Download LARVAL GROWTH OF THE COCONUT CRAB BIRGUS LATRO

JOURNAL OF CRUSTACEAN BIOLOGY, 27(4): 616–625, 2007
LARVAL GROWTH OF THE COCONUT CRAB BIRGUS LATRO WITH A DISCUSSION
ON THE DEVELOPMENT MODE OF TERRESTRIAL HERMIT CRABS
Fang-Lin Wang, Hwey-Lian Hsieh, and Chang-Po Chen
(FLW, HLH, and CPC) Research Center for Biodiversity, Academia Sinica, Taipei 115, Republic of China
(FLW, correspondence: [email protected]; HLH: [email protected]; CPC: [email protected])
ABSTRACT
With intensified harvesting and environment deterioration during the past two decades, a rapid decline in the number of coconut crabs,
Birgus latro, which is a protected species listed in the IUCN Invertebrate Red Data Book, has occurred on many islands. Thus, it is
important to protect this species by establishing conservation areas and/or replenish natural population by larval cultivation. In this study,
the development modes were analyzed and the effect of enriched diet on larval growth and survival were examined. Two types of zoeal
development patterns were found. In general, zoeae took 29-33 days to complete five zoeal stages and metamorphose to glaucothoes.
However, some zoeae directly metamorphosed from the 3rd zoeal to glaucothoe stage in 25;28 days. Morphologically, these zoeae with
accelerated development had thoracic appendages that appeared like the fifth stage zoeae, but with the telson, antennule, and antenna
similar to those of the third stage zoeae. When fed Artemia nauplii enriched with nutritious substances, the zoeae had significantly greater
survivorship and sizes, particularly at the fourth and fifth zoeal stages. Accelerated development may suggest early adaptation to
a terrestrial lifestyle. The adaptation of larval development related to glaucothoe size and zoeal life span is also compared and discussed for
eight terrestrial hermit crab species of Coenobitidae. The comparison suggests four adaptive modes of larval development and these are
described as mangrove adaptation, larger glaucothoe adaptation, smaller glaucothoe adaptation, and hypersaline adaptation. The selective
advantage of each mode may reflect a response to the uniqueness of each specific habitat.
MATERIALS AND METHODS
INTRODUCTION
Larval Sampling
The coconut crab Birgus latro Linnaeus, 1767, is the largest
terrestrial arthropod and inhabits many coral reef lifted
islands throughout Indo-Pacific region, including the Green
Island in Taiwan. It is a terrestrial hermit crab, belonging to
the monospecific genus Birgus in Coenobitidae (Helfman,
1979). Females release their larvae into the sea in the new
moon phase and the larvae remain in the planktonic
community for about a month. After the planktonic stage,
the glaucothoes settle to the bottom, find and carry a small
gastropod shell, and emerge onto the shoreline as a part of
terrestrial hermit crab communities (Reese and Kinzie,
1968). When they reach a size of roughly 1 cm across the
carapace, coconut crabs give up the shell-carrying habit of
their hermit crab ancestors.
With intensified harvesting and adverse environment impacts, the number of coconut crabs declined rapidly during
the past two decades on many islands. The coconut crab is
a world-wide protected species listed in the IUCN Invertebrate Red Data Book since 1983 (Wells, 1983; Bruggren
and McMahon, 1988). However, there is not enough data to
decide if the coconut crab is an endangered species or not,
and therefore it is currently classified as the criteria of ‘data
deficient’ in the 2006 IUCN Red List Threatened species.
Since the habitat of coconut crabs requires the coastal zones,
seashore waters, and land areas, it serves as the flagship
species of islands and is a good indicator for monitoring the
quality of island ecosystems.
The purpose of this study was to establish the methods of
larval cultivation and examine the effect of enriched diet on
larval growth and survival. In addition, the differences in the
adaptation modes of larval development among eight
described coenobitid species was compared and analyzed.
Two ovigerous coconut crabs carrying dark brown, eyed eggs were
captured at the dusk high tide on 30 August 2003 and 4 August 2004. This
coincided with the dark phase of the moon as they walked down to seashore
to wash their eggs on the south rim of Green Island (228409N; 1218309E),
Taiwan. The females were submerged in a vessel containing filtered
seawater (45 lm), and their mature eggs immediately hatched to the first
stage zoeae when the eggs contacted seawater. The crabs were then
released. The next morning these first stages zoeae were brought to the
laboratory.
Cultivation of Larvae Under Laboratory Condition
In 2003, a total of 300 zoeae were reared in 6 aquariums, each contained 50
zoeae with 5 liters of filtered sea water (45 lm). The larvae were fed live
freshly hatched Artemia nauplii three times per day from a strain obtained
from Great Salt Lake (GSL), Utah, U.S.A. (Parker International, Utah,
U.S.A.). Aquarium conditions included gentle bottom aeration, temperature
of 25.4 6 0.98C, salinity of 34.6 6 0.4&, and constant 12L:12D light
cycle. Half of the volume of sea water was withdrawn from each aquarium
just before feeding in order to increase the zoeal opportunity to successfully
capture the live diet. After an hour of feeding, the zoeae were transferred
into a clean aquarium using a large bore pipette with a 5 mm diameter
opening. The aquarium water was half used and half fresh sea water to
allow the zoeae to adapt easily to the new environment. Larval developing
stages were determined according to the larval morphology described by
Reese and Kinzie (1968). Survival rates of zoeae were calculated. The size
of individual was measured as total length (TL) and cephalothoracic length
(CL; Fig. 1). Total length was measured from the tip of the rostrum to the
posterior border of the telson, exclusive of the telson processes. The
cephalothoracic length was from rostral tip to posteromedial end of
carapace.
Effects of Diet Enrichment on Zoeal Development
Freshly hatched Artemia nauplii meet the two general criteria for suitable
prey items for larval decapods in laboratory studies, they: 1) are of an
appropriate size for easy capture and consumption, and 2) contain essential
dietary nutrients. However, some studies on larval culture of decapods
suggested that Artemia nauplii from GSL, Utah, U.S.A. were deficient in
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Table 1. Nutrient components of the enrichment diet (Chuan Kuan
Enterprise Co., Ltd., R.O.C.).
Components
Percentage %
Moisture
Poly-unsaturated fatty acids (PUFA)
(n-3) highly-unsaturated fatty acids
((n-3) HUFA)
Docosahexaenoic acid (DHA)
Eicosapentaenoic acid (EPA)
Phospholipids
Vitamins
Proteolytic enzymes
Carotenoids
1
34
27
11
8
3
+
+
+
Fig. 1. The measurement of the larval size of Birgus latro (modified from
Reese and Kinzie’s study in 1968). A, zoeal stage; B, glaucothoeal stage.
CL: the cephalothoracic length; TL: the total length for larvae.
some essential dietary components (Bookhout and Costlow, 1970). In order
to increase the larval survivorship, a diet enrichment experiment was carried
out in 2004. The enrichment substances were composed of poly-unsaturated
fatty acids (PUFA), (n-3) highly-unsaturated fatty acids ((n-3)HUFAs),
eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), phospholipids,
vitamins, carotenoids, and proteolytic enzymes (Table 1; Chuan Kuan
Enterprise Co., Ltd., R.O.C.). Freshly hatched Artemia nauplii were enriched with these substances in a concentration of 500 ppm for 12 h under
the condition of constant aeration, at a temperature of 24.5 6 0.58C, and
a salinity of 34.4 6 0.6&.
In 2004, a total of 300 zoeae were reared in 6 aquariums, each contained
50 zoeae with 5 liters of filtered sea water (45 lm). Three aquariums were
set as the treatment group and fed on enriched Artemia nauplii, called
EA hereafter. The other three aquariums served as the control group and
were fed nornal Artemia nauplii diet, called NA hereafter. Zoeae were
fed and reared the same procedures followed in 2003 with the temperature
and salinity kept at 23.4 6 0.68C and 34.8 6 0.1& respectively. In
addition to the survival rates, the larval size increment between two
consecutively developing stages was calculated as total length at ‘n þ 1’
stage divided by total length at ‘n’ stage. An overall growth index was
computed as the total length at the last survival stage divided by the total
length at the first stage. The mean growth index was the average of all larval
growth indices.
When zoeae metamorphosed to decapodid, glaucothoes, they were
removed individually to covered plastic beakers (Fig. 2) which hold 10 ml
sea water, a layer of moist sand, and a pile of coral debris which emerged
from water surface, creating a microhabitat similar to seashore in nature and
allowing glaucothoes to move back and forth between ‘sea’ and ‘land’
environment. The beaker rearing conditions were temperature 24.8 6 0.38C
and salinity 34.6 6 0.4&. Glaucothoes were fed pieces of shrimp or clam
meat three times daily and provided small vacant gastropod shells (shell
mouth: 1.65 6 0.16 mm; shell length: 3.68 6 0.34 mm). Once they began
carrying the shell, glaucothoes were transferred into an aquarium simulating
an intertidal environment with a slope that the lower side submerged in
aerated sea water, the middle portion consisted of moist coral debris, and
Fig. 2. The devices used for culturing larvae of Birgus latro. A, a zoearearing aquarium; B, a glaucothoe-rearing glass container holds coral debris
which rises out of the water surface; C, an aquarium simulating intertidal
environments for rearing glaucothoes. Area A is filled with moderately
aerated sea water, Area B with a slope filled with moist coral debris, and
Area C is filled with cotton balls containing fresh water. Numerous vacant,
minute gastropod shells are also deployed within the aquarium.
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Table 2. Duration of the developmental zoeal stages of Birgus latro in these studies compared with Reese and Kinzie’s study. ‘‘—’’ data not available.
Duration of each developmental zoeal stage
Study periods
This study 2003
experiment
Typical development Duration (days)
Stage-skipping
development
This study 2004
experiment
Measurement
items
Type of development
II
III
IV
V
Glaucothoeal
stage after
hatching
Duration of glaucothoes
carrying shells under
laboratory conditions
4;5
6;7
5;8
4;5
4;7
29-33
—
Mean 6 SD
4.8 6 0.7 6.5 6 0.6
(days)
n
287
229
Duration (days)
Mean 6 SD
(days)
n
Typical development Duration (days)
Mean 6 SD
(days)
n
Reese and Kinzie, Stage-skipping
1968
development
I
7.1 6 2.6 4.3 6 0.5 6.1 6 0.5
121
8;16
38
—
18
25-28
12.6 6 2.7
4;5
4;5
4.5 6 0.6 4.3 6 0.4
216
118
Duration (days)
5;6
3;5
the higher side composed of cotton balls moistened by fresh water. The
intent was to create a gradient of salinity differences to induce molting.
—
7
4;8
7;9
5;7
5.4 6 1.4 8.0 6 0.9 5.9 6 0.8
40
20
18
8;9
—
—
6;12
7
27-34
—
12;35
18
21.2 6 8.3
6
—
—
size at the 2nd zoeal stage was larger in TL in 2004 than in
2003 (t-test, P , 0.05). All zoeal stages from the study of
Reese and Kinzie in 1968 were significantly smaller than
those from this study. In 2003 experiment, the greatest
growth index occurred between the second and the third
zoeal stages, being 1.18, while the total growth index was
1.54 and the mean growth index was 1.12. In the 2004
experiment, the greatest growth index occurred between the
first and the second zoeal stages, being 1.23, while the total
growth index was 1.57 and the mean growth index was 1.12.
Survival curves of larvae were shown in Figure 4. The
fifty percent survival point occurred between the second and
the third zoeal stages in both experiments but on the tenth
day in the 2003 experiment and on the ninth day in the 2004
experiment. Survival rates of zoeae at the end of each stage
in 2003 were 87%, 57.3%, 29.3%, 17.7%, 16% and were
95.3%, 69%, 38%, 10%, and 5.7% in 2004.
RESULTS
Zoeal Growth and Survival
The number of zoeal stages of B. latro was variable in the
2003 experiment but constant in the 2004 experiment. In the
2003 experiment, larvae passed through three zoeal stages in
25;28 days or passed through five zoeal stages in 29;33
days before metamorphosing into the glaucothoeal stage.
However, in the 2004 experiment all larvae developed
through five zoeal stages in 27;34 days (Table 2). The
duration of the fourth zoeal stage in 2004 was longer than
that in the 2003 experiment (t-test, P , 0.05), and the other
stages did not differ.
The external morphology of the larvae at each stage was
similar to those described by Reese and Kinzie (1968). The
size of each zoeal stage increased after each molting (Table
3; Fig. 3). The size from the 1st to the fifth zoeal stage
ranged from 3.03 mm to 4.68 mm in total length (TL) and
1.31 mm to 2.52 mm in cephalothoracic length (CL) in the
2003 experiment, and those from 3.06 mm to 4.79 mm in
TL, 1.33 mm to 2.49 mm in CL in the 2004 experiment. The
Accelerated Development of Zoeae
A total of 13 zoeae, 4.3% of the original number of larvae,
metamorphosed to megalopae, glaucothoe, in the 2003
experiment. Among them were 7 individuals (about 54% of
all glaucothoes) that metamorphosed directly from the third
Table 3. Sizes of Birgus latro larvae reared in this study and the results from Reese and Kinzie (1968) in TL = total length; CL = cephalothoracic length.
‘‘—’’ data not available.
Larval sizes (mm; Mean 6 SD)</ENTRY
Stages of Zoeae
Glaucothoes
Study periods
Measurement items
I
II
III
IV
V
G
This study in 2003 experiment
TL
CL
n
TL
CL
n
TL
n
3.03 6 0.07
1.31 6 0.16
12
3.06 6 0.09
1.33 6 0.04
10
2.8 6 0.12
15
3.54 6 0.2
1.53 6 0.13
12
3.77 6 0.14
1.63 6 0.06
10
3.4 6 0.03
15
4.19 6 0.1
2.05 6 0.12
12
4.26 6 0.16
2.07 6 0.07
10
3.9 6 0.1
11
4.44 6 0.09
2.42 6 0.13
12
4.5 6 0.17
2.43 6 0.09
10
4.3 6 0.13
15
4.68 6 0.09
2.52 6 0.1
12
4.79 6 0.18
2.49 6 0.09
10
4.6 6 0.2
11
4.06 6 0.08
1.39 6 0.08
13
4.07 6 0.16
1.96 6 0.08
10
4
—
This study in 2004 experiment
Reese and Kinzie, 1968
WANG ET AL.: BIRGUS LATRO LARVAL GROWTH
stage zoeae (Zoeae III) on the 25th-28th days and named as
Glaucothoe III herein, whereas the rearing individuals
metamorphosed from the fifth stage zoeae (Zoeae V) on
the 29th-33rd days and named as Glaucothoe V herein.
Before metamorphosis, the thoracic appendages of these
Zoeae III individuals looked similar to Zoea V individuals,
but their telson, antennule, and antenna appeared similar to
those of Zoea III individuals, which would normally molt to
the forth stage zoeae (Zoea IV) (Fig. 5). There was no
significant difference between glaucothoe III and glaucothoe
V in size of TL (4.02 6 0.05 mm and 4.08 6 0.1 mm; ttest, P . 0.05). However, zoeae exhibiting abbreviated
development had a significantly shorter zoeal duration than
those which emerged from the fifth stage zoeae (26.7 6 1.1
days and 30.5 6 0.8 days; t-test, P , 0.05).
Some glaucothoes began amphibious life on the 32nd day
in the laboratory in the 2003 experiment. By the 35th day,
surviving glaucothoes were increasingly active on coral
debris exposed to air and once tried to push a gastropod
shell, but did not carry it. All these glaucothoes died without
molting to the first juvenile crab stage.
Shell-Carrying Glaucothoe
There were twenty fifth zoeal stage, 6.7% of the original
number of larvae, metamorphosed to glaucothoes in the
2004 experiment. There was no evidence of abbreviated
zoeal development. Six glaucothoes succeeded in carrying
gastropod shell (Fig. 6) on the 36th day in their amphibious
life until dying between 68 days to 76 days from hatching.
Effects of Diet Enrichment on Zoeal Development
Zoeal size and duration.—The total length of zoeae at the
third stage that were fed with enriched Artemia nauplii as
food (EA) were significantly larger than those in the control
groups fed on normal diets (NA) (t-test, P , 0.05; Fig. 7).
The glaucothoes from the experimental group (EA) were
also larger than NA ones (t-test, P , 0.05; Fig. 7). The
duration of zoeae in EA groups did not differ statistically
from that in the control groups.
Survival rate and metamorphosis.—The survival rates of EA
groups were significantly higher than that of NA ones at the
fourth and the fifth zoeal stages (t-test, P , 0.05; Fig. 8).
Among 20 glaucothoes, 15 individuals (75% of the total)
metamorphosed from EA groups.
DISCUSSION
Heterochronal Morphology and Reduction in
the Number of Zoeal Stages
In the typical development of Birgus latro, as zoea progress
toward metamorphosis the larval characters gradually
become suppressed and then disappear, and the zoea then
displays adult-like characters. However, in this study we
found a heterochronal development in which 5% of Zoea III
individuals possessed a mixture of zoeal and glaucothoeal
characters. The morphology of their telson and segmented
antennal flagella resembled with those at the third zoeal
stage, but their thoracic appendages and setose pleopods
belong to those of the fifth stage zoeae that were ready to
metamorphose into the glaucothoeal stage. These individ-
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Fig. 3. Larval size of Birgus latro (mean 6 SD). The symbol ‘*’ means
that size differed significantly (t-test, P , 0.05). Zoeal sizes at all stages
from Reese and Kinzie’s study were significantly smaller than in this study
(t-test, P , 0.05).
uals succeeded in metamorphosing to the glaucothoeal stage
without going through the fourth zoeal stage. The
phenomenon of heterochronal development was also
reported by Reese and Kinzie (1968), but no changes in
morphological characteristics were described in their study.
This novel morphology is non-genetic in origin, since in
our study one female produced zoeae that progressed through
two different development pathways, one with only three
stages and the other with the typical five stages, while
another female produced zoeae all undergoing typical five
stage development. Moreover, in the study of Reese and
Kinzie in 1968 zoeae were reared in isolation in order to
determine from which zoeal stage the terminal molt to
glaucothoe occurred. They found that 12.5% of Zoea III went
through the terminal larval molt to the postlarval glaucothoes
on the 21st day after hatching, and 58.3% Zoea IV
metamorphosed to glaucothoe after 25-38 days of larval life,
but only 8.3% individuals molted to Zoea V, which finally
died. These results suggest that the larval development of B.
latro has no fixed mode in their evolutionary history and that
B. latro is capable of abbreviating its larval developmental
sequence from the typical five zoeal stages.
In the typical development of Birgus latro, the terminal
zoea appeared to be a little further morphologically developed than those having an abbreviated development with
three zoeal stages. The former possessed more setae and
segments in the telson, antennule, and antenna. By contrast,
this phenomenon does not occur in larvae of Coenobita
clypeatus (Herbst, 1791) which metamorphosed to glaucothoeal stage from Zoea IV, Zoea V, and Zoea VI. The zoea
of C. clypeatus at preceding stages in longer development
series may be less developed than those metamorphosed at
the same stage in shorter series. This suggests retrogressive
development and that Zoea VI from a long series (five or six
stages) were less developed than a terminal Zoea IV
(Provenzano, 1962).
Valentine (1981) stated that unusual environmental stimuli
can alter the level of hormone secretion and produce abnormalities similar to those resulting from mutations. These
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Fig. 4. Survival rates of larval Birgus latro reared in this study during 2003 (A) and 2004 (B). Glaucothoe III, V: indicating the megalopae developed from
the third stage zoeae or from the fifth stage zoeae.
‘‘abnormal’’ individuals would presumably have no special
trouble in reproducing, assuming that they are well adapted.
The morphology and lifecycle could thus be propagated. Later
genetic changes could then fix the new morphology, even
developmental types, in phylogeny. These genetic changes
may be favored by micro-evolution because they would
stabilize a phenotype with significant adaptive value.
Effect of Diet Enrichment on Zoeal Development
The results from the 2004 diet enrichment experiment in this
study showed that addition of nutritional supplements to
food can enhance larval size and survival. The development
of decapod larvae can be divided into two phases: an early
slow growth phase and a later metamorphic phase, which is
characterized by rapid growth and preparation for mor-
WANG ET AL.: BIRGUS LATRO LARVAL GROWTH
621
Fig. 5. The mixture of characters from the Zoea III individuals with skipped development in Birgus latro occurring in this study during 2003. A, lateral
view of the third stage zoea which metamorphosed to glaucothoe which exhibits thoracic appendages and setose pleopods (shown in arrows) that looked
similar to the Zoea V individuals and were clumped by a layer of membrane; B, the zoea molted to the 4th stage had no mixture characters.
phological changes associated with metamorphosis
(McConaugha, 1985). Growth during the early larval stages
consists of a gradual increase in lipid and protein content
over two or more stages. Poor nutritional status during the
zoeal stages of the mud crab, Scylla paramamosain
(Estampador, 1949) appeared to have an adverse effect on
survival of megalopa (Li et al., 1992). Brachyuran larvae
also have dietary requirements for long-chain PUFA before
completing development and metamorphosis. In a series of
studies, larvae of Rhithropanopeus harrisii (Gould, 1841)
were fed Artemia nauplii low in the poly-unsaturated fatty
acids of 20:5x3 (Bookhout and Costlow, 1970; Johns et al.,
1980). These larvae showed a dramatic drop in survival
and displayed a number of abnormalities including partial
molting, unusual carapace spination, and irregularly formed
thoracic appendages during the last zoeal stage. It is evident
that sufficient energy reserves from food for B. latro can
contribute to larval development and metamorphosis.
Some studies have suggested that it may be possible to
culture coconut crabs (Chatterjee, 1977) and experiments on
their cultivation have been carried out at the Marine Station
in Maribago, Philippines (Horstmann, 1976). However, to
date there are no reports of successful cultivation. Our
Fig. 6. A glaucothoe of Birgus latro carries a gastropod shell. This
individual metamorphosed to a glaucothoe from the fifth zoeal stage on the
27th day and began carrying the shell on the 37th day after hatching.
findings and culturing techniques may assist to promote
mass culture of the zoeae and glaucothoes so that young
crabs produced could be used to restock many islands where
stocks have seriously declined and thereby contribute to
replenishing natural population.
Developmental Categories and the Constant or Variable
Number of Larval Stages
Larval development has been described for 8 of 16 known
species of coenobitids. Detailed data are summarized in
Table 4. Based on the flexibility in the number of larval
stages, larval development in this family can be divided into
constant and variable types. The constant type is predominant and has rather fixed ontogenetic growth and
development stages. It consistently recurs in a sequence
with five zoeal stages that the majority of the decapod
species demonstrate (Broad, 1957), but a minimum of two
or a maximum of seven stages are also recorded in some
species (Table 4). The variable type deviates either in the
number or the duration of larval stages from that seen in the
preponderance of related species. This variability has often
been postulated to be a consequence of environmental and/
or genetic induction (Sandifer and Smith, 1979; Table 4).
Fig. 7. Larval sizes of Birgus latro reared under food enriched (EA) or
normal (NA) in 2004 experiment. Zoeae of the third stage in EA group were
significantly larger than control groups (NA). The glaucothoes from EA
groups were also larger than those from NA ones. *: P , 0.05.
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Fig. 8. Cumulative survival rates through the larval stages of Birgus latro
reared under food enriched (EA) or normal (NA). The survival rates of the
forth and fifth zoeal stages were significantly higher in EA groups than in
NA. *: P , 0.05.
During the process of molting, larvae become encumbered by an exuvial cast that prevents swimming and
feeding. Such a dangerous condition can lead to death either
from the mechanical problems or from pelagic predation.
Benzie (1982) suggested that a reduction in the number of
larval molts and faster development would be strongly
selected for up to a point, beyond which further changes of
the developmental plan are more fundamental and more
difficult to achieve.
Development Type and
Ecological Adaptation in Coenobitidae
The adaptive strategies for most decapod species that
progressively become more terrestrial would include a reduction in the number of larval stages and a faster growth
rate (Hartnoll, 1965). The shortened development is
adaptive because it: 1) reduces critical molt periods, 2)
minimizes exposure to suboptimal conditions for growth
and development (such as inadequate nutrition or poor
hydrographic conditions), 3) reduces exposure to predation,
4) reduces dispersal from specialized and restricted adult
habitats, and 5) reduces recruitment mechanisms (Knowlton, 1970; Robert, 1971).
On the evolutionary aspect of habitat utilization, Dobkin
(1963) conjectured that the type of development may be
related to the period of time that different species have
evolved for inhabiting land or freshwater environments.
Those having existed terrestrially or in freshwater for
a greater length of time in evolutionary history would have
an abbreviated development, while those relatively new to
this type of habitat would be expected to have shortening
planktonic stages in their life history. Limited larval
dispersal is also a consequence of shortened larval life, in
conjunction with responses of both larva and adult crab, to
overcome the evolutionary constraints from hydrographic
regimes and osmotic regulation. Within a variety of
environmental condition, such as semi-terrestrial, fresh
water, estuarine, rocky intertidal shores, marine, and
hypersaline, development of phenotypic plasticity would
itself be selected for as a singularly important feature.
The relationships among the glaucothoeal size, zoeal life
span, and given habitats for eight coenobitid species for
which larval development data were compared (Table 5).
The results suggested that there are four modes of larval
development (Table 4; Figs. 9, 10) described as follows.
Mangrove adaptation mode (M1).—The hermit crabs, which
adapt to swamp environments such as mangrove areas, have
a development mode characterized by the largest glaucothoe
size (4.38 mm), the least number of zoeal stages, and the
shortest duration of zoeal life span. This mode is called
herein ‘‘mangrove adaptation mode (M1)’’. An example
species is the Australian land hermit crab, Coenobita
variabilis (McCulloch, 1909) that undergoes abbreviated
development and reaches the glaucothoeal stage in only six
days at 308C after two non-feeding zoeal stages (Harvey,
1992). The adults are distributed intertidally and up to
100 m above tide levels. They are often found behind mangroves, sheltering from the heat of the day under rocks or
logs. These mangroves extend from Exmouth Gulf to North
Queensland in the Northern Australia, forming fringing
forested zones usually with scrub communities along
Table 4. The development modes of species of Coenobitidae reared under laboratory conditions. The symbol ‘*’ reveals the major zoeal stage that
metamorphoses into the glaucothoeal stage.
Adaptation mode
Mangrove
adaptation (M1)
Larger glaucothoe
adaptation (M2)
Smaller glaucothoe
adaptation (M3)
Hypersaline
adaptation (M4)
Development
category
Number of
zoeal stage
Terminal
zoeal stage
Coenobita variabilis
constant
2
2nd
Coenobita capives
constant
5
5th
Coenobita purpureus
constant
5
5th
Coenobita compressus
Coenobita clypeatus
Birgus latro
variable
variable
variable
Coenobita rugosus
constant
4,5
4,5,6
3,5
3,4,5
5
4th, 5th*
4th, 5th*, 6th
3rd, 5th*
3rd, 4th*
5th
Coenobita scaevola
constant
7
7th
Species
Adult habitat
Beach and vicinity, usually
near mangroves
Beach and vicinity, commonly
found on the shore to 600 m
or more inland
Beach and vicinity, commonly
found on the shore to 600 m
or more inland
Beach and vicinity
Beach and inland
Inland
Beach and vicinity, usually
inhabits the shore
Beach only
Reference
Harvey, 1992
Shokita and Yamashiro,
1986; Nakasone, 1988
Nakasone, 1988
Brodie and Harvey, 2001
Provenzano, 1962
This study;
Reese and Kinzie, 1968
Shokita and Yamashiro,
1986
Al-Aidaroos and
Williamson, 1989
623
WANG ET AL.: BIRGUS LATRO LARVAL GROWTH
Table 5. The number of zoeal stages, zoeal life span, length of glaucothoe, and growth indices of Coenobitidae recorded to date.
Species
Coenobita
C. variabilis
C. compressus
C. clypeatus
C. rugosus
C. purpureus
C. cavipes
C. scaevola
Birgus
B. latro
B. latro Zoea III!G
(this study, 2003)
B. latro Zoea V!G
(this study, 2003)
B. latro Zoea V!G
(this study, 2004)
Number of
zoeal stages
Zoeal life
span (days)
Total length of
glaucothoe (mm)
Mean growth
index
Total growth
index
2
4;5
4;6
5
5
5
5;8
19;43
16;25
20;31
24;31
22;34
4.38
4.33
4.30
4.00
4.28
4.33
1.02
1.17
1.17
1.18
1.18
1.22
1.02
1.86
1.85
1.96
1.91
2.18
7
54;80
3.94
1.14
2.16
Harvey, 1992
Brodie and Harvey, 2001
Provenzano, 1962
Shokita and Yamashiro, 1986
Nakasone, 1988
Shokita and Yamashiro, 1986;
Nakasone, 1988
Al-Aidaroos and Williamson, 1989
3;4
3
24;38
25;28
4.00
4.02
1.13
1.12
1.64
1.58
Reese and Kinzie, 1968
This study
5
25;33
4.08
1.12
1.54
This study
5
27;34
4.07
1.12
1.57
This study
landward and seaward margins and river and tidal creek
edges (Hopley et al., 1975). Such habitats are subjected to
extreme or unpredictable fluctuations in salinities and
abbreviated development would be advantageous (Lucas,
1971).
Larger glaucothoe adaptation mode (M2).—The hermit crabs
with a large glaucothoe size (4.28-4.33 mm), but smaller
than that in M1, mode exhibit 4 or 6 zoeal stages rather than
the typical five zoeal stages and have a wider variation in
zoeal life span, ranging from 16-43 days. This mode is
called ‘‘the larger glaucothoe adaptation mode (M2)’’. These
species include Coenobita purpureus (Stimpson, 1858), and
C. cavipes (Stimpson, 1858), which both have the typical
Fig. 9. Comparison of the glaucothoel size and duration of the zoeal life
stage in eight coenobitid species. Four adaptive modes are recognized as
mangrove adaptation (M1), larger glaucothoe adaptation (M2), smaller
glaucothoe adaptation (M3), and hypersaline adaptation (M4).
Reference
five zoeal stages and adults living in the region from the
shore to 600 m or more inland (Nakasone, 1988), C.
compressus (H. Milne Edwards, 1837), a beachfront species
that has inconsistent, 4-5 stages (Brodie and Harvey, 2001),
and C. clypeatus, an inland species, with 4-6 stages
(Provenzano, 1962). It is worth pointing out that C. cavipes
has the greatest growth increment (mean growth index, 1.22;
Table 5) at each intermolt and metamorphoses into a larger
glaucothoe. This feature also occurs in other M2 species in
which the intermolt increment is greater and metamorphosis
is to a larger glaucothoe (Figs. 9, 10).
Smaller glaucothoe adaptation mode (M3).—The hermit
crabs that metamorphose at smaller glaucothoe size (4.00-
Fig. 10. The relationship between mean growth index and total growth
index. The species in M2 category seem to have a faster larval growth rate
and thus become a larger glaucothoe through the four or five zoeal stages.
624
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 4, 2007
4.08 mm), possess fewer zoeal stages (3-5 stages) than
typical and have less variation in zoeal life span, ranging
from 20-38 days are placed in the ‘‘smaller glaucothoe
adaptation mode (M3)’’. These species include B. latro (in
this and Reese and Kinzie’s studies in 1968), and Coenobita
rugosus (H. Milne Edwards, 1837). Coenobita rugosus is
a beach inhabitant and that consistently has five fixed stages
(Shokita and Yamashiro, 1986). Birgus latro, which adult is
the largest terrestrial crustacean and the most inland
distributed hermit crab, has a non-fixed number of zoeal
stages with a tendency toward shorter zoeal stages and
overall zoeal life without the trade-off of a smaller
glaucothoe size (Fig. 9). Although B. latro evolves as a
terrestrial species, it still must to rely on marine environment
for planktonic larval development, dispersal and salt balance
as the hermit crab members of M2 group which predominantly live on coastal forest.
Starting from a normal five zoeal stages, heterochronal
development evolved in Coenobitidae, with both inter- and
intra-species variation in zoeal development patterns. These
patterns were either accelerated or prolonged by changing
molting times in concordance with their habitat conditions,
particularly salinities levels, in addition to factors related to
terrestrial or suboptimal conditions for growth. The
mangrove adapted species, C. variabilis, which undergoes
abbreviated development may reveal the influence of
freshwater. Birgus latro, and M2 species, and other M3
species exhibit strategies allowing them to metamorphose
into larger glaucothoe to help against harshness in intertidal
zone or to decrease molting times and planktonic duration.
The hypersaline inhabitant, C. scaevola, which produces
smallest glaucothoes, seems to accommodate well to its
more marine habitat.
Hypersaline adaptation mode (M4).—The hermit crabs
which metamorphose with the smallest glaucothoe size
(3.94 mm) have the greatest number of zoeal stages (7
stages) and the longest zoeal life span (54-80 days; Table 5)
are categorized as the hypersaline adaptation mode (M4).
This mode includes only the Red Sea species, Coenobita
scaevola (Forskål, 1775). Larval development of C.
scaevola exhibits a condition of ‘‘mark-time molting’’ that
is a kind of delayed development in which the zoeal stage
may enter a sequence of molts with very little morphological
change taking place, although each succeeding instar may
show some slight increase in size (Al-Aidaroos and
Williamson, 1989). When compared with other land hermit
crabs, C. scaevola does not follow the linear relationship in
growth indices where the larger the value of the mean
growth index, the larger the total growth index. This may be
attributed to the large number of zoeal stages for which C.
scaevola is associated with its exclusive beach habitat. C.
scaevola does not have a larger mean growth index, but, it
exhibits a relatively large total growth index after completing six molts. Although it has larger terminal zoeae than in
M2 and M3 species (Fig. 10), it metamorphoses into the
smallest glaucothoe (3.94 mm; Table 5) of all the hermit
crabs reported. Coenobita scaevola, lives close to the edge
of sea where it is exposed to high salinity. Although this
species is not always submerged in seawater, it always
keeps seawater in its shell. This species performs osmoregulation where salinities are greater than 25&, whereas only
a weak regulation is found at lower salinities (Spaargaren,
1977). With the energy intensive demand for osmoregulation in higher salinity water, C. scaevola may produce
smaller eggs and thus rely on longer pelagic zoeal life to
reach a size competent for successful glaucothoe metamorphosis. Al-Aidaroos and Williamson (1989) reported
that C. scaevola went through seven zoeal stages, but this
was based on only two observed glaucothoes. The variation
in the number of zoeal stages may not be detectable and
further detailed study is needed to confirm this observation.
These four developmental modes seem primarily related
to the salinity regimes occupied, but the difference between
M2 and M3 groups is unclear. Future thorough study is
needed to clarify this issue.
ACKNOWLEDGEMENTS
This work was partially supported by the National Science Council,
Research Center for Biodiversity, Academia Sinica and National Taiwan
University. We thank very specially Dr. Daniel Sheehy for his comments
and suggestions on the manuscript.
REFERENCES
Al-Aidaroos, A., and D. I. Williamson. 1989. Larval development of the
land hermit crab Coenobita scaevola (Forskål, 1775) (Crustacea:
Anomura: Coenobitidae) reared in the laboratory. Journal of Natural
History 23: 111-128.
Benzie, J. A. H. 1982. The complete larval development of Caridina
mccullochi, Roux, 1926 (Decapoda, Atyidae) reared in the laboratory. Journal of Crustacean Biology 2: 493-513.
Bookhout, C. G., and J. D. Costlow. 1970. Nutritional effects of Artemia
from different locations on larval development of crabs. Helolander
wiss Meeres 20: 435-442.
Broad, A. C. 1957. Larval development of Palaemonetes pugio
Holthius. Biology Bulletin 12: 144-161.
Brodie, R., and A. W. Harvey. 2001. Development of the terrestrial hermit
crab, Coenobita compressus, in the laboratory. Journal of Crustacean
Biology 21: 715-732.
Burggren, W. W., and B. R. McMahon. 1988. Biology of the land crabs.
Cambridge University Press: New York.
Chatterjee, S. K. 1977. Wildlife in the Andaman and Nicobar Islands.
Tigerpaper 4: 2-5.
Dobkin, S. 1963. The larval development of Palaemonetes paludosus
(Gibbes, 1850) (Decapoda, Palaemonidae), reared in the laboratory.
Crustaceana 6: 21-41.
Estampador, E. P. 1949. Studies on Scylla (Crustacea: Portunidae). I
Revision of the genus. Philippines Journal of Science 78: 95-108.
Forskål, P. 1775. Descriptions Animalium, Avium, Amphibiorum, Piscium,
Insectorum, Vermium. 19 þ xxxii þ 164 pp., Copenhagen.
Gould, A. 1841. Report on the Invertebrata of Massachusetts, comprising
the Mollusca, Crustacea, Annelida, and Radiata. Folsom, Wells, and
Thurston, Cambridge.
Hartnoll, R. G. 1965. Notes on the marine grapsid crabs of Jamaica. Proceedings of the Linnean Society of London 176: 113-147.
Harvey, A. W. 1992. Abbreviated larval development in the Australian
terrestrial hermit crab Coenobita variabilis McCulloch (Anomura:
Coenobitidae). Journal of Crustacean Biology 12: 196-209.
Helfman, G. S. 1979. Coconut crabs and cannibalism. Natural History 88:
77-83.
Hopley, D., S. T. Langsford, J. C. Schofield, M. A. J. Williams, R. P.
Bourman, N. K. Chick, and E. D. Gill. 1975. 1973-1974 Research on
Quaternary Shorelines in Australia and new Zealand a summary report of
the ANZAAS Quaternary Shorelines Committee. Australian Quaternary
Newsletter.
Horstmann, U. 1976. Some aspects on the culture of the coconut crab
(Birgus latro). National Research Council of the Philippines Bulletin
60: 8-13.
WANG ET AL.: BIRGUS LATRO LARVAL GROWTH
Johns, D. M., M. E. Peters, and A. D. Beck. 1980. International study on
Artemia. VI. Nutritional value of geographical and temporal strains of
Artemia: effects on survival and growth of two species of Brachyuran
larvae, pp. 291-304. In, G. Persoone, P. Sorgeloos, D. A. Roels, and E.
Jaspers (eds.), The brine shrimp, Artemia.
Knowlton, R. E. 1970. Effects of environmental factors on the larval
development of Alpheus heterochaelis Say and Palaemonetes vulgaris
Say (Crustacea: Decapoda: Caridea), with ecological notes on larval and
adult Alpheidae and Palaemonidae. Ph.D. thesis. University of North
Carolina.
Li, S., C. Zeng, H. Tanh, G. Wang, and Q. Lin. 1999. Investigations into
the reproductive and larval culture of the mud crab (Scylla paramamosain): A research overview, pp. 121-124. In, C. P. Keenan (ed.),
Mud Crab Aquaculture and Biology. Proceedings of an international
scientific forum held in Darwin, Australia, 21-22 April 1997. ACIAR
Proceedings No. 78, ACIAR, Canberra, Australia.
Linnaeus, C. 1767. Classis V Insecta. Systema Naturae per Regna tria
Naturae 1(2): 533-11327.
Lucas, J. S. 1971. The larval stages of some Australian species of
Halicarcinus (Crustacea, Brachyura, Hymenosomatidae) I. Morphology.
Bulletin of Marine Science 21: 471-490.
McConaugha, J. R. 1985. Nutrition and larval growth, pp. 127-154. In,
A. M. Wenner (ed.), Crustacean growth: Larval growth, Crustacean
Issues 2. A. A. Balkema, Rotterdam.
McCulloch, A. R. 1909. Studies in Australian Crustacea. No. 2. Records
of the Australian Museum 7: 305-314.
Milne Edwards, H. 1837. Histoire naturelle des Crustacés, comprenant
l’anatomie, la physiologie et la classification de ces animaux. Paris:
Librariare Encyclopedique de Roret. Vol. 2, pp. 532.
Nakasone, Y. 1988. Larval stages of Coenobita purpureus Stimpson and
Coenobita cavipes Stimpson reared in the laboratory and survival rates
and growth factors of three land hermit crab larvae (Crustacea:
Anomura). Zoological Science 5: 1105-1120.
625
Provenzano, A. J., Jr. 1962. The larval development of the tropical land
hermit crab Coenobita clypeatus (Herbst) in the laboratory. Crustaceana 4: 207-228.
Reese, E. S., and R. A. Kinzie. 1968. The larval development of the
coconut or robber crab Birgus latro (L.) in the laboratory (Anomura,
Paguridae). Crustaceana Supplement 2: 117-144.
Roberts, M. H., Jr. 1971. Larval development of Pagurus longicarpus Say
reared in the laboratory II. Effects of reduced salinity on larval
development. Biology Bulletin 140: 104-116.
Sandifer, P. A., and T. I. J. Smith. 1979. Possible significance of variation
in the larval development of palaemonid shrimp. Journal of Experimental Marine Biology and Ecology 39: 55-64.
Shokita, S., and A. Yamashiro. 1986. Larval development of the land
hermit crab, Coenobita rugosus H. Milne Edwards and C. cavipes
Stimpson reared in the laboratory. Galaxea 5: 267-282.
Spaargaren, D. H. 1977. On the water and salt economy of some decapod
crustaceans from the Gulf of Aqaba (Red Sea). Netherlands Journal of
Sea Research 11: 99-106.
Stimpson, W. 1858. Crustacea Anomura. Prodromus descriptionis animalium evertabratorum, quae in Expeditione ad Oceanum Pacificum
Septentrionalem a Republica Federata missa, Cadwaladaro Ringgold et
Johanne Rodgers ducibus, observavit et descripsit, Pars 7. Proceedings
of the Academy of Natural Sciences of Philadelphia 10: 225-252.
Valentine, J. W. 1981. Emergence and radiation of multicellular organisms,
pp. 229-257. In, J. Billingham (ed.), Life in the Universe Cambridge:
MIT Press.
Wells, S. M., R. M. Pyle, and N. M. Collins. 1983. Coconut or robber crab.
I.U.C.N. Invertebrate Red Data Book, I.U.C.N.; Gland, Switzerland.
632 pp.
RECEIVED: 12 October 2006.
ACCEPTED: 23 March 2007.