Advertisement

Marine Biology

, 163:102 | Cite as

Spatiotemporal variation and sediment retention effects on nematode communities associated with Halimeda opuntia (Linnaeus) Lamouroux (1816) and Sargassum polyceratium Montagne (1837) seaweeds in a tropical phytal ecosystem

  • Daniel A. S. De Oliveira
  • Sofie Derycke
  • Clélia M. C. Da Rocha
  • Débora F. Barbosa
  • Wilfrida Decraemer
  • Giovanni A. P. Dos Santos
Original paper

Abstract

Nematodes play an important role in ecological processes and are one of the most abundant meiofaunal organisms associated with seaweeds. Yet, knowledge on seaweed bed ecosystems is limited. Nematodes associated with Sargassum polyceratium and Halimeda opuntia were compared in two transects, 80 m apart and parallel to the beach line in Cupe Beach, Brazil. The temporal variation during the dry and rainy seasons and the effect of sediment retention by the seaweed on nematode density and composition were investigated. The differences in nematode communities between the two seasons were mainly caused by the increase in density of the most abundant genera in the rainy season. A significant difference was observed between the nematode communities of the two transects for H. opuntia. The nematode communities of both seaweed species did not differ significantly in the same transect. The genus Euchromadora was dominant in both seaweed species. The amount of sediment retained by the seaweeds did not affect the overall nematode density. However, it was positively correlated with the density of Draconema and Euchromadora in both seaweeds, and both genera were exclusively found associated with seaweeds. This result opposes the idea that the more sediment retained by the seaweed, the higher the nematode overall density and the higher the number of nematodes originally coming from the sediment.

Keywords

Macrophyte Meiofauna Brown Seaweed Nematode Community Halimeda 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank Prof. Dr. Carl Vangestel for the statistical advice, Prof. Dr. Verônica da Fonsêca-Genevois (in memorian) for the incentive and for sharing her experience, The Federal Rural University of Pernambuco (UFRPE) for the logistic support and the Flemish Interuniversity Council—University Development Cooperation (VLIR-UOS) for the grant and financing of the research.

References

  1. Abebe E, Traunspurger W, Andrássy I (2007) Freshwater nematodes: ecology and taxonomy, 1st edn. Cabi Publishing, OxfordshireGoogle Scholar
  2. Alves AS, Caetano A, Costa JL, Costa MJ, Marques JC (2015) Estuarine intertidal meiofauna and nematode communities as indicator of ecosystem’s recovery following mitigation measures. Ecol Indic 54:184–196. doi: 10.1016/j.ecolind.2015.02.013 CrossRefGoogle Scholar
  3. 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(1):50–61Google Scholar
  4. Arroyo NL, Maldonado M, Pérez-Portela R, Benito J (2004) Distribution patterns of meiofauna associated with a sublittoral Laminaria bed in the Cantabrian Sea (north-eastern Atlantic). Mar Biol 144:231–242. doi: 10.1007/s00227-003-1191-8 CrossRefGoogle Scholar
  5. Arroyo NL, Aarnio K, Bonsdorff E (2006) Drifting algae as a means of re-colonizing defaunated sediments in the Baltic Sea. A short-term microcosm study. Hydrobiologia 554:83–95. doi: 10.1007/s10750-005-1008-5 CrossRefGoogle Scholar
  6. Baer J, Stengel DB (2010) Variability in growth, development and reproduction of the non-native seaweed Sargassum muticum (Phaeophyceae) on the Irish west coast. Estuar Coast Shelf S 90:185–194. doi: 10.1016/j.ecss.2010.08.011 CrossRefGoogle Scholar
  7. Bell SS, Walters K, Kern JC (1984) Meiofauna from seagrass habitats: a review and prospectus for future research. Estuaries 7(4):331–338. doi: 10.2307/1351617 CrossRefGoogle Scholar
  8. Brewer DT, Blaber SJM, Salini JP, Farmer MJ (1994) Feeding ecology of predatory fishes from Groote Eylandt in the Gulf of Carpentaria, Australia, with special reference to predation on Penaid prawns. Estuar Coast Shelf S40:577–600. doi: 10.1006/ecss.1995.0039 Google Scholar
  9. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  10. Coull BC, Vernberg WB (1975) Reproductive periodicity of meiobenthic copepods: seasonal or continuous? Mar Biol 32(3):289–293CrossRefGoogle Scholar
  11. Da Rocha CMC, Venekey V, Bezerra TNC, Souza JRB (2006) Phytal marine nematode assemblages and their relation with the macrophytes structural complexity in a Brazilian tropical rocky beach. Hydrobiologia 553:219–230. doi: 10.1007/s10750-005-0923-9 CrossRefGoogle Scholar
  12. De Grisse AT (1969) Redescription ou modification de quelques techniques utilisés dans l’ étude des nématodes phytoparasitaires. Meded. Rijksfakulteit Landbouwwetenschappen Gent 34:251–369Google Scholar
  13. De Oliveira DAS, Dos Santos GAP, Derycke S, Moens T, Decraemer W (2014) Biodiversity and connectivity of marine nematodes associated with algae from two tropical beaches. J Nematol 46(2):152Google Scholar
  14. De Troch M, Gurdebeke S, Fiers F, Vincx M (2001) Zonation and structuring factors of meiofauna communities in a tropical seagrass bed (Gazi Bay, Kenya). J Sea Res 45:45–61. doi: 10.1016/S1385-1101(00)00055-1 CrossRefGoogle Scholar
  15. Derycke S, Vynckt RV, Vanaverbeke J, Vincx M, Moens T (2007) Colonization patterns of Nematoda on decomposing algae in the estuarine environment: community assembly and genetic structure of the dominant species Pellioditis marina. Limnol Oceanogr 52(3):992–1001. doi: 10.4319/lo.2007.52.3.0992 CrossRefGoogle Scholar
  16. Dominguez JML, Bittencourt ACSP, Martin L (1992) Controls on quaternary coastal evolution of the east-northeastern coast Brazil: roles off sea-level history, trade winds and climate. Sediment Geo l80:213–232CrossRefGoogle Scholar
  17. Ferreira Júnior AV (2005) Mapeamento da Zona Costeira Protegida por Arenitos de Praia (Beachrocks) em Anísia Floresta—RN. Master thesis, Federal University of Rio Grande do norteGoogle Scholar
  18. Ferreira CEL, Gonçalves JEA, Coutinho R (2000) Communities structure of fishes and habitat complexity on a tropical rocky shore. Environ Biol Fish 61:353–369CrossRefGoogle Scholar
  19. Fonsêca MS, Calahan JA (1992) A preliminary evaluation of wave attenuation by four species of seagrass. Estuar Coast Shelf S35:565–576. doi: 10.1016/S0272-7714(05)80039-3 CrossRefGoogle Scholar
  20. Frame K, Hunt G, Roy K (2007) Intertidal meiofaunal biodiversity with respect to different algal habitats: a test using phytal ostracodes from Southern California. Hydrobiologia 586(1):331–342. doi: 10.1007/s10750-007-0707-5 CrossRefGoogle Scholar
  21. Gee JM, Warwick RM (1994a) Body-size distribution in a marine metazoan community and fractal dimensions of macroalgae. J Exp Mar Biol Ecol 178:247–259. doi: 10.1016/0022-0981(94)90039-6 CrossRefGoogle Scholar
  22. Gee JM, Warwick RM (1994b) Metazoan community structure in relation to the fractal dimensions of marine macroalgae. Mar Ecol-Prog Ser 103:141–150. doi: 10.1016/0022-0981(94)90039-6 CrossRefGoogle Scholar
  23. Ghobrial MG, Okbah MA, Gharib SM, Soliman AM (2007) Influence of barley straw and submerged macrophytes on fishpond wastewater quality. Egypt J Aquat Res 33(3):68–87Google Scholar
  24. Gibbons MJ (1988) The impact of wave exposure on the meiofauna of Gelidium pristoides (Turner) Kuetzing (Gelidiales: Rhodophyta). Estuar Coast Shelf Sci 21:581–593. doi: 10.1016/0272-7714(88)90070-4 CrossRefGoogle Scholar
  25. Gibbons MJ (1991) Rocky shore meiofauna: a brief overview. Trans R Soc S Afr 47:595–603Google Scholar
  26. Hagerman L (1966) The macro and microfauna associated with Fucus serratus L., with some ecological remarks. Ophelia 3:1–43. doi: 10.1080/00785326.1966.10409631 CrossRefGoogle Scholar
  27. Hicks GRF (1980) Structure of phytal harpacticoid copepod assemblages and the influence of habitat complexity and turbidity. J Exp Mar Biol Ecol 44:157–192. doi: 10.1016/0022-0981(80)90151-3 CrossRefGoogle Scholar
  28. Hopper BE, Meyers SP (1967a) Populations studies on benthic nematodes within a subtropical seagrass community. Mar Biol 11(2):85–96. doi: 10.1007/BF00386510 CrossRefGoogle Scholar
  29. Hopper BE, Meyers SP (1967b) Foliicolous marine nematodes on turtle grass, Thalassia testudinum König, in Biscayne Bay, Florida. Bull Mar Sci Gulf Caribb 17:471–517Google Scholar
  30. Jarvis SC, Seed R (1996) The meiofauna of Ascophyllum nodosum (L.) Le Jolis: characterization of the assemblages associated with two common epiphytes. J Exp Mar Biol Ecol 199:249–267. doi: 10.1016/0022-0981(95)00184-0 CrossRefGoogle Scholar
  31. Jaya P, Vijaya Bhanu Ch, Naveen Babu M, Annapurna C (2012) Phytal nematodes associated with Caulerpa fastigiata and Caulerpa taxifolia of Visakhapatnam coast. Int J Biol Pharm Allied Sci 1(3):331–336Google Scholar
  32. Kenyon RA, Haywood MDE, Heals DS, Loneragan NR, Pendrey RC, Vance DJ (1998) Abundance of fish and crustacean post larvae on portable artificial seagrass units: daily sampling provides quantitative estimates of the settlement of new recruits. J Exp Mar Biol Ecol 232:197–216. doi: 10.1016/S0022-0981(98)00107-5 CrossRefGoogle Scholar
  33. Kito K (1982) Phytal marine nematode assemblage on Sargassum confusum Agardh, with Reference to the structure and seasonal fluctuations. J Fac Sci Hokkaido Univ Ser VI Zool 23(1):143–161Google Scholar
  34. Machado RCA (2015) Estrutura da comunidade fitoplanctônica e hidrologia do ecossistema recifal de porto de galinhas (Pernambuco-Brasil). Ph.D. thesis, Universidade Federal de Pernambuco, Recife, BrazilGoogle Scholar
  35. Montouchet PC (1979) Sur la communauté des animaux vagiles associés a Sargassum cymosum C. Agardh a Ubatuba, État de São Paulo, Brésil. Stud Neotrop Fauna Environ 14:33–64. doi: 10.1080/01650527909360546 CrossRefGoogle Scholar
  36. Moore PG (1971) The nematode fauna associated with holdfasts of kelp Laminaria hyperborea in North-East Britain. J Mar Biol 51:589–604. doi: 10.1017/S0025315400014983 CrossRefGoogle Scholar
  37. Muralikrishnamurty PV (1983) Intertidal phytal fauna of Gangavaram, east coast of India. Indian J Mar Sci 12(2):85–89Google Scholar
  38. NagelkerkenI Van Der, Velde G, Gorissen MW, Meijer GJ, Van’t Hof T, Den Hartog C (2000) Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuar Coast Shelf Sci 51:31–44. doi: 10.1006/ecss.2000.0617 CrossRefGoogle Scholar
  39. Novak R (1982) Spatial and seasonal distribution of the meiofauna in the seagrass Posidonia oceanica. Neth J Sea Res 16:380–388. doi: 10.1016/0077-7579(82)90044-8 CrossRefGoogle Scholar
  40. Ólafsson E, Johnstone RW, Ndaro SGM (1995) Effects of intensive seaweed farming on the meiobenthos in a tropical lagoon. J Exp Mar Biol Ecol 191:101–117. doi: 10.1016/0022-0981(95)00055-V CrossRefGoogle Scholar
  41. Ott J (1967) Vertikalverteilung von Nematoden in Beständen nordadriatischer Sargassaceen. Helgoland Wiss Meer 15:412–428. doi: 10.1007/BF01618638 CrossRefGoogle Scholar
  42. Pape E, Oevelen D, Moodley L, Soetaert K, Vanreusel A (2013) Nematode feeding strategies and the fate of dissolved organic matter carbon indifferent deep-sea sedimentary environments. Deep-Sea Res Pt I 80:94–110. doi: 10.1016/j.dsr.2013.05.018 CrossRefGoogle Scholar
  43. Platt HM, Warwick RM (1983) Free-living marine nematodes. Part. I. British Enoplids. Cambridge University Press, CambridgeGoogle Scholar
  44. Raes M, Vanreusel A (2006) Microhabitat type determines the composition of nematode communities associated with sediment-clogged cold-water coral framework in the Porcupine Seabight (NE Atlantic). Deep-Sea Res Pt I 53:1880–1894. doi: 10.1016/j.dsr.2006.08.012 CrossRefGoogle Scholar
  45. Raes M, Decraemer W, Vanreusel A (2008) Walking with worms: coral-associated epifaunal nematodes. J Biogeogr 35:2207–2222. doi: 10.1111/j.1365-2699.2008.01945.x CrossRefGoogle Scholar
  46. Rieras P, Hubas C (2003) Trophic ecology of nematodes from various microhabitats of the Roscoff Aber Bay (France): importance of stranded macroalgae evidenced through δ13C and δ15N. Mar Ecol-Prog Ser 260:151–159. doi: 10.3354/meps260151 CrossRefGoogle Scholar
  47. Russo AR (1990) The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194(1):1–12. doi: 10.1007/BF00012107 CrossRefGoogle Scholar
  48. Rysgaard S, Christensen PB, Sorensen MV, Funch P, Berg P (2000) Marine meiofauna, carbon and nitrogen mineralization in sandy and soft sediments of Disko Bay, West Greenland. Aquat Microb Ecol 21:59–71CrossRefGoogle Scholar
  49. Schanz A, Polte P, Asmus H (2002) Cascading effects of hydrodynamics on an epiphyte–grazer system in intertidal seagrass beds of the Wadden Sea. Mar Biol 141:287–297. doi: 10.1007/s00227-002-0823-8 CrossRefGoogle Scholar
  50. Schmid-Araya JM, Hildrew AG, Robertson A, Schmid PE, Winterbottom J (2002) The importance of meiofauna in food web: evidence from an acid stream. Ecology 83(5):1271–1285. doi: 10.1890/0012-9658(2002)083[1271:TIOMIF]2.0.CO;2 CrossRefGoogle Scholar
  51. Soetaert K, Heip C (1995) Nematode assemblages of deep-sea and shelf break sites in the North Atlantic and Mediterranean Sea. Mar Ecol-Prog Ser 125:171–183. doi: 10.3354/meps125171 CrossRefGoogle Scholar
  52. Song SJ, Ryu J, Khim JS, Kim W, Yun SG (2010) Seasonal variability of community structure and breeding activity in marine phytal harpacticoid copepods on Ulva pertusa from Pohang, east coast of Korea. J Sea Res 63:1–10. doi: 10.1016/j.seares.2009.08.004 CrossRefGoogle Scholar
  53. StatSoft, Inc. (2004) STATISTICA (data analysis software system), version 7. http://www.statsoft.com
  54. Taylor WMR (1967) Species of Caulerpa (Chlorophyceae) collected on the International Indian Ocean Expedition. Blumea 15:45–53Google Scholar
  55. Taylor RB (1997) Seasonal variation in assemblages of mobile epifauna inhabiting three subtidal brown seaweeds in northeastern New Zealand. Hydrobiologia 361:25–35. doi: 10.1023/A:1003182523274 CrossRefGoogle Scholar
  56. Tientjen JH, Lee JJ (1973) Life history and feeding types of the marine nematode Chromadora macrolaimoides Steiner. Oecologia 12:303–314CrossRefGoogle Scholar
  57. Toyohara T, Nakaoka M, Aioi K (1999) Population dynamics and reproductive traits of phytal gastropods in seagrass bed in Otsuchi Bay, north-eastern Japan. Mar Ecol 19(2–3):162–178. doi: 10.1046/j.1439-0485.1999.2034082.x Google Scholar
  58. Travizi A, Zavodnik N, Zavodnik N (2004) Phenology of Caulerpa taxifolia and temporal dynamics of its epibiontic meiofauna in the port of Malinska (Croatia, northern Adriatic Sea). Sci Mar 68:145–154CrossRefGoogle Scholar
  59. Ullberg J, Ólafsson E (2003) Free-living marine nematodes actively choose habitat when descending from the water column. Mar Ecol Prog Ser 260:141–149. doi: 10.3354/meps260141 CrossRefGoogle Scholar
  60. Van Donk E (1998) Switches between clear and turbid water states in a biomanipulated lake (1986–1996): the role of herbivory on macrophytes. In: Jeppesen E, Søndergaard M, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Springer, New York, pp 290–297CrossRefGoogle Scholar
  61. Venekey V, Fonsêca-Genevois VG, Da Rocha CMC, Santos PJP (2008) Distribuição espaço-temporal da meiofauna em Sargassum polyceratium Montagne (Fucales, Sargassaceae) de um costão rochoso do nordeste do Brasil. Atlântica 30(1):53–67. doi: 10.5088/atlântica.v30i1.823 Google Scholar
  62. Vidotti EC, Rollemberg MCE (2004) Algas: da economia nos ambientes aquáticos à biorremediação e à química analítica. Quím Nova 27(1):139–145. doi: 10.1590/S0100-40422004000100024 CrossRefGoogle Scholar
  63. Warwick RM (1977) The structure and seasonal fluctuation of phytal marine nematode association on the Isles of Scilly. In: Keegan BF, Ceidigh PO, Boaden PJS (eds) Biology of benthic organisms. Pergamon Press, Oxford, pp 577–585CrossRefGoogle Scholar
  64. Warwick RM, Platt HM, Somerfield, PJ (1998) Free-living Marine Nematodes Part III Monhysterids. Synopses of the British fauna (New Series), 53. Field Studies Council: Shrewsbury. ISBN 1-85153-260-9. VIIGoogle Scholar
  65. Wetzel MA, Weber A, Giere O (2002) Re-colonization of anoxic/sulfidic sediments by marine nematodes alter experimental removal of macroalgal cover. Mar Biol 141:679–689. doi: 10.1007/s00227-002-0863-0 CrossRefGoogle Scholar
  66. Wieser W (1951) Untersuchungen über die algaenbewohnende Mikrofauna mariner Hartböden. I. Zur Oekologie und Systematik der Nematodenfauna von Plymouth. Ost Zool Z 3:425–480Google Scholar
  67. Wieser W (1952) Investigations on the microfauna inhabiting seaweeds on rocky coasts. IV. Studies on the vertical distribution of the fauna inhabiting seaweeds below the Plymouth Laboratory. J Mar Biol Assoc UK 31:145–174. doi: 10.1017/S002531540000374X CrossRefGoogle Scholar
  68. Wieser W (1953) Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Arkiv für Zoologie 4:439–484Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Daniel A. S. De Oliveira
    • 1
    • 2
  • Sofie Derycke
    • 3
  • Clélia M. C. Da Rocha
    • 2
  • Débora F. Barbosa
    • 2
  • Wilfrida Decraemer
    • 1
    • 3
  • Giovanni A. P. Dos Santos
    • 4
  1. 1.Department of BiologyGhent UniversityGhentBelgium
  2. 2.Department of BiologyFederal Rural University of PernambucoRecifeBrazil
  3. 3.OD Taxonomy and PhylogenyRoyal Belgian Institute of Natural SciencesBrusselsBelgium
  4. 4.Biology Centrum, Department of ZoologyRecifeBrazil

Personalised recommendations