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Deep-Sea Biodiversity and Biogeography: Insights from the Abyss

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Deep-Sea Biodiversity and Biogeography: Insights from the Abyss International Seabed Authority Seamount Biodiversity Symposium, March 2006 Deep-sea Biodiversity and Biogeography: Perspectives from the Abyss Craig R. Smith, Jeff Drazen, Sarah L. Mincks University of Hawai’i, Manoa, 1000 Pope Rd., Honolulu, Hawaii 96822 USA Abstract. The abyssal seafloor is a vast, interconnected habitat punctuated by seamounts and mid-ocean ridges. A range of factors control community structure and biogeography in the abyss including particulate-organic-carbon flux to the seafloor, water depth, flow regime, ocean circulation, seafloor topography and geologic/evolutionary history. In some basins such as the North Atlantic, regional species diversity declines from the slope to the abyss, possibly due to decreasing food availability. Biogeographic patterns and apparent species ranges vary substantially with size class. Many abyssal megafauna, including macrourid fish and elasipod holothurians, have low to moderate local diversity and very broad (including cosmopolitan) distributions, with trophic regime (or food flux from surface waters) appearing to control species turnover. The macrofauna, in particular polychaetes and crustaceans, exhibits high local diversity, and evidence of species radiation in the abyss. Both taxa have some widely distributed species, but also exhibit substantial turnover at the family and species level over distances of 100-1200 km. However, much of this turnover could be “pseudo-endemism” resulting from undersampling. For some macrofaunal taxa, e.g., the neogastropods, it is argued that the Atlantic abyss contains a non-reproductive “sink” assemblage derived from slope regions. The meiofaunal taxa, including foraminiferans, nematode worms and harpacticoid copepods, are speciose in the abyss. The foraminiferans may have high local diversity but low global diversity, with some species exhibiting bathymetric ranges exceeding 5000 m. The nematodes appear to harbor novel abyssal taxa, but the taxonomy and distribution of this group are too poorly known to draw any biogeographic conclusions. In summary, biogeographic patterns and species ranges in the abyss show substantial variability with body size, life history, and taxonomic identity. Thus, any synthesis of abyssal biogeography, and its application to environmental management, must consider a range of taxa with diverse body sizes and life histories. There are similarities between the abyssal and seamount habitats in patterns of diversity and apparent endemism. Both habitats exhibit (1) high species richness, (2) a long list of rare species, (3) and many species undescribed by taxonomists. Species accumulation curves suggest that many species in any single area remain uncollected. Both habitats exhibit substantial turnover in species lists over small scales (100’s of kilometers). This turnover may reflect actual endemism or sampling artifacts. Because species ranges and levels of endemism are important to prediction of extinction probabilities resulting from mining, modeling studies to assess sampling artifacts in the estimation of endemism are urgently needed. Nature of the abyssal habitat The abyssal seafloor at depths of 3000-6000 m is a vast habitat (Fig. 1), covering approximately 54% of the Earth’s solid surface (Gage and Tyle, 1991). The distribution of this habitat is largely the inverse of the seamounts, consisting of a network of plains punctuated by holes (seamounts) and cracks (mid-ocean ridges and trenches). Abyssal sediments harbor high local biodiversity, with > 100 species each of macrofaunal invertebrates, nematodes worms, harpacticoid copepods, and foraminiferan protozoa in a typical square meter of sediment (Lambshead et al., 2002; Glover et al. 2001; Smith and Demopoulos, 2003; Nozawa et al., submitted; Martinez, personal communication). Enigmatically, the structural complexity of abyssal habitats is very low, especially when 1 compared to other ecosystems characterized by high local diversity, such as tropical rainforests, coral reefs, and some seamounts. Figure 1. Bathymetric map of the ocean floor. The abyss seafloor between 3000 and 6000 m (all the blue except for narrow ocean trenches around ocean margins) covers approximately 54% of the Earth’s surface. Several generalizations can be made about the ecological characteristics of the abyssal habitat, although there clearly are exceptions to all of these generalizations. The habitat consists mostly of plains of fine sediment, and is characterized by low, relatively constant water temperatures between -1 and ~ 2 o C. Most of the abyssal seafloor appears to experience low currents and shows little evidence of sediment erosion; however, some areas (e.g., the seafloor beneath western boundary currents and in the Drake Passage), may experience currents of erosive magnitudes (Hollister and McCave, 1984). Much of the habitat structure of abyss sediments is biogenic, consisting of the tests of giant protozoans (xenophyophores), animal burrows and mounds, feeding traces, and the tracks and trails of mobile megabenthos (Gage and Tyler, 1991; Smith and Demopoulos, 2003. Where hard substrates such as manganese nodules and rock outcrops occur, they appear to support faunal communities distinct from nearby abyssal soft sediments (see reviews in Smith and Demopoulos, 2003; Hannides and Smith, 2004). Abyssal seafloor habitats are often considered to be “food limited” because biotic production depends on the sinking flux of particles from the euphotic zone thousands of meters above. This organic-matter flux is very low, constituting but a few percent of primary production in overlying waters (Smith and Demopoulos, 2003). As a consequence, the biomass, growth rates, reproduction rates and recolonization rates at the abyssal seafloor are typically very low. 2 The fauna of abyssal seafloor habitats is generally poorly sampled and poorly described by taxonomist, with greater than 90% of the polychaete worms, copepods, isopods, and nematodes collected in any given sample typically being new to science. For example, a search of the Ocean Biogeographic Data System reveals less than 20 records at the genus or species level in central equatorial Pacific (Fig. 2). Figure 2. Map of genus and species level records from depths of 3000 – 6000 m in the Ocean Biogeographic Information System (OBIS). What controls biogeographic patterns in the abyss? A number of factors are likely to influence patterns of biogeography and biodiversity at the abyssal seafloor (Hansen, 1975; Rex et al., 2005). (1) Because abyssal habitats are generally very food poor, a major factor is the magnitude of particulate annual organic flux to seafloor, which varies as a function of primary production in the surface ocean. Abyssal habitats underlying upwelling zones along the equator may thus harbor different communities than sediments underlying the oligotrophic central gyres. (2) While the abyssal seafloor generally has low current velocities, current regimes may be much more energetic beneath western boundary currents and beneath the Southern Ocean (Hollister and McCave, 1984). Currents in these regions may resuspend and transport sediments, larvae and adult benthos, dispersing some organisms, and producing inhospitable habitat conditions for others. (3) The availability of hard substrates may also control distribution patterns of benthos, especially because in some regions (e.g., the abyssal equatorial Pacific), hard substrates may be very rare, while in other such as manganese nodule provinces, hard substrates may be very common. (4) Because hydrostatic pressure influences enzyme function and other aspects of organism physiology (Somero, 1992), pressure effects on physiology may well play a role in 3 setting the upper and lower depth limits of abyssal endemics (Somero, 1992). (5) Ocean circulation patterns and seafloor topography also clearly influence biogeographic patterns, isolating some regions of the abyssal seafloor from other regions. (6) Finally, historical events, both geological and oceanographic (e.g., the opening of ocean basins, sea level rise and fall, periods of deep-sea anoxia), have influenced large-scale distribution of patterns of abyssal benthos by controlling the nature and timing of faunal dispersal (e.g., Wilson and Hessler, 1987; Levin et al., 2001; Stuart et el., 2003). Patterns and scales of biogeographic variability in the abyss Large-scale pattern of biodiversity are poorly studied in the abyss, but a few patterns have been documented. In the North Atlantic Ocean, regional species diversity for a variety of taxa in the macrofaunal and megafaunal size classes (0.300 – 20 mm, and > 2 cm in minimum linear dimension, respectively) declines from depths of 3000 to 5000 m (Fig. 3), yielding a diversity maximum in the abyssal zone at its upper limit (3000 m)(Stuart el., 2003). It is not clear whether a similar pattern holds on other ocean basins, and the causes of this pattern remain highly controversial (e.g., Rex et al., 2005). Decreased food availability at abyssal depths is commonly invoked as the ultimate cause of the decrease in diversity in the abyssal North Atlantic (Rex, 2005). Figure 3. Variations in species richness with depth in the Northwest Atlantic. Species richness is estimated for samples of 50 individuals using rarefaction (modified from Rex, 1983). How do the distribution patterns of individual species vary in the abyss; in particular, over what spatial scales do species typically range at the abyssal seafloor? This question is extremely relevant to prediction of extinction
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