Heat tolerance variation reveals vulnerability of tropical herbivore–parasitoid interactions to climate change

Assessing the heat tolerance (CTmax) of organisms is central to understand the impact of climate change on biodiversity. While both environment and evolutionary history affect CTmax, it remains unclear how these factors and their interplay influence ecological interactions, communities and ecosystems under climate change. We collected and reared caterpillars and parasitoids from canopy and ground layers in different seasons in a tropical rainforest. We tested the CTmax and Thermal Safety Margins (TSM) of these food webs with implications for how species interactions could shift under climate change. We identified strong influence of phylogeny in herbivore–parasitoid community heat tolerance. The TSM of all insects were narrower in the canopy and parasitoids had lower heat tolerance compared to their hosts. Our CTmax-based simulation showed higher herbivore–parasitoid food web instability under climate change than previously assumed, highlighting the vulnerability of parasitoids and related herbivore control in tropical rainforests, particularly in the forest canopy.     

Structure and vertical stratification of plant galler–parasitoid food webs in two tropical forests

Abstract 1. Networks of feeding interactions among insect herbivores and natural enemies such as parasitoids, describe the structure of these assemblages and may be critically linked to their dynamics and stability. The present paper describes the first quantitative study of parasitoids associated with gall‐inducing insect assemblages in the tropics, and the first investigation of vertical stratification in quantitative food web structure. 2. Galls and associated parasitoids were sampled in the understorey and canopy of Parque Natural Metropolitano in the Pacific forest, and in the understorey of San Lorenzo Protected Area in the Caribbean forest of Panama. Quantitative host–parasitoid food webs were constructed for each assemblage, including 34 gall maker species, 28 host plants, and 57 parasitoid species. 3. Species richness was higher in the understorey for parasitoids, but higher in the canopy for gall makers. There was an almost complete turnover in gall maker and parasitoid assemblage composition between strata, and the few parasitoid species shared between strata were associated with the same host species. 4. Most parasitoid species were host specific, and the few polyphagous parasitoid species were restricted to the understorey. 5. These results suggest that, in contrast to better‐studied leaf miner–parasitoid assemblages, the influence of apparent competition mediated by shared parasitoids as a structuring factor is likely to be minimal in the understorey and practically absent in the canopy, increasing the potential for coexistence of parasitoid species. 6. High parasitoid beta diversity and high host specificity, particularly in the poorly studied canopy, indicate that tropical forests may be even more species rich in hymenopteran parasitoids than previously suspected.     

Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest

The processes maintaining the enormous diversity of herbivore—parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84 % of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5 %) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar—parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2 %) as exposed caterpillars.     

Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest

Quantitative food webs were constructed to explore the community structure of leaf-mining moths in the family Gracillariidae and their parasitoid wasps in a deciduous forest in Hokkaido, Japan. A whole food web was constructed from data collected from June to October 2001. In the web, 16 leafminer species on seven tree species were attacked by 58 species of hymenopteran parasitoid; 376 links between leafminers and parasitoids were observed. Leafminers were specialist herbivores, but most parasitoids were generalists. Five webs were constructed for the seasonal prevalence of leafminers over the one-year period to reveal the temporal dynamics in community structure. Among the seasonal webs, the first web in June was distinctive because two tree species, Japanese umbrella tree Magnolia obovata and Japanese magnolia M. kobus, supported the community. Second to fourth webs from July to September were dominated by the leafminer species on Japanese oak Quercus crispula, and the fifth web was marked by that on Carpinus cordata. The extent of potential apparent competition among leafminers was evaluated using quantitative parasitoid overlap diagrams. These diagrams suggested that abundant host species are likely to have large indirect effects on less abundant species. Moreover, the potential for apparent competition between leafminer species inhabiting different host tree species can occur, although leafminers sharing the same tree species are prone to interact via shared parasitoids. In this system, particular leafminer species, acting as potential sources of apparent competition, can affect other species as sinks, and control whole-community dynamics. Directed apparent competition may potentially occur around oak trees.     

Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids

1. Most communities of insect herbivores are unlikely to be structured by resource competition, but they may be structured by apparent competition mediated by shared natural enemies. 2. The potential of three guilds of natural enemies (parasitoids, fungal entomopathogens and predators) to influence aphid community structure through indirect interactions is assessed. Based on the biology, we predicted that the scope for apparent competition would be greatest for the predator and least for the parasitoid guilds. 3. Separate fully quantitative food webs were constructed for 3 years for the parasitoid guild, 2 years for the pathogen guild and for a single year for the predator guild. The webs were analysed using standard food web statistics designed for binary data, and using information-theory-based metrics that make use of the full quantitative data. 4. A total of 29 aphid, 24 parasitoid, five entomopathogenic fungi and 13 aphid specialist predator species were recorded in the study. Aphid density varied among years, and two species of aphid were particularly common in different years. Omitting these species, aphid diversity was similar among years. 5. The parasitoid web showed the lowest connectance while standard food web statistics suggested the pathogen and predator webs had similar levels of connectance. However, when a measure based on quantitative data was used the pathogen web was intermediate between the other two guilds. 6. There is evidence that a single aphid species had a particularly large effect on the structure of the pathogen food web. 7. The predator and pathogen webs were not compartmentalized, and the vast majority of parasitoids were connected in a single large compartment. 8. It was concluded that indirect effects are most likely to be mediated by predators, a prediction supported by the available experimental evidence.     

The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: A food web approach

The safety of biological control is a contentious issue. We suggest that constructing and analyzing food webs may be a valuable addition to standard biological control research techniques, as they offer a means of assessing the post-release safety of control agents. Using preliminary data to demonstrate the value of food webs in biocontrol programs, we quantified the extent to which a key agent has infiltrated natural communities in Australia and, potentially, impacted on non-target species. Using these data, we also demonstrate how food webs can be used to generate testable hypotheses regarding indirect interactions between introduced agents and non-target species. We developed food webs in communities invaded to varying degrees by an exotic weed, bitou bush, Chrysanthemoides monilifera ssp. rotundata, and a key biocontrol agent for this weed in Australia, the tephritid fly, Mesoclanis polana. Three food webs were constructed during springtime showing the interactions between plants, seed-feeding insects and their parasitoids. One food web was constructed in a plot of native Australian vegetation that was free of bitou bush (‘bitou-free’), another in a plot of Australian vegetation surrounded by an invasion of bitou bush (‘bitou-threatened’) and a third from a plot infested with a monoculture of bitou bush (‘bitou-infested’). The bitou-free web contained 36 species, the bitou-threatened plot 9 species and the bitou-infested web contained 6 species. One native Australian herbivore attacked the seeds of bitou bush. M. polana, a seed-feeding fly, was heavily attacked by native parasitoids, these being more abundant than the parasitoids feeding on the native seed feeders. A surprising result is that none of the three species of native parasitoids reared from M. polana were reared from any of the native herbivores. The food webs revealed how a highly host-specific biocontrol agent, such as M. polana has the potential to change community structure by increasing the abundance of native parasitoids. The webs also suggest that indirect interactions between M. polana and native non-target species are possible, these been mediated by shared parasitoids. The experiments necessary to determine the presence of these interactions are outlined.     

Interpopulation quality in gypsy moths with implications for success of two pupal parasitoids: Brachymeria intermedia (Nees) and Coccygomimus turionellae (L.)*

Abstract.

• 1 Gypsy moth egg masses were collected from innocuous, release and outbreak populations and reared in the laboratory on synthetic diet under identical conditions.
• 2 Outbreak population gypsy moths hatched sooner, were smaller and less fecund than innocuous or release gypsy moths, but had a higher concentration of total carbohydrates in their haemolymph.
• 3 Pupae from each population source were submitted to parasitization by two pupal parasitoids. Emerging B.intermedia, an established parasitoid of the gypsy moth associated with outbreak populations, were largest on outbreak source gypsy moths. C. turionellae, not a usual parasitoid of the gypsy moth, were largest when emerging from innocuous or release population gypsy moths. Implications for population dynamics of the gypsy moth are discussed.

     

Indirect Interactions in the High Arctic

Indirect interactions as mediated by higher and lower trophic levels have been advanced as key forces structuring herbivorous arthropod communities around the globe. Here, we present a first quantification of the interaction structure of a herbivore-centered food web from the High Arctic. Targeting the Lepidoptera of Northeast Greenland, we introduce generalized overlap indices as a novel tool for comparing different types of indirect interactions. First, we quantify the scope for top-down-up interactions as the probability that a herbivore attacking plant species i itself fed as a larva on species j. Second, we gauge this herbivore overlap against the potential for bottom-up-down interactions, quantified as the probability that a parasitoid attacking herbivore species i itself developed as a larva on species j. Third, we assess the impact of interactions with other food web modules, by extending the core web around the key herbivore Sympistis nigrita to other predator guilds (birds and spiders). We find the host specificity of both herbivores and parasitoids to be variable, with broad generalists occurring in both trophic layers. Indirect links through shared resources and through shared natural enemies both emerge as forces with a potential for shaping the herbivore community. The structure of the host-parasitoid submodule of the food web suggests scope for classic apparent competition. Yet, based on predation experiments, we estimate that birds kill as many (8%) larvae of S. nigrita as do parasitoids (8%), and that spiders kill many more (38%). Interactions between these predator guilds may result in further complexities. Our results caution against broad generalizations from studies of limited food web modules, and show the potential for interactions within and between guilds of extended webs. They also add a data point from the northernmost insect communities on Earth, and describe the baseline structure of a food web facing imminent climate change.     

Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

1. Induced plant responses can affect herbivores either directly, by reducing herbivore development, or indirectly, by affecting the performance of natural enemies. Both the direct and indirect impacts of induction on herbivore and parasitoid success were evaluated in a common experimental system, using clonal poplar trees Populus nigra (Salicales: Salicaceae), the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae), and the gregarious parasitoid Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae). 2. Female parasitoids were attracted to leaf odours from both damaged and undamaged trees, however herbivore‐damaged leaves were three times more attractive to wasps than undamaged leaves. Parasitoids were also attracted to herbivore larvae reared on foliage and to larval frass, but they were not attracted to larvae reared on artificial diet. 3. Prior gypsy moth feeding elicited a systemic plant response that retarded the growth rate, feeding, and survival of gypsy moth larvae, however induction also reduced the developmental success of the parasitoid. 4. The mean number of parasitoid progeny emerging from hosts fed foliage from induced trees was 40% less than from uninduced trees. In addition, the proportion of parasitised larvae that survived long enough to issue any parasitoids was lower on foliage from induced trees. 5. A conceptual and analytical model is provided to describe the net impacts of induced plant responses on parasitoids, and implications for tritrophic interactions and biological control of insect pests are discussed.     

Natural enemies and environmental factors affecting the population dynamics of the gypsy moth

The population densities of the gypsy moth (Lymantria dispar; Lepidoptera: Lymantriidae) may reach outbreak levels that pose considerable economic and environmental impacts to forests in Europe, Asia, Africa and North America. Compared with the situation in its native European range feeding damage by gypsy moth is often found to be more severe in North America and other parts of the world. Thus, the release from natural enemies can be interpreted as an important cause for high feeding damages. Natural enemies, especially parasitoids, can cause delayed density‐dependent mortality, which may be responsible for population cycles. In North America where only few parasitoids have been introduced and the parasitism rates are considerably lower than in Europe, generalist predators play a larger role than in Europe. Many other factors seem to influence the population dynamics of the gypsy moth such as the host plants and weather. Nevertheless, much of the variability in population densities of the gypsy moth may be attributed to interacting effects of weather conditions and attack by natural enemies. In spite of the considerable number of studies on the ecology and population dynamics of the gypsy moth and the impact of their natural enemies, more quantitative information is required to predict the population dynamics of this pest species and to control its economic and ecologic impact.     

Can hyperparasitoids cause large‐scale outbreaks of insect herbivores?

Synchronous population fluctuations occur in many species and have large economic impacts, but remain poorly understood. Dispersal, climate and natural enemies have been hypothesized to cause synchronous population fluctuations across large areas. For example, insect herbivores cause extensive forest defoliation and have many natural enemies, such as parasitoids, that may cause landscape‐scale changes in density. Between outbreaks, parasitoid‐caused mortality of hosts/herbivores is high, but it drops substantially during outbreak episodes. Because of their essential role in regulating herbivore populations, we need to include parasitoids in spatial modelling approaches to more effectively manage insect defoliation. However, classic host‐parasitoid population models predict parasitoid density, and parasitoid density is difficult to relate to host‐level observations of parasitoid‐caused mortality. We constructed a novel model to study how parasitoids affect insect outbreaks at the landscape scale. The model represents metacommunity dynamics, in which herbivore regulation, colonisation and extinction are driven by interactions with the forest, primary parasitoids and hyperparasitoids. The model suggests that parasitoid spatial dynamics can produce landscape‐scale outbreaks. Our results propose the testable prediction that hyperparasitoid prevalence should increase just before the onset of an outbreak because of hyperparasitoid overexploitation. If verified empirically, hyperparasitoid distribution could provide a biotic indicator that an outbreak will occur.     

Parasitism and Food Web Structure in Defoliating Lepidoptera – Parasitoid Communities on Soybean

Food webs are usually regarded as snapshots of community feeding interactions. Here, we describe the yearly and cumulative structure of parasitoid–caterpillar food webs on soybean in central Argentina, analyzing parasitism rates and their variability in relation to parasitoid diversity and food web vulnerability in the system. Lepidoptera larvae were collected along four seasons from soybean crops and reared in laboratory to obtain and identify adults and parasitoids. Eleven species of defoliating Lepidoptera and ten parasitoid species were recorded. Food web statistics showed rather low annual variability, with most variation coefficients in the order of 0.20 and generality showing the most stable values. Parasitism showed the highest variability, which was independent of parasitoid diversity and food web vulnerability, although parasitism rates were negatively related to parasitoid richness. Our study highlights the need to consider food web structure and variability in order to understand the functioning of ecological communities in general and in extensive agricultural ecosystems in particular.     

A survey of hymenopteran parasitoids of forest macrolepidoptera in the central Appalachians

In 1995 and 1996, we conducted a study of the hymenopteran parasitoids of macrolepidopteran larvae in the George Washington National Forest (GWNF), Augusta County, Virginia, and the Monongahela National Forest (MNF), Pocahontas County, West Virginia. Macrolepidopteran larvae were collected from canopy foliage and from under canvas bands placed around tree boles. A total of 115 macrolepidopteran species and 5,235 individual larvae were reared. Forty-two percent (2,221) of the larvae were gypsy moth, Lymantria dispar (L.) (Lymantriidae). A total of 43 primary and secondary (hyperparasitoid) hymenopteran parasitoid species were reared from 46 macrolepidopteran species. Hymenopteran families represented included Ichneumonidae (23 species), Braconidae (19), Eulophidae (6), Perilampidae (1), and Trigonalidae (1). We reared 41 and 28 parasitoid species from the GWNF and the MNF, respectively, with 19 species reared from both forests. Many parasitoid species were collected infrequently, suggesting that they are relatively rare on the sampled hosts. The introduced species Cotesia melanoscela (Ratzeburg) (Braconidae), and Euplectrus bicolor (Swederus) (Eulophidae) were among the most commonly reared parasitoids, the latter reared from native hosts. The four most commonly reared native parasitoids were Meteorus hyphantriae, Riley (Braconidae), Microplitis near hyphantriae (Ashmead) (Braconidae), Aleiodes preclarus Marsh & Shaw, and Euplectrus maculiventris (Westwood) (Eulophidae). A total of 53 new hymenopteran parasitoid-macrolepidopteran host records were documented. Results from this study will be used to evaluate long-term treatment effects of regional applications of Bacillus thuringiensis kurstaki, and the gypsy moth fungus Entomophaga maimaiga Humber, Shimazu & Soper on hymenopteran parasitoids of macrolepidopteran larvae.     

Field confirmation of a mechanism causing synergism between Bacillus thuringiensis and the gypsy moth parasitoid, Apanteles melanoscelus

In 16-ha plots aerially sprayed with single and double applications of Bacillus thuringiensis, percentage parasitism by A. melanoscelus and the number of A. melanoscelus cocoons under burlap strips were higher than in comparable untreated plots in the same area. Strong correlations occurred between percentage parasitism and caterpillar size, with plots having the smallest caterpillars being the most heavily parasitized. However, these parameters were also negatively correlated with number of caterpillars per plot. The increased numbers of parasitoid progeny, i.e., cocoons, found in treated plots showed that corresponding increases in percentage parasitism could not be due simply to improved parasitoid: host ratios. Evidence strongly suggests that the retarding effect of B. thuringiensis infection kept gypsy moth larvae small enough in the treated plots to permit A. melanoscelus females to parasitize relatively large numbers of caterpillars.     

Food web structure changes with elevation but not rainforest stratum

Changes in species richness along elevational gradients are well documented. However, little is known about how trophic interactions between species and, in particular, the food webs that these interactions comprise, change with elevation. Here we present results for the first comparison of quantitative food webs in forest understorey and canopy along an elevational gradient. Replicate quantitative food webs were constructed for assemblages involving 23 species of cavity‐nesting Hymenoptera and 12 species of their parasitoids and kleptoparasites in subtropical rainforest in Australia. A total of 1589 insects were collected using trap nests across 20 plots distributed at sites ranging from 300 to 1100 m a.s.l. Insect abundance, insect diversity and parasitism rate generally decreased with increasing elevation. Food web structure significantly changed with elevation. In particular, weighted quantitative measures of linkage density, interaction evenness, nestedness (weighted NODF) and potential for enemy mediated interactions (PAC) decreased with increasing elevation, and network specialisation (H₂′) increased with increasing elevation, even after controlling for matrix size; but there was no change in weighted connectance. Changes in forest type and temperature along the elevational gradient are likely to be, at least partly, responsible for the patterns observed. We found no significant differences in insect abundance, insect diversity or parasitism rate between canopy and understorey. Furthermore, there were no differences in food web structure between strata. These results contribute further evidence to studies revealing changes in food web structure along natural environmental gradients and provide information that can potentially be used for predicting how communities may respond to climate change.     

The colonization of native phytophagous insects in North America by exotic parasitoids

Classical biological control could have a major environmental cost if introduced natural enemies colonize and disrupt native systems. Although quantifying these impacts is difficult for systems already colonized by natural enemies, the a priori condition for such impacts can be evaluated based on the extent to which exotics have acquired native hosts. We use native host records for exotic parasitoids introduced into North America for biological control to document the number of exotic species that have been recorded from at least one native insect species. We also evaluate the ability of six biological and ecological variables to predict whether or not a parasitoid will move onto natives. Sixteen percent of 313 parasitoid species introduced against holometabolous pests are known from natives. Further, the likelihood that a parasitoid had colonized native hosts was largely unpredictable with respect to the independent variables. We conclude that given the quality of the data available either now or in the foreseeable future, coupled with inherent stochasticity in host shifts by parasitoids, there are no rules of thumb to assist biological control workers in evaluating if an introduced parasitoid will colonize native insect communities. Received: 2 July 1997 / Accepted: 3 August 1997     

Food web complexity and higher-level ecosystem services

Studies mostly focused on communities of primary producers have shown that species richness provides and promotes fundamental ecosystem services. However, we know very little about the factors influencing ecosystem services provided by higher trophic levels in natural food webs. Here we present evidence that differences in food web structure and the richness of herbivores in 19 plant‐herbivore‐parasitoid food webs influence the service supplied by natural enemies, namely, the parasitism rates on hosts. Specifically, we find that parasitoids function better in simple food webs than in complex ones, a result relevant to biological control practice. More generally, we show that species richness per se only contributes partially to the understanding of higher‐level ecosystem services in multitrophic communities, and that changes in food web complexity should also be taken into account when predicting the effects of human‐driven disturbances in natural communities.     

Lepidoptera‐specific insecticide used to suppress gypsy moth outbreaks may benefit non‐target forest Lepidoptera

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Quantitative food webs of dipteran leafminers and their parasitoids in Argentina

The quantitative structure of two host–parasitoid communities based on leaf-mining flies (Diptera, Agromyzidae) in Argentina is described. The two communities consisted of 29 and 27 hosts, 46 and 40 parasitoids, and 193 and 179 recorded host–parasitoid associations. Also, food webs were constructed for one community based solely on samples taken in the wet and dry seasons. Data were expressed as quantitative food webs, and the manner in which food web properties, such as connectance and compartmentalization, were influenced by sampling intensity was explored. The potential importance of indirect effects between hosts mediated by parasitoids (e.g. apparent competition) was assessed using quantitative parasitoid overlap diagrams. The studys results suggest that indirect effects are likely to be important in these highly connected communities. The limitations of the studys analysis, and how the conclusions can be tested experimentally, are discussed.     

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA-based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species-specific parasitoid-hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.