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Larval Development and Complemental Males in Chelonibia Testudinaria, a Barnacle Commensal with Sea Turtles

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Abstract That some barnacles are obligate commensals of sea turtles has long been known; however, little attention has focused on understanding the details of this association. In particular, early life-history traits of turtle barnacles, which may be key to establishing the association, have not been well studied. Here we present the first complete description of larval development in a turtle barnacle. Embryos were collected from Chelonibia testudinaria, a cosmopolitan and conspicuous species, and reared through metamorphosis in the laboratory. We followed sequential molting and described each stage using light microscopy. Development proceeded over nine days at 25°C and the characteristic cirriped pattern of six naupliar stages followed by a cyprid larva was observed. Implications for the association of barnacles with sea turtles are discussed relative to spatio-temporal aspects of cyprid attachment and the life history of sea turtles. Barnacle reproduction typically involves cross-fertilization between hermaphrodites but small complemental males occur in some species. In C. testudinaria, small individuals attached to hermaphrodites were confirmed to be exclusively male. They were located in the external depressions between the shell plates of hermaphrodites, within pits perhaps specialized for their settlement. This attachment location, external to and below the orifice of the hermaphrodite shell, is unique for complemental males. It is not known whether the males of C. testudinaria remain small permanently or eventually grow to become hermaphroditic, as do protandric complemental males in C. patula. Their small size may provide advantages in reducing drag and their attachment location may afford protection from removal.

Affiliations: 1: University of Hawaii, Pacific Biomedical Research Center, Kewalo Marine Lab, 41 Ahui Street, Honolulu, Hawaii 96813, U.S.A. (corresponding author (JDZ); (MGH)


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1. Anderson D. T. 1965 "Embryonic and larval development and segment formation in Ibla quadrivalvis Cuv. (Cirripedia)." Australian Journal of Zoology Vol 13 1 15
2. Anderson D. T. 1986 "The circumtropical barnacle Tetraclitella divisa (Nilsson-Cantell) (Balanomorpha, Tetraclitidae): cirral activity and larval development." Proceedings of the Linnean Society of New South Wales Vol 109 107 116
3. Anderson D. T. 1994 "Barnacles: Structure, Function, Development and Evolution." Chapman and Hall, London
4. Anil A. C. , Desai D. , Khandeparker L. 2001 "Larval development and metamorphosis in Balanus amphitrite Darwin (Cirripedia; Thoracica): significance of food concentration, temperature and nucleic acids." Journal of Experimental Marine Biology and Ecology Vol 263 125 141
5. Balazs G. H. 1995 "Growth rates of immature green turtles in the Hawaiian archipelago." Pp. 117125 in K. A. Bjorndal, ed. Biology and Conservation of Sea Turtles. Smithsonian Institution Press, Washington, D.C
6. Bassindale R. 1936 "The developmental stages of three English barnacles, Balanus balanoides (Linn.), Chthamalus stellatus (Poli) and Verruca stroemia (O.F. Mller)." Proceedings of the Zoological Society of London Vol 106 57 74
7. Batham E. J. 1945 "Description of female, male and larval forms of a tiny stalked barnacle, Ibla idiotica n. sp." Transactions of the Royal Society of New Zealand, Zoology Vol 75 347 356
8. Bjorndal K. A. , Jackson J. B C. 2003 "Roles of sea turtles in marine ecosystems: reconstructing the past." Pp. 259273 in P. L. Lutz, J. A. Musick, and J. Wyneken, eds. The Biology of Sea Turtles Volume II. CRC Press, Washington, D.C
9. Chen Y. 1989 "Cirripedia." Pp. 3873 in C. Wei and Y. Chen, eds. Fauna of Zhejiang: Crustacea, Vol. 6. Zhejiang Science and Technology Publishing House, Hangzhou, Zhejiang
10. Clare A. S. 1995 "Chemical signals in barnacles: old problems, new approaches." Pp. 4967 in F. R. Schram and J. T. Heg, eds. New Frontiers in Barnacle Evolution, Crustacean Issues, Vol. 5. A. A. Balkema, Rotterdam
11. Costlow J. D. Jr. , Bookhout C. G. 1958 "Larval development of Balanus amphitrite var. denticulata Broch reared in the laboratory." Biological Bulletin (Woods Hole) Vol 114 284 295
12. Crisp D. J. 1983 "Chelonobia patula (Ranzani), a pointer to the evolution of the complemental male." Marine Biology Letters Vol 4 281 294
13. Crisp D. J. 1986 "A comparison between reproduction of high- and low-latitude barnacles, including Balanus balanoides and Tetraclita (Tesseropora) pacifica." Pp. 6984 in M.-F. Thompson, R. Sarojini, and R. Nagabhushanam, eds. Biology of Benthic Marine Organisms: Techniques and Methods as Applied to the Indian Ocean. Oxford and IBH Publishing Co., New Delhi
14. Crisp D. J. , Meadows P. S. 1962 "The chemical basis of gregariousness in cirripedes." Proceedings of the Royal Society of London series B, Biological Science Vol 156 500 520
15. Crisp D. J. , Meadows P. S. 1963 "Adsorbed layers: the stimulus to settlement in barnacles." Proceedings of the Royal Society of London series B, Biological Science Vol 158 364 387
16. Darwin C. R. 1852 "A Monograph on the Sub-class Cirripedia, with Figures of All the Species." The Lepadidae; or, Pedunculated Cirripedes. The Ray Society, London (1851)
17. Darwin C. R. 1854 "A Monograph on the Sub-class Cirripedia, with Figures of All the Species." The Balanidae (or Sessile Cirripedes); the Verrucidae, etc. The Ray Society, London
18. Edmondson C. H. 1946 "Reef and Shore Fauna of Hawaii." Bishop Museum, Honolulu, Hawaii
19. Foster B. A. 1983 "Complemental males in the barnacle Bathylasma alearum (Cirripedia: Pachylasmidae)." Pp. 133139 in J. K. Lowry, ed. Papers from the Conference on the Biology and Evolution of Crustacea, Australian Museum Memoir Vol. 18. The Australian Museum, Sydney, New South Wales
20. Foster B. A. 1987 "Barnacle ecology and adaptations." Pp. 113134 in A. J. Southward, ed. Barnacle Biology, Crustacean Issues, Vol. 5. A. A. Balkema, Rotterdam
21. Frick M. G. , Slay C. K. 2000 "Caretta caretta (Loggerhead Sea Turtle) epizoans." Herpetological Review Vol 31 102 103
22. Frick M. G. , Williams K. L. , Robinson M. 1998 "Epibionts associated with nesting loggerhead sea turtles (Caretta caretta) in Georgia, U.S.A." Herpetological Review Vol 29 211 214
23. Gomez E. D. 1975 "Sex determination in Balanus (Conopea) galeatus (L.) (Cirripedia Thoracica)." Crustaceana Vol 28 105 107
24. Green D. 1998 "Epizoites of Galapagos green turtles." P. 63 in R. Byles and Y. Fernandez, eds. Proceedings of the Sixteenth Annual Symposium on Sea Turtle Biology and Conservation. National Marine Fisheries Service
25. Hadfield M. G. 1977 "Chemical interactions in larval settling of a marine gastropod." Pp. 403413 in D. J. Faulkner and W. H. Fenical, eds. Marine Natural Products Chemistry. Plenum, New York, New York
26. Hadfield M. G. , Paul V. J. 2001 "Natural chemical cues for settlement and metamorphosis of marine invertebrate larvae." Pp. 431461 in J. B. McClintock and B. J. Baker, eds. Marine Chemical Ecology. CRC Press, Boca Raton, Florida
27. Hadfield M. G. , Unabia C. R C. , Smith C. M. , Michael T. M. 1994 "Settlement preferences of the ubiquitous fouler Hydroides elegans." Pp. 6574 in M.-F. Thompson, R. Nagabhushanam, R. Sarojini, and M. Fingerman, eds. Recent Developments in Biofouling Control. Oxford and IBH Publishing Co., New Delhi
28. Henry D. P. , McLaughlin P. A. 1967 "A revision of the subgenus Solidobalanus Hoek (Cirripedia Thoracica) including a description of a new species with complemental males." Crustaceana Vol 12 43 58
29. Heg J. T. 1995 "The biology and life cycle of the Rhizocephala (Cirripedia)." Journal of the Marine Biological Association of the United Kingdom Vol 75 517 550
30. Jackson J. B C. 2001 "What was natural in the coastal oceans?." Proceedings of the National Academy of Sciences U.S.A Vol 98 5411 5418
31. Johnstone J. , Frost W. E. 1927 "Anelasma squalicola (Lovn): its general morphology." Proceedings and Transactions of the Liverpool Biological Society Vol 35 27 91
32. Klepal W. 1987 "A review of the comparative anatomy of the males in cirripedes." Oceanography and Marine Biology Annual Review Vol 25 285 351
33. Lang W. H. 1979 "Larval development of shallow water barnacles of the Carolinas (Cirripedia: Thoracica) with keys to naupliar stages." NOAA Technical Report, NMFS Circular Vol 421 1 39
34. Lewis C. A. 1978 "A review of substratum selection in free-living and symbiotic cirripedes." Pp. 207218 in F.-S. Chia and M. E. Rice, eds. Settlement and Metamorphosis of Marine Invertebrate Larvae. Elsevier, New York, New York
35. Loza A. L. , Lopez-Jurado L. F. In press.) "Comparative study of the epibionts on pelagic and mature female loggerhead turtles on the Canary and Cape Verde Islands." Proceedings of the Twenty-Fourth Annual Symposium on Sea Turtle Biology and Conservation. NOAA Technical Memorandum
36. Lucus M. I. , Walker G. L. , Holland D. L. , Crisp D. J. 1979 "An energy budget for the free-swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia)." Marine Biology Vol 55 221 229
37. McLaughlin P. A. , Henry D. P. 1972 "Comparative morphology of complemental males in four species of Balanus (Cirripedia Thoracica)." Crustaceana Vol 22 13 30
38. Mignucci-Giannoni A. A. , Beck C. A. , Montoya-Ospina R. A. , Williams E. H. Jr. 1999 "Parasites and commensals of the West Indian manatee from Puerto Rico." Journal of the Helminthological Society of Washington Vol 66 67 69
39. Miller J. D. 1997 "Reproduction in sea turtles." Pp. 5181 in P. L. Lutz and J. A. Musick, eds. The Biology of Sea Turtles. CRC Press, New York, New York
40. Molenock J. , Gomez E. D. 1972 "Larval stages and settlement of the barnacle Balanus (Conopea) galeatus (L.) (Cirripedia Thoracica)." Crustaceana Vol 23 100 108
41. Monroe R. 1981 "Studies in the Coronulidae (Cirripedia): shell morphology, growth, and function, and their bearing on subfamily classification." Memoirs of the Queensland Museum Vol 20 237 251
42. Monroe R. , Garrett R. 1979 "Chelonibia testudinaria (L.) (Cirripedia, Coronulidae) on Crocodylus porosus Schneider, a new host record." Crustaceana Vol 36 108
43. Monroe R. , Limpus C. J. 1979 "Barnacles on turtles in Queensland waters with descriptions of three new species." Memoires of the Queensland Museum Vol 19 197 223
44. Moyse J. 1961 "The larval stages of Acasta spongites and Pyrgoma anglicum (Cirripedia)." Proceedings of the Zoological Society of London Vol 137 371 392
45. Moyse J. 1971 "Settlement and growth pattern of the parasitic barnacle Pyrgoma anglicum." Pp. 125141 in D. J. Crisp, ed. Fourth European Marine Biology Symposium. Cambridge University Press, Cambridge
46. Moyse J. 1987 "Larvae of lepadomorph barnacles." Pp. 329362 in A. J. Southward, ed. Barnacle Biology. Crustacean Issues, Vol. 5. A. A. Balkema, Rotterdam
47. Newman W. A. 1996 "Cirripedia; Suborders Thoracica and Acrothoracica." Pp. 453540 in J. Forest, ed. Trait de Zoologie, Crustacs, Tome VII, Fascicule 2. Masson, Paris
48. Newman W. A. , Ross A. 1977 "A living Tesseropora (Cirripedia: Balanomorpha) from Bermuda and the Azores; first records from the Atlantic since the Oligocene." Transactions of the San Diego Society of Natural History Vol 18 207 216
49. Newman W. A. , Ross A. 2001 "Prospectus on larval cirriped setation formulae, revisited." Journal of Crustacean Biology Vol 21 56 77
50. Pawlik J. R. 1992 "Chemical ecology of the settlement of benthic marine invertebrates." Oceanography and Marine Biology Annual Review Vol 30 273 335
51. Pillai N. K. 1956 "Development of Balanus amphitrite, with a note on the early larvae of Chelonibia testudinaria." Bulletin of the Central Research Institute of Kerala Vol 6 117 130
52. Pilsbry H. A. 1916 "The sessile barnacles (Cirripedia) contained in the collections of the U. S. National Museum; including a monograph of the American species." U.S. National Museum Bulletin Vol 93 1 366
53. Pritchard P. C H. 1997 "Evolution, phylogeny, and current status in the biology of sea turtles." Pp. 128 in P. L. Lutz and J. A. Musick, eds. The Biology of Sea Turtles. CRC Press, Boca Raton, Florida
54. Rawson P. D. , Macnamee R. , Frick M. G. , Williams K. L. 2003 "Phylogeography of the coronulid barnacle, Chelonibia testudinaria, from loggerhead sea turtles, Caretta caretta." Molecular Ecology Vol 12 2697 2706
55. Rees E. I S. , Walker G. 1993 "A record of the turtle barnacle Chelonobia in the Irish Sea." Porcupine Newsletter Vol 5 189
56. Rittschof D. , Forward R. B. Jr. , Cannon G. , Welch J. M. , McClary M. Jr. , Holm E. R. , Clare A. S. , Conova S. , McKelvey L. M. , Bryan P. , Van Dover C. L. 1998 "Cues and context: larval responses to physical and chemical cues." Biofouling Vol 12 31 44
57. Ross A. , Newman W. A. 1973 "Revision of the coral-inhabiting barnacles (Cirripedia: Balanidae)." Transactions of the San Diego Society of Natural History Vol 17 137 174
58. Ross A. , Newman W. A. 1995 "A coral-eating barnacle, revisited (Cirripedia, Pyrgomatidae)." Contributions to Zoology Vol 65 129 175
59. Seigel R. A. 1983 "Occurrence and effects of barnacle infestation on diamondback terrapins (Malaclemys terrapin)." American Midland Naturalist Vol 109 34 39
60. Zullo V. A. 1982 "A new species of the turtle barnacle Chelonibia Leach, 1817, (Cirripedia, Thoracica) from the Oligocene Mint Spring and Byram Formations of Mississippi." Mississippi Geology Vol 2 1 6

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