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1 Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan
2 Morlab, School of Biological Sciences, Woodland Road, University of Bristol, Bristol BS8 1UG, UK
* To whom correspondence should be addressed. E-mail:
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Abstract |
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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The arrival of the monsoonal rains allows increased activity of red crabs and stimulates the annual migration (Hicks, 1985; Green, 1993). During this breeding migration red crabs, like other terrestrial gecarcinids, must abandon their home ranges and travel down to the coast to mate and spawn (Garth, 1948; Gifford, 1962; Bliss et al., 1978; Lake and O’Dowd, 1991; Pinder and Smits, 1993; Green, 1997). The downward migration normally requires at least a week, and the crabs migrate mainly during the first few hours of the morning and in the late afternoon (Hicks, 1985; Green, 1993). The males excavate burrows, which they must defend from other males, on the lowest shore terraces; mating occurs in or near the burrows. Soon after mating the males start the journey back inland to the forest, while the females lay their eggs and remain in the burrows for 2 weeks (Hicks, 1985; Hicks et al., 1990). At the end of the incubation period the females vacate their burrows and make their way to the coastal cliffs, which almost completely surround the island, to cast their eggs into the ocean. The females then return to the forest while the crab larvae spend 3-4 weeks at sea before returning to land as juvenile crabs (Gibson-Hill, 1947; Hicks, 1985; Hicks et al., 1990).
Since gecarcinid crabs must migrate to the shore to spawn, they must have well-developed navigational mechanisms. The means of navigation during the migrations are unknown, but visual cues, polarized light, magneto-reception, and learning are thought to be involved (Daumer et al., 1963; Herrnkind, 1968; DeWilde, 1973; Bliss et al., 1978; Lohmann et al., 1995; Vannini and Cannicci, 1995; Deutschlander et al., 1999).
Some data are available on the activity levels of terrestrial crustaceans in the natural environment (e.g., Wolcott and Wolcott, 1985; Gherardi et al., 1988; Gherardi and Vannini, 1989; Micheli et al., 1990; Weinstein, 1995), but data comparing the activity patterns of gecarcinid crabs during normal foraging activities and during the migration are sparse (see DeWilde, 1973). The ecology of red crabs is characterized by a period of very low activity during the dry season, followed immediately by a breeding migration (Hicks, 1985; Green, 1997) that may require crabs to travel more than 4 km in less than a week. Such abrupt changes in activity levels impose specific demands on the physiology and metabolism patterns of red crabs.
The availability of food and water changes on a seasonal basis. Particularly during the migration, this could be a major determinant of the strategy, performance, and diel capacity for exercise. Limitations in food have implications for the importance and use of stored fuel reserves, both during the dry season and during the migratory activities. Thus, determining the distances traveled and the duration of the migration as well as the routes and destinations of the crabs was crucial in appreciating the physiological demands.
The aim of this study was to examine activity levels of red crabs in the field during the migration compared to the non-migratory season. The emphasis was to characterize the migration of G. natalis in detail, by determining the direction, speed, and distance traveled during the migration, as well the relationship between the point of origin of crabs in the forest and their shore destinations, thus providing a context for the physiological demands during their annual migration.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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Non-migratory season
Population density. To obtain an index of density for red crabs, twelve stations (A to L) were selected; these included sites on the central plateau and on the upper terraces in both study areas (Fig. 2). All stations were located in primary or mature regrowth forest, but some were very close to cleared areas.
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2 test and were then analyzed by analysis of variance (ANOVA: Systat 5.03). Post hoc testing was by Tukey’s HSD, and P 
0.05 was taken as significant in all cases. Activity patterns. Two separate experiments were conducted to determine the activity patterns of red crabs during the non-migratory season (March 1993; wet season) at station B within Study Area 1 (for location, see Fig. 2). Firstly, crabs were selected at random and observed for a period of 2 min during their normal foraging activities. The distance that each crab walked during the 2 min was recorded (n = 15). During the second experiment, the actual walking speed of foraging crabs was recorded. A crab was chosen at random and observed until it started walking; the crab was then timed for as long as it continued to walk, and the distance it traveled was recorded (n = 14). All crabs used in these two experiments were subsequently captured, sexed, and measured (carapace width). These observations were made when the red crabs are most active, i.e., when the humidity was over 85% (Green, 1993).
Migratory activities
Three methods were used to obtain information about the migration of red crabs: radio tracking to obtain precise speeds, routes, and direction of travel; spray-painting large numbers of crabs to gain information on en masse direction of travel; and counting of crabs at designated stations to provide quantitative snapshots of the numbers of crabs present in various parts of the island.
In Study Area 1, crabs were studied during the migratory season (November/December) of 1993 and 1995, but in Study Area 2 crabs were studied during the 1995 migration season only. The behavior of migrating red crabs in a relatively undisturbed area (Study Area 1) was compared to that of crabs in the inhabited part of the island (Study Area 2). Since red crabs have rather small home ranges during most of the year (Lake and O’Dowd, 1991; Green, 1993; pers obs.), the areas within the rainforest selected for color coding of the red crabs prior to the start of the migration were assumed to be the sites of origin for those crabs.
Radio-tracking of crabs. At the commencement of the migration in 1993, four large male red crabs (mass 400-503 g) were captured at each of two chosen study sites (Blue and Silver sites; for locations see Fig. 3) and fitted with radio transmitters (see below). During the 1995 migration this radio-tracking experiment was repeated by fitting male crabs (mass 415-480 g) originating at those same sites with radio transmitters on 8 and 9 November. Additionally, in 1995, radio transmitters were attached to three large male crabs (mass 460-570 g) at each of two more sites of origin (Yellow and Orange sites; Fig. 4) within Study Area 2, on 9 and 10 November respectively.
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The crabs were tracked daily with a collapsible, directional antenna (A. H. Systems, Chatsworth, CA) connected to a Regal 2000 telemetry receiver (Titley Electronics). Crabs were firstly located by triangulation and, where possible, the location of each crab was confirmed visually. The triangulation technique proved quite reliable, pinpointing the location to within 30 m. The position and time of location for each crab fitted with a radio transmitter was recorded on a topographical map every day.
Color-coding of crabs. The posteriodorsal part of the carapace of crabs was spray-painted with nontoxic acrylic spray-paint, avoiding the eyes and mouthparts. In Study Area 1, at the commencement of the migration in 1993 (on the 17 Nov.), 530 crabs (male and female) were spray-painted yellow and 285 crabs were spray-painted blue (for location of sites, see Fig. 3). During the 1995 migration, 684 crabs were spray-painted blue and 750 were spray-painted silver at their respective sites of origin within Study Area 1 (Fig. 3).
In Study Area 2 (1995), 5622 red crabs were spray-painted different colors at eight locations within primary and mature regrowth forest in the plateau area (see Figs. 4 and Table 1 for location and the number of crabs painted at each site of origin). In Study Area 2, volunteers searched for painted crabs from 0630 to 1100 hours and from 1500 to 1730 between 8 November and 18 December 1995. To maximize sightings, the surveying took place mainly on and alongside roads and tracks, where color-coded crabs could be easily spotted as they crossed. All sightings reported by ANCA (Parks Australia) staff and local residents were also recorded.
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During the 1995 migration season, counting stations were set up on roads in Study Area 1 (2 stations; Fig. 3) and in Study Area 2 (9 stations; Fig. 4). At each counting station three counting grids (each 5 x 5 m) were spray-painted on the road. Counts were carried out at each station at 0800 and 1700 hours every day between 5 November and 18 December (a total of 87 counts at each station). The density of red crabs per square meter ± SEM was calculated from the mean of the three grids at each site. The data were analyzed by analysis of variance (ANOVA), using Systat for Windows version 5.03.
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Results |
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Migratory activities
The monsoonal rains arrived at different times in the two study seasons, resulting in very different migratory behavior of red crabs. In 1993, the rains were late, migration on the plateau was initiated by heavy local rainfall at noon on 17 November. Within an hour, large numbers of red crabs began accumulating on vehicle tracks and open areas within Study Area 1 and commenced their annual migration. The migration started 1 week after the optimal date predicted on the basis of the lunar cycle, and it lasted only about 6 days (Fig. 6).
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Migration activity occurred almost exclusively during daylight. On rainy, overcast days the crabs were seen crossing roads throughout the day, although the numbers decreased during the middle of the day. However, on sunny days there was a distinct period of low activity during the middle of the day (1130–1500). During this time large numbers of red crabs accumulated in the bushes by the sides of the roads and resumed their migration later in the afternoon. A few individuals persisted in migrating for several hours after sunset on some days, but there was no migratory activity at night.
Migratory routes (Study Area 1)
Radio-tracking data showed that red crabs do not necessarily migrate to the nearest coast (Fig. 7a, b; Fig. 8a, b). All crabs with radio transmitters released in the Blue site in 1993 covered about 4.13 km to the northwestern shoreline within 6 days (Fig. 7), rather than walking only 1.8 km to the southeastern shore. Furthermore, the crabs did not need to follow contour lines to direct themselves towards the shoreline. Importantly, crabs radio-tracked from the same point of origin followed remarkably similar routes in both study seasons, and they traveled in surprisingly straight lines (Fig. 7a, b; Fig. 8a, b). The silver-coded crabs from the center of the Island also headed northwest, traveling approximately 2.4 km in as little as 3–4 days (Fig. 8a, b). The Jedda Cave road, where 500 crabs were painted yellow in 1993 (Fig. 3), was used as a travel route by some individuals. Yellow-colored crabs were noted on the road up to 3 days after being painted (Fig. 9a). Other crabs simply crossed the road without taking advantage of easier routes along cleared areas. Sightings of color-coded red crabs (Figs. 9a–c) provided a larger data set confirming that crabs originating from a particular area on the island tend to migrate to similar areas on the shore to carry out their breeding activities.
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During the 1993 migration season, the crabs made progress towards their shore destinations each day (Fig. 7a, b). In contrast, during the 1995 season, 5 of the 7 radio-tracked crabs in Study Area 1 paused in their downward migration to the ocean and remained in one place (within 
20 m diameter) for 2 to 5 days before they resumed their journey to the coast (Fig. 8a, b).
Using the 1993 data and assuming that red crabs walk continuously for 12 h per day (i.e., during the daylight hours), the calculated average walking speed during the migration of the crabs with radio transmitters was 1.1 m · min-1. This was considerably slower than the speed of 4.7 ± 0.4 m · min-1 (n = 17) recorded for red crabs crossing Murray Road (10 m wide) during both of the study seasons. During the return migration, walking speeds for returning males (5.1 ± 0.3 m · min-1; n = 13) and returning females (6.2 ± 0.5 m · min-1; n = 7) crossing Murray Road were significantly faster than those of crabs on their downward migration (P = 0.016).
Migratory routes (Study Area 2)
In Study Area 2 the crabs also traveled predominantly northwest (Fig. 10a, b). Radio-tracking showed that crabs traveled along the sides of a road (thus becoming temporarily diverted from their course towards the shore) before eventually crossing the road to reach the terraces (Fig. 10a, b).
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Of the 5622 red crabs color-coded in eight sites within Study Area 2, 1338 sightings of color-coded crabs, on their downward or return migrations, were recorded. For every 100 color-coded crabs released, the subsequent sightings ranged from 38% for the white-coded crabs to only 6% for the gold-coded crabs (Table 1). The sightings indicated that painted crabs traveled predominantly towards the northwestern coast regardless of their site of origin (Fig. 11). In 4 of the 8 color-coded groups the greatest number of sightings were on Murray Road between grid 1 and grid 8 (for location, see Fig. 4). Crabs originating from the Brown site were an exception as the majority of crabs from this site headed due north.
Terrace activities
At least half of the crabs fitted with radio transmitters descended to the lowest shore terrace, immediately above the ocean. Males on the shore terraces were engaged in digging burrows; in places, burrow density was 3/m2.
In the 1993 season, the first matings were sighted on 25 November, and the return migration of the males began on 28 November and lasted 3 days (Fig. 6). The female red crabs spawned pre-dawn (0300–0400 hours) on 12 and 13 December, and their return migration lasted only 2 days. During the return migration very small individuals (2 cm carapace width) that had not been observed on the downward migration were seen traveling inland with the returning females.
In 1995, the first matings were sighted on 29 November, and the return migration of the males began in earnest on 3 December (Fig. 6). The main return migration of male crabs lasted 5 days, with a few late crabs still walking for 2 more days. The female red crabs spawned pre-dawn on 17 December, with two small-scale spawnings occurring in a few places on the Island on 16 and 18 December. The returning females reached Murray Road on 19 and 20 December in very large numbers.
Density of crabs during the migration
The downward migration (in 1995) lasted from 5 to 26 of November. Prior to 9 November, only a few crabs were seen crossing through the counting grids (see Fig. 4 for locations) and only in certain areas (Fig. 12). The main downward migration showed a wavelike increase and decrease in the number of crabs moving across roads on different days—for example, grid 1b (Fig. 12a), grid 6 (Fig. 12e), and grid 8 (Fig. 12d).
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The lowest densities of crabs, <0.2/m2, were recorded on Phosphate Hill (grids 5, 6, and 7; Fig. 12e, f) and on the Base Line Road (grids 9 and 10; Fig. 12g, h respectively). No crabs were ever recorded in grid 5 (Fig. 4). The number of days during which at least one crab was present in the counting grids ranged from 2 at grid 7 to 11 at grid 6. In contrast, in the grids located on Murray Road, the crab migration lasted from 26 to 34 days.
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Discussion |
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The red crab population
The population of red crabs on Christmas Island was estimated by subdividing the area of the entire Island into three sections: (i) the terraces, with an area of 57.7 km2 and an average density of 0.6 crabs per square meter; (ii) the plateau, with an area of 59.6 km2 and a crab density of 0.15/m2; and (iii) mined or cleared areas, with an area of 16.7 km2 and a density of 0.01/m2 (Lake and O’Dowd, 1991). The estimated population of adult red crabs on Christmas Island was 43.7 million, substantially less than the 120–157 million crabs suggested previously (Hicks, 1985; Hicks et al., 1990). Importantly, the density of red crabs was similar in the mature regrowth forest within Study Area 2 and the relatively undisturbed forest of the terraces in Study Area 1.
The densities of red crabs recorded in this study were very similar to the values of 0.04 to 0.4/m2 obtained by Lake and O’Dowd (1991) in transects. The population density of red crabs is very high; although several studies report the densities of other terrestrial gecarcinids in the range of 0.4 to 6/m2 (Green, 1993, and references therein), these are generally the maximum densities recorded. The densities of red crabs can reach up to 40/m2 on the ocean cliffs and beaches during spawning (Hicks, 1985; pers. obs.). As a consequence of the high biomass, these crabs have a very large impact on forest dynamics (Lake and O’Dowd, 1991; Green, 1993).
The density of red crabs on Christmas Island was related to population structure and altitude. The top plateau is populated predominantly by large males and, progressing towards the shore, the coastal terraces are populated by smaller individuals of both sexes (Fig. 5; Green, 1993, 1997). Crab densities decrease sharply in just 8–10 m when moving from the forest into cleared areas (Lake and O’Dowd, 1991). Walking speeds are slow, and the crabs seem quite sedentary during the non-migratory season; one marked crab was sighted within 15 m of where it was released 8 months earlier. Red crabs appear to be unaffected in their distribution and activities by conditions or events only a few meters removed (Lake and O’Dowd, 1991; pers. obs.), and they tend to have small foraging ranges during the non-migratory phase of the year.
Routes and destinations of migrating crabs
A combination of radio-tracking, color-coding, and counting stations located in various places around the island has revealed valuable information about the migratory patterns of red crabs. Three points have became apparent: firstly, crabs traveled predominantly towards the northwestern shore, which for some of the crabs was twice as far away as the southeastern shore; secondly, the crabs have specific shore destinations to which they apparently return each year; and thirdly, crabs originating from any one area on the plateau tend to travel in a similar direction and thereby reach the shore terraces in proximity to one another. The northwestern shore is much calmer, so the larvae probably have a better chance of landing ashore there after 3 weeks in the ocean. If the chances of recruitment on the northwestern shore are indeed substantially higher then elsewhere, then selective pressure would act in favor of the crabs that return to breed to the same shore where they emerged as larvae, as proposed by Gibson-Hill (1947) and DeWilde (1973).
The mode of navigation used by the red crabs during their migration remains speculative, but this study clearly shows that the crabs do not simply walk "down" toward the ocean as was suggested by Gibson-Hill (1947). Magnetic orientation could certainly account for straight paths taken by the red crabs (Vannini and Chelazzi, 1981; Lohmann et al., 1995). Some gecarcinid crabs are thought to orient themselves towards the bright horizon (Klaassen, 1975; Bliss et al., 1978; Wolcott and Wolcott, 1982); however, although red crabs in the jungle are unable to see the horizon, they do nonetheless avoid entering darkened areas.
If the young crabs can benefit from, or even need to, follow the older crabs to find their way to the shore to breed, then the idea of the "inexperienced" crabs following the "older, more experienced" crabs, proposed by DeWilde (1973), would certainly increase the breeding success of the young individuals. Additionally, traveling in groups would be advantageous in synchronizing the breeding activities. Crabs originating from the Green site and from the Gold site had very similar degrees of dispersal at the coast despite having walked different distances (1.4 km and nearly 3 km respectively); such similarity could only be expected if they traveled as cohorts. Experiments to relocate crabs before and during the migration would provide useful information about the navigation mechanisms used by the red crabs.
A comparison of the two study seasons of 1993 and 1995 in Study Area 1 reveals a 3-week difference in the timing of the start of the downward migration in relation to the lunar phase. In contrast, the spawning date appeared to be very consistent and most predictable from the lunar phase (Fig. 6). The synchronization of the spawning activities of red crabs may be important in maximizing the chances of survival for the newly hatched larvae (Morgan and Christy, 1995). In 1995, the wavelike patterns in densities of crabs crossing through the density estimation grids may be partially attributed to the different distances that crabs may have to travel to reach any given point, but they were at least partially the result of different timing of the initial rainfall in the different parts of the Island (pers. obs.). The counting grids provide snapshot images of the numbers of crabs moving through various parts of the island and further support the conclusion, which was based on sightings of color-coded crabs, that red crabs preferentially migrate towards the northwestern shore.
The radio-tracking data revealed an important difference in the behavior of migrating crabs between the two study seasons. In 1993, the red crabs walked towards their shore destinations every day and walked relatively longer daily distances. In 1995, however, 10 out of 13 radio-tracked crabs made stops of 1 to 7 days duration at various locations before eventually arriving at the shore terraces. A consequence of this behavior is to minimize the duration of time that the entire island’s red crab population is crowded on the shore terraces and the subsequent depletion of local food resources. Since the red crabs embark on their annual breeding migration immediately after the end of the dry season during which their feeding opportunities were greatly reduced (Green, 1993), early arrival of the monsoonal rains provides an opportunity for these animals to stop and feed during their downward migration. Furthermore, if the red crabs were "avoiding" reaching the terraces too early, this implies they "know" how long it will take to reach the shore and do not need to actually come in contact with the seawater to know when they have reached the coast (Hicks, 1985; Hicks et al., 1990; Greenaway, 1994).
The red crabs quite clearly avoid open areas: most crabs would travel for some distance along the side of the road under the cover of vegetation before eventually crossing the road. This observation could explain the more erratic migratory routes of red crabs in the more disturbed part of the island (Fig. 10a, b). Although the red crabs do not have any predators that might take advantage of their exposure in the open, desiccation and elevation in body temperature can reduce endurance and maximum speed of travel (Weinstein and Full, 1994; Weinstein et al., 1994); this behavior minimizes exposure to lower humidity and higher temperatures in the clearings. The walking speed of red crabs crossing the road in this study was very similar to the 5.4 m · min-1 reported previously (Hicks, 1985), but was about 4 times faster than the overall migration speed estimated from the radio-tracking data.
After G. natalis completes its annual breeding activities, most crabs leave the lowest shore terraces and return to the upper terraces and the plateau. At least some crabs appear to follow a route similar to the one they took during their downward migration and to move farther inland than their place of origin (e.g., Fig. 10b).
The environmental conditions restricting activity, coupled to the breeding biology of G. natalis, require the crabs to undertake a long migration after an extended period of relative inactivity. The breeding season, which can last from 3 to 6 weeks, represents the most active period of the year for the red crabs. Such varied activity levels impose quite different physiological demands on the animals. To assess the demands of the migration, we have also examined metabolic fuel stores, metabolic status, and capacity to maintain locomotion in red crabs during their migratory activities (Adamczewska and Morris, 2001).
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Acknowledgments |
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Footnotes |
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Literature Cited |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
) used for density counts during the migration and sites (•) of color coding crabs (where Y = yellow) and of radio-tracking "sites of origin" at Silver and Blue.
, •); sites from Study Area 2 are shown as squares (
, 
symbol shows site of origin. The location of the enlarged section is indicated by the black rectangle.
