Skip to main content

Advertisement

Log in

Are sea snakes pertinent bio-indicators for coral reefs? a comparison between species and sites

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Classical sampling methods often miss important components of coral reef biodiversity, notably organisms that remain sheltered within the coral matrix. Recent studies using sea kraits (sea snakes) as bio-indicators suggest that the guild of predators represented by anguilliform fish (Congridae, Muraenidae, Ophichthidae, henceforth “eels” for simplicity) were far more abundant and diverse than previously suspected. In the current study, eel diversity (similarity and species richness indices) estimated via sea snake sampling (SSS) was compared among six areas of one of the main oceanic biodiversity hotspot of the Pacific Ocean (southwest lagoon of New Caledonia). Based on the eel diversity in the snakes’ diet, the results obtained in six areas, in two snake species, and using different estimates (ANOSIM, Shannon index…) were consistent, suggesting that SSS provided robust information. Analyses also suggested subtle, albeit significant, differences in the eel assemblages among islets. Such spatial differences are discussed in light of local management practices. As SSS is easy to use, cost-effective, and provides the best picture of eel assemblages to date, it can be employed to monitor the eel assemblages in addition to the snakes themselves in many areas of the Indo-Pacific Ocean, thereby providing an index of the top predator biodiversity of many coral reefs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abrams RW, Abrams MD, Schein MW (1983) Diurnal observations on the behavioral ecology of Gymnothorax moringa (Cuvier) and Muraena miliaris (Kaup) on a Caribbean coral reef. Coral Reefs 1:185–192

    Article  Google Scholar 

  • Andréfouët S, Torres-Pulliza D (2004) Atlas des récifs coralliens de Nouvelle-Calédonie, IFRECOR Nouvelle-Calédonie. IRD, Nouméa, p 48

    Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  PubMed  CAS  Google Scholar 

  • Bonnet X, Brischoux F, Pearson D, Rivalan P (2009) Beach-rock as a keystone habitat for sea kraits. Environ Conserv 36:62–70

    Article  Google Scholar 

  • Brischoux F, Bonnet X (2008) Estimating the impact of sea kraits on the anguilliform fish community (Muraenidae, Congridae, Ophichthidae) of New Caledonia. Aquat Liv Res 21:395–399

    Article  Google Scholar 

  • Brischoux F, Bonnet X (2009) Life history of sea kraits in New Caledonia. Zoologia Neocaledonica 7. Mém Mus Nat Hist Nat 198:37–51

    Google Scholar 

  • Brischoux F, Bonnet X, De Crignis M (2007a) A method to reconstruct anguilliform fishes from partially digested items. Mar Biol 151:1893–1897

    Article  Google Scholar 

  • Brischoux F, Bonnet X, Shine R (2007b) Foraging ecology of sea kraits (Laticauda spp.) in the Neo-Caledonian lagoon. Mar Ecol Prog Ser 350:145–151

    Article  Google Scholar 

  • Brischoux F, Bonnet X, Shine R (2009a) Determinants of dietary specialization: a comparison of two sympatric species of sea snakes. Oikos 118:145–151

    Article  Google Scholar 

  • Brischoux F, Bonnet X, Pinaud D (2009b) Fine scale site fidelity in sea kraits: implications for conservation. Biodivers Conserv (in press)

  • Chapman MG, Underwood AJ (1999) Ecological patterns in multivariate assemblages: information and interpretation of negative values in ANOSIM tests. Mar Ecol Prog Ser 180:257–265

    Article  Google Scholar 

  • Cherel Y, Duhamel G, Gasco N (2004) Cephalopod fauna of subantarctic islands: new information from predators. Mar Ecol Prog Ser 266:143–156

    Article  Google Scholar 

  • Cherel Y, Sabatié R, Potier M, Marsac F, Ménard F (2007) New information from fish diets on the importance of glassy flying squid (Hyaloteuthis pelagica) (Teuthoidea: Ommastrephidae) in the epipelagic cephalopod community of the tropical Atlantic Ocean. Fish Bull 105:147–152

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Cogger H, Heatwole H (2006) Laticauda frontalis (de Vis, 1905) and Laticauda saintgironsi n.sp. from Vanuatu and New Caledonia (Serpentes: Elapidae: Laticaudinae)—a new lineage of sea kraits? Rec Aust Mus 58:245–256

    Google Scholar 

  • Colwell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. Version 7.5. Presistent URL<purl.oclc.org/estimates>

  • Froese R, Pauly D (eds) (2006) FishBase. World Wide Web electronic publication. www.fishbase.org, version 12/2006

  • Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558

    Article  Google Scholar 

  • Heatwole H (1999) Sea snakes Australian natural history series. University of New South Wales, Australia

    Google Scholar 

  • Heatwole H, Busack S, Cogger H (2005) Geographic variation in sea kraits of the Laticauda colubrina complex (Serpentes: Elapidae: Hydrophiinae: Laticaudini). Herpetol Monogr 19:1–136

    Article  Google Scholar 

  • Hindell MA, Bradshaw CJA, Harcourt RG, Guinet C (2003) Ecosystem monitoring: are seals a potential tool for monitoring change in marine systems? In: Gales NJ, Hindell MA, Kirkwood R (eds) Marine mammals. Fisheries, tourism and management issues. CSIRO Publishing, Melbourne, pp 330–343

    Google Scholar 

  • Hochberg EJ, Atkinson MJ, Andrefouet S (2003) Spectral reflectance of coral reef bottom-types worldwide and implications for coral reef remote sensing. Remote Sens Environ 85:159–173

    Article  Google Scholar 

  • Hughes TP (1994) Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265:1547–1551

    Article  PubMed  Google Scholar 

  • Ineich I, Laboute P (2002) Sea snakes of New Caledonia. IRD et Muséum national d’Histoire naturelle Editions, Collection Faune et flore tropicales, Paris

  • Ineich I, Bonnet X, Brischoux F, Kulbicki M, Séret B, Shine R (2007) Anguilliform fishes and sea kraits: neglected predators in coral reef ecosystems. Mar Biol 151:793–802

    Article  Google Scholar 

  • Kitahara M, Fujii K (1994) Biodiversity and community structure of temperate butterfly species within a gradient of human disturbance: an analysis based on the concept of generalist vs. specialist strategies. Pop Ecol 36:187–199

    Article  Google Scholar 

  • Koellner T, Hersperger AM, Wohlgemuth T (2004) Rarefaction method for assessing plant species diversity on a regional scale. Ecography 27:532–544

    Article  Google Scholar 

  • Kulbicki M (1997) Bilan de 10 ans de recherche (1985–1995) par l’ORSTOM sur la structure des communautés des poisons lagonaires et récifaux en Nouvelle-Calédonie. Cybium 21:47–79

    Google Scholar 

  • Magurran AE (1988) Ecological diversity and its measurement. Croom Helm Ltd, London, UK

    Google Scholar 

  • McGeoch M (1998) The selection, testing and application of terrestrial insects as bioindicators. Biol Rev 73:181–201

    Article  Google Scholar 

  • Ménard F, Potier M, Romanov E, Jaquemet S, Sabatié R, Cherel Y (2007) New information from predator diets on the importance of two Ommastrephidae: Sthenoteuthis oualaniensis in the Indian Ocean and Hyaloteuthis pelagica in the Atlantic Ocean. GLOBEC Report 24:49–52

    Google Scholar 

  • Niemelä J (2000) Biodiversity monitoring for decision-making. Ann Zool Fenn 37:307–317

    Google Scholar 

  • Noss RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conserv Biol 4:355–364

    Article  Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958

    Article  PubMed  CAS  Google Scholar 

  • Pearson DL, Cassola F (1992) World-wide species richness patterns of tiger beetles (Coleoptera: Cicindelidae): indicator taxon for biodiversity and conservation studies. Conserv Biol 6:376–391

    Article  Google Scholar 

  • Reed RN, Shine R, Shetty S, Cogger H (2002) Sea kraits (Squamata: Laticauda spp.) as a useful bioassay for assessing local diversity of eels (Muraenidae, Congridae) in the western Pacific Ocean. Copeia 2002:1098–1101

    Article  Google Scholar 

  • Rogers CS (1990) Responses to coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202

    Article  Google Scholar 

  • Saint Girons H (1964) Notes sur l’écologie et la structure des populations des Laticaudinae (Serpentes : Hydrophiidae) en Nouvelle-Calédonie. Rev Ecol 111:185–214

    Google Scholar 

  • Séret B, Brischoux F, Bonnet X, Shine R (2008) First record of Cirrimaxilla formosa (Teleostei: Muraenidae) from New Caledonia, found in sea snake stomach contents. Cybium 32:191–192

    Google Scholar 

  • Sheppard CRC (2003) Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425:294–297

    Article  PubMed  CAS  Google Scholar 

  • Shetty S, Shine R (2002a) Sexual divergence in diets and morphology in Fijian sea snakes, Laticauda colubrina (Laticaudidae). Aust Ecol 27:77–84

    Article  Google Scholar 

  • Shetty S, Shine R (2002b) Philopatry and homing behavior of sea snakes (Laticauda colubrina) from two adjacent islands in Fiji. Conserv Biol 16:1422–1426

    Article  Google Scholar 

  • Shine R, Reed RN, Shetty S, Cogger HG (2002) Relationships between sexual dimorphism and niche partitioning within a clade of sea-snakes (Laticaudinae). Oecologia 133:45–53

    Article  Google Scholar 

  • Su Y, Fong S-C, Tu M-C (2005) Food habits of the Sea Snake Laticauda semifasciata. Zool Stud 44:403–408

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Wantiez L, Thollot P, Kulbicki M (1997) Effects of marine reserves on coral reef fish communities from five islands in New Caledonia. Coral Reefs 16:215–224

    Article  Google Scholar 

  • Wilkinson C (2006) Status of coral reefs of the world: summary of threats and remedial action. In: Coté IM, Reynolds JD (eds) Coral reefs conservation. Cambridge University Press. CSIRO Publishing, Melbourne, pp 3–39

    Google Scholar 

Download references

Acknowledgments

B. Seret and R. Cambag helped with eel identifications. I. Ineich, Mayol, A. Lane, O. Lourdais, S. Lorioux, M. De Crignis, D. Pearson, A. Ramirez, M. Guillon, C. Michel, D. Serin, M. Bonnet and A. Lavandier helped during fieldwork. T. Cook and R. Tingley corrected the English. We also thank C. Chevillon, B. Mège, C. Goiran, and D. Ponton (DRN Province Sud, CONCEPT, Aquarium de Nouméa, IRD) for logistical support. We thank the Centre National de la Recherche Scientifique, and the University François Rabelais for funding. The study was carried out under permits #6024-179/DRN/ENV and #6024-3601/DRN/ENV.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to François Brischoux.

Additional information

Communicated by S. A. Poulet.

Appendix 1

Appendix 1

See Table 2.

Table 2 List of the eel species sampled through SSS at the different sampling sites

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brischoux, F., Bonnet, X. & Legagneux, P. Are sea snakes pertinent bio-indicators for coral reefs? a comparison between species and sites. Mar Biol 156, 1985–1992 (2009). https://doi.org/10.1007/s00227-009-1229-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1229-7

Keywords

Navigation