Acta hydrochim. et hydrobiol.

12 (1984)4,463-478

A . K. PANDEY
Department of Zoology, University of Gorakhpur, Gorakhpur, India.

Chemical Signals in Fishes: Theory and Application

Sunmary: I n this paper, a comprehensive survey is presented of the state of knowledge of the occurrence, chemical structure elucidation and biological importance of pheromones in fishes: fright and alarm substances, male and female sexual pheromones, intrasexual stimulants, school formation, social structure and individual recognition, pheromones and fish migration. Especially treated are the problems connected with the chemoreceptionunderchanged environmentalconditions a8 well as the possibilitiesof utilizingpheromonesor substanceswithasimilareffect in fishery.

A very large number of studies has now established that odours emanating from a n individual have encoded message of its race, sex, age, and biological status (DOTU; GILMORE COOK).The naturalist CHARLES DARWINwas t h e first who (in 1877, and cited by RUSSELL) emphasized the roleof chemicalcommunication in the lifeof maninial~, especially i n the human. And now these silent languages have been well recognized t o play a vital role in intercommunications among individuals ranging from protoSHOREY). Earlier, such a system was not known in birds zoans t o humans (BIRCH; and have demonstrated t h a t they are also but the recent studies by JONES BLACK endowed with this faculty. RENGER called these communicator as semiochemihas cals. Those employed for intraspecific communications are known a s pheromones (greek : pherein-to transfer; hbrmon-to excite), the term first coined by KARLSOX and L ~ S C H Ewhile those used for interspecific groups a s allelochemics. Allelochemics R which favour the releaser called allomonas and kairomones when the receiver is benefited. SORDLUNJ) have added two moregroups: synomones and apneiiand LEWIS mones (Fig. 1 ). Pheromones are secreted into the environment (hence called ecto-, or social hormones) and alter t h e behaviour and/or physiology of the recipient either by ingestion, absorption, gustatory (through taste) or through olfactory pathways (HASLER 1957 : WILSON). Chemically, $hey are organic compounds having a molecular weight betand ween 50 a n d 300 (MULLXR-SCHWARZEMOZELL).However, it is pertinent to remark t h a t the air-borne chemicals have lower molecular weights as compared t o those secreted into t h e aquatic environment. Pheromonal studies in fishes have been delayed because they, unlike insects and mammals, live in an aquatic environment and the role of olfaction in thesevertebrates was controversial. Do fishes smell? This was answered by the brilliant study of TEICHMA (1962a, b ) who demonstrated t h a t fishes have exquisitely sensitive organs of smell like dogs. Even 3 or 4 molecules of a n odorant are sufficient to evoke a behavioural response. Studies during the recent years have proved the existence of DE PFEIFFER, 1982) pheromones in fishes (ROSSI;CRAPON CAPRONA1974: STACEY;
3

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Acta hydrochim. et hydrobiol. 1 Y (1984) 5

Chemical Cornmunican t s

{ Serniochemicals

Pheromones ( i n f r o s p e c i f i c signclis sex - a t t r a c t a n t s , alarm subjtances 1

Alieiochemics (interspecific signals i

A 11 o m ones
( f a v o u r ernitferx .spray o f s k u n k , r e p e l l e n t secretions o f 3nsects ;

Koiromones j;Covour r e c e i v e r s iecietians which enables predator t o locate prey.

-

Synomones
[ benificiai t o both errnifter and receiver- f l o r a l scents a n d n e c t a r s ]

Apneumones
[ non -living mater;als, favour receivers decoying m e a t , food groins 1

Fig. 1 . Cllassification of communicatory clieniicals (after KORDLUXDn d LEWIS a 1977; Courtesy D. J. XORDLUND Plentini Press) and Abb. 1. Klassifizierung r o n Koniniunikationscliemikalicn (nach KORDLUND und LEWIS 1977; mit Genehmigung von D. J. XORDLVSI) Plenum Press) und

but our knowledge in this field is still at the embryonic stage because we know their presence only hy behavionral responses, chemically they are largely unknown ( HARA 1975 : KLEEREKOPER : BARBETT a ; CRAPOX DE CAPRONA 1977 1980 ; LILEY1982).

Alarm substances
Like the alarm calls of hirtls and monkeys, the alarm substance of fishes communicates the presence of a nearby danger t o its conspecifics. Phylogenetieally, t h i s chemical system has been recognized from sea anemones (HOWE and SHEIKH) o t the tadpoles of toads (KULZER). The German ethologist VON FRISCH (1938) accidently discovered the fright reaction in the European minnow, Phoxinus phoxinus. When he introduced an injured fish in the school of minnows, all the members then became frightened, retreated and took refuge into a hidden place within 30 s to 1 min. To assess the origin of the alarm substance (substance dalarme, Schreckstoff), he tested pieces a,nd extracts from t h e various components of the body like stomach, gut, liver, spleen, muscle, and skin. A right reaction (reaction deffori, Schreckreaktion) was observed only with t h e skin extract (VON FRISCH 1941). PFEIPFER (1962, 1963, 1969, 1977); S l (1976a, b, 1978, 1979, 1981, 1982a) ~ ~ ~ and MALYVK~NAal. have been busy with the study of the distribution of t h e alarm et substance and the fright reaction in fishes. They demonstrated t h a t the skin of ostariophysian, gonorhynchiform, salmoniforni and other groiips of fishes contains an alarm substance in their large epidermal cells known as club cells (Kolbenzellen) or alarm substance cells (ASC) (Fig. 2 ) . Alarm substance cells do not opendirectly to the surface of the skin, but t.hey release their contents only after a mechanical injury (presumably by a predat.or). The adaptive significance of the alarm pheromone system has been

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465

Fig. 2. Epidermis of Iowa Darter (A) and fathead minnow (B)

ASC =alarm substance cell, BM =basement membrane, DC =darter club cell (KolbenEllen); MC-mucus cell (after SMITH1959; Courtesy, R. J. F. SDUTH and National Research Council of Canada)

Abb. 2. Epidermis von Iowa-Etheostomiden (A) und Pimephales promelas (B).

ASC =Alarmsubstanzzelle, BM =Basalmembran, DC =Etheostomiden-Kolbenzellen, MC =Schleimzelle (nach SMITH 1979; mit Genehmigung von R. J. F. SarITH und National Research Council of Canada)

extensively reviewed by PFEIFFER (1974, 1977) and SMITH (1977,1982b). It isassumed that the alarm pheromone diffusing into the surrounding water alerts and deters the conspecifics from the hunting spot and thus reduces the hunting success of a predator. Further, the possession of alarm substance in fishes also reduces the cannibalism of the youngs. There is ample evidence that the fish shows a strong fright reaction after eating its smaller conspecifics (SMITH 1977). The Chemistry of alarm pheromone attracted wide attention. PFEIEFER LEMEE and
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Beta hydrochim. e t hydrobiol. 12 (1984) 5

working on Phoxinus phoxinus demonstrated it to be a pterine. NEEDHAM (1974) suggested that the pterine might be conjugated with protein. SMJTH (1977) speculated t h a t the species-specificity of the chemical might be due to its attachment with the protein carrier. However, KASUWYAN LEBEDEVA and have strongly condemned the pterine concept. Using the same fish species (Phozinus phozinus), they have shown that the pheromone possesses a molecular weight of approxiniately 1100, behaves in alkaline medium ( p H = 8 ... 9) as an anion and breaksdown when heated. They have suggested it t o be a carbohydrate or related compound containing amino-groups.

Female Sex Pheromones

-4healthy adult male feels sexual stimulation in the presence of a receptive female (DOTY; KEVERNE). male dog can even be attracted to an anoestrous female over a A distance if methyl-p-hydroxy-benzoate is applied to her vulva (GOODWIK et al.) This factor can better be called as 'her factor' and each female is labelled w i t h t h e factor particular to her own species. It was TAVOLGA (1956) who first of all systematically studied the sexual beliaviour of the male gohy fish, Bothygobio sopomfor, in t h e presence of females. H e demonstrated that the spermiated male discriminantes between male and female and also hetween non-gravid and gravid females on the basis of chemical cues released through her vent. Ovarian fluid was sitfficient t o induce courtship behaviour in males even 1954). LILEY(1969) remarked that a definite in the absence of females (TAVOLGA threshold of circulating androgen is sine qua non to render the male different ially sensitive to the sex attractant released by the gravid females. TAVOLUA (1976) suspected 'the endocrine secretion of the testis may affect the olfactory sensitivity'. I n a recent st.udy YAMAZARI WATANABE and have shown that methyl testosterone affects t h e olfactory cells of the nasal epithelium. et and LILEY Let us see where this attractant is synthesized. YARTR~DGE al.; CROW and HONDA (1979, l98Oa, b, 1982a, b) have shown t h a t t h e pheromone is released just after ovulation and have suggested the ovary to be the site of t h e pheromone biosynthesis. However, PAMAZAKIWATANABE and suggested the kidney to be involved in the pheromone prodiiction. But this hypothesis is doiibtful on t h e account of the following reasons
-it does not satisfy the functional (biological) significance of this pheromone, -OKADA e t al. have not found any fraction of the kidney homogenates t o induce a courtship behaviour in males.

Currently, t h e involvement of the ovar>- has been confirmed by MEYER and LILEY who have demonstrated that ovariectomized-oestrogen-treated females are ineffective to males. characterized t h e female sex attractant (substance dynamoChemically, AMOURIQ et al. gene) of Lebistes reticulatus t o be an oestrogen. PARTRIDGE have also suggested it, t o be a lipid or steroid because of its solubility in ether. After an exhaustive study on t h e pond smelt (Hypomesus olidus) pheromone, OKADA et al. have demonstrated the fraction (FP,) on DEAE-Cellulose column that elicited tdhemale courtship behaviour declined in activity after heat (80 "C, 5 min) or trypsin (30 "C, 60min) treatment and suggested t h a t the substance in the genital fluid was either a protein or a substance including protein in its structure. LILEY(personal communication)

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467

believes it to be a sex hormone or its metabolite(s) attached with a protein carrier. The protein fraotion may denote its species specificity and solubility of the pheromone in t h e environmental medium.

Male Sex Pheromones

A male fish broadcasts its presence by permeating the aquatic environment with his factor (the male odour). The odoriferous secretions of the cutaneous anal glands JASKI in Blennius pauo attract the females during the breeding season (EGGERT). (1939) using guppy, Lebistes reticulatus, demonstrated that the male fish secretes a chemical copulin which synchronizes the sexual receptivity in females. A pheromone is found in tlhe Pacific herrings milt t h a t triggers spawning in thegravid females ( N . E. STACEY and A . S . HouRSToN,University of Alberta, MSS). COLOMBOet al. have suspected the male pheromone of Gobius jozo t o be etiocholanolone glucuronide. The most profound effect of a male on females seems to be its influence over t h e neuroendocrine (hypothalamo-hypophyseal-gonad) system of the latter. MOSHER remarked t,hat when a male is introduced into t h e group of females, it stimulates egg production a n d its continued presence leads t o a regular oviposition cycle. A similar observation has also been recorded in the blue gourami, Trichoguster trichopterus, by POLLAK CHRISTIAN, and who noted that paired females (with males) possess ovaries filled with mature ova while ovaries of grouped females (without males) contain almost no ripe ova, but numerous oocytes in the various stages of development. CHIENtried t o solve t h e riddle whether this effect was visual or chemical and found that both t h e factors are equally important. He suggested for the angel fish, Pterophyllum scalare, visual and chemical cues from the male must stimulate t h e release of the gonadotropins releasing factors from the hypothalamus which result in a rapid development of gonads and subsequent ovulation and spawing activities. These d a t a encourage to undertake further studies on the primer pheromonesin fishes which have been extensively recognized in mammals (AVERY;ARON; SCHADLER; MCCLWTOCK).

Intrasexnal Stimulants and School Formation

Reports on male-male and female-female stimulation are rare in vertebrates, but the possibilities have been raised from time to time (COMFORT; CRAPON DECAPROKA 1976). Prom the axillary (under arm) sweat of humans (male and female) rostenol has been identified (KINGSBURY and BROOKSBANK) arouses both the sexes which (MCCOLLOUGH al. in press). I n fishes, the male three-spined stickleback Gasteroet steus aculeatus, gets excited by smelling the odour of his own nest during the breeding season (ARONSON).LOSEY has demonstrated t h a t the male of Hypsoblennius sp. secretes a chemical during its high courting and mating periods that releases the sexual appetitive behaviour and sexual receptivity in other males. CRAPON CAPRONA DE (1976) hypothesized the female-female interacting pheromone(s) in fishes. I n zebra fish, Bruchydanio rerio, the presence of both male-male and female-female attractants BLOOM PERLMUTTER. and Do these pheromohave been demonstrated by BLOOM;
33*

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Acta hydrochim. et hydrobiol. 12 (1984) 5

nes bear any biological importance? To answer this, we have to go back t o 1967 when MCFARLAND Moss speculated the possibility of the involvement of pheromones and in school formation and/or attraction of t h e mature conspecifics towards t h e spawning ground. ALGRANATI has speculated the sexual aggregating pheromones of zebrafish t o be two in number, one attracting male conspecifics and other females. ALGRANATI and PERLMUTTER preoccupied with the isolation and characterization of these are pheromones. I n a preliminary attempt they have demonstrated t h a t t h e attractants are contained in the cholesterol ester fraction (Rf - 0.94) of the thin-layerchromatograms.

Individual Recognibion
Some fishes display a social organization with a boss as the head of colony who is respected by all other members of the group. Since individual recognition is a cornerstone of sociality, so its members must be recognized from individuals of other 1977). TODD al. (1967) have demonstrated t h a t t h e et societies or species (BARNETT yellow bullhead, IctrrZurus natrrlis, ( a nocturnal visually-deficient fish) recognizes individuals of its own group by means of pheromones secreted in the skin mucus. The fish attacks the stranger but remain quiet (or rather attracted) when a member of its own colony is introduced into the aquarium. ROSENBLATT LOSEY and showed t h a t the methanol extract of the mucus was attractive also in the top smelt, Atherinops a.ffinis. I n a later review on the chemical languages of the bullhead, TODD (1971) remarked that the boss of the colony has territory odour, theresidentscommunalodour,eachmemberislabelledwiththepeculiar odourof its own (just like thename in verbal language) and they all live together peacefully because of the love-in (1977 b in press a , b) has demonstrated t h a t pheromone. I n a recent study BARNETT t>hefry of Midas cichlid fish, Cichalosoma citrinellum, discriminates even between its father and mother on the basis of their smell. Even broods and youngs are recognizable t o their parents by the odour secreted in the miicus (ARONSON). The study on t h e origin and chemical nature of these pheromones has now taken a shape of discipline. BARKETT (1981) has demonstrated that a baby cichlid fish discriminates its father and mother on the basis of urineodour. BARNETT (1981) remarked the steroid titers in urine could provide information on sex, and t h a t of peptide chains and 6T-4BLE and SELSET have shown the role in urine could indicate species. SELSET, of faeces in the individual recognition of salmonid fishes. While urine was considered as a major source of mammalian pheromones, TODD(1971) held the view t h a t the mucus was a main source of chemical informat ion in fishes. During the reproductive period the ma,le of some species deposits a layer of mucus on the spawning surface which may serve as a chemical signal marking the breeding site and may perhaps indicates the status of t h e occupant (SMLTH MURPHY). Possibly these marks and bear the same biological significance as the marking fluid ( M P ) of mammals (REER; SUTCLIFFE YOOLE; BRAIXB.WCHARY and and DUTTA 1979, 1981 ; YAHR). presence The of odorants in the skin mucus has been widely described (DUVING al. 1973, 1974; HAet RA 1975, 1977b, 1982b), but we are still a long way from deciphering theinformation inscribed in it.

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469

Pheromones and Migration

How migratory fishes locate their pathways from sea to freshwater and vice-versa JONES). Much work has been done on the homing of has been a mystery (HARDEN remarked the salmonid (anadromous) fishes. I n 1599, CLAUSONFRIIS(cited by SELSET) t h a t these fishes migrate from the nursery areas t o their parent river streams out to sea and then back to their birth places to spawn (the basis of the Parent or Home suggested that each stream has a unique bouquet of Stream Theory). BUCKLAND odonrs and the fish has to follow his nose in t h e detection and discrimination of the natal stream. The role of metabolic products of a specific population (pheromones) as homing cues was proposed by CHIDESTER (in 1924 cited by SOLOMON 1973) and WHITE(1934, 1936), but unfortunately this hypothesis was totally eclipsed by the concept of olfactory imprinting propounded by Wisconsin workers (HASLER 1960, 1966; HASLER WISSY). According to this theory, the youngs lock onto the odours and of aquatic vegetations, soil rnn-off, and other organic chemicals present in the parent stream in their brain and they retain the olfactory memory during the interim and HASLER; HASLERand COOPER; period of their homeward migration (COOPER HASLER al). et (1971) realised the pheromones as an odour tracks t o help guide Again, NORDENG (1973) has demonstrated t h a t the migrahoming, t h e char, Salmo alpinus. SOLOMOX tory Atlantic salmon, Salmo salw, prefers the river in which the youngs of its o w n population are living. After exhaustive studies on Salmo alpinus, Salmo truttcr, and Salmo solar, NORDENG (1977) rejuvenated the pheromone hypothesis. He wrote homeward navigation is an inherent response t o population specific pheromone trails released from the descending smolt. The role of pheromones in the upstream orientation has been recently confirmed in the rainbow trout, Swlmo gairdenpri by EMANUEL DODSON, and and in the sea lamprey, Petromyzon marinus (an anadromous cyclostome) by TEETER. Our knowledge regarding the chemical nature of these navigational cues is still et fragmentary. ATEMA al. have reported t h a t in the alwife, Alosa pseudoharengus, homing pheromones are heat-stable, non-volatile, polar, and have molecular weights less than 1000. Recent studies have demonstrated the char (Salmo alpinus) migratory cue(s) to be present in the faeca1 matter of the smolt (STABELL and SELSET; SELSETand DQVING) have suggested it to be either bile acid(s) or its derivatiand DQVING al. 1980) which probably conveys the information to the brain et ves (SELSET; and SELSET). The role of via the lateral part of the medial olfactory tract (DBVING faecal matter a s navigation cues in the migration of the Atlantic salmon (Sulrno salar) has also been shown by FISKNES DBVING. and

Chemoreception and Water Pollution

Recent studies on various groups of animals have demonstrated t h a t pheromone has a particular binding site on the nasal epithelium to which i t interacts to evoke a behavioural response (VOGT and RIDDIFORD). GENNINGS al. have demonstrated et the presence of receptors for the odoriferous steroid, 5- androst-16-en-3-one, in sow nasal epithelium. This study h a s been further supported by HANCOCK BANNISTER. and

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The molecnlar mechanisms of taste and olfaction have been studied by many workers (see C'AGAN and KARE).The exhaustive studies of HARA(1976a, 1977a, b, 1981, (1978, 1982, 1983) have led t o t h e conclusion t h a t there 1982b) and THOMMEKSEN (1982b) are also chemoreceptor sites (cells) in the olfactory m~icosa fishes. HARA of has given a hypothetical model t o show t h e mode of interaction of amino acids (it is likely t h a t various amino acids found in the mucus serve as feeding stimuli t o fish) with the olfactory receptor site (Fig. 3).
Amino

Acid

Molecule

/:
CQO-

Fig. 3. - hypothetical three-subsite amino 4 acid receptor site

Two charged subsites, one anionic (I) and the other cationic (11). ale arranged around a centre (111)which acconiinodates the a-hydrogen atom of an amino acid molecule. Tlie fourth a-moiety of the amino acid molecule is also an important determinant factor for the stiniulatory effectiveness (after 1 . 4 ~1082b; Courtesy ~ - T. J. HARAand Elsevier Scient. Pub. Co., Amsterdam, The Setlierlands).

I
I

! \
I

i
I
I

I
I I
I

Abb. 3. Eine hypothetische Aminosanre-Rezeptorstelle init drei Unterstellen

I
U

Receptor

Zwei geladene Unterstellen, eine davon anionisch (I) nnd die andere kationisch (11), sind uiii einen Mittelpunkt (111) angeordnet, der das a-Wasserstoffatom eines AniinosiiuremolekiiIs aufninimt. Der vierte a-Anteil des Aminosauremolekiils ist ebenfalls ein wichtiger bestimmender Faktor fiir die Reizwirkung (nach HARa 1982b; niit Genehniignng von T. J. HARA und Elesevier Scient. Pub. Co., Amsterdam, Kiederlande).

BARDACH al. were the first to study the effects of detergents on the chemical et senses of the yellow bullhead, Ictalurus nctfolis, and found t h a t a concentration of 0.3 ppm (a much lower value than that causing sublethal damage) impaired t h e recepFig. 4.Olfactory neuroepithelium of whitefish, Coregon us clupeaforuiis 10 p arid hematein method
1

sect'ion, Baker's

Control (a) with neurons stained black (arrow), after 2 weeks exposure (b). after 4 weeks recovery in uncontaminated water ( c ) , and after 12 weeks recovery ((1) (aftpr BROWS et al., 198'2; Courtesy-T. J. H.~KAandElsevierScient. Pub. Co.. Aiiwterdani, The Xetlierlan~ls).

Abb. 4. Olfaktorisches Beuroepithel vori WeiBf isch, Coregonus clicpeoformis. Rchnitt, von 10 pm, Methode mit saurem Hamatein nach Baker
Kontrolle : (a) mit scliwarz gefarhten Xeuronen (Pfeil). nacli zweiwiiclligrr Einwirknng (h), nacli vierwocliiger Erholung i n u~iverschmutzteiiiWassrr ( c ) und nach zwblfwbrliigrr Erholung (d) (nacli BROWx et al. 1082; niit Genehnrigung von T . 3 . Hax.4 unrl Elsevier Scient. Pub. Co.. Anisterdam, Siedrrlantle).

Fig. 5. Olfactory neuroepitheliuin of rainbow trout, Sadmo gciirdneri

10 : ~ . i j i section, llakcr's acid hematein nietlind. Control (a) with neurons stained black (arrow), after one week exposure (h). after 2 weeks c i p o w r e (c), and after 1 weeks recover? in unoniit:Liiilnatr(I water (rl) (after BROITVS ct a1. 108'2: Conrte. '

. HAR.A 7;;lsevirr Scient. Pub. Co., Anistrrdam. The Setlierlantls). and

Abb. 5. Olfaktorisches Seuroepit.he1 der Regenbogenforelle S'alnio gairdneri. Schnitt von 10 pm, Yetliode init saurem Hamatein nach Baker
Konttolle: (a) init schwarzgefarhten Keuroneri (Pfeil), nacli rinwocliiger Einwirkung (b), nach zweiwochiger Einwirk ung ( c ) und nach zwolfwocliiger Erhnlung in unrerschmutztem U'asser (d) (nacli BKO\VX e t al. 1982; niit Geneliniigung van T. J . HARA und Elsevier Scient. Pub. C o . , Amsterdam, Siederlande).

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tor functioning by causing erosion to the chemosensory organs. HARA n d THOMPSON a have studied the pernicious effects of an anionic detergent (sodium lauryl sulphate), pH (HARA1976b), mercury (Hg), copper (Cu) (HARA al.), cadmium (Cd), nickel et (Ni) and zinc (Zn) (THOMPSON and HARA)and foundHg, Cu, and Cd to have most depressive effects on the chemoreception of fishes (also see, BROWNt al.). EVANS e and HARA (unpublished, cited by BROWN al.), and THOMPSON HARA et and (unpublished, cited by BROWNe t al.) exposed whitefish (Coregonus clupeaformis) and rainbow trout (Salmo gairdneri), respectively, to 2.4 pM copper sulphate solution and noted a loss in the phospholipid stained granules in the receptor neiirons of the olfactory mucosa (Fig. 4, 5). Phospholipids are said to be involved in the electrophysiological activities of the olfactory epithelium (BROWN al.). et The present trends of rapid industrialization and increase in population have changed the quality of the aquatic environment. Such a study regarding the interactionofaquatic pollutants with the pheromonal communications is imperative to undertake. BARNETT (1977 b) has already remarked that a chemically polluted environment can interfere with the success of parental care.

Conclusion
The above facts impel us to say that the chemical languages shape the life of fishes. They communicate the information about the individuals species, status, sex, age or size, reproductive state, individual characteristics, and also even family (race) identification (TODD1971 ; BARNETT 1977). Since these signals are species-specific, it is imperative to manipulate them for the management and conservation of fisheries. I n piscicultural operations, they may be used as a selective stimulant to induce spawning at a time and place convenient t o the fishery managers (LILEY1980). They may also be employed as artificial baits, selective attractants, growth stimulators, inhibitors of aggression and cannibalism (TODD 1971 ; COLYER and JENKINS ; SOLOMON 1977). Further, in a not too distant future we would be able to exploit these chemicals for propagating migratory fishes in new rivers and streams.

Acknowledgements
1 am grateful t o Prof. R.L. BRAHMACHARY, I.S.I., Calcutta, for the critical reading of the manuscript. The author is also indebted to Drs. S. R . LILEY,R . JAN,F. SXITR,Colin BARNETT, , Kjall B. D0v17sc and Houji OKADA their valuable for Toshigaki J. H ~ R AEdward I. POLLAB, help and suggestions.

References
ALGRANATI, D.: Role of sex attractant pheromone(s) on spawning aggregation in the zebraF. fish, Brachydanio rerio: its isolation and partial purification. Diss. Abstr. Inter. 40 3 (1980), 108 p. ALGRINATI, D., and A. PERLUUTTER: F. Attraction of zebrafish, Brachydanio rerio, t o isolated and partially purified chromatographic fractions. Env. Biol. Fish 6 (1981), 31-38.

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~~l/nii,rslrripteingang: 7. 1983. 20. d n s r h i ift des T'erfosseis:

Dr. -1.( P ~ S U E107 Sant Kabir Biuldmg. I-niversity of C:orakhpur, I. Y, T I - 2 7 3 001 Gorakhpur (U.P.). S)