The phylogeny of the genus Udonella has been disputed for quite some time, but recent phylogenetic
analysis of molecular data confirms that the genus is a monopisthocotylean monogenean. Specimens
of Udonella myliobati parasitizing the copepod Lepeophtheirus natalensis, an ectoparasite of
the spotted ragged-tooth shark, (Carcharias taurus) , were collected and studied. A total of 771
monogenean specimens were recovered from 54 infected copepods examined, with a mean intensity
of 14,3 worms per copepod. Most of the monogeneans were found attached to the dorsal surface
of the lateral and frontal marginal membranes of the copepod carapace. Eggs, with filaments
and adhesive discs, were found ventrally on the host, mainly attached to the maxillae and maxillipeds,
in clusters of 12-14. Observations on the morphology, distribution and behaviour of this monogenean
are presented with the aid of light and scanning electron microscopy.The articles have been scanned in colour with a HP Scanjet 5590; 600dpi. 
Adobe Acrobat v.9 was used to OCR the text and also for the merging and conversion to the final presentation PDF-format.University of the North (UNIN).mn201

Dippenaar, Susan M.

Khalil, L.F.

Mokgalong, N.M.

Olivier, P.A.S.

The articles have been scanned in colour with a HP Scanjet 5590; 600dpi. 
Adobe Acrobat v.9 was used to OCR the text and also for the merging and conversion to the final presentation PDF-format.The phylogeny of the genus Udonella has been disputed for quite some time, but recent phylogenetic
analysis of molecular data confirms that the genus is a monopisthocotylean monogenean. Specimens
of Udonella myliobati parasitizing the copepod Lepeophtheirus natalensis, an ectoparasite of
the spotted ragged-tooth shark, (Carcharias taurus) , were collected and studied. A total of 771
monogenean specimens were recovered from 54 infected copepods examined, with a mean intensity
of 14,3 worms per copepod. Most of the monogeneans were found attached to the dorsal surface
of the lateral and frontal marginal membranes of the copepod carapace. Eggs, with filaments
and adhesive discs, were found ventrally on the host, mainly attached to the maxillae and maxillipeds,
in clusters of 12-14. Observations on the morphology, distribution and behaviour of this monogenean
are presented with the aid of light and scanning electron microscopy.University of the North (UNIN).mn201

UPSpace at the University of Pretoria

Onderstepoort Journal of Veterinary Research, 67: 135-140 (2000) Observations on a lesser-known monogenean, Udonella myliobati, from a copepod parasite, Lepeophtheirus nataiensis, parasitizing the spotted ragged-tooth shark, Carcharias taurus, from South African waters PA.S. OLiVIER1 , S.M. DIPPENAAR, L.F. KHALIL and N.M. MOKGALONG Department of Zoology and Biology, University of the North Private Bag X11 06, SOVENGA, 0727 South Africa ABSTRACT P.A.S. OLIVIER, S.M. DIPPENAAR, L.F. KHALIL & N.M . MOKGALONG. 2000. Observations on a lesser-known monogenean, Udonella myliobati, from a copepod parasite, Lepeophtheirus natalensis, parasitizing the spotted ragged-tooth shark, Carcharias taurus, from South African waters. Onderste-poort Journal of Veterinary Research, 67: 135-140 The phylogeny of the genus Udonella has been disputed for quite some time, but recent phylogenetic analysis of molecular data confirms that the genus is a monopisthocotylean monogenean. Speci-mens of Udonella myliobati parasitizing the copepod Lepeophtheirus natalensis, an ectoparasite of the spotted ragged-tooth shark, (Carcharias taurus) , were collected and studied. A total of 771 monogenean specimens were recovered from 54 infected copepods examined, with a mean inten-sity of 14,3 worms per copepod. Most of the monogeneans were found attached to the dorsal sur-face of the lateral and frontal marginal membranes of the copepod carapace. Eggs, with filaments and adhesive discs, were found ventrally on the host, mainly attached to the maxillae and maxillipeds, in clusters of 12-14. Observations on the morphology, distribution and behaviour of this monogenean are presented with the aid of light and scanning electron microscopy. Keywords: Carcharius taurus, Lepeophtheirus natalensis, Monogenea, South Africa, Udonella myliobati INTRODUCTION All described species of the genus Udonel/a John-ston, 1835 are hypersymbionts found exclusively and commonly on caligid copepods parasitizing marine fish (Nichols 1975). In spite of their ubiquity, the phylogenetic position of Udonel/a has long been dis-puted and has kept many a systematist in discussion since the discovery of the type species. The type spe-cies, Udonel/a caligorum Johnson, 1835, was origi-nally regarded as a leech, but was later moved to the Monogenea. However, because it possesses a non-1 E-mail : olivierp@unin .unorth.ac.za Accepted for publication 26 April 2000-Editor ciliated larva and lacks hooks at any stage of devel-opment, some workers doubted its affinity to the Monogenea. The lack of hooks may be an evolution-ary result of its copepod association, whose hard exoskeleton is in all likelihood not suitable for hook penetration (Littlewood, Rhode & Clough 1998). Not-withstanding this, Udonel/a has some similarities to a rhabdocoelian turbellarian , and this led Ivanov (1952) to erect a new class, Udonelloidea, to accom-modate it. Ivanov & Mamkaev (1973) suggested that Udonel/a should be placed in a new order, Udonelli-da, which should be included with the neoophoran Turbellaria. This proposal was accepted by some workers, but rejected by others. Littlewood et al. (1998) concluded, after phylogenetic analysis of molecular data (from complete 188 rRNA and par-tial 288 rRNA genes of a variety of plathyhelminths), 135 Observations on lesser-known monogenean, Udonella my/iobati that u. caligorum is a monopisthocotylean mono-genean. They further suggested possible sister group status with the monogenean genus Gyrodactylus. This conclusion is also supported by previous ultrastructural studies of the tegument and some other structures, such as sensory receptors and spermatozoa (Aken'Ova & Lester 1996). The discovery of a species of Udonella, later identi-fied as Udonella myliobati (Guberlet, 1936), provided Aken'Ova & Lester (1996) with the opportunity to redescribe the species, elaborate on its behaviour and review the genus. The finding of this species in South African waters provided us with the chance of re-examining its morphological features and behav-iour. MATERIALS AND METHODS Caligid copepods, later identified as Lepeophtheirus natalensis Kensley & Grindley, 1973, were observed infecting the skin of live spotted ragged-tooth sharks (Carcharias taurus) in captivity in the aquarium of the Oceanographic Research Institute (ORI) in Durban, South Africa. The copepods were collected using a device, made by a technician at ORI, which operates like a vacuum cleaner. This device was gently applied to the skin of the sharks during a cage dive in the tanks. Collected parasites were preserved and fixed in 70 % ethanol. When the copepods were later ex-amined in the laboratory, they were found to be in-fected by monogeneans of the genus Udonella. Some detached monogeneans, as well as some copepods with attached monogeneans, were stained in Horen's trichrome stain, counterstained with alum carmine, mounted in Canada balsam and examined under a standard microscopy. Cleaning of copepod specimens for SEM studies was facilitated with the aid of a BRANSON 3200 ultrasonic cleaner after which the material (copepods and monogeneans) was dehydrated through graded ethanol (70-100 % at 5-1 0 min. intervals), critical point dried (CPO) and sputter-coated with gold. Measurements were taken from 20 mature specimens. All measurements are given in millimeters. DESCRIPTION Udonella my/iobati (Guberlet, 1936); Aken'Ova & Lester, 1996 Synonym: Calinella myliobati Guberlet, 1936 The total length of the elongated, sub-cylindrical body (Fig. 1 and 2), including the posterior haptor, is 1-1,24 with a maximum width of 0,24-0,42 at midbody. The terminal posterior haptor is more or less rounded, 0,22-0,232 x 0,24-0,248, and lacks hooks or any other structures (Fig. 3) . The anterior 136 FIG. 1 Udonella myliobati, whole mount, ventral view Scale bar = 0,2 mm; ad = adhesive disk; cg = cephalic gland; e = egg; f = filament; ho = head organ; ic = intes-tinal caecum; 0 = ovary; p = pharynx; ph = posterior haptor; t = testis; vf = vitelline follicle end of the body is notched to form two lateral lobes where the cephalic glands open into the head organs (Fig. 1). The glands are situated laterally in the an-terior quarter of the body. The mouth opening (Fig. 4) is subterminal, situated behind the indentation on the ventral surface at the anterior end of the body. The mouth opening leads to a well-developed, elon-gated , eversible pharynx, measuring 0,14-0,16 x 0,096-0,1. The intestinal caecum is large and sack-like, extending to near the posterior end of the body. Occasionally, the contents of the intestinal caecum are dark in colour and dark granules are seen to be expelled via the pharynx and mouth opening. The male reproductive system (Fig. 1) is represented by a single large, roughly round testis, measuring 0,108-0,12 in diameter, situated posterior to the ovary in the middle of the body. No cirrus or cirrus-sac is seen, but in some specimens a small seminal vesicle, the size of which varies from specimen to specimen, is seen near the genital pore. The genital pore is situated ventrally in the anterior quarter of the body (Fig. 4). The female genital system comprises a single large, round ovary, 0,14-0,156 x 0,064-0,07 in diameter. The vitellarium consists of large follicles, extending roughly from the level of the genital pore to the posterior end of the body (Fig. 1). In the re-gion anterior to the testis, the follicles are restricted to the lateral margins, but posterior to the testis the follicles fill the space on the dorsal side of the body. The pyriform-shaped egg (Fig. 5,6 and 8), 0,17-0,19 long with a maximum width of 0,064-0,070, is at-tached by a thin filament, 0,054-0,066 long, to a round adhesive disc, 0,052-0,06 in diameter. DISTRIBUTION AND OTHER OBSERVATIONS Very few male cope pods were recovered and none of these haboured any monogeneans. The percent-age of infected female copepods, randomly selected for inspection, was 100 %. A total of 771 monogene-ans of different stages of development were seen attached to 54 copepods, with a mean intensity of 14,3 specimens per copepod. The range of infection varied from one to 46 worms per copepod. Most of the worms, both mature and immature, were found on the dorsal surface of the carapace, attached to the lateral and frontal marginal membranes. Very few of them were attached to other parts of the cope-pod body (e.g. the genital complex), and even fewer were attached to the cope pod egg sacs. Most of the eggs were encountered on the ventral surface of the cope pod (Fig. 7), and were attached in clusters (Fig. 6) primarily to the maxillae and maxil-lipeds (Fig. 8). Very few eggs were attached to the first thoracic leg and occasionally single eggs were observed on other parts of the copepod body. The number of eggs in each cluster varied from 12-14. PAS. OLIVIER et al. Some of the eggs had hatched and only their empty capsules remained. Eggs have no operculum, and observations on the hatched eggs suggested that there possibly is a weak point in the structure of the FIG.2 Udonella myliobati, SEM micrograph, ventral view FIG.3 Udonella myliobati, SEM micrograph, posterior haptor FIG.4 Udonella myliobati, SEM micrograph, anterior end Abbreviations: m = mouth opening, g = genital pore 137 Observations on lesser-known monogenean, Udonella my/iobati anterior end of the egg capsule, which breaks as a result of pressure from the worm immediately before hatching. In the majority of hatched eggs, the ante-rior part of the capsule was very neatly detached, but only in a few cases the cut surface was torn (Fig. 6) . DISCUSSION Guberlet (1936) described Calinella myliobati at-tached to Trebius /atifurcatus Wilson, 1921 which parasitizes the stingray My/iobatis ca/ifornica from Monterey Bay, California. Although Price (1938) syn-onymized the genus Calinella Monticelli , 1910 with Udonella, he did not discuss the taxonomic status of C. my/iobati. Aken'Ova & Lester (1996) found some monogeneans attached to the copepod Caligus epi-demicus parasitizing the yellow-fin bream, Acantho-pagrus australis from Moreton Bay and other locali-ties in Australia. Their specimens closely resemble those of Guberlet (1936) and they suggested that C. myliobati be placed in the genus Udonella in a new combination. The five known species of Udonella (u. caligorum Johnston, 1835, U. my/iobati (Guberlet, 1936) , U. ophiodontis Kay, 1945, U. papillifera Van der Land, 1967 and U. murmanica Kornakova & Timofeeva, 1981) have all been collected from the caligid cope pod genera Caligus, Trebius and Lepe-ophtheirus, all known to parasitize marine fish. The present material closely resembles Aken'Ova & Lester's (1996) description of U. my/iobati, although the specimens are much larger in size with slight variation in the measurements of the various organs. In spite of this, we have no hesitation in identifying our specimens as U. myliobati. The present speci-mens were found attached to L. nata/ensis para-sitizing spotted ragged-tooth sharks (C. taurus) , and both represent new host records for U. myliobati. Moreover, this is the first geographical record of a species of the genus Udonella from the African seas. The four sharks examined, were in the shark tank at OR!. They were caught off the coast of Natal and had been in captivity for about 18 years. Other parasito-logical investigations of several shark species, in-cluding C. taurus, done at the facilities of the Natal Sharks Board, revealed L. nata/ensisfrom C. taurus. A few unidentified egg capsules were found on one of these cope pods, but none haboured any adult udonellids. Our average burden of 14,3 worms per infected fe-male cope pod was much higher than that of 5,8 found by Kabata (1973) for U. caligorum on Caligus e/ongatus, but less than the 38,7 found by Aken'Ova & Lester (1996). Minchin & Jackson (1993) found the infection rates of U. caligorum on Lepeophtheirus sa/monis highly variable, with the highest being 111 immature and nine adults on a single female copepod. It is, however, considered that the infection 138 FIG . 5 Udonella myliobati, egg with filament and adhesive disk. Scale bar = 0,02 mm FIG. 6 Udonella my/iobati, cluster of eggs and empty egg cap-sules Scale bar = 0,2 mm; s = smooth surface; t = torn surface rate we recorded is much less than the actual rate. The vacuum-like device used to collect the cope pods might have removed some but not all of the worms as many detached monogeneans were observed after preservation of the copepods. A similar obser-vation was made by Minchin & Jackson (1993) who noted some unattached specimens of U. caligorum from Lepeophtheirus sa/monis and C. e/ongatus. The distribution of species of Udonella and their eggs on the cope pod host varies considerably, and de-pends on both the species of Udonella and the cope-pod host species. Aken'Ova & Lester (1996) found that adult U. myliobati are more prevalent on the posterior half of the cope pod C. epidemicus than on the anterior part. Kabata (1973) and Aken'Ova & Les-ter (1996) further reported a high prevalence of adult worms on the genital complex, but no worms were FIG.7 Lepeophtheirus natalensis, lateroventral view showing attachment of adult Udonella my/iobati (laterally) and eggs (ventrally) FIG . 8 Eggs of Udonella my/iobati attached to the maxilla of Lepeophtheirus natalensis FIG.9 Udonella myliobati, whole mount, illustrating dark col-oured melanin of shark epithelial cells in the gut found attached to the ventral side of the copepod. Nichols (1975) found that adult worms of U. ca/i-gorum are more prevalent on the egg sacs of Lepe-ophtheirus longipes than on the carapace. In the present study adult and juvenile worms were more prevalent on the anterior part of the cope pod than the posterior part, and no worms were attached to the genital complex. Minchin & Jackson (1993) found adult worms on L. salmonis predominantly on the P.A.S. OLIVIER et al. dorsal posterior regions of the carapace, less fre-quently on the ventral surfaces and rarely on egg sacs. Adult and immature worms were also present predominantly on the dorsal carapace for U. ca/i-gorum collected from C. elongatus. Schram & Haug (1988) also observed a distribution of adult worms on L. hippoglossi very similar to that of the present study. Kabata (1973) found most of the eggs attached posteriorly on the genital complex and abdomen. Aken'Ova & Lester (1996) found 75 % of unhatched eggs on the ventral and marginal parts of the geni-tal complex. Our observation of egg distribution re-sembled that of Schram & Haug (1988) on Lepeoph-theirus hippoglossi who found that the eggs are attached to the underside of the copepod's carapace at the base of the appendages, particularly the max-illae, but not the genital complex. Minchin & Jackson (1993) found eggs to be distributed mainly on the dorsal and ventral surfaces of the three posterior tagma of the cope pod (fourth free thoracic segment, genital complex and abdomen). No eggs were re-ported attached to any of the cephalic appendages. Sproston (1946) suggested that species of Udonella are detritus feeders, taking mucus and gill epithelium of the fish "kicked" back by the copepod. It has also been suggested that the mainly marginal distribution of the monogeneans on the carapace of the cope pod enables feeding on superficial fish tissues (Kabata 1973). We believe that, in the present case, U. my/io-bati feeds directly on the epithelial cells of the skin of the shark. The dark colouration seen in the gut of the worms (Fig. 9) is possibly due to melanin from the shark epithelial cells in the diet. Udonella species, in common with other monopisthocotylean mono-geneans, are epithelial browsers. This is very simi-lar to the case of the monogenean Macrogyrodacty-Ius polypteri parasitic on the skin of the fish Polypterus senegalus, in which Cable, Harris & Tinsley (1997) have clearly demonstrated, using histochemical tech-niques, that the dark colouration of the gut is due to the presence of melanin . Some of our specimens of U. my/iobati were seen expelling dark granules via the pharynx and mouth opening, similar to those described for M. polypteri, as noted by Khalil (1970) . ACKNOWLEDGEMENTS The authors acknowledge the Oceanographic Re-search Institute for their role in the collection of the material. We are also grateful for financial assistance received from the University of the North (UNIN), the use of research facilities of the Department of Zool-ogy and Biology, and support from the Electron Mi-croscope Unit at UNIN . Mr R. Sandrock of the Instructural Support Services at UNIN is acknowl-edged for the processing of photographic material. 139 Observations on lesser-known monogenean, Udonella myliobati REFERENCES AKEN'OVA, T.O. & LESTER, R.J.G. 1996. Udonella myliobati n. comb. (Platyhelminthes: Udonellidae) and its occurrence in eastern Australia. Journal of Parasitology, 82: 1 017-1 023 . CABLE, J. , HARRIS, P.O. & TINSLEY, R.C. 1997. Melanin depo-sition in the gut of the monogenean Macrogyrodactylus polypteri Mamberg, 1957. International Journal for Parasitol-ogy, 27:1323-1331. GUBERLET, J.E. 1936. Two new ectoparasitic trematodes from the stingray, Myliobatis californica. American Midland Natural-ist, 17:954-964 . IVANOV, A.V. 1952. Structure of Udonella caligorum Johnston , 1835 and the position of Udonellidae in the system of flatworms. Parazitologicheskij Sbornik, 14: 112-163. IVANOV, A.V. & MAMKAEV, V. 1973. Ciliary worms (Turbellaria) , their origin and evolution ; phylogenetic outline, in Guide to the parasites of fishes of Canada, Part I, edited by L. Margolis & Z. Kabata . Canadian Special Publication of Fisheries and Aquatic Sciences, 74:1-209. KABATA, Z. 1973. Distribution of Udonella caligorum Johnston, 1835 (Monogenea: Udonellidae) on Caligus elongatus Nordmann, 1832 (Copepoda: Caligidae). Journal Fisheries Research Board of Canada, 30: 1793-1798. 140 KHALIL, L.F. 1970. Further studies on Macrogyrodactylus poly-pteri on the African freshwater fish Polypterus senegalus. Jour-nal of Helminthology, 64:329-348 . LlTILEWOOD, D.T.J. , ROHDE, K. & CLOUGH, KA 1998. The phylogenetic position of Udonella (Platyhelminthes). Interna-tional Journal of Parasitology, 28:1241-1250. MINCHIN, D. & JACKS,ON, 0.1993. Udonella caligorum John-ston , 1835 (Platyhelminthes: Udonellidae) associated with caligid cope pods on farmed salmon, in Pathogens of wild and farmed fish: sea lice, edited by G.A. Boxshall & D. Defaye. (Ellis Horwood Series in Aquaculture and Fisheries Support) . NICHOLS, K.C. 1975. Observations on lesser-known flatworms: Udonella . International Journal for Parasitology, 5:475-482 . PRICE, E.W. 1938. North American monogenetic trematodes II , the families Monocotylidae, Microbothriidae, Acanthocotylidae and Udonellidae (Capsaloidea) . Journal of the Washington Academy of Sciences, 28:183-198. SCHRAM , T.A. & HAUG, T. 1988. Ectoparasites of the Atlantic halibut, Hippoglossus hippoglossus (L.) From northern Nor-way-Potential pests in halibut aquaculture . Sarsia, 25:213-227. SPROSTON , M.G. 1946. A synopsis of the monogenetic trem-atodes. Transactions of the Zoological Society, London, 25: 185- 600. 

Observations on a lesser-known monogenean, Udonella myliobati, from a copepod parasite, Lepeophtheirus natalensis, parasitizing the spotted ragged-tooth shark, Carcharias taurus, from South African waters

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Observations on a lesser-known monogenean, Udonella myliobati, from a copepod parasite, Lepeophtheirus natalensis, parasitizing the spotted ragged-tooth shark, Carcharias taurus, from South African waters

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