Advancing statistical models to reveal the effect of dissolved oxygen on the spatial distribution of marine taxa using thresholds and a physiologically based index

Abstract

The rapid pace of ocean change has prompted a need to forecast likely future species distributions. Species distribution models are often categorized as either correlative (statistical) or mechanistic, and each has limitations both for advancing understanding and for prediction. Here we sought to benefit from mechanistic understanding of how and why low dissolved oxygen affects species' distributions by applying physiologically informed statistical models to the spatial distribution of sablefish Anoplopoma fimbria, a deep‐dwelling commercially important groundfish. We fit spatial models to trawl‐survey data on catch rate, local temperature and dissolved oxygen, and estimated parameters of the metabolic index, which provided a way to express the temperature‐dependence of oxygen tolerance. We fit generalized linear mixed effects models with Gaussian random fields to capture the latent spatially fixed variables, and included both linear and breakpoint functions for pO2 and the metabolic index. The best fitting models all included breakpoint effects of pO2, and the estimated threshold value of 0.05 atm is close to levels in laboratory studies where metabolism begins to decline. Models based on the metabolic index were not as well supported as those that included pO2, likely because of the decrease in temperature and slight increase in pO2 at deep (> 800 m) depths. These findings illustrate that statistical models of species distributions can be improved by incorporating knowledge of how physiological mechanisms operate. Furthermore, they illustrate that even species with high tolerance for low dissolved oxygen may undergo species distribution shifts in the face of growing oxygen depletion in coastal ocean ecosystems.

Gills, growth, and activity across fishes

“…Notwithstanding these criticisms, the Gill Oxygen Limitation Theory has potentially far-reaching consequences if empirically supported. In addition to the idea that oxygen limitation and gill surface area may be behind the observed declines in maximum size in response to increasing temperature (temperature-size rule/Bergmann's rule/James' rule), mounting evidence from broad, cross-species studies suggests that oxygen limitation may also shape species' geographic distributions and underlie the mass-and temperature-dependence of metabolic rate (Forster et al 2012, Deutsch et al 2020, Rubalcaba et al 2020, Clarke et al 2021, English et al 2022, Essington et al 2022).…”

Species redistribution creates unequal outcomes for multispecies fisheries under projected climate change

“…We used the R package sdmTMB (Anderson et al, 2022) to construct SDMs and make ensemble predictions of future spatial distributions for the species in the DTS complex. The sdmTMB package implements the Stochastic Partial Differential Equation (SPDE) approach (Lindgren et al 2011) to approximating spatial Gaussian random elds as developed in the Integrated Nested Laplace Approximation R package (INLA; Lindgren and Rue 2015).…”

Groundfish biodiversity change in northeastern Pacific waters under projected warming and deoxygenation

“…We included quadratic terms for temperature and log depth to allow species occurrences to peak at intermediate values (Figure 1b-e). We fit a breakpoint function for log dissolved oxygen to reflect the fact oxygen is a limiting factor (Essington et al 2022). That is, each species is expected to have an oxygen threshold, below which oxygen limitation is expected to reduce their probability of occurrence, but above this threshold species should not be sensitive to changes in oxygen concentrations (Fry 1971).…”

“…Most SDM models to date do not account for oxygen (e.g., Cheung et al 2009;Ready et al 2010;Morley et al 2018;Chaikin et al 2022), and in some cases, rely on sea surface temperature when modeling species that live on the seafloor (e.g., Ready et al 2010;García Molinos et al 2016). In addition, demersal marine communities (e.g., groundfish) are highly depth structured because of physiological limits to temperature, hydrostatic pressure (Brown & Thatje 2014), and hypoxia tolerance (Brown & Thatje 2015;Essington et al 2022), as well as light, competition, and food availability (Elith & Leathwick 2009). However, because depth, temperature, and oxygen are closely correlated in many regions, it can be challenging to distinguish the role of each of these variables in determining contemporary species distributions.…”