Marine Biology (1995) 121: 665-671 �9 Springer-Verlag 1995

M. Ram6n �9 R Abelld �9 C. A. Richardson

Population structure and growth of Donax trunculus (Bivalvia: Donacidae) in the western Mediterranean

Received: 18 August 1994 / Accepted: 19 October 1994

Abstract A comparison of shell growth in Donax trun- culus (collected between 1988 and 1990 of Cullera, Spain) has been carried out using an analysis of cohort progres- sion in monthly length frequency distributions, hyaline sur- face shell growth rings and internal microgrowth bands. In the Mediterranean there are two periods of recruitment of D. trunculus, one in the summer (July to September) and the other in winter (December to February). Clams re- cruited to the population in winter display a clear cessa- tion in shell growth during the following summer which may possibly be correlated with spawning, whereas indi- viduals of the summer recruited cohort show no growth cessation the following summer and continue to deposit shell during this period. The normally opaque shell of D. trunculus reveals the presence of translucent hyaline growth rings when the shells are backlit by a strong light source, and these have been shown to be laid down in the shell during summer months. Formation of a hyaline ring is accompanied by a narrowing of the microgrowth pat- terns present in shell sections. Both the hyaline rings and the length frequency distributions have been used to deter- mine the age and growth rate of D. trunculus.

Introduction

Donacidae bivalves are some of the dominant organisms capable of inhabiting the high energy environment of ex- posed sandy beaches (Ansell 1983; Brown and McLach- lan 1990), and as a consequence they are capable of reach- ing high densities in some areas. The shape of the shell is

designed for allowing easy penetration into the sediment, and these clams are excellent burrowers and thus ideally adapted to life in the swash zone (Trueman and Ansell 1969; McLachlan and Young 1982).

The bivalve Donax trunculus is a warmwater temper- ate species and is distributed throughout the Mediterranean and the Atlantic from France to Senegal (Bayed and Guil- lou 1985). In the western Mediterranean, D. trunculus oc- curs in the surf zone down to depths of 2 m in the shallow sublittoral, where it is the dominant macrobenthic organ- ism in communities of generally low species diversity and constitutes the target of a specific fishing activity carried out by an artisanal fleet in that area.

Several studies on the growth of Donax trunculus have been conducted, both in the Mediterranean and on the At- lantic coast (Ansell and Bodoy 1979; Guillou and Le Moal 1980; Bayed and Guillou 1985; Maz6 and Laborda 1988; Neuberger-Cywiak et al. 1990). These workers analysed the monthly progression of the mean size of each cohort identified in size frequency distributions and showed that there is a seasonal pattern to shell growth. Attempts were also made to analyse the external growth rings present on the shell surface, although they were found to be difficult to interpret (Ansell 1983). Recent growth studies of bi- valves from the Mediterranean region, eg. Chamelea gal- lina (Ram6n and Richardson 1992), have analysed micro- growth patterns present in acetate peel replicas of shell sec- tions, and this has allowed the relationship between envi- ronmental factors and shell growth to be investigated. The present paper is an analysis of the growth of D. trunculus in the Mediterranean using both length frequency distribu- tions and shell patterns.

Communicated by O. Kinne, Oldendorf/Luhe M, Ramdn ([]) R Abell6 Institut de Cihncies del Mar (C.S.I.C.), Plaga del Mar s/n, 08039 Barcelona, Spain

C. A. Richardson School of Ocean Sciences, University of Wales-Bangor, Menai Bridge, Gwynedd LL59 5EY, UK

Materials and methods

Samples of Donax trunculus were collected subtidally at approxi- mately monthly intervals between May 1988 and April 1990 from a sandy beach off Callera, on the eastern coast of Spain. Samples were collected from a depth of between 0.5 and 2.5 m using a specially

666

designed experimental dredge similar to that used by local fisher- men but incorporating a smaller steel mesh size bag (4.5x4.5 ram). This dredge was used to study the size distribution of the smaller size classes. The anterior-posterior length of each clam was meas- ured to the nearest 0.1 mm with a digital sliding vernier caliper and length-frequency distributions constructed for each monthly sample.

The method of Bhattacharya included in the ELEFAN software package (Gayanilo et al. 1988) was used to identify and separate the different components in the polymodal length-frequency distribu- tions. Once identified, they were attributed to different cohorts of the population.

In order to analyse shell growth of Donax trunculus, microgrowth patterns present within the shell were analysed using the methodol- ogy described by Ram6n and Richardson (1992). Subsamples of ten shells of a range of sizes (17 to 36 mm in length) were taken from each monthly sample and the right shell valve embedded in resin and sectioned from the umbo to the ventral margin along the axis of max- imum growth. Acetate peel replicas of the sectioned, ground, pol- ished and etched surfaces were then prepared (Richardson et al. 1979; Kennish et at. 1980). Acetate peels were examined in a transmitted light-microscope.

On first examination the shells of Donax trunculus did not ap- pear [o have any marked external surface rings. However, a detailed examination of each shell, hacklit by a strong light source, revealed the occurrence of translucent or hyaline rings.

The yon Bertalanffy growth model parameters were estimated from: (1) the size-age keys, obtained from counting the hy aline bands and the assignment of a date of birth, using the program FISHPARM (Saila et al. 1988) which estimates the growth parameters L~, the asymptotic length, K, the yon Bertalanffy growth constant, and t 0, time of recruitment into the population; and from (2) an analysis of the length-frequency distributions using the software package ELE- FAN (Gayanilo et al. 1988), which estimates the growth parameters L~ and K.

Resul ts

Analys i s of l ength- f requency dis t r ibut ions

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Fig. 1 Donax trunculus. Monthly length-frequency distributions from specimens collected between May 1988 and April 1990. Each scale unit on the Y-axis is equivalent to 5% of population

Fig. 1 shows the length- f requency dis t r ibut ions of Donax trunculus f rom the month ly samples col lec ted be tween 35 / May 1988 and Apr i l 1990. The popula t ion showed two pe- r iods of recru i tment each year, one during July to Septem- 30 ber, wi th c lams reaching a size of 9 to 11 ram, and another ~ ] be tween December and February, with a size range of 8.5 ~ 2s ] to t2 ram. The increase in size o f the recrui ted c lams be- ~ z0 tween 1988 and 1990, de te rmined f rom the size progres- sion of each cohort , is shown in Fig. 2. The f igure suggests -~ i s that be tween 1988 and 1990 the growth rate of the winter and summer recrui t ing cohorts was different. Af te r an in- 10 i t ial s low growth rate, c lams which recrui ted to the popu- lat ion dur ing the winter of 1987 and 1988 (W87, W88) dis- s p l ayed a hal t in growth around 20 m m be tween July and October 1988 and 1989, respect ively , fo l lowed by a rapid increase in growth in November . However , those that were recrui ted dur ing the summers of 1988 and 1989 ($88, $89) showed an a lmost constant increase in shell length dur ing both winter and summer. An analysis of the length-fre- quency dis t r ibut ions , therefore, suggests that the popula- t ion contains two or three dis t inct cohorts , depending on the t ime of year when the sample is col lected.

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Fig. 2 Donax trunculus. Patterns of shell growth of five cohorts be- tween May 1988 and April 1990 determined from monthly progres- sion of mean size of each cohort in length frequency distributions. (S summer; W winter recruited cohorts)

667

Fig. 3 Donax trunculus. Photomicrographs of acetate peel replicas of shell sections. A Clearly defined (large arrows) and poorly de- fined (small arrows) growth bands along the outer shell layer. B In- ner shell layer with numerous growth bands (arrowheads). C Umbo region with growth bands (arrows). D Alternating pattern of widely spaced (large arrows) and narrow spaced (small arrows) growth in- crements separated by growth bands. Scale bars=200 btm

Microgrowth patterns in the shell

The shell of Donax trunculus is composed of three layers, an outer composite prismatic layer, a middle crossed la- mellar layer, and an inner homogeneous/complex crossed lamellar layer (Taylor et al. 1973). The clarity and inter- pretation of the microgrowth patterns in acetate peel rep- licas from these species were found to be more complex than in the bivalve Chamelea gallina (Ram6n and Rich- ardson 1992), which inhabits the same beaches although at slightly greater depths than D. trunculus. In some re- gions of the shell ofD. trunculus, microgrowth bands could be clearly distinguished, whilst in others they were hardly discernible (Fig. 3A). Bands were also observed in the in- ner shell layer and in the umbo region (Fig. 3B, and C, re- spectively), although in general they were less conspicu- ous than the bands in the outer layer of the shell.

Examination of acetate peels of shell sections revealed the presence in the outer shell layer of a pattern of widely

spaced growth increments alternating with a group of nar- row increments (Fig. 3D). Separating each increment there is a narrow growth band. In some regions of the shell the bands were so closely spaced that they had a distinctive appearance and were clearly marked with a slight dark colouration which allowed the band to be traced through the inner layer of the shell to the umbo (Fig. 4A and Fig. 3C, respectively). The dark structure in the outer layer (Fig. 4A) was often associated with a change in the direction of shell growth (Fig. 4B) and was usually not associated with an irregularity on the outer shell surface (Fig. 4C). Al- though occassionally a small cleft in the shell surface did coincide with the dark internal growth line (Fig. 4D).

Back lit by a strong light source the shell of Donax trun- cuIus appears all but opaque except for the presence of translucent or hyaline rings (Fig. 5 A-C). When the posi- tion of the hyaline ring was compared with the internal growth patterns, it was observed that the ring coincided with the start of deposition of the internal dark band. The hyaline ring was seen to be formed at the shell margin in the summer (Fig. 5A). During the autumn and winter the distance between the ring and shell edge steadily increased (Fig. 5B, and C). The percentage of shells in monthly sam- ples (June 1989 to June 1990) displaying a hyaline ring at the shell margin is shown in Fig. 6. The highest percent- age of shells with a ring at the edge were found in samples collected between June and August, when the water tem- peratures were at their highest (Fig. 6). Those shells smaller than 15 mm did not display a hyaline ring, whereas

668

Fig. 4 Donax trunculus. Photomicrographs of acetate peel replicas of shell sections. A Detail of thick dark structure in outer layer re- lated to hyaline ring. Annual band can also be followed through mid- dle layer (arrow). B Clearly defined dark structure associated with change in the direction of shell growth (arrow). C Narrowing of the growth increments (arrow) without any obvious cleft in outer shell layer. D Cleft on shell surface (arrow). Scale bars in A=150 Barn; in B=200 gm; in C and D=250 lain

all those larger than 25 mm displayed it (Fig. 7). In view of the annual nature of the hyaline ring, these structures were used to estimate the age of the shells of this bivalve rather than the less easily distinguishable inter- nal microgrowth patterns, which involved the time consuming method of preparing acetate peels of shell sec- tions.

Estimation of growth parameters

The von Bertalanffy growth parameters (K, L~) estimated using data from measurements of the hyaline growth rings and from the length frequency distributions showed simi- lar values (Table 1). These values compare favourably with those obtained in other studies of Donax trunculus from the Atlantic coast of Europe and from the Mediterranean (Table 1).

Discussion and conclusions

Microgrowth bands separated by growth increments of var- iable width were observed in acetate peel replicas of shell sections of Donax trunculus. The interpretation of the pat- terns in these shells was more difficult than those previ- ously observed in other species of subtidal bivalves, such as Mercenaria mercenaria (Richardson and Walker 1991) and Chamelea gallina (Ram6n and Richardson 1992). Both micro- and macroscopic examination of the shells revealed the presence of a prominent hyaline ring which was found to be deposited in the summer between June and August. Hyaline ring formation coincided with the deposition of narrowly spaced growth bands during the summer months when water temperatures were at a maximum of 22 to 27 ~ Ring formation, however, did not occur in clams smaller than 15 mm, whereas those larger than 25 mm all displayed a ring. Spawning in D. trunculus mainly occurs during the summer months whilst the size at first maturation has been established at a size of around 12.5 mm (Ramdn 1993). During the summer the final stages of gonad maturation take place with concomitant spawning, and this potentially physiological demanding process presumably affects shell formation and lead to the deposition of a hyaline ring. The absence of a ring in sexually immature individuals smaller than 15 mm lends support to such an interpretation.

An estimation of the growth rate of Donax trunculus from an analysis of the length-frequency distributions

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Fig. 6 Donax trunculus. Monthly variation in percentage of shells displaying hyaline ring at shell margin and, for comparison, water temperature at time when each sample was collected (June 1989 to June t990)

Fig. 5 Donax trunculus. Position of translucent hyaline rings (ar- tvwheads) on surface of shells of different sizes backlit by a strong light source. A Shells collected in July 1989. B Shells collected in October 1989. C Shells collected in January 1990. Scale bars=l cm

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Fig. 7 Donax truncuIus. Relationship between occurrence of hya- line rings at shell margin and shell size of clams collected between June and August 1990

showed that there were two recruitments o f c lams to the population each year, One cohort was recruited during the winter whi lst the other entered the population during the summer. Although spawning takes place during summer, the season is long enough to show s o m e intraseasonal var- iability in the gametes emiss ion . Then, the summer cohort may c o m e from the first spawns (June-July) , whereas the winter cohort may c o m e from the latest spawns (Au-

gust -September) . The growth rate of those that were re- cruited during the winter s lowed down and stopped the fol- lowing summer, when they had reached a s ize of ca. 20 m m and had spawned. However , c lams that were re- cruited during the summer did not display in the fo l lowing summer the growth cessat ion observed during summer in the winter recruited cohort. The summer recruited c lams did, however , show a small growth cessation in April and

670

Table 1 Donax truncuIus. Es- timates of the von Bertalanffy growth parameters obtained by various authors

Area L~ K t o Source

Mediterranean (Spain) 41.8 a 0.71 -0.354 Mediterranean (Spain) 46.0 b 0.58 --0.416 Atlantic (France) 48.90 b 0.38 0.29 Atlantic (France) 35.55 b,c 0.785 - Atlantic (France) 32.25 b.c 0.678 - Mediterranean (France) 35.99 b 0.956 0.699 Atlantic (Spain) 43.80 b 0.97 0.10 Atlantic (Spain) 52.84 b 0.55 -

Present study Present study Guillou and Le Moal (1980) Ansell and Lagard~re (1980) Ansell and Lagard~re (1980) Bodoy (1982) Fernfindez et al. (1984) Maz6 and Laborda (1988)

a Age estimated from hyaline growth rings b Age estimated from length-frequency distributions c Age estimated from external growth rings

May ($88), June and July ($88) and December and Janu- ary ($89) (Fig. 2) when they had reached a size of 24, 26 and 23 mm, respectively. There undoubtedly is a differ- ence in the pattern of growth of the summer and winter re- cruits during the summer. Since similar patterns of growth were observed during two consecutive years, it is unlikely that sampling error is envolved. The difference may be at- tributed to a difference in the size of the clams and the time of spawning.

The occurrence of a bimodal recruitment in Donax trun- culus appears to be characteristic of the Mediterranean populations (Moueza and Frenkiel-Renault 1973; Bodoy and Mass6 1979; Bayed and Guillou 1985), whereas in the Atlantic populations there is always a single annual recruit- ment (Ansell and Lagard~re 1980; Guillou and Le Moal 1980).

Our observations on shell growth in Donax trunculus from the Mediterranean are different from those obtained for D. trunculus from the Atlantic coast of Europe. Stud- ies carried out by other authors on the seasonality of shell growth in D. trunculus have shown that the period of growth cessation occurs during the winter rather than in the summer months (Ansell and Lagard~re 1980; Guillou and Le Moal 1980; Bayed and Guillou 1985). However, Ansell and Bodoy (1979) suggest that in addition to a de- crease of growth in winter, another one occurs in the sum- mer. The Atlantic populations of D. trunculus occur inter- tidally and are exposed to lower seawater temperatures than the subtidal Mediterranean populations, where water temperatures rarely fall below 12~ The lower water tem- peratures on the Atlantic coast probably cause the shell growth of D. trunculus to slow down to a greater extent than in the Mediterranean.

The present study has revealed the presence of hyaline growth rings on the shell surface of Donax trunculus, and these rings have been used successfully to estimate the age of this bivalve. Traditionally, it had been considered that this species did not form annual growth rings in the Med- iterranean. Therefore, estimates of the growth of D. trun- culus had relied entirely on the interpretation of length-fre- quency distributions (Moueza 1972; Bodoy 1982; Neuber- ger-Cywiak et al. 1990). In view of the difficulties encoun- tered in establishing age-length relationship, von Berta-

lanffy growth parameters have usually only been estimated for the Atlantic populations (Table 1). This work along with the earlier work of Bodoy (1982) is the first attempt to es- timate growth parameters for the Mediterranean popula- tion. Nevertheless, other studies in the Mediterranean have referred to the seasonality of shell growth but have not sought to establish relationships between length and age (Ansell and Bodoy 1979; Bodoy and Mass6 1979). Whilst our estimates of K and L~ fall within the limits of those ob- tained for the Atlantic populations by other authors (Table 1), the value of K determined by Bodoy (1982) is higher and the value of L= is lower than our estimates for the Med- iterranean. The growth rate of Donax trunculus is higher (K=0.6 to 0.7) than that of Chamelea gall ina (K=0.3 to 0.4; Ramdn 1993), another bivalve which inhabits the same beaches. This is not surprising since D. trunculus, which lives in the more unstable environment of the surf zone, has a short life-span (maximum 2 to 3 yr), (Moueza 1972; Bayed and Guillou 1985; Maz6 and Laborda 1988; present results) compared to C. gall ina (3 to 4 yr; Ramdn and Richardson 1992; Ram6n 1993). The longevity of D. trun- culus in the Mediterranean is also shorter than in Atlantic populations which live to about 5 yr (Ansell and Lagard~re 1980; Guillou and Le Moal 1980).

Acknowledgements Our gratitude is expressed to D. J. Lleonart for his encouragement and statistical advice. Financial support was provided by the Generalitat de Valencia.

References

Ansell AD (1983) The biology of the genus Donax. In: McLachlan A, Erasmus T (eds) Sandy beaches as ecosystems. Junk Publish- ers, The Hague, pp 607-635

Ansell AD, Bodoy A (1979) Comparison of events in the seasonal cycle for Donax vittatus and Donax trunculus in European wa- ters. In: Naylor E, Hartnoll RG (eds) Cyclic phenomena in ma- rine plants and animals. Pergamon Press, New York, pp 191-197

Ansell DA, Lagard~re F (1980). Observations on the biology of Do- nax trunculus and Donax vittatus at Ile d'Oleron (French Atlan- tic coast). Mar Biol 57:287-300

Bayed A, Guillou, J (1985) Contribution ~ l'6tude des populations du genre Donax: la population de D. trunculus L. (Mollusca, Bi- valvia) de Mehdia (Maroc). Annls Inst ocdanogr, Paris 61: 139-147

671

Bodoy A (1982) Croissance saisonni~re du bivalve Donax trunculus (L.) en M6diterran6e nord-occidentale (France). Malacologia 22: 353-358

Bodoy A, Masse H. (1979) Quelques parambtres permettant de suiv- re la production organique d' un mollusque bivalve au cours d'un cycle saisonnier. PuNs Cent natn Exploit Oc6ans (CNEXO) (Ser Acres Colloques) 7:753-766

Brown AC, McLachlan A (1990) Ecology of sandy shores. Elsevi- er, Amsterdam

Fernfindez J, Otero J, Coo A (1984) Contribuci6n al estudio de la co- quina (Donax trunculus L.) en Galicia. Actas IV Simp ib6r Es- tud Benthos mar 2:133-142

Gayanilo FC, Soriano M, Pauly D (1988) A draft guide to the com- pleat ELEFAN. ICLARM Software, 2. International Center for Living Aquatic Resources Management, Manila, Philippines

Guillou J, Le Moal Y (1980) Aspects de la dynamique des popula- tions de Donax vittatus et Donax trunculus en baie de Douarne- nez. Annls Inst oc6anogr, Paris 56:55-64

Kennish MJ, Lutz RA, Rhoads DC (1980) Preparation of acetate peels and fractured sections for observation of growth patterns within the bivalve shell. In: Rhoads DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Appendix 1. Plenum Press, New York, pp 597-602

Maz6 RA, Laborda AJ (1988) Aspectos de la dinfimica de poblaci6n de Donax trunculus L. (Bivalvia: Donacidae) en la Rfa de Bar- quero (Lugo, NW. Espafia). Inv Pesq 52:299-312

McLachlan A, Young N (1982) Effects of low temperature on the burrowing rates of four sandy beach molluscs. J exp mar Biol Ec- ol 65:275-284

Moueza M (1972) Contribution ~ l'6tude de la biologie de Donax trunculus L. (Mollusque Lamellibranche) dans L'Alg6rois: la croissance. Pelagos 4:25-35

Moueza M, Frenkiel-Renault L (1973) Contribution fi l'6tude de la biologie de Donax trunculus L: (Mollusques Lamellibranches) dans L'Alg6rois: la reproduction. Cab Biol mar 14(3):261-283

Neuberger-Cywiak L, Achituv Y, Mizrahi L (1990) The ecology of Donax trunculus Linnaeus and Donax semistriatus Poli from the Mediterranean coast of Israel. J exp mar Biol Ecol 134:203-220

Ram6n M (1993) Estudio de las poblaciones de Chamelea gallina (Linnaeus, 1758) y Donax trunculus Linnaeus, 1758 (Mollusca: Bivalvia) en el Golfo de Valencia (Mediterr~neo occidental). Ph.D. Thesis, University of Barcelona, Spain

Ramdn M, Richardson CA (1992) Age determination and shell growth of Chamelea gallina (Bivalvia: Veneridae) in the west- ern Mediterranean. Mar Ecol Prog Ser 89:15-23

Richardson CA, Crisp DJ, Runham NW (1979) Tidally deposited growth bands in the shell of the common cockle Cerastoderma edule (L.). Malacologia 18:277-290

Richardson CA, Walker P (1991) The age structure of a population of the hard-shell clam Mercenaria rnercenaria from Southamp- ton Water, England, derived from acetate peel replicas of shell sections. Int Counc Explor Sea (ICES) mar Sci Symp 48(2): 229-236

Saila SB, Recksieck CW, Prager MH (1988) Basic Fishery Science Programs. A compendium of microcomputer programs and man- ual of operation. Developments in aquaculture and fisheries sci- ence, Vol 18. Elsevier, Amsterdam

Taylor JD, Kennedy WJ, Hall A (1973) The shell structure and min- eralogy of the bivalvia. II. Lucinacea-Clavagellacea conclusions. Bull Br Mus nat Hist (D: Zool.) 22(9):255-294

Trueman ER, Ansell AD (1969) The mechanisms of burrowing into soft substrata by marine animals. Oceanogr mar Biol A Rev 7: 315-366