Emergent Multiple Predator Effects Research Articles

Predicting prey diversity with multiple predator effects

Emergent multiple predator effects can result in either risk enhancement or reduction for prey populations. However, whether emergent multiple predator effects influence survival of entire prey assemblages is unknown, which could alter community diversity. We tested whether emergent multiple predator effects would lead to changes in survival of multiple prey species that would subsequently alter prey diversity. We experimentally tested whether larval ringed (Ambystoma annulatum) and marbled salamanders (A. opacum) had additive or multiplicative effects on hatchlings of an assemblage of five amphibian prey species using outdoor mesocosms. We also examined this question using data from a previously published experiment. We extended the multiplicative risk model to estimate prey diversity based on individual prey survival probabilities from each mesocosm. We found that predators generally had additive effects on all prey species, as the expected survival of prey was not different from the observed data, indicating a lack of emergent multiple predator effects. Consistent with this result, observed diversity was not different from expected diversity based on our extension of the multiplicative risk model, further indicating predator species had additive effects. Re-analysis of previously published data showed that when emergent multiple predator effects resulted in risk reduction, diversity changed in a manner consistent that outcome. Overall, we found that additive and multiplicative effects of multiple predators contributed to structuring entire prey communities, including influencing community metrics like diversity. Future work should consider further under what conditions diversity enhancement or reduction would occur.

Multiple-Predator Effects and Functional Redundancy of Pond Predators

Functional redundancy occurs when different predator species have similar effects on the diversity, abundance, and composition of a prey community. When multiple predators coexist, their interactions can alter prey survival and ultimately diversity through emergent multiple-predator effects (MPEs). MPEs can be exacerbated by differences in predator behavior; however, little is known about the magnitude of MPEs when predators compete for the same prey or have similar behavioral traits. To understand functional redundancy and the interactions of multiple predators in similar niches, as well as their impacts on the composition of a prey community, we conducted two experiments using two ambystomatid salamander predators (Ambystoma opacum and Ambystoma annulatum). We exposed a suite of tadpole prey (Anaxyrus americanus, Rana sphenocephala, Rana sylvatica, Pseudacris feriarum, and Pseudacris crucifer) to different experimental food webs in a mesocosm experiment, and a single prey species (R. sphenocephala) in microcosm experiment with substitutive and additive designs to test for MPEs. We found no evidence for functional redundancy between the two predators: A. annulatum selectively preyed on competitively dominant prey species (A. americanus) and did not alter community diversity. Ambystoma opacum decreased prey diversity relative to the control because of natural phenological mismatch with A. americanus. Interactions between the two predators (e.g., predator inference) were lacking, indicating that predation risk from each predator was independent for the one prey species we tested. A better understanding of community and ecosystem-level effects by A. annulatum can inform future conservation efforts and management decisions regarding this endemic species.

Functional Responses and Additive Multiple Predator Effects of Two Common Wetland Fish

Understanding trophic interactions is essential for the prediction and measurement of structure and function in aquatic environments. Communities in these ecosystems may be shaped by variables such as predator diversity, prey density and emergent multiple predator effects (MPEs), which are likely to influence trophic dynamics. In this study, we examined the effect of key predatory fish in floodplain wetlands, namely Oreochromis mossambicus and Enteromius paludinosus, towards Chironomidae prey, using a comparative functional response (FR) approach. We used single predator species as well as intra- and interspecific paired species to contrast FRs under multiple predator scenarios. Attack rate and handling time estimates from single predator FRs were used to predict multiple predators’ feeding rates, which were compared to observe multiple predators’ feeding rates to quantify potential MPEs. From single fish trials, each species displayed a significant Type II FR, characterized by high feeding rates at low prey densities. Oreochromis mossambicus had a steeper (initial slope, i.e., higher attack rate) and higher (asymptote of curve, i.e., shorter handling time and higher maximum feeding rate) FR, whereas E. paludinosus exhibited lower-magnitude FRs (i.e., lower attack rate, longer handling time and lower feeding rate). In multiple predator scenarios, feeding rates were well-predicted by those of single predators, both in conspecific and interspecific pairs, and thus we did not find evidence for antagonistic or synergistic MPEs. Predator–prey interactions in wetland systems can have significant consequences on the structure and dynamics of ecological communities. In turn, this could have destabilizing effects on resources in tropical wetlands. These results, although experimental, help us understand how trophic interaction among conspecific or interspecific fish species in Austral tropical wetlands might influence their aquatic prey species. This will help us to understand food web dynamics better.

Density dependence mediates the ecological impact of an invasive fish

AbstractAimThe way in which habitat heterogeneity and predator density affect predator–prey dynamics, space use and prey risk are understudied aspects of foraging ecology, particularly for invasive species. Likewise, how an invasive species’ impact scales with its abundance is poorly understood. We used a model invasive species—lionfish (Pterois volitans)—to understand emergent multiple predator effects and influences of habitat heterogeneity on consumption rate and prey mortality risk.LocationFlorida, USA.MethodsWe considered effects of both predator and prey abundance on density‐dependent impact. We used functional response methodology to quantify the per‐capita effect of P. volitans, assessing concomitant influences of prey refuge (3 levels) and predator density (3 levels) on predator–prey space use and predation efficiency across increasing prey densities (7 levels). We then assessed intraspecific interaction outcomes by comparing observed per‐capita effects with predicted estimates based on consumption rates of individual predators. This allowed us to detect the presence of emergent multiple predator effects (MPEs) and tease apart density‐dependent impacts.ResultsLionfish predatory impact was mediated by predator and prey density but unaffected by refugia. Despite incongruent patch preferences between predators and their prey, predator impacts were context‐independent. We also detected nonlinear scaling of impact with increasing predator abundance. Pairs of lionfish had the greatest per‐capita effect, whose cumulative impact on prey matched that expected of independently foraging predators. At the highest predator density (four fish), antagonistic multiple predator effects precipitated prey risk reduction, in which we observed the lowest per‐capita effect. Across predator abundances, prey mortality rates were inversely density‐dependent.Main conclusionsQuantifying non‐independent consumptive effects of multiple conspecific predators across levels of prey abundance can inform better prediction and understanding of invasive species' density‐dependent effects. Additionally, consideration of heterogeneity‐mediated FRs and predator–prey spatial distributions may facilitate more precise and realistic predictions of invader impact across their invaded range.

Additive multiple predator effects can reduce mosquito populations

1. Multiple predator interactions may profoundly alter ecological community dynamics and can complicate predictions of simpler pairwise predator–prey interaction strengths. In particular, multiple predator effects may lessen or enhance prey risk, with implications for community‐level stability. Such emergent effects may modulate natural enemy efficacy towards target organisms.2. In the present study, a functional response approach was used to quantify emergent multiple predator effects among natural enemies towards the disease vector mosquito complex, Culex pipiens. Conspecific multiple predator–predator interactions of the cyclopoid copepod Macrocyclops albidus (intermediate predator) were quantified by comparing multiple predator consumption simulations, based on individual consumption rates, with multiple predator consumption rates that were experimentally observed. Further, the study examined the influence of the presence of a predator at a higher trophic level, Chaoborus flavicans, on copepod group predation.3. Both predators displayed type II functional responses, with C. flavicans consuming significantly more prey than M. albidus individually. Overall consumption levels of mosquitoes increased with greater predator density and richness. Antagonistic or synergistic emergent multiple predator effects between conspecifics of M. albidus were not detected, and the higher‐level predator did not reduce effects of the intermediate predator. Accordingly, evidence for additive multiple predator interactions was found.4. The lack of predator–predator interference between cyclopoid copepods and larval chaoborid midges provides strong support for their combined application in mosquito biocontrol. It is proposed that there should be increased examination of multiple predator effects in assessments of natural enemy efficacies to better understand overall predatory effects within communities and utilities in vector control.

Emergent intraspecific multiple predator effects shape estuarine trophic dynamics across a gradient of habitat complexity

Estuarine ecosystems are characterized by heterogeneity in species assemblages and habitat complexity, so prey in these systems are often threatened by multiple predators across a mosaic of habitats. When several predator species or conspecifics co-occur, behavioral interactions between them can introduce non-independence to their predator-prey dynamics, which can alter the fate of shared prey. Habitat complexity may regulate these interactions and further impact prey survivorship. We conducted an experiment that manipulated the densities and identities of two ecologically similar estuarine-dependent predators, Red Drum (Sciaenops ocellatus) and Spotted Seatrout (Cynoscion nebulosus), within three habitat complexities. The resulting survivorships of two shared prey types were utilized to determine whether these predators are substitutable, to examine their inter- and intra-specific trophic interactions, and to investigate the impact of habitat structural complexity on their trophic dynamics. The predators differed in their prey preferences and predation pressures, indicating they are generally not substitutable. Interactions between conspecific predators were particularly important in shaping trophic dynamics, and often resulted in combined predation impacts that either enhanced or reduced the survivorship of shared prey as compared to expected values based on foraging rates of individuals. Minimal evidence of interspecific trophic interactions was detected. The observed emergent multiple predator effects differed among the habitats, and were generally intense in intermediate habitat complexity but were either intense or weak in high habitat complexity, depending on the predator combination. These results collectively indicate that prey regulation in this estuarine trophic system is highly dependent on the predator-prey assemblage and habitat context, and enhances our understanding of how multiple predators interactively shape their shared ecosystem.

On the use of functional responses to quantify emergent multiple predator effects

Non-independent interactions among predators can have important consequences for the structure and dynamics of ecological communities by enhancing or reducing prey mortality rate through, e.g., predator facilitation or interference. The multiplicative risk model, traditionally used to detect these emergent multiple predator effects (MPEs), is biased because it assumes linear functional response (FR) and no prey depletion. To rectify these biases, two approaches based on FR modelling have recently been proposed: the direct FR approach and the population-dynamic approach. Here we compare the strengths, limitations and predictions of the three approaches using simulated data sets. We found that the predictions of the direct FR and the multiplicative risk models are very similar and underestimate predation rates when prey density is high or prey depletion is substantial. As a consequence, these two approaches often fail in detecting risk reduction. Finally, parameters estimated with the direct FR approach lack mechanistic interpretation, which limits the understanding of the mechanisms driving multiple predator interactions and potential extension of this approach to more complex food webs. We thus strongly recommend using the population-dynamic approach because it is robust, precise, and provides a scalable mechanistic framework to detect and quantify MPEs.

A spatial theory for emergent multiple predator-prey interactions in food webs.

Predator–prey interaction is inherently spatial because animals move through landscapes to search for and consume food resources and to avoid being consumed by other species. The spatial nature of species interactions necessitates integrating spatial processes into food web theory and evaluating how predators combine to impact their prey. Here, we present a spatial modeling approach that examines emergent multiple predator effects on prey within landscapes. The modeling is inspired by the habitat domain concept derived from empirical synthesis of spatial movement and interactions studies. Because these principles are motivated by synthesis of short‐term experiments, it remains uncertain whether spatial contingency principles hold in dynamical systems. We address this uncertainty by formulating dynamical systems models, guided by core habitat domain principles, to examine long‐term multiple predator–prey spatial dynamics. To describe habitat domains, we use classical niche concepts describing resource utilization distributions, and assume species interactions emerge from the degree of overlap between species. The analytical results generally align with those from empirical synthesis and present a theoretical framework capable of demonstrating multiple predator effects that does not depend on the small spatial or temporal scales typical of mesocosm experiments, and help bridge between empirical experiments and long‐term dynamics in natural systems.

The importance of intraguild predation in predicting emergent multiple predator effects

Prey typically coexist with multiple predator species, each of which presents a predation risk related to its habitat domain and foraging mode. These predator characteristics can be used to predict how the risk from multiple predators will combine to create emergent multiple predator effects for shared prey. Interactions between predators, particularly intraguild predation, can strongly alter prey suppression, though the importance of intraguild predation in multiple predator effects has not been explicitly explored. Furthermore, the vast majority of studies on multiple predator effects has focused on shared prey that are herbivorous, thus experiments focused on mesopredators are needed to evaluate the generality of conclusions made about multiple predator effects. We used a suite of carnivorous arthropods to test a predictive framework of multiple predator effects and to evaluate the role of intraguild predation in shaping these effects. We allowed the wolf spiders Pardosa milvina, Tigrosa helluo, and Rabidosa rabida and the ground beetle Scarites quadriceps to interact and recorded the outcome of all predatory events. We used two tests of multiple predator effects to determine whether predators created risk enhancement, risk reduction, or were substitutable. We found that the occurrence of intraguild predation decreased the overall risk to prey, causing observed multiple predator effects to deviate from predictions. Additionally, we highlight the importance of considering predator identity, as predators were capable of increasing, decreasing, or not altering the success of their competitors. Our study demonstrates that intraguild predation is a critical factor in determining how the risk from multiple predators will combine to affect their prey.

Independent and combined effects of multiple predators across ontogeny of a dominant grazer

Ecosystems host multiple coexisting predator species whose interactions may strengthen or weaken top–down control of grazers. Grazer populations often exhibit size‐structure, but the nature of multiple predator effects on suppression of size‐structured prey has seldom been explicitly considered. In a southeastern US salt‐marsh, we used both field (additive design) and mesocosm (additive‐substitutive design) experiments to test the independent and combined effects of two species of predatory crab on the survival and predator‐avoidance behavior (i.e. a non‐consumptive effect) of both juveniles and adults of a dominant grazing snail. Results showed: 1) juvenile snails were more vulnerable to predation; 2) consumptive impacts of predators were hierarchically nested, i.e. the larger predator consumed both juvenile and adult snails, while the smaller‐bodied predator consumed only juvenile snails; 3) there were no emergent multiple predator effects on snail consumption; and 4) non‐consumptive effects differed from consumptive effects, with only the large predator inducing predator‐avoidance behavior of individuals within either snail ontogenetic class. The smaller predator therefore played a functionally redundant trophic role across the prey classes considered, augmenting and potentially stabilizing trophic regulation of juvenile snails. Meanwhile, the larger predator played a complementary and functionally unique role by both expanding the size‐spectrum of prey trophic regulation and non‐consumptively altering prey behavior. While our study suggests that nestedness of consumptive interactions determined by predator and prey body sizes may allow prediction of the functional redundancy of particular predator species, it also shows that traits beyond predator body size (e.g. habitat domain) may be required to predict potentially cascading non‐consumptive effects. Future studies of multiple predators (and predator biodiversity) should continue to strive towards greater realism by incorporating not only size‐structured prey, but also other aspects of resource and environmental heterogeneity typical of natural ecosystems.

Fortune favours the bold: a higher predator reduces the impact of a native but not an invasive intermediate predator

Emergent multiple predator effects (MPEs) might radically alter predictions of predatory impact that are based solely on the impact of individuals. In the context of biological invasions, determining if and how the individual-level impacts of invasive predators relates to their impacts in multiple-individual situations will inform understanding of how such impacts might propagate through recipient communities. Here, we use functional responses (the relationship between prey consumption rate and prey density) to compare the impacts of the invasive freshwater mysid crustacean Hemimysis anomala with a native counterpart Mysis salemaai when feeding on basal cladoceran prey (i) as individuals, (ii) in conspecific groups and (iii) in conspecific groups in the presence of a higher fish predator, Gasterosteus aculeatus. In the absence of the higher predator, the invader consumed significantly more basal prey than the native, and consumption was additive for both mysid species - that is, group consumption was predictable from individual-level consumption. Invaders and natives were themselves equally susceptible to predation when feeding with the higher fish predator, but an MPE occurred only between the natives and higher predator, where consumption of basal prey was significantly reduced. In contrast, consumption by the invaders and higher predator remained additive. The presence of a higher predator serves to exacerbate the existing difference in individual-level consumption between invasive and native mysids. We attribute the mechanism responsible for the MPE associated with the native to a trait-mediated indirect interaction, and further suggest that the relative indifference to predator threat on the part of the invader contributes to its success and impacts within invaded communities.

Emergent effects of multiple predators on prey survival: the importance of depletion and the functional response

The combined effects of multiple predators often cannot be predicted from their independent effects. Emergent multiple predator effects (MPEs) include risk enhancement, where combined predators kill more prey than predicted by their individual effects, and risk reduction, where fewer prey are killed than predicted. Current methods for detecting MPEs are biased because they assume linear functional responses and/or no prey depletion. As a result, past studies overestimated the occurrence of risk enhancement for additive designs, and tended to overestimate the occurrence of risk reduction for substitutive designs. Characterising the predators' functional responses and accounting for prey depletion reduces biases in detection, estimation, interpretation and generalisation of the emergent effects of predator diversity on prey survival. These findings have implications beyond MPE's and should be considered in all studies aimed at understanding how multiple factors combine when demographic rates are density dependent.

HABITAT COMPLEXITY INFLUENCES CASCADING EFFECTS OF MULTIPLE PREDATORS

Although multiple predator effects and trophic cascades have both been demonstrated in a wide variety of ecosystems, ecologists have yet to incorporate these studies into an experimental framework that also manipulates a common and likely important factor, spatial heterogeneity. We manipulated habitat complexity, the presence of two top predators (toadfish and blue crabs), and one intermediate predator (mud crabs) to determine whether habitat complexity influences the strength of multiple predator interactions across multiple trophic levels in experimental oyster reef communities. In the absence of toadfish, blue crabs caused significant mud crab mortality. Despite also directly consuming mud crabs, toadfish indirectly benefited this intermediate predator by decreasing blue crab consumption of mud crabs. Toadfish suppression of mud crab foraging activity, and thus decreased mud crab encounters with blue crabs, is likely responsible for this counterintuitive result. Contrary to previous investigations which suggest that more complex habitats reduce interference interactions among predators, reef complexity strengthened emergent multiple predator effects (MPEs) on mud crabs. The degree to which these MPEs cascaded down to benefit juvenile oysters (basal prey) depended on both habitat complexity and nonconsumptive effects derived from predator-predator interactions. Habitat complexity reduced the foraging efficiency of each crab species individually but released crab interference interactions when together, so that the two crabs collectively consumed more oysters on complex reefs. Regardless of reef complexity, toadfish consistently decreased consumption of oysters by both crab species individually and when together. Therefore, interactions between predator identity and habitat complexity structure trophic cascades on oyster reefs. Furthermore, these cascading effects of multiple predators were largely mediated by nonconsumptive effects in this system.

Emergent multiple predator effects in an experimental microbial community

AbstractStudies on multiple predator effects have typically focused on metazoans. Here we examined the effects of multiple consumers on bacteria. Specifically, we investigated the separate and combined effects of two common bacterivorous ciliates, Colpidium striatum and Paramecium caudatum, on a simple bacterial assemblage. Non‐additive multiple predator effects emerged for all bacterial species significantly affected by grazing, where bacterial responses in the two‐consumer treatment cannot be predicted by summing the separate effects of the two consumers. Some species showed risk reduction (observed responses less than expected), whereas others showed risk enhancement (observed responses larger than expected). We attributed risk alteration to the interference between the two consumers. Contradictory to theoretical predictions, total bacterial abundance in the two‐consumer treatment did not differ from single‐consumer treatments and consumer‐free controls, due largely to risk reduction and compensatory responses within the bacterial assemblage. Decomposition of particulate organic matter was greater in the two‐consumer treatment than the Paramecium single‐consumer treatment, but did not differ among other treatments. These results suggest that the presence of multiple consumers may have unexpected impacts on the structure and functioning of bacterial communities.

Stage dependent habitat use under conflicting predation pressure: An experimental test with larval and juvenile two-spotted gobies, Gobiusculus flavescens Fabricius

The effect of size, predator types and presence of multiple predators on the microhabitat use of larvae and juveniles of a sublittoral, semipelagically schooling fish, the two-spotted goby ( Gobiusculus flavescens), was tested in two experiments. Larvae (15 and 25 days old, Experiment I) and juveniles (mean ± 1 S.E.: small, 15.9 mm ± 1.28; medium, 19.2 mm ± 1.43; and large, 23.4 mm ± 1.67, Experiment II) were allowed to choose between two sections of the tanks; an upper, representing a water column habitat, and a lower, artificially vegetated, representing the hyperbenthic habitat. Position of larvae or juveniles and the activity level of juveniles were recorded. Predator treatments were: (I) no predators (control), (II) a pelagic predator, the jellyfish Aurelia aurita L., (III) a hyperbenthic predator, the mysid Praunus flexuosus O.F. Müller or (VI) both predator types simultaneously. In Experiment I predators were restricted to the habitat which they were chosen to represent, while goby larvae could move freely. In Experiment II both predators and juvenile gobies were allowed to move freely between compartments. Increasing age caused larval gobies, but not juveniles to shift downwards. Only 25-day-old larvae and small juveniles avoided the mysid by shifting upwards. Larval response to A. aurita was also size dependant: 25-day-old larvae avoided medusae by shifting downwards, while 15 day olds did not. Emergent multiple predator effects were found for the vertical distribution of 15-day-old larvae and small juveniles. Larger juveniles were more active than smaller, both in the upper and the lower sections of tanks. P. flexuosus caused juvenile gobies in their vicinity (i.e. in the lower section) to increase their activity level, while small juveniles (but not medium-sized or large) increased their activity level even when further away (i.e. in the upper section). The presence of A. aurita led to a reduction in activity of small juveniles in its vicinity (i.e. in the upper section), while no response was observed among older juveniles or juveniles further away from the predator (i.e. in the lower section). Emergent multiple predator effects on the activity level of juveniles were not observed.

Does aggregation benefit bark beetles by diluting predation? Links between a group‐colonisation strategy and the absence of emergent multiple predator effects

Abstract. 1. Aggregation in bark beetles (Coleoptera: Scolytidae) aids in mate attraction and resource procurement when colonising well‐defended plants; however, some species colonise primarily poorly defended plants, and intraspecific competition increases mortality. The hypothesis that decreased risk of predation was a potential benefit to aggregation in such circumstances was tested, using the pine engraver, Ips pini (Say) and its two major predators Thanasimus dubius (F.) (Coleoptera: Cleridae) and Platysoma cylindrica (Paykull) (Coleoptera: Histeridae). Both single‐ and multiple‐predator effects, across a range of prey densities, were tested.2. Both male and female colonisation events increased with herbivore density, in an asymptotic fashion.3. Predators decreased the number of colonisers in a density‐dependent manner, consistent with a type II functional response.4. The proportional impact of predators decreased with increased herbivore colonisation densities. These findings indicate that predator dilution may be a viable benefit to aggregation.5. Total emergence of the herbivore also increased with density, although the net replacement rate during one generation was independent of initial arrival density. This was likely due to larval predation, which negates potential relationships between per capita reproductive success and establishment density.6. Each predator species decreased I. pini's net replacement rate by approximately 42%, and their combined effect was approximately 70%.7. Overall, these predators modified their prey's establishment and adult mortality relationships in additive manners. This is somewhat surprising, given the potential for emergent effects due to interactions between multiple predators foraging within a common habitat. The persistence of additivity, rather than risk reduction or enhancement to the prey, may increase the predator‐swamping benefit to aggregation for this herbivore.8. The effects of these predators are substitutable, and likely exert equivalent selective pressures to mask signals at the whole‐plant level.

AN EMERGENT MULTIPLE PREDATOR EFFECT MAY ENHANCE BIOTIC RESISTANCE IN A STREAM FISH ASSEMBLAGE

While two cyprinid fishes introduced from nearby drainages have become widespread and abundant in the Eel River of northwestern California, a third nonindigenous cyprinid has remained largely confined to ≤25 km of one major tributary (the Van Duzen River) for at least 15 years. The downstream limit of this species, speckled dace, does not appear to correspond with any thresholds or steep gradients in abiotic conditions, but it lies near the upstream limits of three other fishes: coastrange sculpin, prickly sculpin, and nonindigenous Sacramento pikeminnow. We conducted a laboratory stream experiment to explore the potential for emergent multiple predator effects to influence biotic resistance in this situation. Sculpins in combination with Sacramento pikeminnow caused greater mortality of speckled dace than predicted based on their separate effects. In contrast to speckled dace, 99% of sculpin survived trials with Sacramento pikeminnow, in part because sculpin usually occupied benthic cover units while Sacramento pikeminnow occupied the water column. A 10-fold difference in benthic cover availability did not detectably influence biotic interactions in the experiment. The distribution of speckled dace in the Eel River drainage may be limited by two predator taxa with very different patterns of habitat use and a shortage of alternative habitats.