Chemical analysis of calcified structures continues to flourish, as analytical and technological advances enable researchers to tap into trace elements and isotopes taken up in otoliths and other archival tissues at ever greater resolution. Increasingly, these tracers are applied to refine age estimation and interpretation, and to chronicle responses to environmental stressors, linking these to ecological, physiological, and life-history processes. Here, we review emerging approaches and innovative research directions in otolith chemistry, as well as in the chemistry of other archival tissues, outlining their value for fisheries and ecosystem-based management, turning the spotlight on areas where such biomarkers can support decision making. We summarise recent milestones and the challenges that lie ahead to using otoliths and archival tissues as biomarkers, grouped into seven, rapidly expanding and application-oriented research areas that apply chemical analysis in a variety of contexts, namely: (1) supporting fish age estimation; (2) evaluating environmental stress, ecophysiology and individual performance; (3) confirming seafood provenance; (4) resolving connectivity and movement pathways; (5) characterising food webs and trophic interactions; (6) reconstructing reproductive life histories; and (7) tracing stock enhancement efforts. Emerging research directions that apply hard part chemistry to combat seafood fraud, quantify past food webs, as well as to reconcile growth, movement, thermal, metabolic, stress and reproductive life-histories provide opportunities to examine how harvesting and global change impact fish health and fisheries productivity. Ultimately, improved appreciation of the many practical benefits of archival tissue chemistry to fisheries and ecosystem-based management will support their increased implementation into routine monitoring.Graphical abstract

Field metabolic rate (FMR) is key to understanding individual and population-level responses to environmental changes, but is challenging to measure in field conditions, particularly in aquatic environments. Here we show that FMR can be estimated directly from the isotopic composition of carbon in fish otoliths (δ¹³C_oto). We describe the relationship between δ¹³C_otovalues and oxygen consumption rate, and report results from laboratory experiments relating individual-level measurements of oxygen consumption rates to δ¹³C_otovalues in Atlantic cod (Gadus morhua). We apply our new δ¹³C_otometabolic proxy to existing δ¹³C_otodata from wild cod and four deepwater fish species to test the validity of inferred FMR estimates. The δ¹³C_otometabolic proxy offers a new approach to study physiological ecology in free-ranging wild fishes. Otolith-based proxies for FMR are particularly promising as they allow retrospective assessment of time-integrated, individual-level FMR throughout an individual fish’s life history.

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 d13C 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 d13C values as a metabolic proxy. Here, we illustrate the great potential of the otolith d13C metabolic proxy in combination with other valuable and well-established approaches. The novel approach of the otolith d13C 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.

Metabolic rate underpins our understanding of how species survive, reproduce and interact with their environment, but can be difficult to measure in wild fish. Stable carbon isotopes (δ¹³C) in ear stones (otoliths) of fish may reflect lifetime metabolic signatures but experimental validation is required to advance our understanding of the relationship. To this end, we reared juvenile Australasian snapper (Chrysophrys auratus), an iconic fishery species, at different temperatures and used intermittent-flow respirometry to calculate standard metabolic rate (SMR), maximum metabolic rate (MMR) and absolute aerobic scope (AAS). Subsequently, we analysed δ¹³C and oxygen isotopes (δ¹⁸O) in otoliths using isotope-ratio mass spectrometry. We found that under increasing temperatures, δ¹³C and δ¹⁸O significantly decreased, while SMR and MMR significantly increased. Negative logarithmic relationships were found between δ¹³C in otoliths and both SMR and MMR, while exponential decay curves were observed between proportions of metabolically sourced carbon in otoliths (M_oto) and both measured and theoretical SMR. We show that basal energy for subsistence living and activity metabolism, both core components of field metabolic rates, contribute towards incorporation of δ¹³C into otoliths and support the use of δ¹³C as a metabolic proxy in field settings. The functional shapes of the logarithmic and exponential decay curves indicated that physiological thresholds regulate relationships between δ¹³C and metabolic rates due to upper thresholds of M_oto. Here, we present quantitative experimental evidence to support the development of an otolith-based metabolic proxy, which could be a powerful tool in reconstructing lifetime biological trends in wild fish.

The fossil record provides the only direct evidence of temporal trends in biodiversity over evolutionary timescales. Studies of biodiversity using the fossil record are, however, largely limited to discussions of taxonomic and/or morphological diversity. Behavioural and physiological traits that are likely to be under strong selection are largely obscured from the body fossil record. Similar problems exist in modern ecosystems where animals are difficult to access. In this review, we illustrate some of the common conceptual and methodological ground shared between those studying behavioural ecology in deep time and in inaccessible modern ecosystems. We discuss emerging ecogeochemical methods used to explore population connectivity and genetic drift, life-history traits and field metabolic rate and discuss some of the additional problems associated with applying these methods in deep time.