colonization; community assembly; energy; environmental filtering; functional beta diversity; species beta diversity
Résumé :
[en] Productivity and environmental stress are major drivers of multiple biodiversity facets and faunal community structure. Little is known on their interacting effects on early community assembly processes in the deep sea (>200 m), the largest environment on Earth. However, at hydrothermal vents productivity correlates, at least partially, with environmental stress. Here, we studied the colonization of rock substrata deployed along a deep‐sea hydrothermal vent gradient at four sites with and without direct influence of vent fluids at 1,700‐m depth in the Lucky Strike vent field (Mid‐Atlantic Ridge [MAR]). We examined in detail the composition of faunal communities (>20 μm) established after 2 yr and evaluated species and functional patterns. We expected the stressful hydrothermal activity to (1) limit functional diversity and (2) filter for traits clustering functionally similar species. However, our observations did not support our hypotheses. On the contrary, our results show that hydrothermal activity enhanced functional diversity. Moreover, despite high species diversity, environmental conditions at surrounding sites appear to filter for specific traits, thereby reducing functional richness. In fact, diversity in ecological functions may relax the effect of competition, allowing several species to coexist in high densities in the reduced space of the highly productive vent habitats under direct fluid emissions. We suggest that the high productivity at fluid‐influenced sites supports higher functional diversity and traits that are more energetically expensive. The presence of exclusive species and functional entities led to a high turnover between surrounding sites. As a result, some of these sites contributed more than expected to the total species and functional β diversities. The observed faunal overlap and energy links (exported productivity) suggest that rather than operating as separate entities, habitats with and without influence of hydrothermal fluids may be considered as interconnected entities. Low functional richness and environmental filtering suggest that surrounding areas, with their very heterogeneous species and functional assemblages, may be especially vulnerable to environmental changes related to natural and anthropogenic impacts, including deep‐sea mining.
Centre de recherche :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Disciplines :
Sciences de l’environnement & écologie Zoologie Sciences aquatiques & océanologie
Auteur, co-auteur :
Alfaro-Lucas, Joan M.
Pradillon, Florence
Zeppilli, Daniela
Michel, Loïc ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Département de Biologie, Ecologie et Evolution
Martinez-Arbizu, Pedro
Tanaka, Hayato
Foviaux, Martin
Sarrazin, Jozée
Langue du document :
Anglais
Titre :
High environmental stress and productivity increase functional diversity along a deep‐sea hydrothermal vent gradient
Date de publication/diffusion :
novembre 2020
Titre du périodique :
Ecology
ISSN :
0012-9658
Maison d'édition :
Wiley-Blackwell, Etats-Unis - District de Columbia
Ardyna, M. et al. 2019. Hydrothermal vents trigger massive phytoplankton blooms in the Southern Ocean. Nature Communications 10:2451.
Ashford, O. S., A. J. Kenny, C. R. Froján, M. B. Bonsall, T. Horton, A. Brandt, G. J. Bird, S. Gerken, and A. D. Rogers. 2018. Phylogenetic and functional evidence suggests that deep-ocean ecosystems are highly sensitive to environmental change and direct human disturbance. Proceedings of the Royal Society B 285:20180923.
Baldrighi, E., D. Zeppilli, R. Crespin, P. Chauvaud, F. Pradillon, and J. Sarrazin. 2018. Colonization of synthetic sponges at the deep-sea Lucky Strike hydrothermal vent field (Mid-Atlantic Ridge): a first insight. Marine Biodiversity 48:89–103.
Baselga, A. 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19:134–143.
Bates, A. E., R. W. Lee, V. Tunnicliffe, and M. D. Lamare. 2010. Deep-sea hydrothermal vent animals seek cool fluids in a highly variable thermal environment. Nature Communications 1:1014.
Bell, J. B., W. D. Reid, D. A. Pearce, A. G. Glover, C. J. Sweeting, J. Newton, and C. Woulds. 2017. Hydrothermal activity lowers trophic diversity in Antarctic hydrothermal sediments. Biogeosciences 14:5705–5725.
Botta-Dukát, Z. 2005. Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16:533–540.
Bris, N., M. Yücel, A. Das, S. M. Sievert, P. LokaBharathi, and P. R. Girguis. 2019. Hydrothermal energy transfer and organic carbon production at the deep seafloor. Frontiers in Marine Science 5:531.
Cardinale, B. J. et al. 2012. Biodiversity loss and its impact on humanity. Nature 486:59–67.
Chapman, A. S. et al. 2019. sFDvent: A global trait database for deep-sea hydrothermal-vent fauna. Global Ecology and Biogeography 28:1538–1551.
Chapman, A. S., V. Tunnicliffe, and A. E. Bates. 2018. Both rare and common species make unique contributions to functional diversity in an ecosystem unaffected by human activities. Diversity and Distributions 24:568–578.
Chase, J. M. 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391.
Chase, J. M., and M. A. Leibold. 2002. Spatial scale dictates the productivity–biodiversity relationship. Nature 416:427–430.
Cuvelier, D., J. Beesau, V. N. Ivanenko, D. Zeppilli, P.-M. Sarradin, and J. Sarrazin. 2014. First insights into macro- and meiofaunal colonisation patterns on paired wood/slate substrata at Atlantic deep-sea hydrothermal vents. Deep Sea Research Part I: Oceanographic Research Papers 87:70–81.
Desbruyères, D. et al. 2001. Variations in deep-sea hydrothermal vent communities on the Mid-Atlantic Ridge near the Azores plateau. Deep Sea Research Part I: Oceanographic Research Papers 48:1325–1346.
Didham, R. K., C. H. Watts, and D. A. Norton. 2005. Are systems with strong underlying abiotic regimes more likely to exhibit alternative stable states? Oikos 110:409–416.
Dray, S.et al. 2019. Adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.3-4. https://CRAN.R-project.org/package=adespatial
Erickson, K. L., S. A. Macko, and C. L. Dover. 2009. Evidence for a chemoautotrophically based food web at inactive hydrothermal vents (Manus Basin). Deep Sea Research Part II: Topical Studies in Oceanography 56:1577–1585.
Fabricius, K., G. De'ath, S. Noonan, and S. Uthicke. 2014. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proceedings of the Royal Society B 281:20132479
Garrard, S. L., C. M. Gambi, B. M. Scipione, F. P. Patti, M. Lorenti, V. Zupo, D. M. Paterson, and C. M. Buia. 2014. Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. Journal of Experimental Marine Biology and Ecology 461:31–38.
Gollner, S., B. Govenar, P. Arbizu, S. Mills, N. Bris, M. Weinbauer, T. M. Shank, and M. Bright. 2015a. Differences in recovery between deep-sea hydrothermal vent and vent-proximate communities after a volcanic eruption. Deep Sea Research Part I: Oceanographic Research Papers 106:167–182.
Gollner, S., B. Govenar, C. R. Fisher, and M. Bright. 2015b. Size matters at deep-sea hydrothermal vents: different diversity and habitat fidelity patterns of meio- and macrofauna. Marine Ecology Progress Series 520:57–66.
Gollner, S., B. Riemer, P. Arbizu, N. Bris, and M. Bright. 2010. Diversity of meiofauna from the 9°50′N East Pacific Rise across a gradient of hydrothermal fluid emissions. PLoS One 5:e12321.
Govenar, B. 2010. Shaping vent and seep communities: habitat provision and modification by foundation species. Pages 403–432 in S. Kiel, editor. The vent and seep biota, aspects from microbes to ecosystems. Topics in Geobiology, Vol. 33. Springer, Berlin, Germany.
Govenar, B. 2012. Energy transfer through food webs at hydrothermal vents: linking the lithosphere to the biosphere. Oceanography 25:246–255.
Govenar, B., L. N. Bris, S. Gollner, J. Glanville, A. Aperghis, S. Hourdez, and C. Fisher. 2005. Epifaunal community structure associated with Riftia pachyptila aggregations in chemically different hydrothermal vent habitats. Marine Ecology Progress Series 305:67–77.
Hall-Spencer, J. M., R. Rodolfo-Metalpa, S. Martin, E. Ransome, M. Fine, S. M. Turner, S. J. Rowley, D. Tedesco, and M.-C. Buia. 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96.
Johnson, K. S., Childress, J. J., Beehler, C. L., and Sakamoto, C. M. 1994. Biogeochemistry of hydrothermal vent mussel communities: the deep-sea analogue to the intertidal zone. Deep Sea Research Part I: Oceanographic Research Papers 41(7):993 –1011.
Johnson, K. S., Childress, J. J., Hessler, R. R., Sakamoto-Arnold, C. M., and Beehler, C. L. 1988. Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep Sea Research Part A. Oceanographic Research Papers 35(10-11):1723 –1744.
Josse, J., J. Pagès, and F. Husson. 2008. Testing the significance of the RV coefficient. Computational Statistics & Data Analysis 53:82–91.
Kroeker, K. J., F. Micheli, M. C. Gambi, and T. R. Martz. 2011. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proceedings of the National Academy of Sciences of the United States of America 108:14515–14520.
Laliberté, E., and P. Legendre. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305.
Lamanna, C. et al. 2014. Functional trait space and the latitudinal diversity gradient. Proceedings of the National Academy of Sciences of the United States of America 111:13745–13750.
Lê, S., J. Josse, and F. Husson. 2008. FactoMineR: An R package for multivariate analysis. Journal of Statistical Software 25:1–18.
Lee, R., and J. Childress. 1996. Inorganic N assimilation and ammonium pools in a deep-sea mussel containing methanotrophic endosymbionts. Biological Bulletin 190:373–384.
Legendre, P. 2014. Interpreting the replacement and richness difference components of beta diversity. Global Ecology and Biogeography 23:1324–1334.
Legendre, P., and M. Cáceres. 2013. Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecology Letters 16:951–963.
Levin, L. A. et al. 2016. Hydrothermal vents and methane seeps: rethinking the sphere of influence. Frontiers in Marine Science 3:72.
Luther, G. W., III, T. F. Rozan, M. Taillefert, D. B. Nuzzio, C. Meo, T. M. Shank, R. A. Lutz, and C. S. Cary. 2001. Chemical speciation drives hydrothermal vent ecology. Nature 410:813.
Macheriotou, L., A. Rigaux, S. Derycke, and A. Vanreusel. 2020. Phylogenetic clustering and rarity imply risk of local species extinction in prospective deep-sea mining areas of the Clarion–Clipperton Fracture Zone. Proceedings of the Royal Society B 287:20192666
Mayfield, M. M., and J. M. Levine. 2010. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecology Letters 13:1085–1093.
McClain, C. R., C. Nunnally, A. S. Chapman, and J. P. Barry. 2018. Energetic increases lead to niche packing in deep-sea wood falls. Biology Letters 14:20180294.
McClain, C. R., and M. A. Rex. 2015. Toward a conceptual understanding of β-diversity in the deep-sea benthos. Annual Review of Ecology, Evolution, and Systematics 46:623–642.
McClain, C. R., and T. A. Schlacher. 2015. On some hypotheses of diversity of animal life at great depths on the sea floor. Marine Ecology 36:849–872.
McGill, B. J., B. J. Enquist, E. Weiher, and M. Westoby. 2006. Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21:178–185.
Micheli, F., C. H. Peterson, L. S. Mullineaux, C. R. Fisher, S. W. Mills, G. Sancho, G. A. Johnson, and H. S. Lenihan. 2002. Predation structures communities at deep-sea hydrothermal vents. Ecological Monographs 72:365–382.
Mittelbach, G. G., C. F. Steiner, S. M. Scheiner, K. L. Gross, H. L. Reynolds, R. B. Waide, M. R. Willig, S. I. Dodson, and L. Gough. 2001. What is the observed relationship between species richness and productivity? Ecology 82:2381–2396.
Mouchet, M. A., S. Villéger, N. W. Mason, and D. Mouillot. 2010. Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Functional Ecology 24:867–876.
Mouillot, D., N. Graham, S. Villéger, N. Mason, and D. R. Bellwood. 2013. A functional approach reveals community responses to disturbances. Trends in Ecology & Evolution 28:167–177.
Mullineaux, L. S., C. H. Peterson, F. Micheli, and S. W. Mills. 2003. Successional mechanism varies along a gradient in hydrothermal fluid flux at deep-sea vents. Ecological Monographs 73:523–542.
Oksanen, J., et al. 2019. vegan: community ecology package. R package version 2.5-4. https://CRAN.R-project.org/package=vegan
Plum, C., F. Pradillon, Y. Fujiwara, and J. Sarrazin. 2017. Copepod colonization of organic and inorganic substrata at a deep-sea hydrothermal vent site on the Mid-Atlantic Ridge. Deep Sea Research Part II: Topical Studies in Oceanography 137:335–348.
Portail, M., Brandily, C., Cathalot, C., Colaço, A., Gélinas, Y., Husson, B., Sarradin, P.-M., Sarrazin, J. 2018. Food-web complexity across hydrothermal vents on the Azores triple junction. Deep Sea Research Part I: Oceanographic Research Papers 131:101–120.
Post, D. M. 2002. The long and short of food-chain length. Trends in Ecology & Evolution 17:269–277.
Quattrini, A. M., C. E. Gómez, and E. E. Cordes. 2017. Environmental filtering and neutral processes shape octocoral community assembly in the deep sea. Oecologia 183:221–236.
R Development Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Reid, W. D., C. J. Sweeting, B. D. Wigham, K. Zwirglmaier, J. A. Hawkes, R. A. McGill, K. Linse, and N. V. Polunin. 2013. Spatial differences in East Scotia ridge hydrothermal vent food webs: influences of chemistry, microbiology and predation on trophodynamics. PLoS One 8:e65553.
Robert, P., and Y. Escoufier. 1976. A unifying tool for linear multivariate statistical methods: the RV-coefficient. Journal of the Royal Statistical Society C 25:257–265.
Ruhl, H. A., J. A. Ellena, and K. L. Smith. 2008. Connections between climate, food limitation, and carbon cycling in abyssal sediment communities. Proceedings of the National Academy of Sciences of the United States of America 105:17006–17011.
Ruhl, H. A., and K. L. Smith. 2004. Shifts in deep-sea community structure linked to climate and food supply. Science 305:513–515.
Sarradin, P.-M., M. Waeles, S. Bernagout, C. Gall, J. Sarrazin, and R. Riso. 2009. Speciation of dissolved copper within an active hydrothermal edifice on the Lucky Strike vent field (MAR, 37°N). Science of the Total Environment 407:869–878.
Sarrazin, J., P. Legendre, F. de Busserolles, M.-C. Fabri, K. Guilini, V. N. Ivanenko, M. Morineaux, A. Vanreusel, and P.-M. Sarradin. 2015. Biodiversity patterns, environmental drivers and indicator species on a high-temperature hydrothermal edifice, Mid-Atlantic Ridge. Deep Sea Research Part II: Topical Studies in Oceanography 121:177–192.
Sarrazin, J., V. Robigou, K. Juniper, and J. Delaney. 1997. Biological and geological dynamics over four years on a high-temperature sulfide structure at the Juan de Fuca Ridge hydrothermal observatory. Marine Ecology Progress Series 13:5–24.
Sen, A., S. Kim, A. J. Miller, K. J. Hovey, S. Hourdez, G. W. Luther, and C. R. Fisher. 2016. Peripheral communities of the Eastern Lau Spreading Center and Valu Fa Ridge: community composition, temporal change and comparison to near-vent communities. Marine Ecology 37:599–617.
Shank, T. M., D. J. Fornari, K. L. V. Damm, M. D. Lilley, R. M. Haymon, and R. A. Lutz. 1998. Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50′N, East Pacific Rise). Deep Sea Research Part II: Topical Studies in Oceanography 45:465–515.
Sievert, S., and C. Vetriani. 2012. Chemoautotrophy at deep-sea vents: past, present, and future. Oceanography 25:218–233.
Snelgrove, P., and Smith, C. R. 2002. A riot of species in an environmental calm: the paradox of the species-rich deep-sea floor. Pages 311–342 in R. N. Gibson, M. Barnes, and R. J. A. Atkinson, editors. Oceanography and marine biology, An annual review 40. CRC Press, London.
Tarasov, V. G., A. V. Gebruk, A. N. Mironov, and L. I. Moskalev. 2005. Deep-sea and shallow-water hydrothermal vent communities: Two different phenomena? Chemical Geology 224:5–39.
Teixidó, N., M. Gambi, V. Parravacini, K. Kroeker, F. Micheli, S. Villéger, and E. Ballesteros. 2018. Functional biodiversity loss along natural CO2 gradients. Nature Communications 9:5149.
Van Dover, C. L. et al. 2018. Scientific rationale and international obligations for protection of active hydrothermal vent ecosystems from deep-sea mining. Marine Policy 90:20–28.
Van Dover, C. L. 2019. Inactive sulfide ecosystems in the deep sea: a review. Frontiers in Marine Science 6:461.
Van Dover, C. V., and J. Trask. 2000. Diversity at deep-sea hydrothermal vent and intertidal mussel beds. Marine Ecology Progress Series 195:169–178.
Vanreusel, A., A. Groote, S. Gollner, and M. Bright. 2010. Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: a review. PLoS ONE 5:e12449.
Vizzini, S., B. Martínez-Crego, C. Andolina, A. Massa-Gallucci, S. D. Connell, and M. C. Gambi. 2017. Ocean acidification as a driver of community simplification via the collapse of higher-order and rise of lower-order consumers. Scientific Reports 7:4018.
Weiher, E., D. Freund, T. Bunton, A. Stefanski, T. Lee, and S. Bentivenga. 2011. Advances, challenges and a developing synthesis of ecological community assembly theory. Philosophical Transactions of the Royal Society B 366:2403–2413.
Zeppilli, D. et al. 2018. Characteristics of meiofauna in extreme marine ecosystems: a review. Marine Biodiversity 48:35–71.
Zeppilli, D., A. Vanreusel, F. Pradillon, S. Fuchs, P. Mandon, T. James, and J. Sarrazin. 2015. Rapid colonisation by nematodes on organic and inorganic substrata deployed at the deep-sea Lucky Strike hydrothermal vent field (Mid-Atlantic Ridge). Marine Biodiversity 45:489–504.
