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International Authority Symposium, March 2006

Deep- Biodiversity and : Perspectives from the Abyss

Craig R. Smith, Jeff Drazen, Sarah L. Mincks University of Hawai’i, Manoa, 1000 Pope Rd., Honolulu, 96822 USA

Abstract. The abyssal seafloor is a vast, interconnected punctuated by and mid- ridges. A range of factors control community structure and biogeography in the abyss including particulate-organic-carbon flux to the seafloor, depth, flow regime, ocean circulation, seafloor and geologic/evolutionary history. In some basins such as the North Atlantic, regional diversity declines from the slope to the abyss, possibly due to decreasing food availability. Biogeographic patterns and apparent species ranges vary substantially with size . Many abyssal megafauna, including macrourid and elasipod holothurians, have low to moderate local diversity and very broad (including cosmopolitan) distributions, with trophic regime (or food flux from surface ) appearing to control species turnover. The macrofauna, in particular and , exhibits high local diversity, and evidence of species in the abyss. Both taxa have some widely distributed species, but also exhibit substantial turnover at the 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 . The meiofaunal taxa, including foraminiferans, 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 appear to harbor novel abyssal taxa, but the 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, 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 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 probabilities resulting from , 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 ’s solid surface (Gage and Tyle, 1991). The distribution of this habitat is largely the inverse of the seamounts, consisting of a network of punctuated by holes (seamounts) and cracks (mid-ocean ridges and ). Abyssal harbor high local biodiversity, with > 100 species each of macrofaunal , nematodes worms, harpacticoid copepods, and foraminiferan in a typical square meter of (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 characterized by high local diversity, such as tropical rainforests, 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 ; 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), 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 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 from the euphotic zone thousands of meters above. This organic- flux is very low, constituting but a few percent of in overlying waters (Smith and Demopoulos, 2003). As a consequence, the , growth rates, reproduction rates and recolonization rates at the abyssal seafloor are typically very low.

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The of abyssal seafloor habitats is generally poorly sampled and poorly described by taxonomist, with greater than 90% of the worms, copepods, isopods, and nematodes collected in any given sample typically being new to . 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 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 (Hollister and McCave, 1984). Currents in these regions may resuspend and sediments, larvae and adult , dispersing some , 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 provinces, hard substrates may be very common. (4) Because hydrostatic influences enzyme function and other aspects of 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, rise and fall, periods of deep-sea anoxia), have influenced large-scale distribution of patterns of abyssal benthos by controlling the 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 , 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 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 probabilities associated with large-scale habitat disturbances, such as manganese-nodule mining (Glover and

4 Smith, 2003; Smith et al., in press). In many ecosystems, species ranges are related to body size (and its correlate longevity) as well as dispersal abilities. Thus, species in different size classes, and in taxa with differentially constrained life history and/or mobility patterns, may show different scales of dispersal. Thus, we pose the question: “How do biogeographic patterns (or species ranges) vary with size and in the abyssal benthos?” For selected taxa from each size class (megafauna, macrofauna, and meiofauna), we will try to answer the following questions:

1) How many deep-sea species are known (i.e., species living below depths of 200 m)? 2) Are there abyssal endemics (i.e., species restricted, as adults, to depths of 3000 – 6000m)? 3) Are there cosmopolitan abyssal species (i.e., species occurring at abyssal depths in most ocean basins?) 4) What proportion of abyssal species are restricted to single basins? 5) Are there local endemics (i.e., species restricted to a single abyssal of an ocean basin)?

Megafauna. Within the megafauna ( > 2 cm in smallest dimension), we examine two taxa. The first are the macrourids, or rattail , most of which are characterized as adults by a benthopelagic (i.e., near-bottom ) lifestyle and planktotrophic larval development. This is a highly successful deep-sea family with over 300 species living below depths of 200 m; however, only 9 known species of rattails live below 3000 m (Marshall and Iwamoto 1973; Jones et al. 2003; Cohen et al. 1990). There is one abyssal endemic species, Coryhaenoids yaquinae, which under the oligotrophic North Pacific gyre, where it apparently out-competes all other rattails under very low food conditions (Wilson and Waples, 1983, 1984). There are two cosmopolitan species occurring in all : C. armatus, at depths of 2000-4700 m, and C. leptolepis at depths of 1900- 3700 m. Four species are restricted to single ocean basins (C. brevibarbis in the North Atlantic, C. yaquinae in the North Pacfic, C. profundus in the NE Atlantic, and C. filicauda in the Southern Ocean (Merrett, 1987, 1992; Iwamoto and Sazonov 1988; Cohen et al., 1990). Only one species with a restricted distribution appears to be rare, suggesting that inadequate sampling is not, in most cases, causing ranges to appear artificially small. In conclusion, the rattails, a major component of the deep-sea fish fauna, exhibit very broad distribution patterns, with flux and larval dispersal likely being very important factors controlling their biogeography.

Among the deep-sea megafauna, the elasipod holothurians are an abundant and diverse group apparently restricted to deep-sea habitats. and photographic survey data for elasipods have been collected extensively at the abyssal seafloor, and the group appears to be quite well described by taxonomists; thus, the biogeographic patterns of elasipods appear to be reasonably well known (Hansen, 1975; Billet, 1991; Bluhm and Gebruk, 1999). There are >100 species of deep-sea elasipods, with ~40 species restricted to abyssal depths, suggesting that the abyss has been a zone of for this group, rather than simply a sink habitat (Hansen, 1975). Six

5 (or ~15%) of the abyssal elasipod holothurians are cosmopolitan, while 18 species (~50%) are restricted to single basins. Four of these restricted species are rare, and thus their apparently restricted ranges may reflect sampling artifacts. Three species of elasipods are regionally endemic, and have only been collected under upwelling zones; one beneath upwelling off northwest , and two beneath upwelling in the eastern equatorial Pacific (Hansen, 1975). In conclusion, the deep-sea elasipods contain a well developed abyssal fauna, with many widely distributed species. Regional endemism appears to be related to high organic carbon flux to the abyssal seafloor. The generally broad distribution of elasipods is likely related in part to dispersal in the by pelagic lecithotrophic larvae (Hansen, 1975), as well as swimming and “” in currents by some species (Gebruk, 1995).

Macrofauna. The macrofauna are animals less than 2 cm in smallest dimension but retained on a 300-500 µm sieve. This is an abundant and speciose size group in abyssal habitats, and macrofaunal taxa exhibit a range of life histories and dispersal abilities. We consider the biogeography of the isopods (commonly known as “pill bugs”) because this group of crustaceans is abundant, diverse, and relatively well sampled (by macrofaunal standards) in some abyssal habitats. Isopods are peracarids (“pouch ”) and brood their young; thus, many have limited dispersal abilities and are expected to have smaller species ranges than rattail fish and elasipod holothurians. More than 500 species of isopods have been collected from the (Wolff, 1962: Wilson, 1987; Brandt, 2005), but their total deep-sea species richness could easily exceed 10,000 (Poore and Wilson, 1993). Hundreds of species of isopods have been collected from abyssal depths, and there is strong evidence that abyssal habitats have supported adaptive radiation in this taxon (Hessler et al., 1979; Wilson, 1987; Brandt et al., 2005). Cosmopolitan species of abyssal isopods do occur, but they appear to constitute only a few percent of the many species found at any single abyssal station (e.g., Brandt et al., 2005). Species turnover in isopods may be high between abyssal sites separated by 100- 3000 kilometers. For example, among a total of 134 isopod species (almost all new to science), Wilson (1987) found only 20 percent overlap (i.e., 80% apparent endemism) in the species lists of two sites separated by 3000 km in the Clarion-Clipperton Zone (CCZ) of the abyssal . However, for most species, only a single individual was collected, and Wilson (1987) estimated that many more isopods species (25-50) remained unsampled at each site; thus, the apparent species turnover between sites, or estimated levels endemism, may be artificially inflated by sampling artifacts. Similarly, Brandt et al. (2005) sampled 6 stations at intervals of 100 – 300 km in the abyssal , and identified ~100 species of isopods, almost all new to science. They found apparent endemism levels between stations of ~50%; i.e., half of the species collected at any one station were collected nowhere else. Once again, most species were rare, making it difficult to resolve restricted species ranges from sampling artifacts. We conclude for the macrofaunal isopods that abyssal species richness is very high and provides evidence of adaptive radiation (or the of new species complexes) in abyssal habitats. Species ranges of 100 – 3000 km could be common, but we are far from certain due to sampling artifacts. Clearly, the abyssal isopods are poorly sampled and contain an enormous diversity of undescribed species.

6 Another macrofaunal taxon, the polychaete worms, has high species diversity in the deep sea and also has a very broad range of life histories and dispersal strategies. More than 200 species of polychaetes have been collected form single abyssal regions (e.g., Glover et al., 2001, 2002), but because (>90%) of species collected in the abyss remain undescribed by taxonomist, the global species rich of deep-sea polychaetes can only be guessed (guesses range to more than 100,000 species; Grassle and Maciolek, 1992). Abyssal endemic polychaetes are extremely likely, but polychaete taxonomy is too poorly known to even speculate on how many total abyssal endemics exist. Some abyssal polychaetes could be cosmopolitan; for example, morphological studies (i.e., studies of worm shape) suggest that one polychaete species (Aurospio dibranchiata) may occur in the abyssal Atlantic, Pacific and Southern Oceans (Glover, Paterson, and Smith, unpublished data). However, molecular studies have shown that “cosmopolitan” morphospecies of polychaetes often are complexes of species with much smaller ranges, so that cosmopolitan species may be rare in the abyss (and elsewhere). Species turnover of polychaetes in the abyss also could be high; for example, Glover et al. (2002) found only 20 – 50% overlap in polychaete species lists between abyssal Pacific stations separated by 200-1200 km (Figs. 4 and 5). Once again, because many species where represented by one or a few individuals in the collection from each site, site endemism is very likely to be overestimated. Modeling studies are required to gauge the potential magnitude of this “pseudo-endemism.” One indication that the turnover of polychaete species may indeed be high in the abyss is that whole families of predatory polychaetes essentially disappear as one move westward 1200 km in the CCZ (i.e., in the abyssal equatorial Pacific)(Glover, Smith, and Menot, unpublished data from the Kaplan Project). This apparent loss of major groups of polychaetes may result from a westward decline in sinking organic carbon flux, and food availability, across the CCZ (Glover et al., 2002).

Figure 4. Station locations in the CCZ (Lettered in black). The 0 – 9oN stations were sampled during the EqPac project and have one set of polychaete working species, while the Domes A, PRA and Echo 1 stations were sampled during a different project and have a separate set of polychaete working species.

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Figure 5. Distribution patterns of polychaetes from central equatorial Pacific abyssal plains at stations separated by 200 – 1200 km: (a) relative proportion of polychaete species that are unique to a site, present in at least two sites, or ubiquitous across all sites, (b) proportion of individuals that belong to species that are unique to a site, present in at least two sites, or ubiquitous across all sites (Modified from Glover et al., 2002).

Another macrofaunal group, snails in the neogastropod taxon, appear to show broader distribution patterns in the abyss than do isopods and polychaetes. Rex et al. (2005) suggest that, in the North Atlantic Ocean, there very few neogastropods restricted to the abyss, and that most abyssal neogastropod may be “sink” populations (i.e., populations of individuals living in such marginal conditions that they cannot reproduce). In this view, the shallower living (or slope) species of neogastropods produce planktotrophic larvae that can be carried long distances and settle out in poor habitats at the abyssal seafloor, where they survive for some but fail to reproduce. If this is correct, they may be very few abyssal endemic species of neogastropods (and possibly other mollusks). However, this “abyssal sink” hypothesis needs further testing, especially in the Pacific, where abyssal habitats are much larger, and typically much more distant from continental slopes, than in the North Atlantic (Fig. 1).

8 Meiofauna. The meiofauna are smaller than the macrofauna, and include animals that pass through a 300-500 µm sieve, but are retained on a sieve size of 42-62 µm. Prodominant meiofauna taxa include the nematode worms, harpacticoid copepods, and protozoan .

The taxonomy and distribution of the foraminiferans may the best known for any meiofaunal taxon. The foraminiferans appear to contain at least 1000 deep-sea species, and often exhibit very high local diversity with more 250 species at a single site (Nozawa et al., submitted; A. Gooday, pers. comm.). A significant number of abyssal morphospecies occur in both the Atlantic and Pacific abyss, but others may occur in single basins (Nozawa et al., submitted). However, the extreme rarity of many apparently local endemics raises the potential of artificially high estimates of endemism. Genetic studies suggest that some foraminiferans my range over depths of 5000 m (Gooday et al., 2004a; Gooday, pers. comm.), so some foraminiferans are likely to be very broadly distributed (Gooday et al., 2004a & b). Once again, better sampling and more genetic studies of widespread morphospecies are needed.

The deep-sea nematodes and harpacticoid copepods also have very high local diversity in the deep sea, typically with >100 species at a single site (e.g., Lambshead et al., 2001; P Martinez, unpublished data). The taxonomy of abyssal forms of these groups is far too poorly known to draw any conclusions about species ranges or biogeography. However, there is evidence that there may be abyssal endemics and abyssal species radiation in the nematodes. DNA sequence studies of abyssal nematodes from the CCZ using the 18s rRNA gene have revealed 70 new species in genera that thus far have been collected only in the abyss (Lambshead et al., in prep.).

In summary, biogeographic patterns and species ranges in the abyss show substantial variability with body size, life history, and taxonomic identity. For some groups, e.g., the elasipod holothurians, isopods , and nematode worms, the abyss has supported species . Thus, evolutionarily novel animals with restricted species ranges may well occur in these taxa. For other taxa, e.g., the neogastropods, the abyss may be so food limited that it has been a marginal habitat over evolutionary time scales. Thus, any biogeographic synthesis must consider a range of taxa with diverse body sizes, life histories, and evolutionary histories.

Obstacles to Abyssal Biogeographic Synthesis

There a number of major obstacle preventing a more complete understanding of biogeographic patterns in the abyss (as well as on seamounts). (1) Far greater than 90% abyssal species richness falls within species that have not been described by taxonomists. Thus, any large scale study of biodiversity must use “working species,” i.e., species differentiated by project taxonomists but not formally described in the scientific . Because every project has its own set of working species (and reference collection)(e.g., Fig 4), substantial effort and resources should be devoted in the near future to intercalibrating working species among national and international programs to allow better understanding of species ranges and biogeography.

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(2) Most abyssal sites are grossly undersampled, making it very difficult to resolve simple species rarity from endemism. Modeling studies designed to illustrate the scale of this problem, and the sample effort needed to avoid “pseudo-endemism,” are urgently needed.

(3) It is very likely that the cryptic species (i.e., species that are morphologically similar but genetically distinct) are common in abyssal habitats, leading to underestimates of species richness and overestimates of species ranges (e.g., Etter et al., 1999). Studies combining morphological and molecular taxonomy are required in a broad variety of taxa to address this problem.

(4) Patterns of population connectivity in deep-sea animal populations are very poorly known, making identification of source and sink populations, and testing of the “abyssal sink” hypothesis (Rex et al., 2005), exceeding difficult at present.

Similarities Between Abyssal and Seamount Biogeography

While the abyssal seafloor differs in many characteristics from seamounts, there are some surprising similarities between the abyssal and seamount habitats in patterns of diversity and apparent endemism. Both habitats exhibit (1) high species richness (many hundreds of macrofaunal and megafaunal species) on the scales of a few hectares, (2) a long list of rare species, and (3) a fauna largely undescribed by taxonomists. Species accumulation curves suggest that many (if not most) species in single areas remain uncollected. Both habitats exhibit substantial turnover (20-50%) in species lists between study units (single seamounts or abyssal seafloor areas of 1-100 km2). This turnover may reflect actual endemism (i.e., restricted species ranges) or sampling artifacts (i.e., species lists are so incomplete that sites appear artificially different). Because species ranges and levels of endemism are extremely important to prediction of species extinction probabilities resulting from mining, modeling studies to assess sampling artifacts in the estimation of endemism and species ranges are urgently needed.

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