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The mating system of the symbiotic pea-crab Dissodactylus crinitichelis (Brachyura, Pinnotheridae): monogamy or promiscuity?

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Abstract

The mating systems of symbiotic crustaceans vary broadly, ranging from monogamy to polygamy to promiscuity. This disparity in mating systems coupled with wide differences in host ecology provides opportunities to study the effect of environmental conditions on the social behavior of marine organisms. In this study, we tested the prediction that symbiotic crustaceans inhabiting relatively large and abundant host species are promiscuous rather than monogamous. The host traits above constraint host monopolization and favor host-switching behaviors by males individuals and, thus, ultimately drive promiscuity as a mating system in symbiotic crustaceans. As a model system we used Dissodactylus crinitichelis, a small ‘pea-crab’ that inhabits the relatively large and abundant sand dollar Encope emarginata. We described the population distribution of D. crinitichelis at two intertidal localities in Sergipe, Brazil, and conducted laboratory experiments to infer the mating system of this species. Dissodactylus crinitichelis inhabit sand dollars as adult heterosexual pairs more frequently than expected by chance alone, but these heterosexual pairs did not exhibit size-assortative pairing. Sexual dimorphism was reversed in D. crinitichelis, with males attaining smaller average body sizes than females but exhibiting more elaborated weaponry (male > female claws). These findings disagree with expectations for monogamous symbiotic crustaceans. Laboratory experiments demonstrated that male and female crabs switch among host individuals rather frequently and heterosexual pairs retrieved from the field did not remain together for long times. Our results argue against social monogamy and in favor of promiscuity in D. crinitichelis. Our study supports the notion that host abundance and large body size (relative to that of symbiotic guests) favor promiscuity in symbiotic crustaceans.

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References

  • Adams J, Edwards AJ, Emberton H (1985) Sexual size dimorphism and assortative mating in the obligate coral commensal Trapezia ferruginea Latreille (Decapoda, Xanthidae). Crustaceana 48:188–194

    Article  Google Scholar 

  • Ambrosio LJ, Baeza JA (2016) Territoriality and conflict avoidance explain a sociality (solitariness) of the endosymbiotic pea crab Tunicotheres moseri. PLoS One. doi:10.1371/journal.pone.0148285

    Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Baeza JA (1999) Indicators of monogamy in the commensal crab Pinnixa transversalis (Milne Edwards & Lucas) (Decapoda: Brachyura: Pinnoteridae): population distribution, male-female association and sexual dimorphism. Rev Biol Mar Oceanogr 34:303–313

    Google Scholar 

  • Baeza JA (2008) Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlantica, in the tropical eastern Pacific coast. Mar Biol 153:387–395

    Article  Google Scholar 

  • Baeza JA (2015) Crustaceans as symbionts: an overview of their diversity, host use and life styles. In: Watling L, Thiel M (eds) The life styles and feeding biology of the Crustacea. Oxford University Press, Oxford, pp 163–189

    Google Scholar 

  • Baeza JA, Asorey CM (2012) Testing the role of male–male competition in the evolution of sexual dimorphism: a comparison between two species of porcelain crabs. Biol J Linn Soc Lond 105:548–558

    Article  Google Scholar 

  • Baeza JA, Hernáez P (2015) Population distribution, sexual dimorphism, and reproductive parameters in the crab Pinnixa valdiviensis Rathbun, 1907 (Decapoda: Pinnotheridae). J Crustac Biol 35:68–75

    Article  Google Scholar 

  • Baeza JA, Piantoni C (2010) Sexual system, sex ratio and group living in the shrimp Thor amboinensis (De Man): relevance to resource-monopolization and sex-allocation theories. Biol Bull 219:151–165

    Article  CAS  Google Scholar 

  • Baeza JA, Stotz W (2003) Host-use and selection of differently colored sea anemones by the symbiotic crab Allopetrolisthes spinifrons. J Exp Mar Biol Ecol 284:25–39

    Article  Google Scholar 

  • Baeza JA, Thiel M (2000) Host use pattern and life history of Liopetrolisthes mitra, a crab associate of the black sea urchin Tetrapygus niger. J Mar Biol Ass UK 80:639–645

    Article  Google Scholar 

  • Baeza JA, Thiel M (2003) Predicting territorial behavior in symbiotic crabs using host characteristics: a comparative study and proposal of a model. Mar Biol 142:93–100

    Article  Google Scholar 

  • Baeza JA, Thiel M (2007) The mating system of symbiotic crustaceans. A conceptual model based on optimality and ecological constraints. In: Duffy JE, Thiel M (eds) Reproductive and social behavior: Crustaceans as model systems. Oxford University Press, Oxford, pp 245–255

    Google Scholar 

  • Baeza JA, Ritson-Williams R, Fuentes MS (2013) Sexual and mating system in a caridean shrimp symbiotic with the winged pearl oyster in the coral triangle. J Zool 289:172–181

    Article  Google Scholar 

  • Baeza JA, Hemphill CA, Ritson-Williams R (2015) The sexual and mating system of the shrimp Odontonia katoi (Palaemonidae, Pontoniinae), a symbiotic guest of the ascidian Polycarpa aurata in the coral triangle. PLoS One. doi:10.1371/journal.pone.0121120

    Google Scholar 

  • Baeza JA, Simpson L, Ambrosio LJ, Guéron R, Mora N (2016) Monogamy in a hyper-symbiotic shrimp. PLoS One. doi:10.1371/journal.pone.0149797

    Google Scholar 

  • Bauer RT (2004) Remarkable shrimps. Oklahoma University Press, Norman

    Google Scholar 

  • Bauer RT, Thiel M (2011) First description of a pure-search mating system and protandry in the shrimp Rhynchocinetes uritai (Decapoda: Caridea). J Crustac Biol 31(2):286–295

    Article  Google Scholar 

  • Bell JL (1984) Changing residence: dynamics of the symbiotic relationship between Dissodactylus mellitae Rathbun (Pinnotheridae) and Mellita quinquiesperforata (Leske) (Echinodermata). J Exp Mar Biol Ecol 82:101–115

    Article  Google Scholar 

  • Campos E, Campos AR, León-González JA (2009) Diversity and ecological remarks of ectocommensals and ectoparasites (Annelida, Crustacea, Mollusca) of echinoids (Echinoidea: Mellitidae) in the Sea of Cortez, Mexico. Parasitol Res 105:479–487

    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 Turtle Newsl 102:5–7

    Google Scholar 

  • Correa C, Thiel M (2003) Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Rev Chil Hist Nat 76:187–203

    Article  Google Scholar 

  • Crawley MJ (2013) Statistical computing—an introduction to data analysis using s-plus. Wiley, London

    Google Scholar 

  • De Bruyn C, Rigaud T, Bruno D, Ridder C (2009) Symbiosis between the pea crab Dissodactylus primitivus and its echinoid host Meoma ventricosa: potential consequences for the crab mating system. Mar Ecol Prog Ser 375:173–183

    Article  Google Scholar 

  • De Bruyn C, David B, Ridder C, Rigaud T (2010) Asymmetric exploitation of two echinoid host species by a parasitic pea crab and its consequences for the parasitic life cycle. Mar Ecol Prog Ser 398:183–191

    Article  Google Scholar 

  • De Bruyn C, David B, Motreuil S, Caulier G, Jossart Q, Rigaud T, De Ridder C (2016) Should I stay or should I go? Causes and dynamics of host desertion by a parasitic crab living on echinoids. Mar Ecol Prog Ser 546:163–171

    Article  Google Scholar 

  • Duffy JE (1996) Eusociality in a coral-reef shrimp. Nature 381:512–514

    Article  CAS  Google Scholar 

  • Duffy JE (2007) Ecology and evolution of eusociality in sponge-dwelling shrimp. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, Oxford, pp 387–409

    Chapter  Google Scholar 

  • Elliott JM (1983) Some methods for the statistical analysis of samples of benthic invertebrates, 3rd edn. Freshwater Biological Association, Far Sawrey

    Google Scholar 

  • Gherardi F (1991) Eco-ethological aspects of the symbiosis between the shrimp Athanas indicus (Coutière 1903) and the sea urchin Echinometra mathaei (de Blainville 1825). Trop Zool 4(1):107–128. doi:10.1080/03946975.1991.10539481

    Article  Google Scholar 

  • Gray IE, McCloskey LR, Weihe SC (1968) The commensal crab Dissodactylus mellitae and its reaction to sand dollar host-factor. J Elisha Mitchell Sci Soc 84:472–481

    Google Scholar 

  • Grove MW, Woodin SA (1996) Conspecific recognition and host choice in a pea crab, Pinnixa chaetopterana (Brachyura: Pinnotheridae). Biol Bull 190:359–366

    Article  Google Scholar 

  • Guilherme PDB, Brustolin MC, Bueno ML (2015) Distribution patterns of ectosymbiont crabs and their sand dollar hosts in a subtropical estuarine sandflat. Rev Biol Trop 63(Suppl. 2):209–220

    Google Scholar 

  • Hartnoll RG (1978) The determination of relative growth in Crustacea. Crustaceana 34(3):281–293

    Article  Google Scholar 

  • Hartnoll RG (1982) Growth. In: Bliss DE, Abele LG (eds) The biology of Crustacea, 2, embryology, morphology and genetics. Academic Press, New York, pp 111–196

    Google Scholar 

  • Jennions MD (1997) Female promiscuity and genetic incompatibility. Trends Ecol Evol 12(7):251–253

    Article  CAS  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  Google Scholar 

  • Jossart Q, Wattier RA, Kastally C, Aron S, David B, Ridder CD, Riguad T (2014) Genetic evidence confirms polygamous mating system in a crustacean parasite with multiple hosts. PLoS One. doi:10.1371/journal.pone.0090680

    Google Scholar 

  • Jr Haefner PA (1990) Morphometry and size at maturity of Callinectes ornatus (Brachyura, Portunidae) in Bermuda. Bull Mar Sci 46:274–286

    Google Scholar 

  • Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Adv Mar Biol 40:81–251

    Article  Google Scholar 

  • Martin JW, Davis GE (2006) Historical trends in crustacean systematics. Crustaceana 79(11):1347–1368

    Article  Google Scholar 

  • Martinelli-Filho JE, Santos RB, Ribeiro CC (2014) Host selection, host-use pattern and competition in Dissodactylus crinitichelis and Clypeasterophilus stebbingi (Brachyura: Pinnotheridae). Symbiosis. doi:10.1007/s13199-014-0292-0

    Google Scholar 

  • Nogata Y, Matsumura K (2005) Larval development and settlement of a whale barnacle. Biol Lett 2:92–93

    Article  Google Scholar 

  • Ocampo EH, Nuñez JD, Cledón M, Baeza JA (2012) Host-specific reproductive benefits, host selection behavior and host use pattern of the pinnotherid crab Calytraeotheres garthi. J Exp Mar Biol Ecol 429:36–46

    Article  Google Scholar 

  • Ory NC, Dudgeon Thiel M (2013) Host-use patterns and factors influencing the choice between anemone and urchin hosts by a caridean shrimp. J Exp Mar Biol Ecol 449:85–92

    Article  Google Scholar 

  • Pérez GHB, Serrato MB, Sanchez CMD (2012) Equinodermos del Caribe colombiano II: Echinoidea Y Holothuroidea. Serie de Publicaciones Especiales de Invemar, Santa Marta

    Google Scholar 

  • Pfaller JB, Alfaro-Shigueto J, Giffoni B, Ishihara T, Mangel JC, Peckham SH, Bjorndal KA, Baeza JA (2014) Social monogamy in the crab Planes major, a facultative symbiont of loggerhead sea turtles. J Exp Mar Biol Ecol 461:124–132

    Article  Google Scholar 

  • Pires-Vanin AMS (2001) Identifying the components of ecological variation in a marine benthic megafauna. Rev bras oceanogr 49(1/2):29–38

    Article  Google Scholar 

  • Reeves MV, Brooks WR (2001) Host selection, chemical detection, and protection of the symbiotic pinnotherid crabs Dissodactylus crinitichelis and Clypeasterophilus rugatus associated with echinoderms. Symbiosis 30:239–256

    Google Scholar 

  • Sainte-Marie B (2007) Sperm demand and allocation in decapod Crustaceans. In: Duffy JE, Thiel M (eds) Reproductive and social behavior: Crustaceans as model systems. Oxford University Press, Oxford, pp 191–210

    Google Scholar 

  • Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 3rd edn. Freeman, San Francisco

    Google Scholar 

  • Thiel M, Zander A, Baeza JA (2003) Movements of the symbiotic crab Liopetrolisthes mitra between its host sea urchin Tetrapygus niger. Bull Mar Sci 72:89–101

    Google Scholar 

  • Wehrtmann IS (1990) Distribution and reproduction of Ambidexter panamense and Palaemonetes schmitti in Pacific Costa Rica (Crustacea, Decapoda). Rev Biol Trop 38:327–329

    Google Scholar 

  • Williams AB (1984) Shrimps, lobsters, and crabs of the Atlantic coast of the eastern United States, Maine to Florida. Smithsonian Institution Press, Washington

    Google Scholar 

  • Wirtz P, Melo GAS, Grave S (2009) Symbioses of the decapod crustaceans along the coast of Espírito Santo, Brazil. Mar Biodivers Rec 2:1–9

    Article  Google Scholar 

  • Yanagisawa Y, Hamaishi A (1986) Mate acquisition by a solitary crab Zebrida adamsii, a symbiont of the sea urchin. J Ethol 4:153–162

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

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Acknowledgements

The authors are grateful to Dr. Sinara Maria Moreira for her help during fieldwork and experimental observations and to Dr. Leandro de Sousa Souto for help with some of the statistical analyses. The authors are also grateful to the reviewers and Dr. Martin Thiel for providing valuable criticism that helped us to improve earlier versions of the present manuscript. All sampling in this study was conducted according to the applicable state and federal laws. Thanks to Sarah Steedman and John L. Ambrosio for correcting the English language in previous versions of this manuscript.

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Correspondence to J. Antonio Baeza.

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Author Douglas Fernandes Rodrigues Alves declares that he has no conflict of interest. Author Gustavo Luis Hirose declares that he has no conflict of interest. Author Samara de P. Barros-Alves declares that she has no conflict of interest. Author J. Antonio Baeza declares that he has no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Alves, D.F.R., Hirose, G.L., Barros-Alves, S.d. et al. The mating system of the symbiotic pea-crab Dissodactylus crinitichelis (Brachyura, Pinnotheridae): monogamy or promiscuity?. Mar Biol 164, 200 (2017). https://doi.org/10.1007/s00227-017-3234-6

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