Skip to main content
SpringerLink
Log in

Hitchhikers reveal cryptic host behavior: new insights from the association between Planes major and sea turtles in the Pacific Ocean

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

Abstract

Studies that incorporate information from habitat-specific ecological interactions (e.g., epibiotic associations) can reveal valuable insights into the cryptic habitat-use patterns and behavior of marine vertebrates. Sea turtles, like other large, highly mobile marine vertebrates, are inherently difficult to study, and such information can inform the implementation of conservation measures. The presence of epipelagic epibionts, such as the flotsam crab Planes major, on sea turtles strongly suggests that neritic turtles have recently occupied epipelagic habitats (upper 200 m in areas with >200 m depth) and that epipelagic turtles spend time at or near the surface. We quantified the effects of turtle species, turtle size, and habitat (neritic or epipelagic) on the frequency of epibiosis (F 0) by P. major on sea turtles in the Pacific Ocean. In neritic habitats, we found that loggerhead (F 0 = 27.6 %) and olive ridley turtles (F 0 = 26.2 %) host crabs frequently across a wide range of body sizes, and green turtles almost never host crabs (F 0 = 0.7 %). These results suggest that loggerheads and olive ridleys display variable/flexible epipelagic-neritic transitions, while green turtles tend to transition unidirectionally at small body sizes. In epipelagic habitats, we found that loggerheads host crabs (F 0 = 92.9 %) more frequently than olive ridleys (F 0 = 50 %) and green turtles (F 0 = 38.5 %). These results suggest that epipelagic loggerheads tend to spend more time at or near the surface than epipelagic olive ridleys and green turtles. Results of this study reveal new insights into habitat-use patterns and behavior of sea turtles and display how epibiont data can supplement data from more advanced technologies to gain a better understanding of the ecology of marine vertebrates during cryptic life stages.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alfaro-Shigueto A, Mangel JC, Bernedo F, Dutton PH, Seminoff JA, Godley BJ (2011) Small-scale fisheries of Peru: a major sink for marine turtles in the Pacific. J Appl Ecol 48:1432–1440

    Article  Google Scholar 

  • Angulo-Lozano L, Nava-Duran PE, Frick MG (2007) Epibionts of olive ridley turtles nesting at Playa Ceuta, Sinaloa, Mexico. Mar Turt Newsl 118:13–14

    Google Scholar 

  • Barceló C, Peckham SH, Marinovic B (2008) What do hitchhikers eat? The diet of Planes cyaneus and their association with loggerhead and olive ridley turtles off the Pacific coast of Baja California Sur, Mexico. NOAA Tech Memo NMFS-SEFSC-569, p 118

  • Bolten AB (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of the sea turtles, vol II. CRC Press, Boca Raton, pp 243–257

    Google Scholar 

  • Brown CH, Brown WM (1995) Status of sea turtles in the Southeastern Pacific: emphasis on Perú. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington, pp 235–240

    Google Scholar 

  • Bugoni L, Fiedler FN, Monteiro DS, Estima SC (2007) Eretmochelys imbricata (Hawksbill), Chelonia mydas (Green), and Caretta caretta (loggerhead) Seaturtle. Epizoans Herpetol Rev 38:199–200

    Google Scholar 

  • Caine EA (1986) Carapace epibionts of nesting loggerhead sea turtles: Atlantic coast of USA. J Exp Mar Biol Ecol 95:15–26

    Article  Google Scholar 

  • Carranza A, Domingo A, Verdi A, Forselledo R, Estrades A (2003) First report of an association between Planes cyaneus (Decapoda: Grapsidae) and loggerhead sea turtles in the Southwestern Atlantic Ocean. Mar Turt Newsl 103:5–7

    Google Scholar 

  • Chace FA (1951) The oceanic crabs of the genera Planes and Pachygrapsus. Proc US Natl Mus 101:65–103

    Article  Google Scholar 

  • Crane J (1937) The Templeton Crocker Expedition, III: Brachygnathous crabs from the Gulf of California and the west coast of Lower California. Zoologica 22:47–48

    Google Scholar 

  • Davenport J (1994) A cleaning association between the oceanic crab Planes minutus and the loggerhead sea turtle Caretta caretta. J Mar Biol Assoc UK 74:735–737

    Article  Google Scholar 

  • Dellinger T, Davenport J, Wirtz P (1997) Comparisons of social structure of Columbus crabs living on loggerhead sea turtles and inanimate flotsam. J Mar Biol Assoc UK 77:185–194

    Article  Google Scholar 

  • Eckert KL, Eckert SA (1988) Pre-reproductive movements of leatherback sea turtles (Dermochelys coriacea) nesting in the Caribbean. Copeia 1988:400–406

    Article  Google Scholar 

  • Faxon W (1895) Reports on an exploration off the west coasts of Mexico, Central and South America, and off the Galapagos Islands, in charge of Alexander Agassiz, by the U.S. Fish Commission steamer, Albatross, during 1891, Lieut-Commander Z.L. Tanner, U.S.N., commanding, 15: The stalk-eyed Crustacea. Mem Mus Comp Zool 18:1–292

    Google Scholar 

  • Frick MG, Pfaller JB (2013) Sea turtle epibiosis. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol III. CRC Press, Boca Raton, pp 399–426

    Chapter  Google Scholar 

  • Frick MG, Williams KL, Robinson M (1998) Epibionts associated with nesting loggerhead sea turtles (Caretta caretta) in Georgia, USA. Herpetol Rev 29:211–214

    Google Scholar 

  • Frick MG, Williams KL, Veljacic D (2000) Additional evidence supporting a cleaning association between epibiotic crabs and sea turtles: how will the harvest of Sargassum seaweed impact this relationship? Mar Turt Newsl 20:11–13

    Google Scholar 

  • Frick MG, Williams KL, Bolten AB, Bjorndal KA, Martins HR (2004) Diet and fecundity of Columbus crabs, Planes minutus, associated with oceanic-stage loggerhead sea turtles, Caretta caretta, and inanimate flotsam. J Crustacean Biol 24:350–355

    Article  Google Scholar 

  • Frick MG, Williams KL, Bresette M, Singewald DA, Herren RM (2006) On the occurrence of Columbus crabs (Planes minutus) from loggerhead turtles in Florida, USA. Mar Turt Newsl 114:12–14

    Google Scholar 

  • Frick MG, Kopitsky K, Bolten AB, Bjorndal KA, Martins HR (2011) Sympatry in grapsoid crabs (genera Planes and Plagusia) from olive ridley sea turtles (Lepidochelys olivacea), with descriptions of crab diets and masticatory structures. Mar Biol 158:1699–1708

    Article  Google Scholar 

  • Graham RT, Witt MJ, Castellanos DW, Remolina F, Maxwell S, Godley BJ, Hawkes LA (2012) Satellite tracking of manta rays highlights challenges to their conservation. PLoS one 7:e36834

    Article  CAS  Google Scholar 

  • Guess RC (1981) A pacific loggerhead captured off California’s northern Channel Islands. Herpetol Rev 12:15

    Google Scholar 

  • Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002) Size-related differences in feeding habitat use of adult female loggerhead turtles Caretta caretta around Japan determined by stable isotope analyses and satellite telemetry. Mar Ecol Prog Ser 233:273–281

    Article  Google Scholar 

  • Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 146:52–64

    Article  Google Scholar 

  • Hatase H, Omuta K, Tsukamoto K (2010) Oceanic residents, neritic migrants: a possible mechanism underlying foraging dichotomy in adult female loggerhead turtles (Caretta caretta). Mar Biol 157:1337–1342

    Article  Google Scholar 

  • Hays GC, Åkesson S, Broderick AC, Glen F, Godley BJ, Luschi DJ, Martin C, Metcalfe JD, Papi F (2001) The diving behavior of green turtles undertaking oceanic migration to and from Ascension Island: dive durations, dive profiles and depth distribution. J Exp Biol 204:4093–4098

    CAS  Google Scholar 

  • Heppell SS, Crowder LB, Menzel TR (1999) Life table analysis of long-lived marine species with implications for conservation and management. In: Musick JA (ed) Life in the slow lane: ecology and conservation of long-lived marine animals. Am Fish Soc, Bethesda, pp 137–148

    Google Scholar 

  • Hernández-Vásquez S, Valadez-González C (1998) Observaciones de los epizoarios encontrados sobre la tortuga golfina Lepidochelys olivacea en La Gloria, Jalisco, México. Cienc Mar 24:119-125

  • Hirji KF, Tan SJ, Elashoff RM (1991) A quasi-exact test for comparing two binomial proportions. Stat Med 10:1137–1153

    Article  CAS  Google Scholar 

  • Hosono T, Minami H (2011) Stable isotope analysis of epibiotic caprellids (Amphipoda) on loggerhead turtles provides evidence of turtle’s feeding history. In: Asakura A (ed) New frontiers in Crustacean Biology: proceedings of the TCS summer meeting, Tokyo, 20-24 September 2009. Koninklijke Brill NV, Leiden, pp 299–309

    Chapter  Google Scholar 

  • Howell EA, Dutton PH, Polovina JJ, Bailey H, Parker DM, Balazs GH (2010) Oceanographic influence on the dive behavior of juvenile loggerhead turtles (Caretta caretta) in the North Pacific Ocean. Mar Biol 157:1011–1026

    Article  Google Scholar 

  • Hubbs CL (1977) First record of mating of ridley turtles in California, with notes on commensals, characters, and systematics. Calif Fish Game 63:263–267

    Google Scholar 

  • Ishihara T, Kamezaki N, Matsuzawa Y, Iwamoto F, Oshika T, Miyagata Y, Ebisui C, Yamashita S (2011) Reentry of juvenile and subadult loggerhead turtles into natal waters of Japan. Curr Herpetol 30:63–68

    Article  Google Scholar 

  • Jones TT, Seminoff JA (2013) Feeding biology: advances from field-based observations, physiological studies, and molecular techniques. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol III. CRC Press, Boca Raton, pp 211–247

    Chapter  Google Scholar 

  • Killingley JS, Lutcavage M (1983) Loggerhead turtle movements reconstructed from 18O and 13C profiles from commensal barnacle shells. Estuar Coast Shelf Sci 16:345–349

    Article  Google Scholar 

  • Kopitsky KL, Pitman RL, Dutton PH (2005) Aspects of olive ridley feeding ecology in the eastern tropical Pacific. NOAA Tech Memo. NMFS-SEFSC-528, p 217

  • Lazo-Wasem E, Pinuo T, Peña de Niz A, Feuerstein A (2011) Epibionts associated with the nesting turtles Lepidochelys olivacea and Chelonia mydas in Jalisco, Mexico: a review and field guide. Bull Peabody Mus Nat Hist 52:221–240

    Article  Google Scholar 

  • Limpus CJ, Limpus DJ (2003) Biology of the loggerhead turtle in western south Pacific Ocean foraging areas. In: Bolten AB, Witherington BE (eds) Biology and conservation of the loggerhead sea turtle. Smithsonian Institution Press, Washington, pp 93–113

    Google Scholar 

  • Miranda L, Moreno RA (2002) Epibiontes de Lepidochelys olivacea (Eschscholtz, 1829) (Reptilia: Testudinata: Cheloniidae) en la región centro sur de Chile. Rev Biol Mar Oceanogr 37:145–146

    Article  Google Scholar 

  • Musick JA, Limpus CJ (1997) Habitat utilization and migration in juvenile sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 137–163

    Google Scholar 

  • Nichols WJ, Resendiz A, Mayoral-Russeau C (2000) Biology and Conservation of Loggerhead Turtles (Caretta caretta) in Baja California, Mexico. NOAA Tech Memo NMFS-SEFSC-443, p 169-171

  • Parker DM, Cooke WJ, Balazs GH (2005) Diet of oceanic loggerhead sea turtles (Caretta caretta) in the central North Pacific. Fish Bull 103:142–152

    Google Scholar 

  • Peckham SH, Maldonado-Diaz D, Tremblay Y, Ochoa R, Polovina J, Balazs G, Dutton PH, Nichols WJ (2011) Demographic implications of alternative foraging strategies in juvenile loggerhead turtles Caretta caretta of the North Pacific Ocean. Mar Ecol Prog Ser 425:269–280

    Article  Google Scholar 

  • Pfaller JB, Frick MG, Reich KJ, Williams KL, Bjorndal KA (2008) Carapace epibionts of loggerhead turtles (Caretta caretta) nesting at Canaveral National Seashore, Florida. J Nat Hist 42:1095–1102

    Article  Google Scholar 

  • Plotkin PT (2010) Nomadic behaviour of the highly migratory olive ridley sea turtle Lepidochelys olivacea in the eastern tropical Pacific Ocean. Endanger Species Res 13:33–40

    Article  Google Scholar 

  • Polovina JJ, Howell E, Parker DM, Balazs GH (2003) Dive-depth distribution of loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea) sea turtles in the central North Pacific: might deep longline sets catch fewer turtles? Fish Bull 101:189–193

    Google Scholar 

  • Polovina JJ, Balazs GH, Howell EA, Parker DM, Seki MP, Dutton PH (2004) Forage and migration habitat of loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea) sea turtles in the central North Pacific Ocean. Fish Oceanogr 13:36–51

    Article  Google Scholar 

  • Pons M, Verdi A, Domingo A (2011) The pelagic crab Planes cyaneus (Dana, 1851) (Decapoda, Brachyura, Grapsidae) in the southwestern Atlantic Ocean in association with loggerhead sea turtles and buoys. Crustaceana 84:425–434

    Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. ISBN 3-900051-07-0

  • Rathbun MJ (1902) Papers from the Hopkins Stanford Galapagos Expedition, 1898–1899, VIII: Brachyura and Macura. Proc Wash Acad Sci 4:275–292

    Google Scholar 

  • Reich KJ, Bjorndal KA, Frick MG, Witherington BE, Johnson C, Bolten AB (2010) Polymodal foraging in adult female loggerheads (Caretta caretta). Mar Biol 157:651–663

    Article  Google Scholar 

  • Rice MR, Balazs GH (2008) Diving behavior of the Hawaiian green turtle (Chelonia mydas) during oceanic migrations. J Exp Mar Biol Ecol 356:121–127

    Article  Google Scholar 

  • Saba VS (2013) Oceanic habits and habitats: Dermochelys coriacea. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol III. CRC Press, Boca Raton, pp 163–188

    Chapter  Google Scholar 

  • Sakai T (1939) Studies on the crabs of Japan, IV: Brachygnatha, Brachyrhyncha. Yokendo, LTD, Tokyo, pp 365–741

    Google Scholar 

  • Schärer MT (2001) A survey of the epibiota of Eretmochelys imbricata (Testudines: Cheloniidae) of Mona Island, Puerto Rico. Rev Biol Trop 51:87–89

    Google Scholar 

  • Schweigger E (1964) El litoral Peruano. Grafica Morsom SA, Lima

    Google Scholar 

  • Seminoff JA, Jones TT, Resendiz A, Nichols WJ, Chaloupka MY (2003) Monitoring green turtles (Chelonia mydas) at a coastal foraging area in Baja California, Mexico: multiple indices describe population status. J Mar Biol Ass UK 83:1355–1362

    Article  Google Scholar 

  • Seminoff JA, Zárate P, Coyne MC, Foley DG, Parker D, Lyon BN, Dutton PH (2007) Post-nesting migrations of Galápagos green turtles Chelonia mydas in relation to oceanographic conditions: integrating satellite telemetry with remote sensed ocean data. Endanger Species Res 4:57–72

    Article  Google Scholar 

  • Steinbeck J, Ricketts EF (1941) Sea of Cortez. Viking Press, New York

    Google Scholar 

  • Wahl M, Mark O (1999) The predominately facultative nature of epibiosis: experimental and observational evidence. Mar Ecol Prog Ser 187:59–66

    Article  Google Scholar 

  • Wicksten MK, Behrens MD (2000) New record of the pelagic crab Planes cyaneus in California (Brachyura: Grapsidae). SCAMIT Newsl 19:7

    Google Scholar 

  • Work TM, Balazs GH (2010) Pathology and distribution of sea turtles landed as bycatch in the Hawaii-based North Pacific pelagic longline fishery. J Wildl Dis 46:422–432

    Article  Google Scholar 

Download references

Acknowledgments

We thank all organizations and people that either supported or participated in crab collections in Japan (Sea Turtle Association of Japan, H Fukuie, S Watanabe, K Kawano, K Saito, M Hara, S Yamashita, K Hashimoto, K Ebisui, and Y Yasuoka), Hawaii (USGS National Wildlife Health Center, Honolulu Field Station, T Work), Samoa, Baja California Sur, México (David & Lucille Packard Foundation, US Fish & Wildlife Service, ProPeninsula, The Ocean Foundation, Equipo ProCaguama, Grupo Tortuguero V de la Toba, J Lucero, JM Rodríguez Barón), Mexico and Central America in 2003 (NMFS Southwest Fisheries Science Center and NOAA, and all scientific and support personnel working on cruises), and Peru (Darwin Sustainable Artisanal Fisheries Initiative—Peru). We also thank J Ferguson (University of Florida, Department of Biology) for statistical advice, and J Houghton and two anonymous reviewers for their valuable scientific and editorial comments.

Author information

Authors and Affiliations

  1. Archie Carr Center for Sea Turtle Research, Department of Biology, University of Florida, Gainesville, FL, 32611, USA

    Joseph B. Pfaller, Alan B. Bolten & Karen A. Bjorndal

  2. Caretta Research Project, Savannah, GA, 31412, USA

    Joseph B. Pfaller

  3. ProDelphinus, Enrique Palacios, 630-204, Lima 18, Peru

    Joanna Alfaro-Shigueto & Jeffrey C. Mangel

  4. Centre for Ecology and Conservation, University of Exeter, Penryn, TR10 9EZ, Cornwall, UK

    Joanna Alfaro-Shigueto & Jeffrey C. Mangel

  5. Marine Turtle Research Program, National Ocean and Atmospheric Administration, National Marine Fisheries Service, Pacific Islands Fisheries Science Center, Honolulu, HI, 96818, USA

    George H. Balazs

  6. Sea Turtle Association of Japan, Osaka, Japan

    Takashi Ishihara

  7. Suma Aqualife Park, Hyogo, Japan

    Takashi Ishihara

  8. Rising Tides Restoration, Dover, DE, 19904, USA

    Kerry Kopitsky

  9. Center for Ocean Solutions, Stanford University, Pacific Grove, CA, 93950, USA

    S. Hoyt Peckham

Authors
  1. Joseph B. Pfaller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joanna Alfaro-Shigueto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. George H. Balazs
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takashi Ishihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kerry Kopitsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeffrey C. Mangel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Hoyt Peckham
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alan B. Bolten
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Karen A. Bjorndal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph B. Pfaller.

Additional information

Communicated by J. D. R. Houghton.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 77 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pfaller, J.B., Alfaro-Shigueto, J., Balazs, G.H. et al. Hitchhikers reveal cryptic host behavior: new insights from the association between Planes major and sea turtles in the Pacific Ocean. Mar Biol 161, 2167–2178 (2014). https://doi.org/10.1007/s00227-014-2498-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2498-3

Keywords

Search

Navigation