Investment in attending to cues and the evolution of amplifiers.

Signals and cues are extensively used in social interactions across diverse communication systems. Here, we extend an existing theoretical framework to explore investment by emitters and perceivers in the fidelity with which cues and signals associated with the former are detected by the latter. Traits of the emitter that improve cue or signal fidelity without adding information are termed 'amplifiers'. We assume that each party can invest in improving fidelity but that it is increasingly costly the more fidelity is improved. Our model predicts that evolution of amplifier traits of a pre-existing cue occurs over a broader range of circumstances than evolution of signalling in situations where the emitter offered no pre-existing cue to the perceiver. It further predicts that the greater the intrinsic informational value of a cue, the more likely it is that the perceiver (and not the emitter) will invest in the fidelity of detecting that cue. A consequence of this predicted asymmetry is that true communication with reciprocal adaptations in emitters and perceivers to improve signal fidelity is likely to occur predominantly for traits of intermediate reliability. The corollary is that uncertainty of the perceiver will then be a key feature of communication. Uncertainty can arise because perceivers misinterpret signals or do not perceive them correctly, but here we argue that uncertainty is more fundamentally at the root of communication because traits that are intrinsically highly informative will induce only the perceiver and not the emitter to invest in improved fidelity of perception of that trait.

Modeling scan and interscan durations in antipredator vigilance.

Many prey species alternate between bouts of foraging and bouts of antipredator vigilance. Models of vigilance typically predict how much total time prey animals should allocate to vigilance but do not specify how that time should be scheduled throughout foraging. Here, we examine how the scheduling of vigilance pays off in terms of food intake and predator detection. Specifically, we study how changes in ecological factors affect the expected duration of scans to look out for predators and the duration of interscan intervals dedicated to foraging. Our framework includes factors like the risk of attack, how difficult it is to locate food and predators, and the distance to protective cover. Our individual-based model makes several predictions about scan and interscan durations, which are discussed in relation to the available empirical evidence in birds and mammals. This model of antipredator vigilance is a first step in incorporating constraints related to food gathering and the detection of predators. Adding such constraints adds a novel dimension to vigilance models and produces a variety of predictions that await empirical scrutiny.

Linking signal fidelity and the efficiency costs of communication.

The handicap principle has been the overarching framework to explain the evolution and maintenance of communication. Yet, it is becoming apparent that strategic costs of signalling are not the only mechanism maintaining signal honesty. Rather, the fidelity of detecting signals can itself be strongly selected. Specifically, we argue that the fidelity of many signals will be constrained by the investment in signal generation and reception by the signaller and perceiver, respectively. Here, we model how investments in signal fidelity influence the emergence and stability of communication using a simple theoretical framework. The predictions of the model indicate that high-cost communication can be stable whereas low-cost intermediates are generally selected against. This dichotomy suggests that the most parsimonious route to the evolution of communication is for initial investment in communicative traits to be driven by noncommunicative functions. Such cues can appeal to pre-existing perceptual biases and thereby stimulate signal evolution. We predict that signal evolution will vary between systems in ways that can be linked to the economics of communication to the two parties involved.

On the evolutionary stability of zero-cost pooled-equilibrium signals.

A key question in the development of understanding of animal communication has been what maintains the honesty of signals, stopping dishonesty (cheating) from spreading. The dominant theory used to address this question is a refinement of Zahavi's handicap principle. The vital thing about handicap signals is that their honesty requires that those signals are costly to the sender over and above the minimum costs associated with transmission; these costs are generally called strategic costs. An alternative "pooled equilibria" has been proposed. If signalling is constrained to two levels, then it can be demonstrated that even if there is no cost associated with giving a signal, there can be a signalling evolutionarily stable strategy (ESS) where signallers are arranged into pools according to their state: those below a threshold give one signal, those above this threshold always give the other. Further, this can be generalized to any finite number of discrete signals. Here we explore the consequence of generalizing to a continuously varying signal form. We show that unless there is some physical impediment to the diversity of signals possible, then pooled-equilibrium signalling strategies are not stable. Such a strategy would be invaded by a more complex signal, where some individuals within a "pool" benefit from signalling their difference from other individuals within the pool. We suggest that such impediments to variation in signal form will be uncommon in nature, and thus so will pooled equilibria.

Density-dependent investment in costly anti-predator defences: an explanation for the weak survival benefit of group living.

A central explanation for group living across animal taxa is the reduced rate of attack by predators. However, many field observations show a weak or non-existent effect of group size on per capita mortality rates. Herein we resolve this apparent paradox. We found that Pieris brassicae larvae defended themselves less readily when in groups than when alone, in that they were more reluctant to regurgitate in response to simulated attacks and produced less regurgitant. Furthermore, a simple model demonstrates that this reluctance was sufficient to cancel out the benefit from being in a group. This conditional strategy can be understood in terms of the costs and benefits of defences. For grouped individuals, defence is less often required because attack rates are lower and the costs of defence may be higher due to competition for resources. These phenomena are likely to be widespread in facultatively gregarious species that utilise anti-predator defences.

By-product information can stabilize the reliability of communication.

Although communication underpins many biological processes, its function and basic definition remain contentious. In particular, researchers have debated whether information should be an integral part of a definition of communication and how it remains reliable. So far the handicap principle, assuming signal costs to stabilize reliable communication, has been the predominant paradigm in the study of animal communication. The role of by-product information produced by mechanisms other than the communicative interaction has been neglected in the debate on signal reliability. We argue that by-product information is common and that it provides the starting point for ritualization as the process of the evolution of communication. Second, by-product information remains unchanged during ritualization and enforces reliable communication by restricting the options for manipulation and cheating. Third, this perspective changes the focus of research on communication from studying signal costs to studying the costs of cheating. It can thus explain the reliability of signalling in many communication systems that do not rely on handicaps. We emphasize that communication can often be informative but that the evolution of communication does not cause the evolution of information because by-product information often predates and stimulates the evolution of communication. Communication is thus a consequence but not a cause of reliability. Communication is the interplay of inadvertent, informative traits and evolved traits that increase the stimulation and perception of perceivers. Viewing communication as a complex of inadvertent and derived traits facilitates understanding of the selective pressures shaping communication and those shaping information and its reliability. This viewpoint further contributes to resolving the current controversy on the role of information in communication.

Evolutionarily stable sexual allocation by both stressed and unstressed potentially simultaneous hermaphrodites within the same population.

Factors influencing allocation of resources to male and female offspring continue to be of great interest to evolutionary biologists. A simultaneous hermaphrodite is capable of functioning in both male and female mode at the same time, and such a life-history strategy is adopted by most flowering plants and by many sessile aquatic animals. In this paper, we focus on hermaphrodites that nourish post-zygotic stages, e.g. flowering plants and internally fertilising invertebrates, and consider how their sex allocation should respond to an environmental stress that reduces prospects of survival but does not affect all individuals equally, rather acting only on a subset of the population. Whereas dissemination of pollen and sperm can begin at sexual maturation, release of seeds and larvae is delayed by embryonic development. We find that the evolutionarily stable strategy for allocation between male and female functions will be critically dependent on the effect of stress on the trade-off between the costs of male and female reproduction, (i.e. of sperm and embryos). Thus, we identify evaluation of this factor as an important challenge to empiricists interested in the effects of stress on sex allocation. When only a small fraction of the population is stressed, we predict that stressed individuals will allocate their resources entirely to male function and unstressed individuals will increase their allocation to female function. Conversely, when the fraction of stress-affected individuals is high, stressed individuals should respond to this stressor by increasing investment in sperm and unstressed individuals should invest solely in embryos. A further prediction of the model is that we would not expect to find populations in the natural world where both stressed and unstressed individuals are both hermaphrodite.

Resolving current disagreements and ambiguities in the terminology of animal communication.

Communication is central to most interactions between organisms. There is currently considerable controversy about the evolution, function and even about the most basic definition of communication. The controversy is linked to definitional ambiguities and disagreements. Here we discuss how some recent disagreements can be resolved and offer a clear set of definitions. Central to our approach is a definition of communication as being a trade between one organism (the informer) and another (the perceiver). The informer exerts influence on the perceiver through the communication process, and the perceiver experiences a change in its informational state (that is, gains information) as a consequence of detecting the communication. We define both influence and information explicitly and delineate between signalling, deceptive communication, and situations where perceivers respond to cues rather than signals. We demonstrate how our definitions allow resolution of conflicts arising in recent publications on the definitions on communication and related terms.

Adaptive changes in size and age at metamorphosis can qualitatively vary with predator type and available defenses.

In many taxa the timing of metamorphosis is plastic in response to predation risk during the pre-metamorphic stage, and trends in both age and body size at metamorphosis have been the subject of much study. The responses to cues of predators are predominantly to be larger or equal-sized at the same age or older at metamorphosis. These observations are in direct contrast with existing theoretical treatments of this plasticity, which mostly predict earlier and smaller metamorphosis and never later and larger metamorphosis without invoking indirect effects on growth rate. Here we resolve the discrepancy between theory and observation using a dynamic state-dependent model that incorporates morphological and behavioral responses to predation risk. We allow prey to choose the optimal activity level and/or investment in defense over the growth period. We show that under certain conditions, metamorphosis at a larger size and later time is likely to be optimal. Our analysis allows us to make testable predictions about the changes in activity level of prey as they grow and how the effect of providing refuges will vary with predator type. Several of these predictions are supported by a meta-analysis of metamorphic responses to caged predators by larval amphibians and insects. Our predictions lead to insights about the feedback effects of antipredator responses on growth and subsequent implications for life history.

Predation risk as a driving force for phenotypic assortment: a cross-population comparison.

Frequency-dependent predation has been proposed as a general mechanism driving the phenotypic assortment of social groups via the 'oddity effect', which occurs when the presence of odd individuals in a group allows a predator to fixate on a single prey item, increasing the predator's attack-to-kill ratio. However, the generality of the oddity effect has been debated and, previously, there has not been an ecological assessment of the role of predation risk in driving the phenotypic assortment of social groups. Here, we compare the levels of body length assortment of social groups between populations of the Trinidadian guppy (Poecilia reticulata) that experience differences in predation risk. As predicted by the oddity effect hypothesis, we observe phenotypic assortment by body length to be greater under high predation risk. However, we found that a number of low-predation populations were also significantly assorted by body length, suggesting that other mechanisms may have a role to play.

The timing of food-deceptive flowers: a commentary on Internicola et al. (2008).

A recent article presents a study of pollinator visitation behaviour that is used to evaluate the selective pressure that pollinator visitation rate might have on the timing of the production of nonrewarding flowers. Here we take issue with the conclusions of the paper that there should be selection pressure for nonrewarding flowers to be available earlier in the season in order to avoid dissimilar sympatric rewarding species. Consideration of selection pressure must take into account temporal variation in total pollinator availability, pollinator longevity and unlearned response, and the stability of plant communities over time, as well as the learned responses of individual pollinators that the original study focused on. Learning alone would not necessarily select for early flowering by nonrewarders if temporal variation in pollinator numbers is strong or naïve pollinators consistently appear throughout the flowering season. Further, we argue that early flowering could simply be a natural corollary of longevity of flowers needed to combat negative frequency-dependent selection and low overall visitation rates by pollinators, rather than a trait that has been specifically selected to reduce temporal overlap with competing rewarding species.

Dynamic state-dependent modelling predicts optimal usage patterns of responsive defences.

Chemical defences against predation often involve responses to specific predation events where the prey expels fluids, such as haemolymph or gut contents, which are aversive to the predator. The common link is that each predation attempt that is averted results in an energetic cost and a reduction in the chemical defences of the prey, which might leave the prey vulnerable if the next predation attempt occurs soon afterwards. Since prey appear to be able to control the magnitude of their responses, we should expect them to trade-off the need to repel the current threat against the need to preserve defences against future threats and conserve energy for other essential activities. Here we use dynamic state-dependent models to predict optimal strategies of defence deployment in the juvenile stage of an animal that has to survive to maturation. We explore the importance of resource level, predator density, and the costs of making defences on the magnitude of the responses and optimal age and size at maturation. We predict the patterns of investment and the magnitude of the deployment of defences to potentially multiple attacks over the juvenile period, and show that responses should be smaller when the costs of defences and/or predation risk are higher. The model enables us to predict that animals in which defences benefit the adult stage will employ different strategies than those that do not use the same defences as adults, and thereby experience a smaller reduction in body size as a result of repeated attacks. We also explore the effect of the importance of adult size, and find that the sex and mating system of the prey should also affect defensive strategies. Our work provides the first predictive theory of the adaptive use of responsive defences across taxa.

Trends in body size across an environmental gradient: a differential response in scavenging and non-scavenging demersal deep-sea fish.

Body size trends across environmental gradients are widely reported but poorly understood. Here, we investigate contrasting relationships between size (body mass) and depth in the scavenging and predatory demersal ichthyofauna (800-4800 m) of the North-east Atlantic. The mean size of scavenging fish, identified as those regularly attracted to baited cameras, increased significantly with depth, while in non-scavengers there was a significant decline in size. The increase in scavenger size is a consequence of both intra and inter-specific effects. The observation of opposing relationships, in different functional groups, across the same environmental gradient indicates ecological rather than physiological causes. Simple energetic models indicate that the dissimilarity can be explained by different patterns of food distribution. While food availability declines with depth for both groups, the food is likely to be in large, randomly distributed packages for scavengers and as smaller but more evenly distributed items for predators. Larger size in scavengers permits higher swimming speeds, greater endurance as a consequence of larger energy reserves and lower mass specific metabolic rate, factors that are critical to survival on sporadic food items.

Are unusually colored eggs a signal to potential conspecific brood parasites?

It has previously been suggested that some species of birds make the last egg in their clutch pale as a signal to potential conspecific brood parasites that incubation has commenced. Here, we use game theory to show that the signaling function of pale eggs can be evolutionarily stable and resistant to cheating and to demonstrate that such a signal can only be maintained under strict conditions. The key conditions are, first, that there is a cost associated with the production of pale eggs (in particular, the cost of a pale egg produced early in the clutch must be more expensive than the cost of one produced later in the clutch) and, second, that the cost of making the last egg pale is not too great (relative to the costs of parasitism). We discuss the likelihood of these conditions being met in real systems and suggest empirical tests that would differentiate this theory from alternative nonadaptive explanations for pale eggs.

Heat loss from giant extinct reptiles.

There is disagreement in the literature about the relative rates of heat loss from a large animal surrounded by either air or water. Here, it is shown that, in most circumstances, the rate at which heat is lost by a large body is significantly greater when it is immersed in water than when it is surrounded by air, assuming that the two fluids are at the same temperature. The only circumstance when this may not apply is when comparing air with fresh water when both are at a temperature somewhere between 0 degrees C and 6 degrees C, the animal is still and water or air currents are negligible. Under these conditions, free convection in water is weak or non-existent, and so the combined effect of conduction and free convection in air becomes comparable to or even greater than that of conduction alone in water. However, in these circumstances, radiation is the dominant mode of heat loss to both media, and so heat losses are approximately the same in both air and water.

The importance of stable schooling: do familiar sticklebacks stick together?

Preferences for rejoining shoals composed of familiar individuals have recently been documented in a variety of small, shallow-water fish species. Such preferences are assumed to be adaptive, since familiar groups have improved anti-predator defences and more stable dominance hierarchies. However, the design of these studies may have created conditions that elevate preferences for familiar individuals. Furthermore, in natural habitats, where significant opportunities for inter-shoal transfer may exist, it is unclear whether shoals stay together long enough for such preferences to develop. Here we present the results of a laboratory study examining whether prior familiarity influences the subsequent shoal composition of sticklebacks (Gasterosteus aculeatus) allowed to re-assort freely in a large arena tank. We show that fish from different familiarity groups associate with familiar conspecifics significantly more than predicted by a model of random assortment, suggesting that even when there is ample opportunity for inter-group transfer, shoal composition can remain stable. We discuss the phenomena that may lead to the formation of familiar groups in natural habitats. In addition, we suggest that familiarity benefits may reduce the relative value of transferring to otherwise more attractive (e.g. larger or more phenotypically matched) groups, and thereby stabilize shoal structure.

Evidence for a rule governing the avoidance of superfluous escape flights.

When an imminent attack by a predator on a group of birds is signalled to non-detectors only by the departure of the detector, non-detectors may make time-wasting false-alarm flights in response to mistaken or non-predator-driven departures. The frequency of false-alarm flights might be reduced if group members assess the reason for single departures before responding. Immediate flights should only occur after multiple simultaneous departures, because these are only likely to be generated by an attack. The response delay between the detectors' departure and the next birds that respond should then be dependent on the number of detectors. On sparrowhawk attack, response delays in redshanks decreased significantly as detector number increased, controlling for raptor conspicuousness and proximity, and flock size and spacing. If response delay is modified because of risk dilution, it should increase with flock size and, consequently, the rate of alarm flights due to mistakes should decrease. However, response delay did not increase and flight frequency due to misidentification of non-raptors or non-predator-driven departures did not decrease with flock size. Significantly more feeding time was lost by birds in small flocks, suggesting that the dilution effect decreased the cost of each false-alarm flight rather than their frequency.

Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation.

Changes in the resources allocated to particular stages of reproduction are expected to influence allocation to, and performance in, subsequent reproductive stages. Experimental manipulation of individual investment patterns provides important evidence that such physiological trade-offs occur, and can highlight the key environmental variables that influence reproductive costs. By temporarily altering the thermal properties of starling nests, we reduced the energetic demand of first-clutch incubation, and examined the effect of this manipulation on performance during the same and the subsequent reproductive attempts. Compared with controls, starlings investing less in incubation were more successful in fledging young, and were more likely to hatch all their eggs if a subsequent reproductive attempt was made. Our results show that incubation demands can limit reproductive success, and that resources saved during incubation can be reallocated to later stages of the same reproductive attempt and to future reproductive attempts. This study also shows that small changes in thermal environment can affect breeding success by altering the energetic demands imposed on incubating parents, independently of the effect of temperature on other environmental variables such as food supply.

Evasive mimicry: when (if ever) could mimicry based on difficulty of capture evolve?

We elucidate the conditions under which an easy-to-catch edible prey species may evolve to resemble another edible species that is much more difficult to capture ('evasive Batesian mimicry'), and the conditions under which two or more edible but hard-to-catch species evolve a common resemblance ('evasive Mullerian mimicry'). Using two complementary mathematical models, we argue that both phenomena are logically possible but that several factors will limit the prevalence of these forms of mimicry in nature. Evasive Batesian mimicry is most likely to arise when it is costly in time or energy for the predator species to pursue evasive prey, when mimics are encountered less frequently than evasive models and where there are abundant alternative prey. Evasive Mullerian mimicry, by contrast, is most likely to arise when evasive prey species differ in abundance, predators are slow to learn to avoid evasive prey and evading capture is costly to the prey. Unequivocal evidence for evasive Batesian or Mullerian mimicry has not yet been demonstrated in the field, and we argue that more empirical work is needed to test whether putative examples are indeed a result of selection to signal difficulty of capture.

The importance of transients' dynamics in spatially extended populations.

Recent theoretical works on the dynamics of metapopulations have highlighted the existence of very long transients (supertransients) with abrupt changes in behaviour which occur following perturbation of the system away from its attractor. If this phenomenon is common in natural systems, populations that do not oscillate can begin to fluctuate wildly without any change in the environmental conditions. However, the frequency of occurrence of supertransients is currently poorly understood even in model systems. Here we explore their occurrence in metapopulation models which relax the important assumption of global synchrony of events implicit in all the coupled map lattice models for which supertransients have so far been demonstrated. We find supertransients in all the models but always only for a very restricted range of parameter combinations. However, we also report for the first time another type of longer-lived transient (mesotransients) that occurs on shorter time-scales than supertransients and is found for a much wider set of conditions. We argue that these medium-term changes in the dynamics of populations can be of more ecological relevance than the long-term changes of supertransients.