filiformis (Rudolphi, 1819) (Digenea: Fellodistomidae) A proposed three-host life history of Monascus in the southwest Atlantic Ocean References

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1 1198 Can. J. Zool. Vol. 76, 1998 References Babin, M., Therriault, J.-C., Legendre, L., and Condal, A Variations in the specific coefficient for natural phytoplankton assemblages: impact on estimates of primary production. Limnol. Oceanogr. 38: Brumbaugh, J.H The anatomy, diet and tentacular feeding mehanism of the dendrochirote holothurian Cucumaria curata Cowles, Ph.D. thesis, Stanford University, Stanford, Calif. Costelloe, J., and Keegan, B.F Feeding and related morphological structures in the dendrochirote Aslia lefevrei (Holothuroidea: Echinodermata). Mar. Biol. (Berl.), 84: Fankboner, P.V Suspension-feeding mechanisms of the armoured sea cucumber Psolus chitonoides Clark. J. Exp. Mar. Biol. Ecol. 31: Filimonova, G.V., and Tokin, L.B Structural and functional peculiarities of the digestive system of Cucumaria frondosa (Echinodermata: Holothuroidea). Mar. Biol. (Berl.), 60: Fish, J.D The biology of Cucumaria elongata (Echinodermata: Holothuroidea). J. Mar. Biol. Assoc. U.K. 47: Hamel, J.-F., Himmelman, J.H., and Dufresne, L Gametogenesis and spawning of the sea cucumber Psolus fabricii (Duben and Koren). Biol. Bull. (Woods Hole, Mass.), 184: Hamel, J.-F., and Mercier, A Spawning of the sea cucumber Cucumaria frondosa in the St. Lawrence Estuary, eastern Canada. South Pac. Comm. Beche-de-Mer Bull. 7: Hamel, J.-F., and Mercier, A. 1996a. Early development, settlement, growth and spatial distribution of the sea cucumber Cucumaria frondosa (Echinodermata: Holothuroidea). Can. J. Fish. Aquat. Sci. 53: Hamel, J.-F., and Mercier, A. 1996b. Evidence of chemical communication during the gametogenesis of holothuroids. Ecology, 77: Hamel, J.-F., and Mercier, A. 1996c. Gonad morphology and gametogenesis of the sea cucumber Cucumaria frondosa. South Pac. Comm. Beche-de-Mer Bull. 8: Hamel, J.-F., and Mercier, A. 1996d. Gamete dispersion and fertilization success of the sea cucumber Cucumaria frondosa. South Pac. Comm. Beche-de-Mer Bull. 8: Jordan, A.J On the ecology and behavior of Cucumaria frondosa (Echinodermata: Holothuroidea) at Lamoine Beach, Maine. Ph.D. thesis, University of Maine, Orono. Lawrence, J.M A functional biology of echinoderms. Croom Helm, London and Sydney. Legault, C., and Himmelman, J.H Relation between escape behavior of benthic invertebrates and the risk of predation. J. Exp. Mar. Biol. Ecol. 170: Massin, C Effects of feeding on the environment: Holothuroidea. In Echinoderm nutrition. Edited by M. Jangoux and J.M. Lawrence. A.A. Balkema, Rotterdam. pp Runnström, J Heteromorphosen bei Larven von Parechinus miliaris und von Cucumaria frondosa. Bergens Museums Aarbok No. 15, Bergen, Norway. pp Runnström, J., and Runnström, S Über die Entwicklung von Cucumaria frondosa Gunnerus und Psolus phantapus Strussenfeld. Bergen Museums Aarbok No. 5, Bergen, Norway. pp Smith, T.B., and Keegan, B.F Seasonal torpor in Neopentadactyla mixta (Oestergren) (Holothuroidea: Dendrochirotida). In Proceedings of the 5th International Echinoderm Conference, Galway, Ireland, September Edited by B.F. Keegan and B.D. O Connor. A.A. Balkema, Rotterdam. pp Starr, M Mécanismes de coordination entre la ponte de certains invertébrés marins et la poussée printanière du phytoplancton. Ph.D. thesis, Université Laval, Ste-Foy, Que. Sutterlin, A.M., and Waddy, S Tentacle movement patterns involved in feeding behavior of the sea cucumber Cucumaria frondosa. Mar. Behav. Physiol. 4: Therriault, J.C., and Levasseur, M Control of phytoplankton production in the lower St. Lawrence Estuary: light and freswater run-off. Nat. Can. 112: Therriault, J.C., and Levasseur, M Freshwater run-off control of spatio-temporal distribution of phytoplankton in the lower St. Lawrence Estuary (Canada). In Proceedings of the NATO Freshwater Sea Workshop, Bodo, Norway. Edited by S. Skresled. Springer-Verlag, New York. pp A proposed three-host life history of Monascus filiformis (Rudolphi, 1819) (Digenea: Fellodistomidae) in the southwest Atlantic Ocean S.R. Martorelli and F. Cremonte Abstract: This is the first record of cercariae of Monascus filiformis (Rudolphi, 1819) and of Chaetognatha as a second intermediate host in the southwest Atlantic Ocean. The morphology of the sporocyst and cercaria from Nucula obliqua (Bivalvia: Nuculidae) and a full description of the metacercaria from hydromedusae are given. The life cycle of M. filiformis involves three hosts. The bivalve N. obliqua is the first intermediate host, Chaetognatha and medusae are the second intermediate hosts, and the jurel Trachurus lathami (Pisces: Carangidae) is the final host. The life cycle of M. filiformis occurs in shallow waters in the Argentine Sea and differs from Køie s experimental scheme for the North Sea in the addition of planktonic invertebrates as second intermediate hosts. The life cycle proposed here follows the general pattern given for the family Fellodistomidae. Received September 12, Accepted January 7, S.R. Martorelli. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Centro de Estudios Parasitológicos y de Vectores (Universidad Nacional La Plata-CONICET), calle 2 No. 584, 1900 La Plata, Argentina. F. Cremonte. 1 Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, Centro de Estudios Parasitológicos y de Vectores (Universidad Nacional La Plata-CONICET), calle 2 No. 584, 1900 La Plata, Argentina. 1 Author to whom all correspondence should be addressed ( postmaster@cepave.edu.ar/cepave@isis.unlp.edu.ar). Can. J. Zool. 76: (1998)

2 Notes 1199 Résumé : C est la première fois que des cercaires de Monascus filiformis (Rudolphi, 1819) sont observées et la première fois aussi que leur présence est constatée chez des chétognathes comme deuxièmes hôtes intermédiaires. On trouvera ici une description détaillée de la morphologie des sporocystes et des cercaires trouvés chez Nucula obliqua (Bivalvia: Nuculidae) et des métacercaires trouvées chez des hydroméduses. Le cycle de M. filiformis nécessite trois hôtes. Le bivalve N. obliqua est le premier hôte intermédiaire, les chétognathes et les méduses servent de deuxièmes hôtes intermédiaires et le poisson Trachurus lathami (Pisces: Carangidae) est l hôte terminal. Le cycle de M. filiformis se passe dans les eaux peu profondes de la mer Argentine et diffère du cycle décrit par Køie dans la mer du Nord en ce que des invertébrés planctoniques viennent s ajouter à la liste des deuxièmes hôtes intermédiaires. Le cycle décrit ici suit la séquence de développement généralement reconnue au sein de la famille des Fellodistomidae. [Traduit par la Rédaction] Introduction Sporocysts belonging to the family Fellodistomidae (Digenea) develop in bivalve molluscs and the daughter sporocysts normally give rise to motile furcocercous cercaria. The metacercariae occur in various invertebrates such as amphipods, molluscs, and echinoderms (Bray 1988). The subfamily Monascinae contains only the type genus Monascus Looss, Numerous species of the genus have been described, but several authors agree that these may be synonymous (Bray and Gibson 1980; Girola et al. 1992). This parasite appears to be cosmopolitan (Gaevskaya et al. 1985). About 52 findings of adult Monascus filiformis (Rudolphi, 1819) have been made around the world. The adult worms occur mainly in Carangidae (Pisces), although a wide range of other fishes are also infested. This parasite species has a wide distribution, which includes not only the Atlantic Ocean and the Mediterranean, Red, and Black seas, but also the Gulf of Mexico, the Mexican Pacific, and the coastal regions of India and the Arabian peninsula (Amato 1982; Gaevskaya 1990). Despite its widespread distribution, there are only two records of the metacercarial stage. One is from the English Channel (North Sea) in Sagitta setosa (Chaetognatha) (Øresland 1986) and the other was from the Argentine Sea (South Atlantic Ocean), where the metacercaria was found parasitizing four species of hydromedusae (Girola et al. 1992). There is a similar lack of information for the cercarial stage. It has been reported only three times. The first record of the cercaria is that of Odhner (1911), who found free cercariae in an aquarium with Nucula nucleus and Abra alba (Bivalvia) from the Baltic Sea. The second and third records are from the North Sea; Rees (1947) found cercariae in N. nucleus and Køie (1979) in Nucula nitidosa. According to Køie (1979), who studied the experimental life cycle of M. filiformis, the parasite has two alternative strategies. Worms may develop into adults in flatfish (e.g., Limanda limanda) that have eaten cercariae, or they may have a facultative intermediate host (e.g., goby) that is preyed on by larger definitive hosts such as Trachurus trachurus. The purpose of this paper is to describe the sporocyst and cercaria of M. filiformis in Nucula obliqua and report the finding of metacercaria in Sagitta sp. (Chaetognatha) from the Argentine Sea. In order to compare the cercaria recorded here, a full description of the metacercaria found in hydromedusae from the same waters by Girola et al. (1992) is given. A life cycle with two intermediate hosts is proposed. Materials and methods Nucula obliqua Lamarck, 1819 (Bivalvia: Nuculidae) were caught in June 1996 in ground nets at a depth of 10 m off the coast of Mar del Plata city (38 0 S, W), Argentina. The bivalves were fixed in 10% formalin, stored in 70% alcohol, and dissected under a stereomicroscope. Specimens of Sagitta sp. were obtained from plankton samples collected during the research cruises of the Eduardo Holmberg in May June 1985 in the Argentinian Uruguayan common fishing zone ( S, W). Metacercariae from the sample found in the hydromedusae Phyalidium sp., Liriope tethraphyla, Eucheilota ventricularis, and Aglauropsis kawari and analyzed by Girola et al. (1992) were studied. The larvae were stained with acetic carmine, cleared in creosote, and mounted in Canada balsam. The measurements are based on 10 specimens of each stage. Means and standard deviations, with ranges in parentheses, are given in millimetres. The drawings were made with the aid of a camera lucida. Results The sporocyst (Fig. 1) Furcocercous cercariae develop in thick-walled sporocyst ± 0.14 ( ) long ± 0.05 ( ) wide. Six to about 12 cercariae (mean = 10) at different developmental stages occur in each sporocyst. The cercaria (Fig. 2) Of the 23 clams examined, one was parasitized by sporocysts containing cercariae. The cercariae had not been released, but contained both primordia of the genitalia and welldeveloped furcae. Measurements of intrasporocyst cercariae: body ± 0.1 ( ) ± 0.05 ( ); oral sucker ± 0.02 ( ) ± 0.02 ( ); ventral sucker ± 0.01 ( ) ± 0.01 ( ). Oral sucker often with longitudinal aperture. Pharynx ± 0.01 ( ) ± 0.08 ( ). Oesophagus lined with tegument, long. Followed by pseudoesophagus about long lined with intestinal cells. Intestine bifurcates just posterior to the ventral sucker, forming short left caecum ± 0.01 ( ) long and right caecum, which reaches to posterior part of body, 0.15 ± 0.03 ( ) long; passes dorsally to the excretory vesicle. Both intestinal caeca lined with intestinal cells and both have a narrow lumen. Excretory vesicle Y-shaped; two voluminous branches reach to pharynx level. Tail attached perpendicular to body. Pore distally on each furca. Flame cell formula could not be determined because material had been fixed.

3 1200 Can. J. Zool. Vol. 76, 1998 Fig. 1. Sporocyst of Monascus filiformis from the clam Nucula obliqua in the Argentine Sea. Scale bar = 0.05 mm ( ) wide. Oesophagus ± 0.01 ( ) long, lined with tegument. Pseudoesophagus about ± ( ) long, lined with intestinal cells. Intestine bifurcates just posterior to ventral sucker into left caecum 0.04 ± 0.01 ( ) long and right caecum, which continues to posterior extremity of body, 0.12 ± 0.03 ( ) long; passes dorsally to excretory vesicle; apparently has no connection with excretory vesicle. Both intestinal caeca are lined with intestinal cells and both have a narrow lumen. Excretory vesicle Y-shaped; two voluminous branches reach to pharynx level. Primordia of the testes are found in tandem on the left side just posterior to bifurcation of excretory vesicle ± 0.17 ( ) long 0.04 ± 0.01 ( ) wide. Ovary pretesticular ± ( ) in diameter. Cirrus sac just anterior to and slightly left of ventral sucker. Atrium and genital pore left of cirrus sac and anterior to ventral sucker. Two specimens of Chaetognatha were parasitized by one and two unencysted metacercaria, very similar to the one described above. Discussion Primordia of testes in tandem on left side just posterior to bifurcation of excretory vesicle ± 0.01 ( ) long ± ( ) wide. Ovary pretesticular ± 0.01 ( ) long 0.01 ± 0.01 ( ) wide. Cirrus sac just anterior and slightly left of ventral sucker. Atrium and genital pore just left of cirrus sac and anterior to ventral sucker. Tail, measured from attachment to bifurcation, 0.92 long. Furcae 0.65 long. The metacercaria (Fig. 3) Body oval to subcylindrical 0.40 ± 0.04 ( ) long 0.2 ± 0.04 ( ) wide. Tegument smooth. Oral sucker ± 0.01 ( ) long ± 0.01 ( ) wide; aperture longitudinal and subterminal. Ventral sucker at midbody ± 0.01 ( ) long ± 0.01 ( ) wide. Pharynx ± 0.01 ( ) long ± This is the first record of the cercaria of M. filiformis and of the Chaetognatha as second intermediate hosts from the southwest Atlantic Ocean. The shape and measurements, both the cercaria and the metacercaria described here resemble the cercariae described by Rees (1947) and Køie (1979) (Table 1). Odhner s (1911) account of the larva is insufficient to allow comparison with the present specimens. Natural infestions of N. obliqua with sporocysts and cercariae, hydromedusae and Chaetognatha with metacercariae, and adults of the jurel Trachurus lathami Nicols, 1920 (Pisces: Carangidae) from the same area of the Argentine Sea suggest that the life cycle of M. filiformis involves three hosts (Fig. 4). The final host, T. lathami, acquires heavy infestions, presumably by eating medusae (Girola et al. 1992) and chaetognaths. This coastal pelagic fish shows an overlapping distribution with the infested hydromedusae (Pacheko-Tack 1988; Girola et al. 1992). Cavalieri (1963) recorded large numbers of the chaetognath Sagitta friderici Ritter-Záhony, 1911 in the stomach of T. lathami from the Mar del Plata area. The author stated that S. friderici inhabits the neritic zone, generally in shallow waters, and proposed that this chaetognath may be an important food for jurel. In the present study, the first intermediate host of this parasite is N. obliqua. The cercariae described by Rees (1947) and Køie (1979) were parasitizing the clams N. nucleus and N. nitidosa, respectively. It is highly likely that the clam infested with M. filiformis in Odhner s (1911) aquarium was N. nucleus and not A. alba. If so, this suggests that M. filiformis shows some specificity for bivalves of the genus Nucula as first intermediate host. The fact that the penetration glands and cystogenous gland cells are absent in the cercaria indicates that the metacercarial stage is brief and that no encystment takes place. This observation agrees with that of Rees (1947). Unencysted metacercaria would be the natural transmission mechanism. To date, all metacercariae found in gelatinous plankton are unen-

4 Notes 1201 Fig. 2. Cercaria of Monascus filiformis from the clam Nucula obliqua in the Argentine Sea, dorsal view. Scale bars = 0.05 mm. (a) Detail of body. (b) Complete specimen. Fig. 3. Metacercaria of Monascus filiformis from a hydromedusa in the Argentine Sea, ventral view. Scale bar = 0.05 mm. Table 1. Measurements (mm) of cercariae of Monascus filiformis by other authors. Rees 1947 Køie 1979 Body Tail (with furca) Oral sucker (diam.) Ventral sucker (diam.) Pharynx Left caecum Not seen cysted, with the single exception of the fellodistomid metacercaria found by Martorelli (1996). The second intermediate hosts, medusae and chaetognaths, may be infested by eating free-swimming cercariae. The high prevalence and intensity of unencysted metacercariae in hydromedusae, as reported by Girola et al. (1992), suggest that these invertebrates are the principal second intermediate hosts in the area under study. The importance of Sagitta sp. as a second intermediate host in these waters is still unknown. An examination of other zooplankton associated with the hydromedusae Phyalidium sp., L. tethraphyla, E. ventricularis, and A. kawari may shed some light on this matter. Based on the habitats of the above hosts, the life cycle of M. filiformis probably takes place in the shallow waters of the Argentine Sea. This life cycle differs from Køie s (1979) sug-

5 1202 Can. J. Zool. Vol. 76, 1998 Fig. 4. Proposed life cycle of Monascus filiformis in the Argentine Sea. gestions for the North Sea, based on experimental infestations, in that it adds invertebrate second intermediate hosts. The life cycle proposed here follows the general pattern for the family Fellodistomidae given by Bray (1988). Acknowledgments The authors gratefully acknowledge access to the collection of bivalves given by Dr. Rody Elías (Departamento de Ciencias Marinas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Argentina), identification of the bivalve specimens by Dra. Marina Aguirre (Departamento Científico Paleontología Invertebrados, Museo de La Plata, Argentina), and revision of the English version of the manuscript by Mariana Cremonte. References Amato, J.F.R Digenetic trematodes of percoid fishes of Florianópolis, southern Brasil Fellodistomidae, Monascidae, Diplangidae, Zoogonidae, and Waretrematidae with description of two new species. Rev. Bras. Biol. 42: Bray, R.A A discussion of the status of the subfamily Baccigerinae Yamaguti, 1958 (Digenea) and the constitution of the family Fellodistomidae Nicoll, Syst. Parasitol. 11: Bray, R.A., and Gibson, D.I The Fellodistomidae (Digenea) of fishes from the northeast Atlantic. Bull. Br. Mus. (Nat. Hist.) Zool. 37: Cavalieri, F Notas preliminares sobre Sagitta (Chaetognatha) del litoral atlántico Argentino. Presencia de Sagitta friderici Ritter-Záhony en el plancton eulitoral. Physis (B. Aires), 24: Gaevskaya, A.V Some comments on trematodes of the genus Monascus Looss, 1907 (Fellodistomidae). In Parasites of animals and plants. Edited by B.Y. Lebedev. Academy of Sciences of the USSR, Far-East Branch, Vladivostok. pp Gaevskaya, A.V., Kovaliova, A.A., and Rodjuk, G.N Parasitofauna of the fishes of the Falkland Patagonian region. NOAA Tech. Rep. NMFS 25. pp Girola, C.V., Martorelli, S.R., and Sardella, N.H Presencia de metacercarias de Monascus filiformis (Digenea, Fellodistomidae) en hidromedusas de Atlántico Sur. Rev. Chil. Hist. Nat. 65: Køie, M On the morphology and life-history of Monascus (=Haplocadus) filiformis (Rudolphi, 1819) Loos, 1907 and Steringophorus furciger (Olson, 1868). Ophelia, 18:

6 Notes 1203 Martorelli, S.R First record of encysted metacercariae in hydrozoan jellyfishes and ctenophores of the southern Atlantic. J. Parasitol. 82: Odhner, T Zum natürlichen System der digenean Trematoden. III. Zool. Anz. 38: Øresland, V Parasites in the chaetognath Sagitta setosa in the western English Channel. Mar. Biol. (Berl.), 92: Pacheko-Tack, R.L Contribución al conocimiento de la biología pesquera del surel Trachurus picturatus australis Nani, 1950 (Piscis, Fam. Carangidae) con algunas consideraciones ecológicas. Tesis doctoral, Universidad Nacional de La Plata, La Plata, Argentina. Rees, W.J A cercaria of the genus Haplocadus from Nucula nucleus (L.). J. Mar. Biol. Assoc. U.K. 26: The relative positions of the jaw joint and the tooth row in mammals Walter Stalker Greaves Abstract: The mammalian jaw joint almost always lies above the tooth row. A model is presented in which the moment arm of the resultant of jaw muscle force is held constant for a series of hypothetical jaw joints. Some of these joints lie above while others lie below the tooth row. The model initially considers the distance from the jaw joint to the last molar (J-M). This span is long when the joint is either high above or far below the tooth row. One can observe in the model that for animals with a posteriorly oriented muscle vector, J-M is shortest (i.e., perpendicular to the arrow representing the jaw muscle force) when the jaw joint is below the level of the tooth row. A short span might be expected in an animal if excess bone and its metabolic cost are to be minimized. Yet the joint is usually above the level of the tooth row in mammals. Therefore, the distance from the joint to molar J-M is almost always longer than expected in the large number of animals with a posteriorly oriented muscle vector. Another measurement of some importance is the distance from the jaw joint to the origin, on the skull, of the head of the arrow representing the muscle force (J-S). This distance is shorter when the joint is above and longer when the joint is below the tooth row. Minimizing the sum of J-M and J-S requires that the jaw joint be located at a point above the level of the tooth row. A high position for the joint corresponds to the actual architecture of mammalian skulls, and permits an economical structure without affecting the leverage of the masticatory apparatus. Résumé : Chez les mammifères, l articulation de la mâchoire est presque toujours située au-dessus de la rangée des dents. On trouvera ici un modèle dans lequel le bras du moment de la force résultante du muscle de la mâchoire est maintenu constant pour une série d articulations mandibulaires hypothétiques. Certaines de ces articulations hypothétiques sont situées au-dessus de la rangée de dents, d autres au-dessous. Le modèle considère d abord la distance entre l articulation et la dernière molaire (J-M). Cette distance est étendue lorsque l articulation est loin au-dessus ou loin au-dessous de la rangée de dents. Le modèle démontre que, chez les animaux dont le vecteur du muscle est orienté vers l arrière, la distance J-M est minimale (i.e., perpendiculaire à la flèche qui représente la force du muscle de la mâchoire) lorsque l articulation est située au-dessous de la rangée de dents. Théoriquement, la distance sera courte chez un animal si l ossature en excès et son coût métabolique doivent être minimisés. Cependant, l articulation de la mandibule chez les mammifères est ordinairement au-dessus de la rangée de dents. La distance de l articulation à la molaire J-M est presque toujours plus longue que prévu théoriquement chez la grande majorité des animaux dont le vecteur du muscle est dirigé vers l arrière. Également d une grande importance est la distance entre l articulation de la mâchoire et l origine, sur le crâne, de la flèche qui représente la force du muscle (J-S). Cette distance est plus courte lorsque l articulation est située au-dessus de la rangée de dents et plus longue lorsque l articulation est au-dessous de la rangée de dents. Pour minimiser la somme des distances J-M et J-S, l articulation doit être située à un point au-dessus de la rangée des dents. La position haute de l articulation correspond effectivement à l architecture réelle du crâne d un mammifère et donne lieu à une structure économique sans affecter la force de l appareil masticateur. [Traduit par la Rédaction] Received June 26, Accepted January 20, W.S. Greaves. Department of Oral Biology (M/C 690), University of Illinois, Chicago, IL 60612, U.S.A. ( wgreaves@tigger.cc.uic.edu). Can. J. Zool. 76: (1998)