Joumal of the American Contol Association, 15(2):92-97, 1999 Copyright A 1999 by the American Mosquito Control Association, Inc.

MOSQUITO AND AQUATIC PREDATOR COMMUNITIES IN GROUND POOLS ON LANDS DEFORESTED FOR RICE FIELD DEVELOPMENT IN CENTRAL SULAWESI.

M. MOGI,' T, SUNAHARA'AND MAKMUR SELOMO,

ABSTRACT, Aquatic habitats, mosquitoes, and larvivorous predators were studied on deforested lands in Central Sulawesi, Indonesia. Open ground pools, mainly in depressions made by the treads of bulldozers and other heavy equipment, were numerous but because of their small size, comprised ca. lEo or less of the total area of the deforested lands studied. The dominant mosquitoes in these pools were Anopheles vagus, vishnui, , and Culex gelidus. The lst 2 species were dominant in clear pools, whereas the latter 2 species were dominant in turbid pools. The dominant metazoans other than mosquitoes were Crus- tacea, Ephemeroptera, and Chironomidae. Both aquatic and surface predators were abundant. Dominant among aquatic predators were Anisoptera and Zygoptera nymphs, Dytiscidae, and Notonectidae. These results are discussed in relation to mosquito control on deforested lands that transitionally but inevitably appear during the course of rice field development projects in Indonesia.

KEY WORDS Deforestation, mosquito, Anopheles, Culex, aquatic predator, Indonesia

INTRODUCTION immediately follows deforestation, malaria epidem- ics may occur within a few months after settlement Development of irrigated rice field systems on (Partono et al. L973). Mosquito control should be deforested lands brings about drastic changes in the started at the early phase of development projects. environment. Closed forest ecosystems are even- The Government of Indonesia has promoted tually replaced by open rice agroecosystems inter- health programs in settlement areas to overcome spersed with farm villages. The transition phase be- disease problems that may hamper development tween these 2 sharply contrasting landscapes may projects (Binol 1983). However, in the case of mos- last for months or even years once a project is be- quito-borne diseases, basic information on mosqui- gun. The present study focuses on mosquito and toes and their ecology in project areas in eastern aquatic predator communities occurring during one Indonesia is virtually nonexistent. One reason for of the subphases of this transition between prede- this gap is that remoteness of such project areas velopment forests and postdevelopment rice lands. impedes surveys. Mosquitoes in forest and rice ecosystems are The aim of this repbn is to describe aquatic hab- well investigated. Howeve! mosquitoes in the tran- itats and associated mosquito larvae and larvivo- sition phase have not been well investigated. An rous predator communities on lands deforested for exception is the record of mosquito fauna and abun- rice field development in Central Sulawesi, eastern dance during the course of the Mahaweli irrigation Indonesia. Such information could be a basis to es- development project in (Amerasinghe tablish ecologically sound and comprehensive strat- and Ariyasena 1990, 1991). These authors also not- egies for control of mosquitoes and mosquito-borne ed sparsity of aquatic predators (fish and diseases in development project areas. predators as a whole, without speciflcation) in open rainwater pools on the recently deforested land. On Indonesia's outer islands, rice field develop- MATERIALS AND METHODS ment projects are being implemented extensively to Study area: The study was conducted in Septem- fill the increasing demand for staple food due to ber 1996 in Toili, Kabupatan Luwuk-Banggai, on population increases. Many of these projects the eastern peninsula of Central Sulawesi. The set- involve settlement of from Java and Bali tlement of this area began in the 1970s' and irri- where malaria has successfully been controlled and gated rice fields already e-xisl around the older vil- people are not immune to malaria. Consequently, lages. However, in the surrounding areas, epidemics of malaria have been reported in the set- deforestation, settlement, and development of new tlement areas including those on Central Sulawesi are still progressing. (Abisudjak and Kotanegara 1989). The occurrence rice fields The area has a slightly seasonal tropical (ca. of filariasis also has been reported in the settlement 1"30'5) climate with a index (100 X number of areas (Partono et al. 1973). As human settlement Q dry months with <60 mm precipitation/number of wet months with >100 mm precipitation) of 14.3- ' Department of Microbiology' Division of Parasitology, 33.3 (Whitten et al. 1988). The mean annual pre- Saga Medical School, Nabeshima 5-1-1, Saga 849-8501' cipitation is 1,500-2,000 mm. The wettest months . are usually June and July but may vary from year 2 Faculty of Public Health, Hasanuddin University' Jl. the wet season was extended and P. Kemerdekaan, Tamalanrea, Ujung Pandang 90245' ln' to year. In 1996, donesia. considerable rains preceded the census.

92 JuNr 1999 MoseumoEs AND PREDAToRCouwuNtttps Il.t INooNsste

The study was done at 2 sites where deforesta- tion, which started 3 months before, had almost Moilong W n=668 been completed. Large trees and their roots had Median=1.1m 4 been removed and the lands had been bulldozed. One site, Moilong Atas (Moilong hereafter), was 70 ha of dry land with light and heavy forests be- fore deforestation. The other site, Topo Delapan (Topo hereafter), was I29 laa. Before deforestation, I'o two thirds of Topo was dry with light forests but (J one third was wet with semiaquatic grass, bushes, (2O 6uo and some taller trees. Moilong and Topo are f Topo n=1250 m above sea level, and ca. 15 km apart. o *W o Median=o.6m z Census: The entire area of each study site was ri 20 inspected on foot. The sizes of all pools were re- corded, with approximation to rectangles (length x width) or circles (diameter). Water depths were 10 (10 cm, except for a few large pools in the wet area of Topo. Fifty-five sampling pools were arbitrarily selected y' from sites where presence of mosquito larvae was z' zoz' 2' z' f t t f z' t z" z9 visually conflrmed. Mosquitoes and predators were Poolsize (m )' collected by a dipper, with 1-30 dips per pool, de- Fig. 1. Frequency distributions of pool size on 2 de- pending on pool size. The dip contents from a sin- forested sites (Moilong and Topo), Central Sulawesi, In- gle pool were combined and sieved through a 1OO- donesia.Size was expressedas exponentsof 2. mesh net. Mosquitoes were sorted out in situ. Mosquitoes and the remaining contents were pre- served separately in lOVo formalin solution for later identification under microscopes. This procedure depressions made by the treads of vehicles engaged was adopted to determine the main mosquito spe- in deforestation and leveling. Total areas ofthe sur- cies most efficiently under the limitations of labor face water in Moilong and Topo were 1,934 m2 and and time available for sampling. 15,119 m2, respectively. The surface water occu- Identification' Mosquito larvae and pupae were pied O.3Vo (Moilong) and l.2Vo (Topo) of the total identified to species with keys of Reid (1968) and deforested area. Sirivanakarn (1976, 1977). Other aquatic metzrzo- All pools were fully exposed to sunlight, without ans were identifled to family or higher levels with emergent and floating macrophytes. However, wa- keys of Ueno (1973) and Kawai (1985). ter quality differed between dry and wet areas. In Analysis: Degree of similarity between faunas dry areas, either in Moilong or Topo, the land sur- was examined with Spearman's coefficient of rank face was largely bare due to loss of or inversion of correlation. Differences in frequencies of occur- the surface soil. Consequently, pools there were rence were tested with Fisher's exact probability generally clear except some muddy pools recently test, because frequencies less than 5 are included in disturbed by working vehicles. A few clear pools most taxa. The calculations follow Sokal and Rohlf had submerged clumps of filamentous green algae. n98l). Pools in the wet area (one third of Topo) were generally turbid with rich infusions from tall grass patially buried in the soil at the time of leveling RESULTS or occasionally from grass piled up and left by bull- dozers. This incomplete work apparently Pool conditions was the result of difficulty of manipulating heavy vehicles Most pools were small (Fig. 1). At Topo, more on the wet land. Below, data for pools in the dry than TOVo of pools had areas less than or equal to areas of both Moilong and Topo were combined 1 m', with a peak frequency at the range of 0.5 and compared with those in the wet area of ToDo. (exclusive)-1 (inclusive) m2. A few pools (1Zo) in the wet area were larger than 25O fi:,., with a max- Mosquitoes imum of 4,00O m,. At Moilong, more than i5Vo of pools had areas less than or equal to 2 m2, with a Fourteen mosquito species were collected (Table peak frequency at the range of l-2 m2. The maxi- 1). Specimens belonging to tlnefraudalrlx subgroup mum pool size at Moilong was 50O mr. This pool of subgenus Ittphoceraomyia of the genus Culex was formed by the flooding of a tributary bloiked were not identified to species because of loss ofkey by downed trees that had been thrown into this trib- setae. The same mosquito species occurred in dry utary. This was the only pool exceeding 250 m, in and wet areas, with a few minor exceptions. How- Moilong. Almost all pools less than 2 m2 were in ever, for the order of dominance, no correlation was 94 JounNal op rsr AvenrceN Mosqurro CoNrnol Assocr.lrroN VoL. 15,No.2

Table 1. Mosquito species collected from open ground pools on deforested lands in central Sulawesi, Indonesia.

Dry area Wet area

Fre- Fre- Difference quencyr quencyr between Species Total no. No./dip (Vo) Total no. No./dip (Vo) frequencies2 A nop hele s p edi t aeniatus 6 o.o2 6 3 0.01 NS Anopheles vagus 420 1.31 72 24 0.08 JJ P < 0.05 Culex bitaeniorhynchus 544 1.70 10 0 0 0 NS Culex fuscanus 4 0.01 10 69 o.23 42 P < 0.05 Culex gelidus 2 0.01 3 2,096 6.99 58 P < 0.001 Culex infula 66 o.2l J 0 0 0 NS Culex nigropunctatus tt 0.05 10 34r t.t4 42 P < 0.05 Culex pseudovishnui 49 0.l5 l0 2 o.o1 8 NS C ulex tritaeniorhynchus 164 0.51 3l 1,263 4.2r 83 P < 0.01 Culex vishnui 812 2.54 79 t0l o.34 50 NS C ulex (Lophoce raomyia) sp. 0 0 0 43 0.14 l4 NS Mansonia sp. I 0.003 3 0 0 0 NS Mimomyia sp. I 0.003 J 0 0 0 NS U ranotaenia (U ranotaenia) sp. l4 0.04 7 0 0 0 NS Total 2.100 3.942

I Percentage no. positive pmls/no. all pools. 'NS, not significant.

found between the areas (Spearman's coefficient of Predators rank correlation r : 0.079, df : 12, P > 0.05). of were Cyclopoida, In dry area pools, Theobald and More than 9OVo Crustacea Some Cyclopoida are predacious but Crustacea Anopheles vagus Doenitz were encountered most here as nonpredators, because Cyclo- frequently. Culex bitaeniorhynchus Giles exceeded were treated poida contributed little to predation mortalities in An. vagus, in numbers collected, but larvae of Cx. mosquito larvae in rice fields (Mogi et al. 1986). bitaeniorhynchus were concentrated in a few pools Predator taxa grouped at family or higher levels with clumps of filamentous green algae. In wet area contmon to dry and wet areas, except for fish pools, the dominant species were Culex tritaenio- were and water mites. Fish were collected in only 2 pools rhynchus Giles and Culex gelidus Theobald. They in the dry area of Topo, but those pools were on were followed by Culex nigropunctatus Edwards, the boundary between dry and wet areas. Water Cx. vishnui, and Culex fuscanus Wiedemann. mites were collected only from 2 pools in the wet Therc, An. vagus was a minor component. Differ- area. ences in frequencies of occurrence were significant In the dry area, Anisoptera nymphs, Notonecti- for An. vagus, Cx. gelidus, Cx. tritaeniorhynchus, dae, and Dytiscidae were dominant aquatic preda- Cx. nigropunctatus, artd Cx. fuscanus. tors, whereas Zygoptera was a minor component. High numbers per dip recorded for Cx. gelidus In the wet area, Dytiscidae, Zygoptera, and Ani- and Cx. tritaeniorhynchus in the wet area were the soptera were dominant. Differences in frequencies result of high concentrations of these species in of occurrence were significant for Zygoptera. Av- some pools with rich infusions of accumulated erage numbers of all aquatic predators per dip were grass. In such pools, densities frequently reached between I and 2. Surface predators all belonged to >10 individuals per dip. Hemiptera. They were less abundant than aquatic predators. Metazoa other than mosquitoes and predators

In addition to mosquitoes, dipper samples in- DISCUSSION cluded a variety of Metazoa (Table 2). The most abundant were Crustacea, Ephemeroptera, and Chi- Rain is the principal source of water on the de- ronomidae in both dry and wet areas. Members of forested lands studied, so the number and size of these groups were collected more frequently (sig- pools would vary according to precipitation. The nificant for Ephemeroptera and Chironomidae) with study was conducted after a period of abundant more numbers per dip in wet areas. The difference rain, so both pool numbers and size were probably in frequencies between areas was also significant at a high level. Without rainfall, pool areas may for Gastropoda. Nevertheless, the metazoan fauna decrease rapidly and under severe drought all pools (including predators but excluding mosquitoes) was except some in the wet area may disappear. How- conelatedsignificantly between the 2 areas(spear- ever,this transitionphase, typically characterized man'sr" : 0.638,dt : 2O,P < 0.01). by numerous temporary open ground pools, is un- JUNE 1999 MoseurroEs AND PREDAToRCovuuNnms rN lNpoNeste 95

Table 2. Metazoa other than mosquitoes collected from open ground pools on deforested lands in Central Sulawesi, Indonesia. Dry area Wet area Fre- Difference quency2 Frequency2 between Taxonl Total no. No./dip (vo) Total no. No./dip (7o) frequencies Gastropoda l0 0.03 34 0.11 A' P < 0.05 Acari Hydrachnellae3 o 0 0 ) o.o2 t7 NS4 Crustacea 1,616 5.05 62 1,499 5.00 76 NS Insecta (L) Ephemeroptera 629 1.97 66 959 J.L I 100 P < 0.05 Zygoptera (L)3 9 0.03 2l 204 0.68 67 P < 0.01 Anisoptera (L)3 155 0.48 76 64 0.21 58 NS Mesoveliidaes 16 0.05 .A 18 0.06 50 NS Veliidae5 79 o.25 69 49 0.16 83 NS Gerridae5 t3 0.04 l3 9 0.03 25 NS Notonectidae3 83 o.26 59 t7 0.06 JJ NS Belostomatidae3 19 0.06 t7 6 o.02 77 NS Corixidae 5 o.o2 7 I 0.003 I '7 NS Trichoptera (L) 0 0 0 0.003 8 NS Dysticidae3 100 0.31 52 134 o.45 83 NS Hydraeridae I 0.003 J 8 0.03 8 NS Hydrophilidae (L)3 l1 0.03 l7 3 0.01 t7 NS Hydrophilidae (A) l4 0.04 t7 4 o.o1 t7 NS Helodidae (L) 0.o1 7 8 0.03 JJ P : O.05 (L) Ceratopogonodae t4 0.04 7 0 0 0 NS Chironomidae (L) 546 1.7| 72 2.687 8.96 100 P < 0.05 Teleostomi3 J 0.01 7 0 0 0 NS Anura (L) 6 o.o2 7 I 0.003 8 NS Total aquatic predators6 384 1.19 497 r.66 Total surface predators 108 o.34 76 o.25 I L or A in parentheses indicates larvae/nymphs and adults, respectively. Thxa without this ' designation include both lavae and adults. Percentage no. positive pools/no. all pools. 3 Aquatic predator n NS, not significant. 5 Surface predator. 6Aquatic predators * Culexfuscanus in Table 1 avoidable in the course of rice field development tritaeniorhynchus wete among several species preceded by deforestation. dominant in open rainwater pools on deforested I-)ominant mosquito species were influenced by lands in Sri Lanka (Amerasinghe and Ariyasena pool conditions that at least partly depend on the l99O). Anopheles vagus is a potential vector of ma- predeforestation conditions (dry vs. wet) of the laria and filariasis (Abisudjak and Kotanegara area. As the 2 areas were continuous in Topo, the 1989), whereas Cx. tritaeniorhynchus, Cx. vishnui, difference is attributed to differential responses of and Cx. gelidus are potential vectors of Japanese ovipositing females to pool conditions. All of the encephalitis virus (Burke and Leake 1988). dominant species are breeders in temporary open shoncoming of this study is that frequencies ground pools, ,A including irrigated rice fields. In Sri of occurrence for all pools were not determined Lanka, dominance ranks of rice field mosquitoes (samples were taken only from mosquito-positive did not rise until the start of irrigation (Amera- pools). Inspection of all pools in a small area (ca. singhe and Indrajith 1994). This more comprehen_ 5OO m') in Moilong indicated that both anophelines sive study included any kind of surface wafer hab_ and culicines occupied ca. SOVoof pools (Sunahara itats with larger surface (e.g., areas marshes), so et al., unpublished data). The study areas were lo- abundance of mosquitoes in temporary pools re_ cated at the periphery of irrigated rice field areas, mained relatively low. which facilitated mosquito colonization. Domestic Anopheles vagus and Cx. vishnui are known as such as and horses in the nearbv rice colonizers of rice flelds -those with sparse vegetation production villages also must have favored transplantation (Mogi .PTty _after and Miyagi mosquitoes by providing blood-meal sources. 1990, Mogi et al. 1995). Anophelei vagus and Cx. Unexpectedly, aedine species utilizing open 96 JounNlr- or rHr AMenrceNMoseurro CoNrnoL Assocrerrotr VoL. 15,No.2

ground pools were not found. In the study area, ACKNOWLEDGMENTS potential species are vexans (Meigen) and Aedes lineatopennis (Ludlow) (Bonne-Wepster We express our sincere appreciation to Basri 1954). Abundance of these floodwater species with Hasanuddin, Rector, and Rusli Ngatimin, Dean of drought-resistant eggs would fluctuate irregularly in Faculty of Public Health, Hasanuddin University, response to rainfall patterns. The absence of these and Yusuf Gayo, Director of East Region Imple- mentation, DGWRD, Ministry of Public Works, species in the limited samples does not exclude the and Head of LIPI (Indonesian Institute of Science) possibility of occasional population bursts under for their approval of this research. We also thank certain circumstances. Chairuddin Rasyad and Syafruddin, Hasanuddin Colonization of ground pools by forest species University, for their help in various ways. This was not conflrmed. In Sri Lanka, Amerasinghe and study was supported by Grant-in-Aid for Monbusho Ariyasena (1990) reported colonization of rainwater International Scientific Research Program (Field pools on deforested lands by shade-loving Aedes Research) (08041197). jamesi (Edwards). Possibilities of such unexpected events also should not be ruled out in Indonesia under drastic and rapid changes in environment. REF'ERENCES CITED In view of poor housing conditions of settlers, Abisudjak, B. and D. Kotanegara. 1989. Transmigration mosquito bites could be at a level where disease and vector-borne diseases in Indonesia, pp. 207-223. epidemics can occlu once pathogens are intro- 1n.' M. W. Service (ed.). Demography and vector-borne duced. For prevention of vector mosquito outbreaks diseases. CRC Press, Inc., Boca Raton, FL. on deforested lands, the Lst tactic to consider is to Amerasinghe, E P and T. G. Ariyasena. 1990. 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