Multiple Predator Effects Research Articles

Assessing biological invasion predatory impacts through interaction strengths and morphological trophic profiling

AbstractBiological invasions are a major stressor on ecosystems worldwide, but tools to predict their predatory impact remain limited. Here, we quantified invader impacts using two complementary approaches: functional responses (to reveal per capita and multiple predator interaction strengths) and ecomorphology (to reveal trophic profiles and competitive overlap). We compared Mozambique tilapia Oreochromis mossambicus, a native southern African cichlid, and a near-trophically analogous invasive congener, the Nile tilapia Oreochromis niloticus. Both Nile tilapia and Mozambique tilapia exhibited a potentially prey population destabilizing Type II functional response. In both single and multiple predator pairings, invasive Nile tilapia had significantly greater prey consumption rates than native Mozambique tilapia, and thereby a greater predatory impact than its native congeneric. Attack rates were greater for Nile tilapia than Mozambique tilapia, with both species showing more similar handling times and maximum feeding rates. No evidence for multiple predator effects was detected within or between these species, and therefore impacts of both species increased additively in the presence of conspecific or heterospecific competitors. Morphological trait analyses found general differences between these two species, with the invasive Nile tilapia having distinctively larger lower jaw closing force, gill resistance and gill raker length, which facilitated greater feeding capacities over the native species. Trophic profiles predicted using morphological trait differences showed high dietary overlap and served as evidence for potential exploitative competition between the two species. These results reveal superior interaction strengths and ecomorphological trait profiles of an invasive over native species which could influence impact and native species replacement dynamics. Novel applications of functional response and ecomorphology provide complementary insights into predatory and competitive impacts from invasive species, aiding impact prediction across environmental contexts.

Non-additive effects of multiple predators alter the biological control of the coffee leaf miner (Leucoptera coffeella)

Although most prey are attacked by multiple predators, much of the ecological theory on prey suppression focuses on the effects of a single predator. The presence of multiple predators can lead to complex interactions such as trait-mediated interactions (TMIIs) and intraguild predation which can influence the suppression of pest populations. Here we explore the effect of two predators, a native anole lizard species Anolis cristatellus (Squamata: Dactyloidae) and a non-native ant species Wasmannia auropunctata (Hymenoptera: Formicidae), on the coffee leaf miner, Leucoptera coffeella (Lepidoptera: Lyonetiidae) (CLM). In a laboratory experiment we examined the effects of these two predators in isolation and when co-occurring. Our results show that when each predator is alone, they are able to consume the CLM in a comparable way. However, when they are together, their effect is not greater than when alone. This indicates that there is a negative effect when both predators co-occur. The results from this experiment have practical implications since both predators are present in coffee agroecosystems in Puerto Rico, where the CLM is considered the main insect pest. Furthermore, these results demonstrate the potential dynamics among several predators in agroecosystems and the potential implications for herbivore regulation.

Additive multiple predator effects increase prey mortality under experimental warming in a rocky intertidal food web

Climate warming is expected to alter species interactions, which are shaped by components of individual foraging behavior. Yet few studies examine species' behavioral responses to inform predictions about how species interactions will be affected by warming. Multiple predator effects (MPEs) may be mediated by climatic warming, especially in highly diverse coastal ecosystems that are prone to extreme warming events. In a laboratory experiment, we quantified the effects of elevated sea water temperature on mortality rates of mussels (Mytilus californianus, Conrad, 1837), and the behavioral responses of their predators: crabs (Romaleon antennarium, Stimpson, 1856) and sea stars (Pisaster ochraceus, Brandt, 1835), to understand how warming affects MPEs and if predators' behavioral responses to warming are indicative of the outcome of MPEs. Sea star effects on mussel mortality did not vary with temperature, but declined threefold in the presence of crabs, due to behavioral avoidance of physical contact with crabs. In contrast, the effect of crabs on mussel mortality was ten times higher under elevated temperature, but was unaffected by sea stars. In mixed predator treatments, crabs caused significant mussel mortality, but sea stars had weaker impacts, regardless of temperature. Consequently, multiple predators had effects that did not differ from those of the more effective crab predator. Increasing temperature in the eastern North Pacific may create locations where crabs become the dominant predator of mussels, with warming increasing predation risk for mussels in this region. Field studies should examine the effects of warming on crab predation on mussels in this system.

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.

Predicting prey diversity with multiple predator effects

Predicting prey diversity with multiple predator effects

Anthropogenic noise does not strengthen multiple-predator effects in a freshwater invasive fish.

Anthropogenic noise has the potential to alter community dynamics by modifying the strength of nested ecological interactions such as predation. Direct effects of noise on per capita predation rates have received much attention but the context in which predation occurs is often oversimplified. For instance, many animals interact with conspecifics while foraging and these nontrophic interactions can positively or negatively influence per capita predation rates. These effects are often referred to as multiple-predator effects (MPEs). The extent to which noise can modulate MPEs and thereby indirectly alter per capita predation remains unknown. To address this question, we derived the relationship between per capita predation rate and prey density, namely the functional response (FR), of single and pairs of the invasive topmouth gudgeon Pseudorasbora parva when feeding on water fleas under two noise conditions: control ambient noise estimated at 95 dB re 1 μPa and ambient noise supplemented with motorboat sounds whose relative importance over ambient noise ranged from 4.81 to 27 dB. In addition, we used video recordings to track fish movements. To detect MPEs, we compared the observed group-level FRs to predicted group-level FRs inferred from the individual FRs and based on additive effects only. Regardless of the number of fish and the noise condition, the FR was always of type II, showing predation rate in a decelerating rise to an upper asymptote. Compared to the noiseless condition, the predation rate of single fish exposed to noise did not differ at high prey densities but was significantly lower at low prey densities, resulting in an FR with the same asymptote but a less steep initial slope. Noise also reduced fish mobility, which might explain the decrease in predation rate at low prey densities. Conspecific presence suppressed the individual response to noise, the FRs of two fish (observed group-level FRs) being perfectly similar between the two noise conditions. Although observed and predicted group-level FRs did not differ significantly, observed group-level FRs tended to fall in the low range of predicted group-level FRs, suggesting antagonism and a negative effect of nontrophic interactions on individual foraging performance. Interestingly, the difference between predicted and observed group-level FRs was not greater with noise, which means that noise did not strengthen MPEs. Our results show that when considering the social context of foraging, here through the presence of a conspecific, anthropogenic noise does not compromise foraging in the invasive P. parva.

Multiple predator effects are modified by search area and prey size

Multiple predator effects are modified by search area and prey size

High temperatures enhance the strength of multiple predator effects in a typical crab-clam system

Although marine heatwaves pose urgent threats to marine life, our understanding of how these events influence interactions between key species in marine ecosystems is still inadequate. Herein, we examined the behavioral mechanisms by which heat regulates multiple predator effects in different foraging systems that include Asian paddle crabs (Charybdis japonica) and swimming crabs (Portunus trituberculatus) by quantifying their predation and competition at two temperatures. Our results show that non-independent multiple predator effects occurred in the conspecific treatment of Asian paddle crabs and in the interspecific treatment, whereas independent multiple predator effects occurred in the conspecific treatment of swimming crabs. Asymmetrical behavior responses of these crabs to competition and heat triggered divergences in multiple predator effects. High temperatures increased the strength of multiple predator effects but did not alter their types. The reason is that heat negatively impacts predation by enhancing aggressive interactions, outweighing its direct positive effects on predation.

Environmental and anthropogenic features mediate risk from human hunters and wolves for moose

AbstractLandscape characteristics, seasonal changes in the environment, and daylight conditions influence space use and detection of prey and predators, resulting in spatiotemporal patterns of predation risk for the prey. When predators have different hunting modes, the combined effects of multiple predators are mediated by the physical landscape and can result in overlapping or contrasting patterns of predation risk. Humans have become super‐predators in many anthropogenic landscapes by harvesting game species and competing with large carnivores for prey. Here, we used the locations of wolf (Canis lupus)‐killed and hunter‐killed moose (Alces alces) in south‐central Scandinavia to investigate whether environmental and anthropogenic features influenced where wolves and hunters killed moose. We predicted that the combined effects of wolves and hunters would result in contrasting spatial risk patterns due to differences in hunting modes. We expected these contrasting spatial risk patterns also to differ temporally. During the hunting season, the probability of a wolf kill increased with distance to bogs, whereas it decreased with increasing building density and distance to clearcuts and young forests. After the hunting season, the probability of a wolf kill increased with increasing terrain ruggedness and decreased with increasing building density, distance to main roads, and distance to clearcuts and young forests. The probability of a hunter kill was highest closer to bogs, main and secondary roads, in less rugged terrain and in areas with lower building density. Hunters killed all moose during the day, whereas wolves killed most moose at night during and after the hunting season. Our findings suggest that environmental and anthropogenic features mediate hunting and wolf predation risk. Additionally, we found that hunter‐ and wolf‐killed moose exhibited contrasting spatial associations to landscape features, most likely due to the different hunting modes displayed by hunters and wolves. However, wolf predation and hunting risks also contrasted over time since wolves killed mostly at night and hunters were restricted to hunting during daytime and during the hunting season. This temporal segregation in risk might therefore suggest that moose could minimize risk exposure by taking advantage of spatiotemporally vacant hunting domains.

Ungulate spatiotemporal responses to contrasting predation risk from wolves and snow leopards.

Spatial responses to risk from multiple predators can precipitate emergent consequences for prey (i.e. multiple-predator effects, MPEs) and mediate indirect interactions between predators. How prey navigate risk from multiple predators may therefore have important ramifications for understanding the propagation of predation-risk effects (PREs) through ecosystems. The interaction of predator and prey traits has emerged as a potentially key driver of antipredator behaviour but remains underexplored in large vertebrate systems, particularly where sympatric prey share multiple predators. We sought to better generalize our understanding of how predators influence their ecosystems by considering how multiple sources of contingency drive prey distribution in a multi-predator-multi-prey system. Specifically, we explored how two sympatric ungulates with different escape tactics-vertically agile, scrambling ibex Capra sibirica and sprinting argali Ovis ammon-responded to predation risk from shared predators with contrasting hunting modes-cursorial wolves Canis lupus and vertical-ambushing, stalking snow leopards Panthera uncia. Contrasting risk posed by the two predators presented prey with clear trade-offs. Ibex selected for greater exposure to chronic long-term risk from snow leopards, and argali for wolves, in a nearly symmetrical manner that was predictable based on the compatibility of their respective traits. Yet, acute short-term risk from the same predator upended these long-term strategies, increasing each ungulates' exposure to risk from the alternate predator in a manner consistent with a scenario in which conflicting antipredator behaviours precipitate risk-enhancing MPEs and mediate predator facilitation. By contrast, reactive responses to wolves led ibex to reduce their exposure to risk from both predators-a risk-reducing MPE. Evidence of a similar reactive risk-reducing effect for argali vis-à-vis snow leopards was lacking. Our results suggest that prey spatial responses and any resulting MPEs and prey-mediated interactions between predators are contingent on the interplay of hunting mode and escape tactics. Further investigation of interactions among various drivers of contingency in PREs will contribute to a more comprehensive understanding and improved forecasting of the ecological effects of predators.

Dataset and R source code of the manuscript 'Anthropogenic noise does not strengthen multiple predator effects in a freshwater invasive fish' by Emilie Rojas et al.

Dataset and R source code of the manuscript 'Anthropogenic noise does not strengthen multiple predator effects in a freshwater invasive fish' by Emilie Rojas et al.

Incorporating nonlinearity with generalized functional responses to simulate multiple predator effects.

Predicting the combined effects of predators on shared prey has long been a focus of community ecology, yet quantitative predictions often fail. Failure to account for nonlinearity is one reason for this. Moreover, prey depletion in multiple predator effects (MPE) studies generates biased predictions in applications of common experimental and quantitative frameworks. Here, we explore additional sources of bias stemming from nonlinearities in prey predation risk. We show that in order to avoid bias, predictions about the combined effects of independent predators must account for nonlinear size-dependent risk for prey as well as changes in prey risk driven by nonlinear predator functional responses and depletion. Historical failure to account for biases introduced by well-known nonlinear processes that affect predation risk suggest that we may need to reevaluate the general conclusions that have been drawn about the ubiquity of emergent MPEs over the past three decades.

Prey defence phenotype mediates multiple-predator effects in tri-trophic food webs.

The emphasis on mechanisms governing the interaction among predators (e.g. cooperation, competition or intraguild predation) has driven the understanding of multiple-predator effects on prey survival and dynamics. However, overwhelming evidence shows that prey can adaptively respond to predators, exhibiting multiple defensive phenotypes to cope with predation. Nevertheless, there is still a relatively scarce theory connecting the emergence of prey defences in complex multi-predator scenarios and their ecological consequences. Using a mathematical approach, we evaluated the prevalence of defended prey phenotypes as a function of predator-induced mortality in a two-predator system, and how prey and phenotype dynamics affect trophic cascades. We also evaluated such responses when prey manifests a general defence against both predators (i.e. risk reducing) or a specialized defence against one predator at the expense of defence against the other predator (i.e. risk trade-off), and when such phenotypes induce fitness and foraging costs. We showed that the emergence of defended phenotypes under multiple predators depends on predator-induced mortality rates, the magnitude of phenotype costs and the effect of the defensive phenotype on the performance of all predators. Risk-reducing phenotypes enhance prioritized responses to predators with high killing rates, but prioritized responses are diminished when prey manifest risk trade-off phenotypes. Finally, we showed that resource abundance across the predation gradient directly depends on the prevalence of certain prey phenotypes and their effect on foraging costs. Ultimately, our results depict the implications of prey defences on prey and basal resources abundance in a multiple predators' environment, highlighting the role of the identity of defensive strategies in mediating the strength and nature of trophic cascades, via consumptive or non-consumptive effects.

The presence of multiple parasitoids decreases host survival under warming, but parasitoid performance also decreases.

Current global changes are reshaping ecological communities and modifying environmental conditions. We need to recognize the combined impact of these biotic and abiotic factors on species interactions, community dynamics and ecosystem functioning. Specifically, the strength of predator-prey interactions often depends on the presence of other natural enemies: it weakens with competition and interference or strengthens with facilitation. Such effects of multiple predators on prey are likely to be affected by changes in the abiotic environment, altering top-down control, a key structuring force in natural and agricultural ecosystems. Here, we investigated how warming alters the effects of multiple predators on prey suppression using a dynamic model coupled with empirical laboratory experiments with Drosophila-parasitoid communities. While multiple parasitoids enhanced top-down control under warming, parasitoid performance generally declined when another parasitoid was present owing to competitive interactions. This could reduce top-down control over multiple generations. Our study highlights the importance of accounting for interactive effects between abiotic and biotic factors to better predict community dynamics in a rapidly changing world and thus better preserve ecosystem functioning and services such as biological control.

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.

Influence of multiple predators decreases body condition and fecundity of European hares.

We assessed the hypothesized negative correlation between the influence of multiple predators and body condition and fecundity of the European hare, from 13 areas in the Netherlands.Year‐round abundance of predators was estimated by hunters. We quantified predator influence as the sum of their field metabolic rates, as this sum reflects the daily food requirements of multiple individuals. We determined the ratio between body mass and hindfoot length of hares as an index of body condition and the weight of their adrenal gland as a measure of chronic exposure to stress, and we counted the number of placental scars to estimate fecundity of hares.As hypothesized, we found that the sum of field metabolic rate of predators was negatively correlated with body condition and the number of placental scars, whereas it was positively related to the weight of the adrenal glands. In contrast to the sum of the field metabolic rate, the total number of predators did not or weakly affect the investigated risk responses.The sum of the field metabolic rate can be a useful proxy for the influence of multiple predators and takes into account predator abundance, type, body weight, and food requirements of multiple predators.With our findings, our paper contributes to a better understanding of the risk effects of multiple predators on prey fitness. Additionally, we identify a potential contributor to the decline of European hare populations.

Predator-specific responses and emergent multi-predator effects on oviposition site choice in grey treefrogs, Hyla chrysoscelis.

Predators affect prey through both consumptive and non-consumptive effects (NCEs), and prey typically face threats from multiple simultaneous predators. While different predators have a variety of NCEs on prey, little is known regarding effects of simultaneous multiple predators on demographic habitat selection. Demographic habitat selection is unique among NCEs, especially in discrete habitat patches; decisions directly affect both distribution and abundance of species across habitat patches, rather than simply abundance and performance within patches. Our goal was to determine strength of avoidance responses to multiple species/species combinations of predatory fish, and responses to predator richness. We assessed responses of ovipositing grey treefrogs (Hyla chrysoscelis) to three predatory fish species and substitutive combination of species. In single-species treatments, treefrogs avoided only one species, Notemigonus crysoleucas. All two-species combinations, and the three-species combination, were avoided, including the Fundulus chrysotus × Noturus phaeus combination, of which neither were avoided alone. This suggests emergent properties of multiple predators, with potential interactive effects among cues themselves or in the perception of cues by treefrogs. Our results indicate effects of multiple predators are not predictable based on individual effects, and illustrate the importance and complexity of effects of demographic habitat selection on distribution and abundance.

Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages

The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species’ impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages.

Prey and predator density-dependent interactions under different water volumes.

Predation is a critical ecological process that directly and indirectly mediates population stabilities, as well as ecosystem structure and function. The strength of interactions between predators and prey may be mediated by multiple density dependences concerning numbers of predators and prey. In temporary wetland ecosystems in particular, fluctuating water volumes may alter predation rates through differing search space and prey encounter rates. Using a functional response approach, we examined the influence of predator and prey densities on interaction strengths of the temporary pond specialist copepod Lovenula raynerae preying on cladoceran prey, Daphnia pulex, under contrasting water volumes. Further, using a population dynamic modeling approach, we quantified multiple predator effects across differences in prey density and water volume. Predators exhibited type II functional responses under both water volumes, with significant antagonistic multiple predator effects (i.e., antagonisms) exhibited overall. The strengths of antagonistic interactions were, however, enhanced under reduced water volumes and at intermediate prey densities. These findings indicate important biotic and abiotic contexts that mediate predator–prey dynamics, whereby multiple predator effects are contingent on both prey density and search area characteristics. In particular, reduced search areas (i.e., water volumes) under intermediate prey densities could enhance antagonisms by heightening predator–predator interference effects.