Abstract
Evaluation of the molting stage of crustaceans is essential for studying their mating behavior because of molt-dependent changes in their behavior. For example, in species in which females mate just after molting, sexually mature premolt females are ready for courtship and postmolt females are ready for copulation. Non-invasive methods of evaluating molt stage are essential in studies of molt-dependent mating behavior so that normal behavior is not disrupted by the evaluation itself. The goal of the present study was to establish a non-invasive evaluation method for the helmet crab Telmessus cheiragonus, which is a model species for research on crustacean sex pheromones. We have identified morphological and behavioral indicators of molt stage. A morphological indicator of molt stage was a change in the color of the edge of telson and sixth abdominal segment, from a dark line to red in premolt animals to white in postmolt animals, which can be observed with the naked eye. A behavioral indicator of molt stage was that premolt females tended to fold their walking legs and chelae to adopt a precopulatory guarded position during artificial handling, whereas late postmolt stage females with developed ovaries and early premolt females in an early molting stage did not show this behavior. These non-invasive morphological and behavioral characteristics are useful indicators of the premolt stage of sexually mature female helmet crabs.
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References
Aiken D (1973) Proecdysis, setal development, and molt prediction in the American lobster (Homarus americanus). J Fish Board Can 30:1337–1344
Bamber S, Naylor E (1997) Sites of release of putative sex pheromone and sexual behaviour in female Carcinus maenas (Crustacea: Decapoda). Estuar Coast Shelf Sci 44:195–202
Burton E, Mitchell B (1987) Moult staging in the Australian freshwater crayfish, Cherax albidus Clark and Cherax destructor Clark (Decapoda: Parastacidae), via uropod setal development. Mar Freshw Res 38:545–552
Chan S-M, Rankin SM, Keeley LL (1988) Characterization of the molt stages in Penaeus vannamei: setogenesis and hemolymph levels of total protein, ecdysteroids, and glucose. Biol Bull 175:185–192
Drach P (1939) Molt and intermolt cycle in decapod crustaceans. Annales de l’Institut Océanographique 19:103–391 (in French)
Gleeson RA (1980) Pheromone communication in the reproductive behavior of the blue crab, Callinectes sapidus. Mar Behav Physiol 7:119–134
Hartnoll R (1969) Mating in the brachyura. Crustaceana 16:161–181
Hoenig JM, Dawe EG, O’Keefe PG (1994) Molt indicators and growth per molt for male snow crabs (Chionoecetes opilio). J Crust Biol 14:273–279
Jivoff P, Hines AH (1998a) Effect of female molt stage and sex ratio ion courtship behavior of the blue crab Callinectes sapidus. Mar Biol 131:533–542
Jivoff P, Hines AH (1998b) Female behaviour, sexual competition and mate guarding in the blue crab, Callinectes sapidus. Anim Behav 55:589–603
Jivoff P, Hines AH, Quackenbush LS (2007) Reproduction biology and embryonic development. In: Kennedy VS, Cronin LE (eds) The blue crab Callinectes sapidus. Maryland Sea Grant College, College Park, pp 255–298
Kamio M (2009) Toward identifying sex pheromones in blue crabs. Ann N Y Acad Sci 1170:456–461
Kamio M, Derby CD (2010) 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 393–412
Kamio M, Matsunaga S, Fusetani N (2000) Studies on sex pheromones of the helmet crab, Telmessus cheiragonus 1. An assay based on precopulatory mate-guarding. Zool Sci 17:731–733
Kamio M, Matsunaga S, Fusetani N (2002) Copulation pheromone in the crab Telmessus cheiragonus (Brachyura : Decapoda). Mar Ecol Prog Ser 234:183–190
Kamio M, Matsunaga S, Fusetani N (2003) Observation on the mating behaviour of the helmet crab Telmessus cheiragonus (Brachyura : Cheiragonidae). J Mar Biol Assoc UK 83:1007–1013
Kamio M, Araki M, Nagayama T, Matsunaga S, Fusetani N (2005) Behavioral and electrophysiological experiments suggest that the antennular outer flagellum is the site of pheromone reception in the male helmet crab Telmessus cheiragonus. Biol Bull 208:12–19
Kamio M, Reidenbach MA, Derby CD (2008) To paddle or not: context dependent courtship display by male blue crabs, Callinectes sapidus. J Exp Biol 211:1243–1248
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 217:1286–1296
Kamio M, Nagakura Y, Yano H (2017) The molting biomarker molecule exists as 2-acetamido-2-deoxy-gluconic acid in urine of blue crabs and helmet crabs. Chem Biodivers 14:e1700063
Kozma MT, Ngo-Vu H, Rump MT, Bobkov YV, Ache BW, Derby CD (2020a) Single cell transcriptomes reveal expression patterns of chemoreceptor genes in olfactory sensory neurons of the Caribbean spiny lobster, Panulirus argus. BMC Genom 21:649
Kozma MT, Ngo-Vu H, Wong YY, Shukla NS, Pawar SD, Senatore A, Schmidt M, Derby CD (2020b) Comparison of transcriptomes from two chemosensory organs in four decapod crustaceans reveals hundreds of candidate chemoreceptor proteins. PLoS ONE 15:e0230266
Lipcius RN, Herrnkind WF (1982) Molt cycle alterations in behavior, feeding and diel rhythms of a decapod crustacean, the spiny lobster Panulirus argus. Mar Biol 68:241–252
Moriyasu M, Mallet P (1986) Molt stages of the snow crab Chionoecetes opilio by observation of morphogenesis of setae on the maxilla. J Crust Biol 6:709–718
Mykles DL, Chang ES (2020) Hormonal control of the crustacean molting gland: insights from transcriptomics and proteomics. Gen Comp Endocrinol 294:113493
Nagao J (1999) Studies on the growth and the reproduction of the helmet crab, Telmessus cheiragonus. Ph. D Thesis. Hokkaido University, Hakodate
Rondeau A, Sainte-Marie B (2001) Variable mate-guarding time and sperm allocation by male snow crabs (Chionoecetes opilio) in response to sexual competition, and their impact on the mating success of females. Biol Bull 201:204–217
Smith SG, Chang ES (2007) Molting and growth. In: Kennedy VS, Cronin LE (eds) The blue crab Callinectes sapidus. Maryland Sea Grant College, College Park, pp 197–254
Sneddon LU, Huntingford FA, Taylor AC, Clare AS (2003) Female sex pheromone-mediated effects on behavior and consequences of male competition in the shore crab (Carcinus maenas). J Chem Ecol 29:55–70
Suzuki Y, Yasuda C, Takeshita F, Wada S (2012) Male mate choice and male–male competition in the hermit crab Pagurus nigrofascia: importance of female quality. Mar Biol 159:1991–1996
Vigh DA, Fingerman M (1985) Molt staging in the fiddler crab Uca pugilator. J Crust Biol 5:386–396
Wada S, OhmoriI H, Goshima S, Nakao S (1997) Shell-size preference of hermit crabs depends on their growth rate. Anim Behav 54:1–8
Yano H, Kamio M, Nagai H (2016) The molting biomarker metabolite N-acetylglucosamino-1, 5-lactone in female urine of the helmet crab Telmessus cheiragonus. Biol Bull 230:143–151
Acknowledgements
We thank Dr. Charles Derby for reading this manuscript and for valuable discussions; Dr. Hiroyuki Munehara of the Usujiri Fisheries Station of Hokkaido University for allowing us to work in those facilities; Dr. Hiroshi Nagai of Tokyo University of Marine Science and Technology for kind support during this project; and Dr. Nobuhiro Fusetani of Hokkaido University and Dr. Shigeki Matsunaga of the University of Tokyo for support at the initial stage of this study. MK was supported by JSPS KAKENHI (grant no. 26450282). HY was supported by a Sasakawa Scientific Research Grant (grant no. 27-718).
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Kamio, M., Osada, H. & Yano, H. Morphological and behavioral indicators of reproductive premolt females of the helmet crab Telmessus cheiragonus. Fish Sci 87, 331–337 (2021). https://doi.org/10.1007/s12562-021-01517-6
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DOI: https://doi.org/10.1007/s12562-021-01517-6