Estuarine, Coastal and Shelf Science 62 (2005) 283–290

www.elsevier.com/locate/ECSS

Population biology of the fiddler crab Uca annulipes(Brachyura: Ocypodidae) in a tropical East African

mangrove (Mozambique)

Carlos Litulo

Departamento de Ciencias Biologicas, Faculdade de Ciencias, Universidade Eduardo Mondlane, C.P. 257 Maputo, Mozambique

Received 21 April 2004; accepted 13 September 2004

Abstract

The community structure of the tropical fiddler crab Uca annulipes (H. Milne Edwards) has been studied in Mozambique for thefirst time. Ten 0.25 m2 squares were randomly sampled on a monthly basis during low tide periods from January to December 2002

at Costa do Sol Mangrove, Maputo Bay, southern Mozambique. A total of 981 crabs were captured, of which 494 were males(50.36%), 231 non-ovigerous females (23.85%) and 253 ovigerous females (25.79%). The overall size frequency distribution wasunimodal, with males being larger than both ovigerous and non-ovigerous females. Females were more abundant in the smallest size

classes while males outnumbered females in the largest ones. The overall sex ratio (1:0.99) did not differ from the expected 1:1proportion, but significant deviations were observed in January, April, August and November. Results indicate that the sizefrequency distributions of this species can also be determined through direct analysis of burrow openings. Breeding took place year-

round with two peaks of spawning in summer (January and December). Recruits were present throughout the year, with highabundance in summer probably due to the high reproductive activity observed in this season. The present results may allow us tosuggest that U. annulipes follows a rapid breeding cycle accompanied by a rapid larval development and settlement in the study area.� 2004 Elsevier Ltd. All rights reserved.

Keywords: Uca annulipes; population structure; reproductive biology; Mozambique; East Africa

1. Introduction

Among the macrofauna commonly found in man-grove forests brachyuran crabs are one of the mostimportant taxa with regard to number of species, densityand total biomass (Nobbs and McGuiness, 1999; Maciaet al., 2001; Skov and Hartnoll, 2001; Skov et al., 2002).Most of the mangrove crabs are fiddler crabs (FamilyOcypodidae, genus Uca) or sesarmid crabs (FamilyGrapsidae, subfamily Sesarminae) (Hartnoll et al.,2002).

E-mail address: litos@imensis.net

0272-7714/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2004.09.009

Ocypodids are the most dominant by number andgroup. They construct burrows and, as deposit-feedersand shredders, they rely for food on organic matter,either fine or coarse, associated with sediment surface(Olafsson and Ndaro, 1997; Skov and Hartnoll, 2001;Skov et al., 2002). Conversely, they can actively benefitfrom organic matter deposited on the sediment surfaceunder enriched situations, nutrient recycling and energyflow (Skov et al., 2002; Ashton et al., 2003).

Approximately 100 species of Uca have been de-scribed, most of which are tropical (Christy and Salmon,1984). These animals play an important part in marineecosystems, converting intertidal organic matter intosmall, bite-sized packages for many predators, both

284 C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

terrestrial (shore birds) and aquatic (marine crabs andfishes).

The study of breeding season in Crustacea canfacilitate the understanding of the adaptive strategiesand reproductive potential of a species and also itsrelationship with the environment and other species. Asreproduction is the main mechanism to guaranteespecies continuity, its study is of major importance.The reproductive strategy of brachyuran crabs isextremely diversified, ultimately shaped to maximizeegg production and offspring survivorship, thus in-creasing the preservation of the species (Hartnoll andGould, 1988).

Six species of fiddler crabs occur in East Africa: Ucaannulipes (H. Milne Edwards), Uca gaimardi (H. MilneEdwards), Uca inversa inversa (Hoffman), Uca vocanshesperiae (Linnaeus), Uca urvilei (H. Milne Edwards)and Uca tetragonon (Herbst) (Hartnoll, 1975; Skov andHartnoll, 2001). Although U. annulipes is the smallest ofthese species (Skov and Hartnoll, 2001), it is probablythe most numerous. It has an exceptionally verticalshore range (Skov and Hartnoll, 2001) and is anomnipresent component of East African mangroves.Like most ocypodids, it can run very fast and hencehides when it is disturbed by human activity. It dwells inburrows, which it digs to a depth of up to 50 cmdepending on shore level (Skov and Hartnoll, 2001).This crab is diurnally active, emerging as the tiderecedes. Mating is restricted to at least 5 or 6 days ofeach lunar cycle due to temporal restriction on optimalspawning time (Backwell and Passmore, 1996).

Often research on Uca annulipes has been restricted tosome behavioural (Backwell and Passmore, 1996;Jennions and Backwell, 1998) and ecological studies(Macia et al., 2001; Skov and Hartnoll, 2001; Skov et al.,2002). Regarding its reproduction, Emmerson (1994,1999) addresses questions related with breeding season,sex ratio and fecundity. Recently, Litulo (in press-a-b)investigated some external factor determining its re-production and fecundity. No previous work has beenpublished on the size structure and breeding season ofU. annulipes from Mozambique.

In the present study, the population biology of Ucaannulipes (H. Milne Edwards, 1837) is assessed withemphasis on size structure, sex ratio, breeding seasonand juvenile recruitment in a tropical mangrove inMaputo Bay, southern Mozambique. The reproductivepatterns in the ocypodidae are also reviewed.

2. Methods

2.1. Site description

Sampling took place at Costa do Sol Mangrove,Maputo Bay, southern Mozambique (25 �51#S and

26 �18#S). The mangrove vegetation of this area isdominated by Avicennia marina, although small patchesof Rizophora mucronata occur (Litulo, in press-b).Regarding crab fauna, Uca annulipes (H. MilneEdwards 1837) is the most dominant crab.

2.2. Sampling and analysis

Samples were taken monthly from January toDecember 2002 during low tide periods. Specimenswere collected by hand during the day-time by twopeople over a period of approximately 1 h over the samearea of about 500 m2.

At each sampling occasion, twenty 0.25 m2

(0.5 m! 0.5 m) squares were set out in the area fromwhich 10 were randomly chosen for sampling. Eachrandomised square was excavated with a corer toa depth of 30 cm. Collected crabs were bagged, labelledand preserved in 70% ethanol until further analysis. Inthe laboratory, specimens were sexed and checked foregg masses. Crab carapace width (CW) was measuredusing vernier calipers (G0.05 mm accuracy) or with theaid of a stereomicroscope (CW! 7.0 mm). Only crabslarger than 7.0 mm CW (the size of the smallest egg-bearing female recorded) were used to calculate thefrequency of ovigerous females. The relation betweencrab CW and burrow diameter was recorded for 110burrows. In this case measures of burrow diameter andcrab carapace width were obtained using a verniercaliper (G0.05 mm). Assessment of recruitment wasbased on the proportion of immature individuals in thesamples.

The population size structure was analysed asa function of the size frequency distribution of theindividuals. Specimens were grouped in 2.0 mm sizeclass intervals, from 4.0 to 22.0 mm CW. The period oftime when ovigerous females were found in the pop-ulation is referred to as the breeding season and all crabssmaller than the smallest egg-bearing female captured(CWZ 7.0 mm) were classified as juveniles.

The chi-square test (c2) was used to evaluate the sexratio and to compare male and female percentage andthe size frequency distribution was tested for normalityby the Kolmogorov–Smirnov Normality test (KS) (Zar,1999). The mean size of males and females andovigerous females and non-ovigerous females wascompared using the Student t-test (Zar, 1999).

3. Results

A total of 981 individuals were sampled during thestudy period, of which 494 were males (50.36%),243 non-ovigerous females (23.85%) and 253 ovige-rous females (25.79%) (Table 1). Size range withineach demographic category was 3.0–20.0 mm CW

285C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

Table 1

Uca annulipesdtotal number and sex ratios of individuals collected monthly at Costa do Sol Mangrove in 2002

Month Males % Non-ovigerous

females

% Ovigerous

females

% Total % Sex ratio

January* 47 4.79 6 0.61 24 80.01 77 7.85 1:0.64

February 31 3.16 13 1.32 21 61.76 65 6.63 1:1.10

March 36 3.67 17 1.73 21 55.26 74 7.54 1:1.06

April* 30 3.06 18 1.84 36 66.67 84 8.56 1:1.80

May 42 4.28 22 2.24 12 35.29 76 7.75 1:0.81

June 41 4.18 27 2.75 6 18.18 74 7.54 1:0.80

July 42 4.28 19 1.94 9 32.14 70 7.14 1:0.67

August* 64 6.52 16 1.63 22 57.89 102 10.40 1:0.59

September 52 5.30 23 2.34 23 50.06 98 9.99 1:0.88

October* 38 3.87 35 3.57 26 42.62 99 10.10 1:1.61

November* 31 3.16 23 2.34 23 50 77 7.85 1:1.48

December 40 4.08 15 1.53 30 66.67 85 8.66 1:1.13

Total 494 50.36 234 23.85 253 51.95 981 100 1:0.99

*Significant deviation from the expected 1:1 proportion (c2 test, p! 0.05).

(meanG SD: 10.33G 2.46) for males, 3.0–17.0 (7.01G2.66) for non-ovigerous females and 7.0–18.5 mm(9.31G 3.20) for ovigerous females. Males were signif-icantly larger than ovigerous females (tZ 13.94,p! 0.05), which in turn were larger than non-ovigerousfemales (tZ 9.31, p! 0.05).

Fig. 1 shows the yearly size frequency distributionsfor all sampled crabs. There was a conspicuous unim-odal size distribution for each sex, with non-normaldistribution for males (KSZ 0.290, p! 0.001), non-ovigerous females (KSZ 0.255, p! 0.001) and oviger-ous females (KSZ 0.235, p! 0.001), respectively.Females were more abundant in the smallest size classes(CW! 6.0 mm) while males were more concentrated inthe largest ones (CWO 13.0 mm).

Monthly size frequency distributions were in generaluni- and bi-modal (Fig. 2). Fairly bimodal distributions

4 6 8 10 12 14 16 18 20 2215

10

5

0

5

10

15

Carapace Width (CW, mm)

Males (n= 494) Non-ovigerous females (n=218) Ovigerous females (n=253)

Fig. 1. Uca annulipes (H. Milne Edwards, 1837). Overall size frequency

distribution of individuals collected at Costa do Sol Mangrove,

Maputo Bay, Southern Mozambique.

were recorded mainly in winter (May, June and July).Young recruits were observed year-round, as expectedfor a species with continuous reproduction.

The monthly number of crabs sampled throughoutthe year is listed in Table 1. Monthly sex ratios and theresults of the proportion analysis obtained according tothe month of collection and groups (males, non-ovigerous females and ovigerous females) were calcu-lated. The overall sex ratio was 1:0.99 and did not differsignificantly from the expected 1:1 proportion (c2 test,pO 0.05). However, significant deviations from theMendelian proportion were found in January, April,August and November (Table 1).

Fig. 3 presents the relationship between burrowdiameter (BD) and carapace width (CW) in Ucaannulipes. This was performed through the measurementof 110 burrows and tenant and yielded a highlysignificant coefficient of determination (r2Z 0.9823,p! 0.001), suggesting that the size structure of thiscrab can also be assessed through direct excavation ofburrow openings.

Reproductive activity, as indicated by the presence ofovigerous females, was continuous throughout the studyperiod (Fig. 4). Highest frequencies of egg-bearingfemales were found in January (80.0%) and December(66.67%). Moreover, their low occurrence in winter(from May to July) is evident.

4. Discussion

The overall size frequency distribution of Ucaannulipes at Costa do Sol Mangrove was unimodal,suggesting a stable population with continuous re-cruitment and constant larval mortality rates, a commonpattern found in other fiddler crabs (e.g. Colby andFonseca, 1984; Thurman, 1985; Costa and Negreiros-Fransozo, 2003). However, it shifted from the normality

286 C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

Carapace Width (mm)

30

20

10

0

10

20

30

Jann=77

30

20

10

0

10

20

Febn=65

30

20

10

0

10

20

Marn=74

30

20

10

0

10

20

Freq

uenc

y (%

)

Aprn=84

30

20

10

0

10

20

Mayn=76

430

20

10

0

10

20

Junn=74

30

20

10

0

10

20

30

Juln=70

30

20

10

0

10

20

Augn=102

30

20

10

0

10

20

Sepn=98

30

20

10

0

10

20

Octn=99

30

20

10

0

10

20

Novn=77

30

20

10

0

10

20

Decn=85

6 8 10 12 14 16 18 20 22 4 6 8 10 12 14 16 18 20 22

Fig. 2. Uca annulipes (H. Milne Edwards, 1837). Monthly size frequency distributions of crabs collected at Costa do Sol Mangrove, Maputo Bay,

Southern Mozambique. White bars: males, grey bars: non-ovigerous females and black bars: ovigerous females.

287C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

for both sexes. Testing departures from Poissondistributions may be used to support the hypothesis ofrandomness and independence of certain time andspatial scales (Zar, 1999). Poisson-like size frequencydistributions can be found in certain situations in fiddlercrabs due to seasonal mortality pulses in harshenvironmental conditions (Thurman, 1985).

Sexual dimorphism in the present population wasobserved, with males reaching larger sizes than females.Sexual dimorphism has been documented in otherbrachyuran crabs (Spivak et al., 1991; Johnson, 2003;Mantelatto et al., 2003). Sastry (1983) and Johnson(2003) suggest that females may have reduced growthrates because they concentrate their energetic budget ongonad development, a fact that may lead to a lowsomatic growth than observed in males. On the otherhand, males reach larger sizes due to the requirement tofertilise more than one female and, at the same time,

2 4 6 8 10 12 14 16 18 202

4

6

8

10

12

14

16

18

20

Car

apac

e W

idth

(C

W, m

m)

Burrow Diameter (BD, mm)

Y = 1.0196X-0.2396r2=0.9823p<0.0001n=110

Fig. 3. Relationship between burrow diameter (BD, mm) and carapace

width (CW, mm) in Uca annulipes from Costa do Sol Mangrove.

J F M A M J J A S O N D10

20

30

40

50

60

70

80

90

100

Sampling period

Fig. 4. Frequency of ovigerous females Uca annulipes from Costa do

Sol Mangrove, Maputo Bay, southern Mozambique. Error bars:

GSD.

males with larger dimensions have greater chances ofobtaining females for copulation and to win intra-specific fights (Christy and Salmon, 1984; Johnson,2003).

Analysis of monthly size frequency distributionsrevealed that the present population presents uni- andbi-modal distributions throughout the study period.This may indicate the existence of two different agegroups in the studied population. Such patterns havebeen attributed to migration, differential mortality andgrowth rates (Diaz and Conde, 1989; Yamaguchi, 2001;Colpo and Negreiros-Fransozo, 2004). Differences inmonthly size frequency distributions are typically foundin individuals that produce several clutches per in-dividual (Rabalais, 1991; Spivak et al., 1991; Moutonand Felder, 1995).

In this study, the overall sex ratio did not differsignificantly from the expected 1:1 ratio, but significantdeviations were observed in some months. In Crusta-ceans, sexual differences in distribution and mortalitymay be responsible for unbalanced sex ratios (Johnson,2003). Disparity in the sex ratio might also result fromdifferential life span and growth rates and samplingartefact (Wenner, 1972; Johnson, 2003). Thurman(1985) and Diaz and Conde (1989) argued that,unbalanced sex ratios could regulate the size of thepopulation by affecting its reproductive potential.

The diameters of Uca annulipes burrows (BD) werecorrelated to crab carapace width (CW). The same trendwas reported by Christy (1982b) in Uca pugilator,Mouton and Felder (1996) in Uca longisignalis, Drayand Paula (1998) in Dotilla fenestrata and Skov andHartnoll (2001) in U. annulipes from Zanzibar (Tanza-nia). The relationship between burrow diameter andanimal size implies that the size structure of this speciesmay be estimated from the analysis of burrow openings,and, shows that crabs fit tightly in the respectivegalleries, which may be fundamental for preventingthem from being displaced from their burrows by largercrabs and predators.

Reproduction of Uca annulipes at Costa do Sol asindicated by the presence of ovigerous females wascontinuous throughout the year, with peaks of occur-rence of egg-bearing females in summer. This is inagreement with previous studies carried out in sub-tropical and tropical areas (Emmerson, 1994; Costa andNegreiros-Fransozo, 2003; Colpo and Negreiros-Fran-sozo, 2004). In most subtropical and tropical regions,reproduction occurs during the warmer months, a periodwhen food sources are more abundant in the plankton(Sastry, 1983; Ashton et al., 2003). Looking at Table 2,it is possible to see that in tropical regions, reproductionis more prolonged than in temperate regions. Addition-ally, year-round reproduction as observed in the presentspecies, ensures a constant larval supply, which maydetermine some aspects of population dynamics such as

288 C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

Table 2

Summary of reproductive patterns and peaks in fiddler crabs from different regions

Species Spawning season Breeding pattern Study site Months Source

Uca annulipes Mar–Apr Seasonal RSA (31 �47#S, 29 �25#E) 2 Emmerson (1994)

Uca annulipes Jan–Dec Continuous Mozambique (25 �51#S, 26 �18#S) 12 Present study

Uca chlorophthalmus Dec–Apr Seasonal RSA (31 �47#S, 29 �25#E) 6 Emmerson (1994)

Uca dussumieri Feb–Dec Continuous Malaysia (03 �24#N, 101 �12#E) 12 MacIntosh (1989)

Uca lactea Jul–Aug Seasonal Japan (130 �16#N, 324 �16#W) 5 Murai et al. (1987)

Uca lactea Jun–Aug Seasonal Japan (130 �16#N, 324 �16#W) 9 Yamaguchi (2001)

Uca longisignalis Apr–Aug Seasonal USA (29 �38#N, 92 �46#W) 6 Mouton and Felder (1995)

Uca minax May–Sep Seasonal USA (33 �21#N, 33 �19#S) 5 Christy (1982b)

Uca panacea Apr–Sep Seasonal USA (29 �19#N, 94 �45#W) 6 Caravello and Cameron (1987)

Uca pugilator May–Sep Seasonal USA (33 �21#N, 33 �19#S) 5 Christy (1982a,b)

Uca pugilator May–Aug Seasonal USA (35 �37#N, 77 �25#W) 4 Colby and Fonseca (1984)

Uca pugnax May–Sep Seasonal USA (33 �21#N, 33 �19#S) 5 Christy (1982a,b)

Uca rosea Sep–Dec Seasonal Malaysia (03 �N, 101 �2#E) 3 Murai et al. (1996)

Uca rosea Sep–Nov Continuous Malaysia (03 �24#N, 101 �12#E) 12 MacIntosh (1989)

Uca spinicarpa Feb–Apr Seasonal USA (29 �38#N, 92 �46#W) 6 Mouton and Felder (1995)

Uca subcylindrica Mar–Sep Seasonal USA (29 �38#N, 92 �46#W) 6 Rabalais and Cameron (1983)

Uca subcylindrica Aug–Sep Seasonal USA (29 �38#N, 92 �46#W) 2 Thurman (1985)

Uca tangeri May–Jul Seasonal Portugal (36 �58#W, 7 �51#S) 3 Wolfrath (1993)

Uca tangeri Aug–Mar Seasonal Spain (36 �23#N, 6 �15#W) 6 Rodriguez et al. (1997)

Uca thayeri Mar–Sep Seasonal Brasil (23 �29#S, 45 �09#W) 10 Costa and Negreiros-Fransozo (2003)

Uca uruguayensis May–Aug Seasonal Argentina (37 �46#S, 57 �27#W) 4 Spivak et al. (1991)

Uca urvillei Jan–May Seasonal RSA (31 �47#S, 29 �25#E) 10 Emmerson (1994)

Uca vocans hesperiae Oct–Nov Seasonal RSA (31 �47#S, 29 �25#E) 8 Emmerson (1994)

Uca vocator Nov–Mar Seasonal Brasil (23 �49#S, 46 �09#W) 9 Colpo and Negreiros-Fransozo (2004)

Uca vocator Jan–Mar Seasonal Brasil (23 �24#S, 45 �03#W) 6 Colpo and Negreiros-Fransozo (2004)

Uca vocator Jan–Apr Seasonal Brasil (23 �24#S, 45 �00#W) 9 Colpo and Negreiros-Fransozo (2004)

continuous recruitment pattern and unimodal sizefrequency distribution, leading to maintenance of sizepopulation (Diaz and Conde, 1989).

The reproductive biology of decapod Crustaceansexhibits a latitudinal pattern, with smaller crabsinhabiting low geographical areas and larger crabshigher ones (Lardies and Castilla, 2001). In the presentstudy, the smallest ovigerous female captured was7.0 mm CW, compared to 8.0 mm CW for the smallestreproducing female found by Emmerson (1994) for Ucaannulipes at Mgazana, South Africa. Considering thepotential differences observed in maturation and re-productive activity related to geographical locations (thedistance between Costa do Sol and Mgazana is about750 km), it is possible to state that U. annulipes attainssexual maturation earlier at Costa do Sol.

More recently, Litulo (in press-b) found that thebreeding season of Uca annulipes is controlled bytemperature and rainfall at Costa do Sol Mangrove.Temperature is known to regulate moulting andoogenesis in crustaceans (Meusy and Peyen, 1988).Rainfall is known to cause changes in the salinity ofwater, and also promote an increase in nutrients ofplanktonic larvae, which can reduce food competitionbetween larvae.

Recruitment was constant throughout the year asa result of the high reproductive activity observed in thepopulation. However, analysing Fig. 2, it may be seenthat the presence of recruits increased at the end of

summer and winter. Costa and Negreiros-Fransozo(2003) and Colpo and Negreiros-Fransozo (2004) havereached the same conclusion. In species with continuousbreeding and recruitment, one would be expected to seerelatively stable size frequency distributions throughoutthe year (Thurman, 1985; Diaz and Conde, 1989).Moreover, in such species, it is common to determinegrowth patterns by analysing graphically the modalprogression of successive size frequency distributions,because larger numbers of juveniles are recruited duringa shorter period (Spivak et al., 1991). In the case of Ucaannulipes, it is not possible to address the same issue assmall number of juveniles was recorded.

Acknowledgements

I would like to thank the Laboratory of Ecology ofthe Universidade Eduardo Mondlane for logistic sup-port. Yolanda Mahanjane is deeply thanked for helpingwith the collections. Thanks to Dr. Eric Wolanski forhis valuable advice when we were attending theThird WIOMSA Scientific Symposium held in Maputobetween 15 and 18 October 2003. Special thanks toDrs. Michael S. Rosenberg, John H. Christy, Martin W.Skov and three referees (R. Hartnoll, E.C. Ashton andE.D. Spivak) for helpful correction that improved themanuscript.

289C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

References

Ashton, E.C., MacIntonsh, D.J., Hoghart, P.J., 2003. A baseline study

of the diversity and community ecology of crab and molluscan

macrofauna in the Sematan mangrove forest, Sarawak, Malaysia.

Journal of Tropical Ecology 19, 127–142.

Backwell, P.R.Y., Passmore, N.I., 1996. Time constraints and multiple

choice criteria in the sampling behaviour and mate choice of the

fiddler crab, Uca annulipes. Behavioural Ecology and Sociobiology

38, 407–416.

Caravello, H.E., Cameron, G.N., 1987. Foraging time in relation to

sex by the Gulf coast fiddler crab (Uca panacea). Oecologia 72,

123–126.

Christy, J.H., Salmon, M., 1984. Evolution of mating systems of

fiddler crabs (Genus Uca). Biological Reviews 59, 483–509.

Christy, J.H., 1982a. Adaptive significance of semilunar cycles of larval

release in fiddler crabs (Genus Uca): test of a hypothesis. Biological

Bulletin 163, 251–263.

Christy, J.H., 1982b. Burrow structure and use in the sand fiddler crab

Uca pugilator (Bosc). Animal Behaviour 30, 687–694.

Colby, D.R., Fonseca, M.S., 1984. Population dynamics, spatial

dispersion and somatic growth of the sand fiddler crab Uca

pugilator. Marine Ecology Progress Series 16, 269–279.

Colpo, K.D., Negreiros-Fransozo, M.L., 2004. Comparison of the

population structure of the fiddler crab Uca vocator (Herbst, 1804)

from three subtropical mangrove forests. Scientia Marina 68, 139–

146.

Costa, T.M., Negreiros-Fransozo, M.L., 2003. Population biology of

Uca thayeri Rathbun, 1900 (Brachyura, Ocypodidae) in a sub-

tropical south American mangrove area: results from transect and

catch-per-unit-effort techniques. Crustaceana 75, 1201–1218.

Diaz, H., Conde, J.E., 1989. Population dynamics and life history of

the mangrove crab Aratus pisonii (Brachyura, Grapsidae) in

a marine environment. Bulletin of Marine Science 45, 149–163.

Dray, T., Paula, J., 1998. Ecological aspects of the populations of the

crab Dotilla fenestrata (Hilgendorf, 1869) (Brachyura: Ocypodi-

dae), in the tidal flats of Inhaca Island (Mozambique). Journal of

Natural History 32, 1525–1534.

Emmerson, W.D., 1994. Seasonal breeding cycles and sex ratios of

eight species of crabs from Mgazana, a mangrove estuary in

Transkei, South Africa. Journal of Crustacean Biology 14, 158–

168.

Emmerson, W.D., 1999. Comparative fecundity and reproduction in

seven crab species from Mgazana, a warm temperate southern

African mangrove swamp. Crustacean Issues 12, 499–512.

Hartnoll, R.G., 1975. The Grapsidae and Ocypodidae (Decapoda:

Brachyura) of Tanzania. Journal of Zoology 177, 305–328.

Hartnoll, R.G., Gould, P., 1988. Brachyuran life history strategies

and the optimization of egg production. Zoological Symposium 59,

1–9.

Hartnoll, R.G., Cannicci, S., Emmerson, W.D., Fratini, S., Macia, A.,

Mgaya, Y., Porri, F., Ruwa, R.K., Shunnula, J.P., Skov, M.W.,

Vannini, M., 2002. Geographic trends in mangrove crab abun-

dance in East Africa. Wetlands Ecology and Management 10,

203–213.

Jennions, M.D., Backwell, P.R.Y., 1998. Variation in courtship ratio

the fiddler crab Uca annulipes: is it related to male attractiveness?

Behavioural Ecology and Sociobiology 9, 605–611.

Johnson, P.T.J., 2003. Biased sex ratios in fiddler crabs (Brachyura,

Ocypodidae): a review and evaluation of the influence of sampling

method, size class and sex-specific mortality. Crustaceana 76,

559–580.

Lardies, M.A., Castilla, J.C., 2001. Latitudinal variation in the

reproductive biology of the commensal crab Pinnaxodes chilensis

(Decapoda: Pinnotheridae) along the Chilean Coast. Marine

Biology 139, 1125–1133.

Litulo, C. Fecundity of the pan-tropical fiddler crab Uca annulipes (H.

Milne Edwards, 1837) from Costa do Sol Mangrove, Maputo Bay,

southern Mozambique. Western Indian Ocean Journal of Marine

Science, in press-a.

Litulo, C. Reproductive aspects of the fiddler crab Uca annulipes (H.

Milne Edwards, 1837) (Brachyura: Ocypodidae) at Costa do Sol

Mangrove, Maputo Bay, southern Mozambique. Hydrobiologia, in

press-b.

Macia, A., Quincardete, I., Paula, J., 2001. A comparison of

alternative methods for estimating population density of the fiddler

crab Uca annulipes at Saco mangrove, Inhaca Island (Mozambi-

que). Hydrobiologia 449, 213–219.

MacIntosh, D.J., 1989. The ecology and physiology of decapods of

mangrove swamps. Proceedings of the Zoological Society of

London 59, 315–341.

Mantelatto, F.L.M., Faria, F.C.R., Garcia, R.B., 2003. Biological

aspects of Mithraculus forceps (Brachyura: Mithracidae) from

Anchieta Island, Ubatuba, Brazil. Journal of the Marine Biological

Association of the United Kingdom 83, 789–791.

Meusy, J., Peyen, G.G., 1988. Female reproduction in malacostracan

Crustacea. Zoological Science 5, 217–265.

Mouton, E.C., Felder, D.L., 1995. Reproduction of the fiddler crabs

Uca longisignalis and Uca spinicarpa in a Gulf of Mexico salt

marsh. Estuaries 18, 469–481.

Mouton, E.C., Felder, D.L., 1996. Burrow distribution and population

estimates for the fiddler crabs Uca longisignalis and Uca spinicarpa

in a Gulf of Mexico salt marsh. Estuaries 19, 51–61.

Murai,M.,Goshima, S.,Henmi,Y., 1987.Analysis of themating system

of the fiddler crab Uca lactea. Animal Behaviour 35, 1334–1342.

Murai, M., Goshima, S., Kawai, K., Yong, H.-S., 1996. Pair formation

in the burrows of the fiddler crab Uca rosea (Decapoda:

Ocypodidae). Journal of Crustacean Biology 16, 522–528.

Nobbs, M., McGuiness, K.A., 1999. Developing methods for

quantifying the apparent abundance of fiddler crabs (Ocypodi-

dade: Uca) in mangrove habitats. Australian Journal of Ecology

24, 43–49.

Olafsson, E., Ndaro, S.G.M., 1997. Impact of the mangrove crabs Uca

annulipes and Dotilla fenestrata on meiobenthos. Marine Ecology

Progress Series 158, 225–231.

Rabalais, N.N., Cameron, J.N., 1983. Abbreviated development of

Uca subcylindrica (Stimpson, 1859) (Crustacea, Decapoda, Ocypo-

didae) reared in the laboratory. Journal of Crustacean Biology 3,

519–541.

Rabalais, N.N., 1991. Egg production in crabs with abbreviated

development. Crustacean Issues 12, 217–234.

Rodriguez, A., Drake, P., Arias, A.M., 1997. Reproductive periods

and larval abundance of the crabs Panopeus africanus and Uca

tangeri in a shallow inlet (SW Spain). Marine Ecology Progress

Series 149, 133–142.

Sastry, A.N., 1983. Ecological aspects of reproduction. In:

Vernberg, F.J., Vernberg, B. (Eds.), The Biology of Crustacea,

vol. 8. Academic Press, New York, pp. 179–270.

Skov, M.W., Hartnoll, R.G., 2001. Comparative suitability of

binocular observation, burrow counting and excavation for the

quantification of the mangrove fiddler crab Uca annulipes (H.

Milne Edwards). Hydrobiologia 449, 201–212.

Skov, M.W., Vannini, M., Shunnula, J.P., Hartnoll, R.G., Cannicii, S.,

2002. Quantifying the density of mangrove crabs: Ocypodidae and

Grapsidae. Marine Biology 141, 725–732.

Spivak, E.D., Gavio, M.A., Navarro, C.E., 1991. Life history and

structure of the world’s southernmost Uca population: Uca

uruguayensis (Crustacea, Brachyura) in Mar Chiquita lagoon

(Argentina). Bulletin of Marine Science 48, 679–688.

Thurman, C.L., 1985. Reproductive biology and population structure

of the fiddler crab Uca subcylindrica (Stimpson). Biological Bulletin

169, 215–229.

290 C. Litulo / Estuarine, Coastal and Shelf Science 62 (2005) 283–290

Wenner, A.M., 1972. Sex ratio as a function of size in marine

Crustacea. American Naturalist 106, 321–350.

Wolfrath, B., 1993. Observations on the behaviour of the European

fiddler crab Uca tangeri. Marine Ecology Progress Series 100,

111–118.

Yamaguchi, T., 2001. The breeding period of the fiddler crab, Uca

lactea (Decapoda, Brachyura, Ocypodidae) in Japan. Crustaceana

74, 285–293.

Zar, J.H., 1999. Biostatistical Analysis. Prentice-Hall, New Jersey,

930 pp.