Moulting of the Semi-Terrestrial Crab Chiromantes Haematocheir (De Haan, 1833) (Decapoda, Sesarmidae) in Taiwan

Crustaceana 90 (14) 1731-1745

MOULTING OF THE SEMI-TERRESTRIAL CRAB CHIROMANTES HAEMATOCHEIR (DE HAAN, 1833) (DECAPODA, SESARMIDAE) IN TAIWAN

HUNG-CHANG LIU1), MING-SHIOU JENG2) and RICHARD G. HARTNOLL3,4) 1) No. 53 Chenggong 11th St., Jhubei City, Hsinchu County, Taiwan 302 2) Research Centre for Biodiversity, Academia Sinica, Nankang, Taipei 115, Taiwan 3) School of Environmental Sciences, University of Liverpool, Liverpool L69 3BX, U.K.

ABSTRACT Population structure and moulting of the semi-terrestrial crab Chiromantes haematocheir (De Haan, 1833) were studied in Taiwan. The crab moults nocturnally in small freshwater pools, and newly moulted crabs and cast integuments were used to assess moult increment. Males reached a larger size (max. CW 36 mm, n = 272) than females (max. CW 33 mm, n = 164): from 22 mm CW males increasingly dominated the population. Size at maturity was estimated at 17.5 mm CW. The percentage moult increment averaged 11.5% in males (5.5-19%, n = 153) and 13.9% in females (7-23%, n = 72). Female increment exceeded male increment for all overlapping size classes. The larger size of mature males, despite a smaller percentage increment, is explained by a higher post-puberty moult frequency. Of the moulting crabs, 25% of males and 38% of females had one or more missing or regenerating peraeopods. In both sexes this reduced the percentage increment, more so the larger number of limbs affected. The moulting conditions for C. haematocheir are not ideal, with constraints in relation to calcium supplies, and shelter. So the moult increments are unsurprisingly less than those of shallow water marine crabs moulting in an optimal environment, but larger than those of land crabs moulting without access to standing water.

RÉSUMÉ La structure de la population et la mue du crabe semi-terrestre Chiromantes haematocheir (De Haan, 1833) ont été étudiées à Taiwan. Le crabe mue la nuit dans des petites mares d’eau douce, et les crabes venant de muer et les téguments rejetés ont été utilisés pour évaluer le taux de croissance à la mue. Les mâles atteignent une taille plus grande (max. CW 36 mm, n = 272) que les femelles (max. CW 33 mm, n = 164): à partir de 22 mm de CW (largeur céphalothoracique) les mâles dominent de plus en plus dans la population. La taille à la maturité a été estimée à 17,5 mm CW. La valeur moyenne de croissance à la mue a été de 11,5% chez les mâles (5,5-19%, n = 153) et 13,9% chez les femelles (7-23%, n = 72). Le taux de croissance femelle a excédé celui des mâles pour toutes les classes de taille se chevauchant. La plus grande taille des mâles matures, en dépit de leur taux de

4) Corresponding author; e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2017Downloaded DOI 10.1163/15685403-00003711 from Brill.com10/02/2021 03:21:35AM via free access 1732 HUNG-CHANG LIU, MING-SHIOU JENG & RICHARD G. HARTNOLL croissance plus faible, est expliquée par une fréquence des mues après la puberté plus élevée. Parmi les crabes en mue, 25% des mâles et 38% des femelles avaient une ou plusieurs pattes manquantes ou en régénération. Dans les deux sexes, cela réduit d’autant plus le taux de croissance que le nombre de pattes affectées est élevé. Les conditions de la mue pour C. haematocheir ne sont pas idéales, avec des contraintes pour la fourniture du calcium, et les abris. Aussi les taux de croissance sont, sans surprise, moindres que ceux des crabes marins d’eau peu profonde muant dans un environnement optimal, mais plus élevés que ceux des crabes terrestres muant sans accès à une eau stagnante.

INTRODUCTION Two components determine the growth rate of crabs: the increase in size at moulting (the moult increment), and the interval between successive moults (the intermoult period). This study will focus on the former, though the latter will be briefly considered. The moult increment can be expressed as an absolute measure, but this renders comparison between different sized crabs difficult. It is preferable to use the “percentage moult increment”, expressed as the percentage increment on moulting of the pre-moult size. Unless otherwise stated, all references to “increment” relate to this factor. Measuring the increment is not straightforward. It can sometimes be determined from the successive peaks in size-frequency distributions, though discrimination is generally limited to the first five or six postlarval instars (Hartnoll, 1978). There may be morphological differences between instars, and on this basis plus bivariate analysis Sasaki & Kuwahara (1999) discriminated 17 instars in Erimacrus isenbeckii (Brandt, 1848): this complex process has not been repeated for other species. The observation of moults of captive specimens is the commonest method, as in Carcinus maenas (Linnaeus, 1758) (cf. Mohamedeen & Hartnoll, 1989): however, there is uncertainty as to how such data relate to performance in the wild (see discussion in Hartnoll, 1982). A marking programme using tags retained at moulting can provide comprehensive data, but is logistically complex and expensive and has been limited to larger species of commercial and/or conservation importance: e.g., Cancer pagurus Linnaeus, 1758 (cf. Edwards, 1965), Callinectes sapidus Rathbun, 1896 (cf. Fitz & Wiegert, 1991), and Birgus latro Linnaeus, 1767 (cf. Drew et al., 2012). For terrestrial crabs, there are limited data on moult increments and in most cases these have been obtained from captive specimens (Hartnoll, 1988b). Moult- ing in terrestrial crabs, such as Birgus latro (cf. Fletcher et al., 1990), Cardisoma guanhumi Latreille, 1828 (cf. Gifford, 1962), and Gecarcinus lateralis (Guérin, 1832) (cf. Wolcott, 1988) usually occurs within their burrows, hence it is difficult to observe moulting behaviour and obtain natural moult increment data. There is, however, one simple method to determine the increment under natural conditions. This is where newly moulted crabs can be collected together with their

Downloaded from Brill.com10/02/2021 03:21:35AM via free access MOULTING OF CHIROMANTES HAEMATOCHEIR 1733 cast integuments, and/or imminently moulting crabs can be collected to then moult very soon in captivity: such studies have previously been in intertidal habitats: e.g., Carcinus maenas (cf. Hogarth, 1975), Hemigrapsus sanguineus (De Haan, 1835) (cf. Kurata, 1962) and Macrophthalmus boteltobagoe Sakai, 1939 (cf. Kosuge, 1993). These cases are few and have generally involved small samples sizes. However, Chiromantes haematocheir (De Haan, 1833) is a common semi- terrestrial crab in Taiwan, and inhabits areas close to swamps and muddy banks of freshwater streams not far from the sea. For this species, individuals that are at the onset of ecdysis, together with recently moulted crabs along with their cast integuments, can all be readily found in the ﬁeld; this provides an unusual opportunity to study moulting behaviour and gather moult increment data for a terrestrial crab. In this paper, the moulting behaviour and the natural moult increment of C. haematocheir are examined on the basis of substantial samples. The effect of limb regeneration on growth increment is also investigated.

MATERIAL AND METHODS

The study area was near the mouth of the Meilun River (23°5837N 121°3618E), Hualien City, Hualien County, eastern Taiwan. In the area there are small springs which form freshwater pools throughout the year, although the amount of water in them changes seasonally. A belt transect (0.5 m × 100 m) was established close to the estuary at the foot of Meilun Hill and monitored for 11 months, from September 2000 to July 2001, so including both the wet (May to September) and dry (October to April) seasons. Chiromantes haematocheir is predominantly nocturnal, so surveys were conducted at night: crabs were hand caught using lamps. To obtain population data, every specimen found outside their burrows within the transect was sampled monthly from March to July 2001. The sex, carapace width (CW), and whether females were ovigerous, were recorded, after which the crabs were released in their original habitat. During the monitoring period, 115 ﬁeld surveys were carried out to collect data on moulting. Moulting behaviour was recorded. To investigate increment, recently moulted crabs (plus their cast shell), and also those close to moulting, were collected: crabs close to moulting were readily identiﬁed by a fragile carapace, an empty intestine and feeble chelae. Collected crabs were kept singly in plastic aquaria (0.3 m L × 0.2 m W × 0.15 m H). The aquaria contained fallen leaves, mud and water taken from the study area to simulate the natural habitat, providing both a dry and a wet area for the crabs: the deepest water allowed complete immersion. The sex and number of

Downloaded from Brill.com10/02/2021 03:21:35AM via free access 1734 HUNG-CHANG LIU, MING-SHIOU JENG & RICHARD G. HARTNOLL missing/regenerating limbs were recorded. Once sufﬁciently hardened, the CW of the newly moulted crabs was measured, and the carapace marked with an indelible pen. They were then released in their original habitats, and any crabs subsequently recaptured undergoing a further moult provided data on the intermoult period. Crabs were also released if they had failed to moult within three days of collection. Percentage moult increment (% MI) was calculated as %MI = (CW2 − CW1)/CW1 × 100 where CW1 and CW2 are premoult and postmoult carapace widths, respectively. In an attempt to determine the size of morphological maturity, measurements were made on the height of the chelar propodus in males, and the width of the pleon in females. These data were not conclusive, and are not reported further. Data on the precipitation and air temperature were obtained from the meteoro- logical station at Hualien City (24°09N 120°41E; 19 m above sea level), a few hundred meters from the study area.

RESULTS

Population structure

In the population surveys, from March to July 2001, 272 males and 164 females were measured (table I; fig. 1). Females had a unimodal distribution, with a modal CW at 17.6-20 mm. Males had no clear mode, with a similar abundance from 15 to 26 mm CW. From 22 mm CW males increasingly dominated the population. Maximum CW in the samples was 35.7 mm in males and 30.0 mm in females. The largest female collected was preparing to moult when caught, and reached 33.3 mm CW after moulting in captivity. Small individuals were rarely found within the transect, with only 18% smaller than 15.0 mm CW: the smallest crab found inside the transect was 10.7 mm CW. The size at maturity was investigated in order to place the moult increment data in context. As reported above, allometric growth analyses were inconclusive, and the only available data on maturity were the incidence of ovigerous females. The smallest ovigerous female was 16.3 mm CW, and the proportion of ovigerous females increased fairly regularly with size (fig. 1). So the size of female maturity is taken as approx. 17 mm CW. On the basis of many other studies on grapsids it is fair to assume that the size of male maturity is similar (Hartnoll, 2015). So from fig. 1 it is clear that this is predominantly a study of mature individuals, particularly in females.

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TABLE I Chiromantes haematocheir (De Haan, 1833): Data on results of monthly sampling for population composition (March-July 2001), and incidence of moulting crabs (September 2000-July 2001). See text for sampling protocols

Month Population composition Moulting crabs Samples Moults/sample Males Females Males Females September 2000 – – 2 0 7 0.3 October 2000 – – 0 0 5 0 November 2000 – – 2 2 8 0.5 December 2000 – – 0 0 12 0 January 2001 – – 0 0 12 0 February 2001 – – 0 3 13 0.2 March 2001 56 53 4 7 16 0.7 April 2001 22 20 69 48 19 6.2 May 2001 65 41 58 10 15 4.5 June 2001 70 17 17 1 3 6.0 July 2001 59 33 0 0 5 0

Moulting behaviour

Individuals of Chiromantes haematocheir approaching ecdysis can be easily identiﬁed. The chelae become paler, the crab stops feeding, and the intestine is empty, no longer having the typical black colour. Chelar muscles atrophy and the crab loses its ability to pinch. The haemolymph becomes milky white. A few hours before ecdysis, the pericardial sacs begin to absorb water and swell, protruding from under the posterior edge of the carapace. Some moulting occurred throughout

Fig. 1. Chiromantes haematocheir (De Haan, 1833). Size distribution of samples collected from March to July, 2001. The numbers above the female bars are the number of females ovigerous.

Downloaded from Brill.com10/02/2021 03:21:35AM via free access 1736 HUNG-CHANG LIU, MING-SHIOU JENG & RICHARD G. HARTNOLL the year, but taking into account the frequency of sampling (table I), it was concentrated from May to June: this was during the early part of the wet season. Moulting occurs in water, preferably small puddles where the depth is adequate to cover the body. If the water is not deep enough, the crab digs down to deepen the puddle. Most moults occur at night, though occasionally by day. The onset of ecdysis is marked by the appearance of a white line between the carapace and pleon, and moulting lasts from several minutes to several hours. The withdrawal of the posterior part of the cephalothorax from the old exoskeleton takes up most of the time. After half of the carapace and appendages have emerged from the exuvium, the rest of the moult is completed within minutes. Cannibalism during ecdysis has never been observed, even when the density of crabs was high. Soft crabs remain beside their exuviae for a few hours, but by dawn they have invariably found refuge. In the natural environment, soft crabs of C. haematocheir do not eat their own exuviae, which are always left in the puddles. However, foraging soft crabs may subsequently eat the exuviae of other crabs. In captive condition a soft crab would eat its own exuvium two or three days after ecdysis.

Moult increment

The increment was recorded in 153 males and 72 females; the increment averaged 11.5 ± 3.1% in males (range 5.5-19%) and 13.9 ± 4.2% in females (range 7.5-23%). Of 225 moulting crabs, 114 males and 45 females did not have missing or regenerating limbs. These 159 undamaged specimens were used to examine the basic distribution of increment by size and sex. The increment varied with size (fig. 2). Males showed increasing increment with increasing CW from 12.5 mm CW to 22.5 mm, decreasing when larger than 22.5 mm CW. However, overall the variation of increment with CW was not significant (fig. 3). Females showed a decreasing moult increment with increasing carapace width throughout the range, which was significant (fig. 3). Females always had a greater average increment than males of the same size class (fig. 2).

Intermoult period and moult frequency

Only seven measures of intermoult period were obtained from the mark- recapture work (ﬁg. 4): all records were from April to June, when C. haematocheir moulted more frequently (table I). The interval ranged from 28 to 51 days and increased with CW: such an increase is the standard pattern in crustaceans (Hartnoll, 1982). However, six of the seven observations were of males, so these results are inadequate to evaluate any sex-related variation.

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Fig. 2. Chiromantes haematocheir (De Haan, 1833). Mean percentage moult increment for each size class of the intact specimens collected from September 2000 to July 2001. Number above each bar is number of moults sampled.

Fig. 3. Chiromantes haematocheir (De Haan, 1833). Percentage moult increment plotted against CW for intact specimens (solid circles, males; open circles, females) collected from September 2000 to July 2001.

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Fig. 4. Chiromantes haematocheir (De Haan, 1833). Intermoult period plotted against CW for the seven marked crabs which were recaptured when moulting a second time.

Further information on size-related moult frequency in the sexes comes from a comparison of the number of observed moulting crabs in each size class with an estimate of the relative frequency of crabs of that size in the population. These values are summarized in table II. This analysis rests on a major assumption, that the size-frequency structure of the population presented in ﬁg. 1 is representative of the population from which the moulting specimens were drawn. This is reasonable, since almost all of the moulting crabs were sampled during March to July 2001, the period when the population survey was conducted. If accepted, then the analysis indicates a high relative level (this analysis gives no information on the absolute frequency of moulting) of moulting at pre-puberty sizes in both sexes, 50% in males, 68% in females. However, after maturity males retain a high relative moult frequency of 59%, whilst in females it declines sharply to 36%.

Effects of regeneration

In moulting female crabs 38% had regenerating or missing limbs, but only 25% in males; overall 29% of the 225 moulting crabs had regenerating or missing limbs. The numbers showing different degrees of limb regeneration, and the respective moult increments, are shown in table III. Of the 42 crabs regenerating one limb, 8 were regenerating a cheliped. The moult increment declined when one limb was regenerating, and more so for two limbs. For greater limb losses the increment was even further reduced, but sample sizes were very small.

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TABLE II Chiromantes haematocheir (De Haan, 1833): Estimation of relative moult frequency in relation to size and sex

Size class (mm CW) Males Females Population Moulting % Population Moulting % No. No. moults No. No. moults ∗ <12.5 5 5 100 0 1 100 ∗ 12.6-15.0 28 16 57 11 7 64 ∗ 15.1-17.5 43 17 40 29 19 66 17.6-20.0 27 22 81 54 26 48 20.1-22.5 40 31 78 48 12 25 22.6-25.0 45 26 58 17 3 18 25.1-27.5 42 21 50 4 2 50 27.6 42 15 38 1 2 100 ∗ ∗ Pre-puberty 76 38 50 40 27 68 Post-puberty 196 115 59 124 45 36

Size of maturity is estimated at 17.5 mm CW. See text for details of derivation of population number and moulting number. Percent moults provides an index of the relative frequency of moulting in that size class and sex: it does not indicate the absolute frequency of moulting or the intermoult period. * Pre-puberty size classes.

DISCUSSION

Population structure

The population structure of Chiromantes haematocheir is characteristic of that found in other grapsoid crabs with indeterminate growth patterns (see Hartnoll, 2015), with no unexpected features. The size of maturity, approx. 17 mm CW, is as usual about half the maximum size (36 mm CW in males, 33 mm CW in females). In Amakusa, Japan the maximum sizes were 40 mm CW in males, 35 mm CW in females, again larger in males: size at maturity was not speciﬁed (Tanaka & Hara,

TABLE III Chiromantes haematocheir (De Haan, 1833), moulting specimens

Limbs regenerating 0 1 2 345 Males Number 114 23 13 3 0 0 % Increment 12.210.48.97.5–– Females Number 45 19 5 2 0 1 % Increment 15.413.18.04.6–5.5

Numbers with all limbs intact, and with different numbers of regenerating limbs. In each case the mean percentage moult increment is given.

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1988). A larger maximum size in males is characteristic of most crabs (Hartnoll, 2015, table I). This is generally attributed to slower growth of mature females due to the smaller moult increments (but see discussion below) and longer intermoult periods associated with the demands of egg production and moult inhibition during incubation. Increased mortality in females due to greater exposure during breeding migrations, incubatory behaviour and larval release is also implicated (Hartnoll, 1982).

Growth pattern In Chiromantes haematocheir, the moult increment of 114 undamaged males averaged 12.2%, with no significant variation with CW. For 45 undamaged females it averaged 15.4%, and declined significantly with CW. Data for both sexes were available from 12.5-22.5 mm CW, and throughout that range the increment was larger in females. With maturity at approx. 17 mm CW, this indicates a larger increment in both immature and mature females. The only other data for moult increment in this crab are from Amakusa, Japan (Tanaka & Hara, 1988). The methods of determining increment are similar, but comparison is not straightforward due to differences in the size range sampled, and methods of analysis. For the size range of moulting reported in the present study, the Amakusa results were as follows (derived from Tanaka & Hara, 1988, fig. 4). Male increment ranged from 2.5-15%, mean approx. 9%; female increment ranged from 6-16%, mean approx. 12%. These values are smaller than those in the present study, but concur in indicating a larger increment in females. The effect of sex on increment in crabs is summarized in Hartnoll (1982). There are examples where the increment is not influenced by sex, such as Carcinus maenas (cf. Crothers, 1967), Rhithropanopeus harrisii (Gould, 1841) (cf. Turoboyski, 1973), Cyclograpsus punctatus H. Milne Edwards, 1837 (cf. Broekhuysen, 1941) and Hymenosoma orbiculare Desmarest, 1823 (cf. Broekhuysen, 1955). However, there are others in which the moult increments are smaller in females than in males, such as Birgus latro (cf. Drew et al., 2013), Cancer pagurus (cf. Bennett, 1974), Metacarcinus magister (Dana, 1852) (cf. Cleaver, 1949; Butler, 1961) and Pachy- grapsus crassipes Randall, 1840 (cf. Hiatt, 1948). The decrease of moult increment in females usually becomes most apparent after puberty, which is not surprising since reproduction then requires a larger proportion of their available resources (Hartnoll, 1982). Extreme effects are found in Uca pugilator (Bosc, 1802) in which mature females may show zero increments (Guyselman, 1953), and in Birgus latro where older mature females may have negative increments (Drew et al., 2013). In contrast, instances where the increment is larger in females, especially after puberty, are rare. The blue crab, Callinectes sapidus has mean moult increments

Downloaded from Brill.com10/02/2021 03:21:35AM via free access MOULTING OF CHIROMANTES HAEMATOCHEIR 1741 of 27% for females and 24% for males over a large size range (Tagatz, 1968). However, the female blue crab has a terminal moult before puberty, and thus these growth data are all from immature females. McLay (1982) found that in the sponge crab, Cryptodromia hilgendorﬁ De Man, 1888 males tended to be smaller than females and moult increments of males were smaller and independent of initial size, whereas moult increments of females were larger but decreased with increasing size: however, further such examples are lacking. Hence the phenomenon of larger increments in mature sized females of Chiromantes haematocheir is very unusual in crabs. There is no obvious explanation of this feature. Males do have larger chelae in the mature phase, so must invest more resources in chelar growth at each moult, potentially limiting their increment. However, such chelar growth patterns are the norm in most crabs, including those where the increments of males are equal to or larger than those of females (Hartnoll, 1982, 2012). So there remains the anomaly that females of Chiromantes haematocheir have larger increments than males, but reach a smaller size. The simplest explanation is that the females moult less often, consequently slowing growth. There are various examples of the intermoult period being extended in mature female crabs, by the combined needs of resource accumulation and inhibition of moulting during incubation (Hartnoll, 1982). The present study indicates that in the mature phase males do moult nearly twice as frequently as females, though these results need conﬁrmation. The second possibility is that higher mortality in mature females limits the size attained. Females showed a higher incidence of missing or regenerating limbs than males, 38% and 25% respectively, perhaps indicative of higher exposure to risk and mortality. The only other data on intermoult period in this species are for Amakusa, Japan (33°N). This study indicates intermoult durations of >300 days, but the data base is small, and the analysis is unclear (Tanaka & Hara, 1988). It is inadequate to differentiate between sexes and stages of maturity, and is surprisingly long in relation to species of similar size and latitude. As noted above, there is a high incidence of limb loss in Chiromantes haematocheir, one effect of which is to reduce the moult increment. The reduction in increment increased with the number of limbs lost or regenerating. The reduction of increment after limb loss is a regular phenomenon in crabs (see Hartnoll, 1982; Drew et al., 2013; McLay, 2015; and examples listed therein). One obvious factor is that resources are diverted to limb regrowth, reducing those available for general body-size increase: a second is that limb loss hinders the accumulation of the resources required for size increase at moulting (Hartnoll, 1982; McLay, 2012; Drew et al., 2013). The severe handicap of multiple limb loss makes early regeneration an imperative, and to accelerate this process the intermoult period may be reduced (Skinner & Graham, 1972; Smith, 1990; Spivak, 1990). This intermoult reduction further limits resources being accumulated for moult increment.

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Habitat, moult increment, and growth rate It is difficult to generalize on the moult increment in relation to habitat, because of the variation with size and sex: see results above, and general discussion in Hartnoll (1982). However, it is generally accepted that optimal conditions for moulting are found in the low intertidal and shallow subtidal marine environments. Such habitats provide the essential requirements of a diverse and dependable food source (for resource accumulation), water supply for post-moult enlargement, calcium supply (dissolved in sea-water) for calcification of the new integument, and a heterogeneous environment offering shelter during the vulnerable moulting and post-moult stages. Under these conditions a general consensus is that for moderately sized crabs (<50 mm maximum CW), and at least the smaller stages of larger species, the moult increment will exceed 20%, often considerably (Hartnoll, 1982, 1983). In contrast, crabs moulting in terrestrial environments (land crabs) may be restricted in the availability of one or more of the above prerequisites. The concept of ‘land crabs’ is complex: this is discussed in terms of the diversity of terrestrial adaptation in Hartnoll (1988a). Part of this diversity relates to the degree of independence from the sea for larval stages: however, this is irrelevant in the present context, where the main issue is the conditions under which the post-larval stages moult. The most adverse circumstance for land crabs is where moulting occurs without access to standing water, either salt or fresh. In many land crabs the diet is not optimal, being of low calorific value and deficient in nitrogen (Nordhaus et al., 2006), making resource acquisition difficult. Water is not available, and must be stored in the pericardial sacs or haemolymph (Hartnoll, 1988b). Calcium is not readily available, and a limited supply is obtained by re-absorption from the old integument prior to ecdysis, which is stored either in the haemolymph, or in gastroliths: this may be supplemented by consuming the cast integument (Hartnoll, 1988b). Further factors are the risk of desiccation, lack of support provided by the buoying effect of water and risks of predation, all favouring a rapid hardening of the moulted crab, which may result in smaller moult increments. However, shelter is usually ensured by using burrows, often plugged during the moult, for example, Birgus latro (cf. Fletcher et al., 1990), Cardisoma guanhumi (cf. Gifford, 1962) and Gecarcinus lateralis (cf. Wolcott, 1988). There are few comprehensive studies of moulting in these extreme ‘land crabs’: as explained in the introduction, direct observations of moulting are difficult. If the anomuran robber crab, Birgus latro, is deemed an honorary crab, then there is a detailed study based upon a large PIT tagging programme on Christmas Island (Drew et al., 2013). This showed that even for small individuals, the increment was <5%. There is also an ongoing PIT tagging study of Johngarthia lagostoma (H. Milne Edwards, 1837) on Ascension Island: in that study almost all

Downloaded from Brill.com10/02/2021 03:21:35AM via free access MOULTING OF CHIROMANTES HAEMATOCHEIR 1743 increments have been <3% (S. B. Weber, N. Weber & R. G. Hartnoll, unpubl.). In Gecarcinus ruricola (Linnaeus, 1758) on Providencia, Columbia, a small sample based on newly moulted crabs found together with their casts, had increments of <10% (Hartnoll et al., 2006): however, their environment was moister than that of J. lagostoma. Thus there is a spectrum of moult increments, ranging from >20% in optimal marine environments, to <5% in extreme terrestrial ones. How does Chiromantes haematocheir fit into this pattern? Its moult increment averaged 11.5% in males, and 13.9% in females, placing it near the middle of the range: how does this match the conditions under which it moults? It has access to water, since it moults in small pools. However, these are freshwater pools, so access to calcium supplies are restricted. The crabs must rely on stored supplies of reabsorbed calcium. This is initially dissolved in the haemolymph, and in Japanese populations subsequently stored in gastroliths in the stomach wall (Numanoi, 1940; Kitami & Honma, 1981). However, in Taiwan, gastrolith formation was not observed (H.-C. Liu, unpubl.), and the haemolymph remains milky white in colour during premoult and ecdysis. The freshwater/terrestrial crab Austrothelphusa transversa (Von Martens, 1868) similarly utilizes the haemolymph as the storage site for calcium (Sparkes & Greenaway, 1984). A notable feature of moulting in C. haematocheir is that it moults fully exposed in shallow pools, rather than within the protection of a burrow. It moults at night, but must be mobile by dawn to take shelter and avoid predation. This need for rapid mobility perhaps limits the increment, and also precludes consumption of the shed integument (the crab must leave the moult site before becoming able to feed). Similar moulting behaviour occurs in the potamonid Madagapotamon humberti Bott, 1965 (cf. Vuillemin, 1970). In such cases the certainty of a water supply clearly outweighs the benefits of a shelter. Given these compromises, it is unsurprising that the increment in C. haematocheir is below that achieved by marine crabs in optimal conditions. Nevertheless, by having access to water, it is able to outperform those land crabs lacking that benefit. Other crabs moulting with partial access to water also show restricted increments. In the high shore grapsid crab, Pachygrapsus crassipes, the moult increments range from about 15% in smaller crabs to 5% in crabs of 40 mm CW (Hiatt, 1948). In the arboreal grapsid, Aratus pisonii (H. Milne Edwards, 1837), the increment ranged from 10% at 12 mm CW to only 3% at 18 mm CW (Warner, 1967). In both cases the low values relate to mature females. So in comparison, C. haematocheir is performing well, and its choice of moulting habit seems to be justified.

REFERENCES

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First received 5 June 2017. Final version accepted 4 July 2017.

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