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

TRACING ORIGIN AND COLLAPSE OF HOLOCENE BENTHIC BASELINE COMMUNITIES IN THE NORTHERN ADRIATIC SEA

The shallow northern Adriatic Sea has a long history of anthropogenic impacts that reaches back many centuries. While the effects of eutrophication, overfishing, pollution, and trawling over recent decades have been extensively studied, the major ecological turnovers during the Holocene as a whole remain poorly explored. In this study, we reconstruct ecological baselines defining benthic ecosystem composition prior to major anthropogenic changes at four stations characterized by low sedimentation and millennial-scale time averaging of molluscan assemblages. We discriminate between natural and anthropogenic drivers based on (1) stratigraphic changes in the composition of molluscan communities observed in sediment cores and (2) changes in concentrations of heavy metals, pollutants, and organic enrichment. The four 1.5-m long sediment cores reach back to the Pleistocene–Holocene boundary, allowing for a stratigraphic distinction of the major sea-level phases of the Holocene. During the transgressive phase and maximum flooding, sea-level and establishment of the modern circulation pattern determined the development of benthic communities in shallow-water, vegetated habitats with epifaunal biostromes and, in deeper waters, with bryozoan meadows. After sea-level stabilization, the composition of these baseline communities remained relatively uniform and started to change markedly only with the intensification of human impacts in the late highstand, leading to a dominance of infauna and a decline of epifauna at all sites. This profound ecological change reduced species richness, increased the abundance of infaunal suspension feeders, and led to a decline of grazers and deposit feeders. We suggest that modern soft-bottom benthic communities in the northern Adriatic Sea today do not show the high geographic heterogeneity in composition characteristic of benthos prior to anthropogenic influences

A decline in molluscan carbonate production driven by the loss of vegetated habitats encoded in the Holocene sedimentary record of the Gulf of Trieste

Carbonate sediments in non-vegetated habitats on the north-east Adriatic shelf are dominated by shells of molluscs. However, the rate of carbonate molluscan production prior to the 20th century eutrophication and overfishing on this and other shelves remains unknown because: (i) monitoring of ecosystems prior to the 20th century was scarceand (ii) ecosystem history inferred from cores is masked by condensation and mixing. Here, based on geochronological dating of four bivalve species, carbonate production during the Holocene is assessed in the Gulf of Trieste, where algal and seagrass habitats underwent a major decline during the 20th century. Assemblages of sand-dwelling Gouldia minima and opportunistic Corbula gibba are time-averaged to >1000 years and Corbula gibba shells are older by >2000 years than shells of co-occurring Gouldia minima. This age difference is driven by temporally disjunct production of two species coupled with decimetre-scale mixing. Stratigraphic unmixing shows that Corbula gibba declined in abundance during the highstand phase and increased again during the 20th century. In contrast, one of the major contributors to carbonate sands – Gouldia minima – increased in abundance during the highstand phase, but declined to almost zero abundance over the past two centuries. Gouldia minima and herbivorous gastropods associated with macroalgae or seagrasses are abundant in the top-core increments but are rarely alive. Although Gouldia minima is not limited to vegetated habitats, it is abundant in such habitats elsewhere in the Mediterranean Sea. This live–dead mismatch reflects the difference between highstand baseline communities (with soft-bottom vegetated zones and hard-bottom Arca beds) and present-day oligophotic communities with organic-loving species. Therefore, the decline in light penetration and the loss of vegetated habitats with high molluscan production traces back to the 19th century. More than 50% of the shells on the sea floor in the Gulf of Trieste reflect inactive production that was sourced by heterozoan carbonate factory in algal or seagrass habitats

Supplement Table 3-Corbula age data

Amino acid racemization data and calibrated estimates of postmortem age of Corbula gibba and Piran 2

Supplement Table 2-Gouldia age data

Amino acid racemization data and calibrated estimates of postmortem age of Gouldia minima collected from the shell bed at Piran 1 and Piran 2

Data from: A decline in molluscan carbonate production driven by the loss of vegetated habitats encoded in the Holocene sedimentary record of the Gulf of Trieste

Carbonate sediments in non-vegetated habitats on the NE Adriatic shelf are dominated by shells of molluscs. However, the rate of carbonate molluscan production prior to the 20th century eutrophication and overfishing on this and other shelves remains unknown because (1) monitoring of ecosystems prior to the 20th century was scarce and (2) ecosystem history inferred from cores is masked by condensation and mixing. Here, based on geochronological dating of four bivalve species, carbonate production during the Holocene is assessed in the Gulf of Trieste, where algal and seagrass habitats underwent a major decline during the 20th century. Assemblages of sand-dwelling Gouldia minima and opportunistic Corbula gibba are time-averaged to > 1,000 years and C. gibba shells are older by >2,000 years than shells of co-occurring G. minima. This age difference is driven by temporally disjunct production of two species coupled with decimeter-scale mixing. Stratigraphic unmixing shows that Corbula gibba declined in abundance during the highstand phase and increased again in the 20th century. In contrast, one of the major contributors to carbonate sands, Gouldia minima, increased in abundance during the highstand phase, but declined to almost zero abundance over the past two centuries. G. minima and herbivorous gastropods associated with macroalgae or seagrasses are abundant in the top-core increments but are rare alive. Although G. minima is not limited to vegetated habitats, it is abundant in such habitats elsewhere in the Mediterranean Sea. This live-dead mismatch reflects the difference between highstand baseline communities (with soft-bottom vegetated zones and hard-bottom Arca beds) and present-day oligophotic communities with organic-loving species. Therefore, the decline in light penetration and the loss of vegetated habitats with high molluscan production traces back to the 19th century. More than 50% of the shells on the seafloor in the Gulf of Trieste reflect inactive production that was sourced by heterozoan carbonate factory in algal or seagrass habitats

Grain size analysis and concentrations of several metals, nutrients and organic pollutants.

<p>Dashed lines indicate threshold values for potential environmental effects according to NOAA sediment quality guidelines and to the Italian Ministerial Decree 26/2010 (ERL: Effects Range-Low; ERM: Effects Range-Median; TEL: Threshold Effects Level). For PAHs, no thresholds are plotted because measured concentrations are considerably lower.</p

Supplementary Table 3

Supplementary Table 3 – Abundances of mollusks in two replicate cores at Po 3 (cores M13 and M14), at Po4 (cores M20 and M21), and in the Bay of Panzano (cores M28 and M29), and concentrations of elements, TOC, and total nitrogen

Responses of molluscan communities to centuries of human impact in the northern Adriatic Sea

<div><p>In sediment cores spanning ~500 years of history in the Gulf of Trieste, down-core changes in molluscan community structure are characterized by marked shifts in species and functional composition. Between the 16^th and 19^th century, a strong heavy metal contamination of the sediments, most notably by Hg, together with the effects of natural climatic oscillations (increased sedimentation and organic enrichment) drive community changes. Since the early 20^th century up to 2013, the combined impacts of cultural eutrophication, frequent hypoxic events and intensifying bottom trawling replace heavy metal contamination and climatic factors as the main drivers. The pollution-tolerant and opportunistic bivalve <i>Corbula gibba</i> and the scavenging gastropod <i>Nassarius pygmaeus</i> significantly increase in abundance during the 20^th century, while species more sensitive to disturbances and hypoxia such as <i>Turritella communis</i> and <i>Kurtiella bidentata</i> become rare or absent. An infaunal life habit and scavenging emerge as the dominant life strategies during the late 20^th century. Down-core shifts in the proportional abundances of molluscan species and functional groups represent a sensitive proxy for past ecological changes and reveal a century-long anthropogenic impact as the main driver behind these processes in the northern Adriatic Sea, offering also a unique perspective for other shallow marine ecosystems worldwide.</p></div

Supplement Table 1-core data

Absolute abundances of molluscs in two cores at Piran 1 and Piran 2, including two surface living assemblages collected by Van Veen grabs at the same sites in 2014 (1 mm mesh size). Complete valves or fragments with umbo preserved were selected from the >1 mm sieve fraction of each increment, identified to species level, and counted. For each species, the higher number of single valves (either right or left) was added to the number of double-valved specimens to get the final count in each increment