PARASITOLOGY B MONOGENEAN PARASITES 10µm AR: AR: B SCALE SCALE

Monogenean parasites of have remarkable adaptations to , 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 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 (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 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 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 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 , 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, trachuri on horse Diclidophora minor (Scale bar: 1 mm) , 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. , 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. Two secreted components are operculum permits the larva to important role in water balance. thought to interact like an epoxy- escape into water where it is Because of this quirk of physiology, resin to attach the head to fish skin propelled by beating cilia. This tiny urea is present in relatively large (Kearn & Evans-Gowing 1998). This larva is only 0.25 mm long in quantities in elasmobranch skin cement is remarkable in that fish skin Entobdella soleae, just visible to the secretions and Acanthocotyle has is wet and slimy and yet the bond is naked eye (Fig. 8), and has the task of exploited this unusual metabolic very strong. When the locomotion locating and attaching itself to the feature for host location. step is completed and the haptor host. Since most monogeneans are Unhatched larvae of other species reattached, the parasite can break specific to only one or two closely respond to different host-derived the adhesive bond instantly. related hosts, this is a very cues. The eggs of the skin parasite There is no need for monogeneans demanding task. Neoentobdella diadema hatch within to move to find food since, whether We know more about how this is seconds in response to shadows cast their diet is epidermis or blood, it is a achieved in E. soleae than in any by cruising or resting stingrays. renewable resource that is always other monogenean. Its host, the Eggs of the gill parasite Diclidophora within reach. It is more likely that common sole, is a nocturnally active luscae are stimulated to hatch locomotion creates opportunities flatfish that spends the daylight by disturbance created as their for sperm exchange between the hours partly buried in sediment at fish hosts (pouting, Trisopterus hermaphrodite adults. Some the sea bed. Adult parasites are luscus) forage. monogeneans, like Entobdella, typically found on the unpigmented The viviparous gyrodactylids exchange spermatophores (packages lower surface of the sole (Fig. 1). The have no cilia and parasites transfer containing sperm) and some, eggs of the parasite hatch at dawn or either directly to new hosts when like Diclidophora merlangi, use soon after and the larvae have all the fishes make contact or by way of ‘hypodermic impregnation’. Others hours of daylight to make contact the substrate as a staging post mate in the conventional way. Adult with a resting sole. Each day, while (Bakke et al. 2007). clamp-bearing monogeneans have fully embryonated eggs are still become sedentary, posing the available, small numbers of larvae Polystoma and the common frog question of how sperm exchange is will emerge at dawn, thereby We have only one native achieved. We know little about their spreading hatching over a period of monogenean parasitising reproductive biology but some adults, days to maximise the chances of in Britain, namely like Diclidophora merlangi, tend to some of them meeting a resting sole. Polystoma integerrimum (Fig. 9). It cluster on the gills and individuals But the parasite has a second option. is a relative of the clamp-bearing gill are sufficiently extensible to make If a sole should settle near fully parasites of fishes but inhabits the contact with each other. embryonated parasite eggs, an bladder of the common frog Rana The freshwater gill parasite unknown chemical (or chemicals) in temporaria, where it attaches, not by Diplozoon paradoxum goes further: the mucus stimulates hatching clamps, but by three pairs of haptor two individuals fuse so that their within 5 minutes, with every chance suckers. A link with the clamp- reproductive ducts communicate that the newly released larvae will bearers is provided by its diet, which permanently (Fig. 7). This unique establish themselves on the host that is blood extracted from blood and remarkable development is provided the stimulus. Once attached vessels in the bladder wall. reflected in the name ‘Diplozoon’, by the haptor and its ring of hooklets, The common frog spends most meaning ‘double ’. the cells bearing cilia that enabled of its time on land, entering water It is advantageous for a sedentary the larva to swim are jettisoned. for just a few weeks in the spring parasite to interact as little as Larvae of E. soleae rarely attach to to breed. Like most other possible with host gill flow to other flatfish species and this strong monogeneans, Polystoma has a reduce the risk of dislodgement selective ability seems to have a free-swimming ciliated larva and and interference with host gaseous chemical basis. egg production and egg laying are exchange. This requires streamlining Many other monogeneans have restricted to the spring period of the body of the parasite. Since rhythmical hatching patterns, but spent by the frog in water. many of these parasites are exposed It is among chemical stimulation of hatching has The larvae attach themselves to a unilateral water current, the gill gone further in species of not to the adult frog but to the gills streamlining can only be achieved by parasites of Acanthocotyle living on the skin of of the tadpole, providing another adopting an asymmetrical shape bony fishes rays. The larvae of Acanthocotyle are link to the gill parasites of fishes. (Fig. 6). Clamps on one side of the unable to swim (they have no cilia) They remain on the gills of the body are attached upstream and that bio- and fail to hatch spontaneously. If a tadpole until host metamorphosis those on the other side of the engineering host ray settles on top of the eggs on takes place and the young frog body are lost. has reached the sea bottom, ray mucus induces leaves the water. At this time the an exceptional hatching in seconds. The larva does larvae leave the gills and migrate Finding a host level not need to swim since by greatly to the bladder where they reach With the exception of gyrodactylids, elongating its body the lower skin sexual maturity and spend the rest which give birth to living young, of the resting host can usually be of their lives. Host hormones

Vol 58 No 2 / the biologist / 31 PARASITOLOGY B MONOGENEAN FISH PARASITES

circulating in blood and accessible individuals rarely carry more than monogeneans can pose a real threat to the parasites in their diet may two or three relatively small adult in situations where fish are confined switch on egg production in the parasites, each up to 5 or 6 mm in as in fish farms and public aquaria. adult parasite and migration of length (Fig. 1). Gyrodactylid monogeneans give larval parasites at host birth to unciliated adults that metamorphosis. Threats from monogeneans establish themselves on the same However, in aquaria the host individual (autoinfection). As Host/parasite co-evolution populations of parasites on captive a result, they avoid the mortality to Amphibians may have inherited soles increase rapidly, since which free-swimming larvae are monogeneans like P. integerrimum invasion success of their free- subjected and populations on from their fish ancestors by a swimming larvae is much higher individual hosts initially increase process of co-evolution. As the hosts than in the open sea. There is a rapidly, even in the wild. However, evolved and speciated, their margin of safety because captive many hosts are able to limit this parasites correspondingly soles can support two or three expansion and may even eliminate speciated, leading to a congruence dozen adult parasites with no the infection by mechanisms that are between lineages of host and obvious ill effects. But the host not yet fully understood (Bakke et al. parasite. On the other hand, Each major seems incapable of preventing 2007). Hosts unable to limit parasite amphibians could have acquired group of further population increase and numbers are unlikely to survive. For their monogeneans by host fish-like unless the sole is treated example, Gyrodactylus salaris is switching, in which a parasite vertebrates (freshwater kills marine notorious as a killer of freshwater transfers from one host (a has its own monogeneans rapidly), the parasite salmon parr ( salar) in , freshwater fish) to an unrelated burden will increase exponentially not just in fish farms but also in the host (an ) sharing the special group and host epidermis will be removed wild, although brown trout (Salmo same environment. It is not easy of blood- faster than the host can replace it. trutta) are able to control the to determine which of these two feeding The osmotic (water) balance of parasite. Britain is currently free mechanisms was involved. monogenean affected fishes will be seriously of G. salaris. However, there can be no doubt gill parasites impaired and pathogenic that the parasite living beneath micro-organisms may gain entry, More reading and references at the eyelids of the hippopotamus leading ultimately to death. Thus www.societyofbiology.org/biologist reached this surprising habitat by host switching, since it is closely TABLE 1 Host common name Host scientific name Parasite Where related to frog parasites and is the A selection of only monogenean parasitising a common British mammal. Its name – Oculotrema fishes and their Marine hippopotami – indicates its host monogenean Common (Dover) sole Solea solea Entobdella soleae Skin parasites. and its strange habitat. Atlantic halibut Hippoglossus Entobdella hippoglossi Skin A fascinating fact is that each Hippoglossus Entobdella vanbenedeni Skin major group of fish-like vertebrates Mackerel Scomber scombrus Kuhnia scombri Gills has its own special group of blood- Kuhnia sprostonae Gills feeding monogenean gill parasites. Grubea cochlear Gills We have met just one of these Whiting Merlangius merlangus Diclidophora merlangi Gills parasite groups, the clamp-bearers Pouting Trisopterus luscus Diclidophora luscae Gills parasitising the bony fishes. The Blue whiting Micromesistius Diclidophora minor Gills implication is that ancestral blood- poutassou feeding monogeneans may have been Red gurnard Aspitrigla cuculus Plectanocotyle gurnardi Gills present on the ancestors of the fish- Grey gurnard Eutrigla gurnardus Plectanocotyle gurnardi Gills like vertebrates before these early Tub gurnard Trigla lucerna Plectanocotyle gurnardi Gills vertebrates diverged, perhaps as far Horse mackerel Trachurus trachurus Gastrocotyle trachuri Gills back as the Ordovician period Pseudaxine trachuri Gills (approximately 490 to 440 million Dogfish Scyliorhinus canicula Leptocotyle minor Skin years ago). This makes the dinosaurs Roker (Thornback ray) Raja clavata Acanthocotyle lobianchi Skin look modern. Stingray Dasyatis pastinaca Neoentobdella diadema Skin In spite of their hooks, clamps and suckers and their feeding activities, monogeneans have little impact on Freshwater their hosts in the wild. About half the Pike Esox lucius Tetraonchus monenteron Gills soles in the North Sea are infected by Grayling Thymallus thymallus Tetraonchus borealis Gills Entobdella soleae and infected Brown trout Salmo trutta sagittata Gills Rainbow trout mykiss Discocotyle sagittata Gills Bream Abramis brama Diplozoon paradoxum Gills Dactylogyrus auriculatus Gills 3-spined stickleback Gasterosteus aculeatus Gyrodactylus gasterostei Skin 9-spined stickleback Pungitius pungitius Gyrodactylus pungitii Skin Roach Rutilus rutilus Neodactylogyrus crucifer Gills

32 / the biologist / Vol 58 No 2 Do you have an opinion on this article? Contact us AT [email protected]