Using ocean models to predict spatial and temporal variation in marine carbon isotopes

Natural-abundance stable isotope ratios provide a wealth of ecological information relating to food web structure, trophic level, and location. The correct interpretation of stable isotope data requires an understanding of spatial and temporal variation in the isotopic compositions at the base of the food web. In marine pelagic environments, accurate interpretation of stable isotope data is hampered by a lack of reliable, spatio-temporally distributed measurements of baseline isotopic compositions. In this study, we present a relatively simple, process-based carbon isotope model that predicts the spatio-temporal distributions of the carbon isotope composition of phytoplankton (here expressed as δ13CPLK) across the global ocean at one degree and monthly resolution. The model is driven by output from a coupled physics-biogeochemistry model, NEMO-MEDUSA, and operates offline; it could also be coupled to alternative underlying ocean model systems. Model validation is challenged by the same lack of spatio-temporally explicit data that motivates model development, but predictions from our model successfully reproduce major spatial patterns in carbon isotope values observed in zooplankton, and are consistent with simulations from alternative models. Model predictions represent an initial hypothesis of spatial and temporal variation in carbon isotopic baselines in ocean areas where a few data are currently available, and provide the best currently available tool to estimate spatial and temporal variation in baseline isotopic compositions at ocean basin to global scales

Compound-specific stable isotope analysis of amino acids in pelagic shark vertebrae reveals baseline, trophic, and physiological effects on bulk protein isotope records

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Magozzi, S., Thorrold, S. R., Houghton, L., Bendall, V. A., Hetherington, S., Mucientes, G., Natanson, L. J., Queiroz, N., Santos, M. N., & Trueman, C. N. Compound-specific stable isotope analysis of amino acids in pelagic shark vertebrae reveals baseline, trophic, and physiological effects on bulk protein isotope records. Frontiers in Marine Science, 8, (2021): 673016, https://doi.org/10.3389/fmars.2021.673016.Variations in stable carbon and nitrogen isotope compositions in incremental tissues of pelagic sharks can be used to infer aspects of their spatial and trophic ecology across life-histories. Interpretations from bulk tissue isotopic compositions are complicated, however, because multiple processes influence these values, including variations in primary producer isotope ratios and consumer diets and physiological processing of metabolites. Here we challenge inferences about shark tropho-spatial ecology drawn from bulk tissue isotope data using data for amino acids. Stable isotope compositions of individual amino acids can partition the isotopic variance in bulk tissue into components associated with primary production on the one hand, and diet and physiology on the other. The carbon framework of essential amino acids (EAAs) can be synthesised de novo only by plants, fungi and bacteria and must be acquired by consumers through the diet. Consequently, the carbon isotopic composition of EAAs in consumers reflects that of primary producers in the location of feeding, whereas that of non-essential amino acids (non-EAAs) is additionally influenced by trophic fractionation and isotope dynamics of metabolic processing. We determined isotope chronologies from vertebrae of individual blue sharks and porbeagles from the North Atlantic. We measured carbon and nitrogen isotope compositions in bulk collagen and carbon isotope compositions of amino acids. Despite variability among individuals, common ontogenetic patterns in bulk isotope compositions were seen in both species. However, while life-history movement inferences from bulk analyses for blue sharks were supported by carbon isotope data from essential amino acids, inferences for porbeagles were not, implying that the observed trends in bulk protein isotope compositions in porbeagles have a trophic or physiological explanation, or are suprious effects. We explored variations in carbon isotope compositions of non-essential amino acids, searching for systematic variations that might imply ontogenetic changes in physiological processing, but patterns were highly variable and did not explain variance in bulk protein δ13C values. Isotopic effects associated with metabolite processing may overwhelm spatial influences that are weak or inconsistently developed in bulk tissue isotope values, but interpreting mechanisms underpinning isotopic variation in patterns in non-essential amino acids remains challenging.The internship of SM at the Woods Hole Oceanographic Institution was funded by the School of Ocean and Earth Science at University of Southampton. Stable isotope analyses were paid by CT and ST research budgets and SM Ph.D. and placement funding

Combining simulation modeling and stable isotope analyses to reconstruct the last known movements of one of Nature’s giants

The spatial ecology of rare, migratory oceanic animals is difficult to study directly. Where incremental tissues are available, their chemical composition can provide valuable indirect observations of movement and diet. Interpreting the chemical record in incremental tissues can be highly uncertain, however, as multiple mechanisms interact to produce the observed data. Simulation modeling is one approach for considering alternative hypotheses in ecology and can be used to consider the relative likelihood of obtaining an observed record under different combinations of ecological and environmental processes. Here we show how a simulation modeling approach can help to infer movement behaviour based on stable carbon isotope profiles measured in incremental baleen tissues of a blue whale (Balaenoptera musculus). The life history of this particular specimen, which stranded in 1891 in the UK, was selected as a case study due to its cultural significance as part of a permanent display at the Natural History Museum, London. We specifically tested whether measured variations in stable isotope compositions across the analysed baleen plate were more consistent with residency or latitudinal migrations. The measured isotopic record was most closely reproduced with a period of residency in sub-tropical waters for at least a full year followed by three repeated annual migrations between sub-tropical and high latitude regions. The latitudinal migration cycle was interrupted in the year prior to stranding, potentially implying pregnancy and weaning, but isotopic data alone cannot test this hypothesis. Simulation methods can help reveal movement information coded in the biochemical compositions of incremental tissues such as those archived in historic collections, and provides context and inferences that are useful for retrospective studies of animal movement, especially where other sources of individual movement data are sparse or challenging to validate.© 2019 Trueman et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited

A global perspective on the trophic geography of sharks

Carbon isotopic analysis reveals global biogeographic traits in shark trophic interactions, and sheds light on the diverse foraging behaviour of sharks

Combining Models of Environment, Behavior, and Physiology to Predict Tissue Hydrogen and Oxygen Isotope Variance Among Individual Terrestrial Animals

Variations in stable hydrogen and oxygen isotope ratios in terrestrial animal tissues are used to reconstruct origin and movement. An underlying assumption of these applications is that tissues grown at the same site share a similar isotopic signal, representative of the location of their origin. However, large variations in tissue isotopic compositions often exist even among conspecific individuals within local populations, which complicates origin and migration inferences. Field-data and correlation analyses have provided hints about the underlying mechanisms of within-site among-individual isotopic variance, but a theory explaining the causes and magnitude of such variance has not been established. Here we develop a mechanistic modeling framework that provides explicit predictions of the magnitude, patterns, and drivers of isotopic variation among individuals living in a common but environmentally heterogeneous habitat. The model toolbox includes isoscape models of environmental isotopic variability, an agent-based model of behavior and movement, and a physiology-biochemistry model of isotopic incorporation into tissues. We compare model predictions against observed variation in hatch-year individuals of the songbird Spotted Towhee (Pipilo maculatus) in Red Butte Canyon, Utah, and evaluate the ability of the model to reproduce this variation under different sets of assumptions. Only models that account for environmental isotopic variability predict a similar magnitude of isotopic variation as observed. Within the modeling framework, behavioral rules and properties govern how animals nesting in different locations acquire resources from different habitats, and birds nesting in or near riparian habitat preferentially access isotopically lighter resources than those associated with the meadow and slope habitats, which results in more negative body water and tissue isotope values. Riparian nesters also have faster body water turnover and acquire more water from drinking (vs. from food), which exerts a secondary influence on their isotope ratios. Thus, the model predicts that local among-individual isotopic variance is linked first to isotopic heterogeneity in the local habitat, and second to how animals sample this habitat during foraging. Model predictions provide insight into the fundamental mechanisms of small-scale isotopic variance and can be used to predict the utility of isotope-based methods for specific groups or environments in ecological and forensic research.</jats:p

Metabolic adjustment enhances food web stability

International audienceUnderstanding ecosystem stability is one of the greatest challenges of ecology. Over several decades, it has been shown that allometric scaling of biological rates and feeding interactions provide stability to complex food web models. Moreover, introducing adaptive responses of organisms to environmental changes (e.g. like adaptive foraging that enables organisms to adapt their diets depending on resources abundance) improved species persistence in food webs. Here, we introduce the concept of metabolic adjustment, i.e. the ability of species to slow down their metabolic rates when facing starvation and to increase it in time of plenty. We study the reactions of such a model to nutrient enrichment and the adjustment speed of metabolic rates. We found that increasing nutrient enrichment leads to a paradox of enrichment (increase in biomasses and oscillation amplitudes and ultimately extinction of species) but metabolic adjustment stabilises the system by dampening the oscillations. Metabolic adjustment also increases the average biomass of the top predator in a tri-trophic food chain. In complex food webs, metabolic adjustment has a stabilising effect as it promotes species survival by creating a large diversity of metabolic rates. However, this stabilising effect is mitigated in enriched ecosystems. Phenotypic plasticity of organisms must be considered in food web models to better understand the response of organisms to their environment. As metabolic rate is central in describing biological rates, we must pay attention to its variations to fully understand the population dynamics of natural communities

The first global deep-sea stable isotope assessment reveals the unique trophic ecology of Vampire Squid Vampyroteuthis infernalis (Cephalopoda)

Vampyroteuthis infernalis Chun, 1903, is a widely distributed deepwater cephalopod with unique morphology and phylogenetic position. We assessed its habitat and trophic ecology on a global scale via stable isotope analyses of a unique collection of beaks from 104 specimens from the Atlantic, Pacific and Indian Oceans. Cephalopods typically are active predators occupying a high trophic level (TL) and exhibit an ontogenetic increase in δ15N and TL. Our results, presenting the first global comparison for a deep-sea invertebrate, demonstrate that V. infernalis has an ontogenetic decrease in δ15N and TL, coupled with niche broadening. Juveniles are mobile zooplanktivores, while larger Vampyroteuthis are slow-swimming opportunistic consumers and ingest particulate organic matter. Vampyroteuthis infernalis occupies the same TL (3.0–4.3) over its global range and has a unique niche in deep-sea ecosystems. These traits have enabled the success and abundance of this relict species inhabiting the largest ecological realm on the planet.Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. The attached file is the published pdf

Metabolic responses to high pCO2 conditions at a CO2 vent site in juveniles of a marine isopod species assemblage

We are starting to understand the relationship between metabolic rate responses and species' ability to respond to exposure to high pCO2. However, most of our knowledge has come from investigations of single species. The examination of metabolic responses of closely related species with differing distributions around natural elevated CO2 areas may be useful to inform our understanding of their adaptive significance. Furthermore, little is known about the physiological responses of marine invertebrate juveniles to high pCO2, despite the fact they are known to be sensitive to other stressors, often acting as bottlenecks for future species success. We conducted an in situ transplant experiment using juveniles of isopods found living inside and around a high pCO2 vent (Ischia, Italy): the CO2 'tolerant' Dynamene bifida and 'sensitive' Cymodoce truncata and Dynamene torelliae. This allowed us to test for any generality of the hypothesis that pCO2 sensitive marine invertebrates may be those that experience trade-offs between energy metabolism and cellular homoeostasis under high pCO2 conditions. Both sensitive species were able to maintain their energy metabolism under high pCO2 conditions, but in C. truncata this may occur at the expense of [carbonic anhydrase], confirming our hypothesis. By comparison, the tolerant D. bifida appeared metabolically well adapted to high pCO2, being able to upregulate ATP production without recourse to anaerobiosis. These isopods are important keystone species; however, given they differ in their metabolic responses to future pCO2, shifts in the structure of the marine ecosystems they inhabit may be expected under future ocean acidification conditions

A global perspective on the trophic geography of sharks

Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.This research was conducted as part of C.S.B.’s Ph.D dissertation, which was funded by the University of Southampton and NERC (NE/L50161X/1), and through a NERC Grant-in-Kind from the Life Sciences Mass Spectrometry Facility (LSMSF; EK267-03/16). We thank A. Bates, D. Sims, F. Neat, R. McGill and J. Newton for their analytical contributions and comments on the manuscripts.Peer reviewe

CONSERVATION PHYSIOLOGY: TOWARDS AN INTEGRATIVE COMPARATIVE FRAMEWORK FOR PREDICTING SPECIES’ RELATIVE VULNERABILITY TO GLOBAL WARMING

Conservation physiology offers powerful approaches to develop mechanistic explanations of shifts in species’ biogeography putatively attributed to Global Warming. Nevertheless, a comparative framework that integrates the multiple physiological traits underlying species’ thermal biology is to date still lacking. Here I demonstrate the fundamental importance of integrating metabolic performance, thermal tolerance and plasticity to provide more accurate predictions on species’ relative vulnerability to Global Warming. Six Caridean species occurring in a common garden were selected as model and acclimated to four temperature treatments: 10, 15, 20 and 25 °C. The effect temperature on their metabolic rates and thermal tolerance limits was tested, and plasticity for these physiological abilities was calculated according to a Reaction Norm approach. Metabolic rate increased exponentially with increasing temperature in all the species examined (except in Pandalus montagui). Nevertheless, species living in thermally unstable environments (Palaemon elegans and Palaemonetes varians) showed higher temperature dependence of metabolism than their subtidal counterparts (Crangon crangon and Palaemon serratus), thereby appearing to be at greater risk from sub-lethal effects of Global Warming. By contrast, the hypothesis of an evolutionary/functional trade-off between thermal tolerance and its plasticity suggests that both the most heat-tolerant species (P. elegans, P. varians and C. crangon) and the most plastic species (P. serratus) are likely to be in danger from acute lethal effects of Global Warming. Both P. montagui and Palaemon macrodactylus are exceptions, appearing to be the most and the least vulnerable species to Global Warming respectively