Rapid prey evolution and the dynamics of two-predator food webs

Traits affecting ecological interactions can evolve on the same time scale as population and community dynamics, creating the potential for feedbacks between evolutionary and ecological dynamics. Theory and experiments have shown in particular that rapid evolution of traits conferring defense against predation can radically change the qualitative dynamics of a predator–prey food chain. Here, we ask whether such dramatic effects are likely to be seen in more complex food webs having two predators rather than one, or whether the greater complexity of the ecological interactions will mask any potential impacts of rapid evolution. If one prey genotype can be well-defended against both predators, the dynamics are like those of a predator–prey food chain. But if defense traits are predator-specific and incompatible, so that each genotype is vulnerable to attack by at least one predator, then rapid evolution produces distinctive behaviors at the population level: population typically oscillate in ways very different from either the food chain or a two-predator food web without rapid prey evolution. When many prey genotypes coexist, chaotic dynamics become likely. The effects of rapid evolution can still be detected by analyzing relationships between prey abundance and predator population growth rates using methods from functional data analysis.     

Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay

Parasites that are transmitted through predator–prey interactions may be used as indicators of trophic relationships between organisms. Yet, they are rarely used as such in the construction of topological (predator–prey) food webs. We constructed food webs of vertebrate trophic interactions using observed diet alone, trophically transmitted parasites alone, and the combination of the two based on data from 31 species of fish from the Bothnian Bay, Finland. The fish food web contained 530 links derived from observed diet, 724 links inferred from parasitism, and 1,058 links calculated from a combination of both stomach contents and parasites. This sub-web constructed from stomach contents had a mean of 17.1 links per fish species, while that using parasites had 23.4 links per fish. Combining the two diet indicators yielded 34.1 links per fish species, illustrating the complementarity of the two methods. Mean number of prey species per fish species was 12.5 using observed diet items, 15.8 using parasites, and 24.5 using both measures together. Mean number of predators per fish species was 7.4 using observed diet, 11.7 using parasites and 15.0 using both. A positive correlation was found between the mean number of parasites and the number of prey taxa in the diet among the fishes. Omnivorous fish had the highest diversity of both parasite species and prey items, while benthophagous fish had among the lowest. Mean total abundance and mean total prevalence of parasites correlated positively with fish size, with piscivores being the largest with the highest abundance and prevalence, while planktivores and benthivores had the lowest. Trophically transmitted parasites may be used to help construct vertebrate sub-webs and derive information about food web processes. Parasites alone provided equivalent if not more information than observed diet. However, resolution is improved by using parasites and observed diet together.     

Effects of trophic skewing of species richness on ecosystem functioning in a diverse marine community

Widespread overharvesting of top consumers of the world's ecosystems has "skewed" food webs, in terms of biomass and species richness, towards a generally greater domination at lower trophic levels. This skewing is exacerbated in locations where exotic species are predominantly low-trophic level consumers such as benthic macrophytes, detritivores, and filter feeders. However, in some systems where numerous exotic predators have been added, sometimes purposefully as in many freshwater systems, food webs are skewed in the opposite direction toward consumer dominance. Little is known about how such modifications to food web topology, e.g., changes in the ratio of predator to prey species richness, affect ecosystem functioning. We experimentally measured the effects of trophic skew on production in an estuarine food web by manipulating ratios of species richness across three trophic levels in experimental mesocosms. After 24 days, increasing macroalgal richness promoted both plant biomass and grazer abundance, although the positive effect on plant biomass disappeared in the presence of grazers. The strongest trophic cascade on the experimentally stocked macroalgae emerged in communities with a greater ratio of prey to predator richness (bottom-rich food webs), while stronger cascades on the accumulation of naturally colonizing algae (primarily microalgae with some early successional macroalgae that recruited and grew in the mesocosms) generally emerged in communities with greater predator to prey richness (the more top-rich food webs). These results suggest that trophic skewing of species richness and overall changes in food web topology can influence marine community structure and food web dynamics in complex ways, emphasizing the need for multitrophic approaches to understand the consequences of marine extinctions and invasions.     

Predator hunting mode influences patterns of prey use from grazing and epigeic food webs

Multichannel omnivory by generalist predators, especially the use of both grazing and epigeic prey, has the potential to increase predator abundance and decrease herbivore populations. However, predator use of the epigeic web (soil surface detritus/microbe/algae consumers) varies considerably for reasons that are poorly understood. We therefore used a stable isotope approach to determine whether prey availability and predator hunting style (active hunting vs. passive web-building) impacted the degree of multichannel omnivory by the two most abundant predators on an intertidal salt marsh, both spiders. We found that carbon isotopic values of herbivores remained constant during the growing season, while values for epigeic feeders became dramatically more enriched such that values for the two webs converged in August. Carbon isotopic values for both spider species remained midway between the two webs as values for epigeic feeders shifted, indicating substantial use of prey from both food webs by both spider species. As the season progressed, prey abundance in the grazing food web increased while prey abundance in the epigeic web remained constant or declined. In response, prey consumption by the web-building spider shifted toward the grazing web to a much greater extent than did consumption by the hunting spider, possibly because passive web-capture is more responsive to changes in prey availability. Although both generalist predator species engaged in multichannel omnivory, hunting mode influenced the extent to which these predators used prey from the grazing and epigeic food webs, and could thereby influence the strength of trophic cascades in both food webs.     

Transient dynamics limit the effectiveness of keystone predation in bringing about coexistence

We analyze the transient dynamics of simple models of keystone predation, in which a predator preferentially consumes the dominant of two (or more) competing prey species. We show that coexistence is unlikely in many systems characterized both by successful invasion of either prey species into the food web that lacks it and by a stable equilibrium with high densities of all species. Invasion of the predator-resistant consumer species often causes the resident, more vulnerable prey to crash to such low densities that extinction would occur for many realistic population sizes. Subsequent transient cycles may entail very low densities of the predator or of the initially successful invader, which may also preclude coexistence of finite populations. Factors causing particularly low minimum densities during the transient cycles include biotic limiting resources for the prey, limited resource partitioning between the prey, a highly efficient predator with relatively slow dynamics, and a vulnerable prey whose population dynamics are rapid relative to the less vulnerable prey. Under these conditions, coexistence of competing prey via keystone predation often requires that the prey's competitive or antipredator characteristics fall within very narrow ranges. Similar transient crashes are likely to occur in other food webs and food web models.     

Foraging theory predicts predator-prey energy fluxes

1. In natural communities, populations are linked by feeding interactions that make up complex food webs. The stability of these complex networks is critically dependent on the distribution of energy fluxes across these feeding links. 2. In laboratory experiments with predatory beetles and spiders, we studied the allometric scaling (body-mass dependence) of metabolism and per capita consumption at the level of predator individuals and per link energy fluxes at the level of feeding links. 3. Despite clear power-law scaling of the metabolic and per capita consumption rates with predator body mass, the per link predation rates on individual prey followed hump-shaped relationships with the predator-prey body mass ratios. These results contrast with the current metabolic paradigm, and find better support in foraging theory. 4. This suggests that per link energy fluxes from prey populations to predator individuals peak at intermediate body mass ratios, and total energy fluxes from prey to predator populations decrease monotonically with predator and prey mass. Surprisingly, contrary to predictions of metabolic models, this suggests that for any prey species, the per link and total energy fluxes to its largest predators are smaller than those to predators of intermediate body size. 5. An integration of metabolic and foraging theory may enable a quantitative and predictive understanding of energy flux distributions in natural food webs.     

Evolution mediates the effects of apex predation on aquatic food webs

Ecological and evolutionary mechanisms are increasingly thought to shape local community dynamics. Here, I evaluate if the local adaptation of a meso-predator to an apex predator alters local food webs. The marbled salamander (Ambystoma opacum) is an apex predator that consumes both the spotted salamander (Ambystoma maculatum) and shared zooplankton prey. Common garden experiments reveal that spotted salamander populations which co-occur with marbled salamanders forage more intensely than those that face other predator species. These foraging differences, in turn, alter the diversity, abundance and composition of zooplankton communities in common garden experiments and natural ponds. Locally adapted spotted salamanders exacerbate prey biomass declines associated with apex predation, but dampen the top-down effects of apex predation on prey diversity. Countergradient selection on foraging explains why locally adapted spotted salamanders exacerbate prey biomass declines. The two salamander species prefer different prey species, which explains why adapted spotted salamanders buffer changes in prey composition owing to apex predation. Results suggest that local adaptation can strongly mediate effects from apex predation on local food webs. Community ecologists might often need to consider the evolutionary history of populations to understand local diversity patterns, food web dynamics, resource gradients and their responses to disturbance.     

Examining the potential effects of species aggregation on the network structure of food webs

One of the key measures that have been used to describe the topological properties of complex networks is the “degree distribution”, which is a measure that describes the frequency distribution of number of links per node. Food webs are complex ecological networks that describe the trophic relationships among species in a community, and the topological properties of empirical food webs, including degree distributions, have been examined previously. Previously, the “niche model” has been shown to accurately predict degree distributions of empirical food webs, however, the niche model-generated food webs were referenced against empirical food webs that had their species grouped together based on their taxonomic and/or trophic relationships (aggregated food webs). Here, we explore the effects of species aggregation on the ability of the niche model to predict the total- (sum of prey and predator links per node), in- (number of predator links per node), and out- (number of prey links per node) degree distributions of empirical food webs by examining two food webs that can be aggregated at different levels of resolution. The results showed that (1) the cumulative total- and out-degree distributions were consistent with the niche model predictions when the species were aggregated, (2) when the species were disaggregated (i.e., higher resolution), there were mixed conclusions with regards to the niche model's ability to predict total- and out-degree distributions, (3) the model's ability to predict the in-degree distributions of the two food webs was generally inadequate. Although it has been argued that universal functional form based on the niche model could describe the degree distribution patterns of empirical food webs, we believe there are some limitations to the model's ability to accurately predict the structural properties of food webs.     

Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission

While the recent inclusion of parasites into food‐web studies has highlighted the role of parasites as consumers, there is accumulating evidence that parasites can also serve as prey for predators. Here we investigated empirical patterns of predation on parasites and their relationships with parasite transmission in eight topological food webs representing marine and freshwater ecosystems. Within each food web, we examined links in the typical predator–prey sub web as well as the predator–parasite sub web, i.e. the quadrant of the food web indicating which predators eat parasites. Most predator– parasite links represented ‘concomitant predation’ (consumption and death of a parasite along with the prey/host; 58–72%), followed by ‘trophic transmission’ (predator feeds on infected prey and becomes infected; 8–32%) and predation on free‐living parasite life‐cycle stages (4–30%). Parasite life‐cycle stages had, on average, between 4.2 and 14.2 predators. Among the food webs, as predator richness increased, the number of links exploited by trophically transmitted parasites increased at about the same rate as did the number of links where these stages serve as prey. On the whole, our analyses suggest that predation on parasites has important consequences for both predators and parasites, and food web structure. Because our analysis is solely based on topological webs, determining the strength of these interactions is a promising avenue for future research.     

Interactions of multiple predators with different foraging modes in an aquatic food web

Top predators can have different foraging modes that may alter their interactions and effects on food webs. Interactions between predators may be non-additive resulting from facilitation or interference, whereas their combined effects on a shared prey may result in emergent effects that are risk enhanced or risk reduced. To test the importance of multiple predators with different foraging modes, we examined the interaction between a cruising predator (largemouth bass, Micropterus salmoides) and an ambush predator (muskellunge, Esox masquinongy) foraging on a shared prey (bluegill sunfish, Lepomis macrochirus) with strong anti-predator defense behaviors. Additive and substitution designs were used to compare individual to combined predator treatments in experimental ponds. The multiple predator interaction facilitated growth of the cruising predator in the combined predator treatments, whereas predator species had substitutable effects on the growth of the ambush predator. The combined predator treatments created an emergent effect on the prey; however, the direction was dependent on the experimental design. The additive design found a risk-reducing effect, whereas the substitution design found a risk-enhancing effect for prey fish. Indirect effects from the predators weakly extended to lower trophic levels (i.e., zooplankton community). Our results highlight the need to consider differences in foraging mode of top predators, interactions between predators, and emergent effects on prey to understand food webs.     

A size-constrained feeding-niche model distinguishes predation patterns between aquatic and terrestrial food webs

Understanding the formation of feeding links provides insights into processes underlying food webs. Generally, predators feed on prey within a certain body-size range, but a systematic quantification of such feeding niches is lacking. We developed a size-constrained feeding-niche (SCFN) model and parameterized it with information on both realized and non-realized feeding links in 72 aquatic and 65 terrestrial food webs. Our analyses revealed profound differences in feeding niches between aquatic and terrestrial predators and variation along a temperature gradient. Specifically, the predator–prey body-size ratio and the range in prey sizes increase with the size of aquatic predators, whereas they are nearly constant across gradients in terrestrial predator size. Overall, our SCFN model well reproduces the feeding relationships and predation architecture across 137 natural food webs (including 3878 species and 136,839 realized links). Our results illuminate the organisation of natural food webs and enables novel trait-based and environment-explicit modelling approaches.     

The predators of insects

Abstract. 1. Insect–insectivore trophic relations were reviewed using presence–absence data from sixty-one invertebrate-dominated food webs and fifteen food webs from Briand's (1983) original forty web collection. From counts of prey links in higher taxa (orders, classes, phyla), six phyla and thirteen classes of non-insect insectivores and fourteen orders of insect predators and prey were found. 2. Detritus-based habitats (phytotelmata, felled logs, carcasses, dungpads) harboured fewer orders of insects, that interact with other insects, than webs from grazer-based (host plants, some galls) and mixed-based systems (aquatic webs). Consumer–resource networks of higher insect taxa in these webs shared several features found in some species-level biological networks: the trend was towards few pairs of strong asymmetrical links, several weak links and many null interactions. 3. From counts of insect predator–insect prey links, hymenopterans as terrestrial predators and parasitoids interacted with the most number of higher insect taxa. Hymenopterans were also linked as prey more often than other terrestrial insects. In freshwater habitats, plecopterans were linked as predators more often than other aquatic taxa, whereas dipterans were listed as prey more often than other insects. 4. Dipterans were linked in the diets of non-insect insectivores from seven of eight common taxonomic classes. Arachnids were identified as insect predators by food web researchers in the largest number of webs, followed by passerine birds and cyprinodont fishes. From analysis of prey links at the ordinal level, predaceous insects were less polyphagous than other predators (other ectotherms and endotherms). 5. Analysis of chain lengths, as expected, showed that insect prey occupied mostly lowermost trophic levels, non-insect insectivores were found mostly at uppermost trophic levels, and predaceous insects were found mostly at intermediate trophic levels across most habitats. 6. This analysis offers evidence that insects are not just occupying intermediate trophic levels in some communities. Indeed, some taxa feed at the upper ends of long food chains, for example eupelmids in galls, staphylinids in carcasses, and perlid plecopterans in streams.     

Effects of evolutionary changes in prey use on the relationship between food web complexity and stability

The relationship between food web complexity and stability has been the subject of a long-standing debate in ecology. Although rapid changes in the food web structure through adaptive foraging behavior can confer stability to complex food webs, as reported by Kondoh (Science 299:1388–1391, 2003), the exact mechanisms behind this adaptation have not been specified in previous studies; thus, the applicability of such predictions to real ecosystems remains unclear. One mechanism of adaptive foraging is evolutionary change in genetically determined prey use. We constructed individual-based models of evolution of prey use by predators assuming explicit population genetics processes, and examined how this evolution affects the stability (i.e., the proportion of species that persist) of the food web and whether the complexity of the food web increased the stability of the prey–predator system. The analysis showed that the stability of food webs decreased with increasing complexity regardless of evolution of prey use by predators. The effects of evolution on stability differed depending on the assumptions made regarding genetic control of prey use. The probabilities of species extinctions were associated with the establishment or loss of trophic interactions via evolution of the predator, indicating a clear link between structural changes in the food web and community stability.     

Trophic cascades alter eco-evolutionary dynamics and body size evolution

Trait evolution in predator–prey systems can feed back to the dynamics of interacting species as well as cascade to impact the dynamics of indirectly linked species (eco-evolutionary trophic cascades; EETCs). A key mediator of trophic cascades is body mass, as it both strongly influences and evolves in response to predator–prey interactions. Here, we use Gillespie eco-evolutionary models to explore EETCs resulting from top predator loss and mediated by body mass evolution. Our four-trophic-level food chain model uses allometric scaling to link body mass to different functions (ecological pleiotropy) and is realistically parameterized from the FORAGE database to mimic the parameter space of a typical freshwater system. To track real-time changes in selective pressures, we also calculated fitness gradients for each trophic level. As predicted, top predator loss generated alternating shifts in abundance across trophic levels, and, depending on the nature and strength in changes to fitness gradients, also altered trajectories of body mass evolution. Although more distantly linked, changes in the abundance of top predators still affected the eco-evolutionary dynamics of the basal producers, in part because of their relatively short generation times. Overall, our results suggest that impacts on top predators can set off transient EETCs with the potential for widespread indirect impacts on food webs.     

Predator personality structures prey communities and trophic cascades

Intraspecific variation is central to our understanding of evolution and population ecology, yet its consequences for community ecology are poorly understood. Animal personality – consistent individual differences in suites of behaviours – may be particularly important for trophic dynamics, where predator personality can determine activity rates and patterns of attack. We used mesocosms with aquatic food webs in which the top predator (dragonfly nymphs) varied in activity and subsequent attack rates on zooplankton, and tested the effects of predator personality. We found support for four hypotheses: (1) active predators disproportionately reduce the abundance of prey, (2) active predators select for predator‐resistant prey species, (3) active predators strengthen trophic cascades (increase phytoplankton abundance) and (4) active predators are more likely to cannibalise one another, weakening all other trends when at high densities. These results suggest that intraspecific variation in predator personality is an important determinant of prey abundance, community composition and trophic cascades.     

Non-consumptive effects of predatory mites on thrips and its host plant

Recent reviews on trait-mediated interactions in food webs suggest that trait-mediated effects are as important in triggering top–down trophic cascades as are density-mediated effects. Trait-mediated interactions between predator and prey result from non-consumptive predator effects changing behavioural and/or life history traits of prey. However, in biological control the occurrence of trait-mediated interactions between predators, prey and plants has been largely ignored. Here, we show that non-consumptive predator effects on prey cascade down to the plant in an agro-ecological food chain. The study system consisted of the predatory mites P. persimilis and N. californicus , the herbivorous non-target prey western flower thrips F. occidentalis and the host plant bean. Irrespective of predator species and risk posed to prey, the presence of predator eggs led to increased ambulation, increased mortality and decreased oviposition of thrips. Furthermore, the presence of predator eggs reduced leaf damage caused by thrips. To our knowledge this is the first experimental evidence suggesting a positive trophic cascade triggered by non-consumptive predator effects on non-target prey in an augmentative biological control system.     

The impact of nonlinear functional responses on the long-term evolution of food web structure

We investigate the long-term web structure emerging in evolutionary food web models when different types of functional responses are used. We find that large and complex webs with several trophic layers arise only if the population dynamics is such that it allows predators to focus on their best prey species. This can be achieved using modified Lotka-Volterra or Holling/Beddington functional responses with effective couplings that depend on the predator's efficiency at exploiting the prey, or a ratio-dependent functional response with adaptive foraging. In contrast, if standard Lotka-Volterra or Holling/Beddington functional responses are used, long-term evolution generates webs with almost all species being basal, and with additionally many links between these species. Interestingly, in all cases studied, a large proportion of weak links result naturally from the evolution of the food webs.     

Bacterial adaptation to sublethal antibiotic gradients can change the ecological properties of multitrophic microbial communities

Antibiotics leak constantly into environments due to widespread use in agriculture and human therapy. Although sublethal concentrations are well known to select for antibiotic-resistant bacteria, little is known about how bacterial evolution cascades through food webs, having indirect effect on species not directly affected by antibiotics (e.g. via population dynamics or pleiotropic effects). Here, we used an experimental evolution approach to test how temporal patterns of antibiotic stress, as well as migration within metapopulations, affect the evolution and ecology of microcosms containing one prey bacterium, one phage and two protist predators. We found that environmental variability, autocorrelation and migration had only subtle effects for population and evolutionary dynamics. However, unexpectedly, bacteria evolved greatest fitness increases to both antibiotics and enemies when the sublethal levels of antibiotics were highest, indicating positive pleiotropy. Crucially, bacterial adaptation cascaded through the food web leading to reduced predator-to-prey abundance ratio, lowered predator community diversity and increased instability of populations. Our results show that the presence of natural enemies can modify and even reverse the effects of antibiotics on bacteria, and that antibiotic selection can change the ecological properties of multitrophic microbial communities by having indirect effects on species not directly affected by antibiotics.     

Introduced species provide a novel temporal resource that facilitates native predator population growth

Non-native species are recognized as important components of change to food web structure. Non-native prey may increase native predator populations by providing an additional food source and simultaneously decrease native prey populations by outcompeting them for a limited resource. This pattern of apparent competition may be important for plants and sessile marine invertebrate suspension feeders as they often compete for space and their immobile state make them readily accessible to predators. Reported studies on apparent competition have rarely been examined in biological invasions and no study has linked seasonal patterns of native and non-native prey abundance to increasing native predator populations. Here, we evaluate the effects of non-native colonial ascidians (Diplosoma listerianum and Didemnum vexillum) on population growth of a native predator (bloodstar, Henricia sanguinolenta) and native sponges through long-term surveys of abundance, prey choice and growth experiments. We show non-native species facilitate native predator population growth by providing a novel temporal resource that prevents loss of predator biomass when its native prey species are rare. We expect that by incorporating native and non-native prey seasonal abundance patterns, ecologists will gain a more comprehensive understanding of the mechanisms underlying the effects of non-native prey species on native predator and prey population dynamics.