**Current and Potential Use of Phytophagous Mites as Biological Control Agent of Weeds**

Carlos Vásquez, Yelitza Colmenárez, José Morales-Sánchez, Neicy Valera, María F. Sandoval and Diego Balza

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/59953

### **1. Introduction**

[29] IUSS Working Group WRB. World reference base for soil resources 2006 (2ed.). World Soil Resources Reports No. 103. Rome: FAO; 2007. <http:// www.fao.org/ag/agl/agll/wrb/doc/wrb2007\_red.pdf> [accessed 20 December 2011] [30] Gul B., Marwat K. B., Hassan G. et al. Impact of tillage, plant population and mulch‐ es on biological yield of maize. Pakistan Journal of Botany 2009;41(5) 2243–2249.

108 Weed Biology and Control

Biological control of weeds by using phytophagous mites may help to contain infestations and reduce their spread in time. Although, eradication is not the goal due to the vastness of the areas, the most desirable scenario is achieved when weeds are no longer a concern and no other control is necessary. However, biological control should not be considered the unique strategy to face weed problems, thus commonly; other methods are still required to attain the desired level of control.

There is an increasingly interest in using mites for biological control of weeds, primarily those belonging to Eriophyidae because of they are host-specific and often weaken the host plant affecting plant growth and reproduction. Although eriophyid mite species impact the fitness of their host plant, it is not clear how much they have contributed to reduction of the population of the target weed. In some cases, natural enemies, resistant plant genotypes, and adverse abiotic conditions have reduced the ability of eriophyid mites to control target weed popula‐ tions. Besides, susceptibility of eriophyids to predators and pathogens may also prevent them from achieving population densities necessary to reduce host plant populations.

In addition to eriophyid mites, tetranychid mites are also being considered as an alternative for weed control. The gorse spider mite, *Tetranychus lintearius* Dufour, has shown to reduce shoot growth on gorse (*Ulex europaeus* L.) by around 36% in impact studies conducted over 2.5 years in Tasmania. New colonies expand rapidly and cause severe damage to gorse plants, but often do not persist in large numbers.

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

Since the use of phytophagous mite species is a safe alternative for controlling weeds, in this chapter we will review some examples of biological control programs using eriophyid and tetranychid mites worldwide.

## **2. The problem with weeds**

Weeds can be defined as plants growing out of place. For example, water hyacinth (*Eichhornia crassipes* (Mart.) Solms) is widely planted as a water ornamental but when environmental conditions are suitable it spreads rapidly obstructing lakes, rivers and rice paddy fields, affecting adversely human activities (fishing, water transport) and biodiversity [1]. Similarly, morning glory is beautiful in the garden, but also it can cause 30% yield loss [2].

Invasive non-native plants are a serious threat to native species, communities, and ecosystems since they can compete with and displace native plants, animals, and other organisms that depend on them, alter ecosystem functions and cycles significantly, hybridize with native species, and promote other invaders [3]. However, according to these authors, reversion, halting or slowing of plant invasion and even restoring badly infested areas to healthy systems dominated by native species is possible but actions to control and manage those invasive plants are required.

Details of weed management approaches will obviously vary from crop to crop. For instance, although weed control remains a major concern in organic agriculture, producers have limited tools for managing weeds [4].

### **3. Weed control techniques**

Weed control techniques can be grouped in the following categories:

	- **a.** Cultural: cultural practices promoting vigorous, dense crops are the most important and least recognized means of preventing weed establishment and encroachment. Also soil fertility, humidity and chemical properties (pH, electrical conductivity, etc.) may favor one plant species over another. Other cultural means of control involve covering a weed infested area with mulches to exclude light.
	- **b.** Mechanical (physical): mechanical control of weeds involves hand pulling or various types of tractor-powered tillage operations.

sulfur mixture known as the Bordeaux mixture, which also was used for broadleaf weed control.

**3.** Biological: Biological methods use weeds' natural antagonists as control agents. The objective of biological control is not weed eradication, but rather the reduction of the population below a level of economic or aesthetic injury.

### **4. Biological control: A weed management approach**

Since the use of phytophagous mite species is a safe alternative for controlling weeds, in this chapter we will review some examples of biological control programs using eriophyid and

Weeds can be defined as plants growing out of place. For example, water hyacinth (*Eichhornia crassipes* (Mart.) Solms) is widely planted as a water ornamental but when environmental conditions are suitable it spreads rapidly obstructing lakes, rivers and rice paddy fields, affecting adversely human activities (fishing, water transport) and biodiversity [1]. Similarly,

Invasive non-native plants are a serious threat to native species, communities, and ecosystems since they can compete with and displace native plants, animals, and other organisms that depend on them, alter ecosystem functions and cycles significantly, hybridize with native species, and promote other invaders [3]. However, according to these authors, reversion, halting or slowing of plant invasion and even restoring badly infested areas to healthy systems dominated by native species is possible but actions to control and manage those invasive plants

Details of weed management approaches will obviously vary from crop to crop. For instance, although weed control remains a major concern in organic agriculture, producers have limited

**1.** Prevention: it consists in avoiding introduction of weeds within an area based on cultural and mechanical practices (such as clean seed use, sanitation of mechanical implements)

**a.** Cultural: cultural practices promoting vigorous, dense crops are the most important and least recognized means of preventing weed establishment and encroachment. Also soil fertility, humidity and chemical properties (pH, electrical conductivity, etc.) may favor one plant species over another. Other cultural means of control involve

**b.** Mechanical (physical): mechanical control of weeds involves hand pulling or various

**2.** Chemical: One of the major contributing factors to the advancement of man's way of life during the 20th century has been the development of chemical compounds for pest control. The first major selective pest controlling compound used was a lime-copper-

morning glory is beautiful in the garden, but also it can cause 30% yield loss [2].

Weed control techniques can be grouped in the following categories:

that ensure sanitary conditions and minimize weed introduction.

covering a weed infested area with mulches to exclude light.

types of tractor-powered tillage operations.

tetranychid mites worldwide.

110 Weed Biology and Control

are required.

tools for managing weeds [4].

**3. Weed control techniques**

**2. The problem with weeds**

Definition: Weed biocontrol strategies are based on the use of natural enemies to suppress the growth of a weed or to reduce its population [5].

Main strategies of Biological Control: There are two basic strategies for implementing the biological control of weeds:


The classical biological control has three disadvantages, such as: high initial costs, limited number of natural enemies for each target weed species and inability to control the biological control agent dissemination after being released in nature [8]. In addition, successful weed control is strongly dependent on favorable conditions promoting biological control agent population increasing, thus stimulating the establishment of epiphytotics to reduce the target weed population [6].

#### **5. Classical biological control of weeds: The beginning**

The first intent of classical biological control of a weed species is documented in south‐ ern India in 1863 and in Sri Lanka in 1865 with introduction of a cochineal mealybug *Dactylopius ceylonicus* Green against the cactus *Opuntia vulgaris* Mill. [9]. Although it failed, it was followed by the release in 1914 of another strain which resulted in the successful control of *O. vulgaris* [10]. After that, introduction of up to 30 separate insect species rendered in the successful control of common pest pear *Opuntia stricta* (Haw.) Haw. by the moth *Cactoblastis cactorum* (Berg), and of other cacti by this moth and different *Dactylo‐ pius* species [10]. Later, the first significant program of classical biological control, involv‐ ing the import of agents following a search in the country of origin of the weed, was the program against *Lantana camara* L. in Hawaii. For this, 23 different insect species from Mexico were shipped to Hawaii, of which 14 were released and eight of these established to give adequate control of lantana in most areas [11].

#### **6. Mites as biological control agents of weeds**

Insects and, in lesser extent, pathogens have long been considered as the main agents of weed control. Specialized literature lists most of the successful using one of these organisms. For example, the search for biological agents to control water hyacinth began in the early 1960s resulting in six arthropod species released around the world including five insect species [*Neochetina bruchi* (Hustache), *N. eichhorniae* (Warner), *Niphograpta albiguttalis* Warren, *Xubida infusellus* (Walker) and *Eccritotarsus catarinensis* (Carvalho)] and only one mite species [*Orthogalumna terebrantis*Wallwork] [12]. As result, the mite and *X. infusellus* have not contrib‐ uted to control and only *N. bruchi*, *N. eichhorniae* and *N. albiguttalis* have been released in numerous infestations since the 1970s and have contributed to successful control of the weed in many locations [12]. Other classical example of predominance of insects as bio control agent is referred to *L. camara*. First attempts were made with importation of 23 insect species to Hawaii from Mexico. After that, thirty-nine insect species have been deliberately or uninten‐ tionally released as biocontrol agents or otherwise associated to lantana worldwide and only 27 of them have established in at least one country or island [13] (see table 1). In contrast, only three fungus species have been used, such as: *Mycovellosiella lantanae* var. *lantanae* (Chupp) Deighton (Mycosphaerellaceae), *Prospodium tuberculatum* (Spegazzini) Arthur (Pucciniaceae) and *Septoria* sp. (Sphaeriopsidaceae) released in South Africa, Australia and Hawaii, respec‐ tively [13]. In turn, only one eriophyid species, so called *Aceria lantanae* (Cook) have been reported on lantana [14] (Fig 1).



**6. Mites as biological control agents of weeds**

**Biological control agent Country released**

*Cremastobombycia lantanella* Busck Hawaii

*Ectaga garcia* Becker Australia

*Hepialus* sp. Hawaii

*Leptostalis* sp. Jamaica *Oxyptilus* sp. Jamaica

*Pseudopyrausta santatalis* (Barnes and McDunnough) Micronesia, Fiji, Hawaii

*Strymon bazochii* (Godart) Australia, Fiji, Hawaii

*Tmolus echion* (L.) Hawaii, Fiji

*Autoplusia illustrata* Guenée Australia, South Africa

*Diastema tigris* Guenée Zambia, Australia, Micronesia, Fiji, Ghana, Hawaii, St.

*Epinotia lantana* Busck Micronesia, Hawaii, Marshall Islands, South Africa,

*Hypena laceratalis* Walker Micronesia, Hawaii, South Africa, Fiji, Australia, Guam *Lantanophaga pusillidactyla* (Walker) Micronesia, Hawaii, Hong Kong, Palau, South Africa

*Neogalea sunia* (Guenée) Australia, Micronesia, Hawaii, South Africa

*Salbia haemorrhoidalis* Guenée Kenya, Zambia, Uganda, Tanzania

Australia

Helena, Tanzania, Uganda

reported on lantana [14] (Fig 1).

LEPIDOPTERA

112 Weed Biology and Control

Insects and, in lesser extent, pathogens have long been considered as the main agents of weed control. Specialized literature lists most of the successful using one of these organisms. For example, the search for biological agents to control water hyacinth began in the early 1960s resulting in six arthropod species released around the world including five insect species [*Neochetina bruchi* (Hustache), *N. eichhorniae* (Warner), *Niphograpta albiguttalis* Warren, *Xubida infusellus* (Walker) and *Eccritotarsus catarinensis* (Carvalho)] and only one mite species [*Orthogalumna terebrantis*Wallwork] [12]. As result, the mite and *X. infusellus* have not contrib‐ uted to control and only *N. bruchi*, *N. eichhorniae* and *N. albiguttalis* have been released in numerous infestations since the 1970s and have contributed to successful control of the weed in many locations [12]. Other classical example of predominance of insects as bio control agent is referred to *L. camara*. First attempts were made with importation of 23 insect species to Hawaii from Mexico. After that, thirty-nine insect species have been deliberately or uninten‐ tionally released as biocontrol agents or otherwise associated to lantana worldwide and only 27 of them have established in at least one country or island [13] (see table 1). In contrast, only three fungus species have been used, such as: *Mycovellosiella lantanae* var. *lantanae* (Chupp) Deighton (Mycosphaerellaceae), *Prospodium tuberculatum* (Spegazzini) Arthur (Pucciniaceae) and *Septoria* sp. (Sphaeriopsidaceae) released in South Africa, Australia and Hawaii, respec‐ tively [13]. In turn, only one eriophyid species, so called *Aceria lantanae* (Cook) have been


**Table 1.** List of biological control agents associated to *L. camara* worldwide

**Figure 1.** Percentage of different groups of biological control agents used against *L. camara*.

In regard to pathogens, Australia led the world with the first deliberate introduction of a plant pathogen as a biocontrol agent, i.e. the rust *Puccinia chondrillina* Bubak & Syd., released in 1971 to control skeleton weed *Chondrilla juncea* L. [10]. Furthermore, several fungal pathogens with mycoherbicide potential (*Sclerotinia sclerotiorum* (Lib.) de Bary in Hyakill™ and *Cercospora rodmanii* Conway, named ABG-5003) have been discovered on diseased water hyacinth plants, but none has become commercially available in the market [8].

#### **7. Eriophyoid as biological agents of weed control**

Eriophyoid mites have long been thought to have a high potential as a source for biological control agents of weeds [17-20] because of their typically high degree of host plant specificity [21]. Also, eriophyoid mites can substantially damage vegetative and reproductive plant parts, thus reduce fitness of the target weed, have high reproductive rates, and disperse widely by wind, which all favor their potential to be effective biological control agents [18, 22-23]. Despite those desirable features exhibited by eriophyoid mites, relatively few species have been introduced as classical biological control agents [19]. This could be account for the fact that relatively few species of Eriophyoidea are considered economic pests [23], which suggests that the impact of most species would be limited by host plant resistance or tolerance, natural enemies, and adverse abiotic conditions, affecting the efficacy of biological control agents [24].

**Biological control agent Country released**

*Aceria lantanae* Cook South Africa, Australia

*Ophiomyia camarae* Spencer South Africa

**Table 1.** List of biological control agents associated to *L. camara* worldwide

9%

Based on [13, 15-16].

114 Weed Biology and Control

23%

*Eutreta xanthochaeta* Aldrich Australia, South Africa, Hawaii

2% 2% 2% 2%

Lepidoptera Coleoptera Hemiptera Diptera Eriophyidae Mycosphaerellaceae Sphaeropsidaceae Pucciniaceae

In regard to pathogens, Australia led the world with the first deliberate introduction of a plant pathogen as a biocontrol agent, i.e. the rust *Puccinia chondrillina* Bubak & Syd., released in 1971 to control skeleton weed *Chondrilla juncea* L. [10]. Furthermore, several fungal pathogens with mycoherbicide potential (*Sclerotinia sclerotiorum* (Lib.) de Bary in Hyakill™ and *Cercospora rodmanii* Conway, named ABG-5003) have been discovered on diseased water hyacinth plants,

Eriophyoid mites have long been thought to have a high potential as a source for biological control agents of weeds [17-20] because of their typically high degree of host plant specificity [21]. Also, eriophyoid mites can substantially damage vegetative and reproductive plant parts, thus reduce fitness of the target weed, have high reproductive rates, and disperse widely by

**Figure 1.** Percentage of different groups of biological control agents used against *L. camara*.

but none has become commercially available in the market [8].

**7. Eriophyoid as biological agents of weed control**

*Ophiomyia lantanae* Froggatt Cook Islands, South Africa, New Caledonia, Kenya, India,

Hong Kong, Hawaii, Guam, Micronesia, Australia, Fiji

32%

28%

There are about 4,000 recognized eriophyoid mite species, and about 80% of currently known species have been recorded in association with a single species of host plant [21], suggesting that there should be a large number of prospective agents available to discover. By far, species from the genus *Aceria* have been widely used in biological control of weeds (Fig 2), probably due to together with *Eriophyes* include about one-third of the known Eriophyoidea revealing high species diversity.

**Figure 2.** Number of Eriophyidae species used as biological control agents of weeds.

The oldest cases of attempts to use eriophyid mites for biological control include *Aceria chondrillae* Canestrini, *A. malherbae* Nuzzaci and *Aculus hyperici* Liro. *Aceria chondrillae* is native to Europe and has been introduced to control *C. juncea* (rush skeletonweed, Asteraceae) in Australia, USA and Argentina [25] and it is considered to be the most effective of the three biological control agents that were released [26].

*Aceria malherbae* is native to Europe and forms galls on developing leaves and stems of *Convolvulus arvensis* L. (Convolvulaceae) [27]. *Aceria malherbae* has been released in the USA in 1989 [17], in Canada in 1989 [28] and in South Africa in 1995 [29].

*Aculus hyperici*, native to Europe, was introduced to control *Hypericum perforatum* L. (Clusia‐ ceae) in Australia [18]. By mid 1994, a total of 245 releases of *A. hyperici* had been made throughout New South Wales and Victoria, being mite populations confirmed at 108 sites. Although the mite significantly reduced shoot and root biomass, field weed populations has not been significantly impacted [18, 30].

As related by [19], since Rosenthal's review in 1996, 13 species have undergone some degree of pre-release, so named: *Aceria genistae* (Nalepa), *A. lantanae*, *Aceria* sp. [boneseed leaf buckle mite, BLBM], *A. salsolae* De Lillo & Sobhian, *A. sobhiani Sukhareva*, *A. solstitialis* de Lillo et al., *A. tamaricis* (Trotter), *A. thalgi Knihinicki et al.*, *A. thessalonicae* Castagnoli, *Cecidophyies rouhol‐ lahi* Craemer, *Floracarus perrepae* Knihinicki & Boczek, *Leipothrix dipsacivagus* Petanović & Rector and *L. knautiae* (Liro), but only four of them have been authorized for introduction (*A. genistae*, *Aceria* sp., *C. rouhollahi* and *F. perrepae*). However, there are much more species have been considered for biological control of weeds [19] (Table 2).



*Aculus hyperici*, native to Europe, was introduced to control *Hypericum perforatum* L. (Clusia‐ ceae) in Australia [18]. By mid 1994, a total of 245 releases of *A. hyperici* had been made throughout New South Wales and Victoria, being mite populations confirmed at 108 sites. Although the mite significantly reduced shoot and root biomass, field weed populations has

As related by [19], since Rosenthal's review in 1996, 13 species have undergone some degree of pre-release, so named: *Aceria genistae* (Nalepa), *A. lantanae*, *Aceria* sp. [boneseed leaf buckle mite, BLBM], *A. salsolae* De Lillo & Sobhian, *A. sobhiani Sukhareva*, *A. solstitialis* de Lillo et al., *A. tamaricis* (Trotter), *A. thalgi Knihinicki et al.*, *A. thessalonicae* Castagnoli, *Cecidophyies rouhol‐ lahi* Craemer, *Floracarus perrepae* Knihinicki & Boczek, *Leipothrix dipsacivagus* Petanović & Rector and *L. knautiae* (Liro), but only four of them have been authorized for introduction (*A. genistae*, *Aceria* sp., *C. rouhollahi* and *F. perrepae*). However, there are much more species have

not been significantly impacted [18, 30].

*Aceria* species

116 Weed Biology and Control

been considered for biological control of weeds [19] (Table 2).

*A. artemisiae* (Canestrini) *Artemisia vulgaris* L.

**Biological control agent Target plant Country**

*A. acacifloris* Meyer *Acacia saligna* (Labill. Wend. (Fabaceae) Australia *A. angustifoliae* Denizhan et al. *Elaeagnus angustifolia* Turkey

*A. bicornis* (Trotter) *Solanum elaeagnifolium* Cav. (Solanaceae) Argentina *A. boycei* (Keifer) *Ambrosia artemisiifolia* L. (Asteraceae) U.SA. *A. burnleya* Keifer *A. saligna* Australia *A. sobhiani* Sukhareva *Acroptilon repens* (L.) DC. (Asteraceae) Uzbekistan *A. centaureae* (Nalepa) *Centaurea diffusa*, *C. stoebe* L. (Asteraceae) Austria (presumed) *Aceria chondrillae* Canestrini *Chondrilla juncea* L. (Asteraceae) USA and Argentina

*A. convolvuli* (Nalepa) *Convolvulus arvensis* L. (Convolvulaceae) Austria *A. cynodoniensis* Sayed *Cynodon dactylon* (L.) Pers. (Poaceae) Egypt *A. dissecti* Petanović *Geranium dissectum* L. (Geraniaceae) Serbia *A. drabae* (Nalepa) *Cardaria draba* (L.) Desv. (Brassicaceae) Austria *A. eleagnicola* Farkas *Elaeagnus angustifolia* L. (Elaeagnaceae) Hungary *A. galiobia* (Canestrini) *Galium mollugo* L., *G. verum* L. (Rubiaceae) Italy *A. geranii* (Canestrini) *Geranium dissectum* Italy *A. imperata* (Zaher & Abou-Awad) *Imperata cylindrica* (L.) Beauv. Egypt *A. jovanovici* Petanović *Lythrum salicaria* L. (Lythraceae) Serbia *A. meliae* (Dong & Xin) *Melia azedarach* L. (Meliaceae) China *A. mississippiensis* Chandrapatya & Baker *Geranium carolinianum* L. (Geraniaceae) Mississippi *A. salsolae* de Lillo & Sobhian *Salsola tragus* L. (Chenopodiaceae) Turkey

(Lamiaceae)

*A. salviae* (Nalepa) *Salvia pratensis* L., *S. verticillata* L.

(Asteraceae) Italy

Austria


**Table 2.** Eriophyid mites species used in biological control worldwide.

#### **8.** *Aceria lantanae* **vs.** *Lantana camara*

The lantana flower gall mite, *A. lantanae* is native to the Gulf of Mexico and it causes to its host plant to produce vegetative galls instead flowers. This tiny mite is about 0.15 mm long, beige and white in color. Mite feeding induces the flower bud develop into a 20-mm-diameter green gall and in high population levels mites form a mildew-like swarm on the surface of the gall. These galls act as nutrient sinks, which causes stunt vegetative growth and up to 90% reduction in seed production in susceptible varieties [31].

Also, two leaf vagrant eriophyid mites, *Shevtchenkella stefneseri* Craemer and *Paraphytoptus magdalenae* Craemer, were described from *L. camara* in Paraguay and Jamaica, however, so far only *A. lantanae* has shown to cause symptoms that could be used to control this plant [32].

#### **9.** *Floracarus perrepae* **vs.** *Lygodium microphyllum*

The Old World climbing fern, *Lygodium microphyllum* (Cav.) R. Br. (Lygodiaceae) is native to wet tropical and subtropical regions of Africa, Asia, Australia, and Oceania [33] and over recent decades has become a hugely problematic and rapidly spreading invasive weed of natural areas across much of southern Florida in the United States [34].

Management of *L. microphyllum* using fire or mechanical control have been ineffective, meanwhile chemical control is expensive, and not economically sustainable over the large areas already infested [35]. Thus, biocontrol is thought to be a more promising strategy for long-term management [33] and *Neomusotima conspurcatalis* Warren (Lepidoptera: Crambidae) has successfully established in Florida as a biological control of *L. microphyllum* [36-37].

Also, the leaf galling mite, *Floracarus perrepae* Knihinicki & Boczek (Eriophyidae) has been commonly found causing damage to this fern species during extensive foreign exploration within its native range [38]. Since then, several studies have been conducted to evaluate potentiality of this eriophyid mite to effectively control fern. Although *F. perrepae* successful colonized *L. microphyllum* field populations in Florida, the observed incidence was unexpect‐ edly low [37]. According to these authors, only 10% of *L. microphyllum* plants showed miteinduced leaf galls, and mite populations died out resulting in only 3% of infested plots after 12-14 months. However, the low rate of *F. perrepae* establishment was not due to failure of mites to transfer onto field plants but a variety of factors such as:

**Biological control agent Target plant Country**

(Pontederiaceae)

(Dipsacaceae)

*L. taraxaci* (Liro) *Taraxacum officinale* F. H. Wigg. (Asteraceae) Finland

*M. lepidifolii* Monfredo & de Lillo *Lepidium latifolium* L. Turkey

*P. cruttwellae* Keifer *Chromolaena odorata* Trinidad *P. euphorbiae* Farkas *Euphorbia cyparissias* L. (Euphorbiaceae) Hungary

*P. nevadensis* Roivainen *Euphorbia esula* L., *E. cyparissias* (Euphorbiaceae) Spain

*Rubus tomentosus* Borkh.

The lantana flower gall mite, *A. lantanae* is native to the Gulf of Mexico and it causes to its host plant to produce vegetative galls instead flowers. This tiny mite is about 0.15 mm long, beige and white in color. Mite feeding induces the flower bud develop into a 20-mm-diameter green gall and in high population levels mites form a mildew-like swarm on the surface of the gall. These galls act as nutrient sinks, which causes stunt vegetative growth and up to 90% reduction

Also, two leaf vagrant eriophyid mites, *Shevtchenkella stefneseri* Craemer and *Paraphytoptus magdalenae* Craemer, were described from *L. camara* in Paraguay and Jamaica, however, so far only *A. lantanae* has shown to cause symptoms that could be used to control this plant [32].

The Old World climbing fern, *Lygodium microphyllum* (Cav.) R. Br. (Lygodiaceae) is native to wet tropical and subtropical regions of Africa, Asia, Australia, and Oceania [33] and over recent decades has become a hugely problematic and rapidly spreading invasive weed of natural

Management of *L. microphyllum* using fire or mechanical control have been ineffective, meanwhile chemical control is expensive, and not economically sustainable over the large areas already infested [35]. Thus, biocontrol is thought to be a more promising strategy for long-term management [33] and *Neomusotima conspurcatalis* Warren (Lepidoptera: Crambidae) has successfully established in Florida as a biological control of *L. microphyllum* [36-37].

(Rosaceae) Germany (presumed)

Brazil

Finland

*L. eichhorniae* (Keifer) *Eichhornia crassipes* (Mart.) Solms

*L. knautiae* (Liro) *Dipsacus fullonum* L., *D. laciniatus* L.

**Table 2.** Eriophyid mites species used in biological control worldwide.

**8.** *Aceria lantanae* **vs.** *Lantana camara*

in seed production in susceptible varieties [31].

**9.** *Floracarus perrepae* **vs.** *Lygodium microphyllum*

areas across much of southern Florida in the United States [34].

*Metaculus* species

118 Weed Biology and Control

*Phyllocoptes* species

*P. gracilis* (Nalepa)


Distinct haplotypes of *L. microphyllum* and *F. perrepae* from populations across Southeast Asia and Australasia have been revealed from genetic testing of the fern and mite and these different genetic strains of mite and genetic forms of *L. microphyllum* mapped out together according to their geographic origin [39]. Thus, bioassays indicated that strains of *F. perrepae* performed best (were most able to induce leaf galls) on the local forms of *L. microphyllum* from which they were collected and presumably were best adapted [39].

High specificity and variations in mite performance and host plant resistance could make eriophyid agents may have difficulty suppressing all forms of a weed throughout its adventive range when both resistant and susceptible weed genotypes are present [25].

Limited broader establishment of *F. perrepae* strains would appear related to the apparent role of fern resistant genotypes, reflecting difficulties in weed biocontrol programs using this eriophyid mite. Hence it seems unlikely that *F. perrepae* will contribute substantially to suppression of *L. microphyllum* in Florida [36].

## **10. Could** *Aceria solstitialis* **be a prospective biological control agent versus** *Centaurea solstitialis***?**

Yellow starthistle, *Centaurea solstitialis* L. (Asteraceae), is native to the northern half of the Mediterranean and currently it has invaded the western USA displacing native plant com‐ munities, reducing plant diversity and forage production for livestock and wildlife [40]. The origin site of this plant species has been explored for prospective biological control agents. Recently an eriophyid mite, *Aceria solstitialis* de Lillo, Cristofaro & Kashefi was discovered damaging *C. solstitialis* in Turkey [41]. However, it is still unclear if *A. solstitialis* could be an effective biological control agent of yellow starthistle, since field and laboratory studies did not yield conclusive results on host specificity and damage level on this host plant [42]. According to these authors, mites remained live on *C. solstitialis*, *Centaurea cyanus* L., *Centaurea diffusa* Lam., *Carthamus tinctorius* L., and *Cynara scolymus* L. 60 days after the start of the experiment. This fact would suggest that *A. solstitialis* is not specific to feed on *C. solstitialis*. Moreover, although young and old *Ce. solstitialis* infested plants became yellow and withered, most of them produced flowers and seeds. Also, damage symptoms by mite feeding was verified on *C. scolymus*, a cultivated species thus hindering possibility of use this eriophyid mite in biological weed control programs. However more detailed studies should be addressed to determine the relationship of mite population size and time of infestation to damage host plants.

#### **11. Other mite groups used in biological control of weeds**

*Tetranychid mites*: Gorse, *Ulex europaeus* L. (Fabaceae), is a thorny shrub native to the temperate Atlantic coast of Europe. Gorse has proven to be an aggressive invader, forming impenetrable, largely monotypic stands that reduce access of grazing animals to fodder, modify native ecosystems and ecosystem processes, and outcompete trees in developing forests [43], mainly in Australia, Chile, New Zealand and the USA [44-46].

The gorse spider mite, *Tetranychus lintearius* (Dufour) is one of the few tetranychid mite species being used for the biological control of gorse in Australia and it is now widespread in Tasmania and Victoria and has become well established in South Australia and Western Australia [47]. Mite populations have shown rapidly increases in the countries where it was released, with colonies forming massive webs over gorse and causing severe bronzing of the foliage. However, populations of the gorse spider mite rarely cause severe damage to the target weed [48]. As previously discussed, natural control mechanisms can interfere with the establishment and development of high population densities that are considered desirable for classical biological control agents [49]. Probably, predators are the main contributors to biotic resistance of spider mites [50]. In this regard, although presence of mite colonies on gorse bushes over a period of 2.5 years from the time of release reduced foliage dry weight by around 36% in Tasmania [51], predation of *T. lintearius* colonies by *Stethorus* sp. and *Phytoseiulus persimilis* Athias Henriot [52], has limited efficacy of control of *T. lintearius* on gorse.

*Oribatid mites*: The water hyacinth, *Eichhornia crassipes* (Mart.) Solms (Pontederiaceae), is native of the Amazon basin [53] and whose capacity for growth and propagation causes major conservation problems with considerable socioeconomic repercussion [54]. Also, it has invaded fresh water bodies causing significant economic and ecological losses, being consid‐ ered to be the worst aquatic weed in South Africa [55]. Several biocontol agents have been used to diminish ecological impact of the plant species, being *Orthogalumna terebrantis* Wallwork (Acari: Oribatida) one of seven biocontrol agents used against the water hyacinth in South Africa and it is currently established at 17 out of the 66 recorded water hyacinth infestation sites across the country [56]. Field observations in South Africa indicate that during summer certain water hyacinth infestations may have more than 50% of the leaf surface area damaged by mite herbivory [56]. Feeding by the nymphs of this mite forms galleries between the parallel veins of the lamina which cause leaf discoloration and desiccation when high mite populations are reached, however it has not contributed to control of the weed [12].

#### **12. Conclusions**

**10. Could** *Aceria solstitialis* **be a prospective biological control agent versus**

Yellow starthistle, *Centaurea solstitialis* L. (Asteraceae), is native to the northern half of the Mediterranean and currently it has invaded the western USA displacing native plant com‐ munities, reducing plant diversity and forage production for livestock and wildlife [40]. The origin site of this plant species has been explored for prospective biological control agents. Recently an eriophyid mite, *Aceria solstitialis* de Lillo, Cristofaro & Kashefi was discovered damaging *C. solstitialis* in Turkey [41]. However, it is still unclear if *A. solstitialis* could be an effective biological control agent of yellow starthistle, since field and laboratory studies did not yield conclusive results on host specificity and damage level on this host plant [42]. According to these authors, mites remained live on *C. solstitialis*, *Centaurea cyanus* L., *Centaurea diffusa* Lam., *Carthamus tinctorius* L., and *Cynara scolymus* L. 60 days after the start of the experiment. This fact would suggest that *A. solstitialis* is not specific to feed on *C. solstitialis*. Moreover, although young and old *Ce. solstitialis* infested plants became yellow and withered, most of them produced flowers and seeds. Also, damage symptoms by mite feeding was verified on *C. scolymus*, a cultivated species thus hindering possibility of use this eriophyid mite in biological weed control programs. However more detailed studies should be addressed to determine the relationship of mite population size and time of infestation to damage host

**11. Other mite groups used in biological control of weeds**

Athias Henriot [52], has limited efficacy of control of *T. lintearius* on gorse.

in Australia, Chile, New Zealand and the USA [44-46].

*Tetranychid mites*: Gorse, *Ulex europaeus* L. (Fabaceae), is a thorny shrub native to the temperate Atlantic coast of Europe. Gorse has proven to be an aggressive invader, forming impenetrable, largely monotypic stands that reduce access of grazing animals to fodder, modify native ecosystems and ecosystem processes, and outcompete trees in developing forests [43], mainly

The gorse spider mite, *Tetranychus lintearius* (Dufour) is one of the few tetranychid mite species being used for the biological control of gorse in Australia and it is now widespread in Tasmania and Victoria and has become well established in South Australia and Western Australia [47]. Mite populations have shown rapidly increases in the countries where it was released, with colonies forming massive webs over gorse and causing severe bronzing of the foliage. However, populations of the gorse spider mite rarely cause severe damage to the target weed [48]. As previously discussed, natural control mechanisms can interfere with the establishment and development of high population densities that are considered desirable for classical biological control agents [49]. Probably, predators are the main contributors to biotic resistance of spider mites [50]. In this regard, although presence of mite colonies on gorse bushes over a period of 2.5 years from the time of release reduced foliage dry weight by around 36% in Tasmania [51], predation of *T. lintearius* colonies by *Stethorus* sp. and *Phytoseiulus persimilis*

*Centaurea solstitialis***?**

120 Weed Biology and Control

plants.

Various studies dealing with effectiveness of mites as biological agents of weed have shown variable results; however some of them clearly have the potential to play a significant role in the classical biological control. Field and laboratory observations have shown the debilitating effect of some mite species on its target plant, opening a gate to be explored in the future. Furthermore, additional aspects as plant genotype interaction with those biological control agents and also interaction with other biological control agents such as pathogens should be addressed to complement the action of the mite agents currently established on susceptible weedy varieties in order to improve biological control programs.

#### **Author details**

Carlos Vásquez1\*, Yelitza Colmenárez2 , José Morales-Sánchez1 , Neicy Valera1 , María F. Sandoval3 and Diego Balza1

\*Address all correspondence to: carlosvasquez@ucla.edu.ve

1 Department of Life Sciences. Faculty of Agronomy. Universidad Centroccidental Lisandro Alvarado. Barquisimeto, Lara State, Venezuela

2 CABI South America. UNESP-Fazenda Experimental LageadoBotucatu, São Paulo State, Brazil

3 National Institute of Agricultural Research. Plant Production Unit. Laboratory of Entomology. Maracay, Aragua State, Venezuela

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299-306.

## *Edited by Vytautas Pilipavičius*

This book is a collection of chapters, concerning the developments within the Weed Biology and Control field of study. The book includes scholarly contributions by various authors pertinent to Agricultural and Biological Sciences. Each contribution comes as a separate chapter complete in itself but directly related to the book's topics and objectives. The target audience comprises scholars and specialists in the field.

Weed Biology and Control

Weed Biology and Control

*Edited by Vytautas Pilipavičius*

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