A statistical framework to explore ontogenetic growth variation among individuals and populations: a marine fish example

Growth is a fundamental biological process, driven by a multitude of intrinsic (within‐individual) and extrinsic (environmental) factors, that underpins individual fitness and population demographics. Focusing on the comprehensive information stored in aquatic and terrestrial organism hard parts, we develop a series of increasingly complex hierarchical models to explore spatial and temporal sources of growth variation, ranging in resolution from within individuals to across a species. We apply this modeling framework to an extensive data set of otolith increment measurements from tiger flathead ( Platycephalus richardsoni ), a demersal commercially exploited fish that inhabits the warming waters of southeast Australia. We recreated growth histories (biochronology) up to four decades in length from seven fishing areas spanning this species' range. The dominant pattern in annual growth was an age‐dependent, allometric decline that varied among individuals, sexes, fishing areas, years, and cohorts. We found evidence for among‐area differences in growth‐rate selectivity, whereby younger fish at capture were generally faster growers. Temporal growth variation was partitioned into two main sources: extrinsic year to year annual fluctuations in environmental conditions and persistent cohort‐specific growth differences, reflecting density dependence and/or juvenile experience. Despite low levels of among‐individual growth synchrony within areas, we detected a regionally coherent signal of increasing average growth rate through time, a trend related to oceanic warming. At the southerly (poleward) range limit, growth was only weakly related to temperature, but farther north in warmer waters this relationship strengthened until closer to the species' equatorward range limit, growth declined with increasing temperatures. We partitioned these species‐wide and area‐specific phenotypic responses into within‐ and among‐individual components using a reaction norm approach. Individual tiger flathead likely possess sufficient growth plasticity to successfully adapt to warming waters across much of their range, but increased future warming in the north will continue to depress growth, affecting individual fitness and even population persistence. Our modeling framework is directly applicable to other long‐term, individual‐based, data sets such as those derived from tree rings, corals, and tag–recapture studies, and provides an unprecedented level of resolution into the drivers of growth variation and the ecological and evolutionary implications of environmental and climatic change.