Bio logy of II (A. Asakura，ed .)，Crust acean Resear ch，Sp ec ial Number6: 57-66，2006

Reproductive biology of laevimanus (Randall，1840) (: Anomura: ) from Inhaca Island，southern Mozambique

Carlos Litulo，Daniela Abreu and Christopher C. Tudge

Abstract.-Hermit crabs are one of the most 2000). Hermit crabs are anomuran decapod abundant taxa in the intertidal habitats of tropi- that developed some strategies cal estuarine areas. Despite this situation ，many to utilize gastropod shells and other type of aspects concerning their population ecology cavities to shelter their uncalcified abdomen. and reproduction are still poorly known.In this According to Litulo (2005)，there are currently study，the reproductive biology of the diogenid more than 900 specie sof hermit crabs world- ，Calcinus laevimanus was studied wide，ranging from the deeper parts of the with emphasis on size structure sex ratio recruit- ， ， oceans to intertidal habitats. Despite this situ- ment，breeding season and fecundity. Monthly ation，the population biology aspects of these samplings were conducted between January organisms are sti ll poorly known，principally in and December 2003 at Inhaca Island，southern Mozambique. Atotal of 1966 crabs were collected ， tro picale nvironments. represented by 760 males and 1206 females. The The large number of studies on hermit crabs size frequency distribution of the present popula- mostly focused on behavioural features such as tion showed an unimodal pattern skewed to the the use of gastropod shells and habitat selection right ，suggesting increased mortality in the larg- in both the 自eld andl aboratory (e.g. ，Tunberg et est size classes. Sexual dimorphism was evidenced al. ，1994 ;B arnes，1999; Turra & Leite，2001 a) by the larger sizes attained by males in relation However，studies on population structure to females. Moreover，sex ratios were female- and reproduction of hermit crabs have been biased during most of the study period. Juvenile conducted for E uropean and Mediterranean recruitment was constant with major peaks in (Lancaster，1988 ;Manjon-Cabeza & Garcia March and May，ovigerous females were present Raso，1994 ，1995 ，1998) ，temperate (Asakura year-round peaking February and April and egg & Kikuchi，19 84;[mazu & Asakura，1 994)， number increased with female size. The present tropical(Kamalaveni ，1949; Ameyaw-Akum自， resultsshow that reproduction and recruitment 19 75; Bertness，19 8 1) including South of Calcinus laevimanus displays high reproduc- American (Fransozo & Mantelatto，199 8; tive activity in the study area，as evidenced by the Mantelatto & Garcia 1999; Bertini& Fransozo constant presence of ovigerous females and the ， ， 2002; Martinelli etal. ，2002) and A 仕ican spe- high number of eggs carried by females. cies (Gherardi & Vannini，1989; Gherardi etal. ， 1994;Litulo ，2004; Litulo & Tudge，2005) . INTRODUCTlON Breedingperiods of hermit crabs have been D ecapod crustaceans represent a large frequently descri bed and reveal continuous number of li vin gspecies that inhabit awide to seasonalpatterns (Bertness，1981; Bertini variety of biotopes. Consequently，the study on & Fransozo，1999 ;Turra & Leite，2000) . decapod crustaceans is promising because the Reproductiveactivity can also be influenced establishment of these animalsin such diverse by the adequacy of shells use dby the crabs habitats derives from the evolution of adap- (Bertness，19 8 1;Mantelatto etal .，2002). tive population st rategies (Mant elatto & Sousa， Moreover，breeding activity can vary in re- 58 c. Litulo et al sponse to competition for shells in natural habi- Oetailed information on weather conditions as tats (Ameyaw-Akumfi，1975) well as detailed descriptions regarding the ecol - In East African region，stud ie son hermit ogy，fauna and ftora of the Island can be found crab biology are scarce (e.g. ，Ameyaw-Akumfi ， in Guerreiro etal. (1 996) 1975; Emmerson & Alexander，1 986; Reddy & Sampling was performed by two people Biseswar，1993) and，in particular reference to during aperiod of 1hour ，covering an area of Mozambique，they have been restricted to be- 300 m 2.Almost all hermit crabs were found in haviour and ecology (Bames，1997 ，1999). small aggregations of 5or more in small pools Calcinus laevimanus (Randall ，1840) is that were regularly searched during the study one of the most common hermit crabs in the period as reported for Calcinus tibic enin the Indo-Pacific region (Gherardi & Vannini，1989; southern Atlantic (Fransozo & Mantelatto， Reddy & Biseswar，1993; Tudge，1995a). At 1998). After collection，all individuals were both ebb and tlood tides ，C. laevimanus dis- bagged and transported immediately to the perse to feed on the substrate ，picking at the laboratory where they were removed by care- detritus-covered rocks and pebbles with its fully cracking each shel l. Sex was determined chelipeds (Gherardi & Vannini ，1989). With based on the position of gonopores (coxae of the incoming high tide ，it retreats into the rocks pereiopod 3for females and pereiopod 5for or pebbles. Often research on this species has males).The cephalothoracic shield length (SL been concerned with behaviour (Gherardi & =from the tip of the rostrum to the V-shaped Vannini，1989) and patterns of shell utilization groove at the posterior edge of the carapace) (Reddy & Biseswar，1993). With the exception was measured with the aid of Vernier callipers ( of research on spermatozoaland spermatophore 土 0.05 mmaccuracy) or under adissecting mi- ultrastructure (Tudge，1995b ，c) ，there is no croscope equipped with an ocular micromete r. information available on the general reproduc- Specimens were grouped in 0.5 mmsize -class tive biology of 仁 laevimanus assessed by sys・ intervals ，from 2.0to 10 .5mm . tematized study performed over along period. Ten eggs were removed from each oviger- This study addresses the paucity of information ous female for egg staging. Three stages of and describes the reproductive biology of C embryonic development were microscopically laevimanus from Inhaca Island ，an estuarine identi 自ed based on the amount of yolk and the region in southern Mozambique，with emphasis development of eye pigment (modified from on population size structure ，sex ratio ，juvenile Wada etal. ，1995 and Mantelatto & Garcia， recruitment，breeding season and fecundity. 1999). Stage I(I nitial): light-red ，newly deposited eggs completely filled with yolk and no signs MATERIALSAND METHODS of segmentation.Stage II (I ntermediate): eggs This study was conducted monthly from with less than 80% of yolk，and the develop- January to December 2003 on the full moon， ment of zoea observed.Stage [[[ (Finaり: dark- during low tide in the exposed pebble area grey eggs with less than 5% of yolk and zoea in front of the Marine Biological Station of fully developed just afew days from hatching. Inh aca，Island ，southern Mozambique (26 0 00' Twenty-five ovigerous females with eggs S，33 0 00'E). The climate at this location is a at stage [were selected for egg counting. mixture of tropical and subtropical ，partly in- Pleopods were removed from females，placed ftuenced by the South-Eastern trade wind，and in petri dishes 白l I ed with seawater，and eggs de- anortherly monsoon，but also occasionally tached by the gradual addition of asolution of by strong and cold South-West winds or cy- sodium hypochlorite (7 % ). Bare pleopods were clones from the North-Eas t. The winter (April then discarded by gently stirring in abeaker -September) is usually cold and dry，while filled with 200 ml seawater. Three 1.5 ml sub- summer (October-March) is warm and rainy. samples were taken using apipette ，with eggs Reproductive biolo gyof Calcinus lae vimanus 59 counted under adissecting microscope. The av- 仁二コMales (n =760) E コNon-ovigerous females (n =866 ) erage value obtained was then extrapolated for _ ・圃O vigerous females (n =340) the whole suspension to estimate the number of 芝 eggs (Ramirez L1 odra，2002) . The reproductive activity of the population was assessed asthe percentage of females ca ト rying eggs relative to the total number of fe- males collected (Fransozo & Mantelatto，1998; Turra & Leite，2000; Martinelli etal. ，2002). The monthly occuηence of ovigerous females was assessed through one-way ANOVA fo ト lowed by aScheffe's test for multiple com- parisons. The Chi-square test (X 2)was used to 10 evaluate sex ratio (M:F) and to compare male and female percentages per month.Data was Fi g.1 .Calcinus laevimanus. Overall size frequency distribution of individuals sampled at Inhaca Island ， assessed for normality and homogeneity of southern Mozambique. variance through the Kolmogorov-Smimov and Levene tests and the mean size of individuals is compared by the Student's t-test (Underwood， 1997).The occurrence of juveniles (here de- the study period. There was aunimodal size 自ned as individuals of both sexes smaller than distribution with normal distribution sli ghtl y the smallest ovigerous female) characterized skewed to the right for males (Kolmogorov- the recruitment in the population (Turra & Smirnov test ，KS = 0.986，P > 0.05)，non- Leite，2000) . ovigerous females (KS =0 .982，P > 0.05) and For fecundity analysis，data were analysed ovigerous females (KS =0.977 ，p > 0.05) .The using the linear function (Y =a + bX) of egg size frequency histogram shows ac1 ear preva- lence of individuals of both sexes measuring number (EN) versus shield length (SL). Mean 土 standard deviation (SD) is presented throughout 3.5to 5.5mm S L. The modal size ranged from the tex t. 3.5 to 4.5 mmSL for males and 4.5to 5.5 mm SL for non-ovigerous females and ovigerous females (Fig.1). RESULTS Monthly size frequency distributionsfor A total of 1966 crabs were sampled from males，non-ovigerous females and oviger- which 760 were males (38.7% )，866 non- ous females are shown in Fig. 2，where major ovigerous females (44.0% )and 340 ovigerous differences can be seen between each demo- females (17.3%).Data was homogeneously graphic category. Males often displayed uni distributed (Levene test ，p > 0.05). size and bimodal distribution ，while non-ovigerous (minimum，maximum ，and mean 士 SD) was and ovigerous females tended to be largely uni- 2.5 ，9.8 ，and 4.91 士 1.4 8 mmfor males; 2.0 ， moda l. Larger males were scarce in the popu- 5.5 ，and 4.27 土 0.71 mmfor non-ovigerous lation mainly in March，April ，May ，July and females; and 4.0 ，8 .2mm ，and 4.83 土 0.78 mm September. for ovigerous females respectively. Males were Overall sex ratio (M:F) was 1: 1. 59 in on average larger than ovigerous females (t = favour of females and significantly differed 56.28，p < 0.001)，which in turn were larger from the expected 1: 1(X 2 = 18.18，p <0.05). than non-ovigerous females (t = 48.78，P < Monthly sex ratios were female-bi ased dur- 0.05). ing the study period except for the month of Figure 1depicts the yearly size frequency January，and during the remainder of the year distribution for all hermit crabs sampled during the percentage of females was significantly 60 C .Litulo ela/.

25 -t Jan n= 10 3 15， 10 5 0 5

( ポ ) 〉 υ Z M コ O 凶 25 Z Jul l 15 J n= 184 h 10 。5 5 10 15 20 25

Dec n= 20 3

4 'S' (l '1'a' e '1" o 5 L (m m)

Fig. 2. Ca/cinus /aevimanus. Monthly siz巴什 equency distributions of individu als sampled durin gthe stud y period at lnhac alsland ，so uthern Mozambique ， (White bars = males，g rey bars = non- ovigerous females ， black bars = ovigerous females)

higher than that of males except in June，July bers were observed in August and Decembe r. and December (Table 1). Ca/cinus /aevimanus breeds continuous ly Juveniles (all crabs of both sexes <4.0 mm with peaks in February，April and October. The SL) appeared year-round with hi gher incidence months of Jul y，August and November，showed in March and May(Fig. 3). The lowest num・ the lowest frequency of egg-bear in gfemales Reproductive biology of Calcinus laevimanus 61

(Fig.4) 50

F 旬、 45 The number of eggs ranged from 600 (SL ES =4.0 mm) to 3000 (SL =8.2 mm)，with an av- 石U 』 40 erage of 1504 士 872 eggs. There was astrong ーj 35 positive relationship between increasing egg Z 30 number (EN) and increasing shield length (SL) w > 25 (N= 25 ，〆= 0.96394，p< 0 .001) (Fig. 5). a‘ 4‘ a‘ 4‘ 15 4・ 4‘ DISCUSSION 10 The overall size frequency distribution of 5 both sexes was unimodal with males reaching Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec larger sizes than both ovigerous and non-ovig- MONTHS erous females. This condition has been reported Fig. 3. Calcinus laevimanus. Percentage of juveniles in other populations of Calcinus laevimanus (all crabs く 4.0 mmSL) sampled at Inhaca !sla nd， in East Africa (Gherardi & Vannini，1989) southem Mozambique and in other sub-tropical and tropical hermit crabs: Calcinus tibicen (Herbst，1791) (see Fransozo & Mantelatto，1998) ，Clibanarius ment of megalopae occurs in the same habitat antillensis (Stimpson，1859) ，Clibanarius sc/o- as that occupied by the adults. petarius (Herbst，1796) ，Clibanarius vittatus The lack of larger individuals in the present (Bosc，1802) (see Turra & Leite，2000) ，and population of Calcinus laevimanus is also Loxopagurus loxochelis (Moreira，1901) (see evidenced by its skewed size frequency distri- Martinelli etal. ，2002) .According to Diaz & bution. Gherardi and colleagues (Gherardi & Conde (1989)，unimodality of size 仕equency Vannini，1989; Gherardi et al. ，1994) found a distributions generally characterizes adynamic similar skewed size frequency in their popula- equilibrium for acertain population，and the tions of C. laevimanus and C/ibanarius la e- occuπence of slight variations could reftect re ・ vimanus，respectively. Branco et al (2002) cruitment pulses，growth or different mortality reported the same phenomenon while studying rates. Moreover，this may indicate that settle- apopulation of Dardanus insignis (Saussure，

Table 1. Calcinus laevimanus. Total number of individuals ，percenta ge and sex ratio of crabs sampled at !nhaca !sland ，sout hem Mozambique from January to December 2003. (N =sample size; ns =not sig ni 白cant ， 2 *= significant deviation from the 1:1ratio through the X test ，p く 0.05) Males Females Total Sex ratio Month (川 % (川 % (川 (M:F) January 58 56.31 45 43.69 103 1:0.78ns February 31 18 .7 9 134 81.21 165 1:4.3 2ホ March 44 26.83 120 73. 17 164 1:2.73* April 60 32.6 1 124 67.3 9 184 1:2 .07 ホ May 66 42.04 91 57 .96 157 1: 1. 38* June 74 45.96 87 54.04 161 1: 1. 18 ns July 94 49.4 7 96 50.53 190 1: 1. 02 ns August 53 36.05 94 63.95 147 1: 1. 78* September 57 34.54 108 65 .4 5 165 1:1. 89 キ October 52 36.36 91 63.6 4 143 1:1. 75* November 72 39.13 112 60.87 184 1:1. 56* December 99 48.77 104 51 .2 3 203 1:1. 05 ns Total 760 38.66 1206 61 .3 4 1966 1:1. 59* 62 C. Litulo el al.

501 d 300 注，、、 y= - 1842.114 + 558.4 82 x .・ b E工 戸= 0.964，N =2 5，P < 0 .001 ::-- 401 b W 250 . 0〉 国 z 200 出 30 言 ..・・ コ z 。 (') 150 W 20 Eピ 。w u.. 100 .・・ 10 500 .....・

O 4 567 B 9 JanFebMarAprMayJun Jul AugSepOctNovDec SL (mm) MONTHS Fig. 5. Calcinus la evi manus.Regression analysis Fig. 4. Calcinus laevimanus .Reproductive activity between egg number (EN) and shield length (SL) in indicated by the frequency of ovigerous females females. through the study period at Inhaca Island ，southem Mozambique. (Labels indicate signi 日cant differences calculated by the Scheffe's test for multiple comparisons). their energy for structural metabolism; 2) the larger reproductive effort exhibited by males may be due to their ability to ferti lize more 1858) in 8razi l. Righf-skewed distributio ns than one female; 3) males of larger dimensions may be evidence of high mortality rates in cer- have agreater chance on obtaining females for tain populations (Underwood，1997). Branco et copulation as afunction of intraspeci 自c 白ghts . al. (2002) suggest that alack of larger individu- Moreover，sma ller growth rates of females als in apopulation mightbe physio logical or would be aconsequence of the utilization of be caused by adeficiency of shells in nature. re latively small shells and of the higher energy In fact ，large shells are often in limited sup- all ocation to reproduction in re lation to males ply in nature，so that hermit crabs are thought (Asakura，1992; 8ertini & Fransozo，2000) .We to be under heavy she lllimitation (Reddy & be lieve that allthese factors may influence the Biseswar，1993). Thissituation may be taking size of females in the present population of C. place at lnhaca Island because many people iα evimanus. co ll ect shells during low tide periods to sell in The overa ll and monthly sex ratios differed the markets and hotels for subsistence. This from the expected 1:1 proportion (Table 1). activity may be contributing to the skewness Several causes may lead to this discrepancy， in the size frequency distribution of C. laevi- such as differences between sexes in longevity manus. andgrowth rate ，differentia lmigration ，mortal- Calcinus laevimanus at Inhaca Is land， ity and sex reversa l. Sex reversal (hermaphro- Mozambique，is sexuall ydimorphic with males ditism) has been occasionally reported in her- being generally larger than both ovigerous and mit crabs (Turra ，2004) but the causes ruling its non-ovigerous females (Fig. 1). Asituatio na lso occurrence are still poorly known (Mantelatto seen in the Somalian populations of C. laevi- & Sousa，2000) .According to Werner (1972)， manus (Gherardi & Vannini ，1989). Abrams sex ratios differi ng 仕omthe 1:1are widespread (1988) states that three factors can influence amongcrustaceans. In hermit crabs ，females the sexual dimorphism of hermit crabs :1) tend to be more abundant than males (Ameyaw- the difference in energy available for growth， Akumfi，1975; Imazu & Asakura，1994 ; with males growing more because they do Martine l li et al. ，2002). Turra & Leite (2000) not expend energy in egg production ，but use state that this may be explained by higher mor- Reproductive biology of Calcinus laevimanus 63 tality acting on males or by habitat partitioning， are important mechanisms to stabilize apopula- differential feeding restriction or spatial disper- tion. Discontinuous or prolonged reproduction sion between sexes. Also important to address is also common among subtropical and tropi- is th esearch for and utilization of shells ，which cal hermit crabs. According to Turra & Leite are alimiting resource that may influence the (2000)，any hypothesis to explain the occur- sex ratio ，with males being more successful in rence ofpopulations with seasonal reproductive obtaining adequate shells in relation to females patterns in the tropics and with continuous pat- (Asakura，1992). tems in temperate regions may be based on the In our study juvenile recruitment was con- evolutionary histories of population although tinuous. These observations and the maximum local factors such as competition and sheJl use， size attained bythe specimens may support the should also be considered when assessing the hypothesis that recruitment may occur in the reproductive traits of aspecies or population. same habitats from those occupied by adults. Fecundity (number of eggs per egg c1 utch) Looking at Fig. 3，it can be seen that juveniles increased in proportion with female shield recruit mostly during winter (March-June) in length (Fig. 5). This was to be expected as the the study area. At Inhaca Island ，phyto ・ and egg number of most hermit crabs increases in zooplankton growth occurs from September para Jl el with female size (Mantelatto & Garcia， to November and amajor period of plankton 1999; Turra & Leite，2001 b; Mantelatto et al. ， abundance occurs by March due to nutrient ac- 2002; Litulo，2004; Macpherson & Raventos， cumulation along the winter season (Paula et 2004). SmaJl variations in the number of eggs al. ，1998). These observations may lead us to were observed within the same size classes. suggest that juvenile recruitment is synchro- According to Sastry (1983) and Mantelatto et nized with the abundance of food resources， al. (2002)，this can be related to accidental loss which are crucial for larval and juvenile of eggs，incomplete fertilisation or multiple growth. spawnings. Multiple spawnings (here defined Hermit crabs may display continuous as females spawning several times after each (with or without peaks) or seasonal reproduc- release of previous larvae) are generally char- tive patterns (Bertness，1981; Tunberg etal. ， acteristic in tropical hermit crabs due to small 1994;Manjon-Cabeza & Garcia Raso，1998) variations in environmental parameters，which regardless of the taxonomic group. As noted are very important for egg and larval develop- by Sastry (1983)，populations of agiven spe- ment (Sastry，1983) .The large jump (doubling) cies at different latitudes subjected to particular in egg number observed at about 6mm (SL) environrnental conditions may display different (Fig. 5) could represent the difference between reproductive patterns .Continuous or wide re- first mating (primaparous) and already mated productive periods shown by hermit crabs may (multiparous) females，or more likely is a be aresult of multiple spawnings or asynchrony consequence of agastropod host shell switch in reproduction. to alarger species providing more egg space Ovigerous females of C. la evimanus were (Mantelatto & Garcia，1999). found year-round in the study area but with The characterization of populations in peaks in February，April and October，suggest- natural habitats is important to understand ing acontinuous reproductive pattern (Fig. their life cycle and ecological stability. This 4). A similar pattern was found in Paguristes can be accomplished by describing patterns of tortugae studied by Mantelatto & Sousa (2000) distribution ，density ，dispersion ，sex ratio and and Clibanarius antillensis studied by Turra breeding periods that can be compared to other & Leite (2000). Continuous reproduction is populations of the same species，genus or other important for the determination of several char- taxonomic leve 1. Such comparisons are an im- acteristics of apopulation such as continuous portant strategy to verify differences among larval supply and juvenile recruitment，which populations and to understand the environmen- 64 C. Litulo et al tal constraints that are shaping the structure of season of the hermit crab P etro chirus diogenes these populations (Branco et al. ，2002). This (Anomura: Diogenidae) in the north coast of Sao Paulo State ，Brazi l. In: E. Escobar・Briones & F. data on Calcinus laevimanus is astarting point Alvarez，(eds .)，Modern Approaches to the Study to gaining this understanding for tropical herrnit of Crustacea，Kluwer Academic Publishers，The crabs，especially in the poorly studied region of Netherlands，pp .145 ー 150. East Africa. Bertness ，M. 0. ，1981. Seasonalityin tropical

hermit crab reproduction in the bay of Panama目 Acknowledgements.-We thank the Marine Biotropica ，13: 292-300. Biological Station of Inhaca lsland (EBMI) Branco，J .0 .，Turra ，A .，& Souto，F. X. ，2002. for lo gist ical support，and WIOMSA (Westem Population biology and growth ofthe hermit crab Dardanusinsignis at Armacao do It apocoroy， lndian Ocean Marine Science Association) for southern Brazi l. Joumal ofthe Marine Biologic al financial support. CCT wishes to acknowledge A sso ciation of the United Kingdom，82: 597- the support of Rafael Lemaitre and previous 603 IZ Department chairs at NMNH，Smithsonian Diaz，H .，& Conde ，1. E. ，1989 .Population dynamics Institution ，for access to resources. This manu- and life hi stor yof the mangrove crab A ratus pisonii (Brachyura，Grapsidae) in amarine script was substantially improved by the com- env ir onment. Bulletin of Marine Science，45 ments of two anonymous referees. 14 8- 163. Emmerson，W. 0. ，& Alexander，M. D .，1986. Shell utili zation and mo叩hometrics of the hermit crab LITERATURE CITED Diogenes brevirostr is Stimpson. South African Journal of Zoology，21: 211 -216.

Abrams，P. ，1988 .Sexual differences in resource use Fransozo，A .，& Mantelatto，F . し M.，1998 目 in hermit crabs; consequences and causes. ln : Population structure and reproductive period G. Chelazzi & M. Vannini ，(eds.) ，Behavioural of the tropical hermit crab Calcinus tibi cen Adaptation to the Int ertida lLife ，Plenum ，New (Decapoda: Diogenidae) in the region of York，pp .283 -296 Ubatuba，Sao Paulo，Brazi l. Journal of Ameyaw-Akumti，c. ，19 75. The breedin gbiology Biology，18: 738-745 of two sympatric species of tropical intertidal Gherardi ，F. ，& Vannini ，M .，19 89. Field hermit crabs ，Clibanarius chapini and C. observations on ac tivity and clu sterin gin two senegalensis. Marine Biology，29: 15 -28. intertidal hermit crabs ，C /i banarius vi rescens Asakura，A .，1992 .Population ecology of the sand- and Ca/cinu s/aevimanus (Decapoda，Anomura). dwelling hermit crab Diogenes nitidimanus M arine B ehaviour and Physiolo gy，14 :145 - 159 . Terao. 5. Ecological implication sin the pattems Gherardi ，F. ，Zatteri ，F. ，& Vannini ，M .，1994. of moulting.Journal of Crustacean Biology，12 : Hermit crabs in amangrove swamp: th es tructur e 537-545. of C /i banarius la evi manus clu sters .M arin e A sa kura，A. ，& Kikuchi ，T. ，1 984. Population Biology，12 1:4 1-52 ecology of the sand dwelling hermit crab ， Guerreiro，J .，Freitas ，S. ，Pereira ，P .，Paula ，J .，& Diogenes nitidimanus Terao 2. Migration and Macia，A .，1996 .Sediment macrobenthosof life history .Publications of the Amakusa Marine mangrove flat sat Inhaca Island ，M ozambique Biology Laboratory，7: 109- 123. Cahiers de Biologi eMarine ，37: 309-327. B arne s，D. K. A. ，1997. E cology of tropical Imazu ，M. ，& Asakura，A. ，1994 .Di stribution ， hermit crabs at Quirimba Island ，Mozambique: reproduction and shell utilization patt ern sin distribution ，abundance and activity .M arine three species of int ertidal hermit crabs on ar ocky Ecology Progress Series ，154 ・133- 142 . shor巴 on th ePacitic coast of Japan. Journal of Barnes，D. K. A. ，1999. Ecology of tropical hermit Experimental Marine Biology and Ecolo gy，1 84・ crabs at Quirimba Island ，Mo za mbique: Shell 42-65. characteristics and utilization. Marine Ecolo gy K amalaveni ，S. ，1949. On the ovaries ，copulation Progress Series ，1 83: 241 -251 and egg-formation in the hermit crab， Bertin i，G. ，& Fransozo，A .，2000. Population Clibanarius olivaceus Henderson (Crustacea， dynamics of P etro chirus diogenes(Crustacea ， Decapoda) .Jo urnal of the Zoological Society of Anomura，Diogenidae) in the Ubatuba region ， Indi a，1 :120 - 128 . Sao Paulo ，Brazi l. Crustacean Iss ue s，12: 221 Lancaster，1. ，19 88. Pagurus bernhardus (L). - An 24 1. introducti ont othe lif ehi stor yof hermit crabs . Bertini ，G. ，& Fransozo，A. ，2002. Breeding Field Studies ，7: 189-238. Reproductive biology of Calcinus laevimanus 65

Litulo ，C. ，2004. Fecundity and breeding biology of 75 :791 -802 the herrnit crab Diogenesbr evirostris (Stimpson ， Paula，J. ，Pinto ， 1.， Guambe，1. ，Monteiro ，S. ，Gove ， 1858) (Anomura: Diogenidae) from southern D. ，& Guerreiro，J. ，1998. Seasonal cycles Mozambique. Invertebrate Reproduction and of planktonic communities at Inhaca Island ， Development，46: 41 -46. southern Mozambique.Journal of Plankton Litulo，C. ，2005. Population structure and Research，20: 2165-2178. reproduction of the hermit crab Dardanus Ramirez L1 odra，E .，2002. Fecundity and Ii fe-history deformis (Anomura: Diogenidae) in the Indian strategies in marine invertebrates. Advances in Ocean. Journal of the Marine 8iological Marine 8iology，43: 87- 170 Association of the United Kingdom，85: 883- Reddy，T. ，& 8iseswar，R .，1993. Patterns of shell 887. utilization in two sympatric species of hermit Litulo ，C .，& Tudge，C .，2005. Population structure crabs from the Natal coast (Decapoda，Anomura ， and breeding season ofthe hermit crab Diogenes Diogenidae). Crustaceana，56: 13 -24. brevirostris Stimpson，1858 (Decapoda， Sastry，A. N. ，1983. Ecological aspects of Anomura，Diogenidae) from southern reproduction .In :F .Vernberg & w. Vernberg， Mozambique.Journal of Natural History，39 : (eds .)，The 8iology of Crustacea，8. 2887-2899. Environmental adaptations，Academ ic Press ， Macpherson，E. ，& Raventos，N. ，2004. Population New York，pp. 179-269. structure and reproduction of three sympatric Tudge，C. C .，1995a .Hermit Crabs of the Great species of hermit crabs in the north-western Barrier Reef and Coastal Queensland. 40 Mediterranean. Joumal of the Marine 8iological pp. School of Marine Science，University of Association of the United Kingdom，84 :371 - Queensland，Australia & Backhuys Publishers ， 376 Leiden. Manjon-Cabeza，M. E .，& Garcia Raso，J. E .， Tudge，C. c.， 1995b. Ultrastructure and phylogeny of 1994. Estructura de una poblacion del cangr句o the spermatozoa of the infraorders Thalassinidea ermitano C es topagurus timidus (Crustacea， and Anom ura (Decapoda，Crustacea). 1n: Decapoda，Anomura) de fondos de Posidonia B.G.M.Jamieson ，J. Ausio，& J. ・L. Justine ， oceanica del SE de Espana. Cahiers de 8iologie (eds.) ，Advances in Spermatozoal Phylogeny Marine，35 :225 -236. and . Memoires du Museum national Manjon-Cabeza，M. E. ，& Garcia Raso，J. E. ， d'Histoire naturelle (Paris) ，166 :251 -263. 1995 .Study of Calcinus tuhulαris (Crustacea， Tudge，C. C. ，1995c .The Ultrastructure and Diogenidae) 什om ashallow Posidonia oceanica Phylogeny of Anomuran Crab Spermatozoa meadow. Cahiers de 8iologie Marine，36: 277- 346 pp.Ph.D. Thesis，Zoology Department， 284. University ofQueensland，Brisbane ，Australia. Ma町on-Cabeza，M .E .，& Garcia Raso，J. E. ，1998. Tunberg，B. ，Nelson ，W. G. ，& Smith，G .，1994 . Population structure and growth of the hermit Population ecology of Pagurus maclaughlinae crab Diogenes pugilalor (Decapoda: Anomura Garcia-Gomez (Decapoda: Anomura: Paguridae) Diogenidae) from the Northwestern Atlantic. in the Indian River Lagoon，Florida. Joumal of Journal ofCrustacean 8iology，18: 753-762 Crustacean Biology，14: 686-699. Mantelatto，F し M .，& Garcia，R. 8. ，1999. Tuηa，A. ，& Leite ，F .P. P. ，2000. Population biology Reproductive potential of the hermit crab and growth of three sympatric species of Calcinus tihic en(Anomura) from Ubatuba，Sao intertida lhermit crabs in south-eastern 8razil Paulo，8razi l. Joumal of Crustacean 8iology，19: Journal of the Marine Biological Association of 268-275. the United Kingdom，80: 1061 - 1969 . Mantelatto，F. し M.，& Sousa，L .M .，2000 Turra，A. ，& Leite ，F .P. P. ，2001 a. Shell utilization Population dynamics of the hermit crab pattemsof atropical rocky intertidal herrnit crab Paguristes tortugaeSchmitt ，1933 (Anomura， assemblage: 1. The case ofGrande beach. Joumal Diogenidae) from Anchieta Island ，Ubatuba ， ofCrustacean 8iology，21: 393-406. 8razi l. Nauplius，8・ 185 - 193 Turra，A. ，& Leite ，F. P.P. ，2001 b.Fecundity of Mantelatto，F. L. M.，Alarcon ，V. F.，& Garcia ，R. B. ， three sympatric populations of hermit crabs 2002. Egg production strategies of the tropical (Decapoda，Anomura ，Diogenidae) .Crustaceana ， hermit crab Pagurisles lorlugae from Brazil 74: 1019- 1027. Journal ofCrustacean Biology，22 :390 -397. Tu汀 a，A. ，2005. Intersexuality in hermit crabs: role Martinelli ，1. M .，Mantelatto ，F. L. M .，& Fransozo， and fate of gonopores in intersex individuals A .，2002 .Population structure and breeding Joumal of the Marine Biological Association of season of the South Atlantic hermit crab the United Kingdom，84 :757 -759. Loxopagurus loxochelis (Anomura，Diogenidae) Underwood，A. J ，. 1997. Experiments in Ecology: 合om the Ubatuba re gion ，Brazi l. Crustaceana， their Logical Design and Interpretation Using 66 C .Litulo elal

Analysis of Variance 目 504 pp.Cambridge Ciencias 8iologicas，Faculdade de C ienc ia s， University Pres s，Cambridge. Universidade Eduardo Mondlane，Caixa Posta l257 ， Wada，S. ，Goshima ，S. ，& Nakao，S. ，1995 . Maputo，Mozambique; e-mail: (CL) Lit os @ uem Reproductive biology ofthe hermit crab Pagurus mz. CCT，1 nvertebrate Zoology，M RC 16 3， middendo砂ii 8randt (Decapoda: Anomura: National Muse um of Natural History，Smithsonian Diogenidae) .Crustacean Researc h，24: 23-32. In stitution ，Wa shin gton ，DC 20013-7012，U.S.A. ， Wemer，A. M.，1972. Sex ratio as afunction of size and Department of 8iology，American University， in marine Crustacea 目 American Naturalist ，106 : Washin gton ，D.C. 20016・8007，U.S.A. ;e-mail: 321 -350. tud gec @ si.edu *Author for correspondence Addresses: *CL，DA ，Departamento de