JOURNAL OF CRUSTACEAN BIOLOGY, 27(3): 425–436, 2007
REPRODUCTION OF THE BLACK LAND CRAB, GECARCINUS RURICOLA, IN THE
SAN ANDRES ARCHIPELAGO, WESTERN CARIBBEAN
Richard G. Hartnoll, Mark S. P. Baine, Arne Britton, Yolima Grandas, Jennifer James,
Alejandro Velasco, and Michael G. Richmond
(RGH, correspondence) Port Erin Marine Laboratory, University of Liverpool, Port Erin,
Isle of Man IM9 5ED, British Isles ([email protected]);
(MSPB) Motupore Island Research Centre, University of Papua New Guinea, PO Box 320,
University 134, National Capital District, Papua New Guinea;
(AB, YG, JJ, AV) CORALINA, San Luis Road, KM 26, PO Box 725, San Andres Island, Colombia;
(MGR) School of Life Sciences, Heriot-Watt University, Edinburgh, U.K.
ABSTRACT
Reproductive biology of the black land crab, Gecarcinus ruricola (Linnaeus, 1758), has been studied in the San Andres Archipelago in the
Western Caribbean, on the islands of San Andres and Old Providence. Both sexes become mature at about 50 mm maximum carapace
width, and very few specimens below this size take part in the annual breeding migration. In females the ovaries mature progressively
from January to April, and laying occurs from May to July. There is no evidence that individual females lay more that once in a year. The
breeding migrations were monitored in 2003 and 2004 by recording specimens crossing the coast road (running 50-100 m from the upper
shore). On both San Andres and Old Providence migration was limited to specific stretches of the western shores. On both islands
migration occurred from late April to July, intensity varying with time. Migration peaks were not consistent between islands or years, and
could not be clearly linked to environmental factors. Migrating crabs were mostly female (. 80%), and a proportion were bearing ripe
eggs: on San Andres ovigerous female predominated. Thus some females mated and laid eggs on the landward side of the coast road,
others on the seaward side. Migrating females were on average larger than migrating males, in contrast to the situation in the nonmigrating populations. Log egg number varied isometrically with log carapace width (slope ;3.0): for 70 mm CW the calculated
fecundity was 85,000 eggs. Percentage reproductive investment, based on dry weight, ranged from 1.7 to 9.8%, with a mean of 4.95%.
Recruitment was only observed once, with a mass return of megalops to Old Providence in June 2004. All evidence points to very irregular
recruitment.
INTRODUCTION
accessibility to mainland-based researchers. The third
species, Gecarcinus ruricola (Linnaeus, 1758), is essentially
restricted to Caribbean islands—there are few records for
mainland America. Thus, the records for ‘Florida’ (see
Keith, 1985; Chace and Hobbs, 1969) are in fact confirmed
only by specimens for the island of Loggerhead Key, in the
Tortugas (Carson, 1967): Bliss et al. (1978) report it as
‘‘quite rare’’ at Sabal Point in south east Florida, the sole
mainland location. The references to ‘Nicaragua’ by Chace
and Hobbs (1969) and Keith (1985) are not confirmed in
any other sources, and as no specimens or locations are
cited, this reference as a mainland site is dubious. In
contrast, its island distribution is widespread and well
documented through the Greater and Lesser Antilles and the
Bahamas, from the western end of Cuba eastwards to
Barbados (see Carson, 1967, Table 1, for a comprehensive
summary). It is also recorded from Curacao (off the coast
of Venezuela). In the western Caribbean there are three
outliers: the Swan Islands 150 km north of Honduras (Keith,
1985), and Old Providence and San Andres Islands (jointly
known as the San Andres Archipelago) 250 km east of
Nicaragua (Carson, 1967 and Hartnoll et al., 2006b).
In the Caribbean, Gecarcinus ruricola is the most
terrestrial of the land crabs. It inhabits damp and shaded
forest areas, where it burrows in the soil, or shelters under
rocks or amongst tree roots. It is found many kilometres
from the sea, and to considerable altitudes, .300 m in
The family Gecarcinidae are popularly referred to as ‘land
crabs’, though they are not the only terrestrial crabs, nor
indeed the crabs most completely adapted for a life on land
(see Hartnoll, 1988). Gecarcinids spend most of their adult
life on land, but females must return to the sea to release
their larvae (even the cavernicolous Discoplax longipes
A. Milne-Edwards, 1867 (Ng and Guinot, 2001)), which all
undergo planktotrophic development. The terrestrial adaptation of adult gecarcinids varies widely. The cavernicolous
Discoplax longipes is largely aquatic (Ng and Guinot,
2001). Some, such as several Cardisoma spp., are
essentially supratidal, frequently entering the sea on high
spring tides, and always retaining access to free water.
Others, such as various Gecarcinus and Gecarcoidea
species, can exist many kilometres from the sea, away from
free water, and enter the sea only after the often lengthy
annual spawning migration.
There are three gecarcinids in the Caribbean. Cardisoma
guanhumi (Latreille, 1852) and Gecarcinus lateralis
(Fréminville, 1835) are widespread both on Caribbean
islands and along the adjacent mainland coast. Both have
been relatively well studied (for example: for C. guanhumi
see Costlow and Bookhout, 1968; O’Mahoney and Full,
1984; Wolcott, 1984: for G. lateralis see Klaassen, 1975;
Bliss et al., 1978; Willems, 1982; Wolcott and Wolcott,
1988; Capistran-Barrados et al., 2003), probably due to their
425
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 3, 2007
Table 1. Gecarcinus ruricola. Seasonal ripening of the ovaries from October 2003 to July 2004, determined by changes in ovary size and colour (Y/O ¼
yellow/orange; B/G ¼ brown/green). Only specimens .60 mm CW (above the size of maturity) were included in the analysis. Numbers of crabs in each class
are listed.
San Andres
Old Providence
Ovary size
Ovary colour
Ovary size
Ovary colour
Month
Small
Medium
Large
Y/O
B/G
Small
Medium
Large
Y/O
B/G
Oct 03
Nov 03
Dec 03
Jan 04
Feb 04
Mar 04
Apr 04
May 04
Jun 04
Jul 04
15
12
—
16
15
5
9
7
—
—
7
7
—
2
9
8
1
3
—
—
2
1
—
0
4
4
12
10
—
—
20
20
—
14
19
13
7
8
—
—
4
0
—
4
9
4
15
12
—
—
19
—
15
12
11
5
—
7
23
19
4
—
4
8
8
4
—
1
4
4
1
—
0
0
1
11
—
3
0
1
31
—
18
9
5
7
—
5
20
11
2
—
1
11
15
15
—
6
7
13
Dominica (Chace and Hobbs, 1969), and .1000 m in
Jamaica (Britton et al., 1982). It is mainly nocturnal, except
during the breeding migration when large numbers may be
active by day. Nocturnal activity is stimulated by rainfall,
but inhibited by bright moonlight (Hartnoll et al., 2006b). In
the Caribbean, it is the most widely exploited gecarcinid for
human consumption, though Cardisoma guanhumi is
consumed on a smaller scale (Maitland, 2002).
Despite this ecological and economic interest, G. ruricola
has been very little studied. Carson (1967, 1974) described
its symbiotic relation with flies of the genus Drosophila.
Britton et al. (1982) compared its biometry, distribution and
activity with those of G. lateralis. Prahl and Manjarres
(1983) briefly outlined its coastal distribution around Old
Providence. Mulder and Stam (1987) and Hoeven and
Walters (1998) described distribution and population
structure in Saba. Distribution and abundance have been
studied in Dominica (Magin, 2003). Nevertheless, knowledge regarding the species is still very fragmentary,
especially regarding reproduction. Stebbing (1893) and
Calman (1911) describe the annual breeding migration, the
former in more detail. Hoeven and Walters (1988) briefly
discuss reproduction in Saba. Sjogreen (1999) describes the
breeding migration in Old Providence Island.
In 2002, a comprehensive study programme was initiated
to examine the basic ecology and biology of the species in the
San Andres Archipelago, and the characteristics of
its exploitation. This was triggered by concern that it was
being overexploited. Previous papers from this study cover
population structure, stock size, and relative growth (Hartnoll
et al., 2006b), the landward return and description of the
megalop stage (Hartnoll and Clark, 2006), and implications
for management of the catchery (Baine et al., in press). This
paper reports on the reproductive biology of the species.
Objectives to clarify are the size at maturity, the seasonal
maturation of the gonads, the reproductive migration,
fecundity and reproductive investment, and recruitment.
MATERIALS AND METHODS
Nicaragua (Fig. 1). Within the Archipelago Gecarcinus ruricola occurs
only on the islands of San Andres and Old Providence/Santa Catalina. San
Andres (hereafter referred to as ‘SA’) has an area of 27 km2, a maximum
altitude of ;100 m, and consists of raised coral limestone (Parsons, 1956).
The population is thought to exceed 80,000, and many areas have been
developed for tourism or converted to cultivation—in consequence the
original forest habitat has been much depleted. Old Providence (not to be
confused with New Providence Island in the Bahamas) has an area of
21 km2, a maximum altitude of 360 m, and is connected to the small island
of Santa Catalina (area 1.3 km2) by a floating bridge. The two islands
(hereafter jointly referred to as ‘OP’) are of volcanic origin, have
a combined population of little over 4000, and are relatively undeveloped
with much of the forest ecosystem intact. References to ‘the Archipelago’
relate to SA and OP combined—see Baine et al. (2007) for a review of the
current environmental and demographic status of the Archipelago.
Size at Maturity, and Seasonal Maturation of Ovaries
All references to crab size are to maximum carapace width (CW).
Preliminary studies were made to determine the approximate size at
maturity, and the reproductive season. These studies, together with
background data from other unpublished sources, indicated a size at
maturity of ;50 mm CW in each sex, and a breeding season from April
to July. As a result the following protocols were adopted. Specimens
were collected by the project staff, or when necessary purchased from
crab catchers. Crabs were killed by freezing for ;30 min. at 208C, and
when possible examined fresh. Similar studies were carried out on SA and
OP—the indicated sample sizes apply to the work on each island.
To examine size at maturity, samples were collected only during the
period immediately preceding the breeding season (namely from February
to May). This was to prevent the analysis being confounded by specimens
of ‘mature’ size, but with undeveloped or spent gonads outside the breeding
season. For each sex ideally at least 10 specimens were collected within
each 10 mm CW size class: this was not possible for some sizes.
To examine the seasonal maturation of the ovaries, only females .60
mm CW were sampled. This eliminated immature specimens from the
analysis. A sample of 20 females was examined in each month from
October to April.
For both analyses the following data were recorded from each specimen.
For males: CW; appearance of vas deferens, categorized as immature,
small, medium or large. ‘Immature’ are very small, translucent, and usually
invisible to the naked eye. The other categories are opaque white, and of
increasing size. For females: CW; size of ovary, categorized as immature
(¼ usually invisible), small, medium or large; colour of ovary, categorized
as translucent (immature), yellow-orange (maturing), or brown-green
(mature); condition of spermathecae, categorized as unmated (translucent
and effectively invisible), mated (opaque white, but flattened), or swollen
(opaque white, rounded).
Study Area
The Reproductive Migration
The San Andres Archipelago is an extensive area of islands, banks and cays
in the western Caribbean. It is an offshore province of Colombia, located
some 700 km northwest of mainland Colombia, and 250 km east of
The observations on each island were of crabs observed crossing the coastal
road, which in the areas involved was usually between 50-100 m from the
upper shore. Data are not available on the migration patterns further inland,
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HARTNOLL ET AL.: REPRODUCTION OF GECARCINUS RURICOLA
Fig. 1. The Caribbean, to show the location of the San Andres Archipelago.
where the sex composition may differ, nor on the activity of crabs at the
shore: the precise timing of spawning behaviour by females may differ from
their migration patterns across the road. Logistic constraints precluded
collection of these additional data, which would have been valuable.
Surveys were carried out throughout the breeding season on the known
migration areas (Fig. 2). When migration was sparse surveys were
conducted every third night or so, but the frequency was increased during
periods of higher activity. The procedure was to drive and/or walk, as
appropriate, along the coast road once during the evening, normally between
2000 and 2200 (well after the time of dusk). Preliminary studies had shown
that activity at this time was representative of migration intensity. The road
was divided into sections. On SA it was split into 1 km sections,
conveniently indicated by roadside distance markers, from Km 1 to Km 15.
On OP, since distances were smaller, and migrating numbers greater, the
road was divided into 13 sections over a distance of ;4 km. Within each
section crabs encountered were sexed, CW measured, and presence of eggs
(and in selected specimens, incubation stage) on females recorded. Unless
needed for other studies, the crabs were released unharmed. It is important to
note the limitations of this procedure. Firstly, it was not normally possible to
adequately discriminate seaward and landward migration: by the time that
crabs were spotted by using lights, their activity had been disrupted.
Secondly, no estimate of total numbers migrating per night could be made,
only of the number on the road at the time of the survey. The method
provides only comparable data over time, and between locations, on the
relative numbers migrating. In these respects the data are reliable. On both
islands the coast road is of constant width, so comparisons between location
are valid. All personnel involved had training in the survey procedures, so
surveys on different dates are comparable.
Roadkills were also recorded during the surveys. They were counted,
and where possible sex and presence of eggs recorded. These complemented the data on live crabs.
Fecundity and Reproductive Investment
Determination of fecundity and reproductive investment was made only on
ripe eggs. Females with eggs were collected during the reproductive
migrations. The eggs were removed, and the dry weight of both the female
(without eggs) and the egg mass were determined after drying to constant
weight in an oven at 1008C. Reproductive investment (RI) was determined
by expressing egg mass dry weight as a percentage of female body dry
weight (after removal of the egg mass). This is the most common means of
calculating RI (see Hines, 1982).
To determine fecundity a subsample of eggs (;300) was removed from
the egg masses of selected females before drying. These eggs were counted
using a Bogarov tray, dried as above, and weighed. The results were used to
determine the mean dry weight per egg. This value was used to convert the
dry weight of egg mass to egg number. Log egg number was regressed on
log female CW.
Recruitment
A lookout was kept for returning juveniles during the breeding season, and
detailed observations were made of any occurrence. In addition, in the
absence of formal records, anecdotal information was sought regarding
recruitment events in earlier years.
RESULTS
Size at Maturity
For males from both islands the results (Fig. 3) are similar.
Specimens less than 50 mm CW were either immature, or in
the early stage of maturity, with ‘small’ vas deferens.
Specimens above 50 mm were in almost all cases maturing,
and above 70 mm CW all had ‘medium’ or ‘large’ vas
deferens. The slight differences between the two islands
must be treated with caution, since the data were collected
by different teams. A size at first maturity of 50 mm CW is
a fair conclusion.
The results for females are very similar from the two
islands, so only those for OP are shown in Fig. 4. On all
three criteria—ovary size, ovary colour, and condition of
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 3, 2007
Fig. 2. The islands of San Andres (A) and Old Providence (B). The heavy lines show the main migration zones. The watersheds, and the mean number of
crabs per hectare in forest habitats (see Hartnoll et al., 2006b) are shown. The start and finish points of the migration monitoring areas (start of Km1 to end of
Km 15 on SA; start of section 1 to end of section 13 on OP) are indicated by arrows.
spermathecae—the results are effectively identical. Maturity
occurs at a carapace width of around 50 mm, a similar size
to that in the males. These results were confirmed by
observations made during the breeding migrations (see
below). Very few specimens of either sex ,50 mm CW
participated in the migrations. Furthermore in 2003 only 3
ovigerous females out of ;200 were ,50 mm CW in SA,
and only 8 out of 1050 in OP.
The Reproductive Migration
Seasonal Maturation of Ovaries
Observations were limited to recording crabs crossing the
coast roads, so that the limited personnel resources could
provide an overall record of the relative temporal and spatial
variation in the migrations. This was vital in the context of
recommending management strategies. Absolute numbers
of migrating crabs could not be determined, nor could
the patterns of activity at the water’s edge. Within these
constraints, comparable data were collected for the migrations in 2003 and 2004 in SA and in OP.
Results for the period October 2003 to July 2004 are
presented in Table 1—the gaps were due to unavailability of
survey staff. The results from the two islands are in general
agreement. Over the period October to December the
ovaries were predominantly small in size, and yelloworange in colour. From January to April ovarian maturation
was obvious, with increasing proportions of large and
brown/green ovaries. Then from May to July, as the
breeding season progressed, spent females became apparent
from the increasing proportion with small ovaries: some
small spent ovaries nevertheless retained the brown/green
colouration of ripe ovaries. Females carrying ripe eggs had
small ovaries: there was no evidence of any rapid rematuration, such as might have indicated the production of
a second batch of eggs within the breeding season.
Patterns of Temporal Variation in Migration.—On SA
migration extended from April to July in both 2003 and
2004. However, the migration peaks differed between years.
In 2003 there were activity peaks from 29 May to 5 June,
and on 25 June. In 2004 there was a single peak on 19 May
(Fig. 5A). On OP the 2003 observations extended only from
mid May to mid June (for logistic reasons). Migrations
occurred throughout this period, with no pronounced peaks.
In 2004, migrations occurred from late April to late July:
there was a peak in late April, and a very pronounced peak
on 18-20 May (Fig. 5B). Data from only two years restricts
conclusions. Clearly, the migration season extends over
some three months, but the intensity varies with time. There
is, on each island, substantial variation between years.
Within each year, there is also variation between islands.
HARTNOLL ET AL.: REPRODUCTION OF GECARCINUS RURICOLA
429
Fig. 3. Gecarcinus ruricola. The vas deferens size of males in relation to carapace size, collected in February-May, prior to the breeding season. A, San
Andres. B, Old Providence.
However, in 18-20 May 2004 there was a simultaneous
migration peak on both SA and OP. A longer data series is
needed to determine whether this was just coincidence.
The temporal pattern of roadkills generally reflected, not
surprisingly, the intensity of migration. There were some
inconsistencies, but these could be accounted for by
variation in diurnal timing of peak migration, variation in
traffic flow, and the effect of road closures.
Temporal Variation in Migration, Correlation with
Environment.—On OP between 18 and 23 May 2004 six
observation series were carried out, involving four sections
of road. The results showed differences in peak migration
activity, over this short time period, from 1800 to 0200.
On a longer time scale, attempts were made to correlate
migration activity with moon phase and rainfall. There was
little evidence of correlation with moon phase, but this is not
surprising, since only the activity of crossing the coast road
was recorded. The expected correlation with moon phase is
with the release of larvae into the sea by the females, which
was not investigated. Nevertheless, the migration of females
with very ripe eggs indicated when larval release was
imminent. There was a better correlation between relative
abundance of these ovigerous females and the period around
new moon. There was occasional correlation between
migration activity and recent rainfall, but many other
instances where no such relation was apparent.
Spatial Variation in Migration.—On both islands the
breeding migration was limited to certain parts of the
coastline: this was determined with confidence because of
comprehensive observations along the peripheral coastal
roads. The initial survey strategies were based on the
existing regulations which limited catching during the
breeding season (1 April to 31 July) from the shore to
150 m inland in specific areas. These areas were from Km
11 to Km 14 on SA, and from Lazy Hill (Section 1) to High
Hill (Section 13) in OP (Fig. 2), and for 2003 it was
assumed that these were the main migration zones. On SA it
was soon clear that migration was more extensive, so
broader records were initiated in 2003, and in 2004 formal
observations were made from Km 1 to Km 15. On OP the
designated migration zone was found to be appropriate for
both years.
On SA migration in 2003 was recorded from Km 3 to Km
15, with the greatest numbers observed from Km 11 to Km
14. In 2004 a broader survey recorded migration from Km 1
to Km 15. The largest numbers again occurred from Km 11
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 3, 2007
Fig. 4. Gecarcinus ruricola. Reproductive condition in relation to carapace size for females from Old Providence collected in February-May, prior to the
breeding season. A, ovary size. B, ovary colour. C, spermatheca condition.
to Km 14, but there were also substantial numbers from Km
4 to Km 8 (Fig. 6A). The 2004 data permit a comparison of
the distribution of live crabs and roadkills. The patterns are
broadly similar, except that roadkills were proportionately
higher from Km 3 to Km 7: this reflects the greater traffic
density in that more populated area.
On OP migration was recorded in all sections of the study
area. In 2003 the highest numbers were in sections 10 to 12,
with substantial numbers also in sections 7 to 9, and 13. In
2004 there was a very clear peak in section 11, and lesser
abundance in sections 10 and 12 (Fig. 6B). In 2004
distribution of live crabs and roadkills were compared. The
maximum of road kills was found in section 11, but
proportionately very high numbers in sections 2 to 7. The
latter abundance was due to higher traffic density, and the
fact that these sections lay outside the usual road closure
limits (normally sections 10 to 13).
Size Composition of Migrating Populations.—Details of the
size composition of migrating crabs, based on samples
sexed and measured whilst crossing the coast roads, are
presented in Table 2. The sample of males from SA in 2004
HARTNOLL ET AL.: REPRODUCTION OF GECARCINUS RURICOLA
431
Fig. 5. Gecarcinus ruricola. Timing of migrations in 2004: males, non-ovigerous females, and ovigerous females recorded on the coast roads on each
survey date. A, San Andres. B, Old Providence (some values for 25/04 and 18-20/05 exceed the axis scale: values are given above the open bars).
is small, and values derived from it should be treated with
caution. The total sample sizes between years and between
islands are not comparable, since sampling effort varied.
However, the values for sex ratio and size composition are
comparable.
For both sexes, and both years, sizes were larger on OP
than on SA. This was so for both mean size, and modal size
class. Few of the migrating crabs were below the putative
size at maturity of 50 mm CW (Table 2). The proportion
was very small for females (0.5%-5%), but somewhat larger
for males (2%-9%). The mean size of females was larger
than that for males in all four island/year categories. The
larger proportion of ‘immature’ size males contributed to
this, but does not fully account for it. On OP in particular the
modal size class is larger in females. There are no consistent
trends in crab size between the 2003 and 2004 samples.
Composition of Migrating Populations by Sex and
Reproductive Status.—The proportion of migrating males
crossing the coast roads was always much smaller than that
of females, varying from 3% to 19% of the total sample
(Table 2). There were no consistent trends between years or
islands. Thus during the annual migration only a small
proportion of the mature males visited the sea. Along the
sampled regions of the coast roads there were no consistent
trends in sex ratio nor in reproductive status of females
(ovigerous versus non-ovigerous) (Fig. 6). There was
a general trend in all data sets for the proportion of males
to be higher in the first half of the migration period than in
the second (Fig. 5).
Females were recorded as either ovigerous or nonovigerous. Egg stage was only determined for small
samples, since it could not generally be differentiated in
the field at night with the equipment available. These limited
samples were predominantly of very ripe eggs. Ripe females
ready to lay, and spent females which had shed their eggs,
could not be distinguished in the field. These limitations
restricted the potential analysis, and constrained description
of female migration. Some conclusions can be drawn from
the fairly complete data sets for SA and OP in 2004 (Figures
5 and 6). In the SA series both non-ovigerous and ovigerous
females were present throughout the sampling period from
mid April to early July. On the majority of occasions
ovigerous females predominated. On OP the samples
extended from late April to late July. In that series the
occurrence of ovigerous females was less regular, being on
occasions absent for sequences of five or six samples. In the
majority of samples non-ovigerous females were more
abundant.
Fecundity and Reproductive Investment
These determinations were made only with ripe eggs: some
loss during incubation must be assumed. Fecundity was
determined for 55 females with ripe eggs collected on SA.
They ranged in size from 51.3-90.0 mm CW, with a mean of
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 3, 2007
Fig. 6. Gecarcinus ruricola. Spatial distribution of migrations in 2004. Males, non-ovigerous females, and ovigerous females recorded on the coast roads in
each section. A, San Andres. B, Old Providence.
70.0 mm CW. The dry weight of each egg mass was
determined. This was then converted to egg number using
a value determined for the dry weight per egg. Five samples
of 300-400 eggs from different females were counted, dried
and weighed. The mean dry weight ranged from 3.305 to
4.105 g egg1, with an overall mean of 3.505 g egg1. The
calculated egg number ranged from 18,000 for a female of
53 mm CW to 213,000 for a female of 86 mm CW. Log egg
number was regressed on log CW (Fig. 7):
Log10 egg number ¼ 2:91 log10 CW20:442 ðr2 ¼ 0:61Þ:
The slope is not significantly different from isometry, i.e.,
a value of 3.0. The mean size of the ovigerous females
sampled was 70.0 mm CW, for which the above relationship
predicts a fecundity of 85,000 eggs.
Reproductive investment, on a dry weight basis, was
calculated for the same sample of 55 females. Values ranged
from 1.7% to 9.8%, with a mean of 4.95%. There was no
relationship between reproductive investment and carapace
width (r2 ¼ 0.037).
Recruitment
The only recruitment event observed was on OP in June
2004. Enormous numbers of megalops were observed
emerging from the sea and migrating landwards. They then
crossed the coast road in numbers sufficient to turn it red:
initially those crossing were megalops, but after a delay
occasioned by heavy rain, those crossing had moulted to the
first crab instar. A full account of this event is given in
Hartnoll & Clark (2006). That paper also provides a description of the megalops. The only earlier anecdotal records
of recruitment were for OP in 1992 and 1998.
DISCUSSION
Size at Maturity
There was convincing evidence that specimens of both
sexes matured at a size close to 50 mm CW, with good
agreement between the different indices. For males these
indices were enlargement of the vas deferens, and
participation in the breeding migration. For females they
were ovarian maturation, evidence of mating (spermathecal
condition), production of eggs, and participation in the migration. Sexual maturity occurred at about 50% of the maximum
Carapace width, which is about 110 mm in the Archipelago
(Hartnoll et al., 2006b). In Gecarcoidea natalis (Pocock,
1888), both sexes mature at about 45 mm CW, and have
a maximum size just over 100 mm CW (Hicks, 1985). In
Epigrapsus notatus (Heller, 1865), the smallest ovigerous
female was 17 mm CW, and the largest female 35 mm CW
(Liu and Jeng, 2005). These represent similar size relationships in all three species.
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HARTNOLL ET AL.: REPRODUCTION OF GECARCINUS RURICOLA
Table 2. Gecarcinus ruricola. Composition by size and sex of all migrating crabs measured on the coast roads on SA and OP in 2003 and 2004. All
measurements are in mm carapace width.
Male
Island
SA
OP
Female
Year
Number
% ,50 mm
Mean
Mode
Number
% ,50 mm
Mean
Mode
% males
2003
2004
2003
2004
89
32
211
254
5
9
2
7
63.9
67.1
71.5
66.7
65-70
60-65
75-80
65-70
563
999
2185
1065
2
2
0.5
5
67.3
67.4
74.1
71.2
65-70
60-65
80-85
70-75
13
3
9
19
Seasonal Maturation of the Ovaries
This occurred progressively over the period from January to
April. Then from May onwards, as the breeding season
developed, increasing proportions of small spent ovaries
were found. There were no signs of re-ripening ovaries in
females bearing ripe eggs, as would indicate that they would
soon produce a second batch of eggs. This is in contrast to
various other temperate and tropical crabs where ovarian
maturation is completed within the incubation period, and
relaying occurs with minimal interlude (Hartnoll, 1963,
1965a, 1965b). This slow maturation, and lack of obvious
re-maturation, suggests (though does not prove) that despite
the fairly lengthy breeding season, individual females produce only one batch of eggs per year. There is uncertainty as
to whether other gecarcinids can produce more than one
batch per season. In various species the breeding season is
extended, with several peaks of migration, but there is no
clear evidence for multiple batches in individual females—
see Gecarcoidea natalis (Hicks, 1985), Epigrapsus notatus
(Liu & Jeng, 2005) and Johngarthia lagostoma (H. Milne
Edwards, 1837) (see Hartnoll et al., 2006b). The presence of
substantial populations of adults in inland areas throughout
the migration season, as in Gecarcoidea natalis (Hicks,
1985), indicates that not all specimens participate in any one
migration peak. However, based on ovary condition Gifford
(1962) suggested that Cardisoma guanhumi may spawn
more than once per season, and captive females of
Gecarcinus lateralis can produce up to three batches within
a season (Klaasen, 1975). Marking studies showed that
some females of Gecarcoidea lalandii H. Milne Edwards,
1837 could lay twice within a season (Liu and Jeng, 2007).
Seasonal iteroparity has an important bearing upon lifetime
reproductive investment (see below). The slow growth of
gecarcinids has been attributed to their poor quality diet
(Nordhaus et al., 2006), and the equally slow ovarian rematuration could have the same cause. Those species where
seasonal iteroparity is postulated are species living nearest to
the shoreline, where diet may be more varied and nitrogen
rich: they are also species which inhabit mainland areas, as
well as islands. It may be that their increased reproductive
output enables them to resist greater predation pressure, and
so survive in the more challenging mainland ecosystems.
Reproductive Migration
Since a primary aim of the project was to develop
management strategies, widescale descriptions of the
migration patterns in time and space were imperative. Thus
effort was concentrated on crabs crossing the coast roads,
and data were not gathered on events in the landward forest,
nor on the shoreline. Ideally future studies should
concentrate on limited areas of intense migration, and
examine the composition and behaviour of migrating crabs
at different stages in the course of their movement from the
forest to the shore, and back again. The study on
Gecarcoidea natalis by Hicks (1985) offers a model for this.
Analysis of the temporal patterns of migration is restricted
by having records for only two years, of which not all
are comprehensive. Migration was predominantly nocturnal,
though during the heaviest periods it also occurred
during the day. Nocturnal migration seems the norm in
gecarcininids—see Discoplax longipes A. Milne Edwards,
1867 (Ng and Guinot, 2001), Epigrapsus notatus (Liu and
Jeng, 2005), Gecarcinus lateralis (Klaasen, 1975; Bliss
et al., 1978; Wolcott and Wolcott, 1982), Cardisoma
guanhumi (Gifford, 1962), Johngarthia lagostoma (Fimpel,
1975; Hartnoll et al., 2006a), and Johngarthia planatus
(Stimpson, 1860) (see Ehrhardt and Niaussat, 1970). Only
Gecarcoidea natalis is predominantly diurnal (Hicks, 1985).
On both islands of the archipelago, migration of
G. ruricola occurred over the period from April to July,
but there was not consistency in the pattern. Efforts to
correlate activity with environmental factors were constrained by limitations of the data. There was some
correlation of migratory activity with recent rainfall, and
the migration period did correlate overall with the rainy
season, which is a general trend in gecarcinids. It is the case
in Cardisoma hirtipes Dana, 1851 (Gibson-Hill, 1947;
Shokita, 1971), Cardisoma guanhumi (Gifford, 1962),
Epigrapsus notatus (Liu and Jeng, 2005), Gecarcinus
lateralis (Klaasen, 1975; Wolcott and Wolcott, 1982),
Gecarcoidea lalandei (Liu and Jeng, 2007), Gecarcoidea
natalis (Gibson-Hill, 1947; Hicks, 1985), and Johngarthia
lagostoma (Hartnoll et al., 2006a). Given the dehydration
Fig. 7. Gecarcinus ruricola. Log egg number plotted against log carapace
width. Females from San Andres Island with late stage eggs.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 3, 2007
risk during the extensive overland migrations to the sea the
advantages of a humid environment are clear. In Gecarcinus
ruricola, there was evidence that the migration of females
with ripe eggs was greater at the period around new moon,
suggesting that larval release may be concentrated at such
periods. Lunar rhythms of egg hatching are recorded in
other land crabs. In Gecarcoidea natalis, it is concentrated
in the last quarter (Hicks, 1985), as it is in G. lalandii (Liu
and Jeng, 2007). There was greater larval release at full
moon in Columbia for Gecarcinus lateralis (Klaasen, 1975),
and immediately after full moon in Bermuda (Wolcott and
Wolcott, 1982). In Epigrapsus notatus, larval release is in
the period following full moon (Liu and Jeng, 2005). In
Cardisoma guanhumi, spawning is concentrated near the
full moon (Gifford, 1962).
The spatial limits of migration were consistent on each
island, both with regard to our observations, and in relation
to anecdotal data from previous years. The data are reliable,
since the continuous coast roads on each island facilitate
comprehensive observation. Road kills would clearly
indicate if migrations were occurring in other areas (other
than on Santa Catalina, where there is no continuous road).
The intensity of migration appears to differ on the basis of
observations of live crabs, and of road kills. However, this
can be explained by differences in traffic density, and by the
effect of selective road closures. The reasons for the limited
migration zones are not obvious. The migration zones are
adjacent to the areas of highest crab density (Hartnoll et al.,
2006b), and on OP (no data are available for SA) they are
the same as the zones of recruitment (Hartnoll & Clark,
2006). Thus the parsimonious explanation is that the adult
crabs predominantly remain in the areas close to where they
recruited, and later retrace their steps to the sea. On
Christmas Island, however, both the migration of the adults
and the return of the megalops occurred on all sides of the
island (Hicks, 1985).
In Gecarcinus ruricola, the crabs crossing the coast road
were predominantly females, males always comprising less
that 20% of the total, often much less. It is clear that few
males reached the sea, and it must be assumed that mating
activity is concentrated on the landward side of the coast
road. In Johngarthia lagostoma, females also predominate
5:1 at the shoreline (Hartnoll et al., 2006a). This contrasts
with Gecarcoidea natalis, where males and females migrate
to the sea in similar numbers, and only after both indulge in
‘dipping’ in the sea, does courtship and mating occur
(Hicks, 1985). In contrast, in the cavernicolous Discoplax
longipes, no males were observed in the migration (Ng and
Guinot, 2001). There is a clear inter-specific variation from
no migrating males, to males and females migrating in equal
numbers. The structure of the female genital opening helps
to explain this variation. In the gecarcinids the female
openings are normally occluded by a rigid calcified
operculum: see Hartnoll (1968a) for Gecarcinus ruricola,
and Hartnoll (unpublished) for Cardisoma, Gecarcoidea
and Johngarthia. It is probably a general feature of the
family. Local decalcification allows this operculum to
become mobile for a period of days, and only during that
interval is the female able to copulate, and to lay eggs (see
Hartnoll, 1968b for example). This short term availability of
females entrains male behaviour. Thus where females lay in
their residential area (as in Discoplax), they are not
subsequently available to males, so no males migrate.
Conversely, in Gecarcoidea natalis females lay only after
dipping in the sea, so there must be a mass male migration to
benefit from this limited shoreline female availability.
Gecarcinus ruricola occupies an intermediate status. Some
females lay (and therefore mate) prior to the final migration
to the sea, whilst others mate and lay only near to the shore.
Thus a proportion of males migrate with the females, but
females are in the majority.
The size composition of the migrating crabs was
surprising, in that overall males were smaller than females.
This is in contrast to size distributions determined both in
the population studies, and from the market sampling
surveys (Hartnoll et al., 2006b), where males were larger in
each case. From the sex composition of migrating crabs it is
clear that only a small proportion of males migrate close to
the sea, and it may be that these are ones which have had
less success in mating during earlier stages of the migration.
Since larger males in a variety of crabs have been shown to
be competitively superior, it could be expected that the
residual unmated migrant males will be generally smaller.
The females crossing the coast roads comprised both
some without eggs, and also a proportion bearing eggs. The
latter were almost entirely composed of females with very
ripe eggs, and it is postulated that they were proceeding to
the sea for imminent larval release. Females with early stage
eggs were very rare, and this concurs with the general
pattern in gecarcinids—see Epigrapsus notatus (Liu and
Jeng, 2005), Gecarcinus lateralis (Bliss et al., 1978),
Gecarcoidea natalis (Hicks, 1985), and Johngarthia
lagostoma (Hartnoll et al., 2006a). In gecarcinids generally
females lay near the end of the migration, and incubate the
eggs within burrows or other refuges, presumably to protect
them from desiccation (Klaassen, 1975; Bliss et al., 1978),
and emerge only to progress to the sea for hatching.
Klaassen (1975) suggests that Gecarcinus lateralis must
release its larvae within 10 hours of emerging from its
burrow. Exceptionally, in the cavernicolous Discoplax
longipes eggs are laid and incubated in the caves where
they live, and the females with ripe eggs migrate directly to
the sea (Ng and Guinot, 2001). In Gecarcinus ruricola, the
proportion of ovigerous females crossing the coast road was
higher on SA than on OP. This could be because the coast
road is generally further from the sea on OP, providing more
suitable areas for shelter, laying and incubation on the
seaward side.
Fecundity and Reproductive Investment
Fecundity and reproductive investment could only be
determined from ripe egg masses, since early eggs were
rarely encountered. Thus since there must be some egg loss
during incubation, values will be lower that those determined for early eggs, as is the standard protocol (see
Hines, 1982). However, the difference is unlikely to exceed
10% (Oh & Hartnoll, 1999). Fecundity was determined as
between 18,000 and 213,000, with a calculated 85,000 eggs
at 70 mm CW. In Gecarcinus lateralis, egg number ranged
from 20,000 to 110,000, but relation with CW was not
clarified (Klaasen, 1975). In Epigrapsus notatus, egg
435
HARTNOLL ET AL.: REPRODUCTION OF GECARCINUS RURICOLA
number ranged from 12,000 to 58,000 eggs, with ;45,000
at 30 mm CW. In Cardisoma guanhumi, numbers ranged
from 20,000 to .600,000 (Henning, 1975), but again
without relation to body size being defined. These data are
hard to compare; nevertheless, the egg number for
G. ruricola at 70 mm CW (;70 g DW) is well below the
global estimate of 250,000 for crabs of that weight (Hines,
1982).
Reproductive investment averaged ;5% per brood. Since
only a single brood is postulated each year, annual RI is also
5%. The reproductive period probably extends over 10 years
or more, giving a lifetime RI of .50%. The RI is a better
basis than fecundity for comparing reproductive output
between species, since it is not confounded by variation in
egg size. Values for other land crabs are not available, but
for a wide range of marine crabs the RI per brood averages
10%, though a number of marine species have values of 5%
or less (Hines, 1982; Hartnoll, 2006). However, if the value
for G. ruricola is typical of gecarcinids, then it is relatively
low. There are two potential explanations for this low value.
One is the problem of accumulating sufficient resources for
ovarian maturation on a low-energy and low-nitrogen diet of
predominantly plant material (see discussion and references
in Nordhaus et al., 2006). An alternative suggestion is that
the size of the egg mass is constrained by the need to
provide an adequate oxygen supply to the developing
embryos in the interior of the egg mass. In marine crabs,
there can be reduction of oxygen levels within the egg mass,
and the females employ special behaviour patterns to detect
and remedy such a problem (see discussion and references
in Baeza and Fernandez, 2002). No studies have been made
on terrestrial crabs, such as G. ruricola, which do not access
free water during incubation. For them the problems of
oxygenation could be greater, limiting viable egg mass size.
The lifetime RI of .50% for G. ruricola is hard to
compare with other species, since the life span of most crabs
is poorly documented. However, it is lower than the annual
RI for the small number of free-living tropical marine
species which have been studied (Hartnoll, 2006). So
despite its longevity, G. ruricola nevertheless has a relatively
low lifetime fecundity. This will increase the problems of
population maintenance.
Recruitment
Only a single recruitment event was observed, on OP in
June 2004. This is fully described in Hartnoll and Clark
(2006), and little can be added to the discussion in that
paper. The only other record of mass recruitment in
G. ruricola was in Jamaica in 2006, where again there are
no other recent records (Karl Aiken, personal communication). A common feature of the two events above is that they
both occurred close to full moon: further records are needed
to see if this is a consistent aspect. Recruitment is spasmodic
and unpredictable, seemingly a general feature of gecarcinids. Consequently the long duration of reproductive life,
exceeding 10 years or so, must be an important factor in
sustaining populations in the face of uncertain recruitment.
Populations can be heavily biased to larger sizes, notably as
in Johngarthia lagostoma on Ascension Island (Hartnoll
et al., 2006a), suggesting recruitment bottlenecks. However,
it may be that sampling bias plays a substantial role in
generating such distributions.
ACKNOWLEDGEMENTS
This investigation was supported by the UK Darwin Initiative for the
Survival of Species, project 162/11/015, ‘Sustainable management of the
black land crab, Gecarcinus ruricola, Colombia’. Many thanks to the nonauthor staff of the Columbian Government Agency CORALINA in Old
Providence and San Andres for help with the collection and analysis of
material, and for logistic support in the Archipelago. Thanks also to those
island crab catchers who assisted in the fieldwork—without their expertise
this study would not have been possible. We also thank the Natural History
Museum, London, for the loan of material of Cardisoma and Gecarcoidea.
Dr Karl Aiken of the University of West Indies, Jamaica, generously
provided unpublished details of the mass recruitment event in Jamaica.
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RECEIVED: 6 June 2006.
ACCEPTED: 4 December 2006.