PARASITOLOGY B MONOGENEAN FISH PARASITES 10µm AR: AR: b SCALE SCALE Monogenean parasites of fishes have remarkable adaptations to parasitism, but according to Dr Graham Kearn these fascinating organisms are virtually unknown to naturalists MONOGENEANS THE ULTIMATE FISH PARASITES 28 / the biologist / Vol 58 No 2 MAIN IMAGE, LEFT Fig. 4. A lateral view of the haptor of Tetraonchus monenteron from pike gills, showing one of the two lateral pairs of large hooks that impale the gill leaflets by counter-rotation. Photo: Richard Evans-Gowing by scanning electron microscope. Scale bar: 10µm. Reproduced from Kearn (2004) with kind permission of Springer Science and Business Media. © Springer 2004 nyone who has gone bIOgraphy elasmobranchs) as well as bony material or pollution enters the gill pond-dipping will be fishes (teleosts). One of the largest chamber, parasites may also be familiar with monogeneans, measuring up to subjected by their hosts to ‘coughing’ planarians. They glide 2cm in length, is Entobdella pulses, in which the strength of the with no apparent effort hippoglossi from the skin of water flow may be suddenly and Aacross the substrate, propelled as if the halibut. It was also the first briefly increased and its direction on a magic carpet by microscopic monogenean to be recorded, temporarily changed. Thus a parasite motile hairs (cilia). Planarians are by Müller in 1776, but a satisfactory must at all times attach itself securely flatworms (platyhelminths) and are Dr Graham Kearn description was not published to the gills and be capable of resisting free-living (non-parasitic), but many was awarded the until 1858 by Van Beneden, the extra stresses generated during of their relatives have embarked on a degree of D.Sc whose excellent illustration ‘coughing’ episodes. It might be parasitic lifestyle. Some of us may (University of is reproduced in Fig. 2. thought that attachment to fish skin recall from our school days the Birmingham) A surprising recent discovery is would be less challenging, especially in 1974 and was complex life cycles of other parasitic visiting fellow in that Atlantic halibut hosts a second if the host is a flatfish or a fish that flatworms, the pork tapeworm, the Department species of Entobdella (Kearn et al. spends part of the day resting. Taenia solium, and the sheep liver of Parasitology, 2007). This parasite, named However, flatfishes are capable fluke, Fasciola hepatica. Few, University of Entobdella vanbenedeni, is as big of sudden bursts of speed and however, are familiar with Queensland, as, sometimes bigger than, attachment organs of skin parasites Australia in monogeneans, despite the fact that E. hippoglossi. The two parasites must meet these challenges. 1975-1976 and most common fishes harbour one or again in 1990-1991, are superficially similar, but Hooks are the ‘hallmark’ of more species of these parasites and the Seto careful comparison reveals monogeneans. These elegantly (Table 1, page 34). Marine Biological consistent differences in anatomical shaped structures (Fig. 3) occur at As summarised by Kearn (1998, Laboratory, detail that have gone unrecognised the posterior end of the body on a 2004) most monogeneans live on University of Kyoto, since the 18th century. muscular, often disc-shaped Japan in 1990. the skin (Fig. 1) or gills of fishes and He is the author of Two groups of monogeneans make attachment organ called the haptor many are host specific, i.e. each more than 130 an especially large contribution to (Fig. 2). Hooks are of two sizes: up to monogenean species is restricted to research papers our freshwater fauna. These are 16 tiny hooklets, ranging in length a single, or to one or two closely and review articles dactylogyrids, gill parasites that from about 7 to 40 µm, arranged related fish species (Table 1). The and two books. have speciated extensively on fish radially on the haptor disc, and consequence of this phenomenon of the carp family (Cyprinidae), and one or two pairs of more massive is that, following a cursory gyrodactylids, found on the skin and hooks (Fig. 4), which may reach examination of a detached parasite gills of many of our freshwater fishes 0.5mm in length. The hooklets in the absence of the host, a specialist and also on some marine hosts. mainly serve to pin the small larva to is often able to name the host fish. Dactylogyrids and gyrodactylids lie the delicate outer layer of cells Life cycles of tapeworms and at the other (epidermis) of the host’s skin, while flukes involve at least two hosts, but end of the size spectrum from the larger hooks may pass through monogeneans have relatively simple E. hippoglossi, ranging in length the epidermis into the thicker and cycles with only one host. They from 0.5 to 2mm. tougher inner layer of the skin or spread directly from fish to fish A monogenean lives in the bladder dermis, providing anchorage for the either by way of freely swimming of our common frog, Rana much larger adult parasites. larvae (oncomiracidia) propelled temporaria, and others infect by cilia, or by contagion, adult or chelonian reptiles (terrapins). juvenile parasites transferring Another occursin what seems a between fishes when they make most unlikely habitat, beneath the contact. Others infect Chelonian eyelids of the hippopotamus. reptiles (terrapins). Marine hosts Table 1 (page 32) shows a selection include Attachment of common British marine and sharks and Gill parasites are continually freshwater fishes and their rays as well exposed to strong gill- monogenean parasites. Marine hosts as bony fish ventilating currents generated include sharks and rays by their fish hosts. On (cartilaginous fishes or occasions when particulate Vol 58 No 2 / the biologist / 29 PARASITOLOGY B MONOGENEAN FISH PARASITES Some skin parasites like Entobdella use movements of the large hooks embedded in the haptor to generate suction. The gill parasite Tetraonchus uses counter-rotation of its two lateral pairs of large hooks (Fig. 4) to impale the bases of two adjacent gill leaflets (the tiny flaps that contain blood and extract oxygen from the Fig. 1. The lower surface of a common sole (Solea solea) infected gill-ventilating current). by two adult specimens of the monogenean Entobdella soleae. But it is among the gill parasites of Colour lithograph from a water-colour by Annie Willis in bony fishes that bio-engineering has Cunningham, 1890. reached an exceptional level. Some Fig. 2. An early drawing by Van Beneden (1858) of Entobdella of these lowly flatworms have hippoglossi – the first monogenean to be described. developed three or four pairs of Note posterior, saucer-shaped sucker (haptor) with clamps, each with two opposable embedded hooks. semi-circular jaws capable of (a) grasping one or two gill leaflets For Fig. 4 (Fig. 5). Some of these gill parasites see main image Fig. 5. (a) A clamp- are asymmetrical. For example page 28 bearing monogenean, Pseudaxine trachuri on horse Diclidophora minor (Scale bar: 1 mm) mackerel, Trachurus trachurus, has and (b) an enlarged 25 or more clamps on one side of the view of a clamp body (Fig. 6). The parasite must (Scale bar: 100 µm). possess a surprisingly sophisticated Image Dr Paul sensory/motor system to co-ordinate Thomas. the operation of these clamps. The sizes of Tetraonchus and related parasites are limited by the (b) need to fit between two adjacent gill leaflets, but no such restriction applies to the clamp-bearing parasites and many of them are large, from 0.5 to 1cm long (Figs. 5–7). Fig. 3. A variety of monogenean hooks Feeding (not to scale). Skin parasitic monogeneans like Entobdella soleae feed on host Fig. 7. Two fused individuals epidermal cells. A large protrusible of Diplozoon paradoxum. glandular pharynx is used to erode Scale bar: 1 mm. and ingest host epidermis. Image Dr Paul Thomas. Monogeneans have no blood system and intestinal branches transport nutrients to remote parts of the body. The parasites exploit the wound healing properties of host epidermal cells, which migrate from the edge of the feeding wound and repair the lesion. Damage inflicted at a single feeding site by E. soleae probably heals within 24 hours. Damage to the host in the wild is therefore minimal, but this is not the case in fish farms and aquaria. Gill parasites like Tetraonchus also feed on epidermis but the larger clamp-bearing gill parasites like Diclidophora and Pseudaxine ingest blood, as indicated by intestinal Fig. 9. An adult Polystoma deposits of the indigestible brown or Fig. 6. Pseudaxine trachuri, an Fig. 8. A living larva of integerrimum from the black pigment haematin derived asymmetrical clamp-bearing Entobdella soleae. bladder of a common gill parasite. Note brown or frog. Scale bar: 1 mm. from host haemoglobin (Fig. 6). black pigment (haematin) Specimen donated derived from ingested host by Professor Locomotion and mating blood. Scale bar: 500µm. Richard Tinsley. All monogeneans, with the exception Image Dr Paul Thomas. Image Dr Paul Thomas. of clamp-bearing monogeneans, are 30 / the biologist / Vol 58 No 2 capable of moving from place to place monogeneans lay eggs. These eggs reached by its anterior adhesive pads. on the host in the manner of a leech. have shells made of a tough protein In this case the identity of the E. soleae has adhesive glandular pads called sclerotin and are released into chemical hatching stimulus is known on the head that are used for the sea, lake or river. The larva, – it is urea, a waste product of protein temporary attachment when the usually ciliated, embryonates inside metabolism that is retained in the parasite changes the location of its the egg. A detachable lid or bodies of sharks and rays and has an haptor.