Advertisement

Marine Biology

, Volume 158, Issue 12, pp 2717–2726 | Cite as

Salinity effects on the coexistence of cryptic species: a case study on marine nematodes

  • N. De MeesterEmail author
  • S. Derycke
  • D. Bonte
  • T. Moens
Original Paper

Abstract

The coexistence of four cryptic species of Rhabditis (Pellioditis) marina (Nematoda: Rhabditidae) at small geographical scale challenges ecological competition theory and was therefore studied in the laboratory at two different salinities, where their performance in combined cultures was compared with that in monospecies cultures. We found that three of the four cryptic species were able to coexist, but that interspecific interactions (competition and facilitation) were common. Salinity had an effect on these interactions, with a shift from contest to scramble competition. This shift may result from an increased population development of two of the four species at the lower salinity in the monospecific cultures. This experiment demonstrates that abiotic conditions may play an important role in achieving coexistence between cryptic species and can alter the interspecific interactions between them.

Keywords

Internal Transcribe Space Lower Salinity Salinity Tolerance Cryptic Species Assemblage Structure 
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

Funding for this research was obtained from the Flemish Fund for Scientific Research (FWO) through project 3G040407, and from Ghent University through projects 011060002 and 01GA1911 W. S.D. is a postdoctoral fellow with the FWO. Annelien Rigaux is acknowledged for help with the monospecific experiments.

References

  1. Anderson M (2001) A new method for non parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  2. Anderson M (2004) PERMDISP: a FORTRAN computer program for permutation analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  3. Andrassy I (1983) A taxonomic review of the suborder Rhaditina (Nematoda: Secernentea). Office de la Recherche Scientifique et Technique Outre-Mer, ParisGoogle Scholar
  4. Anger K (1991) Effects of temperature and salinity on the larval development of the Chinese mitten crab Eriocheir sinensis (Decapoda: Grapsidae). Mar Ecol Prog Ser 72:103–110CrossRefGoogle Scholar
  5. Barata C, Hontoria F, Amat F, Browne R (1996) Competition between sexual and parthenogenetic Artemia: temperature and strain effects. J Exp Mar Biol Ecol 196:313–328. doi: 10.1016/0022-0981(95)00137-9 CrossRefGoogle Scholar
  6. Begon M, Harper J, Townsend C (1996) Ecology: individuals, populations, and communities, 3 edn. Blackwell Science, OxfordGoogle Scholar
  7. Bengtsson J (1987) Competitive dominance among cladocera: are single-factor explanations enough? Hydrobiologia 145:245–257. doi: 10.1007/BF02530285 CrossRefGoogle Scholar
  8. Bertness M, Leonard G (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989. doi: 10.1890/0012-9658(1997)078[1976:TROPII]2.0.CO;2 CrossRefGoogle Scholar
  9. Bhadury P, Austen M, Bilton D, Lambshead P, Rogers A, Smerdon G (2008) Evaluation of combined morphological and molecular techniques for marine nematode (Terschellingia spp.) identification. Mar Biol 154:509–518. doi: 10.1007/s00227-008-0945-8 CrossRefGoogle Scholar
  10. Bickford D, Lohman D, Sodhi N, Ng P, Meier R, Winker K, Ingram K, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. doi: 10.1016/j.tree.2006.11.004 CrossRefGoogle Scholar
  11. Capstick C (1959) The distribution of free-living nematodes in relation to salinity in the middle and upper reaches of the River Blyth estuary. J Anim Ecol 28:189–210CrossRefGoogle Scholar
  12. Cardinale B, Palmer M, Collins S (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429. doi: 10.1038/415426a CrossRefGoogle Scholar
  13. Chandler G, Fleeger J (1987) Facilitative and inhibitory interactions among estuarine meiobenthic harpacticoid copepods. Ecology 68:1906–1919CrossRefGoogle Scholar
  14. Chesson P (1991) A need for niches? Trends Ecol Evol 6:26–28CrossRefGoogle Scholar
  15. Coomans A (2000) Nematode systematics: past, present and future. Nematology 2:3–7. doi: 10.1163/156854100508845 CrossRefGoogle Scholar
  16. Coull BC (1999) Role of meiofauna in estuarine soft bottom habitats. Aust J Ecol 24:327–343. doi: 10.1046/j.1442-9993.1999.00979.x CrossRefGoogle Scholar
  17. Coulson T, Godfray HCJ (2007) Single-species dynamics. In: May RMC, McLean AR (eds) Theoretical ecology: principles and applications. Oxford University Press, Oxford, pp 17–34Google Scholar
  18. Crombie A (1947) Interspecific competition. J Anim Ecol 16:44–73Google Scholar
  19. Dailidiene I, Davuliene L (2006) Spatial and temporal variation of water salinity in the Curonian Lagoon. In: Evolutions in hydrography, 6th–9th November 2006, Provincial House Antwerp, Belgium: proceedings of the 15th International Congress of the International Federation of hydrographic societies. Special Publication of the Hydrographic Society 55, pp 178–182Google Scholar
  20. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. D. Appleton, New YorkGoogle Scholar
  21. De Mesel I, Derycke S, Swings J, Vincx M, Moens T (2006) Role of nematodes in decomposition processes: does within-trophic group diversity matter? Mar Ecol Prog Ser 321:157–166CrossRefGoogle Scholar
  22. Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren J, Vincx M, Moens T (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103CrossRefGoogle Scholar
  23. Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2006) Seasonal dynamics of population genetic structure in cryptic taxa of the Pellioditis marina complex (Nematoda: Rhabditida). Genetica 128:307–321. doi: 10.1007/s10709-006-6944-0 CrossRefGoogle Scholar
  24. Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2007) Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Mar Biol 151:1799–1812. doi: 10.1007/s00227-007-0609-0 CrossRefGoogle Scholar
  25. Derycke S, Fonseca G, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2008a) Disentangling taxonomy within the Rhabditis (Pellioditis) marina (Nematoda, Rhabditidae) species complex using molecular and morphological tools. Zool J Linn Soc 152:1–15. doi: 10.1111/j.1096-3642.2007.00365.x CrossRefGoogle Scholar
  26. Derycke S, Remerie T, Backeljau T, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2008b) Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Mol Ecol 17:3306–3322. doi: 10.1111/j.1365-294X.2008.03846.x CrossRefGoogle Scholar
  27. Diaz H, Bevilacqua M (1986) Larval development of Aratus pisonii (Milne Edwards) (Brachyura, Grapsidae) from marine and estuarine environments reared under different salinity conditions. J Coast Res 2:43–49Google Scholar
  28. Dietrich G, Kalle K (1957) Allgemeine Meereskunde: Eine Einführung in die Ozeanographie, 8 edn. Gebrüder Bornträger, BerlinGoogle Scholar
  29. dos Santos G, Derycke S, Fonsêca-Genevois V, Coelho L, Correia M, Moens T (2008) Differential effects of food availability on population growth and fitness of three species of estuarine, bacterial-feeding nematodes. J Exp Mar Biol Ecol 355:27–40. doi: 10.1016/j.jembe.2007.11.015 CrossRefGoogle Scholar
  30. dos Santos G, Derycke S, Fonsêca-Genevois V, Coelho L, Correia M, Moens T (2009) Interactions among bacterial-feeding nematode species at different levels of food availability. Mar Biol 156:629–640. doi: 10.1007/s00227-008-1114-9 CrossRefGoogle Scholar
  31. Dunson W, Travis J (1991) The role of abiotic factors in community organization. Am Nat 138:1067–1091CrossRefGoogle Scholar
  32. Egler F (1954) Vegetation science concepts I. Initial floristic composition, a factor in old-field vegetation development with 2 figs. Plant Ecol 4:412–417. doi: 10.1007/BF00275587 CrossRefGoogle Scholar
  33. Ettema C (1998) Soil nematode diversity: species coexistence and ecosystem function. J Nematol 30:159Google Scholar
  34. Fonseca G, Derycke S, Moens T (2008) Integrative taxonomy in two free-living nematode species complexes. Biol J Linn Soc 94:737–753. doi: 10.1111/j.1095-8312.2008.01015.x CrossRefGoogle Scholar
  35. Foran J (1986) A comparison of the life history features of a temperate and a subtropical Daphnia species. Oikos 46:185–193CrossRefGoogle Scholar
  36. Fouquet A, Vences M, Salducci M, Meyer A, Marty C, Blanc M, Gilles A (2007) Revealing cryptic diversity using molecular phylogenetics and phylogeography in frogs of the Scinax ruber and Rhinella margaritifera species groups. Mol Phylogenet Evol 43:567–582. doi: 10.1016/j.ympev.2006.12.006 CrossRefGoogle Scholar
  37. Gómez A, Temprano M, Serra M (1995) Ecological genetics of a cyclical parthenogen in temporary habitats. J Evol Biol 8:601–622. doi: 10.1046/j.1420-9101.1995.8050601.x CrossRefGoogle Scholar
  38. Gómez A, Carmona MJ, Serra M (1997) Ecological factors affecting gene flow in the Brachionus plicatilis complex (Rotifera). Oecologia 111:350. doi: 10.1007/s004420050245 CrossRefGoogle Scholar
  39. Grainger J (1958) First stages in the adaptation of poikilotherms to temperature change. In: Prosser C (ed) Physiological adaptation. American Physiological Society, Washington, DC, pp 79–91Google Scholar
  40. Heip CHR, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489Google Scholar
  41. Højgaard DP (1998) Impact of temperature, salinity and light on hatching of eggs of Anisakis simplex (Nematoda, Anisakidae), isolated by a new method, and some remarks on survival of larvae. Sarsia 83:21–28Google Scholar
  42. Hubbell SP (2005) Neutral theory in community ecology and the hypothesis of functional equivalence. Funct Ecol 19:166–172. doi: 10.1111/j.0269-8463.2005.00965.x CrossRefGoogle Scholar
  43. Huettel R (1986) Chemical communicators in nematodes. J Nematol 18:3–8Google Scholar
  44. Hughes A, Inouye B, Johnson M, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi: 10.1111/j.1461-0248.2008.01179.x CrossRefGoogle Scholar
  45. Hutchinson G, MacArthur R (1959) A theoretical ecological model of size distributions among species of animals. Am Nat 93:117–125CrossRefGoogle Scholar
  46. Ilieva-Makulec K (2001) A comparative study of the life strategies of two bacterial-feeding nematodes under laboratory conditions. III. Influence of the initial nematode density on the interactions of Acrobeloides nanus (de Man 1880) Anderson and Dolichorhabditis dolichura (Schneider 1866) Andrassy 1983 in mixed cultures. Pol J Ecol 49:137–144Google Scholar
  47. Jensen T, Hessen D, Faafeng B (2001) Biotic and abiotic preferences of the cladoceran invader Limnosida frontosa. Hydrobiologia 442:89–99. doi: 10.1023/A:1017530609557 CrossRefGoogle Scholar
  48. Jonsson M, Malmqvist B (2003) Mechanisms behind positive diversity effects on ecosystem functioning: testing the facilitation and interference hypotheses. Oecologia 134:554–559. doi: 10.1007/s00442-002-1148-5 Google Scholar
  49. Kaiser M, Attrill M, Jennings S, Thomas D, Barnes D, Brierley A, Polunin N, Raffaelli D, Williams P (2005) Marine ecology: processes, systems, and impacts. University Press Oxford, OxfordGoogle Scholar
  50. Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216CrossRefGoogle Scholar
  51. Lambshead P, Boucher G (2003) Marine nematode deep sea biodiversity–hyperdiverse or hype? J Biogeogr 30:475–485. doi: 10.1046/j.1365-2699.2003.00843.x CrossRefGoogle Scholar
  52. Leibold M, McPeek M (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410CrossRefGoogle Scholar
  53. Lomnicki A (1988) Population ecology of individuals. Princeton University Press, New JerseyGoogle Scholar
  54. Lowe C, Kemp S, Diaz-Avalos C, Montagnes D (2006) How does salinity tolerance influence the distributions of Brachionus plicatilis sibling species? Mar Biol 150:377–386. doi: 10.1007/s00227-006-0366-5 CrossRefGoogle Scholar
  55. Moens T, Vincx M (1998) On the cultivation of free-living marine and estuarine nematodes. Helgol Mar Res 52:115–139. doi: 10.1007/BF02908742 Google Scholar
  56. Moens T, Vincx M (2000) Temperature and salinity constraints on the life cycle of two brackish-water nematode species. J Exp Mar Biol Ecol 243:115–135. doi: 10.1016/S0022-0981(99)00113-6 CrossRefGoogle Scholar
  57. Moens T, Vierstraete A, Vincx M (1996) Life strategies in two bacterivorous marine nematodes: preliminary results. PSZN I Mar Ecol 17:509–518. doi: 10.1111/j.1439-0485.1996.tb00524.x CrossRefGoogle Scholar
  58. Moens T, dos Santos G, Thompson F, Swings J, Fonsêca-Genevois V, Vincx M, De Mesel I (2005) Do nematode mucus secretions affect bacterial growth? Aquat Microb Ecol 40:77–83CrossRefGoogle Scholar
  59. Nicholson A (1954) An outline of the dynamics of animal populations. Aust J Zool 2:9–65. doi: 10.1071/ZO9540009 CrossRefGoogle Scholar
  60. Ortells R, Gómez A, Serra M (2003) Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis. Freshw Biol 48:2194–2202. doi: 10.1046/j.1365-2427.2003.01159.x CrossRefGoogle Scholar
  61. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
  62. Tietjen J, Lee J (1972) Life cycles of marine nematodes. Oecologia 10:167–176. doi: 10.1007/BF00347988 CrossRefGoogle Scholar
  63. Trewick S (1998) Sympatric cryptic species in New Zealand Onychophora. Biol J Linn Soc 63:307–329. doi: 10.1006/bijl.1997.0197 CrossRefGoogle Scholar
  64. Vanfleteren J (1980) Nematodes as nutritional models. In: Zuckerman B (ed) Nematodes as biological models, vol 2. Academic Press, New York, pp 47–80Google Scholar
  65. Violle C, Nemergut DR, Pu Z, Jiang L (2011) Phylogenetic limiting similarity and competitive exclusion. Ecol Lett. doi: 10.1111/j.1461-0248.2011.01644.x
  66. Vrijenhoek R, Schutz S, Gustafson R, Lutz R (1994) Cryptic species of deep-sea clams (Mollusca: Bivalvia: Vesicomyidae) from hydrothermal vent and cold-water seep environments. Deep Sea Res I 41:1171–1189. doi: 10.1016/0967-0637(94)90039-6 CrossRefGoogle Scholar
  67. Walker B (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23CrossRefGoogle Scholar
  68. Webb C, Ackerly D, McPeek M, Donoghue M (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. doi: 10.1146/annurev.ecolsys.33.010802.150448 CrossRefGoogle Scholar
  69. Webb C, Gilbert G, Donoghue M (2006) Phylodiversity-dependent seedling mortality, size structure, and disease in a Bornean rain forest. Ecology 87:123–131. doi: 10.1890/0012-9658(2006)87[123:PSMSSA]2.0.CO;2 CrossRefGoogle Scholar
  70. Wellborn G, Cothran R (2007) Niche diversity in crustacean cryptic species: complementarity in spatial distribution and predation risk. Oecologia 154:175–183. doi: 10.1007/s00442-007-0816-x CrossRefGoogle Scholar
  71. Westerbom M, Kilpi M, Mustonen O (2002) Blue mussels, Mytilus edulis, at the edge of the range: population structure, growth and biomass along a salinity gradient in the north-eastern Baltic Sea. Mar Biol 140:991–999. doi: 10.1007/s00227-001-0765-6 CrossRefGoogle Scholar
  72. Williams W (1998) Salinity as a determinant of the structure of biological communities in salt lakes. Hydrobiologia 381:191–201. doi: 10.1023/A:1003287826503 CrossRefGoogle Scholar
  73. Williams H, Ormerod S, Bruford M (2006) Molecular systematics and phylogeography of the cryptic species complex Baetis rhodani (Ephemeroptera, Baetidae). Mol Phylogenet Evol 40:370–382. doi: 10.1016/j.ympev.2006.03.004 CrossRefGoogle Scholar
  74. Zhang DY (2004) Coexistence of cryptic species. Ecol Lett 7:165. doi: 10.1111/j.1461-0248.2004.00569.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • N. De Meester
    • 1
    Email author
  • S. Derycke
    • 1
    • 2
  • D. Bonte
    • 3
  • T. Moens
    • 1
  1. 1.Marine Biology Unit, Department of BiologyGhent UniversityGhentBelgium
  2. 2.Center for Molecular Phylogeny and EvolutionGhent UniversityGhentBelgium
  3. 3.Terrestrial Ecology Unit, Department of BiologyGhent UniversityGhentBelgium

Personalised recommendations