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High Species Richness in Deep-Sea Chemoautotrophic Whale Skeleton Communities

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High Species Richness in Deep-Sea Chemoautotrophic Whale Skeleton Communities MARINE ECOLOGY PROGRESS SERIES Vol. 260: 109–114, 2003 Published September 30 Mar Ecol Prog Ser High species richness in deep-sea chemoautotrophic whale skeleton communities Amy R. Baco1, 2,*, Craig R. Smith1 1Department of Oceanography, 1000 Pope Road, Honolulu, Hawaii 96822, USA 2Present address: Woods Hole Oceanographic Institution, Biology Department, MS#33 2-14 Redfield, Woods Hole, Massachusetts 02543, USA ABSTRACT: While biodiversity in deep-sea soft sediments appears to be high, little is known about diversity levels on deep-sea hard substrates. To determine the contribution of potentially abundant whale-skeleton habitats to deep-sea biodiversity, we compare the local macrofaunal species richness and composition on 3 sulfide-rich whale skeletons to assemblages from vents, seeps, and other deep- sea hard substrates. Based on rarefaction curves, whale skeleton diversity is higher than diversity in any other deep-sea hard substrate habitat. The average local species richness (185 spp.) on single chemoautotrophic whale skeletons approaches known levels of global cold-seep macrofaunal species richness (229 spp.), and exceeds the richness of the most speciose vent field known (121 spp.). Species richness on the whale skeletons is also substantially higher than on other deep-sea non- reducing hard substrates, such as manganese nodules and rocks. Richness levels approach those in deep-sea soft sediments and exceed some shallow-water hard substrates. This high species richness may be explained by unusually high trophic diversity on whale bones due to the presence of sulphophiles, generalized organic-enrichment respondents, whale-bone consumers, and back- ground hard-substrate fauna such as suspension and deposit feeders. High species richness levels on whale skeletons and deep-sea sponge stalks suggest deep-sea hard substrates may harbor higher levels of diversity than previously recognized. KEY WORDS: Whale fall · Species richness · Biodiversity · Deep sea · Hard substrate Resale or republication not permitted without written consent of the publisher INTRODUCTION geographical distribution, dynamics, and chemical con- ditions, each is likely to harbor characteristic macrofau- Documentation of biodiversity patterns in the deep sea nal communities with distinct patterns of biodiversity. is fundamental to understanding the ecological and evo- Here we begin evaluation of biodiversity patterns in lutionary novelties of the ocean. A number of studies one type of potentially abundant hard-substrate com- suggest that deep-sea soft-sediments often contain high munity in the deep sea: sulfide-rich whale skeletons. levels of local diversity, and global biodiversity in deep- Smith & Baco (2003) estimate that, at any given time, sea sediments may be similarly high (reviewed in Snel- there may be >500 000 sulfide-rich whale skeletons at grove & Smith 2002). While substantially more data are the deep-sea floor. Prior to the advent of industrial required to critically evaluate the biodiversity of the whaling in approximately 1800, the number of sulfide- sedimentary deep sea, even less is known of biodiversity rich whale skeletons may have been 2- to 5-fold higher patterns on deep-sea hard substrates. Hard substrates (Butman et al. 1995, Smith & Baco 2003). occur in a range of divergent deep-ocean habitats, in- Whale falls may promote high biodiversity in the cluding rock outcrops, manganese nodules, hydro- deep sea by providing hard substrates, organic enrich- thermal vents, cold seeps, sponge stalks and whale ment, and free sulfides at a typically sediment-covered, skeletons. Because these habitats vary dramatically in organic-poor deep-sea floor (Bennett et al. 1994, But- *Email: [email protected] © Inter-Research 2003 · www.int-res.com Table 1. Comparison of macrofaunal species richness from whale skeletons and rocks from the California slope, as well as from other hard substrates. All deep-sea studies used 300 µm or smaller mesh sieves. Shallow-water studies used 500 µm or larger mesh sizes 110 Habitat Depth Number of Number of Number of Surface area Fisher’s Evenness Source (m) individuals macrofaunal polychaete (or volume) α (J’) sampled species species sampled Deep-sea hard substrates San Nicolas (SN) whale skeletona 960 5 120 190 106 0.83 m2 38.90 0.60 This study Santa Catalina Basin (SCB) whale skeletona,b 1240 20 632 180 105 1.26 m2 27.19 0.46 This study San Clemente Basin (SCL) whale skeletona,b 1910 11 555 102 48 1.05 m2 15.44 0.24 This study Mid-Atlantic Ridge hydrothermal 1600 20 044 25 6 24.7 l of mussels 3.02d 0.43d Van Dover & Trask (1999) vent mussel bedsc San Clemente cold seepc 1800 16 613 86 29 ~3 m2 of vestimen- 11.89d 0.60d Poehls et al. (unpubl. data) tiferan tubes Manganese nodules 4500–5800 ~120 32 2 0.11 m2 11.98d 0.82d Mullineaux (1987) Deep-sea sponges 4100 1 933 104 35 0.11 m2 23.25d 0.54d Beaulieu (2001) Deep-sea rocks (near SN skeleton) ~960 147 26 12 <0.3 m2 9.17 0.37 This study Shallow-water hard substrates Mar EcolProg Ser260:109–114, 2003 Lophelia pertusa (coral) reefs 260 4 626 298 72 9.34 l of coral Jensen & Frederiksen (1992) Pocillopora damicornis (coral) 0–6 951 101 0 31.49 l of coral 28.59d 0.77d Austin et al. (1980), Jensen & Frederiksen (1992) Intertidal mussel beds 0 78 353 70 17 ~80 l of mussels 8.58d 0.61d Van Dover & Trask (1999) Rocky intertidal 0 214 37 species 0.09 m2 Dean & Connell (1987) in Annelida Temperate (>50° N) rocky shoreline 10–15 14 094 137 44 32 pan scourers Gee & Warwick (1996) aNeither mobile megafauna (fishes, galathaeids), which escaped collection, nor sediment infauna were included in these estimates bData were combined for skeletons sampled at 2 time points. The SCB skeleton had 96 species in 1995 and 149 species in 1999. The SCL skeleton had 96 species in 1995 and >27 species in 2000 cExamples given represent the most comparable study of that habitat type from the literature. Mean diversity for single vent sites is about 50 to 60 species, and about 11 species for seeps dRe-calculated from original data foil required tofullycoverbonesur- weighing theamountofaluminum surface areas were estimatedby using adissectingmicroscope. Bone macrofauna were sorted tospecies were stainedwithRoseBengal,and ferred to80% ethanol.Samples seawater solutionandlatertrans- ately fixedin10% formaldehyde/ Allsampleswere covery. immedi- the surfaces ofthebonesuponre- visible epifaunawasremoved from box residues ona300µmsieve.All transport wascollectedbywashing from thebonesintoboxduring to thesurface andepifaunathatfell samples.) Theboxeswere brought sent aslightunderestimate forthese sity andabundanceestimatesrepre- with themanipulatorarm, sodiver- from bonesduringinitialcollection boxes. (Somefaunamayhavefallen manipulator andplacedinsealed or remotely operatedvehicle(ROV) were collectedusingasubmersible and 33° 15’ N,119° 20’ W).Bones depths (960m,33° 15’ N,119° 56’ W tions inthegeneralvicinityatsimilar 118° 9’ W)aswellrocks at2loca- Clemente Basin,1910m,32° 26’ N, 1240 m,33° 12’ N,118°29’ San W; 119° 59’ SantaCatalinaBasin, W; 2000 (SanNicolas,960m,33° 20’ N, California slopebetween1995and from eachof3skeletonsonthe we collected1to7vertebral bones ness levelsonlipid-richwhalefalls, determine macrofaunal speciesrich- be remarkably diverse. California, andwediscoverthemto hundreds ofkilometersoff southern rich whaleskeletonsseparatedby faunal speciesrichnesson3sulfide- 1998). Here weevaluatemacro- site (Bennettetal.1994,Smith studies were conductedatasingle munity composition,andthese tatively addressed whale-fallcom- only2studieshavequanti- However, man etal.1995,Smith&Baco2003). Study sitesandsampling. MATERIALS ANDMETHODS MATERIALS To Baco & Smith: Diversity on deep-sea whale skeletons 111 faces in a monolayer. The sampled surface area of the faunal species in 10 phyla collected in 5120 individuals bones above the sediment-water interface for each (Table 1). The Santa Catalina Basin (SCB) skeleton skeleton, as well as the total numbers of macrofaunal also had very high species richness with 180 species. individuals and species, are given in Table 1. Sediment The San Clemente Basin (SCL) skeleton had lower fauna, bone meiofauna, and mobile megafauna are not species richness, with 102 species. Stable isotope stud- included in these estimates. ies indicate that the SCL skeleton fauna are not depen- For the 2 skeletons sampled at more than 1 time dent on chemoautotrophic production (Baco-Taylor point, Santa Catalina Basin and San Clemente Basin, 2002, Baco & Smith unpubl. data). The range of niches species lists were combined for data analyses. For each associated with chemoautotrophic production may be of these skeletons, the communities at the times sam- absent at this site, resulting in substantially lower pled appeared to be in the same successional stage levels of species richness. (dominant species, etc.) and changes in diversity were The most speciose taxon on all 3 whale skeletons related to sampling intensity. was the polychaetes, with particular diversity in the Data analyses. The available data on quantitative families Dorvilleidae, Ampharetidae, and Polynoidae. studies of hard substrate macrofauna that are listed in Molluscs were numerically dominant at all 3 sites with Table 1 come from a variety of studies. All of the deep- the chemoautotrophic-endosymbiont hosting mytilid sea hard substrate studies included for comparison used bivalve Idas washingtonia the most abundant (Baco- a sieve mesh size of 300 µm or smaller. Shallow-water Taylor 2002, Baco & Smith unpubl. data). studies
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