Tongue Replacement in a Marine Fish (Lutjanus guttatus) by a Parasitic Isopod (Crustacea: Isopoda) Author(s): Richard C.

Brusca and Matthew R. Gilligan Reviewed work(s): Source: Copeia, Vol. 1983, No. 3 (Aug. 16, 1983), pp. 813-816 Published by: American Society of Ichthyologists and Herpetologists Stable URL: http://www.jstor.org/stable/1444352 . Accessed: 05/12/2011 09:13
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ICHTHYOLOGICAL

NOTES

813

eggs from a normal, female, European smelt (Osmeruseperlanus), when fertilized with sperm from hermaphrodites, produce large numbers of successfully developing embryos. To my knowledge, this is the first evidence of hermaphroditism in the species 0. mordax. There have been three other reports of hermaphroditism in the genus Osmerus:Hofmeister (1939), Jensen (1949) and Lillelund (1965), all in the European smelt, 0. eperlanus.
0.5u

Fig. 1. Ten microncrosssectionof a rainbowsmelt hermaphrodite gonad with perinucleolus stage primaryoocytes interspersedbetween lobulescontaining spermatogonia(tissue fixed with Davidson'sfixative; stain). paraffinembedding;Mallory-Heindenhain's

Acknowledgments.-I wish to thank Bob Fawcett, Hunt Howell, Philip Sawyer and C. W. Walker for their various contributions to this paper.
LITERATURE CITED

K. HOFMEISTER, T.

1939.

beim Stint (Osmerus L.). eperlanus Zwitterbildungen in the anadromous rainbow smelt, OsmerusmorZ. Morph. Okol. Tiere 35:221-245. dax, two hermaphroditic specimens were found JENSEN, B. 1949. Biological investigationson the I. on 26 March 1981 in the Bellamy River, New smelt (Osmerus eperlanusL.). Vidensk. Medd. Naturhist. Foren. Kbh. 3:73-109. Hampshire. The specimens measured 143 and K. 141 mm standard length and were estimated to LILLELUND, 1965. Weitere Untersuchungen ilber bei den Hermaphroditismus Osmerus (L.) be 2-3 years old based on the age-length relaeperlanus aus der Elbe. Z. Morph. Okol. Tiere 55:410-424. established by the New Hajnpshire Fish tionship K. and Game Department (R. S. Fawcett, pers. YAMAMOTO, 1956. Studies on the formation of fish eggs. I. Annual cycle in the development of comm.). obscura. ovarian eggs in the flounder, Liopsetta J. Initial field observations showed the two specFac. Sci. HokkaidoUniv. VI, Zool. 12:362-379. imens to be unusual in that they did not extrude eggs or milt when pressure was applied to the DOUGLAS E. GROUT, ZOOLOGY DEPARTMENT, abdomen (others collected were ripe with UNIVERSITY OF NEW HAMPSHIRE, DURHAM, spawn). Upon dissection, the gonads of both fish 03824. Accepted 12 June NEW HAMPSHIRE were similar in gross appearance to the testes 1982. of recently spawned males. Except for being slightly thinner due to the lack of mature sperm, the dimensions of the gonads were within the Copeia, 1983(3), pp. 813-816 ? 1983 by the American Society of range of measurements of testes in the normal, Ichthyologists and Herpetologists prespawned smelt collected. After histological preparation, the gonads were examined microscopically and found to TONGUE REPLACEMENT IN A MARINE contain both spermatogonia and numerous pri- FISH (LUTJANUS GUTTATUS) BY A PARAmary oocytes (Fig. 1). Spermatogonia were SITIC ISOPOD (CRUSTACEA: ISOPOfound within the boundaries of the lobules that DA).-In the Gulf of California, Mexico, the are characteristic of teleost testes. Primary oo- isopod crustacean Cymothoa exigua Schioedte and cytes in the perinucleolus stage, which are char- Meinert causes the degeneration of most of the acterized by many nucleoli on the periphery of tongue of its host fish, the snapper Lutjanus a large nucleus with chromatin threads scat- guttatus (Steindachner), and attaches to the retered in the central region (Yamamoto, 1956), maining tongue stub and floor of the fish's were found within the spaces between the lob- mouth by hook-like pereopods. In this position ules. the isopod superficially resembles the tongue of The immature state of the gametes in these its host fish. There is no indication of reduced specimens made it impractical to speculate feeding or respiratory ability in infested hosts. whether the fish were functional hermaphro- We herein hypothesize that these isopods serve dites. Lillelund (1965) indicated, however, that as mechanical replacement for the fish's tongue,

Untersuchungen

iiber

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COPEIA, 1983, NO. 3

the Fig. 1. Lutjanusguttatus, spotted rose snapper, from the Gulf of California,with the parasiticisopod Cymothoa exiguaattached in the mouth where it has destroyed the tongue (left), and a non-infested individualwith a normal tongue (right).

Fig. 2. Preserved specimen of Lutjanusguttatus showingrelativesize of the isopod in the mouth. The gill cover andjaws have been partlyremoved to show how far posterior to the tongue base the isopod has attached.

and represent the first known case (in animals) of functional replacement of a host structure by a parasite. Isopod crustaceans in the Cymothoidae are ectoparasites on hundreds of species of marine and freshwater fishes throughout the world's tropical and temperate regions. They parasitize most commercial fish species but probably do not cause significant rates of mortality among their hosts. Brusca (1981) has pointed out that genera infesting buccal and gill chambers probably represent a more advanced phyletic lineage within the family than do genera attaching on the outer epidermis. Probably all species of Cymothoidae are protandrous hermaphrodites. Buccal-gill infesting species enter the gills of the host as males after a short, free-living juvenile stage, to later become functional females in the host's gills or mouth. In some species, copulation occurs within the gill chamber while in others it may occur in the buccal region. The source of nutritional energy for the large, mouth-inhabiting females is unknown, and it has been suggested that individuals in at least some of these species are actually non-feeding commensals, rather than parasites (reviewed in Brusca, 1981). Romestand and Trilles (1977a, b) described the histological alterations associated with the isopod-induced degeneration of the tongue in the sparid fish Boop boops (L.). They conclude that the disorganization and regression of the connective tissue and cartilage of the tongue is a result of 'hematophagie' ("blood

feeding") by the parasite and that decreased blood circulation at the site of attachment is a proximate cause of the degeneration. Vu-TafnTub (1973) reported on the increased likelihood of Boopboopsto grow vomerine teeth when parasitized by the buccal cymothoid parasite Meinertia oestroides. In Nov. 1979, one of us (MRG) examined 37 specimens of the spotted rose snapper Lutjanus guttatus caught on hook and line by fishermen near Guaymas, Sonora, Mexico. Of these, two had parasitic isopods (Cymothoa exigua) attached in the mouth and in both cases more than 90% of the fish's tongue was absent. Fig. 1 shows the mouth of a freshly caught specimen containing an isopod, compared with a noninfested individual. The relative size of the isopod in the mouth cavity is seen in a preserved and dissected specimen (Fig. 2), which shows it to be somewhat larger than the tongue. In life, the isopods were firmly attached to the floor of the fish's mouth by their seven pairs of hooklike pereopods. Both parasitized fish appeared to be in good condition, with full intestines and adipose deposits in the visceral cavity; one had a 20 X 50 mm piece of fish in its stomach. The two host fish were young adults (165 mm and 270 mm standard length) of a species that grows to a length of 80 cm (Thomson et al., 1979). Recent migration of these isopods to the mouths of their hosts from the gill chambers is unlikely; there is no space in the fish's buccal cavities or gill chambers that could accommo-

ICHTHYOLOGICAL date parasites approaching this size. There was very close fit between the dorsal curvatures of the isopods' exoskeletons and the shapes of the fishes' palates (convex anteriorly; more V-shaped posteriorly). Minor abrasion by the medial process of the vomerine tooth patch of the fish was evident on the first two thoracic segments of both isopods. It is clear that: 1) excepting a small proximal stub, tongues were absent in the host fish, 2) the isopods were firmly attached to the floor of the mouth in a position that superficially resembled a tongue and 3) the isopods fit well enough in the mouth to allow the hosts' vomerine tooth patch to score the anterior thoracic somites of the parasites, presumably during feeding by the hosts, during which the isopod might serve the same function as the missing tongue. In fishes, unlike most other vertebrates, the tongue is a non-protrusible extension of the underlying branchial skeleton (and a covering for the basibranchials and basihyal) and has no skeletal muscle components of its own. It is primarily a mechanical device to hold prey in the mouth against the vomerine and palatine teeth in the roof of the mouth while being processed. There is no evidence that the teleost tongue is essential to respiration (Hughes and Shelton, 1958; Harder, 1958). Its replacement by a parasite would not appear to be a complex phenomenon. The central question is whether the fitness of the fish, in evolutionary terms, is reduced more by the total absence of a tongue, with no isopod taking its place, or by having the isopod attached in its place. From the evidence presented we propose the hypothesis that a fish with an "isopod tongue," while perhaps not feeding as efficiently as a non-parasitized fish, feeds more efficiently than a fish with no tongue at all and no isopod in its place. It seems evident that, in isopods of this size, any displacement of host body volume that would create more space for them in the mouth must involve host tissue that the fish can somehow afford to lose. In gillinhabiting isopods, for example, the size of the eroded cavity within the gill filaments of the host is usually identical in size with the isopod itself (Comeaux, 1942; Bowman, 1960; Bowman and Mariscal, 1968; Brusca, 1978). Naturally, there must be a limit to the amount of gill erosion that a fish can tolerate without respiratory impairment. Several workers have noted apparent decreased health in host fish sustaining multiple gill infestations of cymothoid iso-

NOTES

815

pods, particularly when hosts were placed in stressful environments (Keys, 1928; Westman and Nigrelli, 1955; Lewis and Hettler, 1968; Turner et al., 1969; Lanzing and O'Conner, 1975). However, it is apparent that almost the entire tongue can be replaced in the spotted rose snapper with little, if any, effect on the fish's health. That these parasitized fish were healthy and apparently feeding well supports this contention. Mimicry of host body functions by parasites is not unknown. A classic example in animals is the induction of supernumerary larval molts in the flour beetle Tribolium by the microsporan parasite Nosema. Nosema produces a juvenile hormone-like substance which stimulates growth and larval molts in the host but deters adult development, resulting in giant larvae (Fisher and Sanborn, 1964). "Replacement" of host organs is also known but usually involves emasculation and replacement of host gonad body volume by the parasites (Cheng, 1964). In these cases, however, normal host organ function is naturally lost. We know of no case in animals of what could be interpreted as both structural and functional replacement of a host organ or body part by a parasite (T. C. Cheng and G. L. Hoffman, pers. comm.). If tongue replacement is an adaptive strategy by the isopod, that is, a behavioral adaptation permitting growth of the isopod to a large (brooding) size in the host's mouth while maintaining the host's feeding function, then we might expect to see greater host-specificity in this species, since this suggests a more intimate association than seen in most other cymothoid species. However, Cymothoaexigua has a fairly low host specificity and has been reported from eight species of fish (in 6 families) in the eastern Pacific, including two other species of Lutjanus (Brusca, 1981). In all cases females attach in the host's mouth while males are found attached to the gills. This suggests that tongue replacement may not be a highly evolved or obligate evolutionary strategy, but rather that functional replacement of the tongue by this isopod is an evolutionary consequence of preadaptation to having a body plan which is well suited to this function. The authors gratefully acknowledge the critical reviews of this manuscript by G. J. Bakus, T. E. Bowman, E. W. Iverson, B. Kensley, M. Moser, C. Swift and D. A. Thomson. This is contribution 396 of the Allan Hancock Foundation, USC; funded in part by a grant

816 from the National (DEB80 17835). Science

COPEIA, 1983, NO. 3 Foundation

eriennes et pt rygofdiennes chez Boop boops (L.) (Pisces, Sparidae), en rapport avec l'Isopode phor'tique intrabuccal Meinertia. Vie et Milieu 14:225232. 1955. PrelimWESTMAN, J. R., AND J. R. NIGRELLI. inary studies of menhaden and their mass mortalities in Long Island and New Jersey waters. New York Fish and Game J. 2:142-153.

LITERATURE CITED
T. BOWMAN, E. 1960. Description and notes on the biology of Lironeca puhi, n. sp. (Isopoda: Cymothoidae), parasite of the Hawaiian moray eel, Gymnothorax eurostus (Abbott). Crustaceana 1:82-91. - ANDR. N. MARISCAL. 1968. Renocila hertero, zota, a new cymothoid isopod, with notes on its host, the anemone fish, Amphiprionakallopisosin the Seychelles. Crustaceana 14:97-104. R. BRUSCA, C. 1978. Studies on the cymothoid fish symbionts of the eastern Pacific (Isopoda, Cymothoidae). I. Biology of Nerocila californica. Crustaceana 34:141-154. . - 1981. A monograph on the Isopoda Cymothoidae (Crustacea) of the eastern Pacific. Zool. J. Linnean Soc. 73:117-199. CHENG,T. 1964. The biology of animal parasites. W. B. Saunders, Philadelphia. G. COMEAUX, T. 1942. Parasitic isopods of fishes from the Grand Isle, Louisiana region. Proc. Louisiana Acad. Sci. 6:86. F. FISHER, M., ANDR. C. SANBORN.1964. Nosema as a source of juvenile hormone in parasitized insects. Biol. Bull. 126:235-252. W. 1958. Anatomie der Fishe. E. SchweizHARDER, bart'sche Verlag, Stuttgart. G. HUGHES, M., ANDG. SHELTON.1958. The mechanism of gill ventilation in three freshwater teleosts. J. Exper. Biol. 35:807-823. KEYS,A. B. 1928. Ectoparasites and vitality. Amer. Nat. 62:279-282. W. LANZING, J. R., AND P. F. O'CONNER. 1975. Infestation of luderick (Girella tricuspidata) populations with parasitic isopods. Australian J. Marine Freshwater Res. 26:355-361. LEWIS,R. M., ANDW. F. HETTLER.1968. Effect of temperature and salinity on the survival of young Atlantic menhaden, Brevoortia tyrannus. Trans. Amer. Fish. Soc. 97:344-349. M. ROMESTAND, B., ANDJ.-P. TRILLES.1977a. Influence des cymothoiadiens (Crustacea, Isopoda, Flabellifera) sur certaines constantes hematologiques des poissons h6tes. Zeitschrift ffir Parasitenkunde 52:91-95. . 1977b. Degenerescence de la , AND langue des bogues (Boop boops L., 1758) (Tel6osthens, Sparidae) parasitees par Meinertia oestroides (Risso, 1826) (Isopoda, Flabellifera, Cymothoidae). Ibid. 54:47-53. AND A. N. KERTHOMSON,D. A., L. T. FINDLEY STITCH. 1979. Reef fishes of the Sea of Cortez. John Wiley, New York. ANDR. R. GIVEN. 1969. TURNER,C. H., E. E. EBERT Man-made reef ecology. Calif. Fish and Game, Fish. Bull. 146. K. 1963. Sur la presence de dents vomVu-T^N-Tui,

RICHARD BRUSCA, C. Allan Hancock Foundation, University of Southern California, Los Angeles, California 90007, and MATTHEWR. GILLIGAN, Dept. Biology,Savannah State College,Savannah, Georgia 31404.

Copeia, 1983(3), pp. 816-817 ? 1983 by the American Society of Ichthyologists and Herpetologists

DESIGNATION
THE MOSA Rosen sexual AMAZON

OF A LECTOTYPE FOR

Poecilia formosa (Girard), was based on a male and a female, no one previously has reported that the type material includes two taxa. In his original description, Girard (1859) clearly stated that Limia formosa was based on a male and a female which he described separately. Unlike most of Girard's descriptions, this two-page account is unusually detailed and leaves no doubt as to the identity of his specimens. He stated that the male resembled that of Limia poecilioides Girard, a species subsequently assigned to the synonymy of Poecilia latipinna (Lesueur), whereas he remarked that the female differed widely from the male. Based on examination of the male syntype by Carl L. Hubbs in 1958 at the Museum National d'Histoire Naturelle in Paris (cat. 439), we confirm that this specimen represents P. latipinna. It is an adult 29 mm SL received from the Smithsonian Institution, ex USNM 3508. It has 13 dorsal and 9 anal fin rays and 16 scales around the caudal peduncle-counts that are consistent with those of P. latipinna from the Brownsville, Texas, area (D 12-14, A 9, c. ped. sc. 16; UMMZ 157346). Girard recorded only 7 anal fin rays in the male, a number unknown in any molly in the United States or adjacent parts of Mexico. The female was said to have 12 dorsal and 10 anal fin rays, equivalent to 11 dorsal and 9 anal fin rays as counted by the method proposed by Hubbs and Lagler (1958:20-21), which we fol-

MOLLY, POECILIA FOR(PISCES: POECILIIDAE).-Although and Bailey (1963:54) noted that the uni(all-female), gynogenetic Amazon molly,