Evidence for boundary layer oxygen diffusion limitation as a key driver of asteroid wasting

Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of sea star wasting is unresolved. We hypothesize that asteroid wasting is a sequela of microbial organic matter remineralization near respiratory surfaces which leads to boundary layer oxygen diffusion limitation (BLODL). Wasting lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before wasting onset, concomitant with and followed by the proliferation of putatively facultative and strictly anaerobic taxa. Bacterial cell abundance increased dramatically prior to wasting onset in experimental incubations. Wasting susceptibility was significantly correlated with rugosity (a key determinant of boundary layer thickness) of animal surfaces. At a semi-continuously monitored field site (Langley Harbor), wasting predictably occurred at annual peak or decline in phytoplankton biomass. Finally, wasting individuals from 2013 - 2014 bore stable isotopic signatures reflecting anaerobic processes and altered C and N metabolisms. These convergent lines of evidence support our hypothesis that BLODL is associated with wasting both in contemporary SSW events and during the 2013-2014 SSW mass mortality event, potentially driven by phytoplankton-derived OM. The impacts of BLODL may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential. Significance StatementSea star wasting disease affected multiple species of asteroids and has caused mass mortality in the Northeast Pacific Ocean since 2013. The underlying cause of wasting is unknown. We hypothesized that wasting may be due to respiratory deficit resulting from heterotrophic bacterial consumption of organic matter, resulting in oxygen depletion, near animal surfaces. Here, we provide convergent lines of evidence for this hypothesis, including shifts in microbial assemblage abundance and composition during wasting which suggest surface tissues experience sub-oxic conditions. Organic matter amendment results in asteroid wasting, and we provide elemental evidence for anaerobic conditions during mass mortality in 2013-2014. Our results are entirely consistent with environmental correlates of wasting in prior studies, including thermal stress and upwelling.