Craig A. Layman

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.

Niche width collapse in a resilient top predator following ecosystem fragmentation

Much research has focused on identifying species that are susceptible to extinction following ecosystem fragmentation, yet even those species that persist in fragmented habitats may have fundamentally different ecological roles than conspecifics in unimpacted areas. Shifts in trophic role induced by fragmentation, especially of abundant top predators, could have transcendent impacts on food web architecture and stability, as well as ecosystem function. Here we use a novel measure of trophic niche width, based on stable isotope ratios, to assess effects of aquatic ecosystem fragmentation on trophic ecology of a resilient, dominant, top predator. We demonstrate collapse in trophic niche width of the predator in fragmented systems, a phenomenon related to significant reductions in diversity of potential prey taxa. Collapsed niche width reflects a homogenization of energy flow pathways to top predators, likely serving to destabilize remnant food webs and render apparently resilient top predators more susceptible to extinction through time.

PREDATOR-DRIVEN PHENOTYPIC DIVERSIFICATION IN GAMBUSIA AFFINIS

Abstract Predation is heterogeneously distributed across space and time, and is presumed to represent a major source of evolutionary diversification. In fishes, fast‐starts–udden, high‐energy swimmingbursts–are often importan tin avoiding capture during a predator strike. Thus, in the presence of predators, we might expect evolution of morphological features that facilitate increased fast‐start speed. We tested this hypothesis using populations of western mosquitofish (Gambusia affinis) that differed in level of predation by piscivorous fish. Body morphology of G. affinis males, females, and juveniles diverged in a consistent manner between predatory environments. Fish collected from predator populations exhibited a larger caudal region, smaller head, more elongate body, and a posterior, ventral position of the eye relative to fish from predator‐free populations. Divergence in body shape largely matched a priori predictions based on biomechanical principles, and was evident across space (multiple populations) and time (multiple years). We measured maximum burst‐swimming speed for male mosquitofish and found that individuals from predator populations produced faster bursts than fish from predator‐free populations (about 20% faster). Biomechanical models of fish swimming and intrapopulation morphology‐speed correlations suggested that body shape differences were largely responsible for enhanced locomotor performance in fish from predator populations. Morphological differences also persisted in offspring raised in a common laboratory environment, suggesting a heritable component to the observed morphological divergence. Taken together, these results strongly support the hypothesis that divergent selection between predator regimes has produced the observed phenotypic differences among populations of G. affinis. Based on biomechanical principles and recent findings in other species, it appears that the general ecomorphological model described in this paper will apply for many aquatic taxa, and provide insight into the role of predators in shaping the body form of prey organisms.

BODY SIZE AND TROPHIC POSITION IN A DIVERSE TROPICAL FOOD WEB

We use stomach contents and stable isotope ratios of predatory fishes, collected over a 10-year time span from a species-rich river in Venezuela, to examine potential body-size–trophic-position relationships. Mean body size of predator taxa and their prey (determined by stomach content analyses) were significantly correlated, but trophic position of predators (estimated by stable isotope ratios) was not correlated with body size. This reflects no apparent relationship between body size and trophic position among prey taxa. Primary consumer taxa (algivores and detritivores) in this system are characterized by diverse size and morphology, and thus predatory fish of all body sizes and feeding strategies are able to exploit taxa feeding low in the food web. Regardless of relative body size, predators exploit short, productive food chains. For any given food chain within a complex web where predators are larger than their prey, trophic position and body size are necessarily correlated. But in diverse food webs...

Spatiotemporal variation in fish assemblage structure in tropical floodplain creeks

Biotic assemblages of aquatic floodplain systems have great potential to randomly reshuffle during annual flood periods, and have been described both as stochastically and deterministically assembled. However, only a limited number of studies have been conducted in relatively few habitat types. To evaluate large-bodied fish assemblage structure of floodplain creeks, we used experimental gill nets to sample fishes at sites spaced at even intervals within three creeks in consecutive dry seasons. A total of 60 species were collected, 41 of which were collected both years. The most frequently collected species were piscivores and algivores/detritivores. Multivariate analysis suggested non-random patterns of assemblage structure in both years. Correspondence analysis (CA) of the species abundance-by-site matrix for 2001 suggests species assemblages were most similar among sites within the same creek regardless of depth or longitudinal position. Discriminant function analysis (DFA) correctly predicted 100% of samples based on creek identity, and species ordination scores revealed creek-specific species subsets. In 2002, CA and DFA did not distinguish creeks based on species assemblages. Instead, we observed a significant positive relationship between assemblage composition and site depth and position along the creek longitudinal gradient. Assemblages were most similar among sites of comparable depth and longitudinal position, regardless of creek identity. Predators occurred almost exclusively at mouth and mid-reach sites. Flood duration prior to our 2002 sampling period was prolonged due to abnormally heavy rainfall in November and December 2001 (typically the falling-water period), and may account for the observed inter-annual variation in fish assemblage structure.

Native Predators Do Not Influence Invasion Success of Pacific Lionfish on Caribbean Reefs

Biotic resistance, the process by which new colonists are excluded from a community by predation from and/or competition with resident species, can prevent or limit species invasions. We examined whether biotic resistance by native predators on Caribbean coral reefs has influenced the invasion success of red lionfishes (Pterois volitans and Pterois miles), piscivores from the Indo-Pacific. Specifically, we surveyed the abundance (density and biomass) of lionfish and native predatory fishes that could interact with lionfish (either through predation or competition) on 71 reefs in three biogeographic regions of the Caribbean. We recorded protection status of the reefs, and abiotic variables including depth, habitat type, and wind/wave exposure at each site. We found no relationship between the density or biomass of lionfish and that of native predators. However, lionfish densities were significantly lower on windward sites, potentially because of habitat preferences, and in marine protected areas, most likely because of ongoing removal efforts by reserve managers. Our results suggest that interactions with native predators do not influence the colonization or post-establishment population density of invasive lionfish on Caribbean reefs.

Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish

Ecosystems are intricately linked by the flow of organisms across their boundaries, and such connectivity can be essential to the structure and function of the linked ecosystems. For example, many coral reef fish populations are maintained by the movement of individuals from spatially segregated juvenile habitats (i.e., nurseries, such as mangroves and seagrass beds) to areas preferred by adults. It is presumed that nursery habitats provide for faster growth (higher food availability) and/or low predation risk for juveniles, but empirical data supporting this hypothesis is surprisingly lacking for coral reef fishes. Here, we investigate potential mechanisms (growth, predation risk, and reproductive investment) that give rise to the distribution patterns of a common Caribbean reef fish species, Haemulon flavolineatum (French grunt). Adults were primarily found on coral reefs, whereas juvenile fish only occurred in non-reef habitats. Contrary to our initial expectations, analysis of length-at-age revealed that growth rates were highest on coral reefs and not within nursery habitats. Survival rates in tethering trials were 0% for small juvenile fish transplanted to coral reefs and 24–47% in the nurseries. As fish grew, survival rates on coral reefs approached those in non-reef habitats (56 vs. 77–100%, respectively). As such, predation seems to be the primary factor driving across-ecosystem distributions of this fish, and thus the primary reason why mangrove and seagrass habitats function as nursery habitat. Identifying the mechanisms that lead to such distributions is critical to develop appropriate conservation initiatives, identify essential fish habitat, and predict impacts associated with environmental change.

Nutrient supply from fishes facilitates macroalgae and suppresses corals in a Caribbean coral reef ecosystem

On coral reefs, fishes can facilitate coral growth via nutrient excretion; however, as coral abundance declines, these nutrients may help facilitate increases in macroalgae. By combining surveys of reef communities with bioenergetics modeling, we showed that fish excretion supplied 25 times more nitrogen to forereefs in the Florida Keys, USA, than all other biotic and abiotic sources combined. One apparent result was a positive relationship between fish excretion and macroalgal cover on these reefs. Herbivore biomass also showed a negative relationship with macroalgal cover, suggesting strong interactions of top-down and bottom-up forcing. Nutrient supply by fishes also showed a negative correlation with juvenile coral density, likely mediated by competition between macroalgae and corals, suggesting that fish excretion may hinder coral recovery following large-scale coral loss. Thus, the impact of nutrient supply by fishes may be context-dependent and reinforce either coral-dominant or coral-depauperate reef communities depending on initial community states.