Saturday 17 March 1990
Organised by The University of Bristol and the British Chelonia Group
The Dr. R.N. Smith Memorial Lecture was given by Dr. R.A. Avery, University of Bristol.
PARASITES AND THE BIOLOGY OF CHELONIANS
R.A. AVERY, B.Sc., Ph.D. Department of Zoology, University of Bristol, Woodland Road, Bristol.
This essay is based on the second R.N. Smith Memorial Lecture, delivered at Bristol University on 17th March1990. It was a wide-ranging talk, and at times I departed from the text; as a result some of the prepared topics were missed out. The written record here corresponds to the prepared text.
Most wild animals are infected with parasites and potential pathogens such as bacteria and viruses, and chelonians are no exception. As one example of a study of these, I will quote the work of Esch et al. (1979) on helminth parasites (worms) of yellow-bellied terrapins (Trachemys scripta) in South Carolina. Esch and his colleagues examined 78 terrapins, and found ten species of parasitic worms: five Acanthocephala (thorny-headed worms), three Trematoda (flatworms or flukes) and two Nematoda (roundworms). Some of the terrapins were infected with six species of worms simultaneously. These parasites are all found inside the body, and are called endoparasites.
Ectoparasites, in contrast, are found on the external surfaces of their hosts; they include such animals as ticks, mites, fleas and lice. In the days before the Second World War, when tortoises - particularly spur-thighed tortoises (Testudo graeca) -were imported into Britain in large numbers for the pet trade, many owners became familiar with large, reddishbrown ticks Hyalomma aegyptianum. With increasing levels of concern for animal welfare, and rising standards, these were usually removed before the animals were exported from the country of origin in the 1950s and 1960s. They are now almost never seen in Britain, because they are adapted to warm climates and do not seem to be able to survive here on captive-bred tortoises.
Other tortoise parasites persist, however. Foremost amongst these are the nematodes or roundworms. These are found mostly in the intestine; there is a number of different species. The largest is called Angusticaecum holopterum. These worms are creamy white in colour and may grow to as much as 15cm. in length; they belong to an order called the Ascaroidea, which also includes the large roundworms of man, Ascaris lumbricoides. Occasionally one of these worms may be expelled from the gut of its host, and appears in the faeces of the animal, much to the consternation of its owner. One of the surprising things about this parasite is that the details of its life cycle are not known; we do not know how tortoises become infected.
Much smaller are Atractis dactyluris. They rarely exceed 7mm in length and are semi-transparent. The female worms produce little larvae (very like minute versions of their parents) which pass out with the faeces of the host and contaminate the environment by wriggling into the soil or onto herbage. Infection of a new host, or reinfection of an animal which already contains some of the worms, takes place when the tortoise accidentally swallows a larva while it is feeding. How long the free-living larvae can survive depends partly on the temperature and humidity - they are favoured by damp conditions - and in captivity can depend on the standard of hygiene: a cage which is cleaned regularly will contain fewer larvae than one which is not.
Most of these generalisations apply also to the genus Tachygonetria, although these worms are even smaller, usually only one or two millimetres in length. They belong to the order Oxyuroidea, which also includes the human pinworms which are commonly found as an infection in children. These worms can be present in the colon (large intestine) of tortoises in very large numbers. A careful study of the Tachygonetria worms in six Spur-thighed tortoises (Testudo graeca) by G.A. Schad (1963) showed that there were eight species which could be readily identified. The detailed distribution of each species was slightly different. This was demonstrated by freezing the intestines of freshly-killed tortoises in liquid air to immobilise the worms, and then thawing them out again and counting the worms in slices of intestine cut both longitudinally and transversely. The species assorted themselves both longitudinally - some were commonest at the anterior end of the colon, some at the posterior, and yet others in the middle - and radially - some were commonest at the centre of the colon, others near its periphery. Schad also demonstrated that the species differed in their feeding habits, some being relatively indiscriminate feeders on gut contents, others specialising on bacteria. The species vary in other aspects of their biology too: in wild Horsfield's tortoises (Testudo horsfieldi) the proportions of different species were shown to vary both seasonally and with the age of the host (Dubinina, 1949).
What effects do these, and other tortoise parasites, have on their hosts? The short answer is that we do not know. There is a tendency to think that because a parasite like Angusticaecum is large relative to the size of its host, or because Tachygonetria may be very numerous (many thousands have been found in a single tortoise), they must be detrimental. There is no firm evidence for this, however. They might even be beneficial: it could be argued, at least as an hypothesis which can be tested experimentally, that nematode worms in the tortoise intestine are beneficial because they help to break up the food particles or feed on bacteria. Some other parasites, however, are far more likely to be positively harmful: Hyalomma ticks, for example, can transmit many diseases (Arthur, 1962), although 1 know of no firm evidence that they transmit diseases to tortoises. Many diseases of other reptiles are transmitted by ticks or mites, however, for example a blood protozoan called Karyolysus is transmitted among Scandinavian lizards by mites (Svahn, 1974).
These parasites are harmful, but the effects of some invading organisms on reptiles can be quite subtle - for example, the well-known ability of some bacteria to induce behavioural fever in lizards (Kluger, 1979); the animals seek higher temperatures when placedi n a temperature gradient than they do when uninfected.
There is probably a spectrum of parasites and diseases from those which are always harmful (the much feared "red-leg" disease of amphibians, caused by bacteria in the genus Aeromonas, would be a herpetological example), through those which are sometimes harmful, those which are rarely harmful, to those which are beneficial. In some infections the outcome varies with circumstances. This is an area of biology which has received very little ecological study; we really know extraordinarily little about the importance of parasites and diseases in the lives of animals, especially in the field. This is certainly true of chelonians. We know almost nothing, for example, about what effects the widespread infection of terrapins with Salmonella (review in Cooper, 1981) might have on animals in the wild. Amongst the few animals which have been studied in detail in this respect are fence lizards (Sceloporus occidentalis), and because these are reptiles and the work (Schall, 1983) is both interesting and important, I shall spend some time discussing it.
Amongst the parasites of fence lizards in California are malaria parasites Plasmodium mexicanum, which are protozoans (i.e. single celled animals). Unlike the malaria parasites of man, however, which belong to different species, these are believed to be relatively harmless. Very careful studies by Schall and his colleagues have shown, however, that infection can have some effects, although these may be small and rather subtle. The presence of parasites may alter the thermoregulatory behaviour of the lizards, for example, although the evidence for this is conflicting. They may reduce the amount of fal stored prior to hibernation, and they may reduce the size of the testes in males and the clutch in females in summer. Because heavy infections result in some anaemia, they may reduce the ability of the lizards to escape predators, by reducing their stamina and the speed at which they can run. Growth rates of juveniles may be reduced. Finally, in carefully staged encounters between otherwise evenly-matched rival male lizards, it has been shown that an infected lizard has a reduced chance of winning. It must be emphasized that all of these effects are small. Probably not many fence lizards in nature ever die from a malaria infection: many probably recover and become immune to further infection. The antibodies may possibly confer some protection against other diseases, too, in the same way that vaccination with cowpox protected humans from smallpox. The disease may in the long term act to maintain the genetic health of the lizard stock, in much the same way as predators in nature can be regarded as beneficial for the prey as a species by removing weaker individuals before they are able to breed. The role of diseases in nature can clearly be very subtle.
This is probably true, in fact, of most biological phenomena. One of the ways I like to illustrate this to my students is by discussing the work of Chelazzi and Calzolai (1986) on thermoregulation in Hermann's tortoises. These authors showed that tortoises in a familiar environment heated up more rapidly when they were basking in the morning, and maintained more stable body temperatures subsequently, than those recently introduced into the same environment but with which they were not yet familiar. I would never have thought of doing this experiment. The moral is "do not take anything for granted, and investigate everything". I am sometimes tempted to suggest as an axiom that all natural phenomena are more complex and subtle than we first suppose.
This has recently been illustrated by my own work on wall lizards Todarcis muralis) in Italy. I spent several weeks observing closely the behaviour of a colony on a large, south-facing rampart of the mediaeval city of Lucca: the aim was to determine to what extent the animals hunt actively for their food, and to what extent they are "sit-and-wait" or "sentinel" predators (wall lizards feed mostly on insects). Some lizard species have a strategy which is intermediate between these extremes (Pietruszka, 1986). It soon became apparent that not only are wall lizards "intermediate" in this respect, but that there are many other factors which complicate this analysis. For example, adult males, adult females and juveniles tended to have daily activity cycles which reached a peak at slightly different times. There was competititon for what little shade was available in the middle of the day, and males - being biggest - tended to acquire the most favourable sites, in the shade of overhanging vegetation from which they could "sit-and-wait". Often they would do this in a headdown posture 2-3 feet from the foot of the wall, clearly scanning the vegetation at ground level for moving insects. Females and juveniles rarely did this; indeed, juveniles did not sit-and-wait much at all, because they were kept moving by competition with the bigger adults. (Feminists may be glad to hear that the males did not have it all their own way - they in turn were frequently chased off by geckos, which were even bigger). The juveniles spent more time off the wall, in vegetation at its base, again because of the competition: the ground level vegetation was a less favourable habitat because the lizards there were more vulnerable to predation by birds and cats. These subtleties were unexpected: they had not been forseen at the outset of the study.
As a final example I shall quote the work of Adrian Hailey and his colleagues on habitat separation between Hermann's tortoises (Testudo hermanni) and spur-thighed tortoises (T. graeca); see Wright et al., 1988. As is well known, these two species co-exist in parts of Greece. Their biology differs, however. Testudo graeca tended to occupy more open habitats, and so overall often had slightly higher body temperatures and were less active in the middle of the day (because they were more exposed to the intensely hot sunshine). At any one site, however, the two species behaved in the same way: so it is the habitat selected which determines thermoregulatory characteristics such as body temperature and the details of the activity cycle, and not vice versa.
I began with parasites, and the talk moved on to a consideration of ecology and behaviour. The common theme has been the subtlety of the lives of wild animals. We should beware glib generalisations in biology they are probably not true. I am sure that this will be demonstrated with increasing frequency in the coming years, and 1 think it likely that studies of chelonians will have a part to play in adding to our understanding of this wonderful complexity.
I am not primarily a specialist on chelonians, and so I count it as a particular privilege to have been asked to deliver the second R.N. Smith Memorial Lecture. I benefitted over the years from many discussions of chelonian and parasite biology with my colleague the late Dick Smith. Sadly, these are no longer possible. I am still able to derive great pleasure, however, from my continued association with Adrian Hailey and Roger Meek; they too are a source of stimulation and encouragement. I am particularly grateful to Roger Meek for several suggestions as to topics which might be included in this lecture.
Arthur D.R. 1962 Ticks and Disease. Pergamon Press.
Chelazzi G. and CarIzolai R. 1986. Thermal benefits from familiarity with the environment in a reptile. Oecologia 68, 557-558.
Cooper J.E. 1981 Bacteria. In Diseases of the Reptilia Vol. 1. Eds. J.E. Cooper and O.F. Jackson, Academic Press, 165-191.
Dubinina M.N. 1949. Materials on the parasitology of tortoises (in Russian). Parazitologicheskii Sbornik 11, 61-62.
Esch G.W, Gibbons J.W. and Bourque J.E. 1979. Species diversity of helminth parasites in Chrysemys s. scripta from a variety of habitats in South Carolina. Journal of Parasitology 65, 633-638.
Muger MA. 1979. Fever in ectotherms: evolutionary implications. American Zoologist 19, 295-304.
Pietruszka R.D. 1986. Search tactics of desert lizards: how polarised are they? Animal Behaviour 34, 1742-1758.
Schad G.A. 1963. Niche diversification in a parasite species flock. Nature 198, 404-406. Schall JJ. 1983. Lizard malaria: host-parasite ecology. In Lizard Ecology: Studies of a Model Organism. Eds. R.B. Huey, E.R. Pianka and T.W Schoener, Harvard University Press, 84-100.
Svahn K. 1974, Incidence of blood parasites of the genus Karyolysus in Scandinavian lizards. Oikos 25 45-53.
Wright J., Steer E. and Hailey A. 1988. Habitat separation in tortoises and the consequences for activity and thermoregulation. Canadian Journal of Zoology 66, 1537-1544
Testudo Volume Three Number Two 1990