effects of environmental conditions on

bark changes with DBH, thereby impacting bryophyte diversity [15-18]. Therefore, revealing the relationship between DBH

In this study, we examined the role of shrine forests in the conservation of epiphytic bryophytes. Based on our results, we

The study was conducted at a shrine forest of the Shimogamo Shrine, Kyoto, Japan (Figure 3). This shrine may have been

"Tadasu-no-mori" and covers approximately 12.4 ha. One of the dominant trees is *Aphananthe aspera* (Thunb.) Planch, of which the forest contains more than 300 individuals. However, the numbers of *Celtis sinensis* Pers. and *Cinnamomum* 

and epiphytic bryophyte diversity is useful for understanding the effects of shrine forests on these species.

founded before 8th century [19] and is designated a World Heritage Site. The shrine forest is known as the

discuss the effective conservation methods for epiphytic bryophytes in fragmented forests.

bryophytes; however, the effects of forest structure on these species have not been sufficiently addressed.

To understand the relationship between forest structure and bryophyte diversity, we focused on the diameter at breast height (DBH) of trees in shrine forests for the following reasons. First, large trees in shrine forests are often regarded as sacred and are preferentially preserved. Second, DBH is deeply related to bryophyte diversity because the nature of tree bark changes with DBH, thereby impacting bryophyte diversity [15-18]. Therefore, revealing the relation‐ ship between DBH and epiphytic bryophyte diversity is useful for understanding the effects of shrine forests on these species.

## **2. Objective**

**The Importance of Large Trees in Shrine Forests for the Conservation of Epiphytic Bryophytes**

Shrines in Japan are often surrounded by forests known as *chinju-no-mori* (shrine forests; Figure 1). Previous studies have shown that shrine forests contribute to the conservation of biodiversity, particularly in urban areas where green area is severely limited, although these forests are often fragmented by the city matrix. For example, shrine forests promote the diversity of birds [1, 2], trees [3], grasses [4], and ferns [5]. These forests can thus be regarded as important for biodiversity

Shrine forests are also important habitats for bryophytes in urban areas [6-10]. Oishi [8] found approximately 30–60

Bryophytes are unique among plants in that they lack vascular bundles and cuticle layers on their leaves (Figure 2); they absorb water and nutrients through their leaf surfaces instead of through roots [11]. This character allows bryophytes to grow on tree bark where soils are scarce; some bryophytes strongly prefer to grow on tree bark [10]. Thus, tree bark is an

Left: Nakaragi shrine and its shrine forest, Kyoto prefecture **Figure 1.** Shrine forests: Left: Nakaragi shrine and its shrine forest, Kyoto prefecture; Right: Enlarged view of the

As the leaf section shows, the body structure of bryophytes is very simple and lacks vascular bundles.

Several studies have examined epiphytic bryophytes in fragmented forests, including shrine forests. Oishi [8] showed that species richness in fragmented forests is strongly affected by patch size and maintenance. In fragmented forests, the forest edge dries more quickly because of its greater exposure to strong wind and light intensity (edge effects); therefore, patch size is closely connected with drought stress [12-13], which impacts bryophyte diversity [8]. This drought stress causes severe damage to species vulnerable to desiccation, such as bryophytes on tree bases [8-9]. In another study, Hylander et

Several studies have examined epiphytic bryophytes in fragmented forests, including shrine forests. Oishi [8] showed that species richness in fragmented forests is strongly affected by patch size and maintenance. In fragmented forests, the forest edge dries more quickly because of its greater exposure to strong wind and light intensity (edge effects); therefore, patch size is closely connected with drought stress [12-13], which impacts bryophyte diversity [8]. This drought stress causes severe damage to species vulnerable to desiccation, such as bryophytes on tree bases [8-9]. In another study, Hylander et al. [14] found that bryophytes on convex forms (e.g., logs, tree bases, and mesic ground) are more vulnerable to desiccation than those

**Figure 2.** *Plagiomnium actum* (left) and a leaf section (right). As the leaf section shows, the body structure of bryophytes

al. [14] found that bryophytes on convex forms (e.g., logs, tree bases, and mesic ground) are more vulnerable to

Conversely, some bryophytes prefer to grow at sunny sites. For these species, maintenance such as tree cutting or trimming is necessary to increase light intensity in the forest interior [8]. Previous studies [6-10] have partly revealed the effects of environmental conditions on bryophytes; however, the effects of forest structure on these species have not been

To understand the relationship between forest structure and bryophyte diversity, we focused on the diameter at breast height (DBH) of trees in shrine forests for the following reasons. First, large trees in shrine forests are often regarded as sacred and are preferentially preserved. Second, DBH is deeply related to bryophyte diversity because the nature of tree bark changes with DBH, thereby impacting bryophyte diversity [15-18]. Therefore, revealing the relationship between DBH

Conversely, some bryophytes prefer to grow at sunny sites. For these species, maintenance such as tree cutting or trimming is necessary to increase light intensity in the forest interior [8]. Previous studies [6-10] have partly revealed the effects of environmental conditions on

In this study, we examined the role of shrine forests in the conservation of epiphytic bryophytes. Based on our results, we

The study was conducted at a shrine forest of the Shimogamo Shrine, Kyoto, Japan (Figure 3). This shrine may have been

"Tadasu-no-mori" and covers approximately 12.4 ha. One of the dominant trees is *Aphananthe aspera* (Thunb.) Planch, of which the forest contains more than 300 individuals. However, the numbers of *Celtis sinensis* Pers. and *Cinnamomum* 

and epiphytic bryophyte diversity is useful for understanding the effects of shrine forests on these species.

founded before 8th century [19] and is designated a World Heritage Site. The shrine forest is known as the

discuss the effective conservation methods for epiphytic bryophytes in fragmented forests.

epiphytic bryophyte species, including endangered species, on tree bark in several shrine forests.

**in Urban Areas**

Japan

Japan

**Introduction Shrine forests**

in urban areas.

**Bryophytes in shrine forests**

important habitat for bryophytes.

4582 Biodiversity in Ecosystems - Linking Structure and Function

Figure 1. Shrine forests

Right: Enlarged view of the shrine forest

Figure 2. *Plagiomnium actum* (left) and a leaf section (right)

**Environmental factors for bryophytes in shrine forests**

**1.3. Environmental factors for bryophytes in shrine forests**

desiccation than those on concave forms.

is very simple and lacks vascular bundles.

sufficiently addressed.

on concave forms.

**Objective**

**Methods Study site**

shrine forest

List of authors and their affiliations

Yoshitaka Oishi1 and Keizo Tabata2

<sup>2</sup> Faculty of Agriculture, Kinki University

1Department of Forest Science, Faculty of Agriculture, Shinshu University

In this study, we examined the role of shrine forests in the conservation of epiphytic bryo‐ phytes. Based on our results, we discuss the effective conservation methods for epiphytic bryophytes in fragmented forests.

## **3. Methods**

### **3.1. Study site**

The study was conducted at a shrine forest of the Shimogamo Shrine, Kyoto, Japan (Figure 3). This shrine may have been founded before 8th century [19] and is designated a World Heritage Site. The shrine forest is known as the "Tadasu-no-mori" and covers approximately 12.4 ha. One of the dominant trees is *Aphananthe aspera* (Thunb.) Planch, of which the forest contains more than 300 individuals. However, the numbers of *Celtis sinensis* Pers. and *Cinnamomum camphora* (L.) J. Presl have recently increased [20]. The dynamics of the trees in this forest have been reported by Tabada et al. [20-23].

### **3.2. Bryophyte survey**

In 2006, we surveyed the epiphytic bryophyte flora at the study site. We recorded the occur‐ rence of species and their cover on each *A. aspera* individual*.* The DBH of *A. aspera* was measured in 2002 by one of the authors. The average DBH was 161.5 ± 82.4 cm (mean ± standard deviation), the maximum was 420.0 cm, and the smallest was 27.0 cm. To understand the relationship between bryophyte diversity and DBH, we analyzed the changes in bryophyte life forms and reproductive strategies in addition to those of species richness and cover.

### **3.3. Bryophyte life form**

Bryophytes change their forms according to light intensity and humidity [24]. For example, in sunny and dry environments, bryophytes maintain water content in their bodies by forming contact mats similar to cushions [24]. Conversely, in dark and humid environments, bryo‐

**Figure 3.** Study site (Tadasu-no-mori, Shimogamo Shrine). A. Location of the study site , revised from Fig. 1 in Oishi [9]; B. Tadasu-no-mori forest; C. Bryophytes on tree trunks

phytes increase photosynthetic efficiency by forming flat mats similar to fans [24]. Therefore, bryophyte life forms are useful for evaluating habitat environmental conditions, and several studies have used them for this purpose [8-10, 25-26].

### **3.4. Reproductive strategy**

Bryophytes have two main reproductive strategies: sexual reproduction by spores and asexual reproduction by gemmae, fragile body parts, etc [27]. Sexual reproduction may be further classified into monoicous and dioicous types. Monoicous bryophytes have both antheridia and archegonia on the same shoot, while dioicous bryophytes have these organs on different shoots. Therefore, monoicous bryophytes have more opportunities for fertilization than do dioicous ones. Bryophytes with asexual reproduction can also reproduce more frequently than dioicous species. We hypothesized that this difference in reproductive frequency would affect the habitat preferences of bryophytes.

### **4. Analysis** Figure 3. Study site (Tadasu-no-mori,

**Proof Corrections Form** 

**Chapter Title: The importance of large trees in shrine forests for the conservation of epiphytic** 

**PROOF CORRECTIONS FORM** 

**No. Delete Replace with** 

**Author(s) Name(s): Yoshitaka Oishi & Keizo Tabata** 

**bryophytes in urban areas** 

**1** 25 As the leaf section shows, the body structure of

**4** Fig. 3 Figure 3(Please replace the Fig. 3 with the new

**4** 47 Figure 3. Study site (Tadasu-no-mori,

**5** Fig.4 Figure 4 (Please replace the Fig. 4 with the new

Shimogamo Shrine)

forest (below)

one).

bryophytes is very simple and lacks vascular

#### **4.1. DBH and bryophyte diversity** Shimogamo Shrine)

First, we compared the DBH values of trees with and without epiphytic bryophytes using the *t*-test to reveal the characteristics of trees with bryophytes. We then examined the effects of DBH on the diversity at both the community and species levels. The flow chart of this study is presented as Figure 4. A. Location of the study site (above), revised from Fig. 1 in Oishi [9]; B. Tadasu-no-mori A. Location of the study site , revised from Fig. 1 in Oishi [9]; B. Tadasu-no-mori forest; C. Bryophytes on tree trunks

(This sentence is a part of the caption for Fig. 2.)

**Figure 4.** Flow chart of this study

### **4.2. Community level**

phytes increase photosynthetic efficiency by forming flat mats similar to fans [24]. Therefore, bryophyte life forms are useful for evaluating habitat environmental conditions, and several

**Figure 3.** Study site (Tadasu-no-mori, Shimogamo Shrine). A. Location of the study site , revised from Fig. 1 in Oishi

**Page No.** 

**Line** 

bundles.

one).

Bryophytes have two main reproductive strategies: sexual reproduction by spores and asexual reproduction by gemmae, fragile body parts, etc [27]. Sexual reproduction may be further classified into monoicous and dioicous types. Monoicous bryophytes have both antheridia and archegonia on the same shoot, while dioicous bryophytes have these organs on different shoots. Therefore, monoicous bryophytes have more opportunities for fertilization than do dioicous ones. Bryophytes with asexual reproduction can also reproduce more frequently than dioicous species. We hypothesized that this difference in reproductive frequency would affect

studies have used them for this purpose [8-10, 25-26].

[9]; B. Tadasu-no-mori forest; C. Bryophytes on tree trunks

4604 Biodiversity in Ecosystems - Linking Structure and Function

**3.4. Reproductive strategy**

the habitat preferences of bryophytes.

The relationships between bryophyte diversity (total species richness and cover) and the DBH of *A. aspera* were examined using Pearson's product-moment correlation coefficients. Addi‐ tionally, we examined the correlations of DBH with both the richness of the life forms and the species richness of each life form. The life forms recorded at the study site were short turfs (t), small cushions (cu), dendroids (D), rough mats (Rm), smooth mats (Sm), thalloid mats (Th), thread-like forms (Tl), wefts (W), and fans (F). These forms were classified according to the system of Bates [24]. Finally, we examined the correlation of DBH with the ratio of the species richness of dioicous species (RDi). This ratio was calculated as follows:

RDi=species richness of dioicous bryophytes/total species richness

The value of RDi therefore increases with the dominance of dioicous species.

### **4.3. Species level**

To understand the preferences of each species for DBH, we examined the changes in the relative dominance of each species (RDo) as DBH increased. To clarify the relationship between RDo and DBH, the *A. aspera* trees with epiphytic bryophytes were evenly divided into three categories (small, medium, and large). The relative dominance was calculated as follows:

1

RDo=cover of each species on trees of one category (small, medium, or large)/total cover of the species

This analysis was conducted for species that occurred more than 10 times at the study site.

### **5. Results**

### **5.1. Presence/absence of bryophytes**

Bryophytes were found on 181 of the 313 *A. aspera* trees at the study site. We compared the DBH of trees with and without bryophytes using the *t*-test. The DBH values of trees with bryophytes were significantly higher than those without bryophytes (*t=*-5.4, d.f.=311, *p* < 0.01; Figure 5). In the following analysis, we examined the relationships between tree DBH and bryophyte diversity in trees with bryophytes.

**Figure 5.** Comparison of DBH between trees with/without epiphytic bryophytes

### **5.2. Bryophyte flora**

We found 42 bryophyte species (28 mosses and 14 liverworts) on the *A. aspera* trees, including two endangered species [*Leskeella pusilla* (Mitt.) Nog. and *Hypnodontopsis apiculata* Z. Iwats. & Nog.]. Figure 6 displays several species found at the study site. The most frequently observed species was *Trocholejeunea sandvicensis* (Gottsche) Mizut. (73 times), followed by *Metzgeria lindbergii* Schiffn. (64 times), *Rhynchostegium pallidifolium* (Mitt.) A. Jaeger (62 times), *Macvicaria ulophyl*la (Steph.) S. Hatt. (58 times), and *Frullania parvistipula* Steph. (58 times). The species with the largest total cover was *T. sandvicens*, followed by *R. pallidifolium*l, *M. lindbergii*, *Rhynchostegium inclinatum* (Mitt.) A. Jaeger, and *M. ulophylla*. The complete species list is presented in the Appendix.

Figure 5. Comparison of DBH between trees with/without epiphytic bryophytes

**Figure 6.** Several bryophyte species found at the study site

Figure 6. Several bryophyte species found at the study site

### **5.3. Bryophyte diversity**

RDo=cover of each species on trees of one category (small, medium, or large)/total cover of the

This analysis was conducted for species that occurred more than 10 times at the study site.

Bryophytes were found on 181 of the 313 *A. aspera* trees at the study site. We compared the DBH of trees with and without bryophytes using the *t*-test. The DBH values of trees with bryophytes were significantly higher than those without bryophytes (*t=*-5.4, d.f.=311, *p* < 0.01; Figure 5). In the following analysis, we examined the relationships between tree DBH and

We found 42 bryophyte species (28 mosses and 14 liverworts) on the *A. aspera* trees, including two endangered species [*Leskeella pusilla* (Mitt.) Nog. and *Hypnodontopsis apiculata* Z. Iwats. & Nog.]. Figure 6 displays several species found at the study site. The most frequently observed species was *Trocholejeunea sandvicensis* (Gottsche) Mizut. (73 times), followed by *Metzgeria lindbergii* Schiffn. (64 times), *Rhynchostegium pallidifolium* (Mitt.) A. Jaeger (62 times), *Macvicaria ulophyl*la (Steph.) S. Hatt. (58 times), and *Frullania parvistipula* Steph. (58 times). The species with the largest total cover was *T. sandvicens*, followed by *R. pallidifolium*l, *M. lindbergii*,

species

**5. Results**

**5.2. Bryophyte flora**

**5.1. Presence/absence of bryophytes**

4626 Biodiversity in Ecosystems - Linking Structure and Function

bryophyte diversity in trees with bryophytes.

**Figure 5.** Comparison of DBH between trees with/without epiphytic bryophytes

The relationships between the species richness/cover and DBH were examined using Pearson's product-moment correlation coefficients. Both species richness and bryophyte cover were significantly and positively correlated with DBH (Table 1).

*Pylaisiadelpha tenuirostris Trocholejeunea sandvicensis*


**Table 1.** Relationships between bryophyte diversity and DBH

### **6. Life forms and reproductive strategy**

The Pearson's product-moment correlation coefficients between DBH and life form diversity are shown in Table 1. The richness of life forms also increased with increasing DBH. The species richness of dendroids, rough mats, and thalloid mats were significantly and positively correlated with DBH. RDi was also significantly and positively correlated with DBH.

### **7. Preference of each species for large trees**

Bryophytes were observed on 181 *A. aspera* trees, which were divided into three categories based on DBH (small, medium, and large) containing 60, 60, and 61 trees, respectively. The changes in the relative dominance of each species are shown in Figure 7. As seen in the figure, the bryophyte species could be classified into four types based on dominance pattern. Type 1 (three species) preferred to grow on trees with small DBH, type 2 (three species) on trees with middle DBH, and type 3 (nine species) on trees with large DBH. Type 4 (five species) grew almost exclusively on trees with large DBH. pattern. Type 1 (three species) preferred to grow on trees with small DBH, type 2 (three species) on trees with middle DBH,

and type 3 (nine species) on trees with large DBH. Type 4 (five species) grew almost exclusively on trees with large DBH.

**Variables Pearson's product-moment correlation coefficients**

Species richness 0.22\*\* Cover 0.28\*\*

Life form richness 0.19\* Short turfs -0.05 Small cushions 0.07 Dendroids 0.20\*\* Rough mats 0.17\* Smooth mats 0.14 Thalloid mats 0.18\* Thread–like forms 0.14 Wefts 0.14 Fans -0.05 Ratio of the species richness of Dioicous species 0.25\*\*

Life forms

4648 Biodiversity in Ecosystems - Linking Structure and Function

\*\*; *p* < 0.01, \*; *p* < 0.05

**Table 1.** Relationships between bryophyte diversity and DBH

**6. Life forms and reproductive strategy**

**7. Preference of each species for large trees**

The Pearson's product-moment correlation coefficients between DBH and life form diversity are shown in Table 1. The richness of life forms also increased with increasing DBH. The species richness of dendroids, rough mats, and thalloid mats were significantly and positively

Bryophytes were observed on 181 *A. aspera* trees, which were divided into three categories based on DBH (small, medium, and large) containing 60, 60, and 61 trees, respectively. The changes in the relative dominance of each species are shown in Figure 7. As seen in the figure, the bryophyte species could be classified into four types based on dominance pattern. Type 1 (three species) preferred to grow on trees with small DBH, type 2 (three species) on trees with

correlated with DBH. RDi was also significantly and positively correlated with DBH.

Figure 7. Relationships between the dominance of each species and DBH DBH class; 1 = small, 2 = medium, 3 = large The classification of species into types 1–4 is as follows. **Figure 7.** Relationships between the dominance of each species and DBH. DBH class; 1=small, 2=medium, 3=large. The classification of species into types 1–4 is as follows: Type 1: prefer to grow on trees with small DBH, Type 2: prefer to grow on trees with medium DBH, Type 3: prefer to grow on trees with large DBH, Type 4: almost exclusively grow on trees with large DBH

Type 1: prefer to grow on trees with small DBH, Type 2: prefer to grow on trees with medium DBH

## **8. Discussion**

### **8.1. Bryophyte diversity**

We found 42 species on the bark of *A. aspera* alone (313 trees), while Oishi [8-10] found 57 species on the bark of all trees at the site. Approximately, two-thirds of the epiphytic bryo‐ phytes at the study site (containing more than 3000 total trees) were found on *A. aspera,* which indicates the high diversity of bryophytes on this species.

Notably, two endangered species (*L. pusilla* and *H. apiculata*) were found at the site. *L. pusil‐ la,* which is classified as an endangered species on the red list of Kyoto prefecture [28], grows in large forests where desiccation stress is low [6]. Therefore, the large patch sizes of the study site support the occurrence of this species. *H. apiculata* is endemic to Japan and has severely limited habitat; therefore, this species is designated as "critically threatened" on the red list of Japan [29]. Why does this rare species grow at the study site? This species may be threatened by habitat losses caused by development [29]. As mentioned in the introduction, the study was conducted in an area that has long been preserved as a shrine forest. The preservation history of the study site likely contributed to the survival of this species.

### **8.2. Bryophyte diversity and DBH**

Our results indicate that the diversity of both epiphytic bryophytes and life forms increased with DBH. Additionally, the relative dominance of 14 species (Types 3 & 4) increased with DBH; notably, five species (Type 4) occurred almost exclusively on large trees. These results indicate that the presence of large trees can increase the diversity of epiphytic bryophytes and are necessary for the conservation of these species. These relationships may be explained by (1) changes in tree bark and (2) the longer lives of large trees.

### *8.2.1. Changes in tree bark*

The features of tree bark change with tree size: the bark surface of large trees has a higher moisture content and is rougher than that of small trees [30]. This higher moisture content can be important for bryophytes that grow in forms vulnerable to desiccation, such as fans, dendroids, and wefts [24], as reflected in the positive significant correlations of DBH with both the richness values of these life forms and total life form richness.

Furthermore, the rough bark surface of large trees may be more suitable for capturing bryophyte spores/gemmae than is the smooth surface of small trees. At our study site, the dominance of bryophytes with low reproductive frequency (dioicous species) increased with DBH. This result indicates that large trees are especially important for the establishment of bryophytes with low reproductive frequency due to their higher capture ability.

McGee & Kimmerer [31] showed that the occurrence and abundance of epiphytic bryophytes on large maple trees are likely regulated to a greater extent by factors such as dispersal or protonemal establishment than by the habitat requirements of mature gametophytes. Al‐ though we cannot directly apply the results of McGee & Kimmerer [31] to our study because of differences in species and environmental conditions, their results suggest that changes in bark features more strongly affect dispersal or protonemal establishment than mature gametophytes.

### *8.2.2. Longer lives*

**8. Discussion**

**8.1. Bryophyte diversity**

466 10 Biodiversity in Ecosystems - Linking Structure and Function

**8.2. Bryophyte diversity and DBH**

*8.2.1. Changes in tree bark*

indicates the high diversity of bryophytes on this species.

of the study site likely contributed to the survival of this species.

(1) changes in tree bark and (2) the longer lives of large trees.

the richness values of these life forms and total life form richness.

We found 42 species on the bark of *A. aspera* alone (313 trees), while Oishi [8-10] found 57 species on the bark of all trees at the site. Approximately, two-thirds of the epiphytic bryo‐ phytes at the study site (containing more than 3000 total trees) were found on *A. aspera,* which

Notably, two endangered species (*L. pusilla* and *H. apiculata*) were found at the site. *L. pusil‐ la,* which is classified as an endangered species on the red list of Kyoto prefecture [28], grows in large forests where desiccation stress is low [6]. Therefore, the large patch sizes of the study site support the occurrence of this species. *H. apiculata* is endemic to Japan and has severely limited habitat; therefore, this species is designated as "critically threatened" on the red list of Japan [29]. Why does this rare species grow at the study site? This species may be threatened by habitat losses caused by development [29]. As mentioned in the introduction, the study was conducted in an area that has long been preserved as a shrine forest. The preservation history

Our results indicate that the diversity of both epiphytic bryophytes and life forms increased with DBH. Additionally, the relative dominance of 14 species (Types 3 & 4) increased with DBH; notably, five species (Type 4) occurred almost exclusively on large trees. These results indicate that the presence of large trees can increase the diversity of epiphytic bryophytes and are necessary for the conservation of these species. These relationships may be explained by

The features of tree bark change with tree size: the bark surface of large trees has a higher moisture content and is rougher than that of small trees [30]. This higher moisture content can be important for bryophytes that grow in forms vulnerable to desiccation, such as fans, dendroids, and wefts [24], as reflected in the positive significant correlations of DBH with both

Furthermore, the rough bark surface of large trees may be more suitable for capturing bryophyte spores/gemmae than is the smooth surface of small trees. At our study site, the dominance of bryophytes with low reproductive frequency (dioicous species) increased with DBH. This result indicates that large trees are especially important for the establishment of

McGee & Kimmerer [31] showed that the occurrence and abundance of epiphytic bryophytes on large maple trees are likely regulated to a greater extent by factors such as dispersal or protonemal establishment than by the habitat requirements of mature gametophytes. Al‐ though we cannot directly apply the results of McGee & Kimmerer [31] to our study because

bryophytes with low reproductive frequency due to their higher capture ability.

Generally, larger trees live for longer periods than do small trees in similar environments, which provide comparatively more opportunities for bryophyte spore/gemma establishment. This effect may be partly reflected in the positive correlations between DBH and both the species richness and dominance of bryophytes with low reproductive frequency.

### **8.3. The significance of shrine forests**

McGee & Kimmerer [17] described the importance of large trees for the conservation of epiphytic bryophytes in hardwood forests. This study shows that large trees can also contribute to the conservation of epiphytic bryophytes in shrine forests through their preferential bark features and longer lives. The effects of large trees are reflected in the changes of bryophyte life forms diversity and reproductive strategy according to DBH. In shrine forests, large trees are preferentially conserved because they are regarded as sacred. And, the management of shrine forests is effective for the conservation of epiphytic bryophytes.

Contrary to these results, several authors have reported that tree DBH does not strongly impact epiphytic bryophytes [32-33]. The possible explanations for the differences between this study and previous studies are as follow.


### **8.4. History of shrine forests**

This study also indicates that the long history of shrine forests contributes to the conservation of epiphyte diversity. Although this study did not gather sufficient data to examine the relationship between forest history and epiphytic bryophyte diversity, previous work has shown the importance of history for these species [18]. This conservation effect has also been reported in a fragmented forest in Kyoto city [34].

### **8.5. Epiphytic bryophytes and ecosystem**

Epiphytic bryophytes play important roles in water storage [35, 36], nutrient cycling [37], and the retention of inorganic nitrogen [38] in forest ecosystems. These functions of epiphytic bryophytes have been examined not in urban forests but in tropical montane or old growth Douglas fir and western hemlock forests, in which epiphyte biomass is relatively high. The biomass of epiphytic bryophytes in urban forests is comparatively small; however, these organisms may also be important in urban ecosystems. In particular, the role of bryophytes in water storage may contribute to the conservation of biodiversity, as the drought stress caused by edge effects is severe in fragmented urban forests [13].

### **9. Conclusion**

The results of this study indicate that large trees in shrine forests can provide suitable habitats for epiphytic bryophytes and enhance their diversity in urban environments where green area is limited. These trees are especially effective for the conservation of species that are vulnerable to desiccation and/or have low reproductive frequency.

Epiphytic bryophytes are affected by environmental factors such as tree density [15, 33], past landscape structure [18, 34], bark type [39], silvicultural disturbance [40], air pollution [41], etc. By examining the influence of these factors on bryophytes in future studies, we can propose more effective methods for the conservation of these species. Furthermore, we should also examine the ecological roles of epiphytic bryophytes (e.g., water storage) in fragmented forests to understand the importance of their conservation.

## **Appendix**

### **Appendix: Species list**

The bryophyte nomenclature follows that reported by Iwatsuki [27].


The Importance of Large Trees in Shrine Forests for the Conservation of Epiphytic Bryophytes in Urban Areas 13 http://dx.doi.org/ 10.5772/59074 469

organisms may also be important in urban ecosystems. In particular, the role of bryophytes in water storage may contribute to the conservation of biodiversity, as the drought stress caused

The results of this study indicate that large trees in shrine forests can provide suitable habitats for epiphytic bryophytes and enhance their diversity in urban environments where green area is limited. These trees are especially effective for the conservation of species that are vulnerable

Epiphytic bryophytes are affected by environmental factors such as tree density [15, 33], past landscape structure [18, 34], bark type [39], silvicultural disturbance [40], air pollution [41], etc. By examining the influence of these factors on bryophytes in future studies, we can propose more effective methods for the conservation of these species. Furthermore, we should also examine the ecological roles of epiphytic bryophytes (e.g., water storage) in fragmented forests

**Moss Frequency Cover (cm2**

**)**

by edge effects is severe in fragmented urban forests [13].

468 12 Biodiversity in Ecosystems - Linking Structure and Function

to desiccation and/or have low reproductive frequency.

to understand the importance of their conservation.

The bryophyte nomenclature follows that reported by Iwatsuki [27].

*Anomodon giraldii* Müll. Hal. 1 <100 *Aulacopilum japonicum* Broth.ex Card. 21 25000 *Brachymenium nepalense* Hook. 1 <100 *Brachythecium buchanani*i (Hook.) A.Jaeger 1 <100 *Brachythecium populeum* (Hedw.) Schimp. 1 800 *Bryum capillare* Hedw. 4 <100 *Entodon challengeri* (Paris) Card. 30 30000 *Entodon sullivantii* (Müll. Hal.) Lindb. 1 400 *Fabronia matsumurae* Besch. 35 2600 *Haplocladium angustifolium* (Hampe & Müll.Hal.) Broth. 20 600

**9. Conclusion**

**Appendix**

**Appendix: Species list**



## **Acknowledgements**

The author thanks Professor Yukihiro Morimoto for providing critical comments and sug‐ gesting improvements to this chapter, as well as Kaori Kuriyama for assistance with the bryophyte survey. This research was supported by a Grant-in-Aid for Scientific Research (A) (No. 18201008) from the Japan Society for the Promotion of Science.

## **Author details**

Yoshitaka Oishi1\* and Keizo Tabata2


## **References**


[4] Imanishi A, Imanishi J, Murakami K, Morimoto Y, Satomura A. Herbaceous plant species richness and species distribution pattern at the precincts of shrines as nonforest greenery in Kyoto city. Journal of the Japanese Society of Revegetation Tech‐ nology 2005; 31(2) 278-83.

**Moss Frequency Cover (cm2**

*Lejeunea ulicina* (Tayl.) Gottsche, Lindenb.& Nees 1 <100 *Macvicaria ulophylla* (Steph.) S.Hatt. 58 38700 *Metzgeria lindbergii* Schiffn. 64 41500 *Radula constricta* Steph. 5 900 *Trocholejeunea sandvicensis* (Gottsche) Mizut. 73 59800

The author thanks Professor Yukihiro Morimoto for providing critical comments and sug‐ gesting improvements to this chapter, as well as Kaori Kuriyama for assistance with the bryophyte survey. This research was supported by a Grant-in-Aid for Scientific Research (A)

(No. 18201008) from the Japan Society for the Promotion of Science.

1 Department of Forest Science, Faculty of Agriculture, Shinshu University, Japan

[1] Hashimoto H, Murakami K, Morimoto Y. Relative species-area relationship and nest‐ edness pattern of woodland birds in urban area of Kyoto City. Landscape Ecology

[2] Hashimoto H, Sawa K, Tabata K, Morimoto Y, Nishino S. Characteristics of Legacy Trees with Hollows in the Urban Area of Kyoto City, Japan. Journal of the Japanese

[3] Murakami K, Morimoto Y. Landscape ecological study on the woody plant species richness and its conservation in fragmented forest patches in the Kyoto city area.

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\*Address all correspondence to: oishiy@shinshu-u.ac.jp

2 Faculty of Agriculture, Kinki University, Japan

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470 14 Biodiversity in Ecosystems - Linking Structure and Function

**Author details**

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Yoshitaka Oishi1\* and Keizo Tabata2

**)**


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[18] Snäll T, Hagström A, Rudolphi J, Rydin H. Distribution pattern of the epiphyte *Neck‐ era pennata* on three spatial scales-importance of past landscape structure, connectivi‐

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## **Miombo Woodlands Research Towards the Sustainable Use of Ecosystem Services in Southern Africa**

Natasha Sofia Ribeiro, Stephen Syampungani, Nalukui M. Matakala, David Nangoma and Ana Isabel Ribeiro-Barros

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59288

## **1. Introduction**

The Miombo woodlands are the most extensive warm dry forest type in southern Africa [1], covering ca. 2.7 million km2 across seven countries: Tanzania and the Democratic Republic of Congo (DRC) in the north, Angola and Zambia in the east, and Malawi, Zimbabwe and Mozambique in the south [2-4] (Figure 1). It is one of the most important ecosystems in the world, playing an important role at the social, economic and environmental levels. Being an important center of plant biodiversity Miombo is a key provider of goods and services, supporting the livelihoods of more than 65 million of people in the region [4]. The woodlands are also very important to the national economies as they provide timber for exportation. From the environmental point of view Miombo is determinant to energy, carbon and water balance [3,5].

The ecological dynamics of Miombo is strongly influenced by their woody component, particularly by large trees, which play a key role in ecosystem function, primarily in nutrient cycling, accounting for a great deal of the carbon pool. This component is in turn influenced by a combination of climate, disturbances [e.g. drought, fire, grazing and herbivory primarily by elephants (*Loxodonta africana* Blumenbach)] and human activities [6-7]. Growing population in the region over the last 20-25 years has resulted in increased woodland degradation and deforestation. Slash and burn agriculture and charcoal production are the major causes of forest loss and degradation in the Miombo Ecoregion [8-10]. Additionally, the region is experiencing several major investments in mining, commercial agriculture and infrastructures, which have further increased the pressure on the woodlands. In Zambia for example, where

© 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2014 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and eproduction in any medium, provided the original work is properly cited.

**Figure 1.** Map of African vegetation, showing the Miombo woodlands in dark green (Source: White, 1983).

there is large-scale mining for copper, the mining sector has greatly contributed to forest cover and biomass losses. Often, huge tracts of land are cleared to provide space for mining infra‐ structures; at Kalumbila Concession, Solwezi alone, infrastructure development resulted in the loss of more than 7,000 hectares of land [11]. This is often followed by an increased demand for construction timber, creating further pressure on forests.

Changes in the global climatic pattern, *e.g.* 5-15% predicted reduction in precipitation for southern Africa [12], constitute another major threat across the various global ecosystems. In the Miombo Woodlands, they are mainly associated with more extreme wet and dry seasons, *i.e.* drier interior regions, wetter coastal regions, as well as extreme temperatures, which may change disturbances regimes (fire, shifting cultivation, amongst others) and thus the prevailing biodiversity status. According to [13], the combined effect of climate change and disturbances may cause the loss of ca. 40% of the woodlands by the middle of the century. There is an increased concern that the loss of mature trees in landscapes may result in the transformation of the woodlands into scrub or grasslands. This may impose changes in biodiversity and biomass with associated modifications on the pattern of goods and services offered by this ecosystem.

It is widely recognized that Miombo Woodlands have great potential to provide financial resources through Carbon-based Payment for Ecosystem Services (PES) [14], but their function as dynamic C-pools in biogeochemical cycles is largely unknown [15]. In this context, under‐ standing biodiversity and carbon variations under different land use scenarios as well as the rates and the extent to which Miombo recover from disturbances has important implications in the emerging C-based PES schemes [16], which are taking center-stage in the United Nations Framework Convention on Climate Change (UNFCCC) through mechanisms such as Reduc‐ ing Emission from Deforestation and Forest Degradation (REDD+). On the other hand, such assessments will be crucial for future land use decisions to ensure optimal land use benefits, hence ensuring forest conservation and sustainable management [15].

Under the scenario described above, current research efforts in the region aim at understanding the ecology of Miombo including its biodiversity, biomass production and carbon sequestra‐ tion, as well as the role of disturbances and its socio-economic relevance. In this chapter we summarize the existing information on the dynamics of biodiversity and biomass /carbon), in order to identify research gaps and needs. It is our intention to contribute towards a research agenda for the Miombo Woodlands, which is being developed under the context of the Miombo Network of Southern Africa, an alliance of scientists for informed research to decision making in the region.

## **2. Biodiversity dynamics**

there is large-scale mining for copper, the mining sector has greatly contributed to forest cover and biomass losses. Often, huge tracts of land are cleared to provide space for mining infra‐ structures; at Kalumbila Concession, Solwezi alone, infrastructure development resulted in the loss of more than 7,000 hectares of land [11]. This is often followed by an increased demand

**Figure 1.** Map of African vegetation, showing the Miombo woodlands in dark green (Source: White, 1983).

Changes in the global climatic pattern, *e.g.* 5-15% predicted reduction in precipitation for southern Africa [12], constitute another major threat across the various global ecosystems. In the Miombo Woodlands, they are mainly associated with more extreme wet and dry seasons, *i.e.* drier interior regions, wetter coastal regions, as well as extreme temperatures, which may change disturbances regimes (fire, shifting cultivation, amongst others) and thus the prevailing biodiversity status. According to [13], the combined effect of climate change and disturbances may cause the loss of ca. 40% of the woodlands by the middle of the century. There is an increased concern that the loss of mature trees in landscapes may result in the transformation of the woodlands into scrub or grasslands. This may impose changes in biodiversity and

for construction timber, creating further pressure on forests.

4762 Biodiversity in Ecosystems - Linking Structure and Function

Miombo has an estimated diversity of 8,500 plant species, of which ca. 54% are endemic. Together with Mopane, it is amongst the five high biodiversity wilderness areas in the world whose conservation should be prioritized because of their irreplaceability in terms of species endemism [17-18]. The woodlands are characterized by the overwhelming dominance of *Brachystegia* (*Miombo* in Swahili), *Julbernardia* and *Isoberlinia* tree species belonging to the Fabaceae (legume) family [19-20], associated with a variety of other woody plants, such as *Pseudolachnostylis maprouneifolia* Pax., *Burkea africana* Hook and *Diplorhynchus condylocarpon* (Müll.Arg.) Pichon. In mature Miombo these species comprise an upper canopy layer made of 10-20 m high trees and a scattered layer of sub-canopy trees. The understorey is discontinuous and composed of broadleaved shrubs of the genera *Eriosema, Sphenostylis, Kotschya, Dolichos* and *Indigofera*, among others, and suppressed saplings of canopy trees. A sparse but continu‐ ous herbaceous layer of grasses, forbs and sedges composed of *Hyparrhenia, Andropogon, Loudetia, Digitaria* and *Eragrostis* dominate the ground-layer [2,21]. Miombo is usually referred as a homogenous ecosystem, but differences in species composition, diversity and structure occur at a local scale [22]. The origin of these differences is unclear but, geomorphic evolution of the landscape [23], soil moisture and nutrients [24], land uses changes and other anthropo‐ genic disturbances [25] have all been indicated. Figure 2 illustrates Miombo structure and composition and fire occurrence.

**Figure 2.** Illustrative exemple of the Miombo Woodlands. (A) Diversity of tree species; (B) Close up pf *Brachystegia bo‐ hemii*; (C) Regrowing area; (D) Recently burned area. Credits to Isabel Moura, Tropical Research Institute, Portugal (A, B) and Ivete Maquia, Biotechnology Center, Eduardo Mondlane University (C, D)

Only a few Miombo biodiversity studies have been recently published and most of them were focused either on a limited number of tree species and/or on specific geographical locations. Hence, the information on the conservation status of Miombo plant species is scarce. For example, based on the existing national surveys, the number of threatened plant species is difficult, if not impossible, to estimate, but the Sudan-Zambezian zone, to which the Wood‐ lands belong, is reported to have the highest values of threatened species [18]. Since the conservation status of a particular species is a good indicator of the impact of threats and its capacity to provide goods and services [26], site-specific studies confined to one or to a small group of species are of utmost importance to upgrade the existing information and thus help future planning and management programs.

The establishment and management of fully protected areas such as National Parks are often assumed to be the best strategy for conserving species diversity and maintain forest compo‐ sition and structure. To evaluate this assertion, Banda and co-authors [27] conducted a study in western Tanzania in areas with four different levels of protection: a National Park (high protection level), a Game Controlled Area (with tourist hunting of big game animals), a Forest Reserve (with selective harvest of trees), and an Open Area (unrestricted access to forest resources). The authors observed that the forest structure was quite similar in the four sites and that species richness was significantly higher in the Game Controlled Area and Forest Reserve than in the other areas. More recently, Giliba and collaborators [22] assessed species richness, diversity, dominance and exploitation in Bereku Forest Reserve, northern Tanzania, concluding that the use of Miombo products and services by the surrounding communities does not compromise the stability of the woodlands, which are fairly stocked with high tree and shrub species diversity. These studies suggest that National Parks do not always host the greatest diversity of trees or unique species. This may imply that a suite of different types of protection strategies may be the key for conservation in African dry tropical forests [27].

The effect of environmental factors, particularly soil and disturbance history, on tree diversity and size structure was analysed by [19] in and around the Ihombwe village, Kilosa District,Tanzania where shifting cultivation is practiced. The authors observed that there was a considerably high capacity for tree species regeneration, partly due to the relative‐ ly isolated position of the village and also due to the fact that local communities recog‐ nize the importance of the sustainable ecosystem use. However, fires were pointed as the main driver of species composition change as they tend to support the proliferation of fire tolerant species, such as *P. maprouneifolia, Pterocarpus angolensis* DC and *D. condylocarpon* at the expense of dominant Miombo species. Similarly, [27] observed the dominance of *Terminalia sericea* Burch. ex DC.*, Combretum adenogonium* Steud. ex A.Rich., and *C. colinum* Fresen. in dry Miombo of the Katavi-Rukwa ecosystem of western Tanzania due to frequent burning. Also Williams and co-authors [28], working on the effects of slash-and-burn agriculture in the Nhambita community, Sofala Province, Mozambique, observed that in abandoned (regrowing) sites, defining Miombo species were replaced by secondary dominant trees. However, the biodiversity of woody species (i.e. Shannon index and species richness) in older abandonments (>10 years old) and intact woodlands were similar. In general tree biodiversity has not been degraded by the slash-and-burn disturbance, but the time-scale of recovery of defining Miombo species was unclear. In Zambia [29-31] have also suggested that though Miombo systems recover relatively fast in terms of species diversi‐ ty, species composition takes longer to recuperate. In another study in Mozambique, [32] observed that fire and herbivory by elephants are the main drivers of ecosystem struc‐ ture and composition. For example, places with high fire frequency and elephant density were dominated by fire-resistant species such as *T. stenostachya*, *Combretum* spp. and *D. condylocarpon*. Similar results were obtained by [33] in the Miombo Woodlands of northwestern Zimbabwe, where elephants and fires reduced the proportions of large trees, tree heights, stem basal area and densities of all trees. Besides that, tree species frequencies dropped 28–89.6% and the most visible floristic alteration was the replacement of the typical *Brachystegia boehmii* Taub. by *P. maprouneifolia* and Combretaceae species. The results are in line with those from [19,27-28] and are corroborated by the prediction model developed by [34] regarding the impact of elephants and fires on the structure of semi-arid Miombo Woodlands of north-western Zimbabwe. The author hypothesized that elephants alone at a density of 0.27 km-2 would convert the woodland into coppice in 120 years due to massive declines of large trees; the same result would be achieved in 10 years if elephant density

**Figure 2.** Illustrative exemple of the Miombo Woodlands. (A) Diversity of tree species; (B) Close up pf *Brachystegia bo‐ hemii*; (C) Regrowing area; (D) Recently burned area. Credits to Isabel Moura, Tropical Research Institute, Portugal (A,

Only a few Miombo biodiversity studies have been recently published and most of them were focused either on a limited number of tree species and/or on specific geographical locations. Hence, the information on the conservation status of Miombo plant species is scarce. For example, based on the existing national surveys, the number of threatened plant species is difficult, if not impossible, to estimate, but the Sudan-Zambezian zone, to which the Wood‐ lands belong, is reported to have the highest values of threatened species [18]. Since the conservation status of a particular species is a good indicator of the impact of threats and its capacity to provide goods and services [26], site-specific studies confined to one or to a small group of species are of utmost importance to upgrade the existing information and thus help

The establishment and management of fully protected areas such as National Parks are often assumed to be the best strategy for conserving species diversity and maintain forest compo‐ sition and structure. To evaluate this assertion, Banda and co-authors [27] conducted a study in western Tanzania in areas with four different levels of protection: a National Park (high protection level), a Game Controlled Area (with tourist hunting of big game animals), a Forest

B) and Ivete Maquia, Biotechnology Center, Eduardo Mondlane University (C, D)

future planning and management programs.

4784 Biodiversity in Ecosystems - Linking Structure and Function

increased to 2 km-2; the pattern would remain similar if simultaneous fire occurred once every 4.7 years with elephants at 0.27 km-2. Thus, it was predicted that elephants alone can degrade and maintain semi-arid Miombo Woodlands into coppice, largely due to their damaging impacts on mature canopy trees. Fire may also speed up the process by suppression of an already low recruitment. However, this driver alone had less influence on the woodland structure than elephants because of low fuel loads due to heavy graz‐ ing and low grass production as a result of low rainfall and inherently poor soils in the area.

Another important aspect in understanding the biodiversity dynamics in the Miombo Woodlands and in assisting conservation programs, is the application of molecular markers (MM). MM are essential tools to analyse population structure and genetic diversity as well as to identify particular traits (including genotypes and genes) associated with outstanding performances and resilience to extreme environments (*e.g*. fire, drought, high temperatures) [35-37]. The use of MM to understand the dynamics and potentialities of Miombo species is still incipient and only two studies have been published. The first reported on the use of Amplified Fragment Length Polymorphisms (AFLP) to assess the genetic diversity of natural populations of *Uapaca kirkiana* Muel. Arg. from three geographical regions of Malawi, in relation to deforestation, fragmentation and wildfires [38]. AFLP markers revealed moderate differentiation among the studied populations, but very high variation among individuals within populations. The second study was based on the use Inter Simple Sequence Repeat (ISSR) markers to assess genetic diversity in *B. boehmii* and *B. africana* across a fire gradient in the Niassa National Reserve (NNR) [39]. Although fire differentially affected the biodiversity in each species, in general, the overall genetic diversity was high and their survival did not seem to be compromised by the frequency of fires, agreeing with the fact that NNR is one of the least disturbed areas of deciduous Miombo. The results point also to a link between firetolerance and genetic diversity, as judged by the higher diversity levels observed in *B. africana* (fire-tolerant) in comparison to *B. boehmii* (fire-sensitive). Furthermore, *B. boehmii* presented an evolutionary response to fire, i.e. the levels of diversity were lower in frequent fire prone areas than in areas of low fire frequency, a phenomena attributed to the pyrodiver‐ sity-like effect [40]. In both papers, the authors emphasize the need for more intensive genetic studies spanning other populations of these and other important tree species to produce a wider picture of the levels of distribution of genetic diversity across the Miombo Ecoregion and its relation to major threats.

In conclusion, the available literature generally suggests that biodiversity in the miombo woodlands is shaped by disturbances, including anthropogenic actions, and to some extent may be compromised by the ongoing pressures. Despite the risks to which the woodlands are exposed, the species diversity and the levels of genetic diversity are considerably high. This seems to be particularly associated with the apparent resiliency of Miombo to various disturbances. However, there are evidences that typical species not always recover and in some cases may be replaced by secondary species. As a consequence, the range and type of goods and services provided by the woodlands may be altered. This calls for the implementation of management strategies that are appropriate for conserving biodiversity of Miombo.

### **2.1. Biomass and carbon dynamics**

increased to 2 km-2; the pattern would remain similar if simultaneous fire occurred once every 4.7 years with elephants at 0.27 km-2. Thus, it was predicted that elephants alone can degrade and maintain semi-arid Miombo Woodlands into coppice, largely due to their damaging impacts on mature canopy trees. Fire may also speed up the process by suppression of an already low recruitment. However, this driver alone had less influence on the woodland structure than elephants because of low fuel loads due to heavy graz‐ ing and low grass production as a result of low rainfall and inherently poor soils in the

Another important aspect in understanding the biodiversity dynamics in the Miombo Woodlands and in assisting conservation programs, is the application of molecular markers (MM). MM are essential tools to analyse population structure and genetic diversity as well as to identify particular traits (including genotypes and genes) associated with outstanding performances and resilience to extreme environments (*e.g*. fire, drought, high temperatures) [35-37]. The use of MM to understand the dynamics and potentialities of Miombo species is still incipient and only two studies have been published. The first reported on the use of Amplified Fragment Length Polymorphisms (AFLP) to assess the genetic diversity of natural populations of *Uapaca kirkiana* Muel. Arg. from three geographical regions of Malawi, in relation to deforestation, fragmentation and wildfires [38]. AFLP markers revealed moderate differentiation among the studied populations, but very high variation among individuals within populations. The second study was based on the use Inter Simple Sequence Repeat (ISSR) markers to assess genetic diversity in *B. boehmii* and *B. africana* across a fire gradient in the Niassa National Reserve (NNR) [39]. Although fire differentially affected the biodiversity in each species, in general, the overall genetic diversity was high and their survival did not seem to be compromised by the frequency of fires, agreeing with the fact that NNR is one of the least disturbed areas of deciduous Miombo. The results point also to a link between firetolerance and genetic diversity, as judged by the higher diversity levels observed in *B. africana* (fire-tolerant) in comparison to *B. boehmii* (fire-sensitive). Furthermore, *B. boehmii* presented an evolutionary response to fire, i.e. the levels of diversity were lower in frequent fire prone areas than in areas of low fire frequency, a phenomena attributed to the pyrodiver‐ sity-like effect [40]. In both papers, the authors emphasize the need for more intensive genetic studies spanning other populations of these and other important tree species to produce a wider picture of the levels of distribution of genetic diversity across the Miombo Ecoregion

In conclusion, the available literature generally suggests that biodiversity in the miombo woodlands is shaped by disturbances, including anthropogenic actions, and to some extent may be compromised by the ongoing pressures. Despite the risks to which the woodlands are exposed, the species diversity and the levels of genetic diversity are considerably high. This seems to be particularly associated with the apparent resiliency of Miombo to various disturbances. However, there are evidences that typical species not always recover and in some cases may be replaced by secondary species. As a consequence, the range and type of goods and services provided by the woodlands may be altered. This calls for the implementation of

management strategies that are appropriate for conserving biodiversity of Miombo.

area.

4806 Biodiversity in Ecosystems - Linking Structure and Function

and its relation to major threats.

Estimations of biomass and carbon stocks are an essential step in accounting for ecosystem goods and services particularly when considering land use options and strategies to promote carbon sequestration. This is relevant for implementing carbon credit market mechanisms such as REDD+, which seeks to mitigate climate change through enhanced CO2 storage in terrestrial ecosystems.

Biomass and carbon stocks have a pronounced variation across the Miombo Ecoregion. This has been mainly associated to: i) soil fertility and plant nutrition; ii) fires and herbivory; and iii) age and status of the woodland. Woody biomass was observed to range from 1.5 Mg ha-1 (3-6 years old coppice) to 144 Mg ha-1 (mature wet Miombo) [9,41-45]. Dry Miombo ranges between 53-55 Mg ha-1 [45-48]. It is confirmed that wood and soil compartments are the most important of these stocks [48-49], but grass, litter and root may contribute significantly to carbon sequestration. Table 1 presents comparative results of carbon stock density in different compartments across different sites.


**Table 1.** Comparative results of Carbon Stock Density across the Miombo Ecoregion. Source: Adapted from [48].

The dynamics of Miombo is in general influenced by its tree component given its dominance. Wood vegetation is in turn affected by environmental and disturbance factors [1]. Fire is particularly an important factor in Miombo as its behavior, timing, intensity and frequency vary greatly across the ecosystem, thus affecting vegetation structure and biomass differently. Frequent late dry season fires can transform woodland into open tall grass savanna with isolated fire-tolerant canopy trees and scattered understorey trees and shrubs [52] thereby reducing woody biomass. The impact of fires on biomass and carbon stocks has been addressed in a few countries. [53] in Zimbabwe, [54] and [31] in Zambia, and [46] and [55] in Mozambique have observed that fire protected sites had more woody biomass than frequently burned sites. [55] also noted that annual fire suppressed woody biomass development (up to 38 Mgha-1 in the studied area of central Mozambique) while low intensity fires at lower frequencies promoted biomass accumulation. Many studies have reported that once trees reach a certain height, they are less susceptible to fire [54 and references therein]. However, in his 22-year period study in Zambia, [31] found that large and tall trees were just as susceptible to fire as small trees, but their death was gradual and occurred over longer periods of time. In this area, fire alone was responsible for more than 25% of the observed biomass losses. The author concluded that avoided forest degradation at the study sites would have increased standing woody biomass up to 4.0 t ha-1 year-1 over the 22-year period. Recently, [45] found that carbon storage in the tree-dominated ecosystems of the Tanzanian Eastern Arc Mountains has decreased at a mean rate of 1.47 Mg C ha-1 yr-1 (ca. 2% of the stocks of carbon per year) due to 74% forest area loss driven by 5-fold increase in cropland area.

The interactive effect of fire and herbivory by elephants is quite interesting in Miombo. In general, elephants uproot, de-branch and/or debark large trees, increasing fuel-load in the forest ground due to intensified light intensity. Higher fuel loads result in frequent and fierce fires that influence the woodland. [42] and [56] have studied the effect of elephants in Sengwa National Park, Zimbabwe. The study compared areas inside the National Park (high elephant density and fire occurrence) and outside the National Park (low elephant density and fire occurrence) and revealed a reduction in biomass up to 31.8 t ha-1 for the area inside the national park due to elephant grazing. Fires inside the park leveraged elephant's effect by killing young sapling and debarked susceptible trees. [32] and [46] analised the combined effect of fires and elephants in NNR, northern Mozambique, revealing denser woodlands and higher wood biomass in places with low fire frequency and low animal densities. Recently, [48] studied the dynamics of the biomass in the Miombo woodlands in NNR and observed that woody biomass had a net increase of 3 Mg ha-1 in a 5-year period of study. However, when looking at the species level, *Diplorhynchus condylocarpon* presented the highest growth (a net increase of 0.54 Mg ha-1). This species has been reported elsewhere in the region has fire indicator due to its capacity to thrive in high fire frequency environments and to the fact that it is less preferred by elephants. *Julbernardia globiflora* (Benth.), on the other hand, experienced a net decrease in biomass of 0.09 Mg ha-1. The reason might be associated with fire susceptibility as well as high preference by local population and elephants and. As referred above, not many studies have addressed the specific responses to disturbances, though it should be considered fundamental to understand the ecosystem trends. In fact, species dynamics may disclose particular behav‐ iors that are not seen at the ecosystem level, but are important in defining conservation and management strategies, which are not just ecosystem but also species oriented.

The dynamics of Miombo is in general influenced by its tree component given its dominance. Wood vegetation is in turn affected by environmental and disturbance factors [1]. Fire is particularly an important factor in Miombo as its behavior, timing, intensity and frequency vary greatly across the ecosystem, thus affecting vegetation structure and biomass differently. Frequent late dry season fires can transform woodland into open tall grass savanna with isolated fire-tolerant canopy trees and scattered understorey trees and shrubs [52] thereby reducing woody biomass. The impact of fires on biomass and carbon stocks has been addressed in a few countries. [53] in Zimbabwe, [54] and [31] in Zambia, and [46] and [55] in Mozambique have observed that fire protected sites had more woody biomass than frequently burned sites. [55] also noted that annual fire suppressed woody biomass development (up to 38 Mgha-1 in the studied area of central Mozambique) while low intensity fires at lower frequencies promoted biomass accumulation. Many studies have reported that once trees reach a certain height, they are less susceptible to fire [54 and references therein]. However, in his 22-year period study in Zambia, [31] found that large and tall trees were just as susceptible to fire as small trees, but their death was gradual and occurred over longer periods of time. In this area, fire alone was responsible for more than 25% of the observed biomass losses. The author concluded that avoided forest degradation at the study sites would have increased standing woody biomass up to 4.0 t ha-1 year-1 over the 22-year period. Recently, [45] found that carbon storage in the tree-dominated ecosystems of the Tanzanian Eastern Arc Mountains has decreased at a mean rate of 1.47 Mg C ha-1 yr-1 (ca. 2% of the stocks of carbon per year) due to

The interactive effect of fire and herbivory by elephants is quite interesting in Miombo. In general, elephants uproot, de-branch and/or debark large trees, increasing fuel-load in the forest ground due to intensified light intensity. Higher fuel loads result in frequent and fierce fires that influence the woodland. [42] and [56] have studied the effect of elephants in Sengwa National Park, Zimbabwe. The study compared areas inside the National Park (high elephant density and fire occurrence) and outside the National Park (low elephant density and fire occurrence) and revealed a reduction in biomass up to 31.8 t ha-1 for the area inside the national park due to elephant grazing. Fires inside the park leveraged elephant's effect by killing young sapling and debarked susceptible trees. [32] and [46] analised the combined effect of fires and elephants in NNR, northern Mozambique, revealing denser woodlands and higher wood biomass in places with low fire frequency and low animal densities. Recently, [48] studied the dynamics of the biomass in the Miombo woodlands in NNR and observed that woody biomass had a net increase of 3 Mg ha-1 in a 5-year period of study. However, when looking at the species level, *Diplorhynchus condylocarpon* presented the highest growth (a net increase of 0.54 Mg ha-1). This species has been reported elsewhere in the region has fire indicator due to its capacity to thrive in high fire frequency environments and to the fact that it is less preferred by elephants. *Julbernardia globiflora* (Benth.), on the other hand, experienced a net decrease in biomass of 0.09 Mg ha-1. The reason might be associated with fire susceptibility as well as high preference by local population and elephants and. As referred above, not many studies have addressed the specific responses to disturbances, though it should be considered fundamental

74% forest area loss driven by 5-fold increase in cropland area.

4828 Biodiversity in Ecosystems - Linking Structure and Function

Charcoal production is one of the main drivers of Miombo degradation but has been poorly accounted for in biomass and carbon studies. Only one study [57] was found in the literature. This study was conducted in Zambia, by comparing a protected area with a highly disturbed site. The results revealed considerably reduced biomass after logging for charcoal production -150 t ha-1 within *versus* 24 t ha-1 outside the protected area. The authors discuss that better inventory data is urgently required to improve knowledge about the current state of the woodland usage and recovery after logging. They further argue that net greenhouse gas emissions could be reduced substantially by improving the post-harvest management, charcoal production technology and/or providing alternative energy supply.

Although soil is one of the main carbon pools in Miombo, studies that deal with this component are limited [28,48,58-59]. [28] observed that woodland soils were capable of storing >100 t C ha-1, whereas in re-growing areas soil carbon stocks did not exceed 74 t C ha-1. The study concluded that there was a potential for C sequestration in soils on abandoned farmlands. However, there was no discernible increase in soil C stocks within the period of re-growth, suggesting that the rate of accumulation of organic matter in these soils was very slow. On the other hand, [58] observed that agricultural soils in Malawi had 40% less carbon than mature Miombo Woodlands. The authors stated that as the area of land converted to agriculture increases in the region, land in this re-growth state will most likely become the dominant form of Miombo. Therefore studies of the nutrient dynamics in this type of land cover will be essential.

Understanding biomass and carbon recovery (along with biodiversity) rates is essential to predict future scenarios of ecosystem stock densities and thus, its capacity to provide goods and services. Short to medium term (16-50 years) studies in the region reveal a capacity for stock regeneration between 1.0 and 1.8 M g ha-1 yr-1 [1,28,43,60]. In Zambia, [31] reported net changes in aboveground biomass over a 22-year period of -113.4 Mg (-5.16 Mg ha-1 year-1) and 25.7 Mg (1.17 Mg ha-1 year-1) associated with old-growth and re-growth sites, respectively. Biomass loss in old-growth sites was driven by agriculture and fire. The conclusion drawn from these studies indicated that Miombo has capacity to recover after disturbances but at slow rates. The latter can be exacerbated or reverted by recurrent disturbances, compromising ecosystem resiliency. However, given the limited number of studies and the associated short to medium time spans, there are still knowledge gaps such as: i) which species recover and at which rate; ii) what are the thresholds of changes relation to disturbances; iii) what are the rates of soil carbon recovery. Improving the knowledge on recovery rates and patterns is important given the complexity of the ecosystem associated with the varied environmental gradients across the region.

## **3. Research gaps and management needs**

It is evident that there have been a considerable amount of studies undertaken in the Miombo Woodlands. In July 2013 the Miombo Network of Southern Africa met in Maputo, Mozambi‐ que to discuss the existing knowledge and gaps. In general, there is a consensus that much is still to be investigated.

Miombo displays complex vegetation patterns in which dense vegetation alternates with sparsely populated or bare soil in response to environmental and disturbance (deforestation/ degradation, fires and herbivory) factors. Low vegetation cover, in some places, and smallscale variations in others, can produce unpredictable errors in the quantification of ecosystem dynamics. Ignoring this spatial variation can produce inaccurate results, even in fairly homogeneous environments [61-62].

Miombo complexity has introduced limitations in the past in terms of accurate estimations/ mapping of Land Cover and Land Cover Change (LCLCC), biomass/carbon and biodiversity. In fact, there have been several attempts to estimate LCLCC and biomass at the local and national scale, but at the regional level there is still a need to improve and update the existing products. Land cover mapping is important to delineate LC types associated with degradation levels and the role of the associated drivers. The latter is highly relevant in determining the role of ecosystem in the carbon cycle as well as in defining appropriate rehabilitation and conservation strategies. These are particularly important in the context of REDD+ as it would be important to demarcate areas of interest to develop REDD+ projects.

Ecosystem rehabilitation requires a good understanding of its past and present status includ‐ ing the specific and interactive role of the drivers (fire, herbivory, slash and burn agriculture and climate change) as well as of its recovery patterns across environmental gradients. It also requires a better understating of its biodiversity beyond floristic surveys. In this context, the following questions need to be answered:


It is important to recognize that biomass and carbon estimations are very scattered in terms of methods and sampling efforts recalling a need to perform harmonized estimations to better position the region in the international context. Hence, finding benchmark sites is vital as it allows determination of deviations under different land uses. This is particularly important given the fact that the diversity of soils, climate, hydrology and disturbances return highly variable biomass and carbon densities making a comparison among sites not always possible [28,49]. Biomass estimations are also relevant to understand the contribution of different pools (soils, grasses, litter, etc) as well as the role of drivers in the ecosystem biomass/carbon sequestration. Particularly in the case of soil carbon, efforts should focus on identifying and protecting C-rich soils. It is also important to investigate whether fire control on recovering woodlands can stimulate the accumulation of soil C and tree biomass, and hence restore defining Miombo species.

Finally, the use of modern (*e.g*. remote sensing and molecular markers) and harmonized sampling data collection and analysis techniques across the region would contribute to the robustness of data and support improved ecosystem management and conservation strategies.

## **4. The role of the Miombo Network in promoting the Miombo Woodlands sustainability**

Founded in 1995 by a group of regional and international scientists, the Miombo Network is under the auspices of the IGBP/IHDP Land Use and Cover Change (LUCC) Project and the IHDP/IGBP/WCRP Global Changes System for Analysis, Research and Training (START). The Network's goal was to support the development of sustainable Miombo Woodlands manage‐ ment policies and practices through the collaborative data acquisition, from land‐based research, monitoring, remote sensing and other geospatial information technologies. The membership of the network is drawn from government, university and research institutions of the Miombo Ecoregion countries namely: Malawi, Mozambique, Tanzania, Zambia and Zimbabwe. However, there are also member institutions outside Africa due to their passion for Miombo management.

Being a collaborative alliance, the Miombo Network aspires to conduct joint research that contributes to forest policy definition and decision-making. The entry point for this is a strong link with the SADC forestry program, which intends to develop harmonized policies for the region. The Miombo Network has also potential to contribute for the establishment of the REDD+ programme - a programme that has great potential to turn around the economic and environmental value of the ecosystem across the region.

## **5. Final considerations**

**3. Research gaps and management needs**

484 10 Biodiversity in Ecosystems - Linking Structure and Function

still to be investigated.

homogeneous environments [61-62].

following questions need to be answered:

future)?

gradients?

rural and urban dwellers?

It is evident that there have been a considerable amount of studies undertaken in the Miombo Woodlands. In July 2013 the Miombo Network of Southern Africa met in Maputo, Mozambi‐ que to discuss the existing knowledge and gaps. In general, there is a consensus that much is

Miombo displays complex vegetation patterns in which dense vegetation alternates with sparsely populated or bare soil in response to environmental and disturbance (deforestation/ degradation, fires and herbivory) factors. Low vegetation cover, in some places, and smallscale variations in others, can produce unpredictable errors in the quantification of ecosystem dynamics. Ignoring this spatial variation can produce inaccurate results, even in fairly

Miombo complexity has introduced limitations in the past in terms of accurate estimations/ mapping of Land Cover and Land Cover Change (LCLCC), biomass/carbon and biodiversity. In fact, there have been several attempts to estimate LCLCC and biomass at the local and national scale, but at the regional level there is still a need to improve and update the existing products. Land cover mapping is important to delineate LC types associated with degradation levels and the role of the associated drivers. The latter is highly relevant in determining the role of ecosystem in the carbon cycle as well as in defining appropriate rehabilitation and conservation strategies. These are particularly important in the context of REDD+ as it would

Ecosystem rehabilitation requires a good understanding of its past and present status includ‐ ing the specific and interactive role of the drivers (fire, herbivory, slash and burn agriculture and climate change) as well as of its recovery patterns across environmental gradients. It also requires a better understating of its biodiversity beyond floristic surveys. In this context, the

**•** What is the capacity of biodiversity to supply and underpin goods and services (current and

**•** What are the patterns of genetic diversity of important species across environmental

**•** How these changes in biodiversity affect the availability and accessibility of resources to

It is important to recognize that biomass and carbon estimations are very scattered in terms of methods and sampling efforts recalling a need to perform harmonized estimations to better position the region in the international context. Hence, finding benchmark sites is vital as it allows determination of deviations under different land uses. This is particularly important

be important to demarcate areas of interest to develop REDD+ projects.

**•** What are the impacts of the different ecosystem drivers on biodiversity?

**•** How different land cover types affect the existing patterns of biodiversity?

Despite being considered the most important ecosystem of southern Africa, the Miombo Woodlands face some risks. Although policies may be supportive as far as Miombo manage‐ ment is concerned, the woodlands continue to be degraded and deforested. Partly, this is due to the fact that institutions that are responsible for managing the forests have limited human and financial capacity. Additionally, Community-Government partnerships for woodland management need to be enhanced in the region. It would therefore be important that national, regional and international institutions put more effort to establish effective collaborations in order to understand the interplay of issues that affect the management of Miombo Woodlands.

## **Acknowledgements**

The authors thank Isabel Moura (Tropical Research Institute, Portugal) and Ivete Maquia (Biotechnology Center, Eduardo Mondlane University, Mozambique) for providing the photographs for Figure 2.

## **Author details**

Natasha Sofia Ribeiro1 , Stephen Syampungani2 , Nalukui M. Matakala2 , David Nangoma3 and Ana Isabel Ribeiro-Barros4\*

\*Address all correspondence to: aribeiro@itqb.unl.pt

1 Faculty of Agronomy and Forest Engineering, Eduardo Mondlane University, Campus Universitário Principal, Edifício 1, Maputo, Mozambique

2 Copperbelt University, School of Natural Resources, Kitwe, Zambia

3 Mulanje Mountain Conservation Trust, Mulanje, Malawi

4 PlantStress&Biodiversity Group, Biotrop Center, Tropical Research Institute, Quinta do Marquês, Oeiras, Portugal

### **References**


[4] WWF. Miombo Eco-Region "Home of the Zambezi" Conservation Strategy 2011-2020. Harare: WWF-World Wide Fund for Nature; 2012.

management need to be enhanced in the region. It would therefore be important that national, regional and international institutions put more effort to establish effective collaborations in order to understand the interplay of issues that affect the management of Miombo Woodlands.

The authors thank Isabel Moura (Tropical Research Institute, Portugal) and Ivete Maquia (Biotechnology Center, Eduardo Mondlane University, Mozambique) for providing the

1 Faculty of Agronomy and Forest Engineering, Eduardo Mondlane University, Campus

4 PlantStress&Biodiversity Group, Biotrop Center, Tropical Research Institute, Quinta do

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486 12 Biodiversity in Ecosystems - Linking Structure and Function

photographs for Figure 2.

**Author details**

Natasha Sofia Ribeiro1

Ana Isabel Ribeiro-Barros4\*

Marquês, Oeiras, Portugal

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## **Ecological Restoration in Conservation Units**

Suzane Bevilacqua Marcuzzo and Márcio Viera

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59090

## **1. Introduction**

Forest ecosystems have rapidly been transformed into areas for the occupation of the human population and for economic purposes [1]. Rainforests distributed around the planet have been cleared because of a complex set of factors, which vary according to the characteris‐ tics of each region [2]. Among the factors are deforestation for alternative use of the soil (pasture, commercial or subsistence farming, and biofuel generation), tree cutting for the timber industry, wood extraction for energy biomass and poaching [3]. The reduction of vegetation cover leads to a decrease of biodiversity and to an increase of carbon emissions, changing the global climate [1].

The creation and establishment of conservation units is one of the main strategies to ensure biodiversity [4], allowing governments to tackle climate changes and, in the process, ensure biodiversity [5]. Conservation units are protected areas, established to maintain biological diversity and genetic resources, to protect endangered species, to conserve and restore diversity in natural ecosystems [4]. About 10% of the land surface of the planet is under some form of protected area [6]. However, the challenges are huge, because many protected areas are not yet fully implemented or adequately managed [6]. In Brazil, protected areas account for 17% of the Earth's surface [7].

The process of biodiversity preservation in protected areas is not always efficient, leading to lack of connectivity between the different forest remnants. This lack of connectivity affects the movement of organisms between the different environments, influencing the stability of populations, communities and ecological processes. In addition, areas defined as priorities for conservation may show significant environmental changes due to changes in land use [8]. Still, due to the great threat to biodiversity caused by the conversion of natural areas into production systems, conservation units provide adequate guarantees to ensure protection to the environment.

© 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2014 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and eproduction in any medium, provided the original work is properly cited.

Thus, areas altered because of changes in land use can be restored to recover the ecological interactions necessary for biodiversity maintenance. The use of restoration techniques to recover altered ecosystems is considered a fundamental strategy for biodiversity conservation. Ecological restoration has been widely used in Brazil as a measure to reverse the degradation process and enhance biodiversity conservation, ensuring ecosystem services.

In this context, arboreal forest species play a fundamental role in the reconstruction of the three-dimensional and functional structure of the forest (canopy, understory, strata, biomass, carbon, etc.). These species define local patterns of both organic matter accumulation in the soil [9] and nutrient cycling [10]. They help soils against the effects of erosion processes, favoring water infiltration (less runoff) and the definition of the microclimate standards of the habitat (shading, air and soil temperature, etc.) [11]. The tree species increase the abundance and diversity of shelters and foods for the fauna, enhancing the capacity to attract seed dispersers [12].

In this chapter, we will present the bases and methodological strategies of forest restoration in altered areas of the Atlantic Forest, Brazil. We will also address the potential of biodiversity conservation in protected areas. We will show results of restoration actions in altered areas in a conservation unit, focusing on ecosystem biodiversity and its applicability in other biomes.

## **2. Fundaments and strategies of forest restoration in Brazil**

Actions for forest restoration in Brazil were first introduced in areas affected by works of public interest, especially in places altered by the construction of large hydroelectric plants. Restora‐ tion actions were based on the planting of forest species without considering the ecological criteria, including the use of exotic species. These procedures led to the formation of mixed forests with low diversity and potential for land occupation [12]. Later, the original structure of a preserved forest fragment (diversity and successional groups) started to be considered [13]. This analysis served as a basis for the adoption of the recovery method to be applied in the altered environment. Currently, it is proposed that the succession process in restoration areas may occur following multiple trajectories and not a predefined template. These trajec‐ tories exhibit a dynamic equilibrium, where each final community will have its phytosociological and structural peculiarities according to the environment and the history of the ecosystem usage [14].

Defining a strategy for environmental restoration in altered ecosystems requires accurate indicators of the ecology in the biosystem. These indicators allow the use of specific method‐ ologies for each type of tree formation, ensuring a more effective restoration process, regardless of the recovery speed of the ecosystem, which vary enormously among forest ecosystems [15]. One of the main attributes of ecosystems is their ability to change in time. All ecosystems, terrestrial or aquatic, are subject to natural or human disturbances that inflict changes to a greater or lesser degree in time [16].

An ecosystem can be considered stable when it reacts to a disturbance, keeping a state of dynamic equilibrium [17]. However, a degraded ecosystem has undergone disturbances

leading to the decrease of its resilience, with consequent loss of important species and interactions [17]. Resilience is the ability of a system to restore its balance after being disrupted by a condition, that is, its ability to recover [18]. When the ecosystem under‐ goes severe damage, such as extinction of key-species and intensification of degradation (diseases, erosion, leaching and inbreeding), human intervention is required [19]. Accord‐ ing to the authors, this intervention must reverse the degradation processes leveraging local characteristics of auto-restoration.

Thus, areas altered because of changes in land use can be restored to recover the ecological interactions necessary for biodiversity maintenance. The use of restoration techniques to recover altered ecosystems is considered a fundamental strategy for biodiversity conservation. Ecological restoration has been widely used in Brazil as a measure to reverse the degradation

In this context, arboreal forest species play a fundamental role in the reconstruction of the three-dimensional and functional structure of the forest (canopy, understory, strata, biomass, carbon, etc.). These species define local patterns of both organic matter accumulation in the soil [9] and nutrient cycling [10]. They help soils against the effects of erosion processes, favoring water infiltration (less runoff) and the definition of the microclimate standards of the habitat (shading, air and soil temperature, etc.) [11]. The tree species increase the abundance and diversity of shelters and foods for the fauna, enhancing the capacity to attract seed

In this chapter, we will present the bases and methodological strategies of forest restoration in altered areas of the Atlantic Forest, Brazil. We will also address the potential of biodiversity conservation in protected areas. We will show results of restoration actions in altered areas in a conservation unit, focusing on ecosystem biodiversity and its applicability in other biomes.

Actions for forest restoration in Brazil were first introduced in areas affected by works of public interest, especially in places altered by the construction of large hydroelectric plants. Restora‐ tion actions were based on the planting of forest species without considering the ecological criteria, including the use of exotic species. These procedures led to the formation of mixed forests with low diversity and potential for land occupation [12]. Later, the original structure of a preserved forest fragment (diversity and successional groups) started to be considered [13]. This analysis served as a basis for the adoption of the recovery method to be applied in the altered environment. Currently, it is proposed that the succession process in restoration areas may occur following multiple trajectories and not a predefined template. These trajec‐ tories exhibit a dynamic equilibrium, where each final community will have its phytosociological and structural peculiarities according to the environment and the history of the

Defining a strategy for environmental restoration in altered ecosystems requires accurate indicators of the ecology in the biosystem. These indicators allow the use of specific method‐ ologies for each type of tree formation, ensuring a more effective restoration process, regardless of the recovery speed of the ecosystem, which vary enormously among forest ecosystems [15]. One of the main attributes of ecosystems is their ability to change in time. All ecosystems, terrestrial or aquatic, are subject to natural or human disturbances that inflict changes to a

An ecosystem can be considered stable when it reacts to a disturbance, keeping a state of dynamic equilibrium [17]. However, a degraded ecosystem has undergone disturbances

process and enhance biodiversity conservation, ensuring ecosystem services.

4942 Biodiversity in Ecosystems - Linking Structure and Function

**2. Fundaments and strategies of forest restoration in Brazil**

dispersers [12].

ecosystem usage [14].

greater or lesser degree in time [16].

For the success of a restoration process, some factors must be taken into account, namely the historical use of the area, the degradation intensity, the degree of forest fragmentation and the preservation degree of the surrounding vegetation. Thus, altered environments that have little or no vegetation preserved in their surroundings have less capacity to recover, once, mainly in tropical areas, seed dispersal occurs predominantly by animals. The animals hardly ever leave forested areas toward open agricultural areas [20]. Therefore, the presence of forest remnants facilitates the movement of seed dispersers [21].

Another important factor is the length of time and the intensity of the area use. Areas with consolidated agricultural and livestock activities recover more slowly than areas used for itinerant agriculture for short periods of time. In general, more intensely degraded areas have a seed bank with low diversity, limiting self-healing. Additionally, compacted soils and soils with low natural fertility limit the emergence and growth of seedlings.

Thus, for the recovery of natural ecosystems, success lies in the restoration of ecological processes responsible for the reconstruction and maintenance of a functional community [22]. The authors highlight that the effectiveness of this process depends on the use of high biodiversity involving species of trees, shrubs, vines as well as lianas, in addition to the fauna and the interactions between living beings that inhabit that environment. This diversity can be obtained through direct restoration actions of altered environments and guaranteed over time by the natural dynamics of the community restored [22].

The recovery of a degraded environment can be understood as reconstructions of its function and its structure [23]. According to the author, several optional objectives guide the recovery of a degraded ecosystem, namely: the reproduction of the exact original condition of the site (structure and function); the reproduction of conditions similar the conditions before degra‐ dation, enabling the balance of environmental processes; the development of an alternative activity suitable to human use and not simply the reconstitution of the original vegetation, provided this process is carried out to prevent negative environmental impacts; and aban‐ donment, which can lead to a normal succession process or to future degradation if the ecosystem is subject to erosion or other debilitating agent.

## **3. Biodiversity conservation in conservation units**

The Atlantic Forest and the Amazon Rainforest, historically, have had periods of connection, interspersed by periods of isolation. This alternation of isolation and connection with other biotas and the combination with striking geographic factors resulted in high biological diversity and endemic occurrences in these biomes [24]. Although these biomes show immense biological wealth, a significant part of biodiversity is still unknown. Between 1990 and 2006, [25] indicated the discovery of over 1,190 plant species by the scientific community for the Atlantic Forest.

The Atlantic Forest, first region colonized in Brazil, has undergone continuous deforestation and, currently, it is estimated that only 11-16% of the original forest cover remains [26]. Deforestation has resulted in severe changes in ecosystems, especially high fragmentation and degradation of native vegetation and loss of regional species of flora and fauna [27]. In the last decade, the deforestation rate has reduced because of numerous ordinances created to protect the biome, at different levels of government. Among the ordinances, we highlight the "Lei da Mata Atlântica" Law number 11,428 of December 22, 2006, which addresses the use and protection of native vegetation of the Atlantic Forest biome.

The definition of new protected areas represents an important strategy for biodiversity preservation. At the end of the 1990's, Brazil held more than 1,000 public and private conser‐ vation units, totaling approximately 76 million hectares [28]. In the Atlantic Forest biome, protected areas also increased during that period. The main category created was of Environ‐ mental Protection Areas (EPA). This category represents 91% of the total area of sustainable use in conservation units in the biome [29]. However, whole protection areas are not as effective, as they accept human occupation. In the Atlantic Forest biome, it is estimated that 40% of the area of sustainable use in conservation units is already occupied by human population and has no forest cover. Nevertheless, the whole protection areas account for 88% of its total area covered by preserved natural vegetation.

According to recent data from the Ministry of the Environment [7], Brazil has more than 2,100 conservation units, totaling circa 150 million hectares, which account for 17% of the Brazilian territory. The Amazon biome has approximately 73% of the total cover area in conservation units in Brazil, while the Atlantic Forest contributes to 7% [7]. The Atlantic Forest has approx‐ imately 9.7% (107,242 km2) of its territory in protected areas, being only 2% in whole protection conservation units [7].

A large number of rare and/or endangered species, reported on the so-called "red lists" [30, 31], are restricted only to protected areas. Thus, their existence is greatly linked to the future of these conservation units. The Official List of Threatened Species of the Brazilian Flora [31] contains 472 species, four-folds of the previous list of 1992. Of these, 276 species (more than 50%) belong to the Atlantic Forest. The list includes species that have been the most econom‐ ically exploited over time, such as pau-brasil (*Caesalpinia echinata*), palmito juçara (*Euterpe edulis*), araucaria (*Araucaria angustifolia*), jequitibá (*Cariniana ianeirensis*), jaborandi (*Pilocarpus jaborandi*), xaxim (*Dicksonia sellowiana*), jacarandá-da-bahia (*Dalbergia nigra*), canela-sassafrás (*Ocotea odorifera*) and various orchids and bromeliads.

The Official List of Threatened Species of the Brazilian Fauna [30] contains 633 species, including fish and aquatic invertebrates. Seven species have already been listed as extinct in the wild. Of these endangered species of the Atlantic Forest, 185 are vertebrate species (69.8% of all threatened species in Brazil), represented by 118 species of birds, 16 amphibians, 38 mammals and 13 reptiles. In addition, there are 59 fish species facing extinction [30]. A significant part of these endangered species is endemic, such as muriqui-do-sul (*Brachyteles arachnoides*), muriqui-do-norte (*Brachyteles hypoxanthus*) and papagaio-da-cara-roxa (*Amazona brasiliensis*).

## **4. Restoration of the Atlantic Forest**

biotas and the combination with striking geographic factors resulted in high biological diversity and endemic occurrences in these biomes [24]. Although these biomes show immense biological wealth, a significant part of biodiversity is still unknown. Between 1990 and 2006, [25] indicated the discovery of over 1,190 plant species by the scientific community for the

The Atlantic Forest, first region colonized in Brazil, has undergone continuous deforestation and, currently, it is estimated that only 11-16% of the original forest cover remains [26]. Deforestation has resulted in severe changes in ecosystems, especially high fragmentation and degradation of native vegetation and loss of regional species of flora and fauna [27]. In the last decade, the deforestation rate has reduced because of numerous ordinances created to protect the biome, at different levels of government. Among the ordinances, we highlight the "Lei da Mata Atlântica" Law number 11,428 of December 22, 2006, which addresses the use and

The definition of new protected areas represents an important strategy for biodiversity preservation. At the end of the 1990's, Brazil held more than 1,000 public and private conser‐ vation units, totaling approximately 76 million hectares [28]. In the Atlantic Forest biome, protected areas also increased during that period. The main category created was of Environ‐ mental Protection Areas (EPA). This category represents 91% of the total area of sustainable use in conservation units in the biome [29]. However, whole protection areas are not as effective, as they accept human occupation. In the Atlantic Forest biome, it is estimated that 40% of the area of sustainable use in conservation units is already occupied by human population and has no forest cover. Nevertheless, the whole protection areas account for 88%

According to recent data from the Ministry of the Environment [7], Brazil has more than 2,100 conservation units, totaling circa 150 million hectares, which account for 17% of the Brazilian territory. The Amazon biome has approximately 73% of the total cover area in conservation units in Brazil, while the Atlantic Forest contributes to 7% [7]. The Atlantic Forest has approx‐ imately 9.7% (107,242 km2) of its territory in protected areas, being only 2% in whole protection

A large number of rare and/or endangered species, reported on the so-called "red lists" [30, 31], are restricted only to protected areas. Thus, their existence is greatly linked to the future of these conservation units. The Official List of Threatened Species of the Brazilian Flora [31] contains 472 species, four-folds of the previous list of 1992. Of these, 276 species (more than 50%) belong to the Atlantic Forest. The list includes species that have been the most econom‐ ically exploited over time, such as pau-brasil (*Caesalpinia echinata*), palmito juçara (*Euterpe edulis*), araucaria (*Araucaria angustifolia*), jequitibá (*Cariniana ianeirensis*), jaborandi (*Pilocarpus jaborandi*), xaxim (*Dicksonia sellowiana*), jacarandá-da-bahia (*Dalbergia nigra*), canela-sassafrás

The Official List of Threatened Species of the Brazilian Fauna [30] contains 633 species, including fish and aquatic invertebrates. Seven species have already been listed as extinct in the wild. Of these endangered species of the Atlantic Forest, 185 are vertebrate species (69.8%

protection of native vegetation of the Atlantic Forest biome.

of its total area covered by preserved natural vegetation.

(*Ocotea odorifera*) and various orchids and bromeliads.

Atlantic Forest.

4964 Biodiversity in Ecosystems - Linking Structure and Function

conservation units [7].

The Atlantic Forest is one of the so-called global hotspots of biodiversity. The biome comprises 34 regions with high richness of endemic species; however, it is seriously threatened by significant loss of forest cover [32]. Originally distributed in more than 1.3 million km2 , in the eastern side of Brazil, the Atlantic Forest is home to at least 60% of the Brazilian population and approximately 70% of the national GDP is concentrated in this region of the country. Currently, there are degraded and isolated forest fragments with predominantly less than 50 ha [26]. Restoration of altered and fragmented areas is essential to ensure biodiversity maintenance, because protected areas must be connected to suit the functionality of the landscape ecosystem.

In this sense, we conducted a study on the Parque Estadual Quarta Colônia (Figure 1), a state protected area that was created in 2005. Its creation is attributed to a compensatory measure for the construction of a hydroelectric power plant. It is the largest established conservation unit of the "Deciduous Seasonal Forest" in the central region of Rio Grande do Sul State (1,847 ha), part of the Atlantic Forest Biome. A park is a category that aims the conservation of the ecosystem characteristic of a region and the practice of environmental education and recreation [4]. The Parque Estadual Quarta Colônia houses a floral species, *Dyckia agudensis* Irgang & Sobral (Figure 2), seriously threatened of extinction [33]. This species is lithophyte growing on basaltic formations among xerophytic vegetation. *D. agudensis* is at risk of extinction due to habitat fragmentation caused by agricultural activities in the surroundings.

Rugged-to-flat relief comprises the topography of the conservation unit. In some areas of the unit, there used to be small rural properties that were expropriated during the construction of the dam. There are several altered areas, decommissioned parts of the construction site and functional facilities of the plant power. Even before the creation of the conservation unit, some degraded areas of the park had been recovered with the planting of seedlings of native species in the year 2001. Other altered areas that were once abandoned are currently in early regen‐ eration stages, influenced by the natural forest matrix in the surroundings.

The most preserved areas of the park feature a succession mosaic due to anthropogenic interference in the area. The vegetation is classified as medium-to-advanced stage of secondary succession. The early secondary species contribute to greater diversity and the late secondary species appear less pronounced. Understory species possess the greatest number of individ‐ uals and have a characteristic occupation of greater range of luminosity. Thus, they suffer greater influence of soil variables in the definition of ecological niches of plant species [34].

Colônia houses a floral species, *Dyckia agudensis* Irgang & Sobral (Figure 2), seriously threatened of extinction [33]. This

decommissioned parts of the construction site and functional facilities of the plant power. Even before the creation of the

Figure 2. Species critically endangered of extinction (*Dyckia agudensis* Irgang & Sobral) found in the area of the Parque

area. The vegetation is classified as medium-to-advanced stage of secondary succession. The early secondary species

**Figure 1.** Limits of the conservation united (Parque Estadual Quarta Colônia), southern Brazil. conservation unit, some degraded areas of the park had been recovered with the planting of seedlings of native species in the year 2001. Other altered areas that were once abandoned are currently in early regeneration stages, influenced by

the natural forest matrix in the surroundings.

Estadual Quarta Colônia. The most preserved areas of the park feature a succession mosaic due to anthropogenic interference in the **Figure 2.** Species critically endangered of extinction (*Dyckia agudensis* Irgang & Sobral) found in the area of the Parque Estadual Quarta Colônia. Photo 2: Büncher (2011) - Digital Flora of Rio Grande do Sul.

contribute to greater diversity and the late secondary species appear less pronounced. Understory species possess the greatest number of individuals and have a characteristic occupation of greater range of luminosity. Thus, they suffer greater influence of soil variables in the definition of ecological niches of plant species [34]. However, for an ecosystem to be considered restored, it is necessary to analyze its biodiversity and compare it with preserved environments. Based on the principles of the Society for Ecological Restoration [35], a restored ecosystem However, for an ecosystem to be considered restored, it is necessary to analyze its biodiversity and compare it with preserved environments. Based on the principles of the Society for Ecological Restoration [35], a restored ecosystem should present diversity and structure similar to a reference ecosystem. Diversity is commonly measured by determining the richness and abundance of organisms. Similar to the specific composition of species, the vegetation structure

is usually analyzed by its density, biomass, and canopy coverage or by structural aspects of the vegetation, and these measurements are useful to predict the direction of plant succession [36]. Additionally, ecological processes, such as nutrient cycling and soil enzymatic activity [37], are related to stabilization and soil fertility [38]. In the same region of the conservation unit, [10] found that with leaf deposition of the leguminous tree *Parapiptadenia rigida*, soil nutrients returned to 32.4 kg ha-1 yr-1 of Ca, followed by N (26.1), K (3.2), Mg (2.1), S (1.3) and P (1.0 kg ha-1 yr-1).

From 2010 onwards, some attributes were evaluated to verify the recovery of degraded environments. We analyzed the vegetation structure, the diversity and ecological processes, which served as a parameter to evaluate different areas under restoration in the conservation unit. We initially characterized the vegetation in relation to environmental variables of the reference ecosystem to evaluate and monitor the areas under the restoration process. The reference area has been free of anthropic interventions for more than 20 years, and before that, there used to be small farms in the less steep slopes. Currently, it forms a mosaic of different successional stages [39].

Two groups of species composition characterize the forest. One group consists of understory species, which, due to the smaller size, establish on sloping and stable terrain. In this group, *Trichilia clausseni* is the indicator species that exerts a strong influence on forest succession and on the community due to its high density and frequency in forest regeneration. The other group of species is formed by *Nectandra lanceolata* and *Nectandra megapotamica* as dominant in the forest structure. In addition, early secondary species such as *Cupania vernalis*, *Ocotea puberula* and *Casearia sylvestris* indicate the dynamics of clearings in the area.

The monitoring of restoration was carried out in different altered areas of the Parque Estadual Quarta Colônia. The areas monitored (A1 and A2), both with seven years of planting, feature the following characteristics:

**Figure 1.** Limits of the conservation united (Parque Estadual Quarta Colônia), southern Brazil.

the natural forest matrix in the surroundings.

Estadual Quarta Colônia. Photo 2: Büncher (2011) - Digital Flora of Rio Grande do Sul.

Estadual Quarta Colônia.

Figure 1. Limits of the conservation united (Parque Estadual Quarta Colônia), southern Brazil.

Colônia houses a floral species, *Dyckia agudensis* Irgang & Sobral (Figure 2), seriously threatened of extinction [33]. This species is lithophyte growing on basaltic formations among xerophytic vegetation. *D. agudensis* is at risk of extinction

Rugged‐to‐flat relief comprises the topography of the conservation unit. In some areas of the unit, there used to be small rural properties that were expropriated during the construction of the dam. There are several altered areas, decommissioned parts of the construction site and functional facilities of the plant power. Even before the creation of the conservation unit, some degraded areas of the park had been recovered with the planting of seedlings of native species in the year 2001. Other altered areas that were once abandoned are currently in early regeneration stages, influenced by

Figure 2. Species critically endangered of extinction (*Dyckia agudensis* Irgang & Sobral) found in the area of the Parque

However, for an ecosystem to be considered restored, it is necessary to analyze its biodiversity and compare it with preserved environments. Based on the principles of the Society for Ecological Restoration [35], a restored ecosystem

greater influence of soil variables in the definition of ecological niches of plant species [34].

**Figure 2.** Species critically endangered of extinction (*Dyckia agudensis* Irgang & Sobral) found in the area of the Parque

However, for an ecosystem to be considered restored, it is necessary to analyze its biodiversity and compare it with preserved environments. Based on the principles of the Society for Ecological Restoration [35], a restored ecosystem should present diversity and structure similar to a reference ecosystem. Diversity is commonly measured by determining the richness and abundance of organisms. Similar to the specific composition of species, the vegetation structure

The most preserved areas of the park feature a succession mosaic due to anthropogenic interference in the area. The vegetation is classified as medium-to-advanced stage of secondary succession. The early secondary species contribute to greater diversity and the late secondary species appear less pronounced. Understory species possess the greatest number of individuals and have a characteristic occupation of greater range of luminosity. Thus, they suffer

due to habitat fragmentation caused by agricultural activities in the surroundings.

4986 Biodiversity in Ecosystems - Linking Structure and Function

**A1** – covers an area of 2.21 ha. It is a reminiscent of ancient successive crops of tobacco (*Nicotiana tabacum* L.) with about 560 m of the reference area. In the planting, 12 species were used with five pioneers (*Schinnus terebinhtifolius* Raddi, *Inga vera* Willd., *Parapiptadenia rigida* (Benth.) Brenan, *Ateleia glazioviana* Baill., *Psidium cattleyanum* L.) and seven early secondary (*Prunus myrtifolia* (L.) Urb., *Vitex megapotamica* (Spreng.) Moldenke, *Cedrela fissilis* Vell., *Ficus lusch‐ nathiana* (Miq.) Miq., *Luehea divaricata* Mart., *Peltophorum dubium* Sprengel. e *Ocotea puberula* (Rich.)). The soil was prepared by means of subsoiling at an average depth of 35 cm. After‐ wards, trenches were opened along the lines of grooves, and seedlings were planted at spacing of 2.5 m x 2.5 m. Cultural practices were performed for a period of 24 months.

**A2** – covers an area of 2.27 ha. It is about 615 m of the reference area and 78 m far from a slope area with secondary forest in the middle stage of succession. The soil was compacted with presence of construction waste (75% of particle size > 200 mm) [40], originating from the demolition of old facilities. In this region, 24 species were planted, being five pioneers (*Parapiptadenia rigida*, *Psidium cattleyanum*, *Schinus terebinthifolius*, *Enterolobium contortisiliq‐ uum* (Vell.) Morong, *Calliandra brevipes* (Spreng.) J. F. Macbr), 15 early secondary species (*Allophylus edulis* (A.St.-Hil., Cambess. & A. Juss.) Radlk., *Strychnos brasiliensis* (Spreng.) Mart., *Cordia americana* (L.) Gottshling & J.E.Mill., *Luehea divaricata*, *Peltophorum dubium*, *Cedrela fissilis* Vell., *Schizolobium parahyba*, *Cabralea canjerana* (Vell.) Mart, *Handroanthus heptaphyllus*, *Handroanthus chrysotrichus*, *Jacaranda micrantha*, *Eugenia uniflora*, *Campomanesia xanthocarpa* O. Berg, *Vitex megapotamica*, *Cordia trichotoma* (Vell.) Arráb. ex Stend.) and four late secondary species (*Ficus luschnathiana*, *Eugenia involucrata* DC, *Annona rugulosa* (Schltdl.) H. Rainer, *Myrcianthes pungens* (O. Berg.) D. Legrand). The spacing used was 4 m x 4 m with planting in trenches without subsoiling and cultural practices.

The structure of the vegetation diversity and enzymatic activity of the soil are significantly different between the areas under the restoration process and the reference area. It is observed, for example, when comparing the high proportion of pioneering species and reduced basal area growth in areas A1 and A2 (Table 1).


Where: (% P:NP)=percentage of pioneer species (P) in relation to non-pioneer species (NP).

**Table 1.** Structure and diversity in Subtropical Seasonal forest natural area (RA) and areas under restoration process (A1 and A2) in Parque Estadual Quarta Colônia.

Area A1 is in intermediate stage in relation to the other two areas. In area A2, the low density of plants is related to three factors: larger planting spacing; presence of restrictive layers to root growth; and lack of management after planting. The absence of weed control favored the permanent presence of invasive grasses, competing with arboreal individuals and preventing the development of some native species. The lower initial spacing in area A1 provided higher density of plants in the area, which resulted in the rapid canopy coverage in relation to area A2. Area A1 has a higher possibility of achieving the objectives of restoration due to increased canopy coverage. The greater shading of the canopy enabled grass reduction and, consequent‐ ly, the establishment of a greater number of regenerating individuals. The vegetation cover controls the quantity, quality and distribution of light, influencing the growth and survival of seedlings and determining vegetable composition [41]. The importance of richness of tree species and regeneration in the areas undergoing restoration was lower than that observed in the reference area (RA). Because the RA represents secondary forest, attract avifauna, which favors forest development. However, there is a need to manage the areas through the eradi‐ cation of exotic species. The exotic species with most occurrence medium-to-advanced stage of succession, may display predominance of some species, resembling the diversity index of a deployed area.

*Cordia americana* (L.) Gottshling & J.E.Mill., *Luehea divaricata*, *Peltophorum dubium*, *Cedrela fissilis* Vell., *Schizolobium parahyba*, *Cabralea canjerana* (Vell.) Mart, *Handroanthus heptaphyllus*, *Handroanthus chrysotrichus*, *Jacaranda micrantha*, *Eugenia uniflora*, *Campomanesia xanthocarpa* O. Berg, *Vitex megapotamica*, *Cordia trichotoma* (Vell.) Arráb. ex Stend.) and four late secondary species (*Ficus luschnathiana*, *Eugenia involucrata* DC, *Annona rugulosa* (Schltdl.) H. Rainer, *Myrcianthes pungens* (O. Berg.) D. Legrand). The spacing used was 4 m x 4 m with planting in

The structure of the vegetation diversity and enzymatic activity of the soil are significantly different between the areas under the restoration process and the reference area. It is observed, for example, when comparing the high proportion of pioneering species and reduced basal

Age (years) 7 7 ± 20 - - - Planting space (m) 2 x 2 4 x 4 - - - - Average height (m) 3.15 4.30 9.30 0.44 1.00 2.80 Basal area (m²/ha-1) 4.13 4.27 27.13 - - - Density (plants.ha-1) 1,741 297 3,408 23,333 11,388 15,909 Canopy cover (%) 109.3 35.7 - - - - Richness 19 29 49 21 16 42 Diversity (H') 2.31 2.86 3.00 2.23 2.29 2.60 Equability (J') 0.78 0.85 0.78 0.73 0.82 0.69 Zoochoric plants (%) 58.0 70.0 75.2 62.0 56.2 79.5 Anemochoric plants (%) 42.0 30.0 24.8 38.0 43.7 20.5 Sucessional group (% P:NP) 47:53 48:52 18:82 52:48 44:56 12:88 Exotic species (%) 26.3 17.2 0 28.5 31.2 0

Where: (% P:NP)=percentage of pioneer species (P) in relation to non-pioneer species (NP).

**Table 1.** Structure and diversity in Subtropical Seasonal forest natural area (RA) and areas under restoration process

Area A1 is in intermediate stage in relation to the other two areas. In area A2, the low density of plants is related to three factors: larger planting spacing; presence of restrictive layers to root growth; and lack of management after planting. The absence of weed control favored the permanent presence of invasive grasses, competing with arboreal individuals and preventing the development of some native species. The lower initial spacing in area A1 provided higher density of plants in the area, which resulted in the rapid canopy coverage in relation to area A2.

**Arboreal Component Natural Regeneration A1 A2 RA A1 A2 RA**

trenches without subsoiling and cultural practices.

area growth in areas A1 and A2 (Table 1).

5008 Biodiversity in Ecosystems - Linking Structure and Function

(A1 and A2) in Parque Estadual Quarta Colônia.

In natural regeneration, the floristic richness of the RA was enough to enable the development of various species, allowing a higher diversity index in relation to areas under restoration. This was attributed to the increased shading and flow of diaspores of species in reproductive stage. In the regeneration process of areas A1 and A2, zoochoric pioneering species predominated, with great capacity to was *Psidium guajava*, pioneer species with zoochoric dispersal (Table 2).


AD: Absolute Density; AF: Absolute Frequency; SG: Succession Group; P: Pioneer; ES: Early Secondary; LS: Late Secondary. \*Exotic Species.

**Table 2.** Five species better ranked in the regeneration process in the natural reference area (RA) and in areas under restoration process (A1 and A2).

Soil enzymes (amidase, urease, acid phosphatase, and arysulfatase) in the RA, at 0-5 cm of depth, presented higher values than those in restoration areas. Ground cover possibly influenced the enzymatic activity, since the restoration areas feature the presence of invasive grasses. However, in the RA, we can observe a dense layer of litterfall, which can reach 10.9 Mg ha-1 [42] in this type of forest formation. Still, the enzymatic activity is observed in all areas, although with significant differences between the restoration areas and the RA.

In area A2, a significant regeneration was verified under the canopy of *Inga vera*. This indicates that the *Inga* is a key species or a facilitator in the process of ecological restoration. In the restoration process of degraded areas, facilitators are species that, at an early stage of succes‐ sion, alter the conditions of the community, allowing better establishment of other species [43]. A species capable of forming aggregates of other species is considered a facilitator. The colonization processes that occur in the surroundings of this species are called nucleation [44], which occurs mainly by zoochoric dispersal [23].

Among several facilitators, *Inga vera* stands out by offering features that promote an improve‐ ment in environmental conditions, namely large tree crowns, rapid growth [23] and biological nitrogen fixation [45]. Its fruit is a hairy yellowish pod, measuring from 4-12 cm long with white pulp, sweet and edible, which makes it attractive to frugivorous animals, allowing zoochory [46]. The *Inga* is classified as a pioneer species in the ecological succession group. It has wide geographical distribution and is found mainly in the Atlantic Forest biome in Brazil.

Therefore, we evaluated regeneration under the canopy of *Inga vera* (50 plants) 10 years after the planting in area A2. We identified the presence of 756 individuals, belonging to 47 species and distributed among 25 families. The families Fabaceae (five species; 183 individuals), Myrtaceae (four species; 157 individuals) and Solanaceae (four species; five individuals) were the most representative in natural regeneration. Table 3 shows the main species found in natural regeneration.

Regarding the ecological groups, 26 species are pioneers (55.3%), 16 early secondary (34%) and two late secondary (4.3%), two unidentified (4.3%) and a mix of ES/LS (2.1%). In terms of seed dispersion, 29 species are zoochoric (61.7%), 13 are anemochoric (27.7%), two barochoric (4.3%), two unidentified (4.3%) and one authochoric (2.1%).

The Shannon diversity index (H') found was medium (2.68). For high diversity, the index must be greater than 3.0; medium, between 3.0 and 2.0; low, between 2.0 and 1.0 and very low, smaller than 1.0 [47]. The Pielou evenness index (J') was 0.7. This value indicates that some species have high densities, and others have few individuals [48]. The species *Ligustrum lucidum* (21.7%), *Inga vera* (17.9%), *Syzygium cumini* (12.8%), *Baccharis semiserrata* (7.7%), *Psidium guajava* (6.35%) and *Allophylus edulis* (5.3%) altogether represented 71.7% of the density of natural regeneration (542 individuals), a fact that explains the low evenness. The analysis of the index of importance value (IIV) shows that the species *Ligustrum lucidum* (30.2%), *Inga vera* (27.4%), *Syzygium cumini* (19.2%), *Baccharis semiserrata* (18%), *Psidium guajava* (14.9%) and *Allophylus edulis* (12.7%) have the highest values.

The species *Inga vera* and *Allophylus edulis* had fruits most attractive to frugivorous animals [46, 49]. The presence of *Inga* in the degraded area, for its characteristics, has the ability to form


Soil enzymes (amidase, urease, acid phosphatase, and arysulfatase) in the RA, at 0-5 cm of depth, presented higher values than those in restoration areas. Ground cover possibly influenced the enzymatic activity, since the restoration areas feature the presence of invasive grasses. However, in the RA, we can observe a dense layer of litterfall, which can reach 10.9 Mg ha-1 [42] in this type of forest formation. Still, the enzymatic activity is observed in all areas,

In area A2, a significant regeneration was verified under the canopy of *Inga vera*. This indicates that the *Inga* is a key species or a facilitator in the process of ecological restoration. In the restoration process of degraded areas, facilitators are species that, at an early stage of succes‐ sion, alter the conditions of the community, allowing better establishment of other species [43]. A species capable of forming aggregates of other species is considered a facilitator. The colonization processes that occur in the surroundings of this species are called nucleation [44],

Among several facilitators, *Inga vera* stands out by offering features that promote an improve‐ ment in environmental conditions, namely large tree crowns, rapid growth [23] and biological nitrogen fixation [45]. Its fruit is a hairy yellowish pod, measuring from 4-12 cm long with white pulp, sweet and edible, which makes it attractive to frugivorous animals, allowing zoochory [46]. The *Inga* is classified as a pioneer species in the ecological succession group. It has wide geographical distribution and is found mainly in the Atlantic Forest biome in Brazil. Therefore, we evaluated regeneration under the canopy of *Inga vera* (50 plants) 10 years after the planting in area A2. We identified the presence of 756 individuals, belonging to 47 species and distributed among 25 families. The families Fabaceae (five species; 183 individuals), Myrtaceae (four species; 157 individuals) and Solanaceae (four species; five individuals) were the most representative in natural regeneration. Table 3 shows the main species found in

Regarding the ecological groups, 26 species are pioneers (55.3%), 16 early secondary (34%) and two late secondary (4.3%), two unidentified (4.3%) and a mix of ES/LS (2.1%). In terms of seed dispersion, 29 species are zoochoric (61.7%), 13 are anemochoric (27.7%), two barochoric

The Shannon diversity index (H') found was medium (2.68). For high diversity, the index must be greater than 3.0; medium, between 3.0 and 2.0; low, between 2.0 and 1.0 and very low, smaller than 1.0 [47]. The Pielou evenness index (J') was 0.7. This value indicates that some species have high densities, and others have few individuals [48]. The species *Ligustrum lucidum* (21.7%), *Inga vera* (17.9%), *Syzygium cumini* (12.8%), *Baccharis semiserrata* (7.7%), *Psidium guajava* (6.35%) and *Allophylus edulis* (5.3%) altogether represented 71.7% of the density of natural regeneration (542 individuals), a fact that explains the low evenness. The analysis of the index of importance value (IIV) shows that the species *Ligustrum lucidum* (30.2%), *Inga vera* (27.4%), *Syzygium cumini* (19.2%), *Baccharis semiserrata* (18%), *Psidium guajava* (14.9%) and

The species *Inga vera* and *Allophylus edulis* had fruits most attractive to frugivorous animals [46, 49]. The presence of *Inga* in the degraded area, for its characteristics, has the ability to form

although with significant differences between the restoration areas and the RA.

which occurs mainly by zoochoric dispersal [23].

502 10 Biodiversity in Ecosystems - Linking Structure and Function

(4.3%), two unidentified (4.3%) and one authochoric (2.1%).

*Allophylus edulis* (12.7%) have the highest values.

natural regeneration.

Ni=number of individuals; Np=number of plots; D=diameter at 5 cm above the soil (cm); H=height (m); RD=relative density; RF=relative frequency; IIV=index of importance value; EG=ecology group; Disp=dispersion; Zoo=zoochoric; Anemo=anemochoric; Baro=barochoric; Auto=authochoric; \*exotic species.

**Table 3.** Main species found in natural regeneration under the canopy of *Inga vera*, in the restoration area.

nuclei of native and exotic species. This formation is mostly attributed to its great attraction to frugivorous vertebrates, primarily birds and bats. Its main attractive features for the fauna are the fleshy and sweet fruits. In addition, the *Inga* species is capable of forming a large crown, serving as a natural perch for birds that end up defecating or regurgitating in the site.

The negative aspect observed in the study was the presence of exotic species, which account for 19.1% of the total number of species in the regeneration areas, however with 43.6% of the number of individuals. It is highlighted the presence of *Ligustrum lucidum*, *Syzygium cumini* and *Psidium guajava*, invasive exotic species with high zoochoric seed dispersion and a high number of individuals (309) and density (40.9%). Conservation units with total protection should be representative of native species and ecosystems, therefore, the existence of invasive exotic species is not desirable nor permitted [50]. The main management strategies involve the eradication and/or control to contain the spread of exotic species, reducing their abundance and their density and/or mitigating their impacts [51].

Additionally, it is possible to affirm that the two areas under restoration (A1 and A2) are returning to natural succession, given that the diversity, structure and ecological processes show a growing trend in relation to the RA. The enzymatic activity can be considered a good indicator of ecological restoration, evidencing that the two areas under restoration resumed the succession process. However, to allow a greater complexity of the ecosystem, the areas should be managed to remove the exotic species.

## **5. Conclusion**

The effectiveness of ecological restoration is largely attributed to the resilience capacity of an ecosystem, to the restoration actions and to the monitoring of recovery indicators. In this sense, the focus on ecological restoration should take into account that the areas are part of an integrated system, requiring the knowledge of its structure and functions for its sustainability, as well as the individual role of each species, especially those that play a fundamental role in strong interactions and in the resumption of ecological succession.

Temporal analysis of ecosystem attributes comprises the basis for the evaluation of the restoration process, also for the comparison of the speed and direction of its performance in different environments and geographical regions. The use of smaller spacing enables faster recovery of altered areas, because the plants shade the soil more quickly, reducing competition for invasive exotic grasses.

It is essential to take into consideration the performance of key species and the arrangements of functional species, because they keep the ecosystem balanced on several levels, both biotic and abiotic. This fact prevents exotic species from becoming invasive by occupying an ecological emptiness (absence of natural predators and competitors) and from settling in areas under the restoration process.

### **Author details**

Suzane Bevilacqua Marcuzzo and Márcio Viera\*

\*Address all correspondence to: marcio.viera@ufsm.br

Universidade Federal de Santa Maria, Silveira Martins, Brasil

### **References**


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**5. Conclusion**

504 12 Biodiversity in Ecosystems - Linking Structure and Function

for invasive exotic grasses.

under the restoration process.

Suzane Bevilacqua Marcuzzo and Márcio Viera\*

\*Address all correspondence to: marcio.viera@ufsm.br

Universidade Federal de Santa Maria, Silveira Martins, Brasil

**Author details**

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April 2014).

The effectiveness of ecological restoration is largely attributed to the resilience capacity of an ecosystem, to the restoration actions and to the monitoring of recovery indicators. In this sense, the focus on ecological restoration should take into account that the areas are part of an integrated system, requiring the knowledge of its structure and functions for its sustainability, as well as the individual role of each species, especially those that play a fundamental role in

Temporal analysis of ecosystem attributes comprises the basis for the evaluation of the restoration process, also for the comparison of the speed and direction of its performance in different environments and geographical regions. The use of smaller spacing enables faster recovery of altered areas, because the plants shade the soil more quickly, reducing competition

It is essential to take into consideration the performance of key species and the arrangements of functional species, because they keep the ecosystem balanced on several levels, both biotic and abiotic. This fact prevents exotic species from becoming invasive by occupying an ecological emptiness (absence of natural predators and competitors) and from settling in areas

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508 16 Biodiversity in Ecosystems - Linking Structure and Function


## **Actions for the Restoration of the Biodiversity of Forest Ecosystems in Cuba**

Eduardo González Izquierdo, Juan A. Blanco, Gretel Geada López, Rogelio Sotolongo Sospedra, Martín González González, Barbarita Mitjans Moreno, Alfredo Jimenez González and José Sánchez Fonseca

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59333

**1. Introduction**

Human will and interests have used landscapes without limits for different purposes, usually for the economic benefit of a minority [1]. Nowadays, the Earth is threatened daily by the degradation of its ecosystems due to fragmentation. One of the main consequences is biodi‐ versity loss. Despite the economic progress and conservation actions carried out in many countries, the planet is losing genuine tropical forest, which is distributed mainly in the "low and middle income countries". The reasons are diverse: inappropriate use of extractive practices in forestry related to wood and non-wood products, land use change when clearing the forest for agriculture and cattle ranching, tourism development, and others. These reasons have facilitated the introduction of new species that then behave as invasive species [2], which usually produce strong competition with local species, reducing biomass and the forest's productivity.

Ecological restoration of disturbed areas is one of the most important and complex issues that forestry faces, due to the lack of knowledge on the ecological functioning of populations, communities, ecosystems, and natural landscapes. In addition, we must consider other components such as social, political, and economic interests of the local communities [3]. In ecological restoration, we need to keep in mind four elements as priorities: to develop the conservation of biodiversity; to maintain human use; to empower the local communities in the management of the area; and, at the same time, to improve the productivity of an ecosystem. Thus, ecological restoration can be considered the main component for conservation and for sustainable management programmes, particularly in tropical areas [4].

© 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Ecosystems can restore themselves if there are no barriers (biotic or abiotic) that hamper the natural process of passive restoration (natural succession). When ecosystems are too degraded they will not overcome such a state over time, and consequently it will be necessary to implement actions to move the ecosystem towards a succession pathway. This is denominated active or assisted restoration [5]. To improve the design of such active restoration programmes, the study of the vegetable communities contributes important data about the phenological and demographical patterns of species, and species suitable for replacement. Such knowledge will allow estimations of how easy it might be to recover and develop the affected ecosystems [6], and how effective the assisted restoration actions might be.

In this chapter we present the results obtained during the restoration of three tropical forests in Cuba: 1) the mesophyll semi-deciduous forest in the western sector of the Biosphere Reserve"Sierra del Rosario" (BRSR); 2) the riverside forest of the Cuyaguateje River in western Cuba; and 3) the exploited native rainforests of the sector Quibiján-Naranjal of the River Toa in eastern Cuba. The BRSR presents a high variety of ecosystems. Several vegetable formations can be distinguished in the reserve [7–8]: evergreen forest, semi-deciduous forest, and pine forests. The largest formation is semi-deciduous forest, with 40–65% of deciduous trees, shrubs, herbs, scarce epiphytes, and an abundance of climbers. The predominant variant is the mesophyll semi-deciduous forest [9]. The 22 ha of the riverside forest of the Cuyaguateje River belonging to the cooperative "Menelao Mora" is placed in the Pinar del Río province. The forest is classified as a typical riverside forest with an arboreal stratum of 15–20 m of shrubs, herbs, scarce epiphytes, and climbers [10]. The native rainforests of the sector Quibiján-Naranjal of Toa are considered to be true rainforests in Cuba [11], where there are not deciduous elements with an abundance of epiphytes with two main tree strata from 20–25 m and 8–15 m.

### **1.1. Problem statement**

The BRSR is classified according to the International Union for the Conservation of the Nature (UICN) as a Protected Area of Managed Resources: which means that this area type is accorded a larger flexibility for management, conservation, and also some productive activities and services, if done in a sustainable way [6]. This forest has been subjected to extensive exploita‐ tion since the sixteenth century, contributing to its degradation and the lack of valuable timber trees and other important species [12]. The riverside forest of the Cuyaguateje was selected because the landownership system (Cooperative farm) supports active agriculture activities. It has the highest degradation grade among the Cuban riverside forests. It is also disturbed by recurrent inundation episodes [13]. The native rainforest was chosen due to its previous intensive exploitation, the current anthropogenic pressure imposed by the adjacent commun‐ ities [14], and its condition as a rainforest from the Sagua-Baracoa region [11].

At all these sites, disturbances can combine and produce many factors modifying the structure, composition, and functioning of populations, communities, and ecosystems [15], thus chang‐ ing the availability of resources and habitats. The identification, characterization, and under‐ standing of the communities or types of forests are fundamental in order to manage and conserve forest biodiversity [16]. However, although there are some studies to help us identify and define types of forests in the Neotropic, the information is still limited and more research is needed in this area [17], especially in the Caribbean tropical forests. Therefore, conservation and restoration programmes need to include diagnosis in their analysis, for the evaluation of the structure of populations, communities, and ecosystems, and their correlation with present and past disturbances. In this research, we introduce such studies for three different Caribbean forest types.

## **2. Material and methods**

### **2.1. Application area**

Ecosystems can restore themselves if there are no barriers (biotic or abiotic) that hamper the natural process of passive restoration (natural succession). When ecosystems are too degraded they will not overcome such a state over time, and consequently it will be necessary to implement actions to move the ecosystem towards a succession pathway. This is denominated active or assisted restoration [5]. To improve the design of such active restoration programmes, the study of the vegetable communities contributes important data about the phenological and demographical patterns of species, and species suitable for replacement. Such knowledge will allow estimations of how easy it might be to recover and develop the affected ecosystems [6],

In this chapter we present the results obtained during the restoration of three tropical forests in Cuba: 1) the mesophyll semi-deciduous forest in the western sector of the Biosphere Reserve"Sierra del Rosario" (BRSR); 2) the riverside forest of the Cuyaguateje River in western Cuba; and 3) the exploited native rainforests of the sector Quibiján-Naranjal of the River Toa in eastern Cuba. The BRSR presents a high variety of ecosystems. Several vegetable formations can be distinguished in the reserve [7–8]: evergreen forest, semi-deciduous forest, and pine forests. The largest formation is semi-deciduous forest, with 40–65% of deciduous trees, shrubs, herbs, scarce epiphytes, and an abundance of climbers. The predominant variant is the mesophyll semi-deciduous forest [9]. The 22 ha of the riverside forest of the Cuyaguateje River belonging to the cooperative "Menelao Mora" is placed in the Pinar del Río province. The forest is classified as a typical riverside forest with an arboreal stratum of 15–20 m of shrubs, herbs, scarce epiphytes, and climbers [10]. The native rainforests of the sector Quibiján-Naranjal of Toa are considered to be true rainforests in Cuba [11], where there are not deciduous elements

with an abundance of epiphytes with two main tree strata from 20–25 m and 8–15 m.

ities [14], and its condition as a rainforest from the Sagua-Baracoa region [11].

The BRSR is classified according to the International Union for the Conservation of the Nature (UICN) as a Protected Area of Managed Resources: which means that this area type is accorded a larger flexibility for management, conservation, and also some productive activities and services, if done in a sustainable way [6]. This forest has been subjected to extensive exploita‐ tion since the sixteenth century, contributing to its degradation and the lack of valuable timber trees and other important species [12]. The riverside forest of the Cuyaguateje was selected because the landownership system (Cooperative farm) supports active agriculture activities. It has the highest degradation grade among the Cuban riverside forests. It is also disturbed by recurrent inundation episodes [13]. The native rainforest was chosen due to its previous intensive exploitation, the current anthropogenic pressure imposed by the adjacent commun‐

At all these sites, disturbances can combine and produce many factors modifying the structure, composition, and functioning of populations, communities, and ecosystems [15], thus chang‐ ing the availability of resources and habitats. The identification, characterization, and under‐ standing of the communities or types of forests are fundamental in order to manage and conserve forest biodiversity [16]. However, although there are some studies to help us identify and define types of forests in the Neotropic, the information is still limited and more research

and how effective the assisted restoration actions might be.

5122 Biodiversity in Ecosystems - Linking Structure and Function

**1.1. Problem statement**

The Biosphere Reserve "Sierra del Rosario" (BRSR) occupies an area of 25,000 ha at 600 metres above sea level (m.a.s.l) in the Artemisa province (western Cuba) from 22°45´–23°00´N to 82°50 ´–83°10´W. It is part of the National System of Protected Area in Cuba [8]. In the BRSR, the semi-deciduous forest has special importance due to its large area. It constitutes the natural vegetation of Cuba, as high as approximately 600 m.a.s.l. Trees reach a height of 20 to 30 m, the canopy is constituted by two arboreal layers and a shrubby understory, with leaves of approximately 13 to 26 cm of longitude, mostly compound. The herbaceous layer is usually missing. The highest trees usually lose their leaves during the driest period, while those of the second arboreal layer usually conserve their leaves for the entire year [10].

The riverside forest of the Cuyaguateje is located in the Guane municipality of Pinar del Rio Province, from 22°11'–22°13´N to 84°03´–84°05´W, at 10 to 30 m.a.s.l. The native rainforests of the sector Quibiján-Naranjal belong to the mountain formation of Nipe-Sagua-Baracoa, in Toa ´s river basin in the Guantánamo province (Figure 1). The research site is in the riverside forests of the Cuyaguateje, in the river´s middle reaches. This forest's limits to the west are marked by the urban perimeter of Guane, to the north by plantations of the Forest Enterprise Macurije, to the south by the Cooperative of Credits and Strengthened Services "Secundino Serrano", and to the east by the end of the Sierra Cerro of Guane.

**Figure 1.** Geographic location of the study cases. BRSR: Biosphere Reserve "Sierra del Rosario".

### **2.2. Field sampling**

First, the study areas were selected as representative units of the described forest type. Later on, sampling plots were chosen where floristic inventories were carried out. Environmental and dasometric variables were also measured. A group of variables related to human interfer‐ ence and its impact on the structure and quality of the forests was assessed, along with the environmentalvariables (soil, elevation, anddistances fromdifferenthumanactivities).Finally, a proposal of an action plan for the conservation and restoration of these forests was designed.

A random stratified design was used for field sampling, setting down 0.1 hectares plots (50 m x 20 m)following the "Methodology of Quick Inventory" [18–19]. In each plot the diameter and height of all the examples of arboreal species (Height > 2 m and over 5 cm of D1.3, diameter at breast height) were identified and measured. Environmental variables considered were: nutrient content of soil (ppm) of Na, Mg, K, and Ca; pH; content of organic matter in soil (MO); anddistancefromthecentreoftheplottotheareasofhumanactivity(cultivatedlands,housings, and tourist facilities). Sampling data were validated using the curved area species method.

Diversity indexes were calculated using the floristic data from the inventory. Beta diversity (β) was estimated using hierarchical cluster analysis, using Sorensen distance (Bray-Curtis). This distance was estimated as the floristic similarity among the identified groups with the previous analysis calculated with Jaccard's index for qualitative data and the Morisita-Horn index for quantitative data. To identify the indicator species of each one of the identified groups through the cluster analysis, the Dufrene and Legendre method was used [20]. Diversity alpha (α) was calculated with the reciprocal of Simpson index (C inv.) [21], and an unbiased estimator of diversity was calculated using the jack-knife technique.

The horizontal structure was described with the relative values of abundance, dominance, and frequency of each species. In addition, the tree diametric class distributions were described for each plot. The ecological importance index value (IVIE), was calculated for each species as the sum of the parameters in the horizontal structure [22]. To describe the relationships among the variables, a principal components analysis (PCA) was performed, while to determine the association among environmental variables with the distribution and abundance of species for plots a canonical correspondence analysis (CCA) was done.

Key or vulnerable species for high-priority consideration in restoration programmes were identified based on their abundance, dominance, commercial wood potential, and dasometric variables. The design of the restoration proposal was based on the approaches of [5] who suggest 13 steps for restoration strategies.

### **3. Results**

### **3.1. Study of case No. 1: Mesophyll semi-deciduous forest of the Biosphere Reserve "Sierra del Rosario" (BRSR)**

We identified 36 families, 75 genera, and 91 species, with a total of 7,799 individuals registered from 30 sampled plots. The endemism rate was 11.24%, a similar value reported for the complete BRSR (from 11 to 34% [7]). The cluster analysis showed the presence of three groups among the plots, according to the flora composition. This result was tested by the MRPP test, which revealed differences among groups (p< 0.001) and supported the classification into three clusters. The analysis of species indicator [18] in each group is shown in Table 1.

**2.2. Field sampling**

5144 Biodiversity in Ecosystems - Linking Structure and Function

First, the study areas were selected as representative units of the described forest type. Later on, sampling plots were chosen where floristic inventories were carried out. Environmental and dasometric variables were also measured. A group of variables related to human interfer‐ ence and its impact on the structure and quality of the forests was assessed, along with the environmentalvariables (soil, elevation, anddistances fromdifferenthumanactivities).Finally, a proposal of an action plan for the conservation and restoration of these forests was designed. A random stratified design was used for field sampling, setting down 0.1 hectares plots (50 m x 20 m)following the "Methodology of Quick Inventory" [18–19]. In each plot the diameter and height of all the examples of arboreal species (Height > 2 m and over 5 cm of D1.3, diameter at breast height) were identified and measured. Environmental variables considered were: nutrient content of soil (ppm) of Na, Mg, K, and Ca; pH; content of organic matter in soil (MO); anddistancefromthecentreoftheplottotheareasofhumanactivity(cultivatedlands,housings, and tourist facilities). Sampling data were validated using the curved area species method.

Diversity indexes were calculated using the floristic data from the inventory. Beta diversity (β) was estimated using hierarchical cluster analysis, using Sorensen distance (Bray-Curtis). This distance was estimated as the floristic similarity among the identified groups with the previous analysis calculated with Jaccard's index for qualitative data and the Morisita-Horn index for quantitative data. To identify the indicator species of each one of the identified groups through the cluster analysis, the Dufrene and Legendre method was used [20]. Diversity alpha (α) was calculated with the reciprocal of Simpson index (C inv.) [21], and an unbiased estimator of

The horizontal structure was described with the relative values of abundance, dominance, and frequency of each species. In addition, the tree diametric class distributions were described for each plot. The ecological importance index value (IVIE), was calculated for each species as the sum of the parameters in the horizontal structure [22]. To describe the relationships among the variables, a principal components analysis (PCA) was performed, while to determine the association among environmental variables with the distribution and abundance of species for

Key or vulnerable species for high-priority consideration in restoration programmes were identified based on their abundance, dominance, commercial wood potential, and dasometric variables. The design of the restoration proposal was based on the approaches of [5] who

**3.1. Study of case No. 1: Mesophyll semi-deciduous forest of the Biosphere Reserve "Sierra**

We identified 36 families, 75 genera, and 91 species, with a total of 7,799 individuals registered from 30 sampled plots. The endemism rate was 11.24%, a similar value reported for the

diversity was calculated using the jack-knife technique.

plots a canonical correspondence analysis (CCA) was done.

suggest 13 steps for restoration strategies.

**3. Results**

**del Rosario" (BRSR)**


**Table 1.** Indicator species for the three groups, ordered by their IVI (p <0.05), obtained in the floristic inventory carried out in the western sector of BRSR.

According to these results, species related to the secondary forest that could be associat‐ ed with a disturbance like timber extraction predominate in groups 1 and 2. Group 3 contained species from preserved sites, which correspond with plots in the Natural Reserve El Mulo. The results of the CCA analysis were globally significant. The first three axes offered a good solution to the ordination of the sampling units and of the species, because due to the present total variability in the data of abundance of the species (inertia = 2.55) it was possible to explain 23.7% by means of the group of this axes. The analyses reveal that the effect of the soil is not significant in the distribution and presence of species and therefore in the classification of the samples. The variable distance to human establish‐ ments has a bigger effect, mainly related with the plots of group 1 that are the furthest away and therefore less affected by the anthropic action. Group 3 is separated by the composition of species in the parcels or plots of the El Mulo located in more conserved area corresponding to the area nucleus of the reserve (Figure 2).

**Figure 2.** Projection of environmental variables, sampling units, and species in the plane defined by the axes CCA1 and CCA2. The continuous explanatory variables are shown as lines, the categorical explanatory variable is indicated by the colour of sampling unit, and the species with the codes given to their names.

The diversity of species and the equitability (alpha diversity) did not show significant differences (p>0.05) among localities. Therefore, in general, both variables can be considered to have high values. Numerically the areas of El Mulo and Mogote have a higher value that corroborates the characteristic vegetation for the complex of vegetation of Mogote [9]. In the case of El Mulo, the category of "Natural Reserve" favours its conservation and therefore displayed a higher diversity value (Table 2).


**Table 2.** Average of dear diversity by means of the method of "Calculation Jump" (jack-knifing) for mesophyll semideciduous forest in the western sector of the BRSR.


**Table 3.** First 15 arboreal species located by their Value of Ecological Importance in mesophyll semi-deciduous forest in the western sector of the BRSR.

### *3.1.1. Horizontal structure*

**Figure 2.** Projection of environmental variables, sampling units, and species in the plane defined by the axes CCA1 and CCA2. The continuous explanatory variables are shown as lines, the categorical explanatory variable is indicated by

The diversity of species and the equitability (alpha diversity) did not show significant differences (p>0.05) among localities. Therefore, in general, both variables can be considered to have high values. Numerically the areas of El Mulo and Mogote have a higher value that corroborates the characteristic vegetation for the complex of vegetation of Mogote [9]. In the case of El Mulo, the category of "Natural Reserve" favours its conservation and therefore

**Sites Simpson (1/C) VPi Equitativity (E) VP**

**Table 2.** Average of dear diversity by means of the method of "Calculation Jump" (jack-knifing) for mesophyll semi-

San Ramón 17.51 ± 3.09 .8510 ± 0.05 Mogote 18.52 ± 8.54 .8521 ± 0.03 Brazo Fuerte 16.73 ± 2.03 .8581 ± 0.03 Los Hondones 16.33 ± 1.05 .8518 ± 0.04 El Mulo 20.31 ± 2.13 .8231 ± 0.06 Average 17.88 ± 3.50 .8500 ± 0.04

the colour of sampling unit, and the species with the codes given to their names.

displayed a higher diversity value (Table 2).

5166 Biodiversity in Ecosystems - Linking Structure and Function

deciduous forest in the western sector of the BRSR.

The tree species with a higher ecological importance were those with a higher frequency (over 60%), so abundance and dominance are more important to the IVIE. *Roystonea regia* appears in the first position as the typical species in this forest. Other species, such as *Trophis racemo‐ sa* and *Matayba apetala,* are important because of their abundances, and *Ficus aurea* for its dominance (Table 3).

In the El Mogote, the species *Guarea guidonia*, *Roystonea regia*, *Bursera simaruba*, and *Matayba apetala* were present in the lowest and the middle parts, showing how their distributions are central to the altitudinal distribution of this formation [10]. The species *Cecropia schreberiana* was located among the most important by its relative dominance. It has very few individuals with small diameters that inhabit the most exposed places to light. This distribution favours the establishment of early secondary communities. Such communities evolve to establish a homeostasis in an approximately ten-year period. Then they stabilize the canopy in places that have suffered natural or anthropogenic disturbances. This behaviour is typical of pioneer species that will be later substituted in the successional process. *Syzygium jambos* is among the most abundant species, and it shows a high migration capacity, confirming their invasive condition. The abundance of these species demonstrates an increase in the populations of this group of plants and they indicate an altered ecological integrity.

Within the species with intermediate abundance, *Calycophyllum candidissimun*, *Dendropanax arboreus*, and *Samanea saman* hold special interest for future conservation strategies. The species *Chione cubensis*, *Lagetta wrightiana*, and *Terminalia chicharronia* (classified as endemic in "Sierra del Rosario") have a low abundance. However, those species were reported as being very abundant in this formation [10]. In our inventories, their presence only in the areas of San Ramón and Brazo Fuerte gave them the classification of being rare species. Among the most dominant species, the high presence of *Ficus aurea* is the outcome of selective felling being carried out in these forests, due to the scarce commercial value of *Erythrina poeppigiana*. *Roystonea regia*, *Mangifera indica*, *Laurocerasus occidentalis, Swietenia mahagoni,* and *Zanthoxylum martinicense* all reached 59% dominance.

The biggest values of basal area (m²/ha) for the mesophyll semi-deciduous forest were found for the western sector of the reserve, in the areas of El Mulo and Brazo Fuerte. The species *Ficus aurea* with 23.7 m²/ha and *Erythrina poeppigiana* with 18.9 m²/ha showed the biggest values in this parameter.

### *3.1.2. Vertical structure*

These forests presented a high height, with two strata whose emergent trees are *Calophyllum antillanun, Andira inermis, Roystonea regia, Pseudolmedia spuria*, and *Matayba apetala*. All these species can reach up to 35 m in the hollows of San Ramón de Aguas Claras, Los Hondones, Brazo Fuerte, and in the low altitudes of the western part of "El Mogote de Soroa". The canopy was composed of individuals with heights from 20 to 30 m, with slight differences between the areas of hillsides and the summits. In the nature reserve El Mulo, the forest has two arboreal floors. The top stratum (more than 25 m in height) contained emergent *Ficus aurea*, *Eritrina poeppigiana*, *Cecropia schreberiana*, *Didymopanax morototoni*, *Trichospermun mexicanum*, and *Roystonea regia*, among other species. The trees in this layer reach up to 30–35 m in height. The intermediate stratum of mesophyll semi-deciduous forest in the studied areas is occupied by trees between 15 to 10 m tall. The lower stratum was integrated by evergreen species that reached heights of 6 to 12 m. The lower stratum is composed of juvenile individuals of the most abundant and frequent species, such as: *Trophis racemosa*, *Guarea guidonia, Bursera simaruba, Pseudolmedia spuria, Syzygium jambos, Calophyllum antillanun*, and *Dendropanax cuneifolius*. Trees in the lower stratum are usually younger individuals. Regeneration is fundamentally of species typical of secondary forests, except in El Mulo where *Matayba apetala* had regenerated. The similar abundance of sharing species among strata of the forest (Table 4) was determined by the Morisita-Horn index giving analogous values (≥ 80 %).


**Table 4.** Morisita-Horn index of the components of the vertical structure of mesophyll semi-deciduous forest

### *3.1.3. Disturbances and relationship with the forest status*

Within the species with intermediate abundance, *Calycophyllum candidissimun*, *Dendropanax arboreus*, and *Samanea saman* hold special interest for future conservation strategies. The species *Chione cubensis*, *Lagetta wrightiana*, and *Terminalia chicharronia* (classified as endemic in "Sierra del Rosario") have a low abundance. However, those species were reported as being very abundant in this formation [10]. In our inventories, their presence only in the areas of San Ramón and Brazo Fuerte gave them the classification of being rare species. Among the most dominant species, the high presence of *Ficus aurea* is the outcome of selective felling being carried out in these forests, due to the scarce commercial value of *Erythrina poeppigiana*. *Roystonea regia*, *Mangifera indica*, *Laurocerasus occidentalis, Swietenia mahagoni,* and *Zanthoxylum*

The biggest values of basal area (m²/ha) for the mesophyll semi-deciduous forest were found for the western sector of the reserve, in the areas of El Mulo and Brazo Fuerte. The species *Ficus aurea* with 23.7 m²/ha and *Erythrina poeppigiana* with 18.9 m²/ha showed the biggest values

These forests presented a high height, with two strata whose emergent trees are *Calophyllum antillanun, Andira inermis, Roystonea regia, Pseudolmedia spuria*, and *Matayba apetala*. All these species can reach up to 35 m in the hollows of San Ramón de Aguas Claras, Los Hondones, Brazo Fuerte, and in the low altitudes of the western part of "El Mogote de Soroa". The canopy was composed of individuals with heights from 20 to 30 m, with slight differences between the areas of hillsides and the summits. In the nature reserve El Mulo, the forest has two arboreal floors. The top stratum (more than 25 m in height) contained emergent *Ficus aurea*, *Eritrina poeppigiana*, *Cecropia schreberiana*, *Didymopanax morototoni*, *Trichospermun mexicanum*, and *Roystonea regia*, among other species. The trees in this layer reach up to 30–35 m in height. The intermediate stratum of mesophyll semi-deciduous forest in the studied areas is occupied by trees between 15 to 10 m tall. The lower stratum was integrated by evergreen species that reached heights of 6 to 12 m. The lower stratum is composed of juvenile individuals of the most abundant and frequent species, such as: *Trophis racemosa*, *Guarea guidonia, Bursera simaruba, Pseudolmedia spuria, Syzygium jambos, Calophyllum antillanun*, and *Dendropanax cuneifolius*. Trees in the lower stratum are usually younger individuals. Regeneration is fundamentally of species typical of secondary forests, except in El Mulo where *Matayba apetala* had regenerated. The similar abundance of sharing species among strata of the forest (Table 4) was determined by the Morisita-Horn index giving analogous values (≥ 80 %).

> **D1,3 <5 cm height ≥1,5 m**

D1,3 <5 cm height <1,5 m 0,92 0,87 0,80 D1,3 <5 cm height ≥1,5 m 0,90 0,85 D1,3 ≥5 ≤ 10 cm height ≥1,5 m 0,80

**Table 4.** Morisita-Horn index of the components of the vertical structure of mesophyll semi-deciduous forest

**D1,3 ≥5 ≤ 10 cm height ≥1,5 m**

**D1,3 ≥10 cm height "/ >1,5 m**

**D1,3 <5 cm height <1,5 m**

*martinicense* all reached 59% dominance.

5188 Biodiversity in Ecosystems - Linking Structure and Function

in this parameter.

*3.1.2. Vertical structure*

D1,3 ≥10 cm height "/>1,5 m

Ecological disturbances were classified according to their intensity in a scale from 1 to 4, where 1 = without disturbance; 2 = light; 3 = moderate; and 4 = high disturbance. Selective felling, alterations for the construction of roads, clearings, and the felling of trees due to winds, firewood extraction, and for other non-timber forest products were evaluated according to this scale. It was proven that the anthropogenic alterations prevailed: the most intense were related with selective felling, one of the factors that alters the dynamics of the regeneration more than others, changing the structure and composition of the forest.

Results of the principal components analysis were displayed on a correlation matrix between variables describing disturbance and variables describing species structure (Table 5). This table reveals that the first three orthogonal components explain 67% of the present variability. The variables that contributed more to the segregation of the components were: maximum number of individuals, selective felling, total number of individuals, and dominance. The first compo‐ nentrevealstheinverserelationshipbetweenspeciesnumberandbasalareaversusenvironmen‐ tal variables such as the distance of the sampling places from the populated areas and forest clearings. The second and third components confirmed the direct relationship between the quantity ofindividuals and variables such as the intensity of selective felling, extraction of nontimber forest products, and road construction. The high density of individuals in the pertur‐ bedplacesisrelatedtocanopyopeningandhighregenerationofheliophill(suntolerant)species, which usually have small diameters and therefore low values of basal area.


**Table 5.** Main components analysis based on the correlation matrix between the disturbance variables and structural variables.

The relationship among sites, species, and some environmental variables indicates that *Swietenia mahagoni*, *Oxandra lanceolata*, *Tabebuia shaferi*, and *Caesalpinia bahamensis*, among others, reached the biggest values of abundance in environments with low disturbance. This fact indicates that these taxa are characteristic of places only slightly altered, like in the parcels of El Mulo.

Figure 3 shows the results of classifying the sampling units (plots) according to their disturb‐ ance grade.

**Figure 3.** Projection of sampling units (squares) and species (asterisks) in the plane defined by the first two axes of the ACP. The continuous explanatory variables are shown as lines and the categorical explanatory variable is shown ac‐ cording to the colour of the symbol of the sampling unit. Sampling places: (sr1-sr6) — plots of San Ramón; mg1-mg6 plots of El Mogote; bf1-bf6 — plots of Brazo Fuerte; lh1 a lh6 — plots of Los Hondones; eml1-eml6 — plots of El Mulo. Variables: Dist — distances to populational establishments and other human activities; AB — Basal area; Cam roads; AL — height of sea level; 1/D — diversity; TS — selective felling; Esp — specie richness; Ind — individuals' maximum number; PFNM — Non-timber forest products; Cla — Forest spacements. Species codes: (*Eugeni — Eugenia maleolens*); (*Caesal — Caesalpinia bahamensis*); (*Tabebu — Tabebuia shaferi*); (*Pithec — Pithecellobium arboreum*); (*Oxandr — Oxandra lanceolata*); (*Poepi — Poeppigia procera*); (*Cedrel — Cedrela odorata*); (*Comocl — Comocladia dentata*); (*Lauroc — Laurocerasus occidentalis*); (*Sweten — Swietenia mahagoni*)*;* (*Matayd — Matayba domingensis*); (*Cupani — Cupania ameri‐ cana*)*;* (*Trophi — Trophis racemosa*); (*Cecrop — Cecropia shreberiana*)*;* (*Erythr — Erythroxyllum havanense*); (*Spondi — Spon‐ dias mombin*)*;* (*Trichi — Trichilia havanensis*); (*Dendro — Dendropanax arboreus*).

Secondary species characteristic of mesophyll semi-deciduous forest that generally have little commercial value, such as *Matayba apetala* and *Trophis racemosa,* were more abundant in places with moderate to high disturbance levels. These sites coincide with the plots in Brazo Fuerte, Los Hondones, and San Ramón, characterized by the presence of the biggest diversity alpha, and the largest presence of species and abundance. According to these results the hypothesis of intermediate disturbance is corroborated [23]. Such a hypothesis states that the opening of forest gaps favours a much higher level of diversity (at local and regional scales) that would be presented if they lacked those disturbances.

The relationship among sites, species, and some environmental variables indicates that *Swietenia mahagoni*, *Oxandra lanceolata*, *Tabebuia shaferi*, and *Caesalpinia bahamensis*, among others, reached the biggest values of abundance in environments with low disturbance. This fact indicates that these taxa are characteristic of places only slightly altered, like in the parcels

Figure 3 shows the results of classifying the sampling units (plots) according to their disturb‐

**Figure 3.** Projection of sampling units (squares) and species (asterisks) in the plane defined by the first two axes of the ACP. The continuous explanatory variables are shown as lines and the categorical explanatory variable is shown ac‐ cording to the colour of the symbol of the sampling unit. Sampling places: (sr1-sr6) — plots of San Ramón; mg1-mg6 plots of El Mogote; bf1-bf6 — plots of Brazo Fuerte; lh1 a lh6 — plots of Los Hondones; eml1-eml6 — plots of El Mulo. Variables: Dist — distances to populational establishments and other human activities; AB — Basal area; Cam roads; AL — height of sea level; 1/D — diversity; TS — selective felling; Esp — specie richness; Ind — individuals' maximum number; PFNM — Non-timber forest products; Cla — Forest spacements. Species codes: (*Eugeni — Eugenia maleolens*); (*Caesal — Caesalpinia bahamensis*); (*Tabebu — Tabebuia shaferi*); (*Pithec — Pithecellobium arboreum*); (*Oxandr — Oxandra lanceolata*); (*Poepi — Poeppigia procera*); (*Cedrel — Cedrela odorata*); (*Comocl — Comocladia dentata*); (*Lauroc — Laurocerasus occidentalis*); (*Sweten — Swietenia mahagoni*)*;* (*Matayd — Matayba domingensis*); (*Cupani — Cupania ameri‐ cana*)*;* (*Trophi — Trophis racemosa*); (*Cecrop — Cecropia shreberiana*)*;* (*Erythr — Erythroxyllum havanense*); (*Spondi — Spon‐*

Secondary species characteristic of mesophyll semi-deciduous forest that generally have little commercial value, such as *Matayba apetala* and *Trophis racemosa,* were more abundant in places with moderate to high disturbance levels. These sites coincide with the plots in Brazo Fuerte,

*dias mombin*)*;* (*Trichi — Trichilia havanensis*); (*Dendro — Dendropanax arboreus*).

of El Mulo.

520 10 Biodiversity in Ecosystems - Linking Structure and Function

ance grade.

On the other hand, the species *Swietenia mahagoni* and *Caesalpinia bahamensis* have a perfect correlation with sites with the lowest disturbance level, according to the test of Dufrene and Legendre [20]. Such correlation was demonstrated in the field, as these species were located very close to the plots of El Mulo. The opposite result was found for *Cupania americana* and *Cecropia schreberiana*, which were mostly present in sites with a high degree of disturbance. They were observed very near the most perturbed places of Brazo Fuerte, Los Hondones, El Mogote, and San Ramón.

In accordance with the results, indicator species were not present under conditions of moderate disturbance. Such species are fundamentally pioneer species of very wide distribution that surpass different ecological conditions, related with the alteration of environment. Indicator species with a significance level (p <0.05) are shown in Table 6. *Swietenia mahagoni* and *Caesalpinia bahamensis* could be considered as perfect indicators of the lowest disturbance level. On the other hand, *Cupania americana* and *Cecropia schreberiana* were the best indicators of a high degree of disturbance.


**Table 6.** Lists of the main indicator species ordered for IVI (p <0.05) according to the disturbance level.

### *3.1.4. Diameter structure of forest species in the reserve*

The number of woody species of local and commercial interest was reduced, and their diameter distributions presented few individuals in superior categories (Table 7). This can be the result of selective commercial logging, described as one of the main disturbances in the region. These results corroborate those outlined in [24], for "Sierra del Rosario". These authors concluded that in that region, only a few individuals end up having diameters bigger than 20 cm, due to topography and shallow soils. Although the diversity of trees is high, the abundance of forestry species' regeneration with commercial value is low in the mesophyll semi-deciduous forest of the reserve.


**Table 7.** Structure of the diameter class of arboreal species with more than 100 individuals in the sampling places in the western sector of the BRSR.

It seems that in the reserve there is a considerable quantity of species tolerant to disturbances, such as *Talipariti elatum, Bursera simaruba, Calophyllum antillanun, Laurocerasus occidentalis*, and *Guarea guidonia*. They regulate the diametric structure that favours their presence in the forest. This phenomenon could indicate their possible use in reforestation programmes. On the other hand, species of high commercial value like *Swietenia mahagoni* and *Cedrela odorata* are only represented by 28 and 45 individuals, respectively. The stand diametric structure reveals very few individuals in the regeneration category, and also a very minor presence in other diametric classes. This situation puts the future existence of these species at risk.

### *3.1.5. Indicator species*

The regular form in the diametric distribution observed in *Matayba apetala*, *Guarea guidonia*, *Bursera simaruba*, and *Calophyllum antillanun*, with an abundance of juvenile individuals in the inferior categories, suggests tolerance to the competition caused by disturbances in the forest. Therefore, some of these species could be incorporated into a monitoring programme for these ecosystems. Due to their quick growth, they could also be considered for inclusion in a restoration programme in the region. In this context, among the arboreal species suggested as key species are: *Guarea guidonia, Matayba apetala, Pseudolmedia spuria, Calophyllum antillanun, Laurocerasus occidentalis, Mangifera indica, Cecropia schreberiana,* and *Bursera simaruba.* These species possess additional attributes that allow them to provide stability to the ecosystem before the disturbances [21]. The approaches that endorse this selection are related in the following.

Large trees of *Mangifera indica* found in San Ramón de Aguas Claras, El Mogote, Brazo Fuerte, and Los Hondones support a high epiphytic diversity, with flowers like orchids, bromeliads, and others. In addition, such epiphytes are also an important element for wildlife food sources (mainly birds and small mammals), whose populations could be at risk in this reserve. Many fruits are also collected by the residents of the local communities for their own consumption. In "Sierra del Rosario", the presence of *Cecropia schreberiana* allows the establishment of early secondary communities. Such communities develop a homeostasis in around a 10-year cycle, stabilizing the canopy in places that have suffered natural or anthropogenic disturbances. Other species like *Trophis racemosa* and *Syzygium jambos* could be suggested as indicator species of highly disturbed forests in this region. *Trophis racemosa* is located mainly in the medium to high altitudes, while *Syzygium jambos* is distributed in the medium to low areas near rivers or streams.

### *3.1.6. Vulnerable species*

of selective commercial logging, described as one of the main disturbances in the region. These results corroborate those outlined in [24], for "Sierra del Rosario". These authors concluded that in that region, only a few individuals end up having diameters bigger than 20 cm, due to topography and shallow soils. Although the diversity of trees is high, the abundance of forestry species' regeneration with commercial value is low in the mesophyll semi-deciduous forest of

*Guarea guidonia* 471 346 67 35 10 6 2 1 2 1 1 *Bursera simaruba* 420 188 172 44 9 3 2 2 *Calophyllum antillanum* 347 254 48 27 10 2 3 1 1 1

*Mangifera indica* 130 56 3 7 4 7 31 8 2 7 5 *Zanthoxylum martinicense* 122 52 20 21 21 3 2 1 2

**Table 7.** Structure of the diameter class of arboreal species with more than 100 individuals in the sampling places in

It seems that in the reserve there is a considerable quantity of species tolerant to disturbances, such as *Talipariti elatum, Bursera simaruba, Calophyllum antillanun, Laurocerasus occidentalis*, and *Guarea guidonia*. They regulate the diametric structure that favours their presence in the forest. This phenomenon could indicate their possible use in reforestation programmes. On the other hand, species of high commercial value like *Swietenia mahagoni* and *Cedrela odorata* are only represented by 28 and 45 individuals, respectively. The stand diametric structure reveals very few individuals in the regeneration category, and also a very minor presence in other diametric

The regular form in the diametric distribution observed in *Matayba apetala*, *Guarea guidonia*, *Bursera simaruba*, and *Calophyllum antillanun*, with an abundance of juvenile individuals in the inferior categories, suggests tolerance to the competition caused by disturbances in the forest. Therefore, some of these species could be incorporated into a monitoring programme for these ecosystems. Due to their quick growth, they could also be considered for inclusion in a restoration programme in the region. In this context, among the arboreal species suggested as key species are: *Guarea guidonia, Matayba apetala, Pseudolmedia spuria, Calophyllum antillanun, Laurocerasus occidentalis, Mangifera indica, Cecropia schreberiana,* and *Bursera simaruba.* These

**Number of trees for diameter class d(1,3) (cm) Total 2,5–9 10–19 20–29 30–39 40–49 50–59 60–69 70–79 80–89 90–99 ≥100**

the reserve.

**Species**

the western sector of the BRSR.

*3.1.5. Indicator species*

*Matayba apetala* 502 333 128 40 1

522 12 Biodiversity in Ecosystems - Linking Structure and Function

*Andira inermis* 189 111 51 22 5 *Oxandra lanceolata* 149 99 30 12 6 2 *Laurocerasus occidentalis* 141 91 32 12 4 1 1

*Trichospermun mexicanum* 206 57 89 42 14 3 1

*Talipariti elatum* 116 62 19 12 7 11 2 3

classes. This situation puts the future existence of these species at risk.

In an alarming way, individuals of some commercially important species such as *Lagetta wrightiana* and *Terminalia chicharronia,* which were previously plentiful in these forests (as local residents remember), were present only in the inventories of San Ramón de Aguas Claras and Brazo Fuerte, respectively. For the last species, individuals were not observed in natural regeneration inside the sampled plots. This result supports its consideration of species under threat, according to the species Red List of Cuba [9].

### *3.1.7. Restoration proposal*

The purpose of the proposal is to suggest a group of actions to guide restoration and conservation of forests in the western sector of the BRSR and adjacent areas. In the elaboration of this proposal, the approaches by [5] have been considered. These authors suggest 13 steps or main elements to consider in the elaboration of the plan. These are:


According to the previous steps, the actions for the restoration have been based on the following aspects: 1) it has been kept in mind the previous main scientific research studies carried out in the area that today occupies the Biosphere Reserve of "Sierra del Rosario". Among these, the book *Ecology of Rainforests of Sierra del Rosario* [7] constitutes a summary of the main research carried out in this ecosystem. Other important studies considered aspects of the geology in relation with the presence of hydrocarbons in the eastern part of the reserve [26], agrobiodiversity that the farmers manage in homemade orchards and properties in protected areas [27], and restoration of arboreal diversity of rainforests in the reserve [6]. Also, analysis of research needs in the protected area [30], and the floristic characterization of mesophyll semi-deciduous forest in the western sector of the BRSR, as well as a group of indicator environmental variables of disturbances.

When proposing the restoration plan, we also kept in mind the results of floristic inventories carried out in the Biosphere Reserve of "Sierra del Rosario", as well as the impacts of the traditional extraction of products of forest and other land uses. We also tried to incorporate the perceptions and identification of the environmental services of forest by the local residents of the reserve, according to the approaches of [28]. Opinions of the technical staff of the Ecological Station (the state entity responsible for the protection of the BRSR), and recommen‐ dations of experts on the basic approaches for the conservation and the sustainable forest administration [27, 6] were also taken into account. In addition, guidelines by International Organization of Tropical Wood for restoration, ordination, and rehabilitation of secondary and degraded tropical forests [29], as well as recommendations on the Methodology for the Elaboration of Management Plans for Protected Areas of Cuba [30], were incorporated. Finally, the Management Plan of the Biosphere Reserve of "Sierra del Rosario" for the period 2011– 2015 and the operative Plan of the Reserve were consulted [8].

After this review, it was determined that the main barriers to the restoration are:


Recommended actions for forest restoration:

**•** Adoption of modern silviculture techniques, such as favouring passive reforestation (natural regeneration), enrichment of the natural forest, reforestation with native species, and implementation of agroforestry or silvopastoral systems.


### **3.2. Study of case No. 2: Riparian forest of the River Cuyaguateje**

### *3.2.1. Biodiversity*

**10.** To select the intervention sites;

**12.** Monitoring the restoration processes;

524 14 Biodiversity in Ecosystems - Linking Structure and Function

**13.** To consolidate the restoration process.

indicator environmental variables of disturbances.

2015 and the operative Plan of the Reserve were consulted [8].

and implementation of agroforestry or silvopastoral systems.

ing, and road construction.

Recommended actions for forest restoration:

After this review, it was determined that the main barriers to the restoration are:

value, and gaps in the forest as a result of the wind and the falling of trees.

**•** Natural barriers: dominance of species with little commercial value, invasion of exotic species, irregularities in the diameter classes in distribution of species of high commercial

**•** Social barriers: selective logging, firewood extraction, non-timber forest products harvest‐

**•** Adoption of modern silviculture techniques, such as favouring passive reforestation (natural regeneration), enrichment of the natural forest, reforestation with native species,

**11.** To design strategies to overcome the barriers to the restoration;

According to the previous steps, the actions for the restoration have been based on the following aspects: 1) it has been kept in mind the previous main scientific research studies carried out in the area that today occupies the Biosphere Reserve of "Sierra del Rosario". Among these, the book *Ecology of Rainforests of Sierra del Rosario* [7] constitutes a summary of the main research carried out in this ecosystem. Other important studies considered aspects of the geology in relation with the presence of hydrocarbons in the eastern part of the reserve [26], agrobiodiversity that the farmers manage in homemade orchards and properties in protected areas [27], and restoration of arboreal diversity of rainforests in the reserve [6]. Also, analysis of research needs in the protected area [30], and the floristic characterization of mesophyll semi-deciduous forest in the western sector of the BRSR, as well as a group of

When proposing the restoration plan, we also kept in mind the results of floristic inventories carried out in the Biosphere Reserve of "Sierra del Rosario", as well as the impacts of the traditional extraction of products of forest and other land uses. We also tried to incorporate the perceptions and identification of the environmental services of forest by the local residents of the reserve, according to the approaches of [28]. Opinions of the technical staff of the Ecological Station (the state entity responsible for the protection of the BRSR), and recommen‐ dations of experts on the basic approaches for the conservation and the sustainable forest administration [27, 6] were also taken into account. In addition, guidelines by International Organization of Tropical Wood for restoration, ordination, and rehabilitation of secondary and degraded tropical forests [29], as well as recommendations on the Methodology for the Elaboration of Management Plans for Protected Areas of Cuba [30], were incorporated. Finally, the Management Plan of the Biosphere Reserve of "Sierra del Rosario" for the period 2011–

For alpha diversity, floristic inventories in both borders of the studied area were done every 323 m and natural regeneration was estimated. The specie richness was 38 species, including 21 families and 36 genera. Table 8 shows the 860 individuals of the species (> 2 m of height). Similar results were reported in previous studies [31–32] and also referred to by local farmers since the 1970s. The most representative species found were *Bambusa vulgaris*, *Guazuma ulmifolia*, *Samanea saman*, *Sapindus saponaria*, *Lonchocarpus domingensis*, *Spondias mombin*, *Roystonea regia*, *Trichilia hirta*, and *Bursera simaruba*. Natural regeneration in passive restoration allows abundant recruitment of autochthonous species such as *G. ulmifolia, S. saponaria, L. domingensis, T. citrifolia, S. mahagoni, T. hirta, T. elatum,* and *S. mombin*. These species can create more suitable habitats for other typical species, reducing the impacts of human activities [33] and increasing ecological resilience.



**Table 8.** Arboreal and shrub species identified in the area in the riversides of the River Cuyaguateje (> 2 m height).

During the first year (2000) the area could be recognized by the presence of scarce trees of eight species along the riverside. Figure 4 illustrates how specie richness increased during the rehabilitation process, simultaneously with the reduction of the human cultivation practices, extensive shepherding, and sand extraction from the riverbed.

**Figure 4.** Specie richness trends during the period (2000–2010) according to [13].

Table 9 represents biodiversity expressed by Simpson's index and its reciprocal in each research plot. The highest values of diversity corresponded to plots 3, 5, and 8 in the border 1, and plots 18, 24, 25, and 30 in the border 2. These plots correspond to locations where local farmers had implemented forest rehabilitation measures by themselves. Generally speaking, biodiversity values per plot varied from 1.29 to 12.61 in border 1, and from 0.62 to 14.25 in border 2. Such a trend clearly shows the differences among sites with and without human activity in both borders, since the topography and soils are similar in the whole studied area.

**Species Individuals Dr Species Individuals Dr**

ex DC.

*Andira inermis* (W. Wright) Kunth

**Total 860 100**

4 0,47

*Gmelina arborea* Roxb 34 3,95 *Terminalia catappa* L 6 0,70

*Spondias mombin* L 26 3,02 *Casearia hirsuta* Sw 3 0,35

*Guarea guidonia* L. Sleumer 21 2,44 *Melicoccus bijugatus* Jacq 3 0,35

*Cordia collococca* L 17 1,98 *Annona reticulata* L 2 0,23

*Cedrela odorata* L 16 1,86 *Comocladia dentata* Jacq 2 0,23

*Gerascanthus gerascanthoides* L. 16 1,86 *Cupania americana* L. 2 0,23

Arm 16 1,86 *Cocos nucifera*<sup>L</sup> 1 0,12

*Acacia mangium* Willd. 15 1,74 *Khaya senegalensis* Desr (A. Juss.) 1 0,12

**Table 8.** Arboreal and shrub species identified in the area in the riversides of the River Cuyaguateje (> 2 m height).

extensive shepherding, and sand extraction from the riverbed.

**Figure 4.** Specie richness trends during the period (2000–2010) according to [13].

During the first year (2000) the area could be recognized by the presence of scarce trees of eight species along the riverside. Figure 4 illustrates how specie richness increased during the rehabilitation process, simultaneously with the reduction of the human cultivation practices,

*Talipariti elatum* Frixell (Sw.) 32 3,72

526 16 Biodiversity in Ecosystems - Linking Structure and Function

*Dichrostachys cinerea* (L) Wigth et


**Table 9.** Dominance index and their reciprocal one, of the individuals with d1.3≥ 2.5 cm for plots in each border

The plots with the highest diversity values (8, 18, 24, 25, and 30) could be used as examples of the expected restoration targets for riparian forests in terms of floristic composition. However, they show some signs of past anthropogenic intervention. Ecologically speaking, these plots form a complex mosaic as a result of the processes that favour ecological resilience, thus increasing biodiversity values.

As for beta-diversity and Jaccard´s index of similarity, they are very important for assessing the degree of similarity among communities and the degree of exclusion between two species within the same community, especially when the species become dominant [34–35]. Jaccard's index indicates similarity between rehabilitated borders (0.78) that have 29 species in common (Table 10). Indeed, the high value in flora similarity between borders (0.78) is probably due to the response to similar climatic factors (temperature, humidity, and precipitation), soil type, and latitudinal position, while the differences could be related to structural elements of common species.


**Table 10.** Species in common in both borders that been rehabilitated.

In addition, another element that should be considered in support of this analogy is the occurrence of floods that favour seed dispersion and natural regeneration of pioneer species, while reducing anthropogenic pressure and the presence of typical vegetation such as *G. ulmifolia*, *L. domingensis, T. citrifolia, T. hirta, S. mombin*, and *S. saponaria*. Among both com‐ munities (rehabilitated and control sites) an index of similarity of 0.28 with 14 common species was reported (Table 11). The small similarity between the control and rehabilitated sites could be caused by the short time of the rehabilitation process, the differences include the environ‐ mental conditions, and the human cultivation activities that enhance the presence of species, many of which exhibit invasive behaviour.

If agriculture, extensive shepherding, and sand extraction activities were controlled, while local actors managed the natural regeneration by increasing species numbers (even with exotic species), better ecological conditions will develop in the long term for the transition towards a rehabilitated site, improving the ecosystem's functionality. In addition, such favourable conditions (fertility, humidity, and deposition of seeds) for natural regeneration and the plantation of species like *T. elatum* and *S. mahagoni* would improve the ecosystem's produc‐ tivity. In this sense, in some cases ecosystems degraded anthropogenically can be restored when the external stresses are reduced, with the reintroduction of native species, the removal of the exotic species, and the beginning of the passive restoration processes [36].

within the same community, especially when the species become dominant [34–35]. Jaccard's index indicates similarity between rehabilitated borders (0.78) that have 29 species in common (Table 10). Indeed, the high value in flora similarity between borders (0.78) is probably due to the response to similar climatic factors (temperature, humidity, and precipitation), soil type, and latitudinal position, while the differences could be related to structural elements of

**Number Species Number Species** 1 *Acacia mangium* Willd 16 *Melicoccus bijugatus* Jacq. 2 *Andira inermis* (W. Wright) Kunth ex DC. 17 *Psidium guajava* L.

 *Bambusa vulgaris* Schrader ex Wendland 19 *Samanea saman* Jacq. *Bursera simaruba* (L) Sargent. 20 *Sapindus saponaria* L. *Casearia hirsuta* Sw 21 *Simaruba glauca* D.C. *Cordia collococca* L 22 *Spondias mombin* L *Cupania americana* L. 23 *Swietenia mahagoni* L *Dichrostachys cinerea* (L) Wigth et Arm. 24 *Swietenia macrophyla* King. *Gerascanthus gerascanthoides* L. 25 *Tabernaemontana citrifolia* L. *Gmelina arborea* Roxb. 26 *Talipariti elatum* Frixell (Sw)

12 *Guarea guidonia* L. Sleumer 27 *Terminalia catappa* L 13 *Guazuma ulmifolia* Lam. 28 *Trichilia havanensis* Jacq.

In addition, another element that should be considered in support of this analogy is the occurrence of floods that favour seed dispersion and natural regeneration of pioneer species, while reducing anthropogenic pressure and the presence of typical vegetation such as *G. ulmifolia*, *L. domingensis, T. citrifolia, T. hirta, S. mombin*, and *S. saponaria*. Among both com‐ munities (rehabilitated and control sites) an index of similarity of 0.28 with 14 common species was reported (Table 11). The small similarity between the control and rehabilitated sites could be caused by the short time of the rehabilitation process, the differences include the environ‐ mental conditions, and the human cultivation activities that enhance the presence of species,

If agriculture, extensive shepherding, and sand extraction activities were controlled, while local actors managed the natural regeneration by increasing species numbers (even with exotic species), better ecological conditions will develop in the long term for the transition towards

14 *Lonchocarpus domingensis* (Pers). DC. 29 *Trichilia hirta* L.

**Table 10.** Species in common in both borders that been rehabilitated.

many of which exhibit invasive behaviour.

3 *Anonna reticulata* L 18 *Roystonea regia* HBK O. F. Cook.

common species.

528 18 Biodiversity in Ecosystems - Linking Structure and Function

15 *Mangifera indica* L.


**Table 11.** Species identified in the study area (rehabilitated and control)

Figures 5 and 6 show a diagram of range/abundance of the species in the borders. At both sites, the highest abundance value corresponds to *S. jambos*, which in Cuba is an invasive species linked to human activities. This species is a fruit-bearing shrub introduced in Cuba. It later colonized some mountainous areas along riversides and constitutes a serious obstacle for reforestation.

**Figure 5.** Diagram of the range/abundance of identified species in riversides (1 and 2) of the Cuyaguateje's riversides according to [13].

**Figure 6.** Diagram of the range/abundance for the 15 more representative species of the area that is rehabilitated in borders (1 and 2) of the Cuyaguateje's riversides according to [13]

### *3.2.2. Forest structure*

Figures 5 and 6 show a diagram of range/abundance of the species in the borders. At both sites, the highest abundance value corresponds to *S. jambos*, which in Cuba is an invasive species linked to human activities. This species is a fruit-bearing shrub introduced in Cuba. It later colonized some mountainous areas along riversides and constitutes a serious obstacle for

**Figure 5.** Diagram of the range/abundance of identified species in riversides (1 and 2) of the Cuyaguateje's riversides

**Figure 6.** Diagram of the range/abundance for the 15 more representative species of the area that is rehabilitated in

borders (1 and 2) of the Cuyaguateje's riversides according to [13]

reforestation.

530 20 Biodiversity in Ecosystems - Linking Structure and Function

according to [13].

Table 12 shows the results of horizontal structural parameters of rehabilitated areas under local communities' participation (dominance (D), abundance (A), and frequency (F)), and the ecological importance value index (IVIE) of the species in each border. The species with low IVIE are those typical of the riparian forest, such as: *B. simaruba, A. inermis*, *C. dentata, C. americana, S. mahagoni*, and *R. regia.* According to their relative abundance, the species most sensitive to environmental or anthropogenic disturbances were identified: *A. inermis, C. dentata, S. macrophyla, S. mahagoni, A. reticulata*, and *R. regia*. This parameter can be used as an indicator of the degrading process [34, 37]. Similarly, in border 2 the species with low IVIE had more commercial importance, such as *G. arborea, S. saman*, *G. ulmifolia*, *L. domingensis, S. mahagoni, T. elatum, S. saponaria*, and *R. regia* (Table 12). In the case of *G. arborea,* the value of the IVIE was due to its dominance. This species is not recommended for planting along riversides because it is considered as potentially invasive [38]. It is also not recommended for planting in sites prone to floods due its low survival rate under such conditions.



**Table 12.** Phytosociological Parameters of the riparian forest of the River Cuyaguateje, border (1 and 2). Dr = Relative Dominance; Fr = Relative Frequency; Ar = Relative Abundance; IVIE = Ecological Importance Value Index

Fruit tree species were present with very low values in frequency, dominance, and abundance. Only *P. guajava, M. indica, A. reticulata*, and *M. bijugatus* were observed. Local farmers did not accept *M. bijugatus* because this species is a potentially invasive species [38]. The scarcity in fruits could also be related to the low germination and development rates of *Pouteria cam‐ pechiana* (canistel) and *Calocarpum sapota* (Red Mammee) and the low presence of this species in natural areas. Incorporating fruit trees to reforestation plans could be used as an incentive for local farmers to protect riversides.

Natural regeneration reflects ecosystem fitness. Our results show a good condition with 3,952 in border 1 and 4,564 seedlings in border 2. Nonetheless, it is important to compare the species in the upper canopy stratum with those that are regenerating because their relative frequencies are directly associated to successional processes [36]. Our results indicate that favourable conditions exist for the regeneration and the recruitment of arboreal and shrub species that can increase or diminish in the measure that restrictive factors changes. Logically, it is also related to the approval of local farmers of rehabilitation processes [13].

At both borders, regenerated individuals in the herbaceous stratum were found for *G. ulmifolia, S. saman, L. domingensis, S. saponaria, G. guidonia, R. regia, T. citrifolia, S. mombin, S. saponaria, T. elatum, C. collococca, L. domingensis*, and *B. simaruba*, which are typical species of this forest type. The relative natural regeneration (RNRi) index, which combines abundance and frequency, showed the higher values for *T. citrifolia, S. saman, G. ulmifolia, S. mombin, L. domingensis*, and *S. saponaria*. Of the nine species that were used at the beginning of the reforestation [39] only four were presented in this stratum: *G. arborea, T. elatum, M. indica*, and *P. guajava*. However, very good germination rates of *G. arborea* were observed, a typical feature of invasive species. Its successful establishment will depend on flooding events and silvicultural management.

**Border 1 Border 2**

*Andira inermis* 0,58 1,80 0,49 2,87 *Acacia mangium* 0,95 2,07 0,66 3,68 *Dichrostachys cinerea* 0,08 0,90 1,72 2,70 *Psidium guajava* 0,33 2,07 1,10 3,50 *Comocladia dentata* 1,15 0,90 0,49 2,54 *Andira inermis* 1,43 1,38 0,44 3,25 *Casearia hirsuta* 0,03 0,90 0,74 1,67 *Gerascanthus gerascanthoides* 0,52 1,38 1,10 3.00 *Cupania americana* 0,15 0,90 0,49 1,54 *Melicoccus bijugatus* 0,03 2,07 0,66 2,76 *Swietenia macrophyla* 0,31 0,90 0,25 1,46 *Cocos nucifera* 0,37 0,69 0,22 1,28 *Swietenia mahagoni* 0,22 0,90 0,25 1,36 *Khaya senegalensis* 0,37 0,69 0,22 1,28 *Annona reticulata* 0,14 0,90 0,25 1,29 *Bursera simaruba* 0,21 0,69 0,22 1,12 *Roystonea regia.* 0,05 0,90 0,25 1,20 *Annona reticulata* 0,03 0,69 0,22 0,94

**Species Dr Fr Ar IVIE Species Dr Fr Ar IVIE**

**Totals 100 100 100 300** *Mangifera indica* 0,01 0,69 0,22 0,92

**Table 12.** Phytosociological Parameters of the riparian forest of the River Cuyaguateje, border (1 and 2). Dr = Relative

Fruit tree species were present with very low values in frequency, dominance, and abundance. Only *P. guajava, M. indica, A. reticulata*, and *M. bijugatus* were observed. Local farmers did not accept *M. bijugatus* because this species is a potentially invasive species [38]. The scarcity in fruits could also be related to the low germination and development rates of *Pouteria cam‐ pechiana* (canistel) and *Calocarpum sapota* (Red Mammee) and the low presence of this species in natural areas. Incorporating fruit trees to reforestation plans could be used as an incentive

Natural regeneration reflects ecosystem fitness. Our results show a good condition with 3,952 in border 1 and 4,564 seedlings in border 2. Nonetheless, it is important to compare the species in the upper canopy stratum with those that are regenerating because their relative frequencies are directly associated to successional processes [36]. Our results indicate that favourable conditions exist for the regeneration and the recruitment of arboreal and shrub species that can increase or diminish in the measure that restrictive factors changes. Logically, it is also

At both borders, regenerated individuals in the herbaceous stratum were found for *G. ulmifolia, S. saman, L. domingensis, S. saponaria, G. guidonia, R. regia, T. citrifolia, S. mombin, S. saponaria, T. elatum, C. collococca, L. domingensis*, and *B. simaruba*, which are typical species of this forest type. The relative natural regeneration (RNRi) index, which combines abundance and frequency, showed the higher values for *T. citrifolia, S. saman, G. ulmifolia, S. mombin, L. domingensis*, and *S. saponaria*. Of the nine species that were used at the beginning of the reforestation [39] only four were presented in this stratum: *G. arborea, T. elatum, M. indica*, and *P. guajava*. However,

related to the approval of local farmers of rehabilitation processes [13].

Dominance; Fr = Relative Frequency; Ar = Relative Abundance; IVIE = Ecological Importance Value Index

for local farmers to protect riversides.

532 22 Biodiversity in Ecosystems - Linking Structure and Function

*Terminalia catappa* 0,01 0,69 0,22 0,92

**Totals 100 100 100 300**

Table 13 shows the values of the Modified Ecological Importance Value Index (IVIEA) for both borders. The IVIEA is the most important indicator in evaluating forest dynamics [40]. It integrates horizontal and vertical structures in the mature mass, as in the natural regeneration. *S. saman, B. vulgaris, G. ulmifolia, G. arborea*, and *S. saponaria* were the most important species. Likewise, there are correspondences among plants that are identified in the arboreal stratum and natural regeneration processes in both borders. The appearance of new species in the inferior stratum, not identified in the mature state, indicates the existence of seeds and environmental factors that favour the ultimate rehabilitation of the forest. Source [29] considers that the readiness of different regeneration mechanisms is a crucial factor in the speed and course of secondary succession. Nevertheless, reproduction by seeds is the main mechanism of regeneration of the widely dispersed pioneer species, especially after repeated cultivationfallow cycles over long periods.



**Table 13.** Phytosociological parameters of riparian forest of the River Cuyaguateje area that becomes rehabilitated border (1 and 2), including (IVIEA). Ar = Relative Abundance; Fr = Relative Frequency; Dr = Relative Dominance IVIE = Relative Importance Value Index; RNRi = Relative Natural Regeneration, IVIEA = Enlarged Ecological Importance Value Index

Figure 7 represents the horizontal structure of this forest, expressed by their distribution in three diameter classes. It shows irregularity in their distribution, characteristic of forests that recover from disturbances mostly by natural regeneration. The biggest frequency values were registered in the diameter classes from 2 to 10 cm and the smallest frequencies were found for diameter classes of 20 cm and bigger. This is the typical histogram in an inverted "J". Such a result agrees with [41], who states that forests age irregularly, and that species have the biggest frequency of individuals in small diameter classes. In general, it seems that the ecosystem is formed by heterogeneous populations with irregular diameter classes. This has been previ‐ ously reported for most forests with a complex structure [42–43]. This result also indicates that previous reforestation efforts by state institutions using forest plantations were not suitable, as they did not mimic natural diameter distributions but provided the opportunity for natural regeneration to begin.

**Border 1 Border 2**

*Psidium guajava* 1,5 3,6 2,5 7,5 3,0 10,6 *Cordia collococca* 0,8 3,4 2,4 6,7 1,8 8,5

*Cupania americana* 0,1 0,9 0,5 1,5 8,4 9,9 *Cedrela odorata* 1,8 2,1 3,5 7,4 7,4 *Tabebuia angustata* 1,4 2,7 1,7 5,8 3,0 8,8 *Swietenia macrophyla* 1,8 2,8 2,0 6,6 6,6 *Guarea guidonia* 1,0 2,7 1,5 5,2 2,3 7,4 *Dichrostachys cinerea* 0,9 2,1 2,0 5,0 1,1 6,0 *Terminalia catappa* 0,9 1,8 1,2 3,9 2,7 6,6 *Cupania americana* 5,5 5,5 *Bursera simaruba* 1,2 1,8 1,2 4,2 1,5 5,8 *Terminalia catappa* 0,0 0,7 0,2 0,9 4,0 4,9 *Comocladia dentata* 1,1 0,9 0,5 2,5 3,0 5,6 *Gliricidia sepium* 1,2 1,4 1,5 4,2 0,7 4,9 *Andira inermis* 0,6 1,8 0,5 2,9 1,1 4,0 *Psidium guajava* 0,3 2,1 1,1 3,5 1,1 4,6

*Gerascanthus*

*Dichrostachys cinerea* 0,1 0,9 1,7 2,7 0,8 3,5 *Andira inermis* 1,4 1,4 0,4 3,3 1,1 4,3 *Trichilia havanensis* 2,3 2,3 *Melicoccus bijugatus* 0,0 2,1 0,7 2,8 1,1 3,9 *Melicoccus bijugatus* 2,3 2,3 *Acacia mangium* 0,9 2,1 0,7 3,7 3,7 *Casearia hirsuta* 0,0 0,9 0,7 1,7 1,7 *Bursera simaruba* 0,2 0,7 0,2 1,1 1,8 2,9 *Swietenia macrophyla* 0,3 0,9 0,2 1,5 1,5 *Mangifera indica* 0,0 0,7 0,2 0,9 1,8 2,7 *Swietenia mahagoni* 0,2 0,9 0,2 1,4 1,4 *Casearia hirsuta* 2,2 2,2 *Anonna reticulata* 0,1 0,9 0,2 1,3 1,3 *Trichilia havanensis* 1,5 1,5 **Total 100 100 100 300 100 400** *Cocos nucifera* 0,4 0,7 0,2 1,3 1,3

**Table 13.** Phytosociological parameters of riparian forest of the River Cuyaguateje area that becomes rehabilitated border (1 and 2), including (IVIEA). Ar = Relative Abundance; Fr = Relative Frequency; Dr = Relative Dominance IVIE = Relative Importance Value Index; RNRi = Relative Natural Regeneration, IVIEA = Enlarged Ecological Importance

**<sup>A</sup> Species Ar Fr Dr IVIr RNRi**

*occidentalis* 0,2 2,1 3,1 5,3 2,9 8,3

*gerascanthoides* 0,5 1,4 1,1 3,0 1,5 4,5

*Khaya senegalensis* 0,4 0,7 0,2 1,3 1,3 *Simaruba glauca* 1,1 1,1 *Anonna reticulata* 0,0 0,7 0,2 0,9 0,9 *Syzygium jambos* 0,7 0,7 *Calophyllum antillanun* 0,7 0,7 **Total 100 100 100 300 100 400**

**IVIE A**

**IVIE**

**Species Ar Fr Dr IVIr RNRi**

534 24 Biodiversity in Ecosystems - Linking Structure and Function

*Roystonea regia* 0,1 0,9 0,2 1,2 2,3 3,5

Value Index

*Cordia collococca* 3,2 2,7 1,5 7,3 2,7 10,0 *Cephalanthus*

**Figure 7.** Distribution of all individuals in three diameter classes (Borders 1 and 2 of the area that is rehabilitated) in the Cuyaguateje's riversides.

As for the vertical structure, we found different strata (Figure 8). Although tree ages did not exceed 10 years, disparity in height was observed. Lower in the canopy were those species that present less resilience under disturbances (natural and artificial), because environmental conditions favour pioneer species. Tree height in border 2 is higher, mainly due to the presence of *G*. *arborea* and *B. vulgaris.* In general, frequency distribution in the form of an inverted "J" is certain, fundamentally for low seedling survival rates in plantations during the first years. The largest quantity of individuals have settled down through the natural regeneration in the last few years, although there is the presence of some individuals in the superior strata (up to 20 m in height) as a result of the plantations carried out during the early years.

At both borders, the biggest abundance of individuals was found for the smallest height classes (2 to 5 m), at 56%. As tree height increased, the number of individuals proportionally de‐ creased, reaching less than 8% in the class for 10 m or more of height. At the two borders, 69% of the individuals were present in the smallest heights. Only 5% were found reaching heights above 20 m. In this case, they were individuals of *R. regia*, *S. saman,* or *S. mombin.* These species coincided with those that farmers reported as existing in the riverside before 1970. This fact confirms the date when the water dam "The Cuyaguateje" was built and intensive sand extraction with heavy equipment began along the whole riverside [44].

**Figure 8.** Vertical structure distributed in three classes of height (Borders 1 and 2 of the area that is rehabilitated) in the riverside of the Cuyaguateje.

Therefore, the biggest heights and diameters were represented by the smallest quantity in individuals. Such results coincide with reports by [32], who found low percentages of ach‐ ievements and survivals in the plantations carried out by States Enterprise, as a consequence of the social insubordination of the residents, the inadequate selection of species and plantation methods during the reforestation, together with only partial participation of the local farmers in the reforestation plans. The biggest values of abundance found in the inferior stratum (a result of natural regeneration), indicate that the area has the potential to recover naturally. As [45] states, a high number of juvenile and young adults can be indicative of a stable or even an expansive population.

### *3.2.3. Conservation degree of the rehabilitated area*

The conservation grade that is presented to an ecosystem is conditioned by the different indicators evaluated. Consideration of the behaviour of these indicators allowed for the inclusion of various elements in planning the complete forest rehabilitation. Identifying the causes of deterioration constitutes a fundamental link in their later management. Starting from the results obtained in the indicators evaluated according to [13], it was proven that the ecosystem is at the beginning of the rehabilitation stage: forest cover reached 72% of the surface, the modification degree was in the stocking category, the forest has recovered 26% of the original species, impacting on the recovery of the secondary forest. The summary of the evaluated aspects is shown in Table 14. If the different conservation categories suggested by [46] are used, and the sum of the values is assigned to each one of the evaluated parameters, the conservation degree of the vegetation cover was in the range of 10, indicating that it was fairly conserved (Table 15).


**Table 14.** Summary of indicators evaluated to determine the conservation degree of the riparian forest alongside in the River Cuyaguateje according to [13 and 46]


**Table 15.** Rehabilitation grade of riparian forest in its middle reaches.

of the individuals were present in the smallest heights. Only 5% were found reaching heights above 20 m. In this case, they were individuals of *R. regia*, *S. saman,* or *S. mombin.* These species coincided with those that farmers reported as existing in the riverside before 1970. This fact confirms the date when the water dam "The Cuyaguateje" was built and intensive sand

> Border 1 Border 2

2-5 5-10 ≥ 10 Total **Classes of height**

**Figure 8.** Vertical structure distributed in three classes of height (Borders 1 and 2 of the area that is rehabilitated) in the

Therefore, the biggest heights and diameters were represented by the smallest quantity in individuals. Such results coincide with reports by [32], who found low percentages of ach‐ ievements and survivals in the plantations carried out by States Enterprise, as a consequence of the social insubordination of the residents, the inadequate selection of species and plantation methods during the reforestation, together with only partial participation of the local farmers in the reforestation plans. The biggest values of abundance found in the inferior stratum (a result of natural regeneration), indicate that the area has the potential to recover naturally. As [45] states, a high number of juvenile and young adults can be indicative of a stable or even

The conservation grade that is presented to an ecosystem is conditioned by the different indicators evaluated. Consideration of the behaviour of these indicators allowed for the inclusion of various elements in planning the complete forest rehabilitation. Identifying the causes of deterioration constitutes a fundamental link in their later management. Starting from the results obtained in the indicators evaluated according to [13], it was proven that the ecosystem is at the beginning of the rehabilitation stage: forest cover reached 72% of the surface,

extraction with heavy equipment began along the whole riverside [44].

536 26 Biodiversity in Ecosystems - Linking Structure and Function

riverside of the Cuyaguateje.

an expansive population.

*3.2.3. Conservation degree of the rehabilitated area*

**Individuals**

The arguments mentioned previously present the result of the rehabilitation of the riversides of the Cuyaguateje, achieved through the participation of the executer actors (farmers and families). Study [5] shares similar approaches, indicating that rehabilitation does not imply that the site achieves an original, pre-disturbance ecological state. As the author explains, it is possible that a forest can recover its ecosystem function without recovering its structure completely. In many cases, the plantation of native trees or dominant pioneer species of ecological importance can help to start the rehabilitation process. Source [47] considers that ecological rehabilitation is an intermediate level between a degraded system and a restored ecosystem, with a composition and structure that can be similar or dissimilar to that of predisturbance. The restored system can be self-sustaining and used to provide ecological services, as in wooden production, medicinal products, and food, among others.

### *3.2.4. Participative strategy for the rehabilitation of the Cuyaguateje's riversides*

Local actors' perception about the riparian forest of the River Cuyaguateje is very important for successful biodiversity restoration. As outlined by [47]: "In Cuba the care and the conser‐ vation of the biodiversity has advanced, and the existence of legal, logistical and infrastructural means that guarantee the operation of a good part of the environmental system, but this is still not enough". Participative methods applied in the present research contributed towards positive positions about the economic, environmental, and social perception of the local actors that live and work adjacently to the riparian forest. This study promoted environmental education as a result of the training that was implemented in this area. Local residents also have a particular perception of the legislation for the protection of the riverside forest. Figure 9 shows that the biggest incidence of infractions made by the local actors in the riversides of the River Cuyaguateje was during the period 2001–2004. A gradual decrease was observed, starting from 2004, when the participative work took place. A change in local residents' perspective was probably a consequence of acquired knowledge and environmental con‐ sciousness.

**Figure 9.** Trends of the infractions made by the local actors in the Cuyaguateje´s riversides in the period 2001–2010.

Frequency analysis on the perception of local actors about regulations showed that 83% (24/29) of the interviewed actors could be classified as having the positions of advanced perception (Figure 10). It is very promising to realize that 78% (18/23) of the local residents are in advanced positions, or in other words, they know the regulations applicable in the riverside (minimum forest width, compulsory reforestation, and silvicultural management to be carried out, etc.). Local actors that only recognize the authority of the Forest State Service (FSS) and the fact that it has more than enough forest patrimony 22% (5/23) are classified as having intermediate positions. The lack of local residents classified in last group indicates a change in the perception and knowledge of legislation from the date of the initial surveys. This demonstrates the influence of the training actions and the high motivation showed by locals at the participative workshops and visits to the field.

*3.2.4. Participative strategy for the rehabilitation of the Cuyaguateje's riversides*

538 28 Biodiversity in Ecosystems - Linking Structure and Function

sciousness.

workshops and visits to the field.

Local actors' perception about the riparian forest of the River Cuyaguateje is very important for successful biodiversity restoration. As outlined by [47]: "In Cuba the care and the conser‐ vation of the biodiversity has advanced, and the existence of legal, logistical and infrastructural means that guarantee the operation of a good part of the environmental system, but this is still not enough". Participative methods applied in the present research contributed towards positive positions about the economic, environmental, and social perception of the local actors that live and work adjacently to the riparian forest. This study promoted environmental education as a result of the training that was implemented in this area. Local residents also have a particular perception of the legislation for the protection of the riverside forest. Figure 9 shows that the biggest incidence of infractions made by the local actors in the riversides of the River Cuyaguateje was during the period 2001–2004. A gradual decrease was observed, starting from 2004, when the participative work took place. A change in local residents' perspective was probably a consequence of acquired knowledge and environmental con‐

**Figure 9.** Trends of the infractions made by the local actors in the Cuyaguateje´s riversides in the period 2001–2010.

Frequency analysis on the perception of local actors about regulations showed that 83% (24/29) of the interviewed actors could be classified as having the positions of advanced perception (Figure 10). It is very promising to realize that 78% (18/23) of the local residents are in advanced positions, or in other words, they know the regulations applicable in the riverside (minimum forest width, compulsory reforestation, and silvicultural management to be carried out, etc.). Local actors that only recognize the authority of the Forest State Service (FSS) and the fact that it has more than enough forest patrimony 22% (5/23) are classified as having intermediate positions. The lack of local residents classified in last group indicates a change in the perception and knowledge of legislation from the date of the initial surveys. This demonstrates the influence of the training actions and the high motivation showed by locals at the participative

**Figure 10.** Distribution of frequencies obtained according to the perception of local actors on legislation governing the Cuyaguateje's riversides.

Our results contrasted with other studies without previous participative work from the local communities, such as the one carried out for [48] on the riversides of the River Caona. In that case, frequencies of high awareness positions were considerably low, about 30% (4/13). Therefore, it seems likely that the inclusion of a Participative Action Investigation (PAI) allowed the local actors to acquire knowledge on regulations for the protection of the riverside forests. Our results were also validated by the positions of the farmers and officials of the Forest State Service (FSS) during interviews and fieldwork. A good example is the change perceived in the farmer Noel Pérez. He became the informal leader of the community. A qualitative jump was perceived in his knowledge of the Forest Law, because he made several infractions until the year 2002, due to ignorance of the established regulations. After the training carried out in the participative workshops, the sense of ownership and commitment toward the riverside forest increased. This was evidenced in the results obtained in reforestation and establishment of the plantations, with the area belonging to Mr Pérez becoming the forest laboratory of the University Campus of Guane municipality and the Pinar del Río University.

Another example that confirms the necessity of introducing participative methods in the recovery of riparian forests is the study carried out by [49], in the basin of the River Sesesmiles (Honduras). These authors declared that 90% (18/20) of the local farmers did not know the legislation about the width of riverside fringes, although 75% (15/20) of the residents recog‐ nized the necessity of receiving training on the topic, and that is the state that watches over the execution of the established protection laws.

The approach in our research is that tree populations are the main agent to be managed when transforming the ecosystem. With an active participation of local residents it was possible to use their experience and to discuss with the scientists which tree species were more important for ecosystem rehabilitation. Most of the local residents showed a high degree of awareness (Figure 11). About 78% (18/23) of the interviewed farmers showed knowledge on the species that should be planted: they recognized the species typical of the ecosystem, and they identified the characteristics of such species with regard to their function in the riverside forests. Participative workshops together with the application of PAI created learning environments that allowed forest scientists to explain the reality better, and at the same time to find solutions to the problems identified by the local actors. In other words, PAI was used as a mean of social mobilization. The importance of traditional, experience-based knowledge by farmers was demonstrated by the selection of species and management regimes. Preference was observed towards tree species and autochthonous shrubs that can establish and grow by passive reforestation. The knowledge of the present species in the ecosystem is necessary. According to [33], the presence of multiple species provides the security that ecosystem health will be maintained during disturbances or other environmental changes.

**Figure 11.** Distribution of frequencies of awareness of local residents on the appropriateness of forest species for river‐ sides' restoration.

Local residents also showed knowledge on plantation times needed to obtain the best survival rates. Such times were related to previous results in riparian forests [10, 43–44, 50]. It is also important to recognize ownership status. Up to 92% (11/12) of the landowners behaved in terms of positions of advanced knowledge. They outlined as the main difficulties of achieving reforestation: the inadequate selection of species, the time for plantation, and especially the extensive impact of equine livestock. This livestock belongs to people that come from urban areas but who are not landowners.

Native farmers' knowledge of ecological communities and populations was of key importance. Their experiences contributed valid approaches about the species, reforestation methods, and the management of the restoration process. For example, the local Antonio Santoyo served as a guide to identify the species during the surveys of the riversides. He also indicated in workshops and interviews the most suitable species and the best methods for planting them.

Local empirical knowledge should be combined with the techniques of modern science to search for management regimes most suitable for the local ecological conditions. Farmers have accumulated knowledge that can be analysed by forest scientists, who in turn have scientific theories that can be put into practice. This is why it is important to implement participative methodologies. Social-participative ecosystem rehabilitation, with appropriate foundations, can be realizable and constitute an answer to some of the issues Cuba is facing at the moment. The decentralization of the environmental administration reinforces the grade of responsibility and the local residents' rights to forests. The knowledge that people have about their region, traditional uses of natural resources, location of the species, and in some cases the form of propagation of the plants, are important questions to consider in forest management plans. Indeed, to guarantee the success of reforestation it is important to combine academics´ and farmers´ knowledge on forest restoration practices. Unfortunately, this view has been usually dismissed in current research process not only for restoration but also in general silviculture.

(Figure 11). About 78% (18/23) of the interviewed farmers showed knowledge on the species that should be planted: they recognized the species typical of the ecosystem, and they identified the characteristics of such species with regard to their function in the riverside forests. Participative workshops together with the application of PAI created learning environments that allowed forest scientists to explain the reality better, and at the same time to find solutions to the problems identified by the local actors. In other words, PAI was used as a mean of social mobilization. The importance of traditional, experience-based knowledge by farmers was demonstrated by the selection of species and management regimes. Preference was observed towards tree species and autochthonous shrubs that can establish and grow by passive reforestation. The knowledge of the present species in the ecosystem is necessary. According to [33], the presence of multiple species provides the security that ecosystem health will be

**Figure 11.** Distribution of frequencies of awareness of local residents on the appropriateness of forest species for river‐

Local residents also showed knowledge on plantation times needed to obtain the best survival rates. Such times were related to previous results in riparian forests [10, 43–44, 50]. It is also important to recognize ownership status. Up to 92% (11/12) of the landowners behaved in terms of positions of advanced knowledge. They outlined as the main difficulties of achieving reforestation: the inadequate selection of species, the time for plantation, and especially the extensive impact of equine livestock. This livestock belongs to people that come from urban

Native farmers' knowledge of ecological communities and populations was of key importance. Their experiences contributed valid approaches about the species, reforestation methods, and the management of the restoration process. For example, the local Antonio Santoyo served as a guide to identify the species during the surveys of the riversides. He also indicated in workshops and interviews the most suitable species and the best methods for planting them.

Local empirical knowledge should be combined with the techniques of modern science to search for management regimes most suitable for the local ecological conditions. Farmers have

maintained during disturbances or other environmental changes.

540 30 Biodiversity in Ecosystems - Linking Structure and Function

sides' restoration.

areas but who are not landowners.

Local residents were also aware of the socio-economic functions that riparian forests offer. Figure 12 shows that only 20% (6/29) of the local residents viewed the forest as useful only for timber. However, 72% (21/29) of local residents attributed to forests other functions of economic and social importance. This denotes that a transformation has been achieved as to the economic perception of the forest by locals. This result contrasted with those obtained by [48], where 77% of the interviewees assumed the forest to be exclusively a source of timber. In the same way, [49] diagnosed that only 45% of the farmers of the riverside of the River Sesesmiles (Honduras) perceived the riparian forests as having both economic and social value, because they offered products like fruits, firewood, and wood for the consumption of the family. According to [37], one of the goals of forest restoration could be the sustainable supply of goods and specific natural services for the social benefit of local residents.

**Figure 12.** Distribution of frequencies obtained according to the perception of local actors about the socio-economic importance of riparian forest

As for the perception of the environmental function of the riparian forest, 52% (12/23) of local residents interviewed had an environmental knowledge of the protection of the soil (an intermediate position). This understanding seems to be transmitted from ancestors, but it could be changed by the participatory research methods. Nowadays, 48% (11/23) of the farmers (owners and tenants) that are adjacent to the riversides of the River Cuyaguateje are in positions of advanced awareness, identifying the forest function on controlling soil erosion. They relate this ecosystem service to water quality and biological diversity. Local residents also recognize the impact that forests have beyond their boundaries (Figure 13).

**Figure 13.** Distribution of frequencies obtained according to the perception of local actors about the environmental function of riparian forest.

In general, all the local actors recognized the forest's environmental functions. A group of them perceived the forest as an important element in the control of the current soil erosion in their farms. This aspect can be linked to the economic importance of forests, because farmers do not only see the forest as a source of timber, but rather they appreciate it as a tool for soil recovery that favours their crops and, therefore, their economy. No interviewed farmers were in late positions of awareness. The biggest proportion of advanced awareness was found for farmers that have lived all their lives in areas adjacent to the riverside, showing a sense of ownership toward this ecosystem. Therefore, the ownership status also influences the change of the perception in this variable. It highlights the polarization of the answers of the studied variable. Such a phenomenon especially affected the positions of advanced awareness, in which the interviewees identified the function of the forest in controlling the erosion of soil, and they related the forest with water quality and fauna migration. They also recognized the impact of the forest on the recovery of soil nutrients and food. As a consequence, there is an increment cultivation practices in bordering areas the forest. The testimonies aired in the workshops showed that farmers have appropriated the knowledge because they already attributed importance to the necessity of riverside protection. Therefore, they have not removed the soils of riverbanks; nor has the riverbed been altered by the formation of gullies in the areas lacking vegetation.

Local farmers were also asked "in their opinion, what are the causes of the present deterioration in the Cuyaguateje´s riversides: direct or indirect human activity for long periods?" It was observed that all the local actors knew the causes of deterioration; these were identified as external and internal causes. In Figure 14, the positions of advanced knowledge are 69% (20/29), with an important representation of those who have always lived in this community. The four tenants represented in the figure, are also from this location: they gave up their lands in a moment of their life and after Cuban´s "special period" they got them back as tenants.

(owners and tenants) that are adjacent to the riversides of the River Cuyaguateje are in positions of advanced awareness, identifying the forest function on controlling soil erosion. They relate this ecosystem service to water quality and biological diversity. Local residents

**Figure 13.** Distribution of frequencies obtained according to the perception of local actors about the environmental

In general, all the local actors recognized the forest's environmental functions. A group of them perceived the forest as an important element in the control of the current soil erosion in their farms. This aspect can be linked to the economic importance of forests, because farmers do not only see the forest as a source of timber, but rather they appreciate it as a tool for soil recovery that favours their crops and, therefore, their economy. No interviewed farmers were in late positions of awareness. The biggest proportion of advanced awareness was found for farmers that have lived all their lives in areas adjacent to the riverside, showing a sense of ownership toward this ecosystem. Therefore, the ownership status also influences the change of the perception in this variable. It highlights the polarization of the answers of the studied variable. Such a phenomenon especially affected the positions of advanced awareness, in which the interviewees identified the function of the forest in controlling the erosion of soil, and they related the forest with water quality and fauna migration. They also recognized the impact of the forest on the recovery of soil nutrients and food. As a consequence, there is an increment cultivation practices in bordering areas the forest. The testimonies aired in the workshops showed that farmers have appropriated the knowledge because they already attributed importance to the necessity of riverside protection. Therefore, they have not removed the soils of riverbanks; nor has the riverbed been altered by the formation of gullies in the areas lacking

Local farmers were also asked "in their opinion, what are the causes of the present deterioration in the Cuyaguateje´s riversides: direct or indirect human activity for long periods?" It was

function of riparian forest.

vegetation.

also recognize the impact that forests have beyond their boundaries (Figure 13).

542 32 Biodiversity in Ecosystems - Linking Structure and Function

**Figure 14.** Distribution of frequencies obtained according to the perception of local actors on the deterioration causes of the Cuyaguateje's riversides.

As for the native farmers, cited deterioration causes were: dike construction, tree logging, sand extraction, and agricultural activities for tobacco production and other crops. Interestingly, they identified these causes as external, even the use of the soils for agricultural cultivation is for them a problem caused by their predecessors. Such a position shows low self-awareness of their impact on the environment, because they only identified responsibility in other actors different from themselves. Similar results were obtained by [48], who reported that 46% of the interviewees considered that the causes of forest deterioration are multiple, but never included the rural owners of these lands. Most of the farmers perceive the borders of the river as being their own property, or at least they think that they are entitled to use them and to manage them, in spite of the fact that the land is state property. Such aspect coincided with the results of [48–49].

Using available historical data and taking into account the riversides' situation in the year 2000 (the presence of scarce isolated trees), it can be assumed that the riversides were subjected to anthropogenic pressures, larger even than the natural causes mentioned above. Besides deforestation of the riversides, the riverbed has also been distorted, conditioned fundamen‐ tally by the expansion of agriculture, the lack of appropriate conservation techniques, and dike construction. In a general way, it is evident that the deterioration of native forests conditioned irreversible changes in the riverbed, both in the width of the river and in the formation of bends in the waterways [31–32].

**Figure 15.** Distribution of frequencies obtained according to the perception of local actors on the most interested in reforestation in the Cuyaguateje's riversides.

Farmers that inhabit and work in the Cuyaguateje's riversides have always witnessed a deforested landscape. According to their recollections, the first reforestation actions began in the year 2000, with an audit procedure in which the Forest State Service, and businesses (Forest Enterprise Macurije, Tobacco Enterprise, and Enterprise of Several Cultivations) participated. It was coordinated by the Municipal Government's Direction. In that year, 22 hectares were planted for the first time. The biggest incidences of social indiscipline also happened. Starting from the year 2006, a gradual recovery of the riverside forest was observed, with the estab‐ lishment of some trees that were planted and others that have colonized the site in a natural way as a consequence of the decrease of anthropogenic pressure (resulting from the knowledge acquired in the training workshops that began in the year 2004).

When local farmers were asked who is most interested in reforesting the riversides of the River Cuyaguateje, 96% of the interviewees (28/29) were considered in one way or another to have an interest in the reforestation, locating them in positions of intermediate and advanced awareness (Figure 15).

The behaviour of the local residents during the different participatory activities indicates a high disposition for auto-transformation. They proposed collective actions for their own community. They recognized the importance of their approaches in the rehabilitation process and that they can be part of decision-making about the tasks that impact the solutions of the outlined problems. In the same way, they recognized the necessity of collective action and participation: the systemic integration of everybody is necessary to implement actions. The previous position indicates the need to focus on the relationships among the local actors from a sociological perspective, where the cooperation of everybody prevails. Previous results on top-down approaches were not positive; it is necessary to integrate local residents´ opinions and decide with them what is conceived for their environment.

It is important in the rehabilitation process to focus on science, technology, and society. This requires that rehabilitation plans should have a range of political and strategies designed to incorporate feedback from local actors' experiences. To achieve the effective contribution of the executive managers, they have to be motivated and prepared by education. Therefore, one of the first actions to implement should be training stakeholders and decision-makers on the principles of sustainability. The decision-making actors should not adopt a technocratic and authoritarian position; they should frame their administration in the socio-cultural and natural context in which the problem is found. Coinciding with [48], we think this is one of the reasons why the traditional approaches to stop the problems associated with riverside management have, in most cases, failed. Therefore, to get sustainable forest administration of the riverside forests, the institutions, especially the Forest State Service, have to get adopt the paradigm 'Science, Technology, and Society'.

As for the local residents´ perceptions about the actions of changes toward the reforestation, it was observed that 78% of the executive actors (18/23) have carried out positive actions to the benefit of the riversides, including the decrease of cultivation and cattle ranching activities (Figure 16). A participative forest administration has become a primordial element in the strategies of forest administration: a structured collaboration between the government and the local actors (farmers) to manage forest resources in order to obtain common and sustainable objectives. Previous works have been executed, although not all of them have been favourable in outcomes. The failures have been mainly caused by the lack of participation of the local residents, such as the case of disproportionate plantation of exotic species (*G. arborea* and *A. mangium*) which have disordered the natural landscape. Such inadequate species selection produced low survival rates of *G. arborea* in the areas where floods last the longest. It is therefore necessary to increase the local knowledge and perception of riverside forests, since the points of view of the community actors are fundamental for achieving sustainable management. In this aspect, it is important to highlight the case of the rural community leader Noel Pérez for the good results obtained in that group's property. The Forest State Service has already certified four hectares of forest established on their property.

Farmers that inhabit and work in the Cuyaguateje's riversides have always witnessed a deforested landscape. According to their recollections, the first reforestation actions began in the year 2000, with an audit procedure in which the Forest State Service, and businesses (Forest Enterprise Macurije, Tobacco Enterprise, and Enterprise of Several Cultivations) participated. It was coordinated by the Municipal Government's Direction. In that year, 22 hectares were planted for the first time. The biggest incidences of social indiscipline also happened. Starting from the year 2006, a gradual recovery of the riverside forest was observed, with the estab‐ lishment of some trees that were planted and others that have colonized the site in a natural way as a consequence of the decrease of anthropogenic pressure (resulting from the knowledge

**Figure 15.** Distribution of frequencies obtained according to the perception of local actors on the most interested in

When local farmers were asked who is most interested in reforesting the riversides of the River Cuyaguateje, 96% of the interviewees (28/29) were considered in one way or another to have an interest in the reforestation, locating them in positions of intermediate and advanced

The behaviour of the local residents during the different participatory activities indicates a high disposition for auto-transformation. They proposed collective actions for their own community. They recognized the importance of their approaches in the rehabilitation process and that they can be part of decision-making about the tasks that impact the solutions of the outlined problems. In the same way, they recognized the necessity of collective action and participation: the systemic integration of everybody is necessary to implement actions. The previous position indicates the need to focus on the relationships among the local actors from a sociological perspective, where the cooperation of everybody prevails. Previous results on top-down approaches were not positive; it is necessary to integrate local residents´ opinions

acquired in the training workshops that began in the year 2004).

and decide with them what is conceived for their environment.

awareness (Figure 15).

reforestation in the Cuyaguateje's riversides.

544 34 Biodiversity in Ecosystems - Linking Structure and Function

**Figure 16.** Distribution of frequencies obtained according to the perception of local actors on their tendency to the change in the Cuyaguateje's riversides.

The final variable tested was the local perception of the most suitable method for reforestation. Figure 17 shows the results of perception analysis, with most of the actors leaning towards natural regeneration (74%, 17/23). The main condition of achieving successful implementation is to eliminate the barriers that prevent natural regeneration. Regarding this issue, [51] outlined that when the stressing factors are eliminated in a degraded ecosystem, there is a trend that restoration follows. These authors asserted that success of the restoration does not only depend on the costs, funding sources, or the political will of the interested institutions. The main issue is the participation of the local communities with the power of decision over restoration plans.

As for the selected species, all the ones established during the regeneration or the plantations are valid. The improvement of a degraded system can also begin by means of the plantation of native trees, of dominant pioneer species and those of more ecological weight: all those that protect the riversides of the river. In this approach, local residents outlined the necessity of reforestation with native species, in addition to just leaving the land without agricultural management. Among the species that were identified as suitable for natural regeneration are: *L. domingensis, G. ulmifolia*, *S. saman, T. catappa, T. hirta*, *S. saponaria, T. angustata, B. simaruba*, *C. collococca*, *T. citrifolia, R. regia, C. dentata, A. reticulata*, *C. hirsuta*, *A. inermis*, and *S. mombin.* It was also identified *G. sepium*, to be regenerated through direct seeding or by planting stakes.

**Figure 17.** Distribution of frequencies obtained according to the perception of local actors on the most suitable refores‐ tation method in the Cuyaguateje's riversides.

#### *3.2.5. Correlation between studied variables*

Table 16 presents the correlation analysis of the variables studied, applying the correlation coefficient Spearman´s Rho. Significant relationships among several variables were found: local actors, perception of the environmental function, and the tendency to change. The variable "interest for the reforestation" was highly correlated with the perception of the environment, and less significantly with the perception of the suitable species. Correlation was also observed among the following variables: local actors, reforestation methods, ownership status, and origins of those interviewed.


\* The correlation is significant at the level 0.05 (bilateral).

The final variable tested was the local perception of the most suitable method for reforestation. Figure 17 shows the results of perception analysis, with most of the actors leaning towards natural regeneration (74%, 17/23). The main condition of achieving successful implementation is to eliminate the barriers that prevent natural regeneration. Regarding this issue, [51] outlined that when the stressing factors are eliminated in a degraded ecosystem, there is a trend that restoration follows. These authors asserted that success of the restoration does not only depend on the costs, funding sources, or the political will of the interested institutions. The main issue is the participation of the local communities with the power of decision over restoration plans.

As for the selected species, all the ones established during the regeneration or the plantations are valid. The improvement of a degraded system can also begin by means of the plantation of native trees, of dominant pioneer species and those of more ecological weight: all those that protect the riversides of the river. In this approach, local residents outlined the necessity of reforestation with native species, in addition to just leaving the land without agricultural management. Among the species that were identified as suitable for natural regeneration are: *L. domingensis, G. ulmifolia*, *S. saman, T. catappa, T. hirta*, *S. saponaria, T. angustata, B. simaruba*, *C. collococca*, *T. citrifolia, R. regia, C. dentata, A. reticulata*, *C. hirsuta*, *A. inermis*, and *S. mombin.* It was also identified *G. sepium*, to be regenerated through direct seeding or by planting stakes.

**Figure 17.** Distribution of frequencies obtained according to the perception of local actors on the most suitable refores‐

Table 16 presents the correlation analysis of the variables studied, applying the correlation coefficient Spearman´s Rho. Significant relationships among several variables were found: local actors, perception of the environmental function, and the tendency to change. The

tation method in the Cuyaguateje's riversides.

*3.2.5. Correlation between studied variables*

546 36 Biodiversity in Ecosystems - Linking Structure and Function

\*\* The correlation is significant at the level 0.01 (bilateral).

**Table 16.** Correlation analysis among the studied variables. Correlation coefficient Spearman´s Rho.

In other words, the local actors that are interested in reforestation also attribute importance to protection of the environment and at the same time they are those that have the best knowledge on the most suitable species for reforestation. Obviously, there was a change of attitude in the local actors related with the assimilation of knowledge. This behaviour is achieved when there is an empowerment of local actors regarding the problem to be solved, and they are motivated to promote the commitment and the responsibility of each one of them towards the local forest. In such a sense, [47] stated: "among social actors, psychological and social elements mediate. This does not mean that a concern for the environmental questions necessarily implies proenvironment behaviour. To achieve this point, a committed participation of the involved actors is needed". Those individuals that manifest sensitivity towards the environment are the most interested in reforesting the area and at the same time they plead for the insertion of the participative silviculture for the rehabilitation. This indicates a change of attitude and sense of ownership toward the riverside.

### *3.2.6. Participative strategy and work lines for the rehabilitation of the riparian forest of the River Cuyaguateje*

The information needed to elaborate the participative strategy was:


The objective of the strategy was to rehabilitate the riparian forest of the River Cuyaguateje in their middle reaches through participative silviculture and the method Participative Action Investigation, strengthening the capacities of the local actors, guiding them towards sustain‐ able forest management, and to be based on the perceptions of the local actors, institutions, and technologies. The specific objectives were:


To achieve this participative rehabilitation, several strategic lines were proposed:

**1.** *Analysis and real organization of the context.* This line is focused on two basic objectives: one to locate the area and the other to organize the context. Having broad information on the topic is needed, which should include theoretical foundations and existing regulations, as well as the practical experience on previous programmes and strategies related to the topic.

environment behaviour. To achieve this point, a committed participation of the involved actors is needed". Those individuals that manifest sensitivity towards the environment are the most interested in reforesting the area and at the same time they plead for the insertion of the participative silviculture for the rehabilitation. This indicates a change of attitude and sense

*3.2.6. Participative strategy and work lines for the rehabilitation of the riparian forest of the River*

**•** Characterization of the structure and composition of the rehabilitated forest with the

**•** The results of encounters, interviews, workshops, visits, participative observations, and

**•** The results of the work carried out during a ten-year period in a case study of rehabilitation and "Participative Action Investigation", which served as a basis for the feedback of the

The objective of the strategy was to rehabilitate the riparian forest of the River Cuyaguateje in their middle reaches through participative silviculture and the method Participative Action Investigation, strengthening the capacities of the local actors, guiding them towards sustain‐ able forest management, and to be based on the perceptions of the local actors, institutions,

**•** To achieve the success of the strategies, methodologies, and programmes proposed by the state for the recovery of the riparian forest of the River Cuyaguateje in its middle reaches.

**•** To improve the ecological state of the riversides and the River Cuyaguateje, reforesting it with the participation of the local actors, with preferably autochthonous fruit-bearing and wood species, although exotic ones can be used if their adaptation has been proved,

**•** To encourage the integration of local actors in the rehabilitation of this fluvial ecosystem,

**•** To contribute with information and experiences to improve the performances that are carried out in the rehabilitation of the riparian forest of the River Cuyaguateje and other

**1.** *Analysis and real organization of the context.* This line is focused on two basic objectives: one to locate the area and the other to organize the context. Having broad information on the topic is needed, which should include theoretical foundations and existing regulations,

whenever the established technical and juridical norms are followed.

and their use of politics and management with sustainability approaches.

To achieve this participative rehabilitation, several strategic lines were proposed:

**•** Meetings with technicians and specialists at municipal, provincial, and national levels.

consultation of the different local actors, decision-makers, and executives.

The information needed to elaborate the participative strategy was:

of ownership toward the riverside.

548 38 Biodiversity in Ecosystems - Linking Structure and Function

participation of local actors.

and technologies. The specific objectives were:

*Cuyaguateje*

strategy.

rivers in the country.



**Table 17.** Resulting conglomerates by means of Ward's linking method.

### **3.3. Study of case No. 3: The native rainforests of the Toa´s sector Quibiján-Naranjal**

*3.3.1. Diversity of species in native forests exploited in the basin of the River Toa (sector Quibiján-Naranjal)*

A total of 36 plots were sampled that represented the overall ecosystem. The cluster analysis based on Sorensen's similarity showed four clusters (Table 17).

The first conglomerate accounted for plots containing species of high economic and ecological value, such as *B. buceras, C. antillanum, H. elatus*, and *Purdiaea velutina*. These plots, although distant from each other, presented very similar flora. The second conglomerate was also notorious for the presence of species with high commercial value and ecological importance, such as: *Castilla elastica, G. guara, Spondias mombin*, *Cedrela odorata*, and *Carapa guianensis*. An important proportion of the present species in the study, are heliophytes species (which grow best under direct sunlight), many of them commercially important and reported in Neotropical forests such as *C. antillanum, C. utile,* and *B. capitata*. Conglomerates III and IV presented a mix of species (*C. antillanum*, *C. peltata*, *H. elatus*, *C. odorata*, *C. guianensis*, *A. inermis*, and *J. vulga‐ ris*) that varied in abundance. The presence of pioneer species clearly indicates anthropic activities. These species had regenerated easily because the seeds are big and heavy, which favours germination. In general, the four groups share almost all the species, the rare species being *Guazuma tomentosa, L. domingensis,* and *G. sepium*.

### *3.3.2. Structure of the native forests in the sector Quibiján-Naranjal of Toa*

Regarding the horizontal structure of the forest, Table 18 shows the 10 species with the highest abundance, frequency, dominance, and IVIE. The species with more IVIE were *H. elatus, C. antillanum, S. laurifolium, G. guara,* and *T. catappa.* This ecological importance value index represents the intricate relationships that the species maintain with other species of plants and organisms that help to maintain the dynamic and functional balance of the ecosystems [36].



**Table 18.** Abundance, Frequency, Dominance, and IVIE of the native forests of the sector Quibiján-Naranjal of Toa.

**3.3. Study of case No. 3: The native rainforests of the Toa´s sector Quibiján-Naranjal**

**Conglomerates Plots Total** Conglomerate 1 1; 8;11; 2; 36; 3; 28; 15; 34; 13; 14; 16; 21; 35; 5; 19; 31; 29; 32 19 Conglomerate 2 6; 7; 12; 10; 30 5 Conglomerate 3 4; 18; 17; 27; 33; 9; 24;26 8 Conglomerate 4 20; 22; 23; 25 4

based on Sorensen's similarity showed four clusters (Table 17).

**Table 17.** Resulting conglomerates by means of Ward's linking method.

550 40 Biodiversity in Ecosystems - Linking Structure and Function

being *Guazuma tomentosa, L. domingensis,* and *G. sepium*.

*3.3.2. Structure of the native forests in the sector Quibiján-Naranjal of Toa*

*Naranjal)*

*3.3.1. Diversity of species in native forests exploited in the basin of the River Toa (sector Quibiján-*

A total of 36 plots were sampled that represented the overall ecosystem. The cluster analysis

The first conglomerate accounted for plots containing species of high economic and ecological value, such as *B. buceras, C. antillanum, H. elatus*, and *Purdiaea velutina*. These plots, although distant from each other, presented very similar flora. The second conglomerate was also notorious for the presence of species with high commercial value and ecological importance, such as: *Castilla elastica, G. guara, Spondias mombin*, *Cedrela odorata*, and *Carapa guianensis*. An important proportion of the present species in the study, are heliophytes species (which grow best under direct sunlight), many of them commercially important and reported in Neotropical forests such as *C. antillanum, C. utile,* and *B. capitata*. Conglomerates III and IV presented a mix of species (*C. antillanum*, *C. peltata*, *H. elatus*, *C. odorata*, *C. guianensis*, *A. inermis*, and *J. vulga‐ ris*) that varied in abundance. The presence of pioneer species clearly indicates anthropic activities. These species had regenerated easily because the seeds are big and heavy, which favours germination. In general, the four groups share almost all the species, the rare species

Regarding the horizontal structure of the forest, Table 18 shows the 10 species with the highest abundance, frequency, dominance, and IVIE. The species with more IVIE were *H. elatus, C. antillanum, S. laurifolium, G. guara,* and *T. catappa.* This ecological importance value index represents the intricate relationships that the species maintain with other species of plants and organisms that help to maintain the dynamic and functional balance of the ecosystems [36].

**No. Species Abundance (%) Frequency (%) Dominance (%) IVIE (%)** *Hibiscus elatus* Sw. 9,54 63,9 11,0 84,38 *Calophyllum antillanum* Britton 8,11 61,10 2,81 72,04 *Sapium laurifolium* Griseb. 5,19 61,10 1,26 64,78

Table 19 shows how *Jambosa vulgaris* is one of the most abundant species, and it is also recognized in Cuba as invasive taxa [38]. This species is altering the structure and function of the forest. That fact is corroborated by [41–42], who stated that for this plant community valuable species are *C. antillanum, A. inermis,* and *H. elatum*, but generally in a smaller pro‐ portion. Owing to the anthropic pressure of the local communities, the species that are more plentiful are of scarce woody value; prevailing in higher proportions are *Syzygium jambos* and other species like *C. peltata, G. guidonia, L. domingensis*, and *Bursera simaruba*. Source [55] confirmed that these species present good adaptation to the soil and climatic conditions of the strip forest of the River Toa.


**Table 19.** Main species best represented in terms of sociological position in the native forests of the sector Quibiján-Naranjal of Toa.

Regarding the vertical structure of the forest, Table 19 shows that the main species with better sociological positions are *Syzygium jambos* in the lower canopy layer and *C. antillanum* in the intermediate canopy layer. In the superior canopy stratum, *C. guianensis* stands out together with *H. elatus.* These results indicate that in the forest there are not stable relationships in all the strata, nor is there evidence of the application of silvicultural systems. It seems that all canopy layers are affected by traditional management with a high intensity of indiscriminate tree felling, either for housing, firewood, or gap opening for agricultural cultivation. The superior stratum presents few species of economic importance [43]. Many of the existent species are not represented in all the strata. On the other hand, [53] outlines that a certain species takes an important role in the structure and composition of the forest when it is represented in all its strata. The author also said that the more regular the distribution of the individuals of a species in the vertical structure of a forest (gradual decrease of the number of trees as you ascend from the inferior stratum to the superior), so higher value in the phytoso‐ ciological position.

### *3.3.3. Influences of environmental variables in the structure of the native forest.*

The results of canonical correspondence analysis (CCA) were globally significant (trace = 1.876, F = 2.27, and P = 0.002). The first four axes of the CCA offered a solution to the ordination of units of samplings and of species. Total variability in the data of species abundance (inertia = 3.609) explained 49.2% of the relationship between environmental variables and species distribution, and 26% of the variance of species distributions in each group. These results indicate a strong gradient (Table 20), because for ecological data the value of inertia is typically low (smaller than 10%), especially when they present strong gradients [50]. The significance test of the first canonical axis demonstrated that this was also statistically significant, with auto-value = 0.316, F = 2.15, and P = 0.0020 (Figures 18 and 19).


**Table 20.** Result of the canonical correspondence analysis (CCA) of species abundance, transformed logarithmically in each one of the 36 sampling units in the function of their environmental variables.

The negative end of the axis 1 (CCA 1) shows a relationship with "distance to the highway (DCAR)" and with "distance to housing (DVIV)". Although in a smaller proportion, the negative end of the axis 2 (CCA 2) is also related to increases of the altitude (Alt), and slope (PEN). The positive end of axis 3 (CCA 3) is associated to match increase (P), distance to the highway (DCAR), and organic matter (MO), and in its negative end it is related to distance to the highway (Figure 19). Plots of group I correspond to slope gradient and altitude (Figure 18 and 19), while plots of group III are ordered following a gradient of distance to the highway and housing. The results of the ordination using the CCA 1 and CCA 3 show an evident distinction for the separation among plots of groups I, II, and IV for the variables' explanatory measures and for the separation of group III. While *C. elastica, G. guara, C. odorata, T. catappa,* and *S. mombin* species are present in plots of group III, they are associated with distance to the highway and distance to roads, coinciding with observations in the research area that research plots of group III have bigger anthropogenic activity that facilitates the development of secondary species.

Regarding the vertical structure of the forest, Table 19 shows that the main species with better sociological positions are *Syzygium jambos* in the lower canopy layer and *C. antillanum* in the intermediate canopy layer. In the superior canopy stratum, *C. guianensis* stands out together with *H. elatus.* These results indicate that in the forest there are not stable relationships in all the strata, nor is there evidence of the application of silvicultural systems. It seems that all canopy layers are affected by traditional management with a high intensity of indiscriminate tree felling, either for housing, firewood, or gap opening for agricultural cultivation. The superior stratum presents few species of economic importance [43]. Many of the existent species are not represented in all the strata. On the other hand, [53] outlines that a certain species takes an important role in the structure and composition of the forest when it is represented in all its strata. The author also said that the more regular the distribution of the individuals of a species in the vertical structure of a forest (gradual decrease of the number of trees as you ascend from the inferior stratum to the superior), so higher value in the phytoso‐

The results of canonical correspondence analysis (CCA) were globally significant (trace = 1.876, F = 2.27, and P = 0.002). The first four axes of the CCA offered a solution to the ordination of units of samplings and of species. Total variability in the data of species abundance (inertia = 3.609) explained 49.2% of the relationship between environmental variables and species distribution, and 26% of the variance of species distributions in each group. These results indicate a strong gradient (Table 20), because for ecological data the value of inertia is typically low (smaller than 10%), especially when they present strong gradients [50]. The significance test of the first canonical axis demonstrated that this was also statistically significant, with

**Number of canonical axis: 4 Axis 1 Axis 2 Axis 3 Axis 4 Total Inertia**

Auto-values: 0,316 0,250 0,198 0,173 3,609

Sum of auto-values 3,609

Sum of canonical auto-values 1,902

**Table 20.** Result of the canonical correspondence analysis (CCA) of species abundance, transformed logarithmically in

Correlation species — environmental values: 0,956 0,931 0,884 0,938

of data of species : 8,8 15,7 21,2 26,0

of relation of species-environmental values: 16,6 29,8 40,1 49,2

each one of the 36 sampling units in the function of their environmental variables.

*3.3.3. Influences of environmental variables in the structure of the native forest.*

auto-value = 0.316, F = 2.15, and P = 0.0020 (Figures 18 and 19).

ciological position.

552 42 Biodiversity in Ecosystems - Linking Structure and Function

Accumulated percentage of the variance

**Figure 18.** Projection of environmental variables, in census units and 15 species of bigger IVIE of the analysis of canoni‐ cal correspondence in relation to the axes ACC1 and ACC2. The plots are the rhombuses, the species are the triangles, and the ecological variables are the arrows. Codes: Hibiela = *Hibiscus elatus*, Caloant = *Calophyllum antillanum*, Sapilau = *Sapium laurifolium*, Guargua = *Guarea guara*, Cecrpel = *Cecropia peltata*, Termcat = *Terminalia catappa*, Jambvul = *Jambosa vulgaris*, Sponmom = *Spondias mombin*, Andiine = *Andira inermis*, Zantmar = *Zanthoxylum martenicense*, Caragui *= Carapa guianensis*, Didymor = *Didymopanax morototonii*, Cedrodo = *Cedrela odorata*, Castela = *Castilla elastica*, Buchecap = *Buche‐ navia capitata.*

**Figure 19.** Projection of environmental variables, plots, and species of canonical correspondence analysis in relation to the axes ACC1 and ACC3. Codes: Hibiela = *Hibiscus elatus*, Caloant = *Calophyllum antillanum*, Sapilau = *Sapium laurifoli‐ um*, Guargua = *Guarea guara*, Cecrpel = *Cecropia peltata*, Termcat = *Terminalia catappa*, Jambvul = *Jambosa vulgaris*, Spon‐ mom = *Spondias mombin*, Andiine = *Andira inermis*, Zantmar = *Zanthoxylum martinicense*, Caragui = *Carapa guianensis*, Didymor = *Didymopanax morototonii*, Cedrodo = *Cedrela odorata*, Castela = *Castilla elastica*, Buchecap = *Buchenavia capitata*.

### *3.3.4. Proposal for rehabilitation of native forests in the sector Quibiján-Naranjal of Toa*

To design the restoration proposal, we have considered the approach by [5], who suggested 13 steps for the restoration plan.


**Figure 19.** Projection of environmental variables, plots, and species of canonical correspondence analysis in relation to the axes ACC1 and ACC3. Codes: Hibiela = *Hibiscus elatus*, Caloant = *Calophyllum antillanum*, Sapilau = *Sapium laurifoli‐ um*, Guargua = *Guarea guara*, Cecrpel = *Cecropia peltata*, Termcat = *Terminalia catappa*, Jambvul = *Jambosa vulgaris*, Spon‐ mom = *Spondias mombin*, Andiine = *Andira inermis*, Zantmar = *Zanthoxylum martinicense*, Caragui = *Carapa guianensis*, Didymor = *Didymopanax morototonii*, Cedrodo = *Cedrela odorata*, Castela = *Castilla elastica*, Buchecap = *Buchenavia capitata*.

To design the restoration proposal, we have considered the approach by [5], who suggested

**•** *Step 1: Definition of the reference ecosystem.* Knowledge of the region and its land-use history has been kept in mind when planning research to be carried out in the area. These are

**•** *Step 2: Evaluate the current state of the ecosystem or community.* Evaluate the structure, com‐ position of species, and their ecological function. The study identified 24 families, 49 genera, and 52 species of angiosperm plants, for a total of 1507 individuals. The families with higher abundance increased the biodiversity, but they did not contain most of the individuals. This fact evidenced changes in the structure and composition of the species in the study area, as a consequence of selective logging, timber and firewood extraction, gap opening for subsistence agriculture, and road opening. These were the main sources of disturbances in

*3.3.4. Proposal for rehabilitation of native forests in the sector Quibiján-Naranjal of Toa*

13 steps for the restoration plan.

554 44 Biodiversity in Ecosystems - Linking Structure and Function

reflected in [11, 50, and 55].

the secondary forest to the riverside of the River Toa.

**•** *Step 8: Selecting the appropriate species for forest restoration*. This is a very important step for the success of the restoration plan. It is the fundamental axis in any reforestation project that seeks to be carried out in a certain area with the objective of re-establishing ecological values and of conservation of the ecosystem in general. The application of modern silvicultural techniques that seek to go beyond the traditional ones, such as: the spaced group technique or planted selection forest, reforestation with native species, passive reforestation (using natural regeneration), and using agroforestry systems (the method of Taungya). This will frame a new vision in the silvicultural development of the local Enterprise for the sake of increasing the technical personnel's skill and training level. Combined with the nucleation strategy described by [55–57] that also contributes to the recruitment of native species, it will increase the effectiveness of the restoration of tropical forests. With the objective of achieving the quick recovery of the forest, species recommended [5] are: *H. elatus, C. antillanum*, and *B. capitata.* These species present high percentages of natural regeneration in places that have been affected by the action of the winds, selective logging, and the effect of borders of roads or agricultural cultivations. It is recommended to use species of high economic value and those that present high values of relative abundance, relative frequency, relative dominance, and importance value index, such as *H. elatus, C. antillanum, C. guia‐ nensis, D. cubensis,* and *T. dubia*.


## **4. Conclusions**

The three study cases introduced in this chapter shows how restoration of degraded tropical forests is possible, if management plans are implemented in a thorough way and they involve local residents and administrations at different levels. The assessment of forest ecosystems condition is complex, and changing it will have a multifactorial impact that depends not only on the forest's structure but also on ecosystem resilience and on-going human pressure. The natural and induced changes in the flora have an influence on the sequence of ecological succession. Therefore, to design a potential restoration strategy, planning must begin from the holistic assessment of the ecosystem functioning (composition and structure) and the partici‐ pative action of local communities.

Based on our results we can conclude that: 1) the illegal selective logging and the exploitation of forest for wood and non-woody forest products are the main stresses placed on the Cuban forest ecosystems in the last hundred years. 2) The implementation of modern silviculture techniques that use key species identified during intensive forest assessment should be the starting point for restoration of tropical forests. 3) The participative techniques during the rehabilitation and restoration process should play a crucial role in the cases where the local communities govern the area to be restored. We think that such conclusions are applicable to most of the tropical forests around the world, without forgetting their own local particularities.

## **Author details**

relative dominance, and importance value index, such as *H. elatus, C. antillanum, C. guia‐*

**•** *Step 9: Propagating and handling of the species.* The species selected present their own qualities for forestry. Therefore, it is important to have knowledge of their characteristics, how to spread them, and how they are to be managed. The success of the programmes and

**•** *Step 10: Selecting sites.* Selected sites were chosen as product of field research that could give us precise information regarding scale levels and their regime of disturbances, as well as

**•** *Step 11: Defining the strategy to overcome the barriers to the restoration.* In this step it should be determined how to use the so-called modern silviculture techniques that go beyond traditional forestry, such as: the technique of spaced dense groups for plantation, refores‐ tation with native species, passive reforestation (using natural regeneration), and the

**•** *Step 12: Monitoring of the restoration process.* Monitoring is fundamental to understanding the behaviour of the ecosystem over time, to predict and/or to prevent unwanted changes, and for evaluating if objectives are met or whether pertinent modifications should be made. **•** *Step 13: Consolidating the restoration process*. The consolidation of a restoration project implies that most of the barriers to restoration have been identified and overcome, and that the ecosystem evolves according to the outlined objectives. The maintenance works and monitoring programmes should indicate that the process goes on in a satisfactory way and the ecosystem begins to show self-sustaining properties, such as the enrichment of species, wildlife recovery, and re-establishment of environmental services related with the quality

The three study cases introduced in this chapter shows how restoration of degraded tropical forests is possible, if management plans are implemented in a thorough way and they involve local residents and administrations at different levels. The assessment of forest ecosystems condition is complex, and changing it will have a multifactorial impact that depends not only on the forest's structure but also on ecosystem resilience and on-going human pressure. The natural and induced changes in the flora have an influence on the sequence of ecological succession. Therefore, to design a potential restoration strategy, planning must begin from the holistic assessment of the ecosystem functioning (composition and structure) and the partici‐

Based on our results we can conclude that: 1) the illegal selective logging and the exploitation of forest for wood and non-woody forest products are the main stresses placed on the Cuban forest ecosystems in the last hundred years. 2) The implementation of modern silviculture techniques that use key species identified during intensive forest assessment should be the

*nensis, D. cubensis,* and *T. dubia*.

556 46 Biodiversity in Ecosystems - Linking Structure and Function

plantation projects depends on this knowledge.

the level of anthropization in the ecosystem.

agroforestry systems (the method of Taungya).

of the water and the soil [55–57].

pative action of local communities.

**4. Conclusions**

Eduardo González Izquierdo1\*, Juan A. Blanco2 , Gretel Geada López3 , Rogelio Sotolongo Sospedra4 , Martín González González5 , Barbarita Mitjans Moreno6 , Alfredo Jimenez González7 and José Sánchez Fonseca 8

\*Address all correspondence to: eduardo@upr.edu.cu

1 Forest Research Centre, Pinar del Río University, Pinar del Río, Cuba

2 Universidad Pública de Navarra, Pamplona, Spain

3 Biology Department, Pinar del Río University, Pinar del Río, Cuba

4 Forestry Department, Pinar del Río University, Pinar del Río, Cuba

5 Sociocultural Studies Department, Pinar del Río University, Pinar del Río, Cuba

6 Municipal University Centre of Guane, Pinar del Río University, Guane, Cuba

7 Agricultural Department, Artemisa University, Artemisa, Cuba

8 Agroforestry Department, Guantánamo University, Guantánamo, Cuba

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[32] Mitjans B., Bonilla M., Suárez A. G., González E., and González M. Estado de conser‐ vación del bosque de ribera del río Cuyaguateje (Municipio Guane). In: Proceedings of III International Symposium of Ecological Restoration, Santa Clara, Cuba. 2010. [33] Barrera J.; Contreras N.; Rodríguez V.; Moreno A. and Montoya S. Manual para la Restauración Ecológica de los Ecosistemas Disturbados del Distrito Capital. Secreta‐ ría Distrital de Ambiente (SDA), Pontificia Universidad Javeriana (PUJ). Bogotá,

[34] Magurran A. E. Ecological diversity and its measurement. Princeton University

[35] Moreno C. E. Métodos para medir la biodiversidad. M&T — Manuales Tesis SEA,

[36] Vales M., Vilamajó D., and Herrera P. Especies forestales e integridad ecológica en fragmentos de bosques semideciduos de la provincia de La Habana, Cuba. In: Pro‐

[37] SER Principios de SER Internacional sobre la restauración ecológica. Society for Eco‐ logical Restoration (SER) Internacional. Grupo de trabajo sobre ciencia y políticas.

[38] González L. R., Rankin R., and Palmarola A. (Eds.) Plantas invasoras en Cuba. Bissea

[39] Servicio Estatal Forestal (SEF) Informe Balance anual de la dinámica forestal y la re‐

[40] Jaramillo H. Guía para estudiar estructura de Bosque Natural UTLVT/FACAAM/ Escuela de Ciencias Forestales y Ambientales. http//:www.scrib.com/doc/27722564.

[41] Lamprecht H. Silvicultura en los trópicos. Los ecosistemas forestales en los bosques tropicales y sus especies arbóreas. Posibilidades y métodos para un aprovechamiento sostenido. Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) Gmobh.

[42] Samek V. Regiones Fitogeográficas de Cuba. Dpto. de Ecología Forestal. Academia

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www.ser.org y Tucson: Society for Ecological Restoration International. 2004.

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## **Biodiversity in Metal-Contaminated Sites – Problem and Perspective – A Case Study**

E. Roccotiello, P. Marescotti, S. Di Piazza, G. Cecchi, M.G. Mariotti and M. Zotti

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59357

## **1. Introduction**

Metal contamination is one of the major environmental problems in the world, posing significant risks to ecosystems and human population in abiotic environmental compartments (soil, water, air) and in the related biota (e.g., uptake by fungi and plants).

The primary causes of soil contamination are intensive industrial activities and inade‐ quate waste disposal and treatment (although these categories vary widely across Eu‐ rope) [1]. Good knowledge of the content and variability of metals in soils linked to both the contribution of parent rock (lithogenic sources) and human activities (anthropogenic sources) is also necessary for evaluating metal pollution. These tasks are particularly difficult to achieve in ancient populated areas, such as the European Mediterranean region, where unpolluted soils are almost impossible to find [2, 3]. Among anthropogenic sour‐ ces, mining activities are the fourth largest source of land pollution (e.g., 7% of the National Priority (Superfund) Sites in the USA; [4]).

About 2.5 million sites in Europe produce potentially polluting activities [5]. With the help of improved data collection, the number of recorded polluted sites is expected to increase, as are research studies on the topic. Considering present tendencies and laws, contaminated sites will presumably rise by up to 50% by 2025 [5]. Although still at a low rate, there has nonetheless been progress in the remediation of contaminated sites.

Around 59,000 sites have already been remediated. Nonetheless, it should be noted that around 340,000 sites may need urgent remediation [5]. However, conventional technologies for metalcontaminated soil remediation have often been expensive and disruptive [6].

© 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and eproduction in any medium, provided the original work is properly cited.

A good tool for evaluating environmental damage might be the Ecological Risk Assessment (ERA), which is already used in the US [7, 8] and in some countries in the European Union (e.g., Netherlands, [9] and the UK [10]), while in Italy, it still remains largely unknown. Consequently, threshold contaminant concentration, according to Italian law [11], is a humanbased risk that lacks consideration in terms of biodiversity and ecosystem services.

Before starting to plan restoration of polluted industrial environments, the 'target condition' should first be assessed. However, the remediation of a contaminated site with all its particular biotic and abiotic characteristics seems unrealistic. Several authors have indicated the lack of data providing detailed characterization of the biotic and abiotic components of environments in a pre-industrial condition and have highlighted that communities did not return to their previous states [12-15].

The best approach for preserving or restoring the biodiversity of metal-contaminated envi‐ ronments should be site-specific characterization. For this purpose, the evaluation of the surrounding area's biodiversity, a choice of best reasonable target condition for biotic com‐ ponents and the selection of tolerant organisms occurring on the polluted sites are essential. Among the biotic components of soil, fungi and plants are the pioneer organisms that play a key role in the colonization of contaminated sites.

### **1.1. Biodiversity in metal-contaminated sites**

The physicochemical properties of metal-contaminated environments tend to inhibit soilforming processes and affect the area's biodiversity by exerting a strong selective pressure on fungi and plants [16-19]. Specifically, the bulk metal content of soils and its metal releasability are among the most important edaphic factors determining vegetation composition. Other than metal toxicity, vegetation successions are also retarded by low nutrient status, poorly developed soil structure and water-restricted conditions [20].

In addition, microorganism communities play a significant part in the detoxification of noxious chemicals and in the control of plant growth [21], and also provide pivotal information about soil metal bioavailability [22]. Metalliferous biota is increasingly exploited for the stabilization or active remediation of the metal-contaminated ecosystems and represents an important research topic in the contemporary field of green technology [23, 24].

It is well-known that a number of plants and fungi are able to survive and actively grow in metal-contaminated soils. For instance, recent studies [25] have shown that some arbuscular mycorrhizal fungi from Cu-contaminated soils [*Claroideoglomus claroideum* (N.C. Schenck and G.S. Sm.) C. Walker and A. Schüßler in association with *Imperata condensata* Steud. and *Rhizophagus irregularis* (Błaszk., Wubet, Renker and Buscot) C. Walker and A. Schüßler in association with carrot roots] are able to compartmentalize Cu in spores as a survival strategy in polluted environments. Additionally, microfungi are essential in colonizing and detoxifying metal-contaminated soil ecosystems and consequently have environmental and economic significance [16, 26-28].

Mine dumps cause high selective pressure, enabling bacteria and microfungi to be the first organisms able to re-colonize mine soils [29]. Under this pressure, microfungal communities change their composition and several resistant strains are selected [28]. In addition, plant communities have established a primary succession on mine wastes [30] and can be exploited for biogeochemical prospecting and mine stabilization (e.g., abandoned mines contaminated with arsenic, antimony and tungsten [17]).

### **1.2. Selecting native fungi and plants for bioremediation**

A good tool for evaluating environmental damage might be the Ecological Risk Assessment (ERA), which is already used in the US [7, 8] and in some countries in the European Union (e.g., Netherlands, [9] and the UK [10]), while in Italy, it still remains largely unknown. Consequently, threshold contaminant concentration, according to Italian law [11], is a human-

Before starting to plan restoration of polluted industrial environments, the 'target condition' should first be assessed. However, the remediation of a contaminated site with all its particular biotic and abiotic characteristics seems unrealistic. Several authors have indicated the lack of data providing detailed characterization of the biotic and abiotic components of environments in a pre-industrial condition and have highlighted that communities did not return to their

The best approach for preserving or restoring the biodiversity of metal-contaminated envi‐ ronments should be site-specific characterization. For this purpose, the evaluation of the surrounding area's biodiversity, a choice of best reasonable target condition for biotic com‐ ponents and the selection of tolerant organisms occurring on the polluted sites are essential. Among the biotic components of soil, fungi and plants are the pioneer organisms that play a

The physicochemical properties of metal-contaminated environments tend to inhibit soilforming processes and affect the area's biodiversity by exerting a strong selective pressure on fungi and plants [16-19]. Specifically, the bulk metal content of soils and its metal releasability are among the most important edaphic factors determining vegetation composition. Other than metal toxicity, vegetation successions are also retarded by low nutrient status, poorly

In addition, microorganism communities play a significant part in the detoxification of noxious chemicals and in the control of plant growth [21], and also provide pivotal information about soil metal bioavailability [22]. Metalliferous biota is increasingly exploited for the stabilization or active remediation of the metal-contaminated ecosystems and represents an important

It is well-known that a number of plants and fungi are able to survive and actively grow in metal-contaminated soils. For instance, recent studies [25] have shown that some arbuscular mycorrhizal fungi from Cu-contaminated soils [*Claroideoglomus claroideum* (N.C. Schenck and G.S. Sm.) C. Walker and A. Schüßler in association with *Imperata condensata* Steud. and *Rhizophagus irregularis* (Błaszk., Wubet, Renker and Buscot) C. Walker and A. Schüßler in association with carrot roots] are able to compartmentalize Cu in spores as a survival strategy in polluted environments. Additionally, microfungi are essential in colonizing and detoxifying metal-contaminated soil ecosystems and consequently have environmental and economic

based risk that lacks consideration in terms of biodiversity and ecosystem services.

previous states [12-15].

significance [16, 26-28].

key role in the colonization of contaminated sites.

developed soil structure and water-restricted conditions [20].

research topic in the contemporary field of green technology [23, 24].

**1.1. Biodiversity in metal-contaminated sites**

5642 Biodiversity in Ecosystems - Linking Structure and Function

Critical environmental conditions related to high metal concentration are present either in natural soils (e.g., serpentinitic and ultramafic soils; [31, 32 and references therein]) and in anthropogenic contaminated sites (such as industrial, agricultural and mining sites [33, 1 and references therein]).

Fungi and plants from metal-rich soils develop specific strategies to cope with metals via avoidance, accumulation or hyperaccumulation [34]. Care should be taken in choosing the right species for the application of bioremediation techniques, because the introduction of alien fungi and plants may alter and disrupt indigenous ecosystems [35], or may be unsuitable for local climate conditions [36]. Therefore, a more appropriate option is to find native hyperac‐ cumulator fungi and plants that have adapted to growing on metalliferous sites, and use them for soil bioremediation in the same region [37, 38].

Bioremediation process consists of two main approaches: 1) myco- and phytostabilization; 2) myco- or phyto-extraction. Myco- and phyto-stabilization are mechanisms that immobi‐ lize pollutants – mainly metals – within the root zone, by adsorption, chelation and metal ion precipitation, thus preventing migration of contaminants by erosion, leaching and runoff [39,40].

Myco- and phyto-extraction are typically used to uptake metals, metalloids and radionuclides. The metals accumulate in the fruit-bodies or in the plant's aboveground biomass and can be removed or recovered by harvesting and burning the biomass.

Several organisms, including microbes, micro- and macro-fungi, agricultural and vegetable crops, ornamentals and wild metal hyperaccumulating plants have been tested both in laboratory and field conditions for selecting and providing organisms able to clean-up metalliferous substrates [24].

In fact, recent studies have shown how macrofungi such as *Trametes versicolor* (L.) Lloyd [41] and microfungi such as *Aspergillus niger* Tiegh. [42], *A. terreus* Thom [43], *A. versicolor* (Vuill.) Tirab. [44], *Penicillium notatum* Westling [45], *Rhizopus arrhizus* A. Fisch. [46], *Trichoderma atroviride* P. Karst. [47], *T. viride* Pers. [48] are able to absorb Cu from contaminated liquid and solid matrices.

Similarly, plant taxa naturally occurring in metalliferous soils have been selected, tested and confirmed as hyperaccumulators under experimental conditions for different metals like Ni (e.g., *Alyssum bertolonii* Desv., *A. murale* Waldst. & Kit., *A. lesbiacum* (Candargy) Rech.f., *A.* *corsicum* Duby) and Cd (*Thlaspi caerulescens* J.Presl & C.Presl and *Arabidopsis halleri* (L.) O'Kane & Al-Shehbaz) [49-54].

Little information is available about the processes occurring at the soil-rhizosphere level. Though roots are the only organ directly interacting with soil trace elements, most of the studies on hyperaccumulation by plants have focused on above-ground organs. Less than 10% of the known hyperaccumulator species have been investigated at the rhizosphere level [55].

Bacteria and fungi in the hyperaccumulator rhizosphere may exhibit increased metal tolerance by i) acting as a plant growth promoting microorganisms; ii) modifying metal speciation and solubility; iii) influencing plant trace element concentrations [55, 56-58].

Fungal species not identified as mycorrhizae have also been found in the hyperaccumulator rhizosphere [59, 60]. The role of these organisms still needs to be established, but some have been identified as able to concentrate and volatilize pollutants [61]. The knowledge about hyperaccumulators and associated microorganisms continuously increases, thus suggesting the significant roles of bacteria and fungi in hyperaccumulation.

## **2. Case study – Multidisciplinary investigations on biodiversity into a sulphide-rich waste-rock dump**

The present review illustrates the results of a six-year multidisciplinary study aimed at understanding the relationships among the mineralogy and chemistry of the Libiola mine (eastern Liguria, Italy, Fig. 1) and the metal uptake by fungi and plants spontaneously growing in the mine-waste dump. The mine is located in a moderately steep mountainous terrain at an altitude between 40 and 400 m asl, close to the Liguria sea coast.

This mine had already been known during the Bronze Age [63] and was industrially exploited from 1864 until 1962. During this period, it produced over 1 Mt of Fe-Cu sulphides with an average grade ranging from 7 to 14 Cu wt%, thus representing one of the most important Fe-Cu sulphide mines [64, 65] in Italy. Sulphide mineralization occurs within the Jurassic ophiolites of the Northern Apennines (Vara supergroup; [66]) and is geologically characterized primarily by pillow basalts with minor serpentinites, gabbros and ophiolitic breccias. During exploitation, five major waste-rock dumps were built up through the progressive accumula‐ tion of heterogeneous sterile rocks (derived from galleries and open-pit excavations) and nonvaluable ore-fragments, with metal concentrations below the economic cut-off produced during beneficiation processes [67]. The soils of the dumps are characterized by severe edaphic conditions due to their peculiar physical (steep slopes, low moisture retainability, impermea‐ bilization due to cementification and hardpan formation; [68]) and chemical (high Cr-, Cu-, Co-, Ni- and Zn-concentrations, low pH values and the low availability of essential macronu‐ trients) properties. This site presents several environmental problems as a result of active acid mine drainage (AMD) processes, which determines the water acidification and metal pollution of soils and waters.

Biodiversity in Metal-Contaminated Sites – Problem and Perspective – A Case Study 5 http://dx.doi.org/10.5772/59357 567

**Figure 1.** Location of Libiola mine site (from [62], modified).

*corsicum* Duby) and Cd (*Thlaspi caerulescens* J.Presl & C.Presl and *Arabidopsis halleri* (L.) O'Kane

Little information is available about the processes occurring at the soil-rhizosphere level. Though roots are the only organ directly interacting with soil trace elements, most of the studies on hyperaccumulation by plants have focused on above-ground organs. Less than 10% of the known hyperaccumulator species have been investigated at the rhizosphere level [55].

Bacteria and fungi in the hyperaccumulator rhizosphere may exhibit increased metal tolerance by i) acting as a plant growth promoting microorganisms; ii) modifying metal speciation and

Fungal species not identified as mycorrhizae have also been found in the hyperaccumulator rhizosphere [59, 60]. The role of these organisms still needs to be established, but some have been identified as able to concentrate and volatilize pollutants [61]. The knowledge about hyperaccumulators and associated microorganisms continuously increases, thus suggesting

**2. Case study – Multidisciplinary investigations on biodiversity into a**

The present review illustrates the results of a six-year multidisciplinary study aimed at understanding the relationships among the mineralogy and chemistry of the Libiola mine (eastern Liguria, Italy, Fig. 1) and the metal uptake by fungi and plants spontaneously growing in the mine-waste dump. The mine is located in a moderately steep mountainous terrain at an

This mine had already been known during the Bronze Age [63] and was industrially exploited from 1864 until 1962. During this period, it produced over 1 Mt of Fe-Cu sulphides with an average grade ranging from 7 to 14 Cu wt%, thus representing one of the most important Fe-Cu sulphide mines [64, 65] in Italy. Sulphide mineralization occurs within the Jurassic ophiolites of the Northern Apennines (Vara supergroup; [66]) and is geologically characterized primarily by pillow basalts with minor serpentinites, gabbros and ophiolitic breccias. During exploitation, five major waste-rock dumps were built up through the progressive accumula‐ tion of heterogeneous sterile rocks (derived from galleries and open-pit excavations) and nonvaluable ore-fragments, with metal concentrations below the economic cut-off produced during beneficiation processes [67]. The soils of the dumps are characterized by severe edaphic conditions due to their peculiar physical (steep slopes, low moisture retainability, impermea‐ bilization due to cementification and hardpan formation; [68]) and chemical (high Cr-, Cu-, Co-, Ni- and Zn-concentrations, low pH values and the low availability of essential macronu‐ trients) properties. This site presents several environmental problems as a result of active acid mine drainage (AMD) processes, which determines the water acidification and metal pollution

solubility; iii) influencing plant trace element concentrations [55, 56-58].

the significant roles of bacteria and fungi in hyperaccumulation.

altitude between 40 and 400 m asl, close to the Liguria sea coast.

**sulphide-rich waste-rock dump**

of soils and waters.

& Al-Shehbaz) [49-54].

5664 Biodiversity in Ecosystems - Linking Structure and Function

**Figure 2.** Contour maps of selected elements (Fe2O3, Cr2O3, Cu and Ni) in the main waste-rock dump of the Libiola mine (from [67], modified).

We evaluated the plant and fungal diversity in these contaminated soils in order to 1) identify factors that influenced the pioneer fungi and plants colonizing this stressed environment; 2) identify and select tolerant and hyperaccumulating plants and fungal strains suitable for mine remediation.

The waste-rock materials deposited in the mining area are mainly gravely-sandy sediments with a relatively uniform particle size distribution in the range 2-64 mm; the silt and clay fractions are subordinate components and vary from 5% to 26%. Most of the dumps evidence strong superficial cementation induced by Fe-oxides precipitating from acid sulphate water seepage, which determines the formation of centimetre-thick impermeable hardpans on several parts of the exposed surface of the dumps [67, 68].

Due to active and widespread AMD processes, the pH of waste-dump soils is generally acidic (3.5-4.3) and significantly low, compared to the surrounding serpentinitic and basaltic soils (6.2-6.8) [30, 69, 68].

The mineralogical and lithological composition of the waste-rock materials is quite homoge‐ neous throughout the mine area, though the relative proportions of the detected lithotypes and mineral species significantly vary from site to site. The studied samples are mainly composed of polycrystalline rock fragments, which can be grouped into the following lithological classes [65, 67, 68]: 1) serpentinites 20%-50%; 2) basalts 5%-10%; 3) sulphide mineralizations (2%-10%); 4) massive Fe-oxyhydroxides and -oxides clasts (35%-65%). Other subordinate components (3%-6%) are represented by garnet- and epidote-rich rodingites, polygenic ophiolitic breccias and brecciated basalts.

The mineral species occurring within the waste-rock dump [65, 67, 68] can be divided into three major groups on the basis of their origin and/or origin: 1) host rocks and gangue minerals; 2) ore minerals with different degrees of alteration; 3) authigenic secondary minerals. Serpen‐ tine minerals (60%-70% of the recognized mineral species) and Fe-oxyhydroxides (mainly goethite) are by far the most abundant species, respectively representing the main rockforming minerals of the lithotypes of the surrounding area and the main authigenic minerals forming as a result of the ongoing AMD processes. Sulphides (mainly pyrite and chalcopyrite) are subordinate but important components from an environmental point of view, either for their role in triggering the AMD processes and/or for the release of metals (particularly Fe, Cu and Zn). Magnetite, Cr-bearing magnetite and chromian spinels are the only Cr-bearing minerals, whereas serpentines are the main Ni-bearing minerals. Nevertheless, they are stable mineral species, even in this highly reactive environment, that likely do not contribute significantly to the bioavailable fraction of toxic metals.

According to the mineralogical and lithological composition, the waste rock dumps of the Libiola mine are invariably characterized by very high concentrations of several potentially toxic metals (such as Ti, Mn, Co, Ni, V, Cr, Cu, Zn and Cd). Although a notable variability is always present and several hot spots have been found (see, for example, Fig. 2), most of the detected metals (in particular Cr, Cu, Co, Ni and Zn) strongly exceed the Italian limits for residential and industrial sites [11].

Xero-acidophilous plant communities characterize the areas surrounding the mine site. These are different aspects of sclerophyllous evergreen maquis and mixed sclerophyllous evergreen and deciduous shrub thickets (pseudomaquis) formed by *B. sempervirens* L. and/or *Genista desoleana* Valsecchi, *Erica arborea* L., *Calicotome spinosa* (L.) Link., *Juniperus oxycedrus* L. subsp. *oxycedrus* and *Arbutus unedo* L. Chamaephytic and sub-shrubby layers are well represented by *Euphorbia spinosa* L. subsp. *ligustica* (Fiori) Pignatti, *Helichrysum italicum* (Roth) G. Don, *Minuartia laricifolia* (L.) Schinz. and Thell subsp. *ophiolitica* Pignatti, *Thymus* sp.pl., and *Satureja montana* L.; Maritime pine (*Pinus pinaster* Aiton) old reforestations are also present. Less frequent are relics of holm oak (*Quercus ilex* L.), pubescent oak (*Quercus pubescens* Willd.) copses and thermophile mixed woods [3, 70, 71].

We evaluated the plant and fungal diversity in these contaminated soils in order to 1) identify factors that influenced the pioneer fungi and plants colonizing this stressed environment; 2) identify and select tolerant and hyperaccumulating plants and fungal strains suitable for mine

The waste-rock materials deposited in the mining area are mainly gravely-sandy sediments with a relatively uniform particle size distribution in the range 2-64 mm; the silt and clay fractions are subordinate components and vary from 5% to 26%. Most of the dumps evidence strong superficial cementation induced by Fe-oxides precipitating from acid sulphate water seepage, which determines the formation of centimetre-thick impermeable hardpans on

Due to active and widespread AMD processes, the pH of waste-dump soils is generally acidic (3.5-4.3) and significantly low, compared to the surrounding serpentinitic and basaltic soils

The mineralogical and lithological composition of the waste-rock materials is quite homoge‐ neous throughout the mine area, though the relative proportions of the detected lithotypes and mineral species significantly vary from site to site. The studied samples are mainly composed of polycrystalline rock fragments, which can be grouped into the following lithological classes [65, 67, 68]: 1) serpentinites 20%-50%; 2) basalts 5%-10%; 3) sulphide mineralizations (2%-10%); 4) massive Fe-oxyhydroxides and -oxides clasts (35%-65%). Other subordinate components (3%-6%) are represented by garnet- and epidote-rich rodingites,

The mineral species occurring within the waste-rock dump [65, 67, 68] can be divided into three major groups on the basis of their origin and/or origin: 1) host rocks and gangue minerals; 2) ore minerals with different degrees of alteration; 3) authigenic secondary minerals. Serpen‐ tine minerals (60%-70% of the recognized mineral species) and Fe-oxyhydroxides (mainly goethite) are by far the most abundant species, respectively representing the main rockforming minerals of the lithotypes of the surrounding area and the main authigenic minerals forming as a result of the ongoing AMD processes. Sulphides (mainly pyrite and chalcopyrite) are subordinate but important components from an environmental point of view, either for their role in triggering the AMD processes and/or for the release of metals (particularly Fe, Cu and Zn). Magnetite, Cr-bearing magnetite and chromian spinels are the only Cr-bearing minerals, whereas serpentines are the main Ni-bearing minerals. Nevertheless, they are stable mineral species, even in this highly reactive environment, that likely do not contribute

According to the mineralogical and lithological composition, the waste rock dumps of the Libiola mine are invariably characterized by very high concentrations of several potentially toxic metals (such as Ti, Mn, Co, Ni, V, Cr, Cu, Zn and Cd). Although a notable variability is always present and several hot spots have been found (see, for example, Fig. 2), most of the detected metals (in particular Cr, Cu, Co, Ni and Zn) strongly exceed the Italian limits for

several parts of the exposed surface of the dumps [67, 68].

5686 Biodiversity in Ecosystems - Linking Structure and Function

polygenic ophiolitic breccias and brecciated basalts.

significantly to the bioavailable fraction of toxic metals.

residential and industrial sites [11].

remediation.

(6.2-6.8) [30, 69, 68].

The study area is characterized by bare soils or by different successions of plant communities ranging from herbaceous to arboreal layers (Fig. 3). In all the plots, species richness and vegetation cover were extremely low and the flora showed acidophilous traits [30]. The bare soil is a substrate with an almost complete absence of vegetation (Fig. 3B). The herbaceous layer has pioneer vegetation dominated by discontinuous communities of low-sized grasses and herbs such as *Deschampsia flexuosa* (L.) Trin., *M. laricifolia* subsp. *ophiolitica, Sesamoides interrupta* (Boreau) G.López*, Festuca robustifolia* Markgr.-Dann. and, in sites with more developed soil, also by *Cerastium ligusticum* Viv*.* and *Asplenium adiantum-nigrum* L.. The subsequent layers are colonized by *Thymus vulgaris* L.*, S. montana, E. spinosa* subsp. *ligustica*.

The shrub layer is mainly located on serpentine debris on the edge of the landfill areas and colonized by semi-natural plant communities dominated by *E. spinosa* subsp. *ligustica*, *Alyssoides utriculata* (L.) Medik., *T. caerulescens, Silene paradoxa* L.*, F. robustifolia* and *H. itali‐ cum* (Fig. 3C).

Despite harsh environmental conditions, the waste-rock dump has been progressively colonized since 2008 by several plants of *Pinus pinaster* Aiton, already found naturally on metal-rich sites, thereby establishing ectomycorrhizal symbiosis (ECM) [72]. The maritime pine populations constituting the tree layer derive from seeds dispersed by the surround‐ ing plants and employed for the revegetation of fired areas (Fig. 3D). A few herbaceous species such qw *D. flexuosa, M. laricifolia* subsp*. ophiolitica* and *F. robustifolia* are associated with *P. pinaster*. The absence of the shrub layer in the mine dump and the presence of the tree layer strictly composed of pine is particularly uncommon, and the success of *P. pinaster* colonization is mainly due to the presence of *Scleroderma polyrhizum* (J.F. Gmel.) Pers (Fig. 4A) and *Telephora terrestris* Ehrh. (Fig. 4B) ectomycorrhizic with pine (see Fig. 4C-D) [69]. Maritime pine is known to be able to cope with some limiting factors such as a low level of macronutrients, a lack of organic matter and water stress, typical of dismissed mining areas [73] such as the one in our study. In addition, we found that *P. pinaster* is able to completely exclude toxic metals from its tissue (Fig. 5), thereby acting as a phytostabiliz‐ er, as demonstrated by bioaccumulation (i.e., BF = shoot:soil metal concentration) and translocation (i.e., TF = shoot:root metal concentration) factors (BFs>1 and TFs<1, respective‐ ly [68]). Where metal concentrations decrease [30, 68], plants constitute semi-natural Mediterranean serpentine vegetation, typical to NW Italy [70, 71]

**Figure 3.** Libiola mine site **A**) View of the mine waste rock dump; **B - D**) sampling sites; **B)** bare soil with no vegeta‐ tion; **C**) shrub layer; **D**) tree layer with macrofungi.

**Figure 4.** Macrofungi at the Libiola mine and their ECM symbiosis. **A)** *S. polyrhizum*; **B)** *T. terrestris*; **C)** *P. pinaster* roots with ECM fungi; **D**) details of root apex with ECM fungi; blue cotton staining.

**Figure 5.** ESEM micrographs of *P. pinaster* with EDS spectra. **A**) *P. pinaster* leaves showed soil particles on stomata, but no metals were detected inside tissues; Bar = 20 μm. **B**) *P. pinaster* stems; Bar = 200 μm **C**). *P. pinaster* roots with ECM fungi; Bar = 100 μm. **D**) details of root hairs; Bar = 10 μm. EHT: 30 KV, WD: 14 mm, detector: Centaurus.

**Figure 3.** Libiola mine site **A**) View of the mine waste rock dump; **B - D**) sampling sites; **B)** bare soil with no vegeta‐

**Figure 4.** Macrofungi at the Libiola mine and their ECM symbiosis. **A)** *S. polyrhizum*; **B)** *T. terrestris*; **C)** *P. pinaster* roots

with ECM fungi; **D**) details of root apex with ECM fungi; blue cotton staining.

tion; **C**) shrub layer; **D**) tree layer with macrofungi.

5708 Biodiversity in Ecosystems - Linking Structure and Function

Among the mine plants screened for Ni accumulation in plant tissue, only the well-known metal hyperaccumulator *Thlaspi caerulescens* J. & C. Presl and *A. utriculata* yielded a positive response (Fig. 6). The latter was recently confirmed as a new Ni facultative hyperaccumulator, able to concentrate more than 1000 mg kg-1 Ni DW in leaves [74]. Plant efficiency tests were carried out on native soils to evaluate the growing ability and the ecophysiology of this promising species, and recent experiments have confirmed its suitability for phytoextraction (data not shown).

Soil samples collected from the *A. utriculata* rhizosphere and barren mine soils were examined to determine microfungal flora. On the whole, the majority of isolated colonies belonged to the genus *Aspergillus*, *Botrytis, Clonostachys*, *Penicillium* and *Trichoderma* (Fig. 7). Regarding *A. utriculata,* the rhizosphere were isolated species such as *Eurotium amstelodami* L. Mangin, *Aspergillus carbonarius* (Bainier) Thom, *A. tubingensis* Mosseray, *Penicillium waksmanii* K.M. Zalessky and *Rhodotorula* spp. not found in other mine soil samples. We can hypothesize that these microfungi, growing in the hyperaccumulator rhizosphere, may function as plant growth promoting factors altering element solubility and increasing plant metal uptake.

**Figure 6.** *Alyssoides utriculata* **A**) in the mine dump; **B**) positive leaf trichome DMG test, light microscopy micrographs; **C, D**) ESEM micrographs and EDS spectrum of leaf trichomes storing Ni, up to 8%; Bar = 100 μm. EHT: 30 KV, WD: 14 mm, detector: Centaurus.

The ectomychorrizal macrofungi collected reveal a highly significant metal accumulation, in particular Cu>1000 mg kg-1 in *Telephora terrestris* and Ag>50000 μg kg-1 in *Scleroderma polyrhi‐ zum*. When present in mine sites, these fungi are able to actively absorb most of the potential toxic elements in the sites' basidiomata. The absorption sequence Cu>Zn>Cr>Ni>Co obtained for these macrofungi overlaps well with the sequences obtained using EDTA extractions and water leaching tests [69, 68]. Both species also established ECM symbiosis with pine and we could not exclude that they played a role in the phytostabilization process at the root level.

Finally, we studied soil microfungi to test the growth responses of culturable isolated micro‐ fungal strains in copper enriched media and to evaluate their potential use in mycoremedia‐ tion. The species most recurrent were filamentous microfungi: *Trichoderma harzianum, Clonostachys rosea* and *Aspergillus alliaceus.* We hypothesized that these fungi were particularly tolerant/resistant to copper. The Cu tolerance level of *T. harzianum* and *C. rosea* were tested *in vitro* at increasing Cu(II) concentrations. The tests showed a Cu(II)-tolerance capability ranging from 100 to 400 mg L-1 [75]. These preliminary analyses proved that several fungal species were able to grow in Cu-contaminated media, thereby underlying the importance of selecting new Biodiversity in Metal-Contaminated Sites – Problem and Perspective – A Case Study 11 http://dx.doi.org/10.5772/59357 573

**Figure 7.** Microfungi isolated from mine site: **A**) *Rhizopus oryzae* Went & Prins. Geerl., acid fuchsine staining, light mi‐ croscopy; **B**) *Clonostachys rosea* (Link Schroers, Samuels, Seifert & W. Gams, acid fuchsine staining, light microscopy; **C**) sclerotia of *Aspergillus alliaceus* Thom & Church, stereomicroscopy; **D**) *Botrytis cinerea* Pers. ex Nocca & Balb., acid fuch‐ sine staining, light microscopy.

tolerant strains and testing their potential metal uptake capabilities for application to mycor‐ emediation protocols.

Silver, a noble metal of historical and economic importance, also indicated a high concentration in the Libiola mine soil. Even if silver is usually not considered an environmental contaminant, Ag+ represents one of the most toxic metals to bacteria, algae and fish [76], and can damage cellular components and reduce enzymatic activities. Some studies have shown that bacteria, yeasts and macrofungi can accumulate silver; however, the chemical form of Ag in the macrofungal fruit-bodies was not investigated in detail [77, 78, 76]. In this context, we have tested the potential Ag+ accumulation by microfungi isolated from the Libiola mine soils. First, we tested the *in vitro* growth capabilities on Ag+ -enriched media by *Aspergillus alliaceus*, *Trichoderma* sp., *C. rosea* in order to select the most tolerant microfungal strain. *Trichoderma* sp. showed the best and speediest capabilities for growing *in vitro* on media spiked with 400 mg kg-1 of Ag+ , uptaking 150 mg kg-1 dry weight (Fig. 8), as confirmed by ICP-MS analysis.

The ectomychorrizal macrofungi collected reveal a highly significant metal accumulation, in particular Cu>1000 mg kg-1 in *Telephora terrestris* and Ag>50000 μg kg-1 in *Scleroderma polyrhi‐ zum*. When present in mine sites, these fungi are able to actively absorb most of the potential toxic elements in the sites' basidiomata. The absorption sequence Cu>Zn>Cr>Ni>Co obtained for these macrofungi overlaps well with the sequences obtained using EDTA extractions and water leaching tests [69, 68]. Both species also established ECM symbiosis with pine and we could not exclude that they played a role in the phytostabilization process at the root level.

**Figure 6.** *Alyssoides utriculata* **A**) in the mine dump; **B**) positive leaf trichome DMG test, light microscopy micrographs; **C, D**) ESEM micrographs and EDS spectrum of leaf trichomes storing Ni, up to 8%; Bar = 100 μm. EHT: 30 KV, WD: 14

mm, detector: Centaurus.

572 10 Biodiversity in Ecosystems - Linking Structure and Function

Finally, we studied soil microfungi to test the growth responses of culturable isolated micro‐ fungal strains in copper enriched media and to evaluate their potential use in mycoremedia‐ tion. The species most recurrent were filamentous microfungi: *Trichoderma harzianum, Clonostachys rosea* and *Aspergillus alliaceus.* We hypothesized that these fungi were particularly tolerant/resistant to copper. The Cu tolerance level of *T. harzianum* and *C. rosea* were tested *in vitro* at increasing Cu(II) concentrations. The tests showed a Cu(II)-tolerance capability ranging from 100 to 400 mg L-1 [75]. These preliminary analyses proved that several fungal species were able to grow in Cu-contaminated media, thereby underlying the importance of selecting new

The considered contaminated environment chiefly affected the biodiversity of the area and exerted a strong selective pressure on the local flora and mycoflora. These results suggest the use of *P. pinaster*, *A. utriculata*, *T. terrestris, S. polyrhizum, T. harzianum* and *C. rosea* for devel‐ oping experimental protocols of bioremediation and habitat restoration for avoiding ecosys‐ tem disruption.

**Figure 8.** Ag accumulation tests. **A**-**B**) Screening test of microfungal growth capability on silver enriched media; **C**) microscopic detail of the selected *Trichoderma* sp. strain **D**) *Trichoderma* sp. growth.

The study highlighted differences between mineralogy, geochemistry, flora and mycology among strongly polluted selected sites of the Libiola mine, which are key points for future reclamation of the area. In particular, our results evidenced the significant control of soil mineralogy and chemistry on the biodiversity of the mining area, as well as on the capacity of mycoflora and flora to accumulate specific metals. Knowing what the factors are influencing the first colonization by plants and the interaction among plants, fungi and soils, allow us to develop a method for the land restoration of metal polluted sites in a manner that minimizes interventions and costs.

## **3. Future perspectives – How to apply what we have learned**

Due to the complexity of soil and *in-situ* conditions, each contaminated site requires its own strategy and site-specific designs for decontamination, especially in Mediterranean areas. Multi-element contaminated soils contain several pollutants; consequently, it is necessary to screen out fungi and plants that can survive on different pollutants simultaneously and to accumulate or stabilize some of them.

The use of metal tolerant species adapted to native conditions can assist in balancing the ecological pressure generated by soil pollution. Consequently, it is necessary to evaluate the potential bioremediation of native fungi and plants from contaminated sites before choosing other species suitable for bioremediation.

Phytostabilization may be employed as a temporary solution until new techniques are available. However, for large contaminated sites (e.g., mining or industrial sites), phytostabi‐ lization likely represents the best option for ecosystem restoration [79]. Moreover, belowground restoration success involves the employment of native microfungi for developing and improving the soil microbial biomass [80].

In the joint use of plants and soil microorganisms, plants provide a C source for microorgan‐ isms, which absorb, degrade or release elements for plant absorption [81]. The plant allocates most of the metals to their roots so that plant shoots can be more efficient under metal stress [82]. Rhizospheric fungi are able to alleviate the stress of metals on plant growth through soil bioremediation (bioaugmentation) and can sometimes alleviate the unfavourable effects of metal on plant growth by the process of phytostabilization [83]. With the employment of the right soil, microfungi and ECM fungi, we can avoid amendments to soil, thereby improving organic matter and soil-forming processes that are essential for the colonization of pioneer plant species. These species will guarantee the durable, sustainable and ecological restoration of polluted mine sites, thereby increasing soil fertility.

The enormous potential of native fungi and plants that are able to colonize metal-contaminated soils need to be studied in-depth in order to preserve the natural genetic resources of metal‐ liferous habitats and to increase our basic knowledge about the natural adaptation mechanisms of hyperaccumulators in order to employ them in phytoremediation purposes.

## **Acknowledgements**

The study highlighted differences between mineralogy, geochemistry, flora and mycology among strongly polluted selected sites of the Libiola mine, which are key points for future reclamation of the area. In particular, our results evidenced the significant control of soil mineralogy and chemistry on the biodiversity of the mining area, as well as on the capacity of mycoflora and flora to accumulate specific metals. Knowing what the factors are influencing the first colonization by plants and the interaction among plants, fungi and soils, allow us to develop a method for the land restoration of metal polluted sites in a manner that minimizes

**Figure 8.** Ag accumulation tests. **A**-**B**) Screening test of microfungal growth capability on silver enriched media; **C**)

Due to the complexity of soil and *in-situ* conditions, each contaminated site requires its own strategy and site-specific designs for decontamination, especially in Mediterranean areas. Multi-element contaminated soils contain several pollutants; consequently, it is necessary to screen out fungi and plants that can survive on different pollutants simultaneously and to

**3. Future perspectives – How to apply what we have learned**

microscopic detail of the selected *Trichoderma* sp. strain **D**) *Trichoderma* sp. growth.

574 12 Biodiversity in Ecosystems - Linking Structure and Function

interventions and costs.

accumulate or stabilize some of them.

The authors wish to thank Carmela Sgrò for technical support provided during the laboratory work and Cristina Brusco for reviewing the paper for the English language.

## **Author details**

E. Roccotiello1\*, P. Marescotti2 , S. Di Piazza1 , G. Cecchi1 , M.G. Mariotti1 and M. Zotti1

\*Address all correspondence to: enrica.roccotiello@unige.it

1 Polo Botanico Hanbury, DISTAV-Department of Earth, Environment and Life Sciences, University of Genoa, Corso Dogali, Genoa, Italy

2 DISTAV-Department of Earth, Environment and Life Sciences, University of Genoa, Corso Europa, Genoa, Italy

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## **Underutilized Crops and Intercrops in Crop Rotation as Factors for Increasing Biodiversity on Fields**

Franc Bavec and Martina Bavec

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59131

## **1. Introduction**

Protection of biodiversity in intensive agricultural areas was one of the priorities of Common Agricultural Policy (CAP) and Agri-environmental payment (AEP 2007-2013) [1]. In general, AEP measures include crop rotation, the greening of fields, organic agriculture, soil coverage in water protected areas, etc., which depend on detailed national measures. In the new EU perspective of the Greening CAP reform 2014-2020 [2], three basic measures are foreseen in the first pillar: (i) maintaining permanent grassland; and (ii) crop diversification (a farmer must cultivate at least 2 crops when his arable land exceeds 10 hectares and at least 3 crops when his arable land exceeds 30 hectares. The main crop may cover at most 75% of arable land, and the two main crops at most 95% of the arable area); (iii) maintaining an "ecological focus area" of at least 5% of the arable area of the holding for farms with an area larger than 15 hectares (excluding permanent grassland) – i.e. field margins, hedges, trees, fallow land, landscape features, biotopes, buffer strips, afforested area. This figure will rise to 7% in 2017 according to the Commission report and the legislative proposal (CAP reform [2], MEMO 13/621, 26.6.2013). In the 2nd pillar documents (Regulation EU 1305/2013, 17.12.2013),'biodiversity' is mentioned 12 times and is mainly focused on conversion into organic farming, the protection of biodiversity in Nature 2000 areas and forest biodiversity conservation statuses of species and habitats, as well as enhancing the public amenity value of Nature 2000 areas or other high value nature areas. In these documents, we were mainly faced with general terms of biodi‐ versity, however the detailed measures in the second pillar should be defined on a national level. There is also the EU Biodiversity Strategy to 2020, which is trying to halt the loss of biodiversity and the degradation of ecosystem services in the EU by 2020. It is also trying to feasibly restore biodiversity, while stepping up the EU contribution to averting global biodiversity loss. In case of pollinators and their vs. pollinators' plants, they are mentioned

© 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2015 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

only in introduction of document. In the agricultural part the focus is only on maximising agricultural areas across grasslands, arable land and permanent crops that are covered by biodiversity-related measures under the CAP so as to ensure the conservation of biodiversity and to bring about a measurable improvement in the conservation status of species and habitats affected by agriculture and in the provision of ecosystem services as compared to the EU 2010 Baseline, thus contributing to enhance sustainable management; without mentioned intercrops and diverse – alternative crops.

### **2. Aim and methodology**

The Biodiversity Strategy to 2020, compared to previous documents, places more emphasis on field crop areas, but the measurements for 55.9 mio ha of field crop areas in Europe (FAO stat, 2012) are still not defined clearly enough, which is why special measurements for increasing the biodiversity of crops are needed on the intensive fields. As we can see in the Greening CAP reform 2014-2020 [2], these actions manage only a small portion of the 2nd and/or 3rd crop, and all of those can be produced in monoculture. Further on, the 1st Pillar supports more green washing than actual change of crop rotation, crop structure and diversity of field crops on the fields. Pillar 2, which depends on national regulations and is more open to potentially important measurements (like intercropping and introduction of alternative - rare - underu‐ tilized crops into field crop production for increasing biodiversity) is rarely mentioned in regulations and strategies. Sometimes its importance is unknown to administration workers, which is probably the reason why officers are not interested in their implementation (a good example is the Slovenian Ministry for Agriculture and Environment). A review of relevant literature, research and practical experiences of the authors will be present in this chapter.

### **3. Crop rotation**

It is a fact that intensive agriculture and dominant monoculture based on high chemical inputs and even genetically modified organisms in some countries are destroying the fields biodi‐ versity. The decreasing soil biodiversity does not support the natural cycles for sustaining good soil characteristics and natural plant nutrition pathways. For those in the system, like the US Corn Belt where these issues are key environmental problems include water contamination by nutrients and herbicides emitted from cropland, a lack of non-agricultural habitat to support diverse communities of native plants and animals and a high level of dependence on petro‐ chemical energy in the dominant cropping systems. In addition, projected changes in this region's climate, which include increases in the proportion of precipitation coming from extreme events, could make soil and water conservation in existing cropping systems more difficult [3]. In spite of the professionals' scepticisms about intensive systems, the authors Liebman et al. [3] concluded that increasing biodiversity through the strategic integration of perennial plant species can be a viable strategy for reducing the reliance on purchased inputs and for increasing agro ecosystem health and resilience in the US Corn Belt. It is our concern that the measures in the EU Greening CAP reform 2014-2020 in the first pillar will not solve these kinds of problems in European countries either.

only in introduction of document. In the agricultural part the focus is only on maximising agricultural areas across grasslands, arable land and permanent crops that are covered by biodiversity-related measures under the CAP so as to ensure the conservation of biodiversity and to bring about a measurable improvement in the conservation status of species and habitats affected by agriculture and in the provision of ecosystem services as compared to the EU 2010 Baseline, thus contributing to enhance sustainable management; without mentioned

The Biodiversity Strategy to 2020, compared to previous documents, places more emphasis on field crop areas, but the measurements for 55.9 mio ha of field crop areas in Europe (FAO stat, 2012) are still not defined clearly enough, which is why special measurements for increasing the biodiversity of crops are needed on the intensive fields. As we can see in the Greening CAP reform 2014-2020 [2], these actions manage only a small portion of the 2nd and/or 3rd crop, and all of those can be produced in monoculture. Further on, the 1st Pillar supports more green washing than actual change of crop rotation, crop structure and diversity of field crops on the fields. Pillar 2, which depends on national regulations and is more open to potentially important measurements (like intercropping and introduction of alternative - rare - underu‐ tilized crops into field crop production for increasing biodiversity) is rarely mentioned in regulations and strategies. Sometimes its importance is unknown to administration workers, which is probably the reason why officers are not interested in their implementation (a good example is the Slovenian Ministry for Agriculture and Environment). A review of relevant literature, research and practical experiences of the authors will be present in this chapter.

It is a fact that intensive agriculture and dominant monoculture based on high chemical inputs and even genetically modified organisms in some countries are destroying the fields biodi‐ versity. The decreasing soil biodiversity does not support the natural cycles for sustaining good soil characteristics and natural plant nutrition pathways. For those in the system, like the US Corn Belt where these issues are key environmental problems include water contamination by nutrients and herbicides emitted from cropland, a lack of non-agricultural habitat to support diverse communities of native plants and animals and a high level of dependence on petro‐ chemical energy in the dominant cropping systems. In addition, projected changes in this region's climate, which include increases in the proportion of precipitation coming from extreme events, could make soil and water conservation in existing cropping systems more difficult [3]. In spite of the professionals' scepticisms about intensive systems, the authors Liebman et al. [3] concluded that increasing biodiversity through the strategic integration of perennial plant species can be a viable strategy for reducing the reliance on purchased inputs and for increasing agro ecosystem health and resilience in the US Corn Belt. It is our concern

intercrops and diverse – alternative crops.

5842 Biodiversity in Ecosystems - Linking Structure and Function

**2. Aim and methodology**

**3. Crop rotation**

Biodiversity and plant protection against plant diseases and pests research is becoming an important issue in the world. For example, crop diseases are the most important natural disasters for food production and food safety, they are also one of the main reasons confining sustainable development of agricultural production. The discovery of the biodiversity mechanism (instead of chemicals and genetic modified organisms) to control crop diseases can reasonably guide the rational deployment and rotation of different crops and establish an optimization of different crop combinations [4].

The transformation of agriculture in the past half-century has triggered a decline in bees and other insect pollinators. In this case it is concluded [5] that areas of cultivated land farming, field margins, field edges and paths, headlands, fence-lines, rights of way, and nearby uncultivated patches of land are important refuges for many pollinators. According to the authors of this chapter, the yield of buckwheat increased twice in cases of pollination by honey bees compared to isolated plants by covering plots without honey bees (not published data). Likewise, crops including at least 800 cultivated plants depend on animal pollination in a functional biodiversity, which can be increased by intercrops and more diverse crop species in crop rotation. These solutions were not clearly defined and supported by professionals and policy makers, not even in the EU CAP reform and at the country levels as separate measures in Pillar 2 (like in Slovenia).

## **4. Biodiversity and the multifunctional importance of alternative field crops 1**

Intensive agriculture based on monoculture evidently reduces fields' biodiversity (Fig. 1) including the number of utilized crops and in consequence reduces natural health and nutritional compounds in the food. As reported by Jacobsen et al. [6], we have to safeguard both biodiversity and arable land for future agricultural food production, and we need to protect genetic diversity to safeguard ecosystem resilience. They conclude that majority of the research funding currently available for the development of genetically modified crops would be much better spent in other research areas of plant science, e.g., nutrition, policy research, governance, and solutions close to local market conditions if the goal is to provide sufficient food for the world's growing population in a sustainable way.

Introduction of alternative (rare, underutilized, disregarded, neglected, new and alternative GMO free) crops into the structure of field crop rotation can increase plant biodiversity and the nutritional and health value of food. Alternative crops are rich natural resources of essential amino acids, antioxidants, minerals, stimulators and other usable compounds, which are often limited to products from just a few main crops produced over the world. Production of

<sup>1</sup> The section based on research of Bavec F. presented in the Agrosym 2011 paper, which content is republished with permission.

**Figure 1.** Comparison of negative effects of monoculture and positive effects of crop rotation, alternative crops and intercrops on biodiversity parameters

underutilized crops shall help to increase resistance to plant diseases, predators, and helping us to produce food without synthetic pesticides [7]. The described organic production of underutilized field crops represents a very important option for an environmentally acceptable crop production and a niche for 'special organic' products. The selling of this kind of products is of special interest for small scale farms, because it is a better solution compared to producing and selling cheaper products on global markets. But in this case the consumers, advisers and farmers need professional knowledge about the preferences of underutilized crops, produc‐ tion characteristics, clear guidelines for organic production, post-harvest technology, food processing including product certification and clear marketing strategies. The support given by educational, research and governmental institutions should also be in accordance with these needs. Each specific possibility and activity of each country can influence the consumerproducer relationships and the effective marketing by specific or/and niche products based on underutilized crops [8, 9].

A rich biodiversity of produced edible underutilized field crops encompasses cereals and pseudo cereals including millets, pulse crops, root and tuber crops, oil seed crops and dyes, some of which (including fibre crops) are usable for creating new market niches based on small scale production and processing. Furthermore, some of them are also suitable for industrial processing. Depending on the country, some of these plants are indigenous, and based on spread secondary diversity, some are completely new, sometimes even exotic. The under‐ standing and use of underutilized crops is based mainly on tradition and the specifics of their growth circumstances. Most of them are unknown to a great percentage of agronomists. But the interest for underutilized crops is also increasing with publishers, because during the last decades a few publications spread the knowledge about underutilized field crops [10, 11, 12] with a special attention to temperate climate [7].

For example, in Slovenia temperate climate circumstances are predominant and just a small part is Mediterranean. For those, the tropic crops should be introduced into the temperate climate with special attention to a growth period of less than 160 frost free days, such as those for genotypes of sweet corn (*Zea mays* L. var. *saccharata*), batata (*Ipomea batata* L.) and other tropical tuber crops, specific genotypes of grain amaranths (*Amaranthus* sp.), quinoa (*Cheno‐ podium quinoa* L.), groundnut (*Arachis hypogea* L.), vignas (*Vigna* ssp.), etc. The next factor is the system of reproduction based on plant parts growth in greenhouse conditions during winter time like in the case of batata. The spelt which is well adapted to temperate climates (*Triticum aestivum* L. ssp. *spelta* MacKey) has been forgotten, however todays introduced into crop rotations on many organic farms with field crop production during the last decade. Other farro group cereals such as einkorn (*Tritium monocccum* L.), emmer (*Triticumdico*ccum L.), etc. are introduced into organic farming just like sample crops on a few farms. Buckwheat (*Fagopyrum esculentum* L.), proso millet (*Panicum milliaceum* L.) and oil seed pumpkins (*Cucurbita pepo* L. group Pepo) were traditional, but neglected until the last decade when their production started to increase. The group of alternative oil crops such as false flax (*Camelina sativa* L.), saflower (*Carthamus tinctorius* L.), garden poppy (*Papaver somniferum* L. ssp. *somniferum* Kadereit) are being researched and considered for eventual introduction into crop rotations. We are also looking at some legumes and the group of millets from Africa-potential crops for dry condi‐ tions described in the book Organic production and use of alternative crops by Bavec and Bavec [7]. In changing climate conditions some crops like millets from Africa and quinoa from the Andes might play an important role for creating new stress-tolerant species and genotypes for future agriculture. However, quinoa is described as a crop with high biodiversity value, which maintains productivity even on rather poor soils and high salinity [13].

underutilized crops shall help to increase resistance to plant diseases, predators, and helping us to produce food without synthetic pesticides [7]. The described organic production of underutilized field crops represents a very important option for an environmentally acceptable crop production and a niche for 'special organic' products. The selling of this kind of products is of special interest for small scale farms, because it is a better solution compared to producing and selling cheaper products on global markets. But in this case the consumers, advisers and farmers need professional knowledge about the preferences of underutilized crops, produc‐ tion characteristics, clear guidelines for organic production, post-harvest technology, food processing including product certification and clear marketing strategies. The support given by educational, research and governmental institutions should also be in accordance with these needs. Each specific possibility and activity of each country can influence the consumerproducer relationships and the effective marketing by specific or/and niche products based on

**Figure 1.** Comparison of negative effects of monoculture and positive effects of crop rotation, alternative crops and

underutilized crops [8, 9].

intercrops on biodiversity parameters

5864 Biodiversity in Ecosystems - Linking Structure and Function

Traditional cropping systems of undeveloped countries contain numerous genotypes of domesticated crop species, as well as their wild relatives. The richness of plant biodiversity of traditional agro-ecosystems is comparable with natural systems. It is one of the reasons why underutilized crops have to play a greater role, especially in organic farming. Underutilized crops bring diversity into crop rotations and provide new possibilities for soil cultivation. Organic farming, which is based on traditional farming systems, offers a way of promoting the diverse food and food risks, it increases pollinator insects and reduces plant insects and disease incidence, it is efficient in labour use and it also brings an intensification of production with acceptable resources, a maximization of returns and stability under responsible technol‐ ogies. Underutilized crops help local communities to be more independent while using the local resources for production and transport expense reduction. A similar option might be used for organically produced underutilized crops [14]. The use of underutilized field crops has resulted in an in ceased product competitiveness, a rich nutritional and health value of food, in tradition, locality, special quality according to organic production guidelines and even in market attractions. The health and nutritional rich products, especially if they are produced according to organic farming guidelines, represent a special niche in the market of the developed world.

Knowledge about food health and nutritional attributes based on underutilized crops is very useful for promotion, decision support for producers and for the buying motivation of consumers. Special attention needs to be given to the coexistence of pollinator insects and buckwheat, to antioxidants in food (tocopherols in oil crops, squalen in grain amaranths, anthocyanins in sweet potato, etc.), to rich amino acid compositions (grain amaranths, quinoa, partly buckwheat, partly legumes, etc.), to gluten free foods for people with celiac disease (buckwheat, grain amaranth, quinoa, millets), to good quality fibre food (whole grained spelt and other cereals), to food rich in minerals, vitamins and their good balance, etc. Many of them are used in pharmacology and alternative medicine, like oil seed pumpkins [15], buckwheat [16, 17, 18], amaranths [19, 20], etc.

The above information show a very interdisciplinary approach to alternative field crops, which can help to change the structure of crop diversity with clear steps towards a better social and economic behaviour. At the field level the rich crop diversity supports multifunctional processes like more sustainable nutrient cycles, caused by different root systems and different nutrient uptakes. A bigger variety of crops in crop rotation leads to more permanent soil covers of plants during growth periods, especially if they are grown in stubble crops. If some of them are grown as green manure they can have an important influence on soil fertility, because of more rich micro-organisms activity. In cases such as *Brasicaceaes*, for example white mustard (*Sinapis alba*), the crop also has a phytosanitary effect. Diverse crops encourage more sustain‐ able production systems because of the positive effects on relationships between predators and pests (Fig. 1). They also decrease plant diseases in crop rotation, because of their life cycle breaks.

## **5. Intercropping — Unexploited beneficial measure 2**

Intercropping (sowing two or more crops together) represents a high valued strategy for long term sustainable plant production management, due to its many beneficial effects like effects on increasing diversity of cultivated crops, nitrogen fixations by legumes [21, 22, 23, 24] instead of synthetic N fertilisers, weed control, yield stability, inter-specific complementarity, a more efficient use of environmental sources, soil coverage in under-sown crops, a higher protein

<sup>2</sup> The section based on research of Bavec F. presented in the Agrosym 2011 paper, which content is republished with permission.

content in seeds used for grain feed or silage mixture (especially important after BSE crises, etc.). Because of the complexity of these systems, intercropping has been neglected in practice and just partly researched as a plant production system under climates and cultivation circumstances worldwide. The research is deficient, especially in the case of intercropping impacts on biodiversity [25].

with acceptable resources, a maximization of returns and stability under responsible technol‐ ogies. Underutilized crops help local communities to be more independent while using the local resources for production and transport expense reduction. A similar option might be used for organically produced underutilized crops [14]. The use of underutilized field crops has resulted in an in ceased product competitiveness, a rich nutritional and health value of food, in tradition, locality, special quality according to organic production guidelines and even in market attractions. The health and nutritional rich products, especially if they are produced according to organic farming guidelines, represent a special niche in the market of the

Knowledge about food health and nutritional attributes based on underutilized crops is very useful for promotion, decision support for producers and for the buying motivation of consumers. Special attention needs to be given to the coexistence of pollinator insects and buckwheat, to antioxidants in food (tocopherols in oil crops, squalen in grain amaranths, anthocyanins in sweet potato, etc.), to rich amino acid compositions (grain amaranths, quinoa, partly buckwheat, partly legumes, etc.), to gluten free foods for people with celiac disease (buckwheat, grain amaranth, quinoa, millets), to good quality fibre food (whole grained spelt and other cereals), to food rich in minerals, vitamins and their good balance, etc. Many of them are used in pharmacology and alternative medicine, like oil seed pumpkins [15], buckwheat

The above information show a very interdisciplinary approach to alternative field crops, which can help to change the structure of crop diversity with clear steps towards a better social and economic behaviour. At the field level the rich crop diversity supports multifunctional processes like more sustainable nutrient cycles, caused by different root systems and different nutrient uptakes. A bigger variety of crops in crop rotation leads to more permanent soil covers of plants during growth periods, especially if they are grown in stubble crops. If some of them are grown as green manure they can have an important influence on soil fertility, because of more rich micro-organisms activity. In cases such as *Brasicaceaes*, for example white mustard (*Sinapis alba*), the crop also has a phytosanitary effect. Diverse crops encourage more sustain‐ able production systems because of the positive effects on relationships between predators and pests (Fig. 1). They also decrease plant diseases in crop rotation, because of their life cycle

Intercropping (sowing two or more crops together) represents a high valued strategy for long term sustainable plant production management, due to its many beneficial effects like effects on increasing diversity of cultivated crops, nitrogen fixations by legumes [21, 22, 23, 24] instead of synthetic N fertilisers, weed control, yield stability, inter-specific complementarity, a more efficient use of environmental sources, soil coverage in under-sown crops, a higher protein

2 The section based on research of Bavec F. presented in the Agrosym 2011 paper, which content is republished with

**5. Intercropping — Unexploited beneficial measure 2**

developed world.

breaks.

permission.

[16, 17, 18], amaranths [19, 20], etc.

5886 Biodiversity in Ecosystems - Linking Structure and Function

Farmers and researchers carry out different cropping systems to increase productivity and sustainability by using crop rotations, relay cropping, and intercropping of different annual crops. An associated culture often involves cereals and legumes due to its advantages for soil conservation, weed control, lodging resistance, yield increment, hay curing, forage preserva‐ tion over pure legumes, high crude protein content and protein yield. Different seeding ratios or planting patterns have been practised for cereal-legume intercropping. Bean yields in an intercrop culture are usually less sown than those obtained from sole bean stands. It is possible to increase yields with suitable management practices such as the use of optimum plant population and improved bean cultivars. However, bean yields in intercrops represent a surplus to the main maize crop yield. In EU countries, cowpea is rarely used in intercropping with cereals on small-scale farms. A number of indices such as land equivalent ratio, relative value total and monetary advantage have been proposed to describe the competition within and economic advantages of intercropping systems (from unpublished review, Bavec et al., Univ. Maribor). However, such indices have not been used for climbing bean (*Phaseolus vulgaris* L.) and maize intercropping to evaluate the competition among species and to evaluate the economic advantages of each intercropping system.

Intercropping of climbing bean and maize is a common production system on small scale farms and of interest to researchers in Latin America, as well as in South Africa, Ethiopia and other African countries. In a temperate climate, this type of intercropping has traditionally been practised 30 years ago, also on small-scale farms in Slovenia, Romania and in other Middle and Eastern European countries. Despite the fact that intercropping systems should involve integrating crops, using space and labour more efficiently, recommendations supporting good sole cropping systems, in which net incomes are also higher.

In Slovenia, two cases of conversion from a manual to mechanized production system of intercropped bean and maize production was established on an approximate 4 to 6 ha planting area per year, where the bean seeds are used for silage fed to ruminants (farm Jankovič, Vihre/ Krško), and for human consumption (farm Jakob, Lipovci). In the other European countries we also practically lost this traditional production system, although it still exists in some poor and self-sufficient small-scale farms, with some attention on the dry climate due to recent climate changes [26].

In general, important benefits of intercropping cereals with legumes are the following: more available nitrogen due to nitrogen fixation with legumes-with up to 84 % of nitrogen may be derived from fixation by the climbing bean, maize and bean intercropping may help converse a deficiency of bean production in European countries, in that it involves integrating crops using space and labour more efficiently, increased efficient competitions of cereals with weeds, improved soil structure, reduced loss of plant nutrients, less damage of plants due to pathogens and insects, especially in organic farming systems. Based on the available literature, most researches have focused on intercropping bush beans in non-European growing conditions. Because of the different canopy characteristics of bush beans, data for bush beans are not comparable with climbing bean maize intercropping – this has only been reported by Gebeye‐ hu et al. [27]. However, there is a lack of scientifically relevant information about promising plant ratios of maize-climbing bean intercropping systems, especially for the ones produced in European temperate zones under integrated or organic production systems.

In this paper we want to focus our attention on two additional reasons for the proposed intercropping climbing bean/maize in temperate climate vs. marginal regions for maize (to FAO group 400) production [28], which are also suitable for growing climbing beans, due to temperatures and humidity, enabling a simple and environmentally friendly production. In this case the soil preparation is conventional (ploughing in autumn, pre-sowing soil prepara‐ tion in spring), the same machine is used for sowing maize and bean seeds. The bean seeds need to be sown close to the maize strips at the stage when the maize has few true leaves, after the 1st or 2nd inter-row mechanical hoeing, close to the strips of the maize plants. For harvesting the maize bean whole plant mixture a silage combine is used, but for the seed harvesting a cereal combine and eventual separation of the bean and maize seeds could take place. The second benefit is the production of protein rich silage caused by bean grains, which contain approximately 20% of crude proteins. These kinds of proteins are good and might be a relatively cheap replacement for animal source proteins, which are not allowed for ruminants feed after the appearance of BSE 'mad cow disease'.

In cereal-legume intercropping, cereal crops establish uniform canopy structures and then legume crops and the roots of cereal crops grow to a greater depth than those of legume crops with less lodging consequences [29]; however the agronomic traits of genotypes need to be well adapted for intercropping. Climbing bean cultivars need specific adaptations to intercrops using predominantly morphological maize types grown in the area [27]. Somewhat earlier maize cultivars can give an improved net income when intercropped with climbing beans, because they are resistant to stem lodging. This indicates that the component crops probably have differing spatial and temporal use of environmental resources such as radiation, water and nutrients. Therefore, this cropping system may help improve productivity of low external input farming, which depends largely on natural resources such as rainfall and soil fertility. The intercropping productivity is largely dependent on planting date and plant population of its components. Small-scale farmers have practised traditional cropping techniques, such as intercropping, in which they unknowingly manipulate the plant population [28] because that way, interspecies competition is stronger.

The effects of intercrops on weed communities were characterised in terms of growth, species diversity (richness and evenness), and floristic and functional composition. Intercrops and barley monocultures generally produced similar effects on the companion weed communities, whereas pea effects were less suppressive and more variable. Spring-emerging species generally increased its relative importance in the intercrop weed communities; whereas winter-emerging species were usually less abundant in intercrops. Divergence in the abun‐ dance of winter and summer emerging weeds could be attributed to the different canopy dynamics of intercrops and monocultures [30].

Plant diversity based on intercropping systems includes potentially important mechanism for chemically mobilizing nutrients in otherwise-unavailable forms of one or more limiting soil nutrients, such as phosphorus (P) and micronutrients (iron (Fe), zinc (Zn) and manganese (Mn)). In case of phosphorus-mobilizing, crop species improve P nutrition for themselves and neighbouring non-P-mobilizing species by releasing acid phosphatases, protons and/or carboxylates into the rhizosphere which increases the concentration of soluble inorganic P in soil. Similarly, on calcareous soils with a very low availability of Fe and Zn, Fe-and Znmobilizing species, such as graminaceous monocotyledonous and cluster-rooted species, benefit themselves, and also reduce Fe or Zn deficiency in neighbouring species, by releasing chelating substances [31].

Only in one EU research programme a survey was carried out within five European countries with regard to the practice of cereal grain legume intercropping. The most commonly used combination was spring barley-spring pea with 27 other combinations between pulses and cereals. 72 % of all examples consisted of spring varieties and the rest of winter varieties, mainly a special case of the French South West with a mild winter climate. Intercrops were mainly used for feeding purposes. Yield stability, effective weed suppression, and good quality of feed were reported as the best outcomes. The negative outcomes were complicated mechanical weed regulation, unequal maturation and additional costs for separation. The interviewed farmers showed predominantly positive prospects for the development of intercropping on their farms, problems with sowing techniques being the only importance [32].

Based on the statements in this chapter, we can once again underline the importance of the use of well-known [33] and new findings of beneficial intercropping effects on productivity and biodiversity in different farming systems [34] which is especially very important in changing climates [35]. Because the fact that intercropping is a more expensive and complicated cultivation than sole crop production, intercrops need wider support (like new research and simulation models) [36] that will be included in farming systems as a basic environmental measure at the field production level.

## **6. Conclusions**

researches have focused on intercropping bush beans in non-European growing conditions. Because of the different canopy characteristics of bush beans, data for bush beans are not comparable with climbing bean maize intercropping – this has only been reported by Gebeye‐ hu et al. [27]. However, there is a lack of scientifically relevant information about promising plant ratios of maize-climbing bean intercropping systems, especially for the ones produced

In this paper we want to focus our attention on two additional reasons for the proposed intercropping climbing bean/maize in temperate climate vs. marginal regions for maize (to FAO group 400) production [28], which are also suitable for growing climbing beans, due to temperatures and humidity, enabling a simple and environmentally friendly production. In this case the soil preparation is conventional (ploughing in autumn, pre-sowing soil prepara‐ tion in spring), the same machine is used for sowing maize and bean seeds. The bean seeds need to be sown close to the maize strips at the stage when the maize has few true leaves, after the 1st or 2nd inter-row mechanical hoeing, close to the strips of the maize plants. For harvesting the maize bean whole plant mixture a silage combine is used, but for the seed harvesting a cereal combine and eventual separation of the bean and maize seeds could take place. The second benefit is the production of protein rich silage caused by bean grains, which contain approximately 20% of crude proteins. These kinds of proteins are good and might be a relatively cheap replacement for animal source proteins, which are not allowed for ruminants

In cereal-legume intercropping, cereal crops establish uniform canopy structures and then legume crops and the roots of cereal crops grow to a greater depth than those of legume crops with less lodging consequences [29]; however the agronomic traits of genotypes need to be well adapted for intercropping. Climbing bean cultivars need specific adaptations to intercrops using predominantly morphological maize types grown in the area [27]. Somewhat earlier maize cultivars can give an improved net income when intercropped with climbing beans, because they are resistant to stem lodging. This indicates that the component crops probably have differing spatial and temporal use of environmental resources such as radiation, water and nutrients. Therefore, this cropping system may help improve productivity of low external input farming, which depends largely on natural resources such as rainfall and soil fertility. The intercropping productivity is largely dependent on planting date and plant population of its components. Small-scale farmers have practised traditional cropping techniques, such as intercropping, in which they unknowingly manipulate the plant population [28] because that

The effects of intercrops on weed communities were characterised in terms of growth, species diversity (richness and evenness), and floristic and functional composition. Intercrops and barley monocultures generally produced similar effects on the companion weed communities, whereas pea effects were less suppressive and more variable. Spring-emerging species generally increased its relative importance in the intercrop weed communities; whereas winter-emerging species were usually less abundant in intercrops. Divergence in the abun‐ dance of winter and summer emerging weeds could be attributed to the different canopy

in European temperate zones under integrated or organic production systems.

feed after the appearance of BSE 'mad cow disease'.

5908 Biodiversity in Ecosystems - Linking Structure and Function

way, interspecies competition is stronger.

dynamics of intercrops and monocultures [30].

Based on the lack of environmental indicators which influence the functional biodiversity in the field, a precisely described importance of crop rotation, introduction of underutilized crops and intercrops, is given. Due to their many beneficial effects (crop rotation, nitrogen fixations by legumes instead of synthetic N fertilisers, weed suppression, yield stability, inter-specific complementarily, more efficient use of environmental sources, soil cover at under-sown crops, higher protein content in the seeds for grain feed or silage mixture, especially important after BSE crises), inter-cropping and underutilized crops represents a high valued strategy for long term biodiversity and sustainable plant production management. Because of the farmland intensification and complexity of biodiversity, intercropping and underutilized crops have been neglected in practice and only partly researched as a plant production system under different cultivation circumstances (sometimes site specific). More diverse crops and inter‐ cropping support a more stable ecosystem productivity, especially in the case of intercrops with legumes; here the inputs of artificial nitrogen can be significantly reduced. However, ecological intensification of agriculture depends on simple and clear ecologically oriented agro-environmental policies all over the world, which will not support »green washing« of conventional agriculture or »conventionalisation« of organic farming. Because of climate changes, the alternative field crops and intercrops need more political support and should be taken into account in EU CAP and OECD policies, which do not include suggested measures on national levels as part of environmental payments, not even outside Europe. Because of their importance, intercrops and alternative crops need to be a part of biodiversity indicators at field and landscape levels.

## **Acknowledgements**

The idea for this paper came as part of the project 'CRP V4-1137 Alternative field crops in different production systems and crop rotations as a base for adaptation to climate changes and food supply with food and feed' supported by the Ministry of Education, Science and Sport and the Ministry of Agriculture and the Environment, for which we are thankful.

### **Author details**

Franc Bavec\* and Martina Bavec

\*Address all correspondence to: franci.bavec@um.si

University of Maribor, Faculty of Agriculture and Life Sciences, Hoce/Maribor, Slovenia

### **References**


[4] Yang J., Shi Z-F., Gao D., Liu L., Li C. Y. Mechanism on biodiversity managing crop diseases. Yichuan. 2012;34 1390-1398.

cropping support a more stable ecosystem productivity, especially in the case of intercrops with legumes; here the inputs of artificial nitrogen can be significantly reduced. However, ecological intensification of agriculture depends on simple and clear ecologically oriented agro-environmental policies all over the world, which will not support »green washing« of conventional agriculture or »conventionalisation« of organic farming. Because of climate changes, the alternative field crops and intercrops need more political support and should be taken into account in EU CAP and OECD policies, which do not include suggested measures on national levels as part of environmental payments, not even outside Europe. Because of their importance, intercrops and alternative crops need to be a part of biodiversity indicators

The idea for this paper came as part of the project 'CRP V4-1137 Alternative field crops in different production systems and crop rotations as a base for adaptation to climate changes and food supply with food and feed' supported by the Ministry of Education, Science and Sport and the Ministry of Agriculture and the Environment, for which we are thankful.

University of Maribor, Faculty of Agriculture and Life Sciences, Hoce/Maribor, Slovenia

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592 10 Biodiversity in Ecosystems - Linking Structure and Function

**Acknowledgements**

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\*Address all correspondence to: franci.bavec@um.si

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