Bull. Org. mond. SantJ 1963, 29, SuppI., pp. 19-24 Bull. Wid Hlth Org.

Arthropod Vectors of Public Health Importance

D. J. LEWIS I

In spite of the outstanding successes achieved in the control of vectors with insecticides, serious difficulties have been encountered in recent years. This has led to renewed interest in the possibilities ofbiological and other methods of control. The author reviews briefly relevant aspects ofthe biology ofvectors, with examplesfrom various groups. A thorough knowledge of the ecology of the vectors and their breeding habits may some- times permit control by manipulation of the environment, by attacking reservoirs of disease, or by the introduction ofpredators, pathogens or parasites. The injudicious use of these methods may, however, upset the biological balance and recoil dangerously. Answers to theproblems involved will befound more readily ifspecialists can arrange to payfrequent visits to the field and undertake field work themselves. There is also a need for closer co-operation among workers in different scientific disciplines; this would enable the various approaches to be co-ordinated and promote the achievement of integrated control.

DDT has been in use for some 20 years and, with whose biology is likely to explain some current other modern insecticides, has achieved many out- difficulties in malaria eradication. Chironomidae, standing successes. Resistance, difficulties of organ- although not exactly " vectors ", are a serious pest ization and application, and harmful effects on on the Nile and an example of the lesser known beneficial organisms and even on man himself have, groups. A few years ago the principal species was however, renewed interest in biological and other found to be new to science, and the early stages of means of control. The time has come to review the most species are still undescribed. strategy of controlling of medical Cytological studies, as used for the Prosimuliun importance. I shall discuss some aspects of the hirtipes complex in North America, may solve biology of vectors that are relevant to control at the problems of the Simulium neavei complex of Africa. present day, and give some examples from various Other requirements for the blackflies (Simuliidae) groups. are studies of the non-anthropophilic form of S. damnosum and the species of northern South America. Recent investigations of ticks have shown Detailed studies of vectors are continually re- that " Ornithodorus moubata" comprises three vealing the existence of sibling species; these intro- species. duce problems of identification but help to clarify epidemiology and sometimes facilitate species DISTRIBUTION sanitation. Current studies of Phlebotomus in Kenya have shown that three species may transmit kala- Few works on taxonomy or biology deal extensive- azar there but they are only distinguishable by ly with distribution and there is much scope for characters of the males. Many species of sandflies further study, not only in disease-ridden areas but (Phlebotominae) have been discovered by examina- in those where infection may spread or be awaiting tion of the cibarial armature, and one wonders how discovery, such as some of the parts of Africa where many species of biting arthropods remain unre- kala-azar is unknown. Little is yet known of the cognized because they lack such a taxonomically blackflies in the Yemen where onchocerciasis is useful structure. Reid (1962) believes that many reported to occur. species await discovery, and he discusses the recently recognized balabacensis MORPHOLOGY The morphology of the system of anal hooks of 1 Scientific Staff, Medical Research Council, c/o British Museum (Natural History), London, England. blackfly larvae may explain why they are killed by

1312 -19- 20 D. J. LEWIS extremely small amounts of DDT and have been measures may very soon regain much of their old slow to show any resistance. The insecticide causes importance (Symes et al., 1962). the hooks to release their hold so that the larvae are The chironomid pest at Khartoum is an unforesee- swept downstream. They thus have prolonged con- able result of the building of the Sennar dam 354 kilo- tact with the drifting insecticide and may be eaten metres upstream; further biological research would by predators or find themselves in unsuitable still be necessary to show whether a larvicide is likely to water (Field, 1961). be always effective, what type, formulation and con- By studying changes in internal structures of centration should be used, and when and where it many it is possible to estimate their physio- should be applied. logical age, a knowledge of which is necessary for Breeding conditions of blackflies are such that understanding host-pathogen relationships and eva- control is very successful in some places and im- luating the effect of control measures. Changes practicable in others. In difficult areas it is necessary in the tunica propria of the ovarioles are often to adopt intermittent or other partial methods of difficult to see and interpret, but follicular relics, control, to find new methods of attack, or to define and sometimes other structures, give the important areas which cannot be dealt with. Blackfly larvae information that an has ingested blood and are among the few particle-feeding inhabitants of possibly parasites. streams, and Hynes (1960) has suggested that an insoluble suspended-solid insecticide could be used BREEDING CONDMIONS to kill blackfly larvae while affecting few other organisms. S. damnosum and Glossina tachinoides The nature of the larval and pupal environment in Nigeria sometimes breed in atypical sites; this often determines methods of control. The larvae should be considered in relation to any plans for of many African sandflies and of tsetse are eradication. dispersed in the soil, so that control must often be Chrysops silacea, the vector of Loa loa, breeds in directed against the adults. wet mud and could be controlled by flooding, but Some breeding places of Anopheles gambiae and this might lead to an increase in the number of Aedes aegypti are so restricted that it is more . Fortunately, larvicides can be used at practical to kill the larvae than to attack the adults infrequent intervals because the larval stage lasts with residual insecticides. Filaria vectors of the nearly a year. Long ago studies of the larval ecology Aedes scutellaris group in the Pacific breed in small of houseffies led to useful control measures, but collections of water but these are too numerous to these were sometimes neglected after the introduc- be dealt with easily. An important vector, Culex tion of residual insecticides and resistance was pipiens fatigans, is particularly resistant to some followed by outbreaks of flies and flyborne disease. insecticides and the control of its breeding places, The trombidiid-mite vectors of scrub typhus are although they are largely domestic, presents adminis- difficult to control if the vegetation is too dense to trative problems. Water plants have an important allow an insecticide to reach the soil. (Traub & influence on some mosquitos. Eight years after the Dowling, 1961). Jebel Auliya reservoir was created on the White to Nile the ecological succession of plants, difficult INSECTS foresee, produced huge masses of floating grass ECOLOGY OF ADULT which harboured larvae of the relatively harmless This is a vast subject, some aspects of which are Anopheles pharoensis. It is important to control also dealt with in the paper by Dr Davis (see this the harvesting of the grass or other activities that Supplement, page 127). might cause this mosquito to be replaced by large numbers of dangerous anophelines. Introduced The environment exotic plants, such as water hyacinth (which harbours larvae of filaria vectors in the orient and has reached Exophilic species. Most vectors live out of doors the Nile) and Potamogeton perfoliatus (which where many are difficult to attack with chemicals. shelters mosquito larvae in the Gezira canals), In the Sudan Republic, the sandfly vector of leish- might be important in some of the new or proposed maniasis lives in soil cracks, in Kenya largely in the reservoirs. These and other aquatic plants are likely air shafts of certain termite hills, and in Costa Rica to receive special attention because anti-larval among vegetation. Further knowledge may well ARTHROPOD VECTORS OF PUBLIC HEALTH IMPORTANCE

lead to insecticidal or other control methods. Past Movement. Many insects move quickly through studies of sandflies in the Middle East have been open country and are stopped by vegetation. A devoted mainly to endophilic species, and current tree barrier is a useful protection against Tanytarsus work in outdoor habitats is likely to add to our (Chironomidae) in the northern Sudan in a situation understanding of zoonoses. In South America, where the cost of studying and controlling the early some of the sandfly vectors of leishmaniasis and stages might be prohibitive. The flight of S. damno- mosquito vectors ofjungle yellow fever are far from sum, and therefore its biting and egg-laying activities, houses and impossible to control. Some exophilic are hindered by thick forest. Clearing for agri- sandflies and mosquitos (Colbourne, 1962) stay culture, which is unfavourable to S. neavei, is likely indoors just long enough for residual insecticide to to increase the mobility of S. damnosum in some affect them. In contrast to most insects are certain very wet regions and, with it, the risk of oncho- more or less endophilic anophelines and the body- cerciasis. Forest clearance could protect people lice and bed-bugs. from Chrysops silacea but is more expensive than using larvicides. Protective clearings often deter Vegetation. Trees and bushy vegetation provide Glossina palpalis from biting people. a suitable environment for many insects, and Central American sandfly vectors of cutaneous Nulliparous andparousfemales. It is often import- leishmaniasis are diminishing owing to deforestation. ant to distinguish parous females. In blackflies, for In the Sudan Gezira irrigated area, the almost instance, it is otherwise impossible to interpret the complete absence of vegetation except cotton and observed rate of infection with Onchocerca because millet probably causes nearly all Anopheles gambiae the proportion of parous females observed often to rest in houses and be affected by residual spray. depends on the time of capture. The virtual disappearance of Simulium woodi from Egg-laying. Very large numbers of eggs of some the Cholo area of Nyasaland after forest-clearance species of Simulium can easily be obtained by for tea-growing (Lewis, 1961) suggests that oncho- closely-confining or decapitating gravid females. cerciasis may sometimes be controlled unintention- The young larvae would be useful for tests with ally by deforestation. The vegetational requirements insecticides whereas old ones are often difficult to of S. neavei give it a sporadic distribution and so obtain. In this and other ways much research can set the scene for its eradication from Kenya. The be done in spite of the difficulty or impossibility of well-known extensive studies of tsetse environment maintaining a laboratory colony of blackflies. have led to large-scale control by discriminative clearing. Owing to increased costs this has been partly replaced by the use of insecticides but there ASSOCIATED is sometimes a risk that the flies will return to the Various animals besides vectors play a part in unaltered environment. Lumsden (1962) considers epidemiology. that research on the of Glossina has ecology given Zoonoses. diseases are disappointing results with regard to its main aim, Many arthropod-borne and he emphasizes the need for frequent reappraisal zoonoses and it is sometimes easier to attack the in view of changing situations. animal reservoir-such as dogs in some leishmaniasis areas-than the vector. The medical of Clearing of vegetation sometimes does harm, as significance some sandflies, ticks and migrating birds is being in the Malayan rubber areas where it caused Ano- clarified by studies of certain viruses (Hoogstraal, pheles maculatus and malaria to increase. 1962). Behaviour Simulium and crabs. The discovery of the remark- Rest. The effect of residual insecticides depends able association between immature S. neavei and largely on resting habits. Some of the triatomid crabs led to the extermination of this important " " vector in Kenya, and the association is now being vectors of Chagas' disease are domestic but, in after engorgement, may live in deep cracks for studied other territories. months and escape the effects of insecticide, so that Natural enemies. The term " biological control" improved housing seems to be the only permanent is sometimes used for applied biological control method of control. Blackflies and tsetse flies may (Beirne, 1962) and sometimes for both this and the bite near houses but few enter them to rest. influence of all the biological agents that, with 22 D. J. LEWIS

other factors, effect the " regulation " of all species Competitors. Harmless species may compete (Turnbull & Chant, 1961). There have been relative- with, and replace, pests (Beirne, 1960), as in Kenya, ly few attempts at biological control of medically where Phlebotomus garnhami sometimes crowds out important insects, but introduction of natural P. martini, the vector of kala-azar (Minter-personal enemies might at least contribute to control in communication, 1962). conjunction with other factors (Simmonds, 1960). Applied biological control of biting flies may prove Animals for human food. Larvicides for simuliids more difficult than that of agricultural pests (Beirne, sometimes kill fish directly or by destroying their 1960) because the immature stages of most biting prey, and control of S. metallicum was delayed in flies inhabit water or damp places where environ- for this reason. On the Upper Volta, mental changes affect them and their enemies. Arnoult & D'Aubenton (1960) advised that larvicide Jenkins (1960) considers that the numerous predators should not be used during the breeding time of of medically important insects may prove less useful certain fish in the early rains. It has recently been than pathogens and parasites. found that DDT may accumulate in passage from I will refer only briefly to a few examples of one animal to another, and Jamnback (1962) has natural enemies. Jenkins (1960) mentions Empusa accordingly been investigating larvicides less stable papatassi as a parasite of sandflies but found no than DDT. published indication of particularly promising Successor insects. There is sometimes a risk that enemies of these insects. Numerous nematodes have a harmful arthropod will take the place of one that been found in a few sandflies and it may be that has been controlled. other parasitized flies are incapacitated and therefore escape capture. Blackflies, on the other hand, have PRACTICAL IMPORTANCE many parasites, among which protozoans and mermithids appear to be the most important Bites and allergic effects (Jenkins, 1960). A digenetic trematode attacks I will refer briefly to pests that do not transmit Simulium exiguum in Venezuela and seems to prevent pathogens, because in some places they are more it from biting, but this parasite requires three hosts important and more difficult to control than vectors, and would probably be easier to protect than to and because their study in temperate regions is multiply. The danger to blackflies' enemies from relevant to vector control in warm countries. In- insecticides varies from one situation to another. numerable infestations of biting insects must have A single eradication campaign may leave a " sword occurred without being reported because inhabitants of Damocles "-a threat of catastrophic outbreaks become desensitized. With the progressive develop- of simuliids (Hynes, 1960); on the other hand, in ment of new areas and increasing travel, however, some rivers successful chemical control has operated the arrival of newcomers is obliging authorities to for years and the larvae, in their specialized niche, undertake extensive programmes of control. Chiro- may have few enemies. Much can be done to nomidae are a pest in scattered places in India, protect enemies by careful choice and application of Africa and North America, and at Wadi Halfa on insecticides. the Nile many people are admitted to hospital with Houseflies are sometimes apparently controlled by asthma attributed to these flies. The notorious out- ants in Puerto Rico and Malaya (Pimentel, 1955; breaks of Simulium griseicolle bring many human Reid, 1953). It is often difficult to see the value or activities to a halt. future use of some enemies, and it is interesting to note Buxton's (1955) opinion that enemies of tsetse Transmission of disease puparia might be more effective than was realized Transmission dynamics. In Tahiti an experimental and that ways might be found of making use of combination of drug therapy and partial mosquito them. control, accompanied by observations on the potential transmissions index, have stopped filariasis Scavengers. Houseflies are surprisingly scarce in transmission (WHO Expert Committee on Filariasis, some countries (Simmonds, 1960, and others). One 1962). It is hoped that where Simulium damnosum possible cause is the removal of breeding media by is difficult to control, partial measures may lead to dung beetles (Lewis, 1958), which have been intro- reduction of the serious symptoms of onchocerciasis. duced into Fiji for this purpose (Howden, 1962). The lesser symptoms are by no means negligible, ARTHROPOD VECTORS OF PUBLIC HEALTH IMPORTANCE 23

however, and it is desirable eventually to stop of which blackflies can transmit other filariae transmission altogether. The number of flies neces- Gambian sleeping sickness might spread into sary to maintain transmission may vary from place healthy districts where Glossina tachinoides occurs. to place as in the case of plague fleas on rats. Season of transmission. It is sometimes possible CONTROL to restrict control measures to a limited transmission season. In Ghana, Marr & Lewis have found little In considering measures against any arthropod transmission at a time when larviciding is difficult pest it is necessary to decide whether control is because the rivers flow intermittently. practicable or whether it is better to remove people from danger, to protect them with drugs or repellents, Associated pests. It is sometimes necessary to or to destroy the animal reservoir of a disease. If consider more than one pest at a time, for instance control is feasible it is occasionally advisable to in Nigeria when people settling on land cleared of consider the possibility of eradication. Control can Glossina tachinoides are assailed by other pests. An be achieved by modifying the environment, by occasional hazard is schistosome infection of people applied biological control, by insecticides, by steri- who control mosquitos and black flies. It is some- lizing males or various other new methods, or by times possible to control more than one vector by integrated control (Picket, 1949; Van den Bosch & use of a single pesticide. Thus, a certain molluscicide Stern, 1962).1 can kill mosquito larvae (Gretillat, 1962), and residual insecticides for anophelines have been INVESTIGATIONS known to affect triatomid vectors of Chagas' disease There is much scope for improvement in control, (Symes et al., 1962), sandflies, culicine vectors of but many problems exist and others are sure to filariasis, Aedes aegypti, Xenopsylla cheopis and arise. New methods of investigation are developed, other pests. Information is required, however, about such as the important age-grouping technique the effect of antimalarial spraying, and cessation of largely unheard of a few years ago, and researches spraying, on other diseases. sometimes involve botany, hydrology and other Secondary vectors. Secondary vectors of malaria non-zoological subjects. Fortunately, the eradica- are now attracting attention, and Simulium exiguum tion of malaria in many countries has freed some may prove to be a secondary vector of onchocerciasis. entomologists for work on new problems. All the time, the vast literature in many languages is in- Spread ofvectors and disease. Vectors may spread, creasing. No research organization can attack its with disastrous results, as in the case of Anopheles problems from every possible angle, and there is an gambiae in and Egypt. Kala-azar evidently increasing need for visits and field work by special- spread to eastern Kenya in recent decades and may ists, and for identification of considerable numbers of extend to other areas where suitable sandflies now arthropods of " difficult " groups. Arrangements for exist without the disease. If yellow fever virus collaboration should allow specialists to make plans reached eastern Asia it would find vectors in the many months ahead, taking into consideration both shape of Aedes aegypti and A. albopictus. Oncho- their own programmes and the best times for field cerciasis may spread into areas now thinly populated. work. Many people must have carried this long-living parasite from Africa to various countries, in some 1 See also the paper by Laird in this Supplement, page 147.

ACKNOWLEDGEMENTS

I am grateful to Dr L. P. Corbet, Dr J. A. Reid, Dr B. N. Smallman and Dr H. E. Welch for various data used in compiling this paper. 24 D. J. LEWIS

RItSUMI

L'application des insecticides aux arthropodes vecteurs effet d'intervenir a diff6rents niveaux, selon divers pro- de certaines affections a inscrit a son actif toute une cedes: modification du milieu ambiant, destruction des s6rie de succes remarquables; depuis quelques annees animaux reservoirs de maladies, introduction d'agents cependant, la methode se heurte a des difficult6s consi- predateurs, pathogenes ou parasites. d6rables qui tiennent notamment au d6veloppement de Toutefois il ne faut pas perdre de vue qu'appliques la r6sistance des vecteurs envers les insecticides et aux sans menagement ces methodes risquent de bouleverser effets nocifs de ces derniers sur des organismes utiles du 1'equilibre biologique et d'avoir des repercussions dange- monde vivant. Une telle situation a donn6 un regain reuses. Les specialistes envoyes sur le terrain ou ils d'actualit6 a d'autres formes de lutte, et surtout aux prennent part aux activites pratiques s'attachent a trouver procedes biologiques. des solutions a ces problemes. Par ailleurs le besoin se Empruntant ses exemples A divers groupes de vecteurs, fait de plus en plus sentir d'une collaboration etroite entre I'auteur analyse rapidement certaines particularit6s de travailleurs scientifiques appartenant a diverses disci- leur biologie qui presentent de l'int6ret pour la conception plines. Un tel effort se donne pour but l'etablissement et la mise au point de moyens de lutte nouveaux. Une d'un programme global de lutte contre les arthropodes connaissance at la fois plus approfondie et plus pr6cise qui sont importants du point de vue de la sante publique en divers domaines - taxonomie, morphologie, distri- en tant que vecteurs de maladies. bution, ecologie, modes de reproduction - permet en

REFERENCES

Arnoult, J. & d'Aubenton, F. (1960). Med. trop., 20, 607 Lewis, D. J. (1958) Trans. roy. ent. Soc. Lond., 110, 81 Beirne, B. P. (1960) Biological control-research in Lewis, D. J. (1961) J. anim. Ecol., 30, 303 Canada. In: American Institute of Biological Sciences, Lumsden, W. H. R. (1962) Nature (Lond.), 195, 1139 Biological control of insects of medical importance, Picket, A. D. A. (1949) Canad. Ent., 81, 67 Washington, D. C., p. 94 (mimeographed report of a Pimentel, D. (1955) J. econ. Ent., 48, 28 conference) Reid, J. A. (1953) Bull. No. 7, Inst. Med. Res. Malaya Beime, B. P. (1962) Ann. Rev. Ent., 7, 387 Reid, J. A. (1962) In: Verhandlungen des XI. internationa- Buxton, P. A. (1955) The natural history of tsetse flies, len Kongresses far Entomologie, Wien, 1960, vol. 2, London, Lewis p. 302 Colboume, M. J. (1962) Trans. roy. Soc. trop. Med. Hyg., Simmonds, F. J. (1960) Activities of the Commonwealth 56, 179 Institute of Biological Control. In: American Institute Field, G. (1961) J. econ. Ent., 54, 607 of Biological Sciences, Biological control of insects of Gretillat, S. (1962) Bull. Wld Hlth Org., 26, 67 medical importance, Washington, D.C., p. 98 (mimeo- Hoogstraal, H. (1962) In: Verhandlungen des XI. inter- graphed report of a conference) nationalen Kongresses fiir Entomologie, Wien, 1960, Symes, C. B., Thompson, R. C. M. & Busvine, J. R. vol. 3, p. 87 (1962) Insect control in public health, Amsterdam, Howden, H. F. (1962) Proc. roy. ent. Soc. Lond. C, Elsevier 27, 23 Traub, R. & Dowling, M. A. C. (1961) J. econ. Ent., Hynes, H. B. N. (1960) Ann. trop. Med. Parasit., 54, 331 54, 654 Jamnback, H. (1962) Mosquito News, 22, 384 Turnbull, A. L. & Chant, D. A. (1961) Canad. J. Zool., Jenkins, D. W. (1960) Pathogens, parasites andpredators 39, 697 of medically important insects. In: American Institute Van den Bosch, R. & Stem, V. M. (1962) Ann. Rev. Ent., of Biological Sciences, Biological control of insects of 7, 367 medical importance, Washington, D.C., p. 6 (mimeo- World Health Organization, Expert Committee on graphed report of a conference) Filariasis (1962) Wld Hlth Org. techn. Rep. Ser., 233