Malaria transmission - mosquitoes, humans and their behaviour
In his article on entomology and evolution, J.R. Busvine (1993) writes of the "few cases" where it has been suggested that a genetically controlled change of behaviour may have followed insecticide use. My study of the response of the malaria vector, Anopheles farauti, to use of DDT residual spray in houses in the Solomon Islands is one of those cases (Taylor, 1975) but, to judge from Busvine's comments it is unusual in being unambiguous.
The main work was carried out on the island of Makira, or San Cristobal, between June 1971 and April 1973, and involved regular, indoor and outdoor, human-biting catches from dusk to dawn, at four villages. Two of the study villages, Baunasughu and Manibwena, were sprayed in October 1971, during the first cycle of routine six-monthly house spraying, at a rate of 2.0 g of technical DDT/m², on Makira. The other two villages, Arohane and Maniparegho, were left unsprayed until October 1972. As happened elsewhere in the Solomons, two other, closely related and equally important, malaria vector species, Anopheles koliensis and Anopheles punctulatus, disappeared throughout Makira after the first spray round and showed no subsequent resurgence. During the interim year at Arohane and Maniparegho, however, both species continued to be caught.
In contrast, the numbers of farauti caught at Baunasughu and Manibwena dropped immediately after the first spray -round but some eight months later the numbers started to increase markedly and soon attained the original levels. Along with the resurgence in numbers, the catches revealed a change from a pre-spraying population which fed primarily indoors (indoors : outdoors, 1.46 : 1.00) and throughout the night, to a post-spraying population which fed predominantly outdoors (0.52 : 1.00) in the three hours after sunset (80%; with 47% biting in the first hour and almost none after midnight). Moreover, before spraying, the indoor and outdoor biting cycles differed significantly (with the outdoor biting being greater in the first three hours) but after the resurgence the cycles were identical. Two other pieces of evidence came from Arohane and Maniparegho - firstly, the ultimate commencement fo spraying did not affect the numbers caught; and, secondly, the behaviour pattern altered progessively over the interim year. The implication was that the original farauti population in the small area containing only the two unsprayed villages had been replaced gradually by a newly dominant population from the surrounding area.
The farauti behaviour change certainly did not involve any increased avoidance of DDT. In a parallel experiment at Arohana, a single house was sprayed in April 1972 and the results showed that the pre-spraying population was deterred from entering this single DDT-sprayed house in an otherwise unsprayed (entering sprayed : unsprayed, 0.25 : 1.00). This did not alter after general spraying, in fact the rate of entry into houses may even have increased slightly. What emerged also was that the deterrent effect declined sharply some four months after the DDT was sprayed onto the walls. Even in areas under spray cover for over ten years, susceptibility testing showed no physiological resistance to DDT and any farauti female which did enter and feed in a house was vulnerable to its lethal effect.
At the time, for lay purposes, I used the term "behavioural species" to describe the apparently changed population of farauti and emphasised that the change was no more than part of the cause of continuing malaria transmission in some areas of the Solomons, despite house-spraying operations of a high standard. Traditionally, the Melanesian people retired indoors at sunset but in more "enlightened" areas this habit broke down (a combination of changed working hours and the money to buy artificial lighting) and, especially on northern Guadalcanal, they could be found out of doors well after dusk. With the change to early-evening biting, the fact was that the mosquito had no need to enter houses and malaria transmission could continue unabated. I tried hard to underline how this would affect the predicted success of the Malaria Eradication programme but the "authorities" in the Solomons and WHO refused to accept my findings; let alone heed my warnings about the absolute need for efficiency in the MEP operations. Sadly, time has shown me to be correct. In 1962, before any DDT house-spraying, the malaria parasite rate in blood-films from adult Melanesians was around 30%. By the early 1970's the case rate was no more than 17.5/1000 per annum; but by 1983 this had risen to some 340/1000. During the Second World War, within weeks of the 1942 landings, the malaria rate in soldiers of the US forces on Guadalcanal rose from zero to 1558/1000. The opposing Japanese had even higher rates of infection and the capacity of the Americans to implement effective control measures was a crucial factor in their ultimate victory. One of those measures was blanket larviciding by aerial spraying; this gave nearly 100% kill of larvae and, in 1972, an elderly villager asked me why the MEP did not adopt the same tactic. Quite apart from the cost of such operations, he gave me a simple justification as to why not - he admitted that the local bird populations had dropped dramatically.
What may have been true, but was irresolvable at that time, is that my study revealed the existence of "cryptic sibling species" which were (or are) morphologically farauti. The ongoing work based at the University of Queensland (Foley et al., 1993) already has revealed at least six sibling species of farauti based on electrophoretic keys. Dr. J.H. Bryan (personal communication) tells me that further species may be delineated from the Solomons and Vanuatu. The separation out of farauti No. 1 larvae by exposure to salinity (Foley et al., 1993) poses the intriguing possibility that my observation of behaviour changes, being based on data from villages by, or not far from, the coast, could reflect an elimination of a fresh water (perhaps more abundant or more dominant) farauti. This would tie in also with the fact that the resumption of malaria transmission in the Solomons occurred mostly in areas where mangroves were found, i.e. with brackish pools on the inland side.
Much remains to be done, however, as apart from a few night catches, Foley et al. (1993) present sparse information to interpret the significance of the allozyme species. During my PhD research, which was prior to my going to the Solomons, I recorded the flight activity of farauti from Rabaul, Papua New Guinea. In the normal tropical daylength, 12h light and 12h dark, this population was highly crepuscular, with little activity between the peaks which came after light-off and light-on. When the light:dark regime was changed to constant dark, the bimodal activity continued showing that the rhythm was circadian in nature (Taylor, 1969). The crepuscular pattern suggests, however, that my recordings were of a post-spraying population. Spencer et al. (1974) decribed work from Papua New Guinea where results were rather like those from the Solomons; pre-spraying farauti females could be trapped man-biting at all times of the night with a preponderance between 9 pm and 3 am; post-spraying the dominant numbers were between 6 and 9 pm. Their report, however, gives no indication of any difference between indoor and outdoor biting patterns. Using a genetic technique, Dr. Bryan delineated females which she trapped on Guadalcanal in 1972 as farauti No. 1, which she had found also to be the species encountered in the New Hebrides (now Vanuatu) from whence the holotype farauti had been named by Laveran in 1901. House spraying on Guadalcanal had started in 1963 so farauti sensu stricto may well be the dominant post-spraying species. One of the earliest field studies of farauti was in the New Hebrides (Daggy, 1945), where, unlike in any other location, it was found to bite by day as well as throughout the night, albeit in shady places. The highest numbers, however, were caught in the first hour after sunset.
Could the problem of a change in the observed behaviour of a vector have been predicted? in 1962, during preparatory work for the MEP pilot project, it was established that the vectors were susceptible to DDTand that they habitually rested on the indoor walls of houses after a blood meal, but, to quote Macgregor (1968), "In the absence of a professional Entomologist, investigations of vector bionomics had to be deferred". Later an entomologist did become available (from March 1964 to October 1968) but, although the problem of residual transmission by farauti was recognised, "the reasons why this species showed such an unsatisfactory response to DDT house spraying in certain parts of the project area could not be determined". The work on unsprayed islands had remained concentrated on collections of mosquitoes resting inside houses by day because "while only one night catch could be carried out during a twenty-four hour period many different villages could be inspected during daylight hours" (Slooff, 1972). If the programme adopted on Makira had been followed in 1962; that is all-night human-biting catches (initially 24h human-biting catches were undertaken) made simultaneously both indoors and outdoors and at regualr intervals for whatever time was necessary to encompass seasonal climatic changes; the outcome might have been different.
Although much of the foregoing may seem somewhat historical, the story does have much contemporary significance. The modern belief in the value of impregnated bed nets for malaria control has considerable merit and it is perhaps ironic that the Americans on Guadalcanal in 1943 believed that the enforced (military discipline) use of bed nets impregnated with DDT 5% in kerosene was the most valuable single measure against mosquito bites. However, as I pointed out to Dr. Brian Greenwood of the MRC Banjul laboratories, there seems to be an over-generous assumption that people will retreat under the nets from sunset to sunrise and, at least, he and his colleagues have taken note of my findings (Lindsay et al., 1993). In the Solomons, the MEP house-spraying with DDT acted in much the same way as the permethrin impregnated mosquito bed nets - it deterred the vectors from entry and killed those which did enter. Service (1993), although dealing primarily with active community participation in self-help schemes for the control of vector-borne disease, comments on "people's perceptions and customs" and describes problems with the use of impregnated bed nets, such as their resemblance to a shroud. The recognition of people's behaviour as a factor in the vector-human relationship is not mentioned. Recent experience from living in Africa is that the hours between sunset and midnight are a time of much social and domestic activity, with children no less active than adults and commonly sitting outside the house, especially when there is electricity to light up the compound. On an evening in 1972, a large congregation attended an outdoor evening service held on Nggela Island to commemorate a major event in the Christian history of the Solomons; one of the unintended results was a significant malaria epidemic - so delicate was the balance between the interruption and resumption of transmission.
Finally, I would like the emphasise the volume of work involved in the delinetaion of the farauti behaviour change. The core of the effort was 97 separate all-night man-biting catches by a team of three collectors and a supervisor, plus my own monitoring visits. The study ran continously from June 1971 to April 1973 and a total of over 5,000 man-hours was invested. A standard WHO type DDT susceptibility test can reveal insecticide-resistance from no more than a few hours of work. Thus, no one should be surprised that there are several hundred cases of physiological resistance and only a few cases of change of behaviour; the reason is something the laboratory-bound might care to remember.
Purely incidentally, Antenna recently has carried remarks on multiple authorship, especially in relation to the naming of new species (Rose, 1993). The paper by Lindsay et al. (1993) perhaps is even more remarkable and not just because it has eight authors. It is among eight papers, most multi-authored, published in a special Supplement of the Transactions of the Royal Society of Tropical Medicine and Hygiene on the evaluation of malaria control methods in The Gambia. An uncharitable observer might find it curious that at least one of the authors appears on all eight papers - a cynic might suspect an element of self-aggrandisement.
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