Skip to main content
Log in

Diversity and composition of macro- and meiofaunal carapace epibionts of the hawksbill sea turtle (Eretmochelys imbricata Linnaeus, 1822) in Atlantic waters

  • Diversity of marine meiofauna on the coast of Brazil
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

The presence of macro-epibionts on turtle carapaces is a well-known phenomenon, whereby carapaces are occupied by dynamic and fully functional epibiont communities. However, meiofaunal organisms have been largely ignored in turtle shell studies despite their omnipresence and higher abundances and diversity than the macrofauna. Epifauna from the hawksbill sea turtle Eretmochelys imbricata was investigated during summer 2010 with the aim to advance our knowledge on meiofaunal epibiont communities on turtle carapaces and gain insights into their interaction with settled macrofauna. Eighteen epibiont higher taxa were found (17 meiofauna, 5 macrofauna), 5 of which are common for macro- and meiofauna. Meiofauna was present on all turtle carapaces, but macrofauna occurred on only 8 out of 19 investigated carapaces, suggesting that carapace colonization by meiofauna precedes macrofauna recruitment. In addition, the macrofauna embedded on the carapaces increased the microhabitat complexity, favoring richer and more abundant meiofauna communities. The significant positive correlations between meiofauna and macrofauna taxa (up to 90 %) suggests the presence of mutual facilitating processes and indicates the positive effects between meio- and macrofaunal epibionts important for their recruitment and establishment. The hawksbill sea turtle carapaces were occupied by fully functional and active epifaunal communities, with adult and reproductive stages for most meiofaunal and macrofaunal taxa. Turtle carapaces can therefore be seen as a biological substrate that can serve as a platform for faunal dispersal, as has been observed for barnacles, enhancing the geographical distribution of several species through sea turtle migration. In addition to the main focus of this paper on meio- and macrofaunal epibiont communities, we provide an updated list of taxa found on carapaces of the hawksbill sea turtle and discuss the geographical scope and dispersion potential of some of these taxa.

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
Fig. 4

Similar content being viewed by others

Notes

  1. As there are very few marine insects, it is suspicious to find this taxon in turtle carapaces. Although we have found this aquatic insect in the samples taken from the carapaces, we cannot confirm whether the insect was living on the carapace or whether it was a sample contamination.

References

  • Abelson A, Miloh T, Loya Y (1993) Flow patterns induced by substrata and body morphologies of benthic organisms, and their roles in determining availability of food particles. Limnol Oceanogr 38:1116–1124

    Article  Google Scholar 

  • Anderson DT (1994) Barnacles: Structure, Function, Development and Evolution. Chapman and Hall, London

    Google Scholar 

  • Anderson M, Gorley RN (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Amaral FD, Farrapeira CMR, Lira SMA, Ramos CAC (2010) Benthic macrofauna inventory of two shipwrecks from Pernambuco coast, Northeast Brazil. Rev Nordest Zool 1:24–41

    Google Scholar 

  • Attolini FS (1997) Composição e distribuição dos anelídeos poliquetas na plataforma continental da região da Bacia do Campos, RJ, Brasil. Dissertation, University of São Paulo

  • Austen MC, Widdicombe S, Villano-Pitacco N (1998) Effects of biological disturbance on diversity and structure of meiobenthic nematode communities. Mar Ecol Prog Ser 174:233–246

    Article  Google Scholar 

  • Badillo FJ (2007) Epizoítos y parásitos de la tortuga boba (Caretta caretta) en el Mediterráneo Occidental. Dissertation, University of Valencia

  • Barnard JL, Karaman GS (1991) The Families and Genera of Marine Gammaridean Amphipoda (Except Marine Gammaroids) Part 1. Rec Aust Mus Suppl 13:1–417

    Article  Google Scholar 

  • Bellini C, Sanches TM, Formia A (2000) Hawksbill tagged in Brazil captured in Gabon, Africa. Mar Turt Newsl 87:11–12

    Google Scholar 

  • Bjordnal K (1999) Conservation of Hawksbill Sea Turtles: Perceptions and Realities. Chelonian Cons Biol 3:174–176

    Google Scholar 

  • Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. Boca Raton, Florida, pp 229–239

    Google Scholar 

  • Bodin P (1977) Les peuplements de Copépodes Harpacticoïdes (Crustacea) des sédiments meubles de la zone intertidale des côtes charentaises (Atlantique). Mém Mus Natl Hist Nat 104:1–120

    Google Scholar 

  • Braeckman U, Provoost P, Moens T, Soetaert K, Middelburg JJ, Vincx M, Vanaverbeke J (2011a) Biological vs. physical mixing effects on benthic food web dynamics. Plos ONE 6:1–12

    Article  Google Scholar 

  • Braeckman U, Van Colen C, Soetaert K, Vincx M, Vanaverbeke J (2011b) Contrasting macrobenthic activities differentially affect nematode density and diversity in a shallow subtidal marine sediment. Mar Ecol Prog Ser 422:179–191

    Article  Google Scholar 

  • Bugoni L, Krause L, Almeida AO, Bueno AAP (2001) Commensal Barnacles of Sea Turtles in Brazil. Mar Turt Newsl 94:7–9

    Google Scholar 

  • Camargo MG, Lana PC (1995a) Lumbrineridae (Polychaeta: Eunicemorpha) da costa Sul e Sudeste do Brasil. I. Lysarete, Arabelloneris, Lumbrineriopsis, Lumbrinerides, Paraninoe e Ninoe. Iheringia 79:77–91

    Google Scholar 

  • Camargo MG, Lana PC (1995b) Lumbrineridae (Polychaeta: Eunicemorpha) da costa Sul e Sudeste do Brasil. II. Lumbrineris. Iheringia 79:93–120

    Google Scholar 

  • Camargo MG (1993) Lumbrineridae (Annelida: Polychaeta) da costa sul e sudeste do Brasil. Dissertation, University of Paraná

  • Clarke KR, Gorley RN (2006) PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Dahms HU, Qian PY (2005) Exposure of biofilms to meiofaunal copepods affects the larval settlement of Hydroides elegans (Polychaeta). Mar Ecol Prog Ser 297:203–214

    Article  Google Scholar 

  • Dahms HU, HarderT, Qian PY (2004) Effect of meiofauna on macrofauna recruitment:settlement inhibition of the polychaeteHydroideselegansby the harpacticoid copepodTisbe japonica. J Exp Mar Biol Ecol 311:47–61

  • Danovaro R, Fraschetti S, Belgrano A, Vincx M, Galletti M, Albertelli G, Fabiano M (1995) The potential impact of meiofauna on the recruitment of macrobenthos in a subtidal coastal benthic community of the Ligurian Sea (north-western Mediterranean): A field result. In: Eleftheriou A, Ansell AD, Smith CJ (eds) 28th European Marine Biology Symposium - Biology and Ecology of Shallow Coastal Waters, pp 115–122

  • De Loreto BO, Bondioli ACV (2008) Epibionts associated with Green Sea Turtles (Chelonia mydas) from Cananéia, Southeast Brazil. Mar Turt Newsl 122:5–8

    Google Scholar 

  • Dobbs KA, Landry AM Jr (2004) Commensals on nesting hawksbill turtles (Eretmochelys imbricata), Milman Island, northern Great barrier reef, Austrália. Mem Queensland Mus 49:674

    Google Scholar 

  • Dupuy C, Rossignol L, Geslin E, Pascal PY (2010) Predation of mudflat meio-macrofaunal metazoans by a calcareous foraminifer, Ammonia tepida (Cushman, 1926). J Foraminifer Res 40:305–312

    Article  Google Scholar 

  • Epibiont research cooperative (2007) A Synopsis of the Literature on the Turtle Barnacles (Cirripedia: Balanomorpha: Coronuloidea) 1758–2007. Epibiont Res Coop Spec Publi 1:62

    Google Scholar 

  • Fauchald K (1977) The polychaete worms. Definitions and keys to the orders, families and genera. Natural History Museum of Los Angeles County. Science Series 28:1–188

    Google Scholar 

  • Fonsêca-Genevois V, Somerfield PJ, Neves MH, Coutinho R, Moens T (2006) Colonization and early succession on artificial hard substrate by meiofauna. Mar Biol 148:1039–1050

    Article  Google Scholar 

  • Frazier J, Winston J, Ruckdeschel CA (1992) Epizoan communities on marine turtles. III. Bryozoa. Bull Mar Sci 1:1–8

    Google Scholar 

  • Frick MG, Williams KL, Robinson M (1998) Epibionts associates with nesting loggerhead sea turtles (Caretta caretta) in Georgia, USA. Herpetol Rev 29:211–213

    Google Scholar 

  • Frick MG, Ross A, Williams KL, Bolten AB, Bjordnal KA, Martins HR (2003) Epibiotic Associates of Oceanic-Stage Loggerhead Turtles from the Southeastern North Atlantic. Mar Turt Newsl 101:18

    Google Scholar 

  • Frick MG, Williams KL, Veljacic D, Pierrard L, Jackson JA, Knight SE (2000) Newly documented epibiont species from nesting loggerhead sea turtles (Caretta caretta) in Georgia, USA. Mar Turt Newsl 88:3–5

    Google Scholar 

  • Frick MG, Williams K, Markesteyn EJ, Pfaller JB, Frick RE (2002) New records of epibionts from loggerhead sea turtles Caretta caretta (L.). Bull Mar Sci 3:953–956

    Google Scholar 

  • Frick MG, Pfaller JB (2013) Sea Turtle Epibiosis. In: Wyneken J, Lohmann KJ, Musick JA (eds) The Biology of Sea Turtles, Volume III. CRC, Boca Raton, pp 399–426

    Chapter  Google Scholar 

  • Fuller W, Broderick A, Enever R, Thorne P, Godley BJ (2010) Motile homes: a comparison of the spatial distribution of epibiont communities on Mediterranean sea turtles. J Nat Hist 27:1743–1753

    Article  Google Scholar 

  • 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 367:173–183

    Article  Google Scholar 

  • Grzelak K, Kuklinski P (2010) Benthic assemblages associated with rocks in a brackish environment of the southern Baltic Sea. J Mar Biol Assoc UK 90:115–124

    Article  Google Scholar 

  • Higgins RP, Thiel H (1988) Introduction to the study of meiofauna. Smithsonian Institution, London

    Google Scholar 

  • Jones DS, Hewitt MA, Sampey A (2000) A checklist of the cirripedia of the South China Sea. Raffles Bull Zool 8:233–307

    Google Scholar 

  • Koivisto M, Westerbom M, Arnkil A (2011) Quality or quantity: small-scale patch structure affects patterns of biodiversity in a sublittoral blue mussel community. Aquatic Biology 12(3):261–270

    Google Scholar 

  • Lana PC (1987) Padrões de distribuição geográfica dos poliquetas errantes (Annelida: Polychaeta) do estado no Paraná. Ciênc Cultura 39:1060–1063

    Google Scholar 

  • Loop KA, Miller JD, Limpus CJ (1995) Nesting by the hawksbill turtle (Eretmochelys imbricata) on Milman Island, Great Barrier Reef, Australia. Wildl Res 22:241–252

    Article  Google Scholar 

  • Maranhão GMB (2003) Distribuição espaço-temporal da meiofauna e nematofauna no ecossistema recifal de Porto de Galinhas, Ipojuca, Pernambuco, Brasil. Dissertation, Federal University of Pernambuco

  • Marcovaldi MA, Sales G, Thomé JCA, Silva ACCD, Gallo BMG, Lima EHSM, Lima EP, Bellini C (2006) Sea turtles and fishery interactions in Brazil: identifying and mitigating potential conflicts. Mar Turt Newsl 112:4–8

    Google Scholar 

  • Meadows PS, Meadows A, Murray MH (2012) Biological modifiers of marine benthic seascapes: Their role as ecosystem engineers. Geomorphology 157–158:31–48

    Article  Google Scholar 

  • Meziane T, Sanabe MC, Tsuchiya M (2002) Role of fiddler crabs of a subtropical intertidal flat on the fate of sedimentary fatty acids. J Exp Mar Biol Ecol 270:191–201

    Article  CAS  Google Scholar 

  • Morgado EH (1980) A endofauna de Schizoporella unicornis (Johnston, 1847) (Bryozoa), no litoral norte de São Paulo. Dissertation, University State of Campinas

  • Nogueira JMM (2000) Anelídeos poliquetas associados ao coral Mussismilia hispida (Verrill, 1868) em ilhas do litoral do Estado de São Paulo. Phyllodocida, Amphinomida, Eunicida, Spionida, Terebellida e Sabellida. PhD thesis, Universidade de São Paulo, São Paulo

  • Norling P, Kautsky N (2007) Structural and functional effects of Mytilus edulis on diversity of associated species and ecosystem functioning. Mar Ecol Prog Ser 351:163–17

    Article  Google Scholar 

  • Oláfsson E (2003) Do macrofauna structure meiofauna assemblages in marine soft-bottoms? Vie Millieu 53:249–265

    Google Scholar 

  • Paiva PC (1990) Padrões de distribuição e estrutura tr6fica dos anelídeos poliquetas da plataforma continental do litoral norte do Estado de São Paulo. Dissertação de mestrado. Universidade de São Paulo

  • Pfaller JB, Bjorndal KA, Reich KJ, Williams KL, Frick MG (2006) Distribution patterns of epibionts on the carapace of loggerhead turtles, Caretta caretta. J Mar Biol Assoc UK – Biodiversity Records 5381:1. http://www.mba.ac.uk/jmba/ Accessed 9 August 2013

  • Reis MO (1995) Estrutura e dinâmica da macrofauna bêntica de poliquetos da região entremarés de praias da Ilha de São Sebastião (SP). Dissertation, University State of Paulista

  • Raes M, Vanreusel A (2005) The metazoan meiofauna associated with a cold-water coral degradation zone in the Porcupine Seabight (NE Atlantic). In: Freiwald A., Roberts J.M. (eds), Cold-water Corals and Ecosystems. Berlin, pp 821–847

  • Rullier F (1974) Quelques annélides polychètes de Cuba recueillies dans les éponges. Trav Mus Hist Nat 14:9–77

    Google Scholar 

  • San Martín G (2003) Fauna Iberica. Vol. 21. Annelida, Polychaeta II: Syllidae. Museo Nacional de Ciencias Naturales. CSIC, Madrid

    Google Scholar 

  • Santa-Isabel LM, Leão ZMAN, Peso-Aguiar MC (2000) Polychaetes from Guarajuba coral reefs, Bahia, Brasil. Bull Mar Sci 67:645–653

    Google Scholar 

  • Santos JP, Soares CMA (1999) Crustacea Amphipoda Gammaridae da praia de piedade, Jaboatão dos Guararapes-Pernambuco-Brasil. Trabalho Oceanog 27:61–72

    Google Scholar 

  • Sarmento V, Barreto FS, Santos JP (2011) The response of meiofauna to human trampling on coral reefs. Sci Mar 75:559–570

    Article  Google Scholar 

  • Schärer M (2003) A survey of the epibiota of Eretmochelys imbricata (Testudines: Cheloniidae) of Mona Island, Puerto Rico. Rev Biol Trop 51:87–90

    PubMed  Google Scholar 

  • Serrano A, San Martín G, López E (2006) Ecology of Syllidae (Annelida: Polychaeta) from shallow rocky environments in the Cantabrian Sea (South Bay of Biscay). Sci Mar 225–235

  • Silva KPB (2012) Diversidade e heterogeneidade espacial de Nmatoda no ecossistema recifal de Paripueira, AL-Brasil. Dissertation, Federal University of Alagoas

  • Snelgrove PVR (1994) Hydrodynamic enhancement of invertebrate larval settlement in microdepositional environments: colonizing tray experiments in a muddy habitat. J Exp Mar Biol Ecol 176:149–166

    Article  Google Scholar 

  • Souza RCR (1989) A fauna dos bancos de areia de Phragmatopoma lapidosa Kinberg, 1867 (Annelida, Polychaeta) da região de Ubatuba, SP. Dissertation, University State of Campinas

  • Spaccesi FG, Rodrigues Capítulo A (2012) Benthic communities on hard substrates covered by Limnoperna fortunei Dunker (Bivalvia, Mytilidae) in a freshwater estuarine beach (Río de la Plata, Argentina). J Limnol 71:144–153

  • Sundelin B, Elmgren E (1991) Meiofauna of an experimental soft bottom ecosystem- effects of macrofauna and cadmium exposure. Mar Ecol Prog Ser 70:245–255

    Article  Google Scholar 

  • Torres-Pratts H, Schärer HMT, Schizas NV (2009) Genetic diversity of Chelonibia caretta, commensal barnacles of the endangered hawksbill sea turtle Eretmochelys imbricata from the Caribbean (Puerto Rico). J Mar Biol Assoc UK 89:719–725

    Article  CAS  Google Scholar 

  • Urbaniak GC, Plous S (2011) Research Randomizer (Version 3.0) [Computer software]. http://www.randomizer.org/ Accessed 10 February 2013

  • Vivaldo SG, Sarabia DO, Salazar CP, Hernandez AG, Lezama JR (2006) Identification of parasites and epibionts in the olive ridley turtle (Lepidochelys olivacea) that arrived to the beaches of Michoacan and Oaxaca, Mexico. Vet Mex 37:431–440

    Google Scholar 

  • Wahl M (1989) Marine Epibiosis.1.Fouling and antifouling - some basic aspects. Mar Ecol Prog Ser 58:175–189

    Article  Google Scholar 

  • Watzin MC (1983) The effects of meiofauna on settling macrofauna: meiofauna may structure macrofaunal communities. Oecologia 59(2):163–166

    Article  Google Scholar 

  • Watzin MC (1986) Larval settlement into marine soft-sediment systems: Interactions with the meiofauna. J Exp Mar Biol Ecol 98(1–2):65–113

    Article  Google Scholar 

  • Witzell WN (1983) Synopsis of biological data on the hawksbill turtles, Eretmochelys imbricata (Linnaeus, 1766). FAO Fish Synop 137:1–86

    Google Scholar 

  • Young PS (1991) The superfamily Coronuloidea leach (Cirripedia, Balanomorpha) from de Brazilian coast, with redescription of Stomatolepas species. Crustaceana 61:190–212

    Article  Google Scholar 

  • Zobrist EC, Coull BC (1992) Meiobenthic interactions with macrobenthic larvae and juveniles: an experimental assessment of the meiofaunal bottleneck. Mar Ecol Prog Ser 88:1–8

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by FACEPE (Fundação de Amparo a Ciência e Tecnologia) grant (IBPG-0027-2.04/10) to the first author and by Federal University of Pernambuco for the laboratory support and the ONG Ecoassociados for the essential help in the field. JI is supported by a Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme (Grant Agreement FP7-PEOPLE-2011-IEF No 300879). The authors acknowledge the Guest Editor, Gustavo Fonseca, and anonymous referees for their valuable comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. A. P. Santos.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOCX 25.4 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Corrêa, G.V.V., Ingels, J., Valdes, Y.V. et al. Diversity and composition of macro- and meiofaunal carapace epibionts of the hawksbill sea turtle (Eretmochelys imbricata Linnaeus, 1822) in Atlantic waters. Mar Biodiv 44, 391–401 (2014). https://doi.org/10.1007/s12526-013-0189-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-013-0189-9

Keywords

Navigation