Habitat selection and potential antiherbivore effects of Peucetia flava (Oxyopidae) on Solanum thomasiifolium (Solanaceae).
Abstract: Several spider species use plants as shelter and foraging sites, but the relationships among these organisms are still poorly known. Lynx spiders of the genus Peucetia do not build webs, and many species live strictly in plants bearing glandular trichomes. Peucetia flava Keyserling 1877 inhabits Solanum thomasiifolium in southeastern Brazil and usually preys on herbivores and other small insects adhered to the glandular trichomes of its host plant. To evaluate the potential anti-herbivore protection of this spider species for S. thomasiifolium, we glued termites used as herbivore models on trichomes of S. thomasiifolium and on neighboring plants lacking glandular trichomes. Leaf miner damage and spider density were recorded for S. thomasiifolium plants in July 1997. There was a positive relationship between plant size and spider density. The removal of termites in S. thomasiifolium by P. flava was higher than in plants without glandular trichomes. The leaf miner damage was negatively related to spider density. Our results suggest that P. flava may be an important plant bodyguard in the defense of S. thomasiifolium from its natural herbivores.

Keywords: Animal-plant interactions, host plant specificity, lynx spider, plant protection
Article Type: Report
Subject: Spiders (Environmental aspects)
Spiders (Behavior)
Plant-animal interactions (Observations)
Habitat selection
Authors: Jacobucci, Giuliano B.
Medeiros, Lenice
Vasconcellos-Neto, Joao
Romero, Gustavo Q.
Pub Date: 09/01/2009
Publication: Name: Journal of Arachnology Publisher: American Arachnological Society Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2009 American Arachnological Society ISSN: 0161-8202
Issue: Date: Sept, 2009 Source Volume: 37 Source Issue: 3
Geographic: Geographic Scope: Brazil Geographic Code: 3BRAZ Brazil
Accession Number: 253537145
Full Text: It is widely known that several spider species use plants as shelter and foraging sites (Foelix 1996), but only in the last few decades have strict associations of spiders with particular plant types or species been described in detail. A variety of spider-plant associations has been described in the Neotropical regions (Barth et al. 1988; Dias & Brescovit 2004; Romero 2006). The associations typically occur because plants have morphological traits that provide suitable foraging, mating, and egg-laying sites for the spiders, shelter for adults and immatures, and nurseries for spiderlings (Romero & Vasconcellos-Neto 2005), thereby improving the probability of the spiders living on them. One of these associations includes jumping spiders (Salticidae) that are strictly associated with Bromeliaceae (Romero & Vasconcellos-Neto 2004a, 2004b, 2005; Romero 2006). For one of these associations, Romero et al. (2006) demonstrated through experiment that the jumping spider Psecas chapoda Peckham & Peckham 1894 contributed to 18% of the total nitrogen of its host terrestrial bromeliad Bromelia balansae, and in general, plants with spiders produced leaves 15% longer than plants from which the spiders were excluded.

Other associations involve spiders that forage on plants with glandular trichomes. For instance, at least 10 lynx spider species of the genus Peucetia (Oxyopidae) live strictly in several plant families and species bearing glandular trichomes in many distinct vegetation types in Neotropical, Nearctic, Palearctic, and Afrotropical regions. The main plant families used by these spiders are Solanaceae, Asteraceae, and Melastomataceae (Vasconcellos-Neto et al. 2007). The specialization of the Peucetia species for plants bearing glandular trichomes may have evolved because insects adhering to these sticky structures may be used as prey by the spiders (Vasconcellos-Neto et al. 2007). Although glandular hairs have probably evolved as a defense against herbivores and pathogenic fungi (Levin 1973, Duffey 1986), they can also mediate mutualistic interactions between plants and spiders or other predators (Dolling & Palmer 1991; Romero et al. 2008).

In South America, Peucetia rubrolineata Keyserling 1877 and P. flava Keyserling 1877 are the most common representatives of the genus. Both species are widely distributed throughout Brazil and occur sympatrically in several localities (Santos & Brescovit 2003; Vasconcellos-Neto et al. 2007). In a forest reserve in the state of Espirito Santo, southeastern Brazil, P. flava is frequently observed in association with Solanum thomasiifolium Sendtn. 1846, a solanaceous plant bearing glandular hairs (Vasconcellos-Neto et al. 2007). While investigating the occurrence of spiders on 70 individuals of S. thomasiifolium, we observed that all individuals were inhabited by P. flava, while none of their neighboring plants (n = 80) had spiders.

To understand this spider-plant interaction better, we addressed the following questions: 1) Is P. flava abundance related to S. thomasiifolium size? 2) Are insect predation rates by P. flava on S. thomasiifolium higher than predation rates by other predators (e.g., ants, other spiders) on neighboring plants without glandular hairs?

This study was performed in the Reserva Natural da Vale do Rio Doce (19[degrees]26'S, 40[degrees]03'W), 30 km north of the city of Linhares, state of Espirito Santo, a forest reserve covered mainly by Atlantic Forest vegetation. The reserve comprises 22,000 ha of forest, elev. 28-65 m above sea level, and a soil rich in sand. The weather is seasonal, with rainfall varying monthly from 30 mm in the dry season (June) to 226 mm in the wet season (January). Mean annual rainfall is 1320 mm. Temperature varies from 10[degrees] to 30[degrees] C (Jesus 1988). Samplings were done in July 1996 and July 1997, in a 4-ha area of common, nativo vegetation on sandy soil, dominated by cacti, bromeliads, herbs, and small shrubs (Peixoto & Gentry 1990).

[FIGURE 1 OMITTED]

To verify whether the abundance of Peucetia flava correlates to the size of Solanum thomasiifolium plants, we estimated the size of plants in a 50-m random transect, in each year by measuring the maximum height of branches with leaves, the maximum canopy diameter, and the perpendicular length to this diameter. These measures were then multiplied to estimate plant size in cubic meters. The number of spiders was recorded on each plant by inspecting branches, leaves, and stems. This relationship was tested using linear regression.

We assessed the effect of spiders as bodyguards on S. thomasiifolium by using termite workers as herbivore models. We used termites instead of leaf-mining larvae because the former are thicker and less tender and, thus, easier to manipulate. In addition, once we attached termites to the surface they were unable to fly; thus, we could accurately judge predation rate. Fifteen plants of S. thomasiifolium and an equal number of similarly-sized neighboring plants without glandular trichomes were randomly selected in the study area. Each plant received ten termites randomly positioned on leaves of different branches, and after 30 min we recorded the number of individuals removed. Termites were affixed with non-toxic white glue (Cascolar[R]) to plants without glandular hairs to prevent them from falling off. This glue had no influence on spider behavior (unpublished data, GQR). Additionally, previous studies have used similar methods for the same purpose and shown that this type of glue does not interfere with predatory (e.g., ant) behavior (e.g., Oliveira et al. 1987). All the plants were checked once during the experiment in an attempt to record predation events. The removal rate of termites from both plant types was compared using a t-test for independent samples.

[FIGURE 2 OMITTED]

To estimate the relationship between P. flava and herbivory on S. thomasiifolium, we calculated spider density and estimated leaf miner damage in July 1997. We evaluated leaf miner herbivory because it is the commonest kind of damage caused by herbivores on S. thomasiifolium in the study area (personal communication). Plants were randomly selected, and four branches of each individual were evaluated for leaf miner damage. The numbers of intact and damaged leaves were recorded for 20 plants, and the ratio between damaged and total leaves was calculated. Spider density was estimated as the ratio between the number of spiders and the plant size in cubic meters. The relationship was tested using linear regression. Data normality and homoscedasticity were verified. Logarithm transformations were applied when necessary prior to the analyses (Zar 1999).

Voucher specimens of the spiders collected (males and females) were deposited in the Arachnological Collection of the Laboratorio de Artropodes Peconhentos, Instituto Butantan, Sao Paulo (accession numbers: IBSP 12982, IBSP 12940, IBSP 12891, and IBSP 12887). Solanum thomasifolium exsiccates were deposited at Universidade Estadual de Campinas Herbarium (UEC-Herbarium).

In 1996, we examined 17 Solanum thomasiifolium plants and found 57 Peucetia flava individuals. In 1997, we recorded 694 spiders on 59 plants. Linear regressions indicated that spider abundance was positively correlated with plant size during both sampling periods (Figure 1). Figure 2 displays the results of the termite removal experiment on the 30 observed plants, with significantly higher predation rates on S. thomasiifolium than for other plants (t = 3.88; df = 28; P < 0.001). Peucetia flava accounted for 11 of the 17 termite predation events observed on S. thomasiifolium (Figure 3). The other six events were recorded on plants without glandular trichomes. Those termites were removed by ants (n = 4) and salticid spiders (n = 2).

Larger plants had more spiders, probably because they provided more suitable habitat sites for the spiders. In a study of salticid-bromeliad association, Romero et al. (2007) showed that Coryphasia monteverde Santos & Romero 2007 inhabited large rosettes of Aechmaea distichantha and suggested that these spiders may actively select their microhabitats based on host plant size. Additionally, large plants may also represent a more suitable resource for many insects that constitute the main prey of the spiders. This hypothesis was proposed by Romero & Vasconcellos-Neto (2004a), who reported that another bromeliad-dwelling salticid, Eustiromastix nativo Santos & Romero 2004, had a similar microspatial distribution on two bromeliad species, possibly because larger plants have a higher probability of being visited by insects as a result of their large surface area.

[FIGURE 3 OMITTED]

Although we have no replicates or exclusion experiments demonstrating the influence of spiders on leaf miner density, observational and correlative data associated with the experiment using termites as herbivore models suggest that P. flava might act as an important plant bodyguard. The higher predation rates of the termite prey models on S. thomasiifolium compared to species without glandular trichomes suggest that P. flava is a very active insect predator, apparently surpassing the performance of sympatric ants and salticid spiders.

The role of Peucetia species in the reduction of the herbivore population and its destructive impact has already been already demonstrated in studies with other plants. For instance, Louda (1982) has shown that P. viridans (Hentz 1832) can decrease herbivore damage to its host plant, Haplopappus venetus (Asteraceae). In addition, Romero et al. (2008) recently showed that P. flava and P. rubrolineata maintain mutualistic relationships with their host plant, Trichogoniopsis adenantha (Asteraceae), the spiders removing herbivores from their host plants and the glandular hairs of the plants improving the spiders' growth by facilitating predation on adhering insects.

In this study, we have provided evidence that the relationship between P. flava and S. thomasifolium might be mutualistic. However, more definite conclusions should be obtained in the future by using spider exclusion experiments in the field.

ACKNOWLEDGMENTS

The authors thank Prof. Dr. Marcelo de Oliveira Gonzaga and Prof. Dr. Adalberto Jose dos Santos for their comments and help in preparing this manuscript. This paper was supported by Curso de Pos-Graduacao em Ecologia, UNICAMP and CAPES.

Manuscript received 14 July 2008, revised 11 April 2009.

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Giuliano B. Jacobucci: Instituto de Biologia, Universidade Federal de Uberlandia, CEP 38400-902, Uberlandia, MG, Brazil. E-mail: jacobucci@inbio.ufu.br

Lenice Medeiros: Departamento do Patrimonio Genetico, Secretaria de Biodiversidade e Florestas, Ministerio do Meio Ambiente e da Amazonia Legal, CEP 70818-900, Brasilia, DF, Brazil

Joao Vasconcellos-Neto: Departamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, CEP 13083-970, CP 6109, Campinas, SP, Brazil

Gustavo Q. Romero: Departamento de Zoologia e Botanica, Instituto de Biociencias, Letras e Ciencias Exatas (IBILCE), Universidade Estadual Paulista, CEP 15054-000, Sao Jose do Rio Preto, SP, Brazil
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