Quantifying physiological influences on otolith microchemistry

Trace element concentrations in fish earstones (‘otoliths’) are widely used to discriminate spatially discrete populations or individuals of marine fish, based on a commonly held assumption that physiological influences on otolith composition are minor, and thus variations in otolith elemental chemistry primarily reflect changes in ambient water chemistry. We carried out a long-term (1-year) experiment, serially sampling seawater, blood plasma and otoliths of mature and immature European plaice (Pleuronectes platessa L.) to test relationships between otolith chemistry and environmental and physiological variables. Seasonal variations in otolith elemental composition did not track seawater concentrations, but instead reflected physiological controls on metal transport and biokinetics, which are likely moderated by ambient temperature. The influence of physiological factors on otolith composition was particularly evident in Sr/Ca ratios, the most widely used elemental marker in applied otolith microchemistry studies. Reproduction also triggered specific variations in otolith and blood plasma metal chemistry, especially Zn/Ca ratios in female fish, which could potentially serve as retrospective spawning indicators. The influence of physiology on the trace metal composition of otoliths may explain the success of microchemical stock discrimination in relatively homogenous marine environments, but could complicate alternative uses for trace element compositions in biominerals of higher organism

Otolith δ13C values as a metabolic proxy: Approaches and mechanical underpinnings

Knowledge of metabolic costs associated with maintenance, foraging, activity and growth under natural conditions is important for understanding fish behaviours and the bioenergetic consequences of a changing environment. Fish performance in the wild and within a complex environment can be investigated by analysing individual-level field metabolic rate and, at present, the natural stable carbon isotope tracer in otoliths offers the possibility to reconstruct field metabolic rate. The isotopic composition of carbon in fish otoliths is linked to oxygen consumption through metabolic oxidation of dietary carbon. The proportion of metabolically derived carbon can be estimated with knowledge of δ13C values of diet and dissolved inorganic carbon in the water. Over the past 10 years, new techniques to study fish ecology have been developed, and these can be used to strengthen the application of otolith δ13C values as a metabolic proxy. Here, we illustrate the great potential of the otolith δ13C metabolic proxy in combination with other valuable and well-established approaches. The novel approach of the otolith δ13C metabolic proxy allows us to track the effects of ontogenetic and environmental drivers on individual fish physiology, and removes a major obstacle to understanding and predicting the performance of free-ranging wild fish.publishedVersio

Locations of marine animals revealed by carbon isotopes

Knowing the distribution of marine animals is central to understanding climatic and other environmental influences on population ecology. This information has proven difficult to gain through capture-based methods biased by capture location. Here we show that marine location can be inferred from animal tissues. As the carbon isotope composition of animal tissues varies with sea surface temperature, marine location can be identified by matching time series of carbon isotopes measured in tissues to sea surface temperature records. Applying this technique to populations of Atlantic salmon (Salmo salar L.) produces isotopically-derived maps of oceanic feeding grounds, consistent with the current understanding of salmon migrations, that additionally reveal geographic segregation in feeding grounds between individual philopatric populations and age-classes. Carbon isotope ratios can be used to identify the location of open ocean feeding grounds for any pelagic animals for which tissue archives and matching records of sea surface temperature are available

Stable isotopes demonstrate seasonally stable benthic-pelagic coupling as newly-fixed nutrients are rapidly transferred through food chains in an estuarine fish community

Seasonal differences in the availability of resources potentially result in food web architecture also varying through time. Stable isotope analyses are a logistically simple but powerful tool for inferring trophic interactions and food web structure, but relatively few studies quantify seasonal variations in food web structure or nutrient flux across multiple trophic levels. We determined the temporal dynamics in stable isotope compositions (carbon, nitrogen and sulfur) of a fish community from a highly seasonal, temperate estuary sampled monthly over a full annual cycle. Sulfur isotope values in fish tissues discriminated among consumers exploiting pelagic and benthic resources but showed no seasonal variation. This implied limited change in the relative consumption of pelagic and benthic resources by the fish community over the study period despite major seasonal changes in phytoplankton biomass. Conversely carbon and nitrogen isotope values exhibited seasonality marked by the commencement of the spring phytoplankton bloom and peak chlorophyll concentration, with δ13C values following expected trends in phytoplankton growth physiology and variation in δ15N values coinciding with changes in major nitrogen sources to plankton between nitrate and ammonium. Isotope shifts in fish muscle were detected within two weeks of the peak spring phytoplankton bloom, suggesting a rapid trophic transfer of carbon and nitrogen along food chains within the estuarine food web during periods of high production. We therefore caution against the assumption that temporal averaging effectively dampens isotopic variability in tissues of higher trophic level animals in highly dynamic ecosystems such as temperate estuaries. This work highlights how stable isotope analyses can be combined with environmental data to gain broader understanding of ecosystem functioning, while emphasising the need for temporally appropriate sampling in stable isotope-based studies

Teleost and elasmobranch eye lenses as a target for life-history stable isotope analyses

Incrementally grown, metabolically inert tissues such as fish otoliths provide biochemical records that can used to infer behavior and physiology throughout the lifetime of the individual. Organic tissues are particularly useful as the stable isotope composition of the organic component can provide information about diet, trophic level and location. Unfortunately, inert, incrementally grown organic tissues are relatively uncommon. The vertebrate eye lens, however, is formed via sequential deposition of protein-filled fiber cells, which are subsequently metabolically inert. Lenses therefore have the potential to serve as biochemical data recorders capturing life-long variations in dietary and spatial ecology. Here we review the state of knowledge regarding the structure and formation of fish eye lenses in the context of using lens tissue for retrospective isotopic analysis. We discuss the relationship between eye lens diameter and body size, describe the successful recovery of expected isotopic gradients throughout ontogeny and between species, and quantify the isotopic offset between lens protein and white muscle tissue. We show that fish eye lens protein is an attractive host for recovery of stable isotope life histories, particularly for juvenile life stages, and especially in elasmobranchs lacking otoliths, but interpretation of lens-based records is complicated by species-specific uncertainties associated with lens growth rates

Individual variation in field metabolic rates of wild living fish have phenotypic and ontogenetic underpinnings: insights from stable isotope compositions of otoliths

Publication history: Accepted - 17 May 2023; Published -13 June 2023.Introduction: Individual metabolism has been identified as a key variable for predicting responses of individuals and populations to climate change, particularly for aquatic ectotherms such as fishes. Predictions of organism standard metabolic rate (SMR), and the thermal sensitivity of metabolic rate are typically based on allometric scaling rules and respirometry-based measures of respiratory potential under laboratory conditions. The relevance of laboratory-based measurement and theoretical allometric rules to predict performance of free-ranging animals in complex natural settings has been questioned, but determining time averaged metabolic rate in wild aquatic animals is challenging. Methods: Here we draw on stable isotope compositions of aragonite in fish otoliths to estimate time averaged experienced temperature and expressed field metabolic rate (FMR) simultaneously and retrospectively at an individual level. We apply the otolith FMR proxy to a population of European plaice (Pleuronectes platessa) from the North Sea during a period of rapid warming between the 1980s to the mid-2000s, sampling otolith tissue grown in both juvenile and adult stages. Results: Among-individual variations in realized mass-specific FMR were large and independent of temperature and scaled positively with body size in adult life stages, contradicting simplistic assumptions that FMR follows scaling relationships inferred for standard metabolic rates (SMR). In the same individuals, FMR in the first summer of life co-varied positively with temperature. Discussion: We find strong evidence for the presence of consistent metabolic phenotypes within the sampled population, as FMR in the first year of life was the strongest single predictor for among individual variation in FMR at the point of sampling. Nonetheless, best fitting models explained only 20% of the observed variation, pointing to large among-individual variation in FMR that is unexplained by body mass, temperature or metabolic phenotype. Stable isotope-derived estimates of field metabolic rate have great potential to expand our understanding of ecophysiology in general and especially mechanisms underpinning the relationships between animal performance and changing environmental and ecological conditions.This work was funded from NERC Case award NE/P009700/1

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

Toward a better understanding of fish‐based contribution to ocean carbon flux

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Moult location and diet of auks in the North Sea inferred from coupled light-based and isotope-based geolocation

Many pelagic seabirds moult their feathers while at sea, which is an energetically costly behaviour. Mortality rates during moult can be high, so spatial and trophic ecology during this critical period is important for understanding demographic patterns. Unfortunately, individual foraging behaviours specifically linked to at-sea moulting are commonly unclear. This paper combines 2 different approaches to geolocation: data from bird-borne geolocation loggers and stable-isotope assignment using carbon and nitrogen isotope maps (isoscapes). Coupling 2 geolocation processes allows some uncertainties associated with isotope-based assignment to be constrained. We applied this approach to quantify species-specific foraging locations and individual trophic variability during feather regrowth in 3 sympatric auk populations breeding on the Isle of May, Scotland (common guillemot Uria aalge, razorbill Alca torda and Atlantic puffin Fratercula arctica). Inferred foraging areas during moult differed between species and feather types. Guillemots likely underwent moult within the southern North Sea, razorbills along the east coast of England and into the southern North Sea and puffins off the east coast of Scotland. Estimates of individual trophic position varied considerably within feather types (up to 1 trophic level difference between individuals), among feather types grown during different time periods and across the 3 species, with guillemots consistently foraging at higher trophic positions than razorbills and puffins. Used in combination, these methods better constrain foraging areas during moulting, and provide a technique to explore individual differences and flexibility in foraging strategy, which is valuable information for both seabird conservation and marine spatial planning

Deep-sea sponge aggregations (Pheronema carpenteri) in the Porcupine Seabight (NE Atlantic) potentially degraded by demersal fishing

Deep-sea sponge aggregations are widely recognised as features of conservation interest and vulnerable marine ecosystems that may particularly require protection from the impact of commercial bottom trawl fishing. In 2011 we revisited deep-sea sponge aggregations in the Porcupine Seabight (NE Atlantic, c. 1200 m water depth) originally described by Rice, Thurston and New (1990, Prog. Oceanogr. 24: 179-196) from surveys in 1983/4. Using an off-bottom towed camera system, broadly comparable to the bottom-towed system originally employed, we resurveyed four key transects detailed in that publication. In the intervening years, there has been a substantial increase in deep-water fishing activity; our primary objectives were therefore to establish the continued presence of Pheronema carpenteri (Hexactinellida, Pheronematidae), the current status of the sponge population, and whether there was any evidence of bottom trawl fishing impact on the sponges and their associated fauna. We noted a very substantial reduction in the standing stock of sponges: in Rice et al.'s (loc. cit.) peak abundance depth range (1210 – 1250 m) numerical density declined from 1.09 to 0.03 ind m-2, and biomass density from 246 to 4 gwwt m-2, between the surveys. Our assessment of available vessel monitoring data suggested that commercial bottom trawling had been occurring in the area, with some indication of focussed effort in the sponge's bathymetric range. We also recorded the presence of multiple apparent seafloor trawl marks on two of the transects. Despite the potential disturbance, the presence of sponge aggregations continued to exert a statistically significant positive influence on the diversity of the local megafaunal assemblage. Similarly, faunal composition also exhibited a statistically significant trend with P. carpenteri numerical density. Megafaunal numerical density, particularly that of ascideans, appeared to be enhanced in the core of Rice et al.'s (loc. cit.) peak abundance depth range potentially reflecting the residual effect of sponge spicule mats. Our observations were suggestive of a substantive impact by bottom trawl fishing; however, a definitive assessment of cause and effect was not possible, being hampered by a lack of temporal studies in the intervening period. Other causes and interpretations were plausible and suggested the need for: (i) a precautionary approach to management, (ii) an improved understanding of sponge natural history, and (iii) temporal monitoring (e.g. seafloor sponge habitat cover)