© 2017 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited

Amon, DJ

Glover, AG

Higgs, ND

Smith, CR

Young, EL

Proceedings of the Royal Society B Biological Sciences

Craig R. Smith

Diva J. Amon

Nicholas D. Higgs

Adrian G. Glover

Emily L. Young

Crossref

Data are inadequate to test whale falls as chemosynthetic stepping-stones using network analysis: faunal overlaps do support a stepping-stone role

© 2017 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.NHM Repositor

Smith, Craig

Amon, Diva

Natural History Museum Repository

rspb.royalsocietypublishing.orgCommentCite this article: Smith CR, Amon DJ, HiggsND, Glover AG, Young EL. 2017 Data areinadequate to test whale falls aschemosynthetic stepping-stones using networkanalysis: faunal overlaps do support astepping-stone role. Proc. R. Soc. B 284:20171281.http://dx.doi.org/10.1098/rspb.2017.1281Received: 7 June 2017Accepted: 20 July 2017Subject Category:EcologyAuthor for correspondence:Craig R. Smithe-mail: craigsmi@hawaii.eduComment on Kiel (2016): A biogeographicnetwork reveals evolutionary links betweendeep-sea hydrothermal vent and methaneseep faunas. Proc. R. Soc. B 283: 20162337.The accompanying reply can be viewed athttp://dx.doi.org/10.1098/rspb.2017.1644& 2017 The Authors. Published by the Royal Society under the terms of the Creative Commons AttributionLicense http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the originalauthor and source are credited.Data are inadequate to test whale falls aschemosynthetic stepping-stones usingnetwork analysis: faunal overlaps dosupport a stepping-stone roleCraig R. Smith1, Diva J. Amon2, Nicholas D. Higgs3, Adrian G. Glover2and Emily L. Young11Department of Oceanography, University of Hawai’i at Manoa, 1000 Pope Road, Honolulu, HI 96822, USA2Life Sciences Department, Natural History Museum, Cromwell Road, London SW7 5BD, UK3Marine Institute, University of Plymouth, Drake Circus, Plymouth PL4 8AA, UKCRS, 0000-0002-3976-0889Kiel [1] provides an interesting analysis of connectivity among bivalve and gas-tropod assemblages at hydrothermal vents, cold seeps and whale falls,suggesting a role for sedimented vents as evolutionary stepping stones betweenvents and seeps, but providing no support for whale falls playing a similar role.We caution that the dataset for whale falls used in Kiel [1], as well as furtheravailable data, are insufficient for network analysis to yield conclusions regard-ing lack of connectivity between whale falls, vents and seeps. Although Kiel [1]listed some limitations of the study, we present several more below to highlightthe weaknesses of the whale-fall analysis.A global connectivity analysis based on presence–absence data [1] relies onthe validity of at least two assumptions:(i) each vent, seep or whale-fall site included in the analysis has been wellsampled; i.e. if a taxon does not occur in the data from a particular site, itis because it is absent from that site, and not a consequence of undersamp-ling. Thus, absence from the data can be assumed to provide ‘evidence ofabsence’; and(ii) the sites representing a particular habitat type are broadly (in fact, globally)distributed,with a substantial sample sizewithin regions (e.g. ocean basins)to avoid geographical biases. In other words, there should bemultiple (wellsampled) sites for each habitat type in all regions across the globe so thatpatterns within regions, and within and between habitats, can be revealed.The datasets for vent and seep habitats inKiel [1]maywellmeet these assumptions,with 32 and 37 apparently well-sampled sites, respectively, distributed broadlyacross the ocean basins. However, the deep-sea whale-fall dataset fails to meetthese assumptions owing to a small number (7) of whale-fall sites, with only twosampled thoroughly for epifauna and sediment infauna. The sampling of sedimentinfauna is particularly important because sedimented vent habitats are identifiedas a linkage between vents and seeps. To make clear the limitations of the Kiel[1] dataset, it is important to discuss the whale-fall sites used in more detail.Kiel [1] included data from seven purported deep-sea whale-fall sites. Oneof the ‘whale-fall’ sites is actually an artificially implanted cow carcass [2]. Cowcarcasses are dramatically smaller, and have different bone sizes and character-istics (e.g. lipid content), than the carcasses of great whales (see Smith et al. [3]for a discussion of the important characteristics of great whale falls) so there islittle reason to expect that the full suite of species responding to a large whalecarcass would be found at a single cow carcass.Two of the ‘whale-fall sites’ used in Kiel [1] off New Zealand and Icelandwere actually isolated bones recovered in trawls from unobserved locations atrspb.royalsocietypublishing.orgProc.R.Soc.B284:201712812the seafloor [4–6]. Because these trawl samples (i) collectedonly portions of whale skeletons, (ii) lack any indicationthat the bones came from a large intact whale fall, (iii) prob-ably sustained significant loss of whale-bone fauna duringthe trauma of trawl recovery (approx. 90% of bone-associatedspecies can fall off whale bones even when carefully collectedby submersible, C. Smith 1988–2005, personal observations),and (iv) did not include sediment infauna, only ‘presencedata’ have any meaning for these ‘whale-fall’ sites. In otherwords, the absence of a taxon from a site could easily beowing to insufficient sampling. The use of trawled bones asadequate samples of entire whale-fall sites (which can containtens of thousands of individuals and hundreds of species dis-tributed both in sediments and over hundreds of bones[3,7,8]), is similar to dredging rocks from a hydrothermalvent and interpreting the attached fauna as representativeof the full suite of species likely to be found at the vent site.Finally, the datasets for the whale-fall sites in MontereyCanyon [9] and the Southern Ocean [10] in Kiel [1] includedlittle or no infaunal sampling. Since vesicomyid bivalves (akey vent–seep–whale-fall molluscan taxon) at whale fallstypically live buried within sediments underlying the bonesand can only be fully identified with substantial sediment-sampling effort [11,12], these two sites are also very likelyundersampled, especially with respect to vesicomyids. Infact, very recent infaunal data from the Monterey canyonwhale fall reveal the presence of vesicomyid genera alsofound at sedimented vents and seeps [13].This leaves two well-sampled whale-fall sites on the north-east Pacific margin in Kiel’s [1] ‘global’ analysis of connectivityamong vent, seep and whale-fall habitats. The small numberand restricted distribution of these whale-fall sites providesminimal opportunity to explore global connectivity patterns,yielding little basis for Kiel’s [1, p. 1] statement that: ‘Thehypothesis that decayingwhale carcasses are dispersal steppingstones linking these environments is not supported.’Although several otherwhale-fall sites, not included inKiel[1], have been sampled well [12,13], the whale-fall dataset isstill too sparse to support a global network analysis [3]. How-ever, shared habitats (e.g. sulfidic hard substrates, sedimentsand bacterial mats [3]), taxa and phylogenetic histories doimplicate whale falls as ecological and evolutionary steppingstones for deep-sea reducing habitats such as vents andseeps. For example, one northeast Pacific whale fall harbours10 genera also known from seeps (Annelida, Dorvilleidae:Paurougia, Ophryotrocha, Schistomeringos, Exallopus; Mollusca,Mytilidae: Idas; Vesicomyidae: Archivesica, Pliocardia,Calyptogena; Hyalogyrinidae: Hyalogyrina; Arthropoda,Isopoda: Illyarachna) and eight genera also known from vents(Annelida, Dorvilleidae: Parougia, Ophryotrocha, Exallopus;Polynoidae: Bathykurila; Mollusca, Mytilidae: Idas;Vesicomyidae: Archivesica, Calyptogena; Hyalogyrinidae:Hyalogyrina) [12]. Smith & Baco [7] report 10 species foundon northeast Pacific whale falls that also occur at hydrothermalvents, and 20 species that also occur at seeps. On a whale skel-eton in the abyssal South Atlantic, Sumida et al. [14] collectedfour genera of annelids shared with hydrothermal ventsand/or cold seeps. Many of the genera and species sharedbetween whale falls, vents and seeps are annelid wormswhich constitute a substantial portion of the diversity indeep-sea chemosynthetic habitats (e.g. [15–17]), suggestingthat a full network analysis of faunal connectivity acrossdeep-sea chemosynthetic habitats should include the Annelida.The faunal overlaps across whale falls, vents and seeps,and the role of whale falls as ecological stepping stones,may well have been greater before the vast reduction ofwhale populations and the loss of whale falls resultingfrom human whaling activities [18]. Palaeo-ecological andphylogenetic studies of taxa associated with deep-sea ventsand seeps also provide evidence for evolutionary connec-tivity with whale falls (reviewed in Smith et al. [3]),including the occurrence of basal clades of bathymodiolinmussels at whale falls [19] and indications of adaptive radi-ation at whale falls of taxa common at vents and seeps (e.g.the annelids in Siboglinidae [20] and Dorvilleidae [21,22]).Because vents, seeps and whale-fall fauna share taxa andphylogenetic histories, there is a strong need for intensivesampling of deep-sea whale-fall communities (including thesediment infauna) inmultiple ocean basins to support networkanalyses of the type conducted by Kiel [1]. This will allow us tofully elucidate global connectivity patterns among these deep-sea reducing habitats, and evaluate the roles that whale fallshave played in supporting biodiversity and maintainingother ecosystem functions across the global ocean [23].Competing interests. We declare we have no competing interests.Funding. Work on this paper was supported by the NSF OCE grant no.1155703 to C.R.S.References1. Kiel S. 2016 A biogeographic network revealsevolutionary links between deep-sea hydrothermalvent and methane seep faunas. Proc. R. Soc. B 283,20162337. (doi:10.1098/rspb.2016.2337)2. Hilario A, Cunha MR, Ge´nio L, Marc¸al AR, Ravara A,Rodrigues CF, Wiklund H. 2015 First clues on theecology of whale falls in the deep Atlantic Ocean:results from an experiment using cow carcasses.Mar. Ecol. 36, 82–90. (doi:10.1111/maec.12246)3. Smith CR, Glover AG, Treude T, Higgs ND, Amon DJ.2015 Whale-fall ecosystems: recent insights intoecology, paleoecology, and evolution. Ann. Rev.Mar. Sci. 7, 571–596. (doi:10.1146/annurev-marine-010213-135144)4. Marshall BA. 1987 Osteopeltidae (Mollusca:Gastropoda): a new family of limpets associatedwith whale bone in the deep sea. J. Molluscan Stud.53, 121–127. (doi:10.1093/mollus/53.2.121)5. Marshall BA. 1994 Deep-sea gastropods from theNew Zealand region associated with recent whalebones and an Eocene turtle. Nautilus (Philadelphia).108, 1–8.6. Waren A. 1989 New and little known Mollusca fromIceland. Sarsia 71, 1–28. (doi:10.1080/00364827.1989.10413419)7. Smith CR, Baco AR. 2003 Ecology of whale falls atthe deep-sea floor. Oceanogr. Mar. Biol. 41,311–354.8. Baco AR, Smith CR. 2003 High species richness indeep-sea chemoautotrophic whale skeletoncommunities. Mar. Ecol. Prog. Ser. 260, 109–114.(doi:10.3354/meps260109)9. Braby CE, Rouse GW, Johnson SB, Jones WJ,Vrijenhoek RC. 2007 Bathymetric and temporalvariation among Osedax boneworms and associatedmegafauna on whale falls in Monterey Bay,California. Deep Sea Res. I 54, 1773–1791. (doi:10.1016/j.dsr.2007.05.014)10. Amon DJ, Glover AG, Wiklund H, Marsh L, Linse K,Rogers AD, Copley JT. 2013 The discovery of a naturalwhale fall in the Antarctic deep sea. Deep Sea Res. II92, 87–96. (doi:10.1016/j.dsr2.2013.01.028)rspb.royalsocietypublishing.orgProc.R.Soc.B284:2017128311. Bennett BA, Smith CR, Glaser B, Maybaum HL. 1994Faunal community structure of a chemotrophicassemblage on whale bones in the deep northeastPacific Ocean. Mar. Ecol. Prog. Ser. 108, 205–223.(doi:10.3354/meps108205)12. Smith CR, Bernardino AF, Baco A, Hannides AK,Altamira I. 2014 The seven-year enrichment:macrofaunal succession in deep-sea sedimentsaround a 30-ton whale fall in the Northeast Pacific.Mar. Ecol. Prog. Ser. 515, 133–149. (doi:10.3354/meps10955)13. Johnson SB, Krylova EM, Audzijonyte A, Sahling H,Vrijenhoek RC. 2017 Phylogeny and origins ofchemosynthetic vesicomyid clams. Syst. Biodivers.15, 346–360. (doi:10.1080/14772000.2016.1252438)14. Sumida PYG et al. 2016 Deep-sea whale fallfauna from the Atlantic resembles that of thePacific Ocean. Sci. Rep. 6, 22139. (doi:10.1038/srep22139)15. Van Dover CL. 2000 The ecology of deep-Seahydrothermal vents. Princeton, NJ: PrincetonUniversity Press.16. Hilario A, Capa M, Dahlgren TG, Halanych KM, LittleCTS, Thornhill DJ, Verna C, Glover AG, Laudet V.2011 New perspectives on the ecology andevolution of siboglinid tubeworms. PLoS ONE 6,e16309. (doi:10.1371/journal.pone.0016309)17. Van Dover CL. 1990 Biogeography of hydrothermalvent communities along seafloor spreading centers.Trends Ecol. Evol. 5, 242–246. (doi:10.1016/0169-5347(90)90063-J)18. Smith CR. 2006 Bigger is better: the role of whalesas detritus in marine ecosystems. In Whales,whaling and ocean ecosystems (eds JA Estes,P DeMaster, DF Doak, TM Williams, RL Brownell Jr),pp. 286–300. Berkeley, CA: University of CaliforniaPress.19. Distel DL, Baco AR, Chuang E, Morrill W, CavanaughC, Smith CR. 2000 Do mussels take wooden steps todeep-sea vents? Nature 403, 725–726. (doi:10.1038/35001667)20. Vrijenhoek R, Johnson S, Rouse G. 2009A remarkable diversity of bone-eating worms(Osedax; Siboglinidae; Annelida). BMC Biol. 7,1–13. (doi:10.1186/1741-7007-7-74)21. Wiklund H, Altamira I, Glover AG, Smith CR, Baco A,Dahlgren TG. 2012 Systematics and biodiversity ofOphryotrocha (Annelida, Dorvilleidae) with descriptionsof six new species from deep-sea whale-fall and wood-fall habitats in the north-east Pacific. Syst. Biodivers.10, 243–259. (doi:10.1080/14772000.2012.693970)22. Thornhill DJ, Struck TH, Ebbe B, Lee RW, Mendoza GF,Levin LA, Halanych KM. 2012 Adaptive radiation inextremophilic Dorvilleidae (Annelida): diversification ofa single colonizer or multiple independent lineages?Ecol. Evol. 2, 1958–1970. (doi:10.1002/ece3.314)23. Roman J et al. 2014 Whales as marine ecosystemengineers. Front. Ecol. Environ. 12, 377–385.(doi:10.1890/130220) 1

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Data are inadequate to test whale falls as chemosynthetic stepping-stones using network analysis: faunal overlaps do support a stepping-stone role

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