Comparative Study of the Female Gametogenic Cycle in Three Populations of Buccinanops Globulosus (Caenogastropoda: Nassariidae) from Patagonia
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Helgol Mar Res DOI 10.1007/s10152-014-0418-z ORIGINAL ARTICLE Comparative study of the female gametogenic cycle in three populations of Buccinanops globulosus (Caenogastropoda: Nassariidae) from Patagonia Marı´a Soledad Avaca • Pablo Martı´n • Silvina van der Molen • Maite Narvarte Received: 24 June 2014 / Revised: 1 October 2014 / Accepted: 29 October 2014 Ó Springer-Verlag Berlin Heidelberg and AWI 2014 Abstract The populations of Buccinanops globulosus a seasonal gametogenic pattern without the occurrence of a from three different sites of northern Patagonia were resting period. Evacuation of mature oocytes (up to compared in the female reproductive cycle over a 2-year 252.5 lm) occurred mainly from September to December study period (September 2006–August 2008). These pop- (austral spring) in BSA and PV and from December to ulations differed in demographic and life-history traits (sex March (austral summer) in BN. Gonad maturation and the ratios, size frequency distributions, growth rates and presence of females carrying egg capsules in the field fecundity). Also, two of these populations show imposex- coincided with changes in water surface temperature and a affected females (Bahı´a San Antonio, BSA and Bahı´a longer day length. Our results indicate that the occurrence Nueva, BN), whereas the other (Playa Villarino, PV) is of imposex in the populations studied apparently does not imposex-free and constitutes a commercial fishery ground affect the gametogenic activity in females. This study for this species. The gametogenic activity of this species provides further insights into the reproductive biology of B. has not been studied earlier. Females showed the same globulosus. The identification of population variation in gonadal stages in the three populations; however, there reproductive traits should lead to more effective manage- were differences in the female size at which each gonadal ment of the species. stage occurred. Monthly variation in gonadal stages and in oocyte size indicated that females of B. globulosus showed Keywords Gonadal cycle Á Imposex Á Reproductive traits Á Nassariidae Á Patagonia Communicated by H.-D. Franke. Introduction M. S. Avaca (&) Á P. Martı´n Á S. van der Molen Á M. Narvarte Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas (CONICET), Buenos Aires, Argentina Determining reproductive processes in marine organisms is e-mail: [email protected] key to understand their reproductive output and population dynamics (Underwood and Keough 2001). The timing of M. S. Avaca Á M. Narvarte reproduction represents a crucial life-history trait, which Instituto de Biologı´a Marina y Pesquera Almirante Storni, Escuela Superior de Ciencias Marinas, Universidad Nacional del influences both the future prospect of offspring and the Comahue, Gu¨emes 1030, 8520 San Antonio Oeste, Rı´o Negro, parental fitness (Varpe et al. 2007). Finely tuned breeding Argentina seasons may be important to provide juveniles with favorable environmental conditions. P. Martı´n Departamento de Biologı´a, Bioquı´mica y Farmacia, Universidad The sexual activity of organisms living in fluctuating Nacional del Sur, San Juan 670, 8000 Bahı´a Blanca, environments is usually a cyclic event, and gametogenic Buenos Aires, Argentina cycles are a fundamental part of this (Giese and Pearse 1974). Gametogenic cycles are intrinsic processes within S. van der Molen Centro Nacional Patago´nico, Blvd Brown 3100, an individual. However, they are influenced by factors that U9120ACF Puerto Madryn, Chubut, Argentina are both internal, such as accumulation of nutrients and 123 Helgol Mar Res hormonal cycles, and external such as temperature and activity to evaluate them in relation to population charac- photoperiod. External factors may initiate and synchronize teristics (origin and presence/absence of imposex) and to the timing of gametogenic events with environmental environmental conditions (day length and water tempera- changes. Thus, the timing of reproduction may vary from ture). We measured oocyte size as a descriptor of the species to species and among populations of the same gonadal activity and to compare this reproductive trait species. among populations. We also provided new information The nassariid whelk Buccinanops globulosus is an regarding gonadal status at mating and oviposition in order endemic macrofaunal species of coastal waters (up to 10 m to illustrate other aspects of the reproductive biology of this depth) found from 34° to 48°S in the southwestern Atlantic species. The results will provide a more complete picture Ocean (Pastorino 1993). Its habitat is restricted to sandy or of the life history of this species and can be used for future muddy patches, where it spends most of the time buried comparisons among populations of B. globulosus. Also, (Scarabino 1977). Like most Neogastropoda species, B. they could help to identify potential links between repro- globulosus is gonochoristic with internal fertilization. This duction and environmental variables. species is considered as a bioindicator of TBT contami- nation in Patagonian waters because females may be im- posex affected, i.e., characteristics of males superimposed Materials and methods onto females (Bigatti et al. 2009). As in other species of the genus, the egg capsules are attached to the callus and the Sample collection adjacent region of the female shell (Penchaszadeh 1971, 1973; Averbuj and Penchaszadeh 2010; Avaca et al. 2012). The present study was conducted in the northern Patagonia, At oviposition, egg capsules are filled with nurse eggs that Argentina, in Golfo San Matı´as (GSM; 40°500S65°100W) provide nutritional support to a single developing embryo. and Golfo Nuevo (GN; 42°290S63°050W). Specimens were Maternal body size is positively related to some proxies of collected monthly from September 2006 to August 2008 reproductive success (number of nurse eggs, egg capsular from three sites for which other life history features of B. area and total length at hatching) at least in one of the globulosus were known (Narvarte et al. 2008; Avaca et al. populations previously studied (Avaca et al. 2012). B. 2013a, b). Two sampling sites were located in SMG (Bahı´a globulosus is a direct developer: Crawling juveniles San Antonio [BSA]: 40°290S, 63°010W and Playa Villarino emerge from the egg capsules and settle in the maternal [PV]: 40°450S, 64°400W) and one in NG (Bahı´a Nueva environment, a behavior that ensures favorable conditions [BN]: 42°460S, 65°020W; Fig. 1). in the short term but limits dispersal (Penchaszadeh 1973). Specimens were attracted with biological baits (mainly Even though this species constitute a fishery resource discarded fish) and collected from the intertidal-low sub- commercially exploited since 2000 in northern Patagonia tidal zones by SCUBA diving or handpicking, at high and (Narvarte 2006), the gametogenic cycle and other repro- low tide, respectively. This method showed to be efficient ductive traits of this species have not been previously to catch individuals of all sizes at each sampling site studied. (Narvarte et al. 2008). Individuals were kept in containers Our recent studies have shown that this nassariid species filled with sea water to maintain them alive. The presence shows great variability among populations in several of females carrying egg masses in the field was recorded at demographic and life-history traits (sex ratios, size fre- each sampling date. Also, non-systematic observations quency distributions, growth rates and fecundity; Narvarte regarding mating activity (i.e., presence of pairs of indi- 2006; Narvarte et al. 2008; Avaca et al. 2012, 2013a, b). viduals constituted by a male located above a female; This suggests that there may also be variation among Avaca et al. 2012) were performed. populations in the species reproductive traits, such as gametogenic activity. Also, the occurrence of imposex may Laboratory techniques introduce variation between imposex-affected and impo- sex-free populations. While imposex is observed in B. In the laboratory, individuals were kept in containers filled globulosus females carrying egg capsules and thus repro- with sea water and processed within the day of collection. duction does not appear to be compromised (Avaca et al. Individuals were selected to cover the whole size range of 2012), there is considerable interest in the knowledge of each population (Narvarte et al. 2008; Avaca et al. 2013a). the gametogenic activity of imposex-affected females. Thus, small individuals, suspected to be juveniles, were In the present study, we investigated the female game- also included in the subsample for histological analysis. togenic cycle in three populations of B. globulosus from With some exceptions, each subsample contained at least Patagonia using histological techniques. We described ten individuals (Table 1). Based on a first examination, female gonadal stages and seasonality of the gametogenic individuals a priori identified as females, were measured in 123 Helgol Mar Res Fig. 1 Location of the sampling sites in Golfo San Matı´as and Golfo Nuevo in northern Patagonia. PV Playa Villarino, BSA Bahı´a San Antonio, BN Bahı´a Nueva Table 1 Number of individuals Date Bahı´a San Antonio Playa Villarino Bahı´a Nueva histologically processed and number of oocytes measured Histology Oocytes Histology Oocytes Histology Oocytes (number of females used to measure the oocytes) for each Sep 06 12 263 (6) 10 186 (6) 15 289 (7) population and collection date Oct 06 11 159 (4) 9 215 (5) 24 284 (7) Nov 06