Predator identity and trait-mediated indirect effects in a littoral food web

Perturbations to the density of a species can be propagated to distant members of a food web via shifts in the density or the traits (i.e. behavior) of intermediary species. Predators with differing foraging modes may have different effects on prey behavior, and these effects may be transmitted differently through food webs. Here we test the hypothesis that shifts in the type of predator present in a food web indirectly affect the prey's resource independent of changes in the density of prey. We assessed the importance of predator identity in mediating the grazing effects of the freshwater snail Physa integra on its periphyton resources using field and mesocosm studies. Field observations showed that Physa used covered habitats more in ponds containing fish than in ponds containing crayfish or no predators at all. A field experiment confirmed that snail behavior depended on predator identity. Physa placed near caged pumpkinseed sunfish (Lepomis gibbosus) selected covered habitats, but Physa placed near caged crayfish (Orconectes rusticus) moved to the surface of the water. The effects of predator identity on periphtyon were then examined in a mesocosm experiment, using caged predators. Habitat use of Physa was similar to their habitat use in the field experiment. In the presence of caged sunfish, periphyton standing crop in covered habitats was reduced to 34% of the standing crop in the presence of crayfish. In contrast, periphyton in near-surface habitats was 110% higher in the presence of fish than in the presence of crayfish. Thus, the effects of predator identity on Physa behavior cascaded through the food web to affect the abundance and spatial distribution of periphyton.     

Effects of micrometazoa on the protistan assemblage of a littoral food web

SUMMARY. 1. Effects of two size-classes of micrometazoa (assemblages of rotifers and of rotifers/cladocerans/copepods) on the abundance and composition of a co-occurring, substrate-associated protistan assemblage were assessed by selectively transferring these groups from a small pond to laboratory microcosms.
2. Addition of micrometazoa to the microcosms resulted in significant changes in the dominance of different protistan groups within 7 days, including a substantial decrease in the abundance of larger omnivorous and bactivorous Protozoa, mostly ciliates, and dominant algal taxa, and an increase in the abundance of heterotrophic microflagellates.
3. Mechanisms whereby micrometazoa reduce the abundance of larger heterotrophic protists may include competition for overlapping resources, but probably involves interference and predation as well. Positive effects of Metazoa on the abundance of heterotrophic microflagellates may result from the elimination of ciliates that prey on and compete with smaller Protozoa.
4. Interactions indicated in this study may alter both quantitative and qualitative aspects of energy flow and mineral cycling in benthic food-webs and be part of a larger trophic cascade involving other Metazoa such as fish.     

Carbon flow in the littoral food web of an oligotrophic lake

Benthic food web dynamics and carbon flow were examined in the littoral zone of Lake Coleridge, a large deep oligotrophic lake, using radioactive and stable isotope techniques in conjunction with analyses of stomach contents of the fauna. We specifically address two hypotheses: (1) that macrophytes only contribute to the carbon flow to higher trophic levels when they have decayed; and (2) that epiphytic algae is the major source of carbon for macroinvertebrates, and thus fish, with only minor contributions from phytoplankton or terrestrial sources. Epiphytic diatoms were a major component of the stomach contents of the gastropod snail Potamopyrgus antipodarum, and of chironomids. Animal remains were also common in the diet of some chironomids, while amorphous organic matter predominated in the stomachs of oligochaetes. A variety of epiphytic algal taxa was found in trichopteran larvae. Feeding rate of P. antipodarum measured with radioactive tracers increased by 10× on decayed macrophytes (Elodea) compared with live material, while feeding rates on characean algae increased by a factor of 3 when decayed material was presented. However, assimilation rates were less than 20% on decayed material compared with 48–52% on live material. Potential carbon sources were easily distinguished based on their ¹³C values, although isotopic ratios showed significant variation among sites. Epiphytic algae showed less variation among sites than macrophytes and were depleted by 4–5 compared with macrophytes. Detrital material, organic matter in the sediments and plankton were significantly depleted in ¹³C relative to macrophytes and slightly depleted relative to epiphytic algae. Most macroinvertebrate taxa showed a similar pattern among sites to macrophytes and epiphytic algae. P. antipodarum and chironomids were slightly enriched compared with epiphytic algae. Ratios for the common bully (Gobiomorphus cotidianus) were generally consistent with a diet dominated by chironomids, while there was some evidence for terrestrial inputs for koaro (Galaxias brevipinnis) and juvenile brown trout. Epiphytic algae appear to underpin much of the production in the littoral zone of this oligotrophic lake, with trichopteran and chironomid larvae mediating carbon flows from algae to fish. Macrophytes do not make a major contribution directly to carbon flow to higher trophic levels even when decayed. The lack of a direct link between macrophytes and higher trophic levels is due to the faunal composition, including a lack of large herbivores.     

Field evidence of trait-mediated indirect interactions in a rocky intertidal food web

Studies on the implications of food web interactions to community structure have often focused on density-mediated interactions between predators and their prey. This approach emphasizes the importance of predator regulation of prey density via consumption (i.e. lethal effects), which, in turn, leads to cascading effects on the prey's resources. A more recent and contrasting view emphasizes the importance of non-lethal predator effects on prey traits (e.g. behaviour, morphology), or trait-mediated interactions. On rocky intertidal shores in New England, green crab ( Carcinus maenas ) predation is thought to be important to patterns of algal abundance and diversity by regulating the density of herbivorous snails ( Littorina littorea ). We found, however, that risk cues from green crabs can dramatically suppress snail grazing, with large effects on fucoid algal communities. Our results suggest that predator-induced changes in prey behaviour may be an important and under-appreciated component of food web interactions and community dynamics on rocky intertidal shores.     

Direct and indirect responses of a freshwater food web to a potent synthetic oestrogen

Endocrine-disrupting chemicals (EDCs) in municipal effluents directly affect the sexual development and reproductive success of fishes, but indirect effects on invertebrate prey or fish predators through reduced predation or prey availability, respectively, are unknown. At the Experimental Lakes Area in northwestern Ontario, Canada, a long-term, whole-lake experiment was conducted using a before-after-control-impact design to determine both direct and indirect effects of the synthetic oestrogen used in the birth control pill, 17α-ethynyloestradiol (EE2). Algal, microbial, zooplankton and benthic invertebrate communities showed no declines in abundance during three summers of EE2 additions (5–6 ng l⁻¹), indicating no direct toxic effects. Recruitment of fathead minnow (Pimephales promelas) failed, leading to a near-extirpation of this species both 2 years during (young-of-year, YOY) and 2 years following (adults and YOY) EE2 additions. Body condition of male lake trout (Salvelinus namaycush) and male and female white sucker (Catostomus commersonii) declined before changes in prey abundance, suggesting direct effects of EE2 on this endpoint. Evidence of indirect effects of EE2 was also observed. Increases in zooplankton, Chaoborus, and emerging insects were observed after 2 or 3 years of EE2 additions, strongly suggesting indirect effects mediated through the reduced abundance of several small-bodied fishes. Biomass of top predator lake trout declined by 23–42% during and after EE2 additions, most probably an indirect effect from the loss of its prey species, the fathead minnow and slimy sculpin (Cottus cognatus). Our results demonstrate that small-scale studies focusing solely on direct effects are likely to underestimate the true environmental impacts of oestrogens in municipal wastewaters and provide further evidence of the value of whole-ecosystem experiments for understanding indirect effects of EDCs and other aquatic stressors.     

Direct and indirect food web regulation of microbial decomposers in headwater streams

The direct and indirect regulation of primary productivity has been well established in autotrophic‐based ecosystems; however, less is known about the processes affecting decomposers in detrital‐based ecosystems. Because, small headwater, woodland streams are a dominate feature in most ecosystems and are tightly linked to terrestrial detritus, understanding decomposer‐mediated functions in these systems is critical for understanding carbon processes across the landscape. In this light, we conducted a microcosm and mesocosm experiment to test the direct and indirect food web effects on decomposers in small stream ecosystems. The results from the microcosm experiment supported an existing literature, demonstrating that nutrients directly stimulate decomposers and that microbivores directly reduce decomposers. Based on well‐founded food web theory in autotrophic systems, we predicted that fishes from different trophic‐functional guilds would indirectly stimulate decomposers by enhancing dissolved nutrients and by reducing microbivore densities. Our mesocosm experiment partially supported these predictions. Specifically, we found that fishes that consumed mostly terrestrial foods increased decomposers from the bottom–up by enhancing allochthonous nutrient loading into the stream ecosystems. Contrary to our predictions, however, predatory fishes that consume microbivores did not increase decomposers from the top–down. Rather, in streams with the predatory fish species, microbivores increased (rather than decreased) on leaf litter. This may have resulted from an experimental artifact associated with refuge provided by leaf packs. In conclusion, our data demonstrate that decomposers are regulated by similar direct and indirect processes important in autotrophic‐based ecosystems. This provides further evidence that food web processes can regulate leaf decomposition and flux of detrital carbon through ecosystems.     

Long‐term variation in the littoral food web of an acidified mountain lake

Evidence of chemical recovery from acidification in European freshwaters has emerged in recent years, with many previously damaged systems responding to decades of reduced acidifying emissions. Biological recovery, however, has often lagged behind, and this has been ascribed to several possible mechanisms, including inertia in the food web. We examined two decades of change in hindcasted food webs for Lochnagar, a Scottish mountain lake, to make inferences about the potential dynamical stability of the system and to assess the prospects for future biological recovery. Although community composition tracked temporal changes in acidity, this was neither sustained nor directional, and mainly manifested as shifts in relative abundances rather than the establishment of more acid‐sensitive species. The food web was highly interconnected and reticulate, especially in years when species richness was low, and subsidized by external inputs of detritus. Among the primary consumers, generalist herbivore–detritivores maintained feeding links with the scant algal resources, which appeared insufficient to support viable populations of specialist grazers. Together, these characteristics, which are shared with many other acidified freshwaters, are likely to make the community dynamically stable and resistant to invasions of potential new colonists, thereby slowing the pace of future biological recovery.     

Multiple predator effects in an intertidal food web

1. We examined the effects of multiple predators from an intertidal boulder food web to test whether and how three different predator species affected the survival of a small amphipod species. 2. Predators were chosen because they differ in their foraging mode, two feeding at the bottom and in benthic refuges (nemertean and shrimp) and one in the water-column (juveniles of a fish). 3. Mortality of amphipods was not affected by nemerteans, but was high in the presence of shrimp or fish. Highest mortalities were observed in predator-combinations that contained both shrimp and fish. Amphipods responded to shrimp by escaping into the water column, while they avoided fish by remaining in the refuge. We conclude that predator-specific defence causes conflicts for prey when both shrimp and fish are present. 4. Comparing observed effects of multiple predators with expected effects revealed risk enhancement for the shrimp + fish combination. A comparison of different predictive models revealed that the multiplicative model was most appropriate, although additive models may work well under certain conditions. 5. Based on known consumption-ranges of the predators used, we conclude that nemerteans were saturated with prey while fish were far from their saturation point. A predator's functional response curve (prey consumption in relation to prey abundance) determines its impact on prey populations. This knowledge appears essential in order to predict whether prey organisms face risk enhancement, risk reduction or additive effects of multiple predators.     

Cascading effects of predatory fish exclusion on the detritus-based food web of a lake littoral zone (Lake Vico, central Italy)

An exclosure experiment was carried out in the reed-dominated littoral zone of a volcanic lake (Lake Vico, central Italy) to test whether the impact of predatory fish on benthic invertebrates cascades on fungal colonisation and breakdown of leaf detritus. The abundance, biomass, and Shannon diversity index of the invertebrate assemblage colonising Phragmites australis leaf packs placed inside: (1) full-exclosure cages, (2) cages allowing access only to small-sized fish predators, and (3) cageless controls, were monitored over a 45-day period together with the mass loss and associated fungal biomass of leaf packs. The species composition of the fungal assemblage was further assessed at the end of the manipulation. In general, invertebrate predators did not show any significant response to fish exclusion, either on a trophic guild or on a single taxon level. In contrast, the exclusion of large predatory fish induced a diverse spectrum of changes in the abundance and population size-structure of dominant detritivore taxa, ultimately increasing the biomass and Shannon diversity index of the whole detritivorous guild. These changes corresponded with significant variations in leaf detritus decay rates as well as in the biomass and assemblage structure of associated fungal colonisers. Our experimental findings provide evidence that in Lake Vico effects of fish predators on invertebrate detritivores influence the fungal conditioning and breakdown of the detrital substrate. We conclude that in lacustrine littoral zones predator-driven constraints may structure lower trophic levels of detritus-based food webs and affect the decomposition of leaf detritus originated from the riparian vegetation.     

Global change effects on a mechanistic decomposer food web model

Global change may affect the structure and functioning of decomposer food webs through qualitative changes in freshly fallen litter. We analyzed the predicted effects of a changing environment on a dynamic model of a donor‐controlled natural decomposer ecosystem near Wekerom, the Netherlands. This system consists of fungi, bacteria, fungivores, bacterivores and omnivores feeding on microbiota and litter as well. The model concentrates on carbon and nitrogen flows through the trophic niches that define this decomposer system, and is designed to predict litter masses and abundances of soil biota. For modeling purposes, the quality of freshly fallen leaf litter is defined in terms of nitrogenous and non‐nitrogenous components, of which refractory and labile forms are present. The environmental impacts of elevated CO₂, enhanced UV‐B and eutrophication, each with their own influence on leaf litter quality, are studied. The model predicts steady‐state dynamics exclusively, for all three scenarios. Environmental changes impact most demonstratively on the highest trophic niches, and affect microbiotic abundances and litter decomposition rates to a lesser extent. We conclude that the absence of trophic cascade effects may be attributed to weak trophic links, and that non‐equilibrium dynamics occurring in the system are generally because of encounter rates based on fractional substrate densities in the litter. We set out a number of experimentally testable hypotheses that may improve understanding of ecosystem dynamics.     

Linearity in the aggregate effects of multiple predators in a food web

Theory in community ecology often assumes that predator species have similar indirect effects and thus can be treated mathematically as a single functional unit (e.g. guild or trophic level). This assumption is questionable biologically because predator species typically differ in their effects, creating the potential for nonlinearities when they coexist. We evaluated the nature of indirect effects caused by three species of hunting spider predators, singly and in multiple species combinations, on grass and herb plants in experimental old-field food webs. Despite the potential for nonlinearity, indirect effects in different multiple predator combinations consistently did not differ significantly from the respective means of the single species effects. Thus, for this experimental system, the whole was simply the average of the parts. Consequently, models which abstract predator species as single trophic levels would successfully predict indirect effects in this system regardless of the composition of the predator fauna.     

Food web structure and the strength of transient indirect effects

The relative importance of direct and indirect effects in ecological communities remains unresolved. Indirect effects may diminish as they propagate through highly reticulate food webs. We tested this hypothesis by assembling replicate food webs of different complexity in laboratory microcosms, and comparing the transmission of indirect effects through these webs. By providing the top predator ( Didinium ) with either one ( Paramecium ) or two ( Paramecium and Colpidium ) species of protists as prey, we created linear or reticulate food webs where we could examine the transient response of predators to an indirect effect. Addition of Chlamydomonas , a small alga consumed by Paramecium , but not by Colpidium , perturbed the system and generated an indirect effect on Didinium . We expected the proportional response of Didinium to Chlamydomonas addition would be smaller in the reticulate web containing alternative, unperturbed prey ( Colpidium ). We measured predator response as predator yield, the maximum number of predators produced prior to overexploitation of prey and subsequent predator decline. The ratio of yield in perturbed bottles to yield in unperturbed bottles measures the proportional response of Didinium to Chlamydomonas addition. We expected this ratio to be smaller with Colpidium present. Contrary to expectations, alternative prey enhanced rather than diminished predator response to the perturbation. This resulted from competition between the prey species, a factor ignored in some simple verbal arguments. Food web complexity may have unanticipated consequences for the strength of indirect effects.     

Predicting the effects of temperature on food web connectance

Few models concern how environmental variables such as temperature affect community structure. Here, we develop a model of how temperature affects food web connectance, a powerful driver of population dynamics and community structure. We use the Arrhenius equation to add temperature dependence of foraging traits to an existing model of food web structure. The model predicts potentially large temperature effects on connectance. Temperature-sensitive food webs exhibit slopes of up to 0.01 units of connectance per 1°C change in temperature. This corresponds to changes in diet breadth of one resource item per 2°C (assuming a food web containing 50 species). Less sensitive food webs exhibit slopes down to 0.0005, which corresponds to about one resource item per 40°C. Relative sizes of the activation energies of attack rate and handling time determine whether warming increases or decreases connectance. Differences in temperature sensitivity are explained by differences between empirical food webs in the body size distributions of organisms. We conclude that models of temperature effects on community structure and dynamics urgently require considerable development, and also more and better empirical data to parameterize and test them.     

Chaotic dynamics of a food web in a chemostat

We analyze a mathematical model of a simple food web consisting of one predator and two prey populations in a chemostat. Monod's model is employed for the dependence of the specific growth rates of the two prey populations on the concentration of the rate-limiting substrate and a generalization of Monod's model for the dependence of the specific growth rate of the predator on the concentrations of the prey populations. We use numerical bifurcation techniques to determine the effect of the operating conditions of the chemostat on the dynamics of the system and construct its operating diagram. Chaotic behavior resulting from successive period doublings is observed. Multistability phenomena of coexistence of steady and periodic states at the same operating conditions are also found.     

Successful invasion of a food web in a chemostat

A food web in a chemostat is considered in which an arbitrary number of competitor populations compete for a single, essential, nonreproducing, growth-limiting substrate, and an arbitrary number of predator populations prey on some or all of the competitor populations. Although any number of predator populations may prey on the same competitor population, each predator population preys on only one competitor population. The dynamics of substrate uptake is modeled by Lotka-Volterra or Michaelis-Menten (Holling type I or II), but the dynamics of competitor uptake is restricted to Lotka-Volterra. Based on certain parameters, the model predicts the asymptotic survival or extinction of each of the different populations and suggests how competitor and/or predator populations could successfully invade the chemostat with or without causing a diverse ecosystem to crash. Similarly, it suggests how the elimination of certain populations could result in a more diverse or less diverse system.     

Reciprocal diversification in a complex plant-herbivore-parasitoid food web

Background  

Plants, plant-feeding insects, and insect parasitoids form some of the most complex and species-rich food webs. According to the classic escape-and-radiate (EAR) hypothesis, these hyperdiverse communities result from coevolutionary arms races consisting of successive cycles of enemy escape, radiation, and colonization by new enemy lineages. It has also been suggested that "enemy-free space" provided by novel host plants could promote host shifts by herbivores, and that parasitoids could similarly drive diversification of gall form in insects that induce galls on plants. Because these central coevolutionary hypotheses have never been tested in a phylogenetic framework, we combined phylogenetic information on willow-galling sawflies with data on their host plants, gall types, and enemy communities.     

Community convergence in a simple microbial food web

Previous studies of communities implicate many potential mechanisms that can create alternate stable states. These include density-dependent foraging behavior, size refuges reached by early colonists, environmental feedback following disturbance, and different initial densities of intraguild predators. Previous work shows that alternate states of varying stability can occur in food webs containing the intraguild predators Blepharisma americanum and Tetrahymena vorax. Differences in colonization history could create the alternate states, consisting of dominance by either Blepharisma or Tetrahymena, but it was unclear whether results depended on effects of initial density or only on changes in the resource base. We manipulated initial densities of both species to determine if density effects alone could create alternate stable states. Convergence of these communities over time indicated that differences in initial density did not create alternate stable states. By default, other factors influenced by colonization history, such as resource availability, may produce alternate states. Models of alternate stable-state phenomena should incorporate differences in resource availability in addition to direct competitive and predatory interactions to provide a more complete depiction of the causes of differences in community composition in otherwise similar habitats.     

Direct and indirect effects of predators on the dominant invertebrates of two freshwater littoral communities

Summary Two congeneric damselfly species, Enallagma traviatum and E. aspersum, dominate the littoral macroinvertebrates of Bays Mountain Lake and of the adjacent fish-free Ecology Pond, respectively (northeastern Tennessee, USA). Extending previous experimental studies, we test seven hypotheses concerning the role of fish (bluegill sunfish, Lepomis macrochirus) and larvaldragonfly (Anax junius) predation, competitive effects on damselflies, and the interaction between competition and predation, in determining invertebrate dominance in these communities. Three types of experiments were conducted: an enclosure experiment within Ecology Pond, an outdoor replicated tub experiment, and a laboratory behavior experiment. The in-situ enclosure experiment showed that E. traviatum larvae were more susceptible to Anax predation than were E. aspersum larvae; a tendency toward greater vulnerability to fish of E. aspersum compared with E. traviatum was not statistically significant. The outdoor tub experiment confirmed both of these trends with statistically significant results. In the tubs, both predators inhibited feeding of both zygopterans (as indicated by reduced fecal mass), particularly for E. aspersum in the presence of fish. This effect appears to have been primarily indirect, mediated through exploitation of the zooplankton. We also detected competitive effects of E. traviatum on E. aspersum: E. traviatum reduced the emergence and increased the exposure above the substrate of E. aspersum. In the absence of predators, E. traviatum inhibited feeding of E. aspersum via interference. In the laboratory behavior experiment, predators inhibited crawling by E. aspersum. E. aspersum was more exposed than was E. traviatum; it swam and crawled more than did E. traviatum, considerably increasing these movements at night. Over all, E. traviatum consistently appeared to be the more cryptic of the two species, and E. aspersum appeared to be much more active. Our results suggest an explanation for the clear difference in structure between communities like Bays Mountain Lake and Ecology Pond: predaceous fish eliminate large invertebrate predators and shift the community toward cryptic forms at relatively low densities, reflecting the effects of both predation and exploitation competition. In the absence of fish, large invertebrate predators are less able to deplete littoral invertebrates but may favor the more active forms, perhaps because these are better able to avoid invertebrate predators.     

Integration of an invasive consumer into an estuarine food web: direct and indirect effects of the New Zealand mud snail

Introduced species interact both directly and indirectly with native species. We examine interactions between the introduced New Zealand mud snail (Potamopyrgus antipodarum) and native estuarine invertebrates and predators through experiments and field studies. A widely held management concern is that when P. antipodarum, which has low nutritional value, becomes abundant, it replaces nutritious prey in fish diets. We tested two key components of this view: (1) that fish consume, but get little direct nutritional value from P. antipodarum; and (2) that P. antipodarum has an indirect negative effect on fish by reducing the energy derived from native prey. We also examined predation by the native signal crayfish, Pacifastacus leniusculus. Laboratory feeding trials showed that both crayfish and fish consume P. antipodarum, a direct effect. Crayfish consumed and successfully digested higher numbers of snails than did fish [Pacific staghorn sculpin (Leptocottus armatus), three spine stickleback (Gasterosteus aculeatus), and juvenile starry flounder (Platicthys stellatus)]. P. antipodarum occurred at low frequencies in the stomachs of wild-caught fish. More interesting were the indirect effects of this invader, which ran counter to predictions. P. antipodarum presence was associated with no change or an increase in the amount of energy derived from native prey by predators. The presence of P. antipodarum also led to increased consumption of and preference for the native amphipod Americorophium salmonis over the native isopod Gnorimosphaeroma insulare. This is an example of short-term, asymmetric, apparent competition, in which the presence of one prey species (snails) increases predation on another prey species (the amphipod).