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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.47 no.5 Valparaíso nov. 2019

http://dx.doi.org/10.3856/vol47-issue5-fulltext-5 

Research Article

Growth and morphometric relationships of the bean clam Donax punctatostriatus Hanley, 1843 in a sandy beach of southern Sinaloa, Mexico

Eduardo Ríos-Jara1 

María del Carmen Esqueda-González1 

Jesús Emilio Michel-Morfin2 

Ernesto López-Uriarte1 

José Salgado-Barragán3 

1Departamento de Ecología, Centro Universitario de Ciencias Biológicas y Agropecuarias Universidad de Guadalajara, Zapopan, Jalisco, México

2Departamento de Estudios para el Desarrollo Sustentable de Zonas Costeras Centro Universitario de la Costa Sur, Universidad de Guadalajara, San Patricio-Melaque Jalisco, México

3Instituto de Ciencias del Mar y Limnología, Unidad Académica de Mazatlán, Sinaloa, México

ABSTRACT

There have been no published studies of the genus Donax in the eastern tropical Pacific. This work describes the morphometric relationships, growth and mortality of the bean clam Donax punctatostriatus Hanley, 1843 in the sandy beach of Isla de la Piedra, south of Mazatlán Bay, Mexico. Direct collections by hand were performed during 20 monthly sample periods (November 2008 to June 2010) in the intertidal zone of the beach. A total of 2,324 clams of different sizes were removed from the sand, then measured and weighed in the laboratory. The length range of the shells was 2.78-25.64 mm (mean = 12.61 ± 4.04 mm). The length-weight relationship of the total sample indicated isometric growth (a = 0.0002 g; b = 3.0 g mm−1, R2 = 0.97); there was positive allometric growth in the recruits (<6.99 mm) (b = 3.4) and in juveniles (b = 3.2); in adults there was negative allometric growth (b = 2.6). Negative allometry of the length/width (log Wd = −0.239 + 0.922 log L) and height/width (log Wd = −0.054 + 0.900 log H) ratio of adults is consistent with a more compressed form of their shell, which assists rapid burying behavior in the sand. The maximum-recorded size of an empty shell (39 mm) was used to set the value of L and to estimate K with the Shepherd (SLCA) method. The average growth rate during the life cycle was 0.43 mm yr−1. Values of L between 29.16 and 34.22 mm were estimated with the Powell-Wetherall method using different class intervals. The mortality coefficient estimated with various methods was variable (0.84-1.15 yr−1). The growth of the clam is rapid and the mortality high, probably because of the characteristics of the habitat, in a subtropical region with high hydrodynamics and sediment transport.

Keywords: Bivalvia; bean clam; sizes; population dynamics; Von Bertalanffy growth model; Mexican Pacific

INTRODUCTION

Members of the genus Donax are commonly found on the high-energy sandy beaches of tropical and temperate regions (Ansell, 1983; Sastre, 1984; Nel et al., 2001; Gaspar et al., 2002a; Laudien et al., 2003). Due to the shape of their shell and well-developed foot, they can burrow easily and quickly into the sand in order to avoid being removed by the waves and currents (McLachlan et al., 1995; De la Huz et al., 2002). Some species of Donax frequently form part of the dominant macrofauna of sandy beach communities, with a low diversity of species (Ramón et al., 1995) due to the uns table conditions (Gaspar et al., 2002a). These clams have an important ecological function because, as very active diggers, they can affect the sediment stability and availability of oxygen, contributing to the regulation of the dynamic and vertical distribution of the infauna (Jaramillo et al., 2007). Their activity as suspension filter feeders produces feces and pseudo-feces that increase the organic material content of the sediment, facilitating the presence of infaunal biota in this habitat (Levinton, 2001; Jaramillo et al., 2007).

The bean clam Donax punctatostriatus Hanley, 1843 (Bivalvia: Donacidae) presents a geographic distribution that ranges from Isla de Cedros, in Baja California Sur (28°N) and Laguna San Ignacio, in the Gulf of California, to Manzanillo, Colima (19°N). Its bathymetric distribution ranges from the intertidal zone to a water depth of 17 m (Coan & Valentich-Scott, 2012). On the sandy beaches of Isla de la Piedra, Mazatlán, D. punctatostriatus is the dominant species together with the anomurous crustacean Emerita ratbunae, which is the dominant species for most of the year and serves as a prey item for marine and terrestrial predators although it is little used by local populations. While this clam is of little commercial interest and is rarely consumed, it used locally to make handcrafts.

Studies related to the population structure of species of the genus Donax have focused on the evaluation of their biometric relationships, growth and mortality (Rhoads & Pannella, 1970; Neuberger-Cywiak et al., 1990; Gaspar et al., 2002a,b). The main environmental factors that influence the morphometry of the shell of Donax species include sediment type (Nel et al., 2001; De la Huz et al., 2002), exposure to waves, water depth, currents, tidal regime, temperature and salinity (Newell & Hidu, 1982; Neuberger-Cywiak et al., 1990; Levinton, 2001; Gaspar et al., 2002b). However, in the Mexican Pacific, biological and ecological knowledge of these species is null, for which reason determination of the growth rate and biometric relationships of D. punctatostriatus will contribute to a fuller understanding of the biotic (endogenous, physiological) and abiotic (exogenous) factors that influence the morphology and population dynamics of this clam in this region of the world.

According to Gaspar et al. (2001), estimates of the length-weight relationship of D. trunculus, D. semistriatus and D. variegatus from the southern coast of Portugal indicate that the latter two species have positive allometric growth, while in D. trunculus is negative allometric. These authors suggest that the species of this genus present opposite growth types because of their different bathymetric distribution. Gaspar et al. (2002a) report inter-specific morphometric differences among Donax species: D. trunculus presents negative allometric growth in both length/height (L/H) and length/width (L/Wd) relationships; D. semistriatus has positive allometry in L/H and isometry in L/Wd while D. variagatus has negative allometry in L/H and positive in L/Wd. According to these authors, negative allometry can be attributed to their distribution in shallow waters. D. trunculus has a compressed shell with a smooth surface, which helps to function as an active and efficient digger, which prevents the clams from being extracted from the beach sediment by the waves and currents (De la Huz et al., 2002; Gaspar et al., 2002a).

Different direct and indirect methods have been used to estimate the growth rate in donacids. Direct methods are based on the size of clams measured between consecutive observable events. This method implies taking direct measurements of particular individuals and extrapolating the results to the entire population. This method has been conducted in populations of D. trunculus from the west coasts of Israel (Neuberger-Cywiak et al., 1990), from the Mediterranean coast of Spain (Ramón et al., 1995), and the southern coast of Portugal (Gaspar et al., 1999). Also, with D. dentifer in the bay of Malaga, Colombia (Riascos & Urban, 2002), with D. serra on the coast of Namibia (Laudien et al., 2003) and with D. hanleyanus in Mar de Las Pampas, Argentina (Herrmann et al., 2009).

The indirect methods are based on the analysis of groups (cohorts) of individuals of approximately similar sizes. These methods have been used in populations of D. trunculus on the coast of Spain (Mazé & Laborda, 1990; De la Huz et al., 2002), D. variabilis roemeri in Veracruz, Mexico (Belmar-Pérez & Guzmán del Próo, 1997), D. denticulatus at Isla Margarita, Venezuela (Marcano et al., 2003) and D. obesulus on the coast of Peru (Aguirre-Velarde & Mendo-Aguilar, 2008). The results of these studies show important differences according to each population and region, even when it is the same species.

The present study describes morphometric relationships, growth parameters (K, L) and mortality rate in a population of D. punctatostriatus from the sandy beach of Isla de la Piedra, located to the south of Mazatlán, Mexico. The research was conducted in order to generate information that contributes to understanding important aspects of the biology and ecology of this clam. In addition, these results may be used in future studies on the dynamics of other populations of this species along with its geographic distribution.

MATERIALS AND METHODS Study area

The Isla de La Piedra is a peninsula with an extensive sandy beach located to the south of the port of Mazatlán, in Sinaloa, Mexico (23°11′59″N, 106°20′19″W) at the Gulf of California (Fig. 1). During 20 months (November 2008 to June 2010), clams were collected directly from the sand by excavating to approximately 30 cm in depth with a hand shovel. This clam has been observed in Isla de La Piedra throughout the year and has vertical migrations in shallow intertidal and subtidal environments (Esqueda-González et al, 2018). The sample size was between 45 and 219 ind month−1, except in the months where there was a great disproportion of organisms towards smaller sizes as a result of recruitment; in those months, a subsample of 25% of the recruits was taken in order to estimate their abundance and sizes. Subsequently, all samples were standardized to 50 individuals through the maximum relative error method (Sparre & Venema, 1995): ε=tn-1×s/x¯×x¯ , where ε is the relative maximum error, tn-1 are the degrees of freedom of the Student t distribution, s is the standard deviation of the sample, x¯ is the mean of the sample and n is the number of clams.

Figure 1 The study area (dotted line) where the bean clam Donax punctatostriatus survey was conducted on Isla de La Piedra, México. 

Laboratory work

Shell length (the maximum distance on the anterior-posterior axis) was determined using a digital Vernier caliper (accurate to ±0.01 mm). Total weight was measured with an analytical balance (accurate to ±0.001 g). For the growth analysis, 77% of the clams were selected and shell height (the maximum distance on the dorsal and ventral axis, across the shell middle axis) and width (the maximum distance on the lateral axis between both valves of the closed-shell) measured. The rest of the clams (23%) were used to study their reproductive cycle (Esqueda-González et al., 2018). Also, a large number of juveniles were observed in July 2009, whereby a subsample of 25% of the individuals of between 3.0 and 7.0 mm in length was taken.

Data analysis

Size frequency distribution and recruitment. Histograms of a monthly size-frequency distribution (class intervals = 1 mm) were constructed for the entire study period. The data were then grouped in order to obtain the distribution of the total number of individuals. The central tendency values and coefficient of variation (CV = (standard deviation /mean) × 100) were obtained, with the latter considered an indicator of recruitment, where high values indicate large size intervals relative to the mean and therefore the possibility of frequent recruitment (Ebert, 1988).

Morphometric relationships. The criterion of Ocaña & Fernández (2011) was followed to separate the recruits and juveniles. According to this criterion, these groups are recognized by the variation in the growth pattern using the relationships length-height, length- width and height-width. The above was done by separating the clams in class intervals of one milli-meter. The length-weight relationship was estimated considering: a) the total number of individuals, b) adults, c) juveniles and d) recruited individuals, using the equation proposed by Le Cren (1951):

W(i)=a×L(i)b

where W(i) = total weight (g), L(i) = length (mm), a = intercept (coefficient of initial growth) and b = slope (coefficient of growth, i.e. relative growth rate of the variables).

For analysis of the morphometric relationship's length-height, length-width and height-width, only adult individuals (L ≥ 12 mm) were considered, and fits were made corresponding to a linear function (Ricker 1973; Laws & Archie, 1981):

logyY=loga+blogX

where Y = height (H) or width (Wd); X = length (L); a = intercept or coefficient of initial growth and b = slope or relative growth rate of the variables.

The coefficient of allometry is expressed by the exponent b in the linear regression equations. In these equations, both measurements are linear and are expressed using the same units, where b = 1 (isometric relationship) and, in the relationship length-weight, the exponent b = 3 describes an isometric growth. The parameters a and b of the biometric relationships were estimated using linear regression analysis and the least-squares method. The degree of association among variables was calculated using the determination coefficient (R2), and ANOVAs were performed in order to determine the 95% confidence intervals to b and the level of R2 significance. In order to determine whether the values of b obtained with the linear regressions were significantly different to the isometric values (b = 1 or b = 3), and to establish whether there is a negative (b < 1 or b < 3) or positive (b > 1 or b > 3) allometric relationship, a t-test (Ho: b = 1 or Ho: b = 3) was performed, with levels of significance of ±95% (α = 0.05) (Sokal & Rohlf, 1995).

Growth and mortality

The growth parameters L and K of the Von Bertalanffy equation were calculated using various analysis routines contained in the software FiSAT II (Fish Stock Assessment Tools II) (Gayanilo et al., 2005). These methods included: a) an electronic analysis of size frequencies (ELEFAN I), b) a Shepherd size composition analysis (SLCA), and c) the method of Powell-Wetherall. For each of the analyses, growth parameters were estimated with three different class intervals (1, 2 and 4 mm). In addition, the data were smoothed using moving average (order 3).

The coefficient of total mortality (Z) was estimated using the methods of Ault & Erhardt (1991) and Beverton & Holt (1956), as well as that of Pauly (software FiSAT II®) (Gayanilo et al., 2005). Donax punctatostriatus is not locally exploited, for which reason Z is assumed to be equal to natural mortality (M). The sex ratio of this population does not differ significantly from ♀1: 1♂ (Esqueda-González et al., 2018); therefore the entire population was evaluated with no separation of the sexes.

RESULTS

Size frequency distribution and recruitment

The length of the clams considered in the analysis was 2.78 to 25.64 mm (mean = 12.61 ± 4.04 mm). Of the total number of clams (2,324), 159 were recruited (2.78 to 6.99 mm), 959 were juveniles (7.0 to 11.99 mm), and 1,206 were adults (12.0 to 25.64 mm) (Table 1, Fig. 2). Clam recruitment occurred throughout the sampling period, but at a higher frequency in the periods April to September 2009 (CV = 29.5-34.6%) and March to June 2010 (CV = 24.2-31.3%). Lower frequencies of recruitment were presented in December 2008, February to March 2009 and January and May 2010 (Fig. 3).

Table 1 The size distribution of the bean clam Donax punctatostriatus in Isla de La Piedra, Sinaloa, Mexico (Nov. 2008-Jun. 2010). SD: standard deviation. 

Group Number of individuals Range of sizes (mm) Mode Mean ± SD
Total 2,324 2.78-25.64 11.0 12.61 ± 4.04
Recruits 159 2.78-6.99 6.49 5.89 ± 0.88
Juveniles 959 7.0-11.99 11.0 9.91 ± 1.40
Adults 1,206 12.0-25.64 12.5 15.64 ± 2.98

Figure 2 The size distribution of the number total of Donax punctatostriatus (November 2008 to June 2010) collected on Isla de La Piedra, Mexico. 

Figure 3 Monthly distribution of size frequencies of Donax punctatostriatus, collected on Isla de La Piedra, Mexico. 

Morphometric relationships

The length-weight relationship obtained from the sample presented a value of a = 0.0002 g and b = 3.0 g mm−1 (R2 = 0.97), indicating isometric growth (Table 2). The recruited and juvenile clams presented positive allometric growth (b = 3.4 and 3.2, respectively) (R2 = 0.84 and 0.91, respectively), while negative allometric growth was found in the adults (b = 2.6; R2 = 0.94). Height or width increases at a slower rate than length hence the negative allometry of the L/Wd and L/H relationships). In the case of the 841 adult clams, the student t-test indicates that the relationships L/W and H/Wd are negative allometric, and the relationship L/H is isometric (P < 0.05) (Table 2).

Table 2 Length-weight relationship and biometrical parameters of Donax punctatostriatus of Isla de La Piedra, Mexico. 

Biometric relation n Biometric equation Determination Coefficient SE of b (95% CI) Relation (t test)
L/W1 2,324 W=0.0002L3.04 0.97* 0.01 (3.019 – 3.059) Isometric
L/W2 159 W=0.00008L3.43 0.84* 0.12 (3.193 – 3.668) Allometric +
L/W3 959 W=0.0001L3.28 0.91* 0.03 (3.224 –3.353) Allometric +
L/W4 1,206 W=0.0005L2.66 0.94* 0.02 (2.624 – 2.699) Allometric -
L/H5 841 log H=-0.202+1.023log L 0.94* 0.009 (1.005 – 1.041) Isometric
L/Wd5 841 log Wd=-0.239+0.922log L 0.84* 0.01 (0.895 – 0.949) Allometric -
H/Wd5 841 log Wd=-0.054+0.900log H 0.93* 0.008 (0.884 – 0.917) Allometric -

n: number of specimens, L: length (mm), W: weight (g), H: height (mm), Wd: width (mm), SD: standard deviation, CI: confidence intervals,

*P < 0.05. 1: total; 2: recruits; 3: Juveniles, and 4-5: adults.

Growth and mortality

After considering the values of L and K of the Von Bertalanffy growth model obtained with the different methods, it was concluded that the Shepherd method presents the most consistent K values. From these values, it was determined that Donax punctatostriatus has a growth rate of 0.43 mm yr−1. The maximum size, taken from an empty shell on Isla de La Piedra (39 mm), was used to fix the value of L and calculate K (Table 3). The asymptotic length was also estimated using the method of Powell-Whetherall, producing values of 29.16 to 34.22 mm. After smoothing the data with a moving average of order 3, this interval was 27.64 to 28.41 mm. The values of mortality of this clam did not notably differ between the methods of Ault and Erhardt (0.84 yr−1) and Pauly (0.88 yr−1), but the value estimated using the method of Beverton and Holt (1.15 yr−1) (Table 4) was considerably higher.

Table 3 Estimations of the growth parameters and K (yr−1) with maximum length L (mm) set to 39 mm for Donax punctatostriatus collected on Isla de La Piedra, Mexico. 

Method
Shepherd Wetherall
K (yr−1) L Z/K
0.430 29.16 3.44
0.420* 28.28 3.19*

*Moving average order 3.

Table 4 Estimations of the natural mortality (M) of Donax punctatostriatus from Isla de La Piedra, Mexico. 

Method Natural mortality
Ault & Erhardt 0.84
Beverton & Holt 1.15
Pauly 0.88

DISCUSSION

The present study represents the first exploration of growth in Donax punctatostriatus. The results of this study have been compared with those available for other species of Donax (Table 5). In D. punctatostriatus, the length-weight relationship was estimated for different age groups; positive allometry was recorded among pre-adults (recruited and juveniles), while negative allometry was found in adults’ clam. The positive allometry in other species of Donax, in juvenile clams, has been associated with individuals that present a reduced capacity for successful burial and remain half-exposed in the sand with a great risk of displacement, especially in the intertidal zone, where the greatest wave activity occurs (Gaspar et al, 2001). The recruits show little variation in terms of shell form and, at this stage, it is highly likely that they will display more feeding activity related to their dispersion and mobility in the entire area swept by the tidal currents. The negative allometry observed in adult clams coincides with that observed in D. trunculus, but differs from that recorded in D. semistriatus and D. variegatus (Gaspar et al., 2001).

Table 5 Biometric relationships of species of the genus Donax. 

Species (depth) n L mean ± SD (min – max) Allometric relationship Allometric equation Determination Coefficient (R2) SE of b (95% CI of b) Relationship (t-test)
Donax faba (0 m)1 13 (NA – 24) H/L H=0.63L+0.68 0.97 Allometric -
Wd/L Wd=0.37L+0.54 0.99 Allometric -
W/L W=0.22L2.89 0.99 Allometric -
Donax serra (0 m)1 30 (NA – 66) H/L H=0.59L0.76 0.97 Allometric -
Wd/L Wd=0.42L-3.48 0.99 Allometric -
W/L W=0.03L3.37 0.99 Allometric +
Donax sordidus (0-5 m)1 22 (NA – 30) H/L H=0.62L+1.89 0.87 Allometric -
Wd/L Wd=0.41L-0.34 0.94 Allometric -
W/L W=0.23L2.93 0.98 Allometric -
Donax hanleyanus (0 m)1 47 (NA – 24) H/L H=0.63L+0.26 0.99 Allometric -
Wd/L Wd=0.48L-0.24 0.97 Allometric -
W/L W=0.11L3.09 0.99 Allometric +
Donax variabilis roemeri–2 (NA – 24) W/L W=0.00047L2.65 Allometric -
Donax semistriatus3 255 27.37 ± 4.62 W/L W=0.00006L3.17 0.92 0.057 (3.06-3.28) Allometric +
(17.40 – 42.80)
Donax trunculus3 740 27.25 ± 5.52 W/L W=0.0006L2.57 0.99 0.049 (2.47-2.67) Allometric -
(16.00 – 44.00)
Donax variegatus3 164 31.25 ± 4.51 W/L W=0.00002L3.37 0.94 0.064 (3.25-3.50) Allometric +
(21.00 – 40.12)
Donax semistriatus4 263 27.31 ± 4.58 H/L NA 0.93 0.018 (1.015-1.085) Allometric +
(17.40 – 42.80) Wd/L 0.87 0.023 (0.94-1.031) Isometric
Donax trunculus4 740 27.25 ± 5.52 H/L log H=-0.67+0.88Log L 0.93 0.009 (0.871-0.905) Allometric -
(16.00 – 44.00) Wd/L log Wd=-0.29+0.86Log L 0.92 0.009 (0.848-0.884) Allometric -
Donax variegatus4 170 30.94 ± 4.77 H/L log H=-0.25+0.93Log L 0.91 0.023 (0.895-0.984) Allometric -
(13.00 – 40.12) Wd/L log Wd=-0.79+1.12Log L 0.90 0.029 (1.065-1.179) Allometric +
D. trunculus5 (0.5-1 m) 1975 25.08 ± 4.69 W/L W=0.0003L2.69 0.96 0.012 (2.67-2.72) Allometric -
(8.91 – 40.03)
D. trunculus5 (1.5-2.0 m) 1167 25.71 ± 5.28 W/L W=0.0003L2.75 0.94 0.020 (2.71-2.79) Allometric -
(11.88 – 41.14)
D. trunculus5 (3.0-6 m) 2917 28.55 ± 5.22 W/L W=0.0004L2.70 0.95 0.011 (2.68-2.72) Allometric -
(10.40 – 44.27)
D. trunculus5 (0.5-1 m) H/L H=0.822L0.88 0.96 0.004 (0.874-0.889) Allometric -
Wd/L Wd=0.221L1.12 0.91 0.008 (1.104-1.135) Allometric +
D. trunculus5 (1.5-2 m) H/L H=0.800L0.88 0.96 0.005 (0.879-0.898) Allometric -
Wd/L Wd=0.250L1.07 0.90 0.011 (1.057-1.099) Allometric +
D. trunculus5 (3.0-6 m) H/L H=0.780L0.89 0.97 0.003 (0.892-0.903) Allometric -
Wd/L Wd=0.326L0.99 0.91 0.006 (0.987-1.010) Isometric
D. striatus6 282 13.11 ± 5.26 H/L H=-0.182+0.98L 0.99 0.005 Allometric -
(3.48 – 28.24) Wd /L Wd=-0.549+1.13L 0.98 0.009 Allometric +
Wd /H Wd=-0.340+1.14A 0.98 0.007 Allometric +
D. denticulatus6 285 15.62 ± 5.77 H/L H=-0.178+1.005L 0.99 0.003 Isometric
(3.94 – 24.39) Wd /L Wd=-0.435+1.028L 0.98 0.006 Allometric +
Wd /H Wd=-0.252+1.022A 0.99 0.006 Allometric +

n: number of individuals, H: height (mm), Wd: width (mm), L: length (mm), W: weight (g), min: L minimum, max: L maximum, SE: standard error, SD: standard deviation, CI: confidence intervals, NA: not available.

Juvenile and recruited clams were excluded from the analysis of the relationships L/H, L/W and H/Wd; it was considered that inclusion of individuals of sizes <12 mm could erroneously influence the estimates, since the shells of young clams present little tridimensional variation during this stage of growth, as demonstrated by the analysis of the biometric relationships of this size group. In some bivalves, the shell can be higher than it is wide at the start of its growth, which allows it to resist removal from the sediment by currents and turbulence (Hinch & Bailey, 1988). However, the shell of the young and adult clams changes its proportions and morphometric with growth. These ontogenic changes in growth type have been related to different life habits; since the juveniles present shells that are more hydrodynamic, they are active diggers in the intertidal zone, while this ability to tunnel diminishes in the adults, favoring a more sedentary lifestyle, as reported in other Donax species (Thayer, 1975; Soares et al., 1996; Gaspar et al., 2002b; Ocaña & Fernández, 2011).

The regression of L/H indicated isometric growth in adults. This growth type is attributed to donacid species that are distributed in shallow to deep water (Gaspar et al., 2002a), although in the case of D. punctatostriatus it corresponds to adult individuals that inhabit shallow water. In the intertidal zone of the beach at Isla de La Piedra, only juveniles and adults of small sizes (7.025.64 mm in length) were found. This is also the case with D. serra, which is distributed between the intertidal and shallow subtidal zones, especially on dissipative beaches (McLachlan, 1996).

The relationship L/Wd, as with that of L/W, presented negative allometric growth in D. punctatostriatus, indicating a trend towards enlargement of the shell, as has been associated with active burrowing bivalve species distributed in shallow waters. This allometry indicates that older shells are thinner in cross-section (L/Wd is negative allometric) but maintain a similar lateral outline (L/H is isometric). According to De la Huz et al. (2002), coarse sediments limit the presence of D. trunculus on exposed sandy beaches of the Iberian Peninsula. Because the capacity for burial among the bivalves that live in soft substrates depends on the particle size of that substrate (Newell & Hidu, 1982), although the individuals that inhabit exposed beaches must bury themselves more rapidly in order to avoid physical removal from the substrate by the actions of the waves and tidal currents. In addition to limiting the distribution of clams such as Mya arenaria, substrates formed by coarse grains present a higher physical resis tance to burial (Newell & Hidu, 1982). The predominance of small clams in the intertidal and large clams in the shallow subtidal zones has been related to intraspecific competition for food and space between the juveniles and adults of D. trunculus (Gaspar et al., 2002b).

The species of the genus Donax presented different growth types. The effect of sediment particle size on shell growth (positive or negative allometry) has been recognized in other bivalve species; the shape of the bivalve determines its capacity for penetration of the substrate, as is the case with Tellina tenuis, Macoma balthica, Donax vittatus and Cerastoderma edule (Trueman et al., 1966; Brown & Trueman, 1991), Donax faba, D. serra, D. sordidus, D. hanleyanus, Mesodesma mactroides, Tivela stultorum and Siliqua patula (McLachlan et al., 1995; Nel et al., 2001; Fiori & Carcedo, 2015), as well as Mactra violacea (Laxmilatha, 2008) and Ruditapes philippinarum (Caill-Milly et al., 2012). In this type of study, it is important to consider local environmental conditions (i.e., sediment type, exposure to waves, the incidence of currents), since these can differ markedly.

The Shepherd method using size-frequency distribution was found to be the most suitable for estimating growth in the population of D. punctatostriatus at Isla de La Piedra, since it produced estimates that were consistent with the different class intervals. In reality, the estimation of growth values from indirect methods based on the analysis of size-frequency distributions can be considered an advantage in this study. Such analysis is more precise when based on data obtained over a long period of sampling (Herrmann et al, 2009). In the study area, the collected individuals mainly comprised recruited and juvenile clams, with small-sized adults (<26 mm) collected at a lower proportion. The use of an empty shell collected in the same beach is a useful reference of the maximum expected size (39 mm) for the clam population in the intertidal environment. However, the estimated maximum L value was still lower (29.16 mm).

The growth values estimated in previous studies of donacids contrast with those obtained in this study (Table 6). There are dissimilarities in the estimates, even among populations of the same species and from the same study area (e.g., D. trunculus or D. hanleyanus), as a result of the use of different methods. For this reason, it is important to recognize inconsistencies related to methodology and differentiate these from variation attributable to natural causes. The values of L, and K obtained in the present study indicate that D. punctatostriatus presents smaller sizes than those observed in other species of Donax from temperate waters (Table 6).

Table 6 Growth parameters estimated with different methods in species of the genus Donax

Species Region Maximum length (mm) Method K (yr−1) L (mm) Reference
Donax variabilis roemeri Tuxpan, Veracruz, Mexico 24 Modal progression 0.520 37.8 Belmar Pérez & Guzmán del Próo (1995)
Donax trunculus West coast Spain 36 Growth rings 0.71 41.8 Ramón et al. (1995)
Donax trunculus West coast Spain 36 Length frequency distribution 0.58 46.0 Ramón et al. (1995)
Donax trunculus South coast Portugal 44 Growth rings 0.58 47.3 Gaspar et al. (1999)
Donax dentifer Málaga Bay, Colombia 30.5 Mark-recapture 0.624 29.3 Riascos & Urban (2002)
Donax serra Namibian coast 82 Mark-recapture 0.274 82 Laudien et al. (2003)
Donax denticulus Ensenada La Guardia, Venezuela 30 Modal progression 1.79 30.0 Marcano et al. (2003)
Donax obesulus Sarapampa, Perú 31 Length frequency distribution 0.991 33.7 Aguirre-Velarde & Mendo-Aguilar (2008)
Donax hanleyanus Mar de Las Pampas, Province of Buenos Aires, Argentina 44 IFM* 0.410 44 Herrmann et al. (2009)
Donax hanleyanus Mar de las Pampas, Province of Buenos Aires, Argentina 40 Length frequency distribution 0.470 44 Herrmann et al. (2009)
Donax hanleyanus Faro Querandí, Atlantic coast, Argentina 40 Length frequency distribution 0.480 44 Herrmann et al. (2009)
Donax punctatostriatus Isla de La Piedra, Sinaloa, Mexico 25.64 Length frequency distribution 0.430 39 Present study

*in situ fluorescent marking (IFM) method.

According to Ansell (1983), mortality rates are high in donacids of tropical latitudes. Mortality in D. punctatostriatus estimated using the method of Beverton and Holt, as well as those of Ault and Erhardt and Pauly, provide a range of values. The value obtained with the Beverton and Holt method seems to be overestimated (1.15 yr−1), because it was designed to estimate fish mortality. On the other hand, the methods of Ault and Erhardt, and Pauly, were consistent in their mortality values (0.84 and 0.88 yr−1); both methods have been more frequently used to estimate mortality in invertebrates, including bivalves (Sparre & Venema, 1995).

At present, only some authors have recorded the mortality of donacids. According to Riascos & Urban (2002), the mortality of D. dentifer in Colombia shows that the populations of the lower part of the intertidal zone are composed of small (2-5 mm) individuals with a mortality of 2.6 yr−1, while the larger (19-25 mm) individuals present a rate of 1.7 yr−1. The small clams found in the low part of the intertidal zone are reported to be more vulnerable to depredation by birds and crabs (Soares et al., 1996, Riascos & Urban, 2002), which could explain the high mortality prevalent in this zone.

The sandy beach of Isla de La Piedra is semi-protected, with a strong influence of the waves and tides; it is a very dynamic, high-energy beach with significant turnover of sediments throughout the year (Montaño-Ley, 1985). The compressed form of the D. punctatostriatus shell enables individuals of this species to tunnel more rapidly into the sediment and avoid being removed from the substrate by the waves and currents. The negative allometry recorded in L/W, L/Wd and H/W in the present study supports this hypothesis. However, the mortality of this species, which is lower than that recorded for D. dentifer by Riascos & Urban (2002), can be explained by the fact that the former species can bury itself much more rapidly and escape possible depredation.

The bivalves exhibit wide morphological variation, which is intimately linked to their life cycle and ecology. It is possible to determine which environmental variables influence the growth and form of the shells of this group of mollusks. The methods used in the present study are only an approximation to the real growth and mortality values of the population of the Isla de La Piedra bean clam. According to these values, this population has a relatively rapid growth rate and moderate mortality compared to populations of other species.

The majority of the marine mollusks of economic importance are distributed in the coastal zones, including the sandy and rocky beaches, and the estuaries and coastal lagoons. Mexico presents very favorable conditions for the exploitation of mollusks since its coastline is more than 10,000 km long (Ruiz-Durá, 1985). However, a problem for adequate exploitation of these mollusks in Mexico is the scarcity of published information on their biology and ecology. Due to the intense exploitation of the main fishing resources traditionally exploited, and the evident decrease of their populations, other species of potential importance are currently considered as a real alternative, which is the case of several clam species of moderate and small sizes with significant populations in specific locations. Exploitation alternatives involve the assessment of their population structure and dynamics for sustainable use.

Although there is relevant information on other species of Donax from different populations of the world, there is little knowledge on the biology and ecology of the bean clam D. punctatostriatus. The population of Isla de La Piedra is of particular interest since it is located on the northern limit of its geographical distribution, in a subtropical region located at the mouth of the Gulf of California, where environmental conditions should have substantial influence, in particular, the temperature and the photoperiod. For example, information on reproductive biology will help understand the strategies of development and survival in this part of the world.

ACKNOWLEDGMENTS

We are grateful to Carlos Sauma, Eva Visueta, María Ana Tovar, and Paul Esqueda for their help during fieldwork. The second author thanks the Consejo Nacional de Ciencias y Tecnología for financial support (Ph.D. scholarship number 90606). The research was held at the Centro Universitario de Ciencias Biológicas y Agropecuarias at Universidad of Guadalajara.

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Recibido: 12 de Julio de 2018; Aprobado: 10 de Junio de 2019

Corresponding author: María del Carmen Esqueda-González (carmen.esqueda@academicos.udg.mx)

Corresponding editor: Claudia Bremec

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