The measurement of stable isotopes in ‘bulk’ animal and plant tissues (e.g., muscle or leaf) has become an important tool for studies of functional diversity from organismal to continental scales. In consumers, isotope values reflect their diet, trophic position, physiological state, and geographic location. However, interpretation of bulk tissue isotope values can be confounded by variation in primary producer baseline values and by overlapping values among potential food items. To resolve these issues, biologists increasingly use compound-specific isotope analysis (CSIA), in which the isotope values of monomers that constitute a macromolecule (e.g., amino acids in protein) are measured. In this review, we provide the theoretical underpinnings for CSIA, summarize its methodology and recent applications, and identify future research directions. The key principle is that some monomers are reliably routed directly from the diet into animal tissue, whereas others are biochemically transformed during assimilation. As a result, CSIA of consumer tissue simultaneously provides information about an animal’s nutrient sources (e.g., food items or contributions from gut microbes) and its physiology (e.g., nitrogen excretion mode). In combination, these data clarify many of the confounding issues in bulk analysis and enable novel precision for tracing nutrient and energy flow within and among organisms and ecosystems.
Reef‐building corals are mixotrophic organisms that can obtain nutrition from endosymbiotic microalgae (autotrophy) and particle capture (heterotrophy). Heterotrophic nutrition is highly beneficial to many corals, particularly in times of stress. Yet, the extent to which different coral species rely on heterotrophic nutrition remains largely unknown because it is challenging to quantify. We developed a quantitative approach to investigate coral nutrition using carbon isotope (δ13C) analysis of six essential amino acids (AAESS) in a common Indo‐Pacific coral (Pocillopora meandrina) from the fore reef habitat of Palmyra Atoll. We sampled particulate organic matter (POM) and zooplankton as the dominant heterotrophic food sources in addition to the coral host and endosymbionts. We also measured bulk tissue carbon (δ13C) and nitrogen (δ15N) isotope values of each sample type. Patterns among δ13C values of individual AAESS provided complete separation between the autotrophic (endosymbionts) and heterotrophic nutritional sources. In contrast, bulk tissue δ13C and δ15N values were highly variable across the putative food sources and among the coral and endosymbiont fractions, preventing accurate estimates of coral nutrition on Palmyra. We used linear discriminant analysis to quantify differences among patterns of AAESS δ13C values, or ‘fingerprints’, of the food resources available to corals. This allowed for the development of a quantitative continuum of coral nutrition that can identify the relative contribution of autotrophic and heterotopic nutrition to individual colonies. Our approach revealed exceptional variation in conspecific colonies at scales of metres to kilometres. On average, 41% of AAESS in P. meandrina on Palmyra are acquired via heterotrophy, but some colonies appear capable of obtaining the majority of AAESS from one source or the other. The use of AAESS δ13C fingerprinting analysis offers a significant improvement on the current methods for quantitatively assessing coral trophic ecology. We anticipate that this approach will facilitate studies of coral nutrition in the field, which are essential for comparing coral trophic ecology across taxa and multiple spatial scales. Such information will be critical for understanding the role of heterotrophic nutrition in coral resistance and/or resilience to ongoing environmental change. A free Plain Language Summary can be found within the Supporting Information of this article.
Consumer foraging behaviors are dynamic, changing in response to prey availability, seasonality, competition, and even the consumer's physiological state. The isotopic composition of a consumer is a product of these factors as well as the isotopic "landscape" of its prey, i.e., the isotopic mixing space. Stable isotope mixing models are used to back-calculate the most likely proportional contribution of a set of prey to a consumer's diet based on their respective isotopic distributions, however they are disconnected from ecological process. Here we build a mechanistic framework that links the ecological and physiological processes of an individual consumer to the isotopic distribution that describes its diet, and ultimately to the isotopic composition of its own tissues, defined as its "isotopic niche." By coupling these processes, we systematically investigate under what conditions the isotopic niche of a consumer changes as a function of both the geometric properties of its mixing space and foraging strategies that may be static or dynamic over time. Results of our derivations reveal general insight into the conditions impacting isotopic niche width as a function of consumer specialization on prey, as well as the consumer's ability to transition between diets over time. We show analytically that moderate specialization on isotopically unique prey can serve to maximize a consumer's isotopic niche width, while temporally dynamic diets will tend to result in peak isotopic variance during dietary transitions. We demonstrate the relevance of our theoretical findings by examining a marine system composed of nine invertebrate species commonly consumed by sea otters. In general, our analytical framework highlights the complex interplay of mixing space geometry and consumer dietary behavior in driving expansion and contraction of the isotopic niche. Because this approach is established on ecological mechanism, it is well-suited for enhancing the ecological interpretation, and uncovering the root causes, of observed isotopic data.
Recent studies connecting the decline of large predators and consumers with the disintegration of ecosystems often overlook that this natural experiment already occurred. As recently as 14 ka, tens of millions of large‐bodied mammals were widespread across the American continents. Within 1000 yr of the arrival of humans, ∼ 80% were extinct including all > 600 kg. While the cause of the late Pleistocene (LP) extinction remains contentious, largely overlooked are the ecological consequences of the loss of millions of large‐bodied animals. Here, we examine the influence of the LP extinction on a local mammal community. Our study site is Hall's Cave in the Great Plains of Texas, which has unparalleled fine‐grained temporal resolution over the past 20 ka, allowing characterization of the community before and after the extinction. In step with continental patterns, this community lost 80% of large‐bodied herbivores and 20% of apex predators at the LP extinction. Using tightly constrained temporal windows spanning full glacial to modern time periods and comprehensive faunal lists, we reconstruct mammal associations and body size distributions over time. We find changes in alpha and beta diversity, and in the statistical moments associated with periods of climate change as well as with the LP extinction event. Additionally, there is a fundamental change in the composition of herbivores, with grazers being replaced by frugivores/granivores starting about 15 ka; the only large‐bodied grazer remaining today is the bison Bison bison. Moreover, the null model program PAIRS reveals interesting temporal patterns in the disassociation or co‐occurrence of species through the terminal Pleistocene and Holocene. Extinct species formed more significant associations than modern ones, and formed more aggregated pairs than do modern species. Further, negative species associations were about three times stronger than positive ones, suggesting that competitive interactions or environmental filtering are a strong force in community structure.
A fundamental question in ecology is understanding how energy and nutrients move through and between food webs, and which sources of production support consumers. In marine ecosystems, these basic questions have been challenging to answer given the limitation of observational methods. Stable isotope analysis of essential amino acids (EAA δ13C) has great potential as a tool to quantify energy and nutrient flow through marine food webs; however, it has been primarily utilized at large spatial scales. Here, we used EAA δ13C analysis to test for connectivity between adjacent subtidal and intertidal components of a nearshore ecosystem in south central Alaska. We measured δ13C of six EAA from four marine producer groups: subtidal kelp (Laminaria sp.), offshore particulate organic matter (POM), and intertidal red (Neorhodomela sp.) and green (Ulva sp.) algae. In addition, we sampled four intertidal invertebrate consumer species spanning a range of trophic/functional groups: Mytilus sp., Strongylocentrotus droebachiensis, Nucella sp., and Pycnopodia helianthoides. Using canonical analysis of principal coordinates (CAP) and isotope mixing models (MixSIAR), we tested for differences among producer EAA δ13C fingerprints and quantified the contribution of producer EAA to consumers. We compared these results to previously published EAA δ13C data on marine producers to examine the generality of this technique. We found the EAA δ13C fingerprints of subtidal kelps (Laminaria), Ulva, and Neorhodomela were highly distinct from one another. Further, our measured EAA δ13C patterns for kelp and red algae matched those previously reported from other localities, suggesting unique and universal EAA δ13C signatures for these groups. However, CAP could not distinguish between microalgae (POM) and Ulva, possibly due to similar biochemical pathways for the synthesis of EAA. Using these producer fingerprints, we found upper trophic‐level invertebrate consumers, Nucella and Pycnopodia, derived more than 60% of their essential amino acids from subtidal kelps. In contrast, the sampled primary consumers in the system, Mytilus and Strongylocentrotus, relied more heavily on Ulva and/or offshore POM. Our results provide evidence for connectivity between two adjacent nearshore ecosystems and exemplify EAA δ13C as a powerful new tool in tracing energy and nutrient flow within and among marine food webs.
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