ABSTRACT. The potential geographical distribution and relative abundance of the Old World screw-worm fly, Chrysomya bezziana Villeneuve (Diptera: Calliphoridae) as determined by climate, was assessed using CLIMEX, a computer program for matching climates. CLIMEX describes the relative growth and persistence of animal populations in relation to climate.
The observed global distribution of C.bezziana was compared with the potential distribution predicted by CLIMEX. The differences in the two distributions indicate the areas at risk of colonization, with particular reference to Australia and the Americas. According to the model, the potential area of permanent colonization in Australia extends south to the mid-coast of New South Wales. Comparison of areas suitable for permanent establishment with the potential summer distribution indicates that large additional areas, carrying most of the continent's livestock, could be colonized in the summer months. Seasonal population growth indices are presented for three ports in Australia at which screw-worm fly specimens have been collected by quarantine authorities. They indicate the relative risk associated with introductions at different places in different seasons and so provide valuable planning information for quarantine authorities.
The CLIMEX predictions for C.bezziana in North America are shown to be similar to the recorded distribution limits of the New World screw-worm fly, Cochliomyia hominivorax (Coquerel). The fly could also colonize South America, as far south as southern Brazil and midway through Argentina.
Key words. Chrysomya bezziana, Cochliomyia hominovorax, myiasis, screw-worm fly, geographical distribution, climate, model, CLIMEX, greenhouse effect, quarantine.
The Old World screw-worm fly, Chrysomya bezziana Villeneuve, is an obligate parasite that poses a major threat to much of the world's livestock. It occurs throughout much of tropical and subtropical Africa, the Indian subcontinent and southeast Asia from southern China in the north to New Guinea in the south (Norris & Murray, 1964). This myiasis-producing fly has been recorded from a wide range of host animals including livestock, wildlife, domestic pets and humans (Spradbery & Vanniasingham, 1980). Gravid females are attracted to wounds or body orifices of potential hosts where each lays approximately 200 eggs. The resulting larvae burrow into the host's tissues creating lesions which may result in loss of condition, maiming, infertility and death (Humphrey et al., 1980).
C.bezziana is acknowledged as an immediate threat to the livestock industries of tropical Australia (Anon., 1979) and also poses a particular threat to the Americas. Assessment of the likely costs to the industries and design of the contingency plans for the control or eradication of any screw-worm fly incursion depend on the probabilities of establishment and on the potential geographical distribution of the fly.
Given an availability of hosts and suitable vegetation, the main factor likely to limit the extent of colonization by the fly is climate. Possible interaction with the resident species of screw-worm fly, Cochliomyia hominivorax (Coquerel) in endemic parts of the Americas may also play a role should C.bezziana enter there.
Attempts have been made to forecast the distribution of screw-worm fly in Australia based on climate, vegetation and host availability (Anon., 1979; Thompson, 1981), but there is wide disagreement between the predictions. Recently, CLIMEX, a computer program for comparing the relative population growth and persistence of animals in relation to season and locality has been developed (Sutherst & Maywald, 1985; Maywald & Sutherst, 1985). CLIMEX enables comparison of the response of a given species to different climates and thereby indicates an animal's potential geographical distribution and relative abundance. CLIMEX can be used, even when no experimental data are available, by employing the known geographical distribution to fix parameter values of the model.
In the present paper the climatic potential for the spread of the Old World screw-worm fly is investigated using CLIMEX.
Materials and Methods
CLIMEX has been developed as a risk assessment tool for use in quarantine and so was ideally suited for the present purpose. The main information generated by the program is an ecoclimatic index (EI) that describes the response of a nominated species of plant or animal to the climate of a given location on a scale from 0 to 100. The index was designed to aid policy makers by producing concise information with which to make decisions. The EI is the product of an annual population growth index (GI) and four annual stress indices which reflect the adversity of the unfavourable seasons. Thus, the GI describes the potential for a build-up in population size during the favourable season, and the EI gives an overall measure of the favourableness of the location for both population growth and persistence. Weekly GI and temperature indices (TI) give a measure of seasonal variation in the favourableness of both moisture and temperature on a scale from 0 to 1.0.
Distribution records for C.bezziana were obtained from the literature (see Norris & Murray, 1964; Baker et al., 1968), museum specimens, personal communications and CSIRO surveys in Papua New Guinea. The temperature and moisture related parameters of the CLIMEX model were estimated by iteration, using the known distribution of C.bezziana in southern Africa. When the parameter values gave a close visual match between the observed and predicted distributions, they were fixed and used to make further projections.
The CLIMEX parameter values that best describe the observed distribution are shown in Table 1. The values indicate that the fly is most successful under hot, wet conditions and that it is sensitive to prolonged cold or dryness. The parameter values reflect the marginal nature of the Eastern Province of South Africa (Baker et al., 1968) from where C.bezziana reputedly died out for unknown reasons after several years of colonization. They also reflect the highly favourable nature of areas further north in the Transvaal and Zimbabwe (Norval et al., 1988).
The observed global distribution of C.bezziana is shown in Fig. 1, with its potential distribution based on the CLIMEX projections. Comparison of the CLIMEX predictions with distribution records for C.bezziana confirmed the climatic favourableness of the numerous African records not used in the fitting of the parameters. Of special interest was the record from Kabete at an altitude of 1820 m in Kenya (see Norris & Murray, 1964), which has a large livestock population and which was assessed to be marginal for the fly (EI=12). Particularly close agreement was observed with Chinese records provided by Professor Fan Zi-de. The records indicated that the northern limit of C.bezziana was in the Fuzhou area of Fujian Province, agreeing precisely with the CLIMEX estimates. Numerous other positive records from Asia were from areas estimated to be climatically favourable for the fly. In Papua New Guinea, where extensive CSIRO surveys were made, all locations were predicted to have climates able to support C.bezziana, with the exception of Wabag at 1980 m elevation, which was estimated to be climatically marginal (EI = 8). Absence of C.bezziana from a few areas is believed to be due to non-climatic factors such as lack of tree cover or livestock (R. S. Tozer, pers. comm.). The differences in the two distributions highlight the areas at potential risk of colonization. In the Americas the results indicate that the fly could persist permanently throughout the tropical and subtropical regions, from southern Brazil to the southern United States. In Australia the fly could permanently inhabit the wet coastal areas of the eastern and northern parts of the continent.
In an effort to delineate the potential for the spread of screw-worm flies in Australia and in North America, more detailed maps of the EI values for these continents are shown in Figs 2A and 3A, respectively. These maps can be compared with the potential summer distributions, as indicated by the annual 'growth indices, GI' for the two areas in Figs 2B and 3B. The latter results (Fig. 2B) indicate that the fly could propagate over large parts of inland and southern Australia in the summer months. The area in which it could become permanently established is much smaller and is confined to the north and east of the continent. Fig. 3B shows that much of the eastern half of North America, as far north as Canada, becomes favourable for population growth in the summer months. However, the fly could not overwinter in average years, except in the south of the continent.
The effect of extreme year-to-year variation in climate on the potential distributions in the two continents are shown in Figs 2C and 2D for Australia, and Figs 3C and 3D for North America. Firstly, given an increase of 3deg.C in temperature and an increase of 20% in summer rainfall (one suggested 'greenhouse' scenario), the climatic potential for fly propagation is likely to increase in both continents, as indicated by the GIs. Conversely, colder winters than average, with a drop of 3deg.C in mean temperatures will result in the area of permanent colonization, indicated by the EIs. shrinking to northern areas in Australia (Fig. 2D) and to isolated foci in North America (Fig. 3D). Hot dry summers are predicted to reduce the population growth and also to cause a temporary contraction of the geographical range of C.bezziana.
The likelihood of successful establishment of C.bezziana arriving on shipping or aircraft in Australia was evaluated (Fig. 4) for the known interceptions. Three ports have been involved: Portland in the south (12 December 1985, 2 July and 19 August 1987, and 22 June 1988), Sydney in the southeast (20 November and 4 December 1987) and Darwin in the tropical north (16 September 1986 and 4 April 1988). On each occasion, except for the April infestation in Darwin, the flies collected were dead adults. Nevertheless they indicated the real risk of an introduction of live flies. The CLIMEX weekly growth indices for average years show the low risk of establishment of C.bezziana in Portland. Flies arriving in Sydney or Darwin, particularly in spring or summer, would experience favourable conditions. The April 1988 introduction of live flies into Darwin was probably too late in the season to enable the population to increase to a size needed to survive the dry season. More detailed analyses were carried out using actual meteorological data for 1988 in Darwin (Fig. 4). The above conclusions were unaltered as April rainfall was only 15% of average and May had average rainfall. The temperature indices (TI) show that Portland is nearly always too cold for development of the flies, Sydney is warm enough in the summer and Darwin always has suitable temperatures. The difference between the GI and TI values indicates the extent of the moisture deficit.
As screw-worm flies are among the most damaging livestock pests, it is vital for quarantine authorities to be able to define the chances of establishment and subsequent areas at risk of colonization by introduced flies. The present results provide that information in a form amenable to rapid interpretation by policy makers. The close agreement between the observed and predicted distributions of C.bezziana outside southern Africa suggests that the species is relatively uniform, at least in relation to its climatic requirements. It is thus possible to have confidence in the predicted results for areas which have yet to be colonized.
The results illustrate the large livestock rearing areas at risk, given that other non-climatic factors, such as tree cover and injuries from tick bites (e.g. Norval er al., 1988), Stephanofilaria lesions (Bruce, 1964) or other traumas are present. Judging by the observations of Baker et al. (1968) in South Africa, the probabilities of colonization of vacant areas by C.bezziana will be greatly increased by livestock movements, even though this species is reputed to be able to fly long distances (Spradbery, personal observations). C.bezziana colonized the Eastern Cape area only after apparent introduction on cattle returning from the Transvaal after a drought (Baker et al., 1968). The Eastern Cape appears to be marginal and protected to the north by high country and the west by desert.
In Australia the main risks are associated with movement of animals to and from countries to the near north. The fly is also likely to enter the Americas, as a recent unconfirmed report of an introduction of C.bezziana into Brazil demonstrates (W. B. Hyman, personal communication). Possible genetic interactions between C.bezziana and C.hominivorax warrant experimental studies on assortative mating and the relative fitness of any hybrids, because they may influence the chances of establishment of C.bezziana in those areas in the Americas still infested with C.hominivorax.
The CLIMEX predictions for Australia are broadly consistent with the predictions of Anon. (1979). They differ only in the extension of the estimated area of potential permanent colonization south along the coast by 10deg. of latitude to the mid-coast of New South Wales (Fig. 2A), which has a climate similar to the Eastern Province of South Africa. The predictions of Thompson (1981) incorporate a much larger area than is likely to be suitable for permanent colonization, based on our results. They more closely follow the potential summer distribution which is much greater than the overwintering areas, as found in practice with C.hominivorax in the U.S.A. Given the projected temperature rises from the 'greenhouse' effect, the potential summer distribution will be extended considerably in all continents. Alternative scenarios of climate change (Watt, 1987) project a continuing cooling trend at higher latitudes in the northern hemisphere which will reduce the size of the potential endemic areas. Indeed, Readshaw (1986, 1987) claimed that the cooling has already reduced the area infested by C.hominivorax.
CLIMEX predictions for C.bezziana in North America agree fairly closely with the observed distribution of C.hominivorax in average years (Anon., 1962; Bushland, 1985) and in years with cold winters (Readshaw, 1986, 1987). The two species obviously have very similar climatic requirements. Projected warming of the summers by 3deg.C with 20% more rain from 'greenhouse' effects had marginal impact on the extent of the fly's possible population growth (Fig. 3D). A reduction of 3deg.C in the mean winter temperature resulted in a reduction of the distribution as shown in Fig. 3D.
Recently, C.bezziana has been introduced to Bahrain in the Persian Gulf (Kloft et al., 1981) and now appears widespread in the region with records from Kuwait, Fujairah and Muscat (Rajapaksa & Spradbery, 1989). These establishments have occurred despite CLIMEX-derived estimates for Bahrain and Muscat which indicate that the climates of the two places are very unfavourable for the fly. The explanation was the creation of favourable habitats by establishment of feedlots in irrigated areas where extensive tree planting has taken place. The flies died out when the feedlots in Bahrain were moved to dry locations.
The recent detection of adults of C.bezziana on livestock vessels returning from the Persian Gulf and Asian ports to the Australian ports of Portland and Darwin and aboard passenger air craft arriving in Sydney from India (Rajapaksa & Spradbery, 1989) suggests that accidental introductions of screw-worm fly could occur at widely different foci in Australia. During fly-trapping surveys in Papua New Guinea, large populations of C.bezziana were indicated throughout the southern coastal area bordering the Torres Strait, from Irian Jaya in the west to the Papua New Guinea island of Daru in the east (J. P. Spradbery, unpublished data). Interisland movements in Torres Strait by local craft and pleasure boats heighten the risk of introduction via domestic animals or human hosts.
There is little doubt that if the screw-worm fly became established in Australia, the costs to the sheep and cattle industries would be very high. Experience in Papua New Guinea, Malaysia, Indonesia and the Middle East reveal high levels of myiasis in livestock with as many as 10% of animals infested at any one time, annual rates of infestation exceeding 100% and calf losses of 30% due to navel strikes (Sigit & Partoutomo, 1981; R.W. Sutherst, personal observations). Experience in southern Africa is similar (e.g. Norval et al. 1988) but the relative rarity of C.bezziana in the rest of Africa is puzzling given its widespread distribution. The intensity of livestock supervision in Africa may provide an explanation. With much of Australia's livestock managed on an extensive scale, current husbandry practices would do little to ameliorate the problem.
Correspondence: Dr R. W. Sutherst, CSIRO Division of Entomology, Long Pocket Laboratories, Private Bag No. 3, Indooroopilly, Queensland 4068, Australia.
The following institutes and individuals provided distribution records for C.bezziana: British Museum (Natural History), Dr B. M. Doube, Professor Fan Zi-de, Dr E. M. Neville, Papua New Guinea Department of Primary Industry, Dr D. P. A. Sands. R. S. Tozer and Dr W. B. Hyman. Dr L. J. Readshaw made some helpful suggestions on the manuscript.
Anon. (1962) Status of the screw-worm in the United States. United States Department of Agriculture, ARS 22-79.
Anon. (1979) Screw-worm fly. Possible prevention and eradication policies for Australia. Australian Bureau of Animal Health, Canberra.
Baker, J.A.F., McHardy, W.M., Thorburn. J A. & Thompson. G.E. (1968) Chrysomya bezziana Villeneuve - some observations on its occurrence and activity in the eastern Cape Province. Journal of South African Veterinary Medical Association, 39, 3-11.
Bruce, W.A. (1964) The history and biology of the hornfly, Haematobia irritans (Linnaeus): with comments on control. North Carolina Agricultural Experiment Station Technical Bulletin, No. 157.
Bushland. R.C. (1985) Eradication program in the Southwestern United States. Entomological Society of America, Miscellaneous Publications, No. 62. 12-15.
Humphrey, J.D., Spradbery, J.P. & Tozer. R.S. (1980) Chrysomya bezziana: pathology of Old World screw-worm fly infestations in cattle. Experimental Pathology, 49, 381-397.
Kloft, W.J., Noll, G.F. & Kloft, E.S. (1981) Durch Transitbefall' bewirkte Einschleppung von Chrysomya bezziana Villeneuve (Dipt., Calliphoridae) in neue geographische Regionen. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie, 3, 151-54.
Maywald, G.F. & Sutherst, R.W. (1985) User's guide to CLIMEX. A computer program for comparing climates in ecology. CSIRO Australia, Division of Entomology Report, No. 35, 29pp.
Norris, K.R. & Murray, M.D. (1964) Notes on the screw-worm fly Chrysomya bezziana (Diptera: Calliphondae) as a pest of cattle in Papua New Guinea. CSIRO Australia, Division of Entomology Technical Paper, No. 6, 1-26.
Norval, R.A.I., Sutherst, R.W., Kurki, J., Gibson, J.D. & Kerr, J.D. (1988) The effect of the brown ear-tick Rhipicephalus appendiculatus on the growth of Sanga and European breed cattle. Veterinary Parasitology, 30, 149-164.
Rajapaksa, N. & Spradbery, J.P. (1989) Incidence of the Old World screw-worm fly. Chrysomya bezziana, on livestock vessels and commercial aircraft. Australian Veterinary Journal (in press).
Readshaw, J . L. (1986) Screwworm eradication a grand delusion? Nature, 320, 407-410.
Readshaw, J.L. (1987) Screwworm eradication and climate. Nature, 328, 767-768.
Sigit, S.H. & Partoutomo, S. (1981) Myiasis in Indonesia. Bulletin de Office International des Epizooties, 93, 173-78.
Spradbery, J.P. & Vanniasingham. J. (1980) Incidence of the screw-worm fly, Chrysomya bezziana, at the Zoo Negara, Malaysia. Malaysian Veterinary Journal, 7, 28-32.
Sutherst, R.W. & Maywald, G.F. (1985) A computerised system for matching climates in ecology. Agriculture Ecosystems and Environment, 13, 281-299.
Thompson, D.R. (1981) Predicted range of Chrysomya bezziana in Australia. Unpublished report. NSW Department of Agriculture. 4pp.
Watt, K.E.F. (1987) An alternative explanation for widespread tree mortality in Europe and North America. International Union of Societies of Foresters, Newsletter, 25, 8-9.
Accepted 15 November 1988