Population and reproductive biology of Callichirus major (Say, 1818) (Decapoda: Axiidae: Callianassidae) in an urban beach, Northeastern Brazil
FLAVIO DE ALMEIDA ALVES-JÚNIOR1*, JULIANNA DE LEMOS SANTANA1, ALINE MARIA FERREIRA FIGUEIREDO2 & MARINA DE SÁ LEITÃO CÂMARA DE ARAÚJO2 1 Laboratório de Carcinologia – Museu de Oceanografia Prof. Petrônio Alves Coelho (MOUFPE). Av. Arquitetura, s/n, Cidade Universitária, Recife, Pernambuco, Brazil. 2 Coleção Didática de Zoologia da UPE, Faculdade de Ciências, Educação e Tecnologia de Garanhuns, Universidade de Pernambuco (UPE). Rua Capitão Pedro Rodrigues, 105, São José, Garanhuns, Pernambuco, Brazil. *Corresponding author: [email protected]
Abstract: The objective of this study was to describe the population and reproductive biology of Callichirus major (Say, 1818) in Pau Amarelo beach, State of Pernambuco, Northeastern Brazil, based on: relative growth, sex ratio, reproductive period and recruitment of juveniles. Samplings were carried out monthly from May 2011 to April 2012. The individuals of C. major were collected with suction pump, fixed and identified in the laboratory. The abiotic variables were analyzed to identify the factors that influence the development of the population. A total of 274 specimens of C. major were collected, in which the sexual dimorphism was evident, especially with the males reaching larger sizes in: Total Length, Carapace Length, Length and Major Cheliped, while the females were significantly heavier than malesin Wet Weight. Females were more abundant than males (1.0♀: 0.65♂), and the recruitment of juvenile was higher in the dry periods. The population of C. major of Pau Amarelo beach presented biometric measurements typical of other species of the same family. This study contributes to the development of new research in the area, even in the Northeast, where there is little documentation on the species in this region. Key words: Body size, sex ratio, mud beach, ghost shrimps, burrowing crustaceans.
Resumo: Biologia populacional e reprodutiva do Callichirus major (Say, 1818) (Decapoda: Axiidae: Callianassidae) em uma praia urbana, Nordeste do Brasil. O objetivo deste estudo foi avaliar a biologia populacional e reprodutiva do Callichirus major na praia de Pau Amarelo, Estado de Pernambuco, Brasil, através dos parâmetros como: crescimento relativo, proporção sexual, período reprodutivo, e recrutamento de juvenis. As amostras foram realizadas mensalmente de Maio de 2011 a Abril 2012. Os indivíduos de C. major foram coletados com auxilio de bomba de sucção e posteriormente fixados e identificados em laboratório. Os parâmetros abióticos foram analisados para identificar quais fatores influenciam o desenvolvimento da população. Um total de 274 espécimes de C. major foram coletados, no qual o dimorfismo sexual foi evidente, especialmente com machos alcançando maiores tamanhos em: Comprimento Total, Comprimento da Carapaça e Comprimento do Quelípodo Maior, enquanto as fêmeas foram significantes apenas no Peso Úmido. Foram observadas as fêmeas mais abundantes que os machos na população (1.0♀: 0.65♂). O recrutamento de juvenis foi maior nos períodos secos. A população de C. major da praia de Pau Amarelo apresentou medidas biométricas típicas de outras comunidades da mesma família. Assim, este estudo
Pan-American Journal of Aquatic Sciences (2018), 13(2):166-178 Biology of C. major in Northeastern Brazil 167
contribui para o desenvolvimento de novas pesquisas na área, baseado que na região Nordeste do Brasil há poucas pesquisas sobre a espécie na região. Palavras-chave: Tamanhos corpóreos, proporção sexual, praia lamosa, camarão fantasma, crustáceos escavadores
Introduction Burrowing crustaceans of the Infraorder Material and Methods Axiidea have as their main ecological feature the Sampling data: Callichirus major was construction of deep galleries in sandy or muddy sampled monthly from May/2011 to March/ 2012 in substrate of shallow waters (Griffis & Chavez 1988), the intertidal zone, from two sites in the muddy occurring in intertidal zones in beaches with low beach of Pau Amarelo (7° 55' S, 34° 49' W; 7° 52' S, hydrodynamics (Rodrigues & Shimizu 1997, Alves- 34° 49" W), located at Municipality of Paulista, Júnior et al. 2014a,b). Their presence is detected by State of Pernambuco (Figure 1). The first site was small apertures frequently surrounded by fecal located in initial portion of Pau Amarelo beach, pellets (Weimer & Hoyt 1964, Frankenberg et al. which have intersection with the Janga beach (7° 55' 1967, Rodrigues & Shimizu 1997, Alves-Júnior et 27" S, 34° 49' 9" W), and the second site was in final al. 2014a). portion of Pau Amarelo beach, intersection with In Brazilian coast, the population aspects of Conceição beach (7° 54' 22" S, 34° 49' 21" W). The ghost shrimps are poorly documented, in especial animals were collected using a suction pump during about the aspects of Callichirus major (Say, 1818), low tide (Hailstone & Stephenson 1961, Rodrigues with studies concentrated in three regions: Southern 1976) and after samples, all individuals were stored and Southeastern regions, with studies performed by in plastic bags, transported to the laboratory and Borzone & Souza (1996), Shimizu (1997), preserved in alcohol 70% until the time of the Rodrigues & Shimizu (1997), Souza et al. (1998), analysis. In the laboratory, each individual was Souza & Borzone (2003) and Peiró et al. (2014); and identified and sexed according to Melo (1999), and Northeastern region by Araújo et al. (2000), Botter- posteriorly classified as juvenile males, juvenile Carvalho et al. (2002, 2007) and Alves-Júnior et al. females, adult males, non-ovigerous adults females (2014a,b). Callichirus major has great importance in and ovigerous females according to Alves-Júnior et benthic communities, due the burrowing activity in al. (2014b). substrates, revolveing the structure of the sediment, Data Analysis: Each specimen had the following causing the resuspension of organic matter and body dimension measured: Total length (TL), heavy metals, which may cause the death of Carapace length (CL), Major cheliped length individuals of meiofauna (Rodrigues & Shimizu (MCL), Telson width (TW) and Wet weight (WW) 1997; Alves-Júnior et al. 2014a). with the aid of a digital caliper (0.01 mm scale). The In the Brazilian beaches, C. major is collected frequency distribution by size class was obtained with suction pumps for utilization as bait in coastal (using 2 mm size classes), to determine the mode of areas, but as observed by Borzone & Souza (1996), each sex. The Student t test and the U de Mann- this method causes changes in all benthic Whitney-Wilcoxon test were applied to assess community, causing imbalance in the populations, whether there is sexual dimorfism in the biometric especially in symbiotic species of C. major (as measures, with homocedastic (TL; CL; TW and mollusks, nematodes, crabs, copepods and WW) and heterocedastic data (MCL) respectively (α polychaetes) (Rodrigues & Shimizu 1997; Souza & = 0.05). Borzone 2003). The overexploitation of C. major The relative growth of C. major was analyzed species may cause alterations in the density of the based on the allometric equation (y = axb) (Huxley animal or even its disappearance (Borzone & Souza 1950), in which the carapace length (CL) was 1996, Rodrigues & Shimizu 1997). Due to these considered the independent variable (x) (Rodrigues factors, the aim of this paper was to analyze the 1985), while the other body dimensions were population and reproductive biology of C. major, dependent variables (y). The level of allometric including the abundance, allometric growth, sex relation of each body dimension was determined for ratio, reproductive period and recruitment at Pau each sex which: if “b” = 1 isometric growth; “b” > 1 Amarelo beach, localized in State of Pernambuco, allometric positive; “b” < 1 allometric negative, for Northeastern Brazil. the wet weight the reference value of “b” will be
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 168 F. DE ALMEIDA ALVES-JÚNIOR ET AL.
Figure 1. Location of the study site at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil. Symbols in S = Station.
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 Biology of C. major in Northeastern Brazil 169 based in 3 (Huxley 1950). The statistical The burrow temperature ranged from 27.6 to significance of the constant 'b' in relation to the unity 34.6 °C (31.1 ± 3.5 °C). The water temperature was calculated with a t test (α = 0.05) (Zar 1996). varied from 28.4 to 34.5 °C (31.5 ± 3.05 °C). The Through a non-hierarchical classification (K-means salinity varied from 32.0 to 37.0 (34.5 ± 2.5) (Table cluster), the inflection point between the I). The following abiotic factors did not vary significative changes for each biometric relation significantly between dry and rainy periods: burrow (especially between juveniles and adults) were temperature (t = 0.54; p = 0.59; r = 0.17), water estimated using the software Past ® (Paleontological temperature (t = 0.62; p = 0.54; r = 0.19) and salinity Statistics Software, version 3.0) (Corgos & Freire (t = 0.86; p = 0.40; r = 0.26). 2006). The sex ratio was analyzed by months and by Table I. Abiotic factors in the samples of C. major at Pau the total study period, and a Chi-square test was Amarelo beach, State of Pernambuco, Northeastern Brazil. applied to verify if the sex ratio deviated significantly from the expected proportion (1:1), burrow water with critical value of χ2 = 3.84. The reproductive Months temperature temperature Salinity period of C. major was based on the proportions of (°C) (°C) ovigerous females, calculated in relation to adult females in each month and classified, according to May/11 27.6 28.4 33.0 Pinheiro & Fransozo (2002), as: seasonal (occurrence of ovigerous females restricted to some Jun/11 29.2 30.2 32.0 months or seasons), continuous (ovigerous females in all months with similar proportions) or seasonal- Jul/11 29.7 29.5 34.0 continuous (ovigerous females in all months, with distinguishable peaks of high reproductive activity Aug/11 31.5 30.3 33.0 in some of them). The identification of the recruitment period was based where the juveniles Set/11 30.7 29.4 35.0 were significantly more abundant than adults by months. The proportion of juveniles on the total Oct/11 31.1 32.3 36.0 crabs sampled by month determined the recruitment period, tested by the chi-square goodness of fit test Nov/11 30.6 33.2 35.0 (χ²) (α = 0.05). Abiotic factors: Burrow and sea water temperatures Dec/11 31.8 34.5 34.0 were measured in situ with a digital thermometer, and the sea water salinity, with a refractometer. The Jan/12 32.3 31.1 36.0 climate in the locality is characterized as megathermal with rainfall concentrated from March Feb/12 34.6 32.6 37.0 to August and a well-defined dry period (September Mar/12 30.4 30.5 35.0 to February), characterizing the As’ climate (Hot Humid Tropical) (Köeppen 1948, Cavalcanti & Kempf 1967/69). The Student t test was applied to A total of 274 individuals of C. major were compare the abiotic factors between the dry and sampled, being 139 females (129 non-ovigerous and rainy periods (α = 0.05) with the minimum, mean (± 10 ovigerous), 90 males and 45 non-sexed juveniles standard deviation) and maximum values of each (Fig. 2). The sex ratio was 1: 0.65 (♀:♂),with variable were estimated. A correlation matrix, with females being significantly more abundant than Pearson’s coefficient of linear correlation (r), was males (χ² = 5.78; p < 0.05), which the females applied to verify the influence of the abiotic factors reached 85.5 % of total of population, especially in in the total abundance of C. major, as well as in the the months of July/2011 (χ² = 4.15; p < 0.05) with abundance of ovigerous females was assessed with 61.8 %, August/ 2011 (χ² = 8.07; p < 0.05), Pearson's coefficient of linear correlation. November/ 2011 (χ² = 4.1; p < 0.05) with 63.33 % and March/ 2012 (χ² = 21.16; p < 0.05) 96 %. Results However, the ovigerous females were not abundant composing only 0.03 % in the collected population in Pau Amarelo beach.
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 170 F. DE ALMEIDA ALVES-JÚNIOR ET AL.
Figure 2. Number of males and females of C. major collected at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil.
Table II. The values minimum (Min.), maximum (Max.), mean and standard deviation (Stand. dev.) of the biometric variables for both the sex of Callichirus major collected at Pau Amarelo beach, State of Pernambuco, Brazil. TL TL CL CL MCL MCL TW TW WW WW Measure ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀
Min. 30.13 36.35 5.74 8.58 7.20 3.30 4.05 3.00 0.11 0.80
Max. 89.90 94.67 19.54 9.95 25.23 17.30 23.08 25.34 1.85 4.25
Mean 51.80 36.35 10.50 9.95 9.10 3.30 10.20 3.93 1.85 2.53
Stand. dev. 12.20 12.63 2.50 1.80 4.80 2.64 4.30 3.32 5.59 2.44
Note: TL = Total length; CL= Carapace length; MCL = Major cheliped length; TW = Telson width; WW = Wet weight. The values TL, CL, MCL, TL in millimeters; WW in grams.
The minimum, maximum, mean and standard both sexes (b = 2.14 for males and b = 1.36 for deviation values are expressed in Table II. females), indicating that C. major chelipeds grow at Significant differences were found between the sizes a higher rate than the carapace, especially for males. of males and females of C. major, being the males The telson width showed positive allometric showing larger sizes when compared to females in growth (Fig. 5) for both sexes (b = 1.83 for males TL (t = -23.37; p = 0.0001), CL (t = 2.09; p = 0.04), and b = 1.17 for females), indicating an expressive MCL (u = 123355; p = 0.045), TW (t = -0.94; p = growth of telson. In relationships CL vs. WW, C. 0.034), while the females showed significant values major showed positive allometric growth (Fig. 6) for in and WW (t = 9.41; p = 0.05). both sexes (b = 4.2315 for males and b = 3.3392 for In relationships between CL vs. TL, was females), indicating an expressive growth of weight. observed a negative allometric growth (Fig. 3) for Analyzing the distribution by size class (CL) of C. females (b = 0.98 for males and b = 0.74 for major, it could be observed that males were more females), while the males grows in isomerism, frequent between 4.0 ˫ 6.0 mm, 8.0 ˫ 10.0, 10.0 ˫ delimiting that C. major grows more in CL when 12.0 and dominating the size classes between 18 ˫ compared to TL only in females. A positive 20 mm, while females were frequent at 6.0 ˫ 8.0, allometric growth was observed in MCL (Fig. 4) for
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 Biology of C. major in Northeastern Brazil 171
Figure 3. Relationship between the Carapace Length (CL) and the Total Length (TL) for males and females of C. major at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil.
Figure 4. Relationship between the Carapace Length (CL) and the Major Cheliped Length (MCL) for males and females of C. major at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil.
12.0 ˫ 14.0 and 16.0 ˫ 18.0 mm and dominating the more frequent than adults (χ² = 5.44 and 6.13, size class above 20 mm (Fig. 7). respectively; p < 0.05), in the period of summer The recruitment of juveniles into the (high temperature period). In other months collected, population (Fig. 8) occurred in all months of the the C. major no showed difference in the frequency year, especially in November/2011 and of juveniles and adults. The adults were significantly February/2012, when juveniles were significantly
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 172 F. DE ALMEIDA ALVES-JÚNIOR ET AL.
Figure 5. Relationship between the Carapace Length (CL) and the Telson Width (TW) for males and females of C. major at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil.
Figure 6. Relationship between the Carapace Length (CL) and the Wet Weight (WW) for males and females of C. major at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil. dominant in July, August and October (χ² = 4.18, significantly correlated to total abundance of C. 5.13 and 7.25, respectively; p < 0.05). major was salinity (Table III). The water The frequency of ovigerous females was temperature was also positively correlated, despite higher in the months of September/ 2011, January/ not significant, to the abundance of total individuals 2012 and February/ 2012, characteristic by months and ovigerous females, but this relationship between of the dry period. The reproductive period presented these variables could exist and be potentially seasonal characteristic, with ovigerous females detected if a larger sampling was carried out. The occurring in only a period (dry season). Among the burrow temperature was negatively correlated to the analyzed abiotic variables, only salinity was abundance of ovigerous females, based on positive
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 Biology of C. major in Northeastern Brazil 173
Figure 7. Relative frequency of size classes for males and females of Callichirus major at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil.
Figure 8. Frequency of juveniles of C. major collected at Pau Amarelo beach, State of Pernambuco, Northeastern Brazil.
Table III. Correlation of the abiotic factors with the abundance of total individuals and ovigerous females of Callichirus major at Pau Amarelo beach, Pernambuco, Northeastern Brazil. Correlation with the abundance of Correlation with the abundance of total individuals ovigerous females WT BT Sal WT BT Sal r 0.4136 0.4091 0.7394 0.5680 -0.0183 0.5818 t 1.3629 1.3449 3.2950 2.0702 -0.0548 2.1462 p 0.2060 0.2115 0.0093 0.0683 0.9575 0.0603
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 174 F. DE ALMEIDA ALVES-JÚNIOR ET AL. correlations mean that the parameters are related to population being associated with dry periods, which an increase in the animal abundance, while negative the environment is with higher temperatures, correlations, cause the decrease in the animal contributing to egg production, reproductive periods abundance. and intra and interspecific factors as combat and predation (Rodrigues 1985). Discussion The differentiation in sex ratio may be related The abiotic variables did not vary to the sampling method, with females, especially the significantly between the dry and rainy periods, but ovigerous females captured more easily, due occur as recorded in Northeastern regions, the dry period is in the highest part of the galleries to promote eggs well defined between (September to February) ventilation, while the males can build deeper which is observed by high temperatures (Köeppen burrows than females (Tunberg 1986, Felder & 1948, Cavalcanti & Kempf 1967/69), thus indicating Lovett 1989, Tamaki et al. 1997, Dworschak 2015), in Pau Amarelo beach an elevated water and burrow this same characteristic was observed by Rowden & temperatures in these periods. Other studies indicate Jones (1994), for Callianassa subterranea that the temperature present seasonal patterns in (Montagu, 1808) and by Botter-Carvalho et al. States of Alagoas and Pernambuco, acting mainly in (2007) and Alves-Júnior et al. (2014a) for C. major. the water and burrows of burrowing crustaceans as Some studies with species of axiideans analyzed by Aragão (1998), Botter-Carvalho et al. showed females attaining larger sizes than males, as (2002, 2007) and Alves-Júnior et al. (2014a). The analyzed by Pezzuto (1993), for Neocallichirus salinity is directly correlated with the dry and rainy mirim (Rodrigues, 1971) and Souza et al. (1998) for periods (Cavalcanti & Kempf 1967/69). However, C. major both in region Southern of Brazil. On the the seasonal variation was not significant in the Pau other hand, several studies with axiideans found Amarelo beach, possibly due to the high input of males larger than females such as those observed by freshwater from rivers existing in the area during all Hailstone and Stephenson (1961) for Trypaea year. australiensis Dana, 1852, Forbes (1973) for In this study, the females were more abundant Callichirus kraussi (Stebbing, 1900), Shimizu than males with proportion of 1: 0.65 (♀:♂), similar (1997) and Alves-Júnior et al. (2014b) for C. major. results were recorded in others groups, for example Thus, those relationships may be associated with the in gebiideans shrimps as Upogebia deltaura (Leach, development somatic observed in males, which the 1816) by Tunberg (1986) in western Sweden, from energy is directed for growth used for the territorial Upogebia pusilla (Petagna, 1792) by Dworschak combat, attributing higher energy to growth in (1988) in Northern Adriatic Sea and Axianassa special as observed in this paper on carapace and australis Rodrigues & Shimizu, 1992 analyzed by cheliped, while the females reached larger sizes, Botter-Carvalho et al. (2015) from State of possibly a larger body may contain more eggs Pernambuco, Brazil. For axiideans shrimps as corroborating with Hartnoll (1985). observed by Dumbauld et al. (1996) with In relationships CL vs TL, the species of C. Neotrypaea californiensis (Dana, 1854) from major sampled in Pau Amarelo beach, showed Willapa Bay, Washington USA and with Callichirus negative growth for females and isometric for males, major by Rodrigues & Shimizu (1997) from State of indicated by most energy investment in independent São Paulo and Alves-Júnior et al. (2014a) from variable (CL) only females, similar results were Piedade beach, State of Pernambuco, both the States found by Nates & Felder (1999) for located in Brazil. Lepidophthalmus louisianensis (Schmitt, 1935). The In the population of C. major sampled at Pau population of C. major studied by Alves-Júnior et al. Amarelo beach, temporal fluctuations of sex ratio (2014b) in Piedade beach, Pernambuco indicated for were observed, with females more abundant in the both the sex growth in the same proportion months of July/ 2011, August/ 2011, November/2011 (isometric growth), however, the negative growth and March/2012, and ovigerous females occurring in analyzed in Pau Amarelo beach can be related the the months of September/ 2011, January/ 2012 and larger protection against predators or combat. February/ 2012, those results corroborates with The relationships CL vs. MCL, for specimens Hernáez & Wehrtmann (2007) with Callichirus of C. major sampled in Pau Amarelo beach, showed seilacheri (Bott, 1955) in Chile and Alves-Júnior et positive allometric growth. A similar result was al. (2014a) from Piedade beach in Brazil, indicating obtained by Alves-Júnior et al. (2014b) for C. major, the presence of females and ovigerous females in the which justifies the cheliped grows at high rates
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 Biology of C. major in Northeastern Brazil 175 compared to carapace, thus, this appendix assists in Amarelo beach, due the strong urbanization in the combat and excavation of gallery (Felder & Lovett, area. 1989). According to Rodrigues (1985) for the same For the recruitment of C. major, it was species and Hailstone & Stephenson (1961) studying observed a continuous input of juveniles along of T. australiensis, whereas the grows rates when year, with peaks in November/2011 and compared cheliped and carapace have changes February/2012. The frequent capture of juveniles during the ontogenic development of animal, but through the suction pump corroborates with these rates are similar between the sexes. These Witbaard & Duineveld (1989) for Callianassa changes are adaptations for life in plankton and subterranea (Montagu, 1808) in the North Sea, posteriorly in benthic habitats as observed in several which observed the galleries of juveniles shallower decapod species after the larval development and compared to adults, being caught frequently. Those indicates onset of maturity (Posey 1986). peaks of juveniles in population are common as In relationships CL vs. TW, specimens of C. analyzed by Rodrigues (1976) in particular in dry major showed positive growth, this relationship periods, results as also observed in Pau Amarelo corroborates with studies in others axiideans shrimps beach, which the recruitment was intensified in the as for example Neotrypaea gigas Dana, 1852 and N. periods of summer, similar results found by Alves- californiensis Dana, 1854 by Witbaard & Duneveld Júnior et al. (2014a) from Piedade beach (between (1989) and C. major observed by Alves-Júnior et al. summer and autumn). The Pau Amarelo beach (2014b). The telson has different functions presents characteristics of an urbanized beach, with throughout the life of the animal, being used in great offer of organic matters and low larval phase in swimming and in adult phases for hydrodynamics (muddy beach), may be an attractive locomotion and in building the galleries (Posey for juveniles can indicate the constant recruitment. 1986, Witbaard & Duneveld 1989). For the population of C. major sampled in Pau In relationships CL vs. WW, C. major showed Amarelo beach, it was possible to observe the positive allometric growth, the high weight presence of ovigerous females in dry periods acquisition in the Pau Amarelo beach, may be (September/ 2011, January/ 2012 and February/ associated the large quantity of organic matters 2012), characteristic by summer in Northeastern along the tidal flat, due the great entrance of polluted regions (Cavalcanti & Kempf 1967/69). Studies in waters through of great urban pressure occurring in Brazilian coast observed the similar results for C. Pau Amarelo. However, this high food supply in the major as Souza et al. (1998), Araújo et al. (2000), area can be intensify the animal growth as increase Botter-Carvalho et al. (2007) and Alves-Júnior et al. in body proportions, as also for females analyzed by (2014a). On the other hand, Peiró et al. (2014) Pianka (1972) the increment of in egg production observed the species of C. major with continuous and rise of weight. reproduction along the year in Ubatuba, State of São The distribution of ghost shrimps C. major by Paulo, Brazil, however, others studies with axiideans size class demonstrated the males occurring in the shrimps, was observed the presence of ovigerous smaller classes, and the females dominating the females in dry periods as Felder & Griffis (1994) for larger classes (unimodal), similar results found by Lepidophthalmus louisianensis (Schmitt, 1935) at Alves-Júnior et al. (2014a) for C. major from Mississippi and Bilodeau et al. (2005), for Piedade beach. Studies with gebiideans shrimps as Callichirus islagrande (Schmitt, 1935) at Louisiana, Botter-Carvalho et al. (2015) observed for both in USA. Axianassa australis with females reaching larger Salinity was significantly correlated to total sizes classes compared to males follow the Gaussian abundance of C. major in Pau Amarelo beach, but distribution. Anthropic impacts on the population of for the abundance of ovigerous females the salinity ghost shrimps can be alter the size class of the showed correlated but no significant. Some studies animal, i.e., overexploitation by fishery as observed indicated the salinity acting on seasonal fluctuations by Hernáez & Wehrtmann (2007) for C. in the population of axiideans and gebiideans seilacheri and Alves-Júnior et al. (2014a) for C. shrimps as analyzed by Hill (1977), Posey (1986) major and environmental factors as coastal erosion and Alves-Júnior et al. (2014a). The water (Botter-Carvalho et al. 2002), deposition of organic temperature and burrow temperature no showing matter or heavy metals on tidal flat (Shimizu 1997), significance. In this paper as observed by Posey those environmental factors are observed in Pau (1986) and Tamaki et al. (1996), although there was no significance the temperature favors the sexual
Pan-American Journal of Aquatic Sciences (2018), 13(2): 166-178 176 F. DE ALMEIDA ALVES-JÚNIOR ET AL. activity, metabolism, egg production, burrowing praia do Sobral, Maceió- Alagoas. Boletim de activity and embryonic development. Estudos de Ciências do Mar, 11: 101–112. Thus, in this paper is possible conclude that Borzone, C. A. & Souza, J. R. B. 1996. A extração de the abiotic factors in Pau Amarelo beach were not corrupto Callichirus major (Decapoda: significant when compared with the abundance of Callianassidae) para uso como iscas em praias this species; the females are more abundant in the do litoral do Paraná: características da pesca. population, which observed in others axiideans Nerítica, 10: 67–79. shrimps in the Brazilian coast. Significant Bott, R. 1955. Ergebnisse der Forschungsreise A. differences in morphology were found between the Zilch 1951 nach El Salvador 18. Dekapoden sizes of males and females of C. major. The (Crustacea) aus El Salvador. Litorale variables CL vs. CT showed allometric negative only Dekapoden, außer Uca. Senckenb Biol, 36: females and isometric for males, while the 45–72. relationships CL vs. MCL, CL vs. TW and CL vs. Botter-Carvalho, M. L., Santos, P. J. P. & Carvalho, P. WW showed allometric positive. The reproductive V. V. C. 2002. Spatial Distribution of period showed occur only the summer (dry period). Callichirus major (Say 1818) (Decapoda: The recruitment of the species occurs in peaks in Callianassidae) on a sandy beach, Piedade, summer. For the correlation matrix only the salinity Pernambuco, Brazil. Nauplius, 10(2): 97–109. showed significant for the total abundance and only Botter-Carvalho, M. L., Santos, P. J. P. & Carvalho, P. related for ovigerous females in population. So, this V. V. C. 2007. Population dynamics of paper increases the aspects about the biology Callichirus major (Say, 1818) (Crustacea, reproductive of C. major in an urban muddy beach Thalassinidea) on a beach in northeastern in Northeastern Brazil. Brazil. Estuarine, Coastal and Shelf Science, 71: 508–516. Acknowledgments Botter-Carvalho, M. L., Costa, L. B., Gomes, L. L., The first and second authors would like to Clemente, C. C. C. & Carvalho, P. V. V. C. thank CAPES (Coordenação de Aperfeiçoamento de 2015. Reproductive biology and population Pessoal de Nível Superior) for the postgraduate structure of Axianassa australis (Crustacea, scholarship on Oceanography. The authors would, Axianassidae) on a sand-mud flat in north- specially, like to thank Dr. Pablo Muniz for his eastern Brazil. Journal of the Marine support and the anonymous reviewers for their Biological Association of the United precious comments on this paper. Kingdom, 95(4): 735–745. Corgos, A. & Freire, J. 2006. Morphometric and References gonad maturity in the spider crab Maja Alves-Júnior, F. A., Araújo, M. S. L. C. & Coelho, P. brachydactyla: a comparison of methods for A. 2014a. Population biology of Callichirus estimating size at maturity in species with major (Say, 1818) (Crustacea: Callianassidae) determinate growth. ICES Journal of Marine at Piedade Beach, Brazil. Journal of Science: Journal du Conseil, 63(5): 851–859. Integrated Coastal Zone Management, Cavalcanti, L. B. & Kempf, M. 1967/69. Estudo da 14(1): 109–118. Plataforma Continental na Área do Recife Alves-Júnior, F. A., Araújo, M. S. L. C. & Feitosa, F. (Brasil). II. Meteorologia e Hidrologia. A. N. 2014b. Crescimento alométrico de Trabalhos Oceanográficos da Universidade Callichirus major (Say, 1818) (Crustacea: Federal de Pernambuco, 9(11): 149–158. Callianassidae) em uma praia arenosa do Dana, J. D. 1852. Conspectus crustaceorum, &c. Nordeste Brasileiro. Tropical Oceanography, Conspectus of the Crustacea of the exploring 42: 13–21. expedition under Capt. C. Wilkes, U.S.N. Aragão, J. O. R. 1998. O impacto do Enso e do Macroura. Proceedings of the Academy of Dipolo do Atlântico no Nordeste do Brasil. Natural Sciences of Philadelphia, 6: 10–28. Bulletin de l’Institut Français d’Études Dana, J. D. 1854. Catalogue and descriptions of Andines, 27(3): 839–844. Crustacea collected in California by Dr. John Araújo, J. S., Calado, T. C. S. & Sá, M. F. P. 2000. L. Le Conte. Proceedings of the Academy of Aspectos reprodutivos de Callichirus major Natural Sciences of Philadelphia, 7: 175– (SAY 1818) (Crustacea: Callianassidae) da 177.
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Received: January 2018 Accepted: May 2018 Published: September 2018
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