Population structure and reproductive biology of the fiddler crab Uca inversa (Hoffman, 1874)...

POPULATION STRUCTURE AND REPRODUCTIVE BIOLOGY OF THECRAB SESARMA RECTUM RANDALL, 1840 (BRACHYURA,SESARMIDAE) IN AN IMPACTED TROPICAL MANGROVE

IN NORTHEAST BRAZIL

BY

F. B. RIBEIRO1,3), H. MATTHEWS-CASCON1) and L. E. A. BEZERRA2,4)1) Laboratório de Invertebrados Marinhos, Departamento de Biologia, Universidade Federal do

Ceará, Av. Mister Hull, s/n, Campus do Pici, Fortaleza, Ceará, Brazil2) Programa de Pós-Graduação em Oceanografia, Departamento de Oceanografia, UniversidadeFederal de Pernambuco, Av. da Arquitetura, s/n, Cidade Universitária, CEP 50670-901 Recife,

Pernambuco, Brazil

ABSTRACT

The population structure and reproductive biology of the semiterrestrial crab Sesarma rectumwere studied in an impacted tropical mangrove in northeast Brazil. Crabs were collected monthlyduring spring low-tide periods from October 2009 through September 2010. A catch-per-unit-effort(CPUE) technique was used to sample the crab population, using two-hour sampling periods by twopeople. A total of 492 crabs was obtained, of which 262 were males, 151 non-ovigerous females,and 79 ovigerous females. Males were significantly larger than females, whether non-ovigerousor ovigerous. There was no significant difference between mean size of the ovigerous and non-ovigerous females. The population showed a unimodal size-frequency distribution, with a normaldistribution for males and non-normal for females. The overall sex ratio (1 : 0.87) did not differsignificantly from the expected 1 : 1 proportion. Ovigerous females were found during the entireperiod, except in March and August 2010. The mean number of eggs was 14 975±5689. The highestnumber of eggs was recorded for the 29 to 31 mm age group. A regression analysis showed that thenumber of eggs increased linearly with carapace width (r2 = 0.70) and abdomen width (r2 = 0.76).Comparisons among populations will help to evaluate the differences among them, as well as tounderstand the environmental and biological constraints that are shaping them.

RESUMEN

La estructura poblacional y la biología reproductiva del cangrejo semiterrestre Sesarma rectumfueron estudiadas en un manglar tropical impactado en el nordeste de Brasil. Los cangrejos fueron

3) Current address: Programa de Pós-Graduação em Ciências Marinhas Tropicais, Instituto deCiências do Mar (LABOMAR), Universidade Federal do Ceará, Av. Abolição 3207, CEP 60165-081, Fortaleza, Ceará, Brazil4) e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2012 Crustaceana 85 (2): 173-188Also available online: www.brill.nl/cr DOI:10.1163/156854012X624646

174 F. B. RIBEIRO, H. MATTHEWS-CASCON & L. E. A. BEZERRA

muestreados mensualmente durante los períodos de marea baja desde Octubre de 2009 a Septiembrede 2010. Para obtener una muestra representativa de la población se utilizó una técnica de capturapor unidad de esfuerzo (CPUE) con períodos de dos horas de colecta realizados por dos personas. Secapturaron un total de 492 individuos: 262 machos, 151 hembras no-ovígeras y 79 hembras ovígeras.El tamaño de los machos fué significativamente mayor que el de las hembras ovígeras y no-ovígeras.No se observaron diferencias significativas entre los tamaños medios de las hembras ovígeras y lasno-ovígeras. La población mostró una distribución unimodal de frecuencias de tamaños, con unadistribución normal en los machos y no normal en las hembras. La proporción sexual (1 : 0,87) nose aleja significativamente de la proporción esperada 1 : 1. Se encontraron hembras ovígeras durantetodo el período de captura excepto en los meses de marzo y agosto de 2010. El número promediode huevos fue de 14 975 ± 5689. El mayor número promedio de huevos se observo en tallas de29 a 31 mm. Tanto el análisis de regresión entre el número de huevos y el ancho del caparazón(r2 = 0,70) como entre el número de huevos y el ancho del abdomen (r2 = 0,76) mostraron unincremento linear. Las comparaciones inter-poblacionales ayudarán a evaluar sus diferencias y aentender las restricciones ambientales e biológicas que las afectan.

INTRODUCTION

According to Golley et al. (1962), crabs are the dominant faunal group inmangrove areas in terms of numbers and biomass. Many studies have demonstratedthe abundance and dominance of the crab families Ocypodidae, Grapsidae, andSesarmidae in tropical mangroves (e.g., Frusher et al., 1994; Skov et al., 2002;Priyadarshani et al., 2008).

The genus Sesarma Say, 1817 comprises 17 species that live in subtropical andtropical regions of the American continent (Ng et al., 2008; Schubart et al., 2010).The family Sesarmidae Dana, 1851, includes terrestrial, semiterrestrial, and limnicorganisms (Hartnoll, 1964; Ng & Davie, 1995; Schubart et al., 2000), and Sesarmarectum Randall, 1840 mainly inhabits mangrove environments (Melo, 1996). Thespecies builds burrows in shaded areas or along the edge of the mangrove, andfeeds on detritus and leaves (Prado, 1999). It is distributed from Brazil, as farsouth as Santa Catarina (Melo, 1996), to Trinidad and Grenada (Von Hagen, 1978;Schubart et al., 1999; Coelho et al., 2008).

Studies of the population biology and reproductive biology of sesarmid crabsare numerous, including S. rectum from subtropical mangroves in southeasternBrazil (Mantelatto et al., 1999; Silva & Chacur, 2002; Silva et al., 2007), butrelatively few studies have been carried out in tropical mangroves in Brazil(Castiglioni et al., 2011). Comparisons among populations will help to evaluatethe differences between them, as well as to understand the environmental andbiological constraints from which those differences originate.

This contribution aimed to elucidate some aspects of the population structureand reproductive biology of S. rectum, including the size structure, sex ratio,reproductive period, and fecundity in an impacted tropical mangrove in the state

POPULATION BIOLOGY OF SESARMA RECTUM IN A BRAZILIAN MANGROVE 175

Fig. 1. Map indicating the sampling area in the Cocó River Ecological Park, municipality ofFortaleza, Ceará, northeastern Brazil.

of Ceará, northeastern Brazil. Understanding the structure of this population cangenerate information of use in the conservation of this area.

MATERIAL AND METHODS

The study site is an impacted mangrove, situated in the Cocó River Ecologi-cal Park in the municipality of Fortaleza, Ceará (3◦45′07.81′′S 38◦29′05.82′′W)(fig. 1). The Cocó River Ecological Park is the largest urban park in South Amer-ica, with an area of 379 ha. Almost all the entire park area shows advanced degra-dation of its ecosystem, with major consequences especially from city expansionpromoted by real-estate speculation, and also from slum areas around the park(Anon., 2006).

Monthly sampling [catch-per-unit-effort (CPUE), 2 people for 2 hours] tookplace during spring low-tide periods from October 2009 through September 2010.


Specimens of Sesarma rectum were obtained manually, some being exposed on thesurface of the mangrove substrate and others captured by digging from burrows.In the laboratory, specimens were identified, sexed according to secondary sexualcharacters (abdomen morphology and number of pleopods), and investigatedfor the presence of eggs on the female pleopods. The carapace width (CW)and female abdomen width (AW) were measured using Vernier callipers (±0.01mm accuracy). The number of crabs collected was recorded for each month.Voucher specimens were deposited in the Crustacean Collection of the MuseuOceanográfico of the Universidade Federal de Pernambuco (MOUFPE#14852;14853).

The precipitation indices of the Cocó River Ecological Park from October 2009to September 2010 were provided by the “Fundação Cearense de Meteorologia eRecursos Hídricos” (FUNCEME).

Population structure

Population size structure was analysed from the size-frequency distribution ofall individuals collected during the study period. Specimens were grouped into2-mm size classes, from 13 to 37 mm CW.

The chi-square test (χ2) was used to evaluate the significance of the sex ratioof the population. Fisher’s test (z) was used to evaluate the sex ratio in eachmonth. Overall size-frequency distributions were tested for normality using theKolmogorov-Smirnov (KS) test (Zar, 1984), and the mean sizes of males andovigerous and non-ovigerous females were compared using Student’s t-test.

Reproductive period and fecundity

The breeding season or reproductive period was determined from the presenceof ovigerous females. To estimate fecundity, 36 ovigerous females with eggs in theinitial stage were selected for egg counts, according to the methodology proposedby Oshiro (1999). The pleopods were removed from the females, placed in Petridishes filled with seawater, and the eggs were detached by gradually adding asolution of sodium hypochlorite. The bare pleopods were then discarded by beinggently stirred in a beaker filled with 50 ml seawater. With a pipette, five subsamplesof 1 ml were taken from the seawater with eggs. The eggs in each subsample werecounted under a dissecting microscope. The mean value obtained was extrapolatedfor the whole suspension in order to estimate the number of eggs. For the fecundityanalysis, data were analysed using the power function (Y = aX+b) of egg number(EN) vs. CW and egg number (EN) vs. AW.

A dispersion diagram was generated for the relationship egg number vs.carapace width (CW), and egg number vs. abdomen width (AW). These valueswere submitted to a regression analysis.


Fig. 2. Sesarma rectum Randall, 1840. Mean size of individuals collected in the Cocó RiverEcological Park, northeast Brazil, October 2009 through September 2010. Black bars, males; white

bars, all females.

RESULTS


A total of 492 specimens of Sesarma rectum were sampled during the studyperiod, of which 262 were males (53.25%), 151 non-ovigerous females (30.69%),and 79 ovigerous females (16.06%). Males ranged from 15.03 to 36.18 mm CW(mean ± SD: 29.31 ± 3.97 mm); non-ovigerous females from 13.43 to 32.92 mmCW (mean ± SD: 26.09 ± 3.97 mm); and ovigerous females from 20.07 to32.56 mm CW (mean±SD: 26.86±2.44 mm). Males were significantly larger thannon-ovigerous females (t = 7.26, p < 0.001) and ovigerous females (t = 6.24,p < 0.001). There was no significant difference between the mean size of theovigerous and non-ovigerous females (t = −1.79, p > 0.05). Fig. 2 shows themean size for all crabs sampled.

The yearly size-frequency distributions for males and females in the samplingperiod shows a conspicuous unimodal size distribution, with a normal distributionfor males (KS = 0.2293, p = 0.0812) and non-normal distribution for females(KS = 0.2602, p = 0.0242) (fig. 3).

The number of crabs sampled monthly throughout the year is listed in table I.The overall sex ratio was 1 : 0.87 (M : F) and did not differ significantly from theexpected sex ratio of 1 : 1 (χ2 = 8.112, p > 0.05). Fisher’s exact test (z) was usedto calculate the deviation from the expected ratio 1 : 1 in each month of sampling.For the overall sex ratio, no significant deviations from the Mendelian proportionwere detected (z, p > 0.05), except in October 2010 (table I).


Fig. 3. Overall size-frequency distribution of Sesarma rectum Randal, 1840 collected in the CocóRiver Ecological Park, northeast Brazil, October 2009 through September 2010. Black bars, males;

white bars, all females.

TABLE ISesarma rectum Randall, 1840. Total number, numbers of males and females, and sex ratio of

individuals collected monthly in Cocó River Ecological Park mangrove, northeastern Brazil

Months Males Females Total Sex ratio2009-2010

Oct/09 28 15 (5) 43 1 : 0.53*Nov/09 23 24 (11) 47 1 : 1.04Dec/09 24 16 (13) 40 1 : 0.66Jan/10 24 22 (18) 46 1 : 0.92Feb/10 21 26 (19) 47 1 : 1.24Mar/10 24 19 (0) 43 1 : 0.79Apr/10 18 19 (1) 37 1 : 1.05May/10 23 27 (2) 50 1 : 1.17Jun/10 15 16 (3) 31 1 : 1.06Jul/10 19 16 (5) 35 1 : 0.84Aug/10 37 24 (0) 61 1 : 0.64Sep/10 6 6 (2) 12 1 : 1

Total 262 230 (79) 492 1 : 0.87

*) Significant deviations from the 1 : 1 proportion in sex ratio (z, p < 0.05).


A total of 79 ovigerous females were collected from all months except March2010 and August 2010 (fig. 4). The highest numbers of ovigerous females were


Fig. 4. Relative frequencies of ovigerous and non-ovigerous females of Sesarma rectum Randall,1840 collected in the Cocó River Ecological Park, October 2009 through September 2010. Black

bars, non-ovigerous females; white bars, ovigerous females.

Fig. 5. Mean monthly rainfall at the Cocó River Ecological Park, October 2009 through September2010.

found in January 2010 and February 2010, corresponding to the beginning of therainy period in Cocó River Ecological Park (fig. 5). Ovigerous females were mostabundant in the 19-22 mm size class, and the mean CW was 26.84 ± 2.44 mm.Fecundity ranged from approximately 4320 (CW = 20.07 mm) to 33 850 (CW =30.29 mm) eggs (mean±SD: 14 975±5689.5). The number of eggs was positivelycorrelated with female carapace width (fig. 6), and the resulting scatter plot showed


Fig. 6. Scatter plot for the relationship between egg number (EN) and female size (CW) in Sesarmarectum Randall, 1840 from the Cocó River Ecological Park, northeast Brazil.

Fig. 7. Scatter plot for the relationship between egg number (EN) and female abdomen width (AW)in Sesarma rectum Randall, 1840 from the Cocó River Ecological Park, northeast Brazil.

a linear trend, expressed by the function EN = 2221.5×CW−42 543 (r2 = 0.7015,

n = 36). Figure 7 shows the relationship between abdomen width and egg number.

As for carapace width, the egg number was positively correlated with female

abdomen width, resulting in a scatter plot showing a linear trend, expressed by

the function EN = 2638.5 × AW − 39 649 (r2 = 0.7676, n = 36).

Most fecund females belonged to size class 29-31 mm, although the highest

numbers of ovigerous females belonged to the size classes of 25-27 and 27-29 mm

(table II).


TABLE IIAverage fecundity by size class with its standard deviation (SD) in ovigerous females of Sesarmarectum Randall, 1840 from Cocó River Ecological Park collected in October 2009 through Septem-

ber 2010; N , number of ovigerous females in each class

Size class N Average fecundity*) SD

19-21 2 5500 1668.7721-23 1 7380 —23-25 15 10 984 2838.1925-27 21 13 184.76 3390.5827-29 24 16 657.5 4405.1329-31 14 20 328.57 6931.8931-33 2 19 320 7608.47

*) = number of eggs.

DISCUSSION


The frequency of size distribution of the population of Sesarma rectum fromthe Cocó River Ecological Park mangrove was unimodal, which may reflecta continuous recruitment, with no disruption of classes and constant mortalityrates, indicating a stable population (Díaz & Conde, 1989), although this areais disturbed. However, some authors (Díaz & Conde, 1989; Silva et al., 2007)studied crab populations of impacted areas and observed that sesarmid crabs, aswell as panopeids and porcellanids, are able to adapt to adverse conditions due totheir phenotypic plasticity (Vergamini & Mantelatto, 2008; Miranda & Mantelatto,2009).

The unimodal distribution is common in decapod crustaceans from tropicalregions, where seasonal climate changes are not very prominent (Warner, 1967;Díaz & Conde, 1989; Bezerra & Matthews-Cascon, 2006). Studies of sesarmidcrabs in Brazil have shown that the animals in different populations reproducecontinuously throughout the year (Leme, 2002, 2005; Nicolau & Oshiro, 2007;Castiglioni et al., 2011). However, even tropical species of crustaceans may showa bimodal distribution, as found by Bezerra & Matthews-Cascon (2007) for Uca(Minuca) thayeri Rathbun, 1900 in a tropical mangrove of the Pacoti River inCeará. The distribution of size frequencies in populations is a very dynamiccharacteristic, and can vary throughout the year as a result of reproductive eventsand rapid larval recruitment (Thurman, 1985).

With respect to the size of the animals, median values of males were signifi-cantly larger than those of females (ovigerous and non-ovigerous), with the largestnumber of individuals of both sexes present in the larger size classes. This probablyoccurs because females concentrate their energy on gonad development (Díaz &


Conde, 1989; Johnson, 2003; Hartnoll, 2006), whereas males grow to large sizes,since large males are more likely to mate and to win intraspecific fights (Christy& Salmon, 1984). Therefore, after the puberty changes, females grow more slowlythan males, a characteristic also observed in, e.g., the amphipod Orchestia gam-marella (Pallas, 1766) (see Charniaux-Cotton, 1957). However, it is important tokeep in mind that this could also be due to collection bias.

Leme (2002) and Castiglioni et al. (2011) also found significantly larger malesthan females for a population of Sesarma rectum in a subtropical mangroveforest in southeastern Brazil and in a tropical mangrove in northeastern Brazil,respectively. However, it should be noted that in some populations of crabs,females may be larger than males, as found by Bedê et al. (2008) for Uca (Minuca)victoriana Von Hagen, 1987 in Rio de Janeiro; and by Costa (2000) and Bezerra& Matthews-Cascon (2006) for Uca (Minuca) thayeri in Ubatuba, São Paulo andUca (Leptuca) leptodactyla (Smith, 1898) in the Pacoti River, Ceará, respectively,although the differences were not significant. However, all these cases involve thegenus Uca, where males have to invest much more in the development of a largechela.

The proportion among males and females is also a feature that reflects thepopulation balance (Fisher, 1930). It is common to find populations of crustaceanswith significant deviations from the expected ratio of 1 : 1, which can be causedby differences in birth rates or mortality rates between the sexes (Johnsson, 2003)and/or the sampling rates (Montague, 1980). The sex ratio found in the presentstudy (1 : 0.87) did not differ significantly from the Fisherian proportion of 1 : 1,although there was a trend for males to be slightly more numerous than females.Similarly, Silva et al. (2007) found no deviations from the expected ratio for apopulation of S. rectum in Paraty, Rio de Janeiro, and neither did Silva & Chacur(2002) for S. rectum in Ubatuba, nor Castiglioni et al. (2011) for S. rectum inArinquindá, Pernambuco. However, in these populations there was also a slighttrend toward a greater abundance of males.

According to Geisel (1972), physiologically and behaviourally homeostaticpopulations, which occupy relatively constant environments, are acclimated totheir microenvironment and show a sex ratio of 1 : 1, or one slightly male-biased,whereas populations that inhabit variable environments will show deviationstoward females, in order to maximize the evolutionary potential due to unequalselection between males and females. Fisher (1930) predicted that in randomlymating populations, the evolutionarily stable sex ratio would be 1 : 1. In this study,the overall sex ratio did not differ significantly from the expected 1 : 1 ratio,suggesting that the S. rectum population in the tropical mangrove of the Cocó Riveris physiologically and behaviourally adapted to its habitat.



Tropical species generally reproduce continuously during the entire year. Inthe tropics, environmental conditions are favourable for the development of thegonads, whereas subtropical and temperate species have seasonal breeding periods(Mouton & Felder, 1995). However, both types of reproduction can be found intropical and subtropical areas (Litulo, 2005; Bezerra & Matthews-Cascon, 2007).

The record of ovigerous females of S. rectum in almost every month of thisstudy indicates that the reproductive activity of this population is continuous, pro-ducing a unimodal distribution of the size classes with adults and juveniles presentyear-round. However, ovigerous females were more frequent at the beginning ofthe rainy season, suggesting a reproductive peak associated with this time of year.Reproductive peaks, represented by the frequency of ovigerous females found inbrachyuran populations, may be associated with abiotic and biotic factors such astemperature, latitude, zonation, photoperiod, rainfall, and food availability (Thor-son, 1950; Sastry, 1983; Pinheiro & Fransozo, 2002). Thus, as the rainy season isalso the time of greatest river discharge, there may be evidence of a relationshipbetween increased nutrient availability and the successful development of larvae(Christy & Morgan, 1988), as well as wider dispersal, and thus this populationmay concentrate its reproductive activity in this rainy period.

Populations of S. rectum studied by Leme (2002, 2004) in Ubatuba also showedcontinuous reproduction throughout the year, but with two peaks of intensity,one during the winter and the other in summer. Castiglioni et al. (2011) alsofound ovigerous females of S. rectum throughout the year in the ArinquindáRiver, Pernambuco, indicating a continuous reproductive period with two peaksof intensity, one during spring and other in summer. The monthly frequency ofovigerous females found by Castiglioni et al. (2011) was positively correlated withair and burrow temperatures. However, Leme (2002, 2004) found no relationshipbetween these peaks and abiotic factors, in contrast to this same species in theCocó River mangrove, which seems to synchronize its reproductive peak with therainy period.

Silva et al. (2007) suggested that the reproductive peak of S. rectum in Paraty(Rio de Janeiro) is closely related to high temperatures: the highest number ofovigerous females in the population occurred two months before the warmestperiod of the year. This delay may be related to larval development time, so thatthe megalopae and juveniles enter the habitat in the most favourable period.

The absence of ovigerous females in March and August 2010 and the lownumber of such females collected in April and May 2010, may be related todifficulties in sampling, since females can be hidden inside the galleries while theyare incubating the eggs. These galleries are excellent shelter from predators and


provide water and humidity, allowing the crabs to avoid exposure to unfavourableconditions such as high temperatures during the critical periods of the day (Powers& Bliss, 1983; Atkinson & Taylor, 1988; Henmi, 2003).

Leme (2002) also found months with low numbers of ovigerous females of a S.rectum population in Ubatuba, and attributed this to the habit of this species to digburrows under grass and shrubs such as Hibiscus sp. for shelter and to escape highsurface temperatures.

Analysis of the fecundity ratio showed that the numbers of eggs vary accordingto carapace width (CW). Inconsistent values could be due to multiple spawningof females, or because they lose a considerable portion of their eggs duringincubation, or else because the quantification method is just an approximation.Egg loss might result from attack by pests or by mechanical abrasion against thesubstrate (Hartnoll, 1969; Hines, 1982).

Inspection of the fecundity of S. rectum according to size class (table II)shows that this species follows the general pattern for brachyurans, with eggnumbers increasing with carapace width (CW) and size of the abdomen (AW).This pattern has been observed in all brachyuran families studied so far, includingPortunidae, e.g., Callinectes danae Smith, 1869 (cf. Costa & Negreiros-Fransozo,1996) and Callinectes ornatus Ordway, 1863 (cf. Mantelatto & Fransozo, 1997);Grapsidae, e.g., Goniopsis cruentata (Latreille, 1813) (cf. Silva & Oshiro, 2002);and Sesarmidae, e.g., Aratus pisonii (H. Milne Edwards, 1853) (cf. Leme &Negreiros-Fransozo, 1998) and S. rectum (see Leme, 2005). The main factorsthat contribute to the variation in fertility in brachyuran crabs are the season, theavailability of food, and the reproductive stage of the females (Costa & Negreiros-Fransozo, 1996).

The mean number of eggs found for the population of S. rectum in the CocóRiver mangrove (14 975 ± 5689 eggs) was higher than that found for some othersesarmid crab populations from Brazil, such as Aratus pisonii (9081 ± 3684 eggs)in Itacuruçá, Rio de Janeiro (Nicolau & Oshiro, 2002); S. rectum (9882 ± 3262eggs) in Ubatuba (Leme, 2004); Armases rubripes (Ratbun, 1897) (4458 ± 2739)in Sepetiba Bay, Rio de Janeiro (Lima et al., 2006); and lower than in other speciessuch as Sesarma sp. (20 400 ± 2469.2) in the Gulf of Mexico (Zimmerman &Felder, 1991).

Differences in the average number of eggs may reflect environmental condi-tions, especially in relation to food availability. Silva et al. (2007), comparing twopopulations of S. rectum, one at Ubatuba and one at Paraty, found low fecundityin the latter, possibly because this area has been reduced by the growth of the city.Thus, the lower fecundity in the S. rectum population at Paraty may be considereda first step toward the local disappearance of this species (Silva et al., 2007).


Regression analysis showed that the number of eggs of S. rectum in the CocóRiver increases with carapace width (CW), as in other brachyurans. In a populationof S. rectum in Paraty, Silva et al. (2007) found a linear regression model (CW ×egg number) with values close to those reported in the present study.

In conclusion, the high fecundity rate found in the present contribution, linkedwith the 1 : 1 sex ratio, the presence of ovigerous females nearly year-round,males larger than ovigerous and non-ovigerous females, and the unimodal distri-bution, all suggest that the S. rectum population in the Cocó River mangrove isphysiologically and behaviourally adapted to its habitat.

ACKNOWLEDGEMENTS

This study was completed by F. B. Ribeiro in the course of obtaining aBachelor’s degree in Biological Sciences from the Federal University of Ceará.The authors thank A. K. M. Araújo for her assistance during fieldwork, M.Sc. L.Peres and M.Sc. M. C. Leite for their help with statistical procedures, Dr. JanetW. Reid for correcting the English text, M.Sc. Carla Piantoni for help with theSpanish, and Dr. T. M. C. Lotufo for comments on the thesis. Special thanks toDr. Fernando Mantelatto and Dr. Christoph Schubart for their valuable criticismsand suggestions, which greatly improved the manuscript. L. E. A. Bezerra thanksPNPD/CAPES and FACEPE (BCT-0039-1.08/10) for providing a post-doctoralscholarship. All sampling in this study was conducted in compliance with currentapplicable state laws (SEMACE 3434/2009/GS/COFLO-NAGUC).

REFERENCES

ANONYMOUS, 2006. Secretaria de Desenvolvimento e Meio Ambiente de Ceará — SEMACE. Atlasdos Manguezais do Nordeste do Brasil: Avaliação das áreas de manguezais dos Estados doPiauí, Ceará, Rio Grande do Norte, Paraíba e Pernambuco. (SEMACE, Fortaleza).

ATKINSON, R. J. A. & A. C. TAYLOR, 1988. Physiological ecology of burrowing decapods.Symposium of the Zoological Society of London, 59: 201-226.

BEDÊ, L. M., L. M. Y. OSHIRO, L. M. D. MENDES & A. A. SILVA, 2008. Comparação daestrutura populacional das espécies de Uca (Crustacea: Decapoda: Ocypodidae) no Manguezalde Itacuruçá, Rio de Janeiro, Brasil. Rev. Brasileira Zool., 25(4): 601-607.

BEZERRA, L. E. A. & H. MATTHEWS-CASCON, 2006. Population structure of the fiddler crabUca leptodactyla Rathbun, 1898 (Brachyura: Ocypodidae) in a tropical mangrove of northeastBrazil. Thalassa, 22(1): 65-74.

— — & — —, 2007. Population and reproductive biology of the fiddler crab Uca thayeri Rathbun,1900 (Crustacea: Ocypodidae) in a tropical mangrove from northeast Brazil. Acta Oecol., 31:251-258.

CASTIGLIONI, D. S., P. J. A. DE OLIVEIRA, J. S. DA SILVA & P. A. COELHO, 2011. Populationdynamics of Sesarma rectum (Crustacea: Brachyura: Grapsidae) in the Ariquindá Rivermangrove, north-east of Brazil. Journ. mar. biol. Assoc. U.K., 92: 1-7.


CHARNIAUX-COTTON, H., 1957. Croissance, régénération et determinisme endocrien des carác-tères sexuels d’Orchestia gammarella (Pallas). Crustacé Amphipode. Ann. Sci. nat., (Zool.Biol. Anim.) 19(4): 411-560.

CHRISTY, J. H. & S. G. MORGAN, 1988. Estuarine immigration by crab postlarvae: mechanisms,reliability and adaptive significance. Mar. Ecol. Prog. Ser., 74: 51-65.

CHRISTY, J. H. & M. SALMON, 1984. Ecology and evolution of mating systems of fiddler crabs(genus Uca). Biol. Rev., 59: 483-509.

COELHO, P. A., A. O. ALMEIDA & L. E. A. BEZERRA, 2008. Checklist of the marine and estuarineBrachyura (Crustacea: Decapoda) of northern and northeastern Brazil. Zootaxa, 1956: 1-58.

COSTA, T. M., 2000. Ecologia de caranguejos semiterrestres do gênero Uca (Crustacea, Decapoda,Ocypodidae) de uma área de manguezal, em Ubatuba (SP): 1-121. (Ph. D. Thesis, Instituto deBiociências, UNESP, Botucatu, SP).

COSTA, T. M. & M. L. NEGREIROS-FRANSOZO, 1996. Fecundidade de Callinectes danae Smith,1869 (Crustacea, Decapoda, Portunidae) na região de Ubatuba (SP), Brasil. Brazilian Arch.Biol. Technol., 39(2): 393-400.

DÍAZ, H. & J. E. CONDE, 1989. Population dynamics and life history of the mangrove crab Aratuspisonii (Brachyura: Grapsidae) in a marine environment. Bull. mar. Sci., 45(1): 148-163.

FISHER, R. A., 1930. The genetical theory of natural selection: 1-318. (Oxford University Press,Oxford).

FRUSHER, S. D., R. L. GIDDINS & T. L. SMITH, 1994. Distribution and abundance of grapsoidcrabs (Grapsidae) in a mangrove estuary: effects of sediment characteristics, salinity tolerances,and osmoregulatory ability. Estuaries, 17(3): 647-654.

GEISEL, J. T., 1972. Sex ratio, rate of evolution, and environmental heterogeneity. American. Nat.,106: 380-387.

GOLLEY, F., H. T. ODUM & R. WILSON, 1962. A synoptic study of the structure and metabolismof a red mangrove forest in southern Puerto Rico in May. Ecology, 43: 9-18.

HAGEN, H.-O. VON, 1978. The systematic position of Sesarma (Sesarma) rectum Randall and anew definition of the subgenus Sesarma (Brachyura, Grapsidae). Crustaceana, 34(1): 45-54.

HARTNOLL, R. G., 1964. The freshwater grapsid crabs of Jamaica. Proc. Linn. Soc. London, 175(2):145-169.

— —, 1969. Mating in the Brachyura. Crustaceana, 16: 161-181.— —, 2006. Reproductive investment in Brachyura. Hydrobiologia, 557: 3-40.HENMI, Y., 2003. Trade-off between brood size and brood interval and the evolution of underground

incubation in three fiddler crabs (Uca perplexa, U. vocans and U. dussumieri). Journ. Crust.Biol., 23(1): 46-54.

HINES, A. H., 1982. Allometric constraints and variables of reproductive effort in brachyuran crabs.Mar. Biol., Berlin, 69: 309-320.

JOHNSON, P. T. J., 2003. Biased sex ratios in fiddler crabs (Brachyura: Ocypodidae): a reviewand evaluation of the influence of sampling method, size class and sex-specific mortality.Crustaceana, 76(5): 559-580.

LEME, M. H. A., 2002. A comparative analysis of the population biology of the mangrove crabsAratus pisonii and Sesarma rectum (Brachyura, Grapsidae) from the north coast of São PauloState, Brazil. Journ. Crust. Biol., 22(3): 553-557.

— —, 2004. Fecundity and fertility of the mangrove crab Sesarma rectum Randall, 1840 (Grap-soidea) from Ubatuba, São Paulo, Brasil. Nauplius, 12(1): 39-44.

— —, 2005. Size at sexual maturity of female crabs Sesarma rectum Randall (Crustacea, Brachyura)and ontogenetic variations in the abdomen relative growth. Rev. Brasileira Zool., 22(2): 433-437.

LEME, M. H. A. & M. L. NEGREIROS-FRANSOZO, 1998. Fecundity of Aratus pisonii (Decapoda,Grapsidae) in Ubatuba Region, state of São Paulo, Brazil. Iheringia, (Zool.) 84: 73-77.


LIMA, G. V., M. R. S. SOARES & L. M. Y. OSHIRO, 2006. Reproductive biology of the sesarmidcrab Armases rubripes (Decapoda, Brachyura) from an estuarine area of the Sahy River,Sepetiba Bay, Rio de Janeiro, Brazil. Iheringia, (Zool.) 96(1): 47-52.

LITULO, C., 2005. Population structure and reproductive biology of the fiddler crab Uca inversa(Hoffman, 1874) (Brachyura: Ocypodidae). Acta Oecol., 27: 135-141.

MANTELATTO, F. L. M. & A. FRANSOZO, 1997. Fecundity of the crab Callinectes ornatusOrdway, 1863 (Decapoda, Brachyura, Portunidae) from the Ubatuba Region, São Paulo, Brazil.Crustaceana, 70(2): 214-226.

— — & — —, 1999. Relative growth of the crab Sesarma rectum Randall, 1840 (Decapoda,Brachyura, Grapsidae) from Bertioga, São Paulo, Brazil. Pakistan Journ. mar. Biol., 5(1): 11-21.

MELO, G. A. S., 1996. Manual de identificação dos Brachyura (Caranguejos e Siris) do litoralBrasileiro: 1-604. (Plêiade FAPESP, São Paulo).

MIRANDA, I. & F. L. MANTELATTO, 2009. Estimating population features of the anomuran crabPetrolisthes armatus (Porcellanidae) in a remaining and impacted mangrove area of the westernAtlantic. Journ. nat. Hist., London, 43(33-34): 2027-2039.

MOCHEL, F. R., 1995. Endofauna do manguezal: 1-121. (EDUFMA, São Luís).MOUTON, E. C. & D. L. FELDER, 1995. Reproduction of the fiddler crabs Uca longisignalis and

Uca spinicarpa in a Gulf of Mexico salt marsh. Estuaries, 18: 469-481.NAGELKERKEN, I., S. J. M. BLABER, S. BOUILLON, P. GREEN, M. HAYWOOD, L. G. KIRTON,

J. O. MEYNECKE, J. PAWLIK, H. M. PENROSE, A. SASEKUMAR & P. J. SOMERFIELD, 2008.The habitat function of mangroves for terrestrial and marine fauna: a review. Aquat. Bot., 89:155-185.

NG, P. K. L. & P. J. F. DAVIE, 1995. The terrestrial sesarmine crabs of the genera Metasesarmaand Geosesarma (Crustacea: Decapoda: Brachyura: Grapsidae) of Ujung Kulon, west Jawa,Indonesia. Trop. Biodiv., 3: 29-43.

NG, P. K. L. & D. GUINOT & P. J. F. DAVIE, 2008. Systema Brachyurorum: Part 1. An annotatedchecklist of extant brachyuran crabs of the world. Raffles Bull. Zool., (Suppl.) 17: 1-286.

NICOLAU, C. F. & L. M. Y. OSHIRO, 2002. Aspectos reprodutivos do caranguejo Aratus pisonii(H. Milne Edwards) (Crustacea, Decapoda, Grapsidae) do manguezal de Itacuruçá, Rio deJaneiro, Brasil. Rev. Brasileira Zool., 19(Suppl. 2): 167-173.

OSHIRO, L. M. Y., 1999. Aspectos reprodutivos do caranguejo guaia Menippe nodifrons Stimpson(Crustacea, Decapoda, Xanthidae) da baia de Sepetiba, Rio de Janeiro, Brasil. Rev. BrasileiraZool., 16: 827-834.

PINHEIRO, M. A. A. & A. FRANSOZO, 2002. Reproduction of the speckled swimming crabArenaeus cribrarius (Brachyura: Portunidae) on the Brazilian coast near 23◦30′S. Journ. Crust.Biol., 22: 416-428.

POWERS, L. W. & D. E. BLISS, 1983. Terrestrial adaptations. In: F. J. VERNBERG &W. B. VERNBERG (eds.), The biology of Crustacea, 8, Environmental Adaptations: 271-334.(Academic Press, New York).

PRADO, A., 1999. Taxonomia, distribuição e ecologia da família Grapsidae (Crustacea, Decapoda,Brachyura) no litoral brasileiro: 1-315. (Master’s Thesis, Universidade Estadual Paulista, SãoPaulo).

PRIYADARSHANI, S. H. R., S. C. JAYAMANNE & Y. N. HIRIMUTHUGODA, 2008. Diversity ofmangrove crabs in Kaldokele, Negombo estuary, Sri Lanka. Sri Lanka Journ. aquat. Sci., 13:109-121.

SASTRY, A. N., 1983. Ecological aspects of reproduction. In: F. J. VERNBERG & W. B. VERNBERG

(eds.), The biology of Crustacea, 8, Environmental adaptations: 179-270. (Academic Press,New York).


SCHUBART, C. D., J. A. CUESTA, R. DIESEL & D. L. FELDER, 2000. Molecular phylogeny, tax-onomy, and evolution of non marine lineages within the American grapsoid crabs (Crustacea:Brachyura). Mol. Phylog. Evol., 15: 179-190.

SCHUBART, C. D., D. HORST & R. DIESEL, 1999. First record of Sesarma rectum Randall(Brachyura: Grapsidae: Sesarminae) from the Lesser Antilles. Crustaceana, 72(5): 537-538.

SCHUBART, C. D., T. WEIL, J. T. STENDERUP, K. A. CRANDALL & T. SANTL, 2010. Ongoingphenotypic and genotypic diversification in adaptively radiated freshwater crabs from Jamaica.In: M. GLAUBRECHT (ed.). Evolution in action — adaptive radiations and the origins ofbiodiversity: 323-349. (Springer-Verlag, Berlin, Heidelberg).

SILVA, S. M. J. & M. M. CHACUR, 2002. Population biology of Sesarma rectum Randall, 1840(Decapoda, Grapsoidea, Sesarmidae) at Itamambuca mangrove in northern littoral of São Paulostate, Brazil. Nauplius, 10(1): 47-51.

SILVA, S. M. J., G. L. HIROSE & M. L. NEGREIROS-FRANSOZO, 2007. Population dynamic ofSesarma rectum (Crustacea, Brachyura, Sesarmidae) from a muddy flat under human impact,Paraty, Rio de Janeiro, Brazil. Iheringia, (Zool.) 97(2): 207-214.

SILVA, Z. D. & L. M. Y. OSHIRO, 2002. Aspectos populacionais de Goniopsis cruentata (Latreille)(Crustacea, Brachyura, Grapsidae) na Baía de Sepetiba, Rio de Janeiro, Brasil. Rev. BrasileiraZool., 19(3): 907-914.

SKOV, M. W., M. VANNINI, J. P. SHUNULA, R. G. HARTNOLL & S. CANNICCI, 2002. Quantifyingthe density of mangrove crabs: Ocypodidae and Grapsidae. Mar. Biol., Berlin, 141: 725-732.

THORSON, G., 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev.,25: 1-45.

THURMAN, C. L., 1985. Evaporative water loss, corporal temperature and the distribution ofsympatric fiddler crabs (Uca) from south Texas. Comp. Biochem. Physiol., 119(1): 279-286.

VERGAMINI, F. G. & F. L. MANTELATTO, 2008. Continuous reproduction and recruitment in thenarrowback mud crab Panopeus americanus (Brachyura, Panopeidae) in a remnant human-impacted mangrove area. Invertebr. Reprod. Dev., 51(1): 1-10.

WANG, B., S. LIANG, W. ZJANG & Q. ZAN, 2003. Mangrove flora of the world. Acta bot. Sinica,45(6): 644-653.

WARNER, G. F., 1967. The life history of the mangrove tree crab Aratus pisonii. Journ. Zool.,London, 153: 321-335.

ZAR, J. H., 1984. Biostatistical analysis (2nd ed.): 1-130. (Prentice-Hall, Englewood Cliffs, NewJersey).

ZIMMERMAN, T. L. & D. L. FELDER, 1991. Reproductive ecology of an intertidal brachyurancrab, Sesarma sp. (nr. reticulatum), from the Gulf of Mexico. Biol. Bull., Woods Hole, 181:387-401.

First received 9 May 2011.Final version accepted 19 October 2011.

Population structure and reproductive biology of the fiddler crab Uca inversa (Hoffman, 1874)...

Documents

Transcript of Population structure and reproductive biology of the fiddler crab Uca inversa (Hoffman, 1874)...