Introduction

Many aspects of organismal ecology may be explained by population processes and structure such as size-frequency distribution, sexual maturity, reproductive period, recruitment, longevity, mortality, and sex ratio. This knowledge is crucial in the study of local and global ecological processes, to propose trends on population features, and to support studies on species conservation (Bauer 1992; Almeida et al. 2012a; Ardovine 2014). Understanding the population structure of decapod crustaceans of economic interest is necessary for the development of conservation strategies, guidelines, and regulations to control their consumption (Almeida et al. 2012a; Hirose et al. 2015; Pinheiro and Almeida 2015; Santos et al. 2016).

Despite the vast diversity and wide geographical distribution of decapod crustaceans (Martin and Davis 2001), common trends in the population structure can be clearly observed in several species. Populations are shaped and/or affected by abiotic factors that change with latitude, and after considering these factors, generalizations can be proposed (Bauer 1989, 1992; Cobo and Fransozo 2003; Castilho et al. 2007; Lardies et al. 2008). Populations from temperate regions tend to have larger individuals with late sexual maturity and short and seasonal reproductive period and recruitment (Bauer 1992; Litulo 2005). On the contrary, subtropical and tropical populations have smaller individuals with early sexual maturity and continuous reproductive period and recruitment (Bauer 1992; Litulo 2005; Almeida et al. 2012a; Hirose et al. 2012).

Sex ratio is another important aspect that might portray the behavior of species (e.g., sexual behavior or mating system), as well as the sexual system (gonochorism and hermaphroditism). The composition and population dynamics of a species might vary over time along the life cycle (Wenner 1972; Correa and Thiel 2003; Terossi and Mantelatto 2010). Wenner (1972) analyzed the sex ratio of some marine crustaceans according to size and proposed four patterns: (1) Standard: the sex ratio is proportional in most size classes, but it is male-biased in the largest size classes; (2) Reversal: represented by a sigmoid curve, the proportion of the sexes varies sharply as individuals grow; it is mostly observed in populations with sexual reversion; (3) Intermediate: juveniles are incorporated into the population in different proportions, resulting in a sex ratio different from 1:1; and (4) Anomalous: the 1:1 ratio is maintained in smaller size classes; there is a deviation towards females in the intermediate classes, and towards males in the larger classes. Terossi and Mantelatto (2010) proposed the “Predominance” pattern, when studying Hippolyte obliquimanus from São Paulo (Brazil), in which females are predominant in almost all size classes (female-biased).

The genus Alpheus comprises a rich and diverse group known as snapping shrimps, with more than 300 species described (De Grave and Fransen 2011; Almeida et al. 2014). The genus is widely distributed in tropical and subtropical marine and estuarine habitats, occurring from the intertidal to the deep sea (Chace 1988; Anker et al. 2006). Basic studies on population biology of Alpheus are still scarce maybe due to its complicated taxonomy, which includes the presence of species complexes (Mathews and Anker 2009). These shrimps are ecologically cryptic (see Felder 1982), which makes monthly samplings difficult and contributes to the lack of information about the life-history of most species.

Alpheus estuariensis is a burrowing shrimp from the Western Atlantic, found from the eastern coast of Florida (USA) down to Santa Catarina, southern Brazil (Christoffersen 1984; Almeida and Mantelatto 2013). They are commonly found in burrows excavated in muddy sediments of estuaries, under rocks and debris, as well as in rotting wood, from the intertidal to 22 m deep (Christoffersen 1984; Almeida et al. 2012b). In these environments, A. estuariensis build deep and complex burrows which are also used as shelter by other crustaceans with which they are associated (Costa-Souza et al. 2014; Oliveira et al. 2015). They are functionally bioturbators, according to Berke’s classification (Berke 2010).

The breeding biology and heterosexual pairing of A. estuariensis in an intertidal mudflat in northeastern Brazil was studied by Costa-Souza et al. (2014). Similar to other tropical species, the population showed continuous breeding, and the proportion of ovigerous females varied along the year. However, the fecundity was lower than in other species of the genus. Approximately 20% of the sampled animals were found in heterosexual pairs of similar-sized individuals, suggesting the occurrence of monogamy. However, despite the wide latitudinal distribution of A. estuariensis, studies on its population structure have not been published until the present moment.

In this study the population structure of A. estuariensis was analyzed and compared with other tropical caridean shrimp populations. We analyzed the size frequency distribution, recruitment, sex ratio, growth, longevity, distribution, and density of shrimps according to sediment type (granulometry). To conclude, we evaluated whether A. estuariensis is well established in the study area, a mangrove remnant situated in an urbanized area.

Materials and Methods

Study Area and Sampling Protocol

The Pontal Bay (14°48′31.1″ S 39°02′08.3″ W), located in Ilhéus, Bahia state, northeastern Brazil, is an estuary formed by the rivers Cachoeira, Fundão, and Santana (Fig. 1). The estuary is formed by muddy areas with mangroves and sandbanks in the lower part of the alluvial plain (Nacif et al. 2003). The bay is surrounded by the city and it is affected by domestic sewage discharge (see Almeida et al. 2006; Souza et al. 2009). The study area comprised an intertidal plain of muddy sediments and sparse rocks that are exposed during the spring tide. Samplings were taken monthly from September 2011 to October 2012 during spring low tide. No samplings occured in October 2012 due to heavy rainfall.

Fig. 1
figure 1

Location of the study area in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image

At the sampling site, three 30 m long transects (T1, T2, and T3) were arranged parallel to the shoreline. The distance between transects was 24 m between T1 and T2 and 12 m between T2 and T3. Between T2 and T3 there was a concave area that was always flooded, even at low tide. In order to avoid placing the transect in such conditions, T3 had to be placed 24 m away from T2. Ten sampling units of 1 m2 were randomly selected from each transect every month, totaling 30 sampling units per month.

Individuals of A. estuariensis were captured from the sampling units using a 50 mm diameter pump made of a PVC pipe. This pump was used as a corer. All burrow openings within the units were pumped. The number of times that the pump was used in each opening was not standardized. The sediment taken with the pump was sieved using a 1.8 mm fine mesh. Individuals were sorted and placed into plastic bottles filled with water from the sampling site and transported to the laboratory for further analyses. Sediment samples were also taken from each transect.

Laboratory Measurements

In the laboratory, each individual was anesthetized on ice and preserved in 70% ethanol. Males were identified based on the presence of the appendix masculina on the endopod of the second pair of pleopods (Bauer 2004). Females were identified based on the absence of the appendix masculina and/or presence of embryos underneath the abdomen (Bauer 2004). Individuals smaller than 5.9 mm of carapace length (smallest breeding female) were considered juveniles (see Costa-Souza et al. 2014); at this stage, the appendix masculina is undeveloped, preventing sex recognition.

The carapace length (CL) of each shrimp (the distance from the tip of the rostrum to the posterior margin of the carapace) was measured with a digital caliper to the nearest 0.01 mm. Small individuals were measured with a stereomicroscope equipped with a camera lucida and ocular micrometer.

Air temperature, rainfall (precipitation), and salinity data were recorded monthly. Air temperature data were obtained from the “Centro de Previsão de Tempo e Estudos Climáticos — CPTEC/INPE” website (http://bancodedados.cptec.inpe.br/estatisticas/). Rainfall data were obtained from the “Instituto do Meio Ambiente e Recursos Hídricos do Estado da Bahia — INEMA-BA” website (http://www.inema.ba.gov.br/monitoramento/indice-precipitacao/). Salinity was recorded with a portable refractometer (Instrutherm). Methods used for the granulometric analysis of T1, T2, and T3 were described by Oliveira et al. (2015) in a natural history study of the alpheid shrimp Salmoneus carvachoi in the same area.

Statistical Analyses

The data samples were grouped in CL classes of 0.5 mm and histograms of size-frequency distribution were used to analyze the population structure (juveniles, males, and females). Recruitment was assessed based on the abundance of individuals smaller than 5.9 mm throughout the year. The sex ratio was defined as the total number of males/total number of females; the chi-squared test with Yates correction was used to compare the total and monthly percentages of males and females. Wenner’s curve was plotted with male data using the percentage of individuals by size class (see Wenner 1972). A significance level of 5% was adopted for all statistical analyses.

To estimate growth parameters males and females were grouped, as the length structure was similar in both sexes, and the sex ratio was ≈1. The CL frequency distribution was used to estimate the growth parameters of the model. Modes were identified by the Bhattacharya method (Bhattacharya 1967), with size-class intervals of 0.5 mm, using FISAT II v. 1.2.2 (Gayanilo et al. 2005). The routine ‘linking of means’ was used to obtain the growth increments. The growth parameters were estimated based on three different mathematical functions: Von Bertalanffy Growth Function (VBGF), Gompertz Growth Function (GGF), and Logistic Growth Function (LGF). The growth curve that best represented the data was chosen based on the Akaike Information Criteria (AIC) (Akaike 1974), using the following equation:AIC = 2 log φ + 2K, where Φ = a minimum likelihood and K = number of model parameters. Afterwards, the variation of the smallest value of AIC (Δi) and the importance of each model (Wi), defined as \( {w}_i={e}^{\raisebox{1ex}{$\left(-0,5{\varDelta}_i\right)100$}\!\left/ \!\raisebox{-1ex}{$\sum {\varDelta}_i$}\right.} \), was calculated. The upper and lower limits (95%) for the confidence intervals of each estimated growth parameter were established using likelihood and bootstrap analyses, both with 1000 interactions (Hood 2006). Longevity was estimated by the growth parameters of the best model, based on the length that represented the 99th percentile of the population (L99%) (Sparre and Venema 1998).

The mean total density and the density of each group (juveniles, females, and males) was calculated for each transect. To calculate density, the total number of individuals per sampling unit (1 m2) in each transect was considered. Differences between densities were analyzed using the Kruskal-Wallis test and Mann-Whitney test a posteriori. Total abundance and per group (total, juveniles, females, and males) were related to the grain size distribution obtained for each transect.

Statistical analyses were performed with PAST - Paleontological Statistics version 2.16 (Hammer et al. 2001). The map was built using the program ArcMap version 10 (ArcGis). All the figures were modified using CorelDRAW Graphics Suite X7.

Results

Environmental Data

The mean air temperature in the study area varied from 22 °C (September 2011) to 27 °C (January and February 2012) (25 ± 2.8 °C; mean ± standard deviation). Rainfall was well distributed throughout the study period, with monthly means varying from 0.1 ± 0.2 cm (September 2012) to 13.9 ± 22.9 cm (August 2012). Drought periods were not observed. The mean salinity varied from 24.5 (December 2011) to 34.3 (May 2012) (30.6 ± 2.3) (Fig. 2). The grain size analysis evidenced small differences in grain size composition between transects, with predominance of coarse silt in T1, fine sand in T2, and very fine sand in T3.

Fig. 2
figure 2

Monthly variation of abiotic factors (temperature, rainfall, and salinity) from September 2011 to October 2012 in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image

Population Structure

A total of 863 individuals were collected, of which 311 (36.0%) were males, 305 (35.4%) females — 134 (43.9%) breeding and 171 (56.1%) non-breeding — and 247 (28.6%) juveniles (Fig. 3). The CL ranged from 5.9 to 14.0 mm (8.2 ± 1.4) in males, from 5.9 to 13.0 mm (7.5 ± 1.6) in females; and from 1.9 to 5.8 mm (4.6 ± 0.8) in juveniles. Males and females did not differ significantly in size (P = 0.660; Mann-Whitney rank sum test). Adults represented more than 50% of the population in most months, except in January 2012 (Fig. 4). Small individuals (< 5.9 mm) occurred in all months, with peaks in December 2011, January 2012, May 2012, and July 2012, indicating a continuous recruitment. The frequency of adult and juvenile shrimps throughout the year was not related to rainfall and temperature distribution (Multiple R: 0.669; P > 0.05).

Fig. 3
figure 3

Frequency distribution by size-class (CL) of the total number of individuals (males, females, and juveniles) of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image
Fig. 4
figure 4

Monthly abundance by size-class (CL) of the shrimp Alpheus estuariensis sampled from September 2011 to October 2012 in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image

Sex Ratio

The total male/female sex ratio (M:F) was 1:1.02 along the year (Table 1). In the sex ratio by size class, the frequency of males and females was proportional in most classes, except in the 5.5–6.0 mm class. In that size class, females were more frequent, while males were dominant in the 11.5–12.0 mm class (Fig. 5).

Table 1 Sex ratio (males:females) of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil, from September 2011 to October 2012
Full size table
Fig. 5
figure 5

Percentage of males by size-class (CL) of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image

Growth

The three growth models were fitted to the data, and two of them achieved a very similar value of AIC (Table 2). Among them, the VBGF was the growth model with the best fit [Length = 14.64*(1-e(−1.21*(age-0.03)))] and lowest AIC value (Fig. 6). Age explained 99% of length variation. The estimated longevity of A. estuariensis was 1.07 years.

Table 2 Growth parameters of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil, from September 2011 to October 2012, for the three tested growth models: von Bertalanffy Growth function (VBGF), Gompertz (GGF), and Logistic (LGF); and analysis of the Akaike information criterion curves. L∝ = asymptotic length; K = growth constant; to = age in the length; ∆I = variation from the smallest value of AIC; wi = importance of each model
Full size table
Fig. 6
figure 6

Age, growth curves, and fitted in von Bertalanffy Growth function (VBGF), Gompertz (GGF) and Logistic (LGF) of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image

Population Distribution

Of the total number of individuals, 596 (69%) were captured in T1, 81 (9%) in T2, and 186 (22%) in T3. The total mean density was 2.2 ± 2.1 ind. m−2. Considering the mean density per transect, the highest value was observed in T1 (4.8 ± 1.9 ind. m−2), followed by T3 (1.6 ± 1.3 ind. m−2), and T2 (0.4 ± 0.7 ind. m−2) (Fig. 7). Density was significantly different between transects (Kruskal-Wallis test and Mann-Whitney posteriori: P < 0.005). The mean density of juveniles, females, and males was also higher in T1, followed by T3 and T2 (Fig. 8). The density of males and females in T1 did not differ significantly (Kruskal-Wallis test and Mann-Whitney a posteriori: P = 0.979) and was higher than that of juveniles (Kruskal-Wallis test and Mann-Whitney a posteriori: P = 0.016). In the other transects, the densities of the three groups did not differ significantly (T2: Kruskal-Wallis test and Mann-Whitney a posteriori: P = 0.550; T3: Kruskal-Wallis test and Mann-Whitney a posteriori: P = 0.560).

Fig. 7
figure 7

Total densities, per sampling unit (1 m2) and transect, of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil. Boxplots with equal letters did not differ significantly

Full size image
Fig. 8
figure 8

Densities per sampling unit (1 m2) of juveniles, females, and males per transect of the shrimp Alpheus estuariensis sampled in Pontal Bay, Ilhéus, Bahia, Brazil

Full size image

Discussion

Population Structure

Adults and juveniles were observed throughout the studied period, with dominance of adults in most months. However, the abundance in each size class was variable. In general, this structure resembles that of many tropical (and few subtropical) marine crustaceans. In these regions, individuals of almost all size classes are often found during all year (Bauer 1989, 1992; Bezerra and Mathews-Cascon 2006, 2007; Vergamini and Mantelatto 2008; Terossi and Mantelatto 2010; Silva et al. 2016). This tendency is directly related to high temperatures with small variation throughout the year seen in tropical regions. High temperatures allow a rapid gonadal development and continuous reproduction, providing a constant input (renewal) of individuals to the population (Sastry 1983; Bauer 1992; Cobo and Fransozo 2003; Litulo 2005). Costa-Souza et al. (2014) recorded a continuous reproductive period for the same population of A. estuariensis, which maintains this population size throughout the years.

Nutrient availability is another determinant factor in the population structure and survival of individuals (Bauer 1992; Bauer and Lin 1994; Litulo 2005). Tropical estuarine environments have a constant supply of resources, due to a high organic matter input(Little 2000; Silva et al. 2016). Although the abundance of A. estuariensis was not related to abiotic factors, the small temperature variation and constant food availability (characteristic of an estuarine environment) probably are the main factors favoring the persistency of the species and modulating its population.

Despite the scarce information on alpheid shrimp populations, the tropical and subtropical marine populations previously studied showed a similar composition to that of A. estuariensis. Populations of Alpheus dentipes (south of Spain), A. carlae (as A. armillatus) (São Paulo, Brazil), and Synalpheus fritzmuelleri (Texas, USA) (Felder 1982; Fernández-Muñoz and García-Raso 1987; Mossolin et al. 2006) also had adults and juveniles in most months. The exception was the alpheid Salmoeus carvachoi, studied at the same time and site as A. estuariensis, which had a lower abundance and was even absent in some months (Oliveira et al. 2015).

The presence of juveniles along the entire year indicates a continuous recruitment in the study area. Many subtropical and tropical crustacean species, including typical mudflat species, exhibit continuous recruitment (Bauer 1992; Litulo 2005; Bezerra and Mathews-Cascon 2006, 2007). However, in A. estuariensis, the abundance in the first two size classes (i.e., supposedly the youngest) was extremely low and was only observed in 4 months. This might indicate a higher mortality of juveniles in the first life stages. In caridean shrimps, the decapodid (megalopa) larva settles on the substrate just before the molt into juvenile (Anger 2006; Chak et al. 2015). Like other burrowing species (e.g., Strasser and Felder 1998), decapodids of A. estuariensis might excavate the sediment where it will shelter, becoming more exposed and vulnerable to predation, increasing the likelihood of early mortality. Juveniles of A. estuariensis probably share the same habitat of the adults, despite the low number of individuals found in the first size classes. On the contrary, Fernández-Muñoz and García-Raso (1987) suggested that small juveniles of A. dentipes (south of Spain) possibly do not live in the same habitat as larger juveniles and adults.

Males and females of A. estuariensis were very similar in size. In some species of Alpheus, such as A. inca, A. carlae, A. normanni, and A. heterochaelis (Nolan and Salmon 1970; Boltaña and Thiel 2001; Mossolin et al. 2006) males are slightly smaller than females. In other species, e.g., A. heterochaelis, females are slightly smaller than males (Rahman et al. 2003). However, despite these small variations among species, the genus Alpheus lacks size dimorphism.

Sex Ratio

The total and monthly sex ratio observed did not differ from the expected 1:1. The sex ratio of a population of A. carlae also did not differ from the expected 1:1 (Mossolin et al. 2006). In A. dentipes, both the total and monthly sex ratio were also similar to the ratio obtained for A. estuariensis (Fernandez-Muñoz and García-Raso 1987).

In many species of Alpheus, including the studied population, individuals are found in heterosexual pairs in the field (Knowlton 1980; Mathews 2002; Correa and Thiel 2003; Bauer 2004; Costa-Souza et al. 2014; Pescinelli et al. 2016). Some of these populations are considered monogamous (Knowlton 1980; Mathews 2002; Pescinelli et al. 2016). Some ecological characteristics of the genus Alpheus may be considered, such as low population density, the high inter and intraspecific competition for refuges, and the cryptic habit. Those features, along with the pairing behavior, are probably the main adaptive factors that contribute to the equal abundance of males and females in the populations (Knowlton 1980; Mathews 2002; Correa and Thiel 2003). Although monogamy has not been confirmed in this population of A. estuariensis (see Costa-Souza et al. 2014), the presence of males paired with ovigerous and non-ovigerous females, the occurrence of size-assortative pairing, and the cryptic habit of those animals may have contributed to the 1:1 sex ratio.

The frequency of males and females was very similar in all size classes. Considering the five sex ratio patterns by size class that have been proposed (see Wenner 1972; Terossi and Mantelatto 2010), the sex ratio observed in A. estuariensis resemble the “Standard Pattern”. According to Wenner (1972), this pattern indicates that the frequencies of males and females are the same in most size classes. However, in the largest classes ahigher prevalence of males might reflect a larger growth of these individuals or the existence of a differential behavior between sexes when they reach certain sizes. Differently, in A. estuariensis the frequency of both sexes in the largest size classes was similar.

Growth

The presence of size-assortative pairing, similar size structure in both sexes, and a 1:1 sex ratio in all size classes indicate that males and females of A. estuariensis have similar growth and mortality rates. In other crustaceans, differences in growth between males and females are common. In Callinectes danae, females have slower growth because they direct energy towards reproduction and spawning migration (Shinozaki-Mendes et al. 2012). In penaeoid shrimps, females are often larger, have lower growth rates and live longer, which is probably an adaptation to increase egg production (Castilho et al. 2012). Different mortality rates between sexes may result in different size structure and sex ratio: in Callichirus major the sex ratio is 1:1 in young adults but the proportion of females increases with size due the higher mortality of males as a result of their agonistic behavior (Souza et al. 1998).

The estimated longevity for A. estuariensis (1.07 years, ~13 months) can be considered intermediate when compared to other caridean shrimps with short life cycles such as Thor manningi (males with 3.5 months~; females with 5 months) (Bauer 1986), and to carideans with long life cycles, such as Palaemon adspersus (males: 3.07 years; females: 2.83 years) (Glamuzina et al. 2014). The longevity of A. estuariensis was very similar to A. carlae and A. dentipes from populations from the subtropical region (Fenandez-Muñoz and Garcia-Raso 1987; Mossolin et al. 2006).

Population Distribution

The highest abundance and density of adults and juveniles was observed in T1, located in the lower intertidal zone. The grain size of T1 (coarse silt) was smaller than that of T2 and T3 (Oliveira et al. 2015). Individuals of S. carvachoi, one of the shrimps associated with A. estuariensis in the study area, were also more abundant in the same transect (Oliveira et al. 2015). The choice of substrate to settle may be influenced by factors such as surface texture (including type of sediment), adult-related cues, salinity, estuarine water, vegetation, and presence of shells (in hermit crabs) [see Strasser and Felder (1998, 1999) and references therein; Anger (2006) and references therein]. The type of sediment might affect burrow structure, density, and distribution of burrowing crustaceans, which also might influence the distribution of burrow-associated fauna (Dworschak 1983; Yanagisawa 1984; Hall-Spencer and Atkinson 1999; Palomar et al. 2005). The higher number of individuals found in T1 indicates that late larval stages might “select” sediments of small grain sizes for settlement. Fine sediments are characterized by the reduced space between particles, poor drainage, lower oxygen concentration, higher organic matter concentration, and “cohesive” properties. Such cohesiveness is extremely important for burrowing organisms and allows the construction and maintenance of their refuges in the sediments, which would be more difficult in the sand (Little 2000). Probably, A. estuariensis selects substrates with fine sediments due to their particular properties. Higher cohesive properties might facilitate burrowing due to the sediment’s poor drainage capacity, which prevents drought during the low tide. Also, the high concentration of organic matter of fine sediments decreases the shrimps’ exposure time during foraging.

According to the results obtained in this study, we conclude that the population structure of A. estuariensis resembles several other tropical crustacean populations. The abundance of individuals is constant throughout the year, as well as recruitment, which is probably related to low variation in temperature and the constant food availability in the studied region. Additionally, although the study site is situated in a mangrove remnant near an urban area, the population seems to be well established. As in other species of Alpheus, males and females of A. estuariensis show similar size and the sex ratio is 1:1. These shrimps do not have long lifespans as other co-generic populations. Finally, we conclude that A. estuariensis prefers to build shelters in fine-grained sediments.