The community effects of phenotypic and genetic variation within a predator population

Natural populations are heterogeneous mixtures of individuals differing in physiology, morphology, and behavior. Despite the ubiquity of phenotypic variation within natural populations, its effects on the dynamics of ecological communities are not well understood. Here, we use a quantitative genetics framework to examine how phenotypic variation in a predator affects the outcome of apparent competition between its two prey species. Classical apparent competition theory predicts that prey have reciprocally negative effects on each other. The addition of phenotypic trait variation in predation can marginalize these negative effects, mediate coexistence, or generate positive indirect effects between the prey species. Long-term coexistence or facilitation, however, can be preceded by long transients of extinction risk whenever the heritability of phenotypic variation is low. Greater heritability can circumvent these ecological transients but also can generate oscillatory and chaotic dynamics. These dramatic changes in ecological outcomes, in the sign of indirect effects, and in stability suggest that studies which ignore intraspecific trait variation may reach fundamentally incorrect conclusions regarding ecological dynamics.     

Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species

Chemotactile cues unintentionally left by animals can play a major role in predator–prey interactions. Specialized predators can use them to find their prey, while prey individuals can assess predation risk. However, little is known to date about the importance of chemotactile cues for generalist predators such as ants. Here, we investigated the response of a generalized predatory ant, Formica polyctena, to cues of two taxonomically distinct prey: a spider (Pisaura mirabilis) and a cricket (Nemobius sylvestris). In analogy, we studied whether crickets and spiders showed antipredator behavior in response to ant cues. When confronted with cues of the two prey species, Formica polyctena workers showed increased residence time and reduced movement speed, which suggests success-motivated searching behavior and thus increased foraging effort. The ants’ response did not differ between cues of the two prey species, coinciding with similar aggression and consumption rates of dead prey. However, the cuticular hydrocarbons, which likely resemble part of the potential cues, differed strongly between the species, with only few methyl-branched alkanes in common. This suggests that ants respond to multiple compounds left by other organisms with prey-search behavior. The two prey species, in turn, showed no detectable antipredator behavior in response to ant cues. Our study shows that ants can detect and respond to chemotactile cues of taxonomically and ecologically distinct prey species, probably to raise their foraging success. Using such chemotactile cues for prey detection may drastically increase their foraging efficiency and thus contribute to the high ecological success of ants.     

Functional responses: a question of alternative prey and predator density

Throughout the study of ecology, there has been a growing realization that indirect effects among species cause complexity in food webs. Understanding and predicting the behavior of ecosystems consequently depends on our ability to identify indirect effects and their mechanisms. The present study experimentally investigates indirect interactions arising between two prey species that share a common predator. In a natural field experiment, we introduced different densities of mealworms (Tenebrio molitor), an alternative prey, to a previously studied predator-prey system in which paper wasps (Polistes dominulus) preyed on shield beetle larvae (Cassida rubiginosa). We tested if alternative prey affects predation on the first prey (i.e., the predator-dependent functional response of paper wasps) by modifying either interference among predators or the effective number of predators foraging on shield beetles. Presence of mealworms significantly reduced the effective number of predators, whereas predator interference was not affected. In this way, the experimentally introduced alternative prey altered the wasps' functional response and thereby indirectly influenced C. rubiginosa density. In all prey-density combinations offered, paper wasps constantly preferred T. molitor. This led to an asymmetrical, indirect interaction between both prey species: an increase in mealworm density significantly relaxed predation on C. rubiginosa, whereas an increase in C. rubiginosa density intensified predation on mealworms. Such asymmetrical outcomes of a fixed food preference can significantly affect the population dynamics of the species involved. In spite of the repeated finding of a Type III functional response in this system, our experiment did not reveal switching behavior in paper wasps. The variety of mechanisms underlying direct and indirect interactions within our study system exemplifies the importance of incorporating alternative prey when investigating the impact of a generalist predator on a focal prey population under realistic field conditions.     

Harvest policies and nonmarket valuation in a predator — prey system

Although prey may not have commercial value, their economic value can be ascertained in a predator-prey model if the predator has a harvest value. The economic optimal (recovery) path of the predator and prey are carefully described when growth is quadratic in the predator (prey) and linear in prey (predator). Parameter values, in part, resembling Pacific halibut are used to provide numerical illustrations.     

Individual- and population-level responses of a keystone predator to geographic variation in prey

Investigating how food supply regulates the behavior and population structure of predators remains a central focus of population and community ecology. These responses will determine the strength of bottom-up processes through the food web, which can potentially lead to coupled top-down regulation of local communities. However, characterizing the bottom-up effects of prey is difficult in the case of generalist predators and particularly with predators that have large dispersal scales, attributes that characterize most marine top predators. Here we use long-term data on mussel, barnacle, limpet, and other adult prey abundance and recruitment at sites spread over 970 km to investigate individual- and population-level responses of the keystone intertidal sunstar Heliaster helianthus on the coast of Chile. Our results show that this generalist predator responds to changes in the supply of an apparently preferred prey, the competitively dominant mussel Perumytilus purpuratus. Individual-level parameters (diet composition, per capita prey consumption, predator size) positively responded to increased mussel abundance and recruitment, whereas population-level parameters (density, biomass, size structure) did not respond to bottom-up prey variation among sites separated by a few kilometers. No other intertidal prey elicited positive individual predator responses in this species, even though a large number of other prey species was always included in the diet. Moreover, examining predator-prey correlations at approximately 80, 160, and 200 km did not change this pattern, suggesting that positive prey feedback could occur over even larger spatial scales or as a geographically unstructured process. Thus individual-level responses were not transferred to population changes over the range of spatial scales examined here, highlighting the need to examine community regulation processes over multiple spatial scales.     

The hearing of an avian predator and its avian prey

Summary Auditory tuning curves of a small songbird, the great tit (Parus major), and of its principal avian predator, the European sparrowhawk (Accipiter nisus), were determined by an operant positive reinforcement conditioning procedure, using the method of constant stimuli. Thresholds were measured by the criterion of a 50% correct response and a d of 1.5 for intra- and interspecific comparison, respectively. The best frequency of both species was 2 kHz, the hawk being 6.5 dB SPL more sensitive than the tit. Although the high-frequency cutoff was very similar in both species, at 8 kHz the great tit was about 30 dB more sensitive than the sparrowhawk. The hearing abilities of the prey and its predator are discussed with reference to the acoustic alarm communication of great tits confronted with sparrowhawks. Two alarm calls lie in the frequency range of the best hearing of both the hawk and the tits: the mobbing call and a call given in response to a nearby hawk when fleeing from it. In contrast, the seeet call, an alarm call given mainly in response to distant flying sparrowhawks, can only be heard well by the tit. The implications of these results for hypotheses concerning the evolution of alarm calls in small songbirds are discussed.     

Overestimations of food abundance: predator responses to prey aggregation

Understanding and predicting the consequences of trophic interactions for community processes requires knowledge of the role of food availability, which is often wrongly conflated with prey abundance. For prey animals in groups, this is not fully understood. Previous work has shown that oystercatchers more frequently attack solitary rather than aggregated limpets and are more successful in predation attempts on singletons. It has also been demonstrated that an attack on one limpet in a group alerts the entire group, all of which then clamp down and become unavailable. I show that Eurasian Oystercatchers (Haematopus ostralegus L.) attack only one limpet in a group and then move on to attack another individual limpet, and I also demonstrate that the distance they move is greater than the distance at which groups of limpets have been known to detect attacks. Thus in the oystercatcher-limpet predator-prey system on rocky shores, groups of limpets are actually one prey item independently of the number of limpets in the group. This has implications for assessment of food supply for avian predators on rocky shores, with consequences for our understanding of previously documented trophic cascades.     

A review of predator diet effects on prey defensive responses

Numerous studies have examined how predator diets influence prey responses to predation risk, but the role predator diet plays in modulating prey responses remains equivocal. We reviewed 405 predator–prey studies in 109 published articles that investigated changes in prey responses when predators consumed different prey items. In 54 % of reviewed studies, prey responses were influenced by predator diet. The value of responding based on a predator’s recent diet increased when predators specialized more strongly on particular prey species, which may create patterns in diet cue use among prey depending upon whether they are preyed upon by generalist or specialist predators. Further, prey can alleviate costs or accrue greater benefits using diet cues as secondary sources of information to fine tune responses to predators and to learn novel risk cues from exotic predators or alarm cues from sympatric prey species. However, the ability to draw broad conclusions regarding use of predator diet cues by prey was limited by a lack of research identifying molecular structures of the chemicals that mediate these interactions. Conclusions are also limited by a narrow research focus. Seventy percent of reviewed studies were performed in freshwater systems, with a limited range of model predator–prey systems, and 98 % of reviewed studies were performed in laboratory settings. Besides identifying the molecules prey use to detect predators, future studies should strive to manipulate different aspects of prey responses to predator diet across a broader range of predator–prey species, particularly in marine and terrestrial systems, and to expand studies into the field.     

Foraging tactics of an ambush predator: the effects of substrate attributes on prey availability and predator feeding success

The foraging sites selected by an ambush forager can strongly affect its feeding opportunities. Foraging cane toads (Rhinella marina) typically select open areas, often under artificial lights that attract insects. We conducted experimental trials in the field, using rubber mats placed under lights, to explore the influence of substrate color and rugosity on prey availability (numbers, sizes, and types of insects) and toad foraging success. A mat's color (black vs. white) and rugosity (smooth vs. rough) did not influence the numbers, sizes, or kinds of insects that were attracted to it, but toads actively preferred to feed on rugose white mats (50% of prey-capture events, vs. a null of 25%). White backgrounds provided better visual contrast of the (mostly dark) insects, and manipulations of prey color in the laboratory showed that contrast was critical in toad foraging success. Insects landing on rugose backgrounds were slower to leave, again increasing capture opportunities for toads. Thus, cane toads actively select backgrounds that maximize prey-capture opportunities, a bias driven by the ways that substrate attributes influence ease of prey detection and capture rather than by absolute prey densities.     

Experimental prey species preferences of Hexaplex trunculus (Gastropoda: Muricidae) and predator–prey interactions with the Black mussel Mytilus galloprovincialis (Bivalvia: Mytilidae)

Hexaplex trunculus is one of the most widespread Mediterranean species of muricid gastropod and lives on rocky, sandy-mud and mud substrata. Although common in the Adriatic Sea, relatively little is known about its ecology especially feeding behaviour. The aim of this study was to explore the aspects of the feeding behaviour of H. trunculus using Arca noae, Modiolus barbatus and Mytilus galloprovincialis as experimental prey. Prey species preference, predator size, prey size choice, feeding rates, handling times and mode and place of attack were analysed. Typically, only M. galloprovincialis was attacked: A. noae rarely at the byssal gape and M. barbatus never. Small (40 mm) H. trunculus could not easily attack large M. galloprovincialis (65 mm) and preferred small (20 mm) and medium (35 mm) sized prey. Conversely, medium (55 mm) and large (70 mm) H. trunculus fed randomly on M. galloprovincialis of all three sizes. The feeding strategy adopted by H. trunculus individuals varied with respect to size. A tendency to drill the prey shell was recorded for small predators, whereas marginal chipping was adopted more frequently by large individuals. On average small, medium and large H. trunculus consumed 2.4±1.6 (range 0–4), 1.2±1.6 (range 0–4) and 2.0±2.1 (range 0–6) M. galloprovincialis, respectively. There was a statistically significant difference in prey-handling time with respect to the method of access adopted, predator and prey sizes. The time required to access a M. galloprovincialis individual by marginal chipping was considerably less than that required for drilling. H. trunculus consumed an average of 0.60±0.80 g M. galloprovincialis tissue dry weight over a 5-week period, that is, ~40% of its own tissue body weight. This translates to an average-sized (55 mm shell height) H. trunculus consuming ~18 M. galloprovincialis of 50 mm shell length (minimum marketable size) per year. H. trunculus showed no preference to drill either the left or right valves of M. galloprovincialis but generally attacked the posterior shell margin.     

Distribution of marine predator hotspots explained by persistent areas of prey

Investigations of distributional and density patterns of marine predators often reveal areas where high abundances of one or many species overlap in space and time (‘biological hotspots’); however, mechanisms underlying hotspot formation are often unclear, leading to difficulties determining spatial and temporal boundaries of protected areas. On the northeast Newfoundland coast, I previously described annually persistent aggregations of a key forage fish species, capelin (Mallotus villosus): (1) two pre- and post-spawning staging areas in deep (>150 m) bathymetric channels, (2) a cluster of four persistently used demersal spawning sites (17–40 m), and (3) a coastal migratory route (<50 m). Through at-sea surveys repeated over 8 years (2000–2003, 2007, and 2009–2011), I show that the majority of predator hotspots identified were spatially associated with (i.e., within 10 km) these persistent capelin areas for breeding seabirds (common murre: 85.2 ± 4.6 %; northern gannet: 66.9 ± 6.6 %), overwintering seabirds (great and sooty shearwaters: 88.0 ± 6.9 %), and baleen whales (humpback, minke, and fin whales: 86.8 ± 8.6 %). Most predator hotspots were closer to the spawning (3.8–14.0 km) relative to the staging areas (13.1–27.6 km), especially for murres and shearwaters. Interspecific differences were attributed to variation in maximum dive depths and dietary preferences. Predators only aggregated within the spawning area, while capelin were spawning, suggesting that interannual variation in association with predator and capelin hotspots was attributed to variation in survey timing relative to capelin spawning. As these areas of persistent capelin are bound by static bathymetric and large-scale oceanographic features and can be delimited in time based on the capelin spawning period, they may be important candidate areas for protection.     

Role of predator switching in an eco-epidemiological model with disease in the prey

In the present paper we propose a modification of a basic eco-epidemiological model by incorporating predator switching among susceptible and infected prey population. A local and global study of the basic model is performed around the disease-free boundary equilibrium and the interior equilibrium to estimate important parameter thresholds that control disease eradication and species coexistence. Next we analyze the switching model from the same perspective in order to elucidate the role of switching on disease dynamics. Numerical simulations are carried out to justify analytical results.     

Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of prey?

Summary. The bolas spider, Mastophora hutchinsoni, attracts Lacinipolia renigera and Tetanolita mynesalis males by mimicking the female moth sex pheromones. However, as the prey species use completely different pheromone blends we conducted experiments to determine how this is accomplished by the predator. The periodicity of L. renigera mate-seeking activities occurs early in the scotophase, whereas male T. mynesalis are active late at night, corresponding with periods when these moths are captured by the spider. The pheromone blend of early-flying L. renigera interferes with attraction of late-flying T. mynesalis to its pheromone in a dose-dependent manner, suggesting the spider must always produce a single sub-optimal “compromise” blend for both species or that it adjusts its allomonal blend to optimize capture of the respective prey species at different times during the night. We delayed (L. renigera) or advanced (T. mynesalis) the periodicity of male activity through photoperiodic manipulation and found that the bolas spider attracted both prey species outside their normal activity windows. These results support the idea that bolas spiders produce components of both species at all times rather than producing the pheromone of each prey species at different times of the night. However, using coupled gas chromatography-electroantennography, we also demonstrated that the spider decreases its emission of the L. renigera pheromone over the course of the night. This modification should reduce the behavioral antagonism of the L. renigera pheromone on T. mynesalis males and increase the predator's success of attracting T. mynesalis during this prey's normal activity window late at night. Received 13 October 2001; accepted 28 December 2001.     

Counterintuitive effects of large-scale predator removal on a midlatitude rodent community

Historically, small mammals have been focal organisms for studying predator-prey dynamics, principally because of interest in explaining the drivers of the cyclical dynamics exhibited by northern vole, lemming, and hare populations. However, many small-mammal species occur at relatively low and fairly stable densities at temperate latitudes, and our understanding of how complex predator assemblages influence the abundance and dynamics of these species is surprisingly limited. In an intact grassland ecosystem in western Montana, USA, we examined the abundance and dynamics of Columbian ground squirrels (Spermophilus columbianus), deer mice (Peromyscus maniculatus), and montane voles (Microtus montanus) on 1-ha plots where we excluded mammalian and avian predators and ungulates, excluded ungulates alone, or allowed predators and ungulates full access. Our goal was to determine whether the relatively low population abundance and moderate population fluctuations of these rodents were due to population suppression by predators. Our predator-exclusion treatment was divided into two phases: a phase where we excluded all predators except weasels (Mustela spp.; 2002-2005), and a phase where all predators including weasels were excluded (2006-2009). Across the entire duration of the experiment, predator and/or ungulate exclusion had no effect on the abundance or overall dynamics of ground squirrels and deer mice. Ground squirrel survival (the only species abundant enough to accurately estimate survival) was also unaffected by our experimental treatments. Prior to weasel exclusion, predators also had no impacts on montane vole abundance or dynamics. However, after weasel exclusion, vole populations reached greater population peaks, and there was greater recruitment of young animals on predator-exclusion plots compared to plots open to predators during peak years. These results suggest that the impacts of predators cannot be generalized across all rodents in an assemblage. Furthermore, they suggest that specialist predators can play an important role in suppressing vole abundance even in lower-latitude vole populations that occur at relatively low densities.     

Effects of predator visibility on prey encounter: a case study on aerial web weaving spiders

Summary Perhaps the most important factor affecting predator-prey interactions is their encounter probability. Predators must either locate sites where prey are active or attract prey to them, and prey must be able to recognize potential predators and flee before capture. In this study we manipulate and describe three components of the foraging system of predatory, web-weaving spiders, the presence of viscid droplets, silk brightness (achromatic surface reflectance), and visibility of the orb pattern, to determine their effect on insect attraction, recognition, and web avoidance. We found that webs with viscid droplets were more visible to prey at close range, but at greater distances the sparkling droplets lured insects to the web area and hence increased insect capture probability. Although the size of viscid droplets and silk brightness are closely correlated (Table 2, Fig. 3), the relationships among droplet size, spider size, and the visual environments in which webs are found are more complicated (Fig. 2, Tables 2, 3). In environments with predictable light exposure, droplet size and hence silk visibility correlate with spider size, and spiders that forage at night produce relatively more visible silks then spiders that forage during the day (Table 3, Fig. 4). In habitats in which light levels are not predictable, silk surface reflectance and spider size are not closely correlated, suggesting that the complexity of the light environment, as well as the visual and foraging behaviors of insects found there, has played an important role in the evolution of spider-insect interactions.Offprint requests to: C.L. Craig     

Comparing environmental influences on coral bleaching across and within species using clustered binomial regression

Differential susceptibility among reef-building coral species can lead to community shifts and loss of diversity as a result of temperature-induced mass bleaching events. We evaluate environmental influences on coral colony bleaching over an 8-year period in the Florida Keys, USA. Clustered binomial regression is used to develop models incorporating taxon-specific responses to the environment in order to identify conditions and species for which bleaching is likely to be severe. By building three separate models incorporating environment, community composition, and taxon-specific responses to environment, we show observed prevalence of bleaching reflects an interaction between community composition and local environmental conditions. Environmental variables, including elevated sea temperature, solar radiation, and reef depth, explained 90% and 78% of variability in colony bleaching across space and time, respectively. The effects of environmental variables were only partially explained (33% of variability) by corresponding differences in community composition. Taxon-specific models indicated individual coral species responded differently to local environmental conditions and had different sensitivities to temperature-induced bleaching. For many coral species, but not all, bleaching was exacerbated by high solar radiation. A 25% reduction in the probability of bleaching in shallow locations for one species may reflect an ability to acclimatize to local conditions. Overall, model results indicate predictions of coral bleaching require knowledge of not just the environmental conditions or community composition, but the responses of individual species to the environment. Model development provides a useful tool for coral reef management by quantifying the influence of the local environment on individual species bleaching sensitivities, identifying susceptible species, and predicting the likelihood of mass bleaching events with changing environmental conditions.     

Effects of life‐history requirements on the distribution of a threatened reptile

Survival and reproduction are the two primary life‐history traits essential for species’ persistence; however, the environmental conditions that support each of these traits may not be the same. Despite this, reproductive requirements are seldom considered when estimating species’ potential distributions. We sought to examine potentially limiting environmental factors influencing the distribution of an oviparous reptile of conservation concern with respect to the species’ survival and reproduction and to assess the implications of the species’ predicted climatic constraints on current conservation practices. We used ecological niche modeling to predict the probability of environmental suitability for the alligator snapping turtle (Macrochelys temminckii). We built an annual climate model to examine survival and a nesting climate model to examine reproduction. We combined incubation temperature requirements, products of modeled soil temperature data, and our estimated distributions to determine whether embryonic development constrained the northern distribution of the species. Low annual precipitation constrained the western distribution of alligator snapping turtles, whereas the northern distribution was constrained by thermal requirements during embryonic development. Only a portion of the geographic range predicted to have a high probability of suitability for alligator snapping turtle survival was estimated to be capable of supporting successful embryonic development. Historic occurrence records suggest adult alligator snapping turtles can survive in regions with colder climes than those associated with consistent and successful production of offspring. Estimated egg‐incubation requirements indicated that current reintroductions at the northern edge of the species’ range are within reproductively viable environmental conditions. Our results highlight the importance of considering survival and reproduction when estimating species’ ecological niches, implicating conservation plans, and benefits of incorporating physiological data when evaluating species’ distributions.     

Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

Predators can initiate trophic cascades by consuming and/or scaring their prey. Although both forms of predator effect can increase the overall abundance of prey's resources, nonconsumptive effects may be more important to the spatial and temporal distribution of resources because predation risk often determines where and when prey choose to forage. Our experiment characterized temporal and spatial variation in the strength of consumptive and nonconsumptive predator effects in a rocky intertidal food chain consisting of the predatory green crab (Carcinus maenas), an intermediate consumer (the dogwhelk, Nucella lapillus), and barnacles (Semibalanus balanoides) as a resource. We tracked the survival of individual barnacles through time to map the strength of predator effects in experimental communities. These maps revealed striking spatiotemporal patterns in Nucella foraging behavior in response to each predator effect. However, only the nonconsumptive effect of green crabs produced strong spatial patterns in barnacle survivorship. Predation risk may play a pivotal role in determining the small-scale distribution patterns of this important rocky intertidal foundation species. We suggest that the effects of predation risk on individual foraging behavior may scale up to shape community structure and dynamics at a landscape level.     

Intraspecific variation in a predator affects community structure and cascading trophic interactions

Intraspecific phenotypic variation in ecologically important traits is widespread and important for evolutionary processes, but its effects on community and ecosystem processes are poorly understood. We use life history differences among populations of alewives, Alosa pseudoharengus, to test the effects of intraspecific phenotypic variation in a predator on pelagic zooplankton community structure and the strength of cascading trophic interactions. We focus on the effects of differences in (1) the duration of residence in fresh water (either seasonal or year-round) and (2) differences in foraging morphology, both of which may strongly influence interactions between alewives and their prey. We measured zooplankton community structure, algal biomass, and spring total phosphorus in lakes that contained landlocked, anadromous, or no alewives. Both the duration of residence and the intraspecific variation in foraging morphology strongly influenced zooplankton community structure. Lakes with landlocked alewives had small-bodied zooplankton year-round, and lakes with no alewives had large-bodied zooplankton year-round. In contrast, zooplankton communities in lakes with anadromous alewives cycled between large-bodied zooplankton in the winter and spring and small-bodied zooplankton in the summer. In summer, differences in feeding morphology of alewives caused zooplankton biomass to be lower and body size to be smaller in lakes with anadromous alewives than in lakes with landlocked alewives. Furthermore, intraspecific variation altered the strength of the trophic cascade caused by alewives. Our results demonstrate that intraspecific phenotypic variation of predators can regulate community structure and ecosystem processes by modifying the form and strength of complex trophic interactions.