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

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

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

Temperature dependence of plankton community metabolism in the subtropical and tropical oceans

Here we assess the temperature dependence of the metabolic rates (gross primary production (GPP), community respiration (CR), and the ratio GPP/CR) of oceanic plankton communities. We compile data from 133 stations of the Malaspina 2010 Expedition, distributed among the subtropical and tropical Atlantic, Pacific, and Indian oceans. We used the in vitro technique to measured metabolic rates during 24 h incubations at three different sampled depths: surface, 20%, and 1% of the photosynthetically active radiation measured at surface. We also measured the % of ultraviolet B radiation (UVB) penetrating at surface waters. GPP and CR rates increased with warming, albeit different responses were observed for each sampled depth. The overall GPP/CR ratio declined with warming. Higher activation energies (Ea) were derived for both processes (GPPChla = 0.97; CRChla = 1.26; CRHPA = 0.95 eV) compared to those previously reported. The Indian Ocean showed the highest Ea (GPPChla = 1.70; CRChla = 1.48; CRHPA = 0.57 eV), while the Atlantic Ocean showed the lowest (GPPChla = 0.86; CRChla = 0.77; CRHPA = 0.13 eV). We believe that the difference between previous assessments and the ones presented here can be explained by the overrepresentation of Atlantic communities in the previous data sets. We found that UVB radiation also affects the temperature dependence of surface GPP, which decreased rather than increased under high levels of UVB. Ocean warming, which causes stratification and oligotrophication of the subtropical and tropical oceans, may lead to reduced surface GPP as a result of increased penetration of UVB radiation.En prens

Metabolic responses of Skagerrak invertebrates to low O2 and high CO2 scenarios, and environmental characteristics during experiments at Kristineberg, Sweden

Coastal hypoxia is a problem that is predicted to increase rapidly in the future. At the same time, we are facing rising atmospheric CO2 concentrations, which are increasing the pCO2 and acidity of coastal waters. These two drivers are well studied in isolation; however, the coupling of low O2 and pH is likely to provide a more significant respiratory challenge for slow moving and sessile invertebrates than is currently predicted. The Gullmar Fjord in Sweden is home to a range of habitats, such as sand and mud flats, seagrass beds, exposed and protected shorelines and rocky bottoms. Moreover, it has a history of both natural and anthropogenically enhanced hypoxia as well as North Sea upwelling, where salty water reaches the surface towards the end of summer and early autumn. A total of 11 species (Crustacean, Chordate, Echinoderm and Mollusc) of these ecosystems were exposed to four different treatments (high or low oxygen and low or high CO2; varying pCO2 of 450 and 1300 µatm and O2 concentrations of 2-3.5 and 9-10 mg/L) and respiration measured after 3 and 6 days, respectively. This allowed us to evaluate respiration responses of species of contrasting habitats to single and multiple stressors. Results show that respiratory responses were highly species specific as we observed both synergetic as well as antagonistic responses, and neither phylum nor habitat explained trends in respiratory responses. Management plans should avoid the generalized assumption that combined stressors will result in multiplicative effects and focus attention on alleviating hypoxia in the region

Seawater carbonate chemistry and respiration rate of Skagerrak invertebrates during experiments at Kristineberg, Sweden

Coastal hypoxia is a problem that is predicted to increase rapidly in the future. At the same time, we are facing rising atmospheric CO2 concentrations, which are increasing the pCO2 and acidity of coastal waters. These two drivers are well studied in isolation; however, the coupling of low O2 and pH is likely to provide a more significant respiratory challenge for slow moving and sessile invertebrates than is currently predicted. The Gullmar Fjord in Sweden is home to a range of habitats, such as sand and mud flats, seagrass beds, exposed and protected shorelines and rocky bottoms. Moreover, it has a history of both natural and anthropogenically enhanced hypoxia as well as North Sea upwelling, where salty water reaches the surface towards the end of summer and early autumn. A total of 11 species (Crustacean, Chordate, Echinoderm and Mollusc) of these ecosystems were exposed to four different treatments (high or low oxygen and low or high CO2; varying pCO2 of 450 and 1300 µatm and O2 concentrations of 2-3.5 and 9-10 mg/L) and respiration measured after 3 and 6 days, respectively. This allowed us to evaluate respiration responses of species of contrasting habitats to single and multiple stressors. Results show that respiratory responses were highly species specific as we observed both synergetic as well as antagonistic responses, and neither phylum nor habitat explained trends in respiratory responses. Management plans should avoid the generalized assumption that combined stressors will result in multiplicative effects and focus attention on alleviating hypoxia in the region

Synergistic effects of hypoxia and increasing CO2 on benthic invertebrates of the central Chilean coast

Ocean acidification (OA) and hypoxic events are an increasing worldwide problem, but the synergetic effects of these factors are seldom explored. However, this synergetic occurrence of stressors is prevalent. The coastline of Chile not only suffers from coastal hypoxia but the cold, oxygen-poor waters in upwelling events are also supersaturated in CO, a study site to explore the combined effect of OA and hypoxia. We experimentally evaluated the metabolic response of different invertebrate species (2 anthozoans, 9 molluscs, 4 crustaceans, 2 echinoderms) of the coastline of central Chile (33°30'S, 71°37'W) to hypoxia and OA within predicted levels and in a full factorial design. Organisms were exposed to 4 different treatments (ambient, low oxygen, high CO, and the combination of low oxygen and high CO) and metabolism was measured after 3 and 6 days. We show that the combination of hypoxia and increased pCO reduces the respiration significantly, compared to a single stressor. The evaluation of synergistic pressures, a more realistic scenario than single stressors, is crucial to evaluate the effect of future changes for coastal species and our results provide the first insight on what might happen in the next 100 years.This research is a contribution to ASSEMBLE (grant agreement no. 227799; funded by the European Community: Research Infrastructure Action under the FP7 “Capacities” Specific Program), ESTRESX project funded by the Spanish Ministry of Economy and Innovation (ref. CTM2012-32603), LINCGlobal (funded by The Spanish National Research Council (CSIC) and The Pontificia Universidad Católica de Chile (PUC) to facilitate interaction between Latin American and Spanish researchers in the field of global change). AS was funded by a fellowship from the Government of the Balearic Islands (Department on Education, Culture and Universities) and the EU (European Social Fund), LR was funded by a fellowship from the Government of Chile (CONICYT, Becas Chile Program) and IH was funded by a JAE-DOC fellowship from the Spanish Government. NAL acknowledged funds by Fondecyt 1090624 during the experimental phase and the Millennium Nucleus Center for the Study of Multiple-drivers on Marine Socio-Ecological Systems (MUSELS) by MINECON Project NC120086 also supported this work during the final stages.Peer Reviewe