UC Davis UC Davis Previously Published Works

Title Studies on the reproductive biology of the mud crab, Rhithropanopeus harrisii: effects of sex ratio and stocking density on egg production

Permalink https://escholarship.org/uc/item/5w97g2x7

Authors Morgan, SG Goy, JW Costlow Jr, JD

Publication Date 2021-06-27

Peer reviewed

eScholarship.org Powered by the California Digital Library University of California Effect of Density, Sex Ratio, and Refractory Period on Spawning of the Mud Crab Rhithropanopeus harrisii in the Laboratory Author(s): Steven G. Morgan, Joseph W. Goy, John D. Costlow and Jr. Source: Journal of Crustacean Biology, Vol. 8, No. 2 (May, 1988), pp. 245-249 Published by: {brill} on behalf of The Crustacean Society Stable URL: http://www.jstor.org/stable/1548316 Accessed: 02-04-2015 12:23 UTC

REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/1548316?seq=1&cid=pdf-reference#references_tab_contents

You may need to log in to JSTOR to access the linked references.

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

The Crustacean Society and are collaborating with JSTOR to digitize, preserve and extend access to Journal of Crustacean Biology. http://www.jstor.org

This content downloaded from 128.120.194.195 on Thu, 02 Apr 2015 12:23:16 UTC All use subject to JSTOR Terms and Conditions JOURNAL OF CRUSTACEAN BIOLOGY, 8(2): 245-249, 1988

EFFECT OF DENSITY, SEX RATIO, AND REFRACTORY PERIOD ON SPAWNING OF THE MUD CRAB RHITHROPANOPEUSHARRISII IN THE LABORATORY

Steven G. Morgan, Joseph W. Goy, and John D. Costlow,Jr.

ABSTR ACT Adult mud crabs, Rhithropanopeusharrisii, were held in the laboratoryfor 14 months at densities of 20 or 40 crabs per 0.5 m2 and at female: male ratios of 2:1, 4:1, and 6:1. Females spawnedfor 9 months duringthe calendaryear and entereda refractoryperiod from November throughJanuary. Field populationsin North Carolinaspawn for only 5 months of the year. Spawningincreased with increasingcrab density and female: male ratio. Ovigers were most abundantin habitats containing 40 crabs at a 6:1 sex ratio (8.3 ovigers per week), and were least abundantin habitatscontaining 20 crabsat a 2:1 ratio(2.8 perweek). However, the highest proportionof crabs spawnedin habitatscontaining 20 crabsat a 6:1 sex ratio. Neither density nor sex ratio affectedfemale mortality.Crabs at the lowest sex ratio (2:1) and highest density (40 crabs) producedlarvae that survived poorly (45% survival to first crab stage). However, larvalviability was good at all otherdensities and sex ratios.Maintaining crabs at high densities and female: male sex ratiosin the laboratory,even duringa portionof the nonbreedingseason, augmentedegg production.These methods can facilitate studies of reproductionand devel- opment of R. harrisii. Temperate brachyuran crabs generally at 25?C,and larval survival is consistently breed only in summer. However, the mud high at about 85-90% (Costlowet al., 1966). crabRhithropanopeus harrisii Gould and the Individuals of Rhithropanopeusharrisii stone crab Menippe mercenaria Say have spawn repeatedlyfrom April to September been induced to mate and spawn during in North Carolina estuaries. Females may winter under laboratory conditions (Mc- oviposit up to four times after a single mat- Conaugha et al., 1980; Goy et al., 1985). ing, requiring3-7 days to spawn again after Rhithropanopeusharrisii is a small, eury- hatching(Morgan et al., 1983). Rhithropan- haline crab that occurs in estuaries from opeus harrisii was induced to spawn into New Brunswick,Canada, to Veracruz,Mex- December by maintainingthem in the lab- ico, and northeasternBrazil. The speciesalso oratory at 24?C and under a 12:12 h day: has been introduced to Coos Bay, Oregon, night photoperiod(Goy et al., 1985). In this San Francisco Bay, California, northwest study, we investigated the duration of re- Europe,and the BlackSea (Williams, 1974). productiveactivity ofR. harrisiithroughout Perhapsthere have been more studies of the the year under laboratoryconditions, and reproductiveand developmental biology of the effect of density and female: male sex R. harrisiithan of any other crab.The nearly ratio on spawning.Both maximization and 100 laboratorystudies of the larval biology efficiency of spawning are considered. The ofR. harrisiiinclude investigationson tem- highestreported natural densities of R. har- peratureand salinity responses (Costlow et risii, 40 crabs/m2(Odum and Heald, 1972), al., 1966), toxicity (Laughlinet al., 1983), is between the densities used in this study. chromatophores (Pautsch, 1967), molting (Freemanand Costlow, 1984), regeneration METHODSAND MATERIALS et (Freeman, 1983), biochemistry (Sanders Adult mud crabs were collected occasionally from al., 1984), predation(Morgan, 1987), larval the Neuse River estuary,North Carolina,from April behavior (Forwardet al., 1986), and larval to August1980 and April through May 1981,and placed release (Rittschoff et al., 1985). The com- in a large(60 x 180 x 50 cm) holding tank. Artificial mon, robust adults spawn frequently and "habitats"were stockedon 1 May 1980 at densities of are to collect and maintain. The larval 20 or 40 crabs(29 or 58/m2),and at female: male ratios easy of approximately 2:1 (14:7, 27:13), 4:1 (16:4, 32:8), development of R. harrisii is brief, taking and 6:1 (18:3, 35:6). Habitats were off-white copolymer approximately17 days to the firstcrab stage tubs (58.5 x 58.5 x 63.5 cm) equipped with under-

245

This content downloaded from 128.120.194.195 on Thu, 02 Apr 2015 12:23:16 UTC All use subject to JSTOR Terms and Conditions 246 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 8, NO. 2, 1988

Table 1. Spawning,mortality, and larval viability of overwintered Rhithropanopeus harrisii maintained at various stocking densities and sex ratios.

Density (crabs/habitat) 20 40 Sex ratio (females: males) 2:1 4:1 6:1 2:1 4:1 6:1 Mean spawning/week Number ovigerous 2.8 + 1.4 4.2 + 1.9 5.7 + 1.1 5.4 + 2.2 7.5 + 3.1 8.3 + 2.1 Percent ovigerous 20 + 10 26 + 12 32 + 6 20 + 8 23 + 10 24 + 6 Mean mortality/week(missing or dead) Number females 2.7 ? 2.0 2.4 + 2.6 2.5 + 2.7 3.5 + 2.8 4.8 + 3.6 5.3 + 3.4 Per cent females 20 + 14 15 + 16 14 + 15 15 ? 12 15 + 11 15 + 10 Number males 1.2 + 1.2 0.2 + 0.4 0.5 + 0.8 1.7 + 1.9 0.6 + 0.8 0.7 + 0.6 Percent males 17 + 17 4 + 9 16 + 28 13 + 15 8 + 10 12 + 11 Larvalviability Number hatchesreared 13 11 11 4 10 9 Mean % survival to megalopa 91 + 6 88 + 22 88 + 6 61 + 24 84 + 15 88 + 19 Mean % survival to crab 89 + 7 86 + 23 87 + 9 45 + 21 74 + 18 84 + 24 Mean numberdays to megalopa 12.5 + 0.9 12.7 + 1.1 12.5 + 0.7 13.0 + 0.4 12.4 + 0.7 12.4 + 0.5 Mean numberdays to crab 19.0 + 1.1 18.9 + 1.4 19.0 + 1.4 18.6 + 0.8 18.1 + 1.0 17.6 + 0.5

gravelfilters, air pumps, and submersibleheaters. A 4 RESULTS cm deep layer of crushed and unbrokenoyster shell was placed in each habitat.A 14:10 h day: night pho- In 1980 and 1981 the breeding seasons toperiodwas providedby 4 fluorescentbulbs placed 1 of R. harrisii in the Neuse River estuary m above the bottom of each habitat. Watertempera- lasted for approximately five months, from tureswere maintainedat 30 and salinitieswere + 1?C, mid-April to the end of September. Breed- kept at approximately12%oo. The habitatswere cleaned and the water was changedbiweekly. Crabs were fed ing by crabs in the laboratory was extended weekly on Ralston Purina Marine Ration no. 25 and by approximately four months. Crabs daily on San FranciscoBay brand (lot no. 3288) Ar- stopped breeding in the laboratory from 5 temia. The diet was occasionally supplementedwith November 1980 until 6 January 1981. The minced clams and fish. number of females declined The habitatswere checkedweekly from 8 May 1980 gravid gradu- until 2 July 1981. Ovigerouscrabs were removed and ally from mid-September through October placed individually in 8 cm diameter culture dishes before crabs entered the refractory period. containing 12%osea water until their eggs hatched. One crab produced eggs on 6 January 1981, Gravid females and missing or dead crabs were re- but a of females placed with crabs of the same sex and approximately steady supply ovigerous the same size to maintain the initial sex ratios and was not obtained until 27 January 1981. densities. These replacementscame from crabs col- More clutches were spawned by crabs lected from the field and maintainedin the largehold- maintained at a higher density and female: ing tank, as well as from gravid females that had pre- male ratios than the lower ones (Tables 1, viously hatchedtheir eggs. The number of clutches Fifty zoeae from each hatchwere rearedunder a 12: 2). produced per 12 h day: night photoperiod.Ten zoeae were placed week was significantly different (SNK, P < in each of five 3.5-cm diameterbowls filled with sea 0.05) for all sex ratios tested. Approxi- waterof 30?Cand 20%o,which was changeddaily. Lar- mately eight females spawned per week at vae were fed daily with an excess of freshly hatched the combinations of and sex San FranciscoBay brand(lot no. 3288) nauplii of Ar- higher density temia. Larval molts and deaths were recordeddaily ratio (40 crabs, 4:1 and 6:1), whereas only until the zoeae metamorphosedto the firstcrab stage. about three spawned per week at the lowest Resultswere compared by analysisof variance(AN- (20 crabs, 2:1). Approximately 20-30% of OVA). When there was not a significantinteraction the females spawned per week (Table 1). betweenthe main effects,the Student-Newman-Keuls Females stocked at the two female: (SNK) means comparisonprocedure was used to test higher for significantdifferences between the sex ratio treat- male ratios (6:1, 4:1) produced a signifi- ments. cantly greater (SNK, P < 0.05) proportion

This content downloaded from 128.120.194.195 on Thu, 02 Apr 2015 12:23:16 UTC All use subject to JSTOR Terms and Conditions MORGAN ETAL.: SPAWNING OF OVERWINTERED RHITHROPANOPEUS 247 of clutches than those at the lower sex ratio. Table 2. ANOVA of spawning,mortality, and larval The of crabs at viability of overwintered Rhithropanopeusharrisii highest proportion spawned maintainedat variousstocking densities and sex ratios. the lowest density (20 crabs)and highest sex Percentagesarcsin-tranformed; * indicatessignificance ratio (6:1). at P < 0.05. Mortality of females (2.4-5.3 per week) was at the Source of greater higher density (40 crabs), p variation d.f MS F P but the percentage of dead females (14-20% per week) was not significantlydifferent be- Number, ovigers tween treatments Sex ratio did Density 1 161.528 43.357 <0.001* (Tables 1, 2). Sex ratio 2 61.277 16.448 <0.001* not have a significanteffect on female mor- Interaction 2 1.090 0.292 0.747 tality (Tables 1, 2). Error 83 3.726 The patternof male mortalitywas similar Percentage,ovigers to that of females. Mortality of males was Density 1 0.026 1.638 0.204 greaterat the higher density (although not Sex ratio 2 0.102 6.465 0.002* quite significant at P < 0.05) than at the Interaction 2 0.020 1.279 0.284 lower density, and the percentageof dead Error 83 0.016 males was similarbetween the two densities Number, dead females (Tables 1, 2). However, mortality of males Density 1 82.669 10.661 0.002* was P < at the lowest Sex ratio 2 1.878 0.242 0.785 greatest(SNK, 0.05) Interaction 2 8.655 1.116 0.332 female: male ratio (2:1), and the proportion Error 83 7.755 of dead males in habitats stocked at the low dead females sex ratiowas significantlygreater (SNK, P < Percentage, Density 1 0.003 0.059 0.809 0.05) than at the intermediate(4:1) but not Sex ratio 2 0.012 0.225 0.799 at the highest (6:1) sex ratio (Tables 1, 2). Interaction 2 0.048 0.928 0.400 Larval viability was usually good regard- Error 83 0.051 less of the crab density or sex ratio at which Number, dead males the clutches were spawned (Table 1). How- Density 1 3.933 3.725 0.057 ever, crabs at the lowest sex ratio (2:1) and Sex ratio 2 8.811 8.344 <0.001* highest density (40 crabs) produced larvae Interaction 2 0.184 0.174 0.840 that survived poorly (Table 2). Larvaefrom Error 83 1.056 all treatments required similar lengths of Percentage,dead males time to metamorphose to megalopae, but Density 1 0.020 0.229 0.634 the larvae of crabs that were maintained at Sex ratio 2 0.304 3.412 0.038* Interaction 2 0.041 0.459 0.634 the higher density (40 crabs) took less time Error 83 0.089 to to first crab than metamorphose stage Percentage,survival to a those at the lower 1, megalop; density (Tables 2). Density 0.138 3.036 0.087* 2 DISCUSSION Sex ratio 0.025 0.553 0.579 Interaction 2 0.171 3.765 0.030* The length of the breeding period of R. Error 522 0.045 harrisiiwas nearlydoubled by inducingcrabs Percentage,survival to crab to spawn in the laboratorylater in the fall Density 1 0.497 10.612 0.002* and earlier in the spring.The breeding sea- Sex ratio 2 0.074 1.579 0.216 son of the Neuse River of R. Interaction 2 0.261 5.570 0.006* population Error 52 0.047 harrisiiextends from mid-April to late Sep- tember, but in the laboratorycrabs spawned Durationto megalopa for an additional four months and entered Density 1 0.028 0.041 0.840 Sex ratio 2 0.144 0.213 0.808 a refractory phase only from November Interaction 2 0.753 1.113 0.336 throughJanuary. Error 52 0.677 The onset of the refractoryperiod of R. Durationto crab harrisiioverwintered in the dur- laboratory Density 1 11.505 8.751 0.005* ing the presentstudy is similar to that found Sex ratio 2 0.415 0.316 0.731 for a subtropical population of R. harrisii Interaction 2 0.853 0.649 0.527 in the St. Johns River estuary, Florida, al- Error 52 1.315 though zoeae have been collected as late as November in Florida (Tagatz, 1968). How-

This content downloaded from 128.120.194.195 on Thu, 02 Apr 2015 12:23:16 UTC All use subject to JSTOR Terms and Conditions 248 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 8, NO. 2, 1988

ever, Goy et al. (1985) found that crabscol- betweenall treatments,mortality of females lected from the Neuse River, North Caro- need not be considered when selecting the lina, in 1979 and held at 24?C in the density and sex ratio for a laboratorypop- laboratorydid not become reproductively ulationof crabs.However, mortality of crabs quiescent until after mid-December. The might be reduced and spawningof females lateronset of the refractoryperiod may have increasedif additionalfood and refugewere been a resultof the lowertemperature (24?C) provided. at which the crabswere maintained. Goy et The mean survival and durationof larvae al. (1985) maintained 45 crabs per habitat of R. harrisiiin the presentstudy were com- (same dimensions as used in this study) at parableto those of larvaehatched from crabs a 2:1 female: male ratio; these crabs pro- that spawnedin the wild duringthe normal duced a mean of 4.3 clutches per week. In breedingseason (Costlow et al., 1966). Thus, the present study, 5.3 clutches were pro- the viability of embryos and larvae was not duced per week by only 40 crabsat the same affected adversely by maintaining crabs in sex ratio and at 30?C. The higher temper- the laboratoryover a long period of time. atures at which the crabs were maintained However, low survival of larvae was ob- duringthe currentstudy may have increased served for crabs maintained at the highest reproductiveoutput, thereby depleting the density and lowest female: male sex ratio. energyreserves more quickly and initiating The poor survivalmay have been an artifact an earlieronset of the refractoryperiod pro- of the low number of hatches reared(four), vided that crabs were not well fed. but Goy et al. (1985) also obtained low sur- Spawningcan be increased simply by in- vival (69%) for R. harrisii maintained at a creasingcrab density and female: male ratio similar density and sex ratio. It is possible in the laboratory.Thus, ovigers were most that the combination of crowding and the abundantin habitatscontaining 40 crabs at high abundance of males in this treatment a 6:1 sex ratio (8.3 ovigers per week), and resulted in more stressfulbehavioral inter- were least abundant in habitats containing actions for females, lower food intake, and 20 crabsat a 2:1 ratio (2.8 per week). How- less yolk for embryos.The durationof larval ever, the difficultyin maintainingartificially development to megalopa was similar be- elevated populations in the laboratory re- tween treatments, but inexplicably devel- sides in the ability to collect females, since opment to first crab stage took longer for the sex ratio of natural populations in the those larvaespawned by females in the least Neuse River estuaryis 1:1.Investigators en- crowded conditions. countering difficulty in collecting females The maintenance of a reproducingpop- should consider maintaining laboratory ulation of R. harrisii in the laboratory is populationsat the highestsex ratio (6:1) and efficientand economical.Egg production can lowest density (20 crabs) due to the high be increasedby stocking crabs at high den- spawningefficiency. sities with a greatly disproportionatenum- Spawningwas greatestwhen males were ber of females. Furthermore,experimenta- least abundant,perhaps because a few males tion on the reproductiveand developmental can mate with many females, and because biology of temperate populations of crabs males apparentlykill females as well as each need not be restrictedto summer months. other. Males are largerand more aggressive The beginningand end of the refractorype- than females, which would be particularly riod may be manipulated by controlling vulnerable to attack while molting. The photoperiodand temperature.Such manip- mortality rate of females may have in- ulation may be useful for studies of the en- creased as the density of males increased. docrinologyof decapod reproduction. The increasedue to the concomitant rise in the numberof females was therebyoffset by ACKNOWLEDGEMENT the higher mortality rate. Mortality of fe- We thank John Christy for commenting on the males also was greaterat the higherdensity manuscript. simply because more females were present; the percentageof dead females was not de- LITERATURE CITED pendent on the stocking density. Because Costlow, J. D., Jr., C. G. Bookhout, and R. J. Monroe. the proportionof dead females was similar 1966. Studies on the larval development of the crab,

This content downloaded from 128.120.194.195 on Thu, 02 Apr 2015 12:23:16 UTC All use subject to JSTOR Terms and Conditions MORGAN ETAL.: SPAWNING OF OVERWINTERED RHITHROPANOPEUS 249

Rhithropanopeusharrisii (Gould). I. The effect of Odum,W. E., and E. J. Heald. 1972. Trophicanalyses salinity and temperatureon larval development.- of an estuarinemangrove community. -Bulletin of PhysiologicalZoology 39: 81-100. MarineScience 22: 671-738. Forward,R. B., Jr., J. K. Douglass,and B. E. Kenney. Pautsch,F. 1967. Pigmentationand color change in 1986. Entrainmentof the larval release rhythm of decapod larvae. Proceedingsof the Symposium on the crab Rhithropanopeusharrisii (Brachyura: Xan- Crustacea,Erakulam, Marine Biological Associa- thidae)by cyclesin salinitychange. -Marine Biology tion of India, Part III, series 2, pp. 1108-1123. 90: 537-544. Rittschoff, D., R. B. Forward,Jr., and D. D. Mott. Freeman,J. A. 1983. Spine regenerationin larvae of 1985. Larval release in the crab Rhithropanopeus the crab, Rhithropanopeusharrisii. -Journal of Ex- harrisii(Gould): chemical cues fromhatching eggs. - perimentalZoology 225: 443-448. ChemicalSenses 10: 567-578. ,and J. D. Costlow,Jr. 1984. Endocrinecon- Sanders,B. M., J. D. Costlow, K. D. Jenkins,and T. trol of apolysisin Rhithropanopeusharrisii larvae. - Marshall. 1984. The effects of varying cupric ion Journalof CrustaceanBiology 4: 1-6. activities on copper uptake and cytosolic distribu- Goy, J. W., S. G. Morgan,and J. D. Costlow,Jr. 1985. tion and growth in crab larvae.-Marine Environ- Studieson the reproductivebiology of the mud crab, mental Research 14: 476-477. Rhithropanopeus harrisii (Gould): induction of Tagatz,M. E. 1968. Biology of the blue crab, Calli- spawningduring the non-breedingseason (Decapo- nectessapidus Rathbun, in the St. Johns River, Flor- da, Brachyura).-Crustaceana49: 83-87. ida.-Fishery Bulletin,United States 67: 17-33. Laughlin, R., W. French, and H. E. Guard. 1983. Williams,A. B. 1974. Crustacea:Decapoda. Marine Acute and sublethal toxicity of tributylin oxide floraand faunaof the northeasternUnited States.- (TBTO)and its putativeenvironmental product, tri- NOAA Technical Report, NMFS Circular398: 1- butylin sulfide (TBTS) to zoeal mud crabs, Rhith- 49. ropanopeusharrisii. -Water, Air and Soil Pollution 20: 69-80. RECEIVED:27 January 1987. ACCEPTED:5 October 1987. McConaugha,J. R., K. McNally,J. W. Goy, and J. D. Costlow, Jr. 1980. Winter induced mating in the stone crab,Menippe mercenaris. -Proceedings of the Addresses:(SGM) Duke University Marine Labo- World MaricultureSociety 11: 544-547. ratory, Beaufort,North Carolina28516 and (current S. G. 1987. Morphologicaland behavioral address)Smithsonian Tropical Research Institute, Box Morgan, of antipredatoryadaptations of decapodzoeae. - Oeco- 2072, Balboa,Republic Panama;(JWG) Duke Uni- Marine North Carolina logia 73: 393-400. versity Laboratory,Beaufort, ,J. W. Goy, and J. D. Costlow,Jr. 1983. Mul- 28516 and (currentaddress) Department of Biology, TexasA & M Texas tiple ovipositions from single matings in the mud University,College Station, 77843; crab Rhithropanopeusharrisii. -Journal of Crusta- (JDC) Duke University MarineLaboratory, Beaufort, North Carolina28516. cean Biology 3: 542-547.

ANNOUNCEMENT

"Les Pylochelidae ou 'Pagures symetriques' (Crustacea Coenobitoidea)" by J. Forest, Museum National d'Histoire Naturelle, Paris, has been published (1987) in Resultats du Campagne MUSORSTOM, 3.A, volume 137, pages 1-254, with 9 plates. ISSN 0078- 9747. This publication is available from: Editions du Museum, 38 rue Geoffroy Saint-Hilaire, 75005 Paris, France. The price is 300 FF.

This content downloaded from 128.120.194.195 on Thu, 02 Apr 2015 12:23:16 UTC All use subject to JSTOR Terms and Conditions