Reproductive Cycle of the Penshell <I>Atrina

BULLETIN OF MARINE SCIENCE, 86(4): 785–801, 2010 doi:10.5343/bms.2009.1077 REPRODUCTIVE CYCLE OF THE PENSHELL ATRINA SEMINUDA (MOLLUSCA: BIVALVIA) IN NORTHERN WATERS OF VENEZUELA L. Freites, C. Cordova, D. Arrieche, L. Montero, N. García, and J. H. Himmelman ABSTRACT We examined reproduction of the pinnid bivalve Atrina seminuda (Lamarck, 1819) in tropical waters off northeastern Venezuela and compare it with reproduction of the same species in temperate waters of Argentina, as reported elsewhere (Soria et al., 2002). In Venezuela, a proportion of individuals was reproducing throughout the year, although there was increased spawning activity in certain periods (May–July 2004, September–November 2004, and February 2005). Stepwise multi-regression analyses correlating the frequency of the different gametogenic stages with various environmental factors suggested that reproduction was likely controlled primarily by temperature and secondarily by food abundance (as measured by chlorophyll a). During the first part of the year gamete production appeared to be supported by food resources obtained from the environment (indicating an opportunistic reproductive strategy), whereas gamete production during a period of relatively low phytoplanktonic food availability (June–September) suggested that it was supported by tissue reserves (a conservative reproductive strategy). The above reproductive pattern contrasts with A. seminuda in Argentina where gametogenesis is highly synchronized among individuals and follows an annual cycle. Also, A. seminuda in Argentina displays only the conservative reproductive strategy, with gamete production occurring during the period of food scarcity in the autumn and probably supported by reserves from the adductor muscle (Soria et al., 2002). Together, these data provide the first comparison of reproduction of the same species in both tropical and temperate waters (separated by 50° in latitude). Reproductive timing should vary in different regions for marine invertebrates with wide geographical distributions (particularly for species distributed along a latitudi- nal gradient), as individuals in different regions are exposed to contrasting environmental conditions. The degree to which conditions vary seasonally increases towards the poles and at high latitudes, thus the period when conditions are appropriate for gamete production and larval survival is likely to be restricted (Lalli and Pearson, 1993). Temperate species usually show highly synchronous reproduction with an annual cycle. Often active gametogenesis takes place in the spring and early summer (when phytoplankton is abundant), spawning occurs in summer, and then there is reproductive rest during the winter. Such patterns are demonstrated by the mussel Mytilus galloprovincialis (Lamarck, 1819) in Galicia, Spain (Villalba, 1995), and Myti- lus edulis (Linnaeus, 1758) in Newfoundland, Canada (Thompson, 1984). In contrast, bivalves in tropical regions generally show continuous and asynchronous reproduction, with some individuals producing gametes and spawning in every month of the year. Examples are Anadara grandis (Broderip and Sowerby, 1829) (Cruz-Soto, 1987), Polymesoda radiata (Ruiz et al., 1998), Arca zebra (Swainson, 1833) (Lista et al., 2006), Atrina maura (Sowerby, 1835) (Angel-Pérez et al., 2007), and Nodipecten Bulletin of Marine Science 785 © 2010 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 786 BULLETIN OF MARINE SCIENCE, VOL. 86, NO. 4, 2010 nodosus (Linnaeus, 1758) (García et al., 2007). Since few species extend from temperate to tropical waters, it is not clear how a species with a wide distribution will adapt to the major shifts in environmental conditions. Changes in reproductive patterns within a species across latitudes have only been documented for a small number of species (Urban and Campos, 1994; Angel-Pérez et al., 2007; Cardoso et al., 2007). One example is the study of Bricelj et al. (1987) on the reproduction of the scallop Argopecten irradians (Lamarck, 1819) in widely separated regions. They show that scallop size-specific fecundity is seven fold greater on the coast of New York, USA (40°N), than near the southern limit of its distribution in Florida, USA (27°N). Further, reproduction in A. irradians has been shown to occur later in the year and at higher water temperatures at more southern latitudes. In Massachusetts, USA (42°N), gonad growth in A. irradians begins in April when temperatures attain about 10 °C, gonad size peaks in July to August, and spawning occurs during August and September (Sastry, 1970); whereas in North Carolina, USA (35°N), gonad growth begins in June when the temperature attains 20 °C, gonad size peaks in September, and spawning occurs in October (Sastry, 1970, 1979). Other studies have indicated differences in the timing of reproductive activities in latitudinally separated populations of the same species of bivalve, and food availability appears to be an important factor in explaning the observed shifts in the reproductive cycles (Newell et al., 1982; Barber and Blake, 1983; Cardoso et al., 2007). Such changes in reproduction presumably represent adaptations to environmental changes (Cantillanez et al., 2005; Avendaño et al., 2008). Reproductive strategies displayed by bivalves, even those within a given geographical region, often vary according to the manner in which energy is provided for reproduction (Bayne, 1973). Some species, such as the cockle Cerastoderma edule (Linnaeus, 1758) (Navarro et al., 1989), show a “conservative” reproductive strategy. Energy reserves are built up over a period and later mobilized to support gamete production. Such reproductive activity is strongly linked to energy transfers between tissues. In contrast, other species, such as the clam Venus mercenaria (Linnaeus, 1758) (Ansell and Lander, 1967) and the cockle Glycymeris glycymeris (Linnaeus, 1758) (Galap et al., 1997), show an “opportunistic” strategy. Gametes are only pro- duced during periods when food is available; otherwise, there is reproductive rest. Interestingly, the mussel Mytilus galloprovincialis Lamarck, 1819 appears to show the conservative strategy in some periods and the opportunistic strategy in others (Villalba, 1995). Atrina seminuda (Lamarck, 1819) is a member of the family Pinnidae, which in- cludes bivalves commonly known by such names as callo de hacha, cucharón, cholga paleta, and fan shell. Atrina species generally live in shallow bays and coastal la- goons, on sandy bottoms or in beds of the seagrass Thallassia testudinum Banks & Soland. ex König (Kuhlmann, 1998; Lodeiros et al., 1999; Munguia, 2004). Although A. seminuda has a very wide geographical distribution in the western Atlantic, from North Carolina in the United States to Patagonia in Argentina (Lodeiros et al., 1999), the only report of its reproduction is by Soria et al. (2002) for a population in Argen- tina where there is a strong seasonal environmental cycle. These authors show that A. seminuda in Argentina has a clearly annual reproductive cycle which finishes in the summer (February). The present study examines reproduction of the penshell A. seminuda in tropical waters in northeastern Venezuela and compares it with the pattern observed for A. seminuda in temperate waters in Argentina, as reported by Soria et al. (2002). freites et al.: reproductive cycle OF ATRINA SEMINUDA 787 Materials and Methods We studied a population of A. seminuda at Guayacán, on the north coast of the Araya Pen- insula, northeastern Venezuela (Fig. 1). The collection site was at 3–7 m in depth on a sandy bottom and this area supported a bed of the seagrass T. testudinum. There is considerable resuspension of sediments in the area due to wave exposure and strong tidal currents (semi- diurnal tides with an average amplitude of 0.82 m). To examine the reproductive cycle, we collected 30 adult individuals (160–220 mm in shell length) by snorkel at fortnightly intervals from March 2004 to February 2005. After removing epibionts, the animals were placed in insulated boxes and transported to the Aquaculture Laboratory of the Fisheries Department of the Oceanographic Institute of Venezuela for analysis. For 14–18 of the individuals, we de- termined shell length, shell dry mass, and total dry tissue mass (drying for 72 hrs at 80 °C) and calculated the condition index (tissue dry mass as a percentage of dry shell mass). We did not determine gonad mass because it is difficult to separate the gonad from the digestive gland. For each of the remaining individuals (n = 12–16; at least six individuals of each sex), we made visual notes on the condition of the gonad and then fixed it in Bouin’s solution for 8 hrs. The gonads were later rinsed in running water, dehydrated by transferring them to increasing concentrations of ethanol (70%, 80%, 90%, 95%, and 100%, progressively), and finally embed- ded in paraffin. We used a microtome to make 5–9 µm sections of portions of each gonad and the sections were stained in Harris’ haemotoxyline and eosine. The sections were examined under a Carl Zeiss optical microscope to classify each gonad according to its developmental stage. We used the stages (1) early active, (2) developing, (3) mature, (4) spawning, and (5) spent, as defined by Soria et al. (2002). We did not use the stage “indifferent” of Soria et al. (2002), as we did not encounter gonads with a total absence of gametes. To characterize the different reproductive stages, we measured the diameter of follicles

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