vol. 31, no. 3, pp. 205–216, 2010 doi: 10.2478/v10183−010−0001−5
Hidden diversity in Arctic crustaceans. How many roles can a species play?
Jan Marcin WĘSŁAWSKI1, Artur OPANOWSKI2, Joanna LEGEŻYŃSKA1, Barbara MACIEJEWSKA3, Maria WŁODARSKA−KOWALCZUK1 and Monika KĘDRA1
1 Instytut Oceanologii PAN, Powstańców Warszawy 55, 81−712 Sopot, Poland
Abstract: The life modes and sizes of 98 species of higher crustaceans (Malacostraca) from Hornsund and Kongsfjorden (Svalbard fjords) were analyzed. The majority (90%) of the species were perennial, K strategists, with eight− to tenfold size differences between newborn and adult specimens. The largest species are carnivores and carrion feeders, while the smallest are sediment−dwelling suspension and deposit feeders. Compared with the crustacean fauna of northern Norway (over 500 species), the Svalbard fjord crustacean fauna is less diverse (below 150 species). The crustacean species populations from the Arctic fjord are more numerous (average number of ind./species/m2) compared to those of the northern Norway boreal fjords. Crustaceans with long life cycles and distinct size dif− ference between juveniles and adults represent three to five ecologically different func− tional “species” each, since the smaller size groups of the same species differ with regard to their mobility, food and habitat use. Thus, crustaceans are ecologically and functionally more diverse than expected from simple species count.
Key words: Arctic benthos, Crustacea, biodiversity, life cycles.
Introduction
On numerous occasions in the history of taxonomy juveniles, males, or fe− males of the same species have been described as separate taxa by naturalists unfa− miliar with their biology. Even when morphological differences are not very strik− ing, marine invertebrate juveniles being much smaller than adults, are nursed in separate habitats to avoid cannibalism. Typically, mobility changes with onto− genic development, and juveniles are slower and less mobile than adults, as is the
Pol. Polar Res. 31 (3): 205–216, 2010
Unauthenticated Download Date | 1/10/18 1:45 AM 206 Jan Marcin Węsławski et al. case, for example, with euphausiids and mysids (Mauchline 1980). Since juveniles and adults are separated by habitat and niche, they act as separate species in terms of their functional roles in a given ecosystem. For the scope of this paper there are two well−established ecological observa− tions about the Arctic: (1) Thorson’s (1936) rule describes the tendency of Arctic species to modify life cycles, reducing larval stages, and investing energy in larger and less−dispersed off− spring. This phenomenon was later identified as one of the effects of K breeding strategy in cold waters (Clarke 1980, 1999, 2003). Recent, extensive studies on Arc− tic benthos confirmed the prevalence of direct development, brooders, and short− −lived lecitotrophic larvae over planktotrophic pelagic stages (Piepenburg et al. 2006, 2007; Fetzer and Arntz 2008). (2) Rapoport’s rule (Stevens 1989) states that Arctic ecosystems are species poor since the ranges of occurrence of particular species in high latitudes tend to be very wide. In consequence Arctic species are less specialized and niches are not densely packed. Recent attempts to confirm this observation have been somewhat dubious; although this seems to be true for benthos in general, and specifically for some taxa, like Mollusca and Bryozoa, other taxa (e.g. Amphipoda) are not at all impoverished in polar waters (Palerud and Vader 1991; Jażdżewski et al. 1995). The aim of the present paper is to propose a new idea that polar water ecosys− tems might be more diverse than previously thought, because of the ecological ef− fects of the prevailing K strategy in macrobenthos populations. This is based on the assumption that the larger the size difference is between adults and offspring, then the larger their ecological separation is. As typical K strategists polar animals are characterized by low mortality and long life spans. Since cold water species grow more slowly and attain larger sizes, the separation of ecological roles within them is stronger compared to inhabitants of warm waters. In effect, in cold−water populations single taxa can be represented by numerous “eco−species” that physi− cally occupy different places in the ecosystem. In warm waters, among the prevail− ing small species, there are usually lesser size differences between juveniles and adults, higher mortality rates, and less numerous populations, all of which means that there is competition among true species. Based on these assumptions, the aim of this paper is to explain why polar shelf waters, which are so productive, are also typically species poor in comparison with warmer waters.
Methods
Macrozoobenthos species were collected with different types of gear from two polar fjords (Hornsund 77°N, and Kongsfjorden 79°N, Svalbard archipelago) (Fig. 1) during summer campaigns of r/v Oceania between 2000 and 2007. Crusta− cean length was measured in a specific way – Amphipoda, Decapoda, Isopoda,
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10o E 20o E 30o E
80o N
Kongsfjord
Spitsbergen
Hornsund
1000m Svalbard archipelago 100m 75o N
Atlantic Waters Arctic Coastal Waters
Fig. 1. Study area.
Mysidacea, Euphausiacea, Cumacea length were measured from the tip of the rostrum to the end of telson, except of Brachyura where the width of carapax was measured. Only malacostracan Crustacea were selected for the present paper since their measurements were the most numerous and complete. Twelve pelagic Crustacea species were also included since most hyperiids and euphausiids are ob− served near the bottom, often feeding at the seabed, and are found frequently in benthic dredges. The minimal taxon size is that of newborn animals commencing independent life. In brooders this is the size after leaving the brood pouch, while in larval developers it is the size of the larvae. “Mean individual size” refers to the av− erage size of an animal in the samples and, although this might be misleading, since samples are always collected from an unknown fraction of the population, it does indicate what size of a given species is most frequent in the system analyzed. “Maximal individual size” is the largest size of a species recorded in the sample collection from a study area, and it represents the ability of a given species to grow to a certain limit if conditions are appropriate. The percentage relation between minimal and maximal size (i.e., what percentage juvenile size is of adult body size)
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Table 1 Summary table of crustacean species characteristics. Length in mm, feeding types: c – car− nivore, s – suspension feeder, h – herbivore, f – filtrator. Mobility types: m – mobile, dm – discretely mobile, nb – nectobenthic, p – pelagic. Zoogeographic types: A – Arctic, AB – arcto−boreal, B – boreal. max/ zoogeo− mean min max feeding mobility n min graphic length length length type type index type AMPHIPODA Acanthostepheia malmgreni (Goës, 1866) 21 7 5 36 7 c m A Ampelisca eschrichtii Krøyer, 1842 11.6 29 3 37 12 s dm AB Anonyx laticoxae Gurjanova, 1962 16 21 3 33 11 c nb A Anonyx nugax (Phipps, 1774) 18.3 19 3.5 44 13 c nb A Anonyx sarsi Steele et Brunel, 1968 17 90 3 30 10 c nb A Apherusa sarsii Shoemaker, 1930 9 9 3 15 5 h m A Apherusa glacialis (Hansen, 1887) 8 91 2 17 9 h m A Arrhis phyllonyx (M. Sars, 1858) 8 95 3.1 19.25 6 s m A Atylus carinatus (Fabricius 1793) 9 12 3 21 7 c m A Byblis gaimardi (Krøyer, 1846) 10 12 3 18 6 s dm AB Calliopius laeviusculus (Krøyer, 1838) 9 10 3 18 6 c m AB Caprella septentrionalis Krøyer, 1838 16 38 3.4 26 8 s dm AB Gammarellus homari (Fabricius, 1779) 21 86 5 35 7 c m AB Gammarus oceanicus Segerstråle, 1947 11 98 4 38 10 s m B Gammarus setosus Dementieva, 1931 12.7 93 4.2 34 8 s m AB Gammarus wilkitzkii Birula, 1907 12 120 3.5 40 11 c m A Goesia depressa (Goës, 1866) 4 6 2.5 11 4 s/f dm AB Halirages fulvocinctus (M. Sars, 1858) 7 11 3 17 6 s m AB Haploops tubicola Liljeborg, 1855 6.4 46 2.5 21 8 s dm AB Harpinia propinqua (G.O. Sars, 1895) 4 9 3 6 2 s m AB Hyperia galba (Montagu, 1815) 4 10 3 7 2 c p B Hyperoche medusarum (Krøyer, 1838) 5 11 3 9.5 3 c p B Idunella aequicornis (G.O. Sars, 1876) 4 3 3 8 3 s m A Ischyrocerus anguipes Krøyer, 1938 8 100 3 17 6 s m AB Lepidepecreum umbo (Goës, 1866) 3.8 8 2 7 4 s m A Melita dentata (Krøyer, 1842) 12 23 3 28 9 s m AB Melita formosa Murdoch, 1866 10.2 38 6 26.5 4 s m A Melita quadrispinosa Vosseler, 1889 8.1 130 4.4 12.9 3 s m AB Menigrates obtusifrons (Boeck, 1861) 5 11 2.5 10 4 c m B Metopa boeckii G.O. Sars, 1892 3.5 5 2.5 4 2 s m A Monoculodes borealis Boeck, 1871 8 21 2.5 15 6 s m AB Monoculodes longirostris (Goës, 1866) 9 20 3 18 6 s m A Monoculodes packardi Boeck, 1871 4.55 28.5 3 9 3 s dm AB Neohela monstrosa (Boeck, 1861) 11 4 3 25 8 f dm AB Onisimus caricus Hansen, 1886 16 84 3 24 8 c m A Onisimus edwardsi (Krøyer, 1846) 9 90 4 14 4 c m AB Onisimus litoralis (Krøyer, 1845) 8 200 3 25 8 c m A Orchomenella minuta (Krøyer, 1846) 5 30 4 9 2 c m A Parapleustes bicuspis (Krøyer, 1838) 9 7 3 12 4 s m AB Parapleustes monocuspis (G.O. Sars, 1893) 6 8 4 13 3 s m AB Pardalisca cuspidata Krøyer, 1842 3 1 3 3 1 s m AB Paroediceros lynceus (M. Sars, 1858) 16 257 4 24 6 s m AB
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Phoxocephalus holbolli (Krøyer, 1842) 3 12 2 5 3 s dm AB Pleustes panopla (Krøyer, 1838) 9 11 3 21 7 c m A Pleusymtes glabroides (Dunbar, 1954) 8 10 2.5 12 5 s m AB Pontoporeia femorata Krøyer, 1842 5.2 51 2 16 8 s m B Protomedeia grandimana Brüggen, 1905 4.6 9 2 7 4 s m AB Rhachotropis aculeata (Lepechin, 1780) 16 10 4 28 7 c m A Rozinante fragilis (Goës, 1866) 10 5 3 20 7 c m A Schisturella pulchra (Hansen, 1887) 8 7 3 12.5 4 s m AB Stegocephalus inflatus Krøyer, 1842 13.7 33 4.3 35.6 8 s m AB Syrrhoe crenulata Goës, 1866 3.1 40 3 8 3 f/s m AB Themisto abyssorum Boeck, 1870 9 300 2.5 17 7 c p AB Themisto libellula (Lichtenstein, 1822) 14 300 2 33 17 c p A Unciola leucopis (Krøyer, 1845) 7.5 42 3 14 5 s m A Weyprechtia pingus (Krøyer, 1838) 12 100 3 25 8 s m A CUMACEA Campylaspis rubicunda (Liljeborg, 1855) 4 11 3 6 2 f/s m AB Diastylis cf rathkei (Krøyer, 1841) 6.2 40 2 15 8 f/s m BA Diastylis goodsiri (Bell, 1855) 8.9 24 3 24 8 f/s m A Diastylis lucifera (Krøyer, 1837) 3.7 12 3 6 2 f/s m B Diastylis scorpioides (Lepechin, 1780) 5.1 8 3 8 3 f/s m A Eudorella emarginata (Krøyer, 1846) 5.55 114 1.9 10.4 5 f/s m AB Leucon nasica (Krøyer, 1841) 3.7 19 2 10 5 f/s m AB Leucon nathorsti Ohlin, 1901 5.5 94 3.2 8.9 3 f/s m AB DECAPODA Eualus gaimardi (Milne Edwards, 1837) 47 48 8 61.4 8 c m AB Hyas araneus (Linné, 1766) 26 18 8 42 5 c m AB Lebbeus polaris (Sabine, 1821) 30.9 334 6 47.9 8 c m AB Pagurus pubescens (Krøyer, 1838) 3.5 11 2 8 4 c m B Pandalus borealis Krøyer, 1844 60.3 121 12 112.5 9 c m AB Sabinea septemcarinata (Sabine, 1821) 51.6 170 10 78.5 8 c m A Sclerocrangon boreas (Phipps, 1774) 32.4 34 12 63 5 c m B Spirontocaris spinus (Sowerby, 1805) 26.6 63 6 48.5 8 c m AB Spirontocaris turgida (Krøyer, 1842) 30 23 8 56 7 c m A ISOPODA Eugerda tenuimana (G.O. Sars, 1868) 3 12 1.5 3.5 2 s dm AB Eurycope sp. 2 20 1.5 3.5 2 s dm AB Gnathiidae sp. 3.5 9 2 4 2 s m A Ilyarachna hirticeps G.O. Sars, 1870 6 8 4 11 3 s m AB Janira sp. 10.9 37 4.2 15 4 s m AB Munna fabricii Krøyer, 1847 3 11 2 4 2 s m AB Munnopsis typica M. Sars, 1861 6 7 4 16 4 s m AB Synidotea nodulosa (Krøyer, 1846) 8 21 3 18 6 s m A MYSIDACEA Erythrops erythrophthalma (Goës, 1864) 6 6 4 10 3 s p AB Mysis oculata (Fabricius, 1780) 16 160 3 32 11 s p A Pseudomma truncatum Smith, 1879 10.9 37 4.2 15 4 s p AB Stilomysis grandis (Goës, 1863) 8 5 3 18 6 s p B EUPHAUSIACEA Thysanoessa rashii (M. Sars, 1864) 14 12 3 22 7 h p AB Thysanoessa inermis (Krøyer, 1846) 16 64 3 30 10 h p A Thysanoessa longicaudata (Krøyer, 1846) 13 8 3 20 7 h p AB Meganyctiphanes norvegica (M. Sars, 1857) 22 21 4 32 8 h p B
Unauthenticated Download Date | 1/10/18 1:45 AM 210 Jan Marcin Węsławski et al. is a proxy for the ecological separation between the development stages of a given species. In addition to the size differences between juveniles and adults, other fac− tors (depth, mobility, feeding mode, habitat) were also considered when estimat− ing how ecologically distant juveniles are from adults (Table 1). Study area covers two fjords of West Spitsbergen, of relatively high latitude (77 to 79°N), yet warmed by the West Spitsbergen Current waters, carrying Atlan− tic waters of 3 to 6 °C temperature and salinity over 34,5 PSU. These fjords use to be dominated by local, coastal waters of mixed origin, freshened and colder than shelf waters (near bottom temperature between −1 and 1 °C in summer, salinity 33 to 34 PSU). Fast ice covers the inner fjord basins from January till late May; de− tailed hydrographic information is presented in the papers by Swerpel (1985), Svendsen et al. (2002), Walczowski and Piechura (2006).
Results
Ninety−eight species of Malacostraca from the fjords were measured and de− scribed regarding their size, zoogeographic affinity, and functional group (Table 1). Twenty percent of the species examined had a juvenile to adult size difference index below 3, while 50% of species had a juvenile to adult size difference index above 6 (Table 1). The relation between the mean size of crustaceans and the juvenile to adult size difference index indicates that the largest species (Decapoda), with the relatively largest juveniles (mysid stage larvae), differ from the majority of amphipod spe− cies that exhibit a rapid increase in the difference index along with increasing mean individual size (Fig. 2). The juvenile to adult size increase was most pro− nounced in carnivorous amphipod species and decapod crustaceans. The least di− verse were small, sediment−dwelling surface deposit−feeders from Isopoda and Amphipoda (Figs. 2 and 3). When zoogeographical affinity is considered, boreal species are best repre− sented by small size groups, since over 60% of boreal species have a size class di− versity index of below 5. Arctic species are best represented by large species, and 60% of them have a size class index above 6. Arcto−boreal species are in an inter− mediate situation (Fig. 4). Two populations of the same species living in hydrologically contrasting fjord basins were measured in five cases. All of these indicated that the population from the warmer water (Kongsfjorden) was represented by smaller specimens in com− parison to the cold−water (Hornsund) animals (Table 2).
Discussion
Advantages of being different from parents. — Most often, juveniles of ma− rine species live close to the sea surface in shallower waters among seaweed or
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18
16 Amphipoda Decapoda 14 Isopoda 12
10
8
6
min/max difference 4
2
0 0 10203040506070 body length (mm)
Fig. 2. Relation between mean size of crustaceans species and minimal to maximal size difference.
Table 2 Size difference (length in mm) between populations of the same species living in cold and warmer site (KGF – Kongsfjorden, HOR – Hornsund) KGF KGF KGF KGF KGF HOR HOR HOR HOR HOR Taxon mean n SD min max mean n SD min max Arrhis phyllonyx 6.3 69 3.5 2 19 9.7 120 4.1 4.2 19.5 Eudorella emarginata 5.5 170 2.6 1 11 5.6 57 2.2 2.8 9.8 Leucon sp. 3.7 19 2 2 10 5.5 9 1.8 3.2 8.9 Monoculodes packardi 3.3 24 1.2 3 8 5.8 33 0.4 5.1 6.8 Eualus gaimardi 34 104 4.5 19 46 47 48 7.2 23.7 61.4 rock crevices that provide shelter (Węsławski and Legeżyńska 2002). As they grow, they tend to live in deeper, more open areas. In addition to physical separa− tion in the environment, juveniles and adults are also frequently separated by their position in the food web and the ecological niches they occupy. Smaller individual size means that smaller prey is available, and such individuals are susceptible to smaller carnivores in comparison to adults. The distinct bimodality in benthos size spectra was regarded by Warwick et al. (1986) and Kendall et al. (1997) as a typi− cal phenomenon observed in waters from the tropics to the Arctic, which provided a way to avoid both competition and predation. The exception is in the Antarctic, where macrofauna juveniles fill the size gap between meio− and macrofauna (Warwick et al. 1986). Many aspects of marine poikilotherms life history are re− lated to body size (Woodward et al. 2005; White et al. 2007). The size and growth rates are usually well correlated with ambient temperature; life in cold water re− sults in slower metabolic rates, longer life spans, and larger adult size, while the
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Size classes and feeding types in crustaceans, Hornsund 100%
80% s 60% sf 40% c 20%
0% 2to3 4to5 6to7 8to9 10+ size class difference min/max Fig. 3. Distribution of feeding types in size classes of Hornsund crustaceans. Feeding categories de− scribed for adult specimens: s – deposit and suspension feeders, sf – suspension feeders and filtrators, c – carnivores and carrion feeders. opposite is true of warm water inhabitants (Rass 1986; Tande 1988; Timofeev 2001; Portner and Payle 2008). This can be however severely modified by factors such as oxygen availability (at high oxygen concentrations animals grow larger; Chapelle and Peck 1999), food provision (inhabitants of oligotrophic regions tend to be smaller; Pfankuche and Soltwedel 1998), or individual taxa growth rates (many molluscs live long at very small size increments; Ambrose et al. 2006). The oligotrophic Central Arctic (primary production below 50g C/m2, Platt 1984), is reported to be populated by very small benthic organisms (Kroncke et al. 2000). The productive Svalbard shelf waters (120 gC/m2, Eilertsen et al. 1989) with their well−coupled pelago−benthic system (Wassman et al. 1991) has a direct positive effect on the larger size of the benthos from this area. Steele and Steele (1975) demonstrated the influence of temperature on egg incu− bation time in several Gammarus species. At boreal temperatures (15 °C in summer), the incubation time is shortened to a few months in gammarids, which allows them to complete more than one life cycle in one year (Jażdżewski 1970; Steele and Steele 1975). In cold water (below 4°C in summer), crustacean egg incubation lasts from 7 to 12 months, which makes an annual life cycle virtually impossible (Steele and Steele 1975; Clarke 1979). Mysis oculata from Arctic and boreal waters differs in growth rate (higher in warm water) and size (larger in cold water) (Węsławski 1989). Even small temperature differences can change the life cycle of crustaceans drastically, as was for instance demonstrated in St. Lawrence Estuary for two pop− ulations of the amphipod Arrhis phyllonyx, in which the colder water population lived for over two years and attained a larger size, while that from warmer waters (temperature higher by about 4°) completed the life cycle in one year and at a smaller size (Sainte−Marie and Brunel 1983). Functional−food separation. — Pelagic herbivores in the Arctic feed well for only a short time during the year. This forces them to wait and live another year if
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Percent of species in zoogeographical groups in size classes
35
30
25
20
15
10
5 AB% 0 2to3 A% 4to5 6to7 8to9 B% 10 + size classes Fig. 4. Differences in size classes index (juveniles to adults size difference) within three main zoogeo− graphical groups of examined crustaceans from Hornsund. A – Arctic, AB – Arcto−boreal and B – bo− real species. development is incomplete. Some pelagic herbivores in Arctic waters belong to the largest known in their class. These include the 1 cm long Calanus hyperboreus, which is one of the largest calanoid copepods; Limacina helicina, one of the larg− est pteropods; and 30 to 50 mm long krill species such as Thysanoessa and Meganyctiphanes), all of which represent very large species compared to their rel− atives from boreal waters (Węsławski et al. 2006). It is known that large adult her− bivorous plankton grazers can temporarily become micropredators, such as the Antarctic krill, Euphausia superba (Opalinski et al. 1997). Similar observations were made with the generally herbivorous ice amphipod, Gammarus wilkitzkii, the largest specimens of which became micropredators (Polterman et al. 2000), and with the juvenile hyperids Themisto libellula, which are herbivorous, while adults are typical predators (Noyon et al. 2009). The mean number of specimens in crustacean populations will be high in polar waters and low in temperate waters if the hypothesis proposed in this paper is valid (low diversity is compensated by the higher abundance of a single species). Rela− tion between body size and abundance was discussed e.g. by White et al. (2007). The mean number of individuals per crustacean species found in an area of 1m2 was low in the northern Norwegian fjord (Oug 2001) and distinctly higher in the Svalbard fjords, which confirms the prevalence of the K strategy in the Arctic at a mean number of individuals per crustacean species from between 2 to 5 (Table 3).
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Table 3 Densities of soft bottom crustaceans found in Svalbard material (own data) and N. Norwe− gian Hollandsfjord (Oug 2001) Hollandsfjorden Kongsfjorden Hornsund Adventfjorden min [ind/m2] 3 10 10 11 mean [ind/m2] 10293950 max [ind/m2] 133 110 560 250 SD 21 21 96 61 number of species 22 13 26 15 mean density [ind/species/m2] 0.5 2.2 1.5 3.3
Depth separation. — Habitat separation (mostly depth) within a population can lead to the speciation mechanism, which refers to juveniles possibly being effi− ciently separated from the adult part of the population. A series of sibling species from the genera Onisimus and Anonyx indicates that not only do the juveniles of each species live in shallower waters than adults do, but that smaller species also live in shallower waters than larger ones do (Węsławski 1990, Węsławski and Legeżyńska (2002). Similar phenomenon was observed among developmental stages of Calanus copepods (Skreslet et al. 2000). Separation by mobility. — Pelagic and nectobenthic species, like krill, mysids, and hyperid amphipods, are known to form shoals segregated by size (and, thus, mobility), with juveniles swimming closer to the surface and closer to the shore than adults (Mauchline 1980). In the current study material, this was ob− served (but not documented) in swarms of decapod crustaceans comprising Pan− dalus borealis, Sabinea septemcarinata, and the mysid Mysis oculata. Overall diversity. — Despite all of the new programs and initiatives (MARBEF – Marine Biodiversity an Ecosystem Functioning Network of Excellence, OBIS – Ocean Biogeography Information System, CoML – Census of Marine Life) set up to investigate such issues, the diversity of North Atlantic crustaceans is still diffi− cult to assess because of the unclear delimitation of zoogeographical provinces and uneven sampling effort. Amphipods have been thoroughly studied, and Palerud and Vader (1991) reported 740 species in the North Atlantic and Svalbard, while Sirenko (2001) recorded 349 species in the Barents Sea and 290 for the High Arctic Kara Sea. In conclusion, we feel that the hypothesis presented in this paper cannot yet be rejected. Indeed, Crustacea do demonstrate an ecological compensation for the taxonomic impoverishment in cold waters; the majority of the species recorded are large and perennial cohorts are well distinguished, and ecological differences be− tween the size and the age groups are evident.
Acknowledgements. — This paper is part of the MARBEF EU 7FP and Census of Marine Life Arctic Ocean Diversity projects.
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Received 4 December 2009 Accepted 24 May 2010
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