**Ecological Flexibility of the Top Predator in an Island Ecosystem — The Iriomote Cat Changes Feeding Patterns in Relation to Prey Availability**

Shinichi Watanabe

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59502

## **1. Introduction**

It has long been recognized that islands contain fewer species than comparable pieces of mainland. It is also well-established that the number of species on islands decreases as island area declines. The most successfully established islands species will be those that combine low extinction rates with high immigration rates and where it is generally more difficult for animals without high dispersal ability at higher trophic levels to live on small islands [1]. In particular, carnivorous mammals at the top of terrestrial trophic chain find it most difficult to establish themselves on islands. Extreme examples are considerably large body sized and complete carnivorous species in the family Felidae.

In the region from south-east Asia to the Ryukyu Archipelago in southern Japan, there are thousands of islands of various sizes [2]. In this region, it is well-documented that biodiversity is particularly high among many taxa [3]. The biodiversity of mammalian fauna in this region was summarized in [4]. Among Felidae, seven species are distributed in this region, most of which are distributed only on the continental islands of Java, Sumatra, Borneo and Taiwan [4]. In particular, the leopard cat *Prionailurus bengalensis*, the most widespread species of East Asian wildcats, is an exception to this rule, occurring on several small islands as well as larger islands and the Asian continent [2, 4].

An example of an extreme case is the Iriomote cat *Prionailurus bengalensis iriomotensis* (Figure 1), which lives on the smallest island (284 km2 , Figure 2) of the Ryukyu Archipelago. The Iriomote cat is unique among the family Felidae, particularly in terms of its food habits [5-8]. Felidae are known as the most successfully evolved and developed predators specialized in feeding on mammalian prey [9, 10]. In contrast, the Iriomote cat preys upon a variety of animals

© 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 reproduction in any medium, provided the original work is properly cited.

such as birds, reptiles, amphibians and insects, in addition to mammals [5-8]. The cat shows functional responses according to the availability of various alternative sources of prey [7]. Its principle prey changes seasonally, as the population density of potential prey items change. Moreover, regional differences in the cat's diet have also been reported [5, 11]. The Iriomote cat's diet is more diversified in habitats in which several vegetative environments are included and more similar in habitats where vegetative environments are uniform [11]. For terrestrial vertebrates on the island, distribution of each species is strongly influenced by various topographic and vegetative environmental factors, and distribution patterns vary depending on the type of species [12]. The cat diet changes flexibly in relation to seasonal and regional differences in prey availability [6, 7, 11]. Thus, it is likely that the preferred habitats for this species will also vary depending on seasons and regions.

**Figure 1.** An Iriomote cat *Prionailurus bengalensis iriomotensis* taken by photo-trap (Mammal Ecology Laboratory, Uni‐ versity of the Ryukyus).

Most animals selectively use environments with a good quality of food patches [13, 14]. It is therefore likely that predators specializing in a particular food type that occurs in specific habitats will be habitat specialists, while predators feeding on a range of different food types will be habitat generalists. Variation in prey availability, i.e., the density and distribution of prey animals in an environment, leads to various predator responses [15-18]. For example, predators specialized in catching particular prey types often produce numerical responses to prey availability, so that the density of predators fluctuates alongside prey density [15-17]. In contrast, non-specialized predators often produce functional responses to prey availability, allowing these predators to switch prey types in relation to the availability of alternative resources [18].

6 Borneo and Taiwan [4]. In particular, the leopard cat *Prionailurus bengalensis*, the most 7 widespread species of East Asian wildcats, is an exception to this rule, occurring on several 8 small islands as well as larger islands and the Asian continent [2,4]. Ecological Flexibility of the Top Predator in an Island Ecosystem — The Iriomote Cat Changes Feeding Patterns… 3 http://dx.doi.org/ 10.5772/59502 355

2 Book Title

In the region from south-east Asia to the Ryukyu Archipelago in southern Japan, there are thousands of islands of various sizes [2]. In this region, it is well-documented that biodiversity is particularly high among many taxa [3]. The biodiversity of mammalian fauna in this region was summarized in [4]. Among Felidae, seven species are distributed in this region, most of which are distributed only on the continental islands of Java, Sumatra,

17

18

19

20

21

such as birds, reptiles, amphibians and insects, in addition to mammals [5-8]. The cat shows functional responses according to the availability of various alternative sources of prey [7]. Its principle prey changes seasonally, as the population density of potential prey items change. Moreover, regional differences in the cat's diet have also been reported [5, 11]. The Iriomote cat's diet is more diversified in habitats in which several vegetative environments are included and more similar in habitats where vegetative environments are uniform [11]. For terrestrial vertebrates on the island, distribution of each species is strongly influenced by various topographic and vegetative environmental factors, and distribution patterns vary depending on the type of species [12]. The cat diet changes flexibly in relation to seasonal and regional differences in prey availability [6, 7, 11]. Thus, it is likely that the preferred habitats for this

**Figure 1.** An Iriomote cat *Prionailurus bengalensis iriomotensis* taken by photo-trap (Mammal Ecology Laboratory, Uni‐

Most animals selectively use environments with a good quality of food patches [13, 14]. It is therefore likely that predators specializing in a particular food type that occurs in specific habitats will be habitat specialists, while predators feeding on a range of different food types will be habitat generalists. Variation in prey availability, i.e., the density and distribution of prey animals in an environment, leads to various predator responses [15-18]. For example, predators specialized in catching particular prey types often produce numerical responses to prey availability, so that the density of predators fluctuates alongside prey density [15-17]. In contrast, non-specialized predators often produce functional responses to prey availability, allowing these predators to switch prey types in relation to the availability of alternative

species will also vary depending on seasons and regions.

3542 Biodiversity in Ecosystems - Linking Structure and Function

versity of the Ryukyus).

resources [18].

22 **Figure2.** Map of East Asia showing islands with 23 wild felid populations (left) according to [2] and **Figure 2.** Map of East Asia showing islands with wild felid populations (left) according to [2] and Iriomote Island (Ryukyu Archipelago, Japan, right) showing the locations of seven study sites where radio-tracking were conducted. Each dark area shows the home range of each studied cat, estimated by the 75% harmonic mean method.

In the case of carnivores, food habits are well-documented at interspecific levels [e.g., 19, 20]. Each felid species takes only a few different mammal prey items, while other carnivores eat various food types. The Felidae family is highly specialized in preying on mammals in terms of having developed morphological and behavioural traits [21, 22]. Thus, Felidae are consid‐ ered typical specialists in terms of food and habitat. Their hunting behaviour is specialized for preying on mammalian prey items [21]. Hence, they often show a numerical response to the density of a particular prey species [e.g., 18, 23]. 24 Iriomote Island (Ryukyu Archipelago, Japan, 25 right) showing the locations of seven study sites 26 where radio-tracking were conducted. Each dark 27 area shows the home range of each studied cat, 28 estimated by the 75% harmonic mean method. 29 An example of an extreme case is the Iriomote cat *Prionailurus bengalensis iriomotensis* (Figure 1), which lives on the smallest island (284 km<sup>2</sup> 30 , Figure 2) of the Ryukyu Archipelago. 31 The Iriomote cat is unique among the family Felidae, particularly in terms of its food habits

The Iriomote cat, however, preys on various types of animals. Its diet flexibly changes in relation to seasonal and regional differences of prey availability [5-8; see also the results in the present study]. It is therefore likely that the Iriomote cat makes use of a variety of habitats and movement patterns in response to spatio-temporal variations in prey availability. 32 [5-8]. Felidae are known as the most successfully evolved and developed predators 33 specialized in feeding on mammalian prey [9,10]. In contrast, the Iriomote cat preys upon a 34 variety of animals such as birds, reptiles, amphibians and insects, in addition to mammals 35 [5-8]. The cat shows functional responses according to the availability of various alternative 36 sources of prey [7]. Its principle prey changes seasonally, as the population density of 37 potential prey items change. Moreover, regional differences in the cat's diet have also been

A comprehensive and accurate analysis of habitat use and selection, particularly when dealing with large home ranges and high habitat diversity across the geographic range of an animal, must encompass multiple spatial scales [24]. A number of studies have been conducted on the habitat use of the Iriomote cat, but these have only investigated the habitat selection on a univariate scale. Sakaguchi [5] emphasized that the Iriomote prefers to use lowlands (< 50 m above sea level) and avoids highlands, yet other factors potentially affecting their habitat use have not been investigated. In the present study, I will therefore quantify seasonal and regional variations in the habitat use and movement patterns of the Iriomote cat using detailed microhabitat measures at point locations and detailing the movement tracks used by the cat. From the results, I will then discuss their feeding strategies in terms of seasonal and regional 38 reported [5,11]. The Iriomote cat's diet is more diversified in habitats in which several 39 vegetative environments are included and more similar in habitats where vegetative variations in prey availability. Furthermore, I will also present the possible reasons for the presence of this species on Iriomote Island.


**Table 1.** Summary of the radio-tracking survey in seven study sites on Iriomote Island.

## **2. Methods**

### **2.1. Field survey**

A field survey was conducted on Iriomote Island (24°20'N, 123°49'E) in the Ryukyu Archipe‐ lago, southern Japan (Figure 2). The island largely consists of highly folded mountains with the highest peak (Mt. Komi) being 469 m above sea level. Its vegetation is mostly natural subtropical evergreen broadleaved forest. Most of the island is protected as a Japanese national park and contains good examples of the natural subtropical forests (see [7] for more informa‐ tion about the island).

Cats were trapped using box traps during the following six periods, May to July and October in 1999, January, June and November in 2000 and November in 2001. For the captures, boxtraps equipped with radio-alarm systems were used. Captured cats were immediately brought to a laboratory and anesthetized by a professional veterinarian with an intramuscular injection of ketamine hydrochloride and xylazine (ketamine hydrochloride 10 mg/kg body weight). The animals were weighed and measured; their age-classes were estimated according to tooth wear, body weight and the delivery history of females [5, 25]. The cats were fitted with 40 g radio collars (Advanced Telemetry Systems Inc., Isanti, Minnesota, USA., or alternatively, collars hand-made in my laboratory).

I captured and radio-tracked a total of 16 adult cats (nine males and seven females) (Table 1) in seven separate study sites (Figure 2). All females were parous when captured, as per evidence of previous suckling marks on their nipples [5, 25]. Each cat remained in the same study site throughout the study period.

The movements of radio-collared cats were continuously monitored for seven-to 10-day periods, either by car or on foot. Locations used by the cats were taken at intervals of at least one hour using the triangulation software Loas version 2.1 (Ecological Software Solutions) from two-to four-points, marked with a handheld global positioning system (GPS; model Garmin GPS II Plus) on roads or trails. I then determined the universal transverse mercator (UTM; zone 51, WGS84 Datum) coordinates of cats' locations using a geographic information system (GIS) and the IDRISI Kilimanjaro version 14 software (Clark Labs, Clark University, Worcester MA, USA).

### **2.2. Scat analysis**

variations in prey availability. Furthermore, I will also present the possible reasons for the

Study site Tracked period Tracked days No. of location

Otomi Jul. 12. 1999 Jan. 19. 2001 79 2 1 545 Maira Jun. 22. 2000 Dec. 25. 2001 33 2 238 Komi Jun. 04. 1999 Dec. 25. 2001 254 1 2 1211 NCA Nov. 20. 2001 Mar. 07. 2002 62 3 340 Funaura Jun. 18. 2000 Feb. 15. 2001 69 1 1 457 Urauchi Jun. 16. 2000 Aug. 28. 2000 13 1 66 Shirahama Oct. 12. 1998 Nov. 06. 1999 155 1 1 1229

**Table 1.** Summary of the radio-tracking survey in seven study sites on Iriomote Island.

Total 665 9 7 4086

A field survey was conducted on Iriomote Island (24°20'N, 123°49'E) in the Ryukyu Archipe‐ lago, southern Japan (Figure 2). The island largely consists of highly folded mountains with the highest peak (Mt. Komi) being 469 m above sea level. Its vegetation is mostly natural subtropical evergreen broadleaved forest. Most of the island is protected as a Japanese national park and contains good examples of the natural subtropical forests (see [7] for more informa‐

Cats were trapped using box traps during the following six periods, May to July and October in 1999, January, June and November in 2000 and November in 2001. For the captures, boxtraps equipped with radio-alarm systems were used. Captured cats were immediately brought to a laboratory and anesthetized by a professional veterinarian with an intramuscular injection of ketamine hydrochloride and xylazine (ketamine hydrochloride 10 mg/kg body weight). The animals were weighed and measured; their age-classes were estimated according to tooth wear, body weight and the delivery history of females [5, 25]. The cats were fitted with 40 g radio collars (Advanced Telemetry Systems Inc., Isanti, Minnesota, USA., or alternatively,

I captured and radio-tracked a total of 16 adult cats (nine males and seven females) (Table 1) in seven separate study sites (Figure 2). All females were parous when captured, as per

Male Female

No. of cats

presence of this species on Iriomote Island.

3564 Biodiversity in Ecosystems - Linking Structure and Function

**2. Methods**

**2.1. Field survey**

tion about the island).

collars hand-made in my laboratory).

Seasonal and local variations on diet compositions among the study sites were examined via scat analysis [6-8]. Scats collected in each study site (Figure 2) were used for the analysis. Diet composition and principal prey items were compared among the sites. I calculated the frequency of occurrences for each prey taxon: mammals, birds, reptiles, amphibians, insects, crustaceans and others; this was done for each season and site.

### **2.3. Data analysis**

### *2.3.1. Environmental measurements*

I measured nine environmental variables related to topographic and vegetative characteristics within habitats to determine regional differences in environments among the study sites, as well as the most important factors that influenced the habitat preferences of the Iriomote cat. IDRISI [26], an integrated GIS and remote sensing software, was used for the analysis and display of digital geospatial information. IDRISI is a PC grid-based system that offers tools for researchers and scientists engaged in analysing earth system dynamics for effective and responsible decision making regarding environmental management [26].

Three topographic variables, elevation (El), slope (Sl) and the presence of drainage (Dr), were derived from digital elevation models (Digital Map 50 m Mesh Elevation, published by the Japan Geographical Survey Institute). The topographic data contained elevation values of one meter precision at the centre of grids by latitudinal 1.5 second and longitudinal 2.25 second; the ground length was roughly 50 m. The elevation data were geometrically-corrected in the UTM coordinate as a raster image showing a 50 m x 50 m grid. Sl and Dr were derived from the image using the Surface and Runoff operations of IDRISI. Elevation data generally contain depressions that hinder flow routing; these were removed and then I calculated the accumu‐ lation of rainfall units per pixel based on the elevation image. Drainage networks can produce a setting for discovering a threshold on the accumulation of runoff [26]. In the present study, the threshold (50 pixels) was able to detect permanent stable water and as such, streams and rivers in the study area were set. These three variables were subdivided into a 10 m x 10 m grid; images of El and Sl were averaged among neighbouring 5 x 5 pixels using the Filter 1

6 Book Title

2 **Figure3.** Mean values (+*SD*) of elevation and slope within the home ranges of the Iriomote 3 cat in seven study sites. **Figure 3.** Mean values (+*SD*) of elevation and slope within the home ranges of the Iriomote cat in seven study sites.

operation of IDRISI. Thus, the distance (10 m) and planimetry (100 m2 ) accuracies in this study were limited by the grid size. 4 Vegetative variables were derived from a digital vegetation map [27], in which vegetation 5 was classified as 29 categories within the study area. Many categories had a few patches, 6 while some categories were very similar to others. I combined similar habitat types and

Vegetative variables were derived from a digital vegetation map [27], in which vegetation was classified as 29 categories within the study area. Many categories had a few patches, while some categories were very similar to others. I combined similar habitat types and broadly classified these in the following five categories; natural forest (NF) including subtropical, evergreen and broad-leaved forests; secondary forest (SF), including pine and artificial forests; coastal vegetation (CV), including mangroves and vegetation along shorelines; rice fields and swamps (RS); croplands and postures (CP). The vegetation classified into five categories was also geometrically-correlated in the same UTM coordinate as the raster image showing a 10 m x 10 m grid. 7 broadly classified these in the following five categories; natural forest (NF) including 8 subtropical, evergreen and broad-leaved forests; secondary forest (SF), including pine and 9 artificial forests; coastal vegetation (CV), including mangroves and vegetation along 10 shorelines; rice fields and swamps (RS); croplands and postures (CP). The vegetation 11 classified into five categories was also geometrically-correlated in the same UTM coordinate 12 as the raster image showing a 10 m x 10 m grid. 13 Since the Iriomote cat prefers to use the boundaries of forests and open lands [28,29], I 14 presumed that the prey availability of some species was high along forest edges, which 15 influenced their food habits. Thus, a variable (FE: presence of forest edges) was derived 16 from the 10 m x 10 m vegetation grid data using the Buffer operation of IDRISI. Forest edge 17 was defined as zones within 50 m toward forests (NF and SF) from other vegetation types.

Since the Iriomote cat prefers to use the boundaries of forests and open lands [28, 29], I presumed that the prey availability of some species was high along forest edges, which influenced their food habits. Thus, a variable (FE: presence of forest edges) was derived from the 10 m x 10 m vegetation grid data using the Buffer operation of IDRISI. Forest edge was defined as zones within 50 m toward forests (NF and SF) from other vegetation types. 18 19 **Table 2.** Percentages of drainages (Dr) and forest edges (FE) in the home ranges of the 20 Iriomote cat in each study site. Variable Otomi Maira Komi NCA Funaura Urauchi Shirahama *G d.f. P* DR 4.9 6.0 5.9 6.7 5.4 7.0 5.4 190 6 <0.0001 FE 18.9 38.6 12.1 12.5 14.2 9.3 14.6 3957 6 <0.0001 Study site


**Table 2.** Percentages of drainages (Dr) and forest edges (FE) in the home ranges of the Iriomote cat in each study site. compared among sites. The differences between the continuous variables (El and Sl, see Figure 3) among study sites were subjected to a Kruskal-Wallis test for those that were significantly different, while the seven other categorical variables (Table 2, Figure 4) were

#### *2.3.2. Habitat types in home ranges* 30 subjected to a likelihood-ratio test (*G*-test) for independence to test for differences.

I estimated the home range of each radio-collared cat from the coordinates of radio-tracking locations using home range estimation software Biotas version 1.0 (Ecological Software Solutions). The home range (HR) was defined as the area enclosed within the 75% utilization contour with the harmonic mean [30]. I overlaid HRs of all radio-collared cats in each study site (Figure 2), in which environments concerning the above nine variables were compared among sites. The differences between the continuous variables (El and Sl, see Figure 3) among study sites were subjected to a Kruskal-Wallis test for those that were significantly different, while the seven other categorical variables (Table 2, Figure 4) were subjected to a likelihoodratio test (*G*-test) for independence to test for differences.

**Figure 4.** Compositions of vegetation types (NF: natural forest; SF: secondary forest; CV: coastal vegetation; RS: rice fields and swamps; CP: croplands and postures) within the home ranges of the Iriomote cat in seven study sites (Ot: Otomi; Ma: Maira; Ko: Komi; NCA: northern coastal area; Fu: Funaura; Ur: Urauchi; Sh: Shirahama).

### *2.3.3. Habitat preferences on cat location*

operation of IDRISI. Thus, the distance (10 m) and planimetry (100 m2

Vegetative variables were derived from a digital vegetation map [27], in which vegetation was classified as 29 categories within the study area. Many categories had a few patches, while some categories were very similar to others. I combined similar habitat types and broadly classified these in the following five categories; natural forest (NF) including subtropical, evergreen and broad-leaved forests; secondary forest (SF), including pine and artificial forests; coastal vegetation (CV), including mangroves and vegetation along shorelines; rice fields and swamps (RS); croplands and postures (CP). The vegetation classified into five categories was also geometrically-correlated in the same UTM coordinate as the raster image showing a 10 m

Since the Iriomote cat prefers to use the boundaries of forests and open lands [28,29], I presumed that the prey availability of some species was high along forest edges, which influenced their food habits. Thus, a variable (FE: presence of forest edges) was derived from the 10 m x 10 m vegetation grid data using the Buffer operation of IDRISI. Forest edge was defined as zones within 50 m toward forests (NF and SF) from other vegetation types.

2 **Figure3.** Mean values (+*SD*) of elevation and slope within the home ranges of the Iriomote

**Figure 3.** Mean values (+*SD*) of elevation and slope within the home ranges of the Iriomote cat in seven study sites.

Vegetative variables were derived from a digital vegetation map [27], in which vegetation was classified as 29 categories within the study area. Many categories had a few patches, while some categories were very similar to others. I combined similar habitat types and broadly classified these in the following five categories; natural forest (NF) including subtropical, evergreen and broad-leaved forests; secondary forest (SF), including pine and artificial forests; coastal vegetation (CV), including mangroves and vegetation along shorelines; rice fields and swamps (RS); croplands and postures (CP). The vegetation classified into five categories was also geometrically-correlated in the same UTM coordinate

6 Book Title

Since the Iriomote cat prefers to use the boundaries of forests and open lands [28, 29], I presumed that the prey availability of some species was high along forest edges, which influenced their food habits. Thus, a variable (FE: presence of forest edges) was derived from the 10 m x 10 m vegetation grid data using the Buffer operation of IDRISI. Forest edge was defined as zones within 50 m toward forests (NF and SF) from other vegetation types.

Study site

Otomi Maira Komi NCA Funaura Urauchi Shirahama *G d.f. P* DR 4.9 6.0 5.9 6.7 5.4 7.0 5.4 190 6 <0.0001 FE 18.9 38.6 12.1 12.5 14.2 9.3 14.6 3957 6 <0.0001

19 **Table 2.** Percentages of drainages (Dr) and forest edges (FE) in the home ranges of the

I estimated the home range of each radio-collared cat from the coordinates of radio-tracking locations using home range estimation software Biotas version 1.0 (Ecological Software Solutions). The home range (HR) was defined as the area enclosed within the 75% utilization contour with the harmonic mean [30]. I overlaid HRs of all radio-collared cats in each study site (Figure 2), in which environments concerning the above nine variables were compared among sites. The differences between the continuous variables (El and Sl, see Figure 3) among study sites were subjected to a Kruskal-Wallis test for those that were significantly different, while the seven other categorical variables (Table 2, Figure 4) were

Otomi Maira Komi NCA Funaura Urauchi Shirahama *G d.f. P* DR 4.9 6.0 5.9 6.7 5.4 7.0 5.4 190 6 <0.0001 FE 18.9 38.6 12.1 12.5 14.2 9.3 14.6 3957 6 <0.0001

**Table 2.** Percentages of drainages (Dr) and forest edges (FE) in the home ranges of the Iriomote cat in each study site.

I estimated the home range of each radio-collared cat from the coordinates of radio-tracking locations using home range estimation software Biotas version 1.0 (Ecological Software Solutions). The home range (HR) was defined as the area enclosed within the 75% utilization

Study site

30 subjected to a likelihood-ratio test (*G*-test) for independence to test for differences.

were limited by the grid size.

12 as the raster image showing a 10 m x 10 m grid.

3 cat in seven study sites.

3586 Biodiversity in Ecosystems - Linking Structure and Function

x 10 m grid.

Variable

1

Variable

18

*2.3.2. Habitat types in home ranges*

20 Iriomote cat in each study site.

21 **2.3.2. Habitat types in home ranges** 

) accuracies in this study

To determine the most important topographic and vegetative characteristics influencing the animals' habitat use, I measured the above nine variables in areas within a 20 m radius of cat location sites fixed by radio-triangulation. To determine seasonal differences in habitat use, the location sites of six cats that were studied during all seasons (spring: April to June; summer: July to September; autumn: November to December; winter: January to March) were compared among seasons with regard to the above environmental characteristics.

To determine the habitat preference of radio-collared cats at each site, environmental charac‐ teristics in areas within a 20 m radius at cat location sites were compared with those at random locations. As many random locations as cat locations were chosen from HRs in each study site, using IDRISI. Mean values of El and Sl and the proportions of occurrence of other seven categorical variables were compared between areas within a 30 m radius at cat locations and random locations.

As a first step, these statistical differences were tested using a Mann-Whitney *U*-test for El and Sl, and using a *G*-test for others. Variables remaining after univariate testing were entered into a logistic regression function following forward stepwise procedures. In the stepwise regres‐ sion, a forward procedure using the likelihood-ratio statistic was employed, which included a variable in the model at *P*=0.05 level, which was removed if said variable's significance fell below 0.10. The percentage of sites classified correctly (radio tracking location vs. random location) and coefficients of determination (Nagelkerke *R*<sup>2</sup> ) determined by the final logistic models, which were indications of the influence of the logistic regression [31], were calculated in each regression.

**Figure 5.** Movement tracks of the Iriomote cat in five study sites shown in digital elevation models. The movement tracks were based on continuous radio-tracking with locations taken every one-to two-hours.

Ecological Flexibility of the Top Predator in an Island Ecosystem — The Iriomote Cat Changes Feeding Patterns… 9 http://dx.doi.org/ 10.5772/59502 361

a logistic regression function following forward stepwise procedures. In the stepwise regres‐ sion, a forward procedure using the likelihood-ratio statistic was employed, which included a variable in the model at *P*=0.05 level, which was removed if said variable's significance fell below 0.10. The percentage of sites classified correctly (radio tracking location vs. random

models, which were indications of the influence of the logistic regression [31], were calculated

**Figure 5.** Movement tracks of the Iriomote cat in five study sites shown in digital elevation models. The movement

tracks were based on continuous radio-tracking with locations taken every one-to two-hours.

) determined by the final logistic

location) and coefficients of determination (Nagelkerke *R*<sup>2</sup>

3608 Biodiversity in Ecosystems - Linking Structure and Function

in each regression.

**Figure 6.** Seasonal elevation changes (mean+*SD*) of the radio-tracking locations of six Iriomote cats in four study sites (Ot: Otomi; Ko: Komi; Fu: Funaura; Sh: Shirahama).

### *2.3.4. Movement pattern*

The movement tracks of radio-collared cats were derived from fulfilled radio-tracking locations (Figure 5) following the procedure in [32]. Data were collected at a rate of at least one hour intervals for more than 24 hours. However, if cats moved less than 100 m and rested at a fixed location, the data were accepted. The movement of each cat was characterized by calculating the daily movement distance (DMD: the sum of straight line distances between consecutive locations during 24-hour tracking sessions).

To determine the most important environmental characteristics influencing the animals' movement patterns, I measured the most important predictors derived from the above analyses of the movement tracks of radio-collared cats (MT) and compared them to the same variables for random tracks (RT), which were created by a Monte Carlo simulation using a random walk program in Biotas. A random walk is the most basic process for creating a spatially unpredictable data set. The process was operated with a point pattern using the same number of cat locations and straight line distance of MT during a consecutive tracking session without any specific direction. This process was able to "walk" in any direction within the home range. These statistical differences were tested using a Mann-Whitney *U*-test.

All statistical analyses were carried out using SPSS 11.5 for Windows (SPSS Inc., Illinois, USA). Statistical differences were accepted as significant when *P* < 0.05.

## **3. Results**

### **3.1. Environmental characteristics among study sites**

I measured nine environmental variables within the home ranges of the radio-collared cats and compared them among study sites (Figure 3). Continuous variables (El and Sl) were significantly different among study sites (one-way ANOVA: *F*=2389 for El and 3468 for Sl, *d.f.*=6, both *P* < 0.0001). Mean values of El were highest in Shirahama, followed by Urauchi and NCA. Those of Otomi, Maira, Funaura and Komi were relatively low. A similar pattern emerged for the case of slopes (Figure 3).

For categorical variables, percentages of drainages (Dr) and forest edges (FE) were also statistically different among sites (*P* < 0.001). Dr was the highest in Urauchi, followed by NCA, Maira and Komi. However, these values varied slightly, ranging from 4.9 to 7.0%, whereas FE varied largely depending on study sites. FE was particularly abundant in Maira, followed by Otomi. These values were lower in other sites.

Composition of vegetation type in each study site is illustrated in Figure 4 and differed significantly among sites (*G*=66826, *d.f.*=24, *P* < 0.0001). In Otomi, NCA, Funaura and Shiraha‐ ma, vegetative environments were relatively uniform and mostly occupied by one or two vegetation types; NF and CP in Otomi, NF in NCA, NF and CP in Funaura and NF and SW in Shirahama. On the other hand, vegetative environments were more complex in Maira, Komi and Urauchi, as these were occupied by five vegetation types.

Ecological Flexibility of the Top Predator in an Island Ecosystem — The Iriomote Cat Changes Feeding Patterns… 11 http://dx.doi.org/ 10.5772/59502 363

*2.3.4. Movement pattern*

362 10 Biodiversity in Ecosystems - Linking Structure and Function

**3. Results**

consecutive locations during 24-hour tracking sessions).

The movement tracks of radio-collared cats were derived from fulfilled radio-tracking locations (Figure 5) following the procedure in [32]. Data were collected at a rate of at least one hour intervals for more than 24 hours. However, if cats moved less than 100 m and rested at a fixed location, the data were accepted. The movement of each cat was characterized by calculating the daily movement distance (DMD: the sum of straight line distances between

To determine the most important environmental characteristics influencing the animals' movement patterns, I measured the most important predictors derived from the above analyses of the movement tracks of radio-collared cats (MT) and compared them to the same variables for random tracks (RT), which were created by a Monte Carlo simulation using a random walk program in Biotas. A random walk is the most basic process for creating a spatially unpredictable data set. The process was operated with a point pattern using the same number of cat locations and straight line distance of MT during a consecutive tracking session without any specific direction. This process was able to "walk" in any direction within the home

All statistical analyses were carried out using SPSS 11.5 for Windows (SPSS Inc., Illinois, USA).

I measured nine environmental variables within the home ranges of the radio-collared cats and compared them among study sites (Figure 3). Continuous variables (El and Sl) were significantly different among study sites (one-way ANOVA: *F*=2389 for El and 3468 for Sl, *d.f.*=6, both *P* < 0.0001). Mean values of El were highest in Shirahama, followed by Urauchi and NCA. Those of Otomi, Maira, Funaura and Komi were relatively low. A similar pattern

For categorical variables, percentages of drainages (Dr) and forest edges (FE) were also statistically different among sites (*P* < 0.001). Dr was the highest in Urauchi, followed by NCA, Maira and Komi. However, these values varied slightly, ranging from 4.9 to 7.0%, whereas FE varied largely depending on study sites. FE was particularly abundant in Maira, followed by

Composition of vegetation type in each study site is illustrated in Figure 4 and differed significantly among sites (*G*=66826, *d.f.*=24, *P* < 0.0001). In Otomi, NCA, Funaura and Shiraha‐ ma, vegetative environments were relatively uniform and mostly occupied by one or two vegetation types; NF and CP in Otomi, NF in NCA, NF and CP in Funaura and NF and SW in Shirahama. On the other hand, vegetative environments were more complex in Maira, Komi

range. These statistical differences were tested using a Mann-Whitney *U*-test.

Statistical differences were accepted as significant when *P* < 0.05.

**3.1. Environmental characteristics among study sites**

emerged for the case of slopes (Figure 3).

Otomi. These values were lower in other sites.

and Urauchi, as these were occupied by five vegetation types.

**Figure 7.** Seasonal slope change (mean+*SD*) of the radio-tracking locations of six Iriomote cats in four study sites (Ot: Otomi; Ko: Komi; Fu: Funaura; Sh: Shirahama).

### **3.2. Habitat use**

#### *3.2.1. Seasonal differences*

I measured the seasonal differences for the major environmental characteristics of six radiocollared cats and the results are shown in Figures 6 to 8. For each cat, El and Sl at cat location sites significantly differed among seasons (Kruskal-Wallis test, *P* < 0.001: Figures 6 and 7). Vegetation types at cat locations were also significantly different among seasons for each cat (*G*-test, *P* < 0.001: Figure 8). Seasonal variations for both topographic variables in males were relatively low and varied comparatively more among females. In particular, a female cat in Shirahama used a lowland habitat during winter and spring, and used a higher habitat during summer and autumn (Figures 6 and 7). The vegetative compositions of used habitats varied relatively among females, more so than among males. Although the environments of cat location sites varied seasonally, environmental conditions essentially differed depending on study sites (Figure 8).


**Table 3.** Results of final logistic regression models regarding environmental variables (El: elevation; Sl: slope; FE: forest edges; SF: secondary forest; CV: coastal vegetation, rice fields and swamps) predicting radio-tracking locations vs. random locations in each study site.

#### *3.2.2. Regional differences*

I measured habitat variables at radio-tracking locations and random locations in each of the study sites; radio-tracking locations were significantly influenced by one to four environmen‐ tal variables depending on study sites. These environmental variables were employed in forward stepwise procedures. By doing so, I obtained predictive models for cat location sites that were correctly classified at 76.4 to 97.4% (Table 3).

Elevation (El) was the only predictor selected in the models in all study sites, which indicates that the cat preferred lowland and avoided areas at higher altitudes in all study sites. In NCA and Urauchi, El was the only important predictor of cat locations. The cat preferred lowland, regardless of vegetative types. In four of five study sites (other than Funaura), El was the most important predictor of cat locations. Slope (Sl) was only chosen in the model in Shirahama that indicates the cat preferred sloping lands.

12 Book Title 1 **Figure7.** Seasonal slope change (mean+*SD*) of the radio-tracking locations of six Iriomote Ecological Flexibility of the Top Predator in an Island Ecosystem — The Iriomote Cat Changes Feeding Patterns… 13 http://dx.doi.org/ 10.5772/59502 365

2 cats in four study sites (Ot: Otomi; Ko: Komi; Fu: Funaura; Sh: Shirahama).

5 **Figure8.** Seasonal vegetative changes for the radio-tracking locations of six Iriomote cats 6 in four study sites (Ot: Otomi; Ko: Komi; Fu: Funaura; Sh: Shirahama). **Figure 8.** Seasonal vegetative changes for the radio-tracking locations of six Iriomote cats in four study sites (Ot: Oto‐ mi; Ko: Komi; Fu: Funaura; Sh: Shirahama).

Although vegetative variables also employed in the models of the five study sites, the influence varied depending on the sites. According to each predictive model, besides lowland areas, the cat preferred areas near forest edges in Maira and Otomi; preferred swamps in Komi, Funaura, and Shirahama; preferred secondary forests in Komi but it was avoided in Shirahama; the cat avoided coastal vegetation in Otomi and Funaura. 7 **3.2. Habitat use**  8 **3.2.1. Seasonal differences**  9 I measured the seasonal differences for the major environmental characteristics of six radio-10 collared cats and the results are shown in Figures 6 to 8. For each cat, El and Sl at cat 11 location sites significantly differed among seasons (Kruskal-Wallis test, *P* < 0.001: Figures 6 12 and 7). Vegetation types at cat locations were also significantly different among seasons for

#### **3.3. Movement pattern** 13 each cat (*G*-test, *P* < 0.001: Figure 8). Seasonal variations for both topographic variables in 14 males were relatively low and varied comparatively more among females. In particular, a 15 female cat in Shirahama used a lowland habitat during winter and spring, and used a higher

4

**3.2. Habitat use**

*3.2.1. Seasonal differences*

364 12 Biodiversity in Ecosystems - Linking Structure and Function

study sites (Figure 8).

vs. random locations in each study site.

that were correctly classified at 76.4 to 97.4% (Table 3).

indicates the cat preferred sloping lands.

*3.2.2. Regional differences*

I measured the seasonal differences for the major environmental characteristics of six radiocollared cats and the results are shown in Figures 6 to 8. For each cat, El and Sl at cat location sites significantly differed among seasons (Kruskal-Wallis test, *P* < 0.001: Figures 6 and 7). Vegetation types at cat locations were also significantly different among seasons for each cat (*G*-test, *P* < 0.001: Figure 8). Seasonal variations for both topographic variables in males were relatively low and varied comparatively more among females. In particular, a female cat in Shirahama used a lowland habitat during winter and spring, and used a higher habitat during summer and autumn (Figures 6 and 7). The vegetative compositions of used habitats varied relatively among females, more so than among males. Although the environments of cat location sites varied seasonally, environmental conditions essentially differed depending on

Otomi -0.030 0.463 -2.073 1.13 83.3 0.366 21.9 0.0051 Maira -0.035 0.821 0.65 85.0 0.339 19.2 0.0138 Komi -0.040 0.745 1.488 0.50 78.9 0.405 42.7 <0.0001 NCA -0.037 2.25 97.4 0.688 16.1 0.0414 Funaura -0.023 -2.385 0.932 1.00 76.4 0.220 23.0 0.0033 Urauchi -0.015 0.71 81.8 0.202 24.7 0.0017 Shirahama -0.015 0.036 -1.483 1.041 0.75 83.0 0.502 18.1 0.0208

**Table 3.** Results of final logistic regression models regarding environmental variables (El: elevation; Sl: slope; FE: forest edges; SF: secondary forest; CV: coastal vegetation, rice fields and swamps) predicting radio-tracking locations

I measured habitat variables at radio-tracking locations and random locations in each of the study sites; radio-tracking locations were significantly influenced by one to four environmen‐ tal variables depending on study sites. These environmental variables were employed in forward stepwise procedures. By doing so, I obtained predictive models for cat location sites

Elevation (El) was the only predictor selected in the models in all study sites, which indicates that the cat preferred lowland and avoided areas at higher altitudes in all study sites. In NCA and Urauchi, El was the only important predictor of cat locations. The cat preferred lowland, regardless of vegetative types. In four of five study sites (other than Funaura), El was the most important predictor of cat locations. Slope (Sl) was only chosen in the model in Shirahama that

<sup>2</sup> *<sup>P</sup>* Logistic coefficient of covariate Correct

ratio (%)

(*R*<sup>2</sup>

) <sup>χ</sup>

El Sl FE SF CV RS Intercept

Study site Nagelkerke

I analysed the movement patterns of 11 cats (five males and six females, see Table 5). The total tracked time and distance were 3012 h and 359.6 km, respectively. DMD of each individual was calculated and is shown in Table 4. The DMD was slightly longer for males (3.36±1.04 km: x ±*SD*, *N*=5) than females (3.02±0.80 km, *N*=6), but lacked the same statistical support (Mann-Whitney U-test, *U*=14, *P*=0.93). Despite slight differences between the sexes, the DMD varied largely among study sites and was the longest in Funaura (4.61 km, *N*=2), followed by Otomi (3.06 km, *N*=1), Komi (3.04 km, N=2), Maira (3.03 km, *N*=2), NCA (2.80 km, *N*=2) and Shirahama (2.26 km, *N*=2), in this order. The DMD was positively related with home range size but lacked statistical supports (*r*=0.522, *N*=5, *P=*0.182, for males; *r*=0.575, *N*=6, *P*=0.116, for females). 16 habitat during summer and autumn (Figures 6 and 7). The vegetative compositions of used 17 habitats varied relatively among females, more so than among males. Although the 18 environments of cat location sites varied seasonally, environmental conditions essentially 19 differed depending on study sites (Figure 8). El Sl FE SF CV RS Intercept Otomi -0.030 0.463 -2.073 1.13 83.3 0.366 21.9 0.0051 Maira -0.035 0.821 0.65 85.0 0.339 19.2 0.0138 Komi -0.040 0.745 1.488 0.50 78.9 0.405 42.7 <0.0001 NCA -0.037 2.25 97.4 0.688 16.1 0.0414 Funaura -0.023 -2.385 0.932 1.00 76.4 0.220 23.0 0.0033 Study site Nagelkerke (*R*<sup>2</sup> ) <sup>χ</sup> <sup>2</sup> *<sup>P</sup>* Logistic coefficient of covariate Correct ratio (%)

Correlations of HR sizes and DMD against mean values of elevation and slopes in HR are shown in Figure 9. For male cats, DMD and HR were negatively closely related with mean values of slope, though not related with mean values of elevation. Meanwhile, there was not significant correlation between elevation and slope (*P* > 0.05). 20 21 **Table 3.** Results of final logistic regression models regarding environmental variables (El: Shirahama -0.015 0.036 -1.483 1.041 0.75 83.0 0.502 18.1 0.0208

Urauchi -0.015 0.71 81.8 0.202 24.7 0.0017

The values of elevation and slope on movement tracks of the cats were compared with random tracks created by the random walk simulation (Table 5). Both variables were significantly lower on movement tracks than those on random tracks in all individuals (Mann-Whitney U-test, *P* < 0.001).


**Table 4.** Movement characteristics of each individual Iriomote cat. DMD (daily movement distance), HR (home range size, estimated by 75% harmonic mean method), mean values of elevation (El) and slope (Sl) in HR.


**Table 5.** Elevation and slope ranges for the movement tracks of the Iriomote cat and for random tracks created by random walk simulations.

The movement tracks that were analysed are shown on the digital elevation model in Figure 5. When the cats went on long-distance walks, they avoided higher lands and selected flat routes to another area. In Otomi, Komi and Funaura, where flat lands largely occur, the movement tracks were distributed relatively uniform, whereas they were concentrated in flat lands in NCA and Shirahama, where these types of area are extremely limited.

#### **3.4. Regional differences of the diet compositions**

I analysed the contents of 805 scats collected within HRs of radio-collared cats: 70 scats in Otomi, 182 scats in Maira, 166 scats in Komi, 169 scats in NCA, 81 scats in Funaura, 45 scats in Urauchi and 92 scats in Shirahama. The result of the scat analysis is summarized in Figure 10. Principal prey groups were different among sites; reptiles and birds in Otomi, reptiles and amphibians in Maira, birds and amphibians in Komi, birds and reptiles in NCA, birds, reptiles and amphibians in Funaura, mammals and birds in Urauchi, and birds in Shirahama, were most frequently preyed upon, respectively.

Study site Cat name Sex Distance (m) Track hour (h) DMD (km) HR (km2

366 14 Biodiversity in Ecosystems - Linking Structure and Function

Otomi E30 M 32880 229 3.45 3.35 47.5 9.60 Maira E36 F 9674 90 2.58 0.70 32.4 8.51

Komi E18 F 52196 458 2.73 0.66 28.4 8.07

NCA W86 M 2898 28 2.46 2.79 67.3 12.2

Funaura W61 M 10536 50 5.09 2.65 47.7 10.4

Shirahama W49 M 140572 1257 2.68 0.55 93.3 16.2

**Table 4.** Movement characteristics of each individual Iriomote cat. DMD (daily movement distance), HR (home range

Random Movement Random Movement Otomi E30 3036 67.9±49.0 25.5±21.8 2004615 <0.00001 12.6±8.72 6.53±5.17 2660791 <0.00001 Maira E36 882 56.9±51.1 22.1±15.9 229749 <0.00001 12.0±8.50 6.44±4.94 209086 <0.00001 E39 694 26.9±15.0 10.8±7.08 67732 <0.00001 7.44±6.04 4.82±3.13 166544 <0.00001

*<sup>U</sup> <sup>P</sup>* Elevation (m: mean<sup>±</sup> *SD* ) Slope (°: mean<sup>±</sup> *SD* ) Study site *<sup>N</sup> <sup>U</sup> <sup>P</sup>*

Komi E18 4669 24.8±29.9 10.8±12.8 7670419 <0.00001 7.39±7.39 4.36±4.86 7626407 <0.00001 E32 1788 37.1±37.4 9.41±13.9 553259 <0.00001 9.17±8.26 3.58±4.51 725216 <0.00001

NCA W86 268 48.2±37.4 16.0±12.8 15260 <0.00001 10.2±6.17 5.08±3.65 18011 <0.00001 W89 719 49.3±38.7 21.6±15.8 145632 <0.00001 11.2±6.92 7.80±5.28 183296 <0.00001

Funaura W61 966 38.4±30.2 28.4±15.6 399199 <0.00001 10.1±7.72 6.54±4.52 311399 <0.00001 W68 4191 44.2±46.1 28.7±22.1 6874122 <0.00001 9.33±7.11 8.68±6.55 8301671 0.00047

Shirahama W49 12720 114 ±80.4 38.8±39.0 33984231 <0.00001 17.6±10.2 15.3±11.1 69846145 <0.00001 W60 2503 107 ±62.1 43.2±42.9 1248043 <0.00001 19.5±10.7 16.4±12.4 2583308 <0.00001

**Table 5.** Elevation and slope ranges for the movement tracks of the Iriomote cat and for random tracks created by

lands in NCA and Shirahama, where these types of area are extremely limited.

**3.4. Regional differences of the diet compositions**

The movement tracks that were analysed are shown on the digital elevation model in Figure 5. When the cats went on long-distance walks, they avoided higher lands and selected flat routes to another area. In Otomi, Komi and Funaura, where flat lands largely occur, the movement tracks were distributed relatively uniform, whereas they were concentrated in flat

I analysed the contents of 805 scats collected within HRs of radio-collared cats: 70 scats in Otomi, 182 scats in Maira, 166 scats in Komi, 169 scats in NCA, 81 scats in Funaura, 45 scats in Urauchi and 92 scats in Shirahama. The result of the scat analysis is summarized in Figure 10.

random walk simulations.

size, estimated by 75% harmonic mean method), mean values of elevation (El) and slope (Sl) in HR.

E39 F 7750 53 3.48 0.49 15.6 5.66

E32 F 20419 146 3.36 1.55 37.6 9.79

W89 M 7936 61 3.14 2.63 66.3 12.3

W68 F 46518 270 4.13 1.75 24.9 6.92

W60 F 28253 369 1.84 0.76 75.9 16.0

) El (m) Sl (°)

The cats' diets were relatively diversified with high frequencies of several prey groups in Otomi, Maira, Komi, NCA and Funaura; however, their diets were narrowed to mainly birds in Urauchi and Shirahama (Figure10).

**Figure 9.** Correlations for daily movement distance (DMD) and home range size (HR) against mean values of elevation and slope in HRs.

**Figure 10.** Seasonal and regional patterns of frequency occurrences (%) of prey groups found in 805 scats of the Irio‐ mote cat.

### **4. Discussion**

#### **4.1. Feeding strategy of the Iriomote cat**

The results of the present study showed seasonal variance in the habitat use of the Iriomote cat. Several studies have shown seasonal effects on the movements and habitat use of felids at various scales [33-39]. Deep snow and severe winter weather were shown to restrict home range size and habitat use [33, 36], as well as the movement patterns [37] of felids. Severe drought during the dry season was similarly shown to restrict movement patterns and the habitat use of some felids [38, 39]. In contrast with the study areas noted above, the climate of the Iriomote is extremely warm and humid throughout the year [40]. Thus, I believe that the seasonal variations in the habitat use of the Iriomote cat in the present study must be related to other factors.

Frequency (%) Frequency (%)

368 16 Biodiversity in Ecosystems - Linking Structure and Function

Mammal Bird Reptile Amphibian Insect Others Spring (n=62) Summer (n=35) Autumn (n=21) Winter (n=48)

Mammal Bird Reptile Amphibian Insect Others Spring (n=56) Summer (n=48) Autumn (n=26) Winter (n=52)

Mammal Bird Reptile Amphibian Insect Others Spring (n=15) Summer (n=12) Autumn (n=12) Winter (n=31)

mote cat.

**4. Discussion**

**4.1. Feeding strategy of the Iriomote cat**

**Figure 10.** Seasonal and regional patterns of frequency occurrences (%) of prey groups found in 805 scats of the Irio‐

The results of the present study showed seasonal variance in the habitat use of the Iriomote cat. Several studies have shown seasonal effects on the movements and habitat use of felids at various scales [33-39]. Deep snow and severe winter weather were shown to restrict home

Otomi

Komi

Maira

Mammal Bird Reptile Amphibian Insect Others Spring (n=13) Summer (n=13) Autumn (n=13) Winter (n=42)

Mammal Bird Reptile Amphibian Insect Others Spring (n=15) Summer (n=15) Autumn (n=20) Winter (n=42)

Mammal Bird Reptile Amphibian Insect Others Spring (n=2) Summer (n=7) Autumn (n=18) Winter (n=18)

Mammal Bird Reptile Amphibian Insect Others Spring (n=46) Summer (n=47) Autumn (n=12) Winter (n=64)

NCA

Funaura

Urauchi

Shirahama

In the present study, there were different levels of seasonal variations between sexes. Male cats had small seasonal variations; meanwhile, female cats used lowland habitats during winter and spring. The different seasonal patterns of habitat use between sexes may be connected to the gender differences in breeding cost. Female Iriomote cats breed and raise their young, while males are not involved in the raising of offspring [25, 41]. The breeding cycle of the cat is not seasonally restricted but a mating peak is recognized between February and April, and females deliver litters between April and June [41]. Accordingly, females need suitable habitats for breeding dens and for nursing their young [25, 41]. Three females were parous when they were captured. Thus, the females preferred and used lowland habitats during breeding; meanwhile, the habitat use of males were not as related to the breeding cycle.

Some studies of carnivores have suggested that suitable structures and sites for breeding dens are essential and limited within the animals' habitats. The distribution of breeding sites affects the habitat use of breeding females [42-45]. The breeding habitat use of Iberian lynxes *Lynx pardinus* is more strongly influenced by distribution of natal hollow trees than by prey availability and breeding females use old growth forests during breeding season [45]. It has also been reported that a female Iriomote cat used a hollow tree for breeding [46]. On Iriomote Island, hollow trees that are large enough in size for the breeding purposes of Iriomote cats were identified among several tree species, mostly *Quercus miyagii*, *Castanopsis sieboldii* and *Machilus thunbergii* (Watanabe, unpub. data); these only occurred in the NF vegetative category in the present study. Contrarily, females used lowland habitats with a low proportion of NF during the breeding season, suggesting that the availability of den sites was not the only important factor for the habitat use of breeding Iriomote cats. They may also use other structures or sites for breeding and as such, it is likely that an increase in food requirements for nursing influences the habitat use of female cats during breeding.

During nursing periods, females with young concentrated their movements near the den [47]. In the present study, the proportions of rice fields and swamps in home ranges of three females were higher than those of other vegetation types during the period. There were an abundance of birds and frogs in the habitat type during this period [7, 12, 40, 48]. Thus, the females intensively used the habitat to prey on abundant food sources for nursing their young.

In addition to seasonal differences, I observed significant alterations of habitat use among the Iriomote cats in different study sites. The habitat use of several widespread felids such as bobcats, lynxes, leopards and tigers have been studied in broad geographic ranges across several climatic zones [39]; the habitat use of each species varies somewhat according to region. This is likely the result of different climates, vegetation structures, or the principal prey species present in completely different environments. For leopard cats *Prionailurus bengalensis*, home range sizes differ among broad regions in Thailand [49-51], in Borneo [52], on Tsushima Island [53] and on Iriomote [5, 47, 54]. On Iriomote, the vegetative and topographic conditions significantly differed among the study sites, which were only several kilometres away from one another. The narrow-regional differences among environments strongly affected the habitat use, movement pattern and diet of the Iriomote cats.

Bekoff et al. [19] assumed that prey distribution strongly affects the habitat use of predators. Generally, vegetation types have a larger effect on the prey distribution of carnivores [e.g., 55-60]. The distribution of principal prey items of the Iriomote cat is also chiefly determined by vegetative environment [7]. The habitat use of the Iriomote cat varied in relation to the regional differences of vegetative environments. Preferred vegetation types differed among regions. In addition, diet composition of the Iriomote cat differed between regions. Therefore, it is my conclusion that the cats changed their use of habitat in order to adapt to differences in prey distribution.

Although most environmental variables affected the habitat use of the Iriomote cat, only elevation showed strong and similar effects within all study sites. All radio-collared cats preferred using lowland habitats, mainly with elevation of less than 50 m, while they hardly used highlands with elevation more than 200 m. In particular, the effect of elevation was more highly correlated with the habitat use of the cats in rough terrains (NCA, Urauchi and Shirahama). Sometimes, elevation contributed as a factor for determining vegetation type and affected the mammalian fauna [e.g., 61-63]. However, this effect was the result of climatic changes that required a vertical interval of several thousand metres. In this study, a vertical interval of only 50 m limited the habitat use and movement of the Iriomote cat. Thus, the small difference of elevation did not cause climatic changes.

Sakaguchi [5] also reported that the Iriomote cat avoided highlands and suggested this to be due to scarce prey resources in the highlands. However, some principal prey items of the Iriomote cat such as reptiles and insects are more abundant in montane forests than in lowland habitats [7]. Thus, I believe that highlands encompass abundant prey items at a similar level of that found in lowland habitats and that prey availability is not a principal factor affecting the avoidance of highlands.

The habitat uses of predators are likely determined by how efficiently they seek and acquire food. This is because predators perform optimum feeding to maximize the efficiency of their energy acquirements [13]. In this regard, prey availability will be an important factor for habitat use. However, at the same time, if there is a high cost for acquiring food, the results will be inefficient. Schoener [64] assumed that energy acquirement efficiency fluctuated according to the relationship between food availability and the cost demanded for acquiring the food.

According to the feeding patterns of the Iriomote cat, the animal is considered to be an opportunistic mobile predator [5]; as such, the feeding cost can be represented as the movement cost expended when seeking prey. Several studies have suggested that movement cost is highly correlated with topographic condition, particularly slope [e.g. 65-67]. Walking speed decreases as the slope on walking routes increase [65] and the energy requirements of humans [66] and goats [67] during walking are much higher on a slope than on a flat surface. In the analysis results of movement tracks of the Iriomote cat, it was shown in all study sites that the animal preferred to move on areas with a lower slope and lower elevation. Thus, I hypothesize that the avoidance of highland areas by the Iriomote cat is a consequence of increasing movement cost based on the optimal feeding strategy: the cat performs habitat use to maximize the energy acquirement efficiency, depending on the cost and benefit of feeding.

Several studies of felids have suggested that the availability of suitable foraging spots in an area is limited [9, 68] and that felids flexibly shift their home range uses in response to prey availability. In studies of bobcats *Lynx rufus*, it has been suggested that prey availability affects home range sizes and large home ranges were reported in habitats with limited prey resources [33]. A cat in an area with scarce prey resources needs to expand its home range to acquire essential hunting spots and prey. However, in the present study, home range sizes tended to contract as the slope in home range increased. If a cat enlarged the home range in hilly habitats where the movement cost was particularly high, the cat acquired more food, but spent much more energy seeking out said prey than it acquired energy.

Corbett [69] reported that feral cats with larger ranges were more likely to use mobile than stationary or ambush hunting strategies, while cats with smaller ranges used stationary or ambush strategies more often. In this study, the movements of cats in hilly areas (NCA and Shirahama) were concentrated in limited lowlands, whereas cats with wide lowland habitats (Otomi, Komi and Funaura) utilized their home ranges uniformly. Thus, it is likely that cats in areas with wide lowland habitats used mobile opportunistic hunting strategies, whereas cats in areas with hilly lands were more inclined to using stationary or ambush hunting strategies in order to raise their feeding efficiency. Consequently, the cats kept small home ranges in hilly areas with high movement cost.

### **4.2. Evolution of flexible habits of the Iriomote cat**

[53] and on Iriomote [5, 47, 54]. On Iriomote, the vegetative and topographic conditions significantly differed among the study sites, which were only several kilometres away from one another. The narrow-regional differences among environments strongly affected the

Bekoff et al. [19] assumed that prey distribution strongly affects the habitat use of predators. Generally, vegetation types have a larger effect on the prey distribution of carnivores [e.g., 55-60]. The distribution of principal prey items of the Iriomote cat is also chiefly determined by vegetative environment [7]. The habitat use of the Iriomote cat varied in relation to the regional differences of vegetative environments. Preferred vegetation types differed among regions. In addition, diet composition of the Iriomote cat differed between regions. Therefore, it is my conclusion that the cats changed their use of habitat in order to adapt to differences in

Although most environmental variables affected the habitat use of the Iriomote cat, only elevation showed strong and similar effects within all study sites. All radio-collared cats preferred using lowland habitats, mainly with elevation of less than 50 m, while they hardly used highlands with elevation more than 200 m. In particular, the effect of elevation was more highly correlated with the habitat use of the cats in rough terrains (NCA, Urauchi and Shirahama). Sometimes, elevation contributed as a factor for determining vegetation type and affected the mammalian fauna [e.g., 61-63]. However, this effect was the result of climatic changes that required a vertical interval of several thousand metres. In this study, a vertical interval of only 50 m limited the habitat use and movement of the Iriomote cat. Thus, the small

Sakaguchi [5] also reported that the Iriomote cat avoided highlands and suggested this to be due to scarce prey resources in the highlands. However, some principal prey items of the Iriomote cat such as reptiles and insects are more abundant in montane forests than in lowland habitats [7]. Thus, I believe that highlands encompass abundant prey items at a similar level of that found in lowland habitats and that prey availability is not a principal factor affecting

The habitat uses of predators are likely determined by how efficiently they seek and acquire food. This is because predators perform optimum feeding to maximize the efficiency of their energy acquirements [13]. In this regard, prey availability will be an important factor for habitat use. However, at the same time, if there is a high cost for acquiring food, the results will be inefficient. Schoener [64] assumed that energy acquirement efficiency fluctuated according to the relationship between food availability and the cost demanded for acquiring the food.

According to the feeding patterns of the Iriomote cat, the animal is considered to be an opportunistic mobile predator [5]; as such, the feeding cost can be represented as the movement cost expended when seeking prey. Several studies have suggested that movement cost is highly correlated with topographic condition, particularly slope [e.g. 65-67]. Walking speed decreases as the slope on walking routes increase [65] and the energy requirements of humans [66] and goats [67] during walking are much higher on a slope than on a flat surface. In the analysis results of movement tracks of the Iriomote cat, it was shown in all study sites that the animal

habitat use, movement pattern and diet of the Iriomote cats.

370 18 Biodiversity in Ecosystems - Linking Structure and Function

difference of elevation did not cause climatic changes.

prey distribution.

the avoidance of highlands.

Consumers can be roughly classified as either specialists with a narrow diet range and generalists with a broad diet range. Discussions on the general or specialist characteristics of predators are common in ecological literature [70]. The distribution of diet widths, i.e., the range of food types eaten by an animal, differs among the various types of consumers [71]. In the case of carnivores, the topic is well-documented at interspecific levels [e.g., 19, 20]. Each felid species takes only a few different prey items of mammals, while other carnivores eat various food types. The family Felidae is highly specialized for preying on mammals in terms of developing their morphological and behavioural traits [21, 22]. Thus, Felidae is considered a typical food specialist. These patterns appear to be in diets of *P*. *bengalensis* in that they feed mostly on mice and rats [39, 51, 72]. However, the Iriomote cat is also considered as being a generalist, because they prey on various types of animals besides mammals [6-8]. What then generalizes their diet?

From an ecological perspective, the diet width of an animal is chiefly determined by the functional limitations of their feeding ability, that is, how many food types in its habitat the animal can consume [71]. For instance, all felids cannot digest vegetable matter due to physiological limitations, though other carnivorous families such as some mustelids and all ursids can. In addition, solitary felids generally do not hunt animals bigger than themselves, due to their morphological and behavioural limitations; however, felid species do hunt in groups, as lions and canids often do [22, 73]. In the diet of the Iriomote cat, *Sus scorfa* (wild pig), the largest animals on Iriomote Island, are hardly eaten. In addition, the Iriomote cat mostly preys on ground-living animals, while arboreal species are infrequently preyed upon [7]. This is likely due to limitations of their feeding ability. However, the Iriomote cat preys on nearly a hundred prey items belonging to wide range of taxonomical groups [7]. Thus, it is possible that they have developed a high feeding technique ability to prey on most types of ground-living animals.

The ancestral species of the Iriomote cat is common to other species of the genus *Prionailurus* [74], which presumably fed on small mammals living in continental environments, in which small mammals coexisted. As such, it is assumed that the Iriomote cat acquired a more diverse diet through further development of feeding functions to include a larger variety of animals.

To improve feeding ability, species are likely to develop morphological or behavioural functions for hunting [22, 73]. However, there is no notable morphological distinction between the Iriomote cat and other closely related species [74]. In addition, it has been reported that the hunting methods of the Iriomote cat have not been well-developed in relation to each of its prey types and is much more primitive than those of other small felids [75]. Furthermore, if a species develop its feeding patterns in relation to feeding on particular food types, they are likely to specialize in a narrow range of food types [76]. According to the dietary studies of *P*. *bengalensis* in other regions, in addition to mammals, they also eat birds, reptiles, amphibians and insects, though at low frequencies [2, 39, 51]. This suggests that the cats are also capable of feeding on these types of prey but that these prey types may be in the minority in environ‐ ments, or are avoided by the cats. Therefore, it is likely that the Iriomote cat's well-developed hunting techniques are related to each of its various prey items.

It is more likely that regional differences of potential food resources influence diet widths of *P*. *bengalensis*. The insular fauna on Iriomote Island is characterized by a geological history that caused the absence of native non-volant small mammals [2], by the humid-subtropical climate that leads to the high abundance of floor-dwelling amphibians [40] and by the island's geographically suitable location for migrant birds that has led to the drastic seasonal changes in the abundance of and species composition of the avifauna [7]. Thus, small vertebrates are remarkably abundant on the island in spite of the scarcity of small mammalian fauna, which may be responsible for large differences in terms of the potential food resources of cats. However, these small vertebrates eaten by the Iriomote cat are commonly also eaten in other regions by other carnivores such as mustelids, viverrids and herpestids [21].

Absolute limits of diet widths are primarily defined by the cats' feeding abilities, but very few animals actually eat all of the different food types they are capable of consuming, thereby exhibiting their fundamental niche. This fundamental niche of a species in the absence of competitors from other species may be restricted to a realized niche in the presence of competitors [71]. In other regions where wild felid populations are present, several species of other carnivores coexist. Interspecific differences of morphological traits and diets among sympatric carnivore species have been reported as evidence for interspecific competition [e.g., 77-79]. Thus, it is likely that sympatric carnivore species compete with felids in the habitats, causing the diet widths of cats to be narrowed. There is no strong competitor for the cat on Iriomote. Thus, its broad diet width range is possibly as evolutionary consequences of ecological release [e.g.70], due to the absence of competitors.

groups, as lions and canids often do [22, 73]. In the diet of the Iriomote cat, *Sus scorfa* (wild pig), the largest animals on Iriomote Island, are hardly eaten. In addition, the Iriomote cat mostly preys on ground-living animals, while arboreal species are infrequently preyed upon [7]. This is likely due to limitations of their feeding ability. However, the Iriomote cat preys on nearly a hundred prey items belonging to wide range of taxonomical groups [7]. Thus, it is possible that they have developed a high feeding technique ability to prey on most types of

The ancestral species of the Iriomote cat is common to other species of the genus *Prionailurus* [74], which presumably fed on small mammals living in continental environments, in which small mammals coexisted. As such, it is assumed that the Iriomote cat acquired a more diverse diet through further development of feeding functions to include a larger variety of animals. To improve feeding ability, species are likely to develop morphological or behavioural functions for hunting [22, 73]. However, there is no notable morphological distinction between the Iriomote cat and other closely related species [74]. In addition, it has been reported that the hunting methods of the Iriomote cat have not been well-developed in relation to each of its prey types and is much more primitive than those of other small felids [75]. Furthermore, if a species develop its feeding patterns in relation to feeding on particular food types, they are likely to specialize in a narrow range of food types [76]. According to the dietary studies of *P*. *bengalensis* in other regions, in addition to mammals, they also eat birds, reptiles, amphibians and insects, though at low frequencies [2, 39, 51]. This suggests that the cats are also capable of feeding on these types of prey but that these prey types may be in the minority in environ‐ ments, or are avoided by the cats. Therefore, it is likely that the Iriomote cat's well-developed

It is more likely that regional differences of potential food resources influence diet widths of *P*. *bengalensis*. The insular fauna on Iriomote Island is characterized by a geological history that caused the absence of native non-volant small mammals [2], by the humid-subtropical climate that leads to the high abundance of floor-dwelling amphibians [40] and by the island's geographically suitable location for migrant birds that has led to the drastic seasonal changes in the abundance of and species composition of the avifauna [7]. Thus, small vertebrates are remarkably abundant on the island in spite of the scarcity of small mammalian fauna, which may be responsible for large differences in terms of the potential food resources of cats. However, these small vertebrates eaten by the Iriomote cat are commonly also eaten in other

Absolute limits of diet widths are primarily defined by the cats' feeding abilities, but very few animals actually eat all of the different food types they are capable of consuming, thereby exhibiting their fundamental niche. This fundamental niche of a species in the absence of competitors from other species may be restricted to a realized niche in the presence of competitors [71]. In other regions where wild felid populations are present, several species of other carnivores coexist. Interspecific differences of morphological traits and diets among sympatric carnivore species have been reported as evidence for interspecific competition [e.g., 77-79]. Thus, it is likely that sympatric carnivore species compete with felids in the habitats, causing the diet widths of cats to be narrowed. There is no strong competitor for the cat on

hunting techniques are related to each of its various prey items.

regions by other carnivores such as mustelids, viverrids and herpestids [21].

ground-living animals.

372 20 Biodiversity in Ecosystems - Linking Structure and Function

However, even when a competitor species is absent in a habitat, the species present will select food types with good quality in order to maximize reward intake [13, 80]. As such, its diet width will be narrower than its fundamental niche. At the one extreme, if the qualities of all food types are uniform and scarce, the predator may employ a generalist strategy that will tend to exhibit a broad diet, i.e., it will hunt and eat many of the food items that it comes into contact with. At the other extreme, if a food type with remarkably high quality is abundant in a habitat, the predator may employ a specialist strategy, have a narrow diet and ignore many of the prey items it comes across, preferring to search for a few specific types of food. In general, animals exhibit strategies ranging across a continuum between these two extremes in relation to food condition in their habitats [13, 80]. In addition, strategies will be more generalized when the food condition in a habitat is scarcer [14].

Food quality is generally determined by its energy content and its feeding efficiency, i.e., the ease of predation [13]. For small felids, food types with good quality are the most common prey item, for example, small terrestrial mammals such as rodents. However, these food types are scarce on Iriomote Island [2, 7]. If preferred food types with good qualities decreased in a habitat, the predator has two choices. First, it might maintain the selectivity of its diet and migrate to another suitable habitat; alternatively, it risks starving by staying in the same habitat. Second, the predator changes the selectivity of its diet and adapts to environmental changes by preying on other food types in the same habitat. In general, such flexible adapta‐ tions to environmental changes in the second choice are more difficult for specialized species [14]. Thus, it is likely that most felid species will opt for the first choice during food scarcity.

In general, island habitats are restricted in terms of food resources compared to those on continents. For animals living in continental habitats, if food conditions worsen, they may escape from starvation by migrating to other habitats with more resources. Indeed, it has been reported that the home ranges of *P*. *bengalensis* on the continent shifts seasonally, seeing them move to other habitats or enlarging their habitat in relation to prey distribution [51]. However, where animals in insular habitats are confined to the same habitats all the time, food conditions can vary. Thus, animals in insular habitats likely need some ecological flexibility in order to adapt to environmental variations. Consequently, it is likely that animals that have adapted to island habitats often have peculiar habits when compared to those found in continental sites [81]. For example, some insectivorous lizards adapted to insular environments have expanded their diets to include nectar, pollen and fruit [82]. To respond to flexibly as it concerns different food types, it may be better for feeding patterns to be unspecialized when it comes to particular food types. This is why the feeding behaviour of the Iriomote cat is more primitive and undeveloped when it comes to particular prey. It is also likely that the opportunistic feeding pattern of the Iriomote cat is suited for flexibly responding to variations in food availability.

*Prionailurus bengalensis* is considered a habitat generalist when compared to other small felids. While other species in the genus inhabit narrow habitat types [39], the habitat of *P*. *bengalen‐ sis* varies [2]. Such flexible habitat use may also play a role allowing the felid population to be present in such a small island. However, the results of the present study showed that the Iriomote cat does not randomly forage for food in its habitat. They might instead have learned about food availability in relation to density and the distribution of prey from short-term experience, and as a result, adopt the most efficient feeding tactics. These flexible feeding patterns, as well as their diversified diets, are uncommon among Felidae. It is likely that the Iriomote cat optimizes most of habitat types on the island.

Therefore, the wide range of food habits of the Iriomote cat results significantly from the peculiar prey fauna of Iriomote Island [7, 40], the lack of competitors on the island [2] and the limited environment due to small island effects [7]. Moreover, I believe that the potential environmental adaptability, i.e., the fundamental niche of *P*. *bengalensis* appears only on Iriomote Island, which is therefore an essential area of study for the behavioural evolution of Felidae.

## **5. Conclusion**

The leopard cat, *Prionailurus bengalensis*, is one of most widespread felids distributed through‐ out Asia. Although there are thousands of islands of various sizes within the range of distri‐ bution of the species, the species lives on several small islands as well as larger islands and the Asian continent. Iriomote Island (284 km2 ) of the Ryukyu Archipelago in southern Japan, is the smallest habitat of this species, on which the Iriomote cat *Prionailurus bengalensis iriomo‐ tensis*, a subspecies of leopard cats, lives.

On Iriomote Island, there are no autochthonous terrestrial small mammals such as rodents, which are generally principal prey of wild felids. Thus, it is likely that there are unique characteristics in the biodiversity of the island and in the ecology of this particular cat as the top predator in the ecosystem. In the present study, I investigated the characteristics of the ecology of the Iriomote cat concerning food habits, habitat use and movement patterns.

I conducted radio-tracking surveys in seven study sites. I examined a location fixed by the radio-tracking in each study site in terms of the cats' habitat preferences related to nine topographic and vegetative variables by using a geographic information system (GIS). Then, the seasonal and regional patterns of the cats' habitat use were examined in terms of feeding patterns.

The results showed that all studied cats selectively used their habitats. Cat locations were significantly influenced by six to eight environmental variables, depending on the study sites. To determine the most important topographic and vegetative factors influencing their habitat use, I attempted a logistic regression function following a forward stepwise approach and with environmental determinants in each study site. Suitable habitats evaluated from logistic regression models more or less differed among study sites. For the comparison of habitat use among study sites, elevation was the only variable to significantly relate to the cats' habitat use in all study sites, while the effects of other variables varied depending on the particular study site. In the results of assessing the prey availability of the cat, distribution and the abundance of their principal prey species were chiefly influenced by vegetative environments. The compositions of vegetative types differed among study sites. Thus, prey distribution and abundance also varied according to site, which potentially influenced the regional differences of suitable habitats.

The diet of the Iriomote cat was examined in terms of the seasonal and regional differences of each prey type by analysing 805 Iriomote cat scat contents collected from various environments in the seven study sites. The results showed that the cat seasonally shifted principal prey items as it concerned food availability. They preyed on items that were abundant in environments. In addition to seasonal differences, the diet compositions also differed among study sites. Thus, it is likely that the cat feeds on abundant prey types depending on the regional differences of environments, as well as seasonal differences.

To determine the most important topographic characteristics influencing Iriomote cats' movement patterns, I measured the elevation and slope of the movement tracks of radiocollared cats and compared them to the same variables on random tracks created by Monte Carlo simulations. The results showed that values of elevation and slope were significantly lower in all individuals on movement tracks than those on random tracks. This suggests that the cat moves from one area to another to avoiding steep paths.

Predators maximize the energy acquirement efficiencies that fluctuate within the relationship between prey abundance and the demanded cost for acquiring prey. For mobile predators such as the Iriomote cat, demanded costs for feeding are significantly determined by costs required for foraging. Thus, highly folded habitats will increase feeding costs. In addition, the cat may avoid areas at high elevation, irrespective of prey abundance.

From the above results, I have concluded that the broad range of food niches of the Iriomote cat likely resulted from making the best possible use of fauna on the small subtropical island. Furthermore, the cat has adapted to the island-wide environment in order to change its principal prey items and feeding patterns in relation to the spatial and temporal variations of food availability. Most small felids may potentially have such flexibility in their ecology. However, this might only be the case in the uniquely biodiverse environment of Iriomote Island.

## **Acknowledgements**

Iriomote cat does not randomly forage for food in its habitat. They might instead have learned about food availability in relation to density and the distribution of prey from short-term experience, and as a result, adopt the most efficient feeding tactics. These flexible feeding patterns, as well as their diversified diets, are uncommon among Felidae. It is likely that the

Therefore, the wide range of food habits of the Iriomote cat results significantly from the peculiar prey fauna of Iriomote Island [7, 40], the lack of competitors on the island [2] and the limited environment due to small island effects [7]. Moreover, I believe that the potential environmental adaptability, i.e., the fundamental niche of *P*. *bengalensis* appears only on Iriomote Island, which is therefore an essential area of study for the behavioural evolution of

The leopard cat, *Prionailurus bengalensis*, is one of most widespread felids distributed through‐ out Asia. Although there are thousands of islands of various sizes within the range of distri‐ bution of the species, the species lives on several small islands as well as larger islands and the

the smallest habitat of this species, on which the Iriomote cat *Prionailurus bengalensis iriomo‐*

On Iriomote Island, there are no autochthonous terrestrial small mammals such as rodents, which are generally principal prey of wild felids. Thus, it is likely that there are unique characteristics in the biodiversity of the island and in the ecology of this particular cat as the top predator in the ecosystem. In the present study, I investigated the characteristics of the ecology of the Iriomote cat concerning food habits, habitat use and movement patterns.

I conducted radio-tracking surveys in seven study sites. I examined a location fixed by the radio-tracking in each study site in terms of the cats' habitat preferences related to nine topographic and vegetative variables by using a geographic information system (GIS). Then, the seasonal and regional patterns of the cats' habitat use were examined in terms of feeding

The results showed that all studied cats selectively used their habitats. Cat locations were significantly influenced by six to eight environmental variables, depending on the study sites. To determine the most important topographic and vegetative factors influencing their habitat use, I attempted a logistic regression function following a forward stepwise approach and with environmental determinants in each study site. Suitable habitats evaluated from logistic regression models more or less differed among study sites. For the comparison of habitat use among study sites, elevation was the only variable to significantly relate to the cats' habitat use in all study sites, while the effects of other variables varied depending on the particular study site. In the results of assessing the prey availability of the cat, distribution and the abundance of their principal prey species were chiefly influenced by vegetative environments.

) of the Ryukyu Archipelago in southern Japan, is

Iriomote cat optimizes most of habitat types on the island.

374 22 Biodiversity in Ecosystems - Linking Structure and Function

Felidae.

patterns.

**5. Conclusion**

Asian continent. Iriomote Island (284 km2

*tensis*, a subspecies of leopard cats, lives.

This study would not have been possible without the support of numerous individuals and institutions. I would especially like to acknowledge Professors M. Izawa, M. Tsuchiya, A. Hagiwara and Dr N. Nakanishi at the University of the Ryukyus, as well as Professor T. Doi at Nagasaki University, Dr M. Okamura and Dr N. Sakaguchi at the Ministry of the Environ‐ ment and Dr A. Takahashi at the National Institute of Polar Research for their valuable comments relating to this study. I am also grateful to the Kumamoto Regional Forestry Office of the Forestry Agency and the Iriomote Wildlife Center of the Japan Ministry of the Environ‐ ment (IWCC) for supporting this research. The scat censuses of the Iriomote cat were con‐ ducted as a part of endangered species conservation projects administered by the Kumamoto Regional Forestry Office. Field work was carried out using IWCC facilities. I also thank the members of the Ecology Laboratory, Faculty of Science, University of the Ryukyus. I also appreciate the kindness of individuals at the IWCC and the many inhabitants of Iriomote Island, Ms C. Matsumoto and Mr M. Matsumoto in particular, for their assistance during the field work. This study was partially funded by the Inui Memorial Trust for Research on Animal Science, Fujiwara Natural History Foundation, Pro Natura Foundation Japan and the 21st Century COE Program of the University of the Ryukyus.

## **Author details**

Shinichi Watanabe\*

Address all correspondence to: watanabe@ma.fuma.fukuyama-u.ac.jp

Department of Marine Bio-Science, Fukuyama University, Japan

## **References**


[8] Watanabe S, Nakanishi N, Izawa M. Habitat and prey resource overlap between the Iriomote cat *Prionailurus iriomotensis* and introduced feral cat *Felis catus* based on as‐ sessment of scat content and distribution. Mammal Study 2003; 28: 47-56.

Regional Forestry Office. Field work was carried out using IWCC facilities. I also thank the members of the Ecology Laboratory, Faculty of Science, University of the Ryukyus. I also appreciate the kindness of individuals at the IWCC and the many inhabitants of Iriomote Island, Ms C. Matsumoto and Mr M. Matsumoto in particular, for their assistance during the field work. This study was partially funded by the Inui Memorial Trust for Research on Animal Science, Fujiwara Natural History Foundation, Pro Natura Foundation Japan and the 21st

[1] MacArthur RH, Wilson EO. The theory of island biogeography. New Jersey: Prince‐

[2] Watanabe S. Factors affecting the distribution of the leopard cat *Prionailurus bengalen‐*

[3] Darlington PJ. Zoogeography: the geographical distribution of animals. New York:

[4] Corbet GB, Hill JE. The mammals of the Indomalayan region. Natural history muse‐

[5] Sakaguchi N. Ecological aspects and social system of the Iriomote Cat *Felis iriomoten‐*

[6] Sakaguchi N, Ono Y. Seasonal change in the food habits of the Iriomote cat *Felis irio‐*

[7] Watanabe S. Ecological flexibility of the top predator in an island ecosystem: food habit of the Iriomote cat. In: Ali M. (ed.) Diversity of Ecosystems. Rijieka: InTech; 2012. p465-484. Available from: http://www.intechopen.com/books/diversity-of-eco‐ systems/ecological-flexibility-of-the-top-predator-in-anisland-ecosystem-food-habit-

Century COE Program of the University of the Ryukyus.

376 24 Biodiversity in Ecosystems - Linking Structure and Function

Address all correspondence to: watanabe@ma.fuma.fukuyama-u.ac.jp

*sis* on East Asian islands. Mammal Study 2009; 34(4): 201-207.

um publications. London: Oxford University Press; 1992.

*motensis*. Ecological Research 1994; 9(2): 167-174.

*sis* (Carnivore; Felidae) PhD thesis. Kyushu University; 1994.

Department of Marine Bio-Science, Fukuyama University, Japan

**Author details**

Shinichi Watanabe\*

**References**

ton University Press; 1967.

John Wiley and Sons; 1957.

of-the-iriomote-cat


[39] Sunquist M, Sunquist F. Wild cats of the World. Chicago and London: The University of Chicago Press; 2002.

[24] Kolowski J, Woolf A. Microhabitat use by bobcats in southern Illinois. Journal of

[25] Okamura M. A study on the reproduction and social systems of the Iriomote cat, *Felis*

[26] Eastman JR. IDRISI Kilimanjaro Tutorial. [CD-ROM] Worcester, MA: Clark Universi‐

[27] Environment Agency, Japan. Natural Environment Information GIS. [CD-ROM] To‐

[28] Sakaguchi N. Habitat of the Iriomote cat and changes in its response to prey availa‐ bility. In: (eds.) Proceedings of the International Symposium on Wildlife Conserva‐

[29] Watanabe S, Nakanishi N, Sakagichi N, Doi T, Izawa M. Temporal changes of land covers analyzed by satellite remote sensing and habitat states of the Iriomote cat *Prio‐ nailurus iriomotensis*. Bulletin of the International Association for Landscape Ecology-

[30] Dixon KR, Chapman, JA. Harmonic mean measure of animal activity areas. Ecology

[31] Freund RJ, Wilson WJ. Regression analysis: statistical modeling of a response varia‐

[32] Watanabe S, Nakanishi N, Izawa M, Doi T. Three-dimensional analysis of home range utilization by the Iriomote cat *Felis iriomotensis* using digital elevation models (DEM) (Perspectives on the mammalian home range study by telemetry).Japanese

[33] Bailey T N. Social organization in a bobcat population. Journal of Wildlife Manage‐

[34] Koehler GM, Hornocker MG. Influences of seasons on bobcats in Idaho. Journal of

[35] Palomares F, Delibes M, Revilla E, Calzada J, Fedriani, JM. Spatial ecology of Iberian lynx and abundance of European rabbits in southwestern Spain. Wildlife Mono‐

[36] Kolowski JM, Woolf A. Microhabitat use by bobcats in southern Illinois. Journal of

[37] McCord CM. Selection of winter habitat by bobcats on the Quabbin Reservation,

[38] Bailey TN. Social organization in a bobcat population. Journal of Wildlife Manage‐

tion, Tokyo, Japan, 21-25 August 1990, Tsukuba and Yokohama; 1991.

Wildlife Management 2002; 66: 822-832.

378 26 Biodiversity in Ecosystems - Linking Structure and Function

ty; 2003.

1980; 61: 1040-1044.

ment 1974; 38: 435-446.

graphs 2001;148: 1-36.

ment 1974; 38: 435-446.

ble. New York: Academic Press; 1998.

Wildlife Management 1989; 53: 197-202.

Wildlife Management 2002; 66: 822-832.

Massachusetts. Journal of Mammalogy 1974; 55: 428-437.

*iriomotensis*. PhD thesis. Kyushu University; 2002.

kyo: Nature Conservation Bureau; 1999 (in Japanese).

Japan 2002; 7(2): 25-34. (in Japanese with English abstract)

Journal of Ecology 2002; 52(2): 259-263. (in Japanese)


servation: present trends and perspectives for the 21st century. Tokyo: Sankyo; 1991. p141-143.


[67] Lachica M, Prieto SO. The energy costs of walking on the level and on negative and positive slopes in the Granadina goat (*Capra hircus*). British Journal of Nutrition 1997; 77: 73-81.

servation: present trends and perspectives for the 21st century. Tokyo: Sankyo; 1991.

[54] Nakanishi N, Okamura M, Watanabe S, Izawa M, Doi T. The effect of habitat on home range size in the Iriomote Cat *Prionailurus bengalensis iriomotensis*. Mammal

[55] Gese EM, Ruff RL, Crabtree RL. Foraging ecology of coyotes (*Canis latrans*): the influ‐ ence of extrinsic factors and a dominance hierarchy. *Canadian Journal of Zoology* 1996;

[56] Joshi AR, Smith JJD, Cuthbert FJ. Influence of food distribution and predation pres‐ sure on spacing behavior in palm civets. Journal of Mammalogy 1995; 76: 1205-1212.

[57] Litvaitis JA, Sherburne JA, Bissonette JA. Bobcat habitat use and home range size in relation to prey density. Journal of Wildlife Management 1986; 50: 110-117.

[58] Powell RA. Effects of scale on habitat selection and foraging behavior of fishers in

[59] Revilla E, Palomares F, Delibes M. Defining key habitats for low density populations of Eurasian badgers in Mediterranean environments. Biological Conservation 2000;

[60] Waller JS, Mace RD. Grizzly bear habitat selection in the Swan Mountains, Montana.

[61] Heaney LR. Small mammal diversity along elevational gradients in the Philippines: an assessment of patterns and hypotheses. Global ecology and biogeography 2001;

[62] Li JS, Song YL, Zeng ZG. 2003. Elevational gradients of small mammal diversity on the northern slopes of Mt. Qilian, China. Global ecology and biogeography 2003; 12:

[63] Rickart EA. Elevational diversity gradients, biogeography, and the structure of mon‐ tane mammal communities in the intermountain region of North America. Global

[64] Schoener T. Theory of feeding strategies. Annual review of ecology and systematics

[65] Tobler W. Three presentations on geographical analysis and modeling: Technical Re‐ port 1993; 93 (1). National Center for Geographic Information and Analysis, Santa

[66] Terrier P, Aminian K, Schutz Y. Can accelerometry accurately predict the energy cost

winter. Journal of Mammalogy 1994; 75: 349-356.

Journal of Wildlife Management 1997; 61: 1032-1039.

Ecology and Biogeography 2001; 10: 77-100.

of uphill/downhill walking? Ergonomics 2001; 44: 48-62.

Barbara University of California.

p141-143.

74: 769-783.

95: 269-277.

10: 15-39.

449-460.

1971; 2: 369-404.

Study 2005; 30(1): 1-10.

380 28 Biodiversity in Ecosystems - Linking Structure and Function


## **Grasses (Poaceae) of Easter Island — Native and Introduced Species Diversity**

Víctor L. Finot, Clodomiro Marticorena, Alicia Marticorena, Gloria Rojas and Juan A. Barrera

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59154

## **1. Introduction**

Rapa Nui (Easter Island, Isla de Pascua), also known as Te Pito O Te Henua, is a small oceanic island of volcanic origin discovered by the Dutch explorer Jakob Roggeveen in April 1722. It has belonged to Chile since 1888 and is administratively part of the Region of Valparaíso, Province Isla de Pascua. At around 163.6 km2 , it is the largest island of the Chilean insular territory, situated in Polynesia, *ca*. 3,700 km from continental Chile in the Pacific Ocean (27°7'S, 109°22'W). Rapa Nui is considered the most remote inhabited island in the world, with a population of nearly 5,800 inhabitants. Approximately 43.5 % of the island territory is under the protection of the National System of Wild Protected Areas of the State of Chile (SNASPE). The Rapa Nui National Park, administered by the National Forest Corporation of Chile (CONAF) was created on 16th January, 1935 and declared a World Heritage Site by UNESCO in 1995 to protect the Rapa Nui culture, and especially the 887 statues known as *moai* [1].

The climate is warm and sub-tropical. The flora of Rapa Nui is extremely poor compared to other oceanic tropical islands [2]. Approximately 40 % of the flora is indigenous. Nearly 23 % of the vascular flora is represented by endemic species, and some 20 species of the native flora, 10 of which are endemic, have disappeared or are endangered, principally due to invasive plants, fire, overgrazing and agriculture, among other factors [3]. Nearly 90 % of the territory corresponds to herbaceous vegetation, with species of Poaceae (grasses) as the principal component, most of them alien [4]. There are, however, very dense little forests composed of species that have come with human beings since the island was colonized. Wetlands are located chiefly in the craters of volcanoes, the largest in Rano Kau (Fig. 1) and others in Ranu Raraku and Ranu Aroi. The flora of these wetlands consists of *Schoenoplectus californicus*, *Persicaria acuminata*, *Cyperus eragrostis*, *Cyperus polystachyos* and *Sorghum halepense*. It has been suggested

© 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.

that the original vegetation of the island was represented by palm-dominated forests that have since disappeared and been replaced by a large number of introduced species that became naturalized. Pollen analyses of lake sediment cores showed a replacement of forests dominated by the palm species *Paschalococcus disperta* by grass-dominated vegetation communities [5]. Deforestation would have occurred either in AD 1000-1200 or 600 years later. It has been suggested that the deforestation of the island occurred due to intense human activity, including clearing, introduction of the Polynesian rat, fire and agriculture, among other factors [7, 8]. However, the existence of vegetation dominated by trees, as well as the proposed ecological disaster, still needs to be proven conclusively [5].

Grasslands present on the island can be divided into two types: 1. Very low grasslands, with high species diversity, overgrazed by livestock, especially horses. 2. Higher grasslands composed almost exclusively of *Melinis minutiflora*.

**Figure 1.** Crater of the volcano Rano Kau. Photo: G. Rojas.

The number of species reported for the island is not consistent in the scientific literature. Most of the differences in number of species occur, probably, because the authors include or exclude cultivated plants, and due to synonyms and nomenclatural changes.

Castro *et al*. [6] report only 40 species of monocots for Rapa Nui from a total of 121 vascular plants; these authors did not specify how many species of Poaceae there are; on the basis of 121 vascular species, Poaceae represent *ca*. 44 % of the entire vascular flora of the island. Previously, Skottsberg [9] indicated 44 species from 18 families of vascular plants, including eight genera and 12 species of Pteridophyta, and 28 genera and 32 species of Spermatophyta; Poaceae comprises 10 species. Two decades before, Fuentes reported *ca.* 124 species from 104 genera and 48 families [10]; five species reported by Fuentes are non-vascular plants and Poaceae numbers 19 species. Zizka [12] reported 100 wild angiosperms. Zizka [13, 14] reported 46 species of Poaceae. Dubois *et al*. [3] found 21 species of grasses. It has been suggested that more than 370 species of vascular plants have been introduced by humans to Rapa Nui, of which some 180 became naturalized [3].

The aim of this chapter is to provide a synopsis of the diversity of the family Poaceae (Grami‐ neae) in Rapa Nui, to provide a catalogue of all species of Poaceae and to analyse the com‐ pleteness of the inventory, to analyse the taxonomic distribution, life cycle, photosynthetic pathway, and phytogeographical origin of Poaceae in Rapa Nui and to compare the diversity of Poaceae in Rapa Nui with those of other oceanic islands. To date, the most complete list of grass species published on the flora of Rapa Nui comprises 46 species [14]. Our data indicate that in Rapa Nui, the family Poaceae comprises 50 species and one infraspecific taxon, from 37 genera and seven subfamilies. Recent taxonomic treatments have followed to update the nomenclature and the classification of the species.

## **2. History of the botanical expeditions to Rapa Nui**

that the original vegetation of the island was represented by palm-dominated forests that have since disappeared and been replaced by a large number of introduced species that became naturalized. Pollen analyses of lake sediment cores showed a replacement of forests dominated by the palm species *Paschalococcus disperta* by grass-dominated vegetation communities [5]. Deforestation would have occurred either in AD 1000-1200 or 600 years later. It has been suggested that the deforestation of the island occurred due to intense human activity, including clearing, introduction of the Polynesian rat, fire and agriculture, among other factors [7, 8]. However, the existence of vegetation dominated by trees, as well as the proposed ecological

Grasslands present on the island can be divided into two types: 1. Very low grasslands, with high species diversity, overgrazed by livestock, especially horses. 2. Higher grasslands

The number of species reported for the island is not consistent in the scientific literature. Most of the differences in number of species occur, probably, because the authors include or exclude

cultivated plants, and due to synonyms and nomenclatural changes.

disaster, still needs to be proven conclusively [5].

3842 Biodiversity in Ecosystems - Linking Structure and Function

composed almost exclusively of *Melinis minutiflora*.

**Figure 1.** Crater of the volcano Rano Kau. Photo: G. Rojas.

The first botanical collections made in Rapa Nui were those of Johann Reinhold Forster and his son Georg, during Cook's second voyage aboard the "Resolution", who sighted Rapa Nui on 13th March, 1774, and the next day landed at Hanga Roa [15]. Both Cook and Forster made similar and interesting comments, mainly on crop species such as sugarcane, potatoes and bananas. They also mentioned *Sophora toromiro* (Fabaceae) as the only native shrub species growing on the island, which was scarce, and with hard and heavy wood [16]. Georg Forster [15] cited 9 species on the island in the *Florulae insularum Australium Prodomus* which three belong to the grass family Poaceae: *Saccharum officinarum*, *Panicum filiforme* and *Avena filifor‐ mis* (=*Lachnagrostis filiformis*).

During a voyage of the Russian ship "Rurik", commanded by Captain Kotzebue, and with Adelbert von Chamisso, a naturalist, on board, it passed by Rapa Nui on a short visit; apparently, a small botanical collection was made [18]. Between 1825 and 1828, Captain Beechey's journey of exploration in the "Blossom" visited several locations in Chile, of which an important record is retained in the publications of Hooker and Arnott (1830 and 1832). The ship arrived at Rapa Nui on 16th November, 1825, but there are no records of plants [19].

Endlicher [20] in *Bermerkungen über die Flora der Südseeinseln*, lists numerous species on the islands they visited. For Rapa Nui, he mentions 11 species previously studied by Chamisso and Forster, but no specimens were deposited in herbarium. In this work, five species of Poaceae were recorded: *Paspalum filiforme*, *Agrostis conspicua*, *Deyeuxia chamissonis* (=*Lachna‐ grostis filiformis*), *Deyeuxia forsteri* (=*Lachnagrostis filiformis*) and *Lepturus repens*.

Savatier, during the campaign of the "Magicienne", reached Rapa Nui in August, 1877. Plants collected on the island are kept in the herbarium of the Museum of Paris, but no list was published. In 1885, Hemsley, in his *Report of the present stage of knowledge of various insular floras* [21], listed species of the island that were present in the work of Endlicher (except *Centaurea apula*), and also mentioned that there were other widely distributed plants that had been collected, such as the already known *Sophora tetraptera* and *Sesuvium portulacastrum*. The zoologist Alexander Agassiz, as a member of the Albatross expedition to the Tropical Eastern Pacific, visited Rapa Nui in 1904, making an important collection of plant specimens that he sent to Cambridge, Gothenburg and Washington.

In 1911, Francisco Fuentes was commissioned by the Chilean government to conduct a study on Rapa Nui. As a result of this work, Fuentes published his *Reseña botánica sobre la isla de Pascua* [10], where he mentions 135 species, of which 40 % are native or naturalized, and of these 25 are typically tropical. Grasses are represented by 19 species and 14 genera. He mentions that grasses cover the entire surface of the island, forming a steppe-like vegetation consisting mainly of *Paspalum orbiculare* (=*P. scrobiculatum* var. *orbiculare*), *Sporobolus indicus*, *Eragrostis diandra* (probably *E. tenuifolia* or *E.atrovirens*), *Andropogon halepensis* (=*Sorghum halepense*) and *Panicum sanguinale* (=*Digitaria sanguinalis*).

Between 5th October, 1916, and 26th, September, 1917, Skottsberg and his wife made a major Swedish expedition to explore and study the Juan Fernández Archipelago and Rapa Nui, which culminated in the publication of *The natural history of Juan Fernández and Easter Island* [17]. On 15th June, they arrived at La Pérouse Bay [19]. They collected 30 species that were probably indigenous or naturalized and four species that were semi-naturalized, but certainly introduced by the first inhabitants because of their usefulness, and 24 species accidentally introduced. This research increased by 23 the species mentioned by Fuentes, in which nine species of grasses are given. In 1927, the names of the plants collected in 1918 by Gusinde were also provided.

The Franco-Belgian mission exploring Rapa Nui from 29th July, 1934, to 3rd January, 1935, collected 61 species; the few that were not reported previously are obviously introduced, and known angiosperms number 142 [16]. The list mentions nine species of grasses, some new with respect to the Skottsberg list, and others that were missing, and notes that there are numerous plants without flowers to identify.

Subsequently, several researchers have conducted the collection of plants, which have been deposited in various herbaria, especially in Chile in the herbarium of the National Museum of Natural History (SGO) and the herbarium of the University of Concepción (CONC) [14]. In this work, 46 grass species have been reported.

## **3. Material and methods**

and Forster, but no specimens were deposited in herbarium. In this work, five species of Poaceae were recorded: *Paspalum filiforme*, *Agrostis conspicua*, *Deyeuxia chamissonis* (=*Lachna‐*

Savatier, during the campaign of the "Magicienne", reached Rapa Nui in August, 1877. Plants collected on the island are kept in the herbarium of the Museum of Paris, but no list was published. In 1885, Hemsley, in his *Report of the present stage of knowledge of various insular floras* [21], listed species of the island that were present in the work of Endlicher (except *Centaurea apula*), and also mentioned that there were other widely distributed plants that had been collected, such as the already known *Sophora tetraptera* and *Sesuvium portulacastrum*. The zoologist Alexander Agassiz, as a member of the Albatross expedition to the Tropical Eastern Pacific, visited Rapa Nui in 1904, making an important collection of plant specimens that he

In 1911, Francisco Fuentes was commissioned by the Chilean government to conduct a study on Rapa Nui. As a result of this work, Fuentes published his *Reseña botánica sobre la isla de Pascua* [10], where he mentions 135 species, of which 40 % are native or naturalized, and of these 25 are typically tropical. Grasses are represented by 19 species and 14 genera. He mentions that grasses cover the entire surface of the island, forming a steppe-like vegetation consisting mainly of *Paspalum orbiculare* (=*P. scrobiculatum* var. *orbiculare*), *Sporobolus indicus*, *Eragrostis diandra* (probably *E. tenuifolia* or *E.atrovirens*), *Andropogon halepensis* (=*Sorghum*

Between 5th October, 1916, and 26th, September, 1917, Skottsberg and his wife made a major Swedish expedition to explore and study the Juan Fernández Archipelago and Rapa Nui, which culminated in the publication of *The natural history of Juan Fernández and Easter Island* [17]. On 15th June, they arrived at La Pérouse Bay [19]. They collected 30 species that were probably indigenous or naturalized and four species that were semi-naturalized, but certainly introduced by the first inhabitants because of their usefulness, and 24 species accidentally introduced. This research increased by 23 the species mentioned by Fuentes, in which nine species of grasses are given. In 1927, the names of the plants collected in 1918 by Gusinde were

The Franco-Belgian mission exploring Rapa Nui from 29th July, 1934, to 3rd January, 1935, collected 61 species; the few that were not reported previously are obviously introduced, and known angiosperms number 142 [16]. The list mentions nine species of grasses, some new with respect to the Skottsberg list, and others that were missing, and notes that there are numerous

Subsequently, several researchers have conducted the collection of plants, which have been deposited in various herbaria, especially in Chile in the herbarium of the National Museum of Natural History (SGO) and the herbarium of the University of Concepción (CONC) [14]. In

*grostis filiformis*), *Deyeuxia forsteri* (=*Lachnagrostis filiformis*) and *Lepturus repens*.

sent to Cambridge, Gothenburg and Washington.

3864 Biodiversity in Ecosystems - Linking Structure and Function

*halepense*) and *Panicum sanguinale* (=*Digitaria sanguinalis*).

also provided.

plants without flowers to identify.

this work, 46 grass species have been reported.

Specimens were collected and preserved in the herbarium of the National Museum of Natural History at Santiago (SGO). Specimens were identified and photographs were taken using a Zeiss Stemi 2000 C stereomicroscope equipped with an Axiocam ERc5s camera. Images were processed with the software Zen 2011.

A database of the species of grasses of Rapa Nui was constructed, based on the databases of two important Chilean herbaria: CONC (Herbarium of the University of Concepción) and SGO (Herbarium of the National Museum of Natural History, Santiago). Specimens deposited in these herbaria and those collected for this project were included. The database contains the following fields: 1. Genus; 2. Species; 3. Common names in Rapa Nui; 4. Origin (native/ introduced/endemic); 4. Geographical origin; 5. Photosynthetic pathway; 6. Life cycle; 7. Subfamily; 8. Tribe; 9. Collector's name; 10. Collector's number; 11. Latitude; 12. Longitude; 13. Altitude; 14. Locality; 15. Date of collection (year); 16. Date (year) of first registration; 17. Herbarium; 18. Herbarium number; 19. Bibliographic citations. A total of 369 specimens were included.

A checklist is provided, including Latin name, origin (endemic, native, introduced), homeland, life cycle (annual, perennial, annual or perennial), photosynthetic pathway (C3/C4) and classification (subfamily, tribe); however, the biogeographic status is sometimes difficult or impossible to establish. Meyer's secondarization index was calculated as the number of native species/number of naturalized species [37].

The diversity of grasses of Rapa Nui was compared with the diversity of grasses of other oceanic islands (Galápagos, Pitcairn, Marquesas, Juan Fernández and Hawaii), using the regional diversity index (D). This index was calculated as D=S/log A, where S is the number of species in the region and A is the area in square kilometres [22]. The floristic affinity between these islands was compared by cluster analysis of presence-absence data for 349 species, using Jaccard coefficient as the similarity measure, UPGMA algorithm and the statistical software Infostat [23]. Species composition was taken from the literature [24-28]. Species accumulation curve and estimated richness was calculated using the software Estimates 8.0 [29].

## **4. Results**

Our database for the island included a total of 369 specimens collected over 12 decades (1900-2013), representing 51 species, 37 genera, 11 tribes and seven subfamilies (Table 1 and 2), that is, approximately 10 % of the total Chilean (continental and insular) grass flora (523 species and 57 infraspecific taxa) [30]. The proportion of species relative to the number of genera is 1.36, similar to the proportion determined by Fuentes [10] for the entire flora of the island (135 species / 104 genera=1.29). Most of the genera are represented only by one or two species, *Paspalum* (five species), *Digitaria* (three species) and *Setaria* (three species) being the most diverse. Details of some Poaceae of Rapa Nui are illustrated in Figs. 1-3.

Only two species (3.9 %) of the family Poaceae are endemic to Rapa Nui (*Rytidosperma paschalis* and *Paspalum forsterianum*). Eight or nine species are most probably native (15 %) and at least 42 (81 %) are introduced (Table 1). Native species are distributed in seven genera (1.29) and alien species in 30 genera (1.4). Among native Poaceae, the genera *Dichelachne* and *Paspalum* include two native species each, whereas the rest of the genera include only one species (*Axonopus*, *Bromus*, *Digitaria*, *Lachnagrostis* and *Piptochaetium*). Among alien Poaceae, the most diverse genera are *Paspalum* (three spp.), *Setaria* (three spp.), *Cenchrus* (two spp.), *Digitaria* (two spp.), *Sorghum* (two spp.) and *Vulpia* (one sp. and one var.).

Although there are relatively few botanical specimens of Poaceae collected in Rapa Nui, the species cited in the botanical literature are well represented in Chilean herbaria. Moreover, only one species was collected for the first time in 2013, suggesting that the inventory of species is fairly comprehensive. The first herbarium specimens entered into our database correspond to those made by Alexander Agassiz, who in 1904 collected 16 specimens representing 12 different species, about 20 % of the currently known diversity of Poaceae in Rapa Nui. By the middle of the 20th century, with the botanical expedi‐ tions made by Fuentes, Skottsberg, Balfour, Williamson & Co., Drapkin and the Mission Franco-Belge, the number of known species reached nearly 50 % of the currently known species number (Fig. 5). An important increase in the number of known species occurred after the botanical trips made by Michel Etienne, who published 24 wild and two cultivat‐ ed species of Poaceae in Rapa Nui [4] and by Georg Zizka, who reported 46 species of grasses, the most comprehensive list until today [13, 14]. In the decade 1981-1990, a total of 149 specimens of Poaceae were collected, most of them by Zizka. In general, the herbarium collections of Poaceae from Rapa Nui are limited. Our database for the island included a total of 369 specimens over 12 decades (1900-2013), including a total of 51 taxa, most of which were known previously [2], and in Zizka's [13, 14] papers.

Most of the species of grasses of the island are introduced, some of them cited very early in the botanical literature, such as *Cynodon dactylon*, *Cenchrus echinatus* and *Sorghum halepense*, as well as some cultivated species, such as *Zea mays*, *Triticum aestivum* and *Arundo donax* [10]. Some native species were collected very early by R. and G. Forster in 1774 [15], for example, *Paspalum forsterianum*, dedicated to them by Flüggé. In Rapa Nui, Forster also collected *Sporobolus indicus*, *Dichelachne micrantha*, *Bromus catharticus* and the type specimen of *Agrostis avenacea* (=*Lachnagrostis filiformis*) [14]. *Stipa horridula* was collected by Skottsberg in Mount Katiki in 1917; this specimen (Skottsberg 660) became the type (lectotype) of *Stipa horridula* published by Pilger in 1922, and considered endemic to the island for a long time. In 1990, Everett and Jacob [30] reduced it to the synonymy of *Stipa scabra* Lindl., later transferred to *Austrostipa* (*A. scabra*). Skottsberg also collected, in 1917, the type specimen (Skottsber 658) of *Danthonia paschalis* Pilg. [=*Rytidosperma paschale* (Pilg.) C.M. Baeza] [17]. This species is one of the two recognized endemic Poaceae from Rapa Nui.

In 1911, Francisco Fuentes collected, among other plants, a specimen published as the holotype of *Paspalum paschale*. This name was soon transferred to genus *Axonopus*(*A. paschalis*), a species considered for a long time endemic to the island. In addition, another 18 species of Poaceae were collected by Fuentes. In 1936, Guillaumin collected eight grass species, most of them

Only two species (3.9 %) of the family Poaceae are endemic to Rapa Nui (*Rytidosperma paschalis* and *Paspalum forsterianum*). Eight or nine species are most probably native (15 %) and at least 42 (81 %) are introduced (Table 1). Native species are distributed in seven genera (1.29) and alien species in 30 genera (1.4). Among native Poaceae, the genera *Dichelachne* and *Paspalum* include two native species each, whereas the rest of the genera include only one species (*Axonopus*, *Bromus*, *Digitaria*, *Lachnagrostis* and *Piptochaetium*). Among alien Poaceae, the most diverse genera are *Paspalum* (three spp.), *Setaria* (three spp.), *Cenchrus* (two spp.),

Although there are relatively few botanical specimens of Poaceae collected in Rapa Nui, the species cited in the botanical literature are well represented in Chilean herbaria. Moreover, only one species was collected for the first time in 2013, suggesting that the inventory of species is fairly comprehensive. The first herbarium specimens entered into our database correspond to those made by Alexander Agassiz, who in 1904 collected 16 specimens representing 12 different species, about 20 % of the currently known diversity of Poaceae in Rapa Nui. By the middle of the 20th century, with the botanical expedi‐ tions made by Fuentes, Skottsberg, Balfour, Williamson & Co., Drapkin and the Mission Franco-Belge, the number of known species reached nearly 50 % of the currently known species number (Fig. 5). An important increase in the number of known species occurred after the botanical trips made by Michel Etienne, who published 24 wild and two cultivat‐ ed species of Poaceae in Rapa Nui [4] and by Georg Zizka, who reported 46 species of grasses, the most comprehensive list until today [13, 14]. In the decade 1981-1990, a total of 149 specimens of Poaceae were collected, most of them by Zizka. In general, the herbarium collections of Poaceae from Rapa Nui are limited. Our database for the island included a total of 369 specimens over 12 decades (1900-2013), including a total of 51 taxa,

*Digitaria* (two spp.), *Sorghum* (two spp.) and *Vulpia* (one sp. and one var.).

3886 Biodiversity in Ecosystems - Linking Structure and Function

most of which were known previously [2], and in Zizka's [13, 14] papers.

the two recognized endemic Poaceae from Rapa Nui.

Most of the species of grasses of the island are introduced, some of them cited very early in the botanical literature, such as *Cynodon dactylon*, *Cenchrus echinatus* and *Sorghum halepense*, as well as some cultivated species, such as *Zea mays*, *Triticum aestivum* and *Arundo donax* [10]. Some native species were collected very early by R. and G. Forster in 1774 [15], for example, *Paspalum forsterianum*, dedicated to them by Flüggé. In Rapa Nui, Forster also collected *Sporobolus indicus*, *Dichelachne micrantha*, *Bromus catharticus* and the type specimen of *Agrostis avenacea* (=*Lachnagrostis filiformis*) [14]. *Stipa horridula* was collected by Skottsberg in Mount Katiki in 1917; this specimen (Skottsberg 660) became the type (lectotype) of *Stipa horridula* published by Pilger in 1922, and considered endemic to the island for a long time. In 1990, Everett and Jacob [30] reduced it to the synonymy of *Stipa scabra* Lindl., later transferred to *Austrostipa* (*A. scabra*). Skottsberg also collected, in 1917, the type specimen (Skottsber 658) of *Danthonia paschalis* Pilg. [=*Rytidosperma paschale* (Pilg.) C.M. Baeza] [17]. This species is one of

In 1911, Francisco Fuentes collected, among other plants, a specimen published as the holotype of *Paspalum paschale*. This name was soon transferred to genus *Axonopus*(*A. paschalis*), a species considered for a long time endemic to the island. In addition, another 18 species of Poaceae were collected by Fuentes. In 1936, Guillaumin collected eight grass species, most of them

**Figure 2.** A-E.*Arundo donax* (Alves 34). F-J. *Axonopus compressus* (Zizka 357). K. *Cenchrus clandestinus* (Alves 57). L-N. *Chloris gayana* (Zizka 562). O-P. *Cenchrus echinatus* (Rodríguez 2202); Q-S. *Digitaria ciliaris* (Alves 13ª). Scale bars: A-B=5 mm; C-J, N, R-S=1 mm; K, O-P=2 mm; L-M, Q=3 mm

**Figure 3.** A-C. *Dichelachne micrantha* (Lücke 15). D-F. *Eleusine indica* (Zizka 330). G-J. *Eragrostis tenuifolia* (Alves 30). K-M. *Lachnagrostis filiformis*. N-P. *Melinis repens* (Zizka 586). Q. *Bothriochloa ischaemum* (Zizka 330). Scale bar: Q=2 mm. Scale bars: B-F, I-L=1 mm; G-H, M, P=2 mm; A, N-O=3 mm

Grasses (Poaceae) of Easter Island — Native and Introduced Species Diversity 9 http://dx.doi.org/ 10.5772/59154 391

D

I

E F G H

A B C

K L M

N O P Q

**Figure 3.** A-C. *Dichelachne micrantha* (Lücke 15). D-F. *Eleusine indica* (Zizka 330). G-J. *Eragrostis tenuifolia* (Alves 30). K-M. *Lachnagrostis filiformis*. N-P. *Melinis repens* (Zizka 586). Q. *Bothriochloa ischaemum* (Zizka 330). Scale bar: Q=2 mm.

J

3908 Biodiversity in Ecosystems - Linking Structure and Function

Scale bars: B-F, I-L=1 mm; G-H, M, P=2 mm; A, N-O=3 mm

Figure 4. A-D. *Melinis minutiflora* (Alves 60). E-F. *Ehrharta stipoides* (Alves 32). G. *Paspalum dilatatum* (Stuessy 11008). H. *Paspalum forsterianum* (Vidal s.n.). I-J. *Paspalum scrobiculatum* (Alves 98). K. *Sorghum halepense*. L-O. *Sporobolus indicus*. Scale bars: A, C-E, J, L = 1 mm; G-I, K, M-O = 2 mm; B = 3 mm **Figure 4.** A-D. Melinis minutiflora (Alves 60). E-F. Ehrharta stipoides (Alves 32). G. Paspalum dilatatum (Stuessy 11008). H. Paspalum forsterianum (Vidal s.n.). I-J. Paspalum scrobiculatum (Alves 98). K. Sorghum halepense. L-O. Sporobolus indicus. Scale bars: A, C-E, J, L=1 mm; G-I, K, M-O=2 mm; B=3 mm

**Figure 5.** Number of specimens and species collected in Rapa Nui in 12 decades between 1904 and 2013

previously known from Fuentes' collection. Guillaumin collected, probably for the first time, *Briza minor*, nowadays naturalized all over the world [16]. Zizka [13, 14] collected and described 46 species representing the most important contribution to the knowledge of the grass family in Rapa Nui.

## **5. Taxonomic distribution of Poaceae in Rapa Nui**

The taxonomic distribution of the species of Poaceae in Rapa Nui is shown in Table 1. Seven subfamilies are represented. In continental Chile, eight subfamilies are present [30], of which only species of the subfamily Aristidoideae are absent in Rapa Nui.

The subfamily Arundinoideae comprises only one species: *Arundo donax*, a perennial C3 reedlike species introduced from southern Europe, probably at the beginning of the 20th century or before. It was mentioned as a component of the Rapa Nui flora by Francisco Fuentes in 1913 [10]. According to our records and the literature [4], it is restricted to the crater of the Rano Kau volcano as a remnant of cultivation [14]. This species is recognized as invasive in Southern Africa, Australia, North America and the Pacific Islands [3].

The subfamily Bambusoideae is represented only by cultivated bamboos of the genus *Bambusa*.

The subfamily Chloridoideae comprises six genera and six species in Rapa Nui (Table 1), all belonging to the subtribe Cynodonteae, most introduced from Tropical Africa, such as *Chloris gayana*, *Cynodon dactylon*, *Eragrostis atrovirens* and *Sporobolus indicus*. Accordig to Zizka [13], the identity of the species of *Eragrostis* in Rapa Nui is not clear. This author mentions *E. spartinoides* (=*E. brownii*) and *E. leptostachya.* In this paper, we follow the revision of the genus *Eragrostis* by Escobar *et al*. [34]. According to these authors, the species of *Eragrostis* inhabiting Rapa Nui correspond to *E. atrovirens* and *E. tenuifolia*. *Eleusine indica* is a cosmopolitan Chloridoideae reported in Rapa Nui early in the 20th century.

The subfamily Danthonioideae comprises only two species in Rapa Nui. One of the species was mentioned only once in the literature dealing with Rapa Nui flora [11], under the name *Gynerium argenteum* a synonym for *Cortaderia selloana*. This species is native to South America and is probably alien in Rapa Nui. It seems that this plant was introduced for erosion control [3]. The second species is *Ritydosperma paschale*, endemic to the island. As was established by Zizka [13], and according to our database, this species is restricted to the slopes of the Rano Kau volcano. It was also collected previously in Pua Katiki [4], but it seems to now be restricted to Rano Kau [14].

The only species of the subfamily Ehrhartoideae known in Rapa Nui is *Ehrharta stipoides* (=*Microlaena stipoides*), a species growing in Africa, Tropical Asia, Australasia and the Pacific [32]. This species is important as forage, but it was reported as invasive in Hawaii and Réunion Island. It was reported in Rapa Nui as a species widely distributed in the island, advantaged by overgrazing [4].

The subfamily Panicoideae comprises 12 genera and 23 species, representing about 44 % of the grass flora of Rapa Nui (Table 1). This clearly contrasts with the total grass flora of Chile, where Panicoideae represents only *ca*. 10 % [30]. *Paspalum*, *Setaria* and *Digitaria* are the most speciose genera.

Panicoideae includes the second endemism of this family from the island, *Paspalum forsteria‐ num*, a species whose conservation status is "Vulnerable" [3]. To this subfamily also belongs *Axonopus paschalis*, long considered endemic to the island. This species was recently included as a synonym of *A. compressus*. According to Morrone [unpublished data, Flora de Chile], *A. paschalis* is morphologically similar to *A. compressus* from which it differs by the size of the leaf blades, the longer, narrower and more rigid leaves, by the hairiness of the spikelets and by the brown superior floret. *Bothriochloa ischaemum* was collected for the first time shortly after it had been introduced to the island; this species behaves invasively [4]. Several other Panicoideae are found, some of them widely recognized as invasive (v. gr. *Setaria parviflora*, *Cenchrus echinatus*, *C. clandestinus*, *Paspalum scrobiculatum*, etc.), others cultivated, such as *Saccharum officinarum*.


**Table 1.** Number of tribes, genera and species of Poaceae in Easter Island

previously known from Fuentes' collection. Guillaumin collected, probably for the first time, *Briza minor*, nowadays naturalized all over the world [16]. Zizka [13, 14] collected and described 46 species representing the most important contribution to the knowledge of the

**Figure 5.** Number of specimens and species collected in Rapa Nui in 12 decades between 1904 and 2013

The taxonomic distribution of the species of Poaceae in Rapa Nui is shown in Table 1. Seven subfamilies are represented. In continental Chile, eight subfamilies are present [30], of which

The subfamily Arundinoideae comprises only one species: *Arundo donax*, a perennial C3 reedlike species introduced from southern Europe, probably at the beginning of the 20th century or before. It was mentioned as a component of the Rapa Nui flora by Francisco Fuentes in 1913 [10]. According to our records and the literature [4], it is restricted to the crater of the Rano Kau volcano as a remnant of cultivation [14]. This species is recognized as invasive in Southern

The subfamily Bambusoideae is represented only by cultivated bamboos of the genus *Bambusa*. The subfamily Chloridoideae comprises six genera and six species in Rapa Nui (Table 1), all belonging to the subtribe Cynodonteae, most introduced from Tropical Africa, such as *Chloris gayana*, *Cynodon dactylon*, *Eragrostis atrovirens* and *Sporobolus indicus*. Accordig to Zizka [13], the identity of the species of *Eragrostis* in Rapa Nui is not clear. This author mentions *E. spartinoides* (=*E. brownii*) and *E. leptostachya.* In this paper, we follow the revision of the genus *Eragrostis* by Escobar *et al*. [34]. According to these authors, the species of *Eragrostis* inhabiting Rapa Nui correspond to *E. atrovirens* and *E. tenuifolia*. *Eleusine indica* is a cosmopolitan

The subfamily Danthonioideae comprises only two species in Rapa Nui. One of the species was mentioned only once in the literature dealing with Rapa Nui flora [11], under the name

**5. Taxonomic distribution of Poaceae in Rapa Nui**

only species of the subfamily Aristidoideae are absent in Rapa Nui.

Africa, Australia, North America and the Pacific Islands [3].

Chloridoideae reported in Rapa Nui early in the 20th century.

grass family in Rapa Nui.

392 10 Biodiversity in Ecosystems - Linking Structure and Function

The subfamily Pooideae comprises 16 species from 15 genera, being the second most diverse subfamily. Whereas Pooideae include most of the grasses of the Chilean flora (74.65 %) [30], in Rapa Nui it represents only *ca*. 31 % (Table 1). A list of the species, homeland, photosynthetic pathway, life cycle and classification (subfamily, tribe) is given in Table 2.

## **6. Phytogeographical origin of Poaceae in Rapa Nui**

As in other oceanic islands, grasses are the most common alien plants occurring in Rapa Nui [3, 33, 35]. The number of endemic, native and alien species of the grass flora in the island is shown in Fig. 6, where we can see that alien plants represent the vast majority of the grass flora (Meyer's secondarization index=0.24). Introduced species are mainly of African, European and Asian origin (Fig. 7, Table 2).

The proportion of alien species in six Poaceae subfamilies (Bambusoideae was not included as it contains only one cultivated species) is shown in Figure 8. All Chlorodoideae seem to be alien, most of African origin. However, the identity of some species, mainly those of *Eragros‐ tis*, is difficult to elucidate. *Eragrostis atrovirens*, *E. spartinoides* and *E. tenuifolia* have been mentioned, however, only *E. atrovirens* and *E. tenuifolia* were recently recognized in Rapa Nui [34]. *Sporobolus indicus* (Chloridoideae) was collected in cultivated field as agrestal weed (vineyards, pineapple).

Most of the species of subfamily Panicoideae and subfamily Pooideae, which constitute the bulk of the grass flora of the island, are alien. The only species of subfamily Ehrhartoideae, *Ehrharta stipoides*, seems to be invasive; this species is widely distributed in the island and expands in cases of overgrazing [4].

**Figure 6.** Percentage of native, endemic and introduced grass species in Rapa Nui

Rapa Nui belongs to the Polynesian Biogeographic Province [36] or Polynesian Floristic Region [37], included among the 25 biodiversity hotspots of the world [38, 39]. Specifically, it belongs to the Eastern Polynesia Subregion of Polynesia and represents the driest island of the subregion, with 1,325 mm of annual precipitation. In effect, there is no native vegetation on the island today and introduced plants outnumber native species due to the deforestation that occurred soon after the arrival of the first Polynesian inhabitants (38).

Introduced species that became naturalized or invasive represent one of the major threats to native species. It has been proposed that aboriginal people significantly modified the vegeta‐ tion of the island [6] and the original vegetation communities were replaced by grasslands. In these plant communities, introduced species became increasingly abundant [40]. According to Aldén [2], the composition of the flora underwent a rapid change from the 18th century, when European people begin to visit the island.

On the other hand, around 70,000 tourists visit the island each year, causing environmental deterioration [41]. As shown in Figure 9, a sharp increase in the amount of alien species occurs in the 1990s; by this time, there are three times the number of alien species present compared to when Francisco Fuentes visited the island in 1911; nevertheless, in the 1910s, aliens already exceed the number of native species. Zizka [14] collected six species of grasses for the first time, all of them introduced. In some cases, nevertheless, we cannot be absolutely sure if certain species are indigenous or were accidentally introduced by man.

**Figure 7.** Geographic origin of the species introduced to Rapa Nui

The subfamily Pooideae comprises 16 species from 15 genera, being the second most diverse subfamily. Whereas Pooideae include most of the grasses of the Chilean flora (74.65 %) [30], in Rapa Nui it represents only *ca*. 31 % (Table 1). A list of the species, homeland, photosynthetic

As in other oceanic islands, grasses are the most common alien plants occurring in Rapa Nui [3, 33, 35]. The number of endemic, native and alien species of the grass flora in the island is shown in Fig. 6, where we can see that alien plants represent the vast majority of the grass flora (Meyer's secondarization index=0.24). Introduced species are mainly of African, European and

The proportion of alien species in six Poaceae subfamilies (Bambusoideae was not included as it contains only one cultivated species) is shown in Figure 8. All Chlorodoideae seem to be alien, most of African origin. However, the identity of some species, mainly those of *Eragros‐ tis*, is difficult to elucidate. *Eragrostis atrovirens*, *E. spartinoides* and *E. tenuifolia* have been mentioned, however, only *E. atrovirens* and *E. tenuifolia* were recently recognized in Rapa Nui [34]. *Sporobolus indicus* (Chloridoideae) was collected in cultivated field as agrestal weed

Most of the species of subfamily Panicoideae and subfamily Pooideae, which constitute the bulk of the grass flora of the island, are alien. The only species of subfamily Ehrhartoideae, *Ehrharta stipoides*, seems to be invasive; this species is widely distributed in the island and

Rapa Nui belongs to the Polynesian Biogeographic Province [36] or Polynesian Floristic Region [37], included among the 25 biodiversity hotspots of the world [38, 39]. Specifically, it belongs

pathway, life cycle and classification (subfamily, tribe) is given in Table 2.

**6. Phytogeographical origin of Poaceae in Rapa Nui**

**Figure 6.** Percentage of native, endemic and introduced grass species in Rapa Nui

Asian origin (Fig. 7, Table 2).

394 12 Biodiversity in Ecosystems - Linking Structure and Function

(vineyards, pineapple).

expands in cases of overgrazing [4].

From a physiological point of view, introduced species mostly show C4 photosynthesis (Fig. 10), and most of the species, both alien and native, are perennial (Fig. 11). It has been demon‐ strated that alien species distantly related to the native flora are more likely to become harmful weeds for regional ecosystems, supporting Darwin's naturalization hypothesis; thus, special attention should be paid to newly introduced species for which there are no close relatives in the regional flora [42]. In Rapa Nui, our data show that species from 30 genera and two subfamilies that do not include native species have been introduced.

**Figure 8.** Taxonomic distribution of the alien species recorded for Rapa Nui

**Figure 9.** Number of native and introduced grass species in Rapa Nui in 12 decades of botanical collections

**Figure 10.** Number of C3 and C4 grass species in Rapa Nui

**Figure 11.** Life cycle of native and alien species of Poaceae in Rapa Nui

**Figure 9.** Number of native and introduced grass species in Rapa Nui in 12 decades of botanical collections

**Figure 8.** Taxonomic distribution of the alien species recorded for Rapa Nui

396 14 Biodiversity in Ecosystems - Linking Structure and Function

**Figure 10.** Number of C3 and C4 grass species in Rapa Nui

## **7. Comparing the diversity of Poaceae in Rapa Nui with other Pacific Islands**

The diversity of grasses in Rapa Nui, calculated as the number of species per area expressed in square kilometres (regional diversity index) is slightly lower than that of the Juan Fernández Archipelago (Fig. 12). According to the literature, Poaceae in Juan Fernández Archipelago comprises 32 genera and 53 species [33, 43]. This number is relatively small compared with Hawaii (216 species) and Galápagos (94 species). From Desventuradas islands (San Félix, San Ambrosio), only two species have been recorded (*Eragrostis kuschelii* and *E. peruviana*), the first one endemic to Chile (Desventuradas Islands). If the identity of the species is considered, Rapa Nui is still more similar to Juan Fernández than to other Pacific islands (Fig. 13). However, taxonomic distribution of the flora of Poaceae is different in these two Chilean islands. C3 Pooideae dominated Poaceae in Juan Fernández, whereas in the more tropical Rapa Nui, C4 Panicoideae are more abundant. In both islands, perennial grasses dominate over annuals.

**Figure 12.** Diversity of Poaceae of Rapa Nui (Easter Island) compared to other oceanic islands

**Figure 13.** Poaceae floristic similarity between Rapa Nui (Easter Island) and other Pacific islands.



0,00 0,26 0,52 0,78 1,04 Distance (J)

**cycle**

I Australia C3 P Pooideae Stipeae

N South America C4 P Panicoideae Paniceae

I Africa C4 P Panicoideae Paniceae

C3 P Pooideae Poeae

C3 P Pooideae Poeae

C4 A Panicoideae Paniceae

**Subfamily Tribe**

Easter Island Juan Fernández Galápagos Marquesas Haw aii Pitcairn

398 16 Biodiversity in Ecosystems - Linking Structure and Function

**Species Origin Homeland C3/C4 Life**

3. *Austrostipa scabra* (Lindl.) S.W.L.

5. *Axonopus compressus* (Sw.) P.

10. *Cenchrus clandestinus* (Hochst. Ex

17. *Dichelachne micrantha* (Cav.)

19. *Digitaria setigera* Roth ex Roem. &

16. *Dichelachne crinita* (L. f.) Hook. f. N Australia, Asia

Jacobs & J. Everett

Chiov.) Morrone

Domin

Schult.

Beauv.

**Figure 13.** Poaceae floristic similarity between Rapa Nui (Easter Island) and other Pacific islands.

1. *Agrostis stolonifera* L. I Europe C3 P Pooideae Poeae 2. *Arundo donax* L. I Europe C3 P Arundinoideae Arundineae

4. *Avena fatua* L. I Europe C3 A Pooideae Poeae

8. *Briza minor* L. I Europa C3 A Pooideae Poeae 9. *Bromus catharticus*Vahl N America C3 P Pooideae Bromeae

11. *Cenchrus echinatus* L. I Cosmopolitan C4 A Panicoideae Paniceae 12. *Chloris gayana* Kunth I Africa C4 P Chloridoideae Cynodonteae 13. *Coix lacryma-jobi* L. I Asia C4 P Panicoideae Andropogoneae 14. *Cortaderia selloana* I South America C3 P Danthonioideae Danthonieae 15. *Cynodon dactylon* (L.) Pers. I Tropical AfricaC4 P Chloridoideae Cynodonteae

& Pacific

18. *Digitaria ciliaris* (Retz.) Koeler N? South America C4 A Panicoideae Paniceae

N Australia, Asia & Pacific

I Australia, Asia & Pacific

6. *Bambusa* sp. C Asia C3 P Bambusoideae Bambuseae 7. *Bothriochloa ischaemum* (L.) Keng I Asia C4 P Panicoideae Andropogoneae


**Table 2.** List of the species of Poaceae in Rapa Nui. Life cycle: A=annual; P=perennial; Origin: EI=Rapa Nui; e=endemic; i=introduced; n=native

### **8. Taxonomic sampling effort**

The collection effort (sampling) is an important part of the taxonomic work on which the knowledge of species richness and, ultimately, the knowledge of biodiversity are based. Although collectors try to find all the species in a region, this goal is almost impossible, or at least very difficult to achieve; thus, the real number of species can only be estimated from the number of observed (collected) species (48). As shown in Table 3 and Figure 14, for a total of 50 observed species, the species richness estimated by different estimators ranges from 58.3 (Bootstrap) to 86.8 (Chao). An increased collection effort for Poaceae in Rapa Nui could yield between eight and 36 additional hitherto unsampled species. As shown in Fig. 15, collections are concentrated only in a few localities, chiefly in Rano Kau, near Hanga Roa, Anakena, and Rano Raraku.


**Table 3.** Estimated species richness of Poaceae in Rapa Nui, using eight different estimators.

**Figure 14.** Species accumulation curve (Sobs) and estimated species curves for 12 decades of sampling, based on Chao 1 and Bootstrap estimators.

**Figure 15.** Map of the localities of Poaceae collected in Rapa Nui. Each point represents at least one collected specimen.

### **9. Concluding remarks**

**Species Origin Homeland C3/C4 Life**

49. *Vulpi amyuros* (L.) C. C. Gmel var.

400 18 Biodiversity in Ecosystems - Linking Structure and Function

**8. Taxonomic sampling effort**

50. *Vulpia myuros* var. *megalura*

*myuros*

(Nutt.) Auquier

i=introduced; n=native

Rano Raraku.

**cycle**

47. *Sporobolus indicus* (L.) R. Br. I Africa C4 P Chloridoideae Cynodonteae 48. *Triticum aestivum* L. I Asia C3 A Pooideae Triticeae

51. *Zea mays* L. I America C4 A Panicoideae Andropogoneae

**Table 2.** List of the species of Poaceae in Rapa Nui. Life cycle: A=annual; P=perennial; Origin: EI=Rapa Nui; e=endemic;

The collection effort (sampling) is an important part of the taxonomic work on which the knowledge of species richness and, ultimately, the knowledge of biodiversity are based. Although collectors try to find all the species in a region, this goal is almost impossible, or at least very difficult to achieve; thus, the real number of species can only be estimated from the number of observed (collected) species (48). As shown in Table 3 and Figure 14, for a total of 50 observed species, the species richness estimated by different estimators ranges from 58.3 (Bootstrap) to 86.8 (Chao). An increased collection effort for Poaceae in Rapa Nui could yield between eight and 36 additional hitherto unsampled species. As shown in Fig. 15, collections are concentrated only in a few localities, chiefly in Rano Kau, near Hanga Roa, Anakena, and

I Europe, Asia, Africa

I Europe, Asia, Africa

**Diversity Estimator Species Richness**

**Table 3.** Estimated species richness of Poaceae in Rapa Nui, using eight different estimators.

Sobs (Mao Tau) 50 ACE 70.6 ICE 73.7 Chao 1 86.8 Chao 2 86.8 Jack 1 69.3 Jack 2 82.2 Bootstrap 58.3 Michaelis-Menten 66.06

**Subfamily Tribe**

C3 A Pooideae Poeae

C3 A Pooideae Poeae

The floras of the oceanic islands are especially prone to serious threats from alien invaders [44], because they have a propensity to include highly adapted specialist rather than generalist species [45]. This is of particular interest, as these ecosystems comprise high numbers of endemic plants, in contrast with continental regions of similar size [6]. For these reasons, it is necessary to have on hand complete lists of the flora indicating alien plants that could be agricultural weeds and invasive species that can put pressure on native ecosystems.

Poaceae contains an important number of species that behave as weeds in natural environ‐ ments (invasive), as well as in ruderal and agricultural habitats all over the world. In Rapa Nui, grasses are the most diverse family of vascular plants; nearly 90 % of the island is covered by grasslands and alien grasses represent nearly 80 % of the Poaceae of the island. A similar situation occurs in other oceanic islands [33]. Several alien species introduced to Rapa Nui are noxious weeds (*Agrostis stolonifera*, *Hordeum murinum*, *Sorghum halepense*, *Lolium perenne*, *Setaria parviflora*), probably introduced accidentally, mostly from Europe. As was previously established [38], Rapa Nui shows the greatest (<1) secondarization index (number of native species/number of naturalized species=0.68) when compared with many other Easter Polyne‐ sian islands. For Poaceae, this index is greater still (0.24).

On the other hand, only two Poaceae endemic to Rapa Nui are recognized. Another two Poaceae considered endemic in previous studies have been the object of taxonomic studies that demonstrate their non-endemic status: *Axonopus paschalis* (=*Axonopus compressus*) and *Stipa scabra* (*Austrostipa scabra*).

Herbarium specimens provide valuable information to appreciate regional plant diversity, as well as to understand plant invasions and geography [46, 47]. A wide array of data (phenology, flowering periodicity, distribution, altitude, morphometry, minimum residence time, new distributional records, etc.), that are important to biodiversity monitoring can be obtained from herbarium specimens [49]. However, herbarium collections in Rapa Nui are relatively scarce.

## **Author details**

Víctor L. Finot1 , Clodomiro Marticorena2 , Alicia Marticorena2 , Gloria Rojas3 and Juan A. Barrera4

\*Address all correspondence to: victorfinotsaldias@gmail.com

1 Department of Animal Production, Faculty of Agronomy, University of Concepción, Chill‐ án, Chile

2 Department of Botany, Faculty of Natural and Oceanographic Resources, University of Concepción, Concepción, Chile

3 National Museum of Natural History, Santiago, Chile

4 Department of Soil Science and Natural Resources, Faculty of Agronomy, University of Concepción, Chillán, Chile

## **References**

species [45]. This is of particular interest, as these ecosystems comprise high numbers of endemic plants, in contrast with continental regions of similar size [6]. For these reasons, it is necessary to have on hand complete lists of the flora indicating alien plants that could be

Poaceae contains an important number of species that behave as weeds in natural environ‐ ments (invasive), as well as in ruderal and agricultural habitats all over the world. In Rapa Nui, grasses are the most diverse family of vascular plants; nearly 90 % of the island is covered by grasslands and alien grasses represent nearly 80 % of the Poaceae of the island. A similar situation occurs in other oceanic islands [33]. Several alien species introduced to Rapa Nui are noxious weeds (*Agrostis stolonifera*, *Hordeum murinum*, *Sorghum halepense*, *Lolium perenne*, *Setaria parviflora*), probably introduced accidentally, mostly from Europe. As was previously established [38], Rapa Nui shows the greatest (<1) secondarization index (number of native species/number of naturalized species=0.68) when compared with many other Easter Polyne‐

On the other hand, only two Poaceae endemic to Rapa Nui are recognized. Another two Poaceae considered endemic in previous studies have been the object of taxonomic studies that demonstrate their non-endemic status: *Axonopus paschalis* (=*Axonopus compressus*) and

Herbarium specimens provide valuable information to appreciate regional plant diversity, as well as to understand plant invasions and geography [46, 47]. A wide array of data (phenology, flowering periodicity, distribution, altitude, morphometry, minimum residence time, new distributional records, etc.), that are important to biodiversity monitoring can be obtained from herbarium specimens [49]. However, herbarium collections in Rapa Nui are relatively scarce.

, Alicia Marticorena2

1 Department of Animal Production, Faculty of Agronomy, University of Concepción, Chill‐

2 Department of Botany, Faculty of Natural and Oceanographic Resources, University of

4 Department of Soil Science and Natural Resources, Faculty of Agronomy, University of

, Gloria Rojas3

and

agricultural weeds and invasive species that can put pressure on native ecosystems.

sian islands. For Poaceae, this index is greater still (0.24).

, Clodomiro Marticorena2

3 National Museum of Natural History, Santiago, Chile

\*Address all correspondence to: victorfinotsaldias@gmail.com

*Stipa scabra* (*Austrostipa scabra*).

402 20 Biodiversity in Ecosystems - Linking Structure and Function

**Author details**

Víctor L. Finot1

Juan A. Barrera4

Concepción, Concepción, Chile

Concepción, Chillán, Chile

án, Chile


[27] Robinson B .L. Flora of the Galapagos Islands. Proceedings of the American Acade‐ my of Arts and Sciences 1902; 38: 77-270.

[14] Zizka G. Flowering plants of Easter Island. Palmarum Hortus Francofurt, 1991;3:

[15] Forster G. Florulae insularum australium prodomus. J. C. Dieterich, Göttingen, 1786.

[16] Guillaumin A., Camus A., Tardieu-Blot, M. L. Plantes vasculaires récoltées à l'Ile de Pâquespar la misión franco-belge. Bull. Mus. Natl. Hist. Nat. Sér., 1936; 2, 8: 552-556.

[17] Skottsberg, C. The natural history of Juan Fernandez and Easter Island, edited by

[18] Kotzebue O. von, Chamisso, A. von, Engelhardt, M. van, Eschscholtz, Horner J. C. A voyage of discovery into the South Sea and Beering's [sic] Straits, for the purpose of exploring a north-east passage undertaken in the years 1815-1818, at the expense of His Highness the chancellor of the empire, Count Romanzoff, in the ship Rurick, un‐ der the command of the lieutenant in the Russian Imperial Navy, Otto von Kotzebue.

[19] Marticorena C. Historia de la exploración botánica de Chile. In: C. Marticorena & R. Rodríguez (eds.), Flora de Chile. 1-62. Editorial Universidad de Concepción. Chile,

[21] Hemsley, W. B. Report on present state of knowledge of various insular floras, being an introduction to the botany of the Challenger expedition. Rep. Sci. Results Voyage

[22] Klopper R. R., Gautier L., Chatelain C., Smith G. F., Spichiger R. Floristics of the an‐ giosperm flora of Sub-Saharan Africa: An analysis of the African plant checklist and

[23] Di Rienzo J. A., Casanoves F., Balzarini M. G., Gonzalez L., Tablada M., Robledo C. W. InfoStat versión Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argen‐

[24] Kingston N., Waldren S., Bradley U. The phytogeographical affinities of the Pitcairn Islands – a model for south-eastern Polynesia? Journal of Biogeography 2003; 30:

[25] Waldren, S., M. I. Weisler, K. C. Hather & D. Morrow. The non-native vascular plants of Henderson Island, South Central Pacific Ocean. Atoll Research Bulletin n°.463, Na‐ tional Museum of Natural History, Smithsonian Institution, Washington DC, USA,

[26] Wagner W. L., Herbst D. R., Khan N., Flynn T. Hawaiian vascular plant updates: A supplement to the Manual of the flowering plants of Hawai'i's ferns and fern allies, 2012. http://botany.si.edu/pacificislandbiodiversity/hawaiianflora/supplement.htm

Carl Skottsberg. Uppsala. Vol. II, Botany, 1921; pp.1920-1956.

[20] Endlicher S. Bermerkungenüberdie Flora der Südseeinseln, 1836.

tina, 2013. http://www.infostat.com.ar (accessed 08 Jul 2014).

Longman, Hurst, Rees, Orme and Brown, 1821.

H.M.S. Challenger. Botany, 1885; 1: 1-75.

database. Taxon 2007; 56(1): 201-208.

1-108.

404 22 Biodiversity in Ecosystems - Linking Structure and Function

1995.

1311-1328.

1999.

(accessed 03 Jul 2014).


## **Plant Structure in the Brazilian Neotropical Savannah Species**

Suzane Margaret Fank-de-Carvalho, Nádia Sílvia Somavilla, Maria Salete Marchioretto and Sônia Nair Báo

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59066

## **1. Introduction**

This chapter presents a review of some important literature linking plant structure with function and/or as response to the environment in Brazilian neotropical savannah species, exemplifying mostly with Amaranthaceae and Melastomataceae and emphasizing the environment potential role in the development of such a structure.

Brazil is recognized as the 17th country in megadiversity of plants, with 17,630 endemic species among a total of 31,162 Angiosperms [1]. The focus in the Brazilian Cerrado Biome (Brazilian Neotropical Savannah) species is justified because this Biome is recognized as a World Priority Hotspot for Conservation, with more than 7,000 plant species and around 4,400 endemic plants [2-3].

The Brazilian Cerrado Biome is a tropical savannah-like ecosystem that occupies about 2 millions of km² (from 3-24° Latitude S and from 41-43° Longitude W), with a hot, semi-humid seasonal climate formed by a dry winter (from May to September) and a rainy summer (from October to April) [4-8]. Cerrado has a large variety of landscapes, from tall savannah woodland to low open grassland with no woody plants and wetlands, as palm swamps, supporting the richest flora among the world's savannahs-more than 7,000 native species of vascular plantswith high degree of endemism [3, 6]. The "cerrado" word is used to the typical vegetation, with grasses, herbs and 30-40% of woody plants [9-10] where trees and bushes display contorted trunk and branches with thick and fire-resistant bark, shiny coriaceous leaves and are usually recovered with dense indumentum [10]. According to [8], natural fires and anthropogenic fires coexisted for thousands of years and, together with the seasonality of

© 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.

rainfall and the poverty of nutrients in the soil are the responsible for the phytophysiognomy of Cerrado.

One of the first systematized studies of Cerrado Biome was the one done in Lagoa Santa, Minas Gerais State, around the year of 1892, by Warming [11], who described the place in aspects of soil, temperature, water precipitation and vegetation. When he [11] described the vegetation of flat grassland, he emphasized the thickness and toughness of Poaceae and Cyperaceae leaves and the abundance of perennial herbs or subshrubs with large lignified underground organs, multiple shoots growing from an underground stem and xeromorphic characteristics, as dense pilosity, coriaceous leaves positioned in acute angle and with reduced size. His [11] conclusion was that the dryness of the air, the harsh and dry clay soil and eventually, the fire occurrence, were responsible for these xeromorphic features of the plants.

Since then, a lot of work has been done to explain some contradictions such as the abundant flowering and budding and no signs of turgor loss during the dry season [10]. In [12] linked the plants physiognomy with the occurrence of fire and proposed an ecological classification of the Cerrado plants: plants which survive only during the rainy season, without any bud or leaf during the dry season (winter); grasses with superficial roots, like *Echinolaena inflexa* (Poir.) Chase and *Tristachya chrysothrix* Nees, which wither when the water is gone in the superficial soil; bushes and small trees with deep roots (up to 11 meters), usually green during all the dry season, which represent the typical vegetation. Leaves of the specimens observed [12] never closed completely their stomata: *Kielmeyera coriacea* Mart., *Annona coriacea* Mart., *Annona furfuracea* A.St.-Hil., *Palicourea rigida* Kunth, *Stryphnodendron obovatum* Benth.(syn=*S. barbati‐ mao*), *Didymopanax vinosum* (Cham. & Schltdl.) Marchal, *Byrsonima coccolobifolia* Kunth, *Cocos leiospatha* Barb. Rodr., *Echinolaena inflexa* (Poir.) Chase , *Andira laurifolia* Benth., *Anacardium pumilum* Walp., *Neea theifera* Oerst. and two species of *Erythroxylon* genus. In [13], perennial species with deep roots were associated to the ability of regenerating the aerial parts after a long dry season or after fire; these type of plants were designated as periodics, because they reduce or eliminate their leaves and branches during the winter, when the available water is rare at the soil surface.

The work [14] indicated that Cerrado soils are deep, with pH between 4,0 and 5,5 (acid) and connected the xeromorphic features in trees to nitrogen deficiency, because the studies done in Cerrado showed that water was not a limiting factor to these plants. In [15] it was added another important aspect to explain xeromorphic features in Cerrado plants: the high levels of aluminum would be a principal cause of mineral deficiency which would affect all Cerrado vegetation. Soils under Cerrado are usually poor, acid, well drained, deep, and show high levels of exchangeable aluminum [16-17]. The soil of the low grassland in the area of the old Experimental Station of hunting and fishing Emas (Pirassununga, São Paulo State) can be as deep as 20 meters and the groundwater is at 17-18 meters below the surface; only the first one to 1.5 meters dries during the winter and roots of at least one tree (*Andira* sp.) can reach the deepest groundwater; a shrub species, *Anacardium humile* A. St.-Hil., with aerial parts reaching 0.5 meters high, can have roots with over three times its shoot length [12]. The underground systems of roots and stems are so big in some species, such as in *Andira laurifolia* Benth., that in [11] it was called an "underground tree". Low concentration of nutrients in the leaves of native species is related with the low concentration of nutrients of the dystrophic soils [18] and the floristic composition and dominance of species is a reflection of it. Cerrado plants absorb significant amount of aluminum and when the leaf concentration is over 1,000 mg Kg-1 the species is referred as Al-accumulative [19]. It is still unknown if this amount of aluminum have any physiological or structural significance in the metabolism of the native plants [20], but the translocation of this element is showed by the presence of aluminum in the phloem and other metabolically active tissues of leaves and seeds and there are at least two plants which cannot survive in medium without aluminum: *Miconia albicans* (Sw.) Steud. (Melastomataceae) and *Vochysia thyrsoidea* Pohl (Vochysiaceae), woody species from Cerrado [18, 20]. Another curious aspect about Cerrado plants is that there are species that only live in calcareous or acid soils and there are also those which are indifferent to soil fertility [21].

The occurrence of wildfire is a common and important factor to be considered in the studies of this Biome vegetation, because it selects structural and physiological features of the plants and act as a renewal element [22]. In [13] were described some strategies which could help the perennial smaller plants to survive fire; during the dry season, some of them reduce or eliminate leaves and shoots and rely on their extensive underground system to re-sprout the aerial system after the dry season or after fire. As examples of fire resistance, in [13] were quoted the plants studied by [11], *Andropogon villosus f. apogynus* (Hack.) Henrard (Poaceae), *Scirpus warmingii* Boeckeler, *Scirpus paradoxus* (Spreng.) Boeckeler and *Rhynchospora warmin‐ gii* Boecheler (Cyperaceae), as well as *Aristida pallens* Cav., explaining that these plants have buds in the base of the aerial system well protected by some layers of sheath blades; the old ones are more external and will burn first, always protecting the newest ones and the internal buds.

An extensive review of the morphological and ecological studies is given in [10], whose author considered the Cerrado a great environment for scientific discussion and discuss the vegetation in a broader perspective, and in [23-24], whose author is more centered in anatomical aspects of Cerrado species.

Although the Cerrado Biome is a hotspot for the conservation of global biodiversity which shelters species fully adapted to survive under harsh conditions of soil and climate of this savannah-like environment [2], only 30% of its biodiversity is reasonably known [25]. Con‐ sidering that the open environments in this Biome are subject to high luminosity and seasonal variation in the rain, how do plants react to adapt themselves? Considering that fire is also a natural event during the dry season, is there any morphological and/or anatomical variations developed to survive? Considering that the groundwater level of some areas can vary in a high degree among the two seasons, how do plants manage to survive? Some of these questions will be addressed and data about it will be shown.

## **2. Methodology**

rainfall and the poverty of nutrients in the soil are the responsible for the phytophysiognomy

One of the first systematized studies of Cerrado Biome was the one done in Lagoa Santa, Minas Gerais State, around the year of 1892, by Warming [11], who described the place in aspects of soil, temperature, water precipitation and vegetation. When he [11] described the vegetation of flat grassland, he emphasized the thickness and toughness of Poaceae and Cyperaceae leaves and the abundance of perennial herbs or subshrubs with large lignified underground organs, multiple shoots growing from an underground stem and xeromorphic characteristics, as dense pilosity, coriaceous leaves positioned in acute angle and with reduced size. His [11] conclusion was that the dryness of the air, the harsh and dry clay soil and eventually, the fire occurrence,

Since then, a lot of work has been done to explain some contradictions such as the abundant flowering and budding and no signs of turgor loss during the dry season [10]. In [12] linked the plants physiognomy with the occurrence of fire and proposed an ecological classification of the Cerrado plants: plants which survive only during the rainy season, without any bud or leaf during the dry season (winter); grasses with superficial roots, like *Echinolaena inflexa* (Poir.) Chase and *Tristachya chrysothrix* Nees, which wither when the water is gone in the superficial soil; bushes and small trees with deep roots (up to 11 meters), usually green during all the dry season, which represent the typical vegetation. Leaves of the specimens observed [12] never closed completely their stomata: *Kielmeyera coriacea* Mart., *Annona coriacea* Mart., *Annona furfuracea* A.St.-Hil., *Palicourea rigida* Kunth, *Stryphnodendron obovatum* Benth.(syn=*S. barbati‐ mao*), *Didymopanax vinosum* (Cham. & Schltdl.) Marchal, *Byrsonima coccolobifolia* Kunth, *Cocos leiospatha* Barb. Rodr., *Echinolaena inflexa* (Poir.) Chase , *Andira laurifolia* Benth., *Anacardium pumilum* Walp., *Neea theifera* Oerst. and two species of *Erythroxylon* genus. In [13], perennial species with deep roots were associated to the ability of regenerating the aerial parts after a long dry season or after fire; these type of plants were designated as periodics, because they reduce or eliminate their leaves and branches during the winter, when the available water is

The work [14] indicated that Cerrado soils are deep, with pH between 4,0 and 5,5 (acid) and connected the xeromorphic features in trees to nitrogen deficiency, because the studies done in Cerrado showed that water was not a limiting factor to these plants. In [15] it was added another important aspect to explain xeromorphic features in Cerrado plants: the high levels of aluminum would be a principal cause of mineral deficiency which would affect all Cerrado vegetation. Soils under Cerrado are usually poor, acid, well drained, deep, and show high levels of exchangeable aluminum [16-17]. The soil of the low grassland in the area of the old Experimental Station of hunting and fishing Emas (Pirassununga, São Paulo State) can be as deep as 20 meters and the groundwater is at 17-18 meters below the surface; only the first one to 1.5 meters dries during the winter and roots of at least one tree (*Andira* sp.) can reach the deepest groundwater; a shrub species, *Anacardium humile* A. St.-Hil., with aerial parts reaching 0.5 meters high, can have roots with over three times its shoot length [12]. The underground systems of roots and stems are so big in some species, such as in *Andira laurifolia* Benth., that in [11] it was called an "underground tree". Low concentration of nutrients in the leaves of

were responsible for these xeromorphic features of the plants.

of Cerrado.

4082 Biodiversity in Ecosystems - Linking Structure and Function

rare at the soil surface.

In order to perform studies about morphology, anatomy or cell biology, as well as when the flora is been studied, it is usual to collect control or testimony material to guarantee species identification and further studies [26]. Vegetative and flowering plant branches are collected, pressed, dried and deposited as control material at some Brazilian Herbaria, following usual techniques [27]. The previous identification of the species is done with the aid of a stereomi‐ croscope, identification keys and specialized literature [28-38]. After previous identification, plant vouchers stay preserved to the study of a taxonomist specialized on the family and for future references, including of the place of occurrence, under a specific number of the principal collector, normally not only in one Herbarium (duplicates are usually distributed).

When studying the leaf anatomy, **histological** samples are obtained from visually healthy green and completely developed leaves, usually from 3rd to 5th node, of pre-identified species; samples can be or not submitted to different fixatives and paraffin embedding medium [39] before slicing it to be studied under an optical microscope (light microscopy). **Cell samples in tissue** for ultrastructural studies can be smaller pieces of the aimed organ submitted to a fixative and post-fixed in heavy metals in the dark, followed by in-block staining [40]. Later, plant pieces are dehydrated and slowly embedded in a harder medium (epoxy or epon resin), to be sliced for observation. Semi-thin sections can be obtained with an ultramicrotome using glass knives, stained and analyzed under the optical microscope in order to localize the cells in the tissues; ultra-thin sections of the same material are obtained with a diamond knife, collected in copper grids and analyzed under a transmission electron microscope (TEM), with or without any additional staining. To be studied under a scanning electron microscope (SEM), sections of the plant are also fixed and post-fixed as indicated for TEM analysis [40], with some modifications because of plant characteristics, but the use of control pieces [41] is necessary to avoid interpretation errors. After that, fixed pieces are dehydrated in ethanol or acetone solution and critical point dried in the proper device, attached to a stub and gold sputtered to be observed under SEM [40].

## **3. Morphology, histology and cell biology studies**

Morphological studies are used to identify and characterize the plant species in taxonomy, but it is also important to understand the behaviour of plants in nature. The first hint on the function is based on the external morphology of the organs. Different plant species can be very alike in habit and vegetative morphology, especially in some plant families as Amaranthaceae, which rely upon some flower details to be truthfully identified, demanding a highly special‐ ized work [33-38, 42-44].

Anatomy and cell biology studies aim to describe and understand the species organs and cells and help taxonomy to define affinities and parental relationships among plant groups. When combined with histochemical analysis they can lead to a better understanding of the cell, tissue or organ function and the interaction between the plant and its environment.

It is usual, in plant structural studies, to bear a description of the aimed plant or organs of interest, assuming that the function is already explained enough by the function of the organ in the plant or by previous researches. As results are subject to interpretation and there are some variables to be considered, it is not usual to connect the structure to the function. However, in the Cerrado species case, since the first studies there is an attempt to explain the structure and relate it to the unique environmental conditions, which was detailed in the introduction of this work, helping to give a broader significance to the structure.

identification and further studies [26]. Vegetative and flowering plant branches are collected, pressed, dried and deposited as control material at some Brazilian Herbaria, following usual techniques [27]. The previous identification of the species is done with the aid of a stereomi‐ croscope, identification keys and specialized literature [28-38]. After previous identification, plant vouchers stay preserved to the study of a taxonomist specialized on the family and for future references, including of the place of occurrence, under a specific number of the principal

When studying the leaf anatomy, **histological** samples are obtained from visually healthy green and completely developed leaves, usually from 3rd to 5th node, of pre-identified species; samples can be or not submitted to different fixatives and paraffin embedding medium [39] before slicing it to be studied under an optical microscope (light microscopy). **Cell samples in tissue** for ultrastructural studies can be smaller pieces of the aimed organ submitted to a fixative and post-fixed in heavy metals in the dark, followed by in-block staining [40]. Later, plant pieces are dehydrated and slowly embedded in a harder medium (epoxy or epon resin), to be sliced for observation. Semi-thin sections can be obtained with an ultramicrotome using glass knives, stained and analyzed under the optical microscope in order to localize the cells in the tissues; ultra-thin sections of the same material are obtained with a diamond knife, collected in copper grids and analyzed under a transmission electron microscope (TEM), with or without any additional staining. To be studied under a scanning electron microscope (SEM), sections of the plant are also fixed and post-fixed as indicated for TEM analysis [40], with some modifications because of plant characteristics, but the use of control pieces [41] is necessary to avoid interpretation errors. After that, fixed pieces are dehydrated in ethanol or acetone solution and critical point dried in the proper device, attached to a stub and gold sputtered to

Morphological studies are used to identify and characterize the plant species in taxonomy, but it is also important to understand the behaviour of plants in nature. The first hint on the function is based on the external morphology of the organs. Different plant species can be very alike in habit and vegetative morphology, especially in some plant families as Amaranthaceae, which rely upon some flower details to be truthfully identified, demanding a highly special‐

Anatomy and cell biology studies aim to describe and understand the species organs and cells and help taxonomy to define affinities and parental relationships among plant groups. When combined with histochemical analysis they can lead to a better understanding of the cell, tissue

It is usual, in plant structural studies, to bear a description of the aimed plant or organs of interest, assuming that the function is already explained enough by the function of the organ in the plant or by previous researches. As results are subject to interpretation and there are some variables to be considered, it is not usual to connect the structure to the function.

or organ function and the interaction between the plant and its environment.

collector, normally not only in one Herbarium (duplicates are usually distributed).

be observed under SEM [40].

4104 Biodiversity in Ecosystems - Linking Structure and Function

ized work [33-38, 42-44].

**3. Morphology, histology and cell biology studies**

Studying the so called xeromorphic features of three leaves, [14] concluded that they could be explained by the soil oligotrophic conditions, given raise to the theory of oligotrophic sclero‐ morphism: the mineral elements deficiency would be the main responsible for the plant characteristics, by limiting its grow; the carbohydrate accumulation is then converted in deposits of thick cuticle, thicker cell walls, wax deposits over the epidermis and other sclero‐ morphic features. High level of aluminum in Cerrado soils, another cause for the oligotrophic scleromorphism [15] is considered the main responsible for the acidity of Cerrado soils [45]. Through the study of eleven Cerrado plants, [46] it was indicated the constant presence of fungi over its leaves, mostly on species without epicuticular wax, and connected this outermost layer over the cuticle layer to environmental adaptation, as protection against any fungus hypha.

Sclerenchymatous elements, fibers and sclereids are distinctive structural features in vegeta‐ tive organs of Cerrado plants, and the presence of gelatinous fibers is frequent, associated or not with the tension wood; besides, it is also constant the impregnation of silica and siliceous bodies, not only in Poaceae and Cyperaceae species, but also in leaf and stem epidermis, roots and xylopodium of *Brasilia sickii* G. M. Barroso (Asteraceae) [23-24]. In epidermis, [24] silica is connected to the protection against excessive transpiration and as a defense mechanism against fungi. In [24], author also explained why the aperture or closure of stomata can be slower in Cerrado plants: it would be due to the thickening of the guard cells walls of a stoma, which can be impregnated with lignin, as in *Ouratea spectabilis* (Mart. ex Engl.) Engl. or have silica incorporated, like in *Esterhazya splendida* J. C. Mikan, *B. sickii* and *Casearia grandiflora* Cambess.

Amaranthaceae family is considered a good representative of the herbs and subshrubs of Cerrado due to its morphology and adaptations that promote survival in adverse conditions (drought and fire), such as tuberous or woody roots, xylopodium, herbaceous or subshrub habit, dense pubescence in aerial portions, senescence of shoots and leaves during the driest season, dependence on rain or fire to re-sprout and/or flowering, fruiting followed by wind dispersion, thick cuticle on epidermis and C4 photosynthetic metabolism [37, 47-48]. The knowledge of the reproductive structures in Amaranthaceae Brazilian species is mostly restricted to the obtained during floristic survey and with taxonomic purpose, with few additional studies of reproductive structures, such as [49], who studied the flower vascular pattern in *Pfaffia jubata* Mart., *Gomphrena macrocephala* A. St.-Hil. and *Froelichia interrupta* (L.) Moq. and [50], with the study of pollen from Cerrado species, helping to understand the phenology of them through the analysis of herbarium species.

In this section, some morphological, histological or cellular aspects of reproductive and vegetative (aerial and underground) organs will be exemplified, discussing the aspects related to the environment where these plants grow and survive and to the function in the plant species, whenever possible.

### **3.1. Reproductive organs — Flower, fruits and seeds**

Amaranthaceae flowers are generally small and densely clustered in terminal or axillary inflorescences (figure 1), pollinated by the wind or by insects, with self-pollinating or out‐ crossing [51]. Due to the hairy perianth, small and dry fruits or seeds, the dispersion is usually done by wind or water [51]. In some genus, small seeds fall from the parent plant and germinate only when the site is again disturbed; seeds can be, also, eaten and dispersed by browsing animals [51].

**Figure 1.** *Pfaffia jubata* Mart. **a**: habit; **b**: median bract; **c:** lateral bract; **d-e:** sepals; **f**: staminal tube; **g**: ovary (*Hatschbach et al. 53625*, MBM). Reproduced from [37] with permission of Hoehnea publisher. The species was considered a good representative of Amaranthaceae family: habit from herb to subshrub, 0.10-0.20 m high, stems erect, densely villous and woody root. Leaves have the upper side densely villous and lower side tomentose. Inflorescence is a spike, isolat‐ ed, simple, terminal, with ferruginous trichomes.

Brazilian species of *Celosia, Chamissoa* and *Amaranthus* have circumscissile capsule fruits, with only one seed in the two last genera and more seeds in the first one; capsules are surrounded by the perianth and parts of the androecium and gynoecium, except in *Amaranthus* where the filaments are free and there is no staminate tube [52]. Dehiscence can be median (*Amaran‐ thus*) or semi basal (*Celosia*) and dispersal is probably done by autochory [52], although [53] considers the accidental endozoochory more probable in *Amaranthus* case, because ruminants usually eat *Amaranthus* inflorescences.

**3.1. Reproductive organs — Flower, fruits and seeds**

4126 Biodiversity in Ecosystems - Linking Structure and Function

animals [51].

Amaranthaceae flowers are generally small and densely clustered in terminal or axillary inflorescences (figure 1), pollinated by the wind or by insects, with self-pollinating or out‐ crossing [51]. Due to the hairy perianth, small and dry fruits or seeds, the dispersion is usually done by wind or water [51]. In some genus, small seeds fall from the parent plant and germinate only when the site is again disturbed; seeds can be, also, eaten and dispersed by browsing

**Figure 1.** *Pfaffia jubata* Mart. **a**: habit; **b**: median bract; **c:** lateral bract; **d-e:** sepals; **f**: staminal tube; **g**: ovary (*Hatschbach et al. 53625*, MBM). Reproduced from [37] with permission of Hoehnea publisher. The species was considered a good representative of Amaranthaceae family: habit from herb to subshrub, 0.10-0.20 m high, stems erect, densely villous and woody root. Leaves have the upper side densely villous and lower side tomentose. Inflorescence is a spike, isolat‐

ed, simple, terminal, with ferruginous trichomes.

Fruits of *Alternanthera, Pfaffia, Gomphrena, Blutaparon, Achyranthes, Cyathula* and *Pseudoplanta‐ go* are one-seeded capsules with two valves included in the perianth sepals which are glabrous to hairy or spine-like; these fruits can carry part of the androecium and gynoecium and sometimes the perianth displays external bristle tufts or modified bracts [34-35, 52]. Wind seems to be responsible for the dispersal of *Alternanthera, Pfaffia, Gomphrena* and *Blutaparon* fruits because of the hairiness of the perianth, which presents long trichomes; species of *Froelichia, Froelichiella*, *Pfaffia* and *Gomphrena* genera from open grassland have their fruit easily dispersed by the wind [34-35, 52].

In [54] wind dispersal of fruits in species which occur in Cerrado regions that were affected by fires, mostly *Gomphrena macrocephala* associating the natural fire with the easier dispersal of its fruits and seed germination. The passage of fire burns grasses and help dispersal of the *G. macrocephala*, *G. pohlii* Moq. and *G. virgata* Mart. fruits; fire also promotes the dehiscence of the fruits, leaving the seeds nearer to the soil [42, 55]. The maturation and dispersal of fruits is exemplified in *G. arborescens* L.f. (figure 2), a native Cerrado plant which behaves the same way of *G. macrochepala* [54]: the inflorescence opens for pollination and closes after that due to a growth of its bracts for the maturation of the fruits; after that, the shoot inclines towards the soil and the inflorescence structure reopens to release the dispersal units in the soil, formed by the seed and parts of the perianth, until the wind carries it. The same phenomenon was observed in *Pfaffia argyrea* Pedersen, *P. cipoana* Marchior. et al., *P. denudata* (Moq.) Kuntze, *P. elata* R. E. Fr., *P. hirtula* Mart., *P. jubata* Mart. *P. minarum* Pedersen, *P. rupestris* Marchior. et al., *P. sarcophylla* Pedersen, *P. siqueiriana* Marchior. et al, *P. townsendii* Pedersen, *P. tuberculosa* Pedersen, *P. velutina* Mart. and *Froelichiella grisea* (Lopr.) R.E.Fr. all Cerrado species which occur in areas subject to burning [37, 55]. *Froelichia* has one-seeded nutlet involved by parts of the gynoecium and androecium, partially because of the connated perianth and presents a wing structure densely hairy which favours the wind dispersal [34, 52].

Although *Alternanthera* and *Blutaparon* genera fruits are usually wind dispersed, *Alternanthera pungens* Kunth have its perianth highly modified, presenting uneven sepals, with the outer two sharply pointed, which can help its adhesiveness in animal skin or fur to be dispersed [52]. The same occurs with *Achyranthes* and *Cyathula* genera, which fruits are dispersed by animals through adhesiveness structures [53]. *Achyranthes* two perianth lateral bracts are thorn-like, the same as in *Pseudoplantago friesii* Suess [52]. *Cyathula* have a set of uncinate bristles which can be considered sterile flowers and play a special function in helping the fruit dispersal attached to skin or fur of animals, a phenomenon called epizoochory [52].

**Figure 2.** Fruits of *Gomphrena arborescens* L.f. are dispersed by the wind. The inflorescence opens for pollination (**A**) and closes after due to a growth of its bracts (**B**) for the maturation of the fruits; after that, the shoot (black arrow) inclines towards the soil (**C**) and the infructescence structure reopens to release the diaspores (white arrow in **C**, **D**, E) in the soil, formed by one seed (red arrow in **E**) and parts of the perianth (blue arrow in **E**), until the wind carries it. **Scale bar**s: A-E: 2 cm.

Amaranthaceae species are well adapted to Cerrado environment and some species display different strategies to survive during the markedly seasonal climate of the Cerrado Biome [47]. Using only data obtained about perennial species, an interesting case is the aerial life cycle of *Froelichiella grisea*, which is endemic of the rocky fields of Chapada dos Veadeiros, Goiás State [34]; this species was registered during the onset of the flowering stage in the field, almost after two years of searching for it, only 20 days after a fire that burned out the vegetation (in August, during the dry season); *Gomphrena lanigera* Pohl ex Moq. also was found only at the same day, at the fruiting stage, revealing an even faster life cycle of the aerial parts [48, 57]. On the other hand, the species *Pfaffia townsendii* and *G. hermogenesii* J.C. Siqueira were found in the same region all year round; whilst the first one was always bearing flowers (it is a well-branched shrub that stands out in the middle of the rocks), the second one was usually found in the vegetative stage, more or less hidden among the surrounding Gramineae (=Poaceae) and Cyperaceae; only after the fire grazed all the grasses of the area, *G. hermogenesii* re-sprouted its aerial organs and was found in the onset of the flowering stage [48, 57]. Another species, *G. arborescens* is usually found at bloom time at RECOR/IBGE and at the Olympic Center of Universidade de Brasília, in Brasília, Federal District, during the rainy station (from November to April) and at vegetative stage from August to October (during winter); in this 0.5 meter high species, leaves were always attached to the shoot at the same time as the flowers and fruits, although in the end of the fruiting stage, some or all the shoots bearing fruits can dry out, in order to release the fruits [58]. Another species, *G. virgata*, found in the same locations than *G. arborescens*, reaches 2.0 m high and is found at vegetative stage from March to July (middle of the dry season) and fruiting goes until September (end of the winter); in the beginning of the bloom period, leaves enter in a senescence process and are detached from the shoot; after dispersing seeds, its aerial parts also dry out, re-sprouting around March (near the end of rainy season) [58]. Found only at the Olympic Center, *G. pohlii* develops its aerial organs up to 1.8 m high from August to November, starting the blooming period in December and finishing fruit dispersion around April, drying out its aerial portions during the winter [58].

As an agent of perturbation in the vegetation of Cerrado, fire can produce variable effects in the flowering and fruiting patterns: whilst flowering is more intense in the herbaceous layer after a fire breaks out, the same phenophases are not affected in trees and shrubs [59]. A thicker pericarp in dry fruits may provide greater protection for seeds, acting as a barrier against high external temperatures, such as in *Kielmeyera coriacea* winged seeds inside dry fruits [60]. Fire increases the dehiscence in anemochoric species [54, 60].

Would be necessary more research in order to understand not only the structures of repro‐ ductive organs, but also describe the relation among flowers and its pollinators in Cerrado species and to understand the phenology of the species, which have different strategies to survive natural and eventual events, since dropping leaves during the flowering/fruiting phase, recycling all aerial parts after completing the fruiting phase, among others.

### **3.2. Vegetative structures of Amaranthaceae and Melastomataceae species**

During the study of Brazilian Amaranthaceae species some morphological characteristics stood out in Cerrado species: well developed subterranean systems with xylopodium, high level of endemism and hairy stem, leaves, flowers and fruits [34, 37, 47, 56], which indicates adaptations of these plants to the environment. Xeromorphy and scleromorphy are common features in leaves of Cerrado species [61]. Although the two terms describe similar morphology results, a xeromorphic plant is adapted to withstand drought and a scleromorphic plant is the result of other limiting factors to its growth instead of water, for instance a restricted nutrient intake [14] or aluminum toxicity [15]. Some aspects of the plants can be genetically determined, developed as a selective advantage, such as the development of xylopodia in *Clitoria guianen‐ sis* Benth. and *Calliandra dysantha* Benth. [62], both Cerrado plants.

Scleromorphism is precocious in all organs, especially the vegetative ones [24], which is why the most aimed organs to study structure are leaves, stem and roots, although the identification of a plant is usually obtained by the study of its reproductive organs. Field observations, morphological, anatomical and cellular data on aerial structures of Amaranthaceae and Melastomataceae species will be emphasized in order to improve the understanding of the surviving strategies used by some species of these families [35, 47, 61].

### *3.2.1. Leaf structure*

**Figure 2.** Fruits of *Gomphrena arborescens* L.f. are dispersed by the wind. The inflorescence opens for pollination (**A**) and closes after due to a growth of its bracts (**B**) for the maturation of the fruits; after that, the shoot (black arrow) inclines towards the soil (**C**) and the infructescence structure reopens to release the diaspores (white arrow in **C**, **D**, E) in the soil, formed by one seed (red arrow in **E**) and parts of the perianth (blue arrow in **E**), until the wind carries it. **Scale**

Amaranthaceae species are well adapted to Cerrado environment and some species display different strategies to survive during the markedly seasonal climate of the Cerrado Biome [47]. Using only data obtained about perennial species, an interesting case is the aerial life cycle of *Froelichiella grisea*, which is endemic of the rocky fields of Chapada dos Veadeiros, Goiás State [34]; this species was registered during the onset of the flowering stage in the field, almost after two years of searching for it, only 20 days after a fire that burned out the vegetation (in August, during the dry season); *Gomphrena lanigera* Pohl ex Moq. also was found only at the same day, at the fruiting stage, revealing an even faster life cycle of the aerial parts [48, 57]. On the other hand, the species *Pfaffia townsendii* and *G. hermogenesii* J.C. Siqueira were found in the same region all year round; whilst the first one was always bearing flowers (it is a well-branched shrub that stands out in the middle of the rocks), the second one was usually found in the vegetative stage, more or less hidden among the surrounding Gramineae (=Poaceae) and Cyperaceae; only after the fire grazed all the grasses of the area, *G. hermogenesii* re-sprouted its aerial organs and was found in the onset of the flowering stage [48, 57]. Another species, *G. arborescens* is usually found at bloom time at RECOR/IBGE and at the Olympic Center of Universidade de Brasília, in Brasília, Federal District, during the rainy station (from November to April) and at vegetative stage from August to October (during winter); in this 0.5 meter high species, leaves were always attached to the shoot at the same time as the flowers and fruits, although in the end of the fruiting stage, some or all the shoots bearing fruits can dry out, in order to release the fruits [58]. Another species, *G. virgata*, found in the same locations than *G. arborescens*, reaches 2.0 m high and is found at vegetative stage from March to July (middle of the dry season) and fruiting goes until September (end of the winter); in the beginning of the bloom period, leaves enter in a senescence process and are detached from the shoot; after dispersing seeds, its aerial parts also dry out, re-sprouting around March (near the end of rainy

**bar**s: A-E: 2 cm.

4148 Biodiversity in Ecosystems - Linking Structure and Function

Leaf anatomical traits are useful to infer adaptations to a specific environment [63-64] and are good predictors of performance [65] because of their common and strong relation‐ ships with functional parameters such as photosynthesis, leaf nutrient content and radial growth [66-69]. Studies with *Macairea radula* (Bonpl.) DC. and *Trembleya parviflora* (D. Don) Cogn. (Melastomataceae) showed quantitative anatomical plasticity in different environ‐ ments [61]: plants on open flooded area of palm swamp had significantly smaller values of specific leaf area and significantly higher values of leaf mesophyll thickness when

compared with leaves partially shaded on non-flooded soil of the Cerrado *sensu stricto,* indicating that the former are smaller and thicker than the latter. Quantitative plasticity may also appear in the leaf flush as an influence of seasonality. Leaves which flushed during dry or wet season, in *Gochnatia polymorpha* (Less.) Cabrera (Asteraceae), showed statistical‐ ly significant differences in the cuticle, mesophyll and abaxial epidermis thickness, stomatal size, stomata and trichomes density, indicating a probable water-status control and an adaptation to seasonality of rainfall in the Cerrado [70]. Furthermore, in [70] the authors emphasized a positive correlation between the increase in the number of trichomes and stomata density in the dry season, and suggested that this relationship would promote a highest control over stomatal conductance and transpiration.

Plants of different physiognomy of Cerrado showed that leaves are hypostomatic in most of the species, whilst there are also amphistomatic species [61, 71-73]. Stomata only on the abaxial surface are an advantageous trait for plants on low relative humidity and high temperature environment because it could reduce the loss of water vapour as the temperature on the abaxial side of the leaf is lower [74-75]. On the other hand, stomata on both surfaces makes it easier the intercellular diffusion of CO2 in mesophyll of thicker leaves [76] and amphistomatic leaves are characteristics of plants living in high-light environments and with high photosynthetic capacity [74]. The same species can display stomata on both or only on one leaf surface in response to the light intensity under which they are grown, which can be related with leaf thickness, photosynthetic capacity and maximum stomatal conductance [75]. Leaves of the same species which were grown on high-light environment can be amphistomatous, thicker and with higher rates of photosynthesis, stomatal conductance for CO2 uptake and loss of water vapour, whilst leaves of plants grown under low-light intensity are hypostomatous and show lower values for the same variables [74-76], demonstrating the plasticity of this feature and its influence on the hydric balance and gas exchange of the plants.

Ericaceae species *Gaylussacia brasiliensis* (Spreng.) Meisn. (figure 3 C and 3E), and species of Myrtaceae [77] and Melastomataceae [61] of cerrado *sensu stricto* and palm swamps have epidermis cells that present simultaneously evaginations of protoplasm and invaginations of the external periclinal cell wall (figure 3A-D). In frontal view the cell walls are sinuous and evagination points are usually shinier (figure 3E-F). Although the function of this feature is unproven, similar structures were found in *Drosera* [78] and named miniature papillose processes, which would be functioning as sensors for mechanical or chemical stimuli.

Emergences are structures of mixed protoderm and ground meristem origin, and are generally found in Melastomataceae leaves (figure 4). These structures are related with the vascular system and ultrastructural and histochemical analyses of the cell walls revealed micro channels permeable to water and nutrients, indicating that these structures are related with the transport of substances and may absorb or exude solutions [61, 79-80].

Phenolic compounds are regarded as protective against the incidence of UV-B radiation and could act as filters or antioxidants [81-84]. These secondary metabolites are also considered inhibitors of herbivory which, along with radiation, function as a stimulator in the biosynthesis of phenolic compounds [85]. Phenolic compounds are very common in leaves of Cerrado plants of diverse physiognomy such as palm swamp, a flooded and open soil, in a dry forest Plant Structure in the Brazilian Neotropical Savannah Species 11 http://dx.doi.org/ 10.5772/59066 417

compared with leaves partially shaded on non-flooded soil of the Cerrado *sensu stricto,* indicating that the former are smaller and thicker than the latter. Quantitative plasticity may also appear in the leaf flush as an influence of seasonality. Leaves which flushed during dry or wet season, in *Gochnatia polymorpha* (Less.) Cabrera (Asteraceae), showed statistical‐ ly significant differences in the cuticle, mesophyll and abaxial epidermis thickness, stomatal size, stomata and trichomes density, indicating a probable water-status control and an adaptation to seasonality of rainfall in the Cerrado [70]. Furthermore, in [70] the authors emphasized a positive correlation between the increase in the number of trichomes and stomata density in the dry season, and suggested that this relationship would promote a

Plants of different physiognomy of Cerrado showed that leaves are hypostomatic in most of the species, whilst there are also amphistomatic species [61, 71-73]. Stomata only on the abaxial surface are an advantageous trait for plants on low relative humidity and high temperature environment because it could reduce the loss of water vapour as the temperature on the abaxial side of the leaf is lower [74-75]. On the other hand, stomata on both surfaces makes it easier the intercellular diffusion of CO2 in mesophyll of thicker leaves [76] and amphistomatic leaves are characteristics of plants living in high-light environments and with high photosynthetic capacity [74]. The same species can display stomata on both or only on one leaf surface in response to the light intensity under which they are grown, which can be related with leaf thickness, photosynthetic capacity and maximum stomatal conductance [75]. Leaves of the same species which were grown on high-light environment can be amphistomatous, thicker and with higher rates of photosynthesis, stomatal conductance for CO2 uptake and loss of water vapour, whilst leaves of plants grown under low-light intensity are hypostomatous and show lower values for the same variables [74-76], demonstrating the plasticity of this feature and its

Ericaceae species *Gaylussacia brasiliensis* (Spreng.) Meisn. (figure 3 C and 3E), and species of Myrtaceae [77] and Melastomataceae [61] of cerrado *sensu stricto* and palm swamps have epidermis cells that present simultaneously evaginations of protoplasm and invaginations of the external periclinal cell wall (figure 3A-D). In frontal view the cell walls are sinuous and evagination points are usually shinier (figure 3E-F). Although the function of this feature is unproven, similar structures were found in *Drosera* [78] and named miniature papillose

processes, which would be functioning as sensors for mechanical or chemical stimuli.

Emergences are structures of mixed protoderm and ground meristem origin, and are generally found in Melastomataceae leaves (figure 4). These structures are related with the vascular system and ultrastructural and histochemical analyses of the cell walls revealed micro channels permeable to water and nutrients, indicating that these structures are related with the transport

Phenolic compounds are regarded as protective against the incidence of UV-B radiation and could act as filters or antioxidants [81-84]. These secondary metabolites are also considered inhibitors of herbivory which, along with radiation, function as a stimulator in the biosynthesis of phenolic compounds [85]. Phenolic compounds are very common in leaves of Cerrado plants of diverse physiognomy such as palm swamp, a flooded and open soil, in a dry forest

highest control over stomatal conductance and transpiration.

416 10 Biodiversity in Ecosystems - Linking Structure and Function

influence on the hydric balance and gas exchange of the plants.

of substances and may absorb or exude solutions [61, 79-80].

**Figure 3.** Leaf epidermis with evaginations and invaginations of external periclinal cell wall. **A-D:** cross section; **E-F:** frontal view. **A:** *Myrcia cordifolia* DC. (Myrtaceae). **B:** *Gomidesia pubescens (DC.) D. Legrand* (Myrtaceae). **C, E:** *Gaylussacia brasiliensis* (Spreng.) Meisn. (Ericaceae). **D, F**: *Lavoisiera bergii* Cogn. (Melastomataceae). Arrow show evagination points in dissociated of epidermal cells (E) and shiny dots in frontal view (F). **Scale bars:** A-D: 20 µm, E-F: 50 µm.

on limestone outcrops or in open areas of Cerrado [26, 61, 73], where the leaves are exposed to high irradiance and high herbivory or fungi infection.

Although the photosynthesis is highly dependent on structural and ultrastructural coordina‐ tion in leaves, the environment is responsible for the relative abundance of a determined subtype of the C4 pathway [86]. The C4 photosynthesis pathway evolved in a great diversity of Kranz anatomy forms, biochemical routes and dimorphism of chloroplast ultrastructure [87-89] and is broadly dispersed among Angiospermae plants, including in the Amaranthaceae family [90-91].

The parenchyma bundle sheath and the mesophyll cell arrangement are the most usual anatomic pattern to determine the C4 photosynthesis pathway [92]. However, the high degree

**Figure 4.** Leaf emergences in Melastomataceae. **A**: Non-glandular emergence (arrow) in margin of *Lavoisiera bergii* Cogn. **B**: Non-glandular emergence (arrow) in adaxial surface of *Macairea radula (*Bonpl.) DC. **C**: Non-glandular (ar‐ row) and glandular (arrowhead) emergences in abaxial surface of *Macairea radula* **Scale bars**: 100 µm

of evolutionary convergence does not guarantee a unique pattern at biochemical or cellular and subcellular levels [86]. The structural type of leaves (Kranz or non-Kranz), the chloroplasts position, the absence or presence of stacked disks (grana) in the thylakoid membranes of chloroplasts and the number of mitochondria are important characteristics to know the photosynthetic metabolism of a plant species [89, 93]. At ultrastructural level, number and concentration of chloroplasts, mitochondria and peroxisomes in the bundle sheath cells are the most reliable criteria to determine the photosynthetic capacity of a plant [94]. However, recent studies showed that the C4 photosynthesis can operate by dimorphic chloroplasts located in different regions of the same cell, as demonstrated in *Orcuttia* sp. and in *Borszczowia aralocaspica* Bunge and *Bienertia cycloptera* Bunge [87, 95-97]. This way, the ultrastructural study of leaves can be a key element to understand the plant metabolism.

Since the first works, leaf anatomical studies done in Brazilian Amaranthaceae species showed a well-developed vascular bundle in *Gomphrena* and *Froelichia* genera, but not in *Alternan‐* *thera* and *Pfaffia* genera [26, 98-101]*.* Intracellular studies are rarer [56, 102-103]. In [103] it is showed a gradual change in the stacked thylakoids of dimorphic chloroplasts in *Gomphrena macrocephala, G. prostrata* Desf. and *G. decipiens* Seub. connecting it with the NADP-ME subtype of C4 photosynthesis pathway, which was the same preliminarily observation done in *G. arborescens* [56]. *Pfaffia jubata* displays the same type of chloroplasts in different leaf tissues, indicating the operation of the C3 pathway of photosynthesis [102]. In [103] are described dimorphic chloroplasts in *G. scapigera* Mart. leaves which ultrastructure was considered compatible with NADP-ME subtype of C4 photosynthesis. These results are coherent with the ones showed in Australian *Gomphrena* species: *G. celosioides* Mart., *G. globosa* L., *G. conica* (R. Br.) Spreng., *G. brachystylis* F. Muell., *G. brownie* Moq., *G. flaccida* R. Br., *G. canescens* R. Br. [93].

Leaves of 13 Amaranthaceae species-*Alternanthera brasiliana* (L.) Kuntze, *A. paronychioides* St.- Hil, *Froelichiella grisea*, *Gomphrena arborescens, G. hermogenesii, G. lanigera, G. pohlii, G. prostrata, G. virgata, Hebanthe eriantha* (Poir.) Pedersen, *Pfaffia glomerata* (Spreng.) Pedersen, *P. gnapha‐ loides* (L.f.) Mart. and *P. townsendii* were studied in order to understand their metabolic pathway of photosynthesis [47, 56]. All the species are native to Brazil and occur in the Cerrado Biome; six of them are endemic to Brazil and one is endemic to the Brazilian Cerrado Biome [38, 48]. All leaves are hairy (trichomes are rarer in *Alternanthera* species), amphistomatic (except *Pfaffia townsendii*), have one cell thick epidermis with stomata more or less leveled to the surrounding epidermal cells and dorsiventral mesophyll (except *F. grisea*, which has isobilateral mesophyll) with collateral bundles. All six *Gomphrena* species have thick-walled parenchymatous bundle sheath and organelles ultrastructure compatible with the operation of NADP-ME subtype of C4 pathway of photosynthesis. Whilst *G. pohlii* and *G. virgata* have a more classical type of Kranz anatomy (figure 5) [47], *G. arborescens*, *G. hermogenesii*, *G. lani‐ gera* and *G. prostrata* have the same type of Kranz anatomy found in most *Gomphrena* species [93, 98, 102-105], classified as "*Gomphrena* type" [89] but all share dimorphic chloroplasts (figure 6) [47]. *Alternanthera* species presented variable anatomy, with organelles positioned towards the vascular bundle in *A. paronychioides* and in the peripheral position in *A. brasili‐ ana* bundle sheath cells. The first *Alternanthera* species was characterized as a C3-C4 intermedi‐ ate species [106] based on its leaf anatomy, CO2 compensation point and activity of key photosynthetic enzymes, but the authors did not mention stomata on both epidermis leaf surfaces, which is considered another fundamental feature to lower the CO2 compensation point [74]. Thus, the position of organelles in bundle sheath cells can be a key element in determining the intermediary metabolic type in *Alternanthera* species (figure 7) [47]. *Froeli‐ chiella*, *Hebanthe* and *Pfaffia* species have leaf anatomy and ultrastructure compatible with C3 metabolism [47]. Chloroplasts of the Kranz cells of C4 plants usually have no grana, present little PSII activity and a larger amount of starch [107] whilst, in C3 plants, the palisade cells show a larger amount of starch than the ones of the spongy parenchyma [108].

of evolutionary convergence does not guarantee a unique pattern at biochemical or cellular and subcellular levels [86]. The structural type of leaves (Kranz or non-Kranz), the chloroplasts position, the absence or presence of stacked disks (grana) in the thylakoid membranes of chloroplasts and the number of mitochondria are important characteristics to know the photosynthetic metabolism of a plant species [89, 93]. At ultrastructural level, number and concentration of chloroplasts, mitochondria and peroxisomes in the bundle sheath cells are the most reliable criteria to determine the photosynthetic capacity of a plant [94]. However, recent studies showed that the C4 photosynthesis can operate by dimorphic chloroplasts located in different regions of the same cell, as demonstrated in *Orcuttia* sp. and in *Borszczowia aralocaspica* Bunge and *Bienertia cycloptera* Bunge [87, 95-97]. This way, the ultrastructural study

**Figure 4.** Leaf emergences in Melastomataceae. **A**: Non-glandular emergence (arrow) in margin of *Lavoisiera bergii* Cogn. **B**: Non-glandular emergence (arrow) in adaxial surface of *Macairea radula (*Bonpl.) DC. **C**: Non-glandular (ar‐

row) and glandular (arrowhead) emergences in abaxial surface of *Macairea radula* **Scale bars**: 100 µm

418 12 Biodiversity in Ecosystems - Linking Structure and Function

Since the first works, leaf anatomical studies done in Brazilian Amaranthaceae species showed a well-developed vascular bundle in *Gomphrena* and *Froelichia* genera, but not in *Alternan‐*

of leaves can be a key element to understand the plant metabolism.

If the evolution of C4 metabolism is associated to the weather and ecological disturbance, is it possible to link some structural changes in leaves of Cerrado plant species to these evolution factors? The evolution of C4 metabolism in these Amaranthaceae species can be related to the development of amphistomatic leaves, associated with increased leaf thickness, thicker bundle sheath cell walls, fast lifespan of the aerial system and well-developed gemmiferous under‐ ground system as adaptation to an open shinny environment with seasonal rain and oligotro‐ phic acid soil, at least partially. Species' survival in adverse environments can be achieved by the operation of C4 photosynthesis and carbon accumulation [109], which is associated with high photosynthesis rate [74]; the accumulated carbon is stored and protected in the under‐ ground organs, explaining the energy source to re-sprout of Cerrado species. Although in [92] trichomes are believed to affect the gas exchange and leaf temperature, reducing the light incidence, *Gomphrena arborescens* developed a translucid tissue surrounding the large trichome bases, which allows the light to reach internal photosynthetic tissue [26], indicating that its trichomes can be more a restriction to herbivory than to reduce leaf temperature or light incidence, the same way as in *G. pohlii* and *G. virgata* [58]; another aspect shared by all Amaranthaceae Cerrado´ species is the constant presence of calcium oxalate druses inside leaves and shoots [26, 47, 57-58], which is considered a highly specialized way of sequester and immobilise calcium [110].

**Figure 5.** *Gomphrena pohlii* Moq. (A) and *G. virgata* Mart. (**B**) (Amaranthaceae) leaves in cross sections. Red arrow indi‐ cates bundle sheath cells with organelles positioned near the inner cell walls, towards the vascular bundle. **Scale bars:** 50 µm.

Large plastoglobuli were found in chloroplasts *F. grisea*, *G. arborescens*, *G. hermogenesii*, *G. pohlii* and *G. virgata*. According to [111], plastoglobule consists of an outer lipid monolayer containing neutral lipids and proteins/enzymes related to lipid metabolism; its dimensions vary from 30 nm to several micrometers. Plastoglobuli shape and size change during devel‐ opment and plastid differentiation, and under stress conditions, clustering of large groups of connected plastoglobuli were observed [111-112]. Lipid and protein storage inside the chloroplasts could support plants' fatty acid regulation, unsaturation and mobilization in response to the stress caused by biotic interactions, especially due to the presence of plasto‐ globulin among its proteins [111, 113]. Although higher plastoglobuli content in chloroplasts could be linked to plant senescence [114], this may not be the case of these Amaranthaceae plants because all leaf samples were visually healthy and green when collected. In *G. hermo‐ genesii* leaves which were infected for some sort of septate endophytic organism (figure 8),

ground system as adaptation to an open shinny environment with seasonal rain and oligotro‐ phic acid soil, at least partially. Species' survival in adverse environments can be achieved by the operation of C4 photosynthesis and carbon accumulation [109], which is associated with high photosynthesis rate [74]; the accumulated carbon is stored and protected in the under‐ ground organs, explaining the energy source to re-sprout of Cerrado species. Although in [92] trichomes are believed to affect the gas exchange and leaf temperature, reducing the light incidence, *Gomphrena arborescens* developed a translucid tissue surrounding the large trichome bases, which allows the light to reach internal photosynthetic tissue [26], indicating that its trichomes can be more a restriction to herbivory than to reduce leaf temperature or light incidence, the same way as in *G. pohlii* and *G. virgata* [58]; another aspect shared by all Amaranthaceae Cerrado´ species is the constant presence of calcium oxalate druses inside leaves and shoots [26, 47, 57-58], which is considered a highly specialized way of sequester

**Figure 5.** *Gomphrena pohlii* Moq. (A) and *G. virgata* Mart. (**B**) (Amaranthaceae) leaves in cross sections. Red arrow indi‐ cates bundle sheath cells with organelles positioned near the inner cell walls, towards the vascular bundle. **Scale bars:**

Large plastoglobuli were found in chloroplasts *F. grisea*, *G. arborescens*, *G. hermogenesii*, *G. pohlii* and *G. virgata*. According to [111], plastoglobule consists of an outer lipid monolayer containing neutral lipids and proteins/enzymes related to lipid metabolism; its dimensions vary from 30 nm to several micrometers. Plastoglobuli shape and size change during devel‐ opment and plastid differentiation, and under stress conditions, clustering of large groups of connected plastoglobuli were observed [111-112]. Lipid and protein storage inside the chloroplasts could support plants' fatty acid regulation, unsaturation and mobilization in response to the stress caused by biotic interactions, especially due to the presence of plasto‐ globulin among its proteins [111, 113]. Although higher plastoglobuli content in chloroplasts could be linked to plant senescence [114], this may not be the case of these Amaranthaceae plants because all leaf samples were visually healthy and green when collected. In *G. hermo‐ genesii* leaves which were infected for some sort of septate endophytic organism (figure 8),

and immobilise calcium [110].

420 14 Biodiversity in Ecosystems - Linking Structure and Function

50 µm.

**Figure 6.** Dimorphic chloroplasts in *Gomphrena* species (Amaranthaceae) observed through an electron transmission microscope. **A:** Granal (black arrow) chloroplast of *Gomphrena arborescens* L.f. spongy parenchyma, with few starch granules (white arrow) and a large plastoglobule (white star). **B**: Granal chloroplast in *G. pohlii* Moq. palisade paren‐ chyma, with well-developed peripheral reticulum (orange arrow) and large plastoglobuli (white stars). **C**: Organelles in *G. arborescens* bundle sheath cell, which are positioned towards the vascular bundle, with chloroplasts with no stacked disks (grana) of thylakoid membranes, but large amount of starch granules (white arrow), large plastoglobuli (white star), and mitochondria (red arrow). Scale bars: A, C: 1 µm; B: 0.5 µm.

**Figure 7.** Leaf anatomy of *Alternanthera* species (Amaranthaceae) observed in cross sections. **A**: *Alternanthera brasiliana* (L.) Kuntze *(*syn=*A. dentata)*. **B**: *A. paronychioides* A. St.-Hil. (syn=*A. ficoidea)*. Black arrow indicates the bundle sheath cell with organelles near the outer cell wall in **A** (C3 species) and towards the vascular bundle in **B** (C3-C4 intermediary species). **Scale bars:** 50 µm.

when compared with non-infected leaves (figure 8), plastoglobuli were reduced in size, which suggests a mobilization of its content due to the interaction with this microorganism.

Leaf surfaces of some Cerrado species of the genus *Gomphrena* presented epicuticular wax crystals in platelet form, oriented in parallel [58], an aspect previously described only in Chenopodiaceae species. If these platelets are present only in Cerrado species, it could be explained as a way of immobilize the excess of carbohydrates produced by a species with high photosynthesis rates and limited growth – as preconized by the theory of oligotrophic scleromorphism [14]. Crystalloid wax projections were found on both leaf surfaces of *Gomphrena arborescens*, *G. pohlii* and *G. virgata*, as platelets distributed in different densities and

**Figure 8.** Chloroplasts in *Gomphrena hermogenesii* J.C. Siqueira bundle sheath cell. **A**: Non-infected sample show the chloroplast with starch (white arrow) and large plastoglobuli (white star); mitochondria (red arrow). **B**: Sample with a septate endophytic microorganism (blue arrow), shows that chloroplast´s large plastoglobuli were mobilized (white circle in B) and the membrane system was disrupted, while starch (white arrow) was preserved. Scale bars: 2 µm.

patterns; epicuticular wax did not prevent the development of fungi hyphae on leaves of none of these three Cerrado native species; however, the development of such a structure should be one adaptation of the Cerrado species, because they present more platelets and ridges of epicuticular waxes in relation to *G. globosa*, an introduced species also studied [58].

There is much work to be done in order to understand all aspects connected to leaf function in Cerrado plants, because more than been the primary photosynthetic organ which produce carbohydrate for the plant, leaves also give place to biotic interactions (it is common to find fungi or insects larvae in leaves) which can affect the plant life, including the onset of the production of complexes chemical compounds of interest because of its biologic activity (alkaloids, tannins or other phenolic compounds, sterols, saponin).

### *3.2.2. Root and stem structure*

Melastomataceae species are found in several physiognomies in the Cerrado, from well drained to periodically or permanently flooded soils [115], displaying anatomical features which give them the ability of survive in different environments. Species of the palm swamps with periodically flooded soils produce an aerenchymatous tissue in roots and stem during the primary and secondary growth [116]. During the primary growth of root and stem the tissue is a schyizolisigenous aerenchyma and schyzogen aerenchyma, respectively. During the secondary growth, root and stem develop phellogen from division of pericicle cells, deriving two cells types, one with square or rectangular shape (compact cells positive for suberin in histochemical test under light microscopy) and another cell with "T" shape (negative for suberin), which are disposed with intercellular spaces, naming the tissue aerenchymatous polyderm. The polyderm of the same organ and species found in well drained soils or emerged in the flooded soils does not have this aerenchymatous aspect [116]. According to [117], these intercellular spaces are filled of gases and longitudinally interconnected emerged parts with immersed parts, providing a low resistance way which facilitates internal diffusion of these gases at long distances throughout the organs of the plant. Although the epidermic cell walls and cuticle of primary roots generally are thin [63, 118], any species show thickness of external periclinal and anticlinal walls of epidermic cells in plants submitted to flooding in palm swamps [116]. This thickness could provide protection against adverse conditions near to root surface in the flooded soils [119].

Gelatinous fibers are different of other sclerenchyma fibers because they have a cellulosic thickening in the inner cell walls (figure 9) which, due to artifact of manufacturing of the blade, disconnects from lignified cell walls and stands out [120]. The most accurate way to observe the gelatinous fibers is the color technique using dyes that differs lignin of cellulose. For example, acid floroglucine will stain only the external layer of wall where there is lignin and safranine-fast green, a double staining, that will stain red the lignified wall and green the gelatinous layer, indicating presence of cellulose [121]. This layer is also called mucilaginous layer or "G" layer and generally occurs in tension wood and underground organs [23, 122-123]. Gelatinous fibers are very common in the Cerrado plants and they usually appear associated with the secondary xylem of stem, mainly in the initial layers of the growth ring [120, 124] but also may appear on other organs such as petiole and raquis of leaves [121]. Generally, the mucilaginous aspect of "G" layer is linked to the ability of aggregate water because the structure is highly hygroscopic [23].

patterns; epicuticular wax did not prevent the development of fungi hyphae on leaves of none of these three Cerrado native species; however, the development of such a structure should be one adaptation of the Cerrado species, because they present more platelets and ridges of

**Figure 8.** Chloroplasts in *Gomphrena hermogenesii* J.C. Siqueira bundle sheath cell. **A**: Non-infected sample show the chloroplast with starch (white arrow) and large plastoglobuli (white star); mitochondria (red arrow). **B**: Sample with a septate endophytic microorganism (blue arrow), shows that chloroplast´s large plastoglobuli were mobilized (white circle in B) and the membrane system was disrupted, while starch (white arrow) was preserved. Scale bars: 2 µm.

There is much work to be done in order to understand all aspects connected to leaf function in Cerrado plants, because more than been the primary photosynthetic organ which produce carbohydrate for the plant, leaves also give place to biotic interactions (it is common to find fungi or insects larvae in leaves) which can affect the plant life, including the onset of the production of complexes chemical compounds of interest because of its biologic activity

Melastomataceae species are found in several physiognomies in the Cerrado, from well drained to periodically or permanently flooded soils [115], displaying anatomical features which give them the ability of survive in different environments. Species of the palm swamps with periodically flooded soils produce an aerenchymatous tissue in roots and stem during the primary and secondary growth [116]. During the primary growth of root and stem the tissue is a schyizolisigenous aerenchyma and schyzogen aerenchyma, respectively. During the secondary growth, root and stem develop phellogen from division of pericicle cells, deriving two cells types, one with square or rectangular shape (compact cells positive for suberin in histochemical test under light microscopy) and another cell with "T" shape (negative for suberin), which are disposed with intercellular spaces, naming the tissue aerenchymatous

epicuticular waxes in relation to *G. globosa*, an introduced species also studied [58].

(alkaloids, tannins or other phenolic compounds, sterols, saponin).

*3.2.2. Root and stem structure*

422 16 Biodiversity in Ecosystems - Linking Structure and Function

**Figure 9.** Gelatinous fibers in the secondary xylem of *Macairea radula (*Bonpl.) DC. (Melastomataceae) stem. Arrow show the "G" layer with cellulosic thickness. **Scale bar**: 50 µm.

In Amaranthaceae species it is common to find a secondary thickening formed by a series of vascular cambia arising successively farther outward from the center of the stem, each producing xylem toward the inside and phloem toward the outside – an anomalous secondary thickening [125-126]. *Amaranthus* spp. can have two or more rings of primary vascular bundles and a complex organization of leaf traces associated with leaf gaps [127]. Some members of the family have vascular bundles included in the medullary tissue of the shoot, with unknown function, which can contribute to leaf vascularization, as in Melasto‐ mataceae and Piperaceae species [128]. The anomalous secondary thickening was found in all investigated members of Amaranthaceae family, which is considered an important group to understand the origin of successive cambia and its products and the variation in the wood anatomy and stem in dicots [126, 129].

Preliminary study of *Gomphrena arborescens* [56] did not show successive vascular cambia in the secondary thickening of the shoot, but the bidirectional activity of a singular vascular cambia adding more cells in the secondary xylem than in the secondary phloem. There were found nucleated fibers and perimedullary amphicribral vascular bundles near the node regions (figure 10) [56], which were connected to the vascularization of a deriving leaf. Further studies are necessary to determine the function of these elements and the reason to this kind of secondary thickening, although it seems to indicate that this species is in transition from herbal to subshrub habit.

**Figure 10.** Transverse sections of *Gomphrena arborescens* L.f. stem. **A**: Perimedullary amphicribral vascular bundles (black arrow) near the node regions, which were connected to the vascularization of a deriving leaf. **B**: Bidirectional activity of a singular vascular cambia (white arrow). **Scale bars**: **A**: 500 µm. **B**: 100 µm.

Although the Raunkiaer system [130] is widely used to classify the life form of plants based on the level of protection of budding structures, new ecological classifications were proposed in Brazil due to the diversity of the subterranean systems found in our flora [131]. The first researcher to use the term "xylopodium" [132], around the year of 1900, described a lignified structure responsible for the regeneration of the aerial parts of a plant, during his studies of the ecology on open fields of Rio Grande do Sul State, in Brazil. Around the year of 1908, [11] another researcher noticed the same structure in Lagoa Santa plants (in Minas Gerais State), but did not attempt to define it. Since then, all the studies trying to understand this organ were concentrated in Cerrado plants [131].

In Amaranthaceae species it is common to find a secondary thickening formed by a series of vascular cambia arising successively farther outward from the center of the stem, each producing xylem toward the inside and phloem toward the outside – an anomalous secondary thickening [125-126]. *Amaranthus* spp. can have two or more rings of primary vascular bundles and a complex organization of leaf traces associated with leaf gaps [127]. Some members of the family have vascular bundles included in the medullary tissue of the shoot, with unknown function, which can contribute to leaf vascularization, as in Melasto‐ mataceae and Piperaceae species [128]. The anomalous secondary thickening was found in all investigated members of Amaranthaceae family, which is considered an important group to understand the origin of successive cambia and its products and the variation in the

Preliminary study of *Gomphrena arborescens* [56] did not show successive vascular cambia in the secondary thickening of the shoot, but the bidirectional activity of a singular vascular cambia adding more cells in the secondary xylem than in the secondary phloem. There were found nucleated fibers and perimedullary amphicribral vascular bundles near the node regions (figure 10) [56], which were connected to the vascularization of a deriving leaf. Further studies are necessary to determine the function of these elements and the reason to this kind of secondary thickening, although it seems to indicate that this species is in transition from

**Figure 10.** Transverse sections of *Gomphrena arborescens* L.f. stem. **A**: Perimedullary amphicribral vascular bundles (black arrow) near the node regions, which were connected to the vascularization of a deriving leaf. **B**: Bidirectional

Although the Raunkiaer system [130] is widely used to classify the life form of plants based on the level of protection of budding structures, new ecological classifications were proposed in Brazil due to the diversity of the subterranean systems found in our flora [131]. The first researcher to use the term "xylopodium" [132], around the year of 1900, described a lignified

activity of a singular vascular cambia (white arrow). **Scale bars**: **A**: 500 µm. **B**: 100 µm.

wood anatomy and stem in dicots [126, 129].

424 18 Biodiversity in Ecosystems - Linking Structure and Function

herbal to subshrub habit.

Studying plants with xylopodium in São Paulo State, [133] author concluded that the super‐ ficial portion of the subterranean system, which originates the first aerial sprouts after burning, is a small subterranean stem – and sometimes is difficult to understand where the stem finishes and where the root starts. Naturally, the subsequent studies were focused in understanding the ontogenesis and the environment were these plants grow. Another study [134] determined that the xylopodium can be formed by the tuberous growth of the primary root near the soil or by the tuberous growth of the hypocotyl; the first one is due to a disturbed environment which prevents the plant to grow naturally (like in *Mimosa multipinna* Benth, *Stryphnodendron adstringens* (Mart.) Coville, *Palicourea rigida* H.B.K and *Kielmeyera coriacea* (Mart.) var. *glab‐ ripes* N. Saddi) and the second one is genetics and independent of the environmental conditions (like in *Clitoria guianensis* Benth. and *Calliandra dysantha* Benth.). Through the study of the xylopodium of *Brasilia sickii* (Asteraceae) [23, 135], it was understood that this organ could be considered a morphological unit, but not an anatomical one; it was stated the need of ontoge‐ netic studies to really understand the origin of any plant xylopodium, since it can be originated from the root in a young xylopodium and from the stem in an older one, always with the predominance of xylem tissue, including gelatinous fibers with the ability of storing water. In [62] authors theorized that the cutting-off of the shoots, at the end of every dry season, would favour the development of xylopodium as an adaption to the conditions prevailing in the grassland or "*campos*" – where these plants are well established. This cutting-off of the shoots could, also, be provided by fire and the hard lignified xylopodium would survive as under‐ ground persistent organs of plants that dwell in savannah-like regions with a dry season lasting from 4-6 months [134]. In [136], *Mandevilla illustris* (Vell.) R.E. Woodson and *M. velutina* K. Schum. (Apocynaceae) from Cerrado were studied and authors concluded that a same plant can have an underground organ formed by a xylopodium (the hard superior portion) and by a fleshy tuberous root; the xylopodium is formed by a cambium tissue, in the junction of the hypocotyl and the primary root, without the participation of the shoot and retaining the capacity of re-sprout the shoot.

In [23], soboles are indicated as common feature in Cerrado plants, an underground horizontal stem which grow out as an erect plant [137]. Sobole of *Annona pygmaea* Warm. can be originated from the hypocotyl, in the begging of the development, or from the top of the root when the primary stem is destroyed; the organ can have aerial portions of leaves and is usually a storage organ with well-developed starchy parenchyma; this kind of plant can perform vegetative reproduction, the same way as the other type of root suckers, the gemmiferous root [62].

In this study [131] are described *Bauhinia forficata* Link, *Centrolobium tomentosum* Guill. ex Benth, *Inga laurina* Willd. and other Cerrado tree species with long roots running in parallel to the surface and showing budding shots. The point of origin to the aerial parts was a typical root without medullary tissue and with primary xylem with centripetal maturation, usually storing starch [131]. In these cases and in herbal or subshrub species from Cerrado, the underground organ is called gemmiferous roots, the second of the root sucker types [62].

The underground system is very important in Cerrado plants, being linked not only to the anchorage, support and water absorption, but also to carbohydrates and water storage and to vegetative reproduction [23, 138]. This Biome is subject to fires since remote ages, which could be caused by electrical discharge or by the primitive men as a strategy to hunt and, most recently, in order to open areas to grow crops [22]; in experimental burned Cerrado areas, the surface temperature is about 74 ºC but, under the soil, heating is drastic not so high, varying from 55 ºC one centimeter below and reaching only few degrees at 5 cm under the surface. Certain savannah species are ephemeral but most of Brazilian Cerrado´s species are perennial [22]. Probably, the temperature difference during the fire can allow underground organs to survive, although the aerial parts are burned out; adding to this the budding characteristic of the xylopodium, soboles and gemmiferous roots, the well-developed underground organs of Cerrado´s species can explain the prevailing perennial habit.

The underground organ of *Gomphrena macrocephala* (Amaranthaceae), a Cerrado species, revealed fructan as the main storage carbohydrate; it was the first reference to this polysac‐ charide in a plant of the superorder Caryophyllidae [139-140]. Fructans are fructose based polysaccharides, usually found in Asteraceae and Gramineae, two of the most evolved families, which indicates it to be a selective advantage [108]. In *G. macrocephala*, the capacity to store fructans instead of starch was considered an advantage developed in response to the environmental stress of the dry season and eventual fires [141]. The fluctuation in fructan content of *G. macrocephala* is connected to photoperiodism: shorter days, typical from the dry winter, induce senescence of the aerial organs and increase in the fructan content whilst long days, typical of the rainy summer, stimulated the development of the aerial organs and resulted in shortage of fructan content [142]. A well-marked seasonality of fructan accumula‐ tion was found in tuberous roots of *Gomphrena marginata* Seub. [143] and authors correlated it with seasonal changes in the availability of water in the soil; the content of fructans decreased during the rainy season and increased during the dry season, keeping almost steady the relative water content of the underground organs. Preliminary data show that tuberous roots of *G. arborescens* only stores fructan (figure 11), whilst in the shoot there was found starch [56]. As *G. arborescens* roots are used in folk medicine to reduce fever, against asthma and bronchitis or as tonic [144-147], along with other Amaranthaceae species used for the same purposes, the isolation and study of their fructans could help to understand the origin of its folk medicinal properties. In roots of *Arctium lappa* L., var. *herkules* there were fructans from inuline series which were proved to be biologically active as cough-suppressing agent in a cat model *in vivo*; the activity of these fructans in suppressing cough was compared to the parameters stablished for antitussive efficiency of drugs commonly used in clinical practice [148]. So, more than a challenge to understand the morphology and anatomy of the underground system in Amaranthaceae species, it is also necessary a more comprehensive study of the carbohydrates and phenology of another species of this family, even to determine if the presence of fructan is widespread or restricted to some members or genera of the family.

storing starch [131]. In these cases and in herbal or subshrub species from Cerrado, the underground organ is called gemmiferous roots, the second of the root sucker types [62].

The underground system is very important in Cerrado plants, being linked not only to the anchorage, support and water absorption, but also to carbohydrates and water storage and to vegetative reproduction [23, 138]. This Biome is subject to fires since remote ages, which could be caused by electrical discharge or by the primitive men as a strategy to hunt and, most recently, in order to open areas to grow crops [22]; in experimental burned Cerrado areas, the surface temperature is about 74 ºC but, under the soil, heating is drastic not so high, varying from 55 ºC one centimeter below and reaching only few degrees at 5 cm under the surface. Certain savannah species are ephemeral but most of Brazilian Cerrado´s species are perennial [22]. Probably, the temperature difference during the fire can allow underground organs to survive, although the aerial parts are burned out; adding to this the budding characteristic of the xylopodium, soboles and gemmiferous roots, the well-developed underground organs of

The underground organ of *Gomphrena macrocephala* (Amaranthaceae), a Cerrado species, revealed fructan as the main storage carbohydrate; it was the first reference to this polysac‐ charide in a plant of the superorder Caryophyllidae [139-140]. Fructans are fructose based polysaccharides, usually found in Asteraceae and Gramineae, two of the most evolved families, which indicates it to be a selective advantage [108]. In *G. macrocephala*, the capacity to store fructans instead of starch was considered an advantage developed in response to the environmental stress of the dry season and eventual fires [141]. The fluctuation in fructan content of *G. macrocephala* is connected to photoperiodism: shorter days, typical from the dry winter, induce senescence of the aerial organs and increase in the fructan content whilst long days, typical of the rainy summer, stimulated the development of the aerial organs and resulted in shortage of fructan content [142]. A well-marked seasonality of fructan accumula‐ tion was found in tuberous roots of *Gomphrena marginata* Seub. [143] and authors correlated it with seasonal changes in the availability of water in the soil; the content of fructans decreased during the rainy season and increased during the dry season, keeping almost steady the relative water content of the underground organs. Preliminary data show that tuberous roots of *G. arborescens* only stores fructan (figure 11), whilst in the shoot there was found starch [56]. As *G. arborescens* roots are used in folk medicine to reduce fever, against asthma and bronchitis or as tonic [144-147], along with other Amaranthaceae species used for the same purposes, the isolation and study of their fructans could help to understand the origin of its folk medicinal properties. In roots of *Arctium lappa* L., var. *herkules* there were fructans from inuline series which were proved to be biologically active as cough-suppressing agent in a cat model *in vivo*; the activity of these fructans in suppressing cough was compared to the parameters stablished for antitussive efficiency of drugs commonly used in clinical practice [148]. So, more than a challenge to understand the morphology and anatomy of the underground system in Amaranthaceae species, it is also necessary a more comprehensive study of the carbohydrates and phenology of another species of this family, even to determine if the presence of fructan

Cerrado´s species can explain the prevailing perennial habit.

426 20 Biodiversity in Ecosystems - Linking Structure and Function

is widespread or restricted to some members or genera of the family.

**Figure 11.** Transverse sections of *Gomphrena arborescens*L.f. root. **A**: After treatment in pure ethanol for at least 7 days, clusters of spherical fructan crystals (white arrow) appear in the cortex region. B: Spherical fructan crystals (black ar‐ row) under polarized light, after dying the section with safranine ethanolic solution. **Scale bars**: **A**: 500 µm. **B**: 100 µm.

## **4. Retrospective and perspectives about Cerrado knowledge and structural studies**

Much of the actual knowledge about the Brazilian savannah or Cerrado Biome and its vegetation is derived from a group of researchers who shared their point of views in a series of Symposia, organized initially by them in order to gather efforts and develop multidiscipli‐ nary research in networks, mostly by initiative of teachers of USP – the São Paulo University [10], who also republished in Portuguese some very important works done by the first foreign researchers [10-11, 132]. The first Symposium was realized in 1962, in São Paulo city: the "*Simpósio Nacional do Cerrado*" was intended to improve the knowledge to grow crops and raise cattle in the region [149]; the second one was realized in Rio de Janeiro, in 1965, where people concluded that most of the knowledge about Cerrado was related to the plant biology and that would be necessary to realize a multidisciplinary approach to create a national policy and also to undertake basic and applied research. The third event was again in São Paulo, in 1971, and gathered so many researchers that it was necessary to realize simultaneous meetings and extend the event in order to allow everybody to present their works [10, 149].

From the year 1975 on, the federal government created a set of programs to speed up the development of federal States in the center of the Cerrado Biome (Goiás, Minas Gerais, Mato Grosso and Federal District) through financial aid for the construction of roads, schools and warehouses, funding agricultural research, providing technical assistance to incorporation of new areas into the production process and encouraging the use of limestone and phosphate to correct the soil pH, among others [150]. More than that, Brazilian Enterprise for Agricultural Research – EMBRAPA – a state-owned company affiliated with the Brazilian Ministry of Agriculture, created its unit Embrapa Cerrados (CPAC) with the aim of developing agricul‐ tural systems viable to the Cerrado Biome and to give technical support to farmers. So, from the fourth Symposium on, realized in 1976, these events were done in Brasília, with the incentive of Embrapa Cerrados; collecting important data for agricultural development, all the work done in this event was of great value to improve the newly approved policy of the Program for Development of Cerrados [149].

According to [149], all the information gathered wasn´t still enough to support the region development, mostly because they were generalized. Among other problems [149], there were: irregular distribution of rain (a challenge to grow crops), the soils low level of fertility, inadequate methods used to cultivate soils leading to soil exhaustion, incidence of illness in monotypic crops and few knowledge about environmental, economic and social peculiarities of the core region of the Cerrado Biome. Embrapa Cerrado leaded the development of networks with institutes, universities, other Embrapa units and state companies to obtain systematic data on every field of interest to understand and com‐ plete the knowledge gaps in order fulfill its own mission. The knowledge gained through political, technical and economic focus, transferred as technical support to the farmers, created a scale gain which benefited all the participants; the technology incorporated by the farmers implicated in rapid increase of cultivated area [149], at a speed that is not currently possible to maintain without a huge loss of biodiversity.

In 1979 the Symposium theme was "Cerrado: use and management" and in 1982 it was the begging of the international comprisement of the event, which was themed "Savannah: food and energy" and shared the concerns in the use of this kind of environment around the world [149]. In 1989, the seventh Symposium was done in order to gather data on the increasing efficiency to produce crops and, in 1996, the VIII National Symposium and the I International Symposium were done in a year where the cultivated area in Cerrado Biome was four times more efficient, during the onset of environmental damages such as soil degradation, weed spreading and pests; from then to now, the rational usage of savan‐ nah areas is the main concern [149-150].

In 2006 [149], the Cerrado region contributed to 33% of the Brazilian Gross Domestic Product, employing around 40% of the labor force. So, in 2008 the theme "Challenges and strategies for the equilibrium between society, agribusiness and natural resources" [149] was chosen to delineate the main discussions of the IX National Symposium of Cerrado and the II Interna‐ tional Symposium of Tropical Savannas; in the third chapter [149] there is a review, in English, about the importance of savannah environments to the global climate change, emphasizing the distribution of this kind of environment in the world, not only in tropical regions of Africa, South America, Asia and Pacific, but also in temperate climate regions of North America (prairies) and derived savannahs in Europe.

According to [151] tropical savannahs are characterized by physiognomies with trees and shrubs and abundance of herbs from Poaceae and Cyperaceae families over dystrophic and sandy soils under a climate with seasonal rainfall. The predominance of bushes and trees over grasses depends on the soil fertility and fire as a natural or anthropomorphic phenomenon, among other environmental characteristics [151]. However, savannah flora presents differen‐ ces: whilst Australian and African savannahs have more deciduous species among bushes and trees, evergreen species are the main representatives of these groups in Brazilian savannah [151-152]. African species can close leaf stomata very rapidly, but this is not the rule for Brazilian species, although there are some exceptions; this characteristic and the deciduous‐ ness can be linked to the shallow root system of African species [151]. Similar to the subterra‐ nean organs of Brazilian species earlier cited in this chapter, Australian savannah species develop lignotubers [153-154] with regenerative and storage functions which allows the resprout after fire. Tropical savannahs are considered more suitable to intensive grain cropping and livestock production, but it is necessary to ponder the need of food production and give value to the ecosystem services of this environment, as the maintenance of fresh water resources and moderation of the Carbon cycle, in order to create another income source for farmers [150] over preserved land.

work done in this event was of great value to improve the newly approved policy of the

According to [149], all the information gathered wasn´t still enough to support the region development, mostly because they were generalized. Among other problems [149], there were: irregular distribution of rain (a challenge to grow crops), the soils low level of fertility, inadequate methods used to cultivate soils leading to soil exhaustion, incidence of illness in monotypic crops and few knowledge about environmental, economic and social peculiarities of the core region of the Cerrado Biome. Embrapa Cerrado leaded the development of networks with institutes, universities, other Embrapa units and state companies to obtain systematic data on every field of interest to understand and com‐ plete the knowledge gaps in order fulfill its own mission. The knowledge gained through political, technical and economic focus, transferred as technical support to the farmers, created a scale gain which benefited all the participants; the technology incorporated by the farmers implicated in rapid increase of cultivated area [149], at a speed that is not

In 1979 the Symposium theme was "Cerrado: use and management" and in 1982 it was the begging of the international comprisement of the event, which was themed "Savannah: food and energy" and shared the concerns in the use of this kind of environment around the world [149]. In 1989, the seventh Symposium was done in order to gather data on the increasing efficiency to produce crops and, in 1996, the VIII National Symposium and the I International Symposium were done in a year where the cultivated area in Cerrado Biome was four times more efficient, during the onset of environmental damages such as soil degradation, weed spreading and pests; from then to now, the rational usage of savan‐

In 2006 [149], the Cerrado region contributed to 33% of the Brazilian Gross Domestic Product, employing around 40% of the labor force. So, in 2008 the theme "Challenges and strategies for the equilibrium between society, agribusiness and natural resources" [149] was chosen to delineate the main discussions of the IX National Symposium of Cerrado and the II Interna‐ tional Symposium of Tropical Savannas; in the third chapter [149] there is a review, in English, about the importance of savannah environments to the global climate change, emphasizing the distribution of this kind of environment in the world, not only in tropical regions of Africa, South America, Asia and Pacific, but also in temperate climate regions of North America

According to [151] tropical savannahs are characterized by physiognomies with trees and shrubs and abundance of herbs from Poaceae and Cyperaceae families over dystrophic and sandy soils under a climate with seasonal rainfall. The predominance of bushes and trees over grasses depends on the soil fertility and fire as a natural or anthropomorphic phenomenon, among other environmental characteristics [151]. However, savannah flora presents differen‐ ces: whilst Australian and African savannahs have more deciduous species among bushes and trees, evergreen species are the main representatives of these groups in Brazilian savannah [151-152]. African species can close leaf stomata very rapidly, but this is not the rule for Brazilian species, although there are some exceptions; this characteristic and the deciduous‐

currently possible to maintain without a huge loss of biodiversity.

Program for Development of Cerrados [149].

428 22 Biodiversity in Ecosystems - Linking Structure and Function

nah areas is the main concern [149-150].

(prairies) and derived savannahs in Europe.

Although there is a lot of data obtained already for Cerrado species, due to the research network which leaded to the creation of Embrapa Cerrados, and later by the increase of the number and quality of the networks created by Embrapa itself and by other Federal Govern‐ ment Agencies policies (as the Milenium Institutes Program, the National Institutes for Science and Technology-INCT Program and the Long-Term Ecological Research Program – PELD, from CNPq), some basic structural studies are still needed to improve the knowledge about the huge diversity of Cerrado´s species (plants, fungi and fauna), preferably multidisciplinary ones, ranging from ecology, morphology and taxonomy to the anatomy and cell biology of species. The structural knowledge is the basis to further development of applied studies (preservation, investigation of pharmacological properties and others). For example, histo‐ chemical investigation in plants can help taxonomy [155-156] and the establishment of patterns for quality control of drugs or micro-scale identification of the potential origin of pharmaco‐ logical properties in Folk medicinal plants, but it is necessary special preparation and fresh material at your disposal [26]. Mostly because of the time consuming and the high cost of pharmacological and pharmaceutical studies, in Brazil there are a great amount of plants used by the population as medicinal [144-147] without almost any scientific study to confirm it.

Since the high humidity and intense heat of the Cerrado´s rainy season favours the develop‐ ment of fungal hyphae on leaf surfaces, including on the Amaranthaceae species *Gomphrena arborescens, G. pohlii* and *G. virgata* [46, 58], the study of the plant-microorganism interaction also can lead to a wide range of applications; for example, health risks to human or stock farming animals' can be avoided simply by preventing the consumption of contaminated food or the medicinal plant. Plants offer a wide range of habitats for microorganisms, including its aerial parts, rhizosphere and internal transport system [157]. This kind of interaction contrib‐ utes to the environmental equilibrium and can play essential roles in agricultural and food safety [157-158]. The plant metabolites against endophytic invaders could be isolated and used for the genetic improvement of crop biochemical defenses; selected microorganism metabolites can be isolated to act as a biological control of crop diseases and herbivores [157].

These and other fields of study demands the basic studies of taxonomy, morphology and anatomy in order to be properly interpreted and, later, lead to application not only on the increase of crop production, but also in the conservation of the few areas of the Cerrado Biome which are still preserved, mostly due to some Conservation Units created to integrate the Conservation Unit System of Brazil. Goiás State is in the center region of the Cerrado Biome and only 15% of the natural savannah was protected in 2002 [159]; originally, savannah vegetation represented 50% of the State territory, and the author claims that the remaining species biodiversity will only be found in Conservation Units about a hundred years from now.

According to [160] the apparent dichotomy between food production and preservation of the natural vegetation is not impossible, because Brazil has already cleared enough area to support all food, fiber and bioenergy production that is necessary to meet not only the own country needs but also the global market. So, maybe it is time to set a new policy not only for agricultural and livestock development, but also to improve infrastructure and the efficiency of these activities and for encouraging and expanding the Conservation Unit System in order to better preserve the huge biodiversity of flora and fauna and its direct and indirect benefices to Brazilian people, now and through the significant amount of research that is still to be done.

## **Acknowledgements**

CAPES, CNPq, FAPDF, FINEP

## **Author details**

Suzane Margaret Fank-de-Carvalho1\*, Nádia Sílvia Somavilla2 , Maria Salete Marchioretto3 and Sônia Nair Báo4

\*Address all correspondence to: suzifankcarvalho@gmail.com

1 Bioscience Coordination, Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq, Brasilia, Brazil

2 Botany Department, Institute of Biological Sciences, Universidade Federal de Juiz de Fora – UFJF, Juiz de Fora,, Brazil

3 PACA Herbarium, Instituto Anchietano de Pesquisas, São Leopoldo, Brazil

4 Cell Biology Department, Institute of Biological Sciences, Universidade de Brasília – UnB, Brasília, Brazil

## **References**

[1] Forzza RC., Leitman PM., Costa AF., Carvalho Jr. AA., : Peixoto AL., Walter BMT., Bicudo C., Zappi D., Costa DP., Lleras E., Martinelli G., Lima HC., Prado J., Steh‐ mann JR., Baumgratz JFA., Pirani JR., Sylvestre L., Maia LC., Lohmann LG., Queiroz LP., Silveira M., Coelho MN, Mamede MC, Bastos MNC, Morim MP, Barbosa MR, Menezes M, Hopkins M, Secco R., Cavalcanti TB., Souza VC. Catálogo de Plantas e Fungos do Brasil-Vol. 1. Rio de Janeiro: Andrea Jakobsson Estúdio/Instituto de Pes‐ quisa Jardim Botânico do Rio de Janeiro; 2010.

[2] Myers N., Mittermeier RA., Mittermeier CG., Fonseca GAB., Kent J. Biodiversity hot‐ spots for conservation priorities. Nature 2000;403 853-858.

species biodiversity will only be found in Conservation Units about a hundred years from

According to [160] the apparent dichotomy between food production and preservation of the natural vegetation is not impossible, because Brazil has already cleared enough area to support all food, fiber and bioenergy production that is necessary to meet not only the own country needs but also the global market. So, maybe it is time to set a new policy not only for agricultural and livestock development, but also to improve infrastructure and the efficiency of these activities and for encouraging and expanding the Conservation Unit System in order to better preserve the huge biodiversity of flora and fauna and its direct and indirect benefices to Brazilian people, now and through the significant amount of research that is still to be done.

1 Bioscience Coordination, Conselho Nacional de Desenvolvimento Científico e Tecnológico

2 Botany Department, Institute of Biological Sciences, Universidade Federal de Juiz de Fora

4 Cell Biology Department, Institute of Biological Sciences, Universidade de Brasília – UnB,

[1] Forzza RC., Leitman PM., Costa AF., Carvalho Jr. AA., : Peixoto AL., Walter BMT., Bicudo C., Zappi D., Costa DP., Lleras E., Martinelli G., Lima HC., Prado J., Steh‐ mann JR., Baumgratz JFA., Pirani JR., Sylvestre L., Maia LC., Lohmann LG., Queiroz LP., Silveira M., Coelho MN, Mamede MC, Bastos MNC, Morim MP, Barbosa MR,

3 PACA Herbarium, Instituto Anchietano de Pesquisas, São Leopoldo, Brazil

, Maria Salete Marchioretto3 and

now.

**Acknowledgements**

**Author details**

Sônia Nair Báo4

Brasília, Brazil

**References**

– CNPq, Brasilia, Brazil

– UFJF, Juiz de Fora,, Brazil

CAPES, CNPq, FAPDF, FINEP

430 24 Biodiversity in Ecosystems - Linking Structure and Function

Suzane Margaret Fank-de-Carvalho1\*, Nádia Sílvia Somavilla2

\*Address all correspondence to: suzifankcarvalho@gmail.com


[31] Barroso GM., Peixoto AL., Ichaso CLF., Costa CG., Guimarães EF., Lima HC. Siste‐ mática de Angiospermas do Brasil. Vol. 3. Viçosa: Imprensa Universitária, Universi‐ dade Federal de Viçosa; 1984

[16] Queiroz-Neto JP. Solos da região dos cerrados e suas interpretações (revisão de liter‐

[17] Reatto A., Correia JR., Spera ST. Solos do bioma Cerrado: aspectos pedológicos. In: Sano.M., Almeida SP.(eds.) Cerrado: Ambiente e Flora. Planaltina: Embrapa; 1998.

[18] Haridasan M. Aluminum accumulation by some cerrado native species of central

[19] Chenery EH. Aluminum in the plant world. Part I. General survey in the dicotyle‐

[20] Haridasan M. Alumínio é um elemento tóxico para as plantas nativas do cerrado? In: Prado CHBA, Casali CA. (eds.) Fisiologia Vegetal: práticas em relações hídricas, fo‐

[21] Ratter JA., Richards PW., Argent G., Gifford DR. Observations on the forests of some mesotrophic soils in central Brazil. Revista Brasileira de Botânica 1978;1 47-58.

[22] Coutinho LM. As queimadas e seu papel ecológico. Brasil Florestal 1980;10(44) 7-23.

[24] Paviani TI. Situação da anatomia ecológica no Brasil. Ciência e Cultura 1984;36(6)

[25] Paiva PHV. A Reserva da Biosfera do Cerrado: fase II. In: Cavalcanti TB., Walter BMT. (eds.) Tópicos atuais em botânica-palestras convidadas do 51° Congresso Na‐ cional de Botânica. Brasília: Sociedade Brasileira de Botânica/Embrapa-Cenargen;

[26] Fank-de-Carvalho SM. Graciano-Ribeiro D. Arquitetura, anatomia e histoquímica das folhas de Gomphrena arborescens L. f. (Amaranthaceae). Acta Botanica Brasilica

[27] Bridson D., Forman L. The herbarium handbook. Richmond: Royal Botanic Gardens

[28] Joly AB. Botânica: Chaves de identificação das plantas vasculares que ocorrem no Brasil, baseadas em chaves de Franz Thomer. 3. ed. São Paulo: Cia Ed. Nacional;

[29] Barroso GM., Guimarães EF., Ichaso CLF., Costa CG., Peixoto AL. Sistemática de An‐ giospermas do Brasil. v1. Rio de Janeiro: Livros Técnicos e Científicos Editora SA;

[30] Barroso GM., Peixoto AL., Ichaso CLF., Costa CG., Guimarães EF., Lima HC. Siste‐ mática de Angiospermas do Brasil. Vol. 2. Viçosa: Imprensa Universitária, Universi‐

[23] Paviani TI. Anatomia vegetal e cerrado. Ciência e Cultura 1978;30(9) 1076-1082.

atura). Revista Brasileira de Ciência do Solo 1982;6 1-12.

tossíntese e nutrição mineral. Barueri: Manole; 2006.

Brazil. Plant and Soil 1982;65 265-273.

432 26 Biodiversity in Ecosystems - Linking Structure and Function

dons. Kew Bulletin 1948;3 173-183.

p47-86.

927-932.

2000. p332-334.

2005;19(2) 377-390.

dade Federal de Viçosa; 1984

Kew; 1992.

1977.

1978.


[59] Miranda HS., Sato MN. Efeitos do fogo na vegetação lenhosa do Cerrado. In: Scariot A., Sousa-Silva JC., Felfilli JM. (eds.). Cerrado: ecologia, biodiversidade e conserva‐ ção. Brasília: Ministério do Meio Ambiente; 2005. p 95-105.

[46] Salatino A., Montenegro G.; Salatino MLF. Microscopia eletrônica de varredura de superfícies foliares de espécies lenhosas do cerrado. Revista. Brasileira de Botânica

[47] Fank-de-Carvalho SM. Contribuição ao conhecimento da anatomia, micromorfologia e ultraestrutura foliar de Amaranthaceae do Cerrado. Thesis. Instituto de Biologia, Doutorado em Biologia Celular e Estrutural, Universidade Estadual de Campinas,

[48] Fank-de-Carvalho SM., Báo SN., Marchioretto MS. Amaranthaceae as a bioindicator of neotropical savannah diversity. In: Lameed GA. (ed.). Biodiversity enrichment in a

[49] Monteiro-Scanavacca WR. Vascularização floral em Amaranthaceae. Ciência e Cul‐

[50] Laboriau MLS. Pollen grain of plants of the "Cerrado"-I. Anais da Academia Brasi‐

[51] Judd WS., Campbell CS., Kellogg EA., Stevens PF., Donoghue MJ. Plant systematics.

[52] Siqueira JC. Frutos e unidades de dispersão em Amaranthaceae. Eugeniana 1984; 7

[53] Pijl, L. van der. (1982). Principles of dispersal in higher plants. Berlim Springer-Ver‐

[54] Coutinho ML. Aspectos ecológicos no Cerrado II. As queimadas e a dispersão de se‐ mentes em algumas espécies anemocórias do estrato herbáceo-subarbustivo. Boletim

[55] Marchioretto MS., Windisch PG., Siqueira JC. Problemas de conservação das espécies dos gêneros Froelichia Moench e Froelichiella R. E. Fries (Amaranthaceae) no Brasil.

[56] Fank-de-Carvalho SM. (2004). Contribuição ao conhecimento botânico de Gomphre‐ na arborescens L.f. (Amaranthaceae)-estudos anatômicos e bioquímicos. (Disserta‐ tion). Instituto de Ciências Biológicas, Mestrado em Botânica, Universidade de

[57] Fank-de-Carvalho SM., Marchioretto MS., Báo SN. Anatomia foliar, morfologia e as‐ pectos ecológicos das espécies da família Amaranthaceae da Reserva Particular do Patrimônio Natural Cara Preta, em Alto Paraíso, Goiás, Brasil. Biota Neotropica 2010;

[58] Fank-de-Carvalho SM., Gomes MRA., Silva PIT., Báo SN. Leaf surfaces of Gomphre‐

na spp. (Amaranthaceae) from Cerrado biome. Biocell 2010; 34(1) 23-35.

A Phylogenetic approach. 2ed. Sunderland, Sinauer Associates; 2002.

Botânico da Universidade de São Paulo 1977; 5 57-64.

Acta Botânica Brasílica 2005; 19(2) 215-219.

Brasília, Brasília, DF, Brazil; 2005.

1986; 9: 117-124.

Campinas, SP, Brazil; 2011.

434 28 Biodiversity in Ecosystems - Linking Structure and Function

tura 1971; 23(3) 339-349.

lang, Heidelberg; 1982.

3-11.

10 77-86.

leira de Ciências 1961; 33(1) 119-130.

diverse world. Rijeka: InTech; 2012. p235-262.


[85] Izaguirre MM., Mazza CA., Svatos A., Baldwin IT., Ballar CL. Solar ultraviolet-B ra‐ diation and insect herbivory trigger partially overlapping phenolic responses in Nic‐ otiana attenuata and Nicotiana longiflora. Annals of Botany 2007; 99 103–109.

[72] Bieras AC., Sajo MG. Leaf structure of the cerrado (Brazilian savanna) woody plants.

[73] Somavilla NS., Kolb RM., Rossatto DR. Leaf anatomical traits corroborate the leaf economic spectrum: a case study with deciduous forest tree species. Brazilian Journal

[74] Mott KA., Gibson AC., O´Leary JW. The adaptive significance of amphistomatic

[75] Mott KA., Michaelson O. Amphistomy as an adaptation to high light intensity in Ambrosia cordifolia (Compositae). American Journal of Botany 1991; 78(1) 76-79.

[76] Parkhurst DF. The adaptative significance of stomatal occurrence on one or both sur‐

[77] Gomes SM., Somavilla NSD., Gomes-Bezerra KM., Miranda SC., De-Carvalho PS., Graciano-Ribeiro D. 2009. Anatomia foliar de espécies de Myrtaceae: contribuições à

[78] Haberland, G. Physiological plant anatomy. London, MacMilan Company Ltd.; 1928.

[79] Sousa HC. Estudo comparativo de adaptações anatômicas em órgãos vegetativos de espécies de Lavoisiera DC. (Melastomataceae) da Serra do Cipó, MG. Thesis. Univer‐

[80] Milanez CRD., Machado SR. Leaf emergences in Microlepsis oleaefolia (DC.) Triana (Melastomataceae) and their probable function: an anatomical and ultrastructural

[81] Landry LG., Chapple CCS., Last RL. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced Ultraviolet-B injury and oxidative damage. Plant Physi‐

[82] Booij-James IS., Dube SK., Jansen MAK., Edelman M., Mattoo AK. Ultraviolet-B radi‐ ation impacts light-mediated turnover of the photosystem II reaction center hetero‐ dimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiology

[83] Bieza K., Lois R. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physi‐

[84] Figueroa FL., Korbee N., Carrillo P., Medina-Sánchez JM., Mata M., Bonomi J., Sán‐ chez-Castillo PM. The effects of UV radiation on photosynthesis estimated as chloro‐ phyll fluorescence in Zygnemopsis decussata (Chlorophyta) growing in a high mountain lake (Sierra Nevada, Southern Spain). Journal of Limnology 2009; 68

leaves. Plant, Cell and Environment 1982; 5: 455-460.

faces of leaves. Journal of Ecology 1978; 66(2) 367-383.

sidade de São Paulo, São Paulo; 1997.

study. Micron 2007; 39 (7) 884-890.

ology 1995;109 1159-1166.

2000; 124 1275-1284.

206-216.

ology 2001; 126 1105-1115.

taxonomia e filogenia. Acta Botanica Brasilica 2009; 23 (1) 223-238.

Trees 2009; 23 451-471.

436 30 Biodiversity in Ecosystems - Linking Structure and Function

of Botany 2014; 37 69-82.


espécies. In: Sano SM., Almeida SP., Ribeiro JF. (Eds.) Cerrado: ecologia e flora. Vol.. 2. Brasília: Embrapa Cerrados; 2008. p 421-1181.


[100] Gavilanes ML. Estudo anatômico do eixo vegetativo de plantas daninhas que ocor‐ rem em Minas Gerais. 1. Anatomia foliar de Gomphrena celosioides Mart. (Amaran‐

[101] Duarte MR., Debur MC. Characters of the leaf and stem morpho-anatomy of Alter‐ nanthera brasiliana (L.) O. Kuntze, Amaranthaceae. Brazilian Journal of Pharmaceut‐

[102] Estelita-Teixeira ME., Handro W. Leaf ultrastructure in species of Gomphrena and Pfaffia (Amaranthaceae). Canadian Journal of Botany 1984;.62(4) 812-817.

[103] Antonucci NP. Estudos anatômicos, ultra-estruturais e bioquímicos da síndrome Kranz em folhas de duas espécies de Gomphrena L. (Amaranthaceae). Dissertation.

[104] Ueno O. Immunogold localization of photosynthetic enzymes in leaves of various C4 plants, with particular reference to pyruvate orthophsphate dikinase. Journal of Ex‐

[105] Muhaidat R., Sage RF., Dengler NG. Diversity of Kranz anatomy and biochemistry in

[106] Rajendrudu G., Prasad JSR., Rama Das VS. C3-C4 species in Alternanthera (Amaran‐

[107] Buchanan BB., Gruissem W., Jones RL. Biochemistry & Molecular Biology of Plants.

[108] Lewis DH. Occurrence and distribution of storage carbohydrates in vascular plants. Pp. 1-52. In.: Lewis DH. (ed) Storage carbohydrates in vascular plants. Cambridge

[109] Borsch T. Clemants S., Mosyakin S. Symposium: Biology of the Amaranthaceae-Che‐ nopodiaceae alliance. Journal of the Torrey Botanical Society 2001; 128(3) 234-235. [110] Volk GM., Goss LJ., Franceschi VR. Calcium Channels are Involved in Calcium Oxa‐ late Crystal Formation in Specialized Cells of Pistia stratiotes L. Annals of Botany

[111] Bréhelin C., Kessler F. The plastoglubule: a bag full of lipid biochemistry tricks. Pho‐

[113] Upchurch R.G. Fatty acid insaturation, mobilization and regulation in the response

[114] Kutík J. The development of chloroplast structure during leaf ontogeny. Photosyn‐

[115] Mendonça RC., Felfili JM., Walter BMT., Silva-Junior MC., Rezende AV., Filgueiras TS., Nogueira PE., Fagg CW. Flora vascular do Bioma Cerrado: checklist com 12.356

[112] Grennan AK. Plastoglobule proteome. Plant Physiology 2008; 147 443-445.

University Press: Society for Exp. Biology, Seminar; 1984. p1-52. Series 19.

C4 eudicots. American Journal of Botany 2007; 94(3) 362-381.

thaceae). Ciência e Agrotecnologia 1999; 23(4) 881-898.

ical Sciences 2004; 40(1) 85-92.

438 32 Biodiversity in Ecosystems - Linking Structure and Function

Universidade Estadual de São Paulo; 2010.

perimental Botany 1998; 49(327) 1637-1646

thaceae). Plant Physiology 1986; 80 409-414.

2004; 93 741-753.

thetica 1998; 35 (4) 481-505.

U.S.A: American Society of Plant Physiologist; 2000.

tochemistry and Photobiology 2008; 84(6) 1388-1394.

of plants to stress. Biotechnology Letters 2008; 30 967-977.


(Amaranthaceae) under rock-field conditions. Theoretical and Experimental Plant Physiology 2013; 25(1) 46-55.

[144] Barros MGAE. Plantas medicinais-usos e tradições em Brasília-DF. Oréades 1982; 8 (14/15) 140-149.

[130] Raunkiaer C. The life forms of plants and statistical plant geography. Oxford: Claren‐

[131] Appezzato-da-Glória B. Morfologia de sistemas subterrâneos-histórico e evolução do

[132] Lindman CAM., Ferri MG. A vegetação do Rio Grande do Sul. Belo Horizonte: Ed.

[133] Rachid M. Transpiração e sistemas subterrâneos da vegetação de verão dos campos Cerrados de Emas. Boletim da Faculdade de Filosofia Ciências e Letras da Universi‐

[134] Rizzini CT., Heringer EP. Studies on the underground organs of trees and shrubs from some southern Brazilian savannas. Anais da Academia Brasileira de Ciências

[135] Paviani TI. Estudos morfológico e anatômico de Brasilia sickii G. M. Barroso. II: anat‐ omia da raiz, do xilopódio e do caule. Revista Brasileira de Biologia 1977; 37(2)

[136] Appezzato-da-Glória B., Estelita MEM. The developmental anatomy of the subterra‐ nean system in Mandevilla illustris (Vell.) Woodson and M. velutina (Mart. ex Sta‐

delm.) Woodson (Apocynaceae). Revista Brasileira de Botânica 2000; 23 7-35. [137] Bell AD., Brian A. Plant form-an illustrated guide to flowering plant morphology.

[138] Hoffmann WA. The relative importance of sexual and vegetative reproduction in Cerrado woody plants. In: Cavalcanti TB., Walter BMT. (eds.), Tópicos atuais em bot‐ ânica-palestras convidadas do 51° Congresso Nacional de Botânica. Brasília: Socie‐

[139] Figueiredo-Ribeiro RCL., Dietrich SMC., Carvalho MAM., Vieira CCJ., Isejima EM., Dias-Tagliacozzo GM., Tertuliano MF. As múltiplas utilidades dos frutanos-reserva de carboidratos em plantas nativas do cerrado. Ciência Hoje 1982; 14(84) 16-18. [140] Figueiredo-Ribeiro RCL. Distribuição, aspectos estruturais e funcionais dos frutanos, com ênfase em plantas herbáceas do cerrado. Revista Brasileira de Fisiologia Vegetal

[141] Vieira CCJ., Figueiredo-Ribeiro RCL. Fructose-containing carbohydrates in the tuber‐ ous root of Gomphrena macrocephala St.-Hil. (Amaranthaceae) at different pheno‐

[142] Moreira MF., Vieira CCJ., Zaidan LBP. Efeito do fotoperíodo no crescimento e no pa‐ drão de acúmulo de frutanos em plantas aclimatizadas de Gomphrena macrocephala

St.-Hil. (Amaranthaceae). Revista. Brasileira de Botânica 1999; 22(3)3 397-403. [143] Silva FG., Cangussu LMB., Paula SLA., Melo GA., Silva EA.. Seasonal changes in fructan accumulation in the underground organs of Gomphrena marginata Seub.

Portland, USA; London, England: Timber Press, Inc; 2008.

dade Brasileira de Botânica/Embrapa-Cenargen; 2000. p231-234.

logical phases. Plant, Cell and Environmentm 1993; 16 919-928.

conhecimento no Brasil. Ribeirão Preto, Brazil: A.S. Pinto Editor; 2003.

don Press; 1934.

440 34 Biodiversity in Ecosystems - Linking Structure and Function

1962; 34 235-247.

1993; 5(2) 203-208.

307-324.

Itatiaia; São Paulo: EDUSP; 1974.

dade de São Paulo, 80 (Botânica) 1947; 5 5-140.


biological control of the phytopatogen Sclerotinia sclerotiorum (LIB.). Brazilan Jour‐ nal of Microbiology 2009; 40 73-78.

