Shell growth and reproductive cycle of the Mediterranean mussel ...

Plankton Benthos Res 5(Suppl.): 214–220, 2010

Plankton & Benthos Research © The Japanese Association of Benthology

Shell growth and reproductive cycle of the Mediterranean mussel Mytilus galloprovincialis in Tokyo Bay, Japan: relationship with environmental conditions NOBUYUKI OKANIWA1,3, TSUZUMI MIYAJI1, TAKENORI SASAKI2 & KAZUSHIGE TANABE1, * 1

Department of Earth and Planetary Science, The University of Tokyo, Hongo 7–3–1, Tokyo 113–0033, Japan Department of Curatorial Studies, The University Museum, The Univesity of Tokyo, Hongo 7–3–1, Tokyo 113–0033, Japan 3 Present address: Rural Policy Department, Rural Development Bureau, Japanese Ministry of Agriculture, Forestry and Fisheries, Kasumigaseki 1–2–1, Tokyo 110–8955, Japan 2

Received 7 March 2010; Accepted 11 May 2010

Abstract: This study investigates shell growth patterns and the reproductive cycle of the Mediterranean mussel Mytilus galloprovincialis in Tokyo Bay, central Japan. A follow-up study of marked mussels within the intertidal zone from July 2007 to September 2008 indicates a remarkably fast annual shell-growth rate and a short life span, reaching the maximum shell length (ca. 70 mm) at age 3 or 4 years. Histological examinations of mussel gonads collected fortnightly revealed that the Tokyo Bay population has a spawning season between late autumn and spring, and attains sexual maturation several months after recruitment. Shell growth patterns for individual mussels show seasonal variations, with high shell-growth rates during spring and summer, and minimal growth from late autumn to early spring. Slow shell growth during winter is possibly controlled by combined environmental (lower air and seawater temperatures, and scarce phytoplankton) and physiological (the reproductive effort expended in gametogenesis and spawning) factors. Key words: Mytilus galloprovincialis, reproductive cycle, shell growth, Tokyo Bay

Introduction The nature of environmental and physiological controls on organism growth is an important subject in ecology. In this regard, bivalve mollusks preserve high-resolution records of life-history traits and environmental change in their incremental shell sequence (e.g., Schöne et al. 2002, 2005, Miyaji et al. 2007). Sessile epifaunal bivalves of the intertidal zone are suitable subjects for analyses of environmental and physiological controls on shell growth, as living animals are in direct contact with the surrounding seawater during high tides and are subaerially exposed during low tides. The epibyssate mytilid Mytilus galloprovincialis Lamarck investigated in the present study originated from the Mediterranean Sea, but has been introduced to mid- and high-latitude coasts in both hemispheres as a result of human activity (Gosling 1992). This species has been described from the Pacific coast of North America (McDonald & Koehn 1988, Cáceres-Martínez 2004), Japan (Wilkins et al. 1983, Ishida et al. 2005), South Africa * Corresponding author: Kazushige Tanabe; E-mail, [email protected]. ac.jp

(Grant & Cherry 1985), and the British Isles (Ahmad & Beardmore 1976). Wild and cultured mussels of this species have been investigated in terms of their growth, population dynamics, and reproductive cycle, in the Mediterranean (e.g., Ceccherelli & Rossi 1984, Abada-Boudjema & Dauvin 1995, Bodin et al. 2004, Lök et al. 2007, Peharda et al. 2007, Sarà & Pusceddu 2008), Atlantic coast of northwest Spain (Villalba 1995, Cáceres-Martínez & Figueras 1998), west coast of southern Africa (Schurink & Griffiths 1991), and Pacific coast of northwest Mexico (Cáceres-Martínez 2004). These previous works demonstrated that the life-history traits of this species are characterized by a high shell-growth rate, short life span, and an early onset of reproduction. However, the nature of environmental controls on shell growth and reproductive cycle in this species remains to be fully determined. In this study, to investigate environmental controls on shell growth and reproductive cycle of M. galloprovincialis in the Northwestern Pacific region, we performed follow-up study of marked individuals and analyzed gonad development on fortnightly collected samples for a population in Tokyo Bay, central Japan.

Shell growth and reproductive cycle of the Mediterranean mussel Mytilus galloprovincialis in Tokyo Bay, Japan

Materials and Methods Study site and follow-up study The intertidal zone along the Nojima Coast, Tokyo Bay (35°1948 N, 139°3753 E), was selected for short- and long-term follow-up studies and periodic sampling of living specimens of the mussel Mytilus galloprovincialis (Fig. 1). From 1 July 2007 to 2 September 2008, about 30 mussels of various sizes were kept in a spherical cage (200 mm in diameter) made of a stainless steel net (2.0 mm mesh) that was set at 80 cm in tidal height where mussels showed a highest individual density (N15–20/1000 cm3). The individual density inside the cage (N7/1000 cm3)was slightly lesser than those at nearby portions. A specimen number was marked on the periostracum surface of each specimen with a waterproof pen and the shell length of each numbered specimen was measured fortnightly using a slide caliper (accuracy, 0.05 mm). During the study period, some individuals died; therefore, new individuals were added to maintain the sample size (N30) for long-term follow-up analysis. Because measurement data for mussels in the cage were obtained at fortnightly intervals throughout the year, they were normalized to enable an analysis of those factors controlling shell growth. According to Winberg (1971), the daily shell length-specific growth rate (Cl) of a given size class can be calculated as Cl(In L2In L1)/(t2t1) , where L1 and L2 are the shell lengths of each size class at times t1 and t2 (in days), respectively. Cl was calculated bimonthly for seven different size classes: 10.0–19.9,

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20.0–29.9, 30.0–39.9, 40.0–49.9, 50.0–59.9, 60–69.9, and 70–79.9 mm in shell length. Analysis of gonad development For the analysis of seasonal changes in gonad development at different ontogenetic stages, 15 mussels of various shell size (20–70 mm in shell length) were collected at fortnightly intervals between 21 April 2007 and 6 April 2008 from a mussel colony at the study site. These live-collected mussels were taken to the laboratory, and the soft tissue was removed from the shell of each mussel, fixed for 12 h with 10 % formic acid solution buffered with pure water, dehydrated through a graded series of ethanol (concentrations of 70, 80, 90, 99.5, and 100%), and then embedded in paraffin (melting point of 58°C). Six-micron-thick transverse sections of each gonad were prepared for each mussel, stained with hematoxylin-eosin, and then observed and photographed under an Olympus VANOX-T AH-2 optical microscope at magnifications of 200–1,000. Sexual maturation was determined based on the spatial ratio of germ cells in follicles for males and the numerical ratio for females. Following the method of Seed (1969) and Goshima et al. (1991), each mussel was assigned to a specific stage of gonad development (i.e., recovery, growing, mature, spawning, or spent). Collection of environmental data For cross-calibration with data on shell growth and gonad development, daily averaged air and surface seawater temperatures, and forthrightly and/or monthly measured salinity and chlorophyll a concentration that were measured during the study period at nearby meteorological stations were utilized. These environmental data were provided from the Kanagawa Agriculture, Forestry and Fisheries Information Center for air temperatures, the Kanagawa Prefectural Fisheries Technical Center for surface seawater temperatures, and the Chiba Prefectural Fisheries Research Center for seawater salinity and chlorophyll a concentration. Results

Fig. 1. Map showing the location of the study site (Nojima Coast; marked by a star symbol), where a population of Mytilus galloprovincialis was studied in Tokyo Bay, central Japan.

Environmental conditions Figure 2A shows 10-day moving averages of air and surface seawater temperatures near the study site. Over the study period, annual air temperature varied from 1°C (February 2008) to 29°C (August 2007 and August 2008), and annual seawater temperature varied from 8°C (January and February of 2008) to 28°C (August 2008). We used monthly seawater salinity data measured at a station located off the Nojima Coast (Fig. 2B). Over the study period, salinity varied from 24 to 34 psu. During the dry period in winter and early spring, salinity was largely invariant (32.5–33.5 psu), but fell to 24–28 psu during the monsoon season in summer and typhoon season in autumn due to an influx of fresh water from nearby rivers. Amounts of Chlorophyll a in seawater were measured at

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Fig. 3. Seasonal variations in the frequency of occurrence of each stage of gonad development for mussels sampled fortnightly from April 2007 to April 2008.

Fig. 2. Environmental data obtained for the study site from April 2007 to September 2008. A. Ten-day moving averages of air temperature and surface seawater temperature. B, C. Monthly measured salinity and chlorophyll a concentration in seawater.

stations located off the Nojima Coast, once or twice a month over the period during April-December 2007 (Fig. 2C). Chlorophyll a concentrations were low (3 m g L1) during late autumn (November–December 2007), and relatively high (5–70 m g L1) in other seasons, with marked monthly fluctuations. High Chlorophyll a concentrations (40–70 m g L1) were observed in August and September of 2007. Reproductive cycle Microscopic observations of gonads mounted on thin sections reveal that in Tokyo Bay, the reproductive cycle of Mytilus galloprovincialis during the study term can be divided into two distinct phases: April to late September in 2007, and October 2007 to April 2008 (Fig. 3). During the first phase, the living population consisted mainly of mussels at the spent stage, with fewer individuals at the mature and spawning stages. Accordingly, during this phase most of the mussels had already spawned their gametes and were

Fig. 4. Growth patterns (shell length data) of marked mussels at the study site between July 2007 and September 2008.

resting from reproductive activity. During the second phase, the living population began gametogenesis simultaneously in October 2007, when approximately 70% of the mussels were at the recovery and growing stages. After November 2007, the proportion of mussels at mature and spawning stages increased to 60–70% and 30%, respectively. Therefore, most of the mussels in the Tokyo Bay population have fully developed gametes and spawn them between late autumn and winter. Age-specific shell growth patterns Figure 4 shows the long-term shell growth patterns of the studied living population of M. galloprovincialis in Tokyo Bay, based on our follow-up study of marked mussels over the period between July 2007 and September 2008. We were unable to recognize growth patterns in the early shell of newly settled spat by the technical difficulty of marking, but growth patterns were identified for three mussels of approximately 18 mm in shell length measured in July 2007, presumably recruited during spring of the same year. These specimens grew to about 40–50 mm in shell length within the first year. For the 2-year-old mussels, yearly rates of


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Fig. 5. Seasonal changes in the mean daily shell-growth rate for each shell-size class of marked mussels from July 2007 to August 2008.

shell growth were about 15 mm, decreasing to 10 mm for 3year-olds. Growth rates showed a rapid decline to about 15 mm as shell length exceeded 50 mm, but growth continued in shells exceeding 70 mm in length. In addition to changes in shell growth rate with age, seasonal variations in growth rate were observed in many individuals. Remarkably high rates of shell growth occurred between June and September; however, even during this summertime period of rapid growth we observed sudden, episodic declines in the growth rates of the marked mussels of different shell-size classes during the middle of July and late August in 2007 and during the middle of August in 2008 (Fig. 5). In other seasons, most of the mussels showed relatively slow rates of shell growth, although they continued growing even during the coldest months of winter (late January to early March). A generalized shell-growth curve for M. galloprovincialis can be drawn by plotting follow-up measurement data for marked-and-recovered mussels. The sigmoidal pattern of shell growth observed in the present species indicates a decrease in growth rate as the shell size approaches its upper limit. This type of growth is appropriately described by Von Bertalanffy, Gompertz, and logistic curves. Since the examined mussels did not secrete clear annual bands in their outer and inner shell portions, we could not calculate a generalized shell growth curve of the marked mussels by plotting mean shell height data versus age (annual increment number from umbo). For this reason, we examined the goodness of fit of measurement data for four randomly sampled mussels (specimen nos. 4, 5, 6, and 23) with sufficient growth records in calculating growth curves on the basis of methods described by previous authors (Bertalanffy 1938, Walford 1946, Yamagishi 1977). For computation,

Fig. 6. Fitting of shell-height data (white rectangles) to von Bertalanffy curves for four selected mussels. L: shell length (mm), K: maximum asymptotic shell length (mm), r: correlation coefficient for Wolford’s linear equation.

the initial shell length at the time of fertilization was fixed at 0.1 mm. The results reveal that the shell growth curve for this species is best fitted by a von Bertalanffy curve (Fig. 6). According to this growth curve, mussels reach 41.9–48.9 mm in shell length at age 1 year, 51.2–63.1 mm at age 2 years, and attain a maximum asymptotic shell length (K in Fig. 6) at age 3 or 4 years. Discussion Reproductive cycle The population of Mytilus galloprovincialis in Tokyo Bay has an extended spawning period from November to March, and develops gonads within 1 year of settlement, when individuals reach 20 mm in shell length. In the Mediterranean (southern France and Adriatic coast of northeast Italy) and the Atlantic coast of northwest Spain, gametogenesis occurs even in 1-year-old mussels, starting during autumn and early winter and followed by ripe and spawning seasons during late spring and summer (Cerccherelli & Rossi 1984, Villalba 1995, Cáceres-Martínez & Figueras 1998, Bodin et al. 2004). Similarly, on the Pacific coast of Baja California in northwest Mexico, the reproductive season occurs from autumn to early spring (CáceresMartínez 2004). In contrast, on the west coast of South

This study

Cerccherelli & Rossi (1984) Abada-Boudjema & Dauvin (1995) Lök et al. (2007) Peharda et al. (2007) Villalba (1995) Cáceres-Martínez & Figueras (1998) Cáceres-Martínez (2004) Schurink & Griffiths (1991)

35–40 mm at age 1

Baja Californian, NW Mexico West coast of South Africa

Tokyo Bay, Japan

3–4 years

1

Winter — — — Late spring–summer Spring Autumn–early spring October–February April–May Nov–Mar 1 1 — — 1 — — —

Spawning season Age of first sexual maturity Life span

3 years 25–28 months 3 years — 3 years — — — 50 mm during the first 14.5 months 16.4–27.7 mm at age 1 46 mm at age 1 39.4 mm during the first 6–8 months 30–40 mm at age 1 — — — Adriatic Sea, Italy Algerian coast Aegean Sea, Turkey Adriatic Sea coast, Croatia Atlantic coast of NW Spain

Environmental controls on annual shell-growth patterns Variations in the annual shell-growth patterns of marine bivalve mollusks are controlled by both exogenous and endogenous factors, including age (e.g., Hall et al. 1974, Berta 1976), tides (House & Farrow 1968, Evans 1972, Ohno 1989), day/night cycles (Clark 1975), temperature (Henderson 1929, Kennish & Olsson 1975), salinity (Davis & Calabrese 1964, Navarro 1988, Marsden &Pilkington 1995), phytoplankton abundance (Ansell 1968, Sato 1997), and biological clock (Rao 1954, Morton 1970, Richardson

Juvenile shell growth rate (shell length)

Age-specific shell growth rate and longevity Zaika (1970) estimated the maximum age of M. galloprovincialis to be 12 years; however, the present study observed high rates of shell growth and short life spans relative to those reported by Zaika (1970). The annual rate of shell growth for mussels in Tokyo Bay is 35–40 mm for individuals at age 1 year, and 15–20 mm for those aged 2 years. The estimated longevity of the population is therefore relatively short, as these mussels may attain a maximum shell size (ca. 70 mm in shell length) at age 3 or 4 years. Similarly, on the Adriatic Sea coast of Italy, the population of M. galloprovincialis consists mainly of 2-yearolds, with rare examples of mussels aged 3 years or older (Cerccherelli & Rossi 1984). These mussels have shell lengths of 39.41.8 mm at age 6–8 months, and 50 mm at age 14.5 months (Cerccherelli & Rossi 1984, Peharda et al. 2007). At other locations, the maximum longevity and annual growth rate of shell length for juveniles are respectively 25–28 months and 16.4–27.7 mm for a population on the Algerian coast (Abada-Boudjema & Dauvin 1995), 3 years and 30–40 mm for a population on the Atlantic coast of northwest Spain (Villalba 1995), and 3 years and 46 mm for a population on the Aegean Sea coast of Turkey (Lök et al. 2007) (Table 1). The age-specific growth rate and longevity of Mytilus species vary according to environmental conditions (Seed & Suchanek 1992). For example, in M. edulis, under optimal conditions mussels can attain lengths of 60–80 mm within 2 years, whereas growth is markedly reduced under the marginal conditions of the high intertidal zone, where mussels require 15–20 years to attain lengths of 20–30 mm (Seed 1976). The available data on shell growth rates and reproductive cycle clearly indicate that the population of M. galloprovincialis in Tokyo Bay has a high rate of annual growth and relatively short life span as in those on the Mediterranean Sea and northeastern Atlantic coasts.

Location

Africa mussels have two protracted spawning seasons, during summer (October–February) and winter (April–May) (Schurink & Griffiths 1991). The above observations indicate that M. galloprovincialis exhibits an early onset of reproduction at age 1 year, although the number, period, and timing of spawning events vary geographically among populations throughout the world (Table 1).

References

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Table 1. Comparison of juvenile shell growth rate, life span, age of first sexual maturity, and spawning season for populations of Mytilus galloprovincialis from different locations.

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1988a, 1988b). The importance of each of these factors varies greatly among different species and among populations of the same species living in different habitats (e.g., Hall et al. 1974). In a study conducted on the Adriatic coast of Croatia, Peharda et al. (2007) reported that cultured mussels (M. galloprovincialis) show the highest growth rates from March to May, when seawater temperatures are relatively low (12– 17°C), and the lowest rates from July to September, when seawater temperatures are highest (22–23°C). The authors suggested that the high growth rate during March–May reflects increased food availability, as this interval coincides with the period of highest primary productivity in the Adriatic Sea. Living mussels of M. galloprovincialis of the present study were subaerially exposed for several hours during each low tide, whereas they were continuously submerged in seawater during neap tide. This observation suggests that both air and seawater temperatures affected the shell growth of living animals. Indeed, high rates of shell growth were observed during April–September in 2007 and 2008, at which times the air and seawater temperatures were 14– 28°C and 15–27°C, respectively (Fig. 2A). However, animals with shell lengths of 20–30 mm showed episodic, marked declines in shell growth rates in September 2007 and August 2008. One explanation of these declines is that a marked reduction in salinity during these intervals led to an abrupt reduction in the rate of shell growth in many individuals. During the interval between November 2007 and March 2008, most animals recorded little shell growth, regardless of shell size. At this time, air and seawater temperatures were 4–12°C and 8–14°C, respectively, chlorophyll a concentrations were low (1–3 m g L1), and most animals developed gonads. These lines of evidence suggest that both environmental factors (i.e., lower air and seawater temperatures and scarce phytoplankton) and physiological ones (i.e. the reproductive effort required for gametogenesis) led to a reduced rate of shell growth in living mussels. Acknowledgements We thank Shin’ichi Sato (Tohoku University Museum) and Shiho Katsuno (University of Tokyo) for their kind advice regarding histological examinations of gonads, and Koji Seike (UT) for his help in the field work, and two anonymous reviewers and the editor Hiroaki Tsutsumi for providing us with critical comments and suggestions to improve this manuscript. We also acknowledge the assistance of staff at the Kanagawa Agriculture, Forestry and Fisheries Information Center and the Chiba Prefectural Fisheries Research Center, who provided environmental data for Tokyo Bay. This work was partly supported by scientific research funding provided by the Japan Society for the Promotion of Science (no. 20340143 in 2008).

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