Combating the sheep blowfly and other insect pests

By February 10th, 2011

CSIR’s research on the sheep blowfly problem began with Ian Mackerras’s appointment to the Division of Economic Entomology in 1928. He was joined by John Nicholson in the early 1930s and by Doug Waterhouse in 1938. The sheep blowfly, Lucilia cuprina, was a cosmopolitan pest of vital importance to Australia’s dominant sheep industry.

In a very fruitful period before the outbreak of World War II, Doug Waterhouse studied its physiology (in particular, digestion and excretion), ecology and population control. His research was a blend of the strategic and tactical and included practical projects like fly dressings and burying carrion to reduce breeding sites. After the war he extended his work on the physiology of digestion and excretion, first on the blowfly, and later on insects capable of digestion of keratin and wax showing that their ability to digest keratin was due to their ability to reduce the disulphide bonds in wool proteins making them susceptible to proteolytic attack.

Doug Waterhouse worked within the CSIRO Division of Entomology for over 60 years, and was its Chief for 21 years. He was responsible for many developments in insect and weed control both in Australia and around the globe, especially in developing countries across Asia and the Pacific and is remembered for his pioneering work on the development of the insect repellent, Aerogard.

Early insect research at CSIR

CSIR’s research on the sheep blowfly problem began in 1928 when Ian Mackerras was approached by the CSIR executive to join the Division of Economic Entomology, (one of the four founding Divisions of CSIR). The aim of the Division was to investigate entomological problems of national importance for which remedies had not been readily forthcoming. Mackerras’s instructions were to develop and direct a program of research in veterinary entomology, including the problems of the sheep blowfly, the buffalo fly and arthropod-borne viral and protozoal diseases of cattle. He moved to Canberra early in 1929 and, in the period before the laboratory became available, travelled extensively, including a trip to the Northern Territory and Western Australia, to make acquaintances among entomologists and primary producers on the sheep blowfly and buffalo fly problems. During the next decade he undertook many arduous field trips throughout Australia, in the process establishing first-hand knowledge of these two problems, and building up among graziers a tremendous fund of goodwill towards research.

In blowfly research, Mackerras headed a team which comprised, for varying periods, AJ Nicholson, M Josephine Mackerras (Ian’s wife), MR Freney, Mary E Fuller, CR Mulhearn, JH Riches (seconded from the Division of Animal Health and Nutrition), FG Holdaway, DF Waterhouse, DJ Lee and FG Lennox (who in his work on insect toxicology, used the larvae of Lucilia cuprina as a test insect and thereby contributed substantially to the blowfly program).

Nicholson had been appointed to the Division as Deputy Chief, but, later, as Senior Entomologist, transferred voluntarily to Mackerras’s section, and spent some time on blowfly research. Nicholson initiated two pieces of research. One was a study of traps and baits, for which he designed ingenious ways to reduce the action of external variables, and the other a study of the effects of temperature on the activity of the adult sheep blowflies. This research was cut short by the illness of the Chief RJ Tillyard which resulted in Nicholson being appointed Acting Chief in April 1933. From then on he had little opportunity for personal research until after the war. Nicholson had arrived from England in 1921 and spent nine years as the first McCaughey Lecturer in Entomology at the University of Sydney where he had a great impact. As Ian Mackerras wrote in his biographical memoir of Nicholson:

He put university teaching of entomology on a firm scientific foundation, and provided the first agricultural graduates to bring a new approach to economic entomology in this country. Young people interested in insects no longer became doctors or schoolteachers and devoted their leisure to their hobby; they took an appropriate degree in a university and made entomology their profession, with ever widening fields of research and ever increasing technical and financial resources before them. It could fairly be said that, so far as Australia is concerned, Nicholson in a sense began it all.

The Division of Economic Entomology had made its mark during the war and the CSIR Executive had come to appreciate the importance of Nicholson’s own field, and his reputation in it. Projects pursued by the Division while he was Chief included: cattle tick research (begun during the war); continued work on the pests of stored grain; ecological studies of additional pasture, forest and fruit pests not previously investigated; research on the new insecticides that had been developed during and after the war; as well as research on insect physiology, plant viruses and experimental population dynamics. Nicholson completed his term as Chief in March 1960, and was appointed to a Senior Research Fellowship to continue his twin studies of population dynamics and natural selection.

The sheep blowfly problem

In 1938 the Australian sheep blowfly was still an enormous problem estimated to be costing the Australian wool losses of £4 million per annum. This was an enormous sum ‘ equivalent in the 1990s, after inflation, to at least two to three hundred million dollars. As Doug Waterhouse explained in his interview with Dr Max Blythe in 1993:

If the sheep blowfly lays its eggs on the fleece or on the skin of a sheep, the eggs hatch and the young larvae abrade the surface of the skin with their mouth-parts. This causes serum to emerge, and the larvae feed on that and keep on scraping. If no further flies come to the wound, the temperature of the sheep rises, the wool stops growing and the larvae fall off when fully grown. When the wool starts growing again there is a thin area of fibre, termed a break, where it had stopped and that greatly reduces the value of the fleece. If more eggs are laid, the wound gets larger and larger. Often bacteria then come in, septicaemia sets in and the sheep dies. It is necessary to do something to prevent death or, if possible, catch the strike early enough so that a break won’t occur.

Merino sheep on a saltbush and grass pasture near Deniliquin

Merino sheep on a saltbush and grass pasture near Deniliquin, NSW. [Photo: CSIRO]

The standard practice in 1938 was to cut the wool from over the strike wound using hand shears, scrape out all the maggots using the back of the shears and then put on a dressing, which often contained an arsenical to kill any remaining larvae. The practice was not very good as sometimes it caused necrotic wounds.

Doug started work in 1938 on physiological aspects of the sheep blowfly. He continued to do so, with interruptions during the Second World War, until the 1950s. He was awarded an MSc by the University of Sydney for a thesis based on this work. At the time it was conventional wisdom that insect physiology, which was then beginning to flourish, could provide the basis of new control measures. Later, physiology was to give way to ecology, then to insect biochemistry, and later again to molecular biology, but when VB Wigglesworth FRS (later Sir Vincent) was making great progress at Cambridge, physiology was seen to be the way ahead. Doug undertook early studies on blowfly behaviour, but soon became interested in insect digestion. He was interested in the conditions under which various poisons are absorbed by the gut or excreted.

Although this work began on the premise that it should prove useful in the design of ingested insecticides (‘stomach poisons’ in the jargon of the time), it never did so. However, it did lead to fascinating discoveries of the role of the ‘goblet cells’ in the midgut and of ‘longitudinal differentiation’ in cell structure. As Doug Waterhouse recalled in his interview with Max Blythe in 1993:

… I looked at what mechanism there was for absorption of poisons in the digestive tract. On the wound in the sheep, the pH is near neutral, sometimes alkaline, certainly no more acid than pH 6.5. By feeding larvae with indicators, however, you could show very clearly that in the centre of the digestive tract there is a very acid region, down to pH 3 to 3.5. The question then was what happened in absorption of anything, including poisons, as it went down through the digestive tract. By using histochemical reactions I could show iron in the cells of this acid region: this was the region where iron was absorbed. Then I looked at other metals, including copper because copper salts were sometimes used in these dressings. I found copper was also absorbed there, but by different cells.

Then the question arose: could one use an arsenical or other compound which would be soluble and absorbed in the acid region of the digestive tract, but not become soluble in the much more alkaline or neutral pH of the wound? The first experiments didn’t show promise, but that particular line was then halted anyway by the discovery that borax and boric acid were very effective stomach poisons for the larvae. They were bland for all the wound tissues; they were bacteriostatic. In fact, we now know that they inhibit the proteolytic enzymes which the blowfly larvae use to digest the tissues. So, we had an effective stomach poison.

These and other results were summarised in a well-researched review (Waterhouse DF, 1957, ‘Digestion in insects’, Annual Review of Entomology, 2: 1-18). While insect physiology produced some notable successes in, for example, the study of insect hormones and the development of synthetic insecticides, it did not live up to its early promise and Doug turned to examine other methods of fly control.

The shift to ecological studies on the sheep blowfly

Whilst the work on blowfly control was Doug’s primary objective, it was clearly important to learn more about the ecology of the species and study the breeding behaviour of the fly, in an attempt to find new methods of reducing fly populations. As Doug recalled in his interview with Max Blythe:

The next question then was: where did the main population of the sheep blowfly breed? If, as was assumed at the time, they bred largely in dead sheep and that was the main source, then it didn’t matter if you scraped the maggots out of the wound onto the ground. If they were more than half grown they could produce fertile flies. But some experiments that I did then showed that, from each of the wounds on an average, you would get perhaps 1 200 adult flies, whereas if you put dead sheep out on trays and collected all of the maggots you would sometimes get no sheep blowflies at all, just plenty of other blowflies. This was partly because they couldn’t get enough food in competition with other species and partly because, when you get a heaving mass of maggots in a carcass, the temperature goes up and this affects many of the processes of

Doug was also involved in an extensive experiment to determine the population density of the fly and its rate of spread in an area of about 50 square miles (> 15 000 ha) of grazing country near Canberra. The experiment, using marked flies, gave valuable indications of the numbers of flies per unit area and of the flight range in a variety of weather conditions. It required a large number of helpers, one of whom was Dawn Calthorpe, later to become Doug’s wife.

A better treatment

In 1939 new information was obtained on the use of repellents for the prevention of fly strike and in the development of dressings for fly-struck sheep. As Doug recalled in his interview with Max Blythe:

The next thing then was to develop a contact poison, or a mixture of poisons, which would kill the maggots very quickly; and then to cut the fleece down to about an inch over the surface, put the dressing on and hope to kill all of those maggots. This was quite a challenge, although just at this time two people in Cambridge ‘ Professor Wigglesworth and Dr Hurst ‘ had done some very interesting work. The cuticle of an insect has got a lipid layer on the surface and then a thicker inner layer, which is protein but it is largely aqueous. What is necessary is to have something, perhaps a mixture, that will go through the lipid layer and then through the protein layer, but without being too damaging to the sheep.

Eventually a mixture of orthodichlorbenzene, kerosene and lysol ‘ which sounds horrible ‘ was found to have this effect. It could be put onto the sheep wound, and as soon as it got there the maggots would be killed and stand out dead, but the wound was not unduly affected. Into this witch’s brew was put boric acid, and there was an inert clay carrier. This led to a dressing called BKB, which was widely used for quite a long time. After the war it was temporarily supplanted by DDT and other chlorinated hydrocarbons, until those were no longer permitted. But BKB did achieve the purpose at that particular time.

A detailed taxonomic study (with SJ Paramonov) demonstrated the differences, both morphological and behavioural, between Lucilia cuprina and L. sericata (the English Sheep Blowfly). This was all interrupted by the start of the war in 1939.

A Cambridge studentship

After the war ended Doug Waterhouse was offered a one-year studentship overseas, which he spent in Cambridge in the laboratory of Professor VB Wigglesworth. Doug described him as:

The father of insect physiology in the world. He had not only written a small Methuen book but later

In Cambridge Doug worked on the peritrophic membrane which in the case of the sheep blowfly is a cylinder, and is produced at the beginning of the midgut. As Doug described:

There’s a secretion ring which squeezes out, as it were, a plastic tube which fits all the way down and surrounds the food being passed down the gut. I was interested to know what function this had in permitting or preventing the passage of material from the food out into the surrounding epithelium, which is where things are absorbed and get into the body. Anything that is taken up by the cells has to pass through this first, and in some insects you have to know how parasites get through it. The malaria parasite, in the case of the mosquito, has to go through the peritrophic membrane before it can penetrate the cells. This membrane varies a bit from one insect group to another, but it has a very interesting structure and obviously has an important function.

Doug Waterhouse in the 1940s

Doug Waterhouse in the 1940s. [Source: Blythe M, Interviews with Dr Douglas Waterhouse available by following the link in the Sources below]

Insect physiological studies after the Second World War

At the end of his studentship he returned to CSIR where he produced a sequence of papers on the physiology of digestion and excretion, first on the blowfly, and later on insects capable of digestion of keratin, and wax. This work involved well-designed and careful observations, assembled in the belief that they would contribute to a better understanding of the mode of action of insecticides. He followed up the observations by Danish workers that the gut of wool-digesting insects was highly alkaline and highly reducing to show that it was the latter that gave them their unique ability to digest keratin.

During the 1950s Rodney Powning, Max Day and Henry Irzykiewicz carried out preliminary investigations of the enzymes of the larvae of the webbing clothes moth Tineola bisselliella, and demonstrated very active proteolytic activity in gut extracts. Using specific inhibitors they showed that this activity did not include thiol-activated proteinases; was poorly affected or unaffected by naturally occurring proteinase inhibitors but may resemble the protease preparation from the microorganism Streptomyces griseus called ‘pronase’ which was subsequently shown by Japanese workers in 1973 to consist of a mixture of peptidases and proteinases. This turned out to be an accurate prediction. In the early 1970s Colin Ward, from the Division of Protein Chemistry in Melbourne showed that the digestive enzymes in Tineola bisselliella were indeed a complex mixture including five trypsin-like enzymes, two chymotrypsin-like enzymes, 15 aminopeptidases, two carboxypeptidases and two metallo-proteinases, the latter substituting for the role that pepsin plays in the acid stomach of higher organisms.

Doug Waterhouse’s work on wool pests also led to an understanding of the detoxifying mechanisms employed by these insects to neutralise inorganic poisons. As Doug recalled:

… we found that there was another enzyme which cut off the -SH groups. Consequently, if you put in things which would otherwise be poisonous, like mercury, lead and arsenic, they formed insoluble sulphides. You could see this happening, because lead and copper sulphides are black, arsenic red or yellow, and antimony red, and so on. So the insects have a built-in mechanism for protecting themselves against quite a number of the inorganic poisons. You could even get protection against fluorine, because they have calcium granules and can produce insoluble calcium fluoride. They also have a mechanism for protection against barium.

Anyway, it became clear that inorganic poisons were not going to be of any use; you would have either to go to organic poisons or alter the structure of the keratin molecule. But just at that time, empirical tests on a whole range of insecticides showed that dieldrin was a very effective moth-proofing agent. It was, in fact, used for the next 20 or so years until chlorinated hydrocarbons became unacceptable on environmental grounds.

In 1953 this work was summarised in four chapters with Max Day in the multi-author textbook tilted Insect Physiology, edited by KD Roeder and published by John Wiley, New York. The articles were:

  • Day MF, Waterhouse DF, ‘Structure of the alimentary system’, pp.273-298
  • Day MF, Waterhouse DF, ‘Functions of the alimentary system’, pp.299-310
  • Day MF, Waterhouse DF, ‘The mechanism of digestion’, pp.311-330
  • Waterhouse DF, Day MF, ‘Function of the gut in absorption, excretion and intermediary metabolism’, pp.331-349.

Scientific leader and integrator

Doug Waterhouse was a renowned entomologist, a fine scientist and an accomplished administrator. He worked within the CSIRO Division of Entomology for over 60 years, and was its Chief for 21 years until his retirement in 1981. When Nicholson retired as Chief of the Division of Entomology, the CSIRO Executive, following a worldwide search, had no hesitation in appointing Doug as his successor in 1961. While Nicholson had steadfastly maintained that he did not wish to increase the size of the Division, that was not Doug’s way. He could foresee many opportunities for working on new ways to control pest species. In 1964 he presented a seminal paper to the CSIRO Executive calling for recognition of a diversity of approaches to pest management ‘ cultural, physical, host resistance, genetic control, behavioural control and biological control. He advocated an integration of these approaches into the practice of integrated pest management (IPM). The ambitious proposal ended with the following statement:

No-one should underestimate the threat posed by insects. They inhabited the earth 300 million years or more before man and will probably inhabit it after the last vertebrate has perished. We do well to prepare for a prolonged contest.

Doug addressed the 12th International Congress of Entomology in London on his plans and on the divisional achievements. Most importantly, he enlisted the full support of the CSIRO Executive. In particular, he gained the ear of Sir Otto Frankel, who was then the executive member responsible for the Division. The plan was approved by CSIRO. It set the Division on course to become internationally recognised as a major centre for entomological research. Doug negotiated not only for three new projects a year, but also for the facilities, including new field stations in Australia and overseas, to support the newly appointed staff. CSIRO’s decision to back Doug was fully vindicated with the favourable findings of the 1978 Marsden Report ‘ an external and independent economic analysis of some of the Division’s research. The analysis demonstrated a return on investment that could truly be called outstanding.

Honours and awards

The blowfly research earned Waterhouse a DSc from the University of Sydney. During his illustrious career Doug received many distinctions and awards which are presented in the accompanying biography Douglas Waterhouse.



This page was last updated on

10 February 2011