Oxygen limitations on marine animal distributions and the collapse of epibenthic community structure during shoaling hypoxia

Abstract

Deoxygenation in the global ocean is predicted to induce ecosystem-wide changes. Analysis of multidecadal oxygen time-series projects the northeast Pacific to be a current and future hot spot of oxygen loss. However, the response of marine communities to deoxygenation is unresolved due to the lack of applicable data on component species. We repeated the same benthic transect (n = 10, between 45 and 190 m depths) over 8 years in a seasonally hypoxic fjord using remotely operated vehicles equipped with oxygen sensors to establish the lower oxygen levels at which 26 common epibenthic species can occur in the wild. By timing our surveys to shoaling hypoxia events, we show that fish and crustacean populations persist even in severe hypoxia (<0.5 mL L(-1) ) with no mortality effects but that migration of mobile species occurs. Consequently, the immediate response to hypoxia expansion is the collapse of community structure; normally partitioned distributions of resident species coalesced and localized densities increased. After oxygen renewal and formation of steep oxygen gradients, former ranges re-established. High frequency data from the nearby VENUS subsea observatory show the average oxygen level at our site declined by ~0.05 mL L(-1) year(-1) over the period of our study. The increased annual duration of the hypoxic (<1.4 mL L(-1) ) and severely hypoxic periods appears to reflect the oxygen dynamics demonstrated in offshore source waters and the adjacent Strait of Georgia. Should the current trajectory of oxygen loss continue, community homogenization and reduced suitable habitat may become the dominant state of epibenthic systems in the northeast Pacific. In situ oxygen occurrences were not congruent with lethal and sublethal hypoxia thresholds calculated across the literature for major taxonomic groups indicating that research biases toward laboratory studies on Atlantic species are not globally applicable. Region-specific hypoxia thresholds are necessary to predict future impacts of deoxygenation on marine biodiversity.

Ecophysiological limits to aerobic metabolism in hypoxia determine epibenthic distributions and energy sequestration in the northeast Pacific ocean

“…Near‐anoxia (∼ 0 mL L −1 ) to severe hypoxia (< 0.5 mL L −1 ) characterizes the deepest parts (> 200 m) of the inlet and normoxia (> 1.4 mL L −1 ) occurs in the shallower depths (< 60 m). Deoxygenation expands the volume of hypoxic and severely hypoxic deep waters into midwater depths over the course of the summer (Chu and Tunnicliffe ) before renewal of deep waters occurs in the fall (Anderson and Devol ). In 2013, remotely operated vehicle (ROV) imagery surveys repeated the same benthic transect line in Saanich Inlet at three times of the hypoxia cycle: before deoxygenation (May), after deoxygenation (September) and at the onset of reoxygenation (October) (Chu and Tunnicliffe ).…”

“…Deoxygenation expands the volume of hypoxic and severely hypoxic deep waters into midwater depths over the course of the summer (Chu and Tunnicliffe ) before renewal of deep waters occurs in the fall (Anderson and Devol ). In 2013, remotely operated vehicle (ROV) imagery surveys repeated the same benthic transect line in Saanich Inlet at three times of the hypoxia cycle: before deoxygenation (May), after deoxygenation (September) and at the onset of reoxygenation (October) (Chu and Tunnicliffe ). This ∼ 3 km transect begins mid‐inlet (∼ 190 m bottom depth), transitions through the zones of severe hypoxia and hypoxia (< 1.4 mL L −1 ), and ends in the normoxic, shallow depths (∼ 45 m).…”

“…In 2013, remotely operated vehicles equipped with oxygen sensors and cameras repeated a bottom transect at three stages of the hypoxic cycle: ( b ) May, before summer deoxygenation and when steep oxygen gradients were evident, ( c ) September, after deoxygenation‐induced expansion of hypoxic waters, and ( d ) October, during re‐oxygenation and re‐establishment of the steep oxygen gradient at the site. In situ oxygen data from Chu and Tunnicliffe (2015 b ).…”

“…As a result, general thresholds are biased toward Atlantic systems, where a majority of past hypoxia research has been performed, and fail to predict in situ species distributions in areas with historically lower oxygen levels such as the northeast Pacific Ocean (Chu and Tunnicliffe ). In such regions, benthic communities are naturally found in lower [O 2 ] env (Keller et al ; Chu and Tunnicliffe ) and respond to hypoxia at much lower oxygen levels than what general thresholds would suggest (Sperling et al ). Although the metabolic relationship between oxygen demand and [O 2 ] env availability is well‐established, few studies have applied as a tool for assessing ecological response of in situ distributions (Deutsch et al ).…”

Biodiversity response to natural gradients of multiple stressors on continental margins

“…An important message arising from these results is that while absolute thresholds can provide a guide, specific laboratory or empirical thresholds derived from one ocean basin may translate poorly to another. In particular, oxygen thresholds determined primarily from laboratory experiments on Atlantic species [45] are unlikely to be applicable to eastern Pacific species [46]; the same may also hold true for temperature and pCO 2 . Finally, the comparison of the eastern Pacific and Arabian Sea suggests that continental margin organisms may be well adapted to naturally occurring environmental stressors, but more sensitive to changes in stressors to which they are not normally exposed.…”