The changes in the histology of thoracic ganglion in females ofMacro-brachium lanchesteri, prior to spawning and post parturial moult, have been described. Based on the differences in size, cell inclusions and differential staining with CHP, four distinct types of neurosecretory cells have been identified in the ganglion. The activity of these cells has been correlated with the ovarian condition of the prawn and evidence for the elaboration of a gonad-stimulating hormone (GSH), by the ganglion has been derived. The, probable regulation of ovarian maturation during a normal ovarian cycle and that during the ovigerous condition ofM. lanchesteri have been illustrated

Katre Shakuntala, .

Narasimha Rao, C.H.

Ravichandra Reddy, S

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503Proc. tndian Acad. Sci. (Anim, Sci.), Vol. 90, Nwnbcr S, September 1981, pp. 503-511.© Printed in India.Studies on tbe neurosecretion of thoracic ganglion in relationto reproduction of female Macrobrachium lanchesteri (de Man)en NARASIMHA RAO, KATRE SHAKUNTALA andS RAVICHANDRA REDDYDepartment of Zoology. Bangalore University. Bangalore 560 056, IndiaMS received Z2 December 1980; revised ZS Aprll19lUAbstract. The changes in the histology of thoracic ganglion in females of Macro-brachium lanchesteri, prior to spawning and post parturial moult, have been des-cribed. Based on the differences in size, cell inclusions and differential staining withCHP, four distinct types of neurosecretory cells have been id.:ntmed in the ganglion.The activity of these cells has been correlated witb the ovarian condition of thePrawn and evidence for the elaboration of a gonad-stiDlulali118 hormone (GSH).by the ganglion has been derived. The probable regulatwn of ovarian maturationduring a normal ovarian cycle and that during the ovigerous condition ofM. lanchesteri have been illustrated.Keywords. Macrobrachium; thoracic gltng!ion; NSC; GSH; ovarian regulation.1. IntroductionThe neurosecretory cells (NSC) of the thoracic ganglion have been described toa considerable extent in reptantians (Enami 1951 ; Matsumoto 1954, 1958;Parameswaran 1956 ; Miyawaki 1960 ; Nagabhushanam and Ranga Rao 1966 ;Gorgees and Rashan 1917). However, similar studies on the natantian decapodsare meagre (Nagabhushanam and Vasantha 1972). Only recently, the types ofNSC have been described in the thoracic ganglion of two species of penaeids(Ramadan and Matta 1976).In brachyuran crustaceans, morphological (Matsumoto 1958, 1962) and experi-mental (Otsu 1963 ; Gomez 1965; Hinsch and Bennet 1979) evidences have indi-cated that the thoracic ganglion is the major site of neuroendocrine factors withgonad accelerating effects and this principle is generally termed the gonad-stimu-Iating hormone (GSH). In their review, Adiyodi and Adiyodi (1970) have pointedout that further critical studies are needed to confirm the suggestions of Otsu (1963)that in adult female crustaceans, GSH is produced even during the sexually quies-cent periods. While the exact nature and activity of the NSC during gonad matu-ration of natantians is notknown, some evidence for GSH activity has been indi-cated in Car/dina rajadhari (Shirwadkar 1977).504 Ol: Narasimha Rao, Katre Shakuntala .and S Ravichandra ReddyIn the ovigerous state, considerable amount of ovarian growth has been reportedin the freshwater natantian Macrobrachium lanchesteri even during the lull repro-ductive season (Rao et al 19&1). Presently, an attempt has been made to identifyand characterize the NSC of thoracic ganglion of M. lanchesteri and correlate theiractivity with the ovarian maturation.2. Material and methudsAdult females of M. Ianchesteri (de Man) were collected from the Agaram tank(near Bangalore) during April, May 1979. The prawns were stocked in the labora-tory, in glass aquaria containing aerated freshwater, at a temperature of26·6 ± 1'06°0. From this stock, active females (total length more than 35mm)were grouped into the following two stages; .Stage I. Premoult individuals prior to spawning; ovary occupying i of thecarapace area, with a number of maturing oocytes, measuring 7l l :63Jiin length (L) and 435-74 Ji in width (W) andStage II.. Prernoult individuals prior to the post parturial moult, after releaseof larvae; ovary indicating a number of growing oocytes, measuring357·83 Ji in Land 260'23 Jl in W.The ovarian histology in the above stages has been described by Rao et al1981.The thoracic ganglion of the above females were dissected out and fixed inBollin's fluid for purposes of histology. Paraffin sections cut at 6 Ji were stainedwith Bargman's chrome-haematoxylin (CHP) (Pearse 1977).3. Results and discussionA knowledge of the precise location of NSC in the thoracic ganglion of natantiansis a prerequisite for studying their nature and secretory activity. Figure 1 indi-cates the distribution of NSC in the thoracic ganglion of M. lanchestert. The NSCt.. - ...... . ~: .. "Figure 1. Macrobrachium lanchesteri : Diagrammatic representation indicating thedistribution of neurosecretory cell aggregations in the thoracic g1.nglion. DM-Dorsc-median; DV-Ventra-median; L-Latera1.Neurosecretion in M. lanchesterl 50$are aggregated into bilaterally arranged discrete groups along the mid-dorsal, mid-ventral and lateral regions. Very few cells are distributed in between these cellgroups and in the mid axis of the ganglion. This arrangement is in conformitywith that described for another natantian Caridina weberi (Nagabhushanam andVasantha 1972).It is most important to know the cytological details of each type of NSC, beforeattempting to study its physiological role. NSC can be easily distinguished fromordinary neurons, by the larger size, large nuclei and elaboration and dischargeof neurosecretory substance (NSS). Depending on the size, the NSC in the thoracicganglion of M. lanchesteri are classifled into four types, viz, A, B, C and D cells.A cells are largest in size, measuring 61' 6 J.l (SE = 5·23 ; n = 4) in diameter(figure 2a). These cells are comparable to the giant cell (Miyawaki 1960) andAIA' cells (Matsumoto 195& ; Nagabhushanam and Ranga Rao 1966) describedfor brachyuran crabs and A cells of the penaeid prawns (Ramadan and Matta 1976).These cells are generally round with ovoid nuclei (25' 611 in diameter; SE = I ·13 ;n =4). The cells are CHP positive. the NSS staining dark purple. A few reddishspherules are also found in the periphery of the cells.The second type-B cells arc medium sized (measuring 30'1 jJ. in diameter;SE = I: 52; n = 10) ; oval to pear-shaped with round or oval nuclei (16' 6 11 indiameter; SE = O'79 ; n = 10) having deeply stained chromatin bodies (figure2b). The NSS is CHP positive. Some cells display intense staining with CHP,the entire cytoplasm taking up dark; purple colour. These cell types are comparableto the median cells of brachyuran crabs (Miyawa!li 1960) and type B cells of Scyllaserrata (Nagabhushanam and Ranga Rao 1966).C cells are comparatively smaller in size, measuring 16·611 (SE = 1'31 ; n = 12)in diameter (figure 2c). They are round or Oval in shape. The cell boundaryof some is not so distinct as was described in penaeid prawns (Ramadan and Matta1976). In the periphery of thenucleus (12'Sp in diameter; SE = 0,62 ; n = 12).darkly stained, pinkish-red agglutinated chromatin is seen. These cells correspondto the type-VI cells described in the eyestalk of another freshwater prawn Palaemonpaucidens (Hisano 1914).The fourth type-D cells are the smallest, measuring 6·4 tl in diameter (figure 2d).They are either oblong or irregular in shape, without a distinct nucleus. The cellsstain red with CHP and sometimes small pinkish-red granules are observed insidethe cell. The cells are distributed throughout the thoracic ganglion ofM. lanchesteri. SUch cells have also been described in brachyurans, where nosecretory function has been attributed (Miyawakl 1960).Changes in the morphological and cytological characteristics of NSC in thethoracic ganglion of the two stages of M. lanchesteri in relation to ovarian matura-tion are represented in table 1. It is evident that while the A cells arc totally absentin the thoracic ganglion of I stage females. their presence is conspicuous in then stage. B, C and D types of cells are present in both the stages. Tho.ugh the Band Ccells and their nuclei increase in size and number there is no marked differencein either the cell number/size and/or cell inclusions in the D type of cells..The Band C cells of I stage females contained moderate CliP positive material,grey in colour and their nuclei included some light-pink chromatin granules. Inthis stage, the cells were distributed along the periphery of the thoracic ganglion,while only few cells were distributed as aggregations in the dorso-lateral regionsP. (8)-2506 Ch Narasimha Rao, Katre Shakuntala and S Ravichandra Reddy(figure 3). The cellular activity in this stage may represent a stage subsequent tothe active state of the thoracic ganglion where the' NSS (may be GSH ?) might havebeen used up by the maturing oocytes of the ovary.In M. lanchesteri.rei the end of the incubation period following spawning, theegg hatches out into a larva and subsequently, after releasing all the larvae, themother undergoes 'apost parturial moult.· During jhe ovigerous state, theimmatureova gradually Increase in their size due to fat-deposition and by the endof incubation period, before the post parturialmoult, the ovaries in the stage IIfemales, contain growing oocytes (Rao et a/ 1981). The NSC of the thoracicganglion in this stage exhibited a high secretory activity, the secretionsstaining dar1l1 purple with CHP.. Apart from this, the A cells showed few phlo-xinophil spherules in the periphery. The nuclei of A, Band Ccell types wereobserved to possess rich chromatin. In the n stage, the A cells were localized inthe ventro-lateral region, B cells dorso-medially and 'ventra-medially. Twoaggregations of C cells were distributed in the lateral region of the thoracic gang-lion (figure 3). The presence or absence of A cells, the increase in the cell number,size, nuclear diameter, staining intensity of B and C cells, in the II stage ascompared to that in I stage suggest the probable production of-increased NSS.A secretory activity and relative abundance of secretory substances in the gaint-Acells of the thoracic ganglion have also been reported in the ovigerous Paratelphusahydrodromous (Parameswaran 1956).The NSC activity observed in the thoracic ganglion of the above stages offemales, reflect the nature of their .elaboration and perhaps the production of GSH.From the above data, it is evident that there is continued production of GSH by theNSC of thoracic ganglion even in the ovigerous state ofM. lanchesterl, accountingfor the marked growth of oocytes in the stage II ovaries. This GSH might beacting {l) directly on the ovary in bringing about ovarian growth and/or (2) QJl themeintenance of secondary sexual characters, viz, plumose ovigerous setae and broodpouch. The present observations in M. lanchesteri provide evidence for thesuggestions of Adiyodi and Adiyodi (1970) that GSH promotes OOC) te growth.The extended ovigerous state of M. Ianchesteri represents the long, intermouljperiod when the Y-organ is suppressed in its. activity (Rao et a/ 1981). Thisfurther testifies the hypothesis of Adiyodi and Adiyodi (1970) that GSH mightabo be, responsible for the suppression of the Y-.organ. In the II stage femalesof M. lanchesteri, the GSH elaborated in the thoracic ganglion might be acting onthe secondary sexual characters mentioned above, probably through a sex hormoneproduced in the ovary. In this. connection, it is interesting to note that an' ovarianhormone (OB) produced in the amphipod, Orchestia gammarella, is klnown tocontrol similar secondary sexual characters (Charniaux...Cotton 1952, 1957).Presuming that a similar OH is elaborated by the ovary of M. lanchesteri, it is nowpossible to suggest that the GSH mediated ovarian growth/suppression of Y-organactivity, may be due to the cues provided by the sensory elements in the pleopods(figure 4 ; see also Passano 1960). It is interesting to note that GSH is producedin the thoracic ganglion of M. Ianchesteri in the lull reproductive season, and thisoffers the first histological proof to the statement of Otsu (1963).In the absence of cues from the sensory elements of the secondary sexual charac..ters, in the I stage females of M. lanchesteri, the extensive maturation of ovary canbe presumed to be due to the elaborate production of GSH (tram thoracic ganglion.\' ~.;:, ~,~,;,~,~~~~G.;:>:~i;-/;:;\"'..k\k~.:?,~.~:~,~.~ <t ~ ~ <"> ~ .... B" ;: -. ;: .~ [ "> ;:,- ~ ~ :::.l'igure2.Macrobrachuunlanchesteri;Neurosecretorycdt(NSC)tY,le;i.ithethoraclcganglion.(>;(50).A-DrepresentthefourNSCtypesdescribedinthetext.v.o -...l508 ell Narasimha Rao, Katre Shakuntola and S Ravichandra ReddyFigure 3. Macrobrachium lanchesterl ; Sectional view of the thoracic ganglion ofthe I and 11 stage females (x ZOO) represented as (a) and (b) respectively insidethe figures. DM, YM and L-NSC aggrcgetions 3S ~Y.:ribcd ill figure 1. A-D, NSCtypes as described in figure 2.Neurosecretion in M. lanchesteri 509Table 1. Macrobrachium /anchesteri: Changes in the morphological and cytc-logical characteristics of neurosecretory cells in the thoracic ganglion of the I and IIstage females.Cell typesAverage Averagecell nucleardiameter ~) diameterfjr)AveragecellnumberOther characteristicsA (>50 p)B(26-50p.)D«8p)IIIIIIIIJII61'628'816· 516·76'46'425·614·917'411·714'44323268633303285Largest, round cells with chromatinrich nuclei, Dark purple CliPpositive NSS in the cytoplasm.Medium, oval, moderately CHPpositive greyish cells. Light pinknuclei with small chromatingranules.Medium, oval to pear-shaped cells.Round or oval nuclei with 3--4deeply stained bodies. Darkpurple NSS in the cytoplasm.Smaller, round or pear-shapedmoderately CHP positive greyishcells with agglutinated light pinkchromatin in the nucleus.Smaller, - round or oval cells with-darkly stained pinkish-redagglutinated chromatin in theperiphery of the cells.Smallest, oblong to irregular shapedcells without distinct nuclei, redin colour.Same as in stage 1.Figure 4. Macrobraehium lanchesteri: Diagram illustrating the probable regu-lation of ovarian maturation during the ovigerous conditions. GSH-GQnad-stimu-lating hormone; MH-Moultin.g hormone; OH-C>varian hormone. .510 ell Narasimha Roo, Katre Shakuntala and S Ravichandra ReddyFigure 5. Macrobrachium lanchesteri : Diagram illustrating the probable regulationof normal ovarian maturation, GSH......aonad-stimulating hormone; GIH---Gonad-inhibiting hormone; MH-Moulting hormone; MIH-Moult-inhibiting hormone.and/or brain r) and reduction in the gonad-inhibiting hormone (GIH ; from theeyestalk). The triggering factors for the above chain of events are perhaps theenvironmental cues impinging upon the receptor systems of the prawn (figure S ;see also Adiyodi and Adiyodi 1970).AcknowledgementsFinancial assistance from the UGC, New Delhi, is gratefully acknowledged,References;.Adiyodi KG and Adiyodi R G 1970 Endocrine control of reproduction in decapod crustacea;Bioi. Rev. 45 121-165Charniaox-Cotton H 1952 Castration chirurgicale chez un Crustaee Arnphipode iOrchesttagammareUa) et determinisme des caracteres sexuel secondaires, Premier resultats ; C.R.Acad. Sci. Paris 234 257{}-2572Charniaux-Cotton H 1957 Croissance, regeneration et determinlsme endocrinien des csracteresscxuels d' Orchestia gammarella pallas (Crustace Amphipode}; Ann. Sci. Nat. 19 411-560Enami M 1951 The source and activities of two chromatophorotropic hormones in crabs of thegenus Sesarma. II. Histology of incretory elements; Biol. Hull. 101 241-258Gomez R 1965 Acceleration of development of gonads by implantation of brain in the crabParatelphusa hydrodromous ; Naturwissenscha!ten 9 216Gorgees N Sand Rashan L J 1977 Further observations en the B-type neurosecretory cells in thethoracic ganglion of the crab Potamon magnum magnum (Pretzman); Z. Mikrosk; Anar.Forsell. 90 959-967Neurosecretion in M. lanchesteri 511Hinsch G Wand Bennett D C 1979 Vitellogcnesis stimulated by thoracic ganglion implants intodestalked immature spider crabs, Libinia emarginata ; Tissue Cetl 11 345-352Hisano H 1974 'The eyestalk neurosecretory cell types in the freshwater prawn PalaemonPl1llcideru. I. A light microscopic study; J. Fac. Sci. Hokkaido Univ. 19 503-514Matsumoto K 1954 Chromatophorotropic activity of the neurosecretory cells in the thoracic gang.lion of Briocheir japoniclls; Bioi. J. Okayama Utu». 1 234-248Matsumoto K 1958 Morphological studies on the neurosecretion in crabs; Bioi. J. Okayama Univ,4 103-176Matsumoto K 1962 Experhnent81 studies on the neurosecretory activities of the thoracic ganglionof a crab. Hemigrapsus ; Gen. Camp. Endacrinol. 2 4-11Miyawald M 1960 On the neurosecretory cells of some decapod crustacea; J. Sci. KumamotoUniv.51-20Nagabhushanam R. and Ranga Rao K 1966 Neurosecretory system of portunid crab, Scyllaserrate; 1. Anat. Soc. India 15 138-144Na,gabhushanam Rand Yasantha N 1972 Neurosecretion in the freshwater prawn, Cartdinaweberi; Broter/a &1'. Cienc. Nat. 61 177-t89Otsu T 1963 Bihormonal control of sexual cycle in the freshwater crab. Potamon dehaani;Embryologica 8 1-20P~roeswaran R. 1956 Neurosecretory cells of the central nervous system of the crab Paratelphusahydrodromous; Quart. J. Microsc, Sci. 97 75-82Pearse AGE 1977 Histochemistry: Theoretical and Applied (Edinburgh: ChurchillLivirtgstone) Vol. 1 pp. 1-759R.a.madan A A and M!l.ttaC 1976 Studies 01 the central nervous system of the prawn 1. A histo-logical study for rnappng the neurosecretory cells; Folia Morpnotogica 24 148-154Rao Ch N, Katre Shakuntala and Ravichandra Reddy S 1981 Moult-reproduction relationshipin the freshwater prawn Macrobrachiam laru:hesteri (de M'.Ul); Proc, Indian Acad Sci. (Anim.Sci, 90 39-52Shirwadkar S 11)7'7 Studies on physiolo,ical ecology of prawn, Caridina rajadhari; Ph.D. ThesisMarathwada University

Studies on the neurosecretion of thoracic ganglion in relation to reproduction of femaleMacrobrachium lanchesteri (de Man)

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Studies on the neurosecretion of thoracic ganglion in relation to reproduction of femaleMacrobrachium lanchesteri (de Man)

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