Growth rate estimation of Hexaplex (Trunculariopsis) trunculus (gastropoda: muricidae) based on mark/recapture experiments in the Ria Formosa lagoon (Algarve coast, southern Portugal).

ABSTRACT This study reports growth rates estimates for Hexaplex (Trunculariopsis) trunculus (Gastropoda: Muricidae) from mark/recapture experiments carried out in the Ria Formosa lagoon (Algarve coast, southern Portugal). A total of 726 specimens (shell length and total weight ranging between 20.65-58.36 mm and 0.86-19.89 g, respectively) were marked with Dymo tape tags and released into a fish culture earth pond. During the marking process, no adverse effects on the whelks' health and behavior or immediate postmarking mortality were detected. Periodical recapture operations were undertaken using a traditional fishing gear designated locally as "wallet-line" and by hand gathering by scuba divers. A total of 170 whelks were caught, with a total of 216 recaptures (shell length and total weight ranging between 36.22-65.97 mm and 4.42-27.35 g, respectively), thus corresponding to a recapture rate of 29.8%. Despite the loss of one tag, all remaining tags were intact and easily readable. Marked individuals presented low monthly growth rates, in terms of shell length (1.0 mm/month or 2.3%/month), shell perimeter (2.0 mm/month or 3.1%/month) and total weight (0.7 g/month or 10.8%/month), which were highly variable between individuals and higher in smaller specimens. Data were used to estimate the von Bertalanffy growth parameters (length and weight) (K= 0.41, [L.sub.[infinity]] = 82.76, [W.sub[infinity]] = 49.97 and [t.sub.0] = 0.05). The growth rate of T. trunculus was compared with results obtained in similar studies with other gastropod species to evaluate its potential for molluscan aquaculture.

KEY WORDS: Hexaplex (Trunculariopsis) trunculus, Gastropoda, Muricidae, mark/recapture, growth rate

INTRODUCTION

Marking methods have been readily applied to several species of gastropods, mainly because of the presence of an external shell on which marks or tags can be attached with little or no adverse effects to the animals (Jones 1979, Gosselin 1993). Such experiments with gastropods have been used in diverse types of studies, to assess movement (Eversole & Anderson 1988, Himmelman 1988), fishing rate (Hancock 1963), field of attraction and effective fishing area of baited traps (Himmelman 1988, McQuinn et al. 1988, Sainte-Marie 1991), species' behavior towards baited traps (Ito et al. 1980), population size and mortality (Hancock 1963) and growth rate (Hancock 1963, Eversole & Anderson 1988).

Various marking techniques have been used in gastropods, such as painting the shell spire with quick drying paints (Hancock & Urquhart 1959, Hancock 1963, Jones 1979, Ito et al. 1980), applying color coded nail polish to the shell (Laxton 1970, Gosselin 1993), attaching rubber bands or nylon lines with tags around the shell (Appeldoorn 1988, Himmelman 1988, McQuinn et al. 1988, Sainte-Marie 1991), gluing a variety of tags to the shell (Hancock & Urquhart 1959, Smith 1987, Eversole & Anderson 1988, Amos & Purcell 2003), scrubbing the shell lip free from the periostracal layer (Hancock & Urquhart 1959, Hancock 1963), drilling and wiring the shell (Laxton 1970, Weil & Laughlin 1984, Kideys & Nash 1993, Kideys 1994), chemically marking the shell and operculum with fluorescent dyes (Kideys & Nash 1993) and using underwater metal detectors to recapture specimens marked with aluminum tags (Crowe et al. 2001).

The muricid gastropod Hexaplex (Trunculariopsis) trunculus (Linnaeus, 1758) is a common inhabitant of the subtidal and intertidal areas of the Ria Formosa lagoon (Algarve coast, southern Portugal), where it is subjected to a locally important artisanal fishery. This activity is traditionally undertaken both by manual harvesting during low tide and with an illegal and artisanal fishing gear known as "wallet-line," but more recently this species has also been caught by scuba divers operating illegally inside the lagoon. Furthermore, because of a growing demand for gastropods in the seafood market, the commercial value of T. trunculus in Portugal has increased markedly in recent years (reaching prices of 10 [euro]--15/kg for first sale), which has been generating high expectations in terms of its potential as a new species for molluscan aquaculture.

Integrated in a general study on the biology, ecology and fishery of T. trunculus in the Ria Formosa lagoon, this work aimed to assess the growth rate of this species by mark/recapture experiments in a fish culture earth pond. To the authors' knowledge, this was the first experiment of this kind ever made with T. trunculus and the first growth data (growth rates and growth parameters) available for this species. Moreover, the information gathered in this study will be most useful for assessing the potential of T. trunculus for molluscan aquaculture, as well as for establishing adequate management measures for this artisanal fishery.

MATERIALS AND METHODS

Mark/Recapture Experiments

Marking experiments were carried out with commercial samples of T. trunculus from the Ria Formosa lagoon (Algarve coast, southern Portugal). Prior to marking, colonizing algae and/ or encrusting organisms (mainly polychaetes) were removed from the shell with a hard brush and a small area of the largest whorl of the shell was carefully smoothed with sandstone and clean dried with absorbent paper. Subsequently, the specimens were tagged with Dymo tape with two alphanumeric characters. The margins of these tags were cut with scissors, ensuring a tag of [approximately equal to] 6 x 4 mm size and facilitating adherence to the rounded and irregular surface of the gastropod shell. The tags were fixed with cyanoacrylate glue and covered with epoxy glue (Fig. 1A), to diminish abrasion of the tag caused by the burrowing movements of the whelks into the sediment and the settlement of encrusting organisms over the tags, which could jeopardize mark retention and readability. The tags were generally fixed between the two most recently deposited growth bands of the last whorl of the shell (Fig. 1A), to prevent eventual dropping of excessive glue from the shell onto the soft body of the gastropods. Finally, after allowing the glue to dry for approximately half hour, marked individuals were rinsed in seawater to avoid potential contamination problems provoked by glue residues, and maintained overnight in an aquarium with running seawater, where they were examined for general condition (comparison of behavior between marked and unmarked specimens).

[FIGURE 1 OMITTED]

Mark/recapture experiments were undertaken in a fish culture earth pond of the Olhao fish culture experimental station, which was previously limited by a plastic net fence (area [approximately equal to] 100 [m.sup.2]; maximum depth [approximately equal to] 2 m). This earth pond receives water directly from the adjacent Ria Formosa lagoon and closely resembles the surrounding natural environment in terms of sediment type, water quality and food availability. Seawater temperature and dissolved oxygen in the earth pond were monitored daily with a multi parameter monitor (Yellow Springs Incorporated, YSI 6820). Periodic recaptures were undertaken monthly, using a traditional fishing gear designated locally as "wallet-line" baited with cockles (Cerastoderma edule) and by hand gathering by scuba divers (whenever water visibility allowed for diving recapture operations).

During the marking process and immediately after the recapture operations, specimens were measured for shell length (SL-mm) (Fig. 1B) with a digital calliper (MITUTOYO Digimatic: CD-15D; precision = 0.01 mm), shell perimeter (SP-mm) of the last whorl of the shell (Fig. 1B) and weighed for total weight (TW-g) on a top loading digital balance (AND: HF-2000 G; precision = 0.01 g). Particular care was taken to drain as much water as possible from the mantle cavity before weighing. On both occasions, the position of the tag on the gastropod shell was also registered to verify the degree of shell deposition (tag position at recapture versus tag position at marking) (Fig. 1C).

Estimation of Growth Rates

Monthly growth rates in terms of unit/month and percentage/ month (mm and %SL/month, mm and %SP/month, g and %TW/ month, no. and %growth bands/month) were estimated with the following equations:

GR = ([S.sub.r] - [S.sub.m]) / ([t.sub.r] - [t.sub.m]) x 30 and %GR = GR / [S.sub.m] x 100

where: GR is the monthly growth rate (unit/month); %GR is the monthly growth rate (%/month); [S.sub.r] is the size at recapture (SL-mm, SP-mm, TW-g or tag position); [S.sub.m] is the size at marking (SL-mm, SP-mm; TW-g or tag position); [t.sub.r] is the day of recapture; and [t.sub.m] is the day of marking.

In the case of multiple recaptures, the size increment used (length, perimeter, weight and tag position) was derived from initial size and last recapture.

The relationships between the individuals' size (shell length at marking process, grouped in 5 mm SL classes) and the respective monthly growth rates (unit/month and percentage/month) were assessed by regression analysis (least squares method) and the degrees of association between variables were estimated by the correlation coefficient (r).

Estimation of Growth Parameters

Whenever the period at liberty (interval between marking and recapture) is small, growth rates may be related to the mean length between marking and recapture ([S.sub.m] + [S.sub.r]/2), using the Gulland-Holt plot (Gulland & Holt 1959). Because the present mark/recapture data lacked small individuals (<20 mm SL), data on growth rates of individuals hatched at the end of June 2004 in the Tavira molluscan aquaculture experimental station were pooled with data on growth rates obtained in mark/recapture experiments. Data were converted into weekly growth rates to increase the number of points in the plot and thus enhance the accuracy of this graphical method. Additionally, recaptured individuals that did not grow during the study period were removed from this estimation of growth parameters.

Growth parameters (K and [L.sub.[infinity]]) were estimated from the Gulland-Holt plot by the following relations (Gulland & Holt 1959):

K = -b and [L.sub.[infinity]] = -a / b

where: K is the growth coefficient; [L.sub.[infinity]] is the asymptotic shell length (SL-mm); a is the linear regression intercept on the Y-axis; and b is the linear regression slope.

The theoretical age at shell length zero ([t.sub.0]) cannot be obtained from mark/recapture data alone (without specific size-at-age information). For the present purposes to was assumed to correspond to the shell length of T. trunculus at hatching ([L.sub.t] = 1.64 [+ or -] 0.22 mm SL, n = 100) (Vasconcelos et al. 2004a) and was calculated from the following expression (von Bertalanffy 1938):

[t.sub.0] = t + 1 / K ln ([L.sub.[infinity]] - [L.sub.i]) / [L.sub.[infinity]]

Subsequently, shell growth of T. trunculus was modeled by applying all these growth parameters (K, [L.sub.[infinity]] and [t.sub.0]) in the von Bertalanffy growth in length function, expressed by the following equation (von Bertalanffy 1938):

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII.]

where: [L.sub.t] is the shell length at age t (SL-mm); [L.sub.[infinity]] is the maximum asymptotic shell length (SL-mm); K is the von Bertalanffy growth coefficient; and to is the theoretical age at shell length zero (years).

After applying the value estimated for maximum asymptotic shell length ([L.sub.[infinity]]) in the weight/length relationship (TW = a x S[L.sup.b]) for this species, the maximum asymptotic total weight ([W.sub.[infinity]]) was obtained. Finally, growth in total weight of T. trunculus was modeled by the von Bertalanffy growth in weight function, by using the following expression (von Bertalanffy 1938):

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII.]

where: [W.sub.t] is the total weight at age t (TW-g); [W.sub.[infinity]] is the maximum asymptotic total weight (TW-g); K is the von Bertalanffy growth coefficient; [t.sub.0] is the theoretical age at total weight zero (years); and n is the slope (b) of the weight/length relationship (TW = a x S[L.sup.h]).

RESULTS

Mark/Recapture Experiments

A total of 726 whelks were marked and released between March 2003 and June 2004. These marked specimens had an average shell length of 44.32 [+ or -] 5.34 mm and average total weight of 8.94 [+ or -] 3.06 g (ranges 20.65-58.36 mm and 0.86-19.89 g, respectively). A careful inspection of the condition of marked individuals held in the aquarium did not reveal any adverse effects on the gastropods health and behavior or immediate postmarking mortality.

Daily monitoring of temperature and dissolved [O.sub.2] in the earth pond (Fig. 2) showed that the average temperature was relatively high (20.7 [+ or -] 4.9[degrees]C), varying between a minimum of 11.0[degrees]C in December 2003 and a maximum of 29.4[degrees]C in August 2003. The average dissolved [O.sub.2] was 7.2 [+ or -] 1.1 mg/L, showing an opposite trend relative to water temperature, with a maximum in May 2004 (11.4 mg/L) and an unexpected minimum in February 2004 (4.2 mg/L).

[FIGURE 2 OMITTED]

In the mark/recapture study, 170 whelks were caught (216 recaptures) with an average shell length of 49.36 [+ or -] 4.92 mm and average total weight of 11.89 [+ or -] 4.08 g (ranges 36.22-65.97 mm and 4.42-27.35 g, respectively). Overall, these 216 recaptures corresponded to a recapture rate of 29.8%. In this context, it is worth emphasizing that most recaptures were caught only once (133 individuals = 78.2%), 30 whelks were recaptured twice (17.7%), six were caught three times (3.5%), and one was recaptured four times (0.6%). In all, 107 dead whelks were recovered from the earth pond during diving operations, corresponding to a mortality rate of 14.7%. After 16 mo from the beginning of the study, only one specimen was recaptured without a tag. All other recaptured specimens had their tags intact and easily readable, most of them presenting recently deposited growth bands (Fig. 1D).

Estimation of Growth Rates

The recaptured whelks presented average monthly growth rates of 1.0 [+ or -] 1.0 mm SL (2.3 [+ or -] 2.6% SL/month), 2.0 [+ or -] 1.6 mm SP (3.1 [+ or -] 2.8% SP/month) and 0.7 [+ or -] 0.6 g TW (10.8 [+ or -] 11.3% TW/month). However, growth rates were highly variable among individuals, with some whelks simply not growing (in terms of shell length, shell perimeter and/or total weight), whereas the fastest growing specimens exhibited much higher growth rates i.e., 4.0 mm SL/ month (13.4% SL/month), 7.4 mm SP/month (15.7% SP/month) or 3.4 g TW/month (59.0% TW/month) (Table 1).

Individually, growth rates varied with size (initial shell length), being highly variable between individuals, and generally higher in smaller than in larger individuals. In fact, individual monthly. growth rates displayed a decreasing trend during ontogeny, a phenomenon that was more evident in the relationships between growth in shell length, shell perimeter and shell deposition as a function of shell length (Figs. 3A, B, C, D, G, H), than in the relationships between growth in total weight in function of shell length (Figs. 3E, F).

[FIGURE 3 OMITTED]

Because of the high interindividual variability observed in monthly growth rates, individual data were grouped in size classes (5 mm SL) and subjected to regression analyses (Fig. 4). After pooling data into size classes, the inverse relationship between size (shell length at marking) and growth rates became even more evident, further strengthening the decreasing trend in growth during ontogeny. This was particularly evident in the relationships SL/month in function of shell length (Figs. 4A, B) and SP/month in function of shell length (Figs. 4C, D), whereas the relationships TW/month in function of shell length (Figs. 4E, F) presented poorer fittings. Furthermore, the relationships established between shell deposition rate (growth bands/month) and shell length (Figs. 4G, H) perfectly illustrate the remarkable decline in shell deposition with specimen size (i.e., during growth), reflected by the high correlation coefficients (r) registered in these regressions.

[FIGURE 4 OMITTED]

Estimation of Growth Parameters

The Gulland-Holt plot of weekly growth rate versus mean shell length (with pooled data from mark/recaptured gastropods and from laboratory hatched gastropods) is illustrated in Figure 5A. After applying this graphical method, the estimated growth parameters were K = 0.008/wk (0.41/y) and [L.sub.[infinity]] = 82.76 mm SL. The calculation of [t.sub.0], assuming the shell length of T. trunculus at hatching of [L.sub.t] = 1.64 mm SL, produced a value of -0.05 y. The von Bertalanffy growth function for T. trunculus in terms of shell length ([L.sub.t] = 82.7611 - [e.sup.-0.41(t+005)]]) is presented in Figure 5B.

[FIGURE 5 OMITTED]

After employing the weight-length relationship (TW = 0.00008S[L.sup.3.022]; n = 2401; r = 0.975; P < 0.05) estimated by Vasconcelos et al. (2004b) for T. trunculus from the Ria Formosa lagoon (Fig. 5C), the von Bertalanffy growth function for this species in terms of total weight (W, = 49.9711 - [[e.sup.-0.41(t+005)]].sup.3.022]) was obtained (Fig. 5D).

DISCUSSION

Mark/Recapture Experiments

Marked gastropods are frequently disturbed and stressed by tagging procedures (Himmelman 1988) that may result in quite different behavior from undisturbed specimens (Sainte-Marie 1991), often exhibiting a period of stress-induced inactivity during release after extended tagging manipulations (McQuinn et al. 1988). In this study, the marking process had no detectable adverse effects on the marked whelks' health and behavior. When returned to the aquarium, marked whelks soon started crawling (within a maximum of 5-10 min), and no behavioral differences were apparent between marked and unmarked individuals. This was probably because T. trunculus quickly withdraws into the shell when removed from seawater, preserving most of the inner moisture.

The recapture rate obtained during these experiments (29.8%) was low, considering that specimens were released inside a fenced area on an earth pond, virtually without potential predators. In this case, the high proportion of uncaught individuals might have been because of the type of bottom in the earth pond (muddy sediment), which favored the burrowing movements of T. trunculus and decreased underwater visibility during recapture operations by hand gathering by scuba divers.

An unexpectedly high mortality rate was registered (14.7%). Besides natural mortality, this might have been caused by other circumstances, namely a possible weakness and fragility of some marked individuals. Indeed, the fact that specimens were obtained from commercial samples meant that neither date of capture nor the conditions under which captured whelks were held were known. Additionally, despite water temperature in the earth pond closely reflecting the environmental conditions in the adjacent Ria Formosa lagoon, dissolved oxygen was low during some periods and might have also contributed to the mortality of marked specimens.

However, this high mortality rate is probably slightly underestimated, because dead individuals could only be recovered from the earth pond bottom by diving, frequently in poor visibility. Moreover, the burrowing behavior of T. trunculus, coupled with the high sedimentation rate inside the earth pond, might have also made difficult the detection of all dead specimens, thus probably contributing to an underestimation of total mortality rate.

Estimation of Growth Rates

The monthly growth rates estimated in this study, in terms of shell length (1.0 mm/month or 2.3%/month), shell perimeter (2.0 mm/month or 3.1%/month) and total weight (0.7 g/month or 10.8%/month) were considered somewhat low, taking into consideration that T. trunculus is supposed to be a species with a short/ medium life-span. Nevertheless, this growth rate is common among muricid species, because according to Spight et al. (1974) a typical young muricid grows only 1-2 mm/month. As expected, monthly growth rates decreased markedly during ontogeny, with smaller specimens growing more rapidly than larger ones. This was particularly evident in growth in terms of shell length, shell perimeter and shell deposition rates, but less noticeable in terms of total weight growth rate. This phenomenon was probably influenced by the seasonal fluctuations in physiological condition and total weight normally associated with the reproductive cycle of the species, being accentuated by the fact that it was virtually impossible to assure the complete removal of water from the shells, thus contributing to some variability in weighing both at marking and recapture operations.

Moreover, monthly growth rates were highly variable among individuals and some whelks did not grow between marking and recapture. The same high interindividual variability in growth rates has been noted in several gastropod species and has been attributed to diverse factors (e.g., Tallmark 1980, Smith 1987 and references therein). In fact, most muricid adults simply do not grow (Spight et al. 1974), and in some experiments with different species, larger specimens (presumably adults) did not grow at all during the study period, after becoming reproductively active, even though they were substantially smaller than their maximum shell length (e.g., Hancock 1959, Laxton 1970, Fotheringham 1971, Spight et al. 1974, Tallmark 1980, Appeldoorn 1988). However, in the present case, despite reduction or even cessation of growth in shell length, T. trunculus continued slowly growing in shell perimeter, total weight and shell deposition, with monthly growth rates that were invariably higher than shell length growth rates.

However, these growth estimates are most likely underestimated, because despite the inclusion of some juveniles in the experiments, marked and recaptured gastropods were dominated by adult specimens (consequently with a much lower growth rate), which obviously induced a significant underestimation of the overall growth rate of the species. Furthermore, notwithstanding the use of a non size-selective fishing gear in the recapture operations, the samples caught through snorkeling and scuba diving could be size-biased, because bigger whelks were more conspicuous and more easily detected than smaller individuals, especially in a burrowing species and under low water visibility conditions. In addition, many animals were recaptured less than 1 year after being marked and during winter and spring, when lower water temperatures and less food availability in the earth-pond might have slowed their metabolism and decreased growth rates. For all these reasons, the present growth rates of T. trunculus should be interpreted with some caution and considered as average values for the size range used in this study (dominated by adults). Extrapolation of the data to juveniles is especially problematic. T. trunculus individuals hatched at the end of June 2004 and maintained until now in the Tavira molluscan aquaculture experimental station presented a much higher growth rate, hatching with 1.64 [+ or -] 0.22 mm SL and reaching 11.66 [+ or -] 2.05 mm SL after 4 mo (end of October 2004), therefore corresponding to a monthly growth rate of 2.5 mm SL/month during the first 4 mo of life (Vasconcelos et al. 2004a).

The comparison of the growth rates of T. trunculus obtained in this study with those obtained for other gastropod species (namely some muricids with high commercial value) was difficult, because most studies had different objectives, different experimental designs (e.g., field vs. laboratory, with vs. without additional food supply) and variable size ranges of the individuals used for growth rate estimations (e.g., juveniles vs. adults) (Table 2). The average monthly growth rate of T. trunculus (1.0 mm/month) compared favorably with those obtained for Ocenebra lurida, Urosalpinx cinerea, Busycon carica and Turbo sarmaticus, being equal to other growth rates estimated for B. carica, Busycon canaliculatum and Ocenebra interfossa. In contrast, the present growth rate was lower than those obtained for B. carica, Ceratostoma foliatum and Cerithium nodulosum and much lower than the growth rates of Ocenebra lumaria, Eupleura caudata, Bolinus brandaris, Concholepas concholepas, Chicoreus virgineus, Strombus gigas and Chicoreus ramosus. In this context, it is worth emphasizing that most of these studies used newly hatched specimens or small juveniles during growth studies, thus growth rates are presumably overestimated considering the overall size ranges (juveniles + adults) of the natural populations of these species. Moreover, some of these species have a maximum size much bigger than T. trunculus. Comparisons of growth rates (mm SL/month) between gastropod species are complicated and should be carefully interpreted.

Estimation of Growth Parameters

The von Bertalanffy growth function in terms of shell length estimated for T. trunculus ([L.sub.t] = 82.76[1-[e.sup.-0.41(t+0.05)]]) further confirmed that the growth of this gastropod species is relatively slow (K = 0.41). According to these data the minimum landing size of T. trunculus (MLS = 50 mm SL) is only attained at 2.20 y old. Furthermore, at 95% of its theoretical maximum shell length (95% [L.sub.[infinity]] = 82.76 mm), the von Bertalanffy growth equation yielded an estimated age of 7.24 y for T. trunculus, which can be considered a relatively short/medium life span for a gastropod species.

The estimated maximum asymptotic shell length ([L.sub.[infinity]] = 82.76 mm) closely approached the maximum size attained locally by T. trunculus. During a general study on the biology, ecology and fishery of this species in the Ria Formosa lagoon, the largest specimen sampled measured 82.84 mm. Nevertheless, specimens of this size were exceptional, because among 2484 T. trunculus measured during a 1-y sampling program, only one individual was bigger than the asymptotic shell length estimated in this study ([L.sub.[infinity]] = 82.76 mm), which was very similar to the maximum size attained by this species in the Ria Formosa lagoon (85 mm SL) (Muzavor & Morenito 1999) and included in the maximum size range reported for T. trunculus by other authors, between 80 mm SL (Poppe & Goto 1991) and 90 mm SL (Macedo et al. 1999).

The von Bertalanffy growth function in terms of total weight estimated for T. trunculus ([W.sub.t] = 49.97[[1-[e.sup.0.41(t+005)].sup.3.022]) indicated that at 2.20 y old (age corresponding to the minimum landing size of T. trunculus - MLS = 50 mm SL) specimens achieved 10.86 g in total weight. The estimated maximum asymptotic total weight ([W.sub.[infinity]] = 49.97 g) was lower than the maximum total weight registered in samples from the Ria Formosa lagoon (58.20 g), but yet again this was an exceptionally heavy individual, because amongst 2401 T. trunculus weighed during a 1-y sampling program, only one specimen was heavier than the asymptotic total weight estimated in the present study ([W.sub.[infinity]] = 49.97 g).

Therefore, and although the von Bertalanffy growth model has been criticized for not adequately representing growth of the entire size range of organisms, in the present case both size (shell length) and weight (total weight) data fitted the growth model satisfactorily.

Aquaculture and Fisheries Considerations

Despite being slightly low and underestimated because of the dominance of adult specimens in the samples, the growth rate estimated through mark/recapture experiments for T. trunculus (1.0 mm/month) may still create some expectations in terms of the potential of this species for molluscan aquaculture, considering that laboratory hatched specimens grow at a much higher rate (2.5 mm/month during the first 4 mo of life) and that the von Bertalanffy growth function indicated an age of 2.20 y to attain the minimum landing size for this species (50 mm SL i.e., 10.86 g TW).

Because environmental and feeding requirements of T. trunculus are not demanding, the culture of this gastropod species could become profitable in the near future, when the crucial phases of the species reproductive cycle (spawning and posthatching development) are better known. Moreover, because of an increasing demand for gastropods in the seafood market, the commercial value of T. trunculus has been continuously rising (reaching values of 10-15 [euro]/kg for first sale) and its abundance in the Ria Formosa lagoon apparently has been decreasing over the last years, probably caused by illegal fishing and consequent overexploitation of the resource.

ACKNOWLEDGMENTS

The authors thank Pedro Pousao-Ferreira for allowing these mark/recapture experiments in an earth pond of the Olhao Fish Culture Pilot Station, as well as their collaborators for monitoring the seawater parameters; Joao Tata-Regala for his help in fencing the earth pond; Susana Carvalho, Rita Constantino and Joao Curdia for their assistance during the recapture operations and Dr. Scoresby Shepherd and Dr. Fred E. Wells, whose suggestions greatly improved the manuscript. This study was partially funded by a PhD grant from the Fundacao para a Ciencia e Tecnologia (FCT: SFRH/BD/5139/2001) and by the DIVERAQUA Project (Interreg IIIA).

LITERATURE CITED

Amos, M. J. & S. W. Purcell. 2003. Evaluation of strategies for intermediate culture of Trochus niloticus (Gastropoda) in sea cages for restocking. Aquaculture 218:235-249.

Appeldoorn, R. S. 1988. Age determination, growth, mortality and age of first reproduction in adult queen conch, Strombus gigas L., off Puerto Rico. Fish. Res. 6:363-378.

Bech, M. 1992. Sediment preference, hiding behaviour and growth rate: Paws in the game of survival of juvenile Chicoreus ramosus (Linnaeus, 1758). Phuket Mar. Biol. Cent. Spec. Publ. 11:79-82.

Crowe, T. P., G. Dobson & C. L. Lee. 2001. A novel method for tagging and recapturing animals in complex habitats and its use in research into stock assessment of Trochus niloticus. Aquaculture 194:383-391.

Eversole, A. G. & W. D. Anderson. 1988. Growth and movement of offshore populations of Busycon carica and B. canaliculatum evidenced by mark and recapture results. J. Shellfish Res. 7:157.

Foster, G. G., A. N. Hodgson & M. Balarin. 1999. Effect of diet on growth rate and reproductive fitness of Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Mar. Biol. 134:307-315.

Fotheringham, N. 1971. Life history patterns of the littoral gastropods Shaskyus festivus (Hinds) and Ocenebra poulsoni Carpenter (Prosobranchia: Muricidae). Ecology 52:742-757.

Gosselin, L. A. 1993. A method for marking small juvenile gastropods. J. Mar. Biol. Assoc. U.K. 73:963-966.

Gulland, J. A. & S. J. Holt. 1959. Estimation of growth parameters for data at unequal time intervals. J. Cons. Int. Explor. Mer. 25:47-49.

Hancock, D. A. 1959. The biology and control of the American whelk tingle Urosalpinx cinerea (Say) on English oyster beds. Fish. Invest. Lond. 22:1-66.

Hancock. D. A. 1963. Marking experiments with the commercial whelk (Buccinum undatum). Spec. Publ. Int. Comm. Northwest Atl. Fish. (ICNAF) 4:176-193.

Hancock, D. A. & A. E. Urquhart. 1959. Methods for marking whelks (Buccinum undatum L.). J. Cons. Int. Expl. Mer. 24:494-496.

Himmelman, J. H. 1988. Movement of whelks (Buccinum undatum) towards a baited trap. Mar. Biol. 97:521-531.

Ito, H., T. Wakui & Y. Dimon. 1980. Methods for marking sea snails, Genus Buccinum. Bull. Hokkaido Reg. Fish. Res. Lab. 45:65-74.

Jones, R. 1979. Materials and methods used in marking experiments in fishery research. FAO Fish. Tech. Paper 190, Rome: FAO. 134 pp.

Kideys, A. E. 1994. Effect of tagging on the growth of the neogastropod, Buccinum undatum in the laboratory. Fish. Res. 20:283-289.

Kideys, A. E. & R. D. M. Nash. 1993. A note on the mortality associated with fluorescent marking in a gastropod. DOGA Turk. J. Zool. 17: 175-178.

Kraeuter, J. N., M. Castagna & R. Bisker. 1989. Growth rate estimates for Busycon carica (Gmelin, 1971) in Virginia. J. Shellfish Res. 8: 219-225.

Lara, E. & E. Montes. 1988. Estado del conocimiento en el cultivo del loco Concholepas concholepas. Inv. Pesq. (Chile) 35:103-107.

Laxton, J. H. 1970. Shell growth in some New Zealand Cymatiidae (Gastropoda: Prosobranchia). J. Exp. Mar. Biol. Ecol. 4:250-260.

Luckens, P. A. 1970. Predation and intertidal zonation at Asamushi. Bull. Biol. Stn. Asamushi 14:33-52.

Macedo, M. C. C., M. I. C. Macedo & J. P. Borges. 1999. Conchas Marinhas de Portugal (Seashells of Portugal). Lisboa, Portugal: Editorial Verho. 516 pp.

MacKenzie, C. L. 1961. Growth and reproduction of the oyster drill Eupleura caudata in the York River, Virginia. Ecology 42:317-338.

Magalhfies, H. 1948. An ecological study of snails of the Genus Busycon at Beaufort, North Carolina. Ecol. Monogr. 18:379-409.

McQuinn, I. H., L. Gendron & J. H. Himmelman. 1988. Area of attraction and effective area fished by a whelk (Buccinum undatum) trap under variable conditions. Can. J. Fish. Aquat. Sci. 45:2054-2060.

Muzavor, S. & P. M. Morenito. 1999. Roteiro Ecologico da Ria Formosa. Vol. IV--Moluscos Gastr6podos. Faro, Portugal: Universidade do Algarve. 85 pp.

Poppe, G. T. & Y. Goto. 1991. European Seashells. Vol. I (Polyplacophora, Claudofoveata, Solenogastra, Gastropoda). Wiesbaden, Germany: Verlag Christa Hemmen. 352 pp.

Ramesh, M. X., C. Raghunuthan & K. Ayyakkannu. 1992. Laboratory observations on food consumption and growth of Chicoreus virgineus--A pilot study. Phuket Mar. Biol. Cent. Spec. Publ. 11:94-95.

Ramon, M. & R. Flos. 2001. First trials to cultivate the muricid gastropod Bolinus brandaris (Linnaeus). Eur. Aquac. Soc. Spec. Publ. 29: 219-220.

Sainte-Marie, B. 1991. Whelk (Buccinum undatum) movement and its implications for the use of tag-recapture methods for the determination of baited trap fishing parameters. Can. J. Fish. Aquat. Sci. 48:751-756.

Smith, B. D. 1987. Growth rate, distribution and abundance of the introduced topshell Trochus niloticus Linnaeus on Guam, Mariana Islands. Bull. Mar. Sci. 41:466-474.

Spight, T. M., C. Birkeland & A. Lyons. 1974. Life histories of large and small murexes (Prosobranchia: Muricidae). Mar. Biol. 24:229-242.

Tallmark, B. 1980. Population dynamics of Nassarius reticulatus (Gastropoda, Prosobranchia) in Gullmar Fjord, Sweden. Mar. Ecol. Prog. Ser. 3:51-62.

Vasconcelos, P., M. B. Gaspar, S. Joaquim, D. Matias & M. Castro. 2004a. Spawning of Hexaplex (Trunculariopsis) trunculus (Gastropoda: Muricidae) in the laboratory: description of spawning behaviour, egg masses, embryonic development, hatchling and juvenile growth rates. Invertebr. Reprod. Dev. 46:125-138.

Vasconcelos, P., M. B. Gaspar & M. Castro. 2004b. Morphometric relationships of the shell of Murex trunculus (Gastropoda: Muricidae) from the Ria Formosa lagoon (Algarve, southern Portugal). In: Proceedings of the XIII Simposio Iberico de Estudios del Bentos Marino, Las Palmas de Gran Canaria, 2004. pp. 97-98.

Von Bertalanffy, L. 1938. A quantitative theory of organic growth. Hum. Biol. 10:181-213.

Weil, E. & R. Laughlin. 1984. Biology, population dynamics, and reproduction of the queen conch Strombus gigas Linne in the Archipielago de los Roques National Park. J. Shellfish Res. 4:45-62.

Yamaguchi, M. 1977. Shell growth and mortality rates in the coral reef gastropod Cerithium nodulosum in Pago Bay, Guam, Mariana Islands. Mar. Biol. 44:249-263.

PAULO VASCONCELOS, (1) * MIGUEL B. GASPAR, (1) ALEXANDRE M. PEREIRA (1) AND MARGARIDA CASTRO (2)

(1) Instituto Nacional de Investigacao Agraria e das Pescas (INIAP/IPIMAR), Centro Regional de Investigacao Pesqueira do Sul (CRIPSul), Avenida 5 de Outubro s/n, P-8700-305 Olhao, Portugal; (2) Centro de Ciencias do Mar (CCMAR), Universidade do Algarve (UAlg), P-8005-139 Faro, Portugal

* Corresponding author. E-mail: [e-mail]

TABLE 1.

Monthly growth rates (shell length, shell perimeter and total weight)
of the Hexaplex (Trunculariopsis) trunculus specimens recaptured in
the earth pond.

Monthly Growth Rate            Shell Length (SL-nm)

      (N=216)              mm/month             %/month

Mean [+ or -] SD       1.0 [+ or -] 1.0     2.3 [+ or -] 2.6
(Min.-Max.)               (0.0-4.0)            (0.0-13.4)

Monthly Growth Rate           Shell Perimeter (SP-mm)

      (N=216)              mm/month             %/month

Mean [+ or -] SD       2.0 [+ or -] 1.6     3.1 [+ or -] 2.8
(Min.-Max.)               (0.0-7.4)            (0.0-15.7)

Monthly Growth Rate            Total Weight (TW-g)

      (N=216)              g/month               %month

Mean [+ or -] SD       0.7 [+ or -] 0.6    10.8 [+ or -] 11.3
(Min.-Max.)               (0.0-3.4)            (0.0-59.0)

TABLE 2.

Comparison of the growth rate of Hexaplex (Trunculariopsis) trunculus
obtained through mark/recapture experiments with growth rates
reported for other gastropod species.

       Species                  Location           Size range (SL-mm)

Hexaplex trunculus      Ria Formosa, Portugal     20-58 mm
Ocenebra lurida         Washington, U.S.A.        12-22 mm
Busycon canaliculatum   South Carolina, U.S.A.             --
Busycon carica          South Carolina, U.S.A.             --
Ocenebra interfossa     Washington, U.S.A.        12-21 mm
Ceratostoma foliatum    Washington, U.S.A.        juveniles
Cerithium nodulosum     Guam, Mariana Islands     25-75 mm (juveniles)
Ocenebra lumaria        Asamushi, Japan                    --
Eupleura caudata        Virginia, U.S.A.                   --
Bolinus brandaris       Catalonia, Spain          >5 mm (juveniles)
Concholepas concholep   Chile                     juveniles
Chicoreus virgineus     Cuddalore, India          70-85 mm
Strombus gigas          Los Roque, Venezuela      30-190 mm
Chicoreus ramosus       Phuket, Thailand          25-45 mm (juveniles)
Urosalpinx cinerea      England, U.K.             juveniles
Busycon carica          North Carolina, U.S.A.    juveniles
Turbo sarmaticus        Port Alfred, South
                          Africa                  42 mm (juveniles)
Busycon carica          Virginia, U.S.A.          juveniles

       Species          Growth rate (SL-mm)           Author(s)

Hexaplex trunculus           1.0 mm/month     * present study
Ocenebra lurida              0.4 mm/month     Spight et al. (1974)
Busycon canaliculatum        1.0 mm/month     Eversole and Anderson
                                                (1988)
Busycon carica               1.0 mm/month     Eversole and Anderson
                                                (1988)
Ocenebra interfossa          1.0 mm/month     Spight et al. (1974)
Ceratostoma foliatum        <2.0 mm/month     Spight et al. (1974)
Cerithium nodulosum      2.3-4.6 mm/month     Yamaguchi (1977)
Ocenebra lumaria             3.7 mm/month     Luckens (1970)
Eupleura caudata             4.0 mm/month     Mackenzie (1961)
Bolinus brandaris            4.3 mm/month     Ramon and Flos (2001)
Concholepas concholep        4.7 mm/month     Lara and Montes (1988)
Chicoreus virgineus      3.0-5.0 mm/month     Ramesh et al. (1992)
Strombus gigas          4.0-15.0 mm/month     Weil and Laughlin
                                                (1984)
Chicoreus ramosus           11.4 mm/month     Bech (1992)
Urosalpinx cinerea           3.0 mm/year      Hancock (1959)
Busycon carica              10.2 mm/year      Magalhaes (1948)
Turbo sarmaticus        2.4-13.8 mm/year      Foster et al. (1999)
Busycon carica              13.2 mm/year      Kraeuter et al. (1989)