Functional benefits of predator species diversity depend on prey identity

Abstract.  1. Determining the functional significance of species diversity in natural enemy assemblages is a key step towards prediction of the likely impact of biodiversity loss on natural pest control processes. While the biological control literature contains examples in which increased natural enemy diversity hinders pest control, other studies have highlighted mechanisms where pest suppression is promoted by increased enemy diversity.
2. This study aimed to test whether increased predator species diversity results in higher rates of predation on two key, but contrasting, insect pest species commonly found in the rice ecosystems of south-east Asia.
3. Glasshouse experiments were undertaken in which four life stages of a planthopper ( Nilaparvata lugens ) and a moth ( Marasmia patnalis ) were caged with single or three-species combinations of generalist predators.
4. Generally, predation rates of the three-species assemblages exceeded expectation when attacking M. patnalis , but not when attacking N. lugens. In addition, a positive effect of increased predator species richness on overall predation rate was found with M. patnalis but not with N. lugens .
5. The results are consistent with theoretical predictions that morphological and behavioural differentiation among prey life stages promotes functional complementarity among predator species. This indicates that emergent species diversity effects in natural enemy assemblages are context dependent; they depend not only on the characteristics of the predators species, but on the identity of the species on which they prey.     

Conserving species‐rich predator assemblages strengthens natural pest control in a climate warming context

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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 pratense and Vicia faba ) and natural enemy species ( Harmonia axyridis , Coleomegilla maculata and Nabis sp.) 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.     

Size‐based interactions across trophic levels in food webs of shallow Mediterranean lakes

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Emergent effects of ground beetles size diversity on the strength of prey suppression

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Understanding biodiversity effects on prey in multi-enemy systems

Biodiversity–ecosystem functioning theory would predict that increasing natural enemy richness should enhance prey consumption rate due to functional complementarity of enemy species. However, several studies show that ecological interactions among natural enemies may result in complex effects of enemy diversity on prey consumption. Therefore, the challenge in understanding natural enemy diversity effects is to predict consumption rates of multiple enemies taking into account effects arising from patterns of prey use together with species interactions. Here, we show how complementary and redundant prey use patterns result in additive and saturating effects, respectively, and how ecological interactions such as phenotypic niche shifts, synergy and intraguild predation enlarge the range of outcomes to include null, synergistic and antagonistic effects. This study provides a simple theoretical framework that can be applied to experimental studies to infer the biological mechanisms underlying natural enemy diversity effects on prey.     

No correlation between the diversity and productivity of assemblages: evidence from the phytophage and predator assemblages in various cotton agroecosystems

Biodiversity research has shown that primary productivity increases with plant species number, especially in many experimental grassland systems. Here, we assessed the correlation between productivity and diversity of phytophages and natural enemy assemblages associated with planting date and intercropping in four cotton agroecosystems. Twenty-one pairs of data were used to determine Pearson correlations between species richness, total number of individuals, diversity indices and productivity for each assemblage every five days from 5 June to 15 September 2012. At the same trophic level, the productivity exhibited a significant positive correlation with species richness of the phytophage or predator assemblage. A significant correlation was found between productivity and total number of individuals in most cotton fields. However, no significant correlations were observed between productivity and diversity indices (including indices of energy flow diversity and numerical diversity) in most cotton fields for either the phytophage or the predator assemblages. Species richness of phytophage assemblage and total individual numbers were significantly correlated with primary productivity. Also, species richness of natural enemy assemblage and total number of individuals correlated with phytophage assemblage productivity. A negative but not significant correlation occurred between the indices of numerical diversity and energy flow diversity and lower trophic-level productivity in the cotton-phytophage and phytophage-predator assemblages for most intercropped cotton agroecosystems. Our results clearly showed that there were no correlations between diversity indices and productivity within the same or lower trophic levels within the phytophage and predator assemblages in cotton agroecosystems, and inter-cropped cotton fields had a stronger ability to support the natural enemy assemblage and potentially to reduce phytophages.     

Additive effects of predator diversity on pest control caused by few interactions among predator species

1. Studies of the impact of predator diversity on biological pest control have shown idiosyncratic results. This is often assumed to be as a result of differences among systems in the importance of predator–predator interactions such as facilitation and intraguild predation. The frequency of such interactions may be altered by prey availability and structural complexity. A direct assessment of interactions among predators is needed for a better understanding of the mechanisms affecting prey abundance by complex predator communities. 2. In a field cage experiment, the effect of increased predator diversity (single species vs. three‐species assemblage) and the presence of weeds (providing structural complexity) on the biological control of cereal aphids were tested and the mechanisms involved were investigated using molecular gut content analysis. 3. The impact of the three‐predator species assemblages of aphid populations was found to be similar to those of the single‐predator species treatments, and the presence or absence of weeds did not alter the patterns observed. This suggests that both predator facilitation and intraguild predation were absent or weak in this system, or that these interactions had counteracting effects on prey suppression. Molecular gut content analysis of predators provided little evidence for the latter hypothesis: predator facilitation was not detected and intraguild predation occurred at a low frequency. 4. The present study suggests additive effects of predators and, therefore, that predator diversity per se neither strengthens nor weakens the biological control of aphids in this system.     

Prey diversity and prey identity affect herbivore performance on different time scales in a long term aquatic food‐web experiment

The question whether and how diversity‐mediated productivity at the base of food‐webs influences adjacent trophic levels is still unclear. Experiments revealed negative effects on consumers due to the increasing dominance of inedible species under grazing pressure, and positive effects due to a greater variety of prey resources. We experimentally investigate two more hypotheses, which have not been addressed in detail so far: first, more diverse primary producer communities potentially use limiting resources more efficiently, and are, therefore, more productive. This effect can be considered functionally similar to a direct enrichment with limiting resources, potentially resulting in a higher stochastic risk of herbivore extinction (‘paradox of enrichment’). Second, in a stable environment, enclosed primary producer communities should evolve towards a ‘climax state’, eventually dominated by one or few prey species. Therefore, long‐term diversity effects in producer communities should more likely result from the specific traits of the dominating species, than from complementarity. To address these hypotheses, we conducted long‐term laboratory experiments, exposing the freshwater grazer Daphnia magna to a gradient of algal species richness (1, 2, 4 or 8 edible chlorophyte species). The experiments were run in batch cultures, without exchange of growth medium after the start of the experiment. Six parameters related to Daphnia population demography, biomass accrual, and stability were followed and determined over a period of up to 263 days. Producer diversity exhibited strong positive effects on the short‐term performance of grazers (first reproduction, first population peak), and on grazer mean standing stocks. However, herbivore long‐term dynamics (day of extinction and temporal stability) depended on prey species identity, namely the presence of Chlamydomonas reinhardtii. Our experiments suggest that both prey diversity and identity can have positive effects on consumer performance, but act on different time scales.     

Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species

Abstract 1. It has become apparent that predators may strongly decrease prey fitness without direct contact with the prey, as they induce the development of defence systems that limit the availability of energy for growth and reproduction. Recent studies suggest that stress proteins may help prey organisms deal with this stress. The pattern is not general, however, and little is known about species differences in physiological traits in coping with predator stress, and covariation of physiological with other antipredator traits. 2. To explore these issues, we quantified levels of constitutive and fish‐induced stress proteins (Hsp60 and Hsp70) and anti‐predator behaviours in larvae of two damselfly species that differ in lifestyle. Both stress proteins were fixed at higher levels in Erythromma najas, which has a slow lifestyle, than in Lestes sponsa, which has a fast lifestyle. Similarly, anti‐predator behaviours were fixed at safer levels in E. najas than in L. sponsa. 3. These results suggest that stress proteins may be part of anti‐predator syndromes of damselfly larvae, and there may be trait co‐specialisation between stress proteins and behavioural anti‐predator traits. Studies formally testing these hypotheses in more species may prove rewarding in advancing our understanding of the functional integration of physiological anti‐predator traits in relation to the prey’s lifestyle.     

Enemy targeting, trade-offs, and the evolutionary assembly of a tortoise beetle defense arsenal

In response to intense enemy selection, immature folivorous insects have evolved elaborate, multi-trait defense arsenals. How enemies foster trait diversification and arsenal assembly depends on which selective mode they impose: whether different enemies select for the same defense or exert conflicting selection on a prey species. Theory has long supposed that the selective advantage of a defense depends on its efficacy against a broad spectrum of enemies, which implies that predator selection is more diffuse than pairwise. Here, we use the multi-trait defense arsenal of the tortoise beetle, Acromis sparsa, which consists of shields, gregariousness and maternal guarding to test whether: (1) diverse enemies have selected for narrowly targeted defenses in the Acromis lineage; (2) newer traits out-performed older ones or vice versa, and; (3) if selection by different enemies results in positive (escalation) trends in defense effectiveness. Because their defenses could be modified or ablated, individuals were rendered differentially protected, and their survival was quantified in a long-term field study. Exclusion experiments evaluated defense efficacy against particular enemy guilds. Logit regression revealed that: (1)no single trait increased survival against the entire enemy suite; (2)trait efficacy was strongly correlated with a particular enemy, consistent with narrow targeting; (3)traits lacked strong cross-resistance among enemies; (4)traits performed synergistically, consistent with the idea of escalation, and; (5)traits interacted negatively to decrease survival, indicative of performance trade-offs. From collation of the phylogenetic histories of arsenal and enemy community assembly we hypothesize that older traits performed better against older enemies and that patterns of both trait and enemy accumulation are consistent with defense escalation. Trade-offs and lack of cross-resistance among defenses imply that enemy selection has been conflicting at the guild level and that negative functional interactions among defenses have fostered the evolution of a defense arsenal of increasing complexity.     

Diversity of protists and bacteria determines predation performance and stability

Predation influences prey diversity and productivity while it effectuates the flux and reallocation of organic nutrients into biomass at higher trophic levels. However, it is unknown how bacterivorous protists are influenced by the diversity of their bacterial prey. Using 456 microcosms, in which different bacterial mixtures with equal initial cell numbers were exposed to single or multiple predators (Tetrahymena sp., Poterioochromonas sp. and Acanthamoeba sp.), we showed that increasing prey richness enhanced production of single predators. The extent of the response depended, however, on predator identity. Bacterial prey richness had a stabilizing effect on predator performance in that it reduced variability in predator production. Further, prey richness tended to enhance predator evenness in the predation experiment including all three protists predators (multiple predation experiment). However, we also observed a negative relationship between prey richness and predator production in multiple predation experiments. Mathematical analysis of potential ecological mechanisms of positive predator diversity—functioning relationships revealed predator complementarity as a factor responsible for both enhanced predator production and prey reduction. We suggest that the diversity at both trophic levels interactively determines protistan performance and might have implications in microbial ecosystem processes and services.     

A cross‐system meta‐analysis reveals coupled predation effects on prey biomass and diversity

Predator diversity and abundance are under strong human pressure in all types of ecosystems. Whereas predator potentially control standing biomass and species interactions in food webs, their effects on prey biomass and especially prey biodiversity have not yet been systematically quantified. Here, we test the effects of predation in a cross‐system meta‐analysis of prey diversity and biomass responses to local manipulation of predator presence. We found 291 predator removal experiments from 87 studies assessing both diversity and biomass responses. Across ecosystem types, predator presence significantly decreased both biomass and diversity of prey across ecosystems. Predation effects were highly similar between ecosystem types, whereas previous studies had shown that herbivory or decomposition effects differed fundamentally between terrestrial and aquatic systems based on different stoichiometry of plant material. Such stoichiometric differences between systems are unlikely for carnivorous predators, where effect sizes on species richness strongly correlated to effect sizes on biomass. However, the negative predation effect on prey biomass was ameliorated significantly with increasing prey richness and increasing species richness of the manipulated predator assemblage. Moreover, with increasing richness of the predator assemblage present, the overall negative effects of predation on prey richness switched to positive effects. Our meta‐analysis revealed strong general relationships between predator diversity, prey diversity and the interaction strength between trophic levels in terms of biomass. This study indicates that anthropogenic changes in predator abundance and diversity will potentially have strong effects on trophic interactions across ecosystems. Synthesis The past centuries we have experienced a dramatic loss of top–predator abundance and diversity in most types of ecosystems. To understand the direct consequences of predator loss on a global scale, we quantitatively summarized experiments testing predation effects on prey communities in a cross‐system meta‐analysis. Across ecosystem types, predator presence significantly decreased both biomass and diversity of prey, and predation effects were highly similar. However, with increasing predator richness, the overall negative effects of predation on prey richness switched to positive ones. Anthropogenic changes in predator communities will potentially have strong effects on prey diversity, biomass, and trophic interactions across ecosystems.     

Interactive effects of productivity and predation on zooplankton diversity

Recent studies suggest the necessity of understanding the interactive effects of predation and productivity on species coexistence and prey diversity. Models predict that coexistence of prey species with different competitive abilities can be achieved if inferior resource competitors are less susceptible to predation and if productivity and/or predation pressure are at intermediate levels. Hence, predator effects on prey diversity are predicted to be highly context dependent: enhancing diversity from low to intermediate levels of productivity or predation and reducing diversity of prey at high levels of productivity or predation. While several studies have examined the interactive effects of herbivory and productivity on primary producer diversity, experimental studies of such effects in predator‐prey systems are rare. We tested these predictions using an aquatic field mesocosm experiment in which initial density of the zooplankton predator Notonecta undulata and productivity were manipulated to test their interactive effects on diversity of seven zooplankton, cladoceran species that were common in surrounding ponds. Two productivity levels were imposed via phosphorus enrichment at levels comparable to low and intermediate levels found within neighboring natural ponds. We used open systems to allow for natural dispersal and behaviorally‐mediated numerical responses by the flight‐capable predator. Effects of predators on zooplankton diversity depended on productivity level. At low and high productivity, prey species richness declined while at high productivity it showed a unimodal relationship with increasing the predator density. Effects of treatments were weaker when using Pielou's evenness index or the inverse Simpson index as measures of prey diversity. Our findings are generally consistent with model predictions in which predators can facilitate prey coexistence and diversity at intermediate levels of productivity and predation intensity. Our work also shows that the functional form of the relationship between prey diversity and predation intensity can be complex and highly dependent on environmental context.     

The effect of multiple natural enemies on a shared herbivore prey

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PREY ADAPTATION AS A CAUSE OF PREDATOR-PREY CYCLES

We analyze simple models of predator-prey systems in which there is adaptive change in a trait of the prey that determines the rate at which it is captured by searching predators. Two models of adaptive change are explored: (1) change within a single reproducing prey population that has genetic variation for vulnerability to capture by the predator; and (2) direct competition between two independently reproducing prey populations that differ in their vulnerability. When an individual predator's consumption increases at a decreasing rate with prey availability, prey adaptation via either of these mechanisms may produce sustained cycles in both species' population densities and in the prey's mean trait value. Sufficiently rapid adaptive change (e.g., behavioral adaptation or evolution of traits with a large additive genetic variance), or sufficiently low predator birth and death rates will produce sustained cycles or chaos, even when the predator-prey dynamics with fixed prey capture rates would have been stable. Adaptive dynamics can also stabilize a system that would exhibit limit cycles if traits were fixed at their equilibrium values. When evolution fails to stabilize inherently unstable population interactions, selection decreases the prey's escape ability, which further destabilizes population dynamics. When the predator has a linear functional response, evolution of prey vulnerability always promotes stability. The relevance of these results to observed predator-prey cycles is discussed.     

Functional traits determine heterospecific use of risk‐related social information in forest birds of tropical South‐East Asia

In birds and mammals, mobbing calls constitute an important form of social information that can attract numerous sympatric species to localized mobbing aggregations. While such a response is thought to reduce the future predation risk for responding species, there is surprisingly little empirical evidence to support this hypothesis. One way to test the link between predation risk reduction and mobbing attraction involves testing the relationship between species’ attraction to mobbing calls and the functional traits that define their vulnerability to predation risk. Two important traits known to influence prey vulnerability include relative prey‐to‐predator body size ratio and the overlap in space use between predator and prey; in combination, these measures strongly influence prey accessibility, and therefore their vulnerability, to predators. Here, we combine community surveys with behavioral experiments of a diverse bird assemblage in the lowland rainforest of Sumatra to test whether the functional traits of body mass (representing body size) and foraging height (representing space use) can predict species’ attraction to heterospecific mobbing calls. At four forest sites along a gradient of forest degradation, we characterized the resident bird communities using point count and mist‐netting surveys, and determined the species groups attracted to standardized playbacks of mobbing calls produced by five resident bird species of roughly similar body size and foraging height. We found that (1) a large, diverse subcommunity of bird species was attracted to the mobbing calls and (2) responding species (especially the most vigorous respondents) tended to be (a) small (b) mid‐storey foragers (c) with similar trait values as the species producing the mobbing calls. Our findings from the relatively lesser known bird assemblages of tropical Asia add to the growing evidence for the ubiquity of heterospecific information networks in animal communities, and provide empirical support for the long‐standing hypothesis that predation risk reduction is a major benefit of mobbing information networks.     

A trait‐based approach reveals the feeding selectivity of a small endangered Mediterranean fish

Functional traits are growing in popularity in modern ecology, but feeding studies remain primarily rooted in a taxonomic‐based perspective. However, consumers do not have any reason to select their prey using a taxonomic criterion, and prey assemblages are variable in space and time, which makes taxon‐based studies assemblage‐specific. To illustrate the benefits of the trait‐based approach to assessing food choice, we studied the feeding ecology of the endangered freshwater fish Barbus meridionalis. We hypothesized that B. meridionalis is a selective predator which food choice depends on several prey morphological and behavioral traits, and thus, its top‐down pressure may lead to changes in the functional composition of in‐stream macroinvertebrate communities. Feeding selectivity was inferred by comparing taxonomic and functional composition (13 traits) between ingested and free‐living potential prey using the Jacob's electivity index. Our results showed that the fish diet was influenced by 10 of the 13 traits tested. Barbus meridionalis preferred prey with a potential size of 5–10 mm, with a medium–high drift tendency, and that drift during daylight. Potential prey with no body flexibility, conical shape, concealment traits (presence of nets and/or cases, or patterned coloration), and high aggregation tendency had a low predation risk. Similarly, surface swimmers and interstitial taxa were low vulnerable to predation. Feeding selectivity altered the functional composition of the macroinvertebrate communities. Fish absence favored taxa with weak aggregation tendency, weak flexibility, and a relatively large size (10–20 mm of potential size). Besides, predatory invertebrates may increase in fish absence. In conclusion, our study shows that the incorporation of the trait‐based approach in diet studies is a promising avenue to improve our mechanistic understanding of predator–prey interactions and to help predict the ecological outcomes of predator invasions and extinctions.     

Keystone nonconsumptive effects within a diverse predator community

The number of prey killed by diverse predator communities is determined by complementarity and interference among predators, and by traits of particular predator species. However, it is less clear how predators' nonconsumptive effects (NCEs) scale with increasing predator biodiversity. We examined NCEs exerted on Culex mosquitoes by a diverse community of aquatic predators. In the field, mosquito larvae co‐occurred with differing densities and species compositions of mesopredator insects; top predator dragonfly naiads were present in roughly half of surveyed water bodies. We reproduced these predator community features in artificial ponds, exposing mosquito larvae to predator cues and measuring resulting effects on mosquito traits throughout development. Nonconsumptive effects of various combinations of mesopredator species reduced the survival of mosquito larvae to pupation, and reduced the size and longevity of adult mosquitoes that later emerged from the water. Intriguingly, adding single dragonfly naiads to ponds restored survivorship of larval mosquitoes to levels seen in the absence of predators, and further decreased adult mosquito longevity compared with mosquitoes emerging from mesopredator treatments. Behavioral observations revealed that mosquito larvae regularly deployed “diving” escape behavior in the presence of the mesopredators, but not when a dragonfly naiad was also present. This suggests that dragonflies may have relaxed NCEs of the mesopredators by causing mosquitoes to abandon energetically costly diving. Our study demonstrates that adding one individual of a functionally unique species can substantially alter community‐wide NCEs of predators on prey. For pathogen vectors like mosquitoes, this could in turn influence disease dynamics.     

A meta‐analysis of non‐consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

Non‐consumptive effects (NCEs) – changes in prey behavior or physiology in response to predator threat – are common and can be as strong as consumptive effects. However, our knowledge of NCEs in arthropod systems is lacking. Factors related to study organism and environment have the potential to influence the occurrence and magnitude of NCEs in arthropod systems. While factors such as coevolutionary history of natural enemies and their prey, predator cue, predator or prey feeding mode, and refuge availability have been theoretically and empirically examined, no trends have been proposed for arthropods. We compiled 62 studies, yielding 128 predator–prey interactions, which explicitly examined NCEs in experiments where arthropods were identified to species, using a previously published database of papers from 1990 to 2005 and a new database of papers published from 2006 to 2015. Using these data, we conducted a meta‐analysis to explore the influence of organismal and environmental characteristics on the magnitude of predator NCEs. Our analysis addressed the following three questions. 1) Does predator–prey coevolution give rise to stronger NCEs than when predator and prey species did not coevolve? 2) What influence does habitat type and refuge availability have on NCEs? 3) How do predator characteristics (cue type, hunting mode and life stage) and prey characteristics (mobility, life stage, specialization, gregariousness and feeding mode) influence NCEs? We found that while NCEs were similar across most measured characteristics, NCEs on prey activity were significantly stronger when predator and prey shared an evolutionary history. Our results support growing evidence that NCEs have a negative effect on prey traits and that behavioral NCEs are stronger than physiological ones. Additional studies are needed to be confident in any emerging patterns, therefore we identify key gaps in the literature on NCEs in arthropod systems and discuss ideas for moving forward.