INTRODUCTION
The gastropod Melampus coffeus (Linnaeus, 1758) belongs to a primitive group of mainly marine pulmonate molluscs commonly found at the upper levels of the intertidal zone of mangroves in the Atlantic Ocean (Martins, Reference Martins and Taylor1996a, Reference Martinsb). The regulation of snail populations in mangroves or tropical estuaries is subjected to processes that are density dependent and independent such as competition and predation, and temperature, rainfall, and salinity, respectively (Roach & Lim, Reference Roach and Lim2000; Maia et al., Reference Maia, Rocha-Barreira and Coutinho2012). In the case of Melampus, predation and food competition seem to be the main density-dependent regulatory factors (Joyce & Weisberg, Reference Joyce and Weisberg1986; Lee & Silliman, Reference Lee and Silliman2006), whereas seasonal fluctuations in water salinity and temperature, which can lead to significant mortality of young animals and eggs, are the most important density-independent factors (Apley, Reference Apley1970; Price, Reference Price1980; McMahon & Russell-Hunter, Reference Mcmahon and Russell–Hunter1981; Maia et al., Reference Maia, Rocha-Barreira and Coutinho2012).
Melampus species present high densities in areas with high salinities (Price, Reference Price1980; McMahon & Russell-Hunter, Reference Mcmahon and Russell–Hunter1981; Fell & Williams, Reference Fell and Williams1985; Burnham & Fell, Reference Burnham and Fell1989). However, observed variation in the densities of M. coffeus did not corroborate the patterns recorded for other species in Melampus; instead, high densities were detected in areas with low salinities (Maia & Coutinho, Reference Maia and Coutinho2013). Other studies show a relationship between the population dynamics of the Ellobiidae family and tidal levels. Some species in Melampus can display an elaborate succession of temporal adjustments in their reproductive and embryonic development, which correspond to submersion during spring tides (Apley, Reference Apley1970; Russell-Hunter et al., Reference Russell-Hunter, Apley and Hunter1972; Spelke et al., Reference Spelke, Fell and Helvenston1995). Maia et al. (Reference Maia, Rocha-Barreira and Coutinho2012) show that, in Melampus coffeus, no reproductive activity occurs during the dry season, after which, increasing rainfall and reduced salinity result in very dense populations of predominantly small individuals.
As a macro-detritivore mollusc, M. coffeus plays an important role in energy transfer in neotropical mangroves and its distribution and abundance appear to be conditioned to the presence of trees in the mangrove, which would represent both a condition and a resource (Joyce & Weisberg, Reference Joyce and Weisberg1986; Lee & Silliman, Reference Lee and Silliman2006). This snail is an air breather and, therefore, migrates to the upper parts of the mangrove vegetation during high tides to avoid drowning (Maia & Tanaka, Reference Maia and Tanaka2007). However, M. coffeus feeds on decaying leaf litter on the sediment surface (Proffitt et al., Reference Proffitt, Johns, Cochrane, Devlin, Reynolds, Payne, Jeppesen, Peel and Linden1993; Proffitt & Devlin, Reference Proffitt and Devlin2005). Maia & Coutinho (Reference Maia and Coutinho2013) indicate congruent distribution patterns of mangrove trees and M. coffeus on the north-eastern Brazilian coast, that is, the greatest availability of food resources and shelter, provided by the mangrove vegetation, correlated with the greatest snail abundance. This result indicates that M. coffeus may be a potential ecological indicator of mangrove areas degraded by deforestation.
The biology and ecology of Ellobiidae is described in studies such as those on larval development, life history and distribution patterns (Apley, Reference Apley1970; Russell-Hunter et al., Reference Russell-Hunter, Apley and Hunter1972, Spelke et al., Reference Spelke, Fell and Helvenston1995). However, little is known about the biology and ecology of M. coffeus (Proffitt et al., Reference Proffitt, Johns, Cochrane, Devlin, Reynolds, Payne, Jeppesen, Peel and Linden1993; Proffitt & Devlin, Reference Proffitt and Devlin2005). The use of this species as a bioindicator requires knowledge not only of species or population characteristics such as specimen size, distribution and density, but also knowledge of how environmental conditions in mangrove estuaries (salinity, vegetation cover) affect M. coffeus over time.
Thus, the goal of this study was to analyse the spatial and temporal distribution of Melampus coffeus in two mangroves, with different salinities on the north-eastern coast of Brazil (Ceará State). In addition, population dynamics parameters such as survival, population density and shell size (shell height – ventral margin of aperture to apex) were correlated with environmental variables (temperature, salinity and relative humidity). Our working hypothesis was that population density and individual shell morphology are influenced by salinity (personal observation). Thus, we expected decreases in population density and increases in the shell size in the season with high salinities.
MATERIALS AND METHODS
Study area
In order to evaluate the spatial and temporal distribution of M. coffeus and the variables that are correlated with its population dynamics, we selected two mangrove forests with different salinity levels and a similar vegetated area in the county of Acaraú, Ceará State, Brazil. The first is located in the middle section of the Acaraú estuary (Acaraú River mangrove), a less saline area with fluvial influence (02°50′59″S, 40°07′41″W) with seasonal fluctuations in water salinity between 0 and 44 ppt. The second mangrove forest is located on the Arpoeiras Beach (Arpoeiras Beach mangrove), a more saline environment due to its proximity to the sea (02°50′17″S 40°04′56″W), with salinities between 10 and 51 ppt.
The coastal zone of Ceará is included in segment IV of the Brazilian coastal division proposed by Schaeffer-Novelli et al. (Reference Schaeffer-Novelli, Molero, Adaime and Camargo1990). Rainfall is low in this area leading to an accumulation of salt due to high rates of evaporation in the estuarine areas, whereas the temperature remains constant throughout the year. In both study areas, the mangrove species Rhizophora mangle Linnaeus (Rhizophoraceae) and Avicennia germinans (Linnaeus) Stearn were equally dominant and there was no evidence of a clear zonation pattern (Maia & Coutinho, Reference Maia and Coutinho2012).
Methodology
FIELD PROCEDURES
Each month between March 2007 and February 2009, five plots (1 m2 each) were randomly selected in each mangrove forest. All specimens found within each plot were counted and measured for shell height, width and aperture height with a caliper (precision = 0.1 mm) and returned to their habitats. The monthly average population density was calculated for each mangrove forest. Water, air and sediment temperatures, and relative humidity were measured with a thermo-hygrometer; salinity was measured with a refractometer. Rainfall data (monthly accumulated total – mm) were obtained from FUNCEME – Fundação Cearense de Meteorologia e Recursos Hídricos (http://www.funceme.br/). Sampling was conducted during daylight spring tides; tides were identified according to the tide tables published on the website by the DHN – Diretoria de Hidrografia e Navegação da Marinha do Brasil (http://www.dhn.mar.mil.br/).
The two-way Analysis of Variance test was used to investigate differences in mean density or shell size (height, width and aperture height) among the different sampling months and study areas (Underwood, Reference Underwood1997). Tukey's multiple comparison test was used when differences were observed.
The Spearman correlation analysis was used to correlate density and shell height with environmental parameters (air, water and sediment temperature, humidity, salinity and rainfall). Other size-variables (width and aperture height) were not used in this analysis because they were highly correlated (R ≥ 0.95). Correlation analyses were conducted between abiotic variables in the studied mangroves.
Size-frequency distribution of M. coffeus (shell height) was determined according to Sturges’ formula: Vi = A/K; where: Vi = class interval, A = amplitude of the (Lt) variable (Max–Min), K = number of classes calculated by: 1 + 3.32 log n where ‘n’ is the total number of individuals. This calculation resulted in an estimated size class interval of 2 mm for the Arpoeiras Beach mangrove and 1.5 mm for the Acaraú River mangrove. These data were used for the determination of population parameters such as growth, recruitment and survival. All results are presented as mean ± standard deviation (SD).
Experiments
A series of experiments were conducted to test the effects of salinity on M. coffeus population density and individual size distribution.
EXPERIMENT I – EFFECTS OF SALINITY ON M. COFFEUS
Eight M. coffeus specimens with similar shell sizes (height = 15 ± 1 mm, and average weight = 0.95427 ± 0.1514 g) were collected at both study areas. These animals were taken to the laboratory, placed in trays (302 × 208 × 63 mm) at a density similar to that found in their natural habitat and sprayed with water at different salinities: Treatment # 1 = 0 ppt, Treatment # 2 = 32 ppt, and Treatment # 3 = 48 ppt. Sediment from the source mangrove and yellow mangrove leaves were added to the trays to provide abundant food. The trays were watered daily for 2 months using the salinity concentrations of each treatment. Shell height (mm) was measured and individual snails were weighed weekly (precision = 0.0001 g).
The effects of salinity on the survival of M. coffeus (%) were assessed through a two-way Analysis of Variance (Salinity treatments and Time in weeks), where Treatment # 1 = 0 ppt, Treatment # 2 = 32 ppt, and Treatment # 3 = 48 ppt (salinity), were applied to each study site. Differences in survival between both study areas were assessed through a one-way Analysis of Variance (Underwood, Reference Underwood1997). Shell growth (final height – initial height) and loss of body weight (final weight – initial weight) were assessed through a two-way Analysis of Variance among the treatments and between the study areas. Tukey's multiple comparison test was used when significant differences were observed.
EXPERIMENT II – EFFECTS OF SALINITY ON M. COFFEUS OF DIFFERENT SIZES
This experiment was performed under the same conditions used in Experiment 1 except using small snails (shell height = 12 ± 1 mm and average weight = 0.46765 ± 0.1607 g) and large snails (shell height 20 ± 1 mm and average weight = 1.85177 ± 0.25335 g) to evaluate the influence of salinity on different size classes.
The effects of salinity on the survival of M. coffeus was assessed through a two-way Analysis of Variance (Salinity treatments and Time in weeks) for each size class (small and large snails). Differences in survival between both size classes were assessed through a one-way Analysis of Variance (Underwood, Reference Underwood1997). Shell growth (final height – initial height) and loss of body weight (final weight – initial weight) was assessed through a two-way Analysis of Variance (Salinity treatments and Time in weeks). Tukey's multiple comparison test was used when significant differences were observed.
EXPERIMENT III – TRANSPLANT
Additionally, an experimental transplant was conducted over 3 months to evaluate the effects of different salinity concentrations on shell height in their natural environment. Thirty individuals randomly collected in the Acaraú River mangrove were transferred to the Arpoeiras Beach mangrove, whereas 30 specimens collected in Arpoeiras Beach mangrove were transferred to the Acaraú River mangrove. Because M. coffeus migrates vertically through the course of a day, feeding on the sediment during low tides and climbing up trees during high tides (Proffitt & Devlin, Reference Proffitt and Devlin2005; Maia & Tanaka, Reference Maia and Tanaka2007), the animals were kept in suitable containers, measuring 1 m in height and 25 cm2, with open tops to allow leaves to enter. These containers, three in each area, were built with a nylon screen on a wooden frame of mangrove branches. All animals were numbered with enamel paint, and had their shell height (mm) measured once a month. A paired Student's t-test was used to evaluate shell growth in the transplanted individuals.
RESULTS
Environmental variables in the study areas
The temperature data from air, water and sediment were similar in both mangrove forests throughout the study. However, the relative air humidity varied in both study areas, between different months, with a 27% minimum humidity registered in the Acaraú River mangrove in October 2008, and an 82% maximum humidity recorded in Arpoeiras Beach mangrove in March 2007. The total accumulated rainfall ranged between 0 and 477.5 mm during this study (recorded in April 2008). According to data provided by FUNCEME, three rainy periods occurred: from March to April 2007, from January to May 2008, and from January to February 2009. Two dry periods were observed from May to December 2007 and from June to December 2008. The analysis indicated a significant correlation between salinity and rainfall in both Arpoeiras Beach (r = −0.890; P < 0.05) and Acarau River (r = −0.825, P < 0.05).
Spatial and temporal distribution of M. coffeus
Significant differences in the population density of M. coffeus were observed among different months at Arpoeiras Beach mangrove and Acaraú River mangrove (Table 1) (Figure 1A). Variation in density between the studied months was similar in both study areas. According to Tukey's test, the population density of M. coffeus in July 2007 was significantly different from densities in January and November 2008 in the Arpoeiras Beach mangrove; the density in March 2007 was different from densities in October 2007, and in October and December 2008, in the Acaraú River mangrove. All other months were statistically similar. Thus, the sampled mangroves forest tend to present lower densities in months with low rainfall and high salinity. No significant differences in density occurred between the study areas (Table 1); M. coffeus densities were similar at both study areas (Figure 1A).
(A) Density (individual m−², mean ± SD) and (B) Shell height (mm) of M. coffeus sampled between March 2007 and January 2009 at the Arpoeiras Beach and Acaraú mangrove forests, Ceará state, Brazil.
Results of two-way Analysis of Variance comparing density and shell size (height, width and aperture height, mm) of Melampus coffeus in the sampling months (May 2007 – January 2009) at the Arpoeiras Beach and Acaraú River mangrove forests, Ceará state, Brazil.
nsNo significant variation; *Significant variation (P < 0.05).
The size of M. coffeus (Figure 1B) was significantly different among months at study areas, considering shell height, width and aperture height (Table 1). At Arpoeiras Beach mangrove, according to Tukey's multiple comparison test, height, width and aperture height were similar in: (1) March, April, June and July 2007, July, August, September, October, November and December 2008, and January 2009; (2) May, July, August, October, November and December 2007; (3) September 2007, March and June 2008; and (4) January, February and April 2008. At Acaraú River mangrove, according to Tukey's multiple comparison test, the following groups of months were similar among themselves and distinct from the others: (1) March 2007, November 2008 and February 2009; and (2) July, August, September and October 2007.
Temporal patterns in shell size at the Arpoeiras Beach mangrove and the Acaraú River mangrove are similar (Figure 1B). In periods of drought, M. coffeus populations tended to have a low density and were composed of large snails. When rainfall increased and salinity levels fell, the populations became denser and were dominated by small individuals. Even though the change in shell size over months was similar in both study areas, the average shell size in the Arpoeiras Beach and in the Acaraú River mangroves was significantly different (Table 1). Thus, we observed that animals collected on the Arpoeiras Beach mangrove had significantly larger shells than those sampled in the Acaraú River mangrove (Figure 1B).
The results, in both study areas, of the correlation analysis between environmental variables (temperature, rainfall, salinity and relative humidity), densities and shell height of M. coffeus confirmed the patterns observed in the graphs, i.e. significant correlation between these factors and salinity (P < 0.05) (Table 2). At Arpoeiras Beach and Acaraú River mangroves, the analysis indicates a positive correlation between M. coffeus densities and rainfall (Arpoeiras Beach mangrove: R = 0.583; Acaraú River mangrove: R = 0.617); and a negative correlation with salinity (Arpoeiras Beach mangrove: R =−0.584; Acaraú River mangrove: R = −0.532). The shell height of M. coffeus were correlated with the same factors at Acaraú River mangrove (Shell height and salinity: R = 0.665; Shell height and rainfall: R = −0.595).
Correlations between Melampus coffeus density, shell height and environmental variables at the Arpoeiras Beach and Acaraú River mangrove forests, Ceará state, Brazil.
nsNo significant variation; *Significant variation (df: 22; P < 0.05).
SIZE-FREQUENCY DISTRIBUTION OF M. COFFEUS
Melampus coffeus shell height frequency distributions at Arpoeiras Beach mangrove, indicate that individuals smaller than 9.6 mm were more frequent during the rainy season and therefore, more size classes were represented in those months (from January to June). However, a few animals reached sizes less than 7.6 mm. In the dry months, the number of juveniles was lower and the number of adults increased in the population, thus, a reduction in the number of size classes was observed. Intermediate sized individuals were observed throughout the period, with those ranging from 13.6 to 21.6 mm being most frequent. Individuals larger than 23.6 mm were observed only in September 2007, and February, March and October 2008. Only one individual was found in each of these months.
Compared with the Arpoeiras Beach mangrove, the Acaraú River mangrove had smaller individuals, with the first size class ranging from 4.9 to 6.4 mm. Few animals reached sizes less than 6.4 mm or larger than 21.4 mm. Intermediate size classes, ranging from 10.9 to 18.4 mm, were more frequent than other classes. In general, the size distribution patterns in the different months were similar in both habitats with larger individuals in the dry season and smaller individuals in the rainy season when salinity decreases.
Salinity experiment
EXPERIMENT I – EFFECTS OF SALINITY ON M. COFFEUS
The survival of individuals (shell height = 15 ± 1 mm) collected at Arpoeiras Beach mangrove and subjected to treatments with different salinities varied over time (Table 3). No deaths were observed until the fourth week in any treatment, after which survival began to decrease in the higher salinity treatment after 4 weeks. In intermediate salinity conditions, only one individual died in the eighth week; all animals survived at zero salinity (Table 4). Moreover, significant differences in survival rates were observed in animals collected in the Acaraú River mangrove subjected to treatments with different salinities over time (Table 3). In this case, deaths were seen in all treatments after the sixth week; the lowest rates of survival were observed in the 48 ppt salinity concentration treatment (Table 4). Nevertheless, no significant differences in survival rates were observed between the two study areas (F 1,46 = 1.1329, P = 0.2927).
Results of two-way Analysis of Variance comparing survival (%) of Melampus coffeus in salinity treatments (0, 32, 48) over time (weeks) between Arpoeiras Beach and Acaraú River mangrove forests (Ceará state, Brazil) and between small (shell height = 12 ± 1 mm) and large (shell height = 20 ± 1 mm) snails.
nsNo significant variation; *Significant variation (P < 0.05).
Survival (%) of small (shell height = 12 ± 1 mm) and large (shell height = 20 ± 1 mm) Melampus coffeus from mangrove forests at Arpoeiras Beach and Acaraú River, Ceará state, Brazil, subjected to different salinities (0, 32, 48) over 8 weeks.
No significant differences were observed in shell growth in different salinity treatments (Table 5) when comparing individuals from the Arpoeiras Beach mangrove and the Acaraú River mangrove. However, these same animals showed a significant treatment- and site-dependent weight loss (Table 5). Weight loss was lower in snails collected in the Acaraú River mangrove and greatest in animals subjected to Treatment #3 (salinity = 48 ppt) (Figure 2A). Weight loss was similar in the other two treatments (salinity = 0 and 32 ppt) (Tukey's test, Figure 2A).
Weight loss (g, mean ± SD) of Melampus coffeus in salinity treatments (0, 32, 48) between (A) Arpoeiras Beach and Acaraú River mangrove forests, Ceará state, Brazil and (B) between small (12 ± 1 mm) and large (20 ± 1 mm) snails.
Results of two-way Analysis of Variance comparing shell growth (mm) and weight loss (g) of Melampus coffeus in salinity treatments (0, 32, 48) at Arpoeiras Beach and Acaraú River mangrove forests, Ceará state, Brazil and between small (shell height = 12 ± 1 mm) and large (shell height 20 ± 1 mm) snails.
nsNo significant variation; *Significant variation (P < 0.05).
EXPERIMENT II – EFFECTS OF SALINITY ON M. COFFEUS OF DIFFERENT SIZES
The second experiment using different size classes of M. coffeus lasted 6 weeks because all animals were dead after this time. There were no significant differences in survival rates between small (shell size = 12 ± 1 mm) and large (20 ± 1 mm) M. coffeus snails among treatments or over time (Table 3). No significant differences in survival were observed between size classes (F 1,34 = 0.05356, P = 0.81836). No deaths were recorded in any of the size classes in Treatment #1 (Table 4). No deaths occurred until the third week in the other two treatments. Treatment #3 had neither large- nor small-sized survivors in weeks five and six (Table 4).
Shell growth was similar between large and small individuals in this treatment (Table 5). However, the same animals presented significant weight loss differences between different treatments (Table 5). Weight loss was greater in large animals than in small ones, especially in the intermediate salinity treatment (Tukey's test, Figure 2B).
EXPERIMENT III – TRANSPLANT
The animals collected in the Acaraú River and transplanted to the Arpoeiras Beach had an average shell height of 15.5 mm ± 1.7, whereas the snails sampled at the beach and taken to the estuary had an average shell height of 14.9 mm ± 1.4. It was not possible to consider all the snails used in the experiment in the statistical analysis because some individuals were lost during the 3 months of experimentation. Significant differences were observed in the average growth of these animals in the experimental time at both study areas. Animals collected from the Arpoeiras Beach mangrove and transplanted to the Acaraú River grew 1.05 mm ± 0.6 from January to February, and 1.71 mm ± 0.8, from February to March (t = −5.49389; gl = 22; P = 0.00016). The animals taken from the Acaraú River mangrove and transplanted to the Arpoeiras Beach mangrove grew 0.78 mm ± 0.76 from the first to the second month, and 1.2 mm ± 0.9 from the second to the third month (t = −6.14707; gl = 15; P = 0.000019). However, the growth rate of individuals from the Arpoeiras Beach mangrove and transferred to Acaraú River mangrove did not differ in comparison to those from the Acaraú River mangrove and transferred to the Arpoeiras Beach mangrove (t = 1.6302; gl = 37; P = 0.111).
DISCUSSION
Salinity and rainfall appear to be associated with the density of M. coffeus populations in both study areas and their shell size at Arpoeiras Beach mangrove. Populations with lower density and composed primarily of large adults occurred in the dry season at both study areas. During the rainy season, when salinity decreases, the populations were denser and small individuals predominated. Our results agree with those of other studies that indicate that salinity is one of the main factors determining the distribution and abundance of species in the Melampus genus, which is found at higher densities in areas of high salinity in estuaries (Kerwin, Reference Kerwin1972; Fell & Williams, Reference Fell and Williams1985; Burnham & Fell, Reference Burnham and Fell1989; Martins, Reference Martins2001; Maia et al., Reference Maia, Rocha-Barreira and Coutinho2012).
We found that seasonal variation in density and shell size was similar in both study areas indicating that temporal variation appears more relevant. However, in general, M. coffeus shell height was greater in the Arpoeiras Beach mangrove than in the Acaraú River mangrove. Shell size differences in Melampus snails and other pulmonate molluscs from neighbouring regions have been reported in other studies (Fell et al., Reference Fell, Murphy, Peck and Recchia1991; Spelke et al., Reference Spelke, Fell and Helvenston1995; Tablado & Gappa, Reference Tablado and Gappa2001), suggesting that the differences observed could be the result of quantitative and qualitative variation in food resources at the two study areas in the present study, although there is no difference in the vegetation type and tree density in both mangroves studied (Maia & Coutinho, Reference Maia and Coutinho2012). Melampus coffeus is a macrodetritivore that feeds on plant debris, preferably mangrove leaves (Proffitt et al., Reference Proffitt, Johns, Cochrane, Devlin, Reynolds, Payne, Jeppesen, Peel and Linden1993; Proffitt & Devlin, Reference Proffitt and Devlin2005). This feeding habit makes the vegetation an important component in the population dynamics of this species. Moreover, salinity stress, in synergy with tides, causes the loss of leaves, which affects flows of carbon and nutrients in estuarine mangroves exposing these systems to potential losses by leaching and transport (Lugo et al., Reference Lugo, Brown and Brinson1988). Thus, net productivity, litter production and export of organic matter are stronger in non-estuarine mangroves, which may lead to differences in food resources available to M. coffeus (Maia & Coutinho, Reference Maia and Coutinho2013). and consequently larger body sizes at Arpoeiras Beach, where the food may be more abundant.
In the present study, the growth rate of individuals from the Arpoeiras Beach mangrove that were transferred to the Acaraú River mangrove did not differ in comparison to those from the Acaraú River mangrove transferred to the Arpoeiras Beach mangrove. However, M. coffeus snails appeared to grow more slowly when transplanted from the Acaraú River mangrove to the Arpoeiras Beach mangrove, thus, environmental conditions in the animals’ native area may prevail over others. Field experiments involving reciprocal transplant discriminating between phenotypic and genotypic variability that may lead to morphological differences have been suggested (Tablado & Gappa, Reference Tablado and Gappa2001). These authors proposed that morphometric differences observed in the different habitats are the result of differential growth rates in response to environmental pressures as well as food availability.
The analysis of size-frequency distribution of M. coffeus showed there were few very small individuals present in both mangroves. The existence of microhabitats that provide refuge from predation, and the limiting conditions of the supralittoral zone may cause high mortality rates in young individuals (Tablado & Gappa, Reference Tablado and Gappa2001). Microhabitats were not sampled in this study. However, we observed that during low tides, when the snails are found on the mangrove sediment, some individuals occupied more humid areas than dry ones, such as mangrove roots encrusted with oysters, crab burrows, the base of low vegetation, or small depressions on tree root surfaces. This pattern has also been reported for other mangrove gastropod species such as Bembicium auratum Quoy & Gaimard, 1834 (Underwood & Barrett, Reference Underwood and Barrett1990), Salinator solida Martens 1878 (Roach & Lim, Reference Roach and Lim2000) and Littoraria angulifera (Tanaka & Maia, Reference Tanaka and Maia2006).
Herjanto & Thomas (Reference Thomas1995) have also observed seasonal differences in distinct cohorts of M. coffeus in Bermuda mangroves where the authors report that summer populations were dominated by juveniles indicating that recruitment occurred in spring or early summer. Additionally, other pulmonate gastropods exhibit temporal patterns in their life cycle and population dynamics. Staikou et al. (Reference Staikou, Lazaridou-Dimitriadou and Pana1990) and Staikou (Reference Staikou1998) observed increased growth rates in Bradybaena fruticum Müller, 1774 and Cepaea vindobonensis Férussac, 1821 during the spring and early summer, respectively, with their reproductive period occurring in early summer. These authors suggested that the observed pattern might be due to more favourable conditions during these periods. In the present study, larger sized shells were clearly observed during drier periods. We believe that the combination of low rainfall and high salinity during the dry season represents a limiting factor to M. coffeus in the Acaraú region study area, and therefore, adults in this area invest in growth and interrupt their reproductive cycle, whereas most young individuals and those belonging to larger size classes, possibly the oldest, cannot withstand a prolonged dry period. The results obtained in the experiments confirm this assumption. Animals at extreme sizes (small and large) subjected to different salinity treatments over a moderate period showed higher mortality rates than individuals of intermediate size.
Moreover, small individuals have a large surface area to volume ratio and may lose water rapidly in the dry season whereas larger (older) individuals may have difficulty regulating water balance (McMahon & Russell–Hunter, Reference Mcmahon and Russell–Hunter1981; Iacarella & Helmuth, Reference Iacarella and Helmuth2011, Reference Iacarella and Helmuth2012) Thus, younger larger individuals may have higher survival in the dry season due to a healthy physiology and lower rates of water loss through evaporation (Britton, Reference Britton1992; McMahon, Reference Mcmahon2001; Iacarella & Helmuth, Reference Iacarella and Helmuth2011, Reference Iacarella and Helmuth2012).
Further studies are necessary to elucidate the processes involved in this gastropod's life cycle and factors that might influence the population dynamics of this species. However, the results from this study may contribute to the use of Melampus coffeus, an important macro-detritivore gastropod, as an ecological indicator of mangrove areas undergoing degradation.
ACKNOWLEDGEMENTS
We are grateful to J.N. Maia and P.S. Ribeiro for field assistance, and to A. Bismark Vasconcelos for the English style review.
FINANCIAL SUPPORT
The Universidade Federal Fluminense and the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq provided a scholarship to the first author.
