Madelaine Venzon

Behaviour and indirect interactions in food webs of plant-inhabiting arthropods

With the increased use of biological control agents, artificial food webs are created in agricultural crops and the interactions between plants, herbivores and natural enemies change from simple tritrophic interactions to more complex food web interactions. Therefore, herbivore densities will not only be determined by direct predator–prey interactions and direct and indirect defence of plants against herbivores, but also by other direct and indirect interactions such as apparent competition, intraguild predation, resource competition, etc. Although these interactions have received considerable attention in theory and experiments, little is known about their impact on biological control. In this paper, we first present a review of indirect food web interactions in biological control systems. We propose to distinguish between numerical indirect interactions, which are interactions where one species affects densities of another species through an effect on the numbers of an intermediate species and functional indirect interactions, defined as changes in the way that two species interact through the presence of a third species. It is argued that functional indirect interactions are important in food webs and deserve more attention. Subsequently, we discuss experimental results on interactions in an artificial food web consisting of pests and natural enemies on greenhouse cucumber. The two pest species are the two-spotted spider mite Tetranychus urticae and the western flower thrips, Frankliniella occidentalis. Their natural enemies are the predatory mite Phytoseiulus persimilis, which is commonly used for spider mite control and the predatory mites Neoseiulus cucumeris and Iphiseius degenerans and the predatory bug Orius laevigatus, all natural enemies of thrips. First, we analyse the possible interactions between these seven species and we continue by discussing how functional indirect interactions, particularly the behaviour of arthropods, may change the significance and impact of direct interactions and numerical indirect interactions. It was found that a simple food web of only four species already gives rise to some quite complicated combinations of interactions. Spider mites and thrips interact indirectly through resource competition, but thrips larvae are intraguild predators of spider mites. Some of the natural enemies used for control of the two herbivore species are also intraguild predators. Moreover, spider mites produce a web that is subsequently used by thrips to hide from their predators. We discuss these and other results obtained so far and we conclude with a discussion of the potential impact of functional indirect and direct interactions on food webs and their significance for biological control.

Diet of a polyphagous arthropod predator affects refuge seeking of its thrips prey.

Antipredator behaviour of prey costs time and energy, at the expense of other activities. However, not all predators are equally dangerous to all prey; some may have switched to feeding on another prey species, making them effectively harmless. To minimize costs, prey should therefore invest in antipredator behaviour only when dangerous predators are around. To distinguish these from harmless predators, prey may use cues related to predation on conspecifics, such as odours released by a predator that has recently eaten conspecific prey or alarm pheromones released by attacked prey. We studied refuge use by a herbivorous/omnivorous thrips, Frankliniella occidentalis, in response to odours associated with a generalist predatory bug, Orius laevigatus, fed either with conspecific thrips or with other prey. The refuge used by thrips larvae is the web produced by its competitor, the two-spotted spider mite, Tetranychus urticae, where thrips larvae experience lower predation risk because the predatory bug is hindered by the web. Thrips larvae moved into this refuge when odours associated with predatory bugs that had previously fed on thrips were present, whereas odours from predatory bugs that had fed on other prey had less effect. We discuss the consequences of this antipredator behaviour for population dynamics. Copyright 2000 The Association for the Study of Animal Behaviour.

Functional response of the predator Eriopis connexa (Coleoptera: Coccinellidae) to different prey types

This work evaluated the functional response of adult females of Eriopis connexa to different densities of Macrosiphum euphorbiae and Tetranychus evansi. When preying upon aphids, E. connexa presented a sigmoidal functional response (Type III). This behavior, however, changed drastically to an exponential (Type II) functional response, when mites (T. evansi), rather than aphids, were offered to E. connexa. Such different patterns showed that this coccinellid needed to adopt distinct strategies according to the kind of prey available. Since predators were believed to be able to regulate prey populations only when adopting Type III functional response. E. connexa would be a good candidate for a biological control agent of M. euphorbiae, but would not suppress a growing population of T. evansi.

Attraction of a generalist predator towards herbivore-infested plants

The occurrence and strength of interactions among natural enemies and herbivores depend on their foraging decisions, and several of these decisions are based on odours. To investigate interactions among arthropods in a greenhouse cropping system, we studied the behavioural response of the predatory bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) towards cucumber plants infested either with thrips (Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)) or with spider mites (Tetranychus urticae Koch (Acari: Tetranychidae)). In greenhouse release‐recapture experiments, the predatory bug showed a significant preference for both thrips‐infested plants and spider mite‐infested plants over clean plants. Predatory bugs preferred plants infested with spider mites to plants with thrips. Experience with spider mites on cucumber leaves prior to their release in the greenhouse had no effect on the preference of the predatory bugs. However, this experience did increase the percentage of predators recaptured. Y‐tube olfactometer experiments showed that O. laevigatus was more attracted to odours from plants infested with spider mites than to odours from clean plants. Thus, O. laevigatus is able to perceive odours and may use them to find plants with prey in more natural conditions. The consequences of the searching behaviour for pest control are discussed.

Suitability of leguminous cover crop pollens as food source for the green lacewing Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae)

Diversification of crops with species that provide suitable pollen for predators may reduce pest population on crops by enhancing predator effectiveness. In this paper we evaluated the suitability of leguminous cover crop pollens to the predatory green lacewing Chrysoperla externa (Hagen). The predator is commonly found in coffee agroecosystems and the plant species tested were pigeon pea and sunn hemp, which are used in organic coffee systems. Newly emerged females and males of C. externa were reared on diets containing pollen of pigeon pea, sunn hemp, or castor bean, used as a control. The reproductive success of C. externa was evaluated when females fed the pollen species and when honey was added to the diets, to verify the predator need for an extra carbohydrate source. Similar intrinsic growth rates were found for females fed on pigeon pea pollen and on sunn hemp pollen but these rates increased significantly when honey was added to the diets. Females fed with pigeon pea pollen plus honey and with sunn hemp pollen plus honey had higher intrinsic growth rates than those fed with castor bean pollen plus honey. Females fed on castor bean pollen only or on honey only, did not oviposit. Leguminous pollen species were equally suitable for C. externa especially when they were complemented with honey. The results suggest that to successfully enhance predator effectiveness, organic coffee plantation should be diversified with plant providing pollen in combination with plant providing nectar.

Absence of odour‐mediated avoidance of heterospecific competitors by the predatory mite Phytoseiulus persimilis

Arthropods use odours associated with the presence of their food, enemies and competitors when searching for patches. Responses to these odours therefore determine the spatial distribution of animals, and are decisive for the occurrence and strength of interactions among species. Therefore, a logical first step in studying food web interactions is the analysis of behaviour of individuals that are searching for patches of food. We followed this approach when studying interactions in an artificial food web occurring on greenhouse cucumber in the Netherlands. In an earlier paper we found that one of the predators of the food web, the predatory mite Phytoseiulus persimilis Athias‐Henriot, used to control spider mites, discriminates between odours from plants with spider mites, Tetranychus urticae Koch, and plants with spider mites plus conspecific predators. The odours used for discrimination are produced by adult prey in response to the presence of predators, and probably serve as an alarm pheromone to warn related spider mites. Other predator species may also trigger production of this alarm pheromone, which P. persimilis could use in turn to avoid plants with heterospecific predators. We therefore studied the response of the latter to odours from plants with spider mites and 3 other predator species, i.e. the generalist predatory bug Orius laevigatus (Fieber), the polyphagous thrips Frankliniella occidentalis and the spider‐mite predator Neoseiulus californicus (McGregor). Both olfactometer and greenhouse release experiments yielded no evidence that P. persimilis avoids plants with any of the 3 heterospecific predators. This suggests that these predators do not elicit production of alarm pheromones in spider mites, and we argue that this is caused by a lack of coevolutionary history. The consequences of the lack of avoidance of heterospecific predators for interactions in food webs and biological control are discussed.

Use of odours by Cycloneda sanguinea to assess patch quality

Adult ladybirds are likely to encounter various species of prey when foraging for oviposition sites. Optimal oviposition theory predicts that females should lay eggs in those sites that are the most suitable for offspring development. Therefore, factors that directly affect offspring mortality, such as the presence of predators and food, are expected to play an important role in the assessment of patch profitability by ladybird predators. Using a Y‐tube olfactometer, we tested whether the predatory ladybird Cycloneda sanguinea L. (Coleoptera: Coccinellidae) can use volatile cues to assess patch profitability and avoid predator‐rich patches. We assessed the foraging behaviour of C. sanguinea in response to odours associated with tomato plants infested with a superior prey, Macrosiphum euphorbiae Thomas (Homoptera: Aphididae), and with an inferior prey, Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae), in the presence or absence of the heterospecific predator Eriopis connexa Mulsant (Coleoptera: Coccinellidae). Females of C. sanguinea significantly preferred plants infested by M. euphorbiae to plants infested by T. evansi and avoided odours emanating from plants on which E. connexa females were present. Our results show that C. sanguinea use volatile cues to assess patch profitability and to avoid patches with heterospecific competitors or intraguild predators.

Searching behaviour of an omnivorous predator for novel and native host plants of its herbivores: a study on arthropod colonization of eucalyptus in Brazil

Adaptation to novel host plants is a much‐studied process in arthropod herbivores, but not in their predators. This is surprising, considering the attention that has been given to the role of predators in host range expansion in herbivores; the enemy‐free space hypothesis suggests that plants may be included in the host range of herbivores because of lower predation and parasitism rates on the novel host plants. This effect can only be important if natural enemies do not follow their prey to the novel host plant, at least not immediately, thus allowing the herbivores to adapt to the novel host plant. Hence, depending on the speed with which natural enemies follow their prey to a new host plant, enemy‐free space on novel host plants may only exist for a limited period. This situation may presently be occurring in a system consisting of the herbivorous moth Thyrinteina arnobia Stoll (Lepidoptera: Geometridae) that attacks various species of Myrtaceae, such as guava (Psidium guajava L.) and jaboticaba (Myrciaria spp.), in Brazil. Since the introduction of eucalyptus (Myrtaceae) species into this country some 100 years ago, the moth has included this plant species in its host range and frequently causes outbreaks, a phenomenon that does not occur on the native host plant species. This suggests that the natural enemies that attack the herbivore on native species are not very effective on the novel host. We tested this hypothesis by studying the searching behaviour of one of the natural enemies, the omnivorous predatory bug Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae). When offered a choice between plants of the two species, the predators (originally collected in eucalyptus plantations) preferred guava to eucalyptus when both plant species were clean, infested with herbivores, or damaged by herbivores but with herbivores removed prior to the experiments. The bugs preferred herbivore‐damaged to clean guava, and showed a slight preference for damaged to clean eucalyptus. These results may explain the lack of impact of predatory arthropods on herbivore populations on eucalyptus and suggests that eucalyptus may offer an enemy‐free space for herbivores.

Interactions mediated by predators in arthropod food webs

Estudos sobre interacoes entre plantas, herbivoros e inimigos naturais sao importantes para o entendimento da dinâmica populacional das especies em teias alimentares, bem como para o sucesso do controle de pragas por inimigos naturais. Os programas de controle biologico fundamentam-se na ocorrencia de sucessoes troficas, onde a adicao de um inimigo natural causa o decrescimo na densidade da presa/hospedeiro e o aumento da biomassa da planta. Entretanto, quando mais de uma especie de inimigo natural e usada para controlar varias pragas no mesmo sistema, teias alimentares artificiais sao criadas e as interacoes tritroficas simples transformam-se em outras mais complicadas. A ocorrencia de interacoes complexas e de onivoria nestas teias alimentares pode modificar a direcao e a intensidade dos efeitos diretos dos inimigos naturais sobre as pragas. Neste artigo, sao apresentados e discutidos os resultados experimentais sobre interacoes mediadas por predadores em uma teia alimentar artificial. Esta teia e formada em plantas de pepino em casa de vegetacao onde o controle biologico e aplicado. A teia constitui-se de duas pragas, o acaro rajado Tetranychus urticae Koch e o tripes Frankliniella occidentalis (Pergande). Para o controle dos acaros rajados sao liberados os acaros predadores Phytoseiulus persimilis Athias-Henriot e Neoseiulus californicus (McGregor). O controle dos tripes e feito atraves de liberacoes do percevejo generalista Orius laevigatus (Fieber) e do acaro predador especialista Neoseiulus cucumeris (Oudemans). Resultados de estudos comportamentais mostraram que algumas destas especies sao atraidas para o mesma planta e nao evitam plantas ocupados por outras especies. Quando estas especies sao encontradas na mesma planta, interacoes complexas ocorrem: (a) predacao intraguilda de O. laevigatus sobre P. persimilis, (b) uso da teia produzida pelo acaro rajado pelas larvas de tripes como refugio contra seus predadores. As consequencias destas interacoes na dinâmica populacional dos predadores e das pragas e no sucesso do controle biologico sao discutidos.

Seletividade de extratos de nim (Azadirachta indica A. Juss.) ao ácaro predador Iphiseiodes zuluagai (Denmark & Muma) (Acari: Phytoseiidae)

The relative toxicity of the leaf, seed and oil neem cake extracts of Azadirachta indica A. Juss (neem) to the predatory mite Iphiseiodes zuluagai (Denmark & Muma) (Acari: Phytoseiidae) was evaluated. To verify the relative toxicity of these extracts on the predatory mite, discriminating concentrations of the extracts were determined for adult females of the Oligonychus ilicis (McGregor) (Acari: Tetranychidae), through the method of concentration-mortality. Coffee leaf disks with 3.5 cm of the diameter were put floating on water and impregnated with dry residue of the extracts. Concentrations of neem extracts which caused mortality (99%) of O. ilicis, after 72h of exposition, were 277.4; 520.9 e 10.9 mg/ml for leaf, seed and oil neem cake, respectively. The discriminating concentration of extract of oil neem cake for O. ilicis females was highly toxic to I. zuluagai; while extract of leaf and seed were selective to the predatory mite.