The role of plasticity and stochasticity in coexistence.

Species coexistence in ecological communities is a central feature of biodiversity. Different concepts, i.e., contemporary niche theory, modern coexistence theory, and the unified neutral theory, have identified many building blocks of such ecological assemblies. However, other factors, such as phenotypic plasticity and stochastic inter-individual variation, have received little attention, in particular in animals. For example, how resource polyphenisms resulting in predator-prey interactions affect coexistence is currently unknown. Here, we present an integrative theoretical-experimental framework using the nematode plasticity model Pristionchus pacificus with its well-studied mouth-form dimorphism resulting in cannibalism. We develop an individual-based model that relies upon synthetic data based on our empirical measurements of fecundity and polyphenism to preserve demographic heterogeneity. We demonstrate how the interplay between plasticity and individual stochasticity result in all-or-nothing outcomes at the local level. Coexistence is made possible when spatial structure is introduced.

Sister predatory mites collectively protect their eggs against predators.

Group-living animals sometimes cooperatively protect their offspring against predators. This behavior is observed in a wide range of taxa but, to the best of our knowledge, this is the first report of its occurrence in arthropods that are not eusocial. Adult female predatory mites Gynaeseius liturivorus protect their eggs against egg predators, the predatory mite species Neoseiulus californicus. In the field, several adult female G. liturivorus were often found on the same plant structures such as folded leaves. We tested whether these females might protect their eggs cooperatively, focusing on kinship between the females. When two adult female G. liturivorus were kept in the absence of egg predators, their reproduction was not affected by their kinship. The presence of egg predators reduced the number of G. liturivorus eggs. However, reproduction of two G. liturivorus sisters was higher than that of two non-sisters. Together, sisters guarded the oviposition site longer than non-sisters. We further tested if non-sisters increased egg guarding by having developed together from eggs to adults and found no such effect. Although it remains unclear how adult female G. liturivorus recognize conspecifics as kin or sisters, our results suggest that G. liturivorus sisters reduced predation on their offspring by cooperatively guarding their eggs.

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.

Niche theory for within-host parasite dynamics: Analogies to food web modules via feedback loops.

Why do parasites exhibit a wide dynamical range within their hosts? For instance, why does infecting dose either lead to infection or immune clearance? Why do some parasites exhibit boom-bust, oscillatory dynamics? What maintains parasite diversity, that is coinfection v single infection due to exclusion or priority effects? For insights on parasite dose, dynamics and diversity governing within-host infection, we turn to niche models. An omnivory food web model (IGP) blueprints one parasite competing with immune cells for host energy (PIE). Similarly, a competition model (keystone predation, KP) mirrors a new coinfection model (2PIE). We then drew analogies between models using feedback loops. The following three points arise: first, like in IGP, parasites oscillate when longer loops through parasites, immune cells and resource regulate parasite growth. Shorter, self-limitation loops (involving resources and enemies) stabilise those oscillations. Second, IGP can produce priority effects that resemble immune clearance. But, despite comparable loop structure, PIE cannot due to constraints imposed by production of immune cells. Third, despite somewhat different loop structure, KP and 2PIE share apparent and resource competition mechanisms that produce coexistence (coinfection) or priority effects of prey or parasites. Together, this mechanistic niche framework for within-host dynamics offers new perspective to improve individual health.

Behavioural differences underlie toxicity and predation variation in blooms of Prymnesium parvum.

Much of the evolutionary ecology of toxic algal blooms (TABs) remains unclear, including the role of algal toxins in the adaptive 'strategies' of TAB-forming species. Most eukaryotic TABs are caused by mixotrophs that augment autotrophy with organic nutrient sources, including competing algae (intraguild predation). We leverage the standing diversity of TABs formed by the toxic, invasive mixotroph Prymnesium parvum to identify cell-level behaviours involved in toxin-assisted predation using direct observations as well as comparisons between genetically distinct low- and high-toxicity isolates. Our results suggest that P. parvum toxins are primarily delivered at close range and promote subsequent prey capture/consumption. Surprisingly, we find opposite chemotactic preferences for organic (prey-derived) and inorganic nutrients between differentially toxic isolates, respectively, suggesting behavioural integration of toxicity and phagotrophy. Variation in toxicity may, therefore, reflect broader phenotypic integration of key traits that ultimately contribute to the remarkable flexibility, diversity, and success of invasive populations.

Size-Dependent Intraguild Predation, Cannibalism, and Resource Allocation Determine the Outcome of Species Coexistence.

AbstractIntraguild predation (IGP), a system in which species compete for resources and prey on each other, is more common than existing theory predicts. In theory, an IG predator and its prey can coexist if the IG predator is a weaker competitor for a shared resource and the predator directly benefits from consuming the prey. However, many species that are IG predators also consume members of their own species (cannibalism). Here, we ask whether cannibalism can help resolve the paradox of IGP systems. Our approach differs from previous work on IGP and cannibalism by explicitly considering the size dependence of predatory interactions and how the benefits of predation are allocated to survival, growth, and fecundity of the predator or cannibal. Our results show that cannibalism facilitates coexistence under conditions that are opposite of those predicted by standard IGP theory: species can coexist when the cannibal is a better competitor on the shared resources, directly benefits little from consuming conspecifics, and allocates resources from predation more toward growth and fecundity over survival. Because the effects of IGP and cannibalism are opposite, when an IGP predator is also a cannibal, coexistence between the IGP predator and its prey is not possible and instead depends on the operation of other coexistence mechanisms (e.g., resource partitioning). These results point to the importance of understanding the relative rates of IGP and cannibalism as well as the resource allocation strategy of the IG predator in determining the likelihood of species coexistence.

Intraguild predation is increased in areas of low prey diversity in a generalist predator community.

Niche differentiation and intraguild predation (IGP) can allow ecologically similar species to coexist, although it is unclear which coexistence mechanism predominates in consumer communities. Until now, a limited ability to quantify diets from metabarcoding data has precluded the use of sequencing data to determine the relative importance of these mechanisms. Here, we pair a recent metabarcoding quantification approach with stable isotope analysis to examine diet composition in a wolf spider community. We compare the prevalence of resource partitioning and IGP in these spiders and test whether factors that influence foraging performance, including individual identity, morphology, prey community and environmental conditions, can explain variation in diet composition and IGP. Extensive IGP is likely the primary coexistence mechanism in this community, and other factors to which foraging variation is often attributed do not explain diet composition and IGP here. Rather, IGP increases as prey diversity decreases. Foragers are driven to IGP where resource niches are limited. We highlight the need to examine how drivers of predator-prey interaction strengths translate into foraging in natural systems.

Stoichiometry and environmental change drive dynamical complexity and unpredictable switches in an intraguild predation model.

We incorporate stoichiometry (the balance of key elements) into an intraguild predation (IGP) model. Theoretical and numerical results show that our system exhibits complex dynamics, including chaos and multiple types of both bifurcations and bistability. Types of bifurcation present include saddle-node, Hopf, and transcritical bifurcations, and types of bistability present include node-node, node-cycle, and cycle-cycle bistability; cycle-cycle bistability has never been observed in IGP ordinary differential equation models. Stoichiometry can stabilize or destabilize the system via the disappearance or appearance of chaos. The species represented in the model can coexist for moderate levels of light intensity and nutrient availability. When the amount of light or nutrients present is extremely high or low, coexistence of the species becomes impossible, potentially harming biodiversity. Interestingly, stoichiometry can facilitate the re-emergence of severely endangered species as light intensity increases. In a temporally changing environment, the system can jump between different unstable states following changes in light intensity, with the trajectory followed depending strongly on initial conditions.

Feeding of mussel-associated leeches Hemiclepsis kasmiana on bitterling embryos: Novel interaction between parasites in a shared host.

We investigated an interaction between bitterlings and a parasitic leech Hemiclepsis kasmiana in freshwater mussel hosts. We found that leeches fed on bitterling eggs and embryos; this may exert a considerable negative effect on bitterling fitness. Host choices by females of three bitterling species may be differently affected by the presence of leeches within mussels; Tanakia limbata apparently avoided laying eggs in infested mussels while T. lanceolata and Acheilognathus rhombeus did not. Our novel findings suggest that relationships between the parasitic leech and the host mussel may be context dependent.

The Fall Armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), Influences Nilaparvata lugens Population Growth Directly, by Preying on Its Eggs, and Indirectly, by Inducing Defenses in Rice.

The fall armyworm (FAW), Spodoptera frugiperda, has become one of the most important pests on corn in China since it invaded in 2019. Although FAW has not been reported to cause widespread damage to rice plants in China, it has been sporadically found feeding in the field. If FAW infests rice in China, the fitness of other insect pests on rice may be influenced. However, how FAW and other insect pests on rice interact remains unknown. In this study, we found that the infestation of FAW larvae on rice plants prolonged the developmental duration of the brown planthopper (BPH, Nilaparvata lugens (Stål)) eggs and plants damaged by gravid BPH females did not induce defenses that influenced the growth of FAW larvae. Moreover, co-infestation by FAW larvae on rice plants did not influence the attractiveness of volatiles emitted from BPH-infested plants to Anagrus nilaparvatae, an egg parasitoid of rice planthoppers. FAW larvae were able to prey on BPH eggs laid on rice plants and grew faster compared to those larvae that lacked available eggs. Studies revealed that the delay in the development of BPH eggs on FAW-infested plants was probably related to the increase in levels of jasmonoyl-isoleucine, abscisic acid and the defensive compounds in the rice leaf sheaths on which BPH eggs were laid. These findings indicate that, if FAW invades rice plants in China, the population density of BPH may be decreased by intraguild predation and induced plant defenses, whereas the population density of FAW may be increased.

Spatiotemporal dynamics induced by intraguild predator diffusion in an intraguild predation model.

An intraguild predation model with intraguild predator diffusion is proposed and studied in this work. It is shown that the local system can have four boundary equilibria and at most two interior equilibria. The interior equilibria may exist even when the system is not uniformly persistent. When only intraguild predator diffusion is incorporated into our three-species model, the resulting model is a partially degenerate reaction-diffusion system. For this partially degenerate system, we show that the solution semiflow is bounded dissipative and the positive orbits of bounded sets are bounded. We also demonstrate that intraguild predator diffusion can lead to the occurrence of spatially nonhomogeneous oscillations and spatiotemporal chaos. Further, we show that intraguild predator diffusion can induce transitions between spatially homogeneous oscillations, spatially nonhomogeneous oscillations and chaos.

Sum of fears among intraguild predators drives the survival of green sea turtle (Chelonia mydas) eggs.

Ecologists have long theorized that apex predators stabilize trophic systems by exerting a net protective effect on the basal resource of a food web. Although experimental and observational studies have borne this out, it is not always clear what behavioural mechanisms among the trophically connected species are responsible for this stability. Fear of intraguild predation is commonly identified as one such mechanism in models and mesocosm studies, but empirical evidence in natural systems remains limited, as the complexity of many trophic systems renders detailed behavioural studies of species interactions challenging. Here, we combine long-term field observations of a trophic system in nature with experimental behavioural studies of how all the species in this system interact, in both pairs and groups. The results demonstrate how an abundant, sessile and palatable prey item (sea turtle eggs, Chelonia mydas) survives when faced by three potential predators that all readily eat eggs: an apex predator (the stink ratsnake, Elaphe carinata) and two mesopredators (the brown rat, Rattus norvegicus, and kukri snake, Oligodon formosanus). Our results detail how fear of intraguild predation, conspecific cannibalism, habitat structure and territorial behaviour among these species interact in a complex fashion that results in high egg survival.

Energetic constraints imposed on trophic interaction strengths enhance resilience in empirical and model food webs.

Food web stability and resilience are at the heart of understanding the structure and functioning of ecosystems. Previous studies show that models of empirical food webs are substantially more stable than random ones, due to a few strong interactions embedded in a majority of weak interactions. Analyses of trophic interaction loops show that in empirical food webs the patterns of the interaction strengths prevent the occurrence of destabilizing heavy loops and thereby enhances resilience. Yet, it is still unexplored which biological mechanisms cause these patterns that enhance food web resilience. We quantified food web resilience using the real part of the maximum eigenvalue of the Jacobian matrix of the food web from a seagrass bed in the Yellow River Delta (YRD) wetland, that could be parametrized by the empirical data of the food web. We found that the empirically based Jacobian matrix of the YRD food web indicated a much higher resilience than random matrices with the same element values but arranged in random ways. Investigating the trophic interaction loops revealed that the high resilience was due to a negative correlation between the negative and positive interaction strengths (per capita top-down and bottom-up effects, respectively) within positive feedback loops with three species. The negative correlation showed that when the negative interaction strengths were strong the positive was weak, and vice versa. Our invented reformulation of loop weight in terms of biomasses and specific production rates showed that energetic properties of the trophic groups in the loop and mass-balance constraints, for example, the food uptake has to balance all losses, created the negative correlation between the interaction strengths. This result could be generalized using a dynamic intraguild predation model, which delivered the same pattern for a wide range of model parameters. Our results shed light on how energetic constraints at the trophic group and food web level create a pattern of interaction strengths within trophic interaction loops that enhances food web resilience.

The evolution of size-dependent competitive interactions promotes species coexistence.

Theory indicates that competing species coexist in a community when intraspecific competition is stronger than interspecific competition. When body size determines the outcome of competitive interactions between individuals, coexistence depends also on how resource use and the ability to compete for these resources change with body size. Testing coexistence theory in size-structured communities, therefore, requires disentangling the effects of size-dependent competitive abilities and niche shifts. Here, we tested the hypothesis that the evolution of species- and size-dependent competitive asymmetries increased the likelihood of coexistence between interacting species. We experimentally estimated the effects of size-dependent competitive interactions on somatic growth rates of two interacting fish species, Trinidadian guppies Poecilia reticulata and killifish Rivulus hartii. We controlled for the effects of size-dependent changes in the niche at two competitive settings representing the early (allopatric) and late (sympatric) evolutionary stages of a killifish-guppy community. We fitted the growth data to a model that incorporates species- and size-dependent competitive asymmetries to test whether changes in the competitive interactions across sizes increased the likelihood of species coexistence from allopatry to sympatry. We found that guppies are competitively superior to killifish but were less so in sympatric populations. The decrease in the effects of interspecific competition on the fitness of killifish and increase in the interspecific effect on guppies' fitness increased the likelihood that sympatric guppies and killifish will coexist. However, while the competitive asymmetries between the species changed consistently between allopatry and sympatry between drainages, the magnitude of the size-dependent competitive asymmetries varied between drainages. These results demonstrate the importance of integrating evolution and trait-based interactions into the research on how species coexist.

Aphid alarm pheromone alters larval behaviour of the predatory gall midge, Aphidoletes aphidimyza and decreases intraguild predation by anthocorid bug, Orius laevigatus.

Intraguild predation is the killing and consuming of a heterospecific competitor that uses similar resources as the prey, and also benefit from preying on each other. We investigated the foraging behaviour of the gallmidge, Aphidoletes aphidimyza, a predator of aphids used for biological control that is also the intraguild prey for most other aphid natural enemies. We focus on how aphid alarm pheromone can alter the behaviour of the gallmidge, and predation by the anthocorid bug Orius laevigatus (O. laevigatus). We hypothesised that gallmidges would respond to the presence of (E)-ß-farnesene (EBF) by leaving the host plant. Since feeding by Aphidoletes gallmidge larvae does not induce EBF emission by aphids, this emission indicates the presence of an intraguild predator. We found that gallmidge larvae reduced their foraging activities and left the plant earlier when exposed to EBF, particularly when aphids were also present. Contrastingly, gallmidge females did not change the time visiting plants when exposed to EBF, but lay more eggs on plants that had a higher aphid density. Lastly, EBF reduced the number of attacks of the intraguild predator, O. laevigatus, on gallmidge larvae, potentially because more gallmidges stopped aphid feeding and moved off the plant at which point O. laevigatus predated on aphids. Our work highlights the importance of understanding how intraguild predation can influence the behaviour of potential biological control agents and the impact on pest control services when other natural enemies are also present.

Enemies with benefits: integrating positive and negative interactions among terrestrial carnivores.

Interactions among terrestrial carnivores involve a complex interplay of competition, predation and facilitation via carrion provisioning, and these negative and positive pathways may be closely linked. Here, we developed an integrative framework and synthesized data from 256 studies of intraguild predation, scavenging, kleptoparisitism and resource availability to examine global patterns of suppression and facilitation. Large carnivores were responsible for one third of mesocarnivore mortality (n = 1,581 individuals), and intraguild mortality rates were superadditive, increasing from 10.6% to 25.5% in systems with two vs. three large carnivores. Scavenged ungulates comprised 30% of mesocarnivore diets, with larger mesocarnivores relying most heavily on carrion. Large carnivores provided 1,351 kg of carrion per individual per year to scavengers, and this subsidy decreased at higher latitudes. However, reliance on carrion by mesocarnivores remained high, and abundance correlations among sympatric carnivores were more negative in these stressful, high-latitude systems. Carrion provisioning by large carnivores may therefore enhance suppression rather than benefiting mesocarnivores. These findings highlight the synergistic effects of scavenging and predation risk in structuring carnivore communities, suggesting that the ecosystem service of mesocarnivore suppression provided by large carnivores is strong and not easily replaced by humans.

Intraguild predation between Pristionchus pacificus and Caenorhabditis elegans: a complex interaction with the potential for aggressive behaviour.

The related nematodes Pristionchus pacificus and Caenorhabditis elegans both eat bacteria for nutrition and are therefore competitors when they exploit the same bacterial resource. In addition to competing with each other, P. pacificus is a predator of C. elegans larval prey. These two relationships together form intraguild predation, which is the killing and sometimes eating of potential competitors. In killing C. elegans, the intraguild predator P. pacificus may achieve dual benefits of immediate nutrition and reduced competition for bacteria. Recent studies of P. pacificus have characterized many aspects of its predatory biting behaviour as well as underlying molecular and genetic mechanisms. However, little has been explored regarding the potentially competitive aspect of P. pacificus biting C. elegans. Moreover, aggression may also be implicated if P. pacificus intentionally bites C. elegans with the goal of reducing competition for bacteria. The aim of this review is to broadly outline how aggression, predation, and intraguild predation relate to each other, as well as how these concepts may be applied to future studies of P. pacificus in its interactions with C. elegans.

How intraguild predation affects the host diversity-disease relationship in a multihost community.

Broad evidence has shown that host diversity can impede disease invasion and reduce the eventual prevalence, but little is known on how species interactions play in shaping this host diversity-disease relationship. Previous work has illustrated that intraguild predation (IGP), combined with parasite-mediated indirect effects, can have strong influences on parasitic infection. Following this line of thinking, we here examine the role of predatory interactions in the disease transmission within a multihost community. Through varying fractions of IGP in a competitive community, we show that, dependent on the fraction of predatory interactions, species richness can switch from enhancing to inhibiting disease establishment/prevalence. Without IGP interactions, high host species richness can likely weaken the 'dilution effect' and in some cases even enhance the disease establishment (and/or prevalence) due to the existence of alternative sources for infection, whereas IGP can generally heighten the negative diversity-disease relationship due to the reduction of encounter rate between prospective hosts and parasites. Although trait-mediated interactions (captured as the infection-induced changes in predation rate) only weakly affect disease prevalence, density-mediated interactions (captured as the additional infection-induced mortality) can pose a relatively strong influence on disease transmission. Our results thus underline the importance of considering species interactions when investigating the host diversity-disease relationship.

Intraguild predation decreases predator fitness with potentially varying effects on pathogen transmission in a herbivore host.

Predators and pathogens often regulate the population dynamics of their prey or hosts. When species interact with both their predators and their pathogens, understanding each interaction in isolation may not capture the system's dynamics. For instance, predators can influence pathogen transmission via consumptive effects, such as feeding on infected prey, or non-consumptive effects, such as changing the prey's susceptibility to infection. A prey species' infection status can, in turn, influence predator's choice of prey and have negative fitness consequences for the predator. To test how intraguild predation (IGP), when predator and pathogen share the same prey/host, affects pathogen transmission, predator preference, and predator fitness, we conducted a series of experiments using a crop pest (Pseudoplusia includens), a generalist predator (Podisus maculiventris), and a generalist pathogen (Autographa californica multicapsid nuclear polyhedrovirus, AcMNPV). Using a field experiment, we quantified the effects of consumptive and non-consumptive predators on pathogen transmission. We found that a number of models provided similar fits to the data. These models included null models showing no effects of predation and models that included a predation effect. We also found that predators consumed infected prey more often when choosing between live infected or live healthy prey. Infected prey also reduced predator fitness. Developmental times of predators fed infected prey increased by 20% and longevity decreased by 45%, compared with those that consumed an equivalent number of non-infected prey. While this research shows an effect of the pathogen on intraguild predator fitness, we found no support that predators affected pathogen transmission.

Intraguild predation enhances biodiversity and functioning in complex food webs.

Intraguild predation (IGP), that is, feeding interaction between two consumers that share the same resource species, is commonly observed in natural food webs. IGP expands vertical niche space and slows down energy flows from lower to higher trophic levels, which potentially affects the diversity and dynamics of food webs. Here, we use food-web models to investigate the effects of IGP on species diversity and ecosystem functioning. We first simulate a five-species food-web module with different strengths of IGP at the herbivore and/or carnivore level. Results show that as the strength of IGP within a trophic level increases, the biomass of its resource level increases because of predation release; this increased biomass in turn alters the energy fluxes and biomass of other trophic levels. These results are then extended by subsequent simulations of more diverse food webs. As the strength of IGP increases, simulated food webs maintain (1) higher species diversity at different trophic levels, (2) higher total biomasses at different trophic levels, and (3) larger energy fluxes across trophic levels. Our results challenge the intuitive hypothesis that food-web structure should maximize the efficiency of energy transfer across trophic levels; instead, they suggest that the assembly of food webs should be governed by a balance between efficiency (of energy transfer) and persistence (i.e., the maintenance of species and biomasses). Our simulations also show that the relationship between biodiversity and ecosystem functioning (e.g., total biomass or primary production) is much stronger in the presence of IGP, reconciling the contrast from recent studies based on food-chain and food-web models. Our findings shed new light on the functional role of IGP and contribute to resolving the debate on structure, diversity and functioning in complex food webs.