Larval habitat of Anopheles philippinensis: a vector of malaria in Bangladesh.

Reviews/Analyses Larval habitat of Anopheles philippinensis: a vector of malaria in Bangladesh M. Elias1 This article reviews the various types of larval habitat of the malaria vectorAnopheles philippinensis Ludlow in Bangladesh and characterizes its breeding ecology. Discussed also are the possible implications of the environmental changes on its breeding habitats resulting from intensified land use brought about by population increase and developments in irrigation and water resources. Introduction Out of 34 known anopheline mosquitos, four species (Anopheles dirus, A. minimus, A. philippinensis, and A. sundaicus) are the principal vectors of malaria in Bangladesh (1-4).a In 1991 and 1992, however, A. aconitus and A. annularis were also identified as vectors of epidemic malaria in Bangladesh (30, 32). Although some information on the vector potential- ity and bionomics of the malaria-carrying mosquitos in Bangladesh has appeared (5-9), detailed infor- mation on different types of breeding habitats, especially of the plain-land malaria vector A. philippinensis (6), is difficult to obtain. The present article reviews the various types of breeding ha- bitats and characterizes the breeding ecology of A. philippinensis in Bangladesh. Discussed also are pos- sible implications on its breeding habitats arising from intensified land use caused by population increases and irrigation and water resources developments. I Professor of Medical Entomology, National Institute of Preven- tive and Social Medicine (NIPSOM), Mohakhali, Dhaka-1212, Bangladesh. Requests for reprints should be sent to this address. a Plan of operation for malaria eradication programme (1960- 1974): A signed document of the Government and WHO. Dhaka, unpublished document, 1960. Reprint No. 5724 Breeding ecology The preferred breeding sites of A. philippinensis are tanks, ponds, marshy lands, and rice fields with good vegetation and with clean water (6, 10-18). Both Christophers (10), in 1912, and Covell (11), in 1927, found that A. philippinensis bred in rice fields in the Andamans. Bose (12), in 1931, stated that this species could be attracted or repelled from village tanks by introducing or removing suitable vegetation. Sen, in 1935, reported that it bred in rice fields in Bengal but that its frequency was low (13). In 1936 Ramsay & Macdonald reported that A. philippinensis required cool water and hence favoured permanent pools with vegetation under slight shade (14). In 1941 Sen reported that the relative frequency of A. philippinensis breeding in ponds overgrown with aquatic weeds was usually 35 times greater than that in rice fields (15). The larvae of this species were recorded also in Bengal in water containing all types of plants, except Lemna (duckweed); however, breeding was most frequenctly associated with the filamentous algae Spirogyra. In 1942 Iyenger reported that A. philippinensis usually bred in ponds and that the main breeding season was from July to October (16). The depth of the water-table below the surface during the breed- ing season appears to have a marked influence on the prevalence of this species. In villages where the water-table was low, the density of A. philippinensis Bulletin of the World Health Organization, 1996, 74 (4): 447-450 © World Health Organization 1996 447 M. Elias was high; in villages where the water-table was close to the ground its density was very low. A significant positive correlation was observed between the den- sity of this species and the depth of the water-table below ground level during the wet season. In 1944 Iyenger reported that A. philippinensis larvae were not commonly found in rice fields and that this species bred mostly in large permanent rather than temporary ponds. Furthermore, it showed a definite preference for ponds fully exposed to sunshine that contained water with a high dis- solved oxygen content. A. philippinensis bred only in clean water and not in water that was even slightly contaminated with sullage or decaying organic mat- ter. The following types of submerged vegetation were most favoured by this species for breeding: Hydrilla verticillata, Ceratophyllum demersum, and the aquatic species of Utricularia and of Najas. These plants form dense subaquatic clumps, which often reach the surface and offer good shelter to the larvae without obstructing full illumination of the water by sunshine. Certain forms of nonfilamentous green al- gae were frequently found in association with A. philippinensis larvae, and evidently form their main food as shown by examination of their gut contents. Stretches of water that contained certain types of aquatic vegetations such as Lemna and Eichhornia speciosa (water hyacinth) and some phytoplankton such as Microcystis aeruginosa, Euglena spp., and other blue-green algae (e.g., Anabaena spp. and Oscillatoria spp.) were unfavour- able breeding areas for A. philippinensis mosquitos (17). In 1944 Covell noted that it bred in tanks, pools, borrow pits and ditches with vegetation (18). Although A. philippinensis did breed in rice fields in Bengal, Sen, in 1948, attributed its generally limited tendency to breed in such fields to the follow- ing factors (19). First, the absence of green algae (Spirogyra) in rice fields because of the increased shade when rice plants grow to heights ¢'75 cm. Second, the water temperature in rice fields, which reaches -420C, i.e., beyond the tolerance limit of the species. Quraishi et al., in 1951, reported that because of changes in the courses, a number of dead rivers had formed in East Bengal (currently Bangladesh) and that A. philippinensis bred in and around such rivers (20). In 1952 a study carried out in Mymensingh dis- trict reported that A. philippinensis usually bred in dead rivers or marshes with submerged vegetation located 0.9-1.80m from the edges (21). The inci- dence of heavy rainfall had a considerable influence on the breeding of this mosquito. Krishnan, in 1969, reported that the favoured breeding places of A. philippinensis were tanks, pools and ditches (22). In 1964 Ghiasuddin reported that tanks with clear water and aquatic vegetation were the pre- ferred breeding sites of this mosquito, and that most of the larvae avoid the heavy shade of overhanging trees.b The larvae were also collected from stagnant water around rice fields, but not in the rice fields themselves. During entomological investigations between 1966 and 1968 in greater Rangpur district (Rangpur, Gaibandha, Kurigram, and Nilphamari districts), A. philippinensis larvae were also collected from tanks and beels (marshlands) with aquatic veg- etation. In the course of malaria eradication and con- trol programme activities, A. philippinensis larvae have been found in several other districts in tanks, ponds, and beels associated with submerged vegeta- tion (N.P. Maheswary, personal communication, 1982). In 1982 Elias et al. also noted that the favoured breeding places of A. philippinensis were tanks, ponds and ditches associated with submerged vegetation (3). Also, in 1987, in Gazipur district (Dhaka) Elias et al. found that the distribution of A. philippinensis larvae was as follows: 64.1% in beels with vegetation; 33.3% in rice fields; and 2.6% in ponds with vegetation. In 1972, in Burma, Khin-Maung-Kyi reported that A. philippinensis bred in stagnant water, es- pecially in wide stretches of water with emergent vegetation, as well as in ponds, tanks, or swamps with grassy edges (28). Also, Macan, in 1948, reported that in Burma it bred in derelict or cultivated rice fields (29). The preferred larval habitat and breeding ecol- ogy of A. philippinensis are summarized in Table 1. Owing to its breeding specificity, insecticidal susceptibility (23, 24), pressure of DDT residual house spraying,c as well as environmental and socio- cultural changes (e.g., intensive land use with modi- fication of crop cultivation pattern, large-scale use of tanks, ponds and marshes for irrigation purposes, increased fishing, repeated flooding of permanent and suitable breeding sites), the presence of A. philippinensis and the incidence of malaria have de- creased in the plains of Bangladesh in recent years. For example, in 1949-50 in a district of Mymensingh division Quraishi et al. recorded catching an average of 6.2-11.7 A. philippinensis per bedroom over 30 min in some villages, where the parasite rate lay in the range 18.7-30.7% (20); they also recorded 168 A. philippinensis larvae in 280 shallow areas in marshy Ghiasuddin M. Report on Anopheles philippinensis Ludlow. Unpublished report, Malaria Eradication Programme, 1964. cInternational assessment of the Malaria Programme, Bangla- desh, 1-28 October 1989. Unpublished document, Malaria Control Programme, 1989. 448 WHO Bulletin OMS. Vol 74 1996 Larval habitat of Anopheles philippinensis in Bangladesh Table 1: Characterization of the breeding ecology of Anopheles philippinensis in Bangladesh Very favourable Favourable Unfavourable Breeding place type Tanks, permanent ponds, Temporary ponds, permanent Rivers, drains, temporary pools, small marshland (beel) pools, ditches, dead rivers, water collections, seepage, saline rice fields water, containers Vegetation type Filamentous alga Spirogyra; Other filamentous algae and Lemna (duckweed), Eichhornia Submerged vegetation such as submerged vegetation speciosa (water hyacinth); some Hydrilla verticillata, Ceratophyllum phytoplankton such as Microcystis demersum; aquatic species aeruginosa and Euglena spp.; blue- of Utricularia and of Najas; and green algae such as Anabaena spp. nonfilamentous green algae and Oscillatoria spp.; plants which grow above the water surface in such a manner as to block direct sunlight; certain floating waterplants such as Azolla pinnata, Salvinia natans and S. cucullata Water type and illumination Clean water exposed to Clean water, light shade Contaminated water with sullage or sunshine with high dissolved decaying organic matter; dense oxygen content shade; heavy flooding and heavy rainfall areas or dead rivers in this district. During a pre- eradication survey in 1960, an average of 0.05-0.29 A. philippinensis were caught per man per hour in the same district of Mymensingh division, and the parasite rate varied from 0.69% to 29.0%.d In contrast over the period 1981-92 in the same dis- trict only seven adult female A. philippinensis were caught in 190 villages surveyed (N.P. Maheswary, personal communication, 1992), and the annual malaria slide positivity rate was 0.29- 4.13%. A very low density of A. philippinensis (0.02- 0.03 man biting rate per night) was also recorded in Rangpur division (zone-3) in 1966-68 (slide positivity rate, 0.06-0.42%). In 1993 Birley reported that although the land west and south of the Jamuna river was highly malarious in 1916, it is not so today, while the area east of this river still has a small risk (31). The reduc- tion in malaria risk in the plains of Bangladesh can be attributed to the intensification of land use and increase in human population density, while the abundance of the A. philippinensis vector appears to have declined as environmental changes have dis- placed its breeding sites. Concomitantly, it has been reported that A. philippinensis has almost disap- peared from West Bengal, India (25-27). Nevertheless, the revival or establishment of new and/or alternative water stretches that are eco- logically suitable for mosquito vector breeding and the resurgence of A. philippinensis and of malaria in the vast plains of Bangladesh cannot be ruled out. d See footnote a, p. 447. On the other hand, the recently identified secondary/ suspected malaria vectors (A. aconitus, A. annularis, A. vagus, and A. subpictus) may assume an impor- tant role in reintroducing malaria to the plains. Envi- ronmental changes brought about by intensified land use, fishing, and the creation of embankments, dams, barrages, irrigation channels, changes in river courses for flood action plans, and/or any other wa- ter resources developments in the plains of Bangla- desh could also alter the malaria transmission pattern. The surveillance and monitoring of disease vectors and of malaria and other vector-borne dis- eases need, therefore, to be carried out at regular intervals. Resume Habitat larvaire d'Anopheles philippinensis, vecteur du paludisme au Bangladesh Cet article pr6sente les divers types d'habitat larvaire du vecteur du paludisme Anopheles philippinensis au Bangladesh et les caract6ristiques ecologiques de sa reproduction. On y examine aussi les reper- cussions possibles des modifications consid6rables de 1'environnement, qui ont perturbe les gites lar- vaires de cette espbce et qui ont ete principalement dues a l'intensification de l'utilisation des sols et au d6veloppement de l'irrigation et des ressources en eau. Globalement, ces modifications ont entraine une reduction de la densit6 d'A. philippinensis. 11 ne faut toutefois pas n6gliger le r6tablissement ou la cr6ation possibles de nouvelles etendues d'eau WHO Bulletin OMS. Vol 74 1996 449 M. Elias qui conviendraient comme gites larvaires pour les moustiques vecteurs, ni la resurgence d'A. philippinensis et par consequent du paludisme qui s'en suivrait dans les vastes regions de plaine du pays. 11 est par consequent important d'exercer a intervalles reguliers une surveillance des vecteurs de maladies et une surveillance du paludisme et autres maladies a transmission vectorielle. References 1. Ahmed T. Checklist of the mosquitoes of Bangladesh. 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