Coupling biogeochemical tracers with fish growth reveals physiological and environmental controls on otolith chemistry

Abstract

Biogeochemical tracers found in the hard parts of organisms are frequently used to answer key ecological questions by linking the organism with the environment. However, the biogeochemical relationship between the environment and the biogenic structure becomes less predictable in higher organisms as physiological processes become more complex. Here, we use the simultaneous combination of biogeochemical tracers and fish growth analyzed with a novel modeling framework to describe physiological and environmental controls on otolith chemistry in an upwelling zone. First, we develop increasingly complex univariate mixed models to describe and partition intrinsic (age effects) and extrinsic (environmental parameters) factors influencing fish growth and otolith element concentrations through time. Second, we use a multivariate mixed model to investigate the directionality and strength between element‐to‐element and growth relationships and test hypotheses regarding physiological and environmental controls on element assimilation in otoliths. We apply these models to continuous element (Na, Sr, Mg, Ba, Li) and growth increment profiles (monthly resolution over 17 yr) derived from otoliths of reef ocean perch (Helicolenus percoides), a wild‐caught, site‐attached, fully marine fish. With a conceptual model, we hypothesize that otolith traits (elements and growth) driven by environmental conditions will correlate both within an otolith, reflecting the time dependency of growth and element assimilation, and among individuals that experience a similar set of external conditions. We found some elements (Sr:Ca and Na:Ca) are mainly controlled by physiological processes, while other elements (Ba:Ca and Li:Ca) are more environmentally influenced. Within an individual fish, the strength and direction of correlation varies among otolith traits, particularly those under environmental control. Correlations among physiologically regulated elements tend to be stronger than those primarily controlled by environmental drivers. Surprisingly, only Ba:Ca and growth are significantly correlated among individuals. Failure to appropriately account for intrinsic effects (e.g., age) led to inflated estimates of among individual correlations and a depression of within individual correlations. Together, the lack of among‐individual correlations of otolith traits in properly formulated models and the biases that can be introduced by not including appropriate intrinsic covariates suggest that caution is needed when assuming multi‐elemental signatures are reflective solely of shared environments.

Using otolith chronologies to understand long‐term trends and extrinsic drivers of growth in fisheries

“…Intra-regional differences in growth arose from variation in environmental influences and population dynamics. Few studies have applied fine-scale growth profiles (Grammer et al 2017), despite their value. Here, we developed seasonally resolved chronologies, which provided nuanced predictions of growth trends which encapsulated and accounted for fluctuations throughout a whole year that may have been otherwise overlooked in broader annual chronologies.…”

“…Limited work has investigated the application of these sclerochronological approaches on temporal scales smaller than annual measurements. Consequently, there is potential to investigate the value of finer scale (such as seasonally or monthly resolved) growth histories, which may offer a higher-resolution approach and capture small-scale, inter-annual variation relating to environmental fluctuations (Izzo et al 2016, Grammer et al 2017.…”

Evaluating estuarine nursery use and life history patterns of Pomatomus saltatrix in eastern Australia

“…It is noted that Jervis Bay, the most marine-dominated estuary, had the lowest average Sr:Ca ratio in the juvenile otoliths. While there was no significant effect of fish length found in the univariate Sr PERM-AN OVA (Table S3), the fish from Jervis Bay were, on average, the smallest (Table S1) and there were therefore possibly some size-related intrinsic effects on otolith chemistry here such as ontogenetic changes in diet (Buckel et al 2004, Engstedt et al 2012 or differing physiology in small P.saltatrix (Grammer et al 2017). Indeed, decreases in Ba:Ca and Sr:Ca ratios have previously been demonstrated in P. saltatrix when switching diet from prawns to fish (Buckel et al 2004).…”

“…growth and diet) and extrinsic (e.g. temperature, salinity) factors in addition to a simple relationship with water chemistry (Sturrock et al 2014, Grammer et al 2017. A recent meta-analysis highlighted this by demonstrating that whilst salinity was the primary driver of both Ba and Sr, Sr was also influenced by factors including the ecological niche, condition, diet and ontogeny of individual species (Izzo et al 2018).…”

Element composition of shark vertebrae shows promise as a natural tag

“…Despite positive indications, our ability to interpret variations in vertebrae chemistry as tracers of elasmobranch environmental histories is still limited, and further evaluations of the effects of extrinsic factors, including temperature, salinity, water chemistry and pH, are paramount to better understand common trends across species and environments, as well as to gain insights into the scale and magnitude at which we are able to reconstruct elasmobranchs' past environmental histories or patterns of habitat use. Moreover, the extent to which intrinsic factors can buffer or magnify environmentally mediated element incorporation in calcified structures and how that potentially introduces interpretation error in environmental and life history reconstructions remain uncertain (Kalish 1989;Sturrock et al 2014Sturrock et al , 2015Loewen et al 2016;Grammer et al 2017;Reis-Santos et al 2018). Here, we found that shark condition (Fulton's K) increased Mn : Ca and Li : Ca (for the laboratory sharks only) and assume that this is evidence of an intrinsic control or physiological influence on element uptake and vertebrae chemical composition (as per Izzo et al 2015), even if further investigation is required.…”