The Return of Shallow Shelf Seas as Extreme Environments: Anoxia and Macrofauna Reactions in the...

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THE RETURN OF SHALLOW SHELF SEAS AS EXTREME ENVIRONMENTS: ANOXIA AND MACROFAUNA REACTIONS IN THE NORTHERN ADRIATIC SEA

MICHAEL STACHOWITSCH1, BETTINA RIEDEL1, AND MARTIN ZUSCHIN2 1Department of Marine Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria2Department of Paleontology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria

1. The Problem

It is a fundamental dogma of ecology that ecosystems change. The long-standing efforts center around detecting, quantifying (rates and directions), and determining the drivers of that change. Today, the focus is often on distinguishing which changes are “natural” and which are “unnatural,” whereby the former are pre-sumably acceptable, and the latter, anthropogenically driven changes, may require remedial action.

Shallow marine environments can serve as a model for this package of issues. Why? Small-scale, gradual change is an omnipresent feature of both marine and terrestrial ecosystems today. Complete, sudden and larger-scale collapses, however, are rare in the marine environment. Such worst-case ecosystem degradation scenarios are tangible, irrefutable case studies of major ecosystem shifts. Here, there can be no doubt about whether change is taking place and no debate about whether the endpoint is a matter of concern. Precisely this scenario is increasingly being encountered in connection with hypoxia/anoxia. It involves coastal eutrophication driven by nutrient loading from point and nonpoint sources, coupled with losses of filtering and buffering capacity of vegetation and suspension feeders (Zhang et al. 2010). Worldwide, anthropogenic eutrophication promotes this phenomenon (Diaz and Rosenberg 2008; Breitburg et al. 2009; Gooday et al. 2009; Rabalais et al. 2010). No other human impacts or pollution sources – oil, heavy metals, organohalogens, radioactivity, marine debris – have this impact, namely, complete and widespread ecosystem collapse characterized by extensive mass mortalities of all key species (Gray et al. 2002; Wu 2002; Sala and Knowlton 2006; Vaquer-Sunyer and Duarte 2008; Levin et al. 2009). Accordingly, shallow coastal seas that suffer hypoxic and anoxic conditions represent the most stressful habitat conceivable, much more so than any “stably extreme” habitat, i.e., characterized by extreme yet constant environmental conditions.

356 MICHAEL STACHOWITSCH ET AL.

Mass mortalities are a prime example – on a large scale and at many levels – of how benthic communities and the overall system respond to pertur-bation. So-called dead zones are the ultimate manifestation and symptom of this phenomenon. The term dead zone was coined in the late 1980s to describe large-scale midsummer hypoxic/anoxic areas, known since the early 1970s and mapped since 1985 in the Gulf of Mexico (Rabalais et al. 2002; Rabalais et al. 2007). It now refers, in general, to areas suffering intermittent, periodic, or permanent hypoxia and anoxia leading to depauperated benthic communities. Today, nearly 415 eutrophic and hypoxic coastal systems have been identified worldwide: of these, 169 are hypoxic, 233 are areas of concern, and 13 are systems in recovery (Diaz and Rosenberg 2008; World Resources Institute, www.wri.org/map/world-hypoxic-and-eutrophic-coastal-areas). Recognized dead zones range from Scandinavian and Baltic waters in Europe to the Chesapeake Bay and the Gulf of Mexico in the USA to Japanese waters. The frequency and extension of hypoxic and anoxic zones are increasing worldwide (Diaz 2001), and dead zones in the world’s oceans are at the top of the list of emerging environmental challenges (UNEP 2004). Moreover, the phenomenon appears to be spreading beyond shallow, semi-enclosed seas (Gilbert et al. 2009). The recent intensification of severe inner-shelf hypoxia and the novel rise of water-column anoxia in larger ecosystems (California Current Large Marine Ecosystem: CCLME) reflect this trend (Levin 2003; Chan et al. 2008).

2. The Model System

The Northern Adriatic Sea is a model for this phenomenon. It combines many features known to be associated with low dissolved oxygen (DO) events (Stachowitsch and Avcin 1988): it is semi-enclosed, shallow (<50 m), and is characterized by soft bottoms, a high riverine input (mainly from the Po River), high productivity, and long water residence times (Ott 1992). As elsewhere in the northern hemisphere, this constellation can be associated with seasonal hypoxia and anoxia in late summer/early fall.

In general, hypoxia and anoxia can develop in the Northern Adriatic during late summer through a combination of certain meteorological and hydrological conditions such as calm weather and water stratification (Franco and Michelato 1992; Malej and Mala i 1995). Low DO events and benthic mortalities have been noted here periodically for centuries (Crema et al. 1991), but their frequency and severity have markedly increased during recent decades. High anthropogenic input of nutrients into the Northern Adriatic (Justi et al. 1995; Danovaro 2003; Druon et al. 2004) has led to a higher production and deposition of organic mat-ter to the bottom than the available oxygen supply to allow its decomposition (Rabalais and Turner 2001). The average long-term decrease in water body trans-parency here over the twentieth century, accompanied by a historical decrease in bottom DO since the early twentieth century, has been outlined by Justi (Justic et al. 1987; Justic 1987). Since the 1980s, severe oxygen deficiencies have been

357THE RETURN OF SHALLOW SHELF SEAS AS EXTREME ENVIRONMENTS

reported here regularly (Hrs-Brenko et al. 1994; Stachowitsch and Fuchs 1995; Penna et al. 2004). The impacted areas range from restricted zones (several square kilometers; Stachowitsch 1992) to approx. 250 km² (Faganeli et al. 1985) to 4,000 km² (Stefanon and Boldrin 1982; D. Degobbis, personal communication 1995), ultimately affecting every region of the Northern Adriatic (Fig. 13 in Ott 1992). Such mortalities were often accompanied and promoted by severe marine snow events (Stachowitsch et al. 1990).

The soft bottoms in the Northern Adriatic feature conspicuous, widely distributed macroepifaunas (Fedra 1978; Zuschin et al. 1999). These consist largely of decimeter-scale, interspecific, high-biomass aggregations termed multi-species clumps (Fedra et al. 1976), or bioherms: one or more shelly hard substrates provide the base for sessile, suspension-feeding colonizers (mostly sponges, ascidians, anemones, or bivalves), which in turn serve as an elevated substrate for additional vagile and hemi-sessile organisms (e.g., brittle stars, crabs, and sea cucumbers) (Zuschin and Pervesler 1996). The presence of a well-developed infauna is expressed in the early designations of the benthic communities here (Schizaster chiajei-community) based on infauna-oriented sampling methods (grabs) by Vatova (1949) and later authors (Gamulin-Brida 1967; Orel and Mennea 1969; Orel et al. 1987; Occhipinti-Ambrogi et al. 2002). An underwater TV-camera sled (Machan and Fedra 1975; Fedra 1978), combined with SCUBA diver taken samples and in situ experimentation, led to the distinction of a predo minant, wide-ranging epifauna-based benthic community named the ORM community based on the biomass dominants, the brittle star Ophiothrix quinquemaculata, the sponge Reniera sp., and the ascidians Microcosmus spp. The mean biomass, measured as wet weight, amounted to 370 (±73) g/m² (Fedra et al. 1976).

The early TV-camera sled work encountered a large zone of decaying benthic organisms in the central Gulf of Trieste, Northern Adriatic Sea, in 1974 (Fig. 1 in Fedra et al. 1976). Oxygen deficiency was postulated for this “graveyard” phenom-enon. Over a 2-week period in September 1983, the course of a mass mortality event in the Gulf of Trieste was more comprehensively documented in situ (Stachowitsch 1984). Within 2–3 days, all sponges and the brittle star Ophiothrix quinquemaculata, which together make up over 60% of the community biomass, were dead. The death of sponges, key components of multi-species clumps, killed sponge-dwellers and other bioherm-associated species. This was accompanied by the emergence of the complete spectrum of macroinfauna organisms, including (in approximate order of emergence) holothurians, burro wing shrimp, sea urchins, polychaetes, sipunculids, and bivalves. A spectrum of stress behaviors – involving avoidance patterns and directed toward reaching more oxygenated water layers – was recorded from arm-tipping in brittle stars and swimming in Squilla mantis to hermit crabs emerging from their gastropods shells. Many motile organisms aggre-gated on higher substrates (sediment mounds) and sessile organisms extended certain body parts higher up into the water column (e.g., the tentacle crowns of sea anemones). Mortality was very rapid. Within 2 days, an estimated 90% of the biomass had died. Certain elements of the fauna apparently survived, including the gastropod Hexaplex trunculus and the sea anemone Ragactis pulchra.


3. The Experimental Solution

One might conclude that the severity of the problem means extensive available docu-mentation and full insight into the processes. This is not the case because the precise onset of hypoxia/anoxia is related to local weather and hydrological conditions and continues to be difficult to predict. Moreover, the course of morta lity is often rapid, within a few days. The result is a patchy narrative of low DO events. Laboratory experiments on responses to decreasing oxygen concentrations also have drawbacks: while conditions can be precisely controlled, they cannot reveal natural behavioral responses, intra- and interspecies interactions, morta lity sequences, and community-level processes. One strategy to overcome these methodological shortcomings and to help close the gap in our knowledge is in situ experimentation (Fig. 1).

The approach involves inducing and fully documenting the course of small-scale experimental anoxia on the seafloor. The University of Vienna’s Experimental Anoxia Generating Unit (EAGU) combines photodocumentation with detailed chemo-physical analyses and allows the behaviors and mortalities of benthic organisms to be analyzed from the onset (Stachowitsch et al. 2007). This 50 × 50 × 50 cm plexiglass unit is designed as a chamber with a detachable instrument lid that bears a digital camera, flashes, a sensor array (oxygen, H2S, temperature, and pH), and a datalogger.

EAGU can be deployed in an open configuration (aluminum frame that permits water exchange) to document normal behavior or in a closed configura-

Figure 1. The Experimental Anoxia Generating Unit (EAGU) consisting (clockwise from the top) of camera housing (ch), sensor ports (sp), datalogger (dl), plexiglass chamber (pc), oxygen sensor (os), flashes (fl), external batteries (eb), and protective metal brackets (mb). Right photo: the chamber is positioned over selected macrofauna organisms, and anoxia is generated by respiration within the sealed-off water body.


tion (plexiglass chamber) that seals the enclosed area off and induces hypoxia and anoxia. A typical deployment consists of a 24-h open configuration followed by ca. 3 days in the closed configuration (until anoxia is generated, mortality of most species is reached, and the initial behaviors of the most resistant species documented).

The EAGU concept has yielded a total of more than a dozen experiments. The system induced anoxia within 2 d in every case, followed by increasing H2S values (Fig. 2). Photographs in 6-min intervals and sensor values in 1-min intervals pro-vided a detailed picture of responses and a correlation with oxygen and H2S. The images are processed into time-lapse sequences and also analyzed image by image. The system triggered responses in both the macroepifauna and macroinfauna. On one level, the observed responses and their sequence corresponded to those of earlier reports here and elsewhere, e.g., arm-tipping in brittle stars (Figs. 3 and 4), the upward movement of mobile species to higher levels on available substrates (Haselmair et al. 2010), and the emergence of infauna (Riedel et al. 2008b).

Thus, the EAGU recreated conditions experienced during typical hypoxia and anoxia events and provided previously unknown detail. The emergence patterns and relative emergence times of infauna individuals became visible, as did speed and distance of post-emergence movement. The system also captured species (e.g., infaunal shrimp) whose in situ behavior has never been documented before, either under normoxic or anoxic conditions. On the community level, a complete range of parallel and successive responses were combined in the individual experiments (Fig. 5).

One unexpected phenomenon was predation of brittle stars by sea anemones (Riedel et al. 2008a). In three deployments, five predatory events were recorded

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Figure 2. Dropping oxygen values (dark line) after deployment of closed configuration, and increasing H2S values after generation of anoxia. Five dissolved oxygen thresholds were distinguished.


Figure 3. Three stages of behavioral responses of the brittle star Ophiothrix quinquemaculata to oxygen depletion: suspension-feeding posture (top), arm-tipping (middle), and clinging to substrate.


Figure 4. Three stages of behavioral responses of the brittle star Ophiothrix quinquemaculata to oxygen depletion. Top: normal suspension-feeding posture with arms outstretched. Middle: arm-tipping with central disc held elevated above the substrate. Bottom: clinging flat on the substrate. In a final stage (see Fig. 5b), the brittle stars often fall onto the sediment surface and may overturn.

involving four anemones (three Cereus pedunculatus and one Calliactis parasitica). Under near anoxic conditions, the anemones made contact with, pulled in, and consumed the brittle stars. The duration of each predatory event lasted from 1 to 7.5 h, and regurgitation was recorded in three of the five events. This phenomenon


was interpreted to reflect the different tolerances and behaviors of the species expe-riencing oxygen deficiency: the anemones are not only highly resistant to anoxia but apparently also benefit by taking advantage of more vulnerable prey. Thus, in a narrow window of opportunity, the combined increased activity of anemones, cou-pled with moribund brittle stars, increased predatory efficiency. This may help explain why sea anemones are often a dominant element in the composition of post-mass mortality benthic communities in the Northern Adriatic Sea.

Figure 5. (a) Initial deployment phase – open configuration. (b) Final image of closed configuration after anoxia. Organism abbreviations: ch, the bivalve Chlamys varia; go, the fish Gobius niger; he, the gastropod Hexaplex trunculus; mi, the ascidian Microcosmus sp.; oc, the sea cucumber Ocnus planci; op, the brittle star Ophiothrix quinquemaculata; ph, the ascidian Phallusia mammilata; ps, the sea urchin Psammechinus microtuberculatus; sc, the infaunal sea urchin Schizaster canaliferus; se, serpulid tubeworm. (Note darkened sediment, brittle stars dead on sediment, and emerged sea urchins sc: three individuals from top right to bottom left). See www.marine-hypoxia.com for video version.


4. The Outlook

Within the lifetime of a single generation of marine biologists, the status of the marine environment has changed dramatically, yielding new “extreme” habitats; recent mapping efforts show that nearly half of all marine habitats are strongly affected by multiple threats (Halpern et al. 2008). Overall, the greatest cumulative impact is on coastal ecosystems (Lotze et al. 2006) – the very systems we rely on for most of our marine goods and services (Worm et al. 2006). They will expe-rience the largest change in biodiversity should present trends in human activity continue (Jenkins 2003). Conservation efforts typically focus on higher trophic levels, and restoring ecosystem structure and function remains an unattainable goal (Lotze et al. 2006).

The rise in new “extreme” habitats is reflected in the current status of overall research – a paradigm shift from basic biological/ecological to conservation-related issues. The traditional research landscape has been fundamentally re-aligned in an attempt to identify and understand perturbed systems, prevent further losses, restore impacted habitats, as well as preserve what remains intact. The four eras of marine research identified by Rupert Riedl (1980) – namely, that of seafarers, of oceanographic expeditions, of marine stations, and of field research – have been amended to include a fifth era (Stachowitsch 2003) devoted to studying deteriorated ecosystems. It differs from earlier eras in its underlying conservation aim, narrower scientific focus, and increasing societal component, ever more centralized and directed funding, greater urgency, and in the reduced validity/interpretability of studying damaged objects. Correspondingly, an ever larger percentage of published papers has a conservation bent (for a literature analysis regarding cetaceans, for example, see Rose et al. 2011), and numerous new journals have a clear conservation focus both in title and content.

The rise of new “extreme” environments has also affected benthic research. One trend has been to bring scientists ever closer to their object of study, i.e., to the bottom as divers or with remotely operated or autonomous instruments. The EAGU experimental approach circumvents both the time limitations of direct diver observations and the unlikelihood of being on-site and fully equipped at critical phases of hypoxia/anoxia events. It successfully mimicked the bio-logical processes observed during previous anoxia in the Northern Adriatic Sea. Moreover, many new organisms could be studied at a new level of detail, including the correlation of all behaviors and mortalities with specific oxygen thresholds. The experimental results are valid both from a broader temporal and spatial perspective. The short temporal scale of the deployments, i.e., the generation of hypoxia, anoxia, behavioral modifications, and mortalities within a few days, agrees well with the rapid course of events observed in a previous mortality here (“rapid death, slow recovery”: Stachowitsch 1991, 1984). This approach therefore captures almost the full range of community responses, albeit with potential deficits in documenting the final responses of the most tolerant species. The small spatial scale also yielded more broadly applicable results. There are no larger-scale


factors here (other adjoining habitats, greater structural heterogeneity, or relief features) that would enable alternative behaviors and escape reactions or directions. The relative habitat homogeneity, coupled with the sessile and hemi-sessile life habits of most filter- and suspension-feeding species – and the restricted movements of common mobile forms such as hermit crabs – means that the phenomena observed in the 50 × 50 cm chambers reflect those at much larger scales.

At the same time, the EAGU has recently been deployed to document immediate post-anoxia developments. The first time-lapse results show the quick arrival of a distinct succession of scavenging organisms: initially fish, followed by hermit crabs, and finally gastropods. The issue of scale will play a greater role in interpreting the EAGU-based recovery results than the respective behavior-generating results. In larger-scale anoxia in the Adriatic and elsewhere, the greater distances involved will considerably hinder the immediate immigration of all but the largest and most mobile scavengers and predators. Nonetheless, the sequence of arrival would probably reflect the one we observed above in the films, with fish arriving first. A first look at the EAGU-related longer temporal aspects of recovery (revisiting deployment “plots” at intervals of months or a year) confirms the “slow recovery” aspect after community destruction: no obvious recolonization has taken place. This aspect is still being evaluated but, clearly, in larger dead zones, the relative contribution of immigration to repopulation will shift more toward other strategies (larval settlement).

Ecosystem collapses and slow recoveries will severely impede the role benthic communities play in sublittoral soft bottoms. In the shallow Northern Adriatic, the benthos is not merely a receiving compartment. Complex feedback processes enable the benthic subsystem to control and help dampen oscillations in the pelagic subsystem (Ott 1992). Ott and Fedra (1977) estimated that the suspension feeders here can remove all the suspended material in the water column every 20 days. This is on the same order of magnitude as calculated for the Oosterschelde (Herman and Scholten 1990), Swedish waters (Loo and Rosenberg 1989), the USA (Cloern 1982), and France (Hily 1991). Such communities have therefore been termed as a “natural eutrophication control” (Officer et al. 1982). They help stabilize the entire ecosystem and their loss makes the system more sensitive to perturbations. Other key functional processes for the overall system, such as bio-turbation and related sedimentary activity, may also be altered by hypoxia/anoxia and the corresponding loss of biodiversity (Rosenberg 2001; Levin 2002; Solan et al. 2004; Sala and Knowlton 2006).

Shelf anoxias have a long geological history and were particularly abundant during sea level highstands and during periods of warm temperatures. They are considered as a prime reason for mass extinctions in the fossil record (Hallam and Wignall 1999; Hallam 2004). The recognition that anoxia has played a major role in structuring benthic communities in continental shelf environments, in both the past and present, has led early efforts to find a common terminology and to describe parallel phenomena (Tyson and Pearson 1991). In the case of the


Northern Adriatic shelf, for example, recent efforts have been devoted to drawing parallels between Paleozoic stationary suspension feeders on the sediment surface and the above-described modern, epifauna-dominated ORM community (McKinney and Hageman 2006; McKinney 2007). One argument is that this striking epifauna depends on the presence of stable hard substrata on the seafloor, is very sensitive to sediment input by flood events and storm-induced sediment resuspension, and is related to seasonally high productivity (Zuschin and Stachowitsch 2009). Moreover, the elevation of organisms above the sediment-water interface in multi-species clumps or bioherms helps to survive hypoxia – a typical seasonal feature of the Adriatic shelf and of many ancient epeiric seas. Accordingly, the gradual disappearance of large epicontinental seas along with their low sedimentation rates and frequent bottom-water hypoxia during the Mesozoic may have supported the more global replacement of this archaic epifauna by modern, bivalve-dominated infaunas.

The current status of the ORM community makes it unlikely that it fulfills its pre-mortality regulatory capacity. Such impacted communities, however, can provide crucial information. They serve as a long-term memory of disturbance events because they indicate the status on three levels: behavioral responses over the short-term, mortality or survival over the midterm, and recolonization over the long-term. In the case of the Northern Adriatic, benthic communities were designated as “eutrophication’s memory mode” (Stachowitsch 1992). Depending on community responses on the behavioral and composition levels, the benthos stores information on prior disturbances over years and even decades. The specific configuration of this memory will depend on the severity of the event, the area affected, and the nature of the recolonization process (e.g., immigration and larval settlement).

The experimental approach will lead to a catalog of species-specific behaviors that can be related to distinct oxygen thresholds. Combined with mortality sequences, this will allow us to better define sensitive and more tolerant (indicator) species. The goal is to synthesize the results into a community-based scenario, providing a generally valid framework for determining the status of benthic com-munities exposed to hypoxia based on species compositions/functional groups. The reactions of benthic organisms to hypoxia/anoxia are expected to be the same whether natural or pollution-related, ancient or modern. Therefore, the behavioral reactions, mortality sequences, and post-anoxia conditions and developments will provide valuable information for a wide range of relevant disciplines.

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