Metabolic plasticity drives mismatches in physiological traits between prey and predator.

Metabolic rate, the rate of energy use, underpins key ecological traits of organisms, from development and locomotion to interaction rates between individuals. In a warming world, the temperature-dependence of metabolic rate is anticipated to shift predator-prey dynamics. Yet, there is little real-world evidence on the effects of warming on trophic interactions. We measured the respiration rates of aquatic larvae of three insect species from populations experiencing a natural temperature gradient in a large-scale mesocosm experiment. Using a mechanistic model we predicted the effects of warming on these taxa's predator-prey interaction rates. We found that species-specific differences in metabolic plasticity lead to mismatches in the temperature-dependence of their relative velocities, resulting in altered predator-prey interaction rates. This study underscores the role of metabolic plasticity at the species level in modifying trophic interactions and proposes a mechanistic modelling approach that allows an efficient, high-throughput estimation of climate change threats across species pairs.

Invasive European green crab (Carcinus maenas) predation in a Washington State estuary revealed with DNA metabarcoding.

Predation by invasive species can threaten local ecosystems and economies. The European green crab (Carcinus maenas), one of the most widespread marine invasive species, is an effective predator associated with clam and crab population declines outside of its native range. In the U.S. Pacific Northwest, green crab has recently increased in abundance and expanded its distribution, generating concern for estuarine ecosystems and associated aquaculture production. However, regionally-specific information on the trophic impacts of invasive green crab is very limited. We compared the stomach contents of green crabs collected on clam aquaculture beds versus intertidal sloughs in Willapa Bay, Washington, to provide the first in-depth description of European green crab diet at a particularly crucial time for regional management. We first identified putative prey items using DNA metabarcoding of stomach content samples. We compared diet composition across sites using prey presence/absence and an index of species-specific relative abundance. For eight prey species, we also calibrated metabarcoding data to quantitatively compare DNA abundance between prey taxa, and to describe an 'average' green crab diet at an intertidal slough versus a clam aquaculture bed. From the stomach contents of 61 green crabs, we identified 54 unique taxa belonging to nine phyla. The stomach contents of crabs collected from clam aquaculture beds were significantly different from the stomach contents of crabs collected at intertidal sloughs. Across all sites, arthropods were the most frequently detected prey, with the native hairy shore crab (Hemigrapsus oregonensis) the single most common prey item. Of the eight species calibrated with a quantitative model, two ecologically-important native species-the sand shrimp (Crangon franciscorum) and the Pacific staghorn sculpin (Leptocottus armatus)-had the highest average DNA abundance when detected in a stomach content sample. In addition to providing timely information on green crab diet, our research demonstrates the novel application of a recently developed model for more quantitative DNA metabarcoding. This represents another step in the ongoing evolution of DNA-based diet analysis towards producing the quantitative data necessary for modeling invasive species impacts.

Theory of Stoichiometric Intraguild Predation: Algae, Ciliate, and Daphnia.

Consumers respond differently to external nutrient changes than producers, resulting in a mismatch in elemental composition between them and potentially having a significant impact on their interactions. To explore the responses of herbivores and omnivores to changes in elemental composition in producers, we develop a novel stoichiometric model with an intraguild predation structure. The model is validated using experimental data, and the results show that our model can well capture the growth dynamics of these three species. Theoretical and numerical analyses reveal that the model exhibits complex dynamics, including chaotic-like oscillations and multiple types of bifurcations, and undergoes long transients and regime shifts. Under moderate light intensity and phosphate concentration, these three species can coexist. However, when the light intensity is high or the phosphate concentration is low, the energy enrichment paradox occurs, leading to the extinction of ciliate and Daphnia. Furthermore, if phosphate is sufficient, the competitive effect of ciliate and Daphnia on algae will be dominant, leading to competitive exclusion. Notably, when the phosphorus-to-carbon ratio of ciliate is in a suitable range, the energy enrichment paradox can be avoided, thus promoting the coexistence of species. These findings contribute to a deeper understanding of species coexistence and biodiversity.

All-you-can-eat buffet: A spider-specialized bat species (Myotis emarginatus) turns into a pest fly eater around cattle.

Determining the dietary spectrum of European insectivorous bats over time is the cornerstone of their conservation, as it will aid our understanding of foraging behavior plasticity in response to plummeting insect populations. Despite the global decline in insects, a restricted number of arthropod pest species thrive. Yet past research has overlooked the potential of European bats to suppress pests harmful to woodlands or livestock, in spite of their economic relevance. Here we investigated the diet composition, its breeding season variations and pest consumption of an insectivorous bat species (Myotis emarginatus), at the northern edge of its range (Wallonia, Belgium). We also explored the prey ecology to gain insight into the hunting strategies and foraging habitats of this bat species. We used DNA metabarcoding to amplify two COI markers within 195 bat droppings collected in June, July and August, thereby identifying 512 prey taxa predominated by Diptera, Araneae and Lepidoptera. Overall, in 97% of the samples we detected at least one of the 58 potential pest taxa, 41 of which targeting trees. The June samples were marked by a diet rich in orb-weaver spiders, in accordance with the archetypal diet of M. emarginatus bats. However, during the highly energy demanding July-August parturition and lactation period, roughly 55% of the dropping samples contained two cattle fly pests (Stomoxys calcitrans and Musca domestica). Moreover, among the 88 Diptera species preyed upon by M. emarginatus in July and August, these flies accounted for around 50% of the taxa occurrences. This plasticity-the switch from a spider-rich to a fly-rich diet-seems providential considering the dramatic ongoing drop in insect populations but this involves ensuring bat-friendly cattle farming. Our results revealed that bats widely consume pest entomofauna, thereby highlighting their potential role as allies of forest managers and farmers.

Biomechanics of biting in loggerhead shrikes: jaw-closing force, velocity and an argument for power.

Differences in the physical and behavioral attributes of prey are likely to impose disparate demands of force and speed on the jaws of a predator. Because of biomechanical trade-offs between force and speed, this presents an interesting conundrum for predators of diverse prey types. Loggerhead shrikes (Lanius ludovicianus) are medium-sized (∼50 g) passeriform birds that dispatch and feed on a variety of arthropod and vertebrate prey, primarily using their beaks. We used high-speed video of shrikes biting a force transducer in lateral view to obtain corresponding measurements of bite force, upper and lower bill linear and angular displacements, and velocities. Our results show that upper bill depression (about the craniofacial hinge) is more highly correlated with bite force, whereas lower bill elevation is more highly correlated with jaw-closing velocity. These results suggest that the upper and lower jaws might play different roles for generating force and speed (respectively) in these and perhaps other birds as well. We hypothesize that a division of labor between the jaws may allow shrikes to capitalize on elements of force and speed without compromising performance. As expected on theoretical grounds, bite force trades-off against jaw-closing velocity during the act of biting, although peak bite force and jaw-closing velocity across individual shrikes show no clear signs of a force-velocity trade-off. As a result, shrikes appear to bite with jaw-closing velocities and forces that maximize biting power, which may be selectively advantageous for predators of diverse prey that require both jaw-closing force and speed.

The low survival rate of European hare leverets in arable farmland: evidence from the predation experiment.

The low survival rate of leverets may significantly contribute to steep population declines and slow recovery of European hares (Lepus europaeus). However, the leveret survival rate in farmlands with different landscape structures is poorly understood, and the existing evidence comes mainly from Western Europe. In this study, we explored the survival of leveret hare dummies along linear semi-natural habitats in homogeneous Central European arable farmland during the main part of the European hare reproduction period (March-April) in 2019 and 2020. The survival rate of hare leverets during the 14-day period was only 22.2%, and all predation events were recorded during the first six days of the experiment. Mammalian predators were responsible for 53.1% of predation events, avian predators for 40.8%, and agricultural operations for 6.1%. The red fox (Vulpes vulpes) was the dominant predator in our study area and was the primary cause of leveret dummy mortality (32.7%), but it also had the highest use-intensity and visit frequency of all of the study plots. Predation by avian predators was associated with patches of lower vegetation height and cover (such as plowed fields) and during daylight hours, whereas the opposite was true for mammalian predators. We propose that improving the habitat quality of arable landscapes by increasing the proportion and quality of extensively used non-farmed habitats (e.g., set-asides, wildflower areas, extensive meadows, fallow land, and semi-natural habitats on arable land) providing cover and shelter for leverets could be an effective management measure for reducing predation risk on leverets.

Selfish herd effects in aggregated caterpillars and their interaction with warning signals.

Larval Lepidoptera gain survival advantages by aggregating, especially when combined with aposematic warning signals, yet reductions in predation risk may not be experienced equally across all group members. Hamilton's selfish herd theory predicts that larvae that surround themselves with their group mates should be at lower risk of predation, and those on the periphery of aggregations experience the greatest risk, yet this has rarely been tested. Here, we expose aggregations of artificial 'caterpillar' targets to predation from free-flying, wild birds to test for marginal predation when all prey are equally accessible and for an interaction between warning coloration and marginal predation. We find that targets nearer the centre of the aggregation survived better than peripheral targets and nearby targets isolated from the group. However, there was no difference in survival between peripheral and isolated targets. We also find that grouped targets survived better than isolated targets when both are aposematic, but not when they are non-signalling. To our knowledge, our data provide the first evidence to suggest that avian predators preferentially target peripheral larvae from aggregations and that prey warning signals enhance predator avoidance of groups.

Fear of the human 'super predator' in native marsupials and introduced deer in Australia.

Recent experiments have demonstrated that carnivores and ungulates in Africa, Asia, Europe and North America fear the human 'super predator' far more than other predators. Australian mammals have been a focus of research on predator naiveté because it is suspected they show atypical antipredator responses. To experimentally test if mammals in Australia also most fear humans, we quantified the responses of four native marsupials (eastern grey kangaroo, Bennett's wallaby, Tasmanian pademelon, common brushtail possum) and introduced fallow deer to playbacks of predator (human, dog, Tasmanian devil, wolf) or non-predator control (sheep) vocalizations. Native marsupials most feared the human 'super predator', fleeing humans 2.4 times more often than the next most frightening predator (dogs), and being most, and significantly, vigilant to humans. These results demonstrate that native marsupials are not naïve to the peril humans pose, substantially expanding the taxonomic and geographic scope of the growing experimental evidence that wildlife worldwide generally perceive humans as the planet's most frightening predator. Introduced fallow deer fled humans, but not more than other predators, which we suggest may result from their being introduced. Our results point to both challenges concerning marsupial conservation and opportunities for exploiting fear of humans as a wildlife management tool.

Prey can detect predators via electroreception in air.

Predators and prey benefit from detecting sensory cues of each other's presence. As they move through their environment, terrestrial animals accumulate electrostatic charge. Because electric charges exert forces at a distance, a prey animal could conceivably sense electrical forces to detect an approaching predator. Here, we report such a case of a terrestrial animal detecting its predators by electroreception. We show that predatory wasps are charged, thus emit electric fields, and that caterpillars respond to such fields with defensive behaviors. Furthermore, the mechanosensory setae of caterpillars are deflected by these electrostatic forces and are tuned to the wingbeat frequency of their insect predators. This ability unveils a dimension of the sensory interactions between prey and predators and is likely widespread among terrestrial animals.

In vitro evaluation of the potential of mites of the family Macrochelidae (Acari: Mesostigmata) as macrobiological agents against the nematode Haemonchus contortus (Strongylida: Trichostrongylidae).

Small ruminants (sheep and goats) constantly suffer from endoparasitoses caused by gastrointestinal nematodes. Among these, the species Haemonchus contortus (Rudolphi, 1803) is considered to be the one of greatest importance within sheep farming. This nematode is difficult to control due to its resistance to most commercial anthelmintics. The aim of the present study was to assess the potential of macrochelid mites as macrobiological agents for controlling endoparasitoses of sheep caused by the nematode, H. contortus. For this, novel in vitro methodology was used, in which assessments were made not only of the predatory ability but also the population growth of mite species (Macrocheles merdarius, Macrocheles robustulus and Holostaspella bifoliata) when offered larvae of the nematode, H. contortus. The predatory ability of the mites, M. merdarius and H. bifoliata were efficient regarding their predatory ability against H. contortus nematode larvae. The mite, M. merdarius exhibited the highest predation rate with mean distribution values for the treated group of 18656 ± 10091 and for the control group of 1178 ± 712 (P < 0.0001). The species, H. bifoliata presented the highest population growth rate, with a percentage acarid recovery rate of 263% in relation to the number added initially. The data from this in vitro predation experiment suggest that, M. merdarius and H. bifoliata showed promise as macrobiological agents for controlling gastrointestinal endoparasitoses of sheep caused by the nematode, H. contortus given that both species reduced the population of this helminth by more 70% and the number of mites recovered was three times greater than the number added.

A systematic review and meta-analysis of unimodal and multimodal predation risk assessment in birds.

Despite a wealth of studies documenting prey responses to perceived predation risk, researchers have only recently begun to consider how prey integrate information from multiple cues in their assessment of risk. We conduct a systematic review and meta-analysis of studies that experimentally manipulated perceived predation risk in birds and evaluate support for three alternative models of cue integration: redundancy/equivalence, enhancement, and antagonism. One key insight from our analysis is that the current theory, generally applied to study cue integration in animals, is incomplete. These theories specify the effects of increasing information level on mean, but not variance, in responses. In contrast, we show that providing multiple complementary cues of predation risk simultaneously does not affect mean response. Instead, as information richness increases, populations appear to assess risk more accurately, resulting in lower among-population variance in response to manipulations of perceived predation risk. We show that this may arise via a statistical process called maximum-likelihood estimation (MLE) integration. Our meta-analysis illustrates how explicit consideration of variance in responses can yield important biological insights.

Tiger beetles produce anti-bat ultrasound and are probable Batesian moth mimics.

Echolocating bats and their eared insect prey are in an acoustic evolutionary war. Moths produce anti-bat sounds that startle bat predators, signal noxiousness, mimic unpalatable models and jam bat sonar. Tiger beetles (Cicindelidae) also purportedly produce ultrasound in response to bat attacks. Here we tested 19 tiger beetle species from seven genera and showed that they produce anti-bat signals to playback of authentic bat echolocation. The dominant frequency of beetle sounds substantially overlaps the sonar calls of sympatric bats. As tiger beetles are known to produce defensive chemicals such as benzaldehyde and hydrogen cyanide, we hypothesized that tiger beetle sounds are acoustically advertising their unpalatability. We presented captive big brown bats (Eptesicus fuscus) with seven different tiger beetle species and found that 90 out of 94 beetles were completely consumed, indicating that these tiger beetle species are not aposematically signalling. Instead, we show that the primary temporal and spectral characteristics of beetle warning sounds overlap with sympatric unpalatable tiger moth (Arctinae) sounds and that tiger beetles are probably Batesian mimics of noxious moth models. We predict that many insect taxa produce anti-bat sounds and that the acoustic mimicry rings of the night sky are hyperdiverse.

Feral frogs, native newts, and chemical cues: identifying threats from and management opportunities for invasive African Clawed Frogs in Washington state.

Invasive species threaten biodiversity globally. Amphibians are one of the most threatened vertebrate taxa and are particularly sensitive to invasive species, including other amphibians. African clawed frogs (Xenopus laevis) are native to Southern Africa but have subsequently become invasive on multiple continents-including multiple parts of North America-due to releases from the pet and biomedical trades. Despite their prevalence as a global invader, the impact of X. laevis remains understudied. This includes the Pacific Northwest of the USA, which now hosts multiple expanding X. laevis populations. For many amphibians, chemical cues communicate important information, including the presence of predators. Here, we tested the role chemical cues may play in mediating interactions between feral X. laevis and native amphibians in the Pacific Northwest. We tested whether native red-legged frog (Rana aurora) tadpoles display an antipredator response to non-native frog (X. laevis) or native newt (rough-skinned newts, Taricha granulosa) predator chemical stimuli. We found that R. aurora tadpoles exhibited pronounced anti-predator responses when exposed to chemical cues from T. granulosa but did not display anti-predator response to invasive X. laevis chemical cues. We also began experimentally testing whether T. granulosa-which produce a powerful neurotoxin tetrodotoxin (TTX)-may elicit an anti-predator response in X. laevis, that could serve to deter co-occupation. However, our short-duration experiments found that X. laevis were attracted to newt chemical stimuli rather than deterred. Our findings show that X. laevis likely poses a threat to native amphibians, and that these native species may also be particularly vulnerable to this invasive predator, compared to native predators, because toxic native newts may not limit X. laevis invasions. Our research provides some of the first indications that native Pacific Northwest species may be threatened by feral X. laevis and provides a foundation for future experiments testing potential management techniques for X. laevis.

Automated escape system: identifying prey's kinematic and behavioral features critical for predator evasion.

Identifying the kinematic and behavioral variables of prey that influence evasion from predator attacks remains challenging. To address this challenge, we have developed an automated escape system that responds quickly to an approaching predator and pulls the prey away from the predator rapidly, similar to real prey. Reaction distance, response latency, escape speed and other variables can be adjusted in the system. By repeatedly measuring the response latency and escape speed of the system, we demonstrated the system's ability to exhibit fast and rapid responses while maintaining consistency across successive trials. Using the live predatory fish species Coreoperca kawamebari, we show that escape speed and reaction distance significantly affect the outcome of predator-prey interactions. These findings indicate that the developed escape system is useful for identifying kinematic and behavioral features of prey that are critical for predator evasion, as well as for measuring the performance of predators.

Modeling a hot, dry future: Substantial range reductions in suitable environment projected under climate change for a semiarid riparian predator guild.

An understanding of species-environmental relationships is invaluable for effective conservation and management under anthropogenic climate change, especially for biodiversity hotspots such as riparian habitats. Species distribution models (SDMs) assess present species-environmental relationships which can project potential suitable environments through space and time. An understanding of environmental factors associated with distributions can guide conservation management strategies under a changing climate. We generated 260 ensemble SDMs for five species of Thamnophis gartersnakes (n = 347)-an important riparian predator guild-in a semiarid and biogeographically diverse region under impact from climate change (Arizona, United States). We modeled present species-environmental relationships and projected changes to suitable environment under 12 future climate scenarios per species, including the most and least optimistic greenhouse gas emission pathways, through 2100. We found that Thamnophis likely advanced northward since the turn of the 20th century and overwinter temperature and seasonal precipitation best explained present distributions. Future ranges of suitable environment for Thamnophis are projected to decrease by ca. -37.1% on average. We found that species already threatened with extinction or those with warm trailing-edge populations likely face the greatest loss of suitable environment, including near or complete loss of suitable environment. Future climate scenarios suggest an upward advance of suitable environment around montane areas for some low to mid-elevation species, which may create pressures to ascend. The most suitable environmental areas projected here can be used to identify potential safe zones to prioritize conservation refuges, including applicable critical habitat designations. By bounding the climate pathway extremes to, we reduce SDM uncertainties and provide valuable information to help conservation practitioners mitigate climate-induced threats to species. Implementing informed conservation actions is paramount for sustaining biodiversity in important aridland riparian systems as the climate warms and dries.

Sublethal effects of a commercial Bt product and Bt cotton flowers on the bollworm (Helicoverpa zea) with impacts to predation from a lady beetle (Hippodamia convergens).

Insecticidal Bacillus thuringiensis Berliner (Bt) toxins produced by transgenic cotton (Gossypium hirsutum L.) plants have become an essential component of cotton pest management. Bt toxins are the primary management tool in transgenic cotton for lepidopteran pests, the most important of which is the bollworm (Helicoverpa zea Boddie) (Lepidoptera: Noctuidae) in the United States (U.S.). However, bollworm larvae that survive after consuming Bt toxins may experience sublethal effects, which could alter interactions with other organisms, such as natural enemies. Experiments were conducted to evaluate how sublethal effects of a commercial Bt product (Dipel) incorporated into artificial diet and from Bt cotton flowers impact predation from the convergent lady beetle (Hippodamia convergens Guérin-Méneville) (Coleoptera: Coccinellidae), common in cotton fields of the mid-southern U.S. Sublethal effects were detected through reduced weight and slower development in bollworm larvae which fed on Dipel incorporated into artificial diet, Bollgard II, and Bollgard 3 cotton flowers. Sublethal effects from proteins incorporated into artificial diet were found to significantly alter predation from third instar lady beetle larvae. Predation of bollworm larvae also increased significantly after feeding for three days on a diet incorporated with Bt proteins. These results suggest that the changes in larval weight and development induced by Bt can be used to help predict consumption of bollworm larvae by the convergent lady beetle. These findings are essential to understanding the potential level of biological control in Bt cotton where lepidopteran larvae experience sublethal effects.

Predation cues induce predator specific changes in olfactory neurons encoding defensive responses in agile frog tadpoles.

Although behavioural defensive responses have been recorded several times in both laboratory and natural habitats, their neural mechanisms have seldom been investigated. To explore how chemical, water-borne cues are conveyed to the forebrain and instruct behavioural responses in anuran larvae, we conditioned newly hatched agile frog tadpoles using predator olfactory cues, specifically either native odonate larvae or alien crayfish kairomones. We expected chronic treatments to influence the basal neuronal activity of the tadpoles' mitral cells and alter their sensory neuronal connections, thereby impacting information processing. Subsequently, these neurons were acutely perfused, and their responses were compared with the defensive behaviour of tadpoles previously conditioned and exposed to the same cues. Tadpoles conditioned with odonate cues differed in both passive and active cell properties compared to those exposed to water (controls) or crayfish cues. The observed upregulation of membrane conductance and increase in both the number of active synapses and receptor density at the postsynaptic site are believed to have enhanced their responsiveness to external stimuli. Odonate cues also affected the resting membrane potential and firing rate of mitral cells during electrophysiological patch-clamp recordings, suggesting a rearrangement of the repertoire of voltage-dependent conductances expressed in cell membranes. These recorded neural changes may modulate the induction of an action potential and transmission of information. Furthermore, the recording of neural activity indicated that the lack of defensive responses towards non-native predators is due to the non-recognition of their olfactory cues.

Behavior and morphology combine to influence energy dissipation in mantis shrimp (Stomatopoda).

Animals deliver and withstand physical impacts in diverse behavioral contexts, from competing rams clashing their antlers together to archerfish impacting prey with jets of water. Though the ability of animals to withstand impact has generally been studied by focusing on morphology, behaviors may also influence impact resistance. Mantis shrimp exchange high-force strikes on each other's coiled, armored telsons (tailplates) during contests over territory. Prior work has shown that telson morphology has high impact resistance. I hypothesized that the behavior of coiling the telson also contributes to impact energy dissipation. By measuring impact dynamics from high-speed videos of strikes exchanged during contests between freely moving animals, I found that approximately 20% more impact energy was dissipated by the telson as compared with findings from a prior study that focused solely on morphology. This increase is likely due to behavior: because the telson is lifted off the substrate, the entire body flexes after contact, dissipating more energy than exoskeletal morphology does on its own. While variation in the degree of telson coil did not affect energy dissipation, proportionally more energy was dissipated from higher velocity strikes and from strikes from more massive appendages. Overall, these findings show that analysis of both behavior and morphology is crucial to understanding impact resistance, and suggest future research on the evolution of structure and function under the selective pressure of biological impacts.

Heuristic test reveals little effect of learning and maturation on early prey capture experiences in a web-building spider.

Behaviors can vary throughout an animal's life and this variation can often be explained by changes associated with learning and/or maturing. Currently, there is little consensus regarding how these processes interact to affect behaviors. Here we proposed a heuristic approach to disentangle the effects of learning and maturation on behavior and applied it to the predatory behaviors of Physocyclus globosus spiderlings. We varied the degree of prey difficulty and familiarity spiderlings received along the first instar and across the molt to the second instar and quantified the time spiderlings spent wrapping prey, as a proxy for prey capture efficiency. We found no overall evidence for learning or maturation. Changes in efficiency were mainly due to the switch from difficult to easy prey, or vice versa. However, there was one treatment where spiderlings improved in efficiency before and after the molt, without a switch in prey type. This provides some indication that difficult prey may offer more opportunity for learning or maturation to impact behavior. Although we found little effect of learning or maturation on prey capture efficiency, we suggest that our heuristic approach is effective and could be useful in investigating these processes in other behaviors and other animals.