Temperature responses of a plant‐insect system using a food‐web performance approach

Evaluation of the performance of a plant‐herbivore system as a whole is difficult due to the lack of fitness parameters that can be applied to both components. The individual use of traditional measures of performance (e.g., r_m, biomass) can provide useful, but incomplete information on the performance of insect herbivores and seldom incorporates plant performance. We propose the use of the net generational productivity (NGP) to evaluate the fitness of the herbivore, which can then be compared directly with the performance of the plant in biomass units, to obtain the food‐web performance ratio (φ_H/P). We compared three biotypes of the potato aphid, Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae), when raised on three different host plants: potato (Solanum tuberosum L. cv. Norland) and two bell peppers (Capsicum annuum L. cv. Fascinato and cv. Crosby) (all Solanaceae) at temperatures ranging from 8 to 36 °C. The temperature profiles of the potato aphid biotypes suggest that this aphid is better suited to temperate climates, and its performance generally depends on the particular host‐plant/biotype association. Plant growth performance showed that potato has a lower thermal tolerance, but has a faster growth rate than bell peppers, especially in the range of 16–24 °C. Temperature variation in the φ_H/P ratio shows that aphids have a greater performance than plants, especially at lower temperatures, at which they can accumulate biomass up to 148 times faster. Because of the aphid's biological inability to withstand long exposures to temperatures above 28 °C, plants have a slight advantage over aphids. Nonetheless, as the performance of plants is extremely reduced at high temperatures, this advantage cannot withstand long‐term exposures to extreme temperatures. This is the first attempt to obtain a parameter capable of determining the climatic profile and performance of a food web in an inclusive yet simple manner.     

Ecology of the aphid pests of protected pepper crops and their parasitoids

Myzus persicae, Macrosiphum euphorbiae, Aphis gossypii and Aulacorthum solani (Homoptera: Aphididae) are principal pests of protected pepper crops in southeastern Spain. Our goal was to determine the incidence of aphids on pepper crops and the role of vegetation surrounding greenhouses as a source of aphids and their parasitoids. The population dynamics were followed in six commercial greenhouses during 3 years. Another 82 greenhouses and their surrounding vegetation were surveyed occasionally. Myzus persicae had the highest incidence in pepper greenhouses followed by M. euphorbiae and A. solani. Parasitism of all aphid species in greenhouses was low, Aphidius matricariae and Aphidius colemani being the most abundant parasitoids. Myzus persicae and Macrosiphum euphorbiae were the most abundant and polyphagous aphids, being present on 77 and 55% of the plants sampled outside greenhouses, respectively; species of Brassicaceae were the main hosts for both aphids. Aulacorthum solani was only present on Malva parviflora and at low numbers. Outside greenhouses, A. matricariae was the most common parasitoid of M. persicae, followed by Diaeretiella rapae and A. colemani. Aphidius matricariae was the most polyphagous, being present in 10 out of 22 aphid species. Macrosiphum euphorbiae and A. solani were both parasitised by A. ervi and Praon volucre. Aphelinus asychis was found on A. solani. Parasitoids were found in other aphids not attacking pepper. The role of natural vegetation as a reservoir of aphid pests of pepper and of parasitoids is discussed.     

Interactions between tomato volatile organic compounds and aphid behaviour

Abstract

In the tritrophic system consisting of tomato, Solanum lycopersicum (L.), the aphid Macrosiphum euphorbiae (Thomas) and its natural enemy, the parasitoid Aphidius ervi (Haliday), it has been shown that the release of volatile organic compounds following aphid attack is responsible for attracting aphid parasitoids in wind tunnel experiments. The main compounds involved in these multitrophic interactions have been characterized and quantified. In this work, the possible activity of such compounds on plant direct defences against the aphid M. euphorbiae was assessed in laboratory tests. The selected compounds were applied to uninfested tomato plants, either by evaporation or contact, and performance of aphids, in terms of plant acceptance, fixing behaviour and aphid development, calculated in standard conditions. The results showed that two compounds, namely methyl salicylate and cis-hex-3-en-1-ol, alter aphid performance. These two compounds have been reported to be those eliciting the best response by A. ervi in terms of flight behavior (wind tunnel bioassay) and antennal stimulation (EAG bioassay).     

A comparison between two strains from Japan and Europe of Aphidius ervi

A European strain of Aphidius ervishall be introduced into Japan for the control of Macrosiphum euphorbiaeon greenhouse tomatoes. We compared this strain, which is originating from The Netherlands (EVP), with a native strain from Hokkaido, Northern Japan (SPR) in several characteristics. The percentage of parasitism of SPR and EVP was significantly different, when attacking three aphid species: 13% and 30% on M. euphorbiaeon tomato, 68% and 93% on Acyrthosiphon pisumon broad bean and 10% and 42% on Aulacorthum solanion sweet pepper, respectively. SPR and EVP differed morphologically (in the colouration of the petiole) and in the esterase banding patterns. Furthermore, cross mating experiments showed that SPR and EVP are partially reproductively isolated from each other. Complete reproductive isolation is evident in the one direction cross (EVP females and SPR males).     

Boosted food web productivity through ocean acidification collapses under warming

Future climate is forecast to drive bottom‐up (resource driven) and top‐down (consumer driven) change to food web dynamics and community structure. Yet, our predictive understanding of these changes is hampered by an over‐reliance on simplified laboratory systems centred on single trophic levels. Using a large mesocosm experiment, we reveal how future ocean acidification and warming modify trophic linkages across a three‐level food web: that is, primary (algae), secondary (herbivorous invertebrates) and tertiary (predatory fish) producers. Both elevated CO₂ and elevated temperature boosted primary production. Under elevated CO₂, the enhanced bottom‐up forcing propagated through all trophic levels. Elevated temperature, however, negated the benefits of elevated CO₂ by stalling secondary production. This imbalance caused secondary producer populations to decline as elevated temperature drove predators to consume their prey more rapidly in the face of higher metabolic demand. Our findings demonstrate how anthropogenic CO₂ can function as a resource that boosts productivity throughout food webs, and how warming can reverse this effect by acting as a stressor to trophic interactions. Understanding the shifting balance between the propagation of resource enrichment and its consumption across trophic levels provides a predictive understanding of future dynamics of stability and collapse in food webs and fisheries production.     

Co‐occurrence of defensive traits in the potato aphid Macrosiphum euphorbiae

1. Insecticide usage selects strongly for resistance in aphid populations, but this could entail fitness costs in other resistance traits. The potato aphid Macrosiphum euphorbiae Thomas exhibits intraspecific variation in susceptibility to parasitism by braconid wasps and provides a suitable species to study the relation between the defensive traits of parasitism and insecticide resistance. 2. Clonal lines (23 in total) of M. euphorbiae were established from aphids collected in 2013 from geographically separate populations in the U.K. Clonal lines belonged to five aphid genotypes, but one genotype predominated (78% of samples), and the facultative endosymbiont Hamiltonella defensa was detected in c. 40% of lines. 3. Total esterase activity in aphid tissues varied significantly between aphid genotypes and collection areas, but there was no clear pattern in relation to H. defensa infection or between collection sites likely to differ in insecticide pressures. 4. Five clonal lines representing low to moderate levels of enzyme activity, which included different aphid genotypes and presence/absence of H. defensa infection, were assayed for their susceptibility to the parasitoid wasp Aphidius ervi Haliday. Aphid mummification varied significantly between aphid genotypes, with low values in one genotype of aphids irrespective of H. defensa presence. 5. The results revealed that aphid lines belonging to the parasitism‐resistant genotype exhibited moderate levels of total esterase activity, indicating a competitve advantage for this genotype of M. euphorbiae when exposed to chemical and biological control factors in agroecosystems.     

The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus

Plant viruses and aphids can interact via contest competition for plant resources and induce changes in plant physiology, which can have effects on a third trophic level. The aim of this study was to determine how the interactions between a circulative plant virus and its aphid vector may affect the performance of an endoparasitoid and how parasitism may affect the efficiency of virus transmission by its aphid vector. The timing when parasitized aphids were transferred to virus-infected lettuce leaves was critical for the performance of A. ervi. Higher parasitoid larvae mortality, longer developmental times and lower percentages of mummification were detected on viruliferous/parasitized aphid nymphs when the time lag between parasitism and exposure to the virus was less than 24 h. No significant differences were detected in virus transmission rate between parasitized and non-parasitized M. euphorbiae aphids.     

Host-locating response by the aphid parasitoid Aphidius ervi to tomato plant volatiles

Abstract

The blend of volatile compounds emitted by tomato plants (Solanum lycopersicum) infested with the potato aphid (Macrosiphum euphorbiae) has been studied comparatively with undamaged plants and aphids themselves. Aphid-infested plants were significantly more attractive towards Aphidius ervi than undamaged plants and aphids themselves. Oriented response towards host-damaged plant, from which aphids were removed just before running the bioassay, did not differ from that recorded for infested plants. Collection of the volatiles and analysis by gas chromatography revealed only quantitative differences between uninfested and aphid-infested plants. Nine compounds, α-pinene, (Z)-3-hexen-1-ol, α-phellandrene, limonene, (E)-β-ocimene, p-cymene, methyl salicylate, (E)-β-caryophyllene and an unknown compound, were emitted at higher levels from aphid-infested plants than from undamaged control plants, whilst no differences were noted for hexanal, 6-methyl-5-hepten-2-one, and humulene (=α-caryophyllene). Synthetic standards of these compounds were tested in wind tunnel bioassays and all elicited a significant increase in oriented flight and landings on the target by the aphid parasitoid Aphidius ervi. (E)-β-caryophyllene resulted the most attractive towards female wasps. These results corroborate the hypothesis that the volatiles produced by the plant in response to aphid attack derive from both jasmonic and salicylic acid pathways, and are exploited by A. ervi as olfactory cues to locate its hosts.     

Predictive power of food web models based on body size decreases with trophic complexity

Food web models parameterised using body size show promise to predict trophic interaction strengths (IS) and abundance dynamics. However, this remains to be rigorously tested in food webs beyond simple trophic modules, where indirect and intraguild interactions could be important and driven by traits other than body size. We systematically varied predator body size, guild composition and richness in microcosm insect webs and compared experimental outcomes with predictions of IS from models with allometrically scaled parameters. Body size was a strong predictor of IS in simple modules (r² = 0.92), but with increasing complexity the predictive power decreased, with model IS being consistently overestimated. We quantify the strength of observed trophic interaction modifications, partition this into density‐mediated vs. behaviour‐mediated indirect effects and show that model shortcomings in predicting IS is related to the size of behaviour‐mediated effects. Our findings encourage development of dynamical food web models explicitly including and exploring indirect mechanisms.     

Impact of a parasitoid on the bacterial symbiosis of its aphid host

Embryo production in aphids is absolutely dependent on the function of symbiotic bacteria, mainly Buchnera, and the growth and development of koinobiont parasitoids in aphids requires the diversion of nutrients from aphid embryo production to the parasitoid. The implication that the bacterial symbiosis may be promoted in parasitized aphids to support the growing parasitoid was explored by analysis of the number and biomass of mycetocytes, and the aphid cells bearing Buchnera, in the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) parasitized by the wasp Aphidius ervi Haliday (Hymenoptera: Braconidae). Aphids hosting a young larval parasitoid bore more mycetocytes of greater total biomass, and embryos of lower biomass than unparasitized aphids. Furthermore, one of the three aphid clones tested, which limited teratocyte growth (giant cells of parasitoid origin having a trophic role), bore smaller mycetocytes and larger embryos, than one or both of the two aphid clones with greater susceptibility to the parasitoid. These data suggest that susceptibility of the aphid‐Buchnera symbiosis to parasitoid‐mediated manipulation may, directly or indirectly, contribute to aphid susceptibility to parasitoid exploitation.     

Use of plants by Myzus persicae in agroecosystems: Potential applications in conservation biological control

Myzus persicae (Sulzer) is a highly polyphagous aphid species that attacks several economically important crop plants. Here, trophic webs involving M. persicae, its host plants and its parasitoids were described and quantified in wheat, oat and alfalfa agroecosystems from central Argentina, with special emphasis on the sub-habitats where interactions occur: crops and adjacent field margins. Three fields cultivated with each crop species and their margins were sampled during three years; aphid abundance and mummification percentage were compared among crop plants and the diverse natural vegetation in the borders. Interactions were described using a quantitative food web approach, and abundance and mummification percentage e data were analysed using a generalized linear model. Four plant species present in the borders (Capsella bursa-pastori, Rapistrum sp., Melilotus sp. and Trifolium repens) hosted M. persicae and its parasitoids. The alfalfa agroecosystem produced a significantly higher number of aphids than oat and wheat; however, in all cases, crops and borders sustained similar aphid abundance. A total of six Aphidiinae species attacked M. persicae, with no significant differences in the richness of parasitoid species between the borders and the crops, but with significant differences in parasitoid abundance, being higher in the crops. Mummification percentage were higher in crops than in the borders, with Lysiphlebus testaceipes, Aphidius colemani and A. ervi being the most abundant species. Almost 70% of M. persicae individuals were collected from fields borders, which highlights the importance of including these sites in studies of trophic interactions in crop fields.     

Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity

Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below‐ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO₂ efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse‐labelled after the drought with ¹³C‐CO₂ to quantify the capture of recent photosynthate and its transfer below‐ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of ¹³C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below‐ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, ¹³C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO₂ efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above‐ground–below‐ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.     

Predicting food‐web structure with metacommunity models

Synthesis Metacommunity theory aims to elucidate the relative influence of local and regional‐scale processes in generating diversity patterns across the landscape. Metacommunity research has focused largely on assemblages of competing organisms within a single trophic level. Here, we test the ability of metacommunity models to predict the network structure of the aquatic food web found in the leaves of the northern pitcher plant Sarracenia purpurea. The species‐sorting and patch‐dynamics models most accurately reproduced nine food web properties, suggesting that local‐scale interactions play an important role in structuring Sarracenia food webs. Our approach can be applied to any well‐resolved food web for which data are available from multiple locations. The metacommunity framework explores the relative influence of local and regional‐scale processes in generating diversity patterns across the landscape. Metacommunity models and empirical studies have focused mostly on assemblages of competing organisms within a single trophic level. Studies of multi‐trophic metacommunities are predominantly restricted to simplified trophic motifs and rarely consider entire food webs. We tested the ability of the patch‐dynamics, species‐sorting, mass‐effects, and neutral metacommunity models, as well as three hybrid models, to reproduce empirical patterns of food web structure and composition in the complex aquatic food web found in the northern pitcher plant Sarracenia purpurea. We used empirical data to determine regional species pools and estimate dispersal probabilities, simulated local food‐web dynamics, dispersed species from regional pools into local food webs at rates based on the assumptions of each metacommunity model, and tested their relative fits to empirical data on food‐web structure. The species‐sorting and patch‐dynamics models most accurately reproduced nine food web properties, suggesting that local‐scale interactions were important in structuring Sarracenia food webs. However, differences in dispersal abilities were also important in models that accurately reproduced empirical food web properties. Although the models were tested using pitcher‐plant food webs, the approach we have developed can be applied to any well‐resolved food web for which data are available from multiple locations.     

Trophic level and basal resource use of soil animals are hardly affected by local plant associations in abandoned arable land

Plants provide resources and shape the habitat of soil organisms thereby affecting the composition and functioning of soil communities. Effects of plants on soil communities are largely taxon‐dependent, but how different functional groups of herbaceous plants affect trophic niches of individual animal species in soil needs further investigation. Here, we studied the use of basal resources and trophic levels of dominating soil meso‐ and macrofauna using stable isotope ratios of carbon and nitrogen in arable fallow systems 3 and 14–16 years after abandonment. Animals were sampled from the rhizosphere of three plant species of different functional groups: a legume (Medicaco sativa), a nonlegume herb (Taraxacum officinale), and a grass (Bromus sterilis). We found virtually no consistent effects of plant identity on stable isotope composition of soil animals and on thirteen isotopic metrics that reflect general food‐web structure. However, in old fallows, the carbon isotope composition of some predatory macrofauna taxa had shifted closer to that of co‐occurring plants, which was particularly evident for Lasius, an aphid‐associated ant genus. Trophic levels and trophic‐chain lengths in food webs were similar across plant species and fallow ages. Overall, the results suggest that variations in local plant diversity of grassland communities may little affect the basal resources and the trophic level of prey consumed by individual species of meso‐ and macrofauna belowground. By contrast, successional changes in grassland communities are associated with shifts in the trophic niches of certain species, reflecting establishment of trophic interactions with time, which shapes the functioning and stability of soil food webs.     

Developmental rates of the aphid Aphis pomi (Aphidoidea: Aphididae) and its parasitoid Aphidius ervi (Hymenoptera: Aphidiidae)

Developmental rates of the aphid Aphis pomi and its parasitoid Aphidius ervi were compared at four constant temperatures (15, 20, 25, 30°C). Aphis pomi required 159.07 degree-days (DD) above lover developmental threshold (LDT) of 0.3°C. Aphidius ervi required 229.73 DD above LDT of 5.98°C. Developmental rate of A. pomi is higher than the developmental rate of A. ervi at the same conditions     

Host plant genotype determines bottom‐up effects in an aphid‐parasitoid‐predator system

Plant genotypes are known to affect performance of insect herbivores and the community structure of both herbivores and higher trophic levels. Still, only a limited number of studies demonstrate differences in the performance of predators and parasitoids because of plant genotypic effects and most of these focus on gall formers. We designed a greenhouse experiment to investigate the effects of host plant genotype on fitness components in a grass‐aphid‐carnivore system. We used clones of quackgrass [Elytrigia repens (L.) Desv. ex Nevski (Poaceae)], the aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae), the parasitoid wasp Aphidius colemani (Viereck) (Hymenoptera: Braconidae), and the predatory lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). The number of aphid offspring differed considerably among plant genotypes. These differences were only in part because of differences in the production of biomass among host genotypes. Therefore, genotypes may differ in their nutritional value for phytophages. The number of aphids attacked by the parasitoid also differed among genotypes and aphid numbers only partly accounted for this effect. Moreover, pupal development time of female parasitoids was affected by plant genotype. We found no differences in mortality, body size, or sex ratio of hatching wasps between genotypes of quackgrass. Development time of the larvae and larval weight of the predatory lacewings differed among genotypes, but not weight of pupae and adults. Generally, the proportion of the total variance explained by the plant genotype was smaller for parasitoids and predators than for aphids. Overall, our experiments indicated that the plant genotype affects tri‐trophic interactions, but also that the strength of these effects decreases along the food chain.     

Temperature influences host instar selection in an aphid parasitoid: support for the relative fitness rule

The relative fitness rule states that parasitoid females should adopt risk‐prone reproductive behaviours when expecting low reproductive success. Temperature influences the reproductive success of insects by affecting their basal metabolic rate during development, their egg load at emergence, and their life expectancy as adults. Using an aphid–parasitoid model system, we investigated the influence of developmental and adult temperature on the risk‐sensitive decision‐making of females. We considered the use of a low‐quality host nymphal instar by the aphid parasitoid Aphidius ervi to be a risk‐prone behaviour. Immature females were reared at 12, 20 or 28 °C and had access to the four nymphal instars of the potato aphid Macrosiphum euphorbiae for oviposition at one of these temperatures. Host selection behaviour was continuously recorded during exploitation of an aphid patch. We observed that warm‐developed females and parasitoids foraging at high temperature attacked low‐quality hosts more frequently than females from other treatments. These results support the hypothesis that a decrease in expected parasitoid reproductive success resulted in risk‐prone behaviours. To our knowledge, this is the first experimental evidence suggesting that temperature influences host stage selection and risk‐sensitive making decision in parasitoids, and the present study is the first to support the relative fitness rule. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●●, ●●–●●.     

Omnivory,vertical food‐web structure and system productivity: stable isotope analysis of freshwater planktonic food webs

1. The energetic hypothesis proposes that the vertical structure of food webs should increase in height with increasing system productivity. I measured the trophic positions and extent of trophic separation between the invertebrate planktivores Mysis relicta and Chaoborus spp. and their putative zooplankton prey along a gradient of lake productivity with the use of stable nitrogen isotopes. 2. In lakes of low productivity, these planktivores were found to be herbivorous, becoming omnivorous at intermediate lake productivities, and only able to be truly zooplanktivorous as lakes approached mesotrophy. A subsequent secondary analysis of literature data revealed that the strength of top‐down trophic cascades among these organisms increased with lake productivity as reflected by relationships between the abundance of planktivores and that of phytoplankton. 3. Increased omnivory under conditions of low productivity, effectively shortening the vertical structure of food webs as predicted by the energetic hypothesis, may produce increased community stability.