Advertisement

Spatial scale influences diversity patterns of free-living nematode assemblages in coral degradation zones from the Caribbean Sea

  • José Andrés Pérez-GarcíaEmail author
  • Diana Marzo-Pérez
  • Maickel Armenteros
Original Paper
  • 19 Downloads

Abstract

Diversity of marine nematodes in coral degradation zones (CDZs) has been poorly studied despite of its contribution to global coral reef diversity; additionally, effects of spatial scales on nematode assemblages are also largely unknown. To fill this gap, we studied the marine nematode assemblages in CDZs from two coral reefs in the Caribbean Sea to describe the diversity, test the effects of spatial scales, and explore if there were adaptive biological trait combinations. We sampled 2 reefs (Ballenatos and Punta Francés), 6 sites, and 20 dead coral piles in a fully nested design identifying the nematodes to species level. CDZs harbored a diverse nematode assemblage of 112 species with large spatial turnover. Differences between reefs in abundance and species density were probably related to differential energy availability, with Punta Francés receiving larger input of material and energy from land. The spatial scale had a significant effect on the species richness, whereas differences in species composition were mainly driven by the scale at which ecological drivers operated (10−1 m for interstitial heterogeneity vs. 105 m for dispersal). Geographical distances in the order of 180 km likely constituted barriers to nematode dispersal and as such promoted assemblage dissimilarity. Our evidence indicated that a particular set of biological traits favored the adaptation of nematodes to CDZs, namely a distinctive combination of armed stoma, ornamented cuticle, and conical tail.

Keywords

Nematodes Coral reef Species richness Species composition Biological traits Dispersal EiE hypothesis 

Notes

Acknowledgments

We appreciate the comments by two anonymous referees that improved the manuscript. We thank Idea Wild fund for providing equipment used during this research.

Funding

This study was partially funded by The Ocean Foundation though the Proyecto 3 Golfos Initiative and by Dalio Family Foundation through a grant to A Apprill and A Santoro.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Data availability

Data generated or analyzed during this study are included in this published article and its supplementary information files.

Supplementary material

12526_2019_945_MOESM1_ESM.pdf (107 kb)
ESM 1 (PDF 107 kb)

References

  1. Alongi DM (1986) Population structure and trophic composition of the free-living nematodes inhabiting carbonate sands of Davies Reef, Great Barrier Reef, Australia. Aust J Mar Freshw Res 37:609–619CrossRefGoogle Scholar
  2. Alves AS, Veríssimo H, Costa MJ, Marques JC (2014) Taxonomic resolution and biological traits analysis (BTA) approaches in estuarine free-living nematodes. Estuar Coast Shelf Sci 138:69–78CrossRefGoogle Scholar
  3. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. In: PRIMER-E. Plymouth, UKGoogle Scholar
  4. Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ et al (2011) Navigating the multiple meanings of β-diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28CrossRefGoogle Scholar
  5. Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, Bamber R et al (2012) The magnitude of global marine species diversity. Curr Biol 22:1–14CrossRefGoogle Scholar
  6. Armenteros M, Ruiz-Abierno A, Fernández-Garcés R, Pérez-García JA, Díaz-Asencio L, Vincx M, Decraemer W (2009a) Biodiversity patterns of free-living marine nematodes in a tropical bay: Cienfuegos, Caribbean Sea. Estuar Coast Shelf Sci 85:179–189CrossRefGoogle Scholar
  7. Armenteros M, Vincx M, Decraemer W (2009b) Cienfuegia gen. nov. (Xyalidae) and Pseudoterschellingia gen. nov. (Linhomoeidae), two new genera of free-living marine nematodes from the Caribbean Sea. J Nat Hist 43:1067–1081CrossRefGoogle Scholar
  8. Armenteros M, Ruiz-Abierno A, Sosa Y, Pérez-García JA (2012) Habitat heterogeneity effects on macro-and meiofauna (especially nematodes) in Punta Francés coral reef (SW Cuban Archipelago). Rev Invest Mar 32:50–61Google Scholar
  9. Armenteros M, Saladrigas D, González-Casuso L, Estevez ED, Kowalewski M (2018) The role of habitat selection on the diversity of macrobenthic communities in three gulfs of the Cuban Archipelago. Bull Mar Sci 94:249–268Google Scholar
  10. Benedetti-Cecchi L, Iken K, Konar B, Cruz-Motta JJ, Knowlton N, Pohle G, Castelli A et al (2010) Spatial relationships between polychaete assemblages and environmental variables over broad geographical scales. PLoS One 5:e2946CrossRefGoogle Scholar
  11. Bik HM, Thomas WK, Lunt DH, Lambshead PJD (2010) Low endemism, continued deep-shallow interchanges, and evidence for cosmopolitan distributions in free-living marine nematodes (order Enoplida). BMC Evol Biol 10:389CrossRefGoogle Scholar
  12. Boström C, Törnroos A, Bonsdorff E (2010) Invertebrate dispersal and habitat heterogeneity: expression of biological traits in a seagrass landscape. J Exp Mar Biol Ecol 390:106–117CrossRefGoogle Scholar
  13. Boucher G (1997) Structure and biodiversity of nematode assemblages in the SW Lagoon of New Caledonia. Coral Reefs 16:177–186CrossRefGoogle Scholar
  14. Callens M, Gheerardyn H, Ndaro SGM, De Troch M, Vanreusel A (2012) Harpacticoid copepod colonization of coral fragments in a tropical reef lagoon (Zanzibar, Tanzania). J Mar Biol Assoc UK 92:1535–1545CrossRefGoogle Scholar
  15. Cao Y, Williams DD, Williams NE (1998) How important are rare species in aquatic community ecology and bioassessment? Limnol Oceanogr 43:1403–1409CrossRefGoogle Scholar
  16. Clarke KR, Gorley RN (2006) Primer v6: User Manual/Tutorial. Primer-E, Ltd, PlymouthGoogle Scholar
  17. Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. http://purl.oclc.org/estimates Google Scholar
  18. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond Ser B Biol Sci 345:101–118CrossRefGoogle Scholar
  19. Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao C-X, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21CrossRefGoogle Scholar
  20. Côté IM, Knowlton N (2014) Coral reef ecosystems. A decade of discoveries. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine community ecology and conservation. Sinauer, Sunderland, pp 299–314Google Scholar
  21. Crist TO, Veech JA (2006) Additive partitioning of rarefaction curves and species–area relationships: unifying α-, β- and γ-diversity with sample size and habitat area. Ecol Lett 9:923–932CrossRefGoogle Scholar
  22. Danovaro R, Bianchelli S, Gambi MC, Mea M, Zeppilli D (2009) α-, β-, γ-, δ- and ε-diversity of deep-sea nematodes in canyons and open slopes of Northeast Atlantic and Mediterranean margins. Mar Ecol Progr Ser 396:197–209CrossRefGoogle Scholar
  23. De Jesús-Navarrete A (2007) Nematodos de los arrecifes de Isla Mujeres y Banco Chinchorro, Quintana Roo, México. Rev Biol Mar Oceanogr 42:193–200CrossRefGoogle Scholar
  24. De Troch M, Raes M, Muthumbi A, Gheerardyn H, Vanreusel A (2008) Spatial diversity of nematode and copepod genera of the coral degradation zone along the Kenyan coast, including a test for the use ofhigher-taxon surrogacy. African J Mar Sci 30:25–33CrossRefGoogle Scholar
  25. Decraemer W, Gourbault NE, Helléouet MN (2001) Cosmopolitanism among nematodes: examples from Epsilonematidae. Vie Milieu 51:11–19Google Scholar
  26. Decraemer W, Coomans A, Baldwin JG (2013) Morphology of nematoda. In: Schmidt-Rhaesa A (ed) Handbook of Zoology. Gastrotricha, Cycloneuralia and Gnathifera. Volumen 2. Nematoda. De Gruyter, Göttingen, Germany, pp 1–59Google Scholar
  27. Flach PZS, Ozorio CP, Melo AS (2012) Alpha and beta components of diversity of freshwater nematodes at different spatial scales in subtropical coastal lakes. Fundam Appl Limnol 108:249–258CrossRefGoogle Scholar
  28. Fontaneto D, Barraclough TG, Chen K, Ricci C, Herniou EA (2008) Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread. Mol Ecol 17:3136–3146CrossRefGoogle Scholar
  29. Gaston KJ, Spicer JI (2004) Biodiversity. An introduction (2nd ed.). Blackwell, HobokenGoogle Scholar
  30. Giere O (2009) Meiobenthology. The microscopic motile fauna of aquatic sediments, 2nd edn. Springer, BerlinGoogle Scholar
  31. Gobin JF (2007) Free-living marine nematodes of hard bottom substrates in Trinidad and Tobago, West Indies. Bull Mar Sci 81:73–84Google Scholar
  32. Gotelli NJ, Colwell RK (2011) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity. Frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54Google Scholar
  33. Hodda M (1990) Variation in estuarine littoral nematode populations over three spatial scales. Estuar Coast Shelf Sci 30:325–340CrossRefGoogle Scholar
  34. Izsak C, Price ARG (2001) Measuring beta-diversity using a taxonomic similarity index, and its relation to spatial scale. Mar Ecol Progr Ser 215:69–77CrossRefGoogle Scholar
  35. Laurie H, Perrier E (2011) Beyond species area curves: application of a scale-free measure for spatial variability of species richness. Oikos 120:966–978CrossRefGoogle Scholar
  36. Li J, Vincx M, Herman PMJ, Heip C (1997) Monitoring meiobenthos using cm-, m- and km-scales in the Southern Bight of the North Sea. Mar Environ Res 43:265–278CrossRefGoogle Scholar
  37. Liao J-X, Yeh H-M, Mok H-K (2015) Meiofaunal communities in a tropical seagrass bed and adjacent unvegetated sediments with note on sufficient sample size for determining local diversity indices. Zool Stud 54:14CrossRefGoogle Scholar
  38. Magurran AE (2004) Measuring biological diversity. Blackwell, OxfordGoogle Scholar
  39. Moens T, Braeckman U, Derycke S, Fonseca G, Gallucci F, Gingold R, Guilini K et al. (2013) Ecology of free-living marine nematodes. In: Schmidt-Rhaesa A (ed) Handbook of Zoology. Gastrotricha, Cycloneuralia and Gnathifera. Volumen 2: Nematoda. De Gruyter, Göttingen, Germany, pp 109–152Google Scholar
  40. Mokievsky V, Azovsky AI (2002) Re-evaluation of species diversity patterns of free-living marine nematodes. Mar Ecol Progr Ser 238:101–108CrossRefGoogle Scholar
  41. Pérez-García JA, Ruiz-Abierno A, Armenteros M (2015) Does morphology of host marine macroalgae drive the ecological structure of epiphytic meiofauna? J Mar Biol Oceanogr 4:1–7CrossRefGoogle Scholar
  42. Platt HM, Warwick RM (1983) Free-living marine nematodes. Part I. British Enoplids. In: Synopses of the British Fauna (New Series), vol 28. The Linnean Society of London and The Estuarine and brackish-Water Sciences Association, CambridgeGoogle Scholar
  43. Platt HM, Warwick RM (1988) Free-Living Marine Nematodes. Part II. British Chromadorids. Vol. 38. 40 vols. In: Synopses of the British Fauna (New Series). The Linnean Society of London and The Estuarine and Brackish-water Sciences Association, LeidenGoogle Scholar
  44. Raes M, De Troch M, Ndaro SGM, Muthumbi A, Guilini K, Vanreusel A (2007) The structuring role of microhabitat type in coral degradation zones: a case study with marine nematodes from Kenya and Zanzibar. Coral Reefs 26:113–126CrossRefGoogle Scholar
  45. Raes M, Decraemer W, Vanreusel A (2008) Walking with worms: coral-associated epifaunal nematodes. J Biogeogr 35:2207–2022CrossRefGoogle Scholar
  46. Rosindell J, Cornell SJ (2013) Universal scaling of species-abundance distributions across multiple scales. Oikos 122:1101–1111CrossRefGoogle Scholar
  47. Ruiz-Abierno A, Armenteros M (2017) Coral reef habitats strongly influence the diversity of macro and meiobenthos in the Caribbean. Mar Biodivers 47:101–111CrossRefGoogle Scholar
  48. Sandulli R, Semprucci F, Balsamo M (2014) Taxonomic and functional biodiversity variations of meiobenthic and nematode assemblages across an extreme environment: a study case in a Blue Hole Cave. Italian J Zool 81:508–516CrossRefGoogle Scholar
  49. Schratzberger M, Warr K, Rogers SI (2007) Functional diversity of nematode communities in the southwestern North Sea. Mar Environ Res 63:368–389CrossRefGoogle Scholar
  50. Semprucci F, Colantoni P, Baldelli G, Rocchi M, Balsamo M (2010) The distribution of meiofauna on back-reef sandy platforms in the Maldives (Indian Ocean). Mar Ecol 31:592–607CrossRefGoogle Scholar
  51. Semprucci F, Colantoni P, Baldelli G, Sbrocca C, Rocchi M, Balsamo M (2013) Meiofauna associated with coral sediments in the Maldivian subtidal habitats (Indian Ocean). Mar Biodivers 43:189–198CrossRefGoogle Scholar
  52. Semprucci F, Colantoni P, Sbrocca C, Baldelli G, Balsamo M (2014) Spatial patterns of distribution of meiofaunal and nematode assemblages in the Huvadhoo Lagoon (Maldives, Indian Ocean). J Mar Biol Assoc UK 94:1377–1385CrossRefGoogle Scholar
  53. Semprucci F, Frontalini F, Losi V, Armynot du Châtelet E, Cesaroni L, Sandulli R, Coccioni R, Balsamo M (2018a) Biodiversity and distribution of the meiofaunal community in the reef slopes of the Maldivian archipelago (Indian Ocean). Mar Environ Res 139:19–26CrossRefGoogle Scholar
  54. Semprucci F, Cesaroni L, Guidi L, Balsamo M (2018b) Do the morphological and functional traits of free-living marine nematodes mirror taxonomical diversity? Mar Environ Res 135:114–122CrossRefGoogle Scholar
  55. Smythe AB (2015) Evolution of feeding structures in the marine nematode order Enoplida. Integr Comp Biol:1–13Google Scholar
  56. Storch D, Bohdalkova E, Okie J (2018) The more-individuals hypothesis revisited: the role of community abundance in species richness regulation and the productivity–diversity relationship. Ecol Lett 21:920–937CrossRefGoogle Scholar
  57. Tarjan AC (1980) An illustrate guide to the marine nematodes. Institute of Food and Agricultural Sciences, University of Florida, GainesvilleGoogle Scholar
  58. Tchesunov A (2013) Order Desmodorida De Coninck, 1965. In: Schmidt-Rhaesa A (ed) Handbook of zoology. Gastrotricha, Cycloneuralia and Gnathifera. Volumen 2: Nematoda. De Gruyter, Göttingen, Germany, pp 399–434Google Scholar
  59. Thistle D, Lambshead PJD, Sherman KM (1995) Nematode tail-shape groups respond to environmental differences in the deep sea. Vie Milieu 45:107–115Google Scholar
  60. Vincx M (1996) Meiofauna in marine and freshwater sediments. In: Hall GS (ed) Methods for the examination of organismal diversity in soils and sediments. CAB International, Wallingford, pp 187–195Google Scholar
  61. Warwick RM, Platt HM, Somerfield PJ (1998) Free-living marine nematodes. Part III. Monhysterids. In: Synopses of the British Fauna (New Series), vol 53. The Linnean Society of London and The Estuarine and Coastal Sciences Association, ShrewsburyGoogle Scholar
  62. Whittaker RJ, Willis KJ, Field R (2001) Scale and species richness: towards a general, hierarchical theory of species diversity. J Biogeogr 28:453–470CrossRefGoogle Scholar
  63. Wiens JJ (2011) The causes of species richness patterns across space, time, and clades and the role of "ecological limits". Q Rev Biol 86:75–96CrossRefGoogle Scholar
  64. Wieser W (1953) Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Ark f Zool 4(26):439–484Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung 2019

Authors and Affiliations

  1. 1.Centro de Investigaciones MarinasUniversidad de La HabanaHabanaCuba

Personalised recommendations