C T White Lecture for 1998

Parasites of Australian Wildlife: the Inside Story.

T. H. Cribb

Department of Microbiology & Parasitology, The University of Queensland, Brisbane AUSTRALIA 4072

It is a distinct pleasure for me to present the C T White Memorial Lecture for 1998 for three reasons. To begin with, C T White, Government Botanist and prominent member of the Queensland Naturalists’ Club was by all accounts a very fine scientist and man. C T White died young, at 60 in 1950, and so my knowledge of him is drawn from the obituary of him in the Queensland Naturalist and the Introductions to a series of other C T White lectures by those who did know him. Evidently, C T White was one of those outstanding naturalists with a broad knowledge of natural history combined with a detailed knowledge of his own field, and a capacity to lead and inspire those who he contacted. It is good to honour such people.

The second pleasure for me is in my own family tradition. The first C T White Lecture in 1951 was given by my maternal grandfather (Professor D. A. Herbert) and subsequent C T White lectures have been given by my mother (1968/9 – “Pollination”) and by my father (1973/4 - “Scents of the Bush”). So, apart from a departure from the subject of botany, it is a pleasure for me to take my turn in this succession (although together they comprise a hard act to follow).

My third pleasure is in a return to the Queensland Naturalists’ Club. Although I have been a member of the Club for (I fear) 30 years, I have not attended much for the last decade. I suppose that I have been doing “other” things but do feel a twinge of guilt in my non-attendance for all this time. Despite this, it was innumerable “Nat’s Club” trips in my youth that formed the basis of my knowledge of and interest in natural history. Indeed, it has been one of the pleasures of my adult scientific career to find myself revisiting sites that I had visited as a boy with the “Nats”.

Parasites

Parasites do not enter into the thinking of naturalists much. Many may see this as a good thing! The reason is that parasites are small, hidden and unpopular. The limited “exposure” that most people have to parasites does not help. The parasites that we are most likely to see or know about are not easily liked. If we see parasites at all it is likely to be fleas on our dogs and cats, ticks that we pick up on a bush-walk, or perhaps pinworms (nematodes) that infect children. I argue however, that, despite their bad press, parasites possess all the characteristics to fascinate the discerning naturalist. They are common (nearly ubiquitous), they are either beautiful or wonderfully ugly, and they often have exquisite adaptations in their biology and their life-cycles.

Parasitism

So what is parasitism? The standard definitions usually incorporate concepts relating to living in long-term or permanent association with a host and gaining shelter or food at the expense of that host. This seems simple enough, but it has some important implications for the general characteristics of parasites. Long-term association between host and parasite means that parasites are usually small relative to their hosts. If they were too large they would become predators that overwhelm their hosts very quickly. The essence of parasitism is usually to take sufficiently little of the host’s resources that the host will not die. In this sense parasites are forwarding-looking conservationists – only using renewable resources!

The second implication of the long-term association implied by parasitism is that it gives the host a chance to react to the parasite. This can be seen both in immediate and evolutionary terms. For example, consider the differences between the interaction between mosquitoes (micro-predators) and their prey and fleas (parasites) and their hosts. Mosquitoes are very delicate and easily killed, but if you are attacked by one you only have a few seconds in which to catch it. In contrast, a flea on your dog may be there for days giving ample opportunity for the dog to track the flea down and kill it – if it can! But, of course, fleas will run through the dogs hair very fast and they are tough and hard to squash. Thus the flea has both immediate behaviour that helps it evade its hosts responses and it has evolved morphology that protects it too.

Because parasites may be a serious drain on host resources it is important for the host to respond to the presence of parasites. They can do this in several different sorts of ways – behavioural, morphological and chemical. Behavioural defences include such simple activities as the washing of hands for humans. Morphological defences encompass the establishment of physical defences such as a thick skin that prevents the penetration of parasites. Chemical defences involve most importantly the immune system of higher vertebrates which generates complex and unique molecules that battle with foreign bodies including parasites. In effect, hosts never take being parasitised lying down.

That the responses of hosts to parasites is rarely completely successful in eliminating them is demonstrated by the fact that parasites are very common. Equally, however, parasites rarely completely overwhelm their hosts in nature (parasitism in the unnatural circumstances of farming and human society may be a different matter). This is because the parasites are responding to the hosts and the hosts respond to the parasites in what mounts to an endless loop of specialisation and counter-specialisation. An important implication of this pattern is that parasites tend to specialise their biology for a narrow range of hosts. This is host-specificity and it is a general feature of parasites that, in the main, the parasites of humans will not infect dogs, and those of kangaroos will not infect koalas.

As a life-style, parasitism has been a great success. Lots of groups of animals have adopted parasitism as a way of life. The proof of this success is in just how common parasites are. I back this statement with the claim that “All Australian species of mammals, birds, reptiles, frogs and fishes are infected with parasites.” This is actually quite a safe claim because it is practically impossible to disprove but still true, nonetheless. Perhaps surprisingly, humans are probably the single best host for parasites. We are known to be infested by fleas, lice, mites, ticks, bugs, flukes, round-worms, thorny-headed worms and myriads of protistan parasites. All in all, over 100 species of parasites have been recorded from humans. The reason for this is that, ultimately, humans go everywhere, swim or roll in everything, get bitten by everything, and, most importantly, eat just about everything, and eat it raw! The fact that the reader may have very few parasites does not change this. In fact, if we were to explore your history carefully, we would probably find that you had been infested with at least head-lice and human pinworms at some stage of your life. The more adventurous you have been (or the less hygienic depending on your perspective) the more parasites you are likely to have had! The lack of human parasites in modern Australia is the (unfortunate for the parasitologist) result of our hygiene, diet and public health measures.

It is not, however, the economically important parasites that interest me particularly. The interest of my research and the rest of this essay is the parasites of Australian wildlife.

Australian wildlife parasites

It is a truism that Australia has a rich and unique fauna – but how many have thought about the menagerie of parasites that every kangaroo, kookaburra and carpet snake carries around with it? Our wildlife has many different types of parasites which can, broadly, be divided into two ecological types – the external and the internal. The external parasites include groups such as fleas, lice, mites and parasitic crustaceans. Because they are external, these tend to be the parasites that are known best to the casual observer. The internal parasites include mainly protistan parasites (single-celled and really too small to bother with!) and the worms or helminths. Amongst the internal parasitic worms there are four major groups – the nematodes (roundworms), the cestodes (tapeworms), the acanthocephalans (thorny-headed worms), and the trematodes (flukes). In entitling this address as I have, I have consciously headed it towards a consideration of the helminths and this last group, the trematodes.

Trematodes

The trematodes or flukes are one of the five major groups of helminths together with the Nematoda, Acanthocephala, Monogenea and Cestoda. Each of these groups is, naturally enough, distinguished by its own particular patterns of morphology, life-cycle and resulting distribution among animals. In Australia none of these groups can be said to be well-known. Perhaps each group has a claim to be least-known in some respects and perhaps

Trematodes comprise a class of the Phylum Platyhelminthes, the “flatworms”. Adult trematodes occur in all classes of vertebrates (fishes, amphibians, reptiles, birds and mammals) and usually in the gut or its outgrowths. The life cycle generally requires two, three or more hosts, but a few have secondarily reduced life cycles so that adults occur in invertebrates. First intermediate hosts are molluscs usually snails or bivalves and these can be marine, freshwater or terrestrial. Asexual reproduction occurs in the first intermediate host in generations of sporocysts and rediae which lead, ultimately, to the production of tailed juveniles of the sexual generation known as cercariae. The cercaria usually leaves the first intermediate host and may attach to, be eaten by, or penetrate the definitive host directly. Alternatively, the cercaria may encyst in the open or encyst in a second intermediate host to be eaten ultimately by the definitive host. Because of its complexity and variability, knowledge of the life cycle is important to reaching an understanding of the biology and taxonomic position of trematodes. best-known in some others but, in general, the trematodes probably symbolise much of what we know and don’t know about the parasites of Australian animals.

Diversity

One of the striking features of parasites is the way in which they have been able to exploit a very wide range of host types and sites in their hosts. Trematodes exemplify this phenomenon well. The majority of trematodes occur in the gut of their hosts (Figs 1 A-C) but they may occur in the hearts of turtles (1D), in the urinary bladder of fishes (1E), the liver of bandicoots (1F), and under the scales of fish (1G). Further, we see dramatic differences in their size and shape. One species, Baiohelmins elegans from the intestine of the water rat (Hydromys chrysogaster) is tiny, no more than a third of a millimetre in length; the largest species are measured in cm or even, in the case of some remarkable thread-like species, metres!

The dependence of trematodes on a mollusc in their life-cycle has a marked affect on the distribution of trematodes among vertebrate hosts. Put simply, trematodes occur in greatest numbers in marine and freshwater systems where molluscs are abundant, although a few families have adapted successfully to infect terrestrial molluscs and vertebrates.

Much of my research is directed towards the detailing of the diversity of trematodes in Australian wildlife. This entails the collecting of specimens, identification and often description of the species, and exploration of the biology of the species in terms of life-cycles, host-specificity, distribution and relationships. It is a big task. The table below shows roughly how many species of vertebrates there are in the various classes and how many species of trematodes are known from each group.

At present there are about 566 species known and, clearly, they are distributed (though unevenly) among all the classes of vertebrates. This number of species is comparable with the number of species of birds in Australia (and will certainly soon exceed it) yet whereas there are dozens, perhaps hundreds of biologists and naturalists with a good knowledge of Australian birds, there are only a handful who know anything about their trematode parasites. Although it is certainly true that we know the parasites of no group of Australian animals comprehensively, the greatest amount of work has gone into those of birds and mammals. This is understandable because these were the first animals that scientists took an interest in when systematic biological work began in Australia. In fact, whereas there are very few undescribed birds and mammals in Australia, new species of fish are still be recognised quite regularly. It is in the fish that the greatest amount of parasitological work remains to be done. The 3300 species of teleosts (bony fishes) known from Australian waters comprises about 60% of our vertebrate fauna. Ongoing studies suggest that practically every species of fish is infected with trematodes yet they have been reported from only about 10% of the species. Current estimates suggest that there may be as many as 5,000 species of trematodes in Australian teleosts alone and perhaps 6,000 in all Australian vertebrates. Such estimates are very vague and uncertain but what is unarguable is that we still know our parasite fauna very poorly.

Isoparorchis hypselobagri

Isoparorchis hypselobagri is a giant trematode found in the swim-bladder of freshwater catfish (Tandanus tandanus) in Australia. It was perhaps the first trematode from an Australian fish to be recognised by a European biologist. In his journal of his famous 1844-5 expedition from Moreton Bay in south-east Queensland to Port Essington in the Northern Territory, Ludwig Leichardt refers to a trematode from the Dawson River as follows:

The water-holes abounded with jew-fish and eels; of the latter we obtained a good supply, and dried two of them, which kept very well. Two species of Limnaea, the one of narrow lengthened form, the other shorter and broader; a species of Paludina, and Cyclas and Unios, were frequent. The jew-fish has the same distoma in its swimming bladder, which I observed in specimens in the Severn River to the southward of Moreton Bay : on examining the intestines of this fish they were full of the shells of Limnaea and Cyclas.

This record was undoubtedly Isoparorchis hypselobagri – there is simply no other species with which it could be confused. In some respects it might could be considered that this was an easy species for Leichardt to find because it is so large (about 5 cm long) but this is ungenerous. Leichardt was in the midst of a biological treasure-trove where practically everything was poorly known. I find it impressive that his interests were sufficiently broad to encompass both the parasites and the diet of the fish that he collected.

This species has a special interest for me because it was one of the first parasites that I studied, and many aspects of its biology remain unresolved. The species was originally described as a unique Australian species Isoparorchis tandani but later it was concluded that it was the same species as is known from the swim bladders of other catfish species across much of Asia. However, in Asia this parasite is known to have a complex four-host life-cycle involving snails as 1^st intermediate hosts, amphipods as 2^nd intermediate hosts, small fish as 3^rd intermediate hosts and the catfish as the final (or definitive) host. This life-cycle cannot work in Australia because Tandanus tandanus never eats fish. Instead it appears (this has not been demonstrated definitively yet) that the life-cycle involves snails as 1^st intermediate hosts, shrimps as 2^nd intermediate hosts, and the catfish as both 3^rd intermediate hosts (the worms have a complex migration in them) and definitive host. This appears to be a clear specialisation of the parasite to local conditions. At this stage it is still uncertain whether this parasite should be considered uniquely Australian or just a variant of the Asian species.

Another striking feature of this parasite is its distribution. Whereas it has been found in the Dawson, Clarence, Brisbane and Severn Rivers, it has only been explored in any detail in the Brisbane River system. Remarkably, the parasite has only been found in Moggill Creek. There seems no clear explanation for this. All the putative hosts in the life-cycle are abundant throughout the system. Clearly something favours transmission in Moggill Creek but it remains completely unknown.

For such a large parasite to be so poorly known is symbolic of the state of the knowledge of parasites of Australian animals.

Importance/pathogenesis/interactions

One of the commonest questions posed to me as a parasitologist when I admit to studying the parasites of wildlife is “Are you trying to get rid of them?” I think I usually cause disappointment when I say that I like them and wouldn’t want to kill them. Perhaps this is unfair. If parasites are so ubiquitous and supposedly draining the life from their hosts, just how significant are they in our wildlife? In the main we still have to admit that we know very little about this. The ideas I discussed earlier have some bearing on this, however. By definition, parasites are a drain on their hosts. However, as discussed earlier, if a parasite is too successful it may kill its host and, consequently, itself. The simple observation is, however, that we rarely find animals dying from their parasites. In part the outward appearance may be misleading. For example, typically, the molluscan 1^st intermediate host in trematode life cycles is castrated by the infection. So, although the snail or bivalve may look perfectly healthy outwardly, it may never reproduce. More typically, however, hosts will have a few parasites that appear to be tolerated. Parasitologists tend to make two broad kinds of inferences from this pattern. The first is that the pathogenesis of parasites may be an “edge effect”. For example, parasites might lead to a small percentage loss of size, or fecundity, or require the host to eat more to compensate for its parasites. One frequent result of parasitism is an increase in predation; the individual in a herd of antelopes or a school of fish that is just a little more heavily parasitised may be the first to succumb to a predator. At a deeper level there is increasing evidence that the constant war of attrition between hosts and their parasites may be a major driver of evolutionary change. There are even compelling theories to suggest that this battle is the explanation, or part of it, for the existence of sexual reproduction.

Conclusion

Parasitologists and parasites tend to feel equally misunderstood – no-one loves them or appreciates them! Yet it is certainly true that they are everywhere, they impinge on the biology of all the larger animals that we take an inordinate interest in, and, yes, they can be fascinating study in their own right.