Using adaptive traits to consider potential consequences of temporal variation in selection: male guppy colour through time and space

Temporal variation in selection is typically evaluated by estimating and comparing selection coefficients in natural populations. Meta‐analyses of these coefficients have yielded important insights, but selection coefficients are limited in several respects, including low statistical power, imperfect fitness surrogates, and uncertainty regarding consequences for trait change. A complementary approach without these limitations is to examine temporal variation in adaptive traits themselves, which is mechanistically easier and more directly relevant to evolutionary consequences. We illustrate this approach by analyzing the colour patterns of male guppies, Poecilia reticulata, from each of six sites in Trinidad in each of 6 years. This system is particularly appropriate for our study because key aspects of colour variation are genetically‐based and responsive to selection. However, although spatial patterns of colour variation have been extensively considered in this system, no study has yet formally assessed annual temporal variation in non‐manipulated populations. Matching previous conclusions for the guppy system, we find that guppies from different sites manifest different colour patterns in association with different predation regimes. We here add the new finding that, although some temporal variation is present, spatial patterns of colour variation are generally consistent across years. These results suggest that, when considering adaptive traits, spatial variation is more important than temporal variation, although our study system might be exceptional in this regard. Additional studies examining spatiotemporal variation in adaptive traits could help to improve our understanding of the role that spatiotemporal variation in selection plays in the evolutionary process. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 108–122.     

Predator response to the coloured eyespots and defensive posture of Colombian four-eyed frogs

Deimatic displays, where sudden changes in prey appearance elicit aversive predator reactions, have been suggested to occur in many taxa. These (often only putative) displays frequently involve different components that may also serve antipredator functions via other mechanisms (e.g., mimicry, warning signalling, body inflation). The Colombian four-eyed frog, Pleurodema brachyops, has been suggested to gain protection against predation through putative deimatic displays where they inflate and elevate the posterior part of their body revealing eye-like colour markings. We exposed stationary artificial frogs to wild predators to test whether the two components (eyespot/colour markings, defensive posture) of their putative deimatic display, and their combination, provide protection from predation without the sudden change in appearance. We did not detect any obvious additive effect of defensive posture and eyespots/colour markings on predation risk, but found a marginally significant trend for model frogs in the resting posture to be less attacked when displaying eyespots/colour markings than when they were not, suggesting that the presence of colour markings/eyespots may provide some protection on its own. Additionally, we found that models in a resting posture were overall more frequently attacked on the head than models in a defensive posture, indicating that a defensive posture alone could help redirect predator attacks to non-vital parts of the body. The trends found in our study suggest that the different components of P. brachyops' coloration may serve different functions during a deimatic display, but further research is needed to elucidate the role of each component when accompanied by sudden prey movement.     

Contrasting Effects of Wolves and Human Hunters on Elk Behavioral Responses to Predation Risk

ABSTRACT Prey behavioral responses to predation risk in wolf-ungulate-plant systems are of interest to wildlife managers. Using Global Positioning System data collected from telemetry-collared elk (Cervus elaphus) and wolves (Canis lupus), we evaluated elk behavioral responses to spatial and temporal variation in wolf- and human-predation risk on a winter range in the Greater Yellowstone Area, USA. We found elk changed grouping patterns and increased movement rates as predation risk increased and that these behavioral changes were habitat dependent. Elk behavioral responses to wolf- and human-predation risk were similar; however, responses to human-predation risk were stronger than responses to wolf-predation risk. These results suggest that predation risk from wolves or human hunters may result in elk spending more time on private rangelands away from public-land winter ranges, which may exacerbate problems of landowner tolerance of elk on livestock pastures. However, increased movement and changing grouping patterns on winter ranges may also disperse elk grazing impacts and lessen elk impacts on any one area.     

Rockpool Gobies Change Colour for Camouflage

Camouflage is found in a wide range of species living in numerous habitat types, offering protection from visually guided predators. This includes many species from the intertidal zone, which must cope with background types diverse in appearance and with multiple predator groups foraging at high and low tide. Many animals are capable of either relatively slow (hours, days, weeks) or rapid (seconds and minutes) colour change in order to better resemble the background against which they are found, but most work has been restricted to a few species or taxa. It is often suggested that many small intertidal fish are capable of colour change for camouflage, yet little experimental work has addressed this. Here, we test rock gobies (Gobius paganellus) for colour change abilities, and whether they can tune their appearance to match the background. In two experiments, we place gobies on backgrounds of different brightness (black or white), and of different colours (red and blue) and use digital image analysis and modelling of predator (avian) vision to quantify colour and luminance (perceived lightness) changes and camouflage. We find that gobies are capable of rapid colour change (occurring within one minute), and that they can change their luminance on lighter or darker backgrounds. When presented on backgrounds of different colours, gobies also change their colour (hue and saturation) while keeping luminance the same. These changes lead to predicted improvements in camouflage match to the background. Our study shows that small rockpool fish are capable of rapid visual change for concealment, and that this may be an important mechanism in many species to avoid predation, especially in complex heterogeneous environments.     

Breeding Phenology of Birds: Mechanisms Underlying Seasonal Declines in the Risk of Nest Predation

Seasonal declines in avian clutch size are well documented, but seasonal variation in other reproductive parameters has received less attention. For example, the probability of complete brood mortality typically explains much of the variation in reproductive success and often varies seasonally, but we know little about the underlying cause of that variation. This oversight is surprising given that nest predation influences many other life-history traits and varies throughout the breeding season in many songbirds. To determine the underlying causes of observed seasonal decreases in risk of nest predation, we modeled nest predation of Dusky Flycatchers (Empidonax oberholseri) in northern California as a function of foliage phenology, energetic demand, developmental stage, conspecific nest density, food availability for nest predators, and nest predator abundance. Seasonal variation in the risk of nest predation was not associated with seasonal changes in energetic demand, conspecific nest density, or predator abundance. Instead, seasonal variation in the risk of nest predation was associated with foliage density (early, but not late, in the breeding season) and seasonal changes in food available to nest predators. Supplemental food provided to nest predators resulted in a numerical response by nest predators, increasing the risk of nest predation at nests that were near supplemental feeders. Our results suggest that seasonal changes in foliage density and factors associated with changes in food availability for nest predators are important drivers of temporal patterns in risk of avian nest predation.     

Predation and the relative importance of larval colour polymorphisms and colour polyphenism in a damselfly

Intraspecific body colour variation is common in many animal species. Predation could be a key selective agent giving rise to variation in body colour, and such variation could be due to genetics (polymorphisms) or phenotypic plasticity (polyphenisms). In this study we examined the degree of colour polymorphism and polyphenism in background colour matching in larvae of the damselfly Coenagrion armatum. In addition, we tested if predation risk is reduced when larvae are exposed to a matching compared to a non-matching background. By raising families of larvae at three different background colours we showed that polymorphism explained about 20 % of the total variation and polyphenism about 35 %. In a predation experiment with fish, we showed that larvae with a body colour matching the background had a higher survival success compared to larvae with a non-matching background colour. We suggest that the background matching is adaptive in terms of survival from predation and that colour diversity is maintained because of spatial and temporal variation in the background experienced by damselfly larvae under field conditions.     

Predation risk and the evolutionary ecology of reproductive behaviour

A large literature exists on the effects of predation risk on foraging and survival-related behaviours. In contrast, with some notable exceptions, relatively few theoretical or experimental studies have examined the effects of predation risk on reproductive behaviours. Existing literature on risk and reproductive behaviour and suggestion directions for future study are reviewed. In particular: (1) effects on predation risk on mating behaviour; (2) the influence of spatial patchiness on interactions between risk and reproductive behaviour; (3) the potential influence of multi-species interactions on the effects of predation risk on mating dynamics; (4) the importance of looking at sets of inter-related antipredator traits; and (5) some effects of predation risk on prey population patterns due to changes in prey reproductive behaviour are discussed. To illustrate various points examples involving fish and other aquatic organisms are used.     

Intuition, functional responses and the formulation of predator-prey models when there is a large disparity in the spatial domains of the interacting species

1. The disparity of the spatial domains used by predators and prey is a common feature of many terrestrial avian and mammalian predatory interactions, as predators are typically more mobile and have larger home ranges than their prey. 2. Incorporating these realistic behavioural features requires formulating spatial predator-prey models having local prey mortality due to predation and its spatial aggregation, in order to generate a numerical response at timescales longer than the local prey consumption. Coupling the population dynamics occurring at different spatial scales is far from intuitive, and involves making important behavioural and demographic assumptions. Previous spatial predator-prey models resorted to intuition to derive local functional responses from non-spatial equivalents, and often involve unrealistic biological assumptions that restrict their validity. 3. We propose a hierarchical framework for deriving generic models of spatial predator-prey interactions that explicitly considers the behavioural and demographic processes occurring at different spatial and temporal scales. 4. The proposed framework highlights the circumstances wherein static spatial patterns emerge and can be a stabilizing mechanism of consumer-resource interactions.     

Predation risk shapes social networks in fission-fusion populations

Predation risk is often associated with group formation in prey, but recent advances in methods for analysing the social structure of animal societies make it possible to quantify the effects of risk on the complex dynamics of spatial and temporal organisation. In this paper we use social network analysis to investigate the impact of variation in predation risk on the social structure of guppy shoals and the frequency and duration of shoal splitting (fission) and merging (fusion) events. Our analyses revealed that variation in the level of predation risk was associated with divergent social dynamics, with fish in high-risk populations displaying a greater number of associations with overall greater strength and connectedness than those from low-risk sites. Temporal patterns of organisation also differed according to predation risk, with fission events more likely to occur over two short time periods (5 minutes and 20 minutes) in low-predation fish and over longer time scales (>1.5 hours) in high-predation fish. Our findings suggest that predation risk influences the fine-scale social structure of prey populations and that the temporal aspects of organisation play a key role in defining social systems.     

Frequency-dependent predation, crypsis and aposematic coloration

Frequency-dependent predation may maintain or prevent colour pattern polymorphisms in prey, and can be caused by a variety of biological phenomena, including perceptual processes (search images), optimal foraging and learning. Most species are preyed upon by more than one predator species, which are likely to differ in foraging styles, perceptual and learning abilities. Depending upon the interaction between predator vision, background and colour pattern parameters, certain morphs may be actively maintained in some conditions and not in others, even with the same predators. More than one kind of predator will also affect stability, and only slight changes in conditions can cause a transition between polymorphism and monomorphism. Frequency-dependent selection is not a panacea for the explanation of variation in animal colour patterns, although it may be important in some systems.     

Coping with Shifting Nest Predation Refuges by European Reed Warblers Acrocephalus scirpaceus

Predation, the most important source of nest mortality in altricial birds, has been a subject of numerous studies during past decades. However, the temporal dynamics between changing predation pressures and parental responses remain poorly understood. We analysed characteristics of 524 nests of European reed warblers monitored during six consecutive breeding seasons in the same area, and found some support for the shifting nest predation refuge hypothesis. Nest site characteristics were correlated with nest fate, but a nest with the same nest-site attributes could be relatively safe in one season and vulnerable to predation in another. Thus nest predation refuges were ephemeral and there was no between-season consistency in nest predation patterns. Reed warblers that lost their first nests in a given season did not disperse farther for the subsequent reproductive attempt, compared to successful individuals, but they introduced more changes to their second nest sites. In subsequent nests, predation risk remained constant for birds that changed nest-site characteristics, but increased for those that did not. At the between-season temporal scale, individual birds did not perform better with age in terms of reducing nest predation risk. We conclude that the experience acquired in previous years may not be useful, given that nest predation refuges are not stable.     

Variable colour patterns indicate multidimensional,intraspecific trait variation and ecological generalization in moths

Animal colour patterns long have provided information about key processes that drive the ecological and evolutionary dynamics of biological diversity. Theory and empirical evidence indicate that variation in colour patterns and other traits among individuals generally improves the performance of populations and species, for example by reducing predation risk, increasing establishment success, improving resilience to environmental change, and decreasing risk of extinction. However, little is known about whether and how variation in colour pattern among species is associated with variation in other phenotypic dimensions. To address this issue, we analysed associations of colour pattern with morphological, behavioural and life-history traits on the basis of data for nearly 400 species of noctuid moths. We found that moths with more variable colour patterns had longer flight activity periods, more diverse habitats and a greater number of host plant species than species with less variable colour patterns. Variable coloration in adult noctuid moths therefore can be considered as indicative of broader niches and generalist diets. Colour pattern variability was not significantly associated with overwintering stage or body size (wing span), and it was independent of whether the colour pattern of the larvae was non-variable, variable or highly variable. Colour pattern variation during the larval stage tended to increase as the duration of the flight activity period increased, but was independent of the length of the larval period, diet breadth and habitat use. The realization that information on colour pattern variation in adult moths, and possibly other organisms, offers a proxy for niche breadth and dietary generalization can inform management and conservation biology.     

Hazardous duty pay and the foraging cost of predation

We review the concepts and research associated with measuring fear and its consequences for foraging. When foraging, animals should and do demand hazardous duty pay. They assess a foraging cost of predation to compensate for the risk of predation or the risk of catastrophic injury. Similarly, in weighing foraging options, animals tradeoff food and safety. The foraging cost of predation can be modelled, and it can be quantitatively and qualitatively measured using risk titrations. Giving‐up densities (GUDs) in depletable food patches and the distribution of foragers across safe and risky feeding opportunities are two frequent experimental tools for titrating food and safety. A growing body of literature shows that: (i) the cost of predation can be big and comprise the forager's largest foraging cost, (ii) seemingly small changes in habitat or microhabitat characteristics can lead to large changes in the cost of predation, and (iii) a forager's cost of predation rises with risk of mortality, the forager's energy state and a decrease in its marginal value of energy. In titrating for the cost of predation, researchers have investigated spatial and temporal variation in risk, scale‐dependent variation in risk, and the role of predation risk in a forager's ecology. A risk titration from a feeding animal often provides a more accurate behavioural indicator of predation risk than direct observations of predator‐inflicted mortality. Titrating for fear responses in foragers has some well‐established applications and holds promise for novel methodologies, concepts and applications. Future directions for expanding conceptual and empirical tools include: what are the consequences of foraging costs arising from interference behaviours and other sources of catastrophic loss? Are there alternative routes by which organisms can respond to tradeoffs of food and safety? What does an animal's landscape of fear look like as a spatially explicit map, and how do various environmental factors affect it? Behavioural titrations will help to illuminate these issues and more.     

Age-dependent traits: a new statistical model to separate within- and between-individual effects

Evolutionary questions regarding aging address patterns of within-individual change in traits during a lifetime. However, most studies report associations between age and, for example, reproduction based on cross-sectional comparisons, which may be confounded with progressive changes in phenotypic population composition. Unbiased estimation of patterns of age-dependent reproduction (or other traits) requires disentanglement of within-individual change (improvement, senescence) and between-individual change (selective appearance and disappearance). We introduce a new statistical model that allows patterns of variance and covariance to differ between levels of aggregation. Our approach is simpler than alternative methods and can quantify the relative contributions of within- and between-individual changes in one framework. We illustrate our model using data on a long-lived bird species, the oystercatcher (Haematopus ostralegus). We show that for different reproductive traits (timing of breeding and egg size), either within-individual improvement or selective appearance can result in a positive association between age and reproductive traits at the population level. Potential applications of our methodology are manifold because within- and between-individual patterns are likely to differ in many biological situations.     

Inside‐container effects drive mosquito community structure in Brazilian Atlantic forest

Metacommunity theory is a convenient framework in which to investigate how local communities linked by dispersal influence patterns of species distribution and abundance across large spatial scales. For organisms with complex life cycles, such as mosquitoes, different pressures are expected to act on communities due to behavioral and ecological partitioning of life stages. Adult females select habitats for oviposition, and resulting offspring are confined to that habitat until reaching adult stages capable of flight; outside‐container effects (OCE) (i.e., spatial factors) are thus expected to act more strongly on species distributions as a function of adult dispersal capability, which should be limited by geographic distances between sites. However, larval community dynamics within a habitat are influenced by inside‐container effects (ICE), mainly interactions with conspecifics and heterospecifics (e.g., through effects of competition and predation). We used a field experiment in a mainland‐island scenario to assess whether environmental, spatial, and temporal factors influence mosquito prey and predator distributions and abundances across spatial scales: within‐site, between‐site, and mainland‐island. We also evaluated whether predator abundances inside containers play a stronger role in shaping mosquito prey community structure than do OCE (e.g., spatial and environmental factors). Temporal influence was more important for predators than for prey mosquito community structure, and the changes in prey mosquito species composition over time appear to be driven by changes in predator abundances. There was a negligible effect of spatial and environmental factors on mosquito community structure, and temporal effects on mosquito abundances and distributions appear to be driven by changes in abundance of the dominant predator, perhaps because ICE are stronger than OCE due to larval habitat restriction, or because adult dispersal is not limited at the chosen spatial scales.     

Possible Linkage between the Ability to Change the Period (τ) of the Prolactin and Cortisol Rhythms in Women and Breast Cancer Risk

The 24 h profiles of plasma hormone concentrations are rhythmic. The circadian period (τ) changes in development, with seasons, and in women with different stages of the menstrual cycle. It is known that the rhythms of prolactin and cortisol are sensitive to environmental time cues, such as changes in day length and phase; however, the importance of these changes is not yet understood. This study investigates whether there is a relation between the ability of a subject to respond to external cues that are associated with seasonal changes causing alteration of the rhythm's periods in cortisol and prolactin and the epidemiologically determined susceptibility to breast cancer. It is shown that the rhythmic output pattern of prolactin and cortisol in vivo is generated by more than one oscillator and structured by more than one rhythmic component. Each cohort of American women, classified on an epidemiologic basis as high risk (HR) or low risk (LR) to develop breast cancer, expresses different rhythmic output patterns of both variables, suggesting that the genetic background as defined by the risk state is related to differences in the circadian time structure, including the ability of the subject to change the rhythm's τ. The LR cohort exhibited a statistically significant change between seasons in the rhythm's τ of both the prolactin and cortisol patterns. In contrast, the HR cohort showed no change in the rhythm's τ between seasons for prolactin and cortisol patterns. These results show that in human beings, the presence of a circannual rhythm in the circadian time structure or the ability to adapt the circadian rhythmic pattern of these variables to external cues, such as seasons, is related to the partly genetically determined risk state to develop breast cancer and may be of importance for human health.     

Seasonal variation of tadpole spatial niches in permanent streams: The roles of predation risk and microhabitat availability

Phenotypic plasticity can improve fitness in unstable environments and can be expressed in many traits, such as life history attributes, growth and behavioural features. Microhabitat choice can have important consequences for development and survival of aquatic organisms and is expected to vary in response to stimuli, such as predation risk, food availability and temperature. At seasonal sites, microhabitat availability and associated benefits may change from season to season, which might lead to altered patterns of microhabitat use by tadpoles. We investigated this hypothesis in 17 streams from two localities in south‐eastern Brazil. We tested whether water level drops significantly during the dry season, whether lower water level results in altered microhabitat availability and whether predation risk changes between seasons, based on predator density. We then tested whether tadpoles change their pattern of microhabitat use, their spatial niche breadth (given by diversity of used microhabitats) and spatial niche overlap (in the case of co‐occurring species). We were able to include in our analyses tadpoles of four species of Hylidae, that occurred throughout both seasons. Stream depth decreased in the dry season, but microhabitat availability remained relatively stable in many streams, and predator density did not change significantly. Tadpoles of three out of the four species studied were more abundant during the dry season, which may be an adaptation to adjust time of metamorphosis to the rainy season. Tadpoles changed their patterns of microhabitat use between seasons, although the potential causing factors investigated did not seem to be responsible. Tadpole plasticity in microhabitat use may indicate the existence of selective pressures that vary through time and space and are still not well understood.     

Climate drives temporal replacement and nested‐resultant richness patterns of Scottish coastal vegetation

Beta diversity quantifies spatial and/or temporal variation in species composition. It is comprised of two distinct components, species replacement and nestedness, which derive from opposing ecological processes. Using Scotland as a case study and a β‐diversity partitioning framework, we investigate temporal replacement and nestedness patterns of coastal grassland species over a 34‐yr time period. We aim to 1) understand the influence of two potentially pivotal processes (climate and land‐use changes) on landscape‐scale (5 × 5 km) temporal replacement and nestedness patterns, and 2) investigate whether patterns from one β‐diversity component can mask observable patterns in the other. We summarised key aspects of climate driven macro‐ecological variation as measures of variance, long‐term trends, between‐year similarity and extremes, for three important climatic predictors (minimum temperature, water‐balance and growing degree‐days). Shifts in landscape‐scale heterogeneity, a proxy of land‐use change, was summarised as a spatial multiple‐site dissimilarity measure. Together, these climatic and spatial predictors were used in a multi‐model inference framework to gauge the relative contribution of each on temporal replacement and nestedness patterns. Temporal β‐diversity patterns were reasonably well explained by climate change but weakly explained by changes in landscape‐scale heterogeneity. Climate was shown to have a greater influence on temporal nestedness than replacement patterns over our study period, linking nestedness patterns, as a result of imbalanced gains and losses, to climatic warming and extremes respectively. Important climatic predictors (i.e. growing degree‐days) of temporal β‐diversity were also identified, and contrasting patterns between the two β‐diversity components revealed. Results suggest climate influences plant species recruitment and establishment processes of Scotland's coastal grasslands, and while species extinctions take time, they are likely to be facilitated by climatic perturbations. Our findings also highlight the importance of distinguishing between different components of β‐diversity, disentangling contrasting patterns than can mask one another.     

Possible linkage between the ability to change the period (tau) of the prolactin and cortisol rhythms in women and breast cancer risk

The 24 h profiles of plasma hormone concentrations are rhythmic. The circadian period (τ) changes in development, with seasons, and in women with different stages of the menstrual cycle. It is known that the rhythms of prolactin and cortisol are sensitive to environmental time cues, such as changes in day length and phase; however, the importance of these changes is not yet understood. This study investigates whether there is a relation between the ability of a subject to respond to external cues that are associated with seasonal changes causing alteration of the rhythm's periods in cortisol and prolactin and the epidemiologically determined susceptibility to breast cancer. It is shown that the rhythmic output pattern of prolactin and cortisol in vivo is generated by more than one oscillator and structured by more than one rhythmic component. Each cohort of American women, classified on an epidemiologic basis as high risk (HR) or low risk (LR) to develop breast cancer, expresses different rhythmic output patterns of both variables, suggesting that the genetic background as defined by the risk state is related to differences in the circadian time structure, including the ability of the subject to change the rhythm's τ. The LR cohort exhibited a statistically significant change between seasons in the rhythm's τ of both the prolactin and cortisol patterns. In contrast, the HR cohort showed no change in the rhythm's τ between seasons for prolactin and cortisol patterns. These results show that in human beings, the presence of a circannual rhythm in the circadian time structure or the ability to adapt the circadian rhythmic pattern of these variables to external cues, such as seasons, is related to the partly genetically determined risk state to develop breast cancer and may be of importance for human health.     

Habitat selection by a large herbivore at multiple spatial and temporal scales is primarily governed by food resources

Habitat selection can be considered as a hierarchical process in which animals satisfy their habitat requirements at different ecological scales. Theory predicts that spatial and temporal scales should co‐vary in most ecological processes and that the most limiting factors should drive habitat selection at coarse ecological scales, but be less influential at finer scales. Using detailed location data on roe deer Capreolus capreolus inhabiting the Bavarian Forest National Park, Germany, we investigated habitat selection at several spatial and temporal scales. We tested 1) whether time‐varying patterns were governed by factors reported as having the largest effects on fitness, 2) whether the trade‐off between forage and predation risks differed among spatial and temporal scales and 3) if spatial and temporal scales are positively associated. We analysed the variation in habitat selection within the landscape and within home ranges at monthly intervals, with respect to land‐cover type and proxys of food and cover over seasonal and diurnal temporal scales. The fine‐scale temporal variation follows a nycthemeral cycle linked to diurnal variation in human disturbance. The large‐scale variation matches seasonal plant phenology, suggesting food resources being a greater limiting factor than lynx predation risk. The trade‐off between selection for food and cover was similar on seasonal and diurnal scale. Habitat selection at the different scales may be the consequence of the temporal variation and predictability of the limiting factors as much as its association with fitness. The landscape of fear might have less importance at the studied scale of habitat selection than generally accepted because of the predator hunting strategy. Finally, seasonal variation in habitat selection was similar at the large and small spatial scales, which may arise because of the marked philopatry of roe deer. The difference is supposed to be greater for wider ranging herbivores.