Metacommunity theory is a conceptual framework addressing the interdependence of local interactions and regional processes, especially when it is difficult to relate community structure and the environment at different spatial scales. To test the applicability of this theory to meiobenthos, 27 deep-sea sediment samples from the Gulf of Mexico were analyzed for meiobenthic and nematode community distribution and structure along with a set of environmental variables. Spatial and temporal heterogeneity in environmental conditions were found among sampling stations, and some variables, such as depth, inorganic carbon, carbon/nitrogen ratio, bottom-water oxygen, and percentage of sand, proved influential on total community abundance. Nematodes were the dominant meiofaunal group and its abundance highly variable among sites and sampling periods. Nematofauna was dominated by bacterivores, which also possessed the highest maturity index. Environmental characteristics showed a significant relation with community structure, not so the dispersal of nematode genera. In light of our findings, we posit that the deep-sea meiobenthos of the Gulf of Mexico may represent a metacommunity following the “species-sorting model.” This inference is based on the different taxonomic structures among sampling stations correlating with environmental differences, in the presence of local niche diversification and limited dispersal.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2
Ansari ZA (2000) Distribution of deep-sea benthos in the proposed mining area of Central Indian Basin. Mar Georesources Geotechnol 18:201–207. https://doi.org/10.1080/10641190009353788
Baguley JG, Montagna PA, Hyde LJ et al (2006) Metazoan meiofauna abundance in relation to environmental variables in the northern Gulf of Mexico deep sea. Deep Sea Res Part I Oceanogr Res Pap 53:1344–1362. https://doi.org/10.1016/j.dsr.2006.05.012
Balsam WL, Beeson JP (2003) Sea-floor sediment distribution in the Gulf of Mexico. Deep Res Part I Oceanogr Res Pap 50:1421–1444. https://doi.org/10.1016/j.dsr.2003.06.001
Bianchelli S, Gambi C, Mea M et al (2013) Nematode diversity patterns at different spatial scales in bathyal sediments of the Mediterranean Sea. Biogeosciences 10:5465–5479. https://doi.org/10.5194/bg-10-5465-2013
Biggs DC, Hu C, Müller-Karger FE (2008) Remotely sensed sea-surface chlorophyll and POC flux at deep Gulf of Mexico benthos sampling stations. Deep Res Part II Top Stud Oceanogr 55:2555–2562. https://doi.org/10.1016/j.dsr2.2008.07.013
Boeckner MJ, Sharma J, Proctor HC (2009) Revisiting the meiofauna paradox: dispersal and colonization of nematodes and other meiofaunal organisms in low- and high-energy environments. Hydrobiologia 624:91–106. https://doi.org/10.1007/s10750-008-9669-5
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19. https://doi.org/10.1007/BF00324627
Bongers T, Alkemade R, Yeates GW (1991) Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the maturity index. Mar Ecol Prog Ser 76:135–142. https://doi.org/10.3354/meps076135
Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251. https://doi.org/10.1016/S0929-1393(98)00123-1
Bouma HA (1972) Distribution of sediments and sedimentary structures in the Gulf of México. In: Rezak R, Henry VJ (eds) Contributions on the geological and geophysical oceanography of the Gulf of Mexico. Gulf Pub. Co., Houston, Tex, p 303
Camus PA, Lima M (2002) Populations, metapopulations, and the open-closed dilemma: the conflict between operational and natural population concepts. Oikos 97:433–438. https://doi.org/10.1034/j.1600-0706.2002.970313.x
Carvalho JC, Cardoso P, Gomes P (2012) Determining the relative roles of species replacement and species richness differences in generating beta-diversity patterns. Glob Ecol Biogeogr 21:760–771. https://doi.org/10.1111/j.1466-8238.2011.00694.x
Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans Biol Sci 345:101–118
Danovaro R, Gambi C, Lampadariou N, Tselepides A (2008) Deep-sea nematode biodiversity in the Mediterranean basin: testing for longitudinal, bathymetric and energetic gradients. Ecography (Cop) 80304020349105. https://doi.org/10.1111/j.2007.0906-7590.05484.x
de Jonge VN, Bouwman LA (1977) A simple density separation technique for quantitative isolation of meiobenthos using the colloidal silica Ludox-TM. Mar Biol 42:143–148. https://doi.org/10.1007/BF00391564
Deming JW, Carpenter SD (2008) Factors influencing benthic bacterial abundance, biomass, and activity on the northern continental margin and deep basin of the Gulf of Mexico. Deep Sea Res Part II Top Stud Oceanogr 55:2597–2606. https://doi.org/10.1016/j.dsr2.2008.07.009
Derycke S, Backeljau T, Moens T (2013) Dispersal and gene flow in free-living marine nematodes. Front Zool 10(1). https://doi.org/10.1186/1742-9994-10-1
Derycke S, Backeljau T, Vlaeminck C et al (2007) Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar Biol 151:1799–1812. https://doi.org/10.1007/s00227-007-0609-0
Derycke S, Fonseca G, Vierstraete A et al (2008) Disentangling taxonomy within the Rhabditis (Pellioditis) marina (Nematoda, Rhabditidae) species complex using molecular and morhological tools. Zool J Linnean Soc 152:1–15. https://doi.org/10.1111/j.1096-3642.2007.00365.x
Dimitriadis C, Koutsoubas D (2011) Functional diversity and species turnover of benthic invertebrates along a local environmental gradient induced by an aquaculture unit: the contribution of species dispersal ability and rarity. Hydrobiologia 670:307–315. https://doi.org/10.1007/s10750-011-0668-6
Ellingsen K (2002) Soft-sediment benthic biodiversity on the continental shelf in relation to environmental variability. Mar Ecol Prog Ser 232:15–27
Escobar-briones E, Signoret M, Hernández M (1999) Variación de la densidad de la infauna macrobéntica en un gradiente batimétrico: Oeste del Golfo de México. Ciencias Mar 25:193–212
Escobar-Briones EG, Díaz C, Legendre P (2008) Meiofaunal community structure of the deep-sea Gulf of Mexico: variability due to the sorting methods. Deep Sea Res Part II Top Stud Oceanogr 55:2627–2633. https://doi.org/10.1016/j.dsr2.2008.07.012
Escobar E, López M, Soto L, Signoret M (1997) Density and biomass of the meiofauna of the upper continental slope in two regions of the Gulf of Mexico. Ciencias Mar 23:463–489
Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784. https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2
Fontana G, Ugland KI, Gray JS et al (2008) Influence of rare species on beta diversity estimates in marine benthic assemblages. J Exp Mar Bio Ecol 366:104–108. https://doi.org/10.1016/j.jembe.2008.07.014
Fraschetti S, Guarnieri G, Gambi C et al (2016) Impact of offshore gas platforms on the structural and functional biodiversity of nematodes. Mar Environ Res 115:56–64. https://doi.org/10.1016/j.marenvres.2016.02.001
Gallucci F, Moens T, Fonseca G (2009) Small-scale spatial patterns of meiobenthos in the Arctic deep sea. Mar Biodivers 39:9–25. https://doi.org/10.1007/s12526-009-0003-x
Gallucci F, Moens T, Vanreusel A, Fonseca G (2008) Active colonisation of disturbed sediments by deep-sea nematodes: evidence for the patch mosaic model. Mar Ecol Prog Ser 367:173–183. https://doi.org/10.3354/meps07537
Gambi C, Danovaro R (2016) Biodiversity and life strategies of deep-sea meiofauna and nematode assemblages in the Whittard Canyon (Celtic margin, NE Atlantic Ocean). Deep Res Part I Oceanogr Res Pap 108:13–22. https://doi.org/10.1016/j.dsr.2015.12.001
Gambi C, Pusceddu A, Benedetti-Cecchi L, Danovaro R (2014) Species richness, species turnover and functional diversity in nematodes of the deep Mediterranean Sea: searching for drivers at different spatial scales. Glob Ecol Biogeogr 23:24–39. https://doi.org/10.1111/geb.12094
Gambi C, Vanreusel A, Danovaro R (2003) Biodiversity of nematode assemblages from deep-sea sediments of the Atacama slope and trench (South Pacific Ocean ). Deep Sea Res Part I Oceanogr Res Pap 50:103/117
Gheskiere T, Hoste E, Vanaverbeke J et al (2004) Horizontal zonation patterns and feeding structure of marine nematode assemblages on a macrotidal, ultra-dissipative sandy beach (De Panne, Belgium). J Sea Res 52:211–226. https://doi.org/10.1016/j.seares.2004.02.001
Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments, Second edn. Springer-Verlag, Berlin
Grimm V, Reise K, Strasser M (2003) Marine metapopulations: a useful concept? Helgol Mar Res 56:222–228. https://doi.org/10.1007/S10152-002-0121-3
Hauquier F, Leliaert F, Rigaux A et al (2017) Distinct genetic differentiation and species diversification within two marine nematodes with different habitat preference in Antarctic sediments. BMC Evol Biol 17:120. https://doi.org/10.1186/s12862-017-0968-1
Huang YB, Chi H (2012) Assessing the application of the jackknife and bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). J Agric For Entomol 61:37–45
Ingels J, Billett DSM, Kiriakoulakis K et al (2011) Structural and functional diversity of Nematoda in relation with environmental variables in the Setúbal and Cascais canyons, western Iberian margin. Deep Sea Res Part II Top Stud Oceanogr 58:2354–2368. https://doi.org/10.1016/j.dsr2.2011.04.002
Ingole BS, Ansari ZA, Rathod V, Rodrigues N (2000) Response of Meiofauna to immediate benthic disturbance in the Central Indian Ocean Basin. Mar Georesources Geotechnol 18:263–272. https://doi.org/10.1080/10641190009353794
Koleff P, Gaston K, Lennon J (2003) Measuring beta diversity for presence–absence data. J Anim Ecol 72:367–382
Leduc D, Rowden A, Bowden D et al (2012) Nematode beta diversity on the continental slope of New Zealand: spatial patterns and environmental drivers. Mar Ecol Prog Ser 454:37–52. https://doi.org/10.3354/meps09690
Leibold MA, Holyoak M, Mouquet N et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x
Logue JB, Mouquet N, Peter H, Hillebrand H (2011) Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol Evol 26:482–491. https://doi.org/10.1016/j.tree.2011.04.009
Martin RG, Bouma AH (1978) Physiography of the Gulf of Mexico. In: Boume AH, Moore GT, Coleman JM (eds) Frameworks, facies and oil-trapping characteristics of the upper continental margin. American Association Petroleum Geologist Studies in Geology, pp 3–19
Mokievskii VO, Udalov AA, Azovskii AI (2007) Quantitative distribution of meiobenthos in deep-water zones of the World Ocean. Oceanology 47:797–813. https://doi.org/10.1134/S0001437007060057
Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17. https://doi.org/10.2307/2332142
Mori AS, Furukawa T, Sasaki T (2013) Response diversity determines the resilience of ecosystems to environmental change. Biol Rev Camb Philos Soc 88:349–364. https://doi.org/10.1111/brv.12004
Naeem S, Duffy JE, Zavaleta E (2012) The functions of biological diversity in an age of extinction. Science 336:1401–1406. https://doi.org/10.1126/science.1215855
Platt H, Warwick R (1983) Freeliving marine nematodes. Part 1: British enoplids. Pictorial key to world genera and notes for the identification of British species. University Press, Cambridge
Platt H, Warwick R (1988) Free-living marine nematodes. Part II: British chromadorids. Brill/Backhuys, for the Linnean Society of London and the Estuarine and Brackish-Water Sciences Association
Rosli N, Leduc D, Rowden AA, Probert PK (2018) Review of recent trends in ecological studies of deep-sea meiofauna, with focus on patterns and processes at small to regional spatial scales. Mar Biodivers 48:13–34. https://doi.org/10.1007/s12526-017-0801-5
Rowe GT, Wei C, Nunnally C et al (2008) Comparative biomass structure and estimated carbon flow in food webs in the deep Gulf of Mexico. Deep Res Part II Top Stud Oceanogr 55:2699–2711. https://doi.org/10.1016/j.dsr2.2008.07.020
Sharma J, Baguley JG, Montagna PA, Rowe GT (2012) Assessment of longitudinal gradients in nematode communities in the deep northern Gulf of Mexico and concordance with benthic taxa. Int J Oceanogr 2012:1–15. https://doi.org/10.1155/2012/903018
Soltwedel T (1997) Meiobenthos distribution pattern in the tropical East Atlantic: indication for fractionated sedimentation of organic matter to the sea floor? Mar Biol 129:747–756
Somerfield P, Warwick R (1996) Meiofauna in marine pollution monitoring programmes. A laboratory manual.
Storch D, Gaston KJ (2004) Untangling ecological complexity on different scales of space and time. Basic Appl Ecol 5:389–400. https://doi.org/10.1016/j.baae.2004.08.001
Stuart CT, Brault S, Rowe GT et al (2017) Nestedness and species replacement along bathymetric gradients in the deep sea reflect productivity: a test with polychaete assemblages in the oligotrophic north-west Gulf of Mexico. J Biogeogr 44:548–555. https://doi.org/10.1111/jbi.12810
Team RC (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://wwwR-project.org/ 2013
Ürkmez D, Sezgin M, Bat L (2014) Use of nematode maturity index for the determination of ecological quality status: a case study from the Black Sea. J Black Sea/Mediterranean Environ 20:96–107
Warwick R, Platt H, Somerfield P (1998) Free-living marine nematodes. Part III. Monhysterids. Synopsis of the British fauna. Cambridge University Press, Cambridge
Wei C-L, Rowe GT, Escobar-Briones E et al (2010) Global patterns and predictions of seafloor biomass using random forests. PLoS One 5:e15323. https://doi.org/10.1371/journal.pone.0015323
Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279–338
Wieser W (1953) Die Beziehung zwischen Mundho¨hlengestalt,Erna¨hrungsweise und Vorkommen bei freilebenden marinen Nematoden. Ark fu¨r Zoolgie 4:439–484
Zeppilli D, Pusceddu A, Trincardi F, Danovaro R (2016) Seafloor heterogeneity influences the biodiversity–ecosystem functioning relationships in the deep sea. Sci Rep 6:26352. https://doi.org/10.1038/srep26352
We are grateful to Vicente Ferreira Bartrina and Ivonne Martínez Mendoza for their hard work collecting deep-sea sediments at sea and for the laboratory assistance (Ivonne), as well as to the crew of R/V Justo Sierra (UNAM) and scientific staff of cruises X1, X2, and X3. We dedicate this contribution to the memory of our friend and colleague Vicente Ferreira Bartrina.
This research was funded by grant 0OE111 from Instituto Nacional de Ecología (INE), Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT), and Consejo Nacional para la Biodiversidad (CONABIO) to the Centro de Investigación Científica y Educación Superior de Ensenada (CICESE) and from the National Council of Science and Technology of Mexico—Mexican Ministry of Energy—Hydrocarbon Trust, project 201441. This research is derived from the first author Ph.D. and the second author M.Sc. research projects. They both benefited from graduate fellowships from Consejo Nacional de Ciencia y Tecnología (CONACYT) to support their graduate programs in marine ecology at CICESE. This is a contribution of the Gulf of Mexico Research Consortium (CIGoM).
Conflict of interest
The authors declare that they have not conflicts of interest.
This article does not contain any studies with animals performed by any of the authors.
Sampling and field studies
This research is based on oceanographic cruises carried out in Mexican waters by Mexican research vessels, which obtained proper clearance from port authorities to operate. No specific permits were necessary to collect environmental or biological samples.
Communicated by M. Schratzberger
About this article
Cite this article
Cisterna-Céliz, J.A., Marcelino-Barros, M., Herguera, J.C. et al. Metacommunity analysis of meiobenthos of deep-sea sediments from the Gulf of Mexico. Mar Biodiv 49, 1217–1231 (2019). https://doi.org/10.1007/s12526-018-0899-0
- Gulf of Mexico
- Deep sea