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Brachyura: Potamoidea: Gecarcinucidae, Potamidae, and Potamonautidae)

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Brachyura: Potamoidea: Gecarcinucidae, Potamidae, and Potamonautidae) JOURNAL OF MORPHOLOGY 270:175–193 (2009) Ultrastructure of Spermatozoa and Spermatophores of Old World Freshwater Crabs (Brachyura: Potamoidea: Gecarcinucidae, Potamidae, and Potamonautidae) Sebastian Klaus,1* Christoph D. Schubart,2 and Dirk Brandis3 1Institut fu¨ r Zoologie, Universita¨t Heidelberg, INF 230, 69120 Heidelberg, Germany 2Biologie I, Universita¨t Regensburg, Universita¨tsstr. 31, 93053 Regensburg, Germany 3Zoologisches Museum, Universita¨t Kiel, Hegewischstr. 3, 24105 Kiel, Germany ABSTRACT We investigated the ultrastructure of sper- tozoal characters were used in several cladistic matozoa and spermatophores of 19 palaeotropical fresh- studies (Jamieson, 1991, 1994; Jamieson et al., water crab species [12 species of the Gecarcinucidae, 6 1995) and largely support the system of classifica- of the Potamidae (Potamiscinae), and 1 species of the tion of the Brachyura as suggested by Guinot Potamonautidae (Deckeniinae: Hydrothelphusini)]. The (1978), that is, the grouping into Podotremata, investigated Potamiscinae have densely packed coeno- spermic spermatophores with the exception of Thai- Heterotremata s.lat., and Thoracotremata. phusa sirikit and Johora singaporensis that exhibit Brachyuran spermatozoa, as with decapod cleistospermia. In contrast, in the Gecarcinucidae the sperm cells in general, are aflagellate and immo- spermatozoa are loosely embedded in a mucous matrix. tile. The acrosome is spherical and consists of a The gecarcinucid and potamiscine sperm differ, further- central perforatorial chamber (also called a ‘‘perfo- more, in acrosomal structure and size. The acrosome in ratorium’’) that contains microtubule-like struc- the Gecarcinucidae is much smaller and spherical, while tures and is surrounded by several acrosomal the larger acrosome in the Potamiscinae has the tend- zones (see Fig. 1). We will term the electron-lucent ency to be depressed. In the Potamiscinae, an additional zone surrounding the perforatorial chamber the middle acrosomal zone evolved between the acrosome ‘‘inner acrosomal zone’’ (as per Jamieson, 1994). ray zone and the outer acrosomal zone. Within the Gecarcinucidae, a differentiation into two groups (Gecar- This zone is usually surrounded externally by the cinucinae and Parathelphusinae) is not supported by the ‘‘acrosome ray zone’’ in the investigated freshwater present spermatological data. The sperm morphology of crabs (but claimed to be absent in Potamon fluvia- Hydrothelphusa aff. madagascariensis (Potamonautidae: tile, P. ibericum, and Potamonautes sidneyi by Gui- Deckeniinae) differs from Potamonautes sidneyi (Pota- not et al., 1997). The ray zone is defined by its dis- monautidae: Potamonautinae) in acrosomal size and tinct, coarse pattern and the potentially homolo- shape, and in the absence of a periopercular rim. A gous structure in podotreme crabs is called the closer relationship of Deckeniinae and Gecarcinucidae ‘‘fingerprint zone’’ (Guinot et al., 1998). Between cannot be confirmed by spermatology. J. Morphol. the acrosome ray zone and the prominent ‘‘outer 270:175–193, 2009. Ó 2008 Wiley-Liss, Inc. acrosomal zone,’’ an additional zone can be distin- KEY WORDS: spermatozoa; spermatophores; fresh- guished in some species. We term this the ‘‘middle water crabs; Brachyura; Potamoidea acrosomal zone.’’ Apically, the acrosome is capped with an electron-dense operculum that contacts the oocyte during a successful fertilization. Beneath the operculum the subopercular material Brachyuran sperm cell morphology has been separates operculum, inner acrosomal material, investigated for more than 100 years (reviewed in and perforatorial chamber, respectively. The acro- Felgenhauer and Abele, 1991; Jamieson and some is embedded in a cup-like nucleus, while Tudge, 2000). Electron microscopy studies espe- between acrosome and nucleus a thin layer of cyto- cially improved our understanding of the morphol- plasm remains, often accompanied by membrane- ogy and function of brachyuran sperm cells. The ous structures that are interpreted as vestigial acrosomal reaction of the complex brachyuran sperm cell during fertilization was resolved by electron microscopic studies (Brown, 1966). Sper- matological investigations revealed both a con- *Correspondence to: Sebastian Klaus, Institut fu¨ r Zoologie, served ground pattern of sperm cell morphology Universita¨t Heidelberg, INF 230, D-69120 Heidelberg, Germany. within the Brachyura, as well as variability E-mail: [email protected] between groups, mainly at the family level and Published online 22 October 2008 in above (Felgenhauer and Abele, 1991; Jamieson, Wiley InterScience (www.interscience.wiley.com) 1994; Jamieson et al., 1995). Brachyuran sperma- DOI: 10.1002/jmor.10678 Ó 2008 WILEY-LISS, INC. 176 S. KLAUS ET AL. Although freshwater crabs represent one of the most diverse groups within the Brachyura, only a few studies on their spermatozoal and spermato- phore morphology have been conducted (Potamo- nautes sidneyi: Jamieson, 1993; Potamon fluviatile: Tudge and Justine, 1994; P. fluviatile and P. iberi- cum: Guinot et al., 1997; Potamiscus beieri:no description, but depicted in Brandis, 2000 as Pota- miscus sp.; Sinopotamon yangtsekiense: Du et al., 1999; Wang et al., 1999; Austrothelphusa trans- versa: no description, but depicted in Jamieson and Tudge, 2000 as Holthuisana transversa). These previously investigated species belong to the Fig. 1. Diagrammatic drawing of a freshwater crab sperma- African family Potamonautidae, subfamily Potamo- tozoon with nomenclature of its morphology. nautinae (P. sidneyi) and to the Eurasian–North African Potamidae, subfamily Potaminae (P. fluvia- tile, P. ibericum) and Potamiscinae (P. beieri, S. mitochondria (Jamieson, 1993). The nucleus has yangtsekiense), and to the Gecarcinucidae (sensu several to many lateral arms that, in the Bra- Klaus et al., 2006; A. transversa). Within the Old chyura, mostly are without microtubules but con- World freshwater crabs, spermatological data on tain chromatin. the African-Madagascan Deckeniinae (the Decke- Brachyuran spermatophores are considered to niidae sensu Klaus et al., 2006) are still lacking. be one of the most simple type in decapod crusta- Also the spermatozoa and spermatophores of the ceans (Subramoniam, 1991). They are spherical neotropical Pseudothelphusoidea and the Tricho- and consist of sperm masses that are enclosed by a dactylidae (Dilocarcinus septemdentatus: Matos mucopolysaccharide matrix. In some brachyurans et al., 1996) still remain largely unexplored. (e.g., Libinia emarginata, Pisidae and Carcinus Freshwater crabs are well adapted to their maenas, Portunidae), the spermatophores were limnic environment, which also affects their mode reported to consist of two distinct layers with the of reproduction. They show direct development outer layer consisting of chitinous material with relatively few but large, lecithotrophic eggs. (Hinsch, 1991; Subramoniam, 1991). The forma- Earlier studies on freshwater crab spermatozoa tion of the spermatophores takes place in the ante- could not detect correlations of sperm morphology rior vasa deferentia, and both apocrine and exo- with their limnic habitat (Guinot et al., 1997). crine secretion of the epithelia are described Nevertheless, it was proposed that the occurrence (Hinsch, 1991). After copulation, when the sperma- of cleistospermia (spermatophores that contain tophores are transferred to the female spermathe- only a single spermatozoon) could be an adaptation cae, they are dissolved and the spermatozoa to reduce polyspermy, and therefore prevent released. Potentially, the seminal fluids may also wastage of eggs (Guinot et al., 1997). play a role in sperm plug formation (e.g., Ovalipes We understand the Old World freshwater crabs ocellatus, Portunidae, Hinsch, 1986, 1991). as one superfamily Potamoidea (as already kept as Several advantages of the mucopolysaccharide- an option by Klaus et al., 2006) that includes the enveloping of the spermatozoa were suggested, here investigated species. This taxonomic approach among them are mechanical protection, prevention is supported by the proposed potamoid monophyly of dehydration, an antimicrobial function and (von Sternberg et al., 1999; Daniels et al., 2006; nutrition of the sperm (Hinsch, 1991; Subramo- Klaus et al., 2006; Cumberlidge et al., 2008), the niam, 1991). Based on the fact that the spermato- recognition of just two Asian families (the Gecarci- phores are dissolved after copulation in the genus nucidae and the Potamidae; Klaus et al., 2006), Geryon (Geryonidae), Hinsch (1988) proposed that and the still unresolved phylogenetic relationship the spermatophores are mainly a packaging device between the three potamoid families (Gecarcinu- for sperm transfer. A more complex function was cidae, Potamidae, and Potamonautidae; Daniels proposed by Beninger et al. (1993). They observed et al., 2006; Cumberlidge et al., 2008). that in Chionoecetes opilio (Majidae), the sperma- In this study, we describe spermatozoal and tophores perform a ‘‘differential dehiscence.’’ In spermatophore morphology of potamoid freshwater this process, free spermatozoa from the initially crabs with the focus on the Asian Gecarcinucidae dehisced spermatophore are available for fertiliza- (12 species), but also including representatives of tion, while the still intact spermatophores store the Potamidae (the Asian subfamily Potamiscinae, the sperm in the female spermathecae. The sper- six species) and one species of the Madagascan matophore pellicle was
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