Vol. 508: 177–185, 2014 MARINE ECOLOGY PROGRESS SERIES Published August 4 doi: 10.3354/meps10877 Mar Ecol Prog Ser OPENPEN ACCESSCCESS β-diversity of deep-sea holothurians and asteroids along a bathymetric gradient (NE Atlantic) Martine C. Wagstaff1,*, Kerry L. Howell2, Brian J. Bett3, David S. M. Billett3, Solange Brault1, Carol T. Stuart1, Michael A. Rex1 1Department of Biology, University of Massachusetts, 100 Morrissey Blvd, Boston, MA 02125 2University of Plymouth, Drake Circus, Plymouth PL4 8AA, UK 3National Oceanography Centre, Southampton SO14 3ZH, UK ABSTRACT: Measuring and understanding patterns of β-diversity remain major challenges in community ecology. Recently, β-diversity has been shown to consist of 2 distinct components: (1) spatial turnover and (2) species loss leading to nestedness. Both components structure deep-sea macrofaunal assemblages but vary in importance among taxa and ocean basins and with energy availability. Here, we present the first evidence for turnover and nestedness along a bathymetric gradient in 2 major megafaunal taxa, holothurians and asteroids. Turnover is the dominant com- ponent of β-diversity throughout bathyal and abyssal zones in both taxa, despite major differences in α-diversity and trophic composition. High spatial turnover suggests a role for evolutionary adaptation to environmental circumstances within depth bands. This pattern differs fundamen- tally from those in some macrofaunal groups in low-energy environments where abyssal nested- ness is high and diversity low, with diversity maintained partly by source-sink dynamics. KEY WORDS: Beta diversity · Nestedness · Turnover · Source−sink dynamics · Deep sea · Echinoderms · Asteroids · Holothurians INTRODUCTION makeup in the deep sea more accessible to ecologists working in other systems. Much is known about patterns of deep-sea α-diver- Deep-sea β-diversity has been interpreted mainly sity and their potential ecological and evolutionary as a process of species replacement along bathymetric drivers (Rex & Etter 2010). However, measuring pat- (Carney 2005) and horizontal (McClain & Hardy 2010) terns of β-diversity and understanding their under - environmental gradients. However, β-diversity has 2 lying causes remain daunting challenges (Carney distinct components: spatial replacement of species 2005, Wei et al. 2010a). Historically, in deep-sea eco - (turnover), and species loss leading to nestedness logy, β-diversity has been referred to as ‘zonation,’ (Baselga 2010, 2012). Nestedness is when smaller meaning depth zones of relatively little faunal change, communities are ordered subsets of species assem- separated by more abrupt shifts called boundaries blages in larger communities. Both species turnover (Le Danois 1948). With improved sampling, it be - and nestedness can contribute to β-diversity in deep- came apparent that most faunal change with depth is sea communities (Brault et al. 2013a,b). gradual and continuous unless interrupted by major One of the strongest environmental gradients in topographic features or sharp changes in oceano- the deep sea is the exponential decrease in food sup- graphic conditions (Rex & Etter 2010). We prefer to ply from particulate organic carbon (POC) flux to the use term β-diversity because it is more widely used sea floor with increasing depth. At abyssal depths in ecology and makes studies of variation in faunal (>4000 m), severely low food supply can limit species © The authors 2014. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 178 Mar Ecol Prog Ser 508: 177–185, 2014 diversity (Tittensor et al. 2011, McClain et al. 2012). (for a map of sampling stations, please see Howell et In macrofaunal molluscs, with depressed abyssal al. 2002). The samples include 43 species of holo - diversity, abyssal communities are nested subsets thurians (Billett 1991) and 43 species of asteroids of lower bathyal communities. These depauperate (Howell et al. 2002). To meet the matrix size and fill abyssal communities are essentially composed of requirements of the analytical methods, we first bathyal species whose depth range extensions are binned stations into 250 m depth increments. This made possible through larval dispersal. This sug- bin size also seemed to capture variation in depth gests that some abyssal populations may be sinks ranges and diversity. Using different bin sizes of 100 that are maintained by continued immigration from to 1000 m did not affect our results. No depth incre- more abundant bathyal sources (Rex et al. 2005). ment explored indicated effects of major hydro - Where abyssal diversity is not depressed, because logical or physiographic features. We then created POC-flux remains relatively high, turnover domi- binary presence-absence matrices of species occur- nates at all depths and abyssal assemblages contain rences in each depth bin. Abundance data are more endemic species (Brault et al. 2013b). reported by Billett (1991) and Howell et al. (2002). We examine bathymetric trends in α- and β-diver- Highest population densities are not found consis- sity in megafaunal asteroids and holothurians in the tently in any part of the depth distributions. We used NE Atlantic to determine the relative importance of only records of positive occurrence within a depth turnover and nestedness. This is the first time nested- bin and presence/absence data in our analyses be - ness versus turnover has been measured in megafau- cause this is the most conservative approach. How- nal taxa. Megafaunal density and biomass decrease ever, we illustrated ranges (Figs. 1 & 2) as though more rapidly with depth than for the macrofauna, they were fully occupied. We estimated α-diversity presumably because large organisms have higher as the number of co-occurring species in a depth bin energy demands and are more vulnerable to the (positive occurrences only). decline in food supply with depth (Rex et al. 2006, Following the practice of several other studies (e.g. Wei et al. 2010b). Our initial hypothesis was that Billett 1991, Jangoux 1982, Roberts & Moore 1997, nestedness β-diversity should predominate in as - Iken et al. 2001, Gale et al. 2013), we also attempted semblages of reduced diversity, whereas turnover to classify the feeding types of the species present β-diversity should predominate where abyssal diver- (in the case of the asteroids, we supply additional sity remains high. information on feeding type in Table S1 in the supplement at www.int-res-com/articles/ suppl/m508 p177_ supp. pdf). Deep-sea holothurians are typically METHODS deposit feeders (Billett 1991) (Fig. 1). Different deposit-feeding modes exist (Roberts & Moore 1997), Geographic setting, biogeographic patterns, and al though we were not able to infer those from our echinoderm biology dataset. Asteroids are more trophically complex. Ana lysis of stomach contents is often uninformative We compare α-diversity, depth distributions, and be cause the majority of species have extraoral β-diversity of holothurians and asteroids collected digestion and are flexible in their diet even intra - from the Porcupine Seabight (PSB) and Porcupine specifically (Jangoux 1982). Jangoux (1982, p. 117) Abyssal Plain (PAP) in the eastern North Atlantic. describes the trophic biology of asteroids as being “at The PSB is an amphitheater-shaped embayment in one and the same time an extensively studied topic the Irish continental margin that opens to the adja- and a still little known matter.” The asteroid assem- cent abyssal plain at 4000 m (Rice et al. 1991). In the blage examined here includes carnivores (predators following, we refer to depths >4000 m as abyssal as and scavengers), suspension feeders, and deposit this depth physiographically marks the beginning of feeders. For some species, direct evidence of diet and the abyssal plain. feeding types exists (although in many cases there The data represent 160 and 209 epibenthic sledge is evidence for polytrophy between regions; see and semi-balloon otter trawl samples for holothurians Table S1 in the Supplement). For the purpose of this and asteroids respectively (131 samples are shared) analysis, we characterized a species according to taken over a 21 yr period from 1977 to 1998 as part the dominant feeding mode when known. For other of the Institute of Oceanographic Sciences Biology species, we inferred diet based on information from Programme in the PSB (Rice et al. 1991) and the either the same species at a different site or evidence BENGAL Program in the PAP (Billett & Rice 2001) from congeneric and confamilial species. If a group Wagstaff et al.: β-diversity in deep-sea echinoderms 179 Holothurian species Number of species 0 5 10 15 20 Parastichopus tremulus Thyone gadeana Mesothuria intestinalis Psolus squamatus Laetmogone violacea Echinocucumis hispida Bathyplotes natans Ypsilothuria talismani Mesothuria milleri Prototrochus zenkevitchi rockallensis Mesothuria lactea Benthogone rosea Paroriza pallens Mesothuria maroccana Hedingia albicans Paelopades grisea Mesothuria cathedralis Elpidia echinata Kolga nana Mesothuria bifurcata Psychropotes depressa Peniagone diaphana Peniagone azorica Benthothuria funebris Molpadia blakei Labidoplax southwardorum Protankyra brychia Deima validum Myriotrochus giganteus Cherbonniera utriculus Oneirophanta mutabilis Molpadiodemas violaceus Benthodytes