BULLETIN OF MARINE SCIENCE, 41(2): 234-241, 1987

REPRODUCTIVE BIOLOGY OF SPP. (CRUSTACEA: ) FROM THE LABU ESTUARY IN PAPUA NEW GUINEA

Norman 1. Quinn and Barbara L. Kajis

ABSTRACT The mud , Scylla spp., is a common estuarine found along the coast of Papua New Guinea. Two species were studied in the Labu estuary near Lae: S. serrala and S. paramamosain. S. serrala becomes sexually mature at a smaller size (lO-cm carapace width) than S. paramamosain (12 em). Both the size of S. serrala at initial reproduction and maximum size of females are smaller than in populations studied at higher latitudes such as Queensland, Australia and South Africa. Reproduction occurs continuously throughout the year in the S. serrala population. The percentage of reproductive females was slightly larger during the change of seasons in March/April and September/October. The parasitic gill barnacle, OclOlasmis cor, did not inhibit reproductive development. There was no variation in the gonadal somatic index associated with lunar periodicity.

Portunid of the Scylla are common in the mangrove swamps of Papua New Guinea. While only one species of Scylla, S. serrata, is commonly recognized in the literature, differences in life history strategies exhibited in this study suggests that two species of Scylla are found in this area: (1) the common S. serrata (Forskal), and (2) the larger, uncommon S. paramamosain Estampador. Local studies have centered on their importance to subsistence fisheries (Purari Delta-Haines, 1979; Opnai, 1980; Labu estuary-Quinn, 1984a; 1984b) rather than on biological aspects. In this study we examined the reproductive biology of S. serrata and S. paramamosain in the Labu estuary south of Lae, Papua New Guinea, concentrating primarily on the former species because of its much greater abundance. Specifically, we investigated the size of females of both species at the onset of sexual maturity. Sexual maturity appears to occur at a smaller size in many tropical compared to subtropical populations of (Heasman, 1980). Higher water temperatures in the tropics are suspected to increase the crabs' growth rate and decrease time to maturity (Fielder and Heasman, 1978). Additionally, we examined the annual and lunar breeding periodicity of Scylla serrata. Temperature and photoperiod are considered the major environmental factors determining breeding periodicities in marine invertebrates (Pillai and Ono, 1978). Heasman (1980) postulated that, owing to the higher year round water temperatures in the tropics, reproductive activities in tropical populations would be more protracted and subject to a lower degree of seasonal variation. As the waters in the Labu estuary are > 25°C year round (Quinn and Kojis, 1986) and day length varies little, we predicted that there would be no distinct spawning season in the Labu populations of Scylla serrata.

MATERIALS AND METHODS

Samples of Scylla serrata and S. paramamosain were purchased in the Lae main market on Saturday mornings from 2 March 1984 to 30 March 1985, totaling 192 males and 498 females. All the crabs had been caught within the previous 4 days in the Rhizophora sp. dominated Labu estuary (6°46'S, 146°57'E). The crabs were gathered by women during low tides using small oval nets or with hooks which are used to drag the crabs out of their burrows (Quinn, 1984a; 1984b).

234 QUINN AND KOnS: SCYLLA SPP. REPRODUCTION IN PAPUA NEW GUINEA 235

Table I. Body morphometries of Scylla spp. in the Labu estuary

Body weight Carapace width

N qg) SD Range (g) ~ (em) SD Range (em) Scylla serrata Females 498 249 116 48-1,090 10.9 16.1 6.4-18.0 Males 192 330 154 72-936 10.6 13.9 7.1-16.1 Scylla pararnarnosain Females 32 533 269 195-1,278 14.8 20.3 10.4-19.8 Males 8 739 327 315-1,180 14.3 17.2 11.9-16.4

Measurements of carapace width (C.W.) were taken across the carapace from the notch between the 8th and 9th antero-Iateral spines to the nearest 0.5 mm using vernier calipers. The crabs were narcotized by being placed in a freezer for 3-5 h and afterwards weighed to the nearest gram. They were next dissected and gonads removed and weighed to the nearest 0.01 g. The color, condition of the gonads and ranked presence of parasitic barnacles were recorded. Crabs displaying obvious ceph- alothoracic damage, malformation or soft shells were not included in the analysis.

RESULTS Size and Weight of Crabs. - The size and weight of the crabs sampled is given in Table 1. Far fewer were sampled, reflecting their low abun- dance in the Lae market and the Labu estuary. However, the data does suggest that S. paramamosain grows to a larger size than S. serrata in the Labu estuary. The modal CW. of female Scylla serrata was 11.5-12.0 cm with about 78% having a modal CW. of 10.0-12.5 cm (Fig. 1A). The modal CW. of sampled males was 10.0-11.0 cm with 81.8% of the males having a CW. between 8.0- 11.5 cm (Fig. 1B). The population was considerably smaller than the 16.0-19.0- cm range most frequently encountered in markets in Ponape (Perrine, 1978). However, the Labu population was larger than the Sundarbans population in India where the mean CW. for females was 9.4 cm and 10.0 cm for males (Chakrabarti, 1981). Female Size at Maturity. -In female Scylla spp. ovaries begin to enlarge and change color when the crab attains sexual maturity. Immature ovaries are trans- lucent. When the crabs become sexually mature, the ovaries initially become white and then tan. The immature oocytes of these ovaries have a reticulated cytoplasm with little yolk present (Fig. 2A). As oocytes enlarge and mature, yolk globules form in the cytoplasm (Fig. 2B) and the ovaries become yellow, orange or red/orange with the latter being the most common color. Using color and size as an indicator of gonad maturity, the percentage of females that had maturing ovaries was calculated for each 3-mm CW. interval (Fig. 3). The size when 50% of S. serrata were sexually mature (SM50) was chosen as an appropriate measure of the size at maturity. SM50 occurred around 10.5 cm CW. in the female crabs. Gonad index values (drained ovary weight/total live weight x 100% = GSI) were grouped according to carapace width. Female Scylla serrata from Labu begin gonadal development in size class 8.5-<9.5 cm with most being reproductive at CW. 10.5-< 11.5 cm. The smallest female crab with mature abdomen and de- veloping gonads was 8.5 cm CW. Larger crabs generally had a higher GSI (Ta- ble 2). There is insufficient data to determine the sexual maturity of Scylla parama- mosain. However, our data do suggest that females of this species undergo their maturity molt at a larger carapace width (12.0 cm) than S. serrata. 236 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

80 A Femal••

g: 80 40 •••1.' -< a: B u u. o 40 a: 20 W m ~ z 20 o

o CARAPACE WJ)TH C ••• I 8 8 10 •• 11 Figure I. Size frequency histograms of carapace width of Scylla serra/a: A, females; B, males.

Annual Periodicity of Female Reproduction. - Using only adult crabs with a gonad weight> 2 g (N = 299), the GSI was calculated for 15 months (Fig. 4). Autocor- relation analysis of GSI revealed no significant annual cycle or any cycle of a lower frequency. The coefficient of variation ranged from 51% to 81%, but without the seasonal pattern observed by Heasman (1980). A portion of the population was reproductive at all times of the year. The total mean of the pooled GSI values over each lunar month was 6.9 with a coefficient of variation of 68%. The period of least reproductive activity was February where the GSI was less than half of the maximum values of April and June and September/October. The GSI was lowest when the estuary waters were warmest which contrasted with observations that the spawning season was during the warmest months [e.g., Hawaii, May to October (Brick, 1974); Philippines, May to September (Arriola, 1940); South Africa, November to March (Hill, 1975); and Thailand, July to December (Varikul

Figure 2. Oocytes of Scylla serra/a at different stages of maturity: A, immature oocytes from pale tan ovary; B, maturing oocytes from bright orange ovary with large yolk vesicles. C, reticulated cytoplasm; G, germinal vesicle; Nu, nucleolus; Y, yolk vesicles. Horizontal lines represent 0.05 mm. QUINN AND KOJIS: SCYLLA SPP. REPRODUCTION IN PAPUA NEW GUINEA 237

100 Females .. 8 . W 0: ::l 10 l- e:( 60 ::!: 8 I- Z rJ) W 40 W 6 U ::l 0: ..J W e:( 0.. > 4 20 en c:l 2

OL,..::.=.:;-~-~~-~-~-~ o 6 8 10 12 14 16 18 20 MAMJJASONDJFM

MONTHS CARAPACE WIDTH (em)

Figure 3. (Left) Percent mature female Scylla serrata at various carapace widths. Figure 4. (Right) Gonad/Somatic index through time for female Scylla serrata. Vertical lines represent the range of values. et aI., 1972) (Table 3)]. Only Pillai and Nair (1968) in India recorded a decrease in reproductive activity during the warmest months (May to August). Lunar Periodicity of Female Reproduction. - To test whether the GSI of 267 females (C.W. > 10.2 cm) exhibited lunar rhythms, the data were put into four groups representing different lunar phases. The GSI ranged from 4.76 during the first quarter lunar phase to 5.92 at the full moon phase (Table 4). A two way ANOV A was performed on GSI values controlling for lunar phases and months. There was no significant differences (P > 0.05) for either the main effects or the interactions (Table 5). Sex Ratios. - About 51% of the Scylla serrata catch were mature males, 40% mature females and 9% juveniles. The sex ratio in marketed adult crabs varied seasonally (Table 6). Males were most common in the market (and presumably in the estuary) from May to October representing 68% of the catch during that

Table 2. Female GSI values by carapace width

('arapaee width (em) Mean GSI N CV% Range

6.5-<7.5 0.20 6 57 0.14-0.39 7.5-<8.5 0.12 25 57 0.08-0.33 8.5-<9.5 1.25 58 273 0.06-15.52 9.5-< 10.5 3.66 101 130 0.05-17.10 10.5-< 11.5 5.15 119 106 0.04-21.47 11.5-<12.5 5.48 131 83 0.04-15.57 12.5-< 13.5 5.64 32 68 0.03-13.36 13.5-< 14.5 5.49 6 109 0.23-15.93 14.5-< 15.5 7.75 8 74 0.74-17.77 15.5-<16.5 9.25 5 75 3.12-19.31 16.5-<17.5 9.12 1 17.5-< 18.5 0.53 1 238 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

Table 3. Spawning periods of Scylla serrala at various latitudes

Location Total spawning period Peak spawning period Latitude Reference Ponape all year no peaks 7°N Perrine, 1978 Labu estuary all year April-June 70S this study PNG Sept.-Oct. Thailand unknown July to Dec. 12°N Yarikul et aI., 1970 India all year Dec. to Feb. 13°N Pillai and Nair, 1968 Philippines all year May to Sept. 15°N Arriola, 1940 Hawaii unknown May to Oct. 200N Brick, 1974 Australia Sept.-March Nov.-Dec. 28"5 Heasman, 1980 South Africa Nov.-March unknown 34"5 Hill, 1975 period. This high ratio of males was possibly due to a higher migration rate of females out of the estuary during this time of year. Parasitic Gill Barnacle Infestation.-About 16% of the juvenile female (C.W. < 10.3 em) and 48% of the adult female Scylla serrata population had parasitic barnacles (Octolasmis cor) on their gills. Three percent of the former and 18% of the latter were heavily infested with barnacles. About equal percentages ofjuvenile and adult males (46% and 51%) had barnacle infestations, while less than 2% of juvenile and 6% of adult males had heavy infestations. Using a t-test, no significant difference was found in the gonad weight, body weight and gonad/somatic index of individuals of Scylla serrata size classes 11.0- 13.0 and> 13.0 cm, with no barnacles and individuals heavily infested. Male Scylla paramamosain had greater barnacle infestation (84%) than females (66%). Over 37% of the females and 50% of the males were heavily infested. Larger individuals of both species were more likely to be infested and infestations were heavier. Their shell condition suggested that they had not molted for some time.

DISCUSSION Minimum carapace width at sexual maturity has been reported over a range of 5.3 cm from various countries (Table 7). The latitudinal pattern suggests that Scylla serrata matures at a larger size at higher latitudes. Hill (1975) noted that growth rate was apparently independent oflatitude and that crabs in South Africa matured when they were older. If this is true, then the equatorial Papua New Guinea populations, matured at a younger age than subtropical populations, spe- cifically at the commencement of Heasman's (1980) growth phase III. Heasman (1980) suggested that mud crabs reach 8-12 cm at the end of their first year and 13-15 cm by the end of the second year. If these growth rates apply to the Labu population, then we could expect 50% of the females to be sexually mature 12 months after spawning. Spawning would then occur when the crabs were one year old rather than when they are three as in Queensland, Australia.

Table 4. Gonad/Somatic index by lunar phase

Lunar phase x OSI SD N

First Quarter 4.76 4.95 86 Full Moon 5.92 4.80 77 Last Quarter 5.15 4.62 77 New Moon 5.77 5.29 92 QUINN AND KOJIS: SCYLLA SPP. REPRODUCfION IN PAPUA NEW GUINEA 239

Table 5. ANOY A of OSI values affected by lunar phase and month

Source or variation Sum of squares df Mean square F Signif F Main effects 560.543 17 32.973 1.310 0.188 Lunar phase 116.712 3 38.904 1.546 0.204 Month 467.298 14 33.378 1.326 0.193 2-Way interactions 683.294 32 21.353 0.848 0.703 Lunar phasc month 683.294 32 21.353 0.848 0.703 Explained 1243.837 49 25.384 1.009 0.466 Residual 5461.294 217 25.167 Total 6705.131 266 25.207

Perrine (1978), studying Scylla serrata in Po nape (7°N), reported the only ex- ception to this latitudinal pattern. Egg-bearing crabs in Ponape were minimally 14.1 cm in carapace width and sexual maturity occurred at 12.0 cm. The size of crabs at sexual maturity in Ponape corresponds closely to S. paramamosain in the Labu estuary. The Labu data, although limited, suggests that S. paramamosain has a different life history strategy to that of S. serrata. The former becomes sexually mature at a larger size and achieves a larger maximum size than the latter. The Ponape anomally bears further study, especially with regard to the light it may throw on the species question in the genus Scylla. The year-round reproductive activity of the tropical Labu population of Scylla serrata supports Heasman's (1980) postulate that reproduction in tropical pop- ulations will be more protracted and less seasonal. Reproductive activity of Scylla serrata occurs year-round at low latitudes and seasonally at higher latitudes. In the Philippines S. serrata spawns throughout the year with the peak occurring from the end of May to the end of September (Arriola, 1940). From observations by local fishermen and himself, Perrine (1978) concluded that mating occurred throughout the year in Ponape (7°N, 157°E). We found that, although a percentage of the population is reproductive all year round, more crabs are reproductive from April-June and September-October, which coincides with the change of seasons in Lae. In subtropical South Africa (Hill, 1975) and Moreton Bay, Aus-

Table 6. Lunar month sex ratios of crabs for sale in the Lae market on Saturday morning between 8-9 am (N is the number of Saturdays)

Month Total males ('!o) Total females ('!o) Total adult crabs N

March 1984 86 (51%) 82 (49%) 168 3 April 1984 III (40%) 163 (60%) 274 3 May 1984 70 (76%) 22 (24%) 92 4 June 1984 not sampled July 1984 127(68%) 60 (32%) 187 2 August 1984 172 (67%) 86 (33%) 258 2 September 1984 152 (68%) 71 (32%) 223 3 October 1984 78 (65%) 42 (35%) 120 1 November 1984 159 (56%) 126 (44%) 285 4 December 1984 not sampled January 1985 295 (71%) 123 (29%) 418 3 February 1985 297 (71%) 252 (29%) 549 4 March 1985 272 (47%) 307 (53%) 579 4 April 1985 54 (28%) 140 (72%) 194 I Total pooled % 59% 41% 240 BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2, 1987

Table 7. Minimum size at sexual maturity-females (All carapace widths, CW, measured from the 9th antero-Iateral spine tips or standardized to this measurement)

Country CW(cm) Latitude Author Malaysia 9.2 SON Ong (1966) Papua New Guinea* 9.0 60S this study Philippines 8.5 8°N Escritor (1970) Thailand 9.3 12°N Yarikul et al. (1972) India 9.7 13°N Raja Bai Naidu (1955) Philippines 10.0 15°N Arriola (1940) Queensland 13.8 28°S Heasman (1980) South Africa 13.7 34°S Hill (1975) • Stnndnrdized to 9th antero-lateral spine tip measurement by multiplying 8.5 em by 1.06. tralia (Heasman, 1980), mating and spawning of Scylla serrata occurred in the summer months. It has been suggested that in tropical estuaries the period of peak spawning generally coincides with periods of high nutrient input associated with monsoonal or cyclonic rainfall (Heasman, 1980). As moderate rainfall occurs throughout the year in Lae (Quinn and Kojis, 1986) it is likely that sufficient nutrients were available for continued reproduction year round. The non-seasonal nature of reproduction probably results in nearly continuous recruitment. This was supported by the lack of any distinct year class structure in the population (Fig. IA, B). The Labu populations were similar to the Malaysian populations (Ong, 1966) in the wide range of carapace widths of mature females. This is probably due to the combined effects of continued moulting after first maturity and a difference in percentage moult increments in individuals at each moult. In Ponape, the movement offemale Scylla serrata out of the estuaries followed a lunar rhythm and was thought to be associated with spawning (Perrine, 1978). Scylla serrata is known to migrate offshore to spawn in Queensland (Hill, 1982), but there was no evidence of this in our study. No crabs were caught in scores of trawls in less than 20-m depth in the narrow continental shelf off the Labu estuary. Villagers never caught berried crabs in their nets which were set daily near the narrow (20-30 m) mouth of the estuary and no berried crabs were sold in the market. However, the Labu villagers were knowledgeable about the color of the eggs and where they were carried on the crabs claiming to have captured berried crabs in the estuary, but knew nothing about spawning movements. The salinities commonly occurring in the estuary (x = 18.40/00)(Quinn and Kojis, 1986) seem to preclude development of crab eggs since they were generally below the accepted survival tolerance limits (200/00)of both zoeal and megalopal stages of the crab (Brick, 1974; Hill, 1974). The parasitic gill barnacle, Octolasmis cor, has been suggested as causing the death of mud crabs (Hashmi and Zaida, 1964) by reducing respiratory efficiency. If this were the case, then one would expect a reduction in biological functions such as reproduction to occur with increasing levels of infestation. On the contrary, there was no significant difference between gonad weight or GSI levels between clean and heavily parasitized Scylla serrata.

ACKNOWLEDGMENTS

This work was funded by the Papua New Guinea University of Technology (Grant 365). We are grateful to the people ofLabu Butu village, particularly M. Sappu, for their co-operation and assistance. QUINNANDKOJlS:SCYLLA SPP.REPRODUCTIONINPAPUANEWGUINEA 241

The use of the laboratory of the Department of Chemical Technology and computing facilities of the Computer Center are gratefully acknowledged.

LITERATURE CITED

Arriola, F. J. 1940. A preliminary study of the life history of Scylla serrata (Forskill). Philipp. J. Sci. 73: 437-455. Brick, R. W. 1974. Effects of water quality, antibiotics, phytoplankton and food on survival and development of larvae of Scylla serrata (Crustacea: Portunidae). Aquaculture 3: 231-244. Chakrabarti, K. 1981. A growth study of the crab Scylla serrata (Forsk~) in the Sundarbans. Indian J. For. 4: 102-106. Fielder, D. F. and M. P. Heasman. 1978. The Mud Crab. Queensland Museum Booklet. 15 pp. Haines, A. K. 1979. The subsistence fishery of the Purari Delta. Sci. New Guinea 6: 80-95. Hashmi, S. S. and S. S. Zaidi. 1964. Incidence of Lepas infestation on the gills of Scylla serrata in Karachi waters. Ag. Pakistan 16: 1. Heasman, M. 1980. Aspects of the general biology and fishery of the mud crab Scylla serrata (Forskill) in Moreton Bay, Queensland. Ph.D. Thesis, University of Queensland. 506 pp. Hill, B. J. 1974. Salinity and temperature tolerance of zoeae of the portunid crab Scylla serrata. Mar. BioI. 25: 21-24. ---. 1975. Abundance, breeding and growth of the crab Scylla serrata in two South African estuaries. Mar. BioI. 32: 119-126. ---, ed. 1982. The Queensland Mud Crab Fishery. Queensland Fish. Infor. Ser. Fish. Res. Br., Fortitude Valley. 54 pp. Ong, K. S. 1966. Observations on the post-larval life history of Scylla serrata reared in the laboratory. Malay. Ag. J. 45: 429-445. Opnai, J. L. 1980. The mangrove crab, Scylla serrata, in the Era and Purari Delta and its fishery. Pages 83-91 in D. Gwyther, cd. Possible effects of the Purari hydroelectric scheme on subsistence and commercial crustacean fisheries in the Gulf of Papua. Workshop 12th December, 1979. Purari River (Wabo) Hydroelectric Scheme Environmental Studies, 15. Department of Environment and Conservation, Waigani, Papua New Guinea. Perrine, D. 1978. The mangrove crab on Ponape. Report on the Marine Resources Division, Ponape. Eastern Caroline Islands. Trust Territory of the Pacific Islands. 66 pp. Pillai, K. K. and N. B. Nair. 1968. Observations on the reproductive cycles of some crabs from the south-west coast ofIndia. J. Mar. BioI. Ass. India. 10: 1-2. --- and Y. Ono. ]978. The breeding cycles of two species ofgrapsid crabs (Crustacea: ) from the north coast of Kyushu, Japan. Mar. BioI. 45: 237-248. Quinn, N. J. 1984a. Dynamics and exploitation of fish resources near the mouth of the Markham River, Papua New Guinea. Ph.D. Thesis, University of Queensland. 220 pp. ---. 1984b. Subsistence fishing of Labu Butu village, Morobe Province. Pages 18-21 in N. J. Quinn, B. L. Kojis and P. Warpeha, eds. Subsistence fishing practices in Papua New Guinea. Appropriate Technology Development Institute Traditional Technology Series. 2. --- and B. L. Kojis. ]986. Annual variation in the nocturnal estuarine assemblage of a tropical estuary. Est. Coast. Shelf Sci. 22: 63-90. Varikul, V., S. Phumiphol and M. Hongpromyart. 1972. Preliminary experiments in pond rearing and some biological studies of Scylla serrata. Pages 366-374 in T. V. R. Pillay, ed. Coastal aquaculture in the Indo-Pacific region. Fishing News (Books), London.

DATEACCEPTED: December] 6, 1986.

ADDRESS: Lizard Island Research Station, P.M.B. 37, Cairns, Queensland 487 I, Australia.