Target size and optimal life history when individual growth and energy budget are stochastic

I extend my previous work on life history optimization when body mass is divided into reserves and structure components. Two important innovations are: (1) effect of finite target size on optimal structural growth; (2) incorporating reproduction in the optimization objective. I derive optimal growth trajectories and life histories, given that the individual is subject to both starvation mortality and exogenous hazards (e.g., predation). Because of overhead costs in building structural mass, it is optimal to stop structural growth close to the target size, and to proceed only by accumulating reserves. Higher overhead costs cause earlier cessation of structural growth and smaller final structures. Semelparous reproduction also promotes early cessation of structural growth, compared to when only survival to target size is maximized. In contrast, iteroparous reproduction can prolong structural growth, resulting in larger final structures than in either the survival or the semelparous scenarios. Increasing the noise in individual growth lowers final structural mass at small target sizes, but the effect is reversed for large target sizes. My results provide predictions for comparative studies. I outline important consequences of my results to additional important evolutionary questions: evolution of sexual dimorphism, optimization of clutch size and evolution of progeny and adult sizes.     

Rainbow trout in seasonal environments: phenotypic trade‐offs across a gradient in winter duration

Survival through periods of resource scarcity depends on the balance between metabolic demands and energy storage. The opposing effects of predation and starvation mortality are predicted to result in trade‐offs between traits that optimize fitness during periods of resource plenty (e.g., during the growing season) and those that optimize fitness during periods of resource scarcity (e.g., during the winter). We conducted a common environment experiment with two genetically distinct strains of rainbow trout to investigate trade‐offs due to (1) the balance of growth and predation risk related to foraging rate during the growing season and (2) the allocation of energy to body size prior to the winter. Fry (age 0) from both strains were stocked into replicate natural lakes at low and high elevation that differed in winter duration (i.e., ice cover) by 59 days. Overwinter survival was lowest in the high‐elevation lakes for both strains. Activity rate and growth rate were highest at high elevation, but growing season survival did not differ between strains or between environments. Hence, we did not observe a trade‐off between growth and predation risk related to foraging rate. Growth rate also differed significantly between the strains across both environments, which suggests that growth rate is involved in local adaptation. There was not, however, a difference between strains or between environments in energy storage. Hence, we did not observe a trade‐off between growth and storage. Our findings suggest that intrinsic metabolic rate, which affects a trade‐off between growth rate and overwinter survival, may influence local adaptation in organisms that experience particularly harsh winter conditions (e.g., extended periods trapped beneath the ice in high‐elevation lakes) in some parts of their range.     

Group‐Size Effect on Vigilance and Foraging in a Predator‐Free Population of Feral Goats (Capra hircus) on the Isle of Rum,NW Scotland

Many previous studies have found that as group size increases, individual vigilance levels decrease and forage intake increases (group‐size effect), but few such studies have considered the impact of within‐group interactions and other confounding factors on the direction of group‐size effects. A free‐ranging population of feral goats (Capra hircus), with little predation threat, was studied on the Isle of Rum (northwest Scotland), from Jun. to Nov. 2000, to investigate the effects of group size on individual vigilance levels and foraging efficiency after taking into account the effect of confounding factors (e.g. sex, season, time of day, habitat, predation risk) and within‐group interactions (via changes in movement rates while feeding). Our results show that, while group size exerted a negative influence on individual vigilance levels and a positive effect on movement rate, foraging efficiency never increased with group size and even decreased at certain times of day. There was no sex difference in individual vigilance in feral goats, but foraging efficiency was higher in females than in males. Goats were more vigilant in fall than in summer. The results imply that the benefits for foraging obtained from the reduced vigilance level in larger groups may be constrained or offset by increased interaction (or competition) within larger groups even in a population that faces negligible predation risk.     

Is optimal foraging a realistic expectation in orb‐web spiders?

Abstract 1. Explanations for web relocation invoking optimal foraging require reliable differentiation between individual sites and overall habitat quality. We characterised natural conditions of resource variability over 20 days in artificial webs of the orb‐web spider Gasteracantha fornicata to examine this requirement. 2. Variability in catch success was high. Day‐to‐day catch success in 90% (18/20) catch sites fitted negative binomial distributions, whereas 10% fitted Poisson distributions. Considered across trap sites (overall habitat), variance in catch success increased proportionally faster than the mean (i.e. Taylor’s Power Law, variance = 0.54mean^1.764). 3. We compared the confidence intervals for the expected cumulative catch in randomly drawn sequential samples from a frequency distribution representing the overall habitat (based on the parameters for Taylor’s power law) and the frequency distribution of expected cumulative catch within each individual catch site [via randomisation based on the mean and negative binomial exponent (k)]. 4. In all cases and across all sample sizes, median values for the power to differentiate habitat and catch sites never exceeded 0.2, suggesting that principles involved in optimal foraging, if operating, must be accompanied by a very high degree of uncertainty. 5. Under conditions of high resource variability, many days must be spent in a single catch site if movement decisions are based on an ability to differentiate current catch site from overall habitat. Empirical evidence suggests this is never met. This may explain why proximal mechanisms that illicit quickly resolved behavioural responses have been more successful in describing web relocation patterns than those associated with optimal foraging.     

Using non‐linear mixed effects models to identify patterns of chick growth in House Sparrows Passer domesticus

For many animals, adult size is an important determinant of fitness. Thus, after a period of food restriction, offspring often grow quickly to approach an optimal size. Offspring can approach an optimal size by increasing mass faster than the peak growth of offspring that do not delay development (compensatory growth) or by extending the period of rapid growth to reach an optimal size (catch‐up growth). Unfortunately, the most common statistical techniques make it difficult to differentiate alternative growth patterns among developing offspring. Here, I show how random effect estimates can be used to uncover important variation in growth in a short‐lived passerine, the House Sparrow Passer domesticus. Specifically, I show that much of the variation in offspring growth can be explained by differences in the timing of peak growth and in final adult size, both within a single population and within treatments of an experimental manipulation. These results suggest that much of the variation in offspring growth may be explained by factors other than growth rate. I also show that offspring that delay development either maintain slow but steady growth across development and reach a small adult size, or extend the period of rapid growth to reach an optimal size, indicative of catch‐up growth. This pattern of extending the period of rapid growth may allow offspring to minimize the cellular damage caused by compensatory growth but still maximize size‐related fitness benefits (e.g. increased survival and fecundity) prior to fledging.     

Logic for designing nature reserves for multiple species

We examine the logic of designing nature reserves to understand better how to integrate the concepts of representativeness and persistence. Simple models of viability are used to evaluate how the expected number of species in the reserve system changes with variation in the risk of extinction among species, their rate of occurrence, and the distribution of species. The optimal size of individual reserves increased with the mean and variance of the probability of extinction among species and with the rate at which the risk of extinction declines with the cost of each reserve. In contrast, the rate of occurrence of species within reserves and their rate of accumulation with increasing reserve area had a relatively minor influence on the optimal size of reserves. Patterns of endemism were most important for the location of reserves. Including differences among species in the analysis reduced the optimal number of individual reserves (and increased the size of each) when operating under a fixed budget compared with reserve designs based on single species. A case study in the city of Melbourne, Australia, demonstrates the conservation value of small (approximately 1 ha) grassland reserves and the underrepresentation of Melbourne's volcanic plains in the region's conservation network.     

Individual‐based ecology of coastal birds

Conservation objectives for non‐breeding coastal birds (shorebirds and wildfowl) are determined from their population size at coastal sites. To advise coastal managers, models must predict quantitatively the effects of environmental change on population size or the demographic rates (mortality and reproduction) that determine it. As habitat association models and depletion models are not able to do this, we developed an approach that has produced such predictions thereby enabling policy makers to make evidence‐based decisions. Our conceptual framework is individual‐based ecology, in which populations are viewed as having properties (e.g. size) that arise from the traits (e.g. behaviour, physiology) and interactions of their constituent individuals. The link between individuals and populations is made through individual‐based models (IBMs) that follow the fitness‐maximising decisions of individuals and predict population‐level consequences (e.g. mortality rate) from the fates of these individuals. Our first IBM was for oystercatchers Haematopus ostralegus and accurately predicted their density‐dependent mortality. Subsequently, IBMs were developed for several shorebird and wildfowl species at several European sites, and were shown to predict accurately overwinter mortality, and the foraging behaviour from which predictions are derived. They have been used to predict the effect on survival in coastal birds of sea level rise, habitat loss, wind farm development, shellfishing and human disturbance. This review emphasises the wider applicability of the approach, and identifies other systems to which it could be applied. We view the IBM approach as a very useful contribution to the general problem of how to advance ecology to the point where we can routinely make meaningful predictions of how populations respond to environmental change.     

Genetic basis of between‐individual and within‐individual variance of docility

Between‐individual variation in phenotypes within a population is the basis of evolution. However, evolutionary and behavioural ecologists have mainly focused on estimating between‐individual variance in mean trait and neglected variation in within‐individual variance, or predictability of a trait. In fact, an important assumption of mixed‐effects models used to estimate between‐individual variance in mean traits is that within‐individual residual variance (predictability) is identical across individuals. Individual heterogeneity in the predictability of behaviours is a potentially important effect but rarely estimated and accounted for. We used 11 389 measures of docility behaviour from 1576 yellow‐bellied marmots (Marmota flaviventris) to estimate between‐individual variation in both mean docility and its predictability. We then implemented a double hierarchical animal model to decompose the variances of both mean trait and predictability into their environmental and genetic components. We found that individuals differed both in their docility and in their predictability of docility with a negative phenotypic covariance. We also found significant genetic variance for both mean docility and its predictability but no genetic covariance between the two. This analysis is one of the first to estimate the genetic basis of both mean trait and within‐individual variance in a wild population. Our results indicate that equal within‐individual variance should not be assumed. We demonstrate the evolutionary importance of the variation in the predictability of docility and illustrate potential bias in models ignoring variation in predictability. We conclude that the variability in the predictability of a trait should not be ignored, and present a coherent approach for its quantification.     

Partitioning within‐species variance in behaviour to within‐ and between‐population components for understanding evolution

Phenotypes vary at multiple hierarchical levels, of which the interspecific variance is the primary focus of phylogenetic comparative studies. However, the evolutionary role of particular within‐species variance components (between‐population, between‐ or within‐individual variances) remains neglected. Here, we partition the variance in an anti‐predator behaviour, flight initiation distance (FID), and assess how its within‐ and between‐population variance are related to life history, distribution, dispersal and habitat ecology. Although the composition of within‐species variance in FID depended on the phylogeny, most variance occurred within populations. When accounting for allometry, density‐dependence, uncertainty in the phylogenetic hypothesis and heterogeneity in data quality, within‐population variance was significantly associated with habitat diversity and population size. Between‐population variance was a significant predictor of natal dispersal, senescence and habitat diversity. Accordingly, not only species‐specific mean values of a behavioural trait, but also its variance within and among populations can shape the evolutionary ecology of species.     

Intragroup competition predicts individual foraging specialisation in a group‐living mammal

Individual foraging specialisation has important ecological implications, but its causes in group‐living species are unclear. One of the major consequences of group living is increased intragroup competition for resources. Foraging theory predicts that with increased competition, individuals should add new prey items to their diet, widening their foraging niche (‘optimal foraging hypothesis’). However, classic competition theory suggests the opposite: that increased competition leads to niche partitioning and greater individual foraging specialisation (‘niche partitioning hypothesis’). We tested these opposing predictions in wild, group‐living banded mongooses (Mungos mungo), using stable isotope analysis of banded mongoose whiskers to quantify individual and group foraging niche. Individual foraging niche size declined with increasing group size, despite all groups having a similar overall niche size. Our findings support the prediction that competition promotes niche partitioning within social groups and suggest that individual foraging specialisation may play an important role in the formation of stable social groupings.     

Life‐history constraints in grassland plant species: a growth‐defence trade‐off is the norm

Plant growth can be limited by resource acquisition and defence against consumers, leading to contrasting trade‐off possibilities. The competition‐defence hypothesis posits a trade‐off between competitive ability and defence against enemies (e.g. herbivores and pathogens). The growth‐defence hypothesis suggests that strong competitors for nutrients are also defended against enemies, at a cost to growth rate. We tested these hypotheses using observations of 706 plant populations of over 500 species before and following identical fertilisation and fencing treatments at 39 grassland sites worldwide. Strong positive covariance in species responses to both treatments provided support for a growth‐defence trade‐off: populations that increased with the removal of nutrient limitation (poor competitors) also increased following removal of consumers. This result held globally across 4 years within plant life‐history groups and within the majority of individual sites. Thus, a growth‐defence trade‐off appears to be the norm, and mechanisms maintaining grassland biodiversity may operate within this constraint.     

Carbohydrate as Fuel for Foraging,Resource Defense and Colony Growth – a Long‐term Experiment with the Plant‐ant Crematogaster nigriceps

Mismatches in nutrient composition (e.g., protein, carbohydrates, lipids, etc.) between consumers and the resources they depend on can have ecological consequences, affecting traits from individual behavior to community structure. In many terrestrial ecosystems, ants depend on plant and insect mutualist partners for carbohydrate‐rich rewards that are nutritionally unbalanced (especially in protein) relative to colony needs. Despite imbalances, many carbohydrate‐feeding ant mutualists dominate communities—both competitively and numerically—raising the question of whether excess carbohydrates ‘fuel’ colony acquisition of limiting resources and growth. In a 10‐month field study, we manipulated carbohydrate access for the obligate plant‐ant Crematogaster nigriceps to test whether carbohydrate availability could be mechanistically linked to ecological dominance via heightened territory defense, increased protein foraging, and colony growth. Supplementation increased aggressive defense of hosts after only two weeks, but was also strongly linked to variation in rainfall. Contrary to predictions, we did not find that supplemented colonies increased protein foraging. Instead, colonies with reduced carbohydrate access discovered a greater proportion of protein baits, suggesting that carbohydrate deprivation increases foraging intensity. We found no significant effect of carbohydrate manipulation on brood or alate production. These results contrast with findings from several recent short‐term and lab‐based nutrient supplementation studies and highlight the role of seasonality and biotic context in colony‐foraging and reproductive decisions. These factors may be essential to understanding the consequences of carbohydrate access in natural plant‐ant systems.     

The ‘truck‐driver’ effect in leaf‐cutting ants: how individual load influences the walking speed of nest‐mates

The foraging behaviour of social insects is highly flexible because it depends on the interplay between individual and collective decisions. In ants that use foraging trails, high ant flow may entail traffic problems if different workers vary widely in their walking speed. Slow ants carrying extra‐large loads in the leaf‐cutting ant Atta cephalotes L. (Hymenoptera: Formicidae) are characterized as ‘highly‐laden’ ants, and their effect on delaying other laden ants is analyzed. Highly‐laden ants carry loads that are 100% larger and show a 50% greater load‐carrying capacity (i.e. load size/body size) than ‘ordinary‐laden’ ants. Field manipulations reveal that these slow ants carrying extra‐large loads can reduce the walking speed of the laden ants behind them by up to 50%. Moreover, the percentage of highly‐laden ants decreases at high ant flow. Because the delaying effect of highly‐laden ants on nest‐mates is enhanced at high traffic levels, these results suggest that load size might be adjusted to reduce the negative effect on the rate of foraging input to the colony. Several causes have been proposed to explain why leaf‐cutting ants cut and carry leaf fragments of sizes below their individual capacities. The avoidance of delay in laden nest‐mates is suggested as another novel factor related to traffic flow that also might affect load size selection The results of the presennt study illustrate how leaf‐cutting ants are able to reduce their individual carrying performance to maximize the overall colony performance.     

Ontogenetic and spatial variation in size‐selective mortality of a marine fish

Although body size can affect individual fitness, ontogenetic and spatial variation in the ecology of an organism may determine the relative advantages of size and growth. During an 8‐year field study in the Bahamas, we examined selective mortality on size and growth throughout the entire reef‐associated life phase of a common coral‐reef fish, Stegastes partitus (the bicolour damselfish). On average, faster‐growing juveniles experienced greater mortality, though as adults, larger individuals had higher survival. Comparing patterns of selection observed at four separate populations revealed that greater population density was associated with stronger selection for larger adult size. Large adults may be favoured because they are superior competitors and less susceptible to gape‐limited predators. Laboratory experiments suggested that selective mortality of fast‐growing juveniles was likely because of risk‐prone foraging behaviour. These patterns suggest that variation in ecological interactions may lead to complex patterns of lifetime selection on body size.     

Behavioral signature of intraspecific competition and density dependence in colony‐breeding marine predators

In populations of colony‐breeding marine animals, foraging around colonies can lead to intraspecific competition. This competition affects individual foraging behavior and can cause density‐dependent population growth. Where behavioral data are available, it may be possible to infer the mechanism of intraspecific competition. If these mechanics are understood, they can be used to predict the population‐level functional response resulting from the competition. Using satellite relocation and dive data, we studied the use of space and foraging behavior of juvenile and adult gray seals (Halichoerus grypus) from a large (over 200,000) and growing population breeding at Sable Island, Nova Scotia (44.0 ^oN 60.0 ^oW). These data were first analyzed using a behaviorally switching state‐space model to infer foraging areas followed by randomization analysis of foraging region overlap of competing age classes. Patterns of habitat use and behavioral time budgets indicate that young‐of‐year juveniles (YOY) were likely displaced from foraging areas near (<10 km) the breeding colony by adult females. This displacement was most pronounced in the summer. Additionally, our data suggest that YOY are less capable divers than adults and this limits the habitat available to them. However, other segregating mechanisms cannot be ruled out, and we discuss several alternate hypotheses. Mark–resight data indicate juveniles born between 1998 and 2002 have much reduced survivorship compared with cohorts born in the late 1980s, while adult survivorship has remained steady. Combined with behavioral observations, our data suggest YOY are losing an intraspecific competition between adults and juveniles, resulting in the currently observed decelerating logistic population growth. Competition theory predicts that intraspecific competition resulting in a clear losing competitor should cause compensatory population regulation. This functional response produces a smooth logistic growth curve as carrying capacity is approached, and is consistent with census data collected from this population over the past 50 years. The competitive mechanism causing compensatory regulation likely stems from the capital‐breeding life‐history strategy employed by gray seals. This strategy decouples reproductive success from resources available around breeding colonies and prevents females from competing with each other while young are dependent.     

Short‐term insurance versus long‐term bet‐hedging strategies as adaptations to variable environments

Understanding how organisms adapt to environmental variation is a key challenge of biology. Central to this are bet‐hedging strategies that maximize geometric mean fitness across generations, either by being conservative or diversifying phenotypes. Theoretical models have identified environmental variation across generations with multiplicative fitness effects as driving the evolution of bet‐hedging. However, behavioral ecology has revealed adaptive responses to additive fitness effects of environmental variation within lifetimes, either through insurance or risk‐sensitive strategies. Here, we explore whether the effects of adaptive insurance interact with the evolution of bet‐hedging by varying the position and skew of both arithmetic and geometric mean fitness functions. We find that insurance causes the optimal phenotype to shift from the peak to down the less steeply decreasing side of the fitness function, and that conservative bet‐hedging produces an additional shift on top of this, which decreases as adaptive phenotypic variation from diversifying bet‐hedging increases. When diversifying bet‐hedging is not an option, environmental canalization to reduce phenotypic variation is almost always favored, except where the tails of the fitness function are steeply convex and produce a novel risk‐sensitive increase in phenotypic variance akin to diversifying bet‐hedging. Importantly, using skewed fitness functions, we provide the first model that explicitly addresses how conservative and diversifying bet‐hedging strategies might coexist.     

Predation risk influences food‐web structure by constraining species diet choice

The foraging behaviour of species determines their diet and, therefore, also emergent food‐web structure. Optimal foraging theory (OFT) has previously been applied to understand the emergence of food‐web structure through a consumer‐centric consideration of diet choice. However, the resource‐centric viewpoint, where species adjust their behaviour to reduce the risk of predation, has not been considered. We develop a mechanistic model that merges metabolic theory with OFT to incorporate the effect of predation risk on diet choice to assemble food webs. This ‘predation‐risk‐compromise’ (PR) model better captures the nestedness and modularity of empirical food webs relative to the classical optimal foraging model. Specifically, compared with optimal foraging alone, risk‐mitigated foraging leads to more‐nested but less‐modular webs by broadening the diet of consumers at intermediate trophic levels. Thus, predation risk significantly affects food‐web structure by constraining species’ ability to forage optimally, and needs to be considered in future work.     

Predator‐induced phenotypic plasticity in an arid‐adapted tropical tadpole

Adaptive phenotypic plasticity is widespread and involves diverse phenotypes. Key environmental stressors, such as predation risk, can simultaneously induce changes in multiple traits, but the magnitude of response is dependent upon the environmental conditions. Species that utilize temporary ponds are expected to exhibit stronger predator‐induced responses in the form of morphology than behaviour (i.e. reduced activity) to meet the demands of rapid development by maintaining high foraging activity while reducing predation risk via morphologically plastic traits. In a laboratory experiment, I examined the effects of predator chemical cues and conspecific alarm cues on activity, development and morphology on Leptodactylus bufonius tadpoles. This species has terrestrial oviposition and completes the early part of its development outside of ephemeral and temporary ponds in the Gran Chaco ecoregion of South America. Tadpoles in the predator treatments exhibited both behavioural and morphological predator‐induced plastic responses. Tadpoles tended to possess shorter, deeper tails when exposed to predators. The greatest reduction in activity was observed in tadpoles exposed to both predator and conspecific alarm cues, which subsequently resulted in the slowest development. Temporary and ephemeral pond adapted species with terrestrial oviposition may capitalize on a head start in development by being able to afford reduced growth rates via a reduction in activity. This may occur when the constraints imposed by pond hydroperiod (e.g. risk of pond drying) are relaxed when compared with species with aquatic oviposition, which must undergo all stages of development during the pond's hydroperiod. Thus, in addition to the predator and hydroperiod gradients, examining phenotypically plastic responses along a ‘terrestriality gradient’ in a comparative framework would provide insights as to the costs and benefits of increasing terrestriality in anuran reproductive modes to environmental stressors.     

Aegean wall lizards switch foraging modes,diet, and morphology in a human‐built environment

Foraging mode is a functional trait with cascading impacts on ecological communities. The foraging syndrome hypothesis posits a suite of concurrent traits that vary with foraging mode; however, comparative studies testing this hypothesis are typically interspecific. While foraging modes are often considered typological for a species when predicting foraging‐related traits or mode‐specific cascading impacts, intraspecific mode switching has been documented in some lizards. Mode‐switching lizards provide an opportunity to test foraging syndromes and explore how intraspecific variability in foraging mode might affect local ecological communities.Because lizard natural history is intimately tied to habitat use and structure, I tested for mode switching between populations of the Aegean wall lizard, Podarcis erhardii, inhabiting undisturbed habitat and human‐built rock walls on the Greek island of Naxos. I observed foraging behavior among 10 populations and tested lizard morphological and performance predictions at each site. Furthermore, I investigated the diet of lizards at each site relative to the available invertebrate community.I found that lizards living on rock walls were significantly more sedentary—sit and wait—than lizards at nonwall sites. I also found that head width increased in females and the ratio of hindlimbs to forelimbs in both sexes increased as predicted. Diet also changed, with nonwall lizards consuming a higher proportion of sedentary prey. Lizard bite force also varied significantly between sites; however, the pattern observed was opposite to that predicted, suggesting that bite force in these lizards may more closely relate to intraspecific competition than to diet.This study demonstrates microgeographic variability in lizard foraging mode as a result of human land use. In addition, these results demonstrate that foraging mode syndromes can shift intraspecifically with potential cascading effects on local ecological communities.