behavioural evidence for body colour signaling in the fiddler crab uca perplexa (brachyura:...

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Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae) Satoshi Takeda * Marine Biological Station, Tohoku University, Asamushi, Aomori 039-3501, Japan Received 8 April 2005; received in revised form 18 August 2005; accepted 19 September 2005 Abstract In the reproductive season, mature females of the fiddler crab Uca perplexa leave their burrows and wander about their habitat for mating. To clarify whether the fiddler crabs respond to colour or luminosity, I examined the behavioural responses of the males to the wandering females before and after the females were painted white, red, black or blue. The behaviours of the males were categorized into three types: lateral–circular wave and lateral–straight wave for courting, and repelling. Before painting, almost all of the males courted the females. After painting, significantly fewer males courted the red-, black- and blue-painted females than courted the white-painted females. These results mean that the fiddler crabs can discriminate colours or luminosity. The role of body colour as a visual signal in crab society is discussed. D 2005 Elsevier B.V. All rights reserved. Keywords: Body colour; Colour discrimination; Fiddler crab; Uca perplexa; Courting display 1. Introduction The vision of brachyurids depends on the environ- ment to which they are adapted (Zeil et al., 1986). For instance, crabs inhabiting bare flat terrain, gener- ally ocypodid crabs, have eyes with vertical resolving power at the top of closely spaced long eyestalks (Zeil et al., 1986; Zeil and Al-Mutairi, 1996). In contrast, crabs inhabiting flat terrain with vegetation, generally grapsid crabs, have stereoptic eyes at the top of widely spaced short eyestalks (Zeil et al., 1986), and can distinguish shapes (Cannicci et al., 2002). Semi-terrestrial crabs have various body colours (e.g., Crane, 1975; Detto et al., 2004). Their body colour changes with growth and body size (e.g., Detto et al., 2004), and in the reproductive season (e.g., Crane, 1975; Detto et al., 2004). The males of some species change their body colour a few minutes after losing a fight or being captured (Crane, 1975; Zucker, 1981; Zeil and Hofmann, 2001). In addition, the spec- ular reflections on the cuticle of the body become polarized after wetting (Zeil and Hofmann, 2001). It has been shown that ocypodid crabs (genus Uca ) have two kinds of visual pigments — a precondition for vision (Harch et al., 2002) — and can distinguish colours (Hyatt, 1975). Although vision and body colour as a potential signal have been studied separately, the role of body colour as a signal in social communication has never been studied. The objective of this study was to see whether semi-terrestrial crabs use their body colour as a signal. Fiddler crabs are suitable for examining this ques- tion because they have various body colours and well- 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.09.021 * Tel.: +81 17 752 3388; fax: +81 71 752 2765. E-mail address: [email protected]. Journal of Experimental Marine Biology and Ecology 330 (2006) 521 – 527 www.elsevier.com/locate/jembe

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Page 1: Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

www.elsevier.com/locate/jembe

Journal of Experimental Marine Biolog

Behavioural evidence for body colour signaling in the fiddler crab

Uca perplexa (Brachyura: Ocypodidae)

Satoshi Takeda *

Marine Biological Station, Tohoku University, Asamushi, Aomori 039-3501, Japan

Received 8 April 2005; received in revised form 18 August 2005; accepted 19 September 2005

Abstract

In the reproductive season, mature females of the fiddler crab Uca perplexa leave their burrows and wander about their habitat

for mating. To clarify whether the fiddler crabs respond to colour or luminosity, I examined the behavioural responses of the males

to the wandering females before and after the females were painted white, red, black or blue. The behaviours of the males were

categorized into three types: lateral–circular wave and lateral–straight wave for courting, and repelling. Before painting, almost all

of the males courted the females. After painting, significantly fewer males courted the red-, black- and blue-painted females than

courted the white-painted females. These results mean that the fiddler crabs can discriminate colours or luminosity. The role of

body colour as a visual signal in crab society is discussed.

D 2005 Elsevier B.V. All rights reserved.

Keywords: Body colour; Colour discrimination; Fiddler crab; Uca perplexa; Courting display

1. Introduction

The vision of brachyurids depends on the environ-

ment to which they are adapted (Zeil et al., 1986).

For instance, crabs inhabiting bare flat terrain, gener-

ally ocypodid crabs, have eyes with vertical resolving

power at the top of closely spaced long eyestalks

(Zeil et al., 1986; Zeil and Al-Mutairi, 1996). In

contrast, crabs inhabiting flat terrain with vegetation,

generally grapsid crabs, have stereoptic eyes at the

top of widely spaced short eyestalks (Zeil et al.,

1986), and can distinguish shapes (Cannicci et al.,

2002).

Semi-terrestrial crabs have various body colours

(e.g., Crane, 1975; Detto et al., 2004). Their body

colour changes with growth and body size (e.g., Detto

0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.jembe.2005.09.021

* Tel.: +81 17 752 3388; fax: +81 71 752 2765.

E-mail address: [email protected].

et al., 2004), and in the reproductive season (e.g.,

Crane, 1975; Detto et al., 2004). The males of some

species change their body colour a few minutes after

losing a fight or being captured (Crane, 1975; Zucker,

1981; Zeil and Hofmann, 2001). In addition, the spec-

ular reflections on the cuticle of the body become

polarized after wetting (Zeil and Hofmann, 2001). It

has been shown that ocypodid crabs (genus Uca) have

two kinds of visual pigments — a precondition for

vision (Harch et al., 2002) — and can distinguish

colours (Hyatt, 1975).

Although vision and body colour as a potential

signal have been studied separately, the role of body

colour as a signal in social communication has never

been studied. The objective of this study was to see

whether semi-terrestrial crabs use their body colour as a

signal.

Fiddler crabs are suitable for examining this ques-

tion because they have various body colours and well-

y and Ecology 330 (2006) 521–527

Page 2: Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

S. Takeda / Journal of Experimental Marine Biology and Ecology 330 (2006) 521–527522

developed social behaviours (Crane, 1975; Zucker and

Denny, 1979). A characteristic feature of the fiddler

crab is hypertrophy of one of the male chelipeds,

resulting in a striking asymmetry (Crane, 1975; Rosen-

berg, 2001). The hypertrophic, or major, cheliped is

used directly in agonistic behaviour and indirectly as a

visual signal, for example as a distinctive indicator of

the male sex during the reproductive season (Salmon

and Stout, 1962; Crane, 1975). The male communicates

to nearby individuals by waving its major cheliped,

which it does in courting females or in signalling

aggression (Crane, 1975). Each species has a peculiar

rhythm and motion of the major cheliped and other

thoracic legs, which allow many species of fiddler

crab to coexist sympatrically (Altevogt, 1969; Crane,

1975).

Fiddler crabs with eyes at the top of long vertical

stalks perceive movement but not shape (Zeil et al.,

1986; Hemmi and Zeil, 2003). Therefore, particular

movements of the body or major cheliped characterized

by coloration and luminosity will be recognized as

signals.

The fiddler crabs have two kinds of mating system

(e.g., Crane, 1975). In one, the male approaches a

nearby female, and they mate on the ground surface

near the entrance to the female’s burrow. In the other, a

wandering female is enticed to enter a male’s burrow,

then they mate in the burrow. In general, the males of

fiddler crabs which mate in their burrows perform

complex waving displays (Crane, 1975). The male

changes the form of his display according to the dis-

tance to a female, and performs his most active display

when a preferred female walks near the entrance of the

burrow (Crane, 1975).

In this study, I examine the role of body colour in

social communication by observing behavioural

responses of males to females painted different colours.

Differing responses to different colours would indicate

the ability to discriminate colour.

2. Materials and methods

2.1. Study site

I studied a population of Uca perplexa on the

sandy shore of Hanejiuchimi Bay, Okinawa Island,

Japan (1288 2V 11W E; 268 37V 44W N) (Takeda,

2003). U. perplexa inhabits sandy and muddy–

sandy shores between low and high water levels of

the neap tide. The soldier crab Mictyris brevidactylus

and the fiddler crab Uca vocans inhabit the sandy

shore below the low water level of the neap tide. M.

brevidactylus is dark blue in the nonreproductive

season, and cobalt blue in the reproductive season,

winter. U. vocans is grey in the nonreproductive

season, and whitish in the reproductive season, sum-

mer. The fiddler crab Uca dussumieri inhabits the

muddy shore of the mangrove forest above the high

water level of the neap tide, and U. crassipes inhabits

mud in the mangrove forest. U. dussumieri is bluish

black and U. crassipes is vermilion. Sometimes the

grapsid crab Helice leachi, which is light brown,

similar to the ground colour, wanders about the hab-

itat of U. perplexa.

In other U. perplexa habitats, the small ocypodid

crabs Scopimera globosa and Tmethypocoelis cerato-

phora dwell (Nakasone, 1977). Both are yellowish

brown, similar to sand.

2.2. Fiddler crabs

The females and males of the fiddler crab U. per-

plexa dig individual burrows close to each other (Naka-

sone and Murai, 1998). On Okinawa Island, the crabs

reproduce from April to September (Nakasone and

Okadome, 1981). The crabs copulate in the male’s

burrow or on the surface of the sand near the burrow

entrance (Nakasone and Murai, 1998). When the male

is larger than the female, they perform either mating

practice. In contrast, when the male is smaller than the

female, they do only surface mating.

Females ready to spawn leave their burrows spon-

taneously or by interaction with nearby males (Naka-

sone and Murai, 1998). Males wave their major

cheliped to attract the females to mate. The waving

form depends on the distance to the female (personal

observation). When the distance is 30 to 50 cm, the

males face the females, flex the major cheliped acute-

ly, and raise and lower it. When the distance is about

30 cm, the males extend the major cheliped at a right

angle, and raise and lower it. When the distance is

shorter than 30 cm, the males laterally extend the

major cheliped (lateral–straight wave). Some subse-

quently raise it, then flex it and bring it back down

to the starting position (lateral–circular wave). The

major cheliped is raised higher in the lateral–circular

wave than in the lateral–straight wave (see Crane,

1975).

The males repel the females very rarely. When a

female approaches a burrow, the owner male slightly

raises and lowers his major cheliped against the female.

The male enters his burrow, or stays outside. When the

male is larger than the female, the male occasionally

flicks the female with his major cheliped.

Page 3: Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

S. Takeda / Journal of Experimental Marine Biology and Ecology 330 (2006) 521–527 523

2.3. Methods

I fenced a quadratic area (60�60 cm) with trans-

parent acrylic plates (9 cm height) on the surface of the

sand over some large males with their own burrows.

The fence was anchored by PVC poles at each corner.

Any gap between the bottom margin of the plates and

the surface of the sand was filled with sand. Crabs

without a burrow were removed from the quadrat.

Empty burrows with no owner and any depressions

were filled with sand, and the surface of the sand in

the quadrat was flattened. I measured the diameter of

each burrow to estimate the carapace width of the

owner male, because a close relationship between the

diameter (X, mm) and the carapace width (Y, mm) was

recognized (Y=1.133X +1.451, r =0.939, n =58).

Males in the quadrat courted females outside it, and

males outside it courted females inside it, which indi-

cates that the crabs could communicate with each other

across the plates.

Subsequently, I captured a large female which

walked about on the sand surface while avoiding the

waving males. Such a female was considered to be

suitable for the test of the response to several males,

because she did not enter burrows easily (Murai, per-

sonal communication). I measured her carapace width,

then put her in a conical white vessel (about 5 cm

diameter) in a corner of the quadrat. About 5 min

later, when most crabs had resumed their surface activ-

ities, I carefully opened the vessel by pulling on a fine

string. Usually the female began walking slowly about

the quadrat. I observed the males’ responses for at least

30 min, and recorded the behaviour pattern when a

male was excited by the female (the female approached

the male or his burrow within 10 cm).

After observation, I recaptured the female and

painted her whole body white, red, blue or black

(Paint-marker PX-30, Mitsubishi, Japan). The luminos-

ities of the red and blue were 39.7, that of the white was

100, and that of the black was 0, as measured using

Adobe Photoshop ver. 3.0 J for Macintosh, although

visual luminosity differs between human and crab due

to the different spectral sensitivities of the human and

crab photoreceptors (e.g., Kelber et al., 2003). The

painted female was released again in the quadrat as

before. Then I recorded the behaviour of the males

towards her. After observation, the painted female

was released in another habitat. The quadrat was set

up again on the sand surface more than 5 m away from

the previous site for the next observation. The field

experiment was conducted between 22 May and 21

June 2000 and between 11 May and 15 June 2001.

The colour of the carapace of the wandering females

varies (Crane, 1975). In the reproductive season, the

pattern follows two types: a simple colour pattern and a

lateral-striped pattern, like that of mature males. In

general, the lateral-striped pattern consists of light

brown and some black strips. The simple pattern is an

ashy red-brown, brown, yellow, white, blue or purple.

Usually, the distal tips of the chelipeds are cobalt blue,

and the proximal part of the merus of the walking legs

is red. These colours become dark when the females are

captured.

In the nonreproductive season, the colour of the

carapace of the females is yellowish brown, similar to

the sand colour.

2.4. Statistical analysis

The Kruskal–Wallis test was used to determine

differences in the carapace width of the females

painted in four colours, the density of males in the

quadrat, and burrow diameter of the males tested with

different coloured females among the four groups. The

G-test was used to determine differences in the beha-

vioural responses to the unpainted females between

males that were smaller and larger than the presented

female, and in the proportion of males that repelled

the females after they were painted among the four

colour groups of smaller or larger males. Fisher’s

exact probability test was used to determine differ-

ences in the proportion of males that courted or re-

pelled the females after painting between the lateral–

circular wavers and lateral–straight wavers that

courted the females before painting in each group,

and between each pair of the four groups of smaller

or larger males. It was also used to determine differ-

ences in the number of quadrats in which the males

did or did not repel the females after painting between

each pair of the four groups. Differences at p b0.05

were taken to be significant.

3. Results

3.1. Female and male sizes

The carapace width did not differ among the four

colour groups of painted females (Kruskal–Wallis test:

df =3, H =1.473, p =0.6884) (Table 1). This means that

the quality of the females did not differ among the four

groups, because larger females have better reproductive

success.

The density in the quadrat did not differ among the

four groups of males tested with the painted females

Page 4: Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

Table 1

Carapace width of females painted in four colours, density of males in the quadrat, and burrow diameter of the males presented with the different

coloured females

Colour White Red Blue Black Total

Female carapace width

Mean (mm) 12.92 12.56 12.75 12.98 12.80

SD 0.75 0.94 1.15 0.71 0.91

Range (mm) 11.60–14.35 11.05–14.10 10.80–14.80 11.85–14.20 10.80–14.80

N 16 17 18 16 67

Male burrow density

Mean 3.69 3.35 3.06 3.81 3.46

SD 1.25 1.22 1.16 1.11 1.20

Range 1–6 1–5 1–5 2–5 1–6

N 16 17 18 16 67

Male burrow diameter

Mean (mm) 10.89 10.95 11.06 10.92 10.95

SD 0.95 1.00 1.13 0.94 1.00

Range (mm) 9.10–13.15 8.90–14.05 8.85–15.60 9.10–13.20 8.85–15.60

N 59 57 55 61 232

S. Takeda / Journal of Experimental Marine Biology and Ecology 330 (2006) 521–527524

(Kruskal–Wallis test: df =3, H =4.009, p =0.2605)

(Table 1). The burrow diameter also did not differ

among the four groups of males (Kruskal–Wallis test:

df =3, H =0.409, p =0.9384) (Table 1).

The proportion of behaviour responses to the un-

painted females before painting differed between the

males that were smaller and larger than the female (G-

test: df =2, G2=10.491, p =0.0053) (Table 2). That is,

when the males courted the females, two-thirds of the

smaller males performed the lateral–circular wave, but

fewer than half of the larger males did so (G-test: df =1,

G2=10.401, p =0.0013) (Table 2). After painting, some

males of both sizes changed their waving behaviour

(Table 2). These results indicate that the males changed

their waving form according to the situation of the

females.

Table 2

Numbers of larger (L) and smaller (S) males that changed their pattern of b

Behaviour White Red

(NaturalYAltered) L S L S

CircularYCircular 9 4 4 2

CircularYStraight 14 1 3 5

CircularYRepulsion 1 3 4 4

(Total) (24) (8) (11) (11)

StraightYCircular 3 0 0 0

StraightYStraight 14 5 17 0

StraightYRepulsion 2 2 14 3

(Total) (19) (7) (31) (3)

RepulsionYStraight 1 0 0 0

RepulsionYRepulsion 0 0 1 0

(Total) (1) (0) (1) (0)

Circular; lateral–circular wave, Straight; lateral–straight wave.

3.2. Individual test

The males that repelled females before they were

painted were excluded from the statistical analysis,

because the mature males were considered to be

attracted by the females before painting. The propor-

tion of males that repelled females after painting did

not differ between the lateral–circular and lateral–

straight wavers in each group of the larger or smaller

males tested with the females painted in different

colours (Fisher’s exact probability test: p N0.05).

When the lateral–circular and lateral–straight wavers

that courted females before painting were pooled, the

proportion of larger or smaller males that repelled

females after painting differed among the four colour

groups (G-test: larger; df =3, G2=26.208, p b0.0001;

ehaviour towards the females after painting

Blue Black Total

L S L S L S

10 0 9 2 32 8

3 0 4 2 24 8

6 5 10 9 21 21

(19) (5) (23) (13) (77) (37)

7 1 1 0 11 1

9 0 6 1 46 6

9 2 13 2 38 9

(25) (3) (20) (3) (95) (16)

0 0 0 0 1 0

2 1 1 1 4 2

(2) (1) (1) (1) (5) (2)

Page 5: Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

Fig. 1. Proportion of larger (A) and smaller (B) males (relative to the presented females) that courted the females before painting and then repelled

them after painting, and proportion of quadrats (C) including males that repelled females after painting. Treatments with different letters are

significantly different (Fisher’s exact probability test, p b0.05).

S. Takeda / Journal of Experimental Marine Biology and Ecology 330 (2006) 521–527 525

smaller; df =3, G2=8.140, p =0.0432). This result

means that the male fiddler crabs discriminated the

colours or luminosities.

To clarify the function of body colour as a signal in

crab society, I compared the proportion of males that

courted or repelled females after painting between each

pair of the four colour groups (Fig. 1A). The larger

males formed two clusters: white; and red, black and

blue (Fig. 1A), and the smaller males showed a signif-

icant difference between white and blue (Fig. 1B).

3.3. Subgroup test

To exclude the possibility that the males’ responses

affected each other (pseudo-replication), I tested the

number of quadrats in which the males did or did not

repel the females using Fisher’s exact probability test.

The four groups formed two clusters: white; and red,

black and blue (Fig. 1C). This result supports the

contention that male fiddler crabs discriminate colours

or luminosity.

4. Discussion

The differences between the behavioural responses

of males of the fiddler crab U. perplexa to conspecific

females before and after painting of the females indicate

that they can discriminate colour or luminosity. Colour

or luminosity functions as a visual signal, promoting

the modification of attitude and motion.

Most U. perplexa males courted unpainted conspe-

cific females larger than themselves by using the later-

al–circular wave. Fiddler crabs can see things above the

level of their eyes well (Layne et al., 1997). This fact

probably explains why the males that were smaller than

the females used a lateral–circular wave to court, be-

cause they have to raise their major chelipeds into the

female’s field of vision. In addition, these facts indicate

that the male fiddler crabs visually measured their

respective sizes, and then chose the appropriate form

of waving.

The U. perplexa males courted the unpainted

females regardless of their relative body size, although

the larger males copulate in the burrow (Nakasone and

Murai, 1998). When the red-, black- or blue-painted

females were presented, the proportion of courting

larger males was significantly lower than that when

the white-painted females were presented. The U. per-

plexa males perhaps recognized a white body colour as

indicating that reproduction is possible, because most

males courted white-painted females as frequently as

the unpainted females.

The smaller males showed a similar tendency, except

that the proportion of courting males was slightly lower

when the white-painted females were presented than

when the unpainted females were presented. On Oki-

nawa Island, another fiddler crab, U. vocans, dwells in

the same biotope (Murai et al., 1982). U. vocans, which

is slightly larger than U. perplexa, becomes whiter in

the reproductive season, and wander about the sandy

flat (Nakasone et al., 1983; Christy and Salmon, 1984).

These facts suggest that larger whitish females are

likely to be U. vocans, and so the colour signal dis-

courages the smaller males of U. perplexa from court-

ing, together with the sexual dimorphism of U.

perplexa whose males are lager than the females

(Crane, 1975).

In addition, the proportion of courting larger males

was much greater than that of smaller males when the

blue-painted females were presented. The soldier crab

Page 6: Behavioural evidence for body colour signaling in the fiddler crab Uca perplexa (Brachyura: Ocypodidae)

S. Takeda / Journal of Experimental Marine Biology and Ecology 330 (2006) 521–527526

M. brevidactylus, with spherical blue body and slender

chelipeds, which is slightly smaller than U. perplexa,

inhabit the same sandy flat (Nakasone and Akamine,

1981; Takeda and Murai, 2004). The soldier crab walks

forwards, unlike the fiddler crabs which walk sideways

(Takeda and Murai, 2004). The sympatric existence of

the soldier crabs and the insufficient experience of the

smaller males may be relevant to the low proportion.

On the other hand, the proportions of courting males

did not differ between the smaller and larger males

when the red- or black-painted females were presented.

These colours perhaps mean that the females are not

ready to reproduce.

Murai et al. (2002) described that the males of the

fiddler crab Uca paradussumieri assess the reproduc-

tive situation of the females by using courting gestures

(tapping and stroking the carapace) and touching the

abdomen. These males perform scarcely any attractive

courting display (Crane, 1975). Instead, they approach

the females and mate near or in the females’ burrows.

In contrast, U. perplexa males attract conspecific

females into the males’ burrows by using courting

display without touch (Nakasone and Murai, 1998).

In addition, some of the males that courted the unpaint-

ed females flicked the painted females with the major

cheliped. These facts strongly suggest that the diurnal

fiddler crab U. perplexa depends on visual signals for

social communication, rather than on chemical signals.

In the New World, some species of fiddler crabs

inhabiting tropical and subtropical tidal flat are fre-

quently prey to birds (e.g., Koga et al., 1998). The

females are camouflaged against the ground in the

reproductive season (Crane, 1975). On the other hand,

the wandering females of U. perplexa have various

body colours, some with lateral stripes, as have other

fiddler crabs in the Old World (Crane, 1975). The

various body colours are considered to disrupt visual

searches by predators (e.g., Dawkins, 1971). The vivid

colour of the wandering females is probably a signal to

distinguish mature females from immature females,

other species and grapsid predator crabs, which are

coloured similar to the ground. The difference in the

strength of predation pressure probably influences the

development of body colour as a visual signal. The

various body colours may be relevant to the speciation

and coexistence of the fiddler crabs in the Old World.

Acknowledgement

I thank Dr. M. Murai, Mrs. Y. Nakano and S. Naka-

mura and other staff of Sesoko Station, Tropical Bio-

sphere Research Center, University of the Ryukyus, for

their help and facilitating my work there. I am grateful

to Dr. M. Murai for his invaluable information and

suggestions for this study. This study was partially

supported by Grant-in-Aid for Scientific Research (C)

from Japan Society for the Promotion of Science (No.

12640605). [PH]

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