Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator–prey system with two prey genotypes, parametrized with data from a well-studied experimental system, and explore how the extent of differences in defence against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary ‘details’ that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.     

Sensory-based niche partitioning in a multiple predator–multiple prey community

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator–prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.     

A field demonstration of the costs and benefits of group living to edible and defended prey

Both theoretical and laboratory research suggests that many prey animals should live in a solitary, dispersed distribution unless they lack repellent defences such as toxins, venoms and stings. Chemically defended prey may, by contrast, benefit substantially from aggregation because spatial localization may cause rapid predator satiation on prey toxins, protecting many individuals from attack. If repellent defences promote aggregation of prey, they also provide opportunities for new social interactions; hence the consequences of defence may be far reaching for the behavioural biology of the animal species. There is an absence of field data to support predictions about the relative costs and benefits of aggregation. We show here for the first time using wild predators that edible, undefended artificial prey do indeed suffer heightened death rates if they are aggregated; whereas chemically defended prey may benefit substantially by grouping. We argue that since many chemical defences are costly to prey, aggregation may be favoured because it makes expensive defences much more effective, and perhaps allows grouped individuals to invest less in chemical defences.     

Prey size diversity hinders biomass trophic transfer and predator size diversity promotes it in planktonic communities

Body size exerts multiple effects on plankton food-web interactions. However, the influence of size structure on trophic transfer remains poorly quantified in the field. Here, we examine how the size diversity of prey (nano-microplankton) and predators (mesozooplankton) influence trophic transfer efficiency (using biomass ratio as a proxy) in natural marine ecosystems. Our results support previous studies on single trophic levels: transfer efficiency decreases with increasing prey size diversity and is enhanced with greater predator size diversity. We further show that communities with low nano-microplankton size diversity and high mesozooplankton size diversity tend to occur in warmer environments with low nutrient concentrations, thus promoting trophic transfer to higher trophic levels in those conditions. Moreover, we reveal an interactive effect of predator and prey size diversities: the positive effect of predator size diversity becomes influential when prey size diversity is high. Mechanistically, the negative effect of prey size diversity on trophic transfer may be explained by unicellular size-based metabolic constraints as well as trade-offs between growth and predation avoidance with size, whereas increasing predator size diversity may enhance diet niche partitioning and thus promote trophic transfer. These findings provide insights into size-based theories of ecosystem functioning, with implications for ecosystem predictive models.     

Phage and bacteria support mutual diversity in a narrowing staircase of coexistence

The competitive exclusion principle states that phage diversity M should not exceed bacterial diversity N. By analyzing the steady-state solutions of multistrain equations, we find a new constraint: the diversity N of bacteria living on the same resources is constrained to be M or M+1 in terms of the diversity of their phage predators. We quantify how the parameter space of coexistence exponentially decreases with diversity. For diversity to grow, an open or evolving ecosystem needs to climb a narrowing ‘diversity staircase'' by alternatingly adding new bacteria and phages. The unfolding coevolutionary arms race will typically favor high growth rate, but a phage that infects two bacterial strains differently can occasionally eliminate the fastest growing bacteria. This context-dependent fitness allows abrupt resetting of the ‘Red-Queen''s race'' and constrains the local diversity.     

In a warmer Arctic,mosquitoes avoid increased mortality from predators by growing faster

Climate change is altering environmental temperature, a factor that influences ectothermic organisms by controlling rates of physiological processes. Demographic effects of warming, however, are determined by the expression of these physiological effects through predator–prey and other species interactions. Using field observations and controlled experiments, we measured how increasing temperatures in the Arctic affected development rates and mortality rates (from predation) of immature Arctic mosquitoes in western Greenland. We then developed and parametrized a demographic model to evaluate how temperature affects survival of mosquitoes from the immature to the adult stage. Our studies showed that warming increased development rate of immature mosquitoes (Q₁₀ = 2.8) but also increased daily mortality from increased predation rates by a dytiscid beetle (Q₁₀ = 1.2–1.5). Despite increased daily mortality, the model indicated that faster development and fewer days exposed to predators resulted in an increased probability of mosquito survival to the adult stage. Warming also advanced mosquito phenology, bringing mosquitoes into phenological synchrony with caribou. Increases in biting pests will have negative consequences for caribou and their role as a subsistence resource for local communities. Generalizable frameworks that account for multiple effects of temperature are needed to understand how climate change impacts coupled human–natural systems.     

An ambusher's arsenal: chemical crypsis in the puff adder (Bitis arietans)

Ambush foragers use a hunting strategy that places them at risk of predation by both visual and olfaction-oriented predators. Resulting selective pressures have driven the evolution of impressive visual crypsis in many ambushing species, and may have led to the development of chemical crypsis. However, unlike for visual crypsis, few studies have attempted to demonstrate chemical crypsis. Field observations of puff adders (Bitis arietans) going undetected by several scent-orientated predator and prey species led us to investigate chemical crypsis in this ambushing species. We trained dogs (Canis familiaris) and meerkats (Suricata suricatta) to test whether a canid and a herpestid predator could detect B. arietans using olfaction. We also tested for chemical crypsis in five species of active foraging snakes, predicted to be easily detectable. Dogs and meerkats unambiguously indicated active foraging species, but failed to correctly indicate puff adder, confirming that B. arietans employs chemical crypsis. This is the first demonstration of chemical crypsis anti-predatory behaviour, though the phenomenon may be widespread among ambushers, especially those that experience high mortality rates owing to predation. Our study provides additional evidence for the existence of an ongoing chemically mediated arms race between predator and prey species.     

How sailfish use their bills to capture schooling prey

The istiophorid family of billfishes is characterized by an extended rostrum or ‘bill’. While various functions (e.g. foraging and hydrodynamic benefits) have been proposed for this structure, until now no study has directly investigated the mechanisms by which billfishes use their rostrum to feed on prey. Here, we present the first unequivocal evidence of how the bill is used by Atlantic sailfish (Istiophorus albicans) to attack schooling sardines in the open ocean. Using high-speed video-analysis, we show that (i) sailfish manage to insert their bill into sardine schools without eliciting an evasive response and (ii) subsequently use their bill to either tap on individual prey targets or to slash through the school with powerful lateral motions characterized by one of the highest accelerations ever recorded in an aquatic vertebrate. Our results demonstrate that the combination of stealth and rapid motion make the sailfish bill an extremely effective feeding adaptation for capturing schooling prey.     

Examining predator–prey body size,trophic level and body mass across marine and terrestrial mammals

Predator–prey relationships and trophic levels are indicators of community structure, and are important for monitoring ecosystem changes. Mammals colonized the marine environment on seven separate occasions, which resulted in differences in species'' physiology, morphology and behaviour. It is likely that these changes have had a major effect upon predator–prey relationships and trophic position; however, the effect of environment is yet to be clarified. We compiled a dataset, based on the literature, to explore the relationship between body mass, trophic level and predator–prey ratio across terrestrial (n = 51) and marine (n = 56) mammals. We did not find the expected positive relationship between trophic level and body mass, but we did find that marine carnivores sit 1.3 trophic levels higher than terrestrial carnivores. Also, marine mammals are largely carnivorous and have significantly larger predator–prey ratios compared with their terrestrial counterparts. We propose that primary productivity, and its availability, is important for mammalian trophic structure and body size. Also, energy flow and community structure in the marine environment are influenced by differences in energy efficiency and increased food web stability. Enhancing our knowledge of feeding ecology in mammals has the potential to provide insights into the structure and functioning of marine and terrestrial communities.     

Predators are less likely to misclassify masquerading prey when their models are present

Masquerading animals have evolved striking visual resemblances to inanimate objects. These animals gain protection from their predators not simply by avoiding detection, but by causing their predators to misclassify them as the ‘models’ that they appear to resemble. Using domestic chicks as predators and twig-mimicking caterpillars as prey, we demonstrated that masquerading prey were more likely to be misclassified as their models when viewed in isolation from their models than when viewed alongside examples of their model, although they benefitted from masquerade to some extent in both conditions. From this, we predict a selection pressure on masqueraders to use microhabitats that reduce the risk of them being viewed simultaneously with examples of their model, and/or to more closely resemble their model in situations where simultaneous viewing is commonplace.     

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

Cost of autotomy drives ontogenetic switching of anti-predator mechanisms under developmental constraints in a land snail

Autotomy of body parts offers various prey animals immediate benefits of survival in compensation for considerable costs. I found that a land snail Satsuma caliginosa of populations coexisting with a snail-eating snake Pareas iwasakii survived the snake predation by autotomizing its foot, whereas those out of the snake range rarely survived. Regeneration of a lost foot completed in a few weeks but imposed a delay of shell growth. Imprints of autotomy were found in greater than 10 per cent of S. caliginosa in the snake range but in only less than 1 per cent out of it, simultaneously demonstrating intense predation by the snakes and high efficiency of autotomy for surviving snake predation in the wild. However, in experiments, mature S. caliginosa performed autotomy less frequently. Instead of the costly autotomy, they can use defensive denticles on the inside of their shell apertures. Owing to the constraints from the additive growth of shells, most pulmonate snails can produce these denticles only when they have fully grown up. Thus, this developmental constraint limits the availability of the modified aperture, resulting in ontogenetic switching of the alternative defences. This study illustrates how costs of adaptation operate in the evolution of life-history strategies under developmental constraints     

A cure for the plague of parameters: constraining models of complex population dynamics with allometries

A major goal of ecology is to discover how dynamics and structure of multi-trophic ecological communities are related. This is difficult, because whole-community data are limited and typically comprise only a snapshot of a community instead of a time series of dynamics, and mathematical models of complex system dynamics have a large number of unmeasured parameters and therefore have been only tenuously related to real systems. These are related problems, because long time-series, if they were commonly available, would enable inference of parameters. The resulting ‘plague of parameters’ means most studies of multi-species population dynamics have been very theoretical. Dynamical models parametrized using physiological allometries may offer a partial cure for the plague of parameters, and these models are increasingly used in theoretical studies. However, physiological allometries cannot determine all parameters, and the models have also rarely been directly tested against data. We confronted a model of community dynamics with data from a lake community. Many important empirical patterns were reproducible as outcomes of dynamics, and were not reproducible when parameters did not follow physiological allometries. Results validate the usefulness, when parameters follow physiological allometries, of classic differential-equation models for understanding whole-community dynamics and the structure–dynamics relationship.     

Paradox lost: variable colour-pattern geometry is associated with differences in movement in aposematic frogs

Aposematic signal variation is a paradox: predators are better at learning and retaining the association between conspicuousness and unprofitability when signal variation is low. Movement patterns and variable colour patterns are linked in non-aposematic species: striped patterns generate illusions of altered speed and direction when moving linearly, affecting predators'' tracking ability; blotched patterns benefit instead from unpredictable pauses and random movement. We tested whether the extensive colour-pattern variation in an aposematic frog is linked to movement, and found that individuals moving directionally and faster have more elongated patterns than individuals moving randomly and slowly. This may help explain the paradox of polymorphic aposematism: variable warning signals may reduce protection, but predator defence might still be effective if specific behaviours are tuned to specific signals. The interacting effects of behavioural and morphological traits may be a key to the evolution of warning signals.