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The ichthyofauna of ocean margin regions is characterised by a succession of different species occurring at different depths. This study was aimed at determining whether the resultant pattern of species richness with depth is a consequence of local factors in a given region or whether it simply reflects the global pattern of fish species distribution in the oceans. Along the ocean margin of the temperate NE Atlantic Ocean in the Porcupine Seabight and Abyssal Plain region, 48°–53°N, a total of 108 demersal fish species were identified from 187 trawls at depths from 240 to 4865 m. Fitting of species accumulation curves predicted an asymptote of 120, indicating that the fauna is 90% described. Baited cameras detected 22 scavenging species with a predicted asymptote of 24 species. Scavenging species represented a constant 22.7% (SD 3.5%) of the total species richness throughout the depth range studied. Species richness per trawl varied between a maximum of 16 at 1600 m and 4 on the abyssal plain > 4000 m with no significant influence of sea floor slope (a measure of topographic heterogeneity). Total species richness was 48 at 1600 m and 10 on the abyssal plain. There is a clear transition between slope species above 3000 m and abyssal species below. The depth at which peak species richness occurs (1100–2000 m) coincides with the depth of the permanent thermocline, presence of Mediterranean overflow water (MOW), seasonally strong currents, resuspension of particulate matter, high biomass of benthic filter feeders and pelagic biomass impinging on the slope. We suggest that these factors increase habitat and resource heterogeneity, thus supporting a wider range of fish species. The local pattern of species richness was compared with the global distribution of maximum depths of marine fish species from FishBase. Globally all three Classes of fishes, Agnatha, Chondrichthyes and Osteichthyes, showed a logarithmic decrease in species with depth, with the deepest observed species in each class occurring at 3003 m, 4156 m and 8370 m, respectively. In contrast, the local distribution of species maximum depths is idiosyncratic with a mean of 16.6 species maxima per 500 m at 1000–3000 m depth followed by three species per 500 m at 3500–4000 m and 11 species per 500 m at 5000 m. It is concluded that global patterns of species richness, as a source of recruitment, exert a weak influence on local patterns of species richness. Rather, global species richness is the sum of numerous regional and local patterns, each determined by characteristic environmental conditions.
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The fish fauna living in a given region is a subset of the global fauna. Thus, before effects of local heterogeneity on biodiversity can be understood it is useful to consider the global trends in distribution of three main classes of fishes which may be independent of local conditions. Globally, the Agnatha (Myxiniformes) Chondrichthyes and Osteichthyes all show a maximum in species number at the shallowest depths (Fig. 2). Variation in size is also greatest at shallower depths but this trend is less pronounced in the Agnatha. These global trends can be the result of at least four possible factors: (i) global patterns of environmental heterogeneity, (ii) decrease in food supply with depth, (iii) evolutionary history of colonisation of the deep sea by fishes, (iv) the deepest parts of the ocean remain insufficiently studied to reveal the high diversity residing there. Mora et al. (2008) show that the bathydemersal species inventory is the least well known of all fish faunas; however, the estimated number of species remaining to be discovered in this zone is insufficient to invalidate the trends observed in Fig. 2. We therefore assume that the existing species inventory accurately reflects global patterns.
High species number and size variation at shallow depths are probably strongly influenced by the heterogeneity of shelf, coastal and estuarine habitats with scope for endemism around islands, reefs, bays and along stretches of coastline. There is also evidence of high diversity around seamounts reflecting topographic and hydrographic heterogeneity (Fock et al. 2002). Generally, in deeper environments there is greater geographic interconnectedness between habitats and the abyssal plains harbour cosmopolitan demersal species that occur throughout all the world’s oceans (e.g. the macrourid Coryphaenoides armatus, King & Priede 2008). At the deepest extremities of the ocean, in the hadal zone at over 6000 m depth, the contiguous abyss subdivides into 22 separate trenches or basins (Angel 1982) isolated to varying degrees from one another, in which 47–56% of species, mostly invertebrates, are endemic to trench systems (Vinogradova 1997). The presence of endemic hadal fishes (Jamieson et al. 2009) with different species in different trenches probably explains the apparent increase in species number at maximum depth in Fig. 2, which deviates from the general regression line. This is similar to the general decrease in terrestrial species richness with increasing altitude on individual mountains but with endemism at summits, resulting in high global species richness at high altitudes (Väre et al. 2003). It is important to note that global and regional species richness trends can therefore be divergent. There is a clear decrease in species richness at extreme depths or altitudes within a locality, but globally, there is an increase in richness at the extremes resulting from summing of all the locally endemic species.
A major driver of both biomass and biodiversity trends in the deep sea may be the attenuation of the food supply from the surface. Most measurements of biomass in relation to depth, either pelagic (Angel & Baker 1982) or benthic (Lampitt et al. 1986), show a logarithmic decrease; approximately 10-fold per 2000 m. It is therefore not surprising that species richness declines with depth as less and less biomass can be supported, particularly as mean body size does not decrease with depth. Rex (1973) shows that biodiversity of gastropods is low in the abyss and attributes this to extremely low productivity in this region but points out that biodiversity can be sustained in such environments by the adoption of small body size. Indeed Rosenzweig (1995) shows that the relationship of diversity versus productivity along a gradient is often unimodal with maximum species richness at intermediate productivity levels.
Within fish species, bigger-deeper trends are often observed (Merrett et al. 1991b), suggesting that dwarfism in the deep sea is not applicable to fishes. The Chondrichthyes are remarkable for their relatively rapid decrease in species richness with depth, resulting in the absence of sharks in the abyss. Priede et al. (2006) argued that one factor may the relatively high energy requirement for Chondrichthyes in maintaining neutral buoyancy by sequestering large volumes of oil compared with the low cost of air bladder buoyancy in the Actinopterygii. However, here we show that the Agnatha, which do not have swim-bladders, have a similar rate of decrease with depth as the Actinopterygii. In addition to the depth trends, regional differences in surface productivity can result in differences in food supply to the deep sea floor and regionally distinct ichthyofaunal assemblages (Merrett 1987, 1992).
The possibility of a relationship between body size and biodiversity has been widely discussed (McClain & Boyer 2009) so it is interesting to note that in all three classes of fishes, there is no trend in body size with depth; mean body length is constant. However, McClain & Boyer (2009) show that generally for metazoa, species richness is highly correlated with body size variation and they argue that greater body size range may allow for greater niche differentiation. This agrees with the observation here that the highest species richness occurs at the shallowest depths where the greatest size variation is present.
As well as the present-day environment, the patterns observed in Figs 2 and 3 are probably also influenced by the history of colonisation of the deep sea that has occurred during the last 70 million years and since establishment of the modern thermohaline circulation that transports oxygen-rich water to the deep sea. Andriashev (1953) proposed two phases of colonisation, an ancient group including the macrourids, and a more recent secondary deep-water group, such as perciformes largely derived from shore-living taxa. However, Howes (1991) argues that in the gadoids (Superorder Paracanthopterygii, Nelson 2006), including ophidioids, lophiformes and macrourids there has been repeated divergence from ancestral forms into abyssal- and shelf-dwelling forms as the modern ocean basin evolved.
According to the species accumulation curves, 90% of the ichthyofauna of the study area has been detectable by trawls and baited cameras (Fig. 4). Mora et al. (2008) show that globally, bathydemersal species inventories are 56% complete and demersal species 81% complete so the Porcupine Seabight area is relatively well sampled. The small trawl that was used is not very effective at catching larger mobile species so that the shark Centroscyllium fabricii which was detected by the baited camera was only caught by a much larger bottom trawl towed at 4 knots (Merrett et al. 1991a). Full characterisation of a fauna is best carried out using a variety of fishing gear, with different species selectivity characteristics. Merrett et al. (1991a) compared results for three different kinds of trawl. We chose the OTSB to obtain unbiased estimates of biodiversity at different depths because it is the only gear capable of being deployed at all depths. In a long-term study such as this it is possible that the ichthyofauna may change over time and, indeed, Bailey et al. (2009) have detected changes in relative abundance of different species during the time course of this sampling programme. However, our statistical analysis showed that there was no change in species composition between sampling periods, so the present analysis is not affected by this observation.
The baited camera selects those species that use olfactory foraging and are attracted to the odour of baits. Coryphaenoides rupestris, for example, has large eyes and a brain with a well-developed optic tectum but only a very small olfactory region (Priede et al. 1999) and is therefore never captured in baited camera images or baited fishing gear such as long lines or traps. However, Coryphaenoides armatus, with large olfactory and reduced optic regions of the brain, is a well-known ubiquitous scavenger at baits (King & Priede 2008). Species appearing at baits can be regarded as scavengers, but they may not be obligate scavengers as some species are often observed to feed on other animals such as amphipods attracted to bait rather than on the bait itself. Collins et al. (2005) showed that the scavenging species (identified as those that attend baited cameras) in the Porcupine Seabight have a significant bigger-deeper trend in body size. They explained this by showing the advantages of large body size for survival during the intervals between rare feeding opportunities at greater depths. This resulted in a slight, but not significant, increase in biomass (kg·km−2) of the scavenging species with depth, despite a decrease in abundance with depth. This contrasted with non-scavengers, which showed no significant trend in body size with depth. The observation that scavengers constitute an almost constant proportion (c. 20%) of the total number of species throughout the depth range (Fig. 7B) is very interesting and suggests that this may represent an optimal size for this functional component of the fish assemblage. There is the possibility, however, that cryptic rare scavenging species were not recognised in the photographs, e.g. the three Ilyophis species of synaphobranchid eels were not detected at baits, but small numbers (< 30 total in all samples) were logged in trawls. We cannot exclude the possibility that species richness at the landers was underestimated by inability to discriminate these rarities in images.
Examining the Porcupine Seabight maximum depths data in Fig. 2, it is evident that the regional data do not follow the global pattern. The Porcupine Seabight data show a more or less constant number of species per depth stratum until 3000 m, where there is a discontinuity between continental slope fauna above and abyssal fauna below. In contrast to the more localised species on the slopes, the abyssal plain species are relatively cosmopolitan, resulting in convergence towards the global fitted line at maximum depth. Koslow (1993) points out that shallower-living (upper and mid-slope) species tend to be restricted to only one side of the Atlantic, whereas many deeper-living species occur on both sides of the ocean. Contrary to the general trend of decrease in species number with depth in the global data set, in the Porcupine area (grey line in Fig. 2) there is an increase in numbers towards 5000 m. Six of the 11 deepest fishes recorded there in the 4500–5000 m depth bin have global maximum depths of occurrence exceeding 5000 m (Froese & Pauly, 2008) but in the Porcupine Abyssal plain they are restricted to the maximum sea floor depth of less than 5000 m resulting in a regional cluster of species at that depth. To a limited extent, global patterns may drive local species richness trends, e.g. Agnatha and Chondrichthyes are absent from the deeper stations because globally, members of these class are unable to survive at abyssal depths. However, we conclude that there is little evidence that the patterns of local species richness with depth in demersal species is a reflection of the global trend, i.e. local niches automatically filled by recruitment from a global pool of characteristic species at each depth stratum. Rather the converse is true; the global trend is the sum of numerous idiosyncratic local faunas that cumulatively generate the distributions seen in Figs 2 and 3.
Local phenomena therefore must determine patterns of species richness. In this paper we use slope as a proxy for topographical heterogeneity; however, the slopes recorded at the trawl stations (Fig. 5) are not fully representative of the range of topography occurring in the study area, as trawling must avoid the most precipitous slopes and rough terrain. Within the range sampled, it is clear that slope does not influence species richness in the trawls.
The most striking result in Fig. 6 is the elevated species richness between 800 and 2500 m with a significant peak at 1500–1600 m. This is reflected in the cumulative presentation in Fig. 7B. Such a pattern could be the result of the mid-domain effect (MDE) where a peak in species richness is observed resulting from random assembly of species within a defined bathymetric zone (Colwell & Lees 2000). Kendall & Haedrich (2006) tested this hypothesis for different regions of the North Atlantic Ocean and found that observed patterns did not match the random assembly null model. The diversity maximum is probably a result of a combination of physical factors and patterns of distribution of pelagic and benthic prey. There are a number of physical factors acting at this depth. For example, 1400 m is the base of the permanent thermocline (Rice et al. 1991) where the temperature reaches 4 °C and below which the temperature remains relatively stable. Flach et al. (1998) found peak current velocities at this depth, reaching 35 cm·s−1 in autumn to winter and resulting in resuspension of particulate matter and creating conditions in which filter feeders occurred in high abundance and biomass. Depths between 800 and 1600 m in the Seabight are dominated by Mediterranean Overflow Water (MOW) with Labrador Sea Water at 1600–1800 m and North Atlantic Deep Water (NADW) below (Howell et al. 2002).
We hypothesise that, in this depth zone, species find distinct niches in different water masses, temperatures and current regimes, resulting in greater species richness than would otherwise occur in a section of continental margin with uniform oceanographic conditions. Furthermore, the presence of sessile filter feeders indicates the possibility for survival of filter-feeding fishes in these localities. The sessile filter feeders themselves may form reefs, creating habitats for specialised fishes (Ross & Quattrini 2007) and further enhancing biodiversity.
The base of the photic zone and interaction with mesopelagic fauna impinging on the slope adds a further dimension of environmental heterogeneity at mid-slope depths. The macrourid Coryphaenoides rupestris is a commercially exploited fish that is most abundant between 800 and 1800 m depth with a peak at 1500 m, so it might be regarded as an archetypal mid-slope species occurring at the zone of peak diversity. It is a visual feeder probably predating in the twilight zone of the mesopelagic as well as exploiting benthic fauna. Mauchline & Gordon (1991) show that benthopelagic fish including C. rupestris feed on epipelagic and mesopelagic fauna that impinge on the continental slope during the day-time at the maximum depth of their diel vertical migratory pattern. They point out that in the Rockall Trough, a region north of the Porcupine Seabight area, maximum demersal fish abundance coincides with the depth of greatest impingement of pelagic fauna on the slope at 1200–1300 m depth. In the Porcupine Seabight area, Gillibrand et al. (2007) discovered a seasonal maximum of pelagic bioluminescence at 1200–1800 m within the MOW layer, indicative of high pelagic biomass at these depths. In addition to pelagic prey, demersal fishes also forage on benthic fauna. Howell et al. (2002) linked the distribution of asteroids to physical oceanography of the Porcupine Seabight and found a peak of diversity at 1800 m, but, in contrast to the demersal fishes, there was an increase in biodiversity again below 4000 m. For bivalves, Olabarria (2005) found a peak of diversity at 1600 m followed by a decrease to 2700 m and maximum diversity at 4100 m.
Peak diversity of fishes at c. 1600 m coincides with a peak in biomass and diversity of several taxa of benthic invertebrates and is probably reinforced by enhanced access to pelagic prey at this depth. However, the analysis of fish biodiversity in relation to heterogeneity is weakened by the coarse scale of trawl sampling, with a mean haul area of 60,000 m−2 and 2–10 km of linear extent. Using such means it is not possible to address the small-scale dynamics discussed by Levin et al. (2001). Ross & Quattrini (2007) surveyed fish fauna associated with coral banks of the NW Atlantic down to 783 m using the Johnson-Sea-link manned submersible and argued that using conventional otter trawls it is possible to define neither fish communities nor habitat relationships. A full understanding of habitat heterogeneity effects on demersal fishes of the NE Atlantic must await the application of new methods capable of high-resolution mapping of habitat utilisation. Uiblein et al. (2002) and Lorance et al. (2002) have observed Synaphobranchus kaupii and Hoplostethus atlanticus on the slopes of the Bay of Biscay by manned submersible and were able to show how their behaviour and abundance were associated with particular habitat features. Unfortunately, surveying sufficient area while retaining fine-scale spatial resolution is challenging and submersibles may also affect the behaviour of the focal animals. As a result, much remains uncertain about both the diversity patterns of deep-water fishes and the factors which cause them (Trenkel et al. 2004a,b).