BUll.ETIN OF MARINE SCIENCE, 46(2): 425-431, 1990

BIOLOGY OF THE ROCK CRAB CHARYBDIS NA TA TOR (HERBST) (BRACHYURA: PORTUNIDAE)

Wayne Sumpton

ABSTRACT Trapping methods were used to sample a population of the crab, Charybdis natator, in Moreton Bay, Queensland. Males outnumbered females in the catch by almost two to one, but females were more abundant in catches during June-July, possibly because of increased feeding activity prior to the main spring spawning period. Female C. natator had two spawning peaks; a major peak in spring and a secondary peak in autumn. They were also capable of at least three ovulations per maturity instar. Examination of ovaries indicated little repro- ductive activity during winter. Fecundity estimates of ovigerous females ranged from 181,000 to 976,000. The reproductive biology of C. natator was similar to that of other subtropical portunids found in the region.

The portunid crab, Charybdis natator, is found in the Indian and western Pacific oceans (Stephenson et aI., 1958), where they contribute to crab fisheries in India (Menon, 1952) and Australia, although they are uncommon in comparison to other more abundant and commercially important crabs such as the mud crab (Scylla serrata) and the sand crab (Portunus pelagicus). In Queensland, Australia, five species of portunid crabs are exploited com- mercially, i.e., Scylla serrata, Portunus pelagicus, Portunus sanguinolentus, Cha- rybdis feriatus and Charybdis natator. The biology of Scylla serrata has been extensively studied (Hill, 1980; Williams and Hill, 1982; Hill et aI., 1982; Hyland et aI., 1984 and Heasman et aI., 1985). Similarly, the reproductive biology of Portunus pelagicus in various parts of its range has also been well documented (Prasad and Tampi, 1951; Smith, 1982; Potter et aI., 1983). More recently Campbell and Fielder (1986) have described the occurrence of ovigerous females and size at sexual maturity of P. pelagicus, P. sanguinolentus and C. feriatus in southern Queensland waters. However, apart from taxonomic descriptions (Stephenson et aI., 1958) and records of occurrence (Barnard, 1950; Ward, 1933), very little is known of the biology of Charybdis nata tor in any area of its distribution. As part of extensive research into the Portunus pelagicus fishery in Moreton Bay, Queensland during 1984-1986, samples of Charybdis natator were also pro- vided by commercial crab pot fishermen. This enabled the documentation of features of the Moreton Bay Charybdis natator population including sex ratios, molting and spawning periods, gonad development cycles and fecundity of fe- males. This paper presents these data and compares the biology of C. natator with other portunids found in the same region.

MATERIALS AND METHODS

Field Sampling.-From June 1985 to November 1986 monthly samples of Charybdis natator were obtained from four commercial crab pot fishermen in Moreton Bay, Queensland (27"5, 153°E). One day each month the total catch from approximately 50 pots from each fisherman was examined. Crabs were sexed, weighed (± 1 g) and their carapace width measured to the nearest millimeter. The molt stage of each crab was assessed using the method of Hiatt (1948), i.e., newly molted, recently molted, intermolt, premolt, ecdysis. From December 1984 to November 1985 gonads of male crabs were removed and Gonosomatic Indices (GSls) calculated as a percentage gonad weight of body weight. Ovaries of mature females

425 426 BULLETIN OF MARINE SCIENCE, VOL. 46, NO.2, 1990

30 Females "=381 >- (J Males ":0694 z 20 ILl ~ a ILl I IE: 10 I I&. -~I ?P. J 0 50 70 90 110 130 150 CARAPACE WIDTH(mm) Figure 1. Length frequency distributions of male (broken line) and female (continuous line) C. natatar taken from pots in Moreton Bay.

were removed and the diameter of oocytes measured using a calibrated eyepiece on a stereomicroscope. On the basis of ovary color and size the following ovarian stages of development were recorded: Inactive: ovaries thin, translucent, no yolk deposition in oocytes. Maturing: ovaries red, not extending into hepatic region, yolk deposition in oocytes. Ripe: ovaries red, covering cardiac region and extending into hepatic region. Spent: ovaries thin, light cream in color, atretic oocytes present. The spermathecae of females were examined for the presence of recently implanted spermatophores and the incidence of gravid females was recorded. Laboratory Experiments.-Mature males and females (size range 75-125 mm) were maintained in- dividually and in pairs in glass aquaria (90 cm' 30 cm· 35 cm) containing 10 cm of sand and recirculating filtered seawater. Mating behavior was observed and records kept oftime intervals between successive egg extrusions and time of larval hatching. The fecundity of 18 females was estimated by removing eggs from the pleopods and drying to constant weight at 70°C. Five subsamples, each of approximately 2,000-5,000 eggs were then weighed (±O.2 mg) and counted under a stereomicroscope. The estimated number of eggs in the egg mass was then calculated.

RESULTS Field Sampling. - Total length frequency distributions of male and female C. natatar obtained from pot catches are shown in Figure I. Males were more abun- dant than females, and were also, on average significantly larger (t = 2.84, P < 0.01). The largest male and female captured during the study were 142 mm and 126 mm, respectively, with maximum recruitment of males into the fishery oc- curring at a greater size (100-105 mm) than for females (90-95 mm). Despite the overall predominance of males, females outnumbered males during June, July 1985 and June 1986 (Fig. 2a). However, from November to May the proportion of males in the catch always exceeded 60%. Fewer than 5% of crabs caught were sexually immature, and the smallest mature male and female were both 71 mm carapace width. No mating pairs, premolt crabs or crabs in the process of ecdysis were captured. There was also no clear trend in molting activity of either sex, although molting of males in particular was limited during September-October of both years (Fig. 2b). Gonosomatic Index (GSI) values ofintermolt male crabs (Fig. 3) suggest that summer (December-February) was the main mating period since GSls were high- est during December, and showed nearly a 50% decline during the following 2 months. Gravid females ranged in size from 78 to 117 mm carapace width (mean = 94.0 mm). When first extruded, eggs were normally red in color, progressively deepening to a dark grey prior to larval hatching. The peak of spawning activity SUMPTON: BIOLOGY OF CHARYBDIS NATA TOR 427

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MONTH Figure 2. a. Seasonal variation in C. nalalor sex ratios. b. Proportion of male (broken line) and female (continuous line) C. nalalor which were either newly or recently molted. occurred during warmer months, notably October (Fig. 4). At this time 70% of females caught in pots were gravid. Egg carrying females were present throughout most ofthe year, although there was comparatively little spawning activity during winter. Numerous gravid females were sampled which also had maturing or ripe gonads, indicating that they might have been able to produce a further brood of eggs shortly after the eggs that they were carrying had hatched. The seasonal ovarian development cycle reinforced the spring spawning peak as deduced from data on sampled gravid females (Fig. 4). During June of both years most females were non-gravid and had inactive or spent ovaries, indicating little reproductive ac- tivity. Despite the lack of gravid females during September 1985, the ovaries of almost 90% of females were either maturing or ripe, suggesting that egg extrusion may have been imminent. The proportion offemales which had inactive ovaries during October was low. At this time most females were also gravid, suggesting, as mentioned earlier, that many were probably capable of a further ovulation shortly after larval hatching. Only four females had spermatophores in their sper- mathecae, indicating recent mating. All were postmolt, had inactive gonads and were sampled during July, November and December 1985 and May 1986. Laboratory Experiments. - The low incidence of juvenile and pubertal females in the catch made it difficult to accurately determine the numbers of maturity instars and ovulations per instar by rearing crabs in the laboratory. Nevertheless, six of the females held in the laboratory ovulated three times before molting, suggesting that the crabs were capable of at least three ovulations per maturity molt. Mating of crabs was observed twice in the laboratory and took place between intermolt males and postmolt females. Prior to copulation both males carried premolt females for two days and on one occasion the male was seen assisting the female during her molt. Copulation occurred shortly after the female had molted and both males remained in post copulatory attendance of the female for a further two days. Successful adhesion of eggs to the pleopods did not take place unless 428 BULLETIN OF MARINE SCIENCE, VOL. 46, NO.2, 1990

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MONTH Figure 3. Seasonal variation in male Gonosomatic Indices (GSI). Standard deviations are shown as vertical bars and sample sizes are indicated above each bar. there was sand in the holding tanks. Hatching of eggs in the laboratory at 25 ± 2°C, occurred II to 15 days after extrusion and the minimum time between larval hatching and extrusion of a further brood of eggs by a female was seven days (at 25°C). Providing the female had mated at her molt the eggs in these subsequent extrusions were always fertile, even in the absence of males. The estimated number of eggs in the egg masses of 18 females ranging in size from 80-117 mm were highly variable. Estimates ranged from 181,230 eggs for a 100 mm carapace width female to 976,248 for a female with a carapace width of 117 mm. The relationship between egg number and carapace width was

Ne = CW(1.78 x 104) - 1.16 X 106 (r = 0.79, P < 0.001, N = 18) where Ne = number of eggs in egg mass, CW = carapace width in millimeters.

DISCUSSION The spawning season of C. natatar recorded in the present study is similar to that obtained for other portunids in the same region by other authors. Thomson SUMPTON: BIOLOGY OF CHARYBDIS NATATOR 429

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MONTH Figure 4. Proportion of mature females with inactive or spent ovaries (broken line) and proportion of ovigerous mature females (continuous line).

(1951) found that most gravid P. pelagicus females were taken between September and April. More recently, Campbell and Fielder (1986) found two peaks in the numbers of gravid P. pelagicus, one in September and the other in February. By comparison, P. sanguinalentus displayed a single spawning period which extended from October to February. Campbell and Fielder (1986) concluded that increases in the proportion of gravid females in the population in early spring were asso- ciated with rising water temperatures. The present study has also found two major spawning peaks for C. nata tar. During winter the low proportion of gravid females and high proportion offemales with inactive gonads indicate that C. natatar does not spawn year round in the subtropical waters of Moreton Bay. Pillai and Nair (1976) found that the closely related Charybdis feriatus bred throughout the year in southwestern Indian waters, although gravid females were more common during January and February. It is thus likely that the cooler conditions during winter in Moreton Bay limit the spawning activity of C. natatar. Fecundity estimates of other portunid species obtained by Campbell (1984) varied depending on the size and maturity instar of the crab but the maximum number of eggs per egg mass was approximately 2.4 million, 1.7 million and 3.2 million for P. pelagicus, P. sanguinalentus and C. feriatus respectively. These estimates place C. natatar below the other commercially exploited species in terms of fecundity. This is not surprising considering the other three species attain a larger size than C. natatar. There are no catch records in Queensland which describe the species breakdown of the total crab catch; however, C. natalar make up as much as 20% of the catch of some fishermen (personal observation). The lower comparative fecundity of C. natalar is unlikely to be the major reason for its limited fishery since interspecific competition, habitat and environmental pa- rameters no doubt also influenced the crabs' distribution and abundance. Williams and Hill (1982) discussed some of the limitations of using data ob- tained from pot catches of Scylla serrata. They concluded that pot catches were not representative of actual population size structure because of differential vul- nerability to capture of subadults. This is likely to be the case for C. natalar also 430 BULLETIN OF MARINE SCIENCE, VOL. 46, NO.2, 1990 since many crabs less than 90 mm carapace width are readily able to escape through the 65 mm wire mesh of the pots (personal observation). Providing that both sexes have an equal probability of capture, the sex that attains the largest size will be better represented in the pot catches. The observed smaller average size of female crabs thus clearly biases sex ratios towards males. In view of this bias it is interesting to note the dominance of females in catches during June of both years. It is well known that crustacean feeding is often greatest prior to gonad maturation and spawning (Hartnoll, 1972). Balanced against this is the decline in metabolic rate and feeding, usually associated with decreased water temperature (Branford, 1979; Leffler, 1972). The greater representation of females in samples during June and July is thus probably a reflection of their increased feeding (and therefore catch ability) prior to the main spring spawning period. Despite the biases associated with using data obtained from pot catches Sump- ton et al. (in preparation) have found gonad development and spawning cycles of Portunus pelagicus deduced from both trawl and pot samples were almost iden- tical. The efficiency of the former method being relatively independent offeeding or molt stage. Laboratory observations on the mating behavior of C. natator correspond with the most common brachyuran pattern (Hartnoll and Smith, 1979) and was iden- tical to the behavior of other portunids described by Campbell (1984). Gonad development of male C. natator was not as seasonal as that of females. This fact, and the low incidence offemales with recently implanted spermatophores, hampers the definition of mating periods. However, the fact that the few recently mated females captured were spread over a range of months (including July), suggests that mating may take place all year round, even though it may be more common during summer when male GSIs are highest. Mating most likely takes place whenever molting mature females are available for copulation. Based on molting data, this is throughout most of the year. In other portunids, viable sperm can be stored by females for several months before eggs are fertilized (Van Engel, 1958). It is, therefore, quite likely that female C. nata tor may also be able to store sperm for some time prior to fertilization and extrusion. The fact that females mated at the molt could also produce successive batches of fertile eggs even in the absence of males indicates that stored sperm could also be used to fertilize successive extrusions within a particular instar.

ACKNOWLEDGMENTS

I gratefully acknowledge the assistance of the following fishermen: P. Conaty, C. Davenport, R. Fursey, A. Groves, R. Honey, D. Smith, G. Smith and F. Somers. A number of colleagues also assisted during the study, notably G. Smith and M. Potter. Comments on early drafts of the manuscript were provided by R. Morton and T. Wassenberg. Thanks also to Miss G. Davidson for typing the manuscript.

LITERATURE CITED

Barnard, K. H. 1950. Descriptive catalogue of South African crustacea (crabs and Shrimps). Ann. S. Afr. Mus. 38: 1-824. Branford, J. R. 1979. Locomotor activity and food consumption by the lobster Homarus gammarus. Mar. Behav. Physiol. 6: 13-24. Campbell, G. R. 1984. A comparative study of adult sexual behaviour and larval ecology of three commercially important portunid crabs from the Moreton Bay region of Queensland, Australia. Unpublished Ph.D. Thesis, University of Queensland. 253 pp. -- and D. R. Fielder. 1986. Size at sexual maturity and occurrence of ovigerous females in three species of commercially exploited portunid crabs in southeast Queensland. Proc. R. Soc. Qld. 97: 79-87. SUMPTON: BIOLOGY OF CHARYBDIS NA TA TOR 431

Hartnoll, R. G. 1972. The biology of the burrowing crab, Corystes cassivelaunus. Bijdr. Dierk. 42: 139-155. --- and S. M. Smith. 1979. Pair formation in the edible crab Cancer pagurus (Decapoda, Brachy- ura). Crustaceana 36: 23-28. Heasman, M. P., D. R. Fielder and R. K. Shepherd. 1985. Mating and spawning in the mud crab, Scylla serrata (Forskal) (Decapoda: Portunidae). Aust. J. Mar. Freshwat. Res. 36: 773-783. Hiatt, R. W. 1948. The biology of the lined shore crab Pachygrapsus crassipes, Randall. Pacif. Sci. 2: 135-213. Hill, B. J. 1980. Effect of temperature on feeding and activity in the crab Scylla serrata. Mar. BioI. 59: 189-192. ---, M. J. Williams and P. Dutton. 1982. Distribution of juvenile, subadult and adult Scylla serrata (Crustacea: Portunidae) on tidal flats in Australia. Mar. bioI. 69: 117-120. Hyland, S. J., B. J. Hill and C. P. Lee. 1984. Movement within and between habitats by the portunid crab Scylla serrata. Mar. BioI. 80: 57-61. Leffler, C. W. 1972. Some effects of temperature on growth and metabolic rate of juvenile blue crabs, Callinectes sapidus, in the laboratory. Mar. BioI. 14: 104-110. Menon, M. K. 1952. A note on the bionomics and fishery of the swimming crab Neptunus san- guinolentus (Herbst) on the Malabar coast. J. Zool. Soc. India 4: 177-184. Pillai, K. K. and N. B. Nair. 1976. Observations on the breeding biology of some crabs from the southwest of India. J. Mar. Assoc. India 15: 754-770. Potter, 1. c., P. J. Chrystal and N. R. Loneragan. 1983. The biology of the blue manna crab Portunus pelagicus in an Australian estuary. Mar. BioI. 78: 75-85. Prasad, R. R. and P. R. S. Tampi. 1951. An account of the fishery and fishing methods of Neptunus pelagicus (Linnaeus) near Mandapam. J. Zool. Soc. India 3: 335-339. Smith, H. 1982. Blue crabs in South Australia-their status, potential and biology. Safic (Adelaide, Australia) 6: 6-9. Stephenson, W., J. J. Hudson and B. Campbell. 1958. The Australian Portunidae (Crustacea: Por- tunidae). II. The genus Charybdis. Aust. J. Mar. Freshwat. Res. 8: 491-507. Thomson, J. M. 1951. Catch composition of the sand crab fishery in Moreton Bay. Aust. J. Mar. Freshwat. Res. 2: 237-244. Van Engel, W. A. 1958. The blue crab and its fishery in Chesapeake Bay, Part 1. Reproduction, early development, growth and migration. Comm. Fish. Rev. 20: 6-17. Ward, M. 1933. New genera and species of marine Decapoda Brachyura. Aust. Zool. 7: 377-394. Williams, M. J. and B. J. Hill. 1982. Factors influencing pot catches and population estimates of the portunid crab Scylla serrata. Mar. BioI. 71: 187-192.

DATEACCEPTED: August 22, 1988.

AnDRESS: Southern Fisheries Research Centre. P.O. Box 76. Deception Bay. 4508, Australia.