Rev. Biol. Trop., 46(3):673-678,1998

Reproductive patterns oC Aratus pisonii (: Grapsidae) Crom an estuarine area oC Sao Paulo Northern Coast, Brazil

Maria Helena de Arruda Lell1e1 & Maria Lucia Negreiros�Fransozol I Departamento de Zoología - Instituto de Biodencias � Caixa Posta1510 - Universidade Estadual Paulista - UNESP- 18618- 000 Botucatu (SP), Brasil. E-milil [email protected]. 2 Departamento de Zoologia - Instituto de Biociencias e Centro de Aqüicultura - Caixa.Postal 510 - Universidade Estadual Paulista - UNESP - 18618-000 Botucatu (SP), Brasil. Fax 014 - 821 3744. E-mail [email protected].

Received 8-VlII-1997. Corrected 8�VI-1998. Accepted 18-VI-1998.

Abstraet: Thispaper describes thefrequency of oecurrenee andreproductive pattems of the treemangrove erab Aratus pisonii. l\10nthly samples were taken from January 1993 lo June 1994 in an estuarinemaIlgrove. from Ubatuba regíon, Braiil. Ntót¡¡} of 1 078 , 489 males and 589 females (131 ovigerous females) w�re eollected.Carapace width ranged)'rpm'4.2 lo 25.9 mm. A surnrner reproductive followedpeak by a recruitment juvenile plllse was verified. FemaI�s \1ll!rem()réabundan! Ihan malesin the interrnediatesize Classes¡'Thesex-ratio in severalmonths was biased t9watdsj'einal�i:suggesting a poligynous popula,tion and migtation of females to fringes al the time of íncu­ batíon. andspawning.

Key -ívórds: Grapsid�e, Repi:óilueti�n, Sex�ratio, Aratuspisonii, Brazil.

The tree Aratus pisanii (H. Milne It ís well known that reproductive periodici­ Edwards 1837) is a tropical sesarminae ty may vary along a latítudinalgradient asa widely distributed in the western Atlantic from functionof envíronmental changes. Therelative central to Brazil, arid in the eastem importance of a given factor as cueing the initi­ Pacific from Nioaragua to (Melo 1996), atiQnof reproductive activities varíes among being commonly found 00 the upper HUoral species ,and' habitats. The identification of this zone in IUangroves. factor can clarify the cau§es of annuaJ ábim­ Many aspects concerning to the Ji fe cycle dance fluctuations in natural populations. and population biology. of A. pisonii have been The frequency of .o,ccurrence and the repro­ studíed in severalenvironments.(Hartnoll1965, ductive period oi the tree mangrove crab A. Wamer 1967, Díaz and Conde 1989;Conde and pisonii in subtropical estuannemangrove sys­ Díaz 1989a b). Tbose studies baverevealed the tem (230 29' S, 45Ciío' W) near the australlimit large plasticity ofthe life historyJeatures shown of its Western AUanticdistribution are ana}yzed by t.his species' populations inhabitingdifferent in .this study to provide information for f�her environments. comparative work. 674 REVISTA DE BIOLOGIA TROPICAL

MATERlALSAND METHODS RESULTS

Ubatuba is located in the northerncoast of Sao During the study period, a total of 1 078 Paulo State, Brazil. The climate in tbis region is were obtained; 489 males, 589 females, of tropical humid tending to subtropícal. Rainfall is which 131 were ovigerous. more intense fromSeptember lO March (springto The size of the individuals ranged from 4.2 summer). The "Comprido" and "Escuro" streams to 25.9 mm CW. The overall size frequency dis­ are the freshwater resource of the area and they tribution presented an unímodal and slightly drain into the Fortaleza Bay. The salinity varies asymmetric shape skewed to the left (Fig. 1). widely due the mixed tide regime in that region. Average size of both males and females was Monthly samples were carried out from 16.8 mm Cw. January 1993 to June 1994 in the fringe area of rnangrove near to the water, where theabundance of A. pisonii had been previously observed to be bigher than in ¡nlet areas. The animals were cap­ Males tured by hand from the roots and branches of the n= 489 mangrove trees. Samplings consisted of 1 hour catch-effort sessions conducted by two people during low lide. AH crabs were sexed and pres­ ence or absence of eggs in the females was recorded. Their carapace width (CW) was mea­ sured to the nearest 0.1 mm using a Vernier '0120 Pernales caliper. The crabs were grouped into eleven size n= 589 ffi 100 classes from 4.1 lO 26.0 mm Cw. ..o � 80 Recruitment pulses were verifiedin frequency 80 of individuals measuringfrom 4.1 to 8.0 mm Cw. 40 Indíviduals smaller than 4.1 mm CW were no! 20 considered due to the difficulty to determine accurately their sexo The reproductive period was determined Size Classes (mm) based on ovigerous female frequency in relation Fig. 1. Size (CW) frequency distribution of all males and to mature female along the year. Since the small­ females of A. pisonii collected during the study periodo est ovigerous females obtained measured 15.0 mm CW, only crabs grouped in the 14.1-16.0 mm size class or larger were regarded mature. As shown in the Fig. 2, juvenile crabs from Reproductive periodicity was statistically exam­ 4.1 to 8.0 mm CW were scarce being the high­ jned by means of binomial proportion analyses est frequencies recorded in June 1993, May and (Goodman 1965). The sex ratio in each month June 1994 (winter). Ovigerous females had and size class were examined by thisanalysis too. been present during almost all the months, vary­ The significance level adopted for all analyses ing from (lune 1993) to 68.2 % (March 1993) were 5%. O of the adult female population. Mean size of Due to the terrestrial habitsof tbis species the ovigerous females was 19.2 2.2 mm CW, association between proportíon of ovigerous ± ranging from 15.0 mm to 25.0 mm CW. The females and two factors (monthly average air ovigerous-ratio (Fig. 3A and B) was positively temperature and rainfall) was analyzed. correlated with monthly average rainfall Temperature and rainfall data were obtained in a (Pearson's linear correlátion, r =0.61; p < 0.01) nearby (4 Km) meteorological station of the and temperature (r = 0.70; p 0.005). University of Sao Paulo. < • LEME & NEGREIROS�I4ANSOZO:"ReproduGtive'. pattemsof Aratuspisoni¡ 75 " " '6

PERCENTAGE 676 REVISTA DE BIOLOGIA TROPICAL

TABLE 1 100 600 -0- Rainfall Variation in the sex-ratio of A. pisonii in each month.

90 o -0- OJigerous 500 Month/year Sample size Proportion 80 1) male/female � 70 e 400 Jan /1993 43 1 :1.86* Q) ¡'I / Feb 53 1 :1.52* � 60 � Mar 49 1 :1.04 A_ a, 050 300!!\, Apr 61 1 :1.35 Q) . \ May 75 1 :1.50* '40 • 1 Jun 45 1 :1.04 -'" 21 200 Jul 49 1: 1.04 � 30 JI ' Aug 29 1 :1.23 "!\�l\,, Sep 58 1 :1.15 20 / V 100 Oct 79 1 :1.02 • \ 1, Nov 62 1 :1.06 10 �vJ· . y Dec 68 1 :1.34 \ 0-0 o o Jan /1994 79 1 :1.82* JFMAMJJASONDJFMAMJ Feb 108 1 :1.35 -1993- -1994- Morths Mar 59 1 :1.27 Apr 53 1 :1.04 May 58 1.41 : 1 Jun 50 1.38 :1

*Statistically different (Goodman test, p < 0.05) 100 -ó- TeflllElraÍl.re 30

90 Deviations were observed in sornesíze class­ 80 es, these differences being statístically signifi­ cant in sorne cases (Table 2). Females were more numerous in the intermediate size classes, from 14.1 to 18.0 mm CW. Immature individu­ als from 4.1 to 14.0 mm CW did not present dif­ ferences in sexual proportions. In large crabs · \, 0 from 22 to 24 mm CW, males were significant­ tI \ 20 tJ ly more numerous than females (Goodman's � VI \ \\ \ · "1 I test, p < 0.05). Only a few specimens largerthan 20 \ ;°\1 24.0 mm were obtaíned. \ I \-0 \ 10 • \•

O��LL��-L���LL��\ 15 TABLE 2 JFMAMJJASONDJFMAMJ -1993- Morths -1994- Variation in the sex-ratio of A. pisonii in each size c/ass.

Size class (mm) Sample size Proportion male/ Fig. 3. Relationship between reproductive period (based on female the frequencyof A. pisonii ovigerous females) and the mean month1y pluviosity (A) and temperature (B). 4.1-6.0 29 1.23 :1 6.1-8.0 35 1 :1.19 8.1 -10.0 58 1.23 :1 10.1-12.0 52 1 : 1 Overall sex-ratio was 1: 1.2, not differing 12.1- 14.0 70 1 :1.26 14.1- 16.0 122 I :1.78* statistically from the 1 : 1 ratio. Remarkable 16.1- 18.0 208 1 : 1.57* deviations from 1 : 1 ratio were registered in 18.1- 20.0 238 1 :1.25 January, Februaryand May 1993 and in January 20.1-22.0 176 1 :1.12 22.1- 24.0 75 1.59 :1 * 1994, favouring females. Only in May andJune 24.1-26.0 17 1.12 :1 1994 males outnumbered females (Table 1). *Statistical1y different (Goodman test, p < 0.05) LEME & NEGREIROS-FRANSOZO: Reproductive pattems of Aratuspisonii 677

DISCUSSION during the rainy season, are conditions that probably prevent zoeae from stranding and The Oyeran size frequency distribution of A. osmoregulatory stress. pisonii is unimodal and asymmetric which usu­ In this study the sex-ratio does not differ ally reflects a population in equilibrium from the 1 : 1 in the smalIest classes but it does (Hartnoll and Bryant 1990). The modal varia­ differ in the intermediate size classes favouring tions in the size frequency distribution along the females and also in larger crabs favouring year were mainly caused by recruitment pulses, males, according to the "anomalous" pattem which were more evident in June 1993, May describedby Wenner (1972). Theig h hest and June 1994 (late autumn and early winter). female proportion in intermediate size classes However, juveniles could be also found in other (from 14 mm CW), match the size in which an months, but in smaller frequencies. This con­ important part of the population is sexually spicuous recruitment was probably a result of active. For A. pisonii, Warner (1967) suggests intense reproductive activity occured in March differential growth rates in which males reach 1993 and February and March 1994 (summer). large sizes faster due to the higher reproductive It can be supposed that the main period of effort of females which do not molt when they megalopa settlement occurred from late sum­ areincubating eggs. mer to earIy autumn, since the larval develop­ According to Giesel (1972) variations in the ment of this species includes four zoeal stages sex-ratio occur primarily during the main sea­ and a megalopa instar in approximately one sonal changes of environmental conditíons. month (Warner 1968). Warner (1967) reported that during the repro­ This reproduction and recruitment pattem ductive period of A. pisonii, females migrate could be a result of the geographical location of from the interior of the mangrove to water edge the studied area, a transitional faunistic region increasing the relative female frequency. with tropicalhumid climate tending to subtropi­ Peculiar characteristics of mangrove fringes, cal. In this latitude, intensive temperature such as humidity conditions provide more suit­ changes are likely to occur more often than in the able grounds to egg development and larval tropics. In this study the temperature was very release (Emmerson 1994). Furthermore, female correlated to the ovigerous rate as had been migration towards the fringes, possibly observed in other studies as the main factor influ­ enhances the chances of mate encounters. encing thereproduction (Fusaro 1980, Jones and Christy and Salmon (1984) assumed that sex­ Simons 1983, Siddiqui andAhmed 1992). ratio is associated to the mating system of each An extended breeding season with a peak of species, but Willson and Pianka (1963) pointed higher activity during the rainy season was out that this is not a cause-effect relationship. It observed in the present study, as those obtained could be suggested that female-biased sex-ratio by Díaz and Conde (1989) and Conde and Díaz observed herein may be related to a poligynous (1989a). Spawning in the rainy season may pro­ mating system in which males could mate with vide a selective advantage to intertidal decapods different females increasing the reproductive populations sínce that periods of higher rainfan output in population (Giesel 1972). However, rate can cause changes in the salinity of water further investigations are necessary to confirm (Pillay and Nair 1971, DeVries et al. 1983) and the relation between sex-ratio and mating sys­ also promote an increase of nutrientsconcentra­ tem in A. pisonii as in other decapods. tion, favouring the development of plank­ totrophic larvae (Siddiqui and Ahmed 1992), and an ¡ncrease of primary productivity and ses­ ACKNOWLEDGMENTS ton availability in the estuary (Rodriguez and Conde 1989). In the populatíon studied herein, To the "Conselho Nacional de Desenvolvi­ higher flow rate and seawards water velocity mento Científico e Tecnológico - CNPq" that 678 REVISTA DE BIOLOGIA TROPICAL provided fellowship for the first author. To Goodman L. A. 1965. On simult�eous confidence intervals Adilson Fransozo fromUNESP, Brazil for their Cor multinomial proportions. Technometrlcs 7: 247-254. suggestions. To the NEBECC memberS who Hartnoll R. G. 1965. Notes 00 the marine grapsid crabs oC helped us during thecollections. ! Jamaica. Proc. Linn. Soco Lond. 176:113-147. Hartnoll R. G. & A. D. Bryant. 1990. Size-Crequency distrl­ butions in decapod crustacea - the quick, the dead, and REFERENCES the cast-offs� J. Biol. 10: 14-19.

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