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(ᖪ 24: 293-303 (2004ٿέ៉ Formosan Entomol. 24: 293-303 (2004)

The Fauna (Culicidae: Diptera) in the Surface Water of Hapen Creek, Ilan,

Hwa-Jen Teng, Meng-Hau Hsue and Yen-Li Wu Medical Entomological Laboratory, Research and Development Center, Center for Disease Control, Department of Health, Taipei,

Taiwan 115, R.O.C. How-Jing Lee* Department of Entomology, National Taiwan University, Taipei, Taiwan 106, R.O.C.

ABSTRACT

A 1-year survey was conducted to understand the mosquito fauna and seasonal abundance of the dominant species in Hapen Creek in the Fushen Botanical Garden, northern Taiwan. Anopheles bengalensis Puri was found to be the most abundant species in terms of the total number collected and its wide distribution at all sampling sites. hayashii Yamada was next and was collected at three out of four sites. Five mosquito groups at Hapen Creek were recognized. Anopheles bengalensis and Cx. hayashii comprised one group, which was dominant in this survey. The average number of An. bengalensis larvae collected per dip increased from April to a peak in June, and then decreased sharply in July. Another peak was found in November and December. For C. hayashii, the first peak was found in October and another in July. The remaining four groups consisted of Cx. nigropunctatus with Cx. halifaxii; Cx. memeticus with An. gigas baileyi; An. lindesayi lindesayi; and Uranotaenia macferlanei. Anopheles lindesayi lindesayi larvae were collected only from February to June in this survey. Water temperature was significantly associated with the number of C. hayashii larvae collected, while total precipitation was associated with the numbers of An. lindesayi lindesayi and An. gigas baileyi collected. From the species correlation analysis of the community to mosquitoes, hemipteran bugs, copepods, and shells were significantly associated with four species of mosquitoes, while shrimp, naucorids, haliplids, dipteran larvae, and water striders were significantly correlated with three species of mosquitoes. Damselflies and stoneflies were positively correlated with two species of mosquitoes. These positive associations with mosquitoes may imply that the species are important natural enemies of mosquitoes or species which coexist with them.

Key words: Anopheles bengalensis, Culex hayashii, stream, seasonal fluctuation

*Correspondence address e-mail: [email protected] ! Mosquito Fauna of Hapen Creek 293 Introduction places and some microhabitats of mosquitoes became temporary pools or The mosquito fauna plays a major dried out. So, a variety of microhabitats role in the decomposition process of are found in this creek. The objectives of organic debris and serves as food for our study were to understand the mos- consumers of higher trophic levels in quito fauna and the seasonal abundance aquatic ecosystems. Predation by of the dominant species in Hapen Creek. mosquito larvae affects the population The environmental impacts of some dynamics and community structure of available factors such as water velocities, freshwater planktonic and bacterial natural enemies, and precipitation, on communities (Carpenter and Kitchell, this community were analyzed and are 1984; Carpenter et al., 1985; Elser and discussed. Carpenter, 1988; Cochran-Stafira and von Ende, 1998). Many mosquitoes breed in Materials and Methods flowing streams, which vary in water velocity, water depth, the coverage of Sampling Sites. The headwaters of plant species and floating plants, water- Hapen Creek are located in the Fushan bed types, and water quality (Rejman- Botanical Garden at 400~1400 m in kova et al., 1992, 1993, 1998; Almiron, elevation. The area of this garden is 1996). These factors determine the 1097.9 ha which it is divided into three species composition of the mosquito fauna areas: water source reserve, the botanical in each stream. Laird (1988) described garden, and the Hapen Nature Preserve. species in the same community and their Annually air temperatures range from 4 possible interactions in various aquatic to 28 oC with an average of 20 oC. habitats used by mosquitoes. However, Average annual precipitation is 2900 mm flowing-stream studies were limited to of which 70% occurs in the summer highly polluted and stable drainage months. The rainy season occurs in ditches. winter, while typhoons bring most of the Efficient natural enemies of mosquito precipitation in summer. Sampling sites larvae in the laboratory are larvivorous were in the area of the Hapen Nature fish (Nelson and Keenan, 1992), Preserve, in which no tourists are damselfly naiads (Miura and Takahashi, allowed to enter. Four sections of the 1988), hemipteran bugs (Diplonychus spp.) creek in three types of habitats (ponded, (Venkatesan et al., 1986), hydrometrids blocked, and flowing streams) were (Palmer et al., 1998), notonedtid bugs chosen according to the sampling results (Wattal et al., 1996), copepods (Nasci et of the first month of this survey. The al., 1987), and freshwater prawns (Collins, characteristics of these four sampling 1998). Other natural enemies have also sites are described in Table 1. been recognized, such as tadpoles, dra- Larval Sampling. A 14-cm-diameter gonfly naiads, Culex fuscanus Widde- dipper was used to collect larvae. The mann, and C. halifaxii Theobald (Laird, dipper was held at an angle of 60o and 1988). 0.6 m from the stream bank. Eighty The Hapen Creek of northern Taiwan samples were taken in each section of the is highly protected from anthropogenic stream for a total of 320 dips per month influences but is frequently affected by (from September 1997 to August 1998), if flooding and drought. During the drought conditions permitted. Occasionally, no months we studied (October-December in samples were taken because of drought at 1997, and April, July, and August in a sampling site. Larvae were identified 1998), water flowed underground in some on site to species under 400X microscopes

ௐαഇסᖪௐ˟˩αٿέ៉ 294 Table 1. Characteristics of the sampling sites in Hapen Creek, Ilan, Taiwan from September 1997 to August 1998 Habitat characteristics Ponded1 stream Blocked stream Flowing stream I Flowing stream II Water depth (cm) 7.5-99 8-37 9-40 6-35 Water velocity (cm/s) 0-9.5 0 0-22 0-21.4 Drought month 8 8 10-12, 4, 7-8 10-12, 4, 7-8 Overhead vegetation coverage Half open Dense vegetation Half open Dense vegetation Streambed Mud+sand Mud+sand Rocks Rocks 1Blocked stream was a side stream of a ponded stream; Flowing stream I was located 10~20 m uptream of Flowing stream II.

and released back at the sampling points temperature, water velocity, water depth, except during for the last 2 months. or monthly rainfall). The population Pupae were brought back to the labora- density of mosquitoes is hard to quantify tory and reared to adults for species with the number of natural enemies in identification. At the same time, speci- the dip data, because most natural mens other than mosquitoes were collec- enemies do not necessarily come to the ted to check the species association with water surface to breathe. Therefore, only mosquito larvae. In addition, water tem- the absence or presence of dip data were perature, water velocity, and water depth analyzed by Spearman’s rank correlation were measured at each site. Monthly analysis to show the association of these rainfall data was obtained from the species to mosquito larvae. Spearman’s Fushan Weather Station. coefficient of rank correlation applies to Statistical Analysis. Species diver- data in the form of a rank (in our case, sity and species packing can estimate the the absence or presence in the dip data). stability of a habitat (Southwood, 1978). The rank-abundance plot or some other Results indices can describe species diversity, while associations of species or utilization Species Composition of Mosquito of resources can be used to estimate Fauna. In Hapen Creek, Anopheles species packing. Diversity indices were bengalensis Puri was the most abundant calculated for each habitat type using the species in terms of the total number Shannon-Wiener information index: collected and its wide distribution at all

H’ = -∑(pi)log(pi); sampling sites (Fig. 1). Culex hayashii where pi is the proportion of the ith Yamada was the second most abundant species in the total sample (Shannon and was found in three out of four sites. 1948). Although An. lindesayi lindesayi Giles In this study, cluster analysis on the larvae were collected at all sampling basis of correlation coefficients was used sites, the size of the population was to group similar mosquito species, be- relatively small. Culex nigropunctatus cause no assumption is needed in this Edwards, Cx. halifaxii Theobald, Cx. analysis concerning the number of groups mimeticus Noe, Uranotaenia annandalei or the group structure (Johnson and Barraud, and An. gigas baileyi Edwards Wichern, 1988). In addition, correlation were found in small numbers at one or analysis was also used to check if the two sampling sites. Among the four number of larvae collected per dip was sampling sites, seven out of eight species associated with any of the physical existed in the blocked stream, however, environmental factors examined (water only two or three species were found in

Mosquito Fauna of Hapen Creek 295 1000280

Anopheles bengalensis



 Culex hayashii 240800 

Anopheles lindesayi

 Culex mimeticus



200600  Culex nigropunctatus

 Culex halifaxii

160400  Uranotaenia macferlanei



 Anopheles gigas baileyi

120200  



80 

Total no. of larvae collected  

  

40 

   

       0  Ponded stream Blocked stream Flowing stream I Flowing stream II Habitat

Fig. 1. Species composition of mosquito fauna in Hapen Creek Ilan, Taiwan.

the ponded stream, flowing stream I, and lensis larvae increased from April to a flowing stream II (Fig. 2). A high number peak in June, and then decreased sharply of mosquito larvae was collected in ha- in July (Fig. 4). Another peak was found bitats of the ponded stream and blocked in November and December. For C. stream, but only a small population hayashii, two peaks were found in existed in the flowing stream I and October and July. The results indicated flowing stream II. Values of the diversity bivotinism for An. bengalensis and Cx. index (H’) for mosquito larvae in the hayashii, although the November popu- blocked stream, flowing stream I, and II, lation of An. bengalensis was much and the ponded stream were 0.88, 0.87, smaller than that in June. Anopheles 0.69, and 0.39, respectively. lindesayi lindesayi larvae were only found Five groups of mosquito fauna in from February to June with small popu- Hapen Creek were recognized by cluster lations in this survey. From the environ- analysis on the basis of species corre- mental factor analysis, the population lation coefficients (Fig. 3). Culex hayashii dynamics of An. bengalensis, An. and An. bengalensis comprised one group, lindesayi lindesayi and Cx. hayashii were and they were the dominant species in independent of water velocity (r = -0.19, this survey. The remaining four groups 0.17, and 0.03; df = 34; p > 0.05) and consist of Cx. nigropunctatus with Cx. water depth (r = 0.13, 0.31, and -0.15; df halifaxii; Cx. mimeticus with An. gigas = 34; p > 0.05). The population of C. baileyi; An. lindesayi lindesayi; and U. hayashii was significantly affected by macferlanei. water temperature (r = 0.37; df = 34; p < Seasonal Abundance of Dominant 0.05) while An. bengalensis and An. Species. The population of An. benga- lindesayi lindesayi were independent of it

ௐαഇסᖪௐ˟˩αٿέ៉ 296 3.5

3.0 Ponded stream Blocked stream 2.5 Fowing stream I Flowing stream II 2.0

1.5 Log abundance 1.0

0.5

0.0 12345678 Species rank

Fig. 2. Species rank-abundance (or dominance-diversity curves) of mosquito fauna for four different habitats in Hapen Creek, Ilan, Taiwan.

Species

AnophelesAnopheles bengalensis bengalensis

CulexCulex hayashii hayashii

AnophelesAnopheles lindesayi lidesayi

CulexCulex mimeticus mim e tic u s

AnophelesAnopheles ggigasbaileyi ig a s b a ile y i

CulexCulex nigropunctatus nigropunctatus

CulexCulex halifaxii

UranotaeniaUranotaenia macferianei macferianei

0.55 0.60 0.65 0.70 0.75 0.80 0.85 0.90 0.95 1.00 1.05 Linkage Distance

Fig. 3. Tree diagram for mosquito fauna in Hapen Creek, Ilan, Taiwan, by cluster analysis on the basis of correlation coefficients with complete linkages. Species from the same branch of the tree diagram represent close lineages of species, and these serve as recognized groups of mosquito fauna.

Mosquito Fauna of Hapen Creek 297 Fig. 4. Monthly abundance of mosquito larvae with water temperature (A) and rainfall (B) in Hapen Creek, Ilan, Taiwan (n = 320)

ௐαഇסᖪௐ˟˩αٿέ៉ 298 Table 2. Association of mosquito larvae with aquatic in Hapen Creek, Ilan, Taiwan by Spearman’s rank correlation analysis (n = 2030) Species1 AB CH CM CHA AL AGB Hemiptera 0.292*** 0.273*** 0.104*** 0.037 0.135*** 0.043 Copepod 0.250*** 0.331*** -0.008 -0.007 0.187*** 0.087*** Shell 0.050* 0.151*** 0.110*** 0.136*** 0.027 -0.005 Shrimp 0.202*** 0.096*** -0.016 -0.013 0.095*** 0.036 Naucoridae 0.062*** 0.048* -0.011 -0.009 0.027 -0.015 Haliplidae 0.068*** 0.050* -0.004 -0.003 -0.019 0.091*** Diptera 0.109*** 0.049* 0.117*** -0.003 0.006 -0.005 Strider 0.060*** 0.004 0.047* -0.008 0.066*** -0.012 Damselfly 0.057* 0.101*** -0.004 -0.003 0.035 -0.005 Stonefly 0.080*** 0.0003 -0.004 -0.003 0.080*** -0.005 Caddisfly 0.050* -0.015 -0.003 -0.002 -0.014 -0.004 Fish -0.020 -0.018 -0.003 -0.003 0.079*** 0.004 Mayfly 0.043 0.009 0.059*** -0.006 0.018 0.041 Dragonfly -0.012 0.019 -0.003 -0.002 -0.014 -0.004 Water mite -0.022 -0.011 -0.002 -0.002 -0.010 -0.003 Tadpole 0.001 0.002 -0.004 -0.003 0.007 -0.005 Neuroptera -0.009 -0.005 -0.001 -0.001 -0.004 -0.001 * p < 0.05; *** p < 0.01. 1AB, Anopheles bengalensis; CH, Culex hayashii; CM, Culux memeticus; CHA, Culex halifaxii; AL, Anopheles lindesayi lindesayi, AGB: Anopheles gigas baileyi.

(r = 0.22, and 0.02; df = 34; p > 0.05). Total monthly rainfall positively affected Discussion the numbers of An. lindesayi lindesayi (r = 0.66; df = 11; p < 0.05) and An. gagas In this survey, seven mosquito baileyi (r = 0.75; df = 11; p < 0.01). species were found in the blocked stream In total, 2639 aquatic organisms while only three species were found at were collected. Among them, hemipteran most of the other locations in Hapen bugs, copepods, and shells were signi- Creek. This indicates that blocked por- ficantly associated with four of six species tions of the stream serve as reservoirs for of mosquitoes while shrimp, naucorids, mosquito species, while both blocked and haliplids, dipteran larvae, and water ponded portions of the stream support striders were found to be significantly high densities of mosquito larvae. A correlated with three species of mosqui- unique characteristic of Hapen Creek is toes (Table 2). Damselflies and stoneflies that its microhabitats are unstable be- were positively correlated with two cause flood and drought conditions may species of mosquitoes, while caddisfly occur at any time of the year. In our larvae, mayflies, and fish were signi- survey period, drought was found in ficantly correlated with only one species. October-December, April, and July- In contrast, dragonflies, water mites, August. Five recognized groups of mos- tadpoles, and Neuroptera showed no quitoes in Hapen Creek represent differ- significant association with the presence ent adaptabilities to various microhabi- of mosquito larvae. tats. The dominant group, An. bengalensis

Mosquito Fauna of Hapen Creek 299 and Cx. hayashii, were capable of may be important benthic feeders. Data adapting to various microhabitats and presented here are descriptive only; they survived in both flowing and stagnant do not indicate which group caused water (Tanaka et al., 1979). the greatest impact on mosquito popu- Seasonal fluctuations of mosquito lations. More research is needed to populations in Hapen Creek differed for understand the interactions within this the different species studied. The number food web. of An. bengalensis was found to be Many general predators showed posi- highest in June, while the peak for Cx. tive associations with mosquito larvae in hayashii was in October and that for An. our study. Because the “natural enemies” lindesayi lindesayi occurred between hypothesis suggests that predators are March and May. These differences may more effective in complex environments be due to the nature of these species (Sheehan, 1986), these predators might adapting to various habitats as well to not have sufficient time to build up physical environment factors. Our preli- relatively stable populations in this unst- minary results showed that water tem- able creek. Overall, such abiotic factors perature positively affected numbers of as drought and flash floods may regulate Cx. hayashi, while rainfall affected populations much of the time in Hapen populations of An. lindesayi lindesayi and Creek, while biotic interactions such as An. gigas baileyi. The positive relation competition and predation may come into with monthly rainfall implies that these play as the stream surface volume two species are highly oxygen-demanding shrinks during periods of drying out. species. This factor might render these From a species analysis of the mosquito species inferior to An. bengalensis. It is community, Hapen Creek was shown to interesting that the lowest water tem- have less-complex trophic levels and rela- perature (16.75 ℃ ) was recorded in tively low species diversity (H’), probably September 1997. A possible explanation because this creek provides many was the lag effect of heavy rainfall in the unpredictable and unstable microhabitats previous month and weather conditions (Polis, 1998). on the collecting date. In our survey, the damselfly was Acknowledgments significantly associated with two mos- quito species while the dragonfly was This study was supported by a re- independent of all of them. This implies search grant (NSC86-2621-B002-015A07) that the damselfly tends to prey closer to from the National Science Council, ROC. the surface of the water where most of We thank the personnel of the Fushan the mosquito larvae aggregate (Laird, Branch, Taiwan Forestry Research 1956). Three species of dipteran larvae Institute for their kind assistance during were also found to be positively asso- the survey period. ciated with mosquito larvae in Hapen Creek. Among them, Dixid larvae, which References live on the water surface, might repre- sent another competitor with mosquito Almiron, W. R., and M. E. Brewer. 1996. larvae. Dragonflies, mayflies, mites, Classification of immature stage tadpoles, and neuropterans that do not habitats of Culicidae (Diptera) collec- share the same niche with mosquito ted in Cordoba, Argentina. Mem. Inst. larvae were temporary members of this Oswaldo Cruz 91: 1-9. community. However, the role of dragon- Carpenter, S. R., and J. F. Kitchell. 1984. and tadpoles is not clear since they Plankton community structure and

ௐαഇסᖪௐ˟˩αٿέ៉ 300 limnetic primary production. Am. Corbet. 1998. Hydrometra stagnorum Nat. 124: 159-172. (L.) (Hemiptera, Hydrometridae) fee- Carpenter, S. R., J. F. Kitchell, and J. R. ding on mosquitoes. Entomol. Mon. Hodgson. 1985. Cascading trophic Mag. 134: 65-68. interactions and lake productivity. Polis, G. A. 1998. Stability is woven by BioScience 35: 634-639. complex web. Nature 395: 744-745. Cochran-Stafira, D. L., and C. N. von Rejmankova, E., K. O. Pope, D. R. Ende. 1998. Integrating bacteria into Roberts, M. G. Lege, R. Andre, J. food webs: studies with Sarracenia Greico, and Y. Alonzo. 1998. Charac- purpurea inquilines. Ecology 79: 880- terization and detection of Anopheles 898. vestitipennis and Anopheles puncti- Collins, A. P. 1998. Laboratory evaluation macula (Diptera: Culicidae) larval of the freshwater prawn, Macro- habitats in Belize with field survey brachium borellii, as a predator of and SPOT satellite imagery. J. Vect. mosquito larvae. Aquat. Sci. 60: 22- Ecol. 23: 74-88. 27. Rejmankova, E., D. R. Roberts, R. E. Elser, J. J., and S. R. Carpenter. 1988. Harbach, J. Pecor, E. L. Peyton, S. Predation-driven dynamics of zoo- Manguin, R. Krieg, J. Polanco, and L. plankton and phytoplankton in a Legters. 1993. Environmental and whole-lake experiment. Oecologia 76: regional determinants of Anopheles 148-154. (Diptera: Culicidae) larval distri- Johnson, R. A., and D. W. Wichern. 1988. bution in Belize, Central America. Applied multivariate statistical ana- Environ. Entomol. 22: 978-992. lysis. 2nd ed., Simon & Schuster, Rejmankova, E., H. M. Savage, M. H. Englewood Cliffs, NJ, 607 pp. Rodriguez, D. R. Roberts, and M. Laird, M. 1956. Studies of mosquitoes and Rejmanek. 1992. Aquatic vegetation freshwater ecology in the South as a basis for classification of Pacific. Bull. Roy. Soc. No. 6. 213 pp. Anopheles albimanus Weideman (Dip- Laird, M. 1988. The natural history of tera: Culicidae) larval habitats. En- larval mosquito habitats. Academic viron. Entomol. 21: 598-603. Press, London, 555 pp. Shannon, D. E. 1948. A mathematical Miura, T., and R. M. Takahashi. 1988. A theory of communication. Bell Syst. laboratory study of predation by Tech. J. 27: 379-423, 563-656. damselfly nymphs, Enallagma civile, Sheehan, W. 1986. Response by specialist upon mosquito larvae, Culex tarsalis. and generalist natural enemies to J. Am. Mosq. Contr. Assoc. 4: 129- agroecosystem diversification: a selec- 131. tive review. Environ. Entomol. 15: Nasci, R. S., S. G. Hare, and M. Vecchione. 456-461. 1987. Habitat associations of mos- Southwood, T. R. E. 1978. Ecological quito and copepod species. J. Am. methods: with particular reference to Mosq. Contr. Assoc. 3: 593-600. the study of insect populations. Chap- Nelson, S. M., and L. C. Keenan. 1992. man and Hall, New York, 524 pp. Use of an indigenous fish species, Tanaka, K., K. Mizusawa, and E. S. Fundulus zebrinus, in a mosquito Saugstad. 1979. A revision of the abatement program: a field compa- adult and larval mosquitoes of rison with the mosquito fish, Gambu- (including the Ryukyu Archipelago sia affinis. J. Am. Mosq. Contr. and the Ogasawara Islands) and Assoc. 8: 301-304. Korea (Diptera: Culicidae). Contrib. Palmer, J. L., M. J. Donnelly, and S. A. Am. Entomol. Inst. 16: 57-59.

Mosquito Fauna of Hapen Creek 301 Venkatesan, P., G. Cornelissen, and F. predatory potential of notonectid bug, Halberg. 1986. Modelling prey-predator Enithares indica (Fabr) against mos- cycles using hemipteran predators of quito larvae. SE Asian J. Trop. Med. mosquito larvae for reducing world- Pub. Health 27: 633-636. wide mosquito-borne disease incidence. Chronobiologia 13: 351-354. Received: Oct. 5, 2004 Wattal, S., T. Adak, R. C. Dhiman, and V. P. Accepted: Nov. 30, 2004 Sharma. 1996. The biology and

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Mosquito Fauna of Hapen Creek 303