Porositology Jodoy, vol. 6, no. I I, I990 343

genetic exchange, noting the prevalence of fixed heterozygosity, the absence of certain genotypes and the wide distri- bution of identical genotypes, as well as deviations from Hardy-Weinberg equi- librium. One flaw in these arguments is the bias introduced by non-random sampling, particularly the emphasis on human isolates among trypanosome stocks that have been characterized. For example, one zymocleme of T. b. rhodesiense with heterozygote iso- enzyme patterns has been repeatedly sampled because as a virulent epidemic strain, it spread widely in the Lake Victoria area. When more balanced

sampling is undertaken, as in Lambwe Valley or Ivory Coas6, the enormous diversity of trypanosome zymodemes present is stunning. Examined in detail, the individual zymodemes are seen to be generated by relatively few patterns for each enzyme, reassorting in every possible combination. This reflects the fact that genetic exchange is not a rare occurrence in the wild. If genetic exchange effectively mobilizes the trait of human infectivity by transferring it into other genetic backgrounds, say of greater fly transmissibility or virulence, it has tremendous epidemiological sig- nificance for sleeping sickness.

References I Mihok, S., Otleno. L.H. and Darji, N. (1990)

Parasrtology IO0 2 19-233 2 Gibson, W.C. and Wellde, B.T. (I 985) Trans.

R Sot. Trap. Med. Hyg. 79,67 I-676 3 Tait. A. and Turner, C.M.R. ( 1990) Parawology

Today 670-75 4 Majiwa, P.A.O. and Otleno, L.H. (I 990) Mol.

Biochem. Parasitol. 40,245-254 5 Tibayrenc. M., Kjellberg. F. and Ayala. F.J.

(1990) Proc. Natf Acad. Ser. USA 87. 2414-2418

6 Mehlitz, D. et al. (I 982) Tropenmed. Porasc. 33, 113-l I8

Wendy Gibson is at the Deportment of Path- ology and Microbiology, University of Bristol

Veterinary School, Longford, Bristol BS I8 7DU. UK.

Interpreting Parasite Host Location Behaviour

A.W. Pike

Studies on host location behaviour by the free-living stages of lparasites are numerous; prominent models include free-swimming stages of trematodes, nematode larvae and ectoparasitic insects. Their host location methods may use both chemical and physical sensory input but many of these studies have attempted only to identify behav- ioural responses to stimuli; they have not been related to any measure of transmission success in a way that would enable their significance tl3 the popu- lation dynamics of host-parasite rela- tionships to be estimated.

It is known that, for some parasites, transmission success may be improved if they orientate themsel,ves towards the host’s preferred habitat; a reper- toire of behavioural patterns has been described that includes tactic and kinetic responses to light, gravity a.nd vibration. Much of this work is associated with trematode cercariae because they are particularly amenable to Istudy in this way. Behavioural patterns relating to the host habitat seem to fall into two categories: those designed to maintain the parasite more or less within a potential host’s microhabitat and those that elicit a burst of activity above that of the maintenance level. The latter activity can be stimulated by, among other things, shadowing of a light source and vibration.

Poulin et al.’ have identified similar behavioural responses in the copepodid of the gill maggot, Sulmincola edwardsii, an ectoparasitic copepod aof salmonids @ I990 Elsewr Science PubIshers Ltd. (UK) 0 / 69470,,%$02.CC

in freshwater. The copepodid is a non- feeding, free-swimming phase in the life cycle that locates a suitable fish host to which it attaches. In certain behavioural respects it resembles those cercariae (eg. Diplostomum) that must locate an active vertebrate host. Thus it has been shown to respond to shadowing of a light source and to vibration by signifi- cantly increasing the rate and duration of swimming activity. This study, and others like it on cercariae, have shown that the free-swimming larvae possess sensory-motor systems that are ca- pable of responding to physical stimuli in the environment. The authors conclude that these responses increase the prob- ability of contact between parasite and potential host. In the context in which these and other similar experiments have been done, it may well be true that the elicited behaviours do indeed improve transmission rates, although such a possibility has not been widely explored or tested. It would be interesting, for example, to compare establishment rates on fish exposed to copepodids in the dark and in light in the way that Schram and Anstensrud’ have done for copepodids of Lernaeeni- cus sprattoe. This work comes closer than most to relating experimentally identified behviour to transmission events in the natural environment. Evaluating the effect of mechanical stim- uli on transmission rates is more dif- ficult.

Difficulties arise when these behav- ioural patterns are placed in a natural

context, not because the behaviour pat- terns may be absent but because there are likely to be confusing elements and counteractive stimuli that may render such behaviour ineffective for their claimed purpose. I would argue there- fore that while the responses to physical cues are undeniable, their effectiveness in improving transmission rates in natural conditions is questionable, especially where the experimental source of stimulation may differ signifi- cantly from that in the parasite’s natural habitat. Having identified some of the responses that parasite larvae make to such cues, the next logical step is to attempt to quantify their contribution to transmission rates.

The elicited response to shadowing is increased movement, and is thought to enhance the likelihood of the parasite contacting the host that has cast the shadow. Furthermore, it is generally believed that the existence of this response pattern enables the parasite larva to conserve energy during its short free-swimming existence. A number of problems come to mind in relating the parasite’s behaviour in the laboratory to transmission dynamics under natural conditions. First, responses to light can only be effective during daylight so their contribution to transmission is not con- tinuous within the natural free-living lifespan of the parasite. Second, tur- bidity in the water may scatter, reduce or even eliminate the stimulus. Third, parasite larvae are not alone in the water column and may in many circum-

344

stances constitute only a small propor- tion of the planktonic fauna. What effect do these other organisms have on the behaviour of the parasite? Do they themselves generate shadowing stimuli or do they disrupt shadows that are created by potential hosts? If there are spurious stimuli emanating from a variety of sources, how quickly do para- sites adapt to this constant sensory bombardment? Do they have some means of discriminating between spuri- ous cues and the real thing and, if so, should we not be attempting to deter- mine the sensitivity of the parasite’s system? Light intensities may be very low In natural conditions so it is import- ant to avoid saturating the receptors and then misinterpreting the apparent lack of discrimination by the parasite. Also, spectral range will vary with depth and water conditions3, and the charac- teristics of the light source must be taken into account.

Larvae in a water column are likely to be exposed to mechanical stimuli, in the form of pressure waves of varying fre- quency and amplitude, from many sources. These could originate from such diverse sources as the propulsive thrust of the tail fin of a fish or the stabilizing movements of its pectoral fins, or the twitching of antennae of copepods swimming quite close to a parasite. In assessing the likely benefits to transmission success of such stimuli, it is therefore relevant to take into con- sideration the likelihood that the para- site responds to spurious signals, and the range of sensitivity of the sensory apparatus receiving the stimuli. Is it reasonable to submit parasite larvae to a mechanical stimulus of undefined characteristics and then interpret the increase in swimming activity as necess- arily being linked to host location? Do the propulsive movements of other nearby parasite larvae, or of other small organisms, stimulate swimming? Or do parasites, destined to attach to ver- tebrates, respond only to low frequency stimulation that might be generated by movement of the host’s appendages?

Sukhdeo and Mettrick refer to the benefits of applying the results of study of the behaviour of free-living nema- todes, such as Coenorhabditls elegans, to the study of parasitic species. This may be true for other groups such as para- sitic copepods. For example, in another recent paper NeilI’ has shown that the free-living copepods Diaptomus kenoi, which normally exhibit a diurnal vertical migration as a predator-avoidance mechanism, abandon this behaviour in the absence of predators. However, they quickly revert to the avoidance

behaviour when predatory Chaoborus tn’vittotus larvae are reintroduced. There is even some evidence that this response has a chemosensory basis since Dioptomus placed in water pre- viously occupied by C. trivittatus larvae initiate the vertical migratory behaviour. Poulin et al.’ rejected the possibility of a chemosensory component to host finding by Salmincola copepodids on the grounds that a gradient was unlikely to establish in large bodies of well-mixed water, an argument similarly advanced by Sukhdeo’ in another context. How- ever, chemosensory stimulation might act as a releaser to stimulate movement in the same way that it has been associ- ated with light and vibration.

In comparing free-living planktonic copepods with the planktonic larvae of parasitic species it has to be recognized that their respective lifespans in this habitat are quite different. However, it IS interesting to speculate that the predator-avoidance behavlour of free- living species has been eliminated from the behavioural repertoire of planktonic

Parasitology Today, vol. 6, no. I I, I990

parasite larvae as a trade-off to enhanced host location potential and thereby improved transmission oppor- tunities. It is by no means certain that these behavioural responses do im- prove parasite transmission rates and in the final analysis it may still be fecundity and chance that play the greater part.

Acknowledgements Helpful discussion with I.G. Priede and comments on the manuscript by P.]. Whitfield are gratefully acknowledged.

References I Poulin. R.. Curtis. M.A. and Rau, M.E. (I 990)

Porasrrology 100.4 1742 I 2 Schram, T.A. and Anstensrud, M. (I 985) Sorsio

70, I 27p I 34 3 Lythgoe, J.N. (1979) The Ecology of V~aon

Oxford Unwerslty Press 4 Sukhdeo, M.V.K. and MettrIck, D.F. (1987)

Adv. Porasitol. 26,73- I44 5 NellI. W.E. (I 990)Noture 345,524-526 6 Sukhdeo. M.V.K. (I 990) Porasrtology Today 6,

234-237

A.W. Pike IS at the Deportment of Zoology, University of Aberdeen, Aberdeen AB9 ZTN, UK.

NEXTMONTH.. .

Intestinal Protozoaand Epithelial Cells

Cercarial Kissing Marks

Perspectives in the Control of Taenia solium

Plasmodium fa/ciParum Surface Antigen p I90

Resistance to Parasitic Nematodes

Parasitoids, Polydnaviruses and Endosymbiosis

Ecdysteroids in Nematodes

Recent Articles in the Trends Journals . . .

Parasite-host coevolution. C.A. Toft and A.J. Karter (I 990) Trends in EcologyandEvolution 5 (IO), 326-329.

Where do human schistosomes come from? An evolutionary approach. C. Combes ( I 990) Trends in Ecology and Evolution

5 ( I O), 334- 337.

Genetic exchange in African trypanosomes. J. Sternberg and A. Tait ( 1990) Trends in Genetics 6 ( IO), 3 17-322.