Multi-species mechanistic model of functional response provides new insights into predator-mediated interactions in a vertebrate community

Prey handling processes are considered a key driver of short-term positive indirect effects between prey sharing the same predator. However, a growing body of research indicates that predators are rarely limited by such processes in the wild. Density-dependent changes in predator foraging behavior can also generate positive indirect effects but they are rarely included as explicit functions of prey densities in functional response models. With the aim of untangling proximate drivers of species interactions in natural communities and improve our ability to quantify interaction strength, we extended the Holling multi-species model by including density-dependent changes in predator foraging behavior. Our model, based on species traits and behavior, was inspired by the vertebrate community of the arctic tundra, where the main predator (the arctic fox) is an active forager feeding primarily on cyclic small rodent (lemming) populations and eggs of various tundra-nesting bird species. Short-term positive indirect effects of lemmings on birds have been documented over the circumpolar Arctic but the underlying proximate mechanisms remain poorly known. We used a unique data set, containing high-frequency GPS tracking, accelerometer, behavioral, and experimental data to parameterize the multi-species model, and a 15-year time series of prey densities and bird nesting success to evaluate interaction strength between species. Our results showed that: (i) prey handling processes play a minor role in our system and (ii) density-dependent changes in predator foraging behavior can be the proximate drivers of a predominant predator-mediated interaction observed in the arctic tundra. Mechanisms outlined in our study have been little studied and may play a significant role in natural systems. We hope that our study will provide a useful starting point to build mechanistic models of predation, and we think that our approach could conceivably be applied to a broad range of food webs.

Living in mixed species groups promotes predator learning in degraded habitats

Living in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.

Chemical Cues from Entomopathogenic Nematodes Vary Across Three Species with Different Foraging Strategies, Triggering Different Behavioral Responses in Prey and Competitors

Chemical cues play important roles in predator–prey interactions. Semiochemicals can aid predator foraging and alert prey organisms to the presence of predators. Previous work suggests that predator traits differentially influence prey behavior, however, empirical data on how prey organisms respond to chemical cues from predator species with different hunting strategies, and how foraging predators react to cues from potential competitors, is lacking. Furthermore, most research in this area has focused on aquatic and aboveground terrestrial systems, while interactions among belowground, soiling-dwelling organisms have received relatively little attention. Here, we assessed how chemical cues from three species of entomopathogenic nematodes (EPNs), each with a different foraging strategy, influenced herbivore (cucumber beetle) and natural enemy (EPN) foraging behavior. We predicted these cues could serve as chemical indicators of increased predation risk, prey availability, or competition. Our findings revealed that foraging cucumber beetle larvae avoided chemical cues from Heterorhabditis bacteriophora (active-foraging cruiser EPNs), but not Steinernema carpocapsae (ambusher EPNs) or Steinernema riobrave (intermediate-foraging EPNs). In contrast, foraging H. bacteriophora EPNs were attracted to cues produced by the two Steinernema species but not conspecific cues. Notably, the three EPN species produced distinct blends of olfactory cues, with only a few semi-conserved compounds across species. These results indicate that a belowground insect herbivore responds differently to chemical cues from different EPN species, with some EPN species avoiding prey detection. Moreover, the active-hunting EPNs were attracted to heterospecific cues, suggesting these cues indicate a greater probability of available prey, rather than strong interspecific competition.

Functional response of Harmonia axyridis preying on Acyrthosiphon pisum nymphs: the effect of temperature

In the current study, we investigated the functional response of Harmonia axyridis adults and larvae foraging on Acyrthosiphon pisum nymphs at temperatures between 15 and 35 °C. Logistic regression and Roger’s random predator models were employed to determine the type and parameters of the functional response. Harmonia axyridis larvae and adults exhibited Type II functional responses to A. pisum, and warming increased both the predation activity and host aphid control mortality. Female and 4th instar H. axyridis consumed the most aphids. For fourth instar larvae and female H. axyridis adults, the successful attack rates were 0.23 ± 0.014 h−1 and 0.25 ± 0.015 h−1; the handling times were 0.13 ± 0.005 h and 0.16 ± 0.004 h; and the estimated maximum predation rates were 181.28 ± 14.54 and 153.85 ± 4.06, respectively. These findings accentuate the high performance of 4th instar and female H. axyridis and the role of temperature in their efficiency. Further, we discussed such temperature-driven shifts in predation and prey mortality concerning prey-predator foraging interactions towards biological control.

Acoustically eavesdropping predators take longer to capture prey signalling in aggregation

Prey signalling in aggregation become more conspicuous with increasing numbers and tend to attract more predators. Such grouping may, however, benefit prey by lowering the risk of being captured due to the predator's difficulty in targeting individuals. Previous studies have investigated anti-predatory benefits of prey aggregation using visual predators, but it is unclear whether such benefits are gained in an auditory context. We investigated whether katydids of the genus Mecopoda gain protection from their acoustically eavesdropping bat predator, Megaderma spasma, when calling in aggregation. In a choice experiment, bats approached calls of prey aggregations more often than those of prey calling alone, indicating that prey calling in aggregation are at higher risk. In prey capture tasks, however, the average time taken, and the number of flight passes made by bats before capturing a katydid, were significantly higher for prey calling in aggregation as compared to calling alone, indicating that prey face lower predation risk when calling in aggregation. Another common anti-predatory strategy, calling from within vegetation, increased the time taken by bats to capture katydids calling alone but did not increase the time taken to capture prey calling from aggregations. The increased time taken to capture a prey calling in aggregation compared to solitary calling prey offers an escape opportunity, thus providing prey signalling acoustically in aggregations with anti-predatory benefits. For bats, greater detectability of calling prey aggregations is offset by lower foraging efficiency, and this trade-off may shape predator foraging strategies in natural environments.

Natural dimethyl sulfide gradients would lead marine predators to higher prey biomass

Finding prey is essential to survival, with marine predators hypothesised to track chemicals such as dimethyl sulfide (DMS) while foraging. Many predators are attracted to artificially released DMS, and laboratory experiments have shown that zooplankton grazing on phytoplankton accelerates DMS release. However, whether natural DMS concentrations are useful for predators and correlated to areas of high prey biomass remains a fundamental knowledge gap. Here, we used concurrent hydroacoustic surveys and in situ DMS measurements to present evidence that zooplankton biomass is spatially correlated to natural DMS concentration in air and seawater. Using agent simulations, we also show that following gradients of DMS would lead zooplankton predators to areas of higher prey biomass than swimming randomly. Further understanding of the conditions and scales over which these gradients occur, and how they are used by predators, is essential to predicting the impact of future changes in the ocean on predator foraging success.

Hemipteran defensive odors trigger predictable color biases in jumping spider predators

Multimodal warning displays often pair one signal modality (odor) with a second modality (color) to avoid predation. Experiments with bird predators suggest these signal components interact synergistically, with aversive odors triggering otherwise hidden aversions to particular prey colors. In a recent study, this phenomenon was found in a jumping spider (Habronattus trimaculatus), with the defensive odor from a coreid bug (Acanthocephala femorata) triggering an aversion to red. Here, we explore how generalizable this phenomenon is by giving H. trimaculatus the choice between red or black prey in the presence or absence of defensive odors secreted from (1) eastern leaf-footed bugs (Leptoglossus phyllopus, Hemiptera), (2) grass stinkbugs (Mormidea pama, Hemiptera), (3) Asian ladybird beetles (Harmonia axyridis, Coleoptera), and (4) eastern lubber grasshoppers (Romalea microptera, Orthoptera). As expected, in the presence of the hemipteran odors, spiders were less likely to attack red prey (compared to no odor). Unexpectedly, the beetle and grasshopper odors did not bias spiders away from red. Our results with the hemipteran odors were unique to red; follow-up experiments indicated that these odors did not affect biases for/against green prey. We discuss our findings in the context of generalized predator foraging behavior and the functions of multimodal warning displays.

Polyrhythmic foraging and competitive coexistence

The current ecological understanding still does not fully explain how biodiversity is maintained. One strategy to address this issue is to contrast theoretical prediction with real competitive communities where diverse species share limited resources. I present, in this study, a new competitive coexistence theory-diversity of biological rhythms. I show that diversity in activity cycles plays a key role in coexistence of competing species, using a two predator-one prey system with diel, monthly, and annual cycles for predator foraging. Competitive exclusion always occurs without activity cycles. Activity cycles do, however, allow for coexistence. Furthermore, each activity cycle plays a different role in coexistence, and coupling of activity cycles can synergistically broaden the coexistence region. Thus, with all activity cycles, the coexistence region is maximal. The present results suggest that polyrhythmic changes in biological activity in response to the earth’s rotation and revolution are key to competitive coexistence. Also, temporal niche shifts caused by environmental changes can easily eliminate competitive coexistence.