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Journal of Comparative Physiology A

, Volume 203, Issue 3, pp 233–243 | Cite as

Hard-shell mating in Neohelice granulata: the role of ecdysone in female receptivity and mate attraction

  • María P. Sal MoyanoEmail author
  • Tomás Luppi
  • Daniel A. Medesani
  • Colin L. McLay
  • Enrique M. Rodríguez
Original Paper
  • 148 Downloads

Abstract

Most brachyuran females become receptive during the intermolt period, a condition considered “derived”. However, as far as we know, studies testing the existence and function of pheromones in decapods are based on species which have mating linked to molting, a condition considered as “ancestral”. For the first time, we studied some physiological and morphological processes involved in Neohelice granulata intermolt female crabs becoming receptive and potentially attracting males. We found that receptive females have mobile vulvae opercula due to a softening process of the cuticle hinge which showed lower calcium levels compared to the hinge of unreceptive females. Local softening of the hinge was stimulated by a low concentration of ecdysone during the intermolt period. A putative pheromone liberated by receptive females to attract males is presumed to be released through the mobile vulvae and not through the urine.

Keywords

Ecdysteroids Hard-shell mating Cuticle softening Vulvae Pheromones 

Notes

Acknowledgements

We wish to thank to Martin Lorusso for his help in the laboratory experiments.We gratefully acknowledge the three anonymous reviewers for their helpful comments on the manuscript. 

Compliance with ethical standards

Funding

Financial support was given by Agencia Nacional de Promoción Científica y Tecnológica: PICTs 1317 and 0763. Grants from both Consejo Nacional de Investigaciones Científicas y Técnicas (PIPI2015, code 11220150100100CO) and the University of Buenos Aires (UBACYT 2016 scientific program, code 20020150100060BA) have also contributed to the current study.

Conflict of interest

The authors declare no competing or financial interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies on human participants performed by any of the authors.

References

  1. Andersen SO (1998) Characterization of proteins from arthrodial membranes of the lobster, Homarus americanus. Comp Biochem Phys A 121:375–383CrossRefGoogle Scholar
  2. Asai N, Fusetani N, Matsunaga S, Sasaki J (2000) Sex pheromones of the hair crab Erimacrus isenbeckii. Part 1: isolation and structures of novel ceramides. Tetrahedron 56:9895–9899CrossRefGoogle Scholar
  3. Atema J, Gagosian RB (1973) Behavioral responses of male lobsters to ecdysones. Mar Behav Physiol 2:15–20CrossRefGoogle Scholar
  4. Atema J, Steinbach M (2007) Chemical communication and social behavior of the lobster, Homarus americanus, and other decapod Crustacea. In: Duffy J, Thiel M (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, Oxford, pp 115–144CrossRefGoogle Scholar
  5. Bauer RT (2011) Chemical communication in decapods shrimps: the influence of mating and social systems on the relative importance of olfactory and contact pheromones. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 277–296Google Scholar
  6. Bélles X (1998) Endocrine effectors in insect vitellogenesis. In: Coast GM, Webster SG (eds) Recent advances in arthropod endocrinology. Cambridge University Press, Cambridge, pp 71–90Google Scholar
  7. Berry FC, Breithaupt T (2010) To signal or not to signal? Chemical communication by urine-borne signals mirrors sexual conflict in crayfish. BMC Biol 8:1–11CrossRefGoogle Scholar
  8. Borowsky B (1991) Patterns of reproduction of some amphipod crustaceans and insights into the nature of their stimuli. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 33–49Google Scholar
  9. Brockerhoff A, McLay CL (2005a) Comparative analysis of the mating strategies in grapsid crabs with special reference to two common intertidal crabs Cyclograpsus lavauxi and Helice crassa (Decapoda: Grapsidae) from New Zealand. J Crust Biol 25:507–520CrossRefGoogle Scholar
  10. Brockerhoff A, McLay CL (2005b) Mating behaviour, female receptivity and male-male competition in the intertidal crab Hemigrapsus sexdentatus (Brachyura: Grapsidae). Mar Ecol Prog Ser 290:179–191CrossRefGoogle Scholar
  11. Bushmann PJ, Atema J (1996) Nephropore rosette glands of the lobster Homarus americanus—possible sources of urine pheromones. J Crust Biol 116:221–231CrossRefGoogle Scholar
  12. Bushmann PJ, Atema J (2000) Chemically mediated mate location and evaluation in the lobster, Homarus americanus. J Chem Ecol 26:883–899CrossRefGoogle Scholar
  13. Caskey JL, Bauer RT (2005) Behavioral test for a possible contact sex pheromone in the caridean shrimp Palaemonetes pugio. J Crust Biol 25:571–576CrossRefGoogle Scholar
  14. Caskey JL, Hasenstein KH, Bauer RT (2009a) Studies on contact sex pheromones of the caridean shrimp Palaemonetes pugio: I. Cuticular hydrocarbons associated with mate recognition. Invertebr Reprod Dev 53:93–103CrossRefGoogle Scholar
  15. Caskey JL, Watson GM, Bauer RT (2009b) Studies on contact sex pheromones of the caridean shrimp Palaemonetes pugio: II. The role of glucosamine in mate recognition. Invertebr Reprod Dev 53:105–116CrossRefGoogle Scholar
  16. Chang ES (1995) Physiological and biochemical changes during the molt cycle in decapod crustaceans: an overview. J Exp Mar Biol Ecol 193:1–14CrossRefGoogle Scholar
  17. Chang ES (2011) The crustacean endocrine system and pleiotropic chemical messengers. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 413–430Google Scholar
  18. Chang ES, Kaufman WR (2005) Endocrinology of crustacea and chelicerata. In: Gilbert LI, Latrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier BV, Oxford, pp 805–842CrossRefGoogle Scholar
  19. Chen HY, Dillaman RM, Roer RD, Watson D (2012) Stage-specific changes in calcium concentration in crustacean (Callinectes sapidus) Y-organs during a natural molting cycle, and their relation to the hemolymphatic ecdysteroid titer. Comp Biochem Phys 163:170–173CrossRefGoogle Scholar
  20. Christy JH, Rittschof D (2011) Deception in visual and chemical communication in crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 313–333Google Scholar
  21. Cooke IM, Haylett B, Weatherby TM (1977) Electrically elicited neurosecretory and electrical responses of the isolated crab sinus gland in normal and reduced calcium salines. J Exp Biol 70:125–149Google Scholar
  22. Dillaman R, Hequembourg S, Gay M (2005) Early pattern of calcification in the dorsal carapace of the blue crab, Callinectes sapidus. J Morphol 263:356–374CrossRefPubMedGoogle Scholar
  23. Dillaman R, Roer R, Shafer T, Modla S (2013) The crustacean integument: structure and function. In: Watling L, Thiel M (eds) Functional morphology and diversity. Oxford University Press, New York, pp 140–166CrossRefGoogle Scholar
  24. Dunham PJ (1988) Pheromones and behavior in the crustaceans. In: Laufer H, Downer GH (eds) Endocrinology of selected invertebrate types. AR Liss, New York, pp 375–392Google Scholar
  25. Eales AJ (1974). Sex pheromone in the shore crab Carcinus maenas and the site of its release from females. Mar Behav Physiol 2:345–355CrossRefGoogle Scholar
  26. Ekerholm M, Hallberg E (2005) Primer and short-range releaser pheromone properties of premolt female urine from the shore crab Carcinus maenas. J Chem Ecol 31:1845–1864CrossRefPubMedGoogle Scholar
  27. Gleeson RA (1991) Intrinsic factors mediating pheromone communication in the blue crab, Callinectes sapidus. In: Martin JW, Bauer RT (eds) Crustacean sexual biology. Columbia University Press, New York, pp 17–32Google Scholar
  28. Gleeson RA, Adams MA, Smith AB (1984) Characterization of a sex pheromone in the blue crab, Callinectes sapidus crustecdysone studies. J Chem Ecol 10:913–921CrossRefPubMedGoogle Scholar
  29. Greenaway P (1983) Uptake of calcium at the post-moult stage by the marine crabs Callinectes sapidus and Carcinus maenas. Comp Biochem Physiol 75:181–184CrossRefGoogle Scholar
  30. Greenaway P (1985) Calcium balance and moulting in the Crustacea. Biol Rev 60:425–454CrossRefGoogle Scholar
  31. Guinot D, Tavares M, Castro P (2013) Significance of the sexual openings and supplementary structures on the phylogeny of brachyuran crabs (Crustacea, Decapoda, Brachyura), with new nomina for higher-ranked podotreme taxa. Zootaxa 3665:1–414CrossRefPubMedGoogle Scholar
  32. Hardege JD, Terschak JA (2011) Identification of crustacean sex pheromones. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 373–392Google Scholar
  33. Hardege JD, Jennings A, Hayden D, Muller CT, Pascoe D, Bentley MG, Clare AS (2002) Novel behavioural assay and partial purification of a female-derived sex pheromone in Carcinus maenas. Mar Ecol Prog Ser 244:179–189CrossRefGoogle Scholar
  34. Hartnoll RG (1968) Morphology of the genital ducts in female crabs. J Linn Soc Zool 47:279–300CrossRefGoogle Scholar
  35. Hartnoll RG (2006) Reproductive investment in Brachyura. Hydrobiologia 557:31–40CrossRefGoogle Scholar
  36. Henmi Y, Murai M (1999) Decalcification of vulvar operculum and mating in the ocypodid crab Ilyoplax pusilla. J Zool 247:133–137CrossRefGoogle Scholar
  37. Herborg LM, Bentley MG, Clare AS, Last KS (2006) Mating behavior and chemical communication in the invasive Chinese mitten crab Eriocheir sinensis. J Exp Mar Biol Ecol 329:1–10CrossRefGoogle Scholar
  38. Horn DHS, Middleton EJ, Wunderlich JA, Hampshire F (1966) Identity of the molting hormones of insects and crustaceans. Chem Commun 1966:339–340Google Scholar
  39. Ituarte RB, Bas C, Luppi TA, Spivak ED (2006) Interpopulational differences in the female reproductive cycle of the southwestern atlantic estuarine crab Chasmagnathus granulatus Dana, 1851 (Brachyura: Grapsoidea: Varunidae). Sci Mar 70:709–718CrossRefGoogle Scholar
  40. Kamio M, Derby CD (2011) Approaches to a molecular identification of sex pheromones in blue crabs. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 393–412Google Scholar
  41. Kamio M, Matsunaga S, Fusetani N (2002) Copulation pheromone in the crab Telmessus cheiragonus (Brachyura: Decapoda). Mar Ecol Prog Ser 234:183–190CrossRefGoogle Scholar
  42. Kamio M, Schmidt M, Germann MW, Kubanek J, Derby CD (2014) The smell of moulting: N-acetylglucosamino-1,5-lactone is a premoult biomarker and candidate component of the courtship pheromone in the urine of the blue crab, Callinectes sapidus. J Exp Biol 217:1286–1296CrossRefPubMedGoogle Scholar
  43. Karplus I, Malecha SR, Sagi A (2000) The biology and management of size variation. In: New MB, Valenti WC (eds) Freshwater prawn culture: the farming of Macrobrachium rosenbergii. Blackwell Science, Malden, pp 259–289CrossRefGoogle Scholar
  44. Kittredge JS, Terry M, Takahashi FT (1971) Sex pheromone activity of the molting hormone crustecdysone on male crabs (Pachygrapsus crassipes, Cancer antennarius and Cancer anthonyi). Fish Bull 96:337–343Google Scholar
  45. López Greco L, Rodríguez E (1998) Size at the onset of sexual maturity in Chasmagnathus granulatus Dana, 1851 (Grapsidae, Sesarminae): a critical overall view about the usual criteria for its determination. Proc Fourth Int Crust Cong 675–689Google Scholar
  46. McLay CL, Becker C (2015) Reproduction in Brachyura. In: Castro P, Davie PJF, Guinot D, Schram FR, von Vaupel Klein JC (eds) Decapoda Brachyura, treatise on zoology—anatomy, taxonomy, biology. Brill, Leiden, pp 185–243Google Scholar
  47. McLay CL, López Greco L (2011) A hypothesis about the origin of sperm storage in the Eubrachyura, the effects of seminal receptacle structure on mating strategies and the evolution of crab diversity: how did a race to be first become a race to be last? Zool Anzeiger 250:378–406CrossRefGoogle Scholar
  48. McLay CL, Sal Moyano MP (2016) Calcium levels in the vulvar opercula of Grapsoids and Ocypodoid crabs (Decapoda: Brachyura). J Crust Biol 36:220–228CrossRefGoogle Scholar
  49. Mykles DL (2011) Ecdysteroid metabolism in crustaceans. J Steroid Biochem Mol Biol 127:196–203CrossRefPubMedGoogle Scholar
  50. Nelson H (1991) Scheduling of reproduction in relation to molting and growth in malacostracan crustaceans. In: Wenner A, Kuris A (eds) Crustacean issues 7. Crustacean egg production. Balkema, Rotterdam, pp 77–113Google Scholar
  51. Reinhart VL, Cromarty SI, Sipala MW, Kass-Simon G (2012) Exposure to the steroid hormone 20-hydroxyecdysone modulates agonistic interactions in male Homarus americanus. Horm Behav 62:605–611CrossRefPubMedGoogle Scholar
  52. Robertson JD (1960) Ionic regulation in the crab Carcinus maenas (L.) in relation to the moulting cycle. Comp Biochem Physiol 1:183–212CrossRefGoogle Scholar
  53. Rodríguez EM, Dezi RE (1987) Análisis de la composición del peso vivo en machos de Uca uruguayenis y Chasmagnathus granulata (Crustacea, Decapoda, Brachyura). Physis 45:31–32Google Scholar
  54. Rodríguez EM, Monserrat JM, Amín OA (1992) Chronic toxicity of ethyl parathion and isobutoxyethanol ester of 2,4-dichlorophenoxyacetic acid to estuarine juvenile and adult crabs. Arch Environ Con Tox 22:140–145CrossRefGoogle Scholar
  55. Rodríguez Moreno PA, Medesani DA, Rodríguez EM (2003) Inhibition of molting by cadmium in the crab Chasmagnathus granulata (Decapoda Brachyura). Aquat Toxicol 64:155–164CrossRefPubMedGoogle Scholar
  56. Roer R, Dillaman R (1984) The structure and calcification of the crustacean cuticle. Am Zool 24:893–909CrossRefGoogle Scholar
  57. Roer RD, Halbrook KE, Shafer TH (2001) Glycosidase activity in the post-ecdysial cuticle of the blue crab, Callinectes sapidus. Comp Biochem Physiol B 128:683–690CrossRefPubMedGoogle Scholar
  58. Sal Moyano MP, Gavio MA, Luppi T (2012a) Mating system of the burrowing crab Neohelice granulata (Brachyura: Varunidae) in two contrasting environments: effect of burrow architecture. Mar Biol 159:1403–1416CrossRefGoogle Scholar
  59. Sal Moyano MP, Luppi TA, Gavio MA, Vallina M, McLay CL (2012b) Receptivity of female Neohelice granulata (Brachyura: Varunidae): different strategies to maximize their reproductive success in contrasting habitats. Helgol Mar Res 66:661–674CrossRefGoogle Scholar
  60. Sal Moyano MP, Silva P, Luppi T, Gavio MA (2014a) Female mate choice by chemical signals in a semi-terrestrial crab. J Sea Res 85:300–307CrossRefGoogle Scholar
  61. Sal Moyano MP, Gavio MA, McLay CL, Luppi T (2014b) Habitat-related differences in the pre-copulatory guarding and copulation behavior of Neohelice granulata (Brachyura, Grapsoidea, Varunidae). J Sea Res 87:8–16CrossRefGoogle Scholar
  62. Shafer TH, Roer RD, Miller CG, Dillaman RM (1994) Postecdysial changes in the protein and glycoprotein composition of the cuticle of the blue crab Callinectes sapidus. J Crust Biol 14:210–219CrossRefGoogle Scholar
  63. Skinner DM, Graham DE, Holland CA, Mykles DL, Soumoff C, Yamaoka LH (1985) Control of molting in Crustacea. In: Wenner A (ed) Crustacean issues 3. Factors in adult growth. Balkema, Rotterdam, pp 3–14Google Scholar
  64. Spivak E (2010) The crab Neohelice (=Chasmagnathus) granulata: an emergent animal model from emergent countries. Helgol Mar Res 64:149–154CrossRefGoogle Scholar
  65. Subramoniam T (2000) Crustacean ecdysteroids in reproduction and embryogenesis. Comp Biochem Physiol C 125:135–156Google Scholar
  66. Webster SG (2015) Endocrinology of molting. In: Chang ES, Thiel M (eds) The natural history of Crustacea: physiology. Oxford University Press, Oxford, pp 1–35Google Scholar
  67. Wyatt TD (2009) Fifty years of pheromones. Nature 457:262–263CrossRefPubMedGoogle Scholar
  68. Wyatt TD (2011) Pheromones and behavior. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 23–38Google Scholar
  69. Zapata MV, López Greco L, Rodríguez EM (2003) Inducción de crecimiento somático en juveniles del cangrejo Chasmagnathus granulatus (Decapoda, Brachyura). II Congreso Iberoamericano Virtual de Acuicultura (http://www.civa2003.org). 971–977
  70. Zar JH (1999) Biostatistical analysis. Prentice Hall Press, New JerseyGoogle Scholar
  71. Zhang D, Zhu J, Lin J, Hardege JD (2011) Surface glycoproteins are not the contact pheromones in the Lysmata shrimp. Mar Biol 157:171–176CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Universidad Nacional de Mar del Plata (UNMdP)Mar del PlataArgentina
  2. 2.Department of Biodiversity and Experimental BiologyFCEN University of Buenos Aires, Institute of Biodiversity, Experimental and Applied Biology (IBBEA), CONICET-UBA. Ciudad Universitaria, Pab. IIBuenos AiresArgentina
  3. 3.School of Biological SciencesUniversity of CanterburyChristchurchNew Zealand

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