17 May 2007 | www.nature.com/nature | £10 THE INTERNATIONAL WEEKLY JOURNAL OF SCIENCE 447, 447, 231– 11 4 2007 May 17 www.nature.com/nature ANTARCTICANTARCTIC BIODIVERSITYBIODIVERSITY The Southern Ocean fauna yields its secrets SPINTRONICS Silicon comes good NATUREJOBS RESEARCH FUNDING Focus on immunology The new philanthropy INFECTIOUS DISEASES no.7143 The accidents of evolution Laser Proof Vol 447 | 17 May 2007 | doi:10.1038/nature05827 LETTERS First insights into the biodiversity and biogeography of the Southern Ocean deep sea Angelika Brandt1, Andrew J. Gooday2, Simone N. Branda˜o1, Saskia Brix1, Wiebke Bro¨keland1, Tomas Cedhagen3, Madhumita Choudhury1, Nils Cornelius2, Bruno Danis4, Ilse De Mesel5, Robert J. Diaz6, David C. Gillan7, Brigitte Ebbe8, John A. Howe9, Dorte Janussen10, Stefanie Kaiser1, Katrin Linse11, Marina Malyutina12, Jan Pawlowski13, Michael Raupach14 & Ann Vanreusel5 Shallow marine benthic communities around Antarctica show trench floor, channel levees and adjacent to fracture zones, and from high levels of endemism, gigantism, slow growth, longevity and water depths between 774 and 6,348 m (Fig. 1; Supplementary late maturity, as well as adaptive radiations that have generated Discussion; Supplementary Tables 1, 2; Supplementary Figs 1, 2). considerable biodiversity in some taxa1. The deeper parts of the This material has greatly improved our knowledge of the biodiversity Southern Ocean exhibit some unique environmental features, of benthic communities in the deep Southern Ocean and enabled us including a very deep continental shelf2 and a weakly stratified to test ideas about large-scale biogeographic and other macroeco- water column, and are the source for much of the deep water in logical patterns5 among deep-water faunas. the world ocean. These features suggest that deep-sea faunas The richness of species inhabiting deep-sea sediments was first around the Antarctic may be related both to adjacent shelf com- demonstrated during the 1960s6,7. Since then, scientists have sought munities and to those in other oceans. Unlike shallow-water to understand the mechanisms that maintain these high levels of Antarctic benthic communities, however, little is known about life benthic diversity at local8 and regional9 scales. We analysed species in this vast deep-sea region2,3. Here, we report new data from assemblages in ANDEEP samples across a range of taxonomic recent sampling expeditions in the deep Weddell Sea and adjacent groups, representing the meiofauna, macrofauna and megafauna areas (748–6,348 m water depth) that reveal high levels of new (Fig. 2) and found substantial levels of unrecorded biodiversity biodiversity; for example, 674 isopods species, of which 585 were (see Supplementary Material). The Foraminifera were represented new to science. Bathymetric and biogeographic trends varied by 158 live species, including 72 monothalamous species, most of between taxa. In groups such as the isopods and polychaetes, slope them undescribed. The nematodes belonged to typical cosmopolitan assemblages included species that have invaded from the shelf. In deep-sea genera (Supplementary Fig. 3), but more than half of the 57 other taxa, the shelf and slope assemblages were more distinct. Abyssal faunas tended to have stronger links to other oceans, 80º W 60º W 40º W 20º W 0º 20º E particularly the Atlantic, but mainly in taxa with good dispersal South Africa capabilities, such as the Foraminifera. The isopods, ostracods and Cape Basin nematodes, which are poor dispersers, include many species cur- 40º S • 40º S rently known only from the Southern Ocean. Our findings chal- Agulhas Basin • South America Polar Front lenge suggestions that deep-sea diversity is depressed in the 50º S 50º S Southern Ocean and provide a basis for exploring the evolutionary significance of the varied biogeographic patterns observed in this Scotia Sea ••• remote environment. •• •• 60º S • •• 60º S •• • Although animal communities inhabiting shallow marine benthic Polar Front• • • • • • • • sen • • environments around Antarctica, notably parts of McMurdo Sound ••• • •• • Weddell Abyssal Plain shau ula • s and the Peninsula region, are well known, there have been few studies Sea • in • n of the deep-water faunas in the adjacent Southern Ocean. The 70º S Belling Weddell Sea • 70º S • ANDEEP (Antarctic benthic deep-sea biodiversity: colonization • history and recent community patterns) project was designed to fill arctic Pe Dronning Maud Land nt this knowledge vacuum4. Between 2002 and 2005, we undertook A three expeditions in the deep Weddell Sea and adjacent areas aboard 80º W 60º W 40º W 20º W 0º 20º E the German research vessel Polarstern. Biological collections and data Figure 1 | Station map. Stations from ANDEEP I (2002) red circles, on environmental and seafloor characteristics were obtained from ANDEEP II (2002) yellow circles and ANDEEP III (2005) green circles. The diverse settings, including continental slope, rise, abyssal plain, blue line indicates the Polar Front. 1Zoological Museum Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany. 2National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, UK. 3Department of Marine Ecology, University of A˚arhus, Finlandsgade 14, 8200 A˚rhus N, Denmark. 4Royal Belgian Institute of Natural Sciences, 29 Rue Vautier, 1000 Brussels, Belgium. 5Biology Department, Marine Biology Section, Ghent University, Krijgslaan 281/S8, 9000 Ghent, Belgium. 6Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, Virginia 23062, USA. 7Marine Biology Laboratory, CP160/15, Universite´ Libre de Bruxelles, 50 Avenue Roosevelt, 1050 Brussels, Belgium. 8Forschungsinstitut Senckenberg, DZMB-CeDAMar, c/o Forschungsmuseum Ko¨nig, Adenauerallee 160, 53113 Bonn, Germany. 9Scottish Association for Marine Science, Dunstaffnage Marine Laboratory, Dunbeg, Oban, Argyll PA37 1QA, UK. 10Forschungs und Naturmuseum Senckenberg, Senckenberganlage 25, 60325 Frankfurt am Main, Germany. 11British Antarctic Survey, Natural Environmental Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK. 12Institute of Marine Biology, FEB RAS, Palchevskogo, 17, 690041 Vladivostok, Russia. 13Department of Zoology & Animal Biology, University of Geneva, 30 Quai Ernest Ansermet, CH 1211 Gene`ve 4, Switzerland. 14Ruhr-Universita¨t Bochum, Universita¨tstrasse 150, 44780 Bochum, Germany. 307 © 2007 Nature Publishing Group LETTERS NATURE | Vol 447 | 17 May 2007 species recognized in selected genera were new to science. At least 100 amphipods and decapods but not for polychaetes, asteroids and ostracod species were distinguished, and .70% of them were new. ophiuroids12. The generally higher degree of eurybathy among Among the macrofauna, the isopods were astonishingly diverse with Antarctic invertebrates was attributed to glacial–interglacial cycles 674 species identified among .13,000 specimens examined, com- of shelf ice advance and retreat, which periodically eliminated shelf pared with 371 species reported from the entire Antarctic continental faunas, pushing species into deeper water or causing their extinction. shelf10. Most (86%) of the isopod species were undescribed and are These cycles probably also led to regular pulses of migration in and presently known only from the Southern Ocean. More than 200 out of Antarctica1. Experimental studies of the pressure and temper- polychaete species were recognized, 81 of them previously unknown. ature tolerances of the pelagic larvae of the shallow-water Antarctic Our samples yielded 160 species of shelled gastropods and bivalves echinoid Sterechinus neumayeri suggested that embryonic stages compared with 279 species on the shelf (,1,000 m)11. Around 40% of potentially could penetrate into deep water13. The unusually deep species were confined to abyssal depths. Among the megafauna, 76 shelf around Antarctica could also facilitate faunal exchanges species of sponges were recognized, 17 of them were undescribed and between shelf and deep-sea habitats2. 37 new for the Southern Ocean (Supplementary Table 3). ANDEEP data strongly suggest that a combination of emergence Whether shelf faunas have colonized the deep ocean, or vice versa, and submergence on Antarctic margins has led to an intermingling of is a central issue for understanding faunal patterns in the Southern species originating in shallow- and deep-water habitats (Fig. 3). The Ocean. Prior to ANDEEP, most of the information on bathymetric Bathymetric distribution (m) distributions around Antarctica concerned shelf and upper-slope 0 2,000 4,000 6,000 10 faunas . A comparison of species distributions on continental Stenetriidae shelves and slopes around Europe and Antarctica revealed signifi- cantly wider depth ranges off Antarctica for bivalves, gastropods, Janiridae 0.69 Joeropsididae 0.99 0.95 Acanthaspidiidae Haploniscidae 0.99 Janiridae 0.99 Dendrotionidae 0.78 1.00 a 500 µm Haplomunnidae b 10 mm Janiridae f Mesosignidae 1 mm 0.89 Macrostylidae c 1 mm 0.98 Janirellidae 0.79 0.69 Ischnomesidae Desmosomatidae 10 µm 0.99 d 1 mm e Nannoniscidae 0.84 Munnopsidae Figure 3 | Isopod phylogenetic relationships and multiple colonizations of the deep sea. Bayesian consensus tree based on the complete 18S rRNA gene (excluding hypervariable regions; numbers on nodes represent statistical support) of 53 species of marine Asellota, and bathymetric distribution of the analysed species (broad lines). Family distribution (thin black lines) is based on ANDEEP data and the world list of