Barbara L. Peckarsky

REVISITING THE CLASSICS: CONSIDERING NONCONSUMPTIVE EFFECTS IN TEXTBOOK EXAMPLES OF PREDATOR-PREY INTERACTIONS

Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.

Prey Exchange Rates and the Impact of Predators on Prey Populations in Streams

We present four lines of evidence that the magnitude of prey exchange (=immigration/emigration) among substrate patches has an overwhelming influence on the perceived effects of predators on prey populations. (1) An extensive review of the literature on predation effects in benthic and littoral freshwater revealed a significant relationship between prey exchange rate and observed predator impact. In streams, studies showing significant predator effects used cages with smaller mesh sizes than studies showing nonsignificant effects. Similarly, there was a highly significant correlation between cage mesh size and the magnitude of predator impact on common prey. Large—scale stream studies indicated that prey drift and colonization rate were inversely related to predator impact on benthic prey. (2) These patterns were confirmed by field experiments and observations where mesh size was directly manipulated or where exchange rates varied among taxa. In Colorado streams we saw greater predator impacts on Baetis prey when immigration/emigration was restricted vs. when the mesh size of the cage was relatively large. Similarly, the effects of trout in California stream pools were greater when prey turnover rates were low. (3) A re—analysis of Peckarskys (1985) data shows an inverse relationship between predator impact and prey mobility within a field experiment. (4) Finally, a model that incorporates both predation and exchange of prey indicates that we ought to expect a lower magnitude of predator effects when exchange rates are high. These results suggest that some discrepancies in past studies may be explained by differences in the exchange rates of prey, and that differences in predator effects across different systems or habitats may be related to variation in the rates of prey dispersal and colonization.

Non-visual communication in freshwater benthos: an overview

This overview of non-visual communication in freshwater benthic animals emphasizes recent studies of the effect of chemical and mechanical signals on predator-prey interactions of benthic macroinvertebrates and amphibians. Prey species use chemical signals to modify their morphological development, life history strategy, feeding, and predator avoidance behavior. The advantages of chemical signals are that they can be used in dark or turbid environments by animals that do not have image-forming eyes. Chemical signals are more persistent than mechanical signals, and they allow species-level identification of predator species. In streams, prey species may use mechanical signals (hydrodynamic pressure waves or sound) to avoid predators approaching from downstream (a situation characteristic of streams and in which chemical signals are unreliable) and to initiate escape responses. Predators often depend on chemical signals to stimulate or inhibit feeding, and they use species-specific mechanical signals to locate or track prey or potential mates. The exact nature of non-visual signals depends on ecological constraints of both the sender and receiver. Responses to non-visual signals may be adapted to local predator conditions. Non-visual signals are effectively used over a wide range of temporal and spatial scales in all aquatic habitats. Organisms often adjust their responses as ontogenic development results in changing size, diet, and habitat.

LIFE HISTORIES AND THE STRENGTHS OF SPECIES INTERACTIONS: COMBINING MORTALITY, GROWTH, AND FECUNDITY EFFECTS

Interactive effects of one species on another may simultaneously influence mortality, growth, and fecundity. To quantify the strength of an interaction between two species, we must therefore use techniques that integrate these various responses into es- timates of overall effect. Demographic models of populations provide such a framework. Here we develop a demographic model describing the life history of a hemimetabolous insect to evaluate the relative importance of predator effects on mortality and growth of damselflies (Enallagma boreale) in fishless ponds and mayflies (Baetis bicaudatus) in trout streams. Previous experiments have shown that dragonfly predators in fishless ponds inflict direct mortality and cause reduced growth rates in Enallagma damselflies. Parameterization of the demographic model from these data show, however, that only the direct mortality effects of dragonflies should significantly influence damselfly population dynamics. This is because damselfly size at emergence does not influence adult female fecundity, so the effects of dragonflies on damselfly larval growth do not influence adult fecundity. Likewise, both trout and stonefly predators inflict mortality on larval Baetis mayflies and cause decreases in growth rates. However, our demographic analyses indicate that the growth effects of both predators should dominate the population-dynamic effects on Baetis. This is because size at emergence translates directly into adult fecundity in mayflies. We also present data suggesting that developmental responses to changes in environmental conditions (e.g., predator abundances, resource availabilities) differ between species depending on these same life history parameters. The biological significance of lethal vs. sublethal predator impacts must be evaluated in a demographic framework to identify whether alterations in growth rate, and the timing of and size at metamorphosis, significantly influence population dynamics. The demographic model used for any particular organism must be tailored to its life history, but the various impacts of interactions with other species can all be integrated into estimates of projected population growth that can then be readily compared among species with different life histories.

Fitness and community consequences of avoiding multiple predators

Abstract We investigated the fitness and community consequences of behavioural interactions with multiple predators in a four-trophic-level system. We conducted an experiment in oval flow-through artificial-stream tanks to examine the single and interactive sublethal effects of brook trout and stoneflies on the size at emergence of Baetis bicaudatus (Ephemeroptera: Baetidae), and the cascading trophic effects on algal biomass, the food resource of the mayflies. No predation was allowed in the experiment, so that all effects were mediated through predator modifications of prey behaviour. We reared trout stream Baetis larvae from just before egg development until emergence in tanks with four treatments: (1) water from a holding tank with two brook trout (trout odour), (2) no trout odour + eight stoneflies with glued mouthparts, (3) trout odour + stoneflies and (4) no trout odour or stoneflies. We ended the experiment after 3 weeks when ten male and ten female subimagos had emerged from each tank, measured the size of ten male and ten female mature nymphs (with black wing pads), and collected algal samples from rocks at six locations in each tank. To determine the mechanism responsible for sublethal and cascading effects on lower trophic levels we made day and night observations of mayfly behaviour for the first 6 days by counting mayflies drifting in the water column and visible on natural substrata in the artificial streams. Trout odour and stoneflies similarly reduced the size of male and female Baetis emerging from artificial streams, with non-additive effects of both predators. While smaller females are less fecund, a fitness cost of small male size has not been determined. The mechanism causing sublethal effects on Baetis differed between predators. While trout stream Baetis retained their nocturnal periodicity in all treatments, stoneflies increased drift dispersal of mayflies at night, and trout suppressed night-time feeding and drift of mayflies. Stoneflies had less effect on Baetis behaviour when fish odour was present. Thus, we attribute the non-additivity of effects of fish and stoneflies on mayfly growth to an interaction modification whereby trout odour reduced the impact of stoneflies on Baetis behaviour. Since stonefly activity was also reduced in the presence of fish odour, this modification may be attributed to the effect of fish odour on stonefly behaviour. Only stoneflies delayed Baetis emergence, suggesting that stoneflies had a greater sublethal effect on Baetis fitness than did trout. Delayed emergence may reduce Baetis fitness by increasing risks of predation and parasitism on larvae, and increasing competition for mates or oviposition sites among adults. Finally, algal biomass was higher in tanks with both predators than in the other three treatments. These data implicate a behavioural trophic cascade because predators were not allowed to consume prey. Therefore, differences in algal biomass were attributed to predator-induced changes in mayfly behaviour. Our study demonstrates the importance of considering multiple predators when measuring direct sublethal effects of predators on prey fitness and indirect effects on lower trophic levels. Identification of an interaction modification illustrates the value of obtaining detailed information on behavioural mechanisms as an aid to understanding the complex interactions occurring among components of ecological communities.

Elemental dynamics in streams

We discuss elemental dynamics in streams and seek to identify areas where there are critical gaps in our understanding. Both landscape-level processes (e.g., geology, land-use practices, vegetation) and heterogeneous in-stream processes influence the supply and availability of elements to the stream biota. Stream ecologists need to consider the relative availability of different compounds or groups of compounds to the biota rather than lumping all forms of an element into operationally-defined units such as dissolved organic nitrogen or carbon. The impact of short-term events like storms on the elemental dynamics in streams needs to be assessed and compared with other controls. The relative importance of longitudinal (upstream), lateral (riparian zone, flood-plains), and in-stream controls of supply and availability of elements needs to be compared in a variety of streams. Availability of essential elements is a key factor controlling rates of primary productivity and decomposition in streams. Whole system manipulations offer a valuable tool for understanding the interactions between elements and all components of the stream food web. We include an action plan of developments that would assist researchers in addressing some of the critical gaps we have identified in our understanding of elemental dynamics in streams.

Alternative Predator Avoidance Syndromes of Stream‐Dwelling Mayfly Larvae

Experiments were conducted to compare the patterns, mechanisms, and costs of predator avoidance behavior among larvae of five species of mayflies that co-occur with the predatory stoneflies, Megarcys signata and Kogotus modestus in western Colorado streams. Mayfly drift dispersal behavior, use of high vs. low food (periphyton or detritus) patches, microhabitat use, positioning, and activity periodicity were observed in the pres- ence and absence of predators in circular flow-through chambers using natural stream water. Also, distances from predators at which prey initiated escape responses were compared among prey and predator species. Costs of predator avoidance behavior were assessed by measuring short-term (24 h) feeding rates of mayflies in the presence or absence of predatory stoneflies whose mouthparts were immobilized (glued) to prevent feeding. The intensity and associated costs of predator avoidance behavior of mayfly species were consistent with their relative rates of predation by stoneflies. Megarcys consumes overwintering generation Baetis bicaudatus > Epeorus longimanus > Cinygmula = Ephem- erella; Kogotus consumes summer generation Baetis > Epeorus deceptivus = Cinygmula; Megarcys eats more mayflies than Kogotus. While Megarcys induced drift by Baetis, Epeo- rus, and Cinygmula, this disruptive predator avoidance behavior only reduced food intake by Baetis and Epeorus. The morphologically defended mayfly species, Ephemerella, neither showed escape behavior from Megarcys, nor any cost of its antipredatory posturing behavior. Only Baetis responded by drifting from Kogotus. No mayfly species shifted microhabitats or spent less time on high-food patches in the presence of foraging stoneflies. However, predators enhanced the nocturnal periodicity of Baetis drift, which was negligible in the absence of stoneflies as long as food was abundant. Lack of food also caused some mi- crohabitat and periodicity shifts and increased the magnitude of both day and night drift of Baetis. Thus, Baetis took more risks of predation by visual, drift-feeding fish not only in the presence of predatory stoneflies, but also when food was low or they were hungry. All other mayflies were generally nocturnal in their use of rock surfaces, as long as food was abundant. Finally, the distances at which different mayfly species initiated acute escape responses were also consistent with relative rates of predation. This study demonstrates alternative predator avoidance syndromes by mayfly species ranging from an initial investment in constitutive morphological defenses (e.g., Ephem- erella) to induced, energetically costly predator avoidance behaviors (e.g., Baetis). Although the costs of Ephemerellas constitutive defense are unknown, experiments show that prey dispersal is the mechanism underlying fecundity costs of induced responses by Baetis to predators, rather than microhabitat shifts to less favorable resources or temporal changes in foraging activity. A conceptual model suggests that contrasting resource acquisition modes may account for the evolution and maintenance of alternative predator avoidance syndromes along a continuum from Baetis (high mobility) to heptageniids (intermediate mobility) to Ephemerella (low mobility). Prey dispersal (swimming) to avoid capture results in reduction of otherwise high fecundity by Baetis, which trades off morphological defense for enhanced ability to acquire resources. Thus, improved foraging efficiency is the selection pressure maintaining the highly mobile life style in Baetis, which increases resource ac- quisition and fecundity, offsetting the high mortality costs associated with this behavior.

VARIATION IN MAYFLY SIZE AT METAMORPHOSIS AS A DEVELOPMENTAL RESPONSE TO RISK OF PREDATION

Animals with complex life cycles often show large variation in the size and timing of metamorphosis in response to environmental variability. If fecundity increases with body size and large individuals are more vulnerable to predation, then organisms may not be able to optimize simultaneously size and timing of metamorphosis. The goals of this study were to measure and explain large-scale spatial and temporal patterns of phe- notypic variation in size at metamorphosis of the mayfly, Baetis bicaudatus (Baetidae), from habitats with variable levels of predation risk. Within a single high-elevation watershed in western Colorado, USA, from 1994 to 1996 we measured dry masses of mature larvae of the overwintering and summer generations of Baetis at 28 site-years in streams with and without predatory fish (trout). We also estimated larval growth rates and development times at 16 site-years. Patterns of spatial variation in mayfly size could not be explained by resource (algae) standing stock, competitor densities, or physical-chemical variables. However, size at metamorphosis of males and females of summer generation Baetis was smaller in fish streams than in fishless streams and decreased as densities of predatory stoneflies increased. Furthermore, overwintering individuals matured at larger sizes than summer generation Baetis, and the size of emerging Baetis declined over the summer, but predominantly in trout streams. Theoretical consideration of the effect of predation risk on size and timing of metamorphosis accurately predicted the observed temporal variation in size and timing of mayflies at emergence in fish and fishless streams. Baetis populations had similar growth rates but followed different developmental trajectories in high and low risk environments. In risky environments larval development was accelerated, resulting in metamorphosis of younger and smaller individuals, minimizing exposure of larvae to risk of mortality from trout predation, but at the cost of future reproduction. In safe environ- ments, larvae extended their development, resulting in larger, more fecund adults. Thus, we propose that large-scale patterns of variation in size and timing of metamorphosis represent adaptive phenotypic plasticity, whereby mayflies respond to variation in risk of predation, thereby maximizing their fitness in variable environments.

DO STONEFLY PREDATORS INFLUENCE BENTHIC DISTRIBUTIONS IN STREAMS

Experimental manipulations were conducted within the substrate of a Wisconsin stream and a Colorado stream to measure the effect of stonefly predators on the distribution of benthic invertebrates. Screen cages containing free predators, predators restricted from foraging, or no pred- ators, allowed prey migration but no predator migration over 3-d periods. The presence of Acroneuria lycorias (Perlidae) in the Wisconsin stream significantly depressed the establishment of prey popu- lations within cage microhabitats. Mechanisms for reduction were consumption of prey by the stone- fly, and predator-avoidance by prey using contact and non-contact cues. The presence of Megarcys signata (Perlodidae) reduced prey colonization in the Colorado stream by the same mechanisms, but restricted predators produced less consistent effects. This result could be due to colonization of cages by prey that could not detect predators without contact. Pteronarcella badia (Pteronarcidae), a large stonefly detritivore that takes occasional prey, did not affect colonization of Colorado stream cages by prey. This differential response by prey to two morphologically similar, but functionally different, stonefly species suggests that predator avoidance was not purely tactile. Chemotactile and non-contact chemical cues are possible mechanisms by which prey differentiated these stoneflies. The presence of A. lycorias and M. signata in experimental cages significantly increased the attrition of mayfly prey, compared to that from cages with no stonefly or a restricted stonefly in each stream. This result suggests that predation and avoidance by prey of contact with foraging predators were responsible for the higher disappearance of mayflies from cages. Free P. badia had a similar effect, probably due to tactile avoidance of this large detritivorous stonefly by some prey in the Colorado stream.

FROM INDIVIDUALS TO ECOSYSTEM FUNCTION: TOWARD AN INTEGRATION OF EVOLUTIONARY AND ECOSYSTEM ECOLOGY

An important goal in ecology is developing general theory on how the species composition of ecosystems is related to ecosystem properties and functions. Progress on this front is limited partly because of the need to identify mechanisms controlling functions that are common to a wide range of ecosystem types. We propose that one general mechanism, rooted in the evolutionary ecology of all species, is adaptive foraging behavior in response to predation risk. To support our claim, we present two kinds of empirical evidence from plant-based and detritus-based food chains of terrestrial and aquatic ecosystems. The first kind comes from experiments that explicitly trace how adaptive foraging influences ecosystem properties and functions. The second kind comes from a synthesis of studies that individually examine complementary components of particular ecosystems that together provide an integrated perspective on the link between adaptive foraging and ecosystem function. We show that the indirect effects of predators on plant diversity, plant productivity, nutrient cycling, trophic transfer efficiencies, and energy flux caused by consumer foraging shifts in response to risk are qualitatively different from effects caused by reductions in prey density due to direct predation. We argue that a perspective of ecosystem function that considers effects of consumer behavior in response to predation risk will broaden our capacity to explain the range of outcomes and contingencies in trophic control of ecosystems. This perspective also provides an operational way to integrate evolutionary and ecosystem ecology, which is an important challenge in ecology.