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.

Breakdown of clonal cooperative architecture in multispecies biofilms and the spatial ecology of predation.

Biofilm formation, including adherence to surfaces and secretion of extracellular matrix, is common in the microbial world, but we often do not know how interaction at the cellular spatial scale translates to higher-order biofilm community ecology. Here we explore an especially understudied element of biofilm ecology, namely predation by the bacterium Bdellovibrio bacteriovorus. This predator can kill and consume many different Gram-negative bacteria, including Vibrio cholerae and Escherichia coli. V. cholerae can protect itself from predation within densely packed biofilm structures that it creates, whereas E. coli biofilms are highly susceptible to B. bacteriovorus. We explore how predator-prey dynamics change when V. cholerae and E. coli are growing in biofilms together. We find that in dual-species prey biofilms, E. coli survival under B. bacteriovorus predation increases, whereas V. cholerae survival decreases. E. coli benefits from predator protection when it becomes embedded within expanding groups of highly packed V. cholerae. But we also find that the ordered, highly packed, and clonal biofilm structure of V. cholerae can be disrupted if V. cholerae cells are directly adjacent to E. coli cells at the start of biofilm growth. When this occurs, the two species become intermixed, and the resulting disordered cell groups do not block predator entry. Because biofilm cell group structure depends on initial cell distributions at the start of prey biofilm growth, the surface colonization dynamics have a dramatic impact on the eventual multispecies biofilm architecture, which in turn determines to what extent both species survive exposure to B. bacteriovorus.

Recovery of a marine keystone predator transforms terrestrial predator-prey dynamics.

Sea otters (Enhydra lutris) and wolves (Canis lupus) are two apex predators with strong and cascading effects on ecosystem structure and function. After decades of recovery from near extirpation, their ranges now overlap, allowing sea otters and wolves to interact for the first time in the scientific record. We intensively studied wolves during 2015 to 2021 in an island system colonized by sea otters in the 2000s and by wolves in 2013. After wolf colonization, we quantified shifts in foraging behavior with DNA metabarcoding of 689 wolf scats and stable isotope analyses, both revealing a dietary switch from Sitka black-tailed deer (Odocoileus hemionus), the terrestrial in situ primary prey, to sea otters. Here we show an unexpected result of the reintroduction and restoration of sea otters, which became an abundant marine subsidy for wolves following population recovery. The availability of sea otters allowed wolves to persist and continue to reproduce, subsequently nearly eliminating deer. Genotypes from 390 wolf scats and telemetry data from 13 wolves confirmed island fidelity constituting one of the highest known wolf population densities and upending standardly accepted wolf density predictions based on ungulate abundance. Whereas marine subsidies in other systems are generally derived from lower trophic levels, here an apex nearshore predator became a key prey species and linked nearshore and terrestrial food webs in a recently deglaciated and rapidly changing ecosystem. These results underscore that species restoration may serve as an unanticipated nutrient pathway for recipient ecosystems even resulting in cross-boundary subsidy cascades.

Evaluating evasion strategies in zebrafish larvae.

An effective evasion strategy allows prey to survive encounters with predators. Prey are generally thought to escape in a direction that is either random or serves to maximize the minimum distance from the predator. Here, we introduce a comprehensive approach to determine the most likely evasion strategy among multiple hypotheses and the role of biomechanical constraints on the escape response of prey fish. Through a consideration of six strategies with sensorimotor noise and previous kinematic measurements, our analysis shows that zebrafish larvae generally escape in a direction orthogonal to the predator's heading. By sensing only the predator's heading, this orthogonal strategy maximizes the distance from fast-moving predators, and, when operating within the biomechanical constraints of the escape response, it provides the best predictions of prey behavior among all alternatives. This work demonstrates a framework for resolving the strategic basis of evasion in predator-prey interactions, which could be applied to a broad diversity of animals.

Prey Shifts Drive Venom Evolution in Cone Snails.

Venom systems are complex traits that have independently emerged multiple times in diverse plant and animal phyla. Within each venomous lineage there typically exists interspecific variation in venom composition where several factors have been proposed as drivers of variation, including phylogeny and diet. Understanding these factors is of broad biological interest and has implications for the development of antivenom therapies and venom-based drug discovery. Because of their high species richness and the presence of several major evolutionary prey shifts, venomous marine cone snails (genus Conus) provide an ideal system to investigate drivers of interspecific venom variation. Here, by analyzing the venom gland expression profiles of ∼3,000 toxin genes from 42 species of cone snail, we elucidate the role of prey-specific selection pressures in shaping venom variation. By analyzing overall venom composition and individual toxin structures, we demonstrate that the shifts from vermivory to piscivory in Conus are complemented by distinct changes in venom composition independent of phylogeny. In vivo injections of venom from piscivorous cone snails in fish further showed a higher potency compared with venom of nonpiscivores demonstrating a selective advantage. Together, our findings provide compelling evidence for the role of prey shifts in directing the venom composition of cone snails and expand our understanding of the mechanisms of venom variation and diversification.

Structured foraging of soil predators unveils functional responses to bacterial defenses.

Predators and their foraging strategies often determine ecosystem structure and function. Yet, the role of protozoan predators in microbial soil ecosystems remains elusive despite the importance of these ecosystems to global biogeochemical cycles. In particular, amoebae-the most abundant soil protozoan predator of bacteria-remineralize soil nutrients and shape the bacterial community. However, their foraging strategies and their role as microbial ecosystem engineers remain unknown. Here, we present a multiscale approach, connecting microscopic single-cell analysis and macroscopic whole ecosystem dynamics, to expose a phylogenetically widespread foraging strategy, in which an amoeba population spontaneously partitions between cells with fast, polarized movement and cells with slow, unpolarized movement. Such differentiated motion gives rise to efficient colony expansion and consumption of the bacterial substrate. From these insights, we construct a theoretical model that predicts how disturbances to amoeba growth rate and movement disrupt their predation efficiency. These disturbances correspond to distinct classes of bacterial defenses, which allows us to experimentally validate our predictions. All considered, our characterization of amoeba foraging identifies amoeba mobility, and not amoeba growth, as the core determinant of predation efficiency and a key target for bacterial defense systems.

Sustainable pest control inspired by prey-predator ultrasound interactions.

Nocturnal moths evolved ultrasound-triggered escape maneuvers for avoiding predatory bats emitting ultrasonic echolocation calls. Using ultrasound for pest control is not a novel concept, but the technique has not been systemized because of the moths' habituation to sounds and the narrow directionality of conventional ultrasound speakers. Here, we report the use of pulsed ultrasonic white noise, which contributes to achieving ecologically concordant plant protection. An ultrasonic pulse, which is temporal mimicry of the search-phase pulse in the echolocation calls of a sympatric bat, was identified using neuroethological screening of eared moth-repelling ultrasounds; these pulses elicit flight-stopping reactions in moths but have no or little auditory adaptation. Such repellent ultrasounds broadcast from the cylindrical omni-azimuth ultrasound emitters suppressed the intrusion of gravid females of pest moths into cultivation fields. Thus, egg numbers and plant damage by hatched larvae were drastically reduced, enabling farmers to substantially skip applications of chemical insecticides for controlling moth pests.

Long-term, climate-driven phenological shift in a tropical large carnivore.

Understanding the degree to which animals are shifting their phenology to track optimal conditions as the climate changes is essential to predicting ecological responses to global change. Species at low latitudes or high trophic levels are theoretically expected to exhibit weaker phenological responses than other species, but limited research on tropical systems or on top predators impedes insight into the contexts in which these predictions are upheld. Moreover, a lack of phenological studies on top predators limits understanding of how climate change impacts propagate through entire ecosystems. Using a 30-y dataset on endangered African wild dogs (Lycaon pictus), we examined changes in reproductive phenology and temperatures during birthing and denning over time, as well as potential fitness consequences of these changes. We hypothesized that their phenology would shift to track a stable thermal range over time. Data from 60 packs and 141 unique pack-years revealed that wild dogs have delayed parturition by 7 days per decade on average in response to long-term warming. This shift has led to temperatures on birthing dates remaining relatively stable but, contrary to expectation, has led to increased temperatures during denning periods. Increased denning temperatures were associated with reduced reproductive success, suggesting that a continued phenological shift in the species may become maladaptive. Such results indicate that climate-driven shifts could be more widespread in upper trophic levels than previously appreciated, and they extend theoretical understanding of the species traits and environmental contexts in which large phenological shifts can be expected to occur as the climate changes.

Fear of predators in free-living wildlife reduces population growth over generations.

Correctly assessing the total impact of predators on prey population growth rates (lambda, λ) is critical to comprehending the importance of predators in species conservation and wildlife management. Experiments over the past decade have demonstrated that the fear (antipredator responses) predators inspire can affect prey fecundity and early offspring survival in free-living wildlife, but recent reviews have highlighted the absence of evidence experimentally linking such effects to significant impacts on prey population growth. We experimentally manipulated fear in free-living wild songbird populations over three annual breeding seasons by intermittently broadcasting playbacks of either predator or nonpredator vocalizations and comprehensively quantified the effects on all the components of population growth, together with evidence of a transgenerational impact on offspring survival as adults. Fear itself significantly reduced the population growth rate (predator playback mean λ = 0.91, 95% CI = 0.80 to 1.04; nonpredator mean λ = 1.06, 95% CI = 0.96 to 1.16) by causing cumulative, compounding adverse effects on fecundity and every component of offspring survival, resulting in predator playback parents producing 53% fewer recruits to the adult breeding population. Fear itself was consequently projected to halve the population size in just 5 years, or just 4 years when the evidence of a transgenerational impact was additionally considered (λ = 0.85). Our results not only demonstrate that fear itself can significantly impact prey population growth rates in free-living wildlife, comparing them with those from hundreds of predator manipulation experiments indicates that fear may constitute a very considerable part of the total impact of predators.

Differences in alternative splicing events in the adaptive strategies of two Daphnia galeata genotypes induced by fish kairomones.

BACKGROUND: Daphnia galeata is a suitable model organism for investigating predator-induced defense. Genes and pathways exhibiting differential expression between fish kairomone-treated and untreated groups in D. galeata have been identified. However, understanding of the significance of alternative splicing, a crucial process of the regulation of gene expression in eukaryotes, to this mechanism remains limited. This study measured life-history traits and conducted short-read RNA sequencing and long-read isoform sequencing of two Korean D. galeata genotypes (KB1 and KE2) to uncover the genetic mechanism underlying their phenotypic plasticity under predation stress. RESULTS: KB1 exhibited strategies to enhance fertility and decrease body length when exposed to fish kairomones, while KE2 deployed an adaptive strategy to increase body length. Full-length transcriptomes from KB1 and KE2 yielded 65,736 and 57,437 transcripts, respectively, of which 32 differentially expressed transcripts (DETs) were shared under predation stress across both genotypes. Prominent DETs common to both genotypes were related to energy metabolism and the immune system. Additionally, differential alternative splicing (DAS) events were detected in both genotypes in response to fish kairomones. DAS genes shared between both genotypes may indicate their significant role in the post-transcriptional stress response to fish predation. Calpain-3, involved in digestion and nutrient absorption, was identified as a DAS gene in both genotypes when exposed to fish kairomones. In addition, the gene encoding thymosin beta, which is related to growth, was found to be a statistically significant DAS only in KB1, while that encoding ultraspiracle protein, also associated with growth, was only identified in KE2. Moreover, transcripts encoding proteins such as EGF-like domain-containing protein, vitellogenin fused with superoxide dismutase, and others were identified overlapping between DAS events and DETs and potentially elucidating their association with the observed phenotypic variation in each genotype. CONCLUSIONS: Our findings highlight the crucial role of alternative splicing in modulating transcriptome landscape under predation stress in D. galeata, emphasizing the requirement for integrating gene expression and splicing analyses in evolutionary adaptation studies.

Noise pollution alters the diet composition of invertebrate consumers both in and beyond a noise-exposed grassland ecosystem.

Anthropogenic noise is ubiquitous globally. However, we know little about how the impacts of noise alter fundamental ecosystem properties, such as resource consumption by invertebrate consumers. Using experimental noise manipulation and faecal DNA metabarcoding, we assessed how the direct and cross-trophic indirect effects of noise altered the dietary richness and specializations of omnivorous grasshoppers in a grassland ecosystem. We found that the experimental noise treatment expanded grasshoppers' dietary richness and resulted in dietary generalizations in both noise-exposed and adjacent relatively quieter areas. Unexpectedly, however, these dietary changes were primarily explained by the direct effect of noise not only in the noise-exposed areas but also in the adjacent quieter areas and were relaxed by indirect effects of noise such as reduced birds and predation risk and increased grasshoppers. Our work suggests that noise pollution can be key in explaining the variation of invertebrate consumers' diets across a gradient of noise-exposed environments.

Non-random sampling measures the occurrence but not the strength of a textbook trophic cascade.

Although sampling the five tallest young aspen in a stand is useful for detecting the occurrence of any aspen recruitment, this technique overestimates the population response of aspen to wolf reintroduction. Our original conclusion that random sampling described a trophic cascade that was weaker than the one described by non-random sampling is unchanged.

Mean reef fish body size decreases towards warmer waters.

Aquatic ectotherms often attain smaller body sizes at higher temperatures. By analysing ~15,000 coastal-reef fish surveys across a 15°C spatial sea surface temperature (SST) gradient, we found that the mean length of fish in communities decreased by ~5% for each 1°C temperature increase across space, or 50% decrease in mean length from 14 to 29°C mean annual SST. Community mean body size change was driven by differential temperature responses within trophic groups and temperature-driven change in their relative abundance. Herbivores, invertivores and planktivores became smaller on average in warmer temperatures, but no trend was found in piscivores. Nearly 25% of the temperature-related community mean size trend was attributable to trophic composition at the warmest sites, but at colder temperatures, this was <1% due to trophic groups being similarly sized. Our findings suggest that small changes in temperature are associated with large changes in fish community composition and body sizes, with important ecological implications.

Body size and trophic position determine the outcomes of species invasions along temperature and productivity gradients.

Species invasions are predicted to increase in frequency with global change, but quantitative predictions of how environmental filters and species traits influence the success and consequences of invasions for local communities are lacking. Here we investigate how invaders alter the structure, diversity and stability regime of simple communities across environmental gradients (habitat productivity, temperature) and community size structure. We simulate all three-species trophic modules (apparent and exploitative competition, trophic chain and intraguild predation). We predict that invasions most often succeed in warm and productive habitats and that successful invaders include smaller competitors, intraguild predators and comparatively small top predators. This suggests that species invasions and global change may facilitate the downsizing of food webs. Furthermore, we show that successful invasions leading to species substitutions rarely alter system stability, while invasions leading to increased diversity can destabilize or stabilize community dynamics depending on the environmental conditions and invader's trophic position.

Tree diversity enhances predation by birds but not by arthropods across climate gradients.

Tree diversity can promote both predator abundance and diversity. However, whether this translates into increased predation and top-down control of herbivores across predator taxonomic groups and contrasting environmental conditions remains unresolved. We used a global network of tree diversity experiments (TreeDivNet) spread across three continents and three biomes to test the effects of tree species richness on predation across varying climatic conditions of temperature and precipitation. We recorded bird and arthropod predation attempts on plasticine caterpillars in monocultures and tree species mixtures. Both tree species richness and temperature increased predation by birds but not by arthropods. Furthermore, the effects of tree species richness on predation were consistent across the studied climatic gradient. Our findings provide evidence that tree diversity strengthens top-down control of insect herbivores by birds, underscoring the need to implement conservation strategies that safeguard tree diversity to sustain ecosystem services provided by natural enemies in forests.

Predator-driven behavioural shifts in a common lizard shape resource-flow from marine to terrestrial ecosystems.

Foraging decisions shape the structure of food webs. Therefore, a behavioural shift in a single species can potentially modify resource-flow dynamics of entire ecosystems. To examine this, we conducted a field experiment to assess foraging niche dynamics of semi-arboreal brown anole lizards in the presence/absence of predatory ground-dwelling curly-tailed lizards in a replicated set of island ecosystems. One year after experimental translocation, brown anoles exposed to these predators had drastically increased perch height and reduced consumption of marine-derived food resources. This foraging niche shift altered marine-to-terrestrial resource-flow dynamics and persisted in the diets of the first-generation offspring. Furthermore, female lizards that displayed more risk-taking behaviours consumed more marine prey on islands with predators present. Our results show how predator-driven rapid behavioural shifts can alter food-web connectivity between oceanic and terrestrial ecosystems and underscore the importance of studying behaviour-mediated niche shifts to understand ecosystem functioning in rapidly changing environments.

Food web context modifies predator foraging and weakens trophic interaction strength.

Trophic interaction modifications (TIM) are widespread in natural systems and occur when a third species indirectly alters the strength of a trophic interaction. Past studies have focused on documenting the existence and magnitude of TIMs; however, the underlying processes and long-term consequences remain elusive. To address this gap, we experimentally quantified the density-dependent effect of a third species on a predator's functional response. We conducted short-term experiments with ciliate communities composed of a predator, prey and non-consumable 'modifier' species. In both communities, increasing modifier density weakened the trophic interaction strength, due to a negative effect on the predator's space clearance rate. Simulated long-term dynamics indicate quantitative differences between models that account for TIMs or include only pairwise interactions. Our study demonstrates that TIMs are important to understand and predict community dynamics and highlights the need to move beyond focal species pairs to understand the consequences of species interactions in communities.

An escape-enhancing circuit involving subthalamic CRH neurons mediates stress-induced anhedonia in mice.

Chronic predator stress (CPS) is an important and ecologically relevant tool for inducing anhedonia in animals, but the neural circuits underlying the associated neurobiological changes remain to be identified. Using cell-type-specific manipulations, we found that corticotropin-releasing hormone (CRH) neurons in the medial subthalamic nucleus (mSTN) enhance struggle behaviors in inescapable situations and lead to anhedonia, predominately through projections to the external globus pallidus (GPe). Recordings of in vivo neuronal activity revealed that CPS distorted mSTN-CRH neuronal responsivity to negative and positive stimuli, which may underlie CPS-induced behavioral despair and anhedonia. Furthermore, we discovered presynaptic inputs from the bed nucleus of the stria terminalis (BNST) to mSTN-CRH neurons projecting to the GPe that were enhanced following CPS, and these inputs may mediate such behaviors. This study identifies a neurocircuitry that co-regulates escape response and anhedonia in response to predator stress. This new understanding of the neural basis of defensive behavior in response to predator stress will likely benefit our understanding of neuropsychiatric diseases.

Comparative Venom Multiomics Reveal the Molecular Mechanisms Driving Adaptation to Diverse Predator-Prey Ecosystems in Closely Related Sea Snakes.

Predator-prey arms races are ideal models for studying the natural selection and adaptive evolution that drive the formation of biological diversity. For venomous snakes, venom is a key bridge linking snakes with their prey, but whether and how venom evolves under the selection of diet remains unclear. Here, we focused on two closely related sea snakes, Hydrophis cyanocinctus and Hydrophis curtus, which show significant differences in prey preferences. Data-independent acquisition (DIA)-based proteomic analysis revealed different degrees of homogeneity in the venom composition of the two snakes, which was consistent with the differential phylogenetic diversity of their prey. By investigating the sequences and structures of three-finger toxins (3FTx), a predominant toxin family in elapid venom, we identified significant differences between the two sea snakes in the binding activity of 3FTx to receptors from different prey populations, which could explain the trophic specialization of H. cyanocinctus. Furthermore, we performed integrated multiomic profiling of the transcriptomes, microRNAs (miRNAs), long noncoding RNAs (lncRNAs), and proteomes of the venom glands; constructed venom-related mRNA-miRNA-lncRNA networks; and identified a series of noncoding RNAs involved in the regulation of toxin gene expression in the two species. These findings are highly informative for elucidating the molecular basis and regulatory mechanisms that account for discrepant venom evolution in response to divergent diets in closely related snakes, providing valuable evidence for the study of coselection and coevolution in predator-prey ecosystems.

Resource Patchiness as a Resolution to the Food Paradox in the Sea.

AbstractAverage concentrations of biota in the ocean are low, presenting a critical problem for ocean consumers. High-resolution sampling, however, demonstrates that the ocean is peppered with narrow hot spots of organism activity. To determine whether these resource aggregations could provide a significant solution to the ocean's food paradox, a conceptual graphical model was developed that facilitates comparisons of the role of patchiness in predator-prey interactions across taxa, size scales, and ecosystems. The model predicts that predators are more reliant on aggregated resources for foraging success when the average concentrations of resources is low, the size discrepancy between predator and prey is great, the predator has a high metabolic rate, and/or the predator's foraging time is limited. Size structure differences between marine and terrestrial food webs and a vast disparity in the overall mean density of their resources lead to the conclusion that high-density aggregations of prey are much more important to the survival of oceanic predators than their terrestrial counterparts, shaping the foraging decisions that are available to an individual and setting the stage on which evolutionary pressures can act. Patches of plenty may be rare, but they play an outsized role in behavioral, ecological, and evolutionary processes, particularly in the sea.