Effect of hypoxia and anoxia on invertebrate behaviour: ecological perspectives from species to community level

Abstract

Coastal hypoxia and anoxia have become a global key stressor to marine ecosystems, with almost 500 dead zones recorded wordwide. By triggering cascading effects from the individual organism to the community and ecosystem-level, oxygen depletions threat marine biodiversity and can alter ecosystem structure and function. By integrating both physiological function and ecological processes, animal behaviour is ideal for assessing the stress state of benthic macrofauna to low dissolved oxygen. The initial response of organisms can serve as an early-warning signal, while the successive behavioural reactions of key species indicate hypoxia levels and help assess community degradation. Here we document the behavioural responses of a representative spectrum of benthic macrofauna in the natural setting in the Northern Adriatic Sea, Mediterranean. We experimentally induced small-scale anoxia with a benthic chamber in 24 m depth to overcome the difficulties in predicting the onset of hypoxia, which often hinders full documentation in the field. The behavioural reactions were documented with a time-lapse camera. Oxygen depletion elicited significant and repeatable changes in general (visibility, locomotion, body movement and posture, location) and species-specific reactions in virtually all organisms (302 individuals from 32 species and 2 species groups). Most atypical (stress) behaviours were associated with specific oxygen thresholds: arm-tipping in the ophiuroid <i>Ophiothrix quinquemaculata</i>, for example, with the onset of mild hypoxia (< 2 mL O₂ L^&minus;1), the emergence of polychates on the sediment surface with moderate hypoxia (< 1 mL O₂ L^&minus;1), the emergence of the infaunal sea urchin <i>Schizaster canaliferus</i> on the sediment with severe hypoxia (< 0.5 mL O₂ L^&minus;1) and heavy body rotations in sea anemones with anoxia. Other species changed their activity patterns, i.e. circadian rhythm in the hermit crab <i>Paguristes eremita</i> or the bioherm-associated crab <i>Pisidia longimana</i>. Intra- and interspecific reactions were weakened or changed: decapods ceased defensive and territorial behaviour, and predator-prey interactions and relationships shifted. This nuanced scale of resolution is a useful tool to interpret present benthic community status (behaviour) and past mortalities (community composition, e.g. survival of tolerant species). This information on the sensitivity (onset of stress response), tolerance (mortality, survival), and characteristics (i.e. life habit, functional role) of key species also helps predict potential future changes in benthic structure and ecosystem functioning. This integrated approach can transport complex ecological processes to the public and decision-makers and help define specific monitoring, assessment and conservation plans

The Relationship between Mollusks and Oxygen Concentrations in Todos Santos Bay, Baja California, Mexico

“…In our study, genera Natica and Acteocina were collected in high oxygen concentrations in the north and central sections of the bay (stations 1, 3, 9, 4, 13, 14, 19, and 21). Although mollusks have been extensively employed in bioaccumulation studies for metal pollution [7,8,31], other studies have evaluated their utility as indicator of oxygen depletion in coastal environments [53,[55][56][57]. We acknowledge that only four genera of the thirteen dominant mollusks collected at TSB were related significantly to DO concentrations by a negative binomial GLM, which means that Truncatella, Donax, Bulla, and Acteocina follow a natural gradient of DO in Todos Santos Bay, Baja California.…”

“…In the Adriatic Sea, Corbula gibba is a clear example of an opportunistic species [53] because it is frequently found in hypoxic conditions (<2 mL L −1 ) and after postanoxic periods [54,55]. It has been demonstrated that C. gibba can survive for 78 h in anoxic conditions [56]. In the present study, Dentalium, Chione, Laevicardium, and Nuculana were found in low DO concentrations (<2 mL L −1 ); furthermore, these genera of bivalves are relatively tolerant to low oxygen levels in Todos Santos Bay.…”

Developments since 2005 in understanding potential environmental impacts of CO2 leakage from geological storage

“…temperature, hypoxia, food shortage, suspended matter) compounding the impact of any single environmental stress (such as CO 2 exposure from CCS leakage) and severely inhibiting the scope for physiological and behavioural adjustments to overcome that stress (Riedel et al, 2014;Queirós et al, 2015). It is unlikely therefore that hypercapnia will act as a single stressor, and caution is needed when assessing tolerances of species to environmental perturbations from studies that have only factored in one variable.…”

Structural and functional responses of harpacticoid copepods to anoxia in the Northern Adriatic: an experimental approach

“…The chamber, originally designed to document macrofauna behaviour during low-DO conditions (see also Riedel et al, 2013), is equipped with a digital camera (Canon EOS 30D; images taken in 6 min intervals), underwater flashes and a sensor array (DO, hydrogen sulphide H 2 S). The sensors were positioned 2 cm above the sediment and values were recorded in 1-min intervals.…”