Journal of the American Mosquito Control Association, 10(4):540-544, 1994 Copyright @ 1994 by the American Mosquito Control Association, Inc.
URBANIZATION AND ITS EFFECTSON THE ECOLOGY OF MOSQUITOESIN MACAU, SOUTHEASTASIA
EMMETT R. EASTON
Centre for Extension Studies, University of Macau, P. O. Box 3001, Macau via Hong Kong
ABSTRACT. Recent urbanization in Macau fras resulted in the precipitous decline to zero in popu- lations ofseveral anophelinevectors ofmalaria wtiile providing optimal habitat for the population increase in culicines.Of I 8 speciesof mosquitoesreported in Macau in recentyears, 15 speciesare included here. Culex quinquefasciatus,Culex sitiens, and Aedesalbopicrur were the most abundant species.Notes are provided for I nophelessinensis, Armigeres magnus,Armigeres subalbatw, Culexfoliatus, Culexfuscanus, Culex infantulus, Culex rubithoracis, Culex sumatranus, Culex tritaeniorhynchus,Mansonia undormis, Toxorhynchites splendens, and Tripteroides sp.
INTRODUCTION ber ofspecies (70) were identified previously in the neighboring colony of Hong Kong (Chau Macau consists geographically of a peninsula l 982). of land connected to a larger island area of main- land China as well as 2 smaller islands that are MATERIALS AND METHODS connected to the peninsula by either 2 roap Adult mosquitoes were collected from March bridges or a causeway. Malaria is no longer a through September 1991 on Taipa Island with a disease of public health importance in the tef- New Jersey light trap (NJLT) (Hausherr's Ma- ritory. Even though Kwoh (1948) reported 6 spo- chine Works, Toms River, NJ) equipped with a cies of anopheline mosquitoes occurring in Ma- 25-W frosted bulb as an attractant. The trap was between 1945 and 1948, and active casesof cau placed on the University of Macau campus. Win- malaria were discussed by GonEalves (1952), only dow collections were made during the same pe- Anopheles sinensis Wiedemann and Anopheles riod with a battery-powered aspirator that was tesselatus Theobald were believed to be present also used for biting collections of female mos- by 1983 (Morais 1984). Urbanization that has quitos attracted to a human volunteer. Larval taken place in recent years has resulted in the collections were made with a standard enamelled reclamation of all swampy or suitable Anopheles dipper (0.47 liter) with an extendable handle to larval habitats on the Macau peninsula. The rap- search fish ponds, irrigation ditches, or cisterns. id urbanization, however, has created suitable A soup ladle with the inside of the spatula end many other peft habitats for the development of painted white was used to sample water collec- mosquito species. This trend is expected to coi[- tions that were too shallow for the dipper. Phy- least 1999, when Macau will become tinue to at totelmata examined for mosquito larvae includ- of the economic zones of mainland China. one ed the leaves of Nepenthes mirabilis prtc}l.er plants In past, studies of mosquitoes in Macau have the that grow vinelike in ravines on granite slopes mainly the vectors of malaria. More concerned along hiking trails on both the islands of Taipa recently, a zoological survey conducted by sci- and Coloane in Macau. The water content of l0 Institute ofTropical Science in entists from the leaves/plant was sampled monthly from January 1988 and 1989 has resulted in Portugal during 1990 to April 1991. l,arvae from pitcher plant becoming available on the cu- more information leaves were allowed to develop to maturity in Macau (Ramos 1990) along with the licines of the laboratory in artificial containers of similar preliminary studies made by Easton (1992a, size as the leaves. Standard mosquito breeders r992c, 1993). (Bioquip Products, Santa Monica, CA) were used well her immediafe The Macau region as as to rear larvae collected from water sources other have long be(n surroundingsin mainland China than pitcher plant leaves. Immatures and adults inveb- consideredremote in respectto scientific were identified with the manual by Chau (1982) fauna, and little tigations regardingthe Oriental for the Hong Kong mosquito fauna, assuming in the literature. In an information has appeared that these 2 areas share many similar faunal el- (Leitao S/ego- early account 1923),the mosquito ements. myia fasciata was mentioned as occurring here, so one purpose of the present study was to de- RESULTS AND DISCUSSION termine if Aedesaegypti (Linn.) still occurs here. A second objective was to identifr other repre- Culex quinquefasciatus Say, the southern house sentativesofthe culicidaebecause a sizablenum- mosquito, is considered the most abundant spe- 540 Drcer\rBER1994 UnsANrzATIox lNp Mecnu MosQtrrrors 541
'l (Table l). It inhabits all domi- ol*l \o co (n cies in the territory ll (.|rO ciles or buildings in Macau that are not centrally :. 1 €15 air conditioned. It is the most important species -alZO l'- o0l N biting man in dwellings during periods of twi- A EI dwellings not 3l light, being able readily to enter I properly The author noted a somewhat ^l screened. ql similar situation in Guangzhou on mainland ol o\o\o ti cnoo o China (Easton and Au Yeung 1986) where living
Until these depressions are filled with fresh water are no spring-fed streams on the island ofTaipa, and stocked with predatory fish, the site will sup- but rainwater can accumulate in man-made dams port mosquito breeding. at higher levels and constantly flows to lower Culex sitiens Wiedemann (l 16 males. 243 fe- levels before emptying into the Pearl River es- males attracted to NJLT) was the second most tuary. During heavy rains, if gutters are not pro- abundant mosquito collected. Apparently rang- vided, serious erosion and mudfalls can occur, ing throughout the Oriental region, it is consid- but when these gutters are semi-clogged with or- ered a brackish water species ofcoastal marshes ganic matter, such as small twigs or leaves, the in Hong Kong (Chau 1982) and may bite humans pools created can also serve as larval habitats. at night some distance away from the sea. Adults Discarded automobile and truck tires often are attracted to the Cultural Centre windows or the moved from Macau across the border to main- NJLT in this study could have been attracted land China. When these tires are left lying in old from Coloane Island (l-2 km distant), as larvae fields that are partly shaded by tall grasses or had been collected from rock crevices near the shrubs, they serve as a mosquito breeding source. sea near Ka-Ho village. This mosquito may now Tires lying in the open sun do not contain live inhabit the water-logged mangrove forest near mosquitoes because summer temperatures great- Taipa Island where a land barrier recently has er than 35"C would soon exceed the upper limit been constructed as a portion of a reclamation of the mosquito's temperature tolerance. The project. This measure now isolates the mangrove beneficial mosquito Toxorhynchites splendens trees from receiving flushes ofsaline water from (Wiedemann) has been found occupying rubber the estuary. The presence of appreciable num- tires (l larva, I pupa, August 27, l99l) in an old bers of this species on windows of the University field near Hac-Sa village on Coloane island. Lar- Cultural Centre (Table l) during early morning vae of Ae. albopictus were found in the same tire hours but not on windows at other parts of the and most likely constituted part ofthe food source campus suggests that they were attracted to a ofthe predatory species. These predatory larvae, colony of nesting P. montanus spalrrowsthat were however, require I Yz-2 months to mature where- living behind a nearby air-conditioning unit. as Ae. albopictus lawae probably can mature in Murphy (1990) briefly mentioned this mosquito 6-7 days. In Macau, Toxorhynchites mosquitoes transmitting Plasmodium j uxtanucleare bird prefer habitats that contain appreciable organic malaria in the vicinity of mangrove forests in matter, such as a tree-hole site, so their use in Singapore. biological control for Ae. albopictus is limited Aedes albopictus (Skuse), even though collect- when the latter are found in abandoned tin cans ed uncommonly by the NJLT, is nevertheless a or in rain gutters where high summer tempera- very common mosquito in wooded areas of Ma- tures (35"C) evaporate sources ofrainwater after cau. On Taipa Island, biting rates of mosquitoes a few days. The tree-hole habitat in Macau is attracted to the lower legs of a human volunteer somewhat limited for mosquito development; the averaged 8-10 females/min over a Vr-h period author has located very few sites that contain during one late afternoon in August. Because le. water for any appreciable period. The upper albopictus often is found in wooded areas, it is branches of Ficus macrocarpa, the Chinese Ban- not considered an urban mosquito on the Macau yan tree, could provide habitats in areas where peninsula. It often bites humans during late af- the trees are shaded. Other tree species that could ternoons in late summer and can be bothersome provide a tree-hole habitat on the islands have to tourists who visit the hiking trails on Taipa a shorter life span due to termites that eventually (Trilho da Taipa Grande) or Coloane (Trilho da kill them. The flame tree, Delonix regia, has been Coloane Grande). The resident Chinese are only planted along roadsides in urban areas and has occasionally observed hiking in Macau on these been observed in Papua New Guinea (E. Easton, trails, so blood meals needed for reproduction unpublished data, I 988) to provide tree-hole sites of this mosquito probably are obtained from di- for Toxorhynchites as well as other species, but urnal avifauna or reptiles. Breeding has been ob- in Macau the water in their upward-spreading served in waste (Lixo) containers that have been branches soon evaporates in summer due to high erected along the trails. Even though the open- daily extreme temperatures. Fig trees (Fictts sp.) ings of these containers are on the sides near the as well as other species of trees growing in a more top, rainwater can accumulate if the containers densely wooded environment (i.e., Agriculture are not emptied on a regular basis, and there is and Forestry Park, Siac Pai Van) would tend to generally ample organic matter present to serve have less exposure to the sun so that water in as larval food. tree-hole habitats would tend to persist longer. larvae of Ae. albopictzs also have been found Notes on other species: Aedes aegypti was not in rain gutters that line the trails or are con- found in Macau during this study. In the neigh- structed along roadways on both islands. There boring colony of Hong Kong, where Ae. aegypti DncervrssR.1994 UnsANrzArroN .lNo Mlceu MosQurrors 543 was reported in the late 1950s, the specimens thoracis (Leicester) larvae have been collected apparently were discovered on vessels arriving from the same site as Cx. foliatu.t above. In Hong from other countries (Chau 1982). In Macau at Kong Cx. rubithoracis commonly inhabits present, Cx. quinquefasciatus occupies urban swampy fields or ground pools and ponds con- habitats in places where Ae. aegypti potentially taining water hyacinth, Eichornia crassipes. could survive, whereas le. albopictus is found in Culex sumatranusBrug inhabits pitcher plant similar water catchments in rural areas that are leaves along with ar. magnus on Coloane Island shaded by trees. On the islands, the mosquitoes' (Ramos 1990) and along the Trilho de Taipa food sources could be diurnallizards(Calotes sp.) Grande hiking trail on Taipa Island (Easton or birds because the mammals and insectivores 1992b\. Larval abundance in the leaves is lowest on Taipa and Coloane islands are all nocturnal during the spring months from March through in habit. May and highest during the winter season from Anopheles sinensls(one female, May 10, 1991, September through February. Even though the NJLT) is believed now to be a relatively uncom- water volume in the leaves in spring is greater mon species in Macau because of urbanization. than at other times of the year because spring is The habirat on the Macau peninsula formerly the period of the greatest amount of rainfall in inhabited by this species (Morais 1984) was re- Macau, most of the leaves have been produced claimed by 1988. Larvae of this species were during late summer of the previous season. New collected by the author on the edge of a grassy leaves do not open on these plants until July or banked reservoir at Siac Pai Van on Coloane August, which accounts for the greater numbers Island, August 199 l. of larvae of both Ar. magnus and Cx. sumatranus Armigeres magnus (Theobald) commonly in- during late summer, and by the spring of the habits leaves of Nepenthes mirabilus where they following year most of the immatures will have grow on granite slopes or ravines on Coloane developed. The existence of lst-instar larvae of Island (Ramos 1990) or on Taipa Island (Easton Cx. sumatranus in the leaves during February as 1992b).1-,arvae were found inhabiting the leaves well as in June, long after the leaves have opened of this plant during all months of the year, but the previous seasons,provides evidence that more highest densities were found from September to than one generation of Cx. sumatranus can de- February with fewer numbers from March to velop per year in one N. mirabilis leaf. l.arvae May. During the spring of the year, there are reared in the laboratory at temperatures only fewer water-containing leaves because newly slightly lower than environmental completed their formed leaves do not open until later summer. life cycles in less than 50 days. In Hong Kong (Chau 1982), Ar. magnus is re- Culex tritaeniorhynchus Dyar. One female, ported also from N. mirabilisleaves, but in other September 8, 1991, on windows of the Univer- areas of the Orient, such as Malaysia, tree holes sity Cultural Centre. In Hong Kong, Chau (1982) seem to be preferred as larval habitat. listed this as a common species in ground pools, Ar mi geres subalbatus (Coquillett) occasionally water hyacinth fields, fish ponds, rice fields, and is attracted to lights from the University build- irrigation ditches where there is emergent vege- ings at night (Table l), and larvae occur in pol- tation. luted waters (Chau 1982). In Hong Kong, it is Mansonia undormis (Theobald). One female, reported to feed on pigs and cattle as well as on September l, 1991, NJLT. The eggsof this spe- humans. cies are laid in clusters on the undersides offloat- Culexfoliatus Brug. Larvae ofthis species were ing leaves ofaquatic vegetation, and larvae pierce collected in a flooded field containing taro plants, and attach to the stems and roots ofwater plants. Colocassia esculenta, near Hac-Sa village on Co- Water hyacinths commonly reach Macau by loane Island, July 1991. In Hong Kong, Chau floating downstream from mainland China when (1982) reported larvae of this species living in one ofthe branches ofthe Pearl River is in flood. side pockets of clear streams such as in the Tai When these plants become established in fresh Po Kau forest area in the New Territories. water habitats on the peninsula or on one ofthe Culex fuscanzs Wiedemann. Adults are at- islands, conditions are favorable for the devel- tracted occasionally to windows on the Univer- opment of Ma. uniformis. sity campus (August l99l). In Hong Kong they Tripteroides sp. Twenty-five or more adults, live in highly polluted ground water area where April I I, 1991, hanging below roofat entrance they prey as larvae on Cx. quinquefascialzs. Ra- of horizontal mine shaft flooded with water, mos (1990) examined larvae collected from a Choec-van, Coloane Island. In Hong Kong, Trip- cement tank on Coloane Island in Macau that teroides aranoides lawae have been reported from also contained Ae. albopictas and Culex palli- bamboo stumps (Chau 1982) and from pitcher dothorax Theobald. plants in West Malaysia (Beaver 1979), but I Culex infantulus Edwards and Culex rubi- have not located larval habitats in Macau. The 544 Jounter, or tHe Ar\,mRrcANMosqurro CoNnor Assoctlrror.r Vor. 10,No.4 food source of this speciesis not known here, Macau. Centre of Macau Studies,University of Ma- but the opening of the mine shaft is shared by 7 cau, Instituto Cultural de Macau. speciesof insectivorous bats (3 speciesof Min- Easton,E. R. 1992b. 1990additionstotheannotated iopterus,2 Myotis sp., one Hipposiderossp., and list of the insectsof Macau. Entomol. News 103:3O- 36. oneRhinolophus sp.)as well as the nesting violet Easton, E. R. 1992c. Ecologicalhabitats of mosqui- whistling thrush, Myiop honeuscaeruleus. toes (Culicidae) in Macau. Proc. XIX International Three additional speciesof Culex reported by Congressof Entomology. Abst. X[C-2,505. Ramos(1990) in Macau,namely Cx. pallidotho- Easton,E. R. 1993. Ecologicalstudies regardingman- rax, Culex pseudovishnuiColless, and Culex va- biting mosquitoes (Diptera: Culicidae) in Macau. Acta gans Wied., were not collected in this study. Parasitol. Portug. l:42. Easton,E. R. and S. S. Au Yeung. 1986. Mosquito captures using a mechanical aspirator and an en- ACKNOWLEDGMENTS cephalitis surveillance trap on Guangzhou City, Guangdong Province, People's Republic of China. Much appreciation is given to Chau Gar-Wai, J. Am. Mosq. Control Assoc. 2:92-93. Pest Control officer, and the technicansworking Gongalves,F.l. 1952. Algumasnolas sobreo palu- in his section ofthe Urban ServicesDepartment, dismoem Macau.An. Inst. Med. Trop. (Lisb.) 9:485- Hong Kong Government,Kowloon, for their help 490. in the identification of certain mosquito species, Kwoh, B. C. S. 1948. A generalreport of Malaria and mosquito control in Macau during the year 1945- particularly Cx. Cx. infantulus, and Cx. foliatus, 1947. Macau Governo de Macau. rubithoracis. The author also acknowledgesM. LritSo, A. D. N. 1923. Apergu nosologique Macao F. Ferreira and M. M. Morais, Health Services et les agentstransmitteurs de la peste. Tellurologie Department, Macau Government, for local in- et Climatologie Medicalesde Macao (Macao Station formation on mosquito breeding sources. Climatique). Morais, M. M. 1984. Servigode Combate ao Sezon- ismo. Relat6rio Annual, Dirreg6o dos Servigos de REFERENCESCITED Safde, Macau. Beaver,R. A. 1979. Faunaand foodwebsofpitcher Murphy, D. H. 1990. Insectsand public health in the plantsin WestMalaysia. Malayan Nat. J. 33(l):1- mangrove ecosystem,pp. 423452. 12.'C. L. Ming 10. and P. K. L. Ng (eds.). Essaysin zoology. Depart- Chau,G. W. 1982. 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