Does Mya truncata reproduce at its southern distribution limit? Preliminary information.

ABSTRACT Previous investigations of the bivalve Mya truncata in the Southern North Sea revealed the absence of the 1987 to 2001 y classes. Because the species' southern-most distribution limit is the southern North Sea, at the Frisian Front, we examined if M. truncata was reproductively active in this region. Histologic sections of reproductive tissues from individuals collected between June and April 2002 revealed synchronous gametogenesis with low numbers of vitellogenic oocytes. The low number of ripe oocytes may be one explanation for repeated recruitment failures of this species at this site.

KEY WORDS: reproduction, Mya truncata, North Sea benthos 

INTRODUCTION

Monitoring of macrobenthos assemblages in the southern North Sea since 1991 has shown constant species diversity and composition (Holtmann et al. 1999). Exceptions are the large bivalves Arctica islandica and Mya truncata that have recruitment patterns leading to populations composed of only a few year classes (Amaro et al. 2003, Witbaard & Bergman 2003). For example, collections in the area during 2000 to 2001 revealed no individuals <13 y of age (Amaro et al. 2003). Comparisons with populations of these species from other areas indicate this age structure is atypical (e.g., Welch et al. 1992, Witbaard & Bergman 2003). Causes for the infrequent recruitment in both species are unknown and require study if these species are to be protected in the framework of conservation of biodiversity in the North Sea (van Berkel et al. 2002).

In this study we focus on bivalve M. truncata that is a characteristic but relatively rare species in the Oyster Ground (southern North Sea) with maximum densities of 1 ind. per [m.sup.-2] (Amaro et al. 2003). The low densities are in contrast with arctic habitats where M. truncata is frequently a numerically dominant species reaching densities of >100 [m.sup.-2] (Welch et al. 1992).

Causes for recruitment failures of this species in the southern North Sea can he from a combination of factors. For example: (1) lack of reproductively active adults; (2) lack of fertilization success because of low adult abundances (e.g., Levitan & Sewell 1998, Metaxas et al. 2002) or unbalanced sex ratios; (3) temporal/ spatial mismatches in the timing of larval release and food supply (e.g., Cushing 1969); or (4) pre and postsettlement mortality agents (e.g., Strasser & Giinther 2001). In this study, we determined if M. truncata has reproductively viable adults at the Frisian Front and if so the time of the year this takes place.

MATERIAL AND METHODS

Clams, Mya truncata were collected between June 2000 and April 2002 from a single location centered at 53[degrees]48'N, 4[degrees]30'E (Fig. 1). Samples were collected using a Triple-D dredge (Bergman & van Santbrink 1994), and specimens were preserved in buffered sea-water formalin (4%) for transportation to the laboratory where they were transferred to 70% alcohol. Sex ratio and reproductive cycle (gametogenesis and oocyte-size distributions) was determined using standard histologic techniques (RamirezLlodra 2000). The sex of each specimen was determined microscopically. A classification scheme of five different gonadal stages was based on methods of Brousseau (1977, 1987) for M. arenaria. Subsets of females were used to determine oocyte diameters using methods of Ramirez-Llodra (2002). A minimum of 100 oocytes was measured for each specimen to determine size-frequency distributions. Laruelle et al. (1994) have shown that measuring 50-200 oocytes per individual provides minimal statistical error at the intraindividual level. To avoid systemic errors, oocytes that showed processing artefacts were not measured.

[FIGURE 1 OMITTED]

RESULTS

A total of 159 specimens were examined; shell lengths ranged from 47 mm to 78 mm (mean = 63 mm, SD = 6 mm). Microscopic inspection of the histologic sections of all specimens showed the species to be gonochoric with 85 of the specimens being males and 74 females (Table 1). The average sex ratio did not differ from unity ([chi square] = 0.022, df = 1 P > 0.05).

Figure 2 a and b shows the proportions of the males and females with gonads in each of the five developmental stages. In June 2000, all specimens were reproductively inactive (50% males and 67% females were spent whereas remaining males and females were in an indifferent stage). In September 2000, females and males with developing gonads (55% males, 83% females) were present, and in December 2000 fewer specimens had developing gonads (44.4% males, 27.3% females). While samples were not collected in 2001, all specimens were ripening at the beginning of February 2002. By April 2002, 80% of males and 72% of females were in a spawned stage, and the remaining males and females were in an indifferent reproductive stage.

[FIGURE 2 OMITTED]

Size-frequency distributions of the oocytes were constructed to determine the timing of spawning (Fig. 3). In June 2000, most of oocytes were between 10 and 25 [micro]m. Because there was no distinct change in the oocyte size between September and December 2000, spawning likely occurred before June. The oocyte size distribution in February 2002 was different from December 2000 (i.e., more uniform with sizes between 55 and 70 [micro]m). However, there was considerable variation among the individuals (Fig. 3). Only one female had an appreciable proportion (21%) of oocytes >70 [micro]m whereas four females had much lower (~4% to 5%) percentages of oocytes of this size and four females (Fig. 4) had no oocytes larger than 55 [micro]m. In the sample from April 2002 the average oocyte size had dropped considerably, and large oocytes (55-70 [micro]m) were almost absent (1%). Therefore in 2002, spawning events occurred between March to April.

[FIGURES 3-4 OMITTED]

DISCUSSION

Our observations, though based on a limited number of samples, suggest that male and female M. truncta display gametogenic synchrony at the study area. In 2000, all specimens collected in June were reactive or spent. In contrast females and males sampled in September and December were either in a developing stage, suggesting that ripening and further spawning occurred either before June or after December 2000. Gonads of males and females collected in February 2002 were ripening.

There were large female differences in oocyte sizes and percentages of large (>70 [micro]m) oocytes were low in number. While there is no published information on M. truncata oocyte size, in the related intertidal species (M. arenaria) ripe oocytes are 65-70-[micro]m diameter (Brousseau 1987). If these dimensions are similar to M. truncata, 60% (5 out of 9) of the February females had ripe oocytes though in low numbers. Because no samples were collected in March, it is impossible to ascertain whether the low proportion of large oocytes were because gonad ripening was still in progress and/or the production of ripe oocytes is low altogether. However, in April 2002 most specimens of both sexes showed spawning characteristics, indicating gonad ripening was limited to February and spawning to between March and April. If this is true, spawning events at the study were limited to the spring, which coincides with lowest bottom water temperatures and low chlorophyll-a concentrations in surface waters (Boon & Duineveld 1998).

Various studies on the reproductive biology of bivalves have demonstrated that temperature and food are the most important exogenous factors influencing the reproductive cycle (Thorson & Jorgensen 1946, Beer 2000, Sastry 1979, Myint & Tyler 1982). Generally, temperature needs to exceed a threshold value for vitellogenesis to proceed. Temperature also affects the transfer of nutrients needed for oocyte growth (Sastry 1979, Rodriguez-Jaramillo et al. 2001). Long-term winter (January, February) sea-water temperatures have risen in the North Sea between the early 1950s and late 1990s (Beare et al. 2002). Although there is no trend in the sea-water winter temperature measured at the surface in the Oyster Ground (Anonymous 2003), the temperature in the winter months have slightly increased. The low number of ripe oocytes found in our study combined with the possible increase of the temperature could be one explanation for the low number of ripe oocytes in February. Because there are no monthly samples throughout the year, it is not possible to assess definitive reproductive periodicity (Ramirez-Llodra 2002, Tyler & Gage 1984) in this species. According to Petersen (1978), more northerly locations M. truncata seems to spawn most of the year or mainly in the spring. Clearly, additional work is required to more fully understand causes of the repeated recruitment failures of this species at the southern limit of its distribution in the southern North Sea.

TABLE 1.
Numbers of M. truncate collected during the sampling survey.

                           Nr. Of     Nr. Of
         Date             Females      Males

03rd June 2000                2          3
07th September 2000          27         31
12th December 2000           13         18
07th February 2002           17         17
01st April 2002              15         16

ACKNOWLEDGMENTS

The authors thank Dr. Ronald Sluys from Amsterdam University, for offering his histological laboratory and Dr. Eva Ramirez-Llodra, Ana Silva, and Rhian Waller, for all the help and advice during practical work at the SOC. The authors also thank the crew of RV Pelagia and Magda Bergman for their help in collecting M. truncata. This manuscript was substantially improved by constructive criticism from Dr. Robert B. Whitlatch. This study was supported by a grant awarded by Fundacao Para a Ciencia e Tecnologia (FCT) and Fundo Social Europeu (FSE) to Teresa Amaro.

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TERESA AMARO, (1),* GERARD DUINEVELD (1) AND PAUL TYLER (2)

(1) Royal Netherlands Institute for Sea Research P.O. Box 59 1790 AB Den Burg, The Netherlands;

(2) School of Ocean and Earth Science, University of Southampton SOC, Southampton SO14 3ZH, United Kingdom

* Corresponding author. E-mail: [e-mail]; Fax: [phone]