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Morphology of Seminal Receptacle of the Harvested Golden Crab Chaceon Chilensis and Its Implication in the Fertilization Process

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Morphology of Seminal Receptacle of the Harvested Golden Crab Chaceon Chilensis and Its Implication in the Fertilization Process Invertebrate Biology 136(2): 199–206. © 2017, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12170 Morphology of seminal receptacle of the harvested golden crab Chaceon chilensis and its implication in the fertilization process Luis Miguel Pardo,1,2,a Constanza Ceroni,1 Marcela Paz Riveros,1 Billy Ernst,3 and Josefa Pino4 1Instituto de Ciencias Marinas y Limnologicas, Laboratorio Costero Calfuco, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile 2Centro FONDAP de Investigacion en Dinamica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile 3Departamento de Oceanografıa, Universidad de Concepcion, Concepcion, Chile 4Programa de Magister en Pesquerıas, Departamento de Oceanografıa, Universidad de Concepcion, Concepcion, Chile Abstract. The external and internal architecture of crab seminal receptacles are closely asso- ciated with mating behavior, sperm transfer, and storage patterns, and ultimately reproduc- tive success. Therefore, describing their anatomy contributes to the development of a greater understanding of crab reproductive biology. In this study, we describe the anatomy and tissue characteristics of the seminal receptacle of the golden crab Chaceon chilensis,a harvested deep-sea species from the Juan Fernandez Archipelago (off central Chile). Females in the late mature stage were used as reference for histological description. Mor- phological features of the seminal receptacle included: (1) a dorsal receptacle–oviduct con- nection, (2) velum and septum separating the dorsal and ventral chambers, (3) extensive glandular epithelium in both chambers, (4) a ribbed chitin line, (5) a highly folded, bilobu- lated ventral chamber, and (6) a simple-type vagina. Some of these traits (2, 3, 4, 5) are novel for crab receptacles and could contradict the generalized idea about the pattern of sperm precedence associated with the location of the receptacle–oviduct connection. Exter- nal sperm plugs were not found in mature females, but variations in the color of opercula occluding the vulva were used to assess sexual maturity. The seminal receptacle of C. chilen- sis has an unusual internal morphology with vast sperm storage capacity and separate stor- age areas for sperm ejaculates, which could allow for cryptic female choice. In cases like these, male–male competition is usually intense and males deliver large quantities of sperm in each mating event, which makes them vulnerable to sperm depletion. Additional key words: reproduction, Brachyura, fishery, sperm storage, mating The seminal receptacles of diverse brachyuran et al. 2003). In crabs, it has been hypothesized that crabs have been described in order to understand the seminal receptacle has a meso-ectodermal origin their role in sperm storage dynamics, fertilization, (McLay & Lopez-Greco 2011) and a generally simi- and multiple paternity (Hartnoll 1968; Sainte-Marie lar morphology among species (i.e., a sac that can et al. 2000; Becker et al. 2011; Gonzalez-Pisani et al. be elongate, globose, or kidney-shaped). However, 2012; Pardo et al. 2013). All of these aspects can fine anatomical configuration and details of internal influence the reproductive success of a species. The architecture of eubrachyuran seminal receptacles are receptacle structure that is unique to Eubrachyurans species specific. allows females to store ejaculates (sperm and semi- Golden crabs, which belong to the family Gery- nal liquid) to produce several broods in short time onidae, are deep-sea crabs mostly distributed on periods under favorable conditions (Fischer & continental slopes and are often intensively har- Thatje 2008) or produce broods without the need of vested around the world (Hastie 1995). In Chile, the a fresh sperm supply over long time periods (Hines golden crab Chaceon chilensis CHIRINO-GALVEZ & MANNING 1989 has been the focus of a small arti- aAuthor for correspondence. sanal fishery in the Juan Fernandez Archipelago E-mail: [email protected] since the early 2000s (Ernst et al. 2011). This fishery, 200 Pardo, Ceroni, Riveros, Ernst, & Pino operating at a depth of 300–1000 m, has shown a was determined according to criteria established pre- high prevalence of males in the catch (Guerrero & viously by Pino (2015). Arana 2009), which could indicate a partial spatial Six individuals were anesthetized by chilling, sac- segregation by sex, as in other geryonids (Melville- rificed, and their gonadal state determined according Smith 1987). to the method of Pardo et al. (2009). This catego- Little information has been reported on seminal rization was based principally on ovarian volume receptacle morphology of golden crabs. Seasonal and maturity of gametes as determined histologically variation in size and turgidity of the seminal recep- (oocytes in early, late, or post-vitellogenesis). The tacle has been described for Chaceon quinquedens lower section of the reproductive tract was carefully (SMITH 1879), Chaceon maritae (MANNING & extracted. A stereomicroscope was used to describe HOLTHUIS 1981), and Chaceon fenerii (MANNING & and photograph the gross external anatomy, includ- HOLTHUIS 1984) (Haefner 1977; Melville-Smith 1987); ing the connection between the seminal receptacle, however, these studies did not provide a detailed the oviduct, and vagina. The reproductive tract was description of the structure. Hinsch (1988), using then fixed in Bouin solution (picric acid, saturated light- and electron-microscopic techniques, provided aqueous solution; formalin, 40% aqueous solution; the first description of sperm and spermatophores acetic acid, glacial; 15:5:1 proportion) for at least inside receptacles of C. fenerii, but the study did 2 days. Samples were dehydrated through an not include a detailed description of the internal ascending ethanol series (50–100%), embedded in anatomy or histological characteristics of the recep- paraffin, and serial sections of 6 lm were cut for tacle. histological analysis. Sections were stained with This study provides a fine-scale description of the hematoxylin–eosin and Masson trichrome tech- morphology of the seminal receptacle and its associ- niques (Lynch et al. 1987). Finally, the histological ated structures from mature female specimens of sections were mounted using PermountÒ (Fisher C. chilensis, using different histological techniques Scientific GSA, Fair Lawn, NJ, U.S.A.) and to identify different components. Anatomical studies observed and photographed using a compound light of receptacles are an important first step toward microscope. addressing questions about sexual selection and pro- viding information relevant to fisheries assessment Results (Sainte-Marie & Lovrich 1994; Hines et al. 2003; McLay & Lopez-Greco 2011; Pardo et al. 2016). The appearance of mature ovaries was similar to that of other brachyurans (Johnson 1980), laying Methods dorsal to the hepatopancreas and extending on either side along the anterior margin of the Mature female golden crabs were obtained in cephalothorax (Fig. 1A). Ovarian lobules connected Juan Fernandez Archipelago (33°350S; 78°400W) dorsally to the seminal receptacles. Each seminal from the commercial catch in November 2012 and receptacle had a cup-shaped appearance (Fig. 1B), sent live to Laboratorio Costero Calfuco at the with the ovary partially enveloping the receptacle on Universidad Austral de Chile in Valdivia. Maturity its dorsal side. The ventral side of the receptacle was Fig. 1. Reproductive system of Chaceon chilensis. A. Dorsal view of the cephalothorax of a mature female with dorsal carapace removed to reveal the ovary in relation to the gills and heart. B. Isolated seminal receptacle showing its rela- tionship to ovary and vagina. C. Vulva (arrow) on ventral surface of female carapace. Scale: A=20 mm; B=5 mm; C=10 mm. G, gills; H, heart; Ov, ovary; RS, seminal receptacle; VA, vagina. Invertebrate Biology vol. 136, no. 2, June 2017 Seminal receptacle of golden crab 201 the cephalothorax, close to the 5/6 sternal thoracic suture. In mature females, the vulvae were ovoid with a blackened margin (Fig. 1C). Dorsal and ventral chambers of seminal recepta- cles were clearly distinguishable in histological sec- tions (Fig. 2A,B). All females analyzed showed ovaries in late vitellogenesis or post-vitellogenesis, with round yolk granules distributed homogeneously within oocytes (Fig. 3A); therefore, all females ana- lyzed were classified as mature females. The zone, where ovaries connected with the receptacle (Fig. 3B), was composed of connective tissue that was tightly bound to the proximal oviduct (Fig. 3C), Fig. 2. Seminal receptacle of Chaceon chilensis. A. Sagit- which appeared not to open completely. Squamous tal histological section. B. Sketch showing internal regions cells derived from the epithelium of the dorsal of the seminal receptacle; each number indicates the area chamber (i.e., dense layer) occluded the receptacle of histological sections shown in subsequent figures. Scale entrance (Fig. 3D). bar=2 mm. DC, dorsal chamber; E, ejaculate; Ov, ovary; The dorsal chamber was externally covered by con- SE, septum; VA, vagina; VC, ventral chamber; VE, velum. nective tissue, followed by collagenous fibers and a dense layer of proliferative cells forming a stratified connected with a short, hardened vagina (Fig. 1B). squamous epithelium (Fig. 4A). Epithelial cells were When seminal receptacles were removed from the observed to slough off toward the lumen of the dorsal females, they were whitish in color with some
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