Reproductive cycle of coexisting mussels, Mytilus californianus and Mytilus galloprovincialis, in Baja California, New Mexico.ABSTRACT The bay mussel mussel, edible freshwater or marine bivalve mollusk. Mussels are able to move slowly by means of the muscular foot. They feed and breathe by filtering water through extensible tubes called siphons; a large mussel filters 10 gal (38 liters) of water per day. , Mytilus galloprovincialis, and the California mussel The California mussel (Mytilus californianus) is a large edible saltwater mussel or marine bivalve mollusk in the family Mytilidae.
This species is native to the west coast of North America, occuring from northern Mexico to the Aleutian Islands of Alaska. , Mytilus californianus, are sympatric sym·pat·ric
Occupying the same or overlapping geographic areas without interbreeding. Used of populations of closely related species. species in the Pacific coast of Baja California Baja California, state, Mexico
Baja California (Span.: bä`hä kälēfōr`nyä), state (1990 pop. 1,660,855), 27,628 sq mi (71,576 sq km), NW Mexico, on the Baja California peninsula. Mexicali is the capital. in northwest Mexico. To determine the reproductive cycle reproductive cycle
The cycle of physiological changes that begins with conception and extends through gestation and parturition. of both species in a coexistence area, a study of quantitative stereology ster·e·ol·o·gy
The study of three-dimensional properties of objects or matter usually observed two-dimensionally.
ster was carried out from January to December 1995, M. californianus and M. galloprovincialis adults were collected from Mina del Fraile an exposed rocky shore Rocky shore is an intertidal area on seacoasts where solid rock predominates. Rocky shores are biologically rich environments, and make the ideal natural laboratory for studying intertidal ecology and other biological processes. and M. galloprovincialis adults were collected in a culture area a protected bay. In both species spawning organisms were found all year round. At population level, M. galloprovincialis had one major reproductive season from autumn to early spring in both sites. In late autumn, gonad gonad /go·nad/ (go´nad) a gamete-producing gland; an ovary or testis.gonad´algonad´ial
indifferent gonad the sexually undifferentiated gonad of the early embryo. follicles follicles,
n the masses that are embedded in a meshwork of reticular fibers within the lobules of the thyroid gland. See also thyroid gland. were full of ripe gametes and developing gametes and some spawning could occur. However, the spawning peak occurred in early winter. Minor spawning conditions were more frequent in M. galloprovincialis from the culture area than in M. galloprovincialis from the Mina del Fraile. These differences were presumably pre·sum·a·ble
That can be presumed or taken for granted; reasonable as a supposition: presumable causes of the disaster. associated with the most stable environmental conditions in the culture area, which could also influence differences in percentage of storage cells found from spring to summer. The reproductive season of M. californianus took place from winter to summer. The major reproductive activity occurred in spring and the resting season took place during autumn. The reproductive season of M. californianus in the studied locality is from winter to summer, whereas the reproductive season of M. galloprovincialis occurs from autumn to early spring.
KEY WORDS: coexistence, reproductive cycle, spawning, Mytilus galloprovincialis, Mytilus californianus
The mytilids, Mytilus californianus (California mussel) and Mytilus galloprovincialis (bay mussel), coexist in the southern part of the west coast of North America North America, third largest continent (1990 est. pop. 365,000,000), c.9,400,000 sq mi (24,346,000 sq km), the northern of the two continents of the Western Hemisphere. . The distribution of M. californianus is from Alaska to Islas Socorro in Mexico, and the distribution of M. galloprovincialis is from central California Central California can refer to one of several divisions or regions of the U.S state of California:
1. crossbreeding; the act or process of producing hybrids.
2. molecular hybridization
3. between them (Martinez-Lage et al. 1997, Martinez-Lage et al. 2002, Caceres-Martinez et al. 2003, del Rio-Portilla & Caceres-Martinez, in prep.). Studies on the reproductive cycle of coexisting species aid in explaining their coexistence strategy. Suchanek (1981) from field studies carried out in Alaska and Washington stated that the reproductive strategy of Mytilus californianus is based on continuous spawning at a very low level throughout an annual cycle. Mytilus edulis (knowing now that bay mussels in Alaska and Washington correspond to M. trossulus) is a classic fugitive species that rarely reaches a large size, but matures early and is characterized by a single massive reproductive output each year.
Different techniques have been used to assess the reproductive condition in mussels. A summary on studies of reproduction seasons in mussels from North America is shown in Figures 1 and 2. Seed (1976) from an analysis of reproduction records for several mytilids from various parts of their geographical range noted that mussels from the warmer more southerly waters of the Northern Hemisphere generally spawn earlier than those further north. Southern species usually reproduce later in the year and have a progressively restricted season further north; northern species exhibit the reverse trend, spawning earlier and with a more extended season further south. A wide reproductive period in the southern part of the Northern Hemisphere has also been observed in other studies (Ferran 1991, Villalba 1995, Caceres-Martinez & Figueras 1998).
[FIGURES 1-2 OMITTED]
Minor local variations in the reproductive cycle of the same mussels species has also been studied. Seed (1976) described that the gonadal gonadal
pertaining to or arising from a gonad. See also testicular, ovarian.
cords formed by epithelial cells which migrate from the mesonephric tubules in the embryo to the gonadal ridge and establish the indifferent development of Mytilus edulis in England was faster in mussels from the low intertidal zone The intertidal zone, also known as the littoral zone, in marine aquatic environments is the area of the foreshore and seabed that is exposed to the air at low tide and submerged at high tide, i.e., the area between tide marks. , than in those from the upper zone and he related these results to food availability. Local variations in the gonadal cycle of Mytilus galloprovincialis were found in Spain and these differences were associated with environmental conditions (Ferran 1991, Villalba 1995), but the gonadal cycle of wild M. galloprovincialis from the low intertidal in·ter·tid·al
Of or being the region between the high tide mark and the low tide mark.
in exposed rocky shores and from those cultured in floating rafts was similar (Caceres-Martinez & Figueras 1998).
There are no studies on the reproductive cycle in coexisting M. galloprovincialis and M. californianus from the same exposed rocky shore in Baja California, Mexico (the southern distribution area of M. galloprovincialis and M. californianus in the Pacific coast of North America) or on the comparison of the reproductive cycle between M. galloprovincialis from exposed and culture conditions. The objectives of this study are to determine the time and duration of the reproductive period of M. californianus front exposed conditions, and of M. galloprovincialis from exposed and culture conditions through quantitative stereology.
MATERIALS AND METHODS
To determine the reproductive cycle using the proportion of germinal Germinal
conflict of capital vs. labor: miners strike en masse. [Fr. Lit.: Germinal]
See : Riot
portrays the sufferings of workers in the French mines. [Fr. Lit. and storage cells in the natural population and the cultured Mytilus galloprovincialis and the natural population of Mytilus californianus, two samplings were planned from January to December 1995. The first sampling was carried out in an exposed rocky shore named Mina del Fraile south of Bahia de Todos Santos (Fig. 3) where M. galloprovincialis and M. californianus coexist in the intertidal zone. Each month, 30 individual adults from each species where recollected from the middle intertidal zone during low tide periods. The morphologic differentiation of both species at the adult stage was easy. See the morphologic criteria established by Caceres-Martinez et al. (2003). A total of 360 mussels from each species were sampled; their mean shell length was 57 [+ or -] 5.8 mm for M. californianus, and 63 [+ or -] 8.2 mm for M. galloprovincialis. The second sampling was carried out taking 30 M. galloprovincialis adults from culture ropes (5 m depth) each month in the culture area located in Bahia de Todos Santos (see Fig. 3). A total of 360 mussels with a mean shell length of 64 [+ or -] 6.3 mm were sampled. Mussels from both samplings were brought to the laboratory in plastic bags and were cleaned with a brush and a jet of seawater seawater
Water that makes up the oceans and seas. Seawater is a complex mixture of 96.5% water, 2.5% salts, and small amounts of other substances. Much of the world's magnesium is recovered from seawater, as are large quantities of bromine. .
[FIGURE 3 OMITTED]
The soft tissue from each mussel was fixed in Davidson's fixative fixative /fix·a·tive/ (fik´sit-iv) an agent used in preserving a histological or pathological specimen so as to maintain the normal structure of its constituent elements.
adj. (Shaw & Batle 1957). An anterior transverse section was taken, including the mantle tissue. Histologic sections with a thickness of 5 [micro]m were cut and stained with hematoxylin hematoxylin /he·ma·tox·y·lin/ (he?mah-tok´si-lin) an acid coloring matter from the heartwood of Haematoxylon campechianum; used as a histologic stain and also as an indicator. and eosin eosin /eo·sin/ (e´o-sin) any of a class of rose-colored stains or dyes, all being bromine derivatives of fluorescein; eosin Y, the sodium salt of tetrabromofluorescein, is much used in histologic and laboratory procedures. . The presence of gametes and storage cells were determined by quantitative stereology using a Weibel (1969) graticule Grat´i`cule
n. 1. A design or draught which has been divided into squares, in order to reproduce it in other dimensions.
Noun 1. following the method described by Briarty (1975), Lowe et al. (1982), Seed and Suchanek (1992), and Caceres-Martinez and Figueras (1998). Five random counts were carried out on each histologic slide. Results are given as a percentage of mantle volume occupied by the gamete gamete (găm`ēt): see reproduction. development stages and cell types or mantle components (MC) defined as ripe gametes (RG). In the female, it is the stage in which oocytes were free within the follicles and some oocytes remained attached to the follicle follicle /fol·li·cle/ (fol´i-k'l) a sac or pouchlike depression or cavity.follic´ular
atretic ovarian follicle an involuted ovarian follicle. wall; whereas in the male, it is the stage when follicles were filled by spermatozoa spermatozoa
see spermatozoon. arranged in characteristic bands. Similar to the females during the developing stage of gametes (DO) when rounded oocytes along with oocytes were found attached to the follicle wall, in the male varying quantities of developing spermatogonic cells were present. Additional observations on the presence of hemocytes around gametes, and conditions of the follicle walls were recorded to determine if gamete reabsorption reabsorption /re·ab·sorp·tion/ (re?ab-sorp´shun)
1. the act or process of absorbing again, as the absorption by the kidneys of substances (glucose, proteins, sodium, etc.) already secreted into the renal tubules.
2. was occurring. The other cell components in the gonad were vesicular vesicular /ve·sic·u·lar/ (ve-sik´u-ler)
1. composed of or relating to small, saclike bodies.
2. pertaining to or made up of vesicles on the skin.
3. cells of connective tissue (VCT VCT Voluntary Counseling and Testing
VCT Vinyl Composition Tile
VCT Saint Vincent and the Grenadines (ISO Country code)
VCT Venture Capital Trust (UK fiscal status) ) and adipogranular cells (AC); empty follicles (EF) were recorded when the points of the indicate an empty area inside the follicle.
The one-way ANOVA anova
see analysis of variance.
ANOVA Analysis of variance, see there was used to determine if gametes (RG and DG) were different among mussel species throughout the study period in both localities and species (Sokal & Rohlf 1987).
Variations in percentage of the different cell types in the mantle volume of Mytilus galloprovincialis from the culture area are shown in Figure 4A. RG and DG were found throughout the study period. RG and DG reached their maximum levels in October and November indicating a major spawning period, but remained up to 50% from December to April. EF were from 12.9% in October to 24.2% in March, values of RG and DG in April were around 50%, but gametes were surrounded by hemocytes and follicle walls were in regression, showing a reabsorption period. The reproductive season started in October and ended in March. AC reached their maximum from May to September whereas VCT rose from April to September showing the storage of reserves during spring and summer, which would be used for the next massive gametogenesis Gametogenesis
The production of gametes, either eggs by the female or sperm by the male, through a process involving meiosis. In animals, the cells which will ultimately differentiate into eggs and sperm arise from primordial germ cells set aside from the . Variations in percentage of the different cell types in the mantle volume of this species from the exposed rocky shore ale shown in Figure 4B. RG and DG were also found throughout the study period with their maximum values in November showing a major spawning period, their prevalence remained up to 40% from December to March, when reabsorbing conditions were observed. reaching minimum values from June to September. EF were recorded throughout the study period reaching their higher values from 18.5% in November to 26.6% in February. At this time, AC were in a lower proportion with minimum values in January and February. VCT were present throughout the study period with maximum values from June to September. The percentage of MC was similar to those described above for this species in culture conditions from November to February; and it was different from March to September, the period when the accumulation of reserves was more intense. In general, differences in percentage of gametes throughout the study period in both localities were significant ([F.sub.(2, 4907)] = 301, P = < 0.01).
[FIGURE 4 OMITTED]
The variations in percentage of the different cell types in the mantle volume of Mytilus californianus from the exposed rocky shore are shown in Figure 4C. RG and DG were found throughout the study period with minimum values from August to December, while maximum values were recorded from January to July (up to 40%). Their maximum values were reached from February to June showing the major spawning activity. EF were recorded throughout the study period at similar percentage values. AC were recorded in all the months sampled, with maximum values in September and October (storage of reserves); their minimum values were reached from March to May. VCT were present throughout the study period with maximum values from September to December. Differences in percentage of gametes throughout the study period in both localities and species were significant ([F.sub.(2, 4907)] = 301, P = < 0.01).
The reproductive season of Mytilus galloprovincialis cultured in Bahia de Todos Santos is more extended than those from the same species in the exposed rocky shore from Mina del Fraile. These observations could be related to environmental conditions. Culture mussels feed underwater at all times and they are not exposed to environmental changes such as desiccation des·ic·ca·tion
The process of being desiccated.
desic·ca or to sharp temperature changes due to tides at midnight or midday. Thus. external conditions during the season of reserves accumulation (i.e. temperature changes, food availability, wave splash, and photoperiod photoperiod /pho·to·pe·ri·od/ (fo´to-per?e-od) the period of time per day that an organism is exposed to daylight (or to artificial light).photoperiod´ic
n. ) seem to be more stable in the culture condition than in exposed rocky shore conditions, allowing a more frequent and intense reproduction (see Fig. 4. A,B). Seed (1976) described that the gonadal development was faster in mussels from the low intertidal than in those from the upper intertidal, relating these results to food availability. Ferran (1991) and Villalba (1995) associated local variations in the gonadal cycle of mussels cultured in Galician bays in Spain to environmental conditions.
Comparing the reproductive season of M. galloprovincialis with M. californianus it is observed that in some months the percentage of MC was similar in culture or exposed rocky shore conditions; however, the reserves accumulation period Accumulation Period
1. The phase in an investor's life when he/she builds up his/her savings and the value of his/her investment portfolio with the intention of having a nest egg for retirement.
2. between species shows differences in reproductive cycles. The most intense spawning period in M. californianus occurred from middle winter to spring. It is clear that M. californianus presents a more extended reproductive season from winter to summer, suggesting that endogenous factors, regulating the reproductive cycle in this species, and the exogenous factors act in conjunction in different ways in comparison to M. galloprovincialis.
A comparison of the reproductive season of M. galloprovinicialis found in this study at regional scale showed a similar pattern to those described for the bay mussel from Washington to southern California (see Fig. 1), which shows a reproductive season between October and April, with the exception of the studies by Graham and Gay (1945), Coe (1932) and Young (1946) in the Pier of Scripps Institution of Oceanography Scripps Institution of Oceanography: see California, Univ. of. and Rocky Point. The first two authors arrived to the conclusion that through spatfall studies; thus it is probable that spawning period could be earlier than stipulated. The last author came to his conclusion from spawning induction in laboratory, which does not represent the reproductive conditions of the mussel population in the wild. There seems to be a pattern of reproduction period from autumn to early spring of bay mussels from Washington to Baja California and from spring to summer in Vancouver Island. Are these differences related to the bay mussel species Mytilus trossulus towards north, and Mytilus galloprovincialis towards south? Or to latitudinal and local conditions? A comparison on reproductive seasons of the bay mussels (M. trossulus and M. galloprovincialis) is necessary using the same technique in the north western coast of North America to determine the reproductive strategy of these two bay mussel species.
On the other hand, reproductive periods of Mytilus californianus recorded in the Pacific coast of North America (see Fig. 2) show spawning periods almost all year round. Our results and those from the mentioned studies in Figure 2, support in part the observations by Suchanek (1981) mentioning that the reproductive strategy of M. californianus is based on continuous spawning at very low level throughout an annual cycle. However, more studies on the spawning intensity or level of this species all year round in comparison to M. galloprovincialis are needed to confirm the observation by Suchanek.
The results of this study show that M. galloprovincialis has a less extended reproductive season in the rocky shore exposed environment than in the culture conditions, and the reproductive cycle of this species in both localities is less extended than those of M. californianus in the exposed rocky shore environment. This period takes place from autumn to early spring, whereas for M. californianus it lakes place from winter to summer, both species having smaller spawning periods all year long.
The mussel settlement season in Bahia de Todos Santos has been recorded in December and January (Curiel-Ramirez & Caceres-Martinez 1999, Curiel-Ramirez 2000), coinciding with the spawning observed for M. galloprovincialis in this study. Current studies on the identification of recently settled mussels sup ports the fact that the majority of the spat from these months correspond to this species (Curiel Ramirez & Caceres-Martinez, in prep), such as it had been mentioned about the necessity of studies on the intensity of spawning in these species. Also, studies are necessary on the settlement intensity of both species by identification of recently settled mussels during the year.
The authors thank S. Guevara from Aquacultura Oceanica for allowing us technical assistance for sampling in their mussel culture facility, The authors also thank Rebeca Vasquez for processing samples. This project was supported by the CICESE CICESE Centro de Investigacion Cientifica y de Educacion Superior de Ensenada (Spanish) project number 623106. Curiel-Ramirez received a grant from Conacyt, Mexico.
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SERGIO CURIEL-RAMIREZ AND JORGE CACERES-MARTINEZ *
Centro de Investigacion Cientifica y de Educacion Superior de Ensenada, Laboratorio de Biologia y Patologia de Organismos Acuaticos del Departamento de Acuicultura, Apdo. Postal 2732, 22800, Ensenada, Baja California
Ensenada is the third-largest city in the Mexican state of Baja California. It is located 116 km (about 70 miles) south of Tijuana, at . , Mexico
* Corresponding author. E-mail: firstname.lastname@example.org