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

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 years) 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.

存在于生物硬质组织中的生物地球化学示踪剂（biogeochemical tracers），常被用于将生物与其生存环境建立关联，以解答核心生态学研究问题。然而，随着生理过程日趋复杂，高等生物体内环境与生物成因结构之间的生物地球化学关联愈发难以预测。本研究将生物地球化学示踪剂与鱼类生长数据相结合，并采用全新的建模框架，对上升流区域内耳石（otolith）化学组成的生理与环境调控机制展开描述。其一，我们构建了复杂度逐步提升的单变量混合模型（univariate mixed models），用以刻画并拆解随时间动态变化的鱼类生长及耳石元素浓度的内在（年龄效应）与外在（环境参数）影响因子。其二，我们采用多变量混合模型（multivariate mixed model）探究元素间及元素与生长间关联的方向与强度，并检验关于耳石中元素同化作用的生理与环境调控假说。我们将上述模型应用于礁栖海鲈（Helicolenus percoides）耳石所提取的连续元素（Na、Sr、Mg、Ba、Li）与生长增量剖面数据，该数据涵盖17年时间尺度下的月分辨率记录，研究对象为野生捕获、定栖性完全海洋鱼类。基于概念模型，我们提出如下假说：由环境条件驱动的耳石性状（元素组成与生长），既会在单个耳石内部存在关联，反映生长与元素同化作用的时间依赖性，也会在经历相似外部环境的个体间呈现相关性。研究结果显示，部分元素（如Sr:Ca与Na:Ca）主要受生理过程调控，而其余元素（如Ba:Ca与Li:Ca）则更多受到环境因素的影响。在单个个体体内，耳石性状间关联的强度与方向存在显著差异，尤其是那些受环境调控的性状。受生理调控的元素间关联，往往强于主要由环境因子驱动的元素间关联。令人意外的是，仅Ba:Ca与生长在个体间存在显著关联。未恰当考虑内在效应（如年龄）的模型，会高估个体间关联的强度，同时低估个体内关联的程度。综上，在构建恰当的模型中未检测到耳石性状的个体间关联，且未纳入合适的内在协变量可能引入系统性偏差，这表明在假设多元素特征仅反映共同环境影响时，需保持审慎态度。