BULLETIN OF MARINE SCIENCE, 73(3): 629–641, 2003
A REVIEW OF THE REPRODUCTIVE PATTERNS OF GASTROPOD MOLLUSKS FROM MEXICO
Dalila Aldana Aranda, Erick Baqueiro Cárdenas, Imelda Martínez Morales, Adriana Zetina Zárate and Thierry Brulé
ABSTRACT The reproductive cycles of seven gastropods were analyzed to determine the variabil- ity and similarities in their cycles under diverse environmental conditions: (1) Hexaplex erythrostomus (Swainson, 1831), a carnivore; and (2) Strombus gracilior Soweby, 1825, an herbivore, both from Conception Bay, Baja California; (3) Strombus pugilis Linnaeus, 1758, an herbivore; (4) Melongena corona (Gmelin, 1791); and (5) Fasciolaria tulipa (Linnaeus, 1758), all carnivores from the littoral zone of Campeche Bank; (6) Melongena corona bispinosa (Philippi, 1844), a carnivore from the littoral zone of the Yucatán Pen- insula; and (7) Strombus gigas Linnaeus, 1758 an herbivore from two different coral reefs, Banco Chinchorro in the Caribbean Sea and Alacranes reef in the Gulf of Mexico. Species inhabiting the same locality differed in their periods of maximum spawning ac- tivity. This study identified two gametogenic strategies as a response to the environment: (1) fast gametogenesis during a short period of time (F. tulipa and S. gigas from Chinchorro), and (2) continuous gametogenesis throughout most of the year (S. gigas from Alacranes, H. erythrostomus, S. gracilior, M. corona, and M. corona bispinosa). Variation in the reproductive cycle of a species among different localities can be related to levels of environmental instability. Predation and competition induce massive spawn- ing and reduction of the spawning period.
Reproductive cycles are a response to life strategies and habitat (Mackie, 1984). Spe- cies can be classified into two groups based on the duration of their reproductive cycle: (1) taquitictic, with short reproductive periods, and (2) braditictic, with extended repro- ductive periods. Species with wide geographical distributions exhibit reproductive strat- egies that are highly variable in both duration and intensity (Bricej and Malouf, 1980; Kennedy and Kratz, 1982; Knaub and Eversole, 1988). The reproductive cycles of these two groups are frequently correlated to latitude, particularly temperature, and food avail- ability (Webber, 1977; Bayne, 1978; Sastry, 1979; Fretter, 1984; Mackie, 1984). Gastropods are an important fisheries resource in Mexico and the knowledge of their reproductive cycle is mandatory for proper management of their populations. The aim of this study was to compare and contrast the reproductive cycles of commercial gastropod populations from Mexico, and examine their variations and similarities with regard to the environmental characteristics of their habitats.
MATERIALS AND METHODS
A summary of the seven gastropods species used in this study is presented in Table 1. Twenty individuals of each species were collected monthly in an effort to cover an annual cycle. Collec- tions were made from an outboard vessel by SCUBA diving. The shell length and width were measured for all animals and the whole organism and soft parts were extracted and weighed in the laboratory. To extract the whole body whorl, the shell was broken with a hammer, excluding Strombus pugilis. They were exposed to microwave radiation in a domestic oven at full power for 15 s, and then pulled out (Berg and Adams, 1984). A section of the visceral mass and gonad was fixed with
Bulletin of Marine Science 629 © 2003 Rosenstiel School of Marine and Atmospheric Science of the University of Miami 630 BULLETIN OF MARINE SCIENCE, VOL. 73, NO. 3, 2003
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Bouin solution for Melongena corona bisbinosa and Strombus gigas from both localities; neutral formalin was used for all other species (Luna, 1968). Samples fixed with Bouin were rinsed after 24 hrs, while those fixed with formalin were kept in the fixative for at least one week. Subse- quently, samples were rinsed for 12 hrs with running tap water and preserved in 70% alcohol with 0.1 % glycerin. Tissue samples (1 cm3) were dehydrated with alcohol, cleared with Xylen, and embedded in 53– 56∞ melting point paraffin. Using a rotation microtome the samples were cut into 7 mm sections for males and 12 mm sections for females. All samples were stained with Hematoxiline–eosine (Luna, 1968). The reproductive cycle was defined in five stages: (Stage I) Rest: the gametes cannot be identi- fied from the microscopic section; (Stage II) Gametogenesis: active cell division, mature gametes may or may not be present; (Stage III) Mature: dominance of mature gametes, although some gametogenesis may be present; (Stage IV) Spawn: partially emptied follicles; and (Stage V) Post- spawn: follicles are partially or totally emptied and broken, eggs and sperms are being reabsorbed, presence of phagocytes (Lucas, 1965).
SAMPLING SITES
Conception Bay, Baja California Sur, is located on the gulf coast of Baja California, at 26∞31¢– 26∞53¢ N and 111∞41¢ – 111∞56¢ W. It is 43 km long and 11 km wide, parallel to the Gulf of Califor- nia, with its mouth to the north. The climate on the eastern coast is arid with an average annual rainfall of 200 mm. Mean annual air temperature is 24ºC, with a range of 18–29.6ºC (García, 1981). Mean depth is 22 m with a maximum of 37 m. During the sampling period, evaporation exceeded precipitation through the year, with significant rain occurring only during January and September. Water temperature fluctuated from a minimum of 20ºC during January to 34ºC in Octo- ber, with salinity reaching its highest value of 38 during June 1980 and the lowest of 35 during June 1979. Campeche Bank is located between 18–20∞ N and 90–91∞ W, on the southwest Gulf of Mexico on the Yucatán peninsula. The central and northern coasts of Campeche are part of the Yucatán peninsula of karstic origin. The central part is bordered to the South by the Champoton River and to the north by the city of Campeche. The central coast is a rocky low profile area of sandy pocket beaches with fine sediments. The area is also comprised of coastal mangroves and small marshes. An ample tidal flat, with abundant input of freshwater forms the northern part. Coastal vegetation is composed of mangrove swamps with muddy and sandy beaches (Lankford, 1974). Tides are semidiurnal (Graffé, 1990). The climate is classified as hot and humid with summer rains, and 5.8% rainfall during winter. Average air temperature is 23∞C and average rainfall is 1132 mm (Garcia, 1981). Chuburna is located between 21∞16¢ N and 89∞49¢ W. It has fine sediments from coastal man- groves and small marshes. Coastal vegetation is composed of mangrove swamps. The tidal flat is 0.6 m, with little upwelling of fresh water from underground spring. Annual average salinity was 58 ± 11, with 45 in March and 85 in August. Average water temperature was 31.5∞C ± 3.84, the minimum temperature was 25∞C in June and the maximum was 38∞C in May. Nitrate and oxygen concentrations were 34 ppm and 3 mg L-1 (Valdés and Real, 1994). Tides are semidiurnal (Graffé, 1990) and the climate is hot and humid with summer rains, and 5.8% rainfall during winter. The average temperature is 25∞ C and rainfall is 1364 mm (Garcia, 1981). Banco Chinchorro is a false atoll located 29 km offshore of southern Quintana Roo, between 18∞23'– 18∞47' N and 87∞14'– 87∞27' W. The 561 km2 oval area is 45 km long and 19 km at the widest part. Water depth in the lagoon decreases from 12 m in the south region to 3 m in the central part, to 2 m in the north. Chinchorro has four keys, two small keys known as Cayo Norte, the largest Cayo Centro, and Cayo Lobos. The climate is hot, and humid with summer and winter rains, 10.2% occurring during winter. The average temperature is 26.1∞ C and rainfall is 1249 mm (Garcia, 1981). 632 BULLETIN OF MARINE SCIENCE, VOL. 73, NO. 3, 2003
Alacranes reef is an oval-shaped bank reef formation, covering an area of 293 km2 with a maxi- mum length and width of 26.5 and 14.8 km, respectively. It is located on the north coast of Yucatán, 80 miles off the coast, between 22o21¢–22o35¢ N and 89o 38¢–89o49¢ W (Korniker and Boyd, 1962). The windward zone of the reef system is at sea level, while the leeward zone is 1–10 m below the surface. These two zones enclose the lagoon. Near the western and southern reef edges are four small islands: Pajaros, Muertos, Perez, and Desterrada (Hilderbrand, et al., 1964). The weather is hot and humid with summer and winter rains, 10.2% occurring during winter. The average tem- perature is 25.5∞C and rainfall is 444 mm (Garcia, 1981).
RESULTS
Given the similarities between male and female gonadic stages, we analyzed both sexes together to obtain the percentage of organisms in the different reproductive stages. Hexaplex erythrostomus (Swainson, 1831) was sampled in Conception Bay from March 1979–May 1980. It is a carnivorous species found in the same habitat as Strombus gracilior on a wider range of substrates, from mud to gravel. A significant percentage of organisms were at rest throughout the year, with up to 40% from July–November and 60% during May 1980 (Fig 1). Gametogenesis occurred during three periods with the highest per- centage during March 1979 (80%), October (40%), and March and April 1980 (80%). Very short periods of maturity proceeded the spawning periods, with a maximum of 30% during June 1979, and January and May 1980. Three spawning periods can be identified during April–December 1979. The major spawning event (90%) took place in May 1979, with two secondary peaks (40%) during July and December 1979. Post-spawn was evi- dent in 20% of the population during June–August after the major spawning period. Strombus gracilior (Soweby, 1825) came from a population in Conception Bay. The habitat was a sandy mud bottom and the water depth was 3–15 m. A very high proportion of organisms at rest were present throughout the year, with peaks from February–April 1979 (> 60%), November–December (> 80%) and February 1980 (60%; Fig. 2). Game-
Figure 1. Hexaplex erythrostomus. Percent of organisms in the different reproductive stages from Conception bay, Baja California Sur, Mexico. ALDANA ARANDA ET AL.: REPRODUCTIVE PATTERNS OF GASTROPODS FROM MEXICO 633
Figure 2. Strombus gracilior. Percent of organisms in the different reproductive stages from Conception Bay, Baja California Sur, México. togenesis was present throughout the year, with a higher incidence from May–October 1979, with over 80% of the population in this phase during May and June. A correspond- ing proportion of mature organisms showed a similar trend to the gametogenic activity, but there were fewer organisms in this phase. Two spawning periods were observed, the first at the beginning of both years from February–March 1979 and 1980, and the second from August–November (20%). A very high proportion (70%) of the population was in a post-spawning stage, but only for a short time (December–March). Strombus pugilis (Linnaeus, 1758) came from a population that extends from Seybaplaya to Campeche city. The habitat is a 5-m deep sublittoral sandy area. Data for this species are sparse, covering April and June 1990 and from April 1996–July 1997, but with a gap from October–January. A period of rest was detected during April and June 1990 and 1996 in up to 20% of the population. A very low frequency of rest (5%) was also detected during August and September 1996 with an increase of up to 30% during June and July 1997 (Fig. 3). Gametogenic activity and mature organisms were present in all samples, except for July 1996 when only mature and spawning organisms were found. Spawning organisms were found in June 1990, from June–September 1996, in February and from May–July 1997. Post spawn was detected during April and June 1990 and in April, June, and September 1996, and February and July 1997. Melongena corona (Linnaeus, 1758) from Campeche Bay has a wide range of habitat preferences, from intertidal mangrove swamps and mud flats to sublittoral sea grass beds. The individuals for this study came from sublittoral grass beds off the coast of Isla Are- nas, northern coast of Campeche. Data for this species covers the period October 1996– April 1997, with a lack of data from May–September. Nevertheless, a significant part of the gametogenic activity and spawning was measured. Few organisms were at the rest stage, with a maximum (10%) during October, declining through the winter (Fig. 4). In contrast, intense gametogenic activity reached its maximum peak in November (80%), declining to 30% during January, with a secondary peak in March (40%). During Janu- ary–April very few organisms had mature gametes, generating a spawn of 65% during January. In February and March an accumulation of mature gametes occurred in up to 634 BULLETIN OF MARINE SCIENCE, VOL. 73, NO. 3, 2003
Figure 3. Strombus pugilis. Percent of organisms in the different reproductive stages from Campeche Bay, Mexico.
30% of the population. This period followed a massive spawn of 90% of the population during April. Over 50% of the population was in a post-spawn stage in October and 20% during March. Fasciolaria tulipa (Linnaeus, 1758) came from intertidal mud and seagrass flats of Isla Arenas and Seybaplaya, Campeche. Although sampling is missing from May–August, the reproductive behavior detected from September 1996–April 1997 gave a clear indica- tion of the reproductive strategy of this species. A rest stage began in December with a maximum of 26% during March and April (Fig 5). After a minimum in December, game- togenic activity began in January with 40% of the population and increased to 50% in
Figure 4. Melongena corona. Percent of organisms in the different reproductive stages from Campeche Bay, Mexico. ALDANA ARANDA ET AL.: REPRODUCTIVE PATTERNS OF GASTROPODS FROM MEXICO 635
Figure 5. Fasciolaria (fasciolaria) tulipa. Percent of organisms in the different reproductive stages from Campeche Bay, Mexico.
April. A very clear maturity stage followed gametogenic activity, with accumulation of mature gametes in over 40% of the population from January–March. A constant spawn followed throughout the year with a maximum during October (70%) and December (54%). A post-spawn pattern followed the spawning stage, with a peak during November (47%). Melongena corona bispinosa (Philippi, 1844) came from the mud flats of Chuburna, Yucatán and reproductive data were obtained for 12 mo (March 1996–February 1997). The rest and spawn stages for organisms in this study were not detected (Fig. 6). Game- togenesis was detected in July (50%) and August (70%), giving rise to an intense accu-
Figure 6. Melongena (corona) bispinosa. Percent of organisms in the different reproductive stages from Chuburna, Yucatán, Mexico. 636 BULLETIN OF MARINE SCIENCE, VOL. 73, NO. 3, 2003
Figure 7. Strombus gigas. Percent of organisms in the different reproductive stages from Banco Chinchorro, Quintana Roo, Mexico. mulation of gametes (Rest stage) with peaks in March (70%), May (80%), December (80%), and February (90%). Gametogenic activity was present in all samples except for May and December. Post-spawned organisms were found in all months, reaching a maxi- mum in June (60%) and a minimum in March and August (10%). Strombus gigas, (Linnaeus, 1758) were collected from the Banco Chinchorro central lagoon. The habitat was coral and sandy bottom and the sampling period covered June– September 1993, during the typical spawning period (presence of egg masses in the field). A rest period is evident in 30% of the population during September (Fig 7). Gametogen- esis was present throughout the sampling period, with 30–40% of the population in this stage from June –August, declining to 20% in September. There was a constant presence of mature organisms throughout the sampling period (30–40%). The spawning period was limited to June–August with a peak during July (40%). Only 10% post-spawn was detected during June. Strombus gigas (Linnaeus, 1758) organisms were sampled from sandy bottoms sub- strates in the west of Perez Island in Alacranes reef from March–November 1989. Sam- pling was designed to cover the spawning period based on the presence of egg masses in the field. A discontinuous resting stage is evident in up to 30% of the population, with only one peak correlated to the spawning period (Fig 8). Gametogenesis was constant throughout the sampling period, with a minimum of 30% during July and a maximum in May (100%); this occurred prior to the accumulation of mature gametes from June–Sep- tember. During the period that covers the spawning season, there was only a very low percentage of the population in the spawn stage. However, the very large percentage of post-spawners clearly defines the spawning period from June–October.
DISCUSSION
Strombus gracilior and H. erithrostomus shared the same habitat, but had very differ- ent life strategies. The former is a herbivore-detritivore with planktotrophic larval devel- opment, and the latter is a predator and scavenger, having direct development from an ALDANA ARANDA ET AL.: REPRODUCTIVE PATTERNS OF GASTROPODS FROM MEXICO 637
Figure 8. Strombus gigas. Percent of organisms in the different reproductive stages from Alacranes reef, Quintana Roo, Mexico.
egg capsule. Although their gonad behavior was similar (prolonged rest period, followed by extended gametogenic activity and clear post-spawn), their spawning periods did not overlap. This could be an adaptive behavior to minimize predation of H. erithrostomus juveniles on S. gracilior postlarvae. Hexaplex erithrostomus had a very brief stage of mature gamete storage, with an al- most continuous spawning period. However, there were peaks of maximum spawning intensity and periods of minimal or no activity. In contrast, S. gracilior had a constant high percentage of the population with mature gametes, but only very brief spawning periods that coincided with the periods of little or no activity of H. erithrostomus. Melongena corona and F. tulipa are species with very similar life strategies, from di- rect larval development to their feeding habits. Fasciolaria tulipa is restricted to the lower littoral and sublittoral zones, while M. corona can be found from upper littoral to sublit- toral. The populations for this study, coming from the same location, had similar gonad behavior (constant gametogenic activity, accumulation of mature gametes, particularly during winter and early spring, year-round spawning, and distinct post spawn and rest periods). There were variations in the intensity of gametogenesis, the proportion of the population accumulating mature gametes, and a clear alternation of the spawning peaks. Melongena corona had its peak spawning period in January and April, while the domi- nant spawning time of F. tulipa was from October–December. The alternation of spawn- ing peaks could be a strategy to minimize competition among the juveniles of these two predators. In contrast, S. pugilis has a different life strategy, from planktrophic larval develop- ment to feeding habits. Despite these differences, S. pugilis shares the same gonadic behavior as M. corona and F. tulipa with constant gametogenic activity throughout the year, accumulation of mature gametes, post-spawn, and rest periods. The only differ- ences are the time of year the mature gametes are stored, and that the spawning period is limited to a single period during summer and autumn. 638 BULLETIN OF MARINE SCIENCE, VOL. 73, NO. 3, 2003
Strombus pugilis and S. gracilior are similar species in different oceans. They have the same type of development, habitat preference, and feeding habits. Even though their re- productive cycle reflected constant gametogenesis, storage of mature gametes, post-spawn, and rest stages, spawning for S. gracilior was restricted to two short periods with an ample rest period, while S. pugilis spawning extended over a wider season and a higher proportion of the population engaged in spawning. For the two S. gigas populations analyzed spawning occurred during the same months, July–August; however, significant variations were evident. The population from Banco Chinchorro had a constant presence of organisms with mature gametes, with up to 40% at the beginning of the spawning period, increasing to 50% at the end of the spawning season, and the maximum percentage of spawners was 40%. There was little evidence of post-spawning (only 10% at the beginning of the season). At this locality, more organ- isms were in a state of readiness for spawning, but there were fewer spawning stages. The population from Alacranes reef showed a preparation for spawning with the total partici- pation of mature organisms. This population had a clear post-spawn and fast gonad re- covery, represented by the high percentage of organisms in gametogenesis during Sep- tember. By the increasing percentage of the rest stage after September, it was apparent that a period of re-absorption in both populations started in autumn. The reproductive seasons reported for S. gigas in the Caribbean were not based on histological results. Instead, the reproductive seasons of S. gigas were obtained by obser- vations of reproductive behavior, with copulating or egg laying. Stoner et al. (1992) sum- marized the reproductive seasons for queen conch based on reproductive behavior. In Bermuda (most northern locality), the reproductive season for S. gigas began in May and ended in September. In the Florida Keys, the reproductive season occurred between mid- January and mid-September. For Venezuela (the most southern locality), reproduction peaked from mid-March to mid-November. Corral and Ogawa (1987) showed that S. gigas at Banco Chinchorro, Quintana Roo, laid eggs year-round. Pérez Pérez and Aldana Aranda (2000) reported a reproductive period of S. gigas in Alacranes reef from May– September. Stoner et al. (1992) noted that there was no apparent trend related to latitude in beginning, end, or length of reproductive season for the queen conch from Bermuda to Venezuela. Geographic comparisons of seasonality in reproduction must be interpreted cautiously due to different methods, frequency and number of observations, and different habitat types. In this study the gametogenic cycles for S. gigas had differences between sites, even though the gonad samples were taken during the same period for Alacranes reef and Banco Chinchorro. Therefore, it is likely that the reproductive activity was influ- enced by temperature and photoperiod conditions. Several authors have stated that duration and intensity of the gonad stages are a func- tion of temperature and food availability (Webber, 1977; Bayne, 1978; Sastry, 1979; Bricelj and Malouf, 1980; Jones, 1981; Kennedy and Krantz, 1982; Fretter, 1984; Mackie, 1984; Shephton, 1987). Temperature and food availability induce gametogenesis and define the length and intensity of recovery periods (Lubet and Choquet, 1971; Bayne, 1978). Spawn- ing also may be induced by temperature (Galtsoff, 1964; Holland and Chew, 1973; Hines, 1979), as well as other factors such as salinity fluctuations (Cain, 1974; Stephner, 1981), currents (Davis and Chanley, 1955; Ino, 1970), and the presence of microalgae (Breese and Robinson, 1981). In summary, the gonadic cycle of any one species may vary in the presence, duration, and intensity of the rest and post-spawn, as well as the duration and intensity of the ALDANA ARANDA ET AL.: REPRODUCTIVE PATTERNS OF GASTROPODS FROM MEXICO 639
Table 2. Reproductive patterns of seven study species from five different localities.
Psatterns Sypecie Localit Gametogenesis 1sIntense gametogenesi Fasciolaria tulipa Campeche Bank, Campeche Strombus gigas Banco Chinchorro, Quintana Roo
2sLow intensity gametogenesi Strombus gigas Aánlacranes reef, Yucat Strombus gracilior Conception Bay, Baja California Hexaplex erythrostomus Conception Bay, Baja California Melongena corona Campeche Bank, Campeche Melongena corona bispinosa Cáahuburna, Yucat n Peninsul Spawning 1gConstant spanwin Melongena corona Campeche Bank, Campeche Melongena corona bispinosa Cáahuburna, Yucat n Peninsul Fasciolaria tulipa Campeche Bank, Campeche Strombus pugilis Campeche Bank, Campeche
2eTwo or more spawning puls Strombus gracilior Conception Bay, Baja California Hexaplex erytrostomus Conception Bay, Baja California
3sOne short spawning pulse Strombus gigas Banco Chinchorro, Quintana Roo Strombus gigas Aánlacranes reef, Yucat Gonad recovery 1nMinimum or no post spaw Strombus gigas Banco Chinchorro, Quintana Roo and rest stage Hexaplex erytrostomus Conception Bay, Baja California
2yFast gonad recover Fasciolaria tulipa Campeche Bank, Campeche Melongena corona bispinosa Cáahuburna, Yucat n Peninsul
3eLimited or no mature stag Hexaplex erytrostomus Conception Bay, Baja California Strombus gigas Aánlacranes reef, Yucat Strombus pugilis Campeche Bank, Campeche
gametogenic, maturity, and spawning periods. We identified two gametogenic strategies as responses to the environment: (1) populations with a short gametogenic stage or a small percentage of gametogenic organisms, which represents fast gametogenesis (F. tulipa and S. gigas from Chinchorro); and (2) populations with a continuous gametogen- esis in a very large number of organisms (S. gigas from Alacranes, H. erythrostomus, S. gracilior, M. corona, and M. corona bispinosa). Three variants were defined based on spawning intensity and duration: (1) populations with one very extended spawning period, with or without a dominant peak (M. corona, F. tulipa, S. pugilis, and M. corona bispinosa); (2) populations with two or more clear peaks or spawning pulses (S. gracilior and H. erythrostomus); and (3) populations with one short defined pulse (S. gigas from both localities). The capacity of gonad regeneration is another factor evident in the duration and inten- sity of the post-spawning and rest periods, as well as in the gametogenic and maturity periods. For this, three variants were identified: (1) populations with or without a very short or low intensity post-spawning and rest period (S. gigas from Banco Chinchorro 640 BULLETIN OF MARINE SCIENCE, VOL. 73, NO. 3, 2003 and H. erythrostomus from Conception Bay); (2) populations with fast gonad recovery, in which only a small percentage of organisms can be detected in gametogenesis, with clear and constant presence of mature gametes (F. tulipa from Campeche Bank and M. corona bispinosa from Chuburna, Yucatán Peninsula); and (3) populations with limited or no mature stage that can support a constant or intense spawn (S. gigas from Alacranes reef). These characteristics are summarized in Table 2. When a competitive pressure was evident as was the case for M. corona and F. tulipa from Campeche Bank, or predatory pressure for S. gracilior and H. erythrostomus from Conception Bay, there was a tendency for shorter, more intense, and alternating cycles.
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DATE SUBMITTED: September 14, 2001. DATE ACCEPTED: August 26, 2002.
ADDRESSES: (D.A.A., A.Z.Z., T.B.) CINVESTAV, IPN Unidad Mérida, Km. 6 Antigua Carretera a Progreso, A. P. 73 Cordemex, C.P. 97310, Mérida, Yucatán, Mexico. (E.B.C.) IPN, Altamira, Aeropuerto Internacional Tampico, Tamaulipas, Mexico. (I.M.M.) Instituto de Ecologia , AC Xalapa, Mexico.