Intersexuality in the porcellanid crab Pisidia longicornis (Crustacea: Decapoda: Anomura: Porcellanidae)

Luciane Augusto de Azevedo Ferreira About the author

Abstract

Intersex specimens of Pisidia longicornis (Linnaeus, 1767) are recorded for the first time and their secondary sexual characters are analyzed. Of 145 specimens of P. longicornis examined in this study, six were identified as intersex individuals. Of these, three presented male secondary sexual characters, well-developed male gonopores and rudimentary female gonopores, whereas the other three had female secondary sexual characters, with female gonopores being more pronounced than the male ones. The present study provides the first record of intersex porcelain crabs.

Malacostraca; porcelain crabs; sexual characters; reproductive biology


Decapod crustaceans are typically gonochoric, with more or less pronounced sexual dimorphism. In the vast majority of decapods, gonopores are situated on the coxae of the third pereopods (P3) in females, and on the coxae of the fifth pereopods (P5) in males. However, there are intersex individuals with gonopore openings on both P3 and P5 (Turra 2004Turra A (2004) Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. Journal of the Marine Biological Association of the United Kingdom 84: 757-759. doi: 10.1017/S0025315404009877h
https://doi.org/10.1017/S002531540400987...
).

Intersexual individuals of a variety of decapod crustaceans have been reported and studied in detail. In Anomura, most studies on intersexuality involve the hermit crab families Coenobitidae and Diogenidae (Turra 2004Turra A (2004) Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. Journal of the Marine Biological Association of the United Kingdom 84: 757-759. doi: 10.1017/S0025315404009877h
https://doi.org/10.1017/S002531540400987...
, Gusev & Zabotin 2007Gusev O, Y Zabotin (2007) Observation of intersexuality in land hermit crabs (Anomura: Coenobitidae). Journal of the Marine Biological Association of the United Kingdom 87(2): 533-536. doi: 10.1017/S0025315407054604
https://doi.org/10.1017/S002531540705460...
, Fantucci et al. 2007Fantucci MZ, Biagi R, Mantelatto FL (2007) Intersexuality in the western Atlantic hermit crab Isocheles sawayai (Anomura: Diogenidae). Marine Biodiversity Records 1: 1-3. doi: 10.1017/S175526720700735X
https://doi.org/10.1017/S175526720700735...
, Sant'Anna et al. 2010Sant'Anna BS, Turra A, Zara FJ (2010) Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology 10: 201-209. doi: 10.3354/ab00283
https://doi.org/10.3354/ab00283...
). Some research has also been conducted on squat lobsters, Galatheidae (Kronenberger et al. 2004Kronenberger K, Brandis D, Turkay M, Storch V (2004) Functional morphology of the reproductive system of Galathea intermedia (Decapoda: Anomura). Journal of Morphology 262: 500-516. doi: 10.1002/jmor.10259
https://doi.org/10.1002/jmor.10259...
) and mole crabs, Hippidae (Subramoniam 1981Subramoniam T (1981) Protandric hermaphroditism in a mole crab, Emerita asiatica (Decapoda: Anomura). The Biological Bulletin 160: 161-174. doi: 10.2307/1540910
https://doi.org/10.2307/1540910...
).

Within the Porcellanidae, Haig (1972Haig J (1972) Galatheidea (Crustacea, Decapoda, Anomura) collected by the F.I.S. Endeavour. Records of the Australian Museum 28(14): 269-289. doi: 10.3853/j.0067-1975.28.1973.411
https://doi.org/10.3853/j.0067-1975.28.1...
) reported a single intersex specimen of Pisidia dispar (Stimpson, 1858) collected in Australia, based on the presence of both male and female pleopods, weakly developed female gonopores on the coxae of P3, and the presence of male secondary characters, such as more robust chelipeds. Based on similar criteria, Gore (1982Gore RH (1982) Porcellanid crabs from the coasts of Mexico and Central America (Crustacea: Decapoda: Anomura). Smithsonian Contributions to Zoology 363: 1-34. doi: 10.5479/si.00810282.363
https://doi.org/10.5479/si.00810282.363...
) mentioned a presumed intersex specimen of Pachycheles chacei Haig, 1956 from Panama.

Intersexuality in porcellanid crabs was recently confirmed in two specimens of Porcellana platycheles (Pennant, 1777), a common European species (Ferreira & Guzmán 2013Ferreira LAA, Guzmán G (2013) Primer registro de intersexualidad en Porcellana platycheles (Pennant, 1777) (Decapoda: Anomura: Porcellanidae). Latin American Journal of Aquatic Research 41(3): 606-610. doi: 103856/vol41-issue3-fulltext-24
https://doi.org/103856/vol41-issue3-full...
). One of them presented gonopore openings on both P3 and P5, combined with female secondary characters, such as the shape of the abdomen and pleopods. The second individual had a single small female gonopore on P5, but also presented conspicuous male and female characters, e.g. male and female pleopods.

This paper reports on a new case of intersexuality in the porcellanid crab, Pisidia longicornis (Linnaeus, 1767), an eastern Atlantic species that is distributed from Norway to Portugal and throughout the Mediterranean Sea (D'Udekem D'Acoz 1999D'Udekem D'acoz C (1999) Inventaire et distribution des crustacés décapodes de l'atlantique nord-orientale, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Paris, Muséum National d'Histoire Naturelle, Collection Patrimoine Naturels 40, 383p.). One hundred and forty-five specimens of Pisidia longicornis from several localities, and which are deposited in the Museum of Zoology, University of São Paulo, São Paulo, Brazil (MZUSP) and National Museum of Natural History, Smithsonian Institution, Washington DC, USA (USNM), were examined under a stereomicroscope. The sex of individuals was determined based on whether the gonopores are located on P3 (males) or P5 (females). Secondary sexual characters were scored based mainly on the morphology of the sternum, abdomen and pleopods (see below). In addition, gills and abdominal chambers were examined in search of macro-parasites (e.g., bopyrid isopods and rhizocephalan barnacles).

In porcelain crabs, the most obvious external secondary characters of females are a broader sternum and abdomen, the latter having a greater number of lateral setae; furthermore, the abdomen covers the entire thoracic sternum, thus protecting the genital pore, while the telson is reaches the coxae of the third maxillipeds.

Females have three pairs of pleopods, located on the third, fourth and fifth abdominal somites. The pleopods are uniramous. They are composed of a non-segmented protopod and endopod with three articulated segments; they are broader and longer in the fifth somite and smaller in the third somite. Males have highly modified pleopods (= gonopods) only on the second somite; their pleopods are biramous, with a long protopod, a well-developed endopod and a greatly reduced exopod.

Of 145 specimens of Pisidia longicornis examined, six individuals were determined as intersex (Table 1). Three individuals presented secondary male characters (narrow abdomen not covering the entire thoracic sternum, gonopods), and had well-developed male gonopores and rudimentary female gonopores. The other three presented female secondary characters (broad thoracic sternum and abdomen, female pleopods), with the female gonopores more developed than the male ones. In addition, two of the three individuals with female features were ovigerous. No parasites were found in any of the intersex individuals.

The frequency of intersex individuals among anomuran crustaceans is low, usually 2-7% in most populations (Gusev & Zabotin 2007Gusev O, Y Zabotin (2007) Observation of intersexuality in land hermit crabs (Anomura: Coenobitidae). Journal of the Marine Biological Association of the United Kingdom 87(2): 533-536. doi: 10.1017/S0025315407054604
https://doi.org/10.1017/S002531540705460...
, Sant'Anna et al. 2010Sant'Anna BS, Turra A, Zara FJ (2010) Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology 10: 201-209. doi: 10.3354/ab00283
https://doi.org/10.3354/ab00283...
, Ferreira & Guzmán 2013Ferreira LAA, Guzmán G (2013) Primer registro de intersexualidad en Porcellana platycheles (Pennant, 1777) (Decapoda: Anomura: Porcellanidae). Latin American Journal of Aquatic Research 41(3): 606-610. doi: 103856/vol41-issue3-fulltext-24
https://doi.org/103856/vol41-issue3-full...
). In Pisidia longicornis, the frequency of intersex individuals, however from different populations and localities, was 4.14%, thus falling in the range indicated by previous authors.

Different hypotheses have been suggested to explain intersexuality in crustaceans, including parasitism (Nielsen 1970Nielsen SO (1970) The effects of the rhizocephalan parasites Peltogaster paguri Rathke and Gemmosaccus sulcatus (Lilljeborg) on five species of paguridan hosts (Crustacea, Decapoda). Sarsia 42: 17-32. doi: 10.1080/00364827.1970.10411160
https://doi.org/10.1080/00364827.1970.10...
, Ginsburger-Vogel 1991Ginsburger-Vogel T (1991) Intersexuality in Orchestia mediterranea Costa, 1853, and Orchestia aestuarensis Wildish, 1987 (Amphipoda): a consequence of hybridization or parasitic infestation? Journal of Crustacean Biology 11: 530-539. doi: 10.2307/1548522
https://doi.org/10.2307/1548522...
), genetic abnormalities (Hough et al. 1992Hough AR, Bannister NJ, Naylor E (1992) Intersexuality in the mysid Neomysis integer. Journal of Zoology 226: 585-588. doi: 10.1111/j.1469-7998.1992.tb07501.x
https://doi.org/10.1111/j.1469-7998.1992...
), environmental contamination (Olmstead & Leblanc 2007Olmstead AW, LeBlanc GA (2007) The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean. International Journal of Biological Science 3(2): 77-84. doi: 10.7150/ijbs.3.77
https://doi.org/10.7150/ijbs.3.77...
, Mazurová et al. 2010Mazurová E, Hilscherová K, Šídlová-Štìpánková T, Köhler HR, Triebskorn R, Jungmann D, Giesy JP, Bláha L (2010) Chronic toxicity of contaminated sediments on reproduction and histopathology of the crustacean Gammarus fossarum and relationship with the chemical contamination and in vitro effects. Journal of Soils and Sediments 10: 423-433. doi: 10.1007/s11368-009-0166-x
https://doi.org/10.1007/s11368-009-0166-...
, Ford 2012Ford AT (2012) Intersexuality in Crustacea: an environmental issue? Aquatic Toxicology 108: 125-129. doi: 10.1016/j.aquatox.2011.08.016
https://doi.org/10.1016/j.aquatox.2011.0...
) and social organization (Tóth & Bauer 2008Tóth E, Bauer RT (2008) Synalpheus paraneptunus (Crustacea: Decapoda: Caridea) populations with intersex gonopores: a sexual enigma among sponge-dwelling snapping shrimps. Invertebrate Reproduction & Development 51(1): 49-59. doi: 10.1080/07924259.2008.9652255
https://doi.org/10.1080/07924259.2008.96...
). Since no bopyrid or rhizocephalan parasites were found associated with intersex Pisidia longicornis individuals, and no abnormalities were found on their carapace, pereopods, abdomen or pleopods, it is unlikely that macro-parasites are the cause of intersexuality in these crabs.

According to Ferreira & Guzmán (2013Ferreira LAA, Guzmán G (2013) Primer registro de intersexualidad en Porcellana platycheles (Pennant, 1777) (Decapoda: Anomura: Porcellanidae). Latin American Journal of Aquatic Research 41(3): 606-610. doi: 103856/vol41-issue3-fulltext-24
https://doi.org/103856/vol41-issue3-full...
) when male and female characters are present in the same porcellanid crab (at least in Porcellana platycheles), the incidence of intersex specimens is low, and there is no evidence of parasitism, intersexuality can be attributed to a genetic abnormality.

The occurrence of intersex specimens is also frequently associated with localities where there is pollution (Gusev & Zabotin 2007Gusev O, Y Zabotin (2007) Observation of intersexuality in land hermit crabs (Anomura: Coenobitidae). Journal of the Marine Biological Association of the United Kingdom 87(2): 533-536. doi: 10.1017/S0025315407054604
https://doi.org/10.1017/S002531540705460...
, Fantucci et al. 2009, Sant'Anna et al. 2010Sant'Anna BS, Turra A, Zara FJ (2010) Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology 10: 201-209. doi: 10.3354/ab00283
https://doi.org/10.3354/ab00283...
, Ferreira & Guzmán 2013Ferreira LAA, Guzmán G (2013) Primer registro de intersexualidad en Porcellana platycheles (Pennant, 1777) (Decapoda: Anomura: Porcellanidae). Latin American Journal of Aquatic Research 41(3): 606-610. doi: 103856/vol41-issue3-fulltext-24
https://doi.org/103856/vol41-issue3-full...
). In the present work, intersex individuals of Pisidia longicornis were indeed collected in regions regularly affected by pollution caused by sunken oil tankers or by illegal fuel discharges into the sea (Vogt & Schramm 1991Vogt H, Schramm W (1991) Conspicuous decline of Fucus in Kiel Bay (Western Baltic): what are the causes? Marine Ecology Progress Series 69: 189-194.) (Table 1). Therefore, it is possible that intersexuality in Pisidia longicornis in this case was caused by environmental contamination. However, since the reproductive function of intersex individuals is still largely unknown, the question whether intersexuality in decapods represents a case of true hermaphroditism or just an occasional genetic aberration remains open (Gusev & Zabotin 2007Gusev O, Y Zabotin (2007) Observation of intersexuality in land hermit crabs (Anomura: Coenobitidae). Journal of the Marine Biological Association of the United Kingdom 87(2): 533-536. doi: 10.1017/S0025315407054604
https://doi.org/10.1017/S002531540705460...
).

In hermit crabs (Coenobitidae and Diogenidae), as well as in peracarids, intersexuality has been attributed to a protogynous event. The intersex individuals may be considered functionally males, since they have male secondary characters such as male-type pleopods (Brook et al. 1994Brook HJ, Rawlings TA, Davis RW (1994) Protogynous sex change in the intertidal isopod Gnorimosphaeroma oregonensis (Crustacea: Isopoda). The Biological Bulletin 187: 99-111., Turra 2004Turra A (2004) Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. Journal of the Marine Biological Association of the United Kingdom 84: 757-759. doi: 10.1017/S0025315404009877h
https://doi.org/10.1017/S002531540400987...
, Fantucci et al. 2007Fantucci MZ, Biagi R, Mantelatto FL (2007) Intersexuality in the western Atlantic hermit crab Isocheles sawayai (Anomura: Diogenidae). Marine Biodiversity Records 1: 1-3. doi: 10.1017/S175526720700735X
https://doi.org/10.1017/S175526720700735...
, 2009, Sant'Anna et al. 2010Sant'Anna BS, Turra A, Zara FJ (2010) Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology 10: 201-209. doi: 10.3354/ab00283
https://doi.org/10.3354/ab00283...
). In contrast, Ferreira & Guzmán (2013Ferreira LAA, Guzmán G (2013) Primer registro de intersexualidad en Porcellana platycheles (Pennant, 1777) (Decapoda: Anomura: Porcellanidae). Latin American Journal of Aquatic Research 41(3): 606-610. doi: 103856/vol41-issue3-fulltext-24
https://doi.org/103856/vol41-issue3-full...
) observed that the secondary sexual characters in intersex individuals of Porcellana platycheles had a greater similarity to females than to males.

Turra (2007Turra A (2007) Reproductive role of intersex hermit crabs. Crustaceana 80(4): 491-494.) identified an ovigerous intersex individual of Clibanarius vittatus (Bosc, 1802) (Diogenidae). The fact that an intersex can be functionally a female is evidence of a sex reversal in diogenids. To the author's best knowledge, no intersex ovigerous individuals have been previously reported in porcellanid crabs. This makes the specimens of Pisidia longicornis of this study the first record of intersexuality in this family.

ACKNOWLEDGEMENTS

I am gratefully to Marcos Tavares (MZUSP), Rafael Lemaitre and Karen Reed (USNM) for granting me access to the collections under their responsibility and for providing a space where I could work. This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) in the form of a grant (2011/06230-2).

  • Brook HJ, Rawlings TA, Davis RW (1994) Protogynous sex change in the intertidal isopod Gnorimosphaeroma oregonensis (Crustacea: Isopoda). The Biological Bulletin 187: 99-111.
  • D'Udekem D'acoz C (1999) Inventaire et distribution des crustacés décapodes de l'atlantique nord-orientale, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Paris, Muséum National d'Histoire Naturelle, Collection Patrimoine Naturels 40, 383p.
  • Fantucci MZ, Biagi R, Mantelatto FL (2007) Intersexuality in the western Atlantic hermit crab Isocheles sawayai (Anomura: Diogenidae). Marine Biodiversity Records 1: 1-3. doi: 10.1017/S175526720700735X
    » https://doi.org/10.1017/S175526720700735X
  • Fantucci MZ, Biagi R, Mantelatto FL (2009) Use of pleopod morphology to determine sexual dimorphism and maturity in hermit crabs: Isocheles sawayai as a model. Helgoland Marine Research 63(2): 169-175. doi: 10.1007/s10152-009-0144-0
    » https://doi.org/10.1007/s10152-009-0144-0
  • Ferreira LAA, Guzmán G (2013) Primer registro de intersexualidad en Porcellana platycheles (Pennant, 1777) (Decapoda: Anomura: Porcellanidae). Latin American Journal of Aquatic Research 41(3): 606-610. doi: 103856/vol41-issue3-fulltext-24
  • Ford AT (2012) Intersexuality in Crustacea: an environmental issue? Aquatic Toxicology 108: 125-129. doi: 10.1016/j.aquatox.2011.08.016
    » https://doi.org/10.1016/j.aquatox.2011.08.016
  • Ginsburger-Vogel T (1991) Intersexuality in Orchestia mediterranea Costa, 1853, and Orchestia aestuarensis Wildish, 1987 (Amphipoda): a consequence of hybridization or parasitic infestation? Journal of Crustacean Biology 11: 530-539. doi: 10.2307/1548522
    » https://doi.org/10.2307/1548522
  • Gore RH (1982) Porcellanid crabs from the coasts of Mexico and Central America (Crustacea: Decapoda: Anomura). Smithsonian Contributions to Zoology 363: 1-34. doi: 10.5479/si.00810282.363
    » https://doi.org/10.5479/si.00810282.363
  • Gusev O, Y Zabotin (2007) Observation of intersexuality in land hermit crabs (Anomura: Coenobitidae). Journal of the Marine Biological Association of the United Kingdom 87(2): 533-536. doi: 10.1017/S0025315407054604
    » https://doi.org/10.1017/S0025315407054604
  • Haig J (1972) Galatheidea (Crustacea, Decapoda, Anomura) collected by the F.I.S. Endeavour. Records of the Australian Museum 28(14): 269-289. doi: 10.3853/j.0067-1975.28.1973.411
    » https://doi.org/10.3853/j.0067-1975.28.1973.411
  • Hough AR, Bannister NJ, Naylor E (1992) Intersexuality in the mysid Neomysis integer. Journal of Zoology 226: 585-588. doi: 10.1111/j.1469-7998.1992.tb07501.x
    » https://doi.org/10.1111/j.1469-7998.1992.tb07501.x
  • Kronenberger K, Brandis D, Turkay M, Storch V (2004) Functional morphology of the reproductive system of Galathea intermedia (Decapoda: Anomura). Journal of Morphology 262: 500-516. doi: 10.1002/jmor.10259
    » https://doi.org/10.1002/jmor.10259
  • Mazurová E, Hilscherová K, Šídlová-Štìpánková T, Köhler HR, Triebskorn R, Jungmann D, Giesy JP, Bláha L (2010) Chronic toxicity of contaminated sediments on reproduction and histopathology of the crustacean Gammarus fossarum and relationship with the chemical contamination and in vitro effects. Journal of Soils and Sediments 10: 423-433. doi: 10.1007/s11368-009-0166-x
    » https://doi.org/10.1007/s11368-009-0166-x
  • Nielsen SO (1970) The effects of the rhizocephalan parasites Peltogaster paguri Rathke and Gemmosaccus sulcatus (Lilljeborg) on five species of paguridan hosts (Crustacea, Decapoda). Sarsia 42: 17-32. doi: 10.1080/00364827.1970.10411160
    » https://doi.org/10.1080/00364827.1970.10411160
  • Olmstead AW, LeBlanc GA (2007) The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean. International Journal of Biological Science 3(2): 77-84. doi: 10.7150/ijbs.3.77
    » https://doi.org/10.7150/ijbs.3.77
  • Sant'Anna BS, Turra A, Zara FJ (2010) Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology 10: 201-209. doi: 10.3354/ab00283
    » https://doi.org/10.3354/ab00283
  • Subramoniam T (1981) Protandric hermaphroditism in a mole crab, Emerita asiatica (Decapoda: Anomura). The Biological Bulletin 160: 161-174. doi: 10.2307/1540910
    » https://doi.org/10.2307/1540910
  • Tóth E, Bauer RT (2008) Synalpheus paraneptunus (Crustacea: Decapoda: Caridea) populations with intersex gonopores: a sexual enigma among sponge-dwelling snapping shrimps. Invertebrate Reproduction & Development 51(1): 49-59. doi: 10.1080/07924259.2008.9652255
    » https://doi.org/10.1080/07924259.2008.9652255
  • Turra A (2004) Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. Journal of the Marine Biological Association of the United Kingdom 84: 757-759. doi: 10.1017/S0025315404009877h
    » https://doi.org/10.1017/S0025315404009877h
  • Turra A (2007) Reproductive role of intersex hermit crabs. Crustaceana 80(4): 491-494.
  • Vogt H, Schramm W (1991) Conspicuous decline of Fucus in Kiel Bay (Western Baltic): what are the causes? Marine Ecology Progress Series 69: 189-194.

Publication Dates

  • Publication in this collection
    Mar-Apr 2015

History

  • Received
    01 Dec 2014
  • Reviewed
    03 Feb 2015
  • Accepted
    28 Feb 2015
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