MARINE INVERTEBRATES (Chapter 8)

Lead Authors:  Alf B. Josefson and Vadim Mokievsky 

Contributing Authors:Melanie Bergmann, Martin E. Blicher, Bodil Bluhm, Sabine Cochrane, Nina V. Denisenko, Christiane Hasemann, Lis L. Jørgensen, Michael Klages, Ingo Schewe, Mikael K. Sejr, Thomas Soltwedel, Jan Marcin We¸sławski and Maria Włodarska-Kowalczuk

SUMMARY

This chapter brings together baseline information on the diversity of marine invertebrates in the Arctic Ocean and discusses the importance of factors that have shaped patterns of biodiversity.

The Arctic Ocean is here defined as the areas north of the Bering Strait on the Pacific side and areas with consistent seasonal sea ice cover on the Atlantic side. The known marine invertebrate fauna of this area comprises c. 5,000 species, representing at least 24 phyla with representatives in all three marine realms: sea ice, pelagic and benthic. About 50% of the Arctic Ocean overlays continental shelf areas at water depths ranging from 0-500 m. This Arctic Shelf constitutes 31% of the total shelf area of the world. More than 90% of the known Arctic invertebrate species occur in the benthic realm. As for terrestrial environments, the most species rich taxon in all realms is Arthropoda, with most species among crustaceans, i.e. >1,500 species according to a recent estimate. Other species-rich taxonomic groups are Annelida, mainly bristle worms (Polychaeta), moss animals (Bryozoa) and Mollusca, including bivalves (Bivalvia) and snails (Gastropoda). Among the meiobenthos (small-sized benthic metazoans, < 1 mm) the predominant groups are free-living nematodes (Nematoda), followed by harpacticoids (Copepoda: Harpacticoida). In terms of abundance and biomass, nematodes and harpacticoid copepods typically dominate the meiofauna (as they do elsewhere), while polychaetes, bivalves and amphipods typically dominate the macrofauna, and echinoderms and crustaceans dominate the megafauna.

“There are areas where the salmon is expanding north to the high Arctic as the waters are getting warmer which is the case in the Inuvialuit Home Settlement area of the Northwest Territories of Canada. Similar reports are heard from the Kolyma River in the Russian Arctic where local Indigenous fishermen have caught sea medusae in their nets. Mustonen 2007.

The number of known marine invertebrate species in the Arctic Ocean is very likely to increase in the future, because vast areas, particularly the deep-sea basins, are under-sampled. For example, a recent estimate suggests that several thousand benthic species have been missed to date. Contrary to paradigms of an impoverished Arctic fauna due to a harsh environment, as seen in the terrestrial realm, the Arctic shelf fauna is not particularly poor, but considered to be of intermediate richness, similar in overall species richness to some other shelf faunas, such as the Norwegian shelf. The pattern of declining species richness with increasing latitude, obvious in the terrestrial realm, is controversial among marine invertebrates and conclusions depend on the taxon and geographic scale studied. A latitudinal decline from the tropics to the Arctic was seen in shelf molluscs, while arthropods seem to show higher diversity in some Arctic areas compared with some non-Arctic areas.

Due to the turbulent geological history with repeated glaciation events over the last 3.5 million years, together with in ineffective isolation from adjacent oceans, in situ evolution of species has been hampered, and as a consequence there are few Arctic endemics, at least on the continental shelves. However, bryozoans contain more endemics than many other groups, possibly partly related to poor dispersal in this group.The present-day invertebrate fauna in the Arctic is a mixture of species with different origins, where the majority have distributions reaching outside the Arctic, i.e. the boreal parts of the adjacent oceans. By and large the Arctic Ocean is a sea of immigrants that have dispersed from adjacent oceans both in historical and in recent time.

Today’s biogeographic drivers of Arctic diversity are clearly seen in the distributions of origins in relation to the two major gateways into the Arctic, i.e. from the Atlantic Ocean and the Pacific Ocean. On the continental shelves the proportions of present-day Pacific and Atlantic species decrease with increasing distance from the Bering Strait and the NE Atlantic, respectively. Current inventories indicate that the Barents Sea has the highest species richness, being ‘enriched’ by sub-Arctic and boreal species. Today’s Arctic deep-sea floor is most closely related to the present North Atlantic fauna, which in a geological time perspective contains a strong Pacific influence.

Like other faunal elements in the Arctic, marine invertebrates are affected by climate warming. The most obvious effects will be on the fauna of the permanent ice (sympagic fauna) which will lose its habitat. However, detecting effects in the other realms is difficult, mainly because there are only few time series data available. It is expected that the fauna with strong boreal influence may show (perhaps temporarily) increased diversity, due to a combination of anticipated increased food availability for the benthos and immigration of species adapted to warmer waters. Signs of borealization are already seen in marginal areas of the Actic Ocean. Long-term estimates of climate change effects on diversity are challenging because of the complex interactions of changes on multiple levels of the Arctic system.

It is recommended that conservation actions are targeted towards whole systems rather than individual species. Since system-focused conservation efforts typically focus on limited regions, we need to know more about diversity patterns at a high spatial resolution, in particular the distribution of Arctic endemics in order to conserve as many unique species as possible. Also we need to identify the ‘biodiversity hotspots’ – the areas which harbor high numbers of unique species due to habitat complexity and other factors.There is a demand for research to get a better understanding of the factors and processes that affect diversity. To achieve this, regional and taxonomic gaps need to be closed and time series are needed to address temporal dynamics and changes in biodiversity. However, since time is probably short before severe effects of climate change will appear, we cannot wait for a high frequency mapping of the whole Arctic. Instead we suggest the establishment, or in some cases continuation, of time series monitoring at selected sites in species rich Arctic areas close to the major gateways, as well as in some areas distant from the gateways into the Arctic. We also suggest protection of areas with the highest proportion of Arctic endemic species, as well as the productive polynyas where pelagic-benthic coupling is strong and that are of high importance for higher taxonomic life

INTRODUCTION

In this chapter, we consider the diversity of invertebrates from the entire benthic, pelagic and sea-ice realms of the Arctic Ocean, broadly defined as areas north of the Bering Strait on the Pacific side and areas with consistent seasonal sea ice cover on the Atlantic side (Bluhm et al. 2011a). This corresponds broadly to the delineation of the Arctic waters made in Fig. 6.4 in the fish chapter (Christiansen & Reist, Chapter 6), but excluding the Bering and Norwegian Seas. We recognize, however, that the literature cited below does not always follow this delineation.

The present invertebrate diversity in the Arctic Ocean area is the net result of many factors acting both in historical and recent time. Like in other systems on Earth, species diversity in the Arctic is influenced by nichebased factors, such as adaptation to different environmental conditions and by dispersal based factors, such as immigration from species pools. The relative importance of these two types of factors is not always easy to disentangle and may vary with scale and the degree of connectivity to other ecosystems.

Niche-based factors like adaptation to different environmental conditions are likely to account for a significant part of biodiversity in the Arctic because it is far from homogeneous. In each of the three realms, invertebrate species inhabit a multitude of different habitats. The pelagic realm contains downwelling or upwelling areas, frontal zones and polynyas with a varying degree of coupling with the benthic realm below. The recent permanent ice-cover in the Central Arctic and seasonal ice in the rest of Arctic act as a specific habitat for sea-ice associated life, and within the ice realm habitats vary from highly productive ice edge areas to more oligotrophic zones in brine channels in the ice, as well as the ice-water interface on the underside of the ice.

The sea floor contains considerable large scale topographic heterogeneity, for instance intertidal coastal areas, semi-enclosed fjords with fjord basins, estuaries of different sizes, an expanded shelf zone with a number of canyons (Voronin, St. Anna) and inner isolated depressions (like Novaya Zemlya Trench), and the deep sea with several basins separated by deep-sea ridges. At smaller scales, benthic areas contain different sediment habitats such as sand and mud as well as harder substrata like boulders and bedrocks. The Arctic Ocean covers a large area, of which about 50% overlays shelf zones, which in turn constitute 31% of the total shelf area of the world (Jakobsson et al. 2004). It is well known that diversity generally increases with the extent of an area (MacArthur & Wilson 1967). If so, we would expect a high total diversity in particular of Arctic shelf fauna relative to deep sea areas.

A conspicuous feature of the sea areas of the Arctic is the strong gradient in salinity, both horizontally from river mouths out into the open sea as well as vertically, from close to fresh near the surface to fully marine at depth. Hence, in addition to seasonal ice melt, salinity gradients are highly influenced by freshwater inputs from mainly the Russian rivers, but also the MacKenzie and Yukon rivers in the western part of the Arctic Ocean. These large rivers together with smaller ones create estuarine systems of different spatial sizes which often harbor a peculiar set of species adapted to cold water of low salinity. The area of most intensive fresh water impact is regarded as a specific zoogeographical unit (Siberian brackish shallow province by Filatova 1957). A consequence of high freshwater inputs is also the permanent stratification of the central Arctic Ocean with a surface salinity of less than 32‰ and a deep water salinity of 34‰ (Gradinger et al. 2010a), thus providing different habitats for planktonic invertebrates, because pelagic organisms, like benthic ones, have different tolerances for low salinity.

Furthermore, different parts of the Arctic have different levels of productivity (Michel, Chapter 14), which also may affect diversity (Currie 1991). Productive areas often have more species than unproductive areas, but the causal relationships are still unclear (Currie et al. 2004) and firm evidence is also lacking for such effects on marine benthic diversity, although hump-shaped relationships have been reported between chlorophyll a and Arctic benthos richness (Witman et al. 2008). An example of an oligotrophic area is the Beaufort Gyre, as compared with a productive area in the Chukchi Sea shelf (Gradinger 2009) or Barents Sea shelf (Sakshaug 1997, Denisenko & Titov 2003).

The Arctic Ocean may be regarded as an open system where the strength of the connections with adjacent oceans has changed over the last 4 million years. Water currents facilitate dispersal from sub-Arctic and boreal parts of adjacent oceans, through the Fram Strait and the Barents Sea from the Atlantic, and the Bering Strait from the Pacific Ocean (e.g. We¸sławski et al. 2011). While the connection with the Pacific has opened and closed over time due to varying sea levels, the deep Atlantic entrance has been widely open. At present, there is some 10 times more Atlantic water than Pacific water flowing into the Arctic Ocean (Loeng et al. 2005).

In addition to habitat complexity and the importance of recent dispersal from adjacent oceans, the turbulent geological history has also been important in shaping present day diversity of Arctic invertebrates. In the comparatively young Arctic Ocean, the evolutionary origin of marine invertebrates reflects a Pacific origin dating back to the opening of the Bering Strait 3.5 million years ago (Adey et al. 2008). Throughout most of the Tertiary, the Arctic Ocean region supported a temperate biota, and fully Arctic conditions developed only during the latest part of this period. Sea ice cover formed c. 3-5 million years ago (Briggs 2003). Over the last 3-5 million years, a series of glaciation periods with intermittent de-glaciations has created an unstable environment with a series of extinction and immigration events shaping present day diversity. These extinction events are thought to have precluded extensive local evolution or endemism on the shelves (Dunton 1992). Furthermore, events during the last 3.5 Myr have allowed great re-distributions of species in the boreal part of the northern hemisphere likely still affecting Arctic diversity today. The most pervasive change occurred during the late ice-free Pliocene, after the opening of the Bering Strait, when extensive transgressions of invertebrates species across the Arctic occurred (Vermeij 1989, 1991, Mironov & Dilman 2010), mainly from the species-rich Pacific center of diversity (Briggs 2003) to the Northern Atlantic, an event called ‘The Great Trans- Arctic Biotic Interchange’ (Briggs 1995). As contended by Briggs (2007), there is little evidence from the marine realm that invasions have decreased native diversity, but rather that they have added to the native diversity, resulting in an overall increased diversity. A result of this major transfer was therefore likely an enrichment of the Northern Atlantic pool of species with Pacific species. This pool of species may be the source of immigration into the Arctic Ocean in recent time.

Against this background we expect that invertebrate diversity in the Arctic Ocean has been shaped to a high degree by dispersal based factors like immigration and a low degree of endemism. We expect the Arctic Ocean to be dominated by wide-range boreal species. In this respect, it is interesting to compare the degrees of endemism in the Arctic with those in the Antarctic, another cold region with similar glaciation history (Krylov et al. 2008), but which has been much more isolated from adjacent oceans by the strong Antarctic Circumpolar Current (ACC). The ACC, formed in the Miocene, is the only current on Earth extending from the sea surface to the sea floor, unimpeded by any landmasses (Hassold et al. 2009). We certainly would predict a much higher degree of endemism in the Antarctic, which as we will see is in fact the case. Furthermore, given that connectivity is strong between the Arctic Ocean and the boreal parts of the Pacific and the Atlantic oceans, we would not expect a markedly lower richness in the Arctic, but fairly similar levels of species richness as in the other oceans, at least in proximity to the two gateways.

In addition to the natural structuring factors, diversity patterns in the Arctic Ocean likely are influenced by variation in sampling methods as well as sampling frequency. For instance, some areas have been extensively investigated for more than a century (Barents Sea), while other less accessible areas (deep Arctic basins) have been relatively poorly studied. This creates a challenge when estimating total numbers of species in the Arctic.

The main questions addressed in this review are:

• Is the marine invertebrate diversity in the Arctic Ocean impoverished compared with adjacent areas?
• Are there large scale diversity patterns within the AO area that can be attributed to dispersal rather than niche adaptation?
• Is the turbulent geological history and openness to adjacent oceans mirrored by a low degree of endemism?
• Are there ‘hotspot’ areas that by virtue of their species diversity should be protected?
• Can we predict what the effects of global warming on invertebrate species diversity?

CONCLUSIONS AND RECOMMENDATIONS

Conclusions

The Arctic Ocean area hosts c. 5,000 species of marine invertebrates, which is a similar level as is found in the other polar environment, Antarctica, and is considered intermediate on a global scale. Arthropoda, mainly crustaeans, is the most speciose group and does not exhibit the decreasing richness with increasing latitude as found in Mollusca.

Although the Arctic contains great morphological heterogeneity and a vast number of environmental gradients, giving the opportunity for extensive niche adaptation, Arctic diversity seems largely a result of extinctions and dispersal events over the last c. 4 million years. Most species have origins from outside the Arctic, and overall there are few species endemic to the Arctic. The degree of endemism varies greatly among different taxonomic groups, where bryozoans for example seem to have a relatively high degree of endemism possibly partly due to their sessile habits and, maybe more importantly, poor dispersal ability.

The glaciation history of the two polar oceans seems fairly similar, but unlike the Antarctic which has a long history of geographic isolation, the Arctic has been, and is, open towards the two major oceans, the Pacific and the Atlantic, although the strength of the connections have varied over the last c. 4 million years. This is a likely explanation for the very low degree of endemism in the Arctic compared with the Antarctic. Today’s biogeographic drivers of Arctic diversity are clearly seen in the distributions of origins in relation to the two major gateways into the Arctic, i.e. from the Atlantic and Pacific Oceans, respectively. On the continental shelves, the proportions of present-day Pacific and Atlantic species decrease with increasing distance from the Bering Strait and the NE Atlantic, respectively. Current inventories indicate that the Barents Sea has the highest species richness, being ‘enriched’ by boreal and sub-Arctic species. Today’s Arctic deep-sea floor is most closely related to the present North Atlantic fauna, which in a geological time perspective contains a strong Pacific influence. The regional species richness is highest in Arctic regions close to the two gateways, the Chukchi Sea for the Pacific and, even higher, the Barents Sea/ Kara Sea for the Atlantic. These observations together with the distribution patterns of zoogeographical affinities indicate the importance of dispersal through the gateways into the Arctic Ocean.

While areas within the Arctic with high species richness have been identified, such as the Barents Sea, it is uncertain if there are real ‘hotspots’ of diversity, i.e. areas with high diversity of unique or endemic species in the Arctic. This is because many of these species may be abundant in waters to the south and thus not unique. The polynyas, ice-free areas within the area of sea ice, may be hot spots in terms of energy flow (Michel, Chapter 14), where benthic and pelagic invertebrates provide food for dense aggregations of birds and mammals.

There are already clear signs of global warming effects on invertebrates, for instance northward expansion of several boreal species. As would be predicted, this borealization has so far occurred in the margins of the Arctic Ocean, primarily at the two major gateways to the boreal parts of the Atlantic and Pacific. The rapidly melting sea ice means loss of habitat for sympagic fauna.

In addition to temperature rise, global change will acidify the oceans, and there is a great concern that this will negatively affect calciferous invertebrates like several benthic as well as pelagic molluscs. Experimental work shows that acidification hampers shell formation in wing snails.

Recommendations

It is recommended that conservation measures are targeted towards whole systems rather than individual species. Specifically, there are urgent needs to document and understand Arctic biodiversity patterns and processes to be able to prioritize conservation efforts.

We need more inventories

This includes the need to know where the highest diversity occurs in the Arctic, particularly for endemic species, in order to conserve as many unique species as possible. Hence, there is a need for:

• Detailed surveys of diversity in hitherto understudied areas like the East Siberian Sea and the Canadian Arctic, together with deep-sea areas of the Central Arctic Basin and at the Arctic-Atlantic frontier. Studies are also needed in the shallow subtidal to 12 meters, which still is an understudied area.
• Increased sampling and taxonomic effort on poorly investigated groups, including several among the meiofauna.
• Establishing and continuing several observation sites for long-term monitoring of marine ecosystems in different parts of the Arctic proper to obtain a more holistic view of the changing Arctic. The existing biological stations together with marine protected areas could serve as a base for such long-term observations.
• A priority focus on consistent time series monitoring at sites in the species-rich Arctic areas close to the major gateways, as well as in some areas distant from the gateways. Given the likelihood of little time before more severe climate change effects will be manifested, this entails both the establishment of some new sites and the continuation of monitoring at existing sites such as the White Sea Biological Station, the Greenland Ecosystem Monitoring in Godthåbsfjorden in W Greenland and Young Sund in NE Greenland, and the HAUSGARTEN observatory west of Svalbard. The number of observatories in both deep and shallow waters has to be increased to include a wide spectrum of testing areas and communities. Repeated sampling should be conducted in the places of former studies, like those of Golikov (1990, 1994a, 1994b, 1994c) in the Laptev and West Siberian Seas. These studies provide a sufficient background to evaluate any changes in recent community structure and composition.

We need research to understand maintenance of diversity so it is recommended:

• To quantify immigration rates of boreal species into the Arctic and investigate the possible influence of global warming on these rates.
• To investigate whether or not immigration of boreal species ‘enriches’ native diversity, and whether immigrants have a negative influence on the native fauna.
• To further implement molecular taxonomy to discover the likely presence of sibling species and to reveal historical migration patterns. The most optimistic estimates predict a diversity of ‘molecular operational taxonomic units’ as much as three times the number of described morphological species, even in such well studied groups as the Polychaeta (Carr et al. 2011).
• To investigate how increased primary production, which may be one consequence of shrinking ice cover, affects species diversity both in the pelagic and the benthic systems. This could be performed in connection with polar fronts and productive polynyas.
• To investigate how climate change influences changes in biogeographic distributions, specifically the borealization process, habitat loss for sympagic fauna and the distribution of calciferous fauna.

Based on present knowledge we recommend protection of the following areas:

• Polynyas which are areas known to be important for maintaining seabird and mammal populations. These areas should be closed for fishing as well as petroleum extraction. The latter is necessary because it is virtually impossible to clean up oil in waters with broken ice.
• Large estuaries, which harbor several of the unique Arctic species.