Chu and Chow Effect Unilateral and Bilateral Ablation

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Effects of Unilateral versus Bilateral Eyestalk Ablation on Moulting and Growth of the

Shrimp, Penaeus chinensis (Osbeck, 1765) (Decapoda, Penaeidea)Author(s): K. H. Chu and W. K. ChowSource: Crustaceana, Vol. 62, No. 3 (May, 1992), pp. 225-233Published by: BRILLStable URL: http://www.jstor.org/stable/20104749 .

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Crustaceana 62 (3) 1992, E. J. Brill, Leiden

EFFECTS OF UNILATERAL VERSUS BILATERAL EYESTALKABLATION ON MOULTING AND GROWTH OF THE SHRIMP,PENAEUS CHINENSIS (OSBECK, 1765) (DECAPODA, PENAEIDEA)

BYK. H. CHU and W. K. CHOW

Department of Biology, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong

RESUMELa crevette Penaeus chinensis a ?t? soumise ? une ablation uni- ou bilat?rale des p?doncules ocu

laires. La dur?e du cycle de mue et l'accroissement en longueur de la carapace ont ?t? suivisau cours d'ecdysies successives. Des animaux intacts ont ?t? utilis?s comme t?moins. Les deuxop?rations ont raccourci le cycle de mue au cours des premi?re et seconde mues apr?s le traite

ment, l'effet de l'ablation bilat?rale ?tant plus prononc?, au moins pendant la premi?re mue.Ceci sugg?re une s?cr?tion faiblement ou non compensatoire de l'hormone inhibant lamue parle p?doncule non amput?, pendant cette p?riode. Aucune crevette ?p?doncul?e n'a surv?cu ?la troisi?me mue apr?s le traitement. Dans les troisi?mes et quatri?mes mues post-op?ratoires,la dur?e du cycle d'une crevette ayant subi une ablation unilat?rale ne diff?rait pas de fa?onsignificative de celle des animaux-t?moins non-?p?doncul?s, ceci sugg?rant une possible s?cr?tion hormonale compensatoire, qui peut ?tre fournie par le p?doncule restant ou par d'autresm?canismes de contr?le de lamue. En dehors d'un pourcentage d'accroissement de la longueurde la carapace significativement plus ?lev? chez les crevettes ?p?doncul?es que chez les t?moins,? la premi?re mue post-op?ratoire, il n'y avait pas de diff?rences significatives dans la croissanceparmi les groupes dans toutes les mues ?tudi?es. La grande variabilit? individuelle dans la croissance a limit? les possibilit?s de comparaison pr?cise entre les groupes.

INTRODUCTIONThe neuroendocrine control of moulting has interested crustacean biologistsfor many decades (Passano, 1960; Chang &O'Connor, 1988). The idea of amoult inhibiting hormone (MIH) secreted by the X-organ sinus gland complex

within the eyestalk has generally been accepted (Skinner, 1985; Chang &O'Connor, 1988). Studies on the effect of eyestalk ablation on the moult cyclehave been primarily concerned with the removal of both eyestalks (e.g.,Nakatani & ?tsu, 1979; Quackenbush & Herrnkind, 1981; Webster, 1985;Synder & Chang, 1986; Koshio et al., 1989; Chu & Leong, 1991), whichpresumably eliminates the MIH, leading to precocious moulting. Nevertheless, the effect of unilateral eyestalk ablation on the moult cycle has beeninvestigated in the penaeids, commonly in conjunction with its effect onovarian maturation (e.g., Browdy & Samocha, 1985; Browdy et al., 1986;Choy, 1987). Removal of both eyestalks was seldom adopted in these studies


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226 K. H. CHU & W. K. CHOWas the high mortality of eyestalkless shrimp would hamper the applicability ofbilateral ablation in controlling maturation for aquacultural purposes. In thesestudies, unilateral eyestalk ablation was found to induce ovarian maturationas well as precocious moulting, suggesting that the unablated eyestalk fails tocompensate for the hormonal secretion by its lost partner. Thus, a lower levelof MIH and gonad inhibiting hormone (GIH) in shrimps with a single eyestalkresults in precocious moulting and ovarian maturation. There are, however,few studies which simultaneously compare the effects of unilateral and bilateraleyestalk ablation on moulting. Two recent studies have yielded inconsistentresults. Molyneaux & Shirley (1988) showed that bilateral, but not unilateral,ablation significantly shortens the moult cycle of the crab, Paralithodes camtschaticus (Tilesius, 1815). However, Chan et al. (1990) demonstrated in Penaeusvannamei Boone, 1931, that both operations result in precocious moulting, butthe effect of unilateral ablation is less pronounced. In both studies only one

moult cycle was followed after eyestalk removal.The objective of the present study is to compare the effect of unilateral andbilateral eyestalk ablation on the moult cycle of the shrimp, Penaeus chinensis(Osbeck, 1765) (formally P. orientalis Kishinouye, 1918). The efficacy ofbilateral ablation in shortening the moult cycle duration of this penaeid hasbeen demonstrated by Chu & Leong (1991), who also suggested that penaeidjuveniles serve as a good system in examining the effects of eyestalk removalbecause of the short moult cycle duration of the animals. The same suggestionhas been made by Chan et al. (1990), who noted other advantages of theshrimp, viz., that they are easily reared in the laboratory and can survive the

moult after eyestalk ablation. In the present study the moult cycle duration andgrowth increment were determined in shrimp after unilateral and bilateraleyestalk ablation. Attempts were made to follow several consecutive moultsafter the operations.

MATERIALS AND METHODSPenaeus chinensis used in this study were hatchery-reared in the Marine

Science Laboratory of the Chinese University of Hong Kong. Juveniles of abody weight of 1.1 to 1.3 g were taken for the experiment. The small rangein the size of animals used would minimize the variation in moult cycle duration. Shrimp were introduced into a water-table that was divided into compartments with perforated perspex plates. Each shrimp was housed in anindividual compartment measuring 9.5

cm x 13.5 cm, and the water depthwas kept at about 10 cm. The water was well aerated and its flow was maintained using a recirculating and filtering system (EHEIM canister filter model1034) with a flow rate of 2160 1 h'1. The turnover time of seawater in thewater-table was about 5 min. Further, about 1/3 of the water was renewedevery three days. Throughout the experimental period, the range of


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EYESTALK ABLATION IN PENAEUS 227temperature and salinity of the seawater was 21-25?C and 30-330/qo, respectively. Shrimp were fed daily with freeze-dried krill or fresh oysters at a rationof about 20% of the body weight.

Shrimp were allowed to moult once in the water-table. Eyestalks wereremoved the day after ecdysis using the cautery method. For shrimp with botheyestalks ablated, the second eyestalk was removed a few hours after removingthe first one. Intact shrimp acted as control.

Shrimp were inspected daily for mortality and moulting. On the third dayafter ecdysis, when the exoskeleton of the shrimp had been hardened (Chu etal., 1988), the carapace length (distance from the posterior orbital margin tothe posterior edge in the mid-dorsal line) of the shrimp was measured with apair of calipers to the nearest 0.1 mm.

RESULTSThe survivorship of shrimp is shown in fig. 1. It should be noted that shrimp

which died before the first postoperative ecdysis were excluded from analysis,and hence apparently no mortality occurred during the first ten days of thestudy. Fig. 1 shows that eyestalkless shrimp sustained a higher mortality thananimals with a single eyestalk or the intact controls. All eyestalkless animalsdied within 40 days after treatment and none of them moulted for a third timeafter ablation. There appeared to be little differences in mortality betweenshrimp with a single eyestalk and the intact controls until the final days of theexperiment.

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20 30 40 50DAYS AFTER TREATMENT

Fig. 1. Survival of Penaeus chinensis which succeed to moult once after eyestalk ablation. A,bilateral eyestalk ablation (n = 28); B, unilateral eyestalk ablation (n = 23); C, intact control(n-23).


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228 K. H. CHU & W. K. CHOW

D 28A 23O 23

DAYS AFTER ECDYSISFig. 2. Cumulative moulting frequency o?Penaeus chinensis at four consecutive moults, I, II, IIIand IV, after eyestalk ablation. Squares, bilateral eyestalk ablation; triangles, unilateral eyestalkablation; circles, intact control. The number of individuals in each group which completed the

moult is indicated to the right of the figure.

In the first two moult cycles after treatment, the cumulative percentage ofmoulted shrimp at a given time was higher in the eyestalk ablated groups than

the intact controls (fig. 2). Further, the eyestalkless animals started to moultearlier than the single eyestalk ablated animals. While the difference between


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EYESTALK ABLATION IN PENAEUS 229Table I

Duration of consecutive moult cycles after unilateral and bilateral eyestalkablation in Penaeus chinensisMoultcyclentact Unilateral Bilateralafter treatment control ablationblation

I12.0?2.1a(23) 10.5 ? 1.4b(23) 9.6 ? 1.7C(28)II13.8?3.3a(14) 11.6 ? 2.0b(18) 9.8?1.0b(4)III6.7 ?2.8 (12) 14.8 ?3.4 (13)-IV7.3 ?3.1(6) 16.4 ?3.0 (7)-Values are expressed as mean ? S.D. (no. of individuals). Values with different alphabets inthe same row are significantly different (P0.05; Student'st test).

single eyestalk ablated animals and the controls appeared to persist in the thirdmoult cycle after treatment, this difference was not evident in the last moultcycle studied. Statistical analysis (table I) showed that in the first twopostoperative moults, the moult cycle duration of shrimp in the two eyestalkablated groups was significantly shorter than that of intact controls (P0.05; Tukey Test after 1-wayANO VA), nor between the single eyestalk ablated animals and the controls inthe third and fourth moults (P>0.05; Student's / test). There also seemed tobe a progressive increase inmoult cycle duration within each group from one

moult to the other.As shown in fig. 3, the percentage increase in carapace length of eyestalkless

shrimp was significantly higher than that of controls in the first moult aftertreatment (P0.05, 1-way ANOVA or Student's t test).

DISCUSSIONThe high mortality of Penaeus chinensis after bilateral eyestalk ablation is in

agreement with most studies on eyestalk ablated crustaceans, which rarely survived three moults after the operation (Mauviot & Castell, 1976; Nakatani &Otsu, 1979; Trider et al., 1979; Freeman et al., 1983). The stress of eyestalk


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230 K. H. CHU & W. K. CHOW12

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EYESTALK ABLATION IN PENAEUS 231ing eyestalk in the single eyestalk ablated animals. This hypothesis can also beinterpreted to be in line with the well-documented observation in many

penaeids, including P. chinensis, that unilateral eyestalk ablation inducesovarian maturation (Arnstein & Beard, 1975; see Primavera, 1985, forreview), as presumably there would be no compensatory secretion of gonadinhibiting hormone from the unablated eyestalk. It has also been demonstratedin some of these studies that unilateral eyestalk ablation also results in

precocious moulting (Browdy & Samocha, 1985; Browdy et al., 1986; Choy,1987). There have been few studies on the effect of unilateral eyestalk ablationin other groups of crustaceans. The lack of compensatory hormonal secretionfrom a single eyestalk has also been proposed by Molyneaux & Shirley (1988),but, although the reduction inmoult cycle duration which they reported in thecrab, Paralithodes camtschaticus, (12 and 24% in single and double eyestalkablated groups, respectively) is comparable to the results of our study, thereduction in the single eyestalk ablated group is not statistically different fromeither the intact or the double eyestalk ablated group. The discrepancy maysimply be due to a greater variation inmoult cycle duration in the crab, whichresults from a wider size range of the animals studied.

In the present study, the reduction in the moult cycle duration of singleeyestalk ablated shrimp, as compared to intact controls, progressivelydecreased from 16% in the second postoperative moult to 11% and 6% in thethird and fourth moults (table I). This finding indicates that there is a compensatory secretion of moult inhibiting hormone after a time lag; yet it is notapparent whether such secretion originates from the unablated eyestalk sinceeyestalkless shrimp did not survive long enough for comparison. It has beensuggested that moulting is controlled by mechanisms other than the Xorgan?sinus gland?Y-organ axis (Chang & O'Connor, 1988), so that activation of these alternative mechanisms may also account for the diminishingeffect of unilateral eyestalk ablation in consecutive moults.

The present study also showed that in P. chinensis bilateral eyestalk ablationincreases the growth increment in first ecdysis after treatment. This finding isconsistent with the observations in other crustaceans (Mauviot &Castell, 1976;Nakatani &?tsu, 1979; Freeman et al., 1983; Koshio et al., 1989). It has beensuggested that the increased moult increment is due to an increase in water

uptake and retention in eyestalkless animals (Passano, 1960; Charmantier etal., 1984; Jackson et al., 1987). In contrast to previous studies, however, thegreater size increase of eyestalkless P. chinensis at ecdysis was not evident in thesecond postoperative moult. The reason is unclear although it should be notedthat with the small size of animals used in this study and considerable variationin growth increment among the individuals, small differences in the increasein carapace length can hardly be discerned. In our study no growth incrementcan be observed in single eyestalk ablated shrimp. The effect of unilateral ablation on growth of penaeids appears to be controversial. In P. canaliculatus


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232 K. H. CHU & W. K. CHOW(Olivier, 1811) this operation results in a greater increment in size thanunablated controls (Choy, 1987), but a slower growth rate was reported in P.semisulcatus De Haan, 1844, after the treatment, despite a shortening of the

moult cycle (Browdy & Samocha, 1985; Browdy et al., 1986). Quackenbush &Herrnkind (1981) showed that in the spiny lobster, Panulirus argus (Latreille,1804), eyestalk ablation has different effects on the moult cycle duration ofanimals in different stages of sexual maturation. Similarly, the degree of

gonadal development may influence the effect of the operation on growthincrement. Further studies on the effect of eyestalk ablation on somatic growthand reproductive maturation are necessary to elucidate the interaction ofregulatory mechanisms of the two processes in the penaeids.

ACKNOWLEDGEMENTSThe authors thank Messrs. M. K. Cheung, K. C. Chung, Y. C. Tarn and

Ms. M. W. Fung for their technical assistance. Discussions with Mr. P. K.K. Leong throughout the study are appreciated. We are also grateful toMrs.Eleanor A. Miles for helpful comments on this manuscript. This research waspartially supported by a student research grant toW. K. Chow from theMingYu Visiting and Research Programme of New Asia College, The ChineseUniversity of Hong Kong.

LITERATURE CITEDArnstein, D. R. & T. W. Beard, 1975. Induced maturation of the prawn Penaeus orientalis

Kishinouye in the laboratory by means of eyestalk removal. Aquaculture, 5: 411-412.Browdy, C. L., A. Hadani, T. M. Samocha &Y. Loya, 1986. The reproductive performanceof wild and pond-reared Penaeus semisulcatus De Haan. Aquaculture, 59: 251-258.Browdy, C. L. &T. M. Samocha, 1985. The effect of eyestalk ablation on spawning, moultingand mating of Penaeus semisulcatus de Haan. Aquaculture, 49: 19-29.Castell, J. D., J. C. Mauviot &J. F. Covey, 1976. The use of eyestalk ablation in nutritionstudies with American lobsters (Homarus americanus). Proceedings of the WorldMariculture Society, 7: 431-441.Chan, K. M., S. M. Rankin & L. L. Keeley, 1990. Effects of 20-hydroxyecdysone injectionand eyestalk ablation on the moulting cycle of the shrimp, Penaeus vannamei. Com

parative Biochemistry and Physiology, 96 (A): 205-209.Chang, E. S. & J. D. O'Connor, 1988. Crustacea: Molting. In: H. Laufer & R. G. H.Downer (eds.), Endocrinology of Selected Invertebrate Types: 259-278. (Alan R. Liss,New York).Charmantier, G., M. Charmantier-Dauresm &D. E. Aiken, 1984. Neuroendocrine control

of hydromineral regulation in the American lobster, Homarus americanus H. MilneEdwards 1837 (Crustacea, Decapoda). General and Comparative Endocrinology, 54:8-19.Choy, S. C, 1987. Growth and reproduction of eyestalk ablated Penaeus canaliculatus(Olivier, 1811) (Crustacea: Penaeidae). Journal of Experimental Marine Biology and

Ecology, 112: 93-107.Chu, K. H., W. W. Cheng, K. M. Cheng &K. M. Leung, 1988. Characterization of moult

stages and changes in mineral levels in body tissues during the moult cycle of the shrimpPenaeus chinensis. Asian Marine Biology, 5: 25-33.


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EYESTALK ABLATION IN PENAEUS 233

Chu, K. H. & P. K. K. Leong, 1991. Effects of eyestalk ablation and limb amputation on themoult cycle of the shrimp Penaeus chinensis. Marine Behaviour and Physiology, 19:27-33.Fingerman, M., 1987. Endocrine mechanisms of Crustacea. Journal of Crustacean Biology, 7:1-24.

Freeman, J. A., T. L. West & J. D. Costlow, 1983. Postlarval growth in juvenileRhithropanopeus harrisii. Biological Bulletin, Marine Biological Laboratory, WoodsHole, 165: 409-415.

Jackson, S. A., M. J. Bruce, E. S. Chang & J. S. Clegg, 1987. Effects of eyestalk ablationupon water relations in the American lobster, Homarus americanus. Journal ofExperimental Zoology, 244: 389-393.

Koshio, S., L. E. Haley & J. D. Castell, 1989. The effect of two temperatures and salinitieson growth and survival of bilaterally eyestalk ablated and intact juvenile Americanlobsters, Homarus americanus, fed brine shrimp. Aquaculture, 76: 373-382.

Mauviot, J. C. &J. D. Castell, 1976. Molt- and growth-enhancing effects of bilateral eyestalkablation on juvenile and adult American lobsters (Homarus americanus). Journal of theFisheries Research Board, Canada, 33: 1922-1929.

Molyneaux, D. B. &T. C. Shirley, 1988. Molting and growth of eyestalk-ablated juvenile redking crabs, Paralithodes camtschatica (Crustacea: Lithodeidae). ComparativeBiochemistry and Physiology, 91 (A): 245-251.

Nakatani, I. &T. Otsu, 1979. The effects of eyestalk, leg, and uropod removal on the molting'

and growth of young crayfish, Procambarus clarkii. Biological Bulletin, Marine BiologicalLaboratory, Woods Hole, 157: 182-188.

Passano, L. M., 1960. Molting and its control. In: T. H. Waterman (ed.), The Physiologyof Crustacea, 1: 473-536. (Academic Press, New York).

Primavera, J. H., 1985. A review of maturation and reproduction in closed thelycum penaeids.In: Y. Taki, J. H. Primavera & J. A. Llobrera (eds.), Proceedings of the First International Conference on the Culture of Penaeid Prawns/Shrimps: 47-64. (South East AsianFisheries Development Center, Manila).

Quackenbush, L. S., 1986. Crustacean endocrinology, a review. Canadian Journal of Fisheriesand Aquatic Sciences, 43: 2271-2282.Quackenbush, L. S. &W. F. Herrnkind, 1981. Regulation of molt and gonadal developmentin the spiny lobster, Panulirus argus (Crustacea: Palinuridae): effect of eyestalk ablation.

Comparative Biochemistry and Physiology, 69 (A): 523-527.Skinner, D. M., 1985. Molting and regeneration. In: D. E. Bliss & L. H. Mantel (eds.), The

Biology of Crustacea, 9: 43-146. (Academic Press, New York).Synder, M. J. & E. S. Chang, 1986. Effects of eyestalk ablation on larval molting rates and

morphological development of the American lobster, Homarus americanus. BiologicalBulletin, Marine Biological Laboratory, Woods Hole, 170: 232-243.Trider, D. J., E. G. Mason &J. D. Castell, 1979. Survival and growth of juvenile Americanlobsters (Homarus americanus) after eyestalk ablation. Journal of the Fisheries ResearchBoard, Canada, 36: 93-97.

Webster, S. G., 1985. The effect of eyestalk removal, wounding and limb loss upon moultingand proecdysis in the prawn Palaemon elegans (Rathke). Journal of the Marine BiologicalAssociation of the United Kingdom, 65: 279-292.Zar, J. H., 1984. Biostatistical Analysis, (ed. 2). (Prentice Hall, London).

Received for publication 19 July 1991.

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