Population ecology and secondary production of congeneric bivalves on a sheltered beach in Southeastern Brazil.
KEY WORDS: molluscs, Tellina lineata, Tellina versicolor, depositivores, growth, mortality, Brazil
Molluscs are important ecological macrobenthic components of marine coastal ecosystems, such as estuaries and sandy beaches, and are exposed to different environmental factors such as temperature, salinity, and currents (Degraeret al. 2007), which in turn affect their distribution and influence their population dynamics, demography, and reproduction (Fuiman et al. 1999, Cardoso et al. 2007). In sheltered sandy beaches, molluscs, especially bivalves, stand out for their high abundance, biomass, and dominant taxa (Olafsson et al. 1993, Urban 1994, Vaughn & Spooner 2006). These organisms play an important role in benthic communities, occupying different niches according to their feeding habits (Jaramillo et al. 2007), affecting sediment stability (Hall 1994) and the nutrient flow from the sediment to the water column (Michaud et al. 2006). They are also a compound part of the diet of several aquatic organisms and can affect energy cycling in the food chain (Paine 1966).
Studies on population biology, biomass, and production of highly dominant species, especially bivalves, provide knowledge regarding their role in the communities, as well as allowing for comparisons between ecosystems (Hibbert 1976). On a latitudinal scale, differences in bivalve growth rate have often been associated to latitudinal temperature gradients (Vakily 1992, Heck et al. 2002, Fiori & Morsan 2004), although other factors such as food quality and quantity, tidal level, and type of sediment appear to play a greater role on a local scale (Beukema et al. 2002, Carmichael et al. 2004). Populations from low intertidal and subtidal areas show higher growth rates and reproductive output due to longer submersion periods, allowing for the ingestion of greater amounts of food (Roseberry et al. 1991, Cardoso et al. 2007).
Members of the Tellinidae family are considered major components of trophic chains in sheltered sandy beaches located in temperate and tropical waters, due to the high number of species, abundance, and their ecological functions (Trevallion 1971, Dekker & Beukema 1999, Lizarralde & Cazzaniga 2009). Most of the tellins are distributed in intertidal beach zones and shallow waters (Trevallion 1971, Denadai et al. 2001), but knowledge regarding Tellina species population parameters is scarce. Some studies are available on the distribution of Tellina petitiana (D'Orbigny, 1846) in relation to environmental factors (Lizarralde 2002), predation by migratory birds (Pagnoni 1997), reproductive cycle (Baron & Ciocco 2001), population biology, and mean biomass (Lizarralde & Cazzaniga 2009). There is also information on Tellina tenuis (Da Costa, 1778) (Dekker & Beukema 1999) and Tellina lutea (W. Wood, 1828) (Selin 2010) population dynamics.
In Brazilian coast, Tellina lineata (Turton, 1819) and Tellina versicolor (De Kay, 1843) are widely distributed, occurring from the states of Ceara (05[degrees] 11' S, 39[degrees]17' W) to Santa Catarina (25[degrees] 57' S, 48[degrees]19' W) (Rios 1994). Arruda et al. (2003) classified both species as depositivores, with distribution in the intertidal region of muddy and sandy-muddy sheltered beaches. Cardoso et al. (2012) reported a high abundance of these species in sheltered beaches at Sepetiba Bay, southeastern Brazil. Few studies, however, have focused on the Tellina species of the South American coast.
The aim of this study was to analyze and compare the population ecology of the two congeneric bivalves, Tellina lineata and Tellina versicolor, in a sheltered beach located in southeastern Brazil, assessing their spatial and temporal distribution, population parameters (growth rate, mortality rate, and life span), and secondary production.
MATERIALS AND METHODS
Study Area and Sampling
Itacuruca is the largest island inside the Sepetiba Bay (22[degrees]54' S, 43[degrees]34' W), Brazil. It harbors several beaches that provide different environments (protected and exposed) for several marine species that use these areas during all or part of their life cycle (Araujo et al. 1997). Among these beaches, Flexeiras beach (22[degrees]56' S, 43[degrees]53' W), characterized as sheltered according to the classification system proposed by McLachlan (1980), is noteworthy for its high richness and macrofauna diversity, mainly molluscs (Cardoso et al. 2011). The Flexeiras beach has a mean salinity of 33 (Cardoso et al. 2011).
Sampling was carried out monthly within the intertidal zone from December 2006 to February 2009, during the low spring tide. Six transects were set up perpendicularly to the shoreline and spaced 20 m apart. At each transect, sampling units (SU) were taken every 3 m, with a 0.04-[m.sub.2] metal sampler at a depth of 25 cm, from the boulder wall to 9 m below the waterline during low tide. Each sample was sieved through a 0.5-mm mesh and the material was taken to the laboratory (Fig. 1).
Sediment samples for particle size analyses were collected with a 3.5-cm-diameter corer to a depth of 15 cm at the lower, middle, and upper strata of two transects (transects 2 and 5).
All individuals were preserved in 70% ethanol and shell lengths of Tellina lineata and Tellina versicolor were measured. The anteroposterior length of the valves in all individuals were measured with calipers (0.01 mm precision), with each species grouped into 1.0-mm-size classes. All soft parts were individually removed, dried at 70[degrees]C for 24 h, weighed on a 0.001-g precision balance to obtain dry weight values, subsequently ashed in a muffle furnace at 600[degrees]C for 4 h, and reweighed to obtain the mass of the ash weight. The ash-free dry mass (AFDM) of each individual from both species was obtained by subtracting the dry mass from the ash mass.
The sediment samples were dried for 24 h at 70[degrees]C in an oven and subsequently passed through a series of sieves (-2.5 to 4.0 phi) in order of size to determine the average grain size (Folk & Ward 1957). The mean particle size was then calculated for the three sampled strata. The beach face slope of each transect was measured by the height difference between the drift and water lines (Emery 1961).
Monthly length-frequency distributions (LFD) for each species were used to estimate growth patterns, following the procedures suggested by Gomez and Defeo (1999) and Defeo et al. (2001): (1) normally distributed components of LFD were separated through the NORMSEP routine of the FISAT program (Gayanilo et al. 1996); (2) absolute ages were assigned to the respective cohorts (lengths) to build an age-length key; and (3) the resulting age-length key for each bivalve was used to fit the generalized von Bertalanffy growth function (VBGF: Gayanilo et al. 1996) by nonlinear least squares:
[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]
where [L.sub.t] is length at time t (mm); [L.sub.[infinity]] is the theoretical maximum length attained by the species; K is the curvature parameter; C accounts for the intensity of seasonal growth oscillations; [t.sub.0] is the theoretical age at zero length; and WP is the winter point, that is, the period of growth reduction, expressed as a decimal fraction of the year. To compare the fitted VBGF between the bivalves, an analysis of the residual sum of squares was performed (Chen et al. 1992). The growth index phi prime [PHI]' = 2[1og.sub.10] ([L.sub.[infinity]]) + [log.sub.10]K (Pauly & Munro 1984, Defeo et al. 1992) was used as a measure of overall growth performance.
The instantaneous mortality rate (Z) was calculated for each species using the length-converted catch curve method (Pauly et al. 1995) of the FISAT program (Gayanilo et al. 1996). The Z estimation was given by: ln (n) = g - Z x t, where N is the number of individuals, g is the intercept of the regression, Z is the unbiased mortality estimated, and t is the estimated age in each cohort (Pauly et al. 1995). The annual mortality rate (A) was obtained by the expression: A = 1 - [e.sup.-Z], according to Ricker (1975). Life span ([t.sub.max]) was estimated by the VBGF growth parameters and based on the maximum length to estimate the maximum age ([T.sub.max]) for both species (Cardoso & Veloso 1996).
The relationship between individual shell length and the AFDM of the soft tissues was estimated by a linear regression analysis, following the equation: In W = ln a + b ln L, where W is the mean AFDM (g); L is the individual length (mm); and a and b are the regression parameters. Production was estimated by the weight-specific growth rate method (Crisp 1984), given by equation P = [SIGMA][SIGMA] [f.sub.i][G.sub.i][w.sub.i][DELTA]t, where f is the mean number of individuals from length class i during the time interval [DELTA]t, [G.sub.i] is the specific growth rate in weight within the length class i, and [w.sub.i] is the mean weight of the length class. [G.sub.i] can be obtained by [G.sub.i] = b x K[([L.sub.[infinity]]/[L.sub.i]) - 1], where b is the exponent of the length-weight relationship, K and [L.sub.[infinity]] are VBGF parameters, and [L.sub.i] is the mean length in the length class i. Annual mean biomass was calculated as B = [SIGMA][SIGMA][f.sub.i][w.sub.i][DELTA]t.
A two-way analysis of variance (ANOVA) was applied to test the null hypothesis that Tellina lineata and Tellina versicolor abundance does not differ among months. Cochran's test (Underwood 1997) was used to test for variance homogeneity and then data were log-transformed to remove variance heterogeneity. Tukey's honest significant difference test was used a posteriori to assess significant differences. Nonlinear models were used to assess the relationship between bivalve density and mean grain size. Student's t-test was used to compare the numerical proportions of T. lineata and T. versicolor in each month. The test of slopes was used to compare mortality rates between the species (Zar 1999). In all statistical analyses, a significance level of 5% was adopted (Zar 1999).
The variation in mean grain size ranged from 0.25 mm (media sand) to 1.30 mm (very coarse sand), with a mean value of 0.59 [+ or -] 0.17 mm. The one-way ANOVA indicated significant differences between mean grain size among strata (F = 4.57, df = 2/159, P < 0.05), Tukey's test detected differences between the upper strata in comparison with the other two strata (P < 0.05). Infra and middle strata were composed of coarse sand, whereas medium sand prevailed at the supralittoral levels. The beach presented a gentle slope, ranging from 1/20 to 1/40 m.
Density was significantly higher for Tellina lineata than Tellina versicolor in all months (t = 3.18; P < 0.05). The highest T. lineata densities were recorded in March and May 2008 (autumn) and February 2009 (summer), whereas the highest T. versicolor population peaks were observed in August 2007 and June and July 2008 (winter). The high standard errors in the monthly density of the species suggest a clumped distribution of individuals (Fig. 2).
The between-month abundance variation of the Tellina lineata population density (5.2-123.75 inds/[m.sup.2]) was higher than Tellina versicolor (1.67-36.67 inds/[m.sup.2]). The relationship between tellinid species density and mean grain size exhibited a different pattern, T. lineata density was not significantly correlated with grain size (n = 27, [r.sup.2] = 0.06, P > 0.05), whereas T. versicolor density significantly increased toward coarse grains (n = 27, [r.sup.2] = 0.13, P = 0.059).
The species were distributed in all sampling levels. Tellina Lineata, however, showed a significant preference for occupying the intermediate levels of the beach (SU 5-8) (F = 17.62, df = 9/ 260, P < 0.01), whereas Tellina versicolor showed higher densities at lower levels (SU 1-3) (F = 20.44, df = 9/260, P < 0.01) (Fig. 3). There was a significant inverse correlation between the distance water line and the population densities for T. lineata and T. versicolor (r = -0.321, P < 0.05).
Both species showed a markedly different population structure (Fig. 4), as reflected by the one-way ANOVA (F = 1021.59; P < 0.01): Tellina lineata was dominated by small length classes ranging from 1 to 12 mm (64% of the total population), whereas the dominant size classes in Tellina versicolor ranged from 13 to 32 mm (ca. 73%).
The analyses of the calculated growth parameters revealed significant variations in individual growth between bivalves: Tellina versicolor grew faster than Tellina lineata, as corroborated by the growth index phi prime ([SIGMA]'). The VBGF model with seasonal oscillation through the performance of nonlinear fitting explained more than 99% of the variance for T. lineata and more than 98% for T. versicolor. Growth parameter estimates were statistically significant (P < 0.05; Table 1).
Moderate intra-annual oscillations in growth reflected a minimal growth period in December (summer) for Tellina lineata (C = 0.41, WP = 1.00) and in September (spring) for Tellina versicolor (C = 0.23, WP = 0.70) (Fig. 5). The life span ([t.sub.max]) corresponding to these estimates was more than 3.15 y (31.28 mm) and 2.86 y (32.37 mm) for T. lineata and T. versicolor, respectively. Both sizes represent the largest individuals sampled from each population.
The comparison of the test of slopes indicated that the mortality rate for Tellina lineata (1.96 [y.sup.-1]) was significantly lower than for Tellina versicolor (6.37 [y.sup.-1]) (t-test = 8.13, P < 0.001). For those range sizes where mortality was estimated, the annual mortality rate (A) was 86% for T. lineata and 99.8% for T. versicolor (Fig. 6, Table 2).
The regression equation between AFDM and length-weight relationship for the bivalve populations were expressed as: [W.sub.T, lineata] = (6 x [10.sup.-6]) [L.sup.2,855] (n = 545, r = 0.97, P < 0.05) and [W.sub.T, versicolor] = (4 x [10.sup.-6]) [L.sup.2,858] (n = 332, r = 0.96, P < 0.05).
The biomass (5), secondary production (P) and turnover rates (P/B) calculated for Tellina lineata (B = 1.391 AFDW g x [m.sup.-2], P = 2.293 AFDW g x [m.sup.-2] x [y.sup.-1], P/B = 1.65 [y.sup.-1]) were higher than for Tellina versicolor (B = 0.577 AFDW g x [m.sup.-2], P = 0.786 AFDW g x [m.sup.-2] x [y.sup.-1], P/B = 1.36 [y.sup.-1]).
The population parameters differed between tellinid species: Tellina lineata showed higher abundance, life expectancy, biomass, secondary production, and turnover rate values, whereas Tellina versicolor showed higher growth and mortality rate. These differences may be caused due to the interaction between both species and their similar lifestyles and food habits.
The distribution of the species is maintained by physical factors associated with biological interactions (McLachlan & Jaramillo 1995). It is unlikely that a single factor will explain patterns of distribution, because a species can occupy distinct habitats. The determination of macrofauna distribution in sandy beaches is difficult, because of the variability of environmental conditions and because most organisms live within the sediment (Amaral et al. 1990). The differences between the density peaks observed for Tellina lineata (autumn and summer) and Tellina versicolor (winter) and the spatial segregation with preference for differentiated levels suggest strategies adopted to avoid possible competition between species, observed in studies on the distribution of macrofauna species in the intertidal zone (Cardoso & Veloso 2003, Mattos & Cardoso 2012). The distribution in these lower beach zones are also related to a higher survival rate due to foraging protection from predators, such as birds and crabs (Zwarts & Wanink 1993). One of the most important factors defining habitat for psammophiles is sediment size. Grain size is considered the most critical factor and exerts direct influence on molluscs burrowing and mobility (Alexander et al. 1993, Ansell & Trevallion 1969). Intertidal or subtidal benthic macrofauna may select for optimal condition. Thus, the correlation positive between T. versicolor and grain size suggests that this species has optimum performance in coarser sands.
The LFD of Tellina versicolor population showed a high percentage of
adults, suggesting a senescent population with a marked absence of recruits (Fig. 4). This population structure could be explained by (1) recruitment failure due to irregular larvae contribution or an adverse effect of hydrodynamic factors (e.g., currents) affecting settlement and (2) low survival of recruits caused by unfavorable habitat conditions. These negative effects of the environment affecting recruitment success have been also documented in other intertidal bivalves inhabiting sandy beaches, tidal flats, and rocky substrates (e.g., Defeo 1996, Caddy & Defeo 2003). These hypotheses should be tested in the future.
The higher growth rate of Tellina lineata in relation to Tellina versicolor can be related to performance of the growth index phi prime, a parameter used to compare the growth intensity between species (Pauly & Munro 1984). Values of WP (point of lowest growth rate during the year) exhibited a different pattern for the two bivalves, T. lineata had its minimal growth in the summer months and T. versicolor during spring. Both periods can be related to higher temperatures and bivalve reproduction (Beukema & Dekker 1999). In subtropical regions, there is an increase in bivalve energy reserves during this period, as well as a reduction in growth and greater energy investment in reproduction (Moura et al. 2008). This pattern is also observed in other species from different taxonomic groups comprising sandy beach macrofauna (Caetano et al. 2006, Petracco et al. 2010). Besides temperature, food availability is also considered as an important parameter controlling growth rate of some Tellina species, because this regulates the beginning/end of the growth period and determines the occurrence of the number of growth periods that will occur during the year (Beukema et al. 1985, Beukema & Desprez 1986). The higher life expectancy recorded for T. lineata in comparison with T. versicolor is related to T. lineata's lower lvalues and lower growth performance rate (phi prime). Organisms with lower growth rates have higher life expectancies (Pauly 1979).
A consistent latitudinal pattern in growth performance was observed for Tellina species, showing higher [SIGMA]' values in low latitudes when compared with higher latitude species (Table 3). Vakily (1992) noted that bivalves grow faster at lower latitudes due to higher temperatures that increase metabolic rates. This pattern, however, may also be related to differences in food availability and plasticity in life habits that allow the species to survive under several temperatures and environmental conditions (Brown 1996, Navarro et al. 2000, Paterson et al. 2003, Cardoso et al. 2007).
The lower mortality rate of Tellina lineata (1.96 [y.sup.-1]), more than three times lower when compared with Tellina versicolor (6.37 [y.sup.-1]), could be related to greater burial depths of this species (Holme 1961). Thus, T. lineata suffers less from predation impacts when compared with T. versicolor, which mainly inhabits shallow waters (Trevallion 1971, Denadai et al. 2001). Other hypothesis would be irregular or spasmodic recruitment pulses that could cause a discontinuity in the arrival of recruits, which could explain the LFD of T. versicolor with the reduction of some year classes, compared with T. lineata (Caddy & Defeo 2003).
The biomass and secondary production values of both species were higher than those found by Warwick et al. (1978) for Tellina fabula (Gmelin, 1791) (B = 0.325 g AFDW [m.sup.-2] and P = 0.292 g AFDW [m.sup.-2] x [y.sup.-1]) in Wales. They suggest that the lower biomass and secondary production values are related to the greater abundance of intermediate-sized individuals in this population, because, in natural populations biomass and secondary production depend on other factors, such as the age structure of the population (Sprung 1993).
The relationship between annual production and mean biomass (P/B) is an adequate method to compare the productivity of different species, populations, and communities (Ansell et al. 1978). Both tellinid species showed higher P/B ratios (Tellina lineata = 1.65/year; Tellina versicolor = 1.36/ year) (Southeastern Brazil, 22[degrees] S) in comparison with those found for other Tellina species, such as T. petitiana (0.97/year) (Argentina, 42[degrees]S) (Lizaralde & Cazzaniga 2009) and T. fabula (0.90/year) (Wales, 51[degrees]N) (Warwick et al. 1978). The higher P/B ratios can be explained by the pattern described by Cardoso and Veloso (2003) for the bivalve Donax hanleyanus, in which higher P/B values are found at lower latitudes. These higher P/B values may be related to greater food availability and individual biomass contributions for energy and nutrient cycling (Souza 1998, Cardoso & Veloso 2003).
The highest abundance of Tellina lineata compared with Tellina versicolor and a spatial distribution with a preference for different levels may be associated with a difference in the species' capacities to use resources available in the marine environment. This can be confirmed by the negative correlation between densities of both species over time. Further experiments are necessary to evaluate interactions between tellinid species, estimating the degree of interactions and effects on population parameters.
We express our deepest gratitude to all fieldwork participants (Bruna Zavarize, Gustavo Mattos, Fabio Sendim, and Carlos Henrique Caetano). We also thank Omar Defeo and anonymous reviewer for their helpful comments that improved the manuscript. Ricardo S. Cardoso was supported by FAPERJ (Fundacao de Amparo a Pesquisa do Estado do Rio de Janeiro) and CT-Infra (Fundo Setorial de Infra-Estrutura) by MCPCNPq (no. E-26/171.164/2006). Tatiana M. B. Cabrini was supported by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) and by Universidade Federal do Rio de Janeiro (UFRJ) post-graduate research studentships.
Alexander, R. R., R. J. Stanton & J. R. Dodd. 1993. Influence of sediment grain size on the burrowing of bivalves: correlation with distribution and stratigraphic persistence of selected Neogene clams. Palaios 8:289-303.
Amaral, A. C. Z., E. H. Morgado, P. P. Lopes, L. F. Belucio, F. P. P. Leite & C. P. Ferreira. 1990. Composition and distribution of the intertidal macrofauna of sandy beaches on Sao Paulo coast. In: Anais II Simposio de Ecossistemas da Costa Sul e Sudeste Brasileira. Estrutura, Funcao e Manejo. Publ. Aciesp, Sao Paulo. 3: 258-273.
Ansell, A. D. & A. Trevallion. 1969. Behavioural adaptations of intertidal molluscs from a tropical beach. J. Exp. Mar. Biol. Ecol. 4:9-35.
Ansell. A. D., D. S. McLusky & A. Trevallion. 1978. Production and energy flow in the macrobenthos of two sandy beaches in south west India. Proc. R. Soc. Edinb. 76:269-296.
Araujo, F. G., A. G. Cruz-Filho, M. C. C. Azevedo. A. C. A. Santos & L. A. M. Fernandes. 1997. Estrutura da comunidade de peixes jovens da margem continental da Baia de Sepetiba, RJ. Acta Biol Leolpold. 19:61-83.
Arruda, E. P., O. Domaneschi & A. C. Z. Amaral. 2003. Mollusc feeding guilds on sandy beaches in Sao Paulo State. Brazil. Mar. Biol. 143:691-701.
Barnett, P. R. O. & J. Watson. 1986. Long-term changes in some benthic species in the Firth of Clyde, with particular reference to Tellina tenuis da Costa. Proc. R. Soc. Edinb. 90B:287-302.
Baron, P. & N. Ciocco. 2001. Reprodutive cycle of the clam Tellina petitiana d'Orbigny 1846 in Nuevo Gulf (Argentina). Veliger 44:370-380.
Beukema, J. & M. Desprez. 1986. Single and dual annual growing seasons in the tellinid bivalve Macoma balthica. J. Exp. Mar. Biol. Ecol. 102:35-45.
Beukema, J. J., E. Knol & G. C. Cadee. 1985. Effects of temperature on the lengths of the annual growing season in the tellinid bivalve Macoma balthica living on tidal flats in the Dutch Wadden Sea. J. Exp. Mar. Biol. Ecol. 90:129-144.
Beukema, J. J., G. Cadee & R. Dekker. 2002. Zoobenthic biomass limited by phytoplankton abundance: evidence from parallel changes in two long-term data series in the Wadden Sea. J. Sea Res. 48:111-125.
Brown, A. C. 1996. Behavioural plasticity as a key factor in the survival and evolution of the macrofauna on exposed sandy beaches. Rev. Chil. Hist. Nat. 69:469-474.
Caddy, J. F. & O. Defeo. 2003. Enhancing or restoring the productivity of natural populations of shellfish and other marine invertebrate resources. FAO Fisheries Technical Paper. No. 448. Rome, Italy: FAO. 159 pp.
Caetano, C. H. S., R. S. Cardoso, V. G. Veloso & E. S. Silva. 2006. Population biology and secondary production of Excirolana braziliensis (Isopoda: Cirolanidae) in two sandy beaches of southeastern Brazil. J. Coast. Res. 22:825-835.
Cardoso. R. S. & V. G. Veloso. 1996. Population biology and secondary production of the sandhopper Pseudorchestoidea brasiliensis (Amphipoda: Talitridae) at Prainha beach, Brazil. Mar. Ecol. Prog. Ser. 142:111-119.
Cardoso, J. F. M. F., J. I. J. Witte & H. W. Van Der Veer. 2007. Habitat related growth and reproductive investment in estuarine waters, illustrated for the tellinid bivalve Macoma balthica (L.) in the western Dutch Wadden Sea. Mar. Biol. 152:1271-1282.
Cardoso, R. S. & V. G. Veloso. 2003. Population dynamics and secondary production of the wedge clam Donax hanleyanus (Bivalvia: Donacidae) on a high-energy, subtropical beach of Brazil. Mar. Biol. 142:153-162.
Cardoso. R. S., G. Mattos, C. H. S. Caetano, T. M. B. Cabrini, L. B. Galhardo & F. Meireis. 2012. Effects of environmental gradients on sandy beach macrofauna of a semi-enclosed bay. Mar. Ecol. (Bert.) 33:106-116.
Carmichael, R. H., A. C. Shriver& I. Valiela. 2004. Changes in shell and soft tissue growth, tissue composition, and survival of quahogs Mercenaria mercenario and softshell clams Mya arenaria, in response to eutrophic-driven changes in food supply and habitat. J. Exp. Mar. Biol. Ecol. 313:75-104.
Chen. Y., D. A. Jackson & H. H. Harvey. 1992. A comparison of von Bertalanffy and polynomial functions in modeling fish growth data. Can. J. Fish. Aquat. Sci. 49:1228-1235.
Crisp, D. J. 1984. Energy flow measurements. In: N. A. Holme, & A. D. McIntyre, editors. Methods for the study of marine benthos. IBP Handbook no. 16. Oxford, UK: Blackwell Scientific Publications, pp. 284-372.
Defeo, O. 1996. Recruitment variability in invertebrates, with emphasis in exposed sandy beach populations: a review. Rev. Chil. Hist. Nat. 69:615-630.
Defeo, O., F. A. Sanchez & J. Sanchez. 1992. Growth study of the yellow clam Mesodesma mactroides: a comparative analysis of three length based methods. Sci. Mar. 56:53-59.
Defeo, O., J. Gomez & D. Lercari. 2001. Testing the swash exclusion hypothesis in sandy beach populations: the mole crab Emerita brasiliensis in Uruguay. Mar. Ecol. Prog. Ser. 212:159-170.
Degraer, S., P. Meire & M. Vine. 2007. Spatial distribution, population dynamics and productivity of Spisula subtruncata: implications for Spisula fisheries in seaduck wintering areas. Mar. Biol. 152:863-875.
Dekker, R. & J. J. Beukema. 1999. Relations of summer and winter temperatures with dynamics and growth of two bivalves, Tellina tenuis and Abra tenuis, on the northern edge of their intertidal distribution. J. Sea Res. 42:207-220.
Denadai, M. R., A. C. Z. Amaral & A. Turra. 2001. Spatial distribution of molluscs on sandy intertidal substrates with rock fragments in south-eastern Brazil. Estuar. Coast. Shelf Sci. 53:733-743.
Emery, K. O. 1961. A simple method of measuring beach profiles. Limnol. Oceanogr. 6:90-93.
Evans, S. & B. Tallmark. 1977. Growth and biomass of bivalve molluscs on a shallow, sandy bottom in Gullmar Fjord (Sweden). Zoon (Uppsala) 5:33-38.
Faure, G. 1969. Ecologie et croissance de Tellina tenuis da Costa sur les cotes de la Charente-Maritime. Tethvs 1:383-393.
Fiori, S. M. & E. M. Morsan. 2004. Age and individual growth of Mesodesma mactroides (Bivalvia) in the southernmost range of its distribution. J. Mar. Sci. 61:1253-1259.
Folk, R. L. & W. C. Ward. 1957. Brazos River bar, a study in significance of grain size parameters. J. Sediment. Petrol. 27:3-26.
Fuiman, L., J. D. Gage & P. A. Lamont. 1999. Shell morphometry of the deep sea protobranch bivalve Ladella pustulosa in the Rockall Though, North-East Atlantic. J. Mar. Biol. Ass. U.K. 79:661-671.
Gayanilo, F. C., P. Sparre & D. Pauly. 1996. The FAO-ICLARM Stock Assessment Tools (FISAT) user's guide. FAO Computerized information series (Fisheries) No 8. Rome, Italy: FAO.
Gomez, J. & O. Defeo. 1999. Life history of the sandhopper Pseudorchestoidea brasiliensis (Amphipoda) in sandy beaches with contrasting morphodynamics. Mar. Ecol. Prog. Ser. 182:209-220.
Hall, S. J. 1994. Physical disturbance and marine benthic communities: life in unconsolidated sediments. Oceanogr. Mar. Biol. 32:179-239.
Heck, K. L., L. D. Coen & D. M. Wilson. 2002. Growth of northern [Mercenario mercenaria (L.)] and southern [M. campechiensis (Gmelin)] quahogs: influence of seagrasses and latitude. J. Shellfish Res. 21:635-642.
Hibbert, C. J. 1976. Biomass and production of a bivalve community on an intertidal mud-flat. J. Exp. Mar. Biol. Ecol. 25:249-261.
Holme, N. A. 1961. Notes on the mode of life of the Tellinidae (Lamellibranchia). J. Mar. Biol. Ass. U.K. 41:699-703.
Jaramillo, E., H. Contreras & C. Duarte. 2007. Community structure of the macroinfauna inhabiting tidal flats characterized by the presence of different species of burrowing bivalves in Southern Chile. Hydrobiologia 580:85-96.
Lizarralde, Z. I. 2002. Distribucion y abundancia de Tellina petitiana (Bivalvia, Tellinidae) en Cerro Avanzado, Chubut, Argentina. Physis 60:7-14.
Lizarralde, Z. 1. & N. J. Cazzaniga. 2009. Population dynamics and roduction of Tellina petitiana (Bivalvia) on a sandy beach of Patagonia, Argentina. Tlialassas 25:45-57.
Mattos, G. & R. S. Cardoso. 2012. Population dynamics of two suspension-feeding bivalves on a sheltered beach in southeastern Brazil: the venerid Anomalocardia brasiliana and the ungulinid Dioplodonta patagonica. Helgol. Mar. Res. 66:393-400.
McLachlan, A. 1980. The definition of sandy beach in relation to exposure: a simple rating system. S. Afr. J. Sci. 76:137-138.
McLachlan, A. & E. Jaramillo. 1995. Zonation on sandy beaches. Oceanogr. Mar. Biol. Anmt. Rev. 33:305-335.
Michaud, E., G. Desrosiers, F. Mermillod-Blondin, B. Sundby & G. Stora. 2006. The functional group approach to bioturbation: II. The effects of the Macoma balthica community on fluxes of nutrients and dissolved organic carbon across the sediment-water interface. J. Exp. Mar. Biol. Ecol. 337:178-189.
Moura, P., M. B. Gaspar & C. C. Monteiro. 2008. Age determination and growth rate of a Callista chione. Aquat. Biol. 5:97-106.
Navarro, J. M., G. E. Leiva, G. Martinez & C. Aguilera. 2000. Interactive effects of diet and temperature on the scope for growth of the scallop Argopecten purpuratus during reproductive conditioning. J. Exp. Mar. Biol. Ecol. 247:67-83.
Negar, G., G. Zohre & N. Habib. 2008. Population growth of the Tellinid bivalve Tellina foliacea in the Hendijan Coast. Persian Gulf. Pak. J. Biol. Sci. 11:788-792.
Olafsson, E., R. Elmgren & O. Papakosta. 1993. Effects of the deposit-feeding benthic bivalve Macoma balthica on meiobenthos. Mar. Biol. 93:457-462.
Pagnoni, G. O. 1997. Poblamiento de la infauna en la zona intermareal del golfo San Jose (Provincia del Chubut) y su importancia en la alimentacion de aves migradoras. Universidad Nacional de La Plata, La Plata.
Paine, R. T. 1966. Food web complexity and species diversity. Am. Nat. 100:65-75.
Paterson. K. J., M. J. Schreider & K. D. Zimmermman. 2003. Anthropogenic effects on seston quality and quantity and the growth and survival of Sidney rock oyster (Saccostrea glomerata) in two estuaries in NSW, Australia. Aquacult. Res. 221:407-426.
Pauly. D. 1979. Gill size and temperature as governing factors in fish growth: a generalization of von Bertalanffy's growth formula. Berichte aus dem lnstitut fur Meereskunde an der Christian-Albrechts, Universitat Kiel. 63:156.
Pauly, D. & J. L.Munro. 1984. Once more on the comparison of growth in fish and invertebrates. Fishbyte 2:21.
Pauly, D., J. L. Munro & N. Abad. 1995. Comparison of age structure and length-converted catch curves of brown trout Salmo trutta in two French rivers. Fish. Res. 22:197-204.
Petracco, M., R. S. Cardoso & T. N. Corbisier. 2010. Population biology of Excirolana armata (Dana. 1853) (Isopoda, Cirolanidae) on na exposed sandy beach in Southeastern Brazil. Mar. Ecol. (Berl.) 31:330-340.
Ricker, W. E. 1975. Computation and interpretation of biological statistics of fish population. Bull. Fish. Res. Board Can. 191:1-382.
Rios, E. C. 1994. Seashells of Brazil. Editora da Fundacao da Universidade do Rio Grande.
Roseberry, L., B. Vicent & C. Lemaire. 1991. Growth and reproduction of Mya arenaria in their intertidal zone of the Saint Lawrence estuary. Can. J. Zool. 69:724-732.
Selin, N. I. 2010. The growth and life span of bivalve mollusks at the Northeastern Coast of Sakhalin Island. Russ. J. Mar. Biol. 36:258-269.
Souza, J. R. B. 1998. Producao secundaria da macrofauna bentonica da Praia de Atami-PR. PhD thesis, Universidade Federal do Parana, Curitiba. Brazil.
Sprung, M. 1993. Estimating macrobenthic secondary production from body weight and biomass: a field test in a non-boreal intertidal habitat. Mar. Ecol. Prog. Ser. 100:103-109.
Stephen, A. C. 1928. Notes on the biology of Tellina tenuis da Costa. J. Mar. Biol. Ass. U.K. 15:683-702.
Trevallion, A. 1971. Studies on Tellina tenuis Da Costa. 111. Aspects of general biology and energy flow. J. Exp. Mar. Biol. Ecol. 7:95-122.
Underwood, A. J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge, UK: Cambridge University Press, 499 pp.
Urban, H. J. 1994. Adaptations of six infaunal bivalves species of Chile: coexistence resulting from differences in morphology, burrowing depth and substrate preference. Arch. Fisch. Meeresforsch. 42:183-193.
Vakily, J. M. 1992. Determination and comparison of growth in bivalves, with emphasis on the tropics and Thailand. Internacional Center for Living Aquatic Resources Management, Manila, Philippines. ICLARM Tech. Rep. 36:125p.
Vaughn, C. C. & D. E. Spooner. 2006. Unionid mussels influence macroinvertebrate assemblage structure in streams. J. N. Am. Bent hoi. Soc. 25:691-700.
Warwick, R. M., C. L. George & J. R. Davies. 1978. Annual macrofauna production in a Venus community. Estuar. Coast. Mar. Sci. 7:215-241.
Wilson, J. G. 1997. Long-term changes in density, population structure and growth rate of Tellina tenuis from Dublin Bay, Ireland. Oceanol. Acta 20:267-274.
Zar, J. H. 1999. Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall.
Zwarts, L. & J. H. Wanink. 1993. How the food supply harvestable by waders in the Wadden Sea depends on the variation in energy density, body weight, biomass. burying depth and behaviour of tidal-flat invertebrates. Neth. J. Sea Res. 31:441-476.
RICARDO S. CARDOSO, (1) * LUDMILA B. GALHARDO (1) AND TATIANA M. B. CABRINI (1,2)
(1) Laboratorio de Ecologia Marinha, Departamento Ecologia e Recursos Marinhos, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Avenida Pasteur, 458, Sala 407, URCA, Rio de Janeiro, CEP 22290-240, Brazil; (2) Programa de Pos-Graduacao em Ecologia, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, CEP 21941-902, Brazil
* Corresponding author. E-mail: rcardoso@!unirio.br
TABLE 1. Growth parameters estimated by nonlinear fitting of the von Bertalanffv growth function for Tellina lineata and Tellina versicolor. Tellina lineata Parameters Mean ([+ or -] SE) P [L.sub.[infinity]] (mm) 32.33 ([+ or -] 1.62) 0.0000 K[ year 0.54 ([+ or -] 0.06) 0.0000 C 0.41 ([+ or -] 0.18) 0.0028 WP 1.00 ([+ or -] 0.06) 0.0000 [t.sub.o]/year -0.31 ([+ or -] 0.06) 0.0001 [PHI]' 2.75 Largest (mm) 31.28 [t.sub.max]/year 3.15 Tellina versicolor Parameters Mean ([+ or -] SE) P [L.sub.[infinity]] (mm) 35.49 ([+ or -] 1.15) 0.0000 K[ year 0.83 ([+ or -] 0.07) 0.0000 C 0.23 ([+ or -] 0.09) 0.0034 WP 0.70 ([+ or -] 0.07) 0.0001 [t.sub.o]/year -0.03 ([+ or -] 0.02) 0.0050 [PHI]' 3.02 Largest (mm) 32.37 [t.sub.max]/year 2.86 TABLE 2. Mortality estimates (Z) for Tellina lineata (n = 20) and Tellina versicolor (n = 9). Tellina lineata Tellina versicolor Parameters Mean ([+ or -] SE) P Mean ([+ or -] SE) P g 8.86 ([+ or -] 0.15) 0.000 17.18 ([+ or -] 0.20) 0.000 Zj year 1.96 ([+ or -] 0.26) 0.000 6.37 ([+ or -] 0.18) 0.000 [R.sup.2] 0.99 0.000 0.92 0.000 n 20 9 TABLE 3. Latitudinal variation in growth performance in species of the genus Tellina. [L.sub.[infinity]] Species K/year (mm) [PHI]' Tellina lineata 0.54 32.33 2.75 Tellina versicolor 0.83 35.49 3.02 Tellina petitiana 0.37 50.51 2.97 Tellina foliacea 1.20 7.70 1.85 Tellina tenuis 0.66 23.24 2.66 Tellina tenuis 0.18 21.10 1.90 Tellina tenuis 0.43 15.50 2.01 Tellina tenuis 0.43 16.80 2.08 Tellina tenuis 0.31 19.70 2.08 Tellina tenuis 0.38 22.40 2.28 Tellina lutea 0.10 76.3 2.77 Species Latitude Source Tellina lineata 22[degrees]57' S Present study Tellina versicolor 22[degrees]57' S Present study Tellina petitiana 42[degrees]46' S Lizaralde and Cazzaniga (2009) Tellina foliacea 49[degrees]15' S Negar et al. (2008) Tellina tenuis 52[degrees]56' N Dekker and Beukema (1999) Tellina tenuis 58[degrees]15' N Evans and Tallmark (1977) Tellina tenuis 55[degrees]45' N Stephen (1928) Tellina tenuis 55[degrees]46' N Barnett and Watson (1986) Tellina tenuis 53[degrees]18' N Wilson (1997) Tellina tenuis 46[degrees]09' N Faure (1969) Tellina lutea 53[degrees]00' N Selin (2010) K, curvature parameter; [L.sub.[infinity]] asymptotic length; [PHI]', growth performance index.
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|Author:||Cardoso, Ricardo S.; Galhardo, Ludmila B.; Cabrini, Tatiana M.B.|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2015|
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