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

Coastal hypoxia and anoxia have become a global key stressor to marine ecosystems, with almost 500 dead zones recorded worldwide. By triggering cascading effects from the individual organism to the community-and ecosystem level, oxygen depletions threaten 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 Ophiothrix quinquemaculata, for example, with the onset of mild hypoxia (< 2 mL O2 L-1), the emergence of polychaetes on the sediment surface with moderate hypoxia (< 1 mL O 2 L-1), the emergence of the infaunal sea urchin Schizaster canaliferus on the sediment with severe hypoxia (< 0.5 mL O 2 Lg-1) and heavy body rotations in sea anemones with anoxia. Other species changed their activity patterns, for example the circadian rhythm in the hermit crab Paguristes eremita or the bioherm-associated crab Pisidia longimana. 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. © 2014 Author (s).This study was financed by the Austrian Science Fund (FWF; projects P17655-B03 and P21542-B17) and supported by the OEAD Bilateral Slovenian Austrian Scientific Technical Cooperation project SI 22/2009Peer Reviewe

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

Coastal hypoxia and anoxia have become a global key stressor to marine ecosystems, with almost 500 dead zones recorded worldwide. By triggering cascading effects from the individual organism to the community-and ecosystem level, oxygen depletions threaten 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 24m 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 Ophiothrix quinquemaculata, for example, with the onset of mild hypoxia (< 2mLO(2) L-1), the emergence of polychaetes on the sediment surface with moderate hypoxia (< 1mLO(2) L-1), the emergence of the infaunal sea urchin Schizaster canaliferus on the sediment with severe hypoxia (< 0.5mLO(2) L-1) and heavy body rotations in sea anemones with anoxia. Other species changed their activity patterns, for example the circadian rhythm in the hermit crab Paguristes eremita or the bioherm-associated crab Pisidia longimana. 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 plan

Photosynthetic activity buffers ocean acidification in seagrass meadows

Macrophytes growing in shallow coastal zones characterised by intense metabolic activity have the capacity to modify pH within their canopy and beyond. We observed diel pH changes in shallow (5–12 m) seagrass (<i>Posidonia oceanica</i>) meadows spanning 0.06 pH units in September to 0.24 units in June. The carbonate system (pH, DIC, and aragonite saturation state (&Omega;_Ar)) and O₂ within the meadows displayed strong diel variability driven by primary productivity, and changes in chemistry were related to structural parameters of the meadow, in particular, the leaf surface area available for photosynthesis (LAI). LAI was positively correlated to mean, max and range pH_NBS and max and range &Omega;_Ar. In June, vertical mixing (as Turbulent Kinetic Energy) influenced max and min &Omega;_Ar, while in September there was no effect of hydrodynamics on the carbonate system within the canopy. Max and range &Omega;_Ar within the meadow showed a positive trend with the calcium carbonate load of the leaves, pointing to a possible link between structural parameters, &Omega;_Ar and carbonate deposition. <br></br> Calcifying organisms, e.g. epiphytes with carbonate skeletons, may benefit from the modification of the carbonate system by the meadow. There is, however, concern for the ability of seagrasses to provide modifications of similar importance in the future. The predicted decline of seagrass meadows may alter the scope for alteration of pH within a seagrass meadow and in the water column above the meadow, particularly if shoot density and biomass decline, on which LAI is based. Organisms associated with seagrass communities may therefore suffer from the loss of pH buffering capacity in degraded meadows

Reactions of a macrobenthic community to anoxia: behaviour and mortality sequences in a time-lapse camera experiment in the Gulf of Trieste

Hypoxien und Anoxien in seichten Küstengewässern stellen ein weltweites Problem dar (Diaz und Rosenberg 2008). Wenn der Anteil an gelöstem Sauerstoff im Wasser unter 2 ml l-1 (Hypoxie) sinkt oder ganz verschwindet (Anoxia) kommt es unter anderem zu Verhaltensveränderungen und physiologischen Anpassungen (Diaz und Rosenberg 1995; Vismann 1991, Mangum 1973), die es den Organismen erlauben kurzfristig Störungen zu überleben. Halten hypoxische und anoxische Bedingungen jedoch über einen längeren Zeitpunkt an, können großflächige Massensterben auftreten. Zwei Faktoren, die Schichtung der Wassersäule (Stratifizierung) sowie der Anstieg der Planktonbiomasse durch Eutrophierung, lassen die Anzahl der betroffenen Gebiete deutlich ansteigen. Über 400 so genannte "dead-zones" wurden bereits beschrieben. Ca. 50% davon sind einmal im Jahr hypoxisch, 17% weniger als einmal im Jahr, und 8% sind permanent hypoxisch (Diaz und Rosenberg 2008). Die Nordadria ist wegen der geringen Tiefe (< 35 m), dem schlammigen Boden, dem hohen Süßwassereinstroms (v.a. durch den Fluss Po, Italien), der hohen Produktivität und der Schichtung der Wassersäule im Spätsommer, ein sehr empfindliches Ökosystem (Stachowitsch und Avcin 1987). Der Großteil der nördlichen Adria wird von macrobenthischen Bodengemeinschaften bedeckt. Im Golf von Trieste setzt sie sich Großteils aus dem Schwamm Reniera spp., dem Schlangenstern Ophiothrix quinquemaculata und der Seescheide Microcosmus sulcatus zusammen, und wird deshalb auch die Ophiothrix-Reniera-Microcosmus Gemeinschaft (ORM-Gemeinschaft) genannt (Fedra et al. 1976). Diese filtrierende Gemeinschaft umfasst ca. 370 ± 73 g m-2 Nassgewicht. Die filtrierenden Organismen können ca. 5% der pelagischen Biomasse pro Tag abbauen (Ott und Fedra 1977) und werden deshalb auch als Puffer oder "natürliche Eutrophierungskontrolle" bezeichnet (Officer et al. 1982). Seit dem dramatischen Anstieg der Eutrophierung kommt es weltweit auch immer öfter zu solchen Sauerstoffkrisen (Gray et al. 2002). Die hohe Primärproduktion im Meer führt anfänglich zu einem Anstieg der Biomasse der Bodenorganismen. Im Frühling kommt es durch die Stratifizierung zu einer Trennung der oberen, sauerstoffreichen von der unteren, sauerstoffärmeren Wasserschicht. Die Bodenorganismen verbrauchen während des Sommers weiteren Sauerstoff und verstärken so die hypoxischen Bedingungen. Im Winter kommt es dann zu einer Durchmischung der kompletten Wassersäule und die Bodenorganismen wachsen wieder. Eutrophierung verstärkt den Effekt der Stratifizierung und führt zur Bildung des so genannten Meeresschnees. Wenn sich dieser über der Sprungschicht ansammelt, wird er auch als "falscher Benthos" bezeichnet. Durch das Auflösen der Sprungschicht, sinkt dieser Meeresschnee zu Boden und bedeckt große Flächen der benthischen Lebensgemeinschaften, die dann aufgrund des Sauerstoffmangels sterben (Ott 1992; Ott und Stachowitsch 1992). Eine „natürliche“ Sauerstoffkrise im Jahr 1983 wurde von Stachowitsch (1984, 1986) photographisch dokumentiert. Mit einem neuen Unterwassergerät, dem Experimental Anoxia Generating Unit (EAGU), das mit Foto- und Sensorausrüstung ausgestattet ist, wurden in einer Tiefe von 24 m im Golf von Trieste in situ Hypoxien und Anoxien induziert. Mit den Fotos und den dazugehörigen Sauerstoffwerten war es möglich, das Auftreten atypischer Verhaltensweisen bestimmter Sauerstoffgrenzwerten (beginnende Hypoxie: ≤ 2 ml l-1 DO; moderate Hypoxie: ≤ 1 ml l-1 DO; schwere Hypoxie: ≤ 0.5 ml l-1 DO sowie Anoxie: 0 ml l-1 DO) zuzuordnen. Während beginnender Hypoxie kommt zum Beispiel die infaunale Muschel Corbula gibba aus dem Sediment heraus und Einsiedlerkrebse (Paguristes eremita) zeigen einen deutlichen Anstieg an Lokomotion. Der Schlangenstern Ophiothrix quinquemaculata reagiert mit einer veränderten Armposition und beginnt entweder sich auf die Arme zu stellen oder sich eng an das Substrat zu ziehen. Die Seescheide Microcosmus sulcatus beginnt mit Körperkontraktionen und schließt währenddessen die beiden Siphonöffnungen. Unter moderater Hypoxie verlassen infaunale Polychaeten das Sediment. Sedimentbewegungen darauf hin deutet, dass der infaunale Seeigel Schizaster canaliferus bald an der Sedimentoberfläche erscheint. Sichtbar wird er (unter anderem auch der Schlangensterne Ophiura spp.) erst in der Kategorie "schwerer Hypoxie". Weiters lässt der epifaunale, reguläre Seeigel Psammechinus microtuberculatus seine Tarnung (z.B. Muschelstücke) los. Erste Mortalitäten (alle ausgewerteten Individuen der Art O. quinquemaculata) traten unter schwerer Hypoxie auf. Mit Ausnahme von C. gibba starben alle anderen Tiere bis zum Ende des Experimentes (Anoxie nach ~ 48 Stunden; H2S 17.9 µM). Diese Arbeit, eingebettet in ein vom FWF gefördertes Projekt, ist ein erster Schritt um (1) einen Verhaltenskatalog unterschiedlicher Arten in Bezug zu verschiedenen Sauerstoffgrenzwerten zu erstellen, und (2) empfindliche und tolerante Arten für die Nordadria zu bestimmen um zukünftig in situ rasch den Status und die Stabilität des Ökosystems zu bestimmen.Hypoxia and anoxia are key threats to shallow coastal ecosystems worldwide, and the northern Adriatic Sea is a case study for such sensitive seas. Benthic community collapse during low dissolved oxygen (DO) events is not a gradual process, but involves a series of sudden steps. Using a new underwater device, the Experimental Anoxia Generating Unit (EAGU), equipped with time-lapse camera and sensor equipment, we artificially induced anoxia in a sublittoral macrobenthic community in 24 m depth in the northern Adriatic Sea. The deployment shows that the oxygen levels beginning (≤ 2 ml l-1 DO), moderate (≤ 1 ml l-1 DO), severe hypoxia (≤ 0.5 ml l-1 DO) and anoxia (0 ml l-1 DO) cause a series of different atypical behaviours and lead to mortality. Under beginning hypoxia the hermit crabs Paguristes eremita left their hiding places under multi-species clumps and moved around actively. Moderate hypoxia caused the emergence from the sediment of polychaetes and the infaunal sea urchin Schizaster canaliferus. At severe hypoxia the epifaunal sea urchin Psammechinus microtuberculatus discarded its camouflage and the first mortality in the brittle star Ophiothrix quinquemaculata occurred. In the present deployment, anoxia caused mortality in all organisms except the bivalve Corbula gibba. Whereas some behaviours are reversible, mortalities lead to long-term shifts in the benthic community and thereby alter the whole ecosystem. The observations in the evaluated deployment are a step forward in compiling a generally valid catalogue of behaviours, a list of sensitive and tolerant species, and a range of potential community compositions. This can help to determine the status and stability of such benthic ecosystems in situ

The Impact of Global Warming and Anoxia on Marine Benthic Community Dynamics: an Example from the Toarcian (Early Jurassic)

The Pliensbachian-Toarcian (Early Jurassic) fossil record is an archive of natural data of benthic community response to global warming and marine long-term hypoxia and anoxia. In the early Toarcian mean temperatures increased by the same order of magnitude as that predicted for the near future; laminated, organic-rich, black shales were deposited in many shallow water epicontinental basins; and a biotic crisis occurred in the marine realm, with the extinction of approximately 5% of families and 26% of genera. High-resolution quantitative abundance data of benthic invertebrates were collected from the Cleveland Basin (North Yorkshire, UK), and analysed with multivariate statistical methods to detect how the fauna responded to environmental changes during the early Toarcian. Twelve biofacies were identified. Their changes through time closely resemble the pattern of faunal degradation and recovery observed in modern habitats affected by anoxia. All four successional stages of community structure recorded in modern studies are recognised in the fossil data (i.e. Stage III: climax; II: transitional; I: pioneer; 0: highly disturbed). Two main faunal turnover events occurred: (i) at the onset of anoxia, with the extinction of most benthic species and the survival of a few adapted to thrive in low-oxygen conditions (Stages I to 0) and (ii) in the recovery, when newly evolved species colonized the re-oxygenated soft sediments and the path of recovery did not retrace of pattern of ecological degradation (Stages I to II). The ordination of samples coupled with sedimentological and palaeotemperature proxy data indicate that the onset of anoxia and the extinction horizon coincide with both a rise in temperature and sea level. Our study of how faunal associations co-vary with long and short term sea level and temperature changes has implications for predicting the long-term effects of “dead zones” in modern oceans

Predator Avoidance in the European Seabass After Recovery From Short-Term Hypoxia and Different CO2 Conditions

Short-term hypoxia that lasts just a few days or even hours is a major threat for the marine ecosystems. The single effect of the human-induced levels of hypoxia and other anthropogenic impacts such as elevated pCO2 can reduce the ability of preys to detect their predators across taxa. Moreover, both processes, hypoxia and elevated pCO2, are expected to co-occur in certain habitats, but the synergic consequences of both processes and the ability of fish to recover remain unknown. To provide empirical evidence to this synergy, we experimentally evaluated the risk-taking behavior in juveniles of the European seabass (Dicentrachus labrax), an important commercial fisheries species after recovering from short-term hypoxia and different pH scenarios. The behavior of seabass juveniles was monitored in an experimental arena before and after the exposure to a simulated predator and contrasted to control fish (BACI design) (current levels of hypoxia and elevated pCO2) using a mechanistic function-valued modeling trait approach. Results revealed that fish recovering from elevated pCO2, alone or combined with hypoxia, presented less avoidance behavior in failing to seek refuge when a simulated predator was present in the arena compared to those exposed to control pCO2 levels. Our results show that recovery from short-term exposure to acidification and hypoxia was not synergistic and suggest that recovery from acidification takes longer than from short-term hypoxia treatment through a potential effect on the sensorial and hence behavioral capacities of fish

Nocturnal fish chorusing activity in the central Red Sea mesophotic reef zone and adjacent shallow sites

Through sharing characteristics of chorus activity, especially in regions that are particularly data deficient, we can aim at a broader, global understanding of fish chorusing and consequently important spatiotemporal changes in habitat use by schooling fish. Here, we identify seasonal changes in fish chorusing activity using passive acoustic monitoring, in the central Red Sea mesophotic and adjacent shallow coral reef zones. For this study, recorders were placed in the mesophotic coral reef zone (70–80 m), and adjacent shallow reef sites (10 m), over 2 weeks during summer and winter seasons. A total of eleven choruses were identified and catalogued according to timing, location and acoustic characteristics of frequency and sound pressure levels. The presence of choruses in both deep and shallow reef sites is indicative of critical habitat for fish foraging, courtship, spawning, and/or migratory activity. All but two choruses were found to originate at or near the mesophotic sites. Four choruses unique to summer and winter (n=3 and 1 respectively) were most prevalent in soundscapes. Temperature and oxygen levels, measured to document conditions under which the choruses were present, showed little change across the mesophotic zone even between seasons, while daily fluctuation occurred in the adjacent shallow sites in both seasons