(Mytilus galloprovincialis Lmk) in Venice Lagoon ...

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Reproductive cycle of the mussel (Mytilus galloprovincialis Lmk) in Venice Lagoon (North Adriatic) a

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Luisa Da Ros , Monica Bressan & Maria Gabriella Marin

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Laboratorio del Consorzio per lo Sviluppo della Pesca e del'Acquicoltura del Veneto , Co.S.P.A.V. V.le Stazione 5, 30015, Chioggia, Italy b

Stazione Idrobiologica, Dipartimento di Biologia , Università di Padova , Via Canali 3, 30015, Chioggia, Italy Published online: 14 Sep 2009.

To cite this article: Luisa Da Ros , Monica Bressan & Maria Gabriella Marin (1985) Reproductive cycle of the mussel (Mytilus galloprovincialis Lmk) in Venice Lagoon (North Adriatic), Bolletino di zoologia, 52:3-4, 223-229 To link to this article: http://dx.doi.org/10.1080/11250008509440522

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~ 1 1 .ZOO^. 52: 223.229 (1985)

Reproductive cycle of the mussel (Mytilus galloprovincialis Lmk) in Venice Lagoon (North Adriatic)


LUISA DA ROS Laboratorio del Consoaio per lo Sviluppo della Pesca e dell’Acquicoltura del Veneto C0.S.P.A.V. 1 7 . 1 ~Stazione 5, 30015 Chioggia (Italy) AIONICA BRESSAN, hlARIA GABRIELLA hlARIN Stazione Idrobiologica. Dipartimento di BIologia, Universitk di Padova Via Canali 3, 30015 Chioggia (Italy)

ABSTRACT The reproductive cycle of Mytilrrs galloprovincialis Lmk cultured in Venice Lagoon has been studied from 1979 to 1982. Histology of the gonads shows that the gametes are ripe from September to hlay, when several spawnings occur with a peak at the end of winter (January February). Reproductive activity is quiescent between July and August but release of gametes is possible even in summer, if only to a limited ex tent . ACKNOWLEDGEMENTS We should like to thank Dr. Paolo Breber for reviewing the manuscript, and hlr. Vito Sabia for drawing the graphs.

(Accepted 14 October 1984)

INTRODUCTION

There are numerous papers on the reproduction of lliytilzrs for Atlantic maters, both European (Field, 1922; Chipper field, 1953; Lubet, 1959; Seed, 1975; Aguirre, 1979; Pieters et ul., 1980; Zandee et al., 1980; Sunila, 1981) and American (Engle & Loosanoff, 1944; Moore & Reish, 1969; Hrs-Brenko, 1971; Newell et al., 1982). Less abundant is the information on the sex cycle of A!. guIloprovincia!is (Lubet, 1959; Renzoni, 1961; Costanzo, 1964; Boucart & Lubet, 1965; Valli, 1971; Renzoni & Giusti, 1972; Dimoftache & Telembici, 1972; Renzoni, 1973; Valli el ul., 1975; Seed, 1975). The conclusions of the various studies sometimes disagree on the time and duration of thc reproductive cycle stages, especially about spawning, and this is probably a reflection of the variety of local ecological conditions. Notwithstanding the importance of mussel culture in Venice Lagoon (Da Ros & Pellizzato, 1983), no work has been done on their reproduction in these waters. The study presented here is part of a more general research programme in support of the local mussel culture industry. MATERIALS AND METHODS I n the periods March-November 1979 and September 1980 - August 1982 monthly samples of 80 to 200 mussels in the size range of 45-65 mm were taken from the mussel parks in the southern part of Venice Lagoon. The animals were brought to the Jaboratory and immediateIy opened by cutting the adductor muscle. Because direct inspection of the gonads was often found unsatisfactory for detailed information (Lubet, 1959; Seed, 1975). subsamples of 10-30 bivalves were mounted for histological examination. The soft parts were separated from the she11 and placed in Davidson’s Fixative (Shaw & Battle, 1957) for 21 hrs. Subsequent dehydration with alcohol and inclusion in paraffin were conducted only on a portion cut from the centre of the gonad. The sections (6-7 pm), cut along a dorso-ventral plane, mere stained with

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L. DA ROS, hl. BRESSAN, h1.C. hlARIN

haematoxylin and eosin. The gonadal stages were classified on a modification of Chipperfield's system (1953), summarised thus: stage 0: sexual inactivity stage 1: developmental stage stage 2: ripe stage stage 3: spawning The relative prevalence of the gonadal stages has been plotted in Figure 1. To express which stage w a s prevalent in the sample as a whole, a gonadal indes (Chipperfield, 1953) was calculated in the following manner. In ezch sample the number of mussels at each stage \\-as multiplied by the numerical index of the stage, the products were added u p and finally the result divided by the number of animals in the sample (Fig. 2). The gonadal index so obtained gives further information about the degree of sexual maturity reached by each sample. It varies from 0 (when all the individuals in the sample are in a resting or spent stage) to 3 (when all are spawning). The incidence of males, females, and undifferentiated animals was also registered. Figure 3 gives the mean monthly water temperature for the periods considered (Brunetti et al., 1983). RESULTS

During the time of study, the annual period of the stages varied somewhat (Fig. 1). Sesual rest as indicated by the contraction of the follicular epithelium (Fig. 4a) generally coincided with the warmer

0

0

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0 0

months of June, July and August (Fig. 3). The highest percentage of individuals showing gametogenetic inactivity was almays to be found in August when the water reached its highest temperature (25926°C). At the end of summer when the temperature dropped to 20°C the germinal epithelium resumed activity (Fig. 4b), producing gametocytes which became mature gametes in two or three weeks. By the beginning of October it was possible to find individuals which were in the stage of spawning (stage 3, Fig. dd) or had spawned already and were forming a cecond set of gametes (Fig. de). Each year sexual ripeness was reached in September and continued through autumn and winter till late spring (May and June). After the first spawning, which occurred sometime between the beginning and the end of September, most of the mussels were noted to be in the stages of maturity (stage 2, Fig. 4c), or spawning (stage 3 ) , or rapidly restoring gametes till the onset of the resting period in summer. The spawnings were frequent but not intense during the minter and spring months. The largest spawnings were in February and March, but sometimes as early as January.

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Fig. 1. - The percentile stages of gonadal development shown monthly for Afjtifus galloprovineialis in the years 1979 to 1982.

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rci1sSEL REPRODUCTION IN VENICE LAGOON

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The gonadal index (Fig. 2) never reached 3 (the highest registered being 2.7), which indicates that all stages may be found at all times of the year within the population. I n Figure 5 the relative incidence of stage 3 shows that spawning mussels are always present, going from a winter maximum to a summer minimum. The sex ratio was close to 1: 1 (49,98'/0 8 , 42,98% 9 , 7.05% undifferentiated).

I n periods of low reproductive activity in which undifferentiated animals were more numerous, there were more males than females. Males and females apparently reached the inactive stage at different times and in different ratios (Sunila, 1981). The only hermaphroditic mussel (Fig. 4f) mas found in November 1981; the male part of the gonad was in a more advanced stage of maturation than the female part.

i20P "g 10

1979

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1982

Time (years)

Fig. 3.

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Mean monthly temperature in the Venetian Lagoon, South Basin, Brunetti et ul., 1983).

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(Data from:

L. DA ROS, hl. BRESSAN, h1.G. hlARIN

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Fig. 4. Photomicrographs of the gonads of Aly~ilrrsgalloprovincialis at various stages in the annual cycle. a ) Resting gonad. Note the extremely reduced follicles (arrows) and the absence of sex cells. ~ 2 5 .b) Developing male gonad (developing stage). x 100. c) Fully ripe male gonad (ripe stage). x25. d) Spawning stage in a male gonad. ~ 2 5 .e) Partially spawning stage (note the re-forming of gametes in the follicular epithelium). x 100. f ) Hermaphroditic 'mussel. The female and male follicles are distributed on two different sides of the gonad. ~ 2 . 5 .

h1USSEL REPRODUCTION I N VENICE LAGOON

DISCUSSION


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The period of spawning in the mussels cultured in Venice Lagoon extends from the end of September through the minter to the beginning of June (Fig. 1). This agrees with Bourcart & Lubet (1965), Hrs-Brenko (1971) and Valli et aZ. (1975), who also observed one uninterrupted period of sexual maturity from September to May. Hrs-Brenko (1971), studying the same species on the other side of the Northern Adriatic, also saw the beginning of reproductive activity in September in relation to the cooling of the water to 20°C. Other researchers in other parts of the Mediterranean (Renzoni, 1961 off Naples, 1962 on the coast of Siracusa; Costanzo, 1964 in the Lago di Ganzirri, Sicily; Bourcart & Lubet, 1965 at Toulon; Renzoni & Giusti, 1972 in the Northern Tyrrhenian Sea; Renzoni, 1973 in the Scardovari Lagoon) reported the onset of gametogenesis for the same period of the year, and the lowering of the temperature as its main cause. It is we11 recognised (Lucas et al., 1978) that gametogenesis, especially in the female, requires a large effort, and Lubet (1959) has experimentally shown that the time required for the formation of sex

products is longer in undcrnourished animals. On the basis of these and other works (Bourcart & Lubet, 1965; Dimoftache & Telembici, 1972; Lubet, 1981; Newell et d.,1982) a clear connection is seen in Venice Lagoon between the reproductive cycle and temperature and food. Gametogenesis during September-October, and subsequent spawnings through \im t e r to late spring, are a direct consequence of the nutrient storage (especially glucides) in the summer (Bressan & Marin, unpublished data) when chlorophyll u values keep constant and a t good levels (Brunetti el al., 1983). This seasonal cycle, in which development of storage reserve tissue and gametogenesis do not happen concurrently but consecutively, confirms the good environmental conditions in Venice Lagoon for cultured mussels, according to the results of Lowe et al. (1982) for a population of ill. edzrlis in North Wales. I n particular the lowering of the temperature sets off gametogenesis, while the abundance of food is responsible for the rapidity of gamete formation (just short of a month in duration). The frequency of individuals spawning and of those already in the phase of re-forming at the end of summer shows that maturity is reached

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Fig. 5.

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l

i

l

r

l

l

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1

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- The percentage of stage 3 for the mussel Afytilus galloprovincialis from

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1979

to

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1982.


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very rapidly (Hrs-Brenko, 1971). Valli et al. (1975), on the other hand, studying the mussels in the Bay of Trieste, found early stages of gametogenesis from the bcginning of summer. Lubet (1978) suggested that temperatures lower than 7-8°C retard the maturation of the gametes and for actual spawning higher values are necessary. The waters of Venice Lagoon never reach such low temperatures for extended periods (Brunetti et al., 1983), and observation of gonads revealed that the maturity persists in the spawning stage (3) and in the subsequent re-forming of gametes during the winter months, The increase of temperature at the end of winter and the Concomitant phytoplankton bloom determine an increase in the number of spawning mussels. Similarly to what was noted by Ceccherelli & Rossi (1984) in a deltaic lagoon of the Northern Adriatic, in May and June there is a heavy setting of juveniles in Venice Lagoon (Pellizzato, personal communication). The larvae that set are probably the outcome of successive spawnings, the older among them postponing metamorphosis till the onset of the favourable conditions borne by spring (Hrs-Brenko & Calabrese, 1969; Hrs-Brenko, 1973 a,b). The stage of sexual quiescence in which follicular tissue is minimal and nutrients are stored (Bressan & Marin, unpublished data) is very short but not universal, individuals with ripe gonads being found even in July and August (Hrs-Brenko, 1971; Valli et al., 197.5). The reproductive cycle of Af. galloprovincialis in Venice Lagoon (one annual cycle, long spawning stage with numerous discharge of eggs and sperm, a short period of sexual rest) is basically the same as that described in other localities by Lubet (1959), Costanzo (1964), Bourcart & Lubet (1965), HrsBrenko (1971), and may be defined as “bradyctic” (Franc, 1960; Lubet, 1981b).

L. DA ROS, hl. BRESSAN, h1.G. hlA

The only discordance in literature is w Renzoni (1961; 1962), who at Naples :: Syracuse reports two reproductive cyc in the course of the year, with two c ferent periods of sexual rest, one in win and one in summer. REFERENCES Aguirre hi.€’., 1979 - Biologia del rnejillon A iilris edulis de cultivo de la Ria de Vi, Bol. Inst. Esp. Oceanogr., 5 (3): 107-159 Bourcart & Lubet, 1965 - Cycle et evolution ( reserves chez hlytilzrs galloprovitzcialis (m lusque bivalve). CIEShl, Raports et pro verbaux des reunions. 18 (2): 155-158. Brunet:i R., hlarin hl., Beghi L. & Bressan I 1983 - Study of the pollution in the Veneti Lagoon’s lower basin durine the .oeriod - 19; 1981. Riv. Idrobiol. (In press). Ceccherelli V.U. & Rossi R.. 1983 - Settlemei growth and production of the mussel hlylil galloprovincialis. Mar. Ecol. Progr. Ser., 1

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Chipperfield P.N., 1953 - Observation on t breeding and on the settlement of AJytil edrilir in the British waters. J. hlar. Bic Ass. U.K., 32: 449476. Costanzo G.. 1964 - Ciclo biologico riproduttil di hfyfilirs galloprovincialis Lmk del Lago Ganzirri (hlessina). Atti SOC. Peloritana S Fis. hlat. Nat., 10: 537-543. Da Ros L. & Pellizzato M., 1983 - Allevamen dei bivalvi. in: Acquacoltura. CLESAV, hl lano: 21-47. Dimoftache G.A.. Telembici A., 1972 - Observ tion physiolofiiques et biochimiques sur l’a tiviti sexuelle chez les moules hfrfilirr ea loprovincialis. Cercetari marine, ORCM, “4

181-203.

Engle J.B., Loosanoff V.L., 1944 - Attachmer of larvae of Afyfilzis edzilis L. Ecology, 25

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Field LA., 1922 Biology and economic valu of the sea mussel hJyfiliis edrrlis. Bull. UI Bur. Fish., 38: 127-259. Franc hi., 1960 - Bivalves, in: Trait6 de Zoolc gie. (P.P. Grass6 ed.). Masson, Paris. Hrs-Brenko hl., 1971 - The reproductive q c l of the hiytilirs galloprovittcialis Lmk in th Northern Adriatic Sea and hJyfi1ri.r eddis a Long Island Sound. Thal. Jugoslav., 7: 533

542.

Hrs-Brenko hl., 1973a - Developpement des gona des, ponte et devages des larves de Mytilrr. sp. en laboratoire. Stud. Rev. GFChI, 52

53-65. Hrs-Brenko hi., 1973b - The study of musse

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-LlUSSEL REPRODUCTION IN VENICE LAGOON larvae and their settlement in Vela Draga Bay (Pula, the Northern Adriatic Sea). Aquaculture, 2: 173-182. Hrs-Brenko hi. & Calabrese A,, 1969 - The combined effects of salinity and temperature on larvae of the mussel Afyfilzis ediilis. hIar. Biol.. 3: 224-226. Lowe Dhf., hfoore hfN. & Bayne B.L., 1982 Aspects of gametogenesis in the marine mussel Afytilrrs edrilis L.. J. Mar. Biol. Ass. U.K., 62: 133-145. Lubet P., 1959 - Recherches sur le cycle sexuel et l’emission des gametes chez les mytilides et sur les pectinides, Rev. Trav. Inst. PCches mar., 23: 338-548. Lubet P., 1981a - Action de la tempe‘rature sur le cycle de reproduction des lamellibranches. Bull. SOC. Zool. France, Tome 106, n: 3: 283-292.

Lubet P.. 1981b - Influence des facteurs externes sur la reproduction des Iamellibranches. Oceanis. G: 469-489. Lucas A.. Calvo J. &L Francart hl., 1978 - L’effort de reproduction dans la strategie dPrnographique de six de I’Atlantique. Haliotis, 9: 107-116.

hloore D.R. 8~Reish DJ., 1969 - Studies on the Afvtilzis edrilis community in Alamitos Bay, California. Veliger. 11: 250-255. Newell R.I.. Hilbish T.J., Kolhn R.K. & Newell C.J.,1982 - Temporal variation in the reproductive cycle of Alytilris edulis L. (Bivalvia, hlytilidae) from localities on the East Coast of the United States. Biol. Bull., 162: 299310.

Pieters H., Kluytmans J.H., Zandee D.I. & Cadee G.C.. 1980 - Tissue composition and reproduction of Afytilzis edzrlis with reference to energy metabolism and gametogenesis. Neth. J. Sea Res., 14: 1-29.

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Renzoni A., 1961 Variazioni istologiche stagionali delle gonadi di Afytilris galloprovinciah Lam. in rapport0 a1 ciclo riproduttivo. Riv. Biol., 44: 45-59. Renzoni A.. 1962 - Ulteriori dati sul ciclo biologic0 riproduttivo di Afytilzrs galloprovim cialis Lmk. Riv. Biol., 55: 37-47. Renzoni A.. 1973 - Dati su accrescimento e cido riproduttivo di Afytilris galloprovincialis Lam. nella Sacca di Scardovari. Boll. Pesca, Pisc., Idrobiol., 28: 205-216. Renzoni A. & Giusti F., 1972 - Further observations on the reproductive cycle of Nytilus galloprovincialis Lam., 5th European Marine Biology Symposium. Piccin, Padova: 295300.

Seed R.. 1975 - Reproduction in Afyfilrrs (hlollusca. Bivalvia) in European waters. Pubbl. Staz. Zool. Napoli. 39, Suppl.: 317-334. Shaw 1V.N. & Battle H.I., 1957 - The gross and the microscopic anatomy of the digestive tract of the oyster Crussostrea virginicia (Gmelin). Can. J. Zool., 35: 325-347. Sunila I.. 1981 - Reproduction of Alytilas edulis L. (Bivalvia) in a brackish water area, the Gulf of Finland. Ann. Zool. Fenn., 18: 121128.

Valli G.. 1971 - Ciclo di maturith sessuale in Afytihis galloprovincialis Lmk di Duino (TS). Boll. Pesca. Pisc. Idrobiol.. 26: 259-265. Valli G., Cerneca F. & Ferrantelli N., 1975 Caratteristiche dell’accrescimento e del periodo riproduttivo in un allevamento sperimentale di Alyfilus galloproviricialis Lam. Boll. Pesca, Pisc. Idrobiol., 30: 299-313. Zandee D.I.. Kluytmans J.H. & Zurburg W., 1980 - Seasonal variations in biochemical composition of Afyfiltis edulis with reference to energy metabolism and gametogenesis. Neth. J. Sea Res., 14: 1-29.