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Interactions Mediated by Predators in Arthropod Food Webs

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Interactions Mediated by Predators in Arthropod Food Webs Março, 2001 Neotropical Entomolgy 30(1) 1 FORUM Interactions Mediated by Predators in Arthropod Food Webs MADELAINE VENZON1, ANGELO PALLINI2 AND ARNE JANSSEN3 1Centro Tecnológico da Zona da Mata, EPAMIG, Caixa postal 216, 36571-000, Viçosa, MG. 2Departamento de Biologia Animal, UFV, 36571-000, Viçosa, MG. 3Section Population Biology, University of Amsterdam, 1098 SM Amsterdam, The Netherlands. Neotropical Entomology 30(1): 1-9 (2001) Interações Mediadas por Predadores em Teias Alimentares de Artrópodes RESUMO - Estudos sobre interações entre plantas, herbívoros e inimigos naturais são importantes para o entendimento da dinâmica populacional das espécies em teias alimentares, bem como para o sucesso do controle de pragas por inimigos naturais. Os programas de controle biológico fundamentam- se na ocorrência de sucessões tróficas, onde a adição de um inimigo natural causa o decréscimo na densidade da presa/hospedeiro e o aumento da biomassa da planta. Entretanto, quando mais de uma espécie de inimigo natural é usada para controlar várias pragas no mesmo sistema, teias alimentares artificiais são criadas e as interações tritróficas simples transformam-se em outras mais complicadas. A ocorrência de interações complexas e de onivoria nestas teias alimentares pode modificar a direção e a intensidade dos efeitos diretos dos inimigos naturais sobre as pragas. Neste artigo, são apresentados e discutidos os resultados experimentais sobre interações mediadas por predadores em uma teia alimentar artificial. Esta teia é formada em plantas de pepino em casa de vegetação onde o controle biológico é aplicado. A teia constitui-se de duas pragas, o ácaro rajado Tetranychus urticae Koch e o tripes Frankliniella occidentalis (Pergande). Para o controle dos ácaros rajados são liberados os ácaros predadores Phytoseiulus persimilis Athias-Henriot e Neoseiulus californicus (McGregor). O controle dos tripes é feito através de liberações do percevejo generalista Orius laevigatus (Fieber) e do ácaro predador especialista Neoseiulus cucumeris (Oudemans). Resultados de estudos comportamentais mostraram que algumas destas espécies são atraídas para o mesma planta e não evitam plantas ocupados por outras espécies. Quando estas espécies são encontradas na mesma planta, interações complexas ocorrem: (a) predação intraguilda de O. laevigatus sobre P. persimilis, (b) uso da teia produzida pelo ácaro rajado pelas larvas de tripes como refúgio contra seus predadores. As conseqüências destas interações na dinâmica populacional dos predadores e das pragas e no sucesso do controle biológico são discutidos. PALAVRAS-CHAVE: Defesa de plantas, odor, atração, comportamento antipredador, predação intraguilda, controle biológico. ABSTRACT – Studies on interactions among plants, herbivores and natural enemies are important for understanding population dynamics of species in food webs, but they are also important for the practice of pest control with natural enemies. Biological control programs heavily rely on the occurrence of trophic cascades, where the addition of one natural enemy causes a decrease of pest densities and an increase of plant biomass. However, when more that one natural enemy is used to control various pests in the same system, artificial food webs are created and simple tritrophic interactions change to more complicated ones. The occurrence of complex interactions and omnivory in these food webs may modify the sign and the strength of direct effects of natural enemies on pests. In this paper, we show and discuss the experimental results on interactions mediated by predators in an artificial food web that occurs on cucumber plants in greenhouses where biological control is applied. The two pests in this food web are the two-spotted spider mite Tetranychus urticae Koch, and the western flower thrips Frankliniella occidentalis (Pergande). The predatory mites Phytoseiulus persimilis Athias-Henriot and Neoseiulus californicus (McGregor) are used to control spider mites, and the generalist predatory bug Orius laevigatus (Fieber) and a specialist predatory mite Neoseiulus cucumeris (Oudemans) are predators of thrips. Results from behavioural studies showed that some of these species are attracted to the same 2 Venzon et al. patch and do not avoid each other’s presence. We show some complex interactions arising from the meeting of these species: (a) the intraguild predation by O. laevigatus on P. persimilis, (b) the use of spider-mite web as a refuge by thrips larvae against their predators. The consequences of such interactions for population dynamics of predators and prey and their implications for success of biological control are discussed. KEY WORDS: Plant defence, odour, attraction, antipredator behavior, intraguild predation, biological control. Arthropod food webs are often complex and species are Besides having a numerical effect on prey through predation, rarely arranged in linear food chains consisting of plants, predators also have a functional effect on prey through herbivores and predators (DeAngelis et al. 1996, Polis & changes in predator attack rate and prey growth rate. These Strong 1996). The occurrence of omnivory and indirect so-called non-lethal effects cause severe consequences for interactions in these food webs can make especially difficult the dynamics of predators and prey (Schmitz et al. 1997, to assign species to distinct trophic levels. In a simple model Lima 1998), because the indirect effects mediated through proposed by Hairston et al. (1960) where each species in a changes in behavior may take place much more rapidly than food web is classified in one of three trophic levels, changes those due to numerical changes (Abrams 1984) and they affect in one trophic level cascade down to lower trophic levels, many more prey than the relatively small numbers that but this may not be true for more complex food webs. This is predators actually consume (Mittelbach, 1988). Although the because herbivore density and plant biomass affect and are majority of studies on interactions in food webs have affected by species that occupy more than one trophic level concentrated on numerical interactions, experiments and (Polis & Strong 1996). theory have shown that functional interactions can equal Feeding on more than one trophic level is a common numerical interactions in strength (Abrams 1995, 1996, phenomenon in ecological communities (Polis 1991, Diehl Menge 1997, Schmitz et al. 1997, Peckarsky & McIntosh 1993, Winemiller 1996). In arthropod food webs, many 1998, Peacor & Werner 2000). predators are generalists and they may not restrict their diets Plants too interact with other members of the food web, to herbivore species but feed also on other predators and for instance with the natural enemies of their herbivores. even on conspecifics (Sabelis 1992). Generalist predators Plants can arrest natural enemies through provision of food are therefore expected not only to interact with other predators or shelter and/or may facilitate prey searching of natural through competition for food, but in many cases also through enemies through the production of herbivore-induced plant intraguild predation. This is defined as the killing and eating volatiles signaling the presence of herbivores (see Sabelis et of species that otherwise use similar resources and are thus al. 1999 for a review). These volatiles vary considerably, potential competitors (Polis et al. 1989). If a generalist depending on plant and herbivore species (Sabelis and van predator preferentially feeds on other predators (intraguild de Baan 1983, Dicke and Sabelis 1988, Takabayashi et al. prey), an increase of herbivore populations is expected due 1991, Dicke 1999), on plant variety (Dicke et al. 1990, Dicke to lower numbers of the intraguild prey and/or due to the 1999), on age of plant tissue (Takabayashi et al. 1994, reduction of time and energy spent by the intraguild predator Scutareanu et al. 1997), and on degree of infestation (Turlings on the herbivores. et al. 1990, Scutareanu et al. 1997). However, the interaction Besides omnivory, indirect interactions in food webs may among plants and natural enemies of their herbivores is prone also modify the strength or even the sign of direct effects of to exploitation by other members of the food web: other natural enemies on herbivores (Wootton 1994). Numerical herbivores and omnivores could use the herbivore-induced indirect interactions occur when one species affects densities plant volatiles to find plants or use the food and shelter of another through an effect on the numbers, density or provided by the plant. Hence, to understand the evolution of biomass of an intermediate species (i.e. competition, apparent such interactions, it is essential to consider their effect in a competition, indirect effects of intraguild predation); food web context (Sabelis et al. 1999). functional indirect interactions emerge when changes in the Interactions such as indirect plant defense and predator way that two species interact occur through the presence of a avoidance by prey have spatial consequences since they cause third (i.e. induced resistance and susceptibility, indirect plant the redistribution of animals and therefore affect the defenses, avoidance of competition) (see Janssen et al. 1998 probability of species interacting. They also have in common for a review of indirect interactions). Direct interactions can that volatile chemical stimuli play an important role, which also be numerical and functional. Predation is a numerical is not
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