David M. Post

Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses

Within an organism, lipids are depleted in 13C relative to proteins and carbohydrates (more negative δ13C), and variation in lipid content among organisms or among tissue types has the potential to introduce considerable bias into stable isotope analyses that use δ13C. Despite the potential for introduced error, there is no consensus on the need to account for lipids in stable isotope analyses. Here we address two questions: (1) If and when is it important to account for the effects of variation in lipid content on δ13C? (2) If it is important, which method(s) are reliable and robust for dealing with lipid variation? We evaluated the reliability of direct chemical extraction, which physically removes lipids from samples, and mathematical normalization, which uses the carbon-to-nitrogen (C:N) ratio of a sample to normalize δ13C after analysis by measuring the lipid content, the C:N ratio, and the effect of lipid content on δ13C (Δδ13C) of plants and animals with a wide range of lipid contents. For animals, we found strong relationships between C:N and lipid content, between lipid content and Δδ13C, and between C:N and Δδ13C. For plants, C:N was not a good predictor of lipid content or Δδ13C, but we found a strong relationship between carbon content and lipid content, lipid content and Δδ13C, and between and carbon content and Δδ13C. Our results indicate that lipid extraction or normalization is most important when lipid content is variable among consumers of interest or between consumers and end members, and when differences in δ13C between end members is <10–12‰. The vast majority of studies using natural variation in δ13C fall within these criteria. Both direct lipid extraction and mathematical normalization reduce biases in δ13C, but mathematical normalization simplifies sample preparation and better preserves the integrity of samples for δ15N analysis.

CAN STABLE ISOTOPE RATIOS PROVIDE FOR COMMUNITY‐WIDE MEASURES OF TROPHIC STRUCTURE?

Stable isotope ratios (typically of carbon and nitrogen) provide one representation of an organisms trophic niche and are widely used to examine aspects of food web structure. Yet stable isotopes have not been applied to quantitatively characterize community-wide aspects of trophic structure (i.e., at the level of an entire food web). We propose quantitative metrics that can be used to this end, drawing on similar approaches from ecomorphology research. For example, the convex hull area occupied by species in δ13C–δ15N niche space is a representation of the total extent of trophic diversity within a food web, whereas mean nearest neighbor distance among all species pairs is a measure of species packing within trophic niche space. To facilitate discussion of opportunities and limitations of the metrics, we provide empirical and conceptual examples drawn from Bahamian tidal creek food webs. These examples illustrate how this methodology can be used to quantify trophic diversity and trophic redundancy in food webs, as well as to link individual species to characteristics of the food web in which they are embedded. Building from extensive applications of stable isotope ratios by ecologists, the community-wide metrics may provide a new perspective on food web structure, function, and dynamics.

Applying stable isotopes to examine food-web structure: an overview of analytical tools

Stable isotope analysis has emerged as one of the primary means for examining the structure and dynamics of food webs, and numerous analytical approaches are now commonly used in the field. Techniques range from simple, qualitative inferences based on the isotopic niche, to Bayesian mixing models that can be used to characterize food‐web structure at multiple hierarchical levels. We provide a comprehensive review of these techniques, and thus a single reference source to help identify the most useful approaches to apply to a given data set. We structure the review around four general questions: (1) what is the trophic position of an organism in a food web?; (2) which resource pools support consumers?; (3) what additional information does relative position of consumers in isotopic space reveal about food‐web structure?; and (4) what is the degree of trophic variability at the intrapopulation level? For each general question, we detail different approaches that have been applied, discussing the strengths and weaknesses of each. We conclude with a set of suggestions that transcend individual analytical approaches, and provide guidance for future applications in the field.

The long and short of food-chain length

Abstract Food-chain length is a central characteristic of ecological communities that has attracted considerable attention for over 75 years because it strongly affects community structure, ecosystem processes and contaminant concentrations. Conventional wisdom holds that either resource availability or dynamical stability limit food-chain length; however, new studies and new techniques challenge the conventional wisdom and broaden the discourse on food-chain length. Recent results suggest that resource availability limits food-chain length only in systems with very low resource availability, and call into question the theoretical basis for dynamical stability as a determinant of food-chain length. Evidence currently points towards a complex and contingent framework of interacting constraints that includes the history of community organization, resource availability, the type of predator–prey interactions, disturbance and ecosystem size. Within this framework, the debate has shifted from a search for singular explanations to a search for when and where different constraints operate to determine food-chain length.

Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play

Interactions between natural selection and environmental change are well recognized and sit at the core of ecology and evolutionary biology. Reciprocal interactions between ecology and evolution, eco-evolutionary feedbacks, are less well studied, even though they may be critical for understanding the evolution of biological diversity, the structure of communities and the function of ecosystems. Eco-evolutionary feedbacks require that populations alter their environment (niche construction) and that those changes in the environment feed back to influence the subsequent evolution of the population. There is strong evidence that organisms influence their environment through predation, nutrient excretion and habitat modification, and that populations evolve in response to changes in their environment at time-scales congruent with ecological change (contemporary evolution). Here, we outline how the niche construction and contemporary evolution interact to alter the direction of evolution and the structure and function of communities and ecosystems. We then present five empirical systems that highlight important characteristics of eco-evolutionary feedbacks: rotifer–algae chemostats; alewife–zooplankton interactions in lakes; guppy life-history evolution and nutrient cycling in streams; avian seed predators and plants; and tree leaf chemistry and soil processes. The alewife–zooplankton system provides the most complete evidence for eco-evolutionary feedbacks, but other systems highlight the potential for eco-evolutionary feedbacks in a wide variety of natural systems.

Lake ecosystems: Rapid evolution revealed by dormant eggs

Natural selection can lead to rapid changes in organisms, which can in turn influence ecosystem processes. A key factor in the functioning of lake ecosystems is the rate at which primary producers are eaten, and major consumers, such as the zooplankton Daphnia, can be subject to strong selection pressures when phytoplankton assemblages change. Lake Constance in central Europe experienced a period of eutrophication (the biological effects of an input of plant nutrients) during the 1960s–70s, which caused an increase in the abundance of nutritionally poor or even toxic cyanobacteria. By hatching long-dormant eggs of Daphnia galeata found in lake sediments, we show that the mean resistance of Daphnia genotypes to dietary cyanobacteria increased significantly during this eutrophication. This rapid evolution of resistance has implications for the ways that ecosystems respond to nutrient enrichment through the impact of grazers on primary production.

NATURAL SELECTION FOR GRAZER RESISTANCE TO TOXIC CYANOBACTERIA: EVOLUTION OF PHENOTYPIC PLASTICITY?

Abstract We studied the selection response of the freshwater grazing zooplankter, Daphnia galeata, to increased abundance of cyanobacteria in its environment. Cyanobacteria are a poor‐quality and often toxic food. Distinct genotypes of D. galeata were hatched from diapausing eggs extracted from three time horizons in the sediments of Lake Constance, Europe, covering the period 1962 to 1997, a time of change in both the prevalence of planktonic cyanobacteria and levels of phosphorus pollution. We assessed whether the grazers evolved to become more resistant to dietary cyanobacteria by exposing genetically distinct clones to two diets, one composed only of the nutritious green alga, Scenedesmus obliquus (good food), and the other a mixture of S. obliquus and the toxic cyanobacterium Microcystis aeruginosa (poor food). Genotype performance was measured as the specific rate of weight gain from neonate to maturity (gj).

INDIVIDUAL VARIATION IN THE TIMING OF ONTOGENETIC NICHE SHIFTS IN LARGEMOUTH BASS

The transition to piscivory is a crucial ontogenetic niche shift for many primarily piscivorous fishes. An early transition to piscivory may increase growth, decrease mortality, and therefore enhance lifetime fitness. Although much is known about the extent and causes of variation in the timing of the shift to piscivory among species and among cohorts within a species, little is known about the extent and causes of variation in the timing of the switch to piscivory among individuals within a single cohort. Here, I link otolith age and growth analysis to direct diet and stable isotope analyses to examine variation in the timing of the transition to piscivory and its causes among individual members of the 1994 largemouth bass cohort in Paul Lake, Michigan. Stable isotope and direct diet analyses indicate that only a few members of the 1994 cohort were able to shift to and sustain piscivory in their first summer of life (early piscivores), while most cohort members would have to wait until their second summer of life to become piscivorous (late piscivores). Significant differences in growth rate between early and late piscivores emerged shortly after 18 June, the first date of possible piscivory by early piscivores, after which early piscivores began to grow at rates nearly twice that of late piscivores. Otolith and stable isotope analyses combined indicate that an early hatching date was necessary, but not sufficient, to explain variation in the timing of the transition to piscivory. All early piscivores were hatched early in the summer, but many early-hatched members of the 1994 cohort did not shift to piscivory in their first summer of life. A combination of at least 10 days of variation in hatching dates and higher-than-average growth rates was required for early piscivores to switch to and sustain piscivory in their first summer of life. Individuals that were able to make the early transition to piscivory most likely benefited from both increased survival and fecundity over much of their life, the combination of which would confer a substantial fitness advantage upon individuals able to make the early transition to piscivory.

Intraspecific variation in a predator affects community structure and cascading trophic interactions.

Intraspecific phenotypic variation in ecologically important traits is widespread and important for evolutionary processes, but its effects on community and ecosystem processes are poorly understood. We use life history differences among populations of alewives, Alosa pseudoharengus, to test the effects of intraspecific phenotypic variation in a predator on pelagic zooplankton community structure and the strength of cascading trophic interactions. We focus on the effects of differences in (1) the duration of residence in fresh water (either seasonal or year-round) and (2) differences in foraging morphology, both of which may strongly influence interactions between alewives and their prey. We measured zooplankton community structure, algal biomass, and spring total phosphorus in lakes that contained landlocked, anadromous, or no alewives. Both the duration of residence and the intraspecific variation in foraging morphology strongly influenced zooplankton community structure. Lakes with landlocked alewives had small-bodied zooplankton year-round, and lakes with no alewives had large-bodied zooplankton year-round. In contrast, zooplankton communities in lakes with anadromous alewives cycled between large-bodied zooplankton in the winter and spring and small-bodied zooplankton in the summer. In summer, differences in feeding morphology of alewives caused zooplankton biomass to be lower and body size to be smaller in lakes with anadromous alewives than in lakes with landlocked alewives. Furthermore, intraspecific variation altered the strength of the trophic cascade caused by alewives. Our results demonstrate that intraspecific phenotypic variation of predators can regulate community structure and ecosystem processes by modifying the form and strength of complex trophic interactions.

PREY PREFERENCE BY A TOP PREDATOR AND THE STABILITY OF LINKED FOOD CHAINS

Recent theoretical studies have shown the potential for chaotic dynamics in simple three-species food chains. Most of these studies have focused on linear food chains, although natural food chains are seldom isolated from the surrounding food web. There is a growing awareness that food web dynamics can be strongly influenced by the behavior and movement of predators, energy, and nutrients across ecosystem and subecosystem boundaries. Motivated by observations from lakes, where the pelagic food web is often linked to the littoral food web by mobile predators, we constructed a simple model to evaluate the dynamics of two food chains linked by a top predator with prey preference. Linking the two food chains had no qualitative effect on model dynamics, although it did increase the density of the top predator. Instead, the prey preference of the top predator changed the system dynamics. We found a range of prey preferences that could eliminate chaos, dampen oscillations, and even produce point stability in a previously oscillatory system. The strength of prey preference required to produce a point attractor in a previously chaotic system was positively related to the dimension of chaos (a measure of the complexity of chaos). Our results suggest that, although chaos is possible in food webs, common processes like prey preference reduce the potential for chaos.