Corresponding author.*

Invertebrate Reproduction and Development, 54:2 (2010) 95–109 95Balaban, Philadelphia/Rehovot

0168-8170/10/$05.00 © 2010 Balaban

Post-larval morphology, growth, and development ofUca cumulanta Crane, 1943 (Crustacea, Decapoda, Ocypodidae)

under laboratory conditions

GUSTAVO LUIS HIROSE , EDUARDO ANTONIO BOLLA JÚNIOR and1*,2 2

MARIA LUCIA NEGREIROS FRANSOZO2

Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Sergipe, UFS,1

Cidade Universitária Prof. “José Aloísio de Campos”, Av. Marechal Rondon, s/n, Jardim Rosa Elze,49100-000 São Cristóvão, Sergipe, Brazil

email: hirose@ufs.brNEBECC (Study Group of Crustacean Biology, Ecology and Culture), Departamento de Zoologia, Instituto de Biociências,2

Universidade Estadual Paulista (UNESP), 18618-000 Botucatu, São Paulo, Brazil

Received 26 January 2010; Accepted 24 May 2010

Abstract

Studies on the post-larval morphology and growth of crabs can allow correct identification of their

early life stages, supporting studies on phylogenetic relationships and ecological aspects. Never-

theless, little is known about the juvenile morphology of ocypodoid crabs worldwide. Uca

cumulanta Crane, 1943 is a fiddler crab commonly found in the intertidal zone of the tropical and

subtropical western Atlantic. This study describes the morphology of the first juvenile stage of

U. cumulanta, its absolute and relative growth, and the appearance and development of its secondary

sexual characters. The antennules of U. cumulanta show morphological peculiarities and could

probably be used as a distinguishing feature for crabs of this genus. The maxillule and the maxilla

have sets of setae forming specialised structures for sorting particles from the sediment. The absolute

growth pattern differed statistically between sexes. The study of relative growth revealed differences

in the relationships cheliped propodus length (CPL), cheliped propodus height (CPH), and abdomen

width (AW) vs. carapace length (CL). These differences between sexes showed that males diverge

from females (in the chelipeds) from 3.04±0.11 mm (VI juvenile stage), and females diverge from

males (in the abdomen) from 3.84±0.13 mm (VII juvenile stage). The pleopods, rudimentary in the

first stage, disappear in the second stage, and then arise in different numbers for each sex from the

third juvenile stage on. The spoon-tipped setae found on the second maxilliped, which are used to

sort food particles, are evident only from the fourth juvenile stage and increase linearly with carapace

growth. The absence of these setae may be the reason why juveniles settle on organic-rich substrates

where they can obtain food.

Key words: Fiddler crabs, juvenile morphology, sex differentiation, spoon-tipped setae

96 G.L. Hirose et al. / IRD 54 (2010) 95–109

Introduction

Studies of the early stages of the life cycle of crabs

facilitate understanding of ecological (supporting studiesof recruitment and distribution, which are very importantfor the regulation of adult populations), physiological,and phylogenetic aspects of these crustaceans (Felder etal., 1985; Anger, 2001). Therefore, post-larval morpho-logical and growth studies are needed to allow correctidentification of these early life stages. Nevertheless,difficulties in rearing and maintenance of juvenile crabsin the laboratory have limited studies to only the larvaland adult stages (Hebling et al., 1982), limiting informa-tion on juvenile ontogeny compared with the availableknowledge of larval development (Guimarães &Negreiros-Fransozo, 2005).

The fiddler crab Uca cumulanta Crane, 1943 iscommon in the intertidal zone of tropical and subtropicalareas (Crane, 1975), although in lower numbers thanmany congeners. The geographical distribution of U.cumulanta is restricted to the western Atlantic, fromCentral America to Rio de Janeiro, Brazil. It inhabitsmuddy and sand-muddy shores, below the mean low-tide level (Melo, 1996). The few reports on its biologyinclude that of Ahmed (1978), who studied the devel-opment of asymmetry in the chelipeds; Chiussi & Díaz(2001), who studied its zone recovery behaviour andorientation; and Pralon & Negreiros-Fransozo (2008),who studied its growth and sexual maturation in aBrazilian tropical mangrove.

The setal morphology of mouthparts of members ofthe genus Uca Leach, 1814 and their relationship to thespatial distribution of adults in the ecosystem have beendescribed (Crane, 1941, 1975; Miller, 1961; Costa &Negreiros-Fransozo, 2001; Bezerra et al., 2006). Thesesetae, known as “spoon-tipped setae,” are located on theinner face of the second maxilliped merus. They areused by crabs to select coarse grains (see Icely & Jones,1978; Thurman II, 1987; Yamaguchi & Ogata, 2000;Yamaguchi & Henmi, 2006), and they appear anddevelop during juvenile development (O’Connor,1990a).

Prolonged periods in laboratory conditions, even

during the larval phase, can exert strong influences on

growth. Artificial laboratory conditions can modify the

moult increment and intermoult period, commonly

retarding growth (see Luppi et al., 2004; Wehrtmann &

Albornoz, 2003) compared to the natural environment.

This procedure for estimating growth has been criticised

by some investigators because of the distinct life phases

of some brachyurans (Hartnoll, 1982; Welch & Epi-

fanio, 1995; Luppi et al., 2004). The use of juvenile

individuals of different sizes collected in the wild can

reduce the effect of laboratory rearing on growth,

because the juveniles are maintained under artificial

conditions for a much shorter time. Hartnoll and Bryant

(2001) and Luppi et al. (2004) used similar procedures

in growth studies, with the aim of reducing laboratory

effects on crab growth.

Rajabai (1954, 1959) provided brief and incomplete

morphological descriptions of juveniles of the ocypo-

doids Dotilla blanfordi Alcock, 1900, Ocypode platy-

tarsis H. Milne Edwards, 1852 and Ocypoda cordimana

Desmarest, 1825.

Ocypodoid species can be considered as a model for

growth studies in brachyurans, especially relative

growth, because of the pronounced sexual dimorphism

between adults of fiddler crabs. The many papers on

adult ocypodoid growth include those by Fransozo et

al. (2002) for Ocypode quadrata (Fabricius, 1887),

Negreiros-Fransozo et al. (2003) for Uca thayeri

Rathbun, 1900; Benetti & Negreiros-Fransozo (2004)

for U. burgersi Holthuis, 1967; Cardoso & Negreiros-

Fransozo (2004) for U. leptodactylus Rathbun, 1898;

Masunari & Disenha (2005) for U. mordax (Smith,

1870); Pinheiro et al. (2005) for Ucides cordatus (L.);

and Costa & Soares-Gomes (2008) for Uca rapax

(Smith, 1870). Juveniles of U. cumulanta were exam-ined by Ahmed (1978), and Hirose & Negreiros-

Fransozo (2008a) studied the juvenile growth and the

secondary sexual characters of U. maracoani (Latreille,

1802) from the South Atlantic.

As mentioned by O’Connor (1990a), the difficulty of

identifying Uca species during the early juvenile phase

prevents ecological investigations of their functional

importance in estuaries. A detailed investigation of the

morphology of the early life cycle of ocypodoid crabs

offers a good way to comprehend their phylogenetic

relationships, ecological distribution, and role in the

ecosystem.

This is the first report on the juvenile morphology of

U. cumulanta. We also provide data on absolute and

relative growth, and the appearance and development of

the secondary sexual characters in this species.

Materials and Methods

Juvenile specimens of U. cumulanta (<5 mm cara-

pace width, CW) were collected by means of a small

paintbrush on the muddy shore at Jabaquara, Paraty,

south coast of the state of Rio de Janeiro (23º12N10OS;

44º43N14.1OW), Brazil. The specimens were transported

alive to the laboratory in small closed plastic boxes

provided with water from the collecting site. These

G.L. Hirose et al. / IRD 54 (2010) 95–109 97

containers were placed in a cooler in order to avoid heat

stress during transport to the laboratory in the Zoology

Department, Biosciences Institute, São Paulo State Uni-

versity (UNESP).

The juveniles were raised in a climate-controlled

room with a constant temperature of 26 ± 1ºC, based on

the annual mean in the sampling area (Silva et al., 2007).

Each specimen was raised separately in an acrylic vessel

filled with 20 mL seawater (salinity 26‰), renewed

daily, and in a photoperiod of 12 h light:12 h dark.

Crabs were fed with an excess of Artemia nauplii, and

the vessels inspected daily for moulting crabs or dead

individuals. The exuviae were fixed in a mixture of 70%

ethanol and glycerin (1: 1). The day of each ecdysis was

recorded, to determine the intermoult period (IP).

Exuviae from first-stage juveniles (n=10) were

considered to be the smallest ones, with rudimentary

uropods present on the sixth pleonite (according to

Hirose & Negreiros-Fransozo, 2008a). The specimens

were dissected, drawn, and described using a stereo-

scopic microscope (Zeiss SV6) and an optical micro-

scope (Zeiss Axioskop2). The terminology for descrip-

tions of setae types is based on Clark et al. (1998) and

Garm (2004). The setae were observed with the use of a

microscope fitted with Nomarski differential inter-ference contrast optics (magnification = 1000×).

Only undamaged exuviae and dead specimens were

used for measurements. The following body parts were

measured under a stereoscopic microscope provided

with an ocular scale: carapace width (CW), carapace

length (CL), cheliped propodus length (CPL), cheliped

propodus height (CPH), and abdomen width (AW)

(Fig. 1). The biometry of the specimens was based on

the procedures adopted by Pralon & Negreiros-Fransozo

(2008) for adult crabs of the same species. The presence

of pleopods and gonopores was also checked; and when

they were detected, they were also drawn under a micro-

scope. Morphological descriptions of the first juvenile

stage and subsequent stages were based on Negreiros-

Fransozo et al. (2007). The setae sequence was

described from the proximal to distal segments of the

appendages.

Growth was determined using Hiatt’s equation of

moult increment (MI) and intermoult period (IP), which

was also used for size and age determination for each

juvenile stage. Hiatt (1948) described growth by means

of the linear equation (Y = a + bX), where the post-

moult CW (= Y) is the dependent variable and the pre-

moult CW (= X) is the independent variable. The study

of absolute growth was based on the CW. The growth

study did not have the objective of extrapolation for all

post-larval phases, but only for the first juvenile devel-

Fig. 1. Uca cumulanta. Body parts measured in this study.CW, carapace width; CL, carapace length; AW, abdomenwidth; CPH, cheliped propodus height; CPL, cheliped pro-podus length.

opment phase (early juveniles), considered here as those

specimens found in the size range of the beginning of

the sexual differentiation of the secondary sexual fea-

tures (VI juvenile stage).

In order to assess the changes in growth patterns

displayed by U. cumulanta in its development, the

relative-growth of morphological characters was esti-

mated (Huxley, 1950). The power function (aY = aX )b

was fitted to log-transformed (logY = loga + blogX) data

on CW, CPL, CPH, and AW, using CL as the in-

dependent variable. Positive allometry is characterisedby b>1, negative allometry by b<1, and isometry by b =

1 (Huxley, 1950). The b value found in each relationship

was tested by the Student’s T test at the 5% significance

level where the null hypothesis was b = 1.0. A covari-

ance analysis (" = 0.05) was used to test slopes and

intercepts of the regressions in the study of absolute and

relative growth (Zar, 1996).

The size at which cheliped and abdomen growth

differentiation occurs in the two sexes was compared by

a K-means clustering analysis, which is based on the

establishment of pre-determined groups, attributing

crabs to one of the groups by means of an iterative

process that minimises the variance within the groups

and maximises the variance among groups. A discri-

minant analysis is then applied, allowing a new classi-

fication of these groups, isolating them in distinct cate-

gories: non-sexually differentiated individuals, males,

and females. The statistical procedure was based on

Sampedro et al. (1999).

Results

Morphology of first juvenile crab

Carapace (Fig. 2A). Approximately square, slightly

convex dorsally, with several surface setae. Front

(Fig. 2C) corresponds to approximately 1/3 of carapace

98 G.L. Hirose et al. / IRD 54 (2010) 95–109

Fig. 2. First juvenile stage: A, dorsal view; B, detail of the lateral margin of the carapace; C, detail of the front; D, sternalplate; E, abdomen; F, pleopods (pl2–pl5) and uropod (u).

width; lateral margins (Fig. 2B) granulate. Sternum

(Fig. 2D) with sparse simple setae and several plumose

marginal setae; abdominal retaining mechanism located

on the 5th somite.

Pereopods (Fig. 3). Chelipeds symmetrical, with

some granules on propodus and dactyl; also some sparse

simple and plumose setae over entire appendage, and

several long plumose setae on coxa. Second, third,

fourth, and fifth pereopods similar, bearing sparse

simple setae.

Antennule (Fig. 4A) with well-developed basal

segment provided with 17 plumose setae and 4 simple

setae. It also has few protuberances and small marginal

spines; two-segmented peduncle with 2 simple setae on

proximal segment; unsegmented endopod (ventral

flagellum) with terminal simple seta; unsegmented

Fig. 3. First juvenile stage: A, third pereopod; B, chelipeddorsal view; C, cheliped lateral view (carpus, propodus, anddactyl).

G.L. Hirose et al. / IRD 54 (2010) 95–109 99

Fig. 4. First juvenile stage: A, antennule; B, antenna;C, mandible; D, maxillule; E, maxilla.

exopod (dorsal flagellum) with 7 long aesthetascs and 1

simple seta.

Antenna (Fig. 4B) with 3-segmented peduncle provi-

ded with 2, 1, 1 simple setae and 3, 1, 0 plumose setae.

Flagellum of 6 segments, with 0, 0, 3, 0, 3, 3 terminal

simple setae; and 1 long terminal, partially plumose

setae on fifth segment (approximately 3 times length of

segment).

Mandible (Fig. 4C) provided with well-chitinised

sharp blade; it has a 3-segmented palp with 3 plumose

setae on the middle segment and 8 plumose setae on the

distal segment.

Maxillule (Fig. 4D), coxal endite with 9 serrate setae,

18 plumodenticulate setae, and 24 serrulate setae. Basial

endite provided with 1 simple and 1 serrate seta on

proximal margin, 5 serrate, 1 small simple, 9 cuspidate,

3 plumose, and 1 plumodenticulate setae on distal

margin. Two-segmented endopod with 1 plumose seta

and 2 simple setae on distal segment. Protopod with 4

serrate setae, 3 of them marginal.

Maxilla (Fig. 4E), bilobed coxal endite with 14 serru-

late setae aligned, 3 serrate and 2 simple setae on proxi-

mal segment, 7 serrulate aligned and 1 simple seta on

distal segment. Bilobed basial endite with 4 sparsely

plumose setae and 10 simple setae on proximal segment,

and 7 plumose, 2 sparsely serrate, and 12 simple setae

Fig. 5. First juvenile stage: A, first maxilliped; B, secondmaxilliped; C, third maxilliped.

on distal segment. Endopod with 1 simple seta on its

basal margin. Exopod (= scaphognathite) with 53 plu-

mose marginal setae and approximately 13 simplesurface setae.

First maxilliped (Fig. 5A), coxal endite with 16

plumose, 7 sparsely plumose, 1 serrate, and 14 simple

setae. Basal endite with 9 plumose setae on its margin,

5 serrate, 4 plumodenticulate, and 2 simple setae, plus

24 small simple setae and 2 small plumose surface setae.

Unsegmented endopod with 13 plumose setae on its

lateral margin, 5 simple, 14 plumose, and 3 apical ser-

rate setae. Two-segmented exopod with 4 plumose setae

on each segment. Epipod well developed, with 22 long

serrulate setae, 1 simple seta, and 1 small plumose seta.

Second maxilliped (Fig. 5B), five-segmented endo-

pod with 3 plumose setae on proximal segment; 13

plumose, 1 sparsely plumose, 4 serrate, and 7 simple

setae on second segment; 2 plumose and 1 simple setae

on third segment; 3 plumose, 4 plumodenticulate, 1

serrate, and 2 simple setae on fourth segment; and 6

serrate and 3 plumodenticulate setae on fifth segment.

Two-segmented exopod with 8 plumose, 2 simple, and

1 cuspidate setae on proximal segment; 1 simple and

4 plumose setae on distal segment. Protopod with 3

plumose setae. Branchia and epipod rudimentary, not

provided with setae.

Third maxilliped (Fig. 5C), four-segmented endopod

with large protuberance on its outer margin, and several

other small protuberances on terminal portion of second

segment. Additionally, it has several setae on each

100 G.L. Hirose et al. / IRD 54 (2010) 95–109

segment as follows: 45, 14, 11, 2, and 0 plumose; 0, 0,

0, 2, 5 serrate and 3, 0, 0, 1, 2 simple setae. Two-

segmented exopod with 12 plumose setae on proximal

segment and 7 plumose setae on distal segment.

Protopod with 3 plumose setae. Epipod with several

(plumose and simple mixed) marginal setae on proximal

region, plus 13 simple (long and short mixed) setae and

8 sparsely plumose setae on median-dorsal region.

Pleon (Fig. 2E). With six somites wider than long,

provided with several simple setae; telson smooth, with

small simple setae and other terminal plumose setae.

Rudimentary pleopods present on second to fifth pleo-

nites (Fig. 2F, pl2–pl5), plus rudimentary uropods

(Fig. 2F, u) on sixth pleonite.

Absolute growth

A total of 49 crabs of several sizes were obtained, of

which 27 were identified as males and 22 as females.

After growth trials, 148 measurements were obtained

from males and 120 from females. The measures of the

CW of pre-moult (CWpr) and post-moult (CWpt)

individuals allowed calculation of the carapace-growth

equation, which did not differ between sexes

(ANCOVA, p <0.05), and therefore these data weregrouped in a single equation (Fig. 6, Table 1).

The size of the smallest juvenile crab obtained

(CW = 1.15 ± 0.07 mm) was considered as the first

juvenile stage, because no morphological description of

laboratory-reared first-stage juvenile crabs of this or any

other ocypodoid species exists. Also, they still had

pleopods and uropod buds remaining from the megalopa

stage (Fig. 2F). The size of these juvenile crabs was used

as the initial size for extrapolation of other juvenile

stages. With the determination of each corresponding

juvenile stage, the CW (Fig. 7A), MI (Fig. 7B), IP

(Fig. 8A), and age (Fig. 8B) for each developmental

stage were determined where statistical differences were

found between sexes (ANCOVA, p <0.05) with the ex-

ception of the relationship crab stages vs. age (Table 1).

After the determination of the carapace growth and

age equations, a new relationship could be obtained

(Fig. 9A). The data for this relationship were trans-

formed for a linear regression analysis and compared

between sexes (Fig. 9B), where significant statistical

differences were found (ANCOVA, p<0.05) (Table 1).

Fig. 6. Linear regression of carapace width (CW) betweenthe pre-moult (pr) and post-moult (pt) relationship(according to the Hiatt growth model). Y = CWpt (mm) andX = CWpr (mm).

Table 1. Results of the regression analysis for the absolute growth relationships

Relationship Sex Fitted equation Slope Intercept r2

b p-value* a p-value*

Hiatt growth model (CWpr vs. CWpt)

Total Linear 1.1003 0.8138 0.2097 0.1366 0.9558

Stages vs. CW M Linear 0.4158 0.3421 0.6102 <0.01 0.9921F 0.4711 0.4279 0.9908

Stages vs. MI M Potential !0.3132 0.5906 28.4190 <0.01 0.9863F !0.3338 31.4110 0.9890

Stages vs. IP M Linear 4.6044 <0.01 6.3664 0.2168 0.9789F 2.8720 12.4100 0.9650

Stages vs. age Total Potential 1.3000 0.2942 12.9687 0.8308 0.9894CW vs. age M Linear 71.2860 <0.01 79.1710 <0.01 0.9936

F 57.0070 52.0190 0.9993

CWpr = pre-moult carapace width; CWpt = post-moult carapace width; CW = carapace width; MI = moult increment; IP =intermoult period; M = males and F = females. *ANCOVA (á = 0.05).

G.L. Hirose et al. / IRD 54 (2010) 95–109 101

Fig. 7. A, mean size (CW mm) and standard deviation for each juvenile stage. B, percentage of moult increment (CW mm)in relation to the mean size between consecutive juvenile stages.

Fig. 8. A, intermoult period (IP) of each developmental stage (mean and standard deviation). Y, IP (days); X, crab stage;*absolute value. B, cumulative age for each developmental stage. Y, age (days); X, crab stage.

Relative growth

The regression analysis between sexes revealed no

statistical difference only for the relationship CW vs. CL

(p >0.05). Therefore these data were grouped in a single

equation, estimated for both sexes.

The pattern of allometric growth differed between

sexes (p <0.05) in the relationships CPL vs. CL, CPH

vs. CL, and AW vs. CL, and positive allometry was

found for both sexes in the relationship CPL vs. CL. The

relationship AW vs. CL showed positive allometry for

females and isometry for males. The relationship CPH

vs. CL showed positive allometry for males and isometry

for females (Table 2).

Cheliped and abdomen asymmetry

The cheliped development showed a different growth

pattern for males and females, which was evident at

approximately 3.2 mm CW (Fig. 10A). With respect to

the abdomen width, the distinction between the sexes

was evident from 3.9 mm CW, which is the VII juvenile

stage (Fig. 10B).

Morphological development

The smallest specimens, around 1.15 mm CW, had

4 pairs of pleopods and 1 pairs of uropods on the ventral

side of the abdomen (Fig. 2F). These pleopod buds

102 G.L. Hirose et al. / IRD 54 (2010) 95–109

Fig. 9. A, growth curve of the relationship: duration in days and moult increment at each juvenile stage; B, comparison of thegrowth of males and females (ANCOVA, p <0.05). J, juvenile stage; Y, age (days); X, CL (mm).

Fig. 10. A, relationship between cheliped propodus length (CLP) and carapace width (CW) showing the size at chelipeddifferentiation for males; B, relationship between abdomen width (AW) and CW showing the size at which females candifferentiate.

Table 2. Result of the regression analysis for the log-transformed morphometric data. CL used as the independent variable

(b = 1)calculatedVariable Sex N Intercept (log) Slope r T Allometry2

a P-value* b P-value*

CW Total 245 !0.006 0.06 0.75 0.86 0.92 18.85 !AW Males 125 !0.470 <0.01 1.02 <0.01 0.78 0.48 =

Females 106 !0.515 1.26 0.89 5.77 +CPL Males 125 !0.356 <0.01 1.84 <0.01 0.70 7.904 +

Females 106 !0.329 1.15 0.83 18.41 +CPH Males 127 !0.933 <0.01 1.84 <0.01 0.70 7.90 +

Females 107 !0.821 1.03 0.74 0.53 =

CL, carapace length; CW, carapace width; AW, abdomen width; CPL, cheliped propodus length; CPH, cheliped propodusheight; (+) positive allometry; (–) negative allometry, and (=) isometry. *ANCOVA (á = 0.05).

G.L. Hirose et al. / IRD 54 (2010) 95–109 103

Table 3. Size, age, and morphological differentiation for each stage

Juvenilestages

Males(CW)

MalesAge (days)

Females(CW)

FemalesAge (days)

Appearance of structure

Mean ±sd Cumulative ±sd Mean ±sd Cumulative ±sd Males Females

I 1.15 ±0.07 13* 1.15 ±0.07 16.5 ±12.02 Pleopods +uropod

Pleopods +uropod

II 1.46 ±0.08 25.8 ±6.64 1.50 ±0.08 33.8 ±10.71III 1.81 ±0.08 45.6 ±10.27 1.88 ±0.09 52.6 ±8.57 Pleopods PleopodsIV 2.18 ±0.09 69.8 ±10.21 2.30 ±0.09 77.4 ±14.10 Spoon-tipped

setaeSpoon-tippedsetae

V 2.59 ±0.10 100.15 ±12.81 2.77 ±0.10 105.0 ±14.39VI 3.04 ±0.11 135.49 ±13.00 3.28 ±0.11 134.75 ±12.32 Larger cheliped GonoporeVII 3.53 ±0.12 175.19 ±14.10 3.84 ±0.13 168.67 ±15.36 larger abdomenVIII 4.07 ±0.13 216.69 ±18.69 4.46 ±0.14 202.67 ±9.03

CW, carapace width; sd, standard deviation; *absolute value.

Fig. 11. Characterisation of the development of male pleo-pods (JIII = 1.9 mm CW; JIV = 2.3 mm CW; JV = 2.8 mmCW; JVI = 3.0 mm CW — carapace widths of the crabs usedin the morphological descriptions).

disappear in the subsequent stages. New pleopod pairs

arise from the first to the second pleonite in males

(around 1.9 mm CW, third juvenile stage) (Fig. 11), and

from the second to the fifth pleonite in females (Fig. 12).

The gonopores could be seen from 3.3 mm CW

(Fig. 13A). As the carapace develops (Fig. 13B), it be-

comes more wide than long, and the front width main-

tains a proportion close to that of the first juvenile stage

(approximately 1/3 of the carapace width). Based on the

growth equation, the events of sexual differentiation and

appearance of certain structures can be related to the

crab stages described here (Table 3).

Appearance of spoon-tipped setae

Spoon-tipped setae were not found on the second

maxilliped merus of the first juvenile stage, but only incrabs from 2.18 and 2.30 mm CW for males and

females, respectively (Fig. 14). These dimensions of the

carapace were estimated by means of the growth

equation, and correspond to the fourth juvenile stage.

The relationship of the number of spoon-tipped setae to

carapace width (Fig. 15) shows that the setae first appear

in small numbers, but their number increases linearly in

proportion to the carapace size. There was no significant

difference (ANCOVA, p<0.05) between sexes for this

relationship.

Discussion

First juvenile crab morphology

Descriptions of juvenile crab morphology are mainly

based on the number of segments and setae present on

appendages (Rieger & Beltrão, 2000), probably because

of the difficulties of examining setae using optical

microscopy. Nevertheless, some appendages of U.

cumulanta show morphological peculiarities and could

probably be used as a distinguishing feature. The

antennules of U. cumulanta have both the exopod and

endopod unsegmented, which has not been reported for

any other crab species for which the first juvenile

morphology is described (see Ingle, 1981; Ingle &

Clark, 1980; Yatsuzuka & Sakai, 1980; Ingle & Rice,

1984; Rodríguez & Paula, 1993; Guerao et al., 1997;

104 G.L. Hirose et al. / IRD 54 (2010) 95–109

Fig. 12. Characterisation of the development of female pleopods (JIII = 1.9 mm CW; JIV = 2.3 mm CW; JV = 2.7 mm CW;JVI = 3.1 mm CW; JVII = 3.7 mm CW; and JVIII = 4.3 mm CW — carapace widths of the crabs used in the morphologicaldescriptions).

Fig. 13. A, female sternite of juvenileVI (JVI = 3.3 mm of CW) when thegonopore first appears, indicated byarrows. B, variation in shape ofcarapace during juvenile development(stages I–VIII).

Fig. 14. CW = 3.4 mm. A, portion of the endo-pod of second maxilliped showing the spoon-tipped setae. B, detail of the spoon-tipped setae.C, schematic drawing of the spoon-tipped setae.Cp, carpus; Dt, dactylus; Mr, merus; Pr,propodus.

G.L. Hirose et al. / IRD 54 (2010) 95–109 105

Table 4. Regression analysis between the development phases (independent variable = cephalothorax length (CL)

Variable Category N Intercept (log) Slope R t (b=1) Allometry2

a P-value b P-value2 2

CPL EJm 125 !0.356 <0.01 1.84 <0.01 0.70 7.904 +Jm 121 0.37 2.01 0.85 13.30 +1

Am 192 0.17 1.74 0.82 13.01 +1

AW EJf 106 !0.515 <0.01 1.26 <0.01 0.89 5.77 +Jf 98 0.88 2.20 0.91 18.42 +1

Af 173 0.24 1.23 0.79 4.91 +1

CPL, cheliped propodus length; AW, abdomen width; EJm, early juvenile male; Jm, juvenile male; Am, adult male; EJf, earlyjuvenile female; Jf, juvenile female; Af, adult female; (+) positive allometry.Data from Pralon and Negreiros-Fransozo (2008).1

ANCOVA (á = 0.05).2

Fig. 15. Linear regression between the number of spoon-tipped setae on the meropodite of the second maxilliped andsize carapace width (CW). Y = number of spoon-tippedsetae; X = CW (mm).

Rieger & Beltrão, 2000; Hebling & Rieger, 2003;

Guimarães & Negreiros-Fransozo, 2005; Negreiros-

Fransozo et al., 2007). Unfortunately, this characteristic

could not be confirmed in the studies by Rajabai (1954,

1959) because they were very incomplete.

The maxillule and the maxilla have sets of setae

which give them a brush aspect. This feature may be

related to the life habit of ocypodid crabs, as according

to Crane (1975) they are detritivores and therefore need

specialised structures for sorting particles from the

sediment.

Absolute growth

The pattern of absolute growth found for U. cumu-

lanta, in which the MI (%) decreases and the IP

increases as the crab develops, differed statistically

between sexes. For each stage analysed, males had

statistically lower MI and IP growth rates than females;

i.e., from 1.8 to 2.0 mm CW, males tended to grow more

slowly than females. This difference became evident

from the JIII, the size at which sexual differentiation

begins, based on the number of pleopods borne by each

sex. This pattern is similar to that observed for U. mara-

coani by Hirose & Negreiros-Fransozo (2008a).

Relative growth

The study of relative growth for the early juvenilestages of U. cumulanta revealed that this species followssimilar patterns previously described for crabs at largersizes than those studied by Pralon & Negreiros-Fransozo(2008) (Table 4).

A comparison of the growth phases studied byPralon & Negreiros-Fransozo (2008) and those studiedhere indicates some differences in the relationships ofthe same body parts, which may reflect the differentdevelopmental conditions between laboratory and field.A distinct allometric coefficient (see Table 4) for thejuvenile phase as a whole was previously observed forU. maracoani by Hirose & Negreiros-Fransozo (2008a).

Chelipeds and abdomen asymmetry

The observed differences in cheliped development

between the sexes revealed that males rapidly diverged

from females (VI juvenile stage on) in this study.

Therefore, it is possible that the energy expenditure

required for this is reflected in the absolute growth of

males in this early development period. This growth

pattern may be related to the agonistic behaviour of male

fiddler crabs, in addition to their elaborate mating

behaviour (Crane, 1975). This is confirmed by the rapid

differentiation of the chelipeds, because the sooner they

106 G.L. Hirose et al. / IRD 54 (2010) 95–109

differentiate, the sooner they can interact with other

males. This same pattern of cheliped differentiation (in

relation to the female abdomen) was found for U.

maracoani studied by Hirose & Negreiros-Fransozo

(2007), and seems to be a common occurrence in this

genus. However, further investigations should be carried

out to confirm the existence of an actual pattern for the

genus Uca.

Ahmed (1978) mentioned juvenile males of U.cumulanta showing major chelipeds from 1.7 mm CWup, whereas in the present study this appendage dif-ferentiation occurs from approximately 3.2 mm CW.Hyman (1920), studying other Uca species, noted thatthey begin this differentiation only from 3 mm CW up.Considering that some Uca species have phenotypicplasticity that appears as a different size range as afunction of certain habitat features, mainly food avail-ability and quality (Colpo & Negreiros-Fransozo, 2003),such variation may be due to differences between thestudy locality of Ahmed (1978) and ours.

Morphological development

Pleopods and uropods were found in the smallestcrabs analysed (JI), which suggests that these appen-dages are remnants from the larval phase (megalopa),and disappear in the later stages. This was also found forU. maracoani by Hirose & Negreiros-Fransozo (2008a).

In females, the four pleopod pairs develop graduallyin the successive stages of postlarval development, andare subsequently used to hold the eggs during incu-bation. At the same time, the gonopores are beingformed. These morphological changes in both sexes arerelated to the transition of these growth phases duringthe ontogeny of U. cumulanta, revealing the changefrom the early juvenile phase (undifferentiated juveniles)to a second step in their juvenile life.

During development subsequent to the first juvenilestage, the front of the carapace retains its initial propor-tions in relation to the carapace width, which classifiesthis species as a member of the wide-front group (sensuCrane, 1975). This classification easily differentiates thisspecies from those with a narrow front, such as U.maracoani, which lives in a similar habitat (Hirose &Negreiros-Fransozo, 2008a).

Appearance of spoon-tipped setae

Fiddler crabs feed on decomposing organic matter,

algae, and microorganisms extracted from the substrate.

The food is sorted by means of a flotation process,

caused by the water of the branchial chamber that floods

the mouth cavity (Miller, 1961). The maxillipeds (not-

ably the second maxilliped) function to sort the food

particles. The spoon-tipped or plumodenticulate setae

present on these appendages, positioned in the central

portion of the mouth cavity, sweep the sand grains,

freeing the adhered organic material. The setae provide

an enlarged surface of stout tips that can prevent sand

grains from being forced onto or through the meropodite

setae when the second maxilliped moves across the

bristles of the first maxilliped endites. These spoon-

tipped setae can also help carry coarse particles away

from the central portion of the cavity. The food thus

freed by the cleaning process is captured and conducted

towards the top of the mouth to be ingested.

The set of setae present on the second maxilliped has

a prominent role in the sediment-grain cleaning process

during feeding. Based on this study, however, the spoon-

tipped setae, the main setae involved in sorting the food

particles, appear only from the fourth juvenile stage.

This raises the question of the importance of the lack of

these setae for feeding in the previous stages, and the

possibility that the first to third juveniles may be ex-

ploiting different food sources from the older juveniles

and adults.

Juvenile fiddler crabs, although morphologically

similar to adults, show anatomical and behaviouraldifferences that could help them exploit different

ecological niches. Because the feeding biology of

juveniles may differ, it could influence larval settlement

(O’Connor, 1993), i.e., the larvae could settle in areas

with a large amount of silt and clay particles because the

organic-matter content of such substrata is much higher

than in sandy sediments (Levinton, 1982).

O’Connor (1990a), studying juveniles of Uca pugi-

lator (Bosch, 1802), observed that they do not develop

specialised mouth structures until they reach the sixth

juvenile stage. It was also noted that these juveniles

could feed more efficiently in substrata with higher

percentages of silt and clay during the early juvenile

stages, maybe because they do not have enough of these

setae to otherwise obtain enough food. But as they get

older and acquire more setae, they can then obtain

enough food from areas low in organic substances, as in

the adult habitat. In addition, settling apart from the

adult habitat could prevent predation of the larvae and

early juveniles by adults, as has been observed in the

laboratory (O’Connor, 1990b). Later when they have

grown large enough, they can join their older

conspecifics.

The same settling behaviour may occur in U. cumu-

lanta, because at the study site, which is rich in silt and

clay (92%) (Hirose & Negreiros-Fransozo 2008b), no

adults were found with the juveniles. Instead, adults

G.L. Hirose et al. / IRD 54 (2010) 95–109 107

were found adjacent to the sampling site, but in the

upper intertidal zone. In another study near the sampling

area (Colpo, 2005), adult populations of U. cumulanta

were found predominantly in areas with lower per-

centages of silt and clay (18%).

Considering the relationship between the number of

spoon-tipped setae and the carapace width in juveniles

of U. cumulanta, the results indicated linear growth.

This agrees with the results obtained by Yamaguchi &

Ogata (2000) for U. lactea (De Haan, 1835) and by

Yamaguchi & Henmi (2006) for U. vocans (Linnaeus,

1758) and U. tetragonon (Herbst, 1790). O’Connor

(1990a) nevertheless estimated that U. pugilator shows

exponential growth in the number of these setae. In both

cases, the number of setae increases from early to

advanced juveniles.

No significant difference between sexes was found

for the relationship of the number of spoon-tipped setae

vs. CW. This contrasts with the hypothesis of Weissburg

(1991) for U. pugnax (Smith, 1870), that females have

more spoon-tipped setae on the mouthparts than males

in order to efficiently separate more food from the

substrate, because females use two minor chelipeds for

feeding while the males use only one. Our data agree

instead with those obtained by Yamaguchi & Ogata(2000) for U. lactea.

Mangroves are ecosystems that should be perma-

nently protected because of their peculiar and fragile

nature. Frequently, mangroves are impacted by environ-

mental changes related to economic development and

tourism. This study contributes to a better comprehen-

sion of the biology of an ocypodoid species by provid-

ing data for population studies, which are fundamental

for conservation of the natural populations, as well as

the coastal areas where the species lives.

Acknowledgments

To the “Fundação de Amparo à Pesquisa do Estado

de São Paulo” (FAPESP) (94/4878-4; 98/3136-4;

04/15194-6), “Conselho Nacional de Desenvolvimento

Científico e Tecnológico” (CNPq) (133740/2008-0), and

“Coordenação de Aperfeiçoamento de Pessoal de

Ensino Superior” (CAPES) for financial support, to

NEBECC members for their help during the fieldwork,

to Dr. Janet W. Reid for her help with the English

revision, and to the referees who contributed to the

improvement of this paper. The crabs in this study were

collected according to Brazilian laws concerning samp-

ling wild animals.

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