Tritrophic System Research Articles

Attraction of parasitic wasps by caterpillar-damaged plants.

Plant volatiles emitted in response to herbivory have been suggested to function as signals to attract natural enemies of herbivores. Most known examples of induced plant volatiles used by natural enemies involve parasitoids that locate caterpillars by means of odours emitted by plants after caterpillar attack. We study the tritrophic system that comprises the parasitoid Cotesia marginiventris, host caterpillars from the genus Spodoptera, and maize plants. Among the volatiles emitted by caterpillar-damaged maize plants, sesquiterpenes and indole are particularly attractive to the parasitoid. The usefulness of these plant volatiles for parasitoids is obvious. Less clear is their benefit to plants that emit them, as in most cases parasitization does not immediately stop caterpillars from damaging plants. However, plants appear to benefit directly from attracting C. marginiventris, as parasitized caterpillars consume considerably less plant tissue than unparasitized caterpillars. It is expected that in systems where parasitoids significantly reduce herbivory, they have contributed to selective pressures that have shaped the phenomenon of herbivore-induced volatile emissions by plants.

Eco-social analysis of an East African agro-pastoral system: Management of tsetse and bovine trypanosomiasis

A key constraint for development of many East African agro-pastoral communities is African animal trypanosomiasis or nagana caused by Trypanosoma spp. and vectored by species of tsetse flies ( Glossina spp.). Suppression of trypanosomiasis through trapping of tsetse fly populations was conducted from 1995 to 2005 at and near Luke, Southwest Ethiopia. Odor baited mass trapping technology was used to suppress adult fly populations to very low levels while tryponocidal drugs were used to treat trypanosome infections in cattle. Data on ecological, economic and social variables were collected and analyzed in the context of eco-social dynamics in the community. The bio-economic model of Regev et al. [Regev, U., Gutierrez, A.P., Schreiber, S.J., Zilberman, D., 1998. Biological and Economic Foundations of Renewable Resource Exploitation. Ecological Economics 26, 227-242] and Gutierrez and Regev [Gutierrez, A.P., Regev, U., 2005. The bioeconomics of tritrophic systems: applications to invasive species. Ecological Economics 52, 382-396] was used as a methodological framework for qualitative evaluation of the effects of tsetse/trypanosomiasis suppression on ecological, economic and social aspects. An objective function for single farmers was formulated to determine the optimal harvesting level of cattle, exposed to high and low levels of risk from tsetse/trypanosomiasis, as measured by the discount rate ( δ) for a given base level pastoral resource ( R = pasture or forage for cattle). The socially optimal objective function for resource exploitation by all farmers is that which maximizes the present value of utility of individuals expending revenues ( consumption) from the revenue stream in ways that enhance the quality of life and yet assures the persistence of the resource base over an infinite time horizon (i.e., renewable resource sustainability). The bio-economic model predicts that reducing risk ( δ) from tsetse and disease increased the cattle populations and their marginal value. The model also predicts that the interaction of decreased δ and increased productivity ( θ) can lead to increased human and cattle populations and hence to over-exploitation of base resources (pastures) that lower environmental carrying capacity and reduced sustainability. Trap catches indicated that tsetse populations were reduced to very low levels, while the disease prevalence decreased from 29% to 10%. This led to a substantial increase in cattle including oxen populations, increased calving rates, increased milk production and increased the per-capita income. The availability of oxen allowed an increase in cultivated land from 12 ha in 1995 to 506 ha in 2005. Revenues ( consumption) were invested in the purchase of more cattle and the establishment of a school for educating village children. Increases in land allocated to crops and other sources of income were also found. The bioeconomic model predicts the solution of the trypanosomiasis problems so transforms the East African agro-pastoral communities that new social structures will be required to cope with the ecological, economic and social consequences of this technological changes on sustainable development ( sensu [Goodland, R., 1995. The concept of environmental sustainability. Annual Review of Ecology and Systematics 26, 1-24]). This insight should not be lost in international rural development programs.

Ozone Degrades Common Herbivore-Induced Plant Volatiles: Does This Affect Herbivore Prey Location by Predators and Parasitoids?

Inducible terpenes and lipoxygenase pathway products, e.g., green-leaf volatiles (GLVs), are emitted by plants in response to herbivory. They are used by carnivorous arthropods to locate prey. These compounds are highly reactive with atmospheric pollutants. We hypothesized that elevated ozone (O(3)) may affect chemical communication between plants and natural enemies of herbivores by degrading signal compounds. In this study, we have used two tritrophic systems (Brassica oleracea-Plutella xylostella-Cotesia plutellae and Phaseolus lunatus-Tetranychus urticae-Phytoseiulus persimilis) to show that exposure of plants to moderately enhanced atmospheric O(3) levels (60 and 120 nl l(-1)) results in complete degradation of most herbivore-induced terpenes and GLVs, which is congruent with our hypothesis. However, orientation behavior of natural enemies was not disrupted by O(3) exposure in either tritrophic system. Other herbivore-induced volatiles, such as benzyl cyanide, a nitrile in cabbage, and methyl salicylate in lima bean, were not significantly reduced in reactions with O(3). We suggest that more atmospherically stable herbivore-induced volatile compounds can provide important long-distance plant-carnivore signals and may be used by natural enemies of herbivores to orientate in O(3)-polluted environments.

Crop domestication creates a refuge from parasitism for a native moth

Summary Insect herbivores are generally more abundant in agro‐ecosystems than in natural ecosystems. One possible cause is that artificial selection of crop plants may have disrupted parasitoid–herbivore interactions. We studied a native tritrophic system to determine if crop domestication has created a refuge for the sunflower moth Homoeosoma electellum from its major parasitoid Dolichogenidea homoeosomae. Parasitoid foraging behaviour on infested wild and agricultural sunflowers was studied using event‐recording software. We used detailed observations on larval feeding location and parasitoid probing behaviour to determine if the lower parasitism on agricultural sunflowers was the result of a structural refuge or a change in parasitoid foraging behaviour. Greater than 20 times more larvae fed on seeds of agricultural sunflowers than on seeds of wild sunflowers. Seed‐feeding enabled larvae to escape parasitoids because their ovipositors were too weak to penetrate the seed. As a consequence, larvae were more likely to be parasitized on wild sunflowers than on agricultural sunflowers, and floret‐feeding larvae were more likely to be parasitized than seed‐feeding larvae. Parasitoids were more stimulated to probe for larvae on wild sunflowers than on agricultural sunflowers. However, they responded to larval feeding location rather than plant genotype. Thus lower parasitism on agricultural sunflowers was due to a structural refuge for larvae rather than a change in parasitoid foraging behaviour. Synthesis and applications. Crop domestication has created a structural refuge from parasitism. The presence of refuges on agricultural plants helps explain why some insects are difficult to regulate using biological control. Studying parasitoid activity on wild relatives of agricultural plants can identify how plant variation contributes to the creation of a refuge. Beneficial plant traits can then potentially be bred back into the crop germplasm in order to enhance the biological control of insect pests in agroecosystems.

Olfactory mediated interactions between Citrus aurantium Toxoptera citricida and Lysiphlebus testaceipes

The objective of this study was to establish whether there are olfactory interactions in the Lysiphlebus testaceipes Toxoptera citricida and Citrus aurantium tritrophic system. The response of male and female L. testaceipes to different odour sources of the host plant C. aurantium, the aphid host T. citricida and aphid-plant complex were investigated using a Y-tube olfactometer. Laboratory experiments were conducted by exposing individually aged male and female L. testaceipes to eight different odour treatments. Response of the parasitoids was taken after 15 min exposure to the volatiles from the different odour sources and based on their orientation to the particular chamber. Seventy percent of both male and female L. testaceipes showed high attractivity to aphid infested leaves. There was no significant difference based on age and sex of the parasitoid on their choice of odour. The organic compounds released by these combinations acted as semiochemicals in the tritrophic interactions and it is suggested that insect feeding induced attraction of the parasitoid L. testaceipes.

Comparing the impact of conventional pesticide and use of a transgenic pest‐resistant crop on the beneficial carabid beetle Pterostichus melanarius

The potential impact of a chemical pesticide control method has been compared with that of transgenic plants expressing a protease inhibitor conferring insect resistance by utilising a tritrophic system comprising the crop plant Brassica napus (L.) (Oilseed rape), the pest mollusc Deroceras reticulatum (Müller) and the predatory carabid beetle Pterostichus melanarius (Illiger). Cypermethrin, as the most widely used pesticide in UK oilseed rape (OSR) cultivation, was selected as the conventional treatment. OSR expressing a cysteine protease inhibitor, oryzacystatin-1 (OC-1), was the transgenic comparator. In feeding trials, D. reticulatum showed no significant long-term effects on measured life history parameters (survival, weight gain, food consumption) as a result of exposure to either the cypermethrin or OC-1 treatment. However, D. reticulatum was able to respond to the presence of the dietary inhibitor by producing two novel proteases following exposure to OC-1-expressing OSR. Similarly, P. melanarius showed no detectable alterations in mortality, weight gain or food consumption when feeding on D. reticulatum previously fed either pesticide-contaminated or GM plant material. Furthermore, as with the slug, a novel form of protease, approximately M(r) 27 kDa, was induced in the carabid in response to feeding on slugs fed OC-1-expressing OSR.

Consequences for a specialist insect and its parasitoid of the response of Allium porrum to conspecific herbivore attack

Recent studies on the leek Allium porrum L. demonstrate that a sharp increase in the release of volatile and nonvolatile sulphur compounds occurs in response to attack by the specialist phytophage, the leek moth Acrolepiopsis assectella (Zeller). The consequences of that response on the developmental capacity and behaviour of the leek moth and on the host-searching behaviour of the parasitoid hymenoptera Diadromus pulchellus Wesmael have been studied. No immediate adverse effect on larval development is seen, but the duration of male development is significantly longer. In addition, an almost 20% decrease is observed in the number of oocytes produced by adult females that developed on attack-damaged leek plants. Leek moths do not avoid damaged plants system- atically. On attacked plants, larvae tend to consume more and females to lay more eggs, although the latter tendency disappears after intensive attack. Concerning host-searching by D. pulchellus, the data indicate that females make use of the induced leek response. Parasitoids are attracted more strongly to attacked plants than to undamaged plants and mechanically damaged plants. The results of this study in a tritrophic system involving a biannual plant suggest a complex defence system combining direct and indirect mechanisms. Sulphur compounds may act by reducing second-generation pests, thereby preventing the specialist insect population from exploding at the expense of the leek.

Interactions among species in a tri-trophic system: the influence of ants on the distribution of the Sinai Baton Blue butterfly

Metapopulation dynamics is now so widely used to describe the distribution and abundance of species living in fragmented landscapes that other ecological factors (e.g. habitat quality) can be overlooked. To determine the precise habitat requirements of an endangered and narrowly endemic lycaenid butterfly, I studied its distribution within a patch of habitat, examining the effects of hostplant choice on larval survival. Ovipositing females were selective in the hostplants chosen: they selected a brief stage of flower-bud development, and preferred plants with many inflorescences. The distribution of surviving larvae was positively correlated to the presence of an attendant ant, suggesting that this ant caused their distribution. However, closer examination of the interactions occurring among species within the tri-trophic system revealed that another species of ant exerted a much stronger influence on larval survival and therefore the distribution of newly eclosed adults.

Bottom‐up trophic cascades and material transfer in terrestrial food webs

AbstractIn contrast to top‐down trophic cascades, few reviews have appeared of bottom‐up trophic cascades. We review the recent development of research on bottom‐up cascades in terrestrial food webs, focusing on tritrophic systems consisting of plants, herbivorous insects, and natural enemies, and attempt to integrate bottom‐up cascade and material transfer among trophic levels. Bottom‐up cascades are frequently reported in various tritrophic systems, and are important to determine community structure, population dynamics, and individual performance of higher trophic levels. In addition, we highlight several features of bottom‐up cascades. Accumulation or dilution of plant nutritional and defensive materials by herbivorous insects provides a mechanistic base for several bottom‐up cascades. Such a stoichiometric approach has the potential to improve our understanding of bottom‐up cascading effects in terrestrial food webs. We suggest a future direction for research by integration of bottom‐up cascades and material transfer among trophic levels.

Genetic variation in response to an indirect ecological effect

Indirect ecological effects (IEEs) are widespread and often as strong as the phenotypic effects arising from direct interactions in natural communities. Indirect effects can influence competitive interactions, and are thought to be important selective forces. However, the extent that selection arising from IEEs results in long-term evolutionary change depends on genetic variation underlying the phenotypic response-that is, a genotype-by-IEE interaction. We provide the first data on genetic variation in the response of traits to an IEE, and illustrate how such genetic variation might be detected and analysed. We used a model tri-trophic system to investigate the effect of host plants on two populations of predatory ladybirds through a clonal aphid herbivore. A split-family experimental design allowed us to estimate the effects of aphid host plant on ladybird traits (IEE) and the extent of genetic variation in ladybird predators for response to these effects (genotype-by-indirect environmental effect interaction). We found significant genetic variation in the response of ladybird phenotypes to the indirect effect of host plant of their aphid prey, demonstrating the potential for evolutionary responses to selection arising from the prey host.

Oak gall wasp communities: Evolution and ecology

Summary Oak cynipids initiate the growth of highly complex galls on plants in the genus Quercus and related genera in the family Fagaceae. These galls support closed communities consisting of high diversities of gall inducers, inquilines and natural enemies. Much research has focussed on oak cynipid communities and they offer significant potential as model tritrophic systems. Nevertheless, key questions regarding their evolution and ecology remain unanswered. (1) Communities associated with different gall wasps vary in composition and structure, but little is known about the processes generating such variation. In particular, the role that phylogeography of component species plays remains unclear. (2) Gall traits (such as structure, location, and phenology) may play important roles in community diversity, but there is little empirical evidence of this. (3) The role of competition in oak cynipid communities is poorly understood. Many oak cynipids share natural enemies, and indirect apparent competition for the avoidance of shared natural enemies may occur between gall wasp species. In addition, direct competition for limiting resources may occur between gall inducers and between their parasitoids. We summarise current understanding of oak cynipid communities, discuss the issues raised above and outline key questions for further research.

Antennal Electrophysiological Responses of Three Parasitic Wasps to Caterpillar-Induced Volatiles from Maize (Zea mays mays), Cotton (Gossypium herbaceum), and Cowpea (Vigna unguiculata)

Many parasitic wasps are attracted to volatiles that are released by plants when attacked by potential hosts. The attractiveness of these semiochemicals from damaged plants has been demonstrated in many tritrophic systems, but the physiological mechanisms underlying the insect responses are poorly understood. We recorded the antennal perception by three parasitoids (Cotesia marginiventris, Microplitis rufiventris, and Campoletis sonorensis) to volatiles emitted by maize, cowpea, and cotton plants after attack by the common caterpillar pest Spodoptera littoralis. Gas chromatography-electroantennography (GC-EAG) recordings showed that wasps responded to many, but not all, of the compounds present at the physiologically relevant levels tested. Interestingly, some minor compounds, still unidentified, elicited strong responses from the wasps. These results indicate that wasps are able to detect many odorant compounds released by the plants. It remains to be determined how this information is processed and leads to the specific behavior of the parasitoids.

Prey–predator mutualism in a tritrophic system on a camphor tree

AbstractWe report the discovery of a mutualistic system encompassing prey–predator interactions. A domatium is a small space in a vein axil on the underside of leaves of woody angiosperms. Cinnamomum camphora Linn. has domatia that harbor a microphytophagous eriophyid mite (sp. 1). We previously reported that a predatory mite, Euseius sojaensis (Ehara), depends on this eriophyid mite as food. We revealed that E. sojaensis also preyed upon another eriophyid mite (sp. 2) that induces galls on leaves, and that the mean area of C. camphora leaves with galls was usually less than half that of leaves without galls. We experimentally tested the effect of E. sojaensis on galls, and confirmed that the presence of E. sojaensis reduced gall induction. Therefore, C. camphora, eriophyid mite sp. 1, and E. sojaensis comprise a mutualistic system, in spite of the prey–predator interactions among them. The conventional concept of mutualism does not apply to such prey–predator interactions, so we defined them as “systematic mutualism.” Here, the system consists of three trophic levels, and individuals that constitute this system benefit from the other species that constitute this system.

Adaptive omnivory and species coexistence in tri-trophic food webs

The commonness of omnivory in natural communities is puzzling, because simple dynamic models of tri-trophic systems with omnivory are prone to species extinction. In particular, the intermediate consumer is frequently excluded by the omnivore at high levels of enrichment. It has been suggested that adaptive foraging by the omnivore may facilitate coexistence, because the intermediate consumer should persist more easily if it is occasionally dropped from the omnivore's diet. We explore theoretically how species permanence in tri-trophic systems is affected if the omnivore forages adaptively according to the “diet rule”, i.e., feeds on the less profitable of its two prey species only if the more profitable one is sufficiently rare. We show that, compared to systems where omnivory is fixed, adaptive omnivory may indeed facilitate 3-species persistence. Counter to intuition, however, facilitation of 3-species coexistence requires that the intermediate consumer is a more profitable prey than the basal resource. Consequently, adaptive omnivory does not facilitate persistence of the intermediate consumer but enlarges the persistence region of the omnivore towards parameter space where a fixed omnivore would be excluded by the intermediate consumer. Overall, the positive effect of adaptive omnivory on 3-species persistence is, however, small. Generally, whether omnivory is fixed or adaptive, 3-species permanence is most likely when profitability ( = conversion efficiency into omnivores) is low for basal resources and high for intermediate consumers.

The bioeconomics of tritrophic systems: applications to invasive species

Adapted species in nature are assumed to have solved renewable resource management problems, and this is examined here using a physiologically based model of energy acquisition and allocation. Newly established invasive species are merely in an early phase of this process in their new environment. Analogies between the economies of humans and other species are used to develop an objective function for individual utility of energy allocation. The objective function includes the physiologically based population dynamics models of the consumer and resource species in a food chain as constraints. The model applies to all trophic levels in a food chain including human harvesting of renewable resources (see also Regev et al. (Regev, U., Gutierrez, A.P., Schreiber, S., Zilberman, D., 1998. Biological and Economic Foundation of Renewable Resource Exploitation. Ecological Economics. 26 (3), 227-242.)). Specifically, the analysis: (1) Attempts to combine ecological and economic theory; (2) Points out the importance of time frame in the two economies (evolutionary vs. market time); (3) Examines the effects of expected uncertainty due to environmental hazards in defining energy acquisition and allocation strategies in two invasive aphid species at the extremes of so called r- and K-strategies and the well adapted Central American cotton–cotton bollweevil system; (4) Evaluates the effects of changes in behavioral and physiological parameters and environmental degradation on the abundance of resource and consumer species.

Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie

BackgroundCoevolution between pairs of antagonistic species is generally considered an endless "arms race" between attack and defense traits to counteract the adaptive responses of the other species.Presentation of the hypothesisWhen more than two species are involved, diffuse coevolution of hosts and parasitoids could be asymmetric because consumers can choose their prey whereas preys do not choose their predator. This asymmetry may lead to differences in the rate of evolution of the antagonistic species in response to selection. The more long-standing the coevolution of a given pair of antagonistic populations, the higher should be the fitness advantage for the consumer. Therefore, the main prediction of the hypothesis is that the consumer trophic level is more likely to win the coevolution race.Testing the hypothesisWe propose testing the asymmetry hypothesis by focusing on the tritrophic system plant/aphid/aphid parasitoid. The analysis of the genetic variability in the virulence of several parasitoid populations and in the defenses of several aphid species or several clones of the same aphid species could be compared. Moreover, the analysis of the neutral population genetic structure of the parasitoid as a function of the aphid host, the plant host and geographic isolation may complement the detection of differences between host and parasitoid trophic specialization.Implications of the hypothesisGenetic structures induced by the arms race between antagonistic species may be disturbed by asymmetry in coevolution, producing neither rare genotype advantages nor coevolutionary hotspots. Thus this hypothesis profoundly changes our understanding of coevolution and may have important implications in terms of pest management.

Information use by the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae), a specialised natural enemy of herbivorous spider mites

Plants can respond to infestation by herbivores with the emission of specific herbivore-induced plant volatiles. Many carnivorous arthropods that feed on herbivorous prey use these volatiles to locate their prey. Despite the growing amount of research papers on the interactions in tritrophic systems, it has remained unclear how carnivorous arthropods use herbivore-induced plant volatiles in prey-location. We investigated three important aspects of information use by the predatory mite Phytoseiulus persimilis, a specialised natural enemy of herbivorous spider mites. First, we showed that the foraging efficiency of predatory mites was not hampered by the presence of volatiles induced by nonprey caterpillars on brussels sprouts plants. Second, we revealed an important role for the volatile compound methyl salicylate. Predatory mites appear to use the presence of this compound, rather than its relative contribution to a volatile blend, to discriminate between two volatile blends. Third, we demonstrated that the role of methyl salicylate in the foraging behaviour of P. persimilis depends on previous experiences of the predators with this compound. Our research improves the understanding of the selection pressures that act on the foraging responses of carnivorous arthropods, and consequently on the selection pressures on volatile emission by plants in response to herbivory.

Reciprocal effects of host plant and natural enemy diversity on herbivore suppression: an empirical study of a model tritrophic system

Many theoretical and empirical studies have shown that species diversity in a trophic level can impact the capture of limited resources in ways that cascade up or down a food web. Only recently, however, have ecologists begun to consider how diversity at multiple trophic levels might act in concert to have opposing or reinforcing effects on resource use. Here, we report the results of an empirical study of a model, tritrophic food web in which we manipulated the diversity of host plant species (Medicago sativa,Trifolium pratenseandVicia faba) and natural enemy species (Harmonia axyridis,Coleomegilla maculataandNabissp.) of a widespread herbivorous pest (the pea aphid,Acyrthosiphon pisum) in laboratory microcosms. We found that increasing natural enemy richness from one to three species increased the proportion of aphids consumed by 0.14. This effect of enemy diversity was due to facilitative interactions and/or a reduction in intraspecific competition in the more diverse assemblages. We also found an independent and additive main effect of host plant richness, with the proportion of aphids consumed by natural enemies decreasing by 0.14 in plant polycultures. A reduction in predator efficiency on a single host plant,Vicia faba, appeared to be responsible for this plant diversity effect. Aphid population sizes were, therefore, simultaneously determined by a top‐down effect of natural enemy diversity, and an opposing bottom‐up effect of host plant diversity that modified enemy–prey interactions. These results suggest that population sizes in nature, and biotic controls over insect pests, are influenced by species diversity at multiple trophic levels.

Bottom‐up and top‐down effects in a tritrophic system: the population dynamics of Plutella xylostella (L.)–Cotesia plutellae (Kurdjumov) on different host plants

Abstract. 1. The effects of host‐plant resistance on the population dynamics of the Diamondback moth, Plutella xylostella L., and its solitary parasitoid, Cotesia plutellae (Kurdjumov), were studied in replicated time‐series experiments.2. Host‐plant resistance did not affect the equilibrial abundance of the Diamondback moth, but it affected the dynamics of Diamondback moth populations.3. The mean population size of Diamondback moth showed no significant difference between Brassica rapa (a susceptible host plant) and Brassica napus (a partially resistant host plant) either in the presence or absence of the parasitoid.4. Time‐series analysis suggests that the dynamics of Diamondback moth on B. rapa were underpinned by delayed density‐dependent processes. In contrast, the dynamics of the moth on B. napus were influenced by a direct density‐dependent process.5. Although measures of short‐term parasitism showed a significantly higher rate of parasitism by C. plutellae on Diamondback moth feeding on B. napus compared with B. rapa, this individual performance does not translate into differences in the population dynamics. Analysis shows no significant difference in the persistence time of the population‐level interaction between the host and parasitoid on the two different host plants.

Host Location of a Pupal Parasitoid in a Tritrophic System Compared to a Model Offering Mechanosensory Cues Only

Several species of hymenopteran parasitoids are able to locate concealed pupal hosts by vibrational sounding. However, the specific role of this technique of mechanosensory host location has not yet been investigated in a natural, tritrophic system with multiple cues. Here we compared the host location of the pupal parasitoid Xanthopimpla stemmator in a tritrophic system with corn borer pupae in maize stem to the behavior on a paper model offering mechanosensory cues only. In general, the behavioral pattern and the behavioral states exhibited by host-searching female parasitoid were identical in the model and in the tritrophic system, while quantitative aspects differed. Our results demonstrate that vibrational sounding maintains its significance for host location in an environment with multiple cues, and that additional cues may increase responsiveness of females.