Abstract
The ecological and evolutionary processes that interact to shape community structure are poorly studied in the largest environment on earth, the deep sea. Phylogenetic data and morphological traits of octocorals were coupled with environmental factors to test hypotheses of community assembly in the deep (250–2500 m) Gulf of Mexico. We found lineage turnover at a depth of 800–1200 m, with isidids and chrysogorgiids at deeper depths and a diversity of species from across the phylogeny occupying shallower depths. Traits, including axis type, polyp shape, and polyp retraction, differed among species occupying the shallowest (250–800 m) and deepest (1200–2500 m) depths. Results also indicated that octocoral species sort along an environmental gradient of depth. Closely related octocoral species sorted into different depth strata on the upper to middle slope, likely due to barriers imposed by water masses followed by adaptive divergence. Within any given depth zone down to 2000 m, the phylogenetic relatedness of co-existing octocorals was random, indicating that stochastic processes, such as recruitment, also shape community structure. At depths >2000 m, octocorals were more closely related than expected by chance due to the diversification of chrysogorgiids and isidids, which retain conserved traits that impart survival at deeper and/or colder depths. Polyp density, size, and inter-polyp distance were significantly correlated with depth, particularly in plexaurids and isidids, highlighting trait lability across depth and supporting that environmental gradients influence octocoral morphology. Our community phylogenetics approach indicates that both environmental filtering and neutral processes shape community assembly in the deep sea.
Similar content being viewed by others
References
Ackerly DD, Schwilk DW, Webb CO (2006) Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology 87:S50–S61
Anderson M, Gorley RN, Clarke RK (2008) Permanova+ for primer: guide to software and statistical methods. PRIMER-E Ltd, Plymouth
Andrews AH, Cordes EE, Mahoney MM, Munk K, Coale KH, Cailliet GM et al (2002) Age growth and radiometric age validation of a deep-sea habitat-forming gorgonian (Primnoa resedaeformis) from the Gulf of Alaska. Hydrobiologia 471(1–3):101–110
Ardila NE, Giribet G, Sánchez JA (2012) A time-calibrated molecular phylogeny of the precious corals: reconciling discrepancies in the taxonomic classification and insights into their evolutionary history. BMC Evol Biol 12:246
Baco AR, Cairns SD (2012) Comparing molecular variation to morphological species designations in the deep-sea coral Narella reveals new insights into seamount coral ranges. PLoS ONE 7(9):e45555
Bayer FM (1981) Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa) with diagnoses of new taxa. Proc Biol Soc Wash 94:902–947
Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745
Bostock HC, Tracey DM, Currie KI, Dunbar G, Handler MR, Mikaloff Fletcher SE, Smith AM, Williams MJM (2015) The carbonate mineralogy and distribution of habitat-forming deep-sea corals in the southwest pacific region. Deep-Sea Res I 100:88–104
Brault S, Stuart CT, Wagstaff MC, McClain CR, Allen JA, Rex MA (2013) Contrasting patterns of α-and β diversity in deep-sea bivalves of the eastern and western North Atlantic. Deep-Sea Res II 92:157–164
Brooke S, Homes M, Young CM (2009) Effects of sediment on two morphotypes of Lophelia pertusa from the Gulf of Mexico. Mar Ecol Prog Ser 390:137–144
Brown A, Thatje S (2014) Explaining bathymetric diversity patterns in marine benthic invertebrates and demersal fishes: physiological contributions to adaptation of life at depth. Biol Rev 89(2):406–426
Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity. PNAS 105:11505–11511
Cairns SD, Bayer F (2001) Studies on western Atlantic Octocorallia (Coelenterata: Anthozoa) Part 1: the genus Chrysogorgia Duchassaing and Michelotti 1864. Proc Biol Soc Wash 114(3):746–787
Cairns SD, Bayer F (2002) Studies on western Atlantic Octocorallia (Coelenterata: Anthozoa) Part 4: the genus Callogorgia Gray 1858. Proc Biol Soc Wash 115(4):840–867
Cairns SD, Bayer F (2004) Studies on western Atlantic Octocorallia (Coelenterata: Anthozoa) Part 4: the genus Paracalyptrophora Kinoshita 1908. Proc Biol Soc Wash 117(1):114–139
Carney RS (1994) Consideration of the oasis analogy for chemosynthetic communities at Gulf of Mexico hydrocarbon vents. Geo-Marine Lett. 14(2–3):149–159
Carney RS (2005) Zonation of deep-sea biota on continental margins. Oceanogr Mar Biol Annu Rev 43:211–279
Cavender-Bares J, Kozak K, Fine P, Kembel S (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715
Chase JM, Leibold MA (2003) Ecological niches linking classical and contemporary approaches. University of Chicago Press, Chicago
Clarke KR, Gorley RN (2015) PRIMER v7: user manual/tutorial. PRIMER-E-LTD, Plymouth
Cordes EE, Bergquist DC, Fisher CR (2009) Macro-ecology of Gulf of Mexico cold seeps. Ann Rev Mar Sci 1:143–168
Cordes EE, Cunha MR, Galeron J, Mora C, Roy OL, Sibuet M et al (2010) The influence of geological, geochemical, and biogenic habitat heterogeneity on seep biodiversity. Mar Ecol 31(1):51–65
Daly M, Brugler MR, Cartwright P, Collins AG, Dawson MN, France SC et al (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182
Doughty CL, Quattrini AM, Cordes EE (2014) Insights into the population dynamics of the deep-sea coral genus Paramuricea in the Gulf of Mexico. Deep Sea Res II 99:71–82
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 17. Mol Biol Evol 29:1969–1973
Dueñas LF, Sánchez JA (2009) Character lability in deep-sea bamboo corals (Octocorallia: Isididae: Keratoisidinae). Mar Ecol Prog Ser 397:11–23
Etter RJ, Bower AS (2015) Dispersal and population connectivity in the deep North Atlantic estimated from physical transport processes. Deep Sea Res I 104:159–172
Etter RJ, Grassle JF (1992) Patterns of species diversity in the deep sea as a function of sediment particle size diversity. Nature 360:576–578
Gabay Y, Fine M, Barkay Z, Benayahu Y (2014) Octocoral tissue provides protection from declining oceanic pH. PLoS ONE 9(4):e91553
Georgian SE, DeLeo D, Durkin A, Gomez CE, Kurman M, Lunden JJ, Cordes EE (2016) Oceanographic patterns and carbonate chemistry in the vicinity of cold-water coral reefs in the Gulf of Mexico: implications for resilience in a changing ocean. Limnol Oceanogr 61:648–665. doi:10.1002/lno.10242
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Soft 22:1–19
Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–871
Graham CH, Fine PVA (2008) Phylogenetic beta diversity: linking ecological and evolutionary processes across space and time. Ecol Lett 11:1265–1277
Graham CH, Parra JL, Rahbek C, McGuire JA (2009) Phylogenetic structure in tropical hummingbird communities. PNAS 106:19673–19678
Grassle JF, Sanders H (1973) Life histories and the role of disturbance. Deep-Sea Res 20:643–659
Grigg RW (1988) Recruitment limitation of a deep benthic hard-bottom octocoral population in the Hawaiian Islands. Mar Ecol Prog Ser 45:121–126
Herrera S, Shank TM, Sánchez JA (2012) Spatial and temporal patterns of genetic variation in the widespread antitropical deep-sea coral Paragorgia arborea. Mol Ecol 21(24):6053–6067
Hessler RR, Sanders HL (1967) Faunal diversity in the deep-sea. Deep-Sea Res 14:65–78
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton
Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV (2013) Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol Biol 13(1):5. doi:10.1186/1471-2148-13-5
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Kim E, Lasker HR, Coffroth MA, Kim K (2004) Morphological and genetic variation across reef habitats in a broadcast-spawning octocoral. Hydrobiologia 530(1–3):423–432
Kraft N, Cornwell W, Webb C, Ackerly D (2007) Trait evolution community assembly and the phylogenetic structure of ecological communities. Am Nat 170:271–283
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91(1):299–305
Lasker HR, Kim K, Coffroth MA (1998) Production settlement and survival of plexaurid gorgonian recruits. Mar Ecol Prog Ser 162:111–123
Leprieur F, Albouy C, De Boroli J, Cowman PF, Bellwood DR, Mouillot D (2012) Quantifying phylogenetic beta diversity: distinguishing between ‘true’ turnover of lineages and phylogenetic diversity gradients. PLoS ONE 7:e42760
Levin LA, Sibuet M (2012) Understanding continental margin biodiversity: a new imperative. Annu. Rev. Mar. Sci. 4:79–112
Levin LA, Sibuet M, Gooday AJ, Smith CR, Vanreusel A (2010) The roles of habitat heterogeneity in generating and maintaining biodiversity on continental margins: an introduction. Mar Ecol 31(1):1–5
Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Anglais 305:127–137
Linares C, Doak DF, Coma R, Díaz D, Zabala M (2007) Life history and viability of a long-lived marine invertebrate: the octocoral Paramuricea clavata. Ecology 88(4):918–928
Losos JB, Leal M, Glor RE, de Queiroz K, Hertz PE, Schettino LR, Lara AC, Jackman TR, Larson A (2003) Niche lability in the evolution of a Caribbean lizard community. Nature 424(6948):542–545
Lunden JJ, McNicholl CG, Sears CR, Morrison CL, Cordes EE (2014) Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification warming and deoxygenation. Front Mar Sci 1:78
Mah CL, Nizinski MS, Lundsten L (2010) Phylogenetic revision of the Hippasterinae (Goniasteridae; Asteroidea): systematics of deep sea corallivores including one new genus and three new species. Zool J Linn Soc 160:266–301
McClain CR, Stegen JC, Hurlbert AH (2012) Dispersal, niche dynamics and oceanic patterns in beta diversity in deep-sea bivalves. Proc R Soc B 22:1993–2002
McFadden CS, van Ofwegen LP (2012) Stoloniferous octocorals (Anthozoa Octocorallia) from South Africa with descriptions of a new family of Alcyonacea a new genus of Clavulariidae and a new species of Cornularia (Cornulariidae). Invert Syst 26:331–356
McFadden CS, France SC, Sánchez JA, Alderslade P (2006) A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol Phyl Evol 41(3):513–527
McFadden CS, Sánchez JA, France SC (2010) Molecular phylogenetic insights into the evolution of Octocorallia: a review. Integr Compar Biol 50(3):389–410
Mosher CV, Watling L (2009) Partners for life: a brittle star and its octocoral host. Mar Ecol Prog Ser 397:81–88
Pante E, Watling L (2012) Chrysogorgia from the New England and Corner Seamounts: Atlantic-Pacific connections. J Mar Biol Assoc UK 92(05):911–927
Pante E, France SC, Couloux A, Cruaud C, McFadden CS, Samadi S, Watling L (2012) Deep-sea origin and in situ diversification of chrysogorgiid octocorals. PLoS One 7:e38357. doi:10.1371/journalpone0038357
Pickett STA, Bazazz FA (1978) Organization of an assemblage of early successional species on a soil moisture gradient. Ecology 59:1248–1255
Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. PNAS 110(10):3961–3966. doi:10.1073/pnas1208931110
Prada C, Schizas NV, Yoshioka PM (2008) Phenotypic plasticity or speciation? A case from a clonal marine organism. BMC Evol Biol 8(1):1
Prouty NG, Fisher CR, Demopoulos AWJ, Druffel ER (2014) Growth rates and ages of deep-sea corals impacted by the Deepwater Horizon oil spill. Deep-Sea Res II
Quattrini AM, Georgian SE, Byrnes L, Falco R, Cordes EE (2013) Niche divergence by deep-sea octocorals in the genus Callogorgia across the continental slope of the Gulf of Mexico. Mol Ecol 22:4123–4140
Quattrini AM, Etnoyer PJ, Doughty CM, English L, Falco R, Remon N et al (2014) A phylogenetic approach to octocoral community structure in the deep Gulf of Mexico. Deep-Sea Res II. doi:10.1016/jdsr2201305027
Quattrini AM, Baums IB, Shank TS, Morrison CS, Cordes EE (2015) Testing the depth differentiation hypothesis in a deepwater octocoral. Proc R Soc B 282(1807). doi:10.1098/rspb.2015.000
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. University Press, Cambridge
R Development Core Team (2012) R: a language and environment for statistical computing R Foundation for Statistical Computing. Vienna Austria. ISBN 3-900051-07-0 http://www.R-projectorg/
Raddatz J, López Correa M, Rüggeberg A, Dullo W, Hansteen T (2011) Bioluminescence in deep-sea isidid gorgonians from the Cape Verde archipelago. Coral Reefs 30(3):579
Radice V, Quattrini AM, Wareham V, Edinger E, Cordes EE (2016) Influence of water mass on the bathymetric distribution of the octocoral genus Paramuricea in the North Atlantic. Deep-Sea Res I 116:253-263
Rex MA (1981) Community structure in the deep-sea benthos. Ann Rev Ecol Syst 12:331–353
Rex MA, Etter RJ (2010) Deep-sea Biodiversity. Harvard University Press, Cambridge
Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171
Ricklefs RE (2006) Evolutionary diversification and the origin of the diversity-environment relationship. Ecology 87(Supplement):S3–S13
Rivas D, Badan A, Ochoa J (2005) The ventilation of the deep Gulf of Mexico. J Phys Oceanogr 35(10):1763–1781
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S et al (2012) MRBAYES 32: efficient Bayesian phylogenetic inference and model selection across a large model space. Syst Biol 61:539–542
Rowley SJ, Pochon X, Watling L (2015) Environmental influences on the Indo-Pacific octocoral Isis hippuris Linnaeus 1758 (Alcyonacea: Isididae): genetic fixation or phenotypic plasticity? Peer J 3:e1128
Sale PF (1977) Maintenance of high diversity in coral reef fish communities. Am Nat 111:337–359
Sánchez JA (1999) Black coral-octocoral distribution patterns on a deep-water reef Imelda bank Caribbean Sea Colombia. Bull Mar Sci 65:215–225
Sánchez JA (2005) Systematics of the bubblegum corals (Cnidaria: Octocorallia: Paragorgiidae) with description of new species from New Zealand and Eastern Pacific. Zootaxa 1014:1–72
Sánchez JA, McFadden CS, France SC, Lasker HR (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987
Savage JA, Cavender-Bares J (2012) Habitat specialization and the role of trait lability in structuring diverse willow (genus Salix) communities. Ecology 93(sp8)
Silvertown J, McConway KJ, Gowing DJ, Dodd ME, Fay MF, Joseph JA, Dolphin K (2006) Absence of phylogenetic signal in the niche structure of meadow plant communities. Proc R Soc B 273:39–44
Snelgrove PVR, Grassle JF, Petrecca RF (1992) The role of food patches in maintaining high deep-sea diversity: field experiments using hydrodynamically unbiased colonization trays. Limnol Oceanogr 37:1543–1550
Somero GN (1998) Adaptations to cold and depth: contrasts between polar and deep-sea animals In: Pörtner HO, Playle RC (eds) Society for Experimental Biology Seminar Series Vol 66 Cambridge University Press, Cambridge MA, pp 33–57
Tripsanas EK, Bryant WR, Phaneuf BA (2004) Slope-instability processes caused by salt movements in a complex deep-water environment Bryant Canyon area northwest Gulf of Mexico. AAPG Bull 88(6):801–823
Velásquez J, Sánchez JA (2015) Octocoral species assembly and coexistence in Caribbean coral Reefs. PloS One 10(7):e0129609
Wagstaff MC, Howell KL, Bett BJ, Billett DS, Brault S, Stuart CT, Rex MA (2014) β diversity of deep-sea holothurians and asteroids along a bathymetric gradient (NE Atlantic). Mar Ecol Prog Ser 508:177–185
Watling L (2007) A review of the genus Iridogorgia (Octocorallia: Chrysogorgiidae) and its relatives chiefly from the North Atlantic Ocean. J. Mar. Biol. Assoc. UK 87:393–402
Watling L, France SC, Pante E, Simpson A (2011) Biology of deep-water octocorals. Adv Mar Biol 60:41–122
Webb CO (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
Widder EA (2010) Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328(5979):704–708
Acknowledgements
We thank the R/Vs Ron Brown, Seward Johnson, Nancy Foster, Atlantis, ROV Jason II, ROV Seaeye Falcon, HOV Johnson-Sea-Link, and HOV Alvin. Thanks to C. Doughty, R. Falco, and N. Remon for help with DNA extractions. C. Fisher, R. Sanders, T. Shank, J. Brooks, and TDI-Brooks provided support. Particular thanks to A. Freestone for helpful suggestions. O. Breedy, S. Cairns, P. Etnoyer, S. France, S. Herrera, B. Horvath, C. McFadden, K. Moore, J. Thoma, J. Sánchez, L. Watling, and L. van Ofwegen provided taxonomic expertise.
Author contribution statement
AMQ and EEC conceived and designed the study. CEG conducted the morphological trait analyses. AMQ performed the research, analyzed the data, and wrote the article with contributions from CEG and EEC.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
Funding was provided by BOEM and NOAA-OER (BOEM contract #M08PC20038) for the Lophelia II project led by TDI-Brooks International. AMQ was supported by the NOAA Nancy Foster Scholarship Program, Temple University Dissertation Completion Grant, and the Lerner-Gray Fund of Marine Research. CEG is under support from the Fulbright-Colciencias Doctoral Scholarship program.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Joel Trexler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Quattrini, A.M., Gómez, C.E. & Cordes, E.E. Environmental filtering and neutral processes shape octocoral community assembly in the deep sea. Oecologia 183, 221–236 (2017). https://doi.org/10.1007/s00442-016-3765-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3765-4