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Beneficial Effects of Flower-Dwelling Predators on Their Host Plant

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Beneficial Effects of Flower-Dwelling Predators on Their Host Plant Ecology, 85(2), 2004, pp. 446±457 q 2004 by the Ecological Society of America BENEFICIAL EFFECTS OF FLOWER-DWELLING PREDATORS ON THEIR HOST PLANT GUSTAVO Q. ROMERO1 AND JOAÄ O VASCONCELLOS-NETO Departamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), C.P. 6109, Campinas, SP, 13083-970 Brazil Abstract. We examined the effects of the sit-and-wait spider Misumenops argenteus (Thomisidae) on the herbivore assemblage and ®tness of the perennial woody shrub Tri- chogoniopsis adenantha (Asteraceae). Because crab spiders prey on both pollinators and phytophagous insects, they can have potentially negative and positive effects on plants. In a manipulative experiment using paired plants, spiders decreased the density of sucking and some endophagous herbivores on the leaves and capitula and reduced the number of damaged achenes produced by the plants. Damaged capitula had a higher proportion of fertilized achenes in plants with spiders than without spiders, but not undamaged capitula. These results indicate that M. argenteus exerted a double positive effect on seed production in T. adenantha. The effect of M. argenteus on herbivores may be taxon speci®c and vary among years with different herbivore abundances. Key words: Asteraceae; direct and indirect effects; ¯oral herbivory; phytophage assemblage; plant ®tness; pollination; seed predators; southeastern Brazil; thomisid spider; Trichogoniopsis ad- enantha; tri-trophic interactions. INTRODUCTION Rypstra 1995, Snyder and Wise 2001, Denno et al. 2002, Moran and Scheidler 2002), and indirectly en- Species that comprise a community may be linked hance plant ®tness (Ruhren and Handel 1999, Snyder directly or indirectly through interactions between re- and Wise 2001). However, other studies have shown sources and consumption (Polis and Winemiller 1996). that spiders or arti®cial models of spiders can prey upon In systems involving three trophic levels, such as (e.g., Morse and Fritz 1982, Morse 1993, 1999) or repel plants, herbivores, and predators, a trophic cascade de- pollinators (Bristowe 1958, Dukas 2001) or change the scribes the positive top-down effects of the third tro- ¯oral architecture so as to impede their access (Ott et phic level on the biomass, richness, or composition of al. 1998). Based on ®eld observations, Louda (1982) the producer species (Hairston et al. 1960, Wootton showed a balance between cost and bene®t effects of 1994, Menge 1995, Abrams et al. 1996, Polis et al. the green lynx spider, Peucetia viridans (Oxyopidae), 2000). Predators frequently have an impact on the den- to the plant Haplopappus venetus (Asteraceae). P. vir- sity, spatial distribution, and diversity of herbivore as- idans reduced the proportion of ¯owers pollinated by semblages, thereby altering the patterns and levels of one-third. However, the release of viable, undamaged herbivory in plant communities (Heads and Lawton seeds was higher on in¯orescence branches with spi- 1984, 1985, Thomas 1989, Spiller and Schoener 1990, 1994, Dial and Roughgarden 1995, Schmitz and Suttle ders than on those without. Although spiders belonging 2001). Predators on ¯owers can also exert a positive to several families commonly forage on ¯owers, with effect by enhancing plant reproductive rates through the exception of the Louda's study, their overall effects the consumption of ¯ower and fruit predators (Schem- on plant ®tness through interactions with pollinators ske 1980, Stephenson 1982, Del-Claro et al. 1996, and seed predators or ¯ower herbivores is largely un- Oliveira et al. 1999). However, if the predators prey known. on or chase away pollinators (Wolf et al. 1975, Elliott In the present study, the ¯ower-dwelling crab spider and Elliott 1991, Lima 1991, Dukas 2001), their pres- Misumenops argenteus (Thomisidae) was experimen- ence becomes costly for the plant. tally manipulated to determine its effects on the as- As third trophic level organisms, spiders can dimin- semblage of capitula (¯owerhead) herbivores and on ish herbivore insect abundance in both natural and the ®tness of the native plant, Trichogoniopsis aden- agroecosystems (reviewed in Wise 1993). Spiders can antha (Asteraceae, see Plate 1). M. argenteus preys on also diminish herbivory or seed predation in plants pollinators and phytophagous insects (Romero and (Louda 1982, Riechert and Bishop 1990, Carter and Vasconcellos-Neto, in press, a) and hence may directly and/or indirectly alter the densities and occupation pat- Manuscript received 30 May 2002; revised 28 April 2003; terns of herbivores and consequently interfere with the accepted 3 June 2003. Corresponding Editor: D. A. Spiller. balance of bene®cial and harmful interactions between 1 E-mail: [email protected] the plant and second trophic level components. The 446 February 2004 EFFECTS OF FLOWER-DWELLING PREDATORS 447 main questions addressed were: (1) Does M. argenteus affect the abundance of ¯ower herbivores and the dam- age they cause to the ¯ower structures of T. adenantha, and (2) does M. argenteus affect the plant's reproduc- tive output? METHODS Study site and organisms The study was done in the Ecological Reserve of the Serra do Japi (238119 S, 468529 W), a subtropical sem- ideciduous mesophilic forest in southeastern Brazil (el- evation ;1000 m), in mid to late summer (February and March) of 2000 and 2001. Trichogoniopsis adenantha (DC) is a small perennial PLATE 1. The crab spider Misumenops argenteus preying on a tephritid ¯y (Trupanea sp.) on the plant Trichogoniopsis shrub (up to 1.8 m high) with glandular trichomes adenantha (Asteraceae). Photo credit: JoaÄo Vasconcellos- (King and Robinson 1987) in which insects frequently Neto. become stuck (see Plate 1). This species is abundant along forest margins at the study site and blooms throughout the year, with a peak in the rainy season is always accompanied by much frass, which distin- (February to April). Each branch produces 2±7 asyn- guishes this damage from that other of phytophages. chronous capitula. Before fertilization, viable achenes The most common pollinators of T. adenantha at the are white in color, but turn black when fertilized. In a study site were the ithomiine butter¯ies Pseudoscada greenhouse, in the absence of ¯oral visitors, achenes erruca, Aeria olena, and Episcada carcinia (Nym- are not fertilized, indicating that plants require polli- phalidae), and several species of ctenuchine moths nators (Romero 2001). (Arctiidae), bees (Apoidea), and hover ¯ies (Syrphidae) T. adenantha capitula are visited by phytophagous (Romero 2001). insects and their parasitoids, as well as pollinators and The crab spider M. argenteus occurred frequently on pollen- and nectar-eating insects. Macrolophus ara- T. adenantha at the study site. It preferentially uses garcanus (Miridae, Heteroptera), aphids, and membra- ¯owering branches and capitula as foraging sites where cids (Homoptera) are the main sucking insects of the it preys on a variety of insects, including phytophagous plant (Romero 2001). The endophagous herbivores and pollinivorous/nectarivorous species (Appendix; were Trupanea sp. (Diptera, Tephritidae), Melanagro- Romero and Vasconcellos-Neto, in press, b). myza sp. (Diptera, Agromyzidae), Asphondylia sp. (co- rolla gall-maker) (Diptera, Cecidomyiidae) and Phal- Experimental design onidia unguifera (Lepidoptera, Tortricidae). Among The experiments described here were conducted endophagous species, Trupanea sp. and Melanagro- close to a natural population of T. adenantha. To de- myza sp. are most common (Romero 2001); adult fe- termine the effects of M. argenteus on the herbivore males oviposit in the ¯oral primordia and their larvae species and on T. adenantha, paired plants were set out feed within the capitula on immature achenes (Almeida along a forest margin, one of which received a single 1997). These Diptera are frequently parasitized by spe- spider and the other did not. The experiments were cies of Braconidae and Chalcidoidea (Hymenoptera). carried out in February±March of 2000 and 2001, and In addition, a common exophagous geometrid larvae used, respectively, 24 and 22 plant pairs, with a dif- (unidenti®ed species) consumes ¯oral tissue, including ferent set of plants each year. For each experiment, 20± achenes and bracts. 40 cm high plants with a single vegetative branch were Achenes in capitula attacked by Trupanea sp. have collected in the ®eld and transplanted to pots (25 cm a comma shape (Romero 2001) and are grouped in a diameter, 18 cm high) with soil from the same place palisade in the center of the capitulum. The puparia of and depth (of margins) to minimize ``bottom-up'' ef- this species are black and opaque (Almeida 1997). fects. When ¯oral primordia appeared, plants were set Achenes in capitula attacked by Melanagromyza sp. do out in pairs (blocks) in the experimental area (0.2 ha) not form a comma, although it also uses the central before the capitula could be colonized by their spe- achenes. Its puparia are light brown and translucent cialized herbivores. A distance of 0.5±1.0 m separated (Almeida 1997). Geometrid damage to achenes is rec- paired plants along the forest margin, and each pair ognized by the removal of the apical region, including was at least 2 m away from its neighbors. One member the pappus, which rarely occurs with endophages. of a pair was chosen randomly to receive a single ®eld- Young geometrid larvae feed on many stigmas and collected M. argenteus (spider-present treatment), and some corollas, but 4th and 5th instars generally
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