Structure and mechanism of diet specialisation: testing models of individual variation in resource use with sea otters

Studies of consumer-resource interactions suggest that individual diet specialisation is empirically widespread and theoretically important to the organisation and dynamics of populations and communities. We used weighted networks to analyze the resource use by sea otters, testing three alternative models for how individual diet specialisation may arise. As expected, individual specialisation was absent when otter density was low, but increased at high-otter density. A high-density emergence of nested resource-use networks was consistent with the model assuming individuals share preference ranks. However, a density-dependent emergence of a non-nested modular network for 'core' resources was more consistent with the 'competitive refuge' model. Individuals from different diet modules showed predictable variation in rank-order prey preferences and handling times of core resources, further supporting the competitive refuge model. Our findings support a hierarchical organisation of diet specialisation and suggest individual use of core and marginal resources may be driven by different selective pressures.     

Individual diet specialisation in sparrows is driven by phenotypic plasticity in traits related to trade‐offs in animal performance

Individual diet specialisation (IS) is frequent in many animal taxa and affects population and community dynamics. The niche variation hypothesis (NVH) predicts that broader population niches should exhibit greater IS than populations with narrower niches, and most studies that examine the ecological factors driving IS focus on intraspecific competition. We show that phenotypic plasticity of traits associated with functional trade‐offs is an important, but unrecognised mechanism that promotes and maintains IS. We measured nitrogen isotope (δ¹⁵N) and digestive enzyme plasticity in four populations of sparrows (Zonotrichia capensis) to explore the relationship between IS and digestive plasticity. Our results show that phenotypic plasticity associated with functional trade‐offs is related in a nonlinear fashion with the degree of IS and positively with population niche width. These findings are opposite to the NVH and suggest that among individual differences in diet can be maintained via acclimatisation and not necessarily require a genetic component.     

An evolutionary ecology of individual differences

Individuals often differ in what they do. This has been recognised since antiquity. Nevertheless, the ecological and evolutionary significance of such variation is attracting widespread interest, which is burgeoning to an extent that is fragmenting the literature. As a first attempt at synthesis, we focus on individual differences in behaviour within populations that exceed the day-to-day variation in individual behaviour (i.e. behavioural specialisation). Indeed, the factors promoting ecologically relevant behavioural specialisation within natural populations are likely to have far-reaching ecological and evolutionary consequences. We discuss such individual differences from three distinct perspectives: individual niche specialisations, the division of labour within insect societies and animal personality variation. In the process, while recognising that each area has its own unique motivations, we identify a number of opportunities for productive 'cross-fertilisation' among the (largely independent) bodies of work. We conclude that a complete understanding of evolutionarily and ecologically relevant individual differences must specify how ecological interactions impact the basic biological process (e.g. Darwinian selection, development and information processing) that underpin the organismal features determining behavioural specialisations. Moreover, there is likely to be co-variation amongst behavioural specialisations. Thus, we sketch the key elements of a general framework for studying the evolutionary ecology of individual differences.     

Environmental stability increases relative individual specialisation across populations of an aquatic top predator

The concept of the niche has long been a central pillar in ecological theory, with a traditional focus on quantifying niches at the species or population level. However, the importance of individual‐level niche variation is increasingly being recognised, with a strong focus on individual specialisation. While examples illustrating the contribution of the individual niche to whole population niche structure are accumulating rapidly, surprisingly little is known about the conditions that shape the differences between these two potentially divergent components. Though theory predicts that stability should influence the extent of such intra‐specific specialisation, we know of no previous study that has investigated its role in individual specialisation, and the differentiation between individual‐ and population niches. Here, we studied the diet of individuals from multiple populations of an aquatic top‐predator, Salmo trutta, inhabiting contrasting stable, groundwater fed and unstable, surface water fed pre‐alpine streams. Based on stomach content analysis, we found that individuals living in stable environments displayed a higher degree of specialisation than those in unstable environments, with the between‐individual component of niche width being approximately twice as high in the former. We subsequently validated these results by evidence gained from stable isotope analysis of muscle tissue. As such, we reveal that environmental stability can significantly influence individual niches within populations, leading to increased specialisation.     

An experimental approach to the formation of diet preferences and individual specialisation in European mink

Individual dietary specialisation can occur within populations even when average diets suggest that the population has a generalist feeding strategy. Individual specialisation may impact fitness and has been related to demographic traits, ecological opportunity, competition, learning and animal personality. However, the causation and formation of individual specialisation are not fully understood. Experiments on animals raised in controlled environments provide an opportunity to examine dietary preferences and learning largely independent from variation in lifetime experiences and ecological opportunity. Here, we use a feeding experiment to examine individual specialisation and learning in captive bred European mink (Mustela lutreola) in an Estonian conservation programme. In a series of cafeteria experiments, animals could choose between one familiar food item (Baltic herring Clupea harengus membras) and two initially novel ones (noble crayfish Astacus astacus and house mouse Mus musculus). In general, mice were rarely eaten whilst crayfish consumption increased over time and fish decreased. At the individual level, there was a mix of generalists and crayfish or fish specialists, and the individuals differed in learning time in relation to novel prey. Our results indicate that individual variation in innate preferences and learning both contributes to individual diet specialisation. The differences in learning indicate individual variation in behavioural plasticity, which in turn can be related to personality. This could be of concern in conservation, as personality has been shown to affect survival in translocations.     

Endocrine mechanisms,behavioral phenotypes and plasticity: known relationships and open questions

Behavior of wild vertebrate individuals can vary in response to environmental or social factors. Such within-individual behavioral variation is often mediated by hormonal mechanisms. Hormones also serve as a basis for among-individual variations in behavior including animal personalities and the degree of responsiveness to environmental and social stimuli. How do relationships between hormones and behavioral traits evolve to produce such behavioral diversity within and among individuals? Answering questions about evolutionary processes generating among-individual variation requires characterizing how specific hormones are related to variation in specific behavioral traits, whether observed hormonal variation is related to individual fitness and, whether hormonal traits are consistent (repeatable) aspects of an individual's phenotype. With respect to within-individual variation, we need to improve our insight into the nature of the quantitative relationships between hormones and the traits they regulate, which in turn will determine how they may mediate behavioral plasticity of individuals. To address these questions, we review the actions of two steroid hormones, corticosterone and testosterone, in mediating changes in vertebrate behavior, focusing primarily on birds. In the first part, we concentrate on among-individual variation and present examples for how variation in corticosterone concentrations can relate to behaviors such as exploration of novel environments and parental care. We then review studies on correlations between corticosterone variation and fitness, and on the repeatability over time of corticosterone concentrations. At the end of this section, we suggest that further progress in our understanding of evolutionary patterns in the hormonal regulation of behavior may require, as one major tool, reaction norm approaches to characterize hormonal phenotypes as well as their responses to environments.In the second part, we discuss types of quantitative relationships between hormones and behavioral traits within individuals, using testosterone as an example. We review conceptual models for testosterone-behavior relationships and discuss the relevance of these models for within-individual plasticity in behavior. Next, we discuss approaches for testing the nature of quantitative relationships between testosterone and behavior, concluding that again reaction norm approaches might be a fruitful way forward.We propose that an integration of new tools, especially of reaction norm approaches into the field of behavioral endocrinology will allow us to make significant progress in our understanding of the mechanisms, the functional implications and the evolution of hormone–behavior relationships that mediate variation both within and among individuals. This knowledge will be crucial in light of already ongoing habitat alterations due to global change, as it will allow us to evaluate the mechanisms as well as the capacity of wild populations to adjust hormonally-mediated behaviors to altered environmental conditions.     

Water temperature and mixing depth affect timing and magnitude of events during spring succession of the plankton

Individual-level diet variation can be easily quantified by gut-content analysis. However, because gut contents are a ‘snapshot’ of individuals’ feeding habits, such cross-sectional data can be subject to sampling error and lead one to overestimate levels of diet variation. In contrast, stable isotopes reflect an individual’s long-term diet, so isotope variation among individuals can be interpreted as diet variation. Nevertheless, population isotope variances alone cannot be directly compared among populations, because they depend on both the level of diet variation and the variance of prey isotope ratios. We developed a method to convert population isotope variances into a standardized index of individual specialization (WIC/TNW) that can be compared among populations, or to gut-content variation. We applied this method to diet and carbon isotope data of four species of frogs of the Brazilian savannah. Isotopes showed that gut contents provided a reliable measure of diet variation in three populations, but greatly overestimated diet variation in another population. Our method is sensitive to incomplete sampling of the prey and to among-individual variance in fractionation. Therefore, thorough sampling of prey and estimates of fractionation variance are desirable. Otherwise, the method is straightforward and provides a new tool for quantifying individual-level diet variation in natural populations that combines both gut-content and isotope data. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Postnatal Dynamics of Developmental Stability and Canalization of Lizard Head Shape Under Different Environmental Conditions

Developmental stability (DS) and canalization are key determinants of phenotypic variation. To provide a better understanding of how postnatal growth is involved in determining the effects of DS and canalization on phenotypic variation, we studied within- and among-individual variation in head shape in ontogenetic series of lizards inhabiting urban and rural environments. Urban lizards exhibited increased fluctuating asymmetry during the early postnatal stages, but asymmetry levels decreased during growth. By contrast, asymmetry remained constant across the investigated size range in the rural population. In addition, urban juveniles were more variable for symmetric shape and deviated more from the group shape-size allometric trajectory, but both indices declined across ontogeny. Congruent patterns of within- and among-individual variation suggest that both DS and canalization may rely on similar underlying mechanisms. Further, the ontogenetic reduction of variation in the urban population suggests that compensatory growth may aid in buffering phenotypic variation and correcting deviances from the established developmental path. Alternatively, passive mechanisms and population dynamics may also explain the decrease of phenodeviants in urban populations. Significant correlations between symmetric and asymmetric shape, as well as similar integration patterns between the two populations, suggest that similar developmental mechanisms regulate head shape in both environments. Overall, these results highlight the relevance of both pre- and post-natal dynamics in determining levels of phenotypic variation, enhancing our understanding of how organisms respond to perturbations to DS and canalization under stressful conditions.     

Individual foraging specialisation in a social mammal: the European badger (Meles meles)

Individual specialisation has been identified in an increasing number of animal species and populations. However, in some groups, such as terrestrial mammals, it is difficult to disentangle individual niche variation from spatial variation in resource availability. In the present study, we investigate individual variation in the foraging niche of the European badger (Meles meles), a social carnivore that lives in a shared group territory, but forages predominantly alone. Using stable isotope analysis, we distinguish the extent to which foraging variation in badgers is determined by social and spatial constraints and by individual differences within groups. We found a tendency for individual badgers within groups to differ markedly and consistently in their isotope values, suggesting that individuals living with access to the same resources occupied distinctive foraging niches. Although sex had a significant effect on isotope values, substantial variation within groups occurred independently of age and sex. Individual differences were consistent over a period of several months and in some instances were highly consistent across the two years of the study, suggesting long-term individual foraging specialisations. Individual specialisation in foraging may, therefore, persist in populations of territorial species not solely as a result of spatial variation in resources, but also arising from individuals selecting differently from the same available resources. Although the exact cause of this behaviour is unknown, we suggest that specialisation may occur due to learning trade-offs which may limit individual niche widths. However, ecological factors at the group level, such as competition, may also influence the degree of specialisation.     

Context-dependent specialisation drives temporal dynamics in intra- and inter-individual variation in foraging behaviour within a generalist bird population

Individual niche variation is common within animal populations, and has significant implications for a wide range of ecological and evolutionary processes. However, individual niche differences may also temporally vary as a result of behavioural plasticity. While it is well understood how niche variation is affected by changes in resource availability, comparatively little is known about the extent to which individual niche differences may vary within the annual cycle due to internal drivers. Here, we assess how time- and energy-constraints imposed by incubating and brood rearing affect inter- and intra-individual variation in the foraging behaviour of lesser black-backed gulls, a generalist seabird with strong individual niche variation. To this end, we compared daily foraging trips of 22 breeding and 23 non-breeding GPS-tracked adult gulls from two colonies in the Southern Bight of the North Sea over the course of the breeding season. We find that breeding birds, unlike non-breeding ones, did indeed alter their foraging behaviour during the breeding season. Both sexes reduced their searching effort by increasingly revisiting earlier foraging locations, allowing for shorter and more frequent foraging trips. Breeding females also showed pronounced shifts in their habitat use and strongly specialised on urbanised foraging habitats throughout the breeding season. Hence, while individual variation in habitat use remained largely consistent within non-breeders and in breeding males, individual variation among breeding females almost completely disappeared. Female lesser black-backed gulls are on average smaller, and therefore often outcompeted by males for the most profitable food sources. The temporal specialisation on spatially reliable anthropogenic food sources during breeding hence suggests a complex interplay between intrinsic competitive constraints, resource reliability and shifting time- and energy budges in shaping temporal dynamics in individual niche variation within our study population.     

Ontogenetic and individual diet variation in amphibian larvae across an environmental gradient

1. Variation among individuals within size or age classes can have profound effects on community dynamics and food‐web structure. We investigated the potential influence of habitat disturbance on intrapopulation niche variation. 2. Amphibians occupy a range of lentic habitats from short‐hydroperiod intermittent ponds to long‐hydroperiod permanent ponds. We quantified ontogenetic diet variation and individual specialisation in wood frog tadpoles (Lithobates sylvaticus) and blue‐spotted salamander larvae (Ambystoma laterale) to investigate the influence of hydroperiod on population niche width across a natural hydroperiod gradient using stable isotope and gut content analyses. In one of the few tests using larval forms, we tested the niche variation hypothesis, which predicts that populations with larger niche widths also have increased individual variation. 3. Our results support the niche variation hypothesis, indicating that more generalised populations exhibit higher within‐individual diet variation. We report gradual changes in the relative importance of diet items, decreased dietary overlap and increased trophic position in L. sylvaticus throughout development. A. laterale became more enriched in δ¹³C and increased in δ¹⁵N throughout its larval period. We did not find a relationship between hydroperiod and niche parameters, indicating that niches are conserved across heterogeneous habitats. In contrast to most documented cases, we estimated low levels of individual specialisation in amphibian larvae. 4. Amphibians are an important link between aquatic and terrestrial ecosystems, whereby diet shifts can influence food‐web structure by altering energy flow pathways and the trophic position of higher consumers, ultimately changing food‐chain length.     

The influence of habitat accessibility on the dietary and morphological specialisation of an aquatic predator

Individual diet and habitat specialisation are widespread in animal taxa and often related to levels of predation and competition. Mobile consumers such as predatory fish can stabilise lake food webs by ranging over a larger area than their prey, thereby switching between habitats. Although, this switching assumes that the predator has equal preference for the available prey, individual diet specialisation and morphological adaptations to different habitats could potentially prevent individuals from switching between habitats. In this study, we assessed the niche width and individual specialisation in Eurasian perch Perca fluviatilis in response to a shift in habitat use by manipulating the ability for this top predator to couple habitats. We ran an eight weeks pond experiment, to test the effect of habitat switching on diet and morphological specialisations. We show that habitat coupling influenced individual diet specialisation and niche use in expected directions where specialisation increased with decreasing habitat switching. In contrast to expectations, the morphological variation decreased with increasing diet specialisation. Our results expand on previous work and suggest that individual specialisation and niche width can impact the ability of mobile predators to couple habitats. Furthermore, it shows the importance of individual specialisations in relation to habitat coupling.     

Population-level consequences of polymorphism, plasticity and randomized phenotype switching: a review of predictions

The consequences of among-individual phenotypic variation for the performance and ecological success of populations and species has attracted growing interest in recent years. Earlier reviews of this field typically address the consequences for population processes of one specific source of variation (plasticity or polymorphism), or consider one specific aspect of population performance, such as rate of speciation. Here we take a broader approach and study earlier reviews in order to summarize and compare predictions regarding several population-level consequences of phenotypic variation stemming from genetic polymorphism, developmental plasticity or randomized phenotype switching. Unravelling cause-dependent consequences of variation may increase our ability to understand the ecological dynamics of natural populations and communities, develop more informed management plans for protection of biodiversity, suggest possible routes to increased productivity and yield in natural and managed biological systems, and resolve inconsistencies in patterns and results seen in studies of different model systems. We find an overall agreement regarding the effects of higher levels of phenotypic variation generated by different sources, but also some differences between fine-grained and coarse-grained environments, modular and unitary organisms, mobile and sessile organisms, and between flexible and fixed traits. We propose ways to test the predictions and identify issues where current knowledge is limited and future lines of investigation promise to provide important novel insights.     

Linking individual diet variation and fecundity in an omnivorous marine consumer

Individual diet variation is a common feature of populations. This variation may be particularly common in near-shore marine benthic habitats where omnivory is prevalent and prey availability is spatially variable. Accurately predicting population responses to anthropogenic change that is occurring rapidly in these systems requires a quantitative link between individual diet variation and fecundity. Here I develop this quantitative link for the European green crab Carcinus maenas, specifically focusing on variation in the relative amounts of plant and animal material included in the diet. I demonstrate both short- and long-term diet variation between crabs as well as large individual variation in fecundity. I then quantitatively link variation in diet and fecundity using a laboratory feeding experiment. Fecundity increased by approximately 5,200 eggs when daily consumption of animal tissue increased by 1 % of body weight, but was not influenced by the most commonly consumed algal species. Results presented here have important implications for understanding population dynamics in general, and also provide information necessary for accurately predicting population growth of this widespread invader.     

Niche expansion and the niche variation hypothesis: does the degree of individual variation increase in depauperate assemblages?

The niche expansion and niche variation hypotheses predict that release from interspecific competition will promote niche expansion in depauperate assemblages. Niche expansion can occur by different mechanisms, including an increase in within-individual, among-individual, or bimodal variation (sexual dimorphism). Here we explore whether populations with larger niche breadth have a higher degree of diet variation. We also test whether populations from depauperate lizard assemblages differ in dietary resource use with respect to variation within and/or among individuals and sexual dimorphism. We found support for the niche expansion and niche variation hypotheses. Populations in assemblages with low phylogenetic diversity had a higher degree of individual variation, suggesting a tendency for niche expansion. We also found evidence suggesting that the mechanism causing niche expansion is an increase in variation among individuals rather than an increase in within-individual variation or an increase in bimodal variation due to sexual dimorphism.     

Population and life-history consequences of within-cohort individual variation

The consequences of within-cohort (i.e., among-individual) variation for population dynamics are poorly understood, in particular for the case where life history is density dependent. We develop a physiologically structured population model that incorporates individual variation among and within cohorts and allows us to explore the intertwined relationship between individual life history and population dynamics. Our model is parameterized for the lizard Zootoca vivipara and reproduces well the species' dynamics and life history. We explore two common mechanisms that generate within-cohort variation: variability in food intake and variability in birth date. Predicted population dynamics are inherently very stable and do not qualitatively change when either of these sources of individual variation is introduced. However, increased within-cohort variation in food intake leads to changes in morphology, with longer but skinnier individuals, even though mean food intake does not change. Morphological changes result from a seemingly universal nonlinear relationship between growth and resource availability but may become apparent only in environments with strongly fluctuating resources. Overall, our results highlight the importance of using a mechanistic framework to gain insights into how different sources of intraspecific variability translate into life-history and population-dynamic changes.     

Variability of individual genetic load: consequences for the detection of inbreeding depression

Inbreeding depression is a key factor affecting the persistence of natural populations, particularly when they are fragmented. In species with mixed mating systems, inbreeding depression can be estimated at the population level by regressing the average progeny fitness by the selfing rate of their mothers. We applied this method using simulated populations to investigate how population genetic parameters can affect the detection power of inbreeding depression. We simulated individual selfing rates and genetic loads from which we computed fitness values. The regression method yielded high statistical power, inbreeding depression being detected as significant (5?% level) in 92?% of the simulations. High individual variation in selfing rate and high mean genetic load led to better detection of inbreeding depression while high among-individual variation in genetic load made it more difficult to detect inbreeding depression. For a constant sampling effort, increasing the number of progenies while decreasing the number of individuals per progeny enhanced the detection power of inbreeding depression. We discuss the implication of among-mother variability of genetic load and selfing rate on inbreeding depression studies.     

The community and ecosystem consequences of intraspecific diversity: a meta‐analysis

Understanding the relationships between biodiversity and ecosystem functioning has major implications. Biodiversity–ecosystem functioning relationships are generally investigated at the interspecific level, although intraspecific diversity (i.e. within‐species diversity) is increasingly perceived as an important ecological facet of biodiversity. Here, we provide a quantitative and integrative synthesis testing, across diverse plant and animal species, whether intraspecific diversity is a major driver of community dynamics and ecosystem functioning. We specifically tested (i) whether the number of genotypes/phenotypes (i.e. intraspecific richness) or the specific identity of genotypes/phenotypes (i.e. intraspecific variation) in populations modulate the structure of communities and the functioning of ecosystems, (ii) whether the ecological effects of intraspecific richness and variation are strong in magnitude, and (iii) whether these effects vary among taxonomic groups and ecological responses. We found a non‐linear relationship between intraspecific richness and community and ecosystem dynamics that follows a saturating curve shape, as observed for biodiversity–function relationships measured at the interspecific level. Importantly, intraspecific richness modulated ecological dynamics with a magnitude that was equal to that previously reported for interspecific richness. Our results further confirm, based on a database containing more than 50 species, that intraspecific variation also has substantial effects on ecological dynamics. We demonstrated that the effects of intraspecific variation are twice as high as expected by chance, and that they might have been underestimated previously. Finally, we found that the ecological effects of intraspecific variation are not homogeneous and are actually stronger when intraspecific variation is manipulated in primary producers than in consumer species, and when they are measured at the ecosystem rather than at the community level. Overall, we demonstrated that the two facets of intraspecific diversity (richness and variation) can both strongly affect community and ecosystem dynamics, which reveals the pivotal role of within‐species biodiversity for understanding ecological dynamics.     

Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology

The idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza. Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes. We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta‐analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub‐specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource‐axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals. These findings are highly relevant to conservation management because they imply ecological non‐exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning. Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators. Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over‐predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.