JOURNAL OF CRUSTACEAN BIOLOGY, 22(1): 157–161, 2002
REPRODUCTIVE CYCLE AND RECRUITMENT PERIOD OF OCYPODE
QUADRATA (DECAPODA, OCYPODIDAE) AT A SANDY BEACH IN
SOUTHEASTERN BRAZIL
Maria Lucia Negreiros-Fransozo, Adilson Fransozo, and Giovana Bertini
(MLNF, AF, GB) NEBECC (Núcleo de Estudos em Biologia, Ecologia e Cultivo de Crustáceos);
(MLNF, AF) Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista, UNESP,
18618-000 Botucatu, SP, Brasil (e-mail: [email protected])
A B S T R A C T
The reproductive cycle and recruitment period of a ghost crab population from Ubatuba, São Paulo,
Brazil were investigated by means of examining the developmental stages of gonads of breeding
crabs and the ingress of young recruits to the studied population. Monthly collections over a one-year
period were carried out during nocturnal low-tide periods at “Vermelha” beach. The morphology of
the abdomen and pleopods was used for sex determination. All captured crabs were measured for
carapace width and dissected for the determination of the development stage of the gonads. A total
of 582 specimens was captured: 271 males, 241 females, and 70 juveniles. Size ranged from 8.5 to
37.5 mm for males, from 9.5 to 39.2 mm for females, and from 5.8 to 12 mm for early juveniles. Median size of males and females did not differ statistically. The frequency of ovigerous females was
markedly low. The onset of sexual maturity in females is achieved at around 23 mm of carapace
width. Mature females with advanced gonad stages were not recorded from May to September. Recruitment of young was highest during summer, but the presence of early and late juvenile specimens
throughout the year indicates that continuous recruitment is taking place in the studied population.
Crabs of the genus Ocypode Fabricius,
1798, known as ghost crabs, are commonly
found in tropical and subtropical sandy
beaches around the world. This genus is represented in the Western Atlantic by Ocypode
quadrata (Fabricius, 1787) which occurs
from Rhode Island, U.S.A. (42°N and 70°W)
to Rio Grande do Sul, Brazil (30°S and
50°W) (Melo, 1996). Despite its broad geographic distribution, little is known about the
reproduction of members of Ocypode in the
Americas.
Haley (1969, 1972) studied the reproductive biology of O. quadrata along the Central Texas coast, but the wide range of distribution of this species justifies other studies in distinct geographic areas to investigate
any possible variation or patterns.
Reproductive periodicity has been studied
in several brachyuran species by monthly
sampling for the frequency of ovigerous females over a year. There are species with females reproducing year-round, others with reproduction occurring each year in one or
more seasons, and still others in which the reproductive period occurs every other year in
one season (usually spring). All of these patterns are correlated with favorable local environmental conditons. According to Costa
and Negreiros-Fransozo (1998), portunid
crabs commonly reproduce continuously in
subtropical and tropical regions because environmental conditions are generally favorable
for feeding, gonad development, and larval release, whereas in temperate regions reproduction is often restricted to the warmer months.
Ovigerous females of O. quadrata possibly
might remain in their burrows while incubating, like in other ocypodid species
(Christy, 1982). In this sense, an investigation
of its reproductive cycle would be more accurate if based on combined results from gonad-development analyses and frequency estimates of first juveniles than based only on
a seasonal account of the ovigerous-ratio.
Reproductive cycle and recruitment of
young were studied for the ghost crab O.
quadrata at “Vermelha” beach (23°27′36″S
and 45°02′54″W), Ubatuba, southeastern
Brazil, by means of obtaining monthly records
of gonad developmental stages and juvenile
frequency within the studied population.
MATERIALS AND METHODS
Climate conditions at Ubatuba are typical of a subtropical region. Mean temperature of the surface waters
is around 18°C in winter and about 29°C in summer (Negreiros-Fransozo et al., 1999). The shallow waters (< 10
157
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 1, 2002
m) at the São Paulo northern coast may be relatively cold
during summer due to the intrusion of South Atlantic Central Current Waters (Pires, 1992).
All emergent crabs were collected during nocturnal
low tide periods throughout 1998, at “Vermelha” beach,
Ubatuba, São Paulo. A transect of 9 m × 500 m along
the beach was scanned for crabs by three collectors each
month. Captured individuals were placed in separate labeled plastic bags and frozen until later analysis.
In the laboratory, crabs were coded, and their maximum carapace width (CW) measured with a caliper (0.1
mm). Crabs were examined under stereomicroscope in order to check the development of abdominal appendages
as follows: early juveniles = pleopods absent; late juveniles = developing pleopods; adult crabs = fully developed pleopods. Condition of gonad development was also
verified under stereomicroscope following, in general, the
criteria suggested by Haley (1972) and Costa and Negreiros-Fransozo (1998). The gonads were classified according to shape, size, and color as follows: Females: Immature (I) = ovary thin and translucent, undifferentiated;
Initial Maturing (IM) = color ranging from opaque white
to pale-yellow, ovary branches and their connection
clearly visible; Advanced Maturing (AM) = ovary fills almost whole thorax cavity, bright orange coloured, lobes
are evident. Males: Immature (I) = testicles and deferent
ducts cannot be observed; Initial Maturing (IM) = testicles are recognized only under magnification, gonad filamentous and transparent or whitish; Advanced Maturing
(AM) = testicles are fully developed, bright white deferent ducts can be clearly divided in their front, median and
back portions.
Environmental data (air temperature, water surface
temperature, and pluviosity) were provided by the “Instituto Oceanográfico” of “Universidade de São Paulo.”
A Kruskal-Wallis test was used for comparing median
size among individual categories (P < 0.05) (Sokal and
Rohlf, 1995).
Pearson’s correlation analysis was used for testing the
association between air temperature, sea water surface
temperature, and pluviosity with the percentage of functionally mature females bearing advanced maturing gonads (α = 0.05) (Sokal and Rohlf, 1995).
RESULTS
A total of 582 crabs, comprising 271 males,
241 females, and 70 early juveniles, was obtained. Males and females were recorded in
all samples, but early juvenile crabs were not
recorded in April, July, or December (Table
1). Ovigerous females comprised a very small
percentage (2.6%) of the total sampled population and of all females captured (6.2%).
Size-frequency distribution using 3 mmwide size classes indicate a bimodal distribution in the population probably corresponding to two age-groups (Fig. 1). Crabs of
both sexes with maturing (= developed) gonads were found. By analyzing the frequency
of maturing individuals in each size class, we
concluded that the beginning of gonad maturation occurs at a mean size of about 20 mm
for males and 23 mm for females.
Table 1. Number of Ocypode quadrata collected each
month throughout 1998 at “Vermelha” beach, São Paulo,
Brazil.
Month
Early
juvenile
crabs
Males
Non-ovigerous
females
Ovigerous
females
Total
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Dec
Total
21
25
6
0
2
6
0
2
3
2
3
0
70
30
37
49
15
15
14
10
22
14
15
30
20
271
29
7
28
23
21
10
27
26
13
9
16
17
226
0
3
5
4
1
0
0
0
0
1
1
0
15
80
72
88
42
39
30
37
50
30
27
50
37
582
Size range within each population category
is 8.5–37.5 mm for males, 9.5–39.2 for females, and 5.8–12 mm for early juveniles.
The median sizes of males and females did not
differ statistically (P > 0.05) (Fig. 2). Carapace width of the ovigerous crabs was 30.4 ±
4.3 mm and varied from 24.5 to 39 mm.
Juvenile and adult crabs were found
throughout the year; however, the highest
captures occurred in austral summer (from
January to March) (Fig. 3). The temporal frequency of early juveniles indicates that the
highest recruitment period occurs during summer months.
Gonads of crabs collected during summer,
early fall, and early spring were found to span
all developmental stages independently of
sex (Fig. 4a, b). For females, all stages of
gonad development co-occurred from October to April, but apparently there were two
pulses of ovigerous females (one from February to May and another from October to
November).
The relative frequency of functionally mature females with advanced mature gonads
tends to increase with increasing air temperature and sea water surface temperature (Fig.
5) (correlation coefficient r = 0.60 for air temperature, r = 0.64 for water surface temperature (P < 0.05)). Additionally, the correlation coefficient for pluviosity was r = 0.67
(P < 0.05).
DISCUSSION
The size-frequency distribution of the sampled population of O. quadrata at “Vermelha”
beach shows a bimodal distribution that could
NEGREIROS-FRANSOZO ET AL.: REPRODUCTIVE CYCLE AND RECRUITMENT OF O. QUADRATA
159
Fig. 1. Seasonal size-frequency distributions of Ocypode quadrata (n = 512). Sex and stages of gonad development are distinguished. Monthly sample sizes in Table 1.
indicate two different age-groups during the
study period. Alberto and Fontoura (1999),
who studied a more southern Brazilian ghost
crab population, found the same pattern of
size distribution of this species. However, it
should be pointed out that the low incidence
of crabs from 16.6 to 24.5 mm of CW in the
present work, particularly in the case of fe-
males, might be due to their cryptic habit.
This could indicate the existence of a critical phase when crabs remain in their burrows
to avoid predation, thus making their capture
more difficult compared to other crabs.
Fig. 2. Ocypode quadrata. Size comparison among
population categories (* indicates significant difference;
P < 0.05). Sample sizes in Table 1.
Fig. 3. Ocypode quadrata. Montly relative frequency of
each population category during the study period. Sample sizes in Table 1.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 22, NO. 1, 2002
Fig. 5. Association between environmental temperature
(air and surface water) with proportion of mature females
throughout the year.
Fig. 4. Ocypode quadrata. Proportion of crabs bearing
gonads in each developmental stage during the study period. a, Females; b, Males (* indicates the presence of
ovigerous females). Monthly sample sizes in Table 1.
Environmental conditions are commonly
mentioned as influencing some physiological processes (Sastry, 1983). Reproductive periodicity of marine organisms is usually associated with variations of certain environmental variables, such as temperature. In the
southeastern Brazilian region, upwelling of
the South Atlantic Central Water current is responsible for the decrease of coastal water
temperature during summer, among other alterations of bottom-water characteristics
(Pires, 1992). As a result, surface-water temperature often follows an equivalent seasonal
trend, which directly influences the biology
of the littoral ghost crab O. quadrata.
As pointed by Alberto and Fontoura (1999)
for a southern Brazilian ghost crab population, the reproductive activity of O. quadrata
in Ubatuba is also characterized by a heterogeneity in female gonad maturation, which
is represented by an extended reproductive
period (from October to May). Based on the
temporal variation of the proportions of crabs
(males and females) with advanced maturing
gonads, it is assumed that reproduction follows a seasonal trend in the Ubatuba region.
However, early juveniles are present yearround, indicating continuous recruitment to
the adult population.
The fact that the abundance of females with
fully developed gonads is positively correlated with air temperature, surface water temperature, and pluviosity (P < 0.05) may indicate that better conditions for gonad development are met during the warmer and rainy
season. On the other hand, a decrease of water temperature caused by the South Atlantic
Central Waters in the warmer months could
delay larval release by ovigerous females, diminishing juvenile recruitment.
Comparatively, the ghost crabs studied in
the North Western Atlantic are bigger than
those studied in the South Western Atlantic.
The maximum sizes attained by the adult
crabs of O. quadrata on the Brazilian coast
have been 39.7 mm of CW (Alberto and Fontoura, 1999), 40.7 mm of CW (Corrêa and
Fransozo, 2000), and 39.2 mm of CW (present study). On the other hand, Milne and
Milne (1946) found a ghost crab as large as
48 mm of CW, and Haley (1969) recorded another one with 53.5 mm of maximum CW.
In our study area, O. quadrata attains maturity at a smaller size than that determined by
NEGREIROS-FRANSOZO ET AL.: REPRODUCTIVE CYCLE AND RECRUITMENT OF O. QUADRATA
Haley (1969 and 1972) on the Texas central
coast (males ≥ 24 mm and females ≥ 26 mm
of CW). Whether such difference represents
genotypic variations or environmental constraints, e.g., different availability of food resources between these studied areas as found
for other brachyuran crabs (Conde and Díaz,
1989; Díaz and Conde, 1989), awaits further
research. However, there are at least two papers (Wolcott, 1978; Robertson and Pfeiffer,
1982) that discuss different kinds of feeding
behavior for O. quadrata (predators, scavengers, or deposit feeders) as a function of
food availability in the habit.
While remaining in their burrows throughout brooding, female ocypodid crabs may either incubate their eggs without feeding (e.g.,
Uca pugilator, Christy, 1982; O. ceratophthalmus, Haley, 1973), or feed actively during such period (e.g., U. vocans, Salmon,
1984). The small number of ovigerous crabs
obtained in this investigation suggest that
they can stay in their burrows for brood protection. Those females were probably just
leaving their burrows for larval release when
they were captured. Further evidence of such
cryptic habit is provided by the fact that all
ovigerous females collected were carrying
eggs about to hatch. Another possibility concerning the low occurrence of ovigerous crabs
could be an artifact of small sample size;
however, other studies on this species (Alberto and Fontoura, 1999; Corrêa and Fransozo, 2000) also found a low percentage of
this demographic category.
ACKNOWLEDGEMENTS
To FAPESP (Fundação de Amparo à Pesquisa no Estado de São Paulo) for providing good infrastructure conditions for investigation (#94/4878-8; #95/8520-3) and
FUNDUNESP (Fundação de Amparo à Pesquisa na Universidade Estadual Paulista) for financial support to the
first author to attend The Crustacean Society 1999 Summer Meeting. Authors are grateful to Rogério C. Costa
for his help during samplings.
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RECEIVED: 11 August 2000.
ACCEPTED: 21 June 2001.