.Inuriuil of the Ainvritan Mosquito Control A.s.soviati<m, 26(l):l-9. 2010 Copyright 2010 by The American Mosquito Control Association.

. Inc.

GEOGRAPHIC DISTRIBUTION OF AEDES EGYPTJ AND AEDES ALBOPICTVS COLLECTED FROM USED TIRES IN VIETNAM
YUKIKO HIGA.' NGUYEN THI YEN.- HITOSHI KAWADA.' TRAN HAI SON.' NGUYEN THUY AND MASAHIRO TAKAGl' ABSTRACT. The spatial distribution of Aedes aegypti and Aedes alhopicfus in environmental and geographical zones, e.g.. urban-rural, coastal-mounlainous, and north-south, was investigated throughout Vietnam. Immature stages were collected from used tire.s along roads. The efiects ol" regions, seasons, and the degree of urbanization on the density and the frequency were statistically analyzed, /itv/c.v tw^ypti predominated in ihe southern and central regions, while .Ae. alhopiclu.s predominated in the northern region, which may be related to climatic conditions {temperature and rainfall). Larval collection from used tires may be suitable lo assess rapidly the current distribution of dengue mosquitoes for estimating health risks and implementing vector control measures. KKY WORDS Aedes aegypti. Aedes albopictu.s. tires, Vietnam

atne et al. 2007. Delatte et al. 2008. Pages et al. 2009, Pistone et al. 2009. Yoosuf et al. 2009). Among insect vector-borne diseases, recent Since DF/DHF vaccine is unavailable for epidemics of the dengue (DF)/dengue hcmorrhagic fever (DHF) disease complex have h;id practical use, transmission can be prevented only great impact on Southeast Asian countries and by reducing human-vector contact. Thus, it is the Americas, where DF/DHF. as well as malaria, important to study the relationship hetween the is serious public health threat (Gubler 1997; distributions of Ae. aegypti and Ae. alhopicttts WHO 2009). The primary vector, Aeik-.s aegypti and environments in order to understand popu(L.), is distributed in tropical countries world- lation trends in changing environments and the wide. The secondary vector, Aede.s alhopicius ecological basis ofthe spatial distribution in order (Skuse), originated in tropical to temperate Asia to develop effective mosquito-control measures; it and has recently spread to the Americas, Europe, would be helpful to assess high-risk areas with and Africa by tire trades (Hawley 1988: Rodhain high vector densities. The difference in the infestation of mosquito vectors along urban-rural and Rosen 1997). gradient has been extensively studied owing to its The geographical distributions of Ae. aegypii ecological and epidemiolgica! importance (Chan and Ae. alhopivtu.s overlap in tropical Asia and etal. 1971a, 1971b; Tsuda et al. 2002; Braks et al. the Americas. However. Ae. aegypti is highly 2003; Rey et al. 2006; Tsuda et al. 2006; Cox et al. adapted to the domestic environment, and 2007; Bagny et al. 2009). Habitat segregation iherefore its abundance is positively correlated between coastal and mountainous environment with increasing urbanization; whereas the distri- has also been recognized: the abundance of Ae. bution of Ae. alhopicius is associated with aegypii and Ae. alhopictu.s was found to be high in vegetation throughout rural and urban areas, coastal areas and forested/mountainous areas, and its abundance is adversely affected by respectively (Hawley 1988, Ishak et al. 1997). This urbanization (Chan et al. 1971a, 1971b; Hawley was related to the introduction of Ae. aegypii 1988; Rndhain and Rosen 1997; Tsuda and from Africa to the new world by boats in lakagi 2001; Braks et al. 2003; Maeiel-de-Freitas seventeenth through nineteenth centuries (Gubler et al. 2006; Rey et al. 2006; Tsuda et al. 2006). 1997) and preference of Ae. alhopictu.\ for The mosquito vectors are affected ditTerently by environments with vegetation (Hawley 1988; environmental factors (Braks et al. 2003, Rey et Niebylski and Craig 1994; Takagi et al. 1995a, al. 2006. Tsuda et al. 2006). The recent involve- 1995b: Maciel-de-Freitas et al. 2006). ment of mosquito vectors in the pandemics of In the present study, we collected immature Chikungunya virus in many countries has increased the importance of examining the current stages of mosquitoes from used tires, which vector situation for potential outbreaks (Senevir- recently drew attention as an important breeding site for dengue vectors (Simard et al. 2005, Roiz et al. 2007.Yee 2008). The spatial distributions of ' Department of Vector Ecology & Environment. Ae. aegypti and Ac. alhopiciu.s in urban-rural, Institute of Tropical Medicine, Nagasaki University, Sakamoto 1-12-4. Nagasaki City. Nagasaki 852-8523. coastal-mountainous, and north-south, were investigated to understand the habitat segregation Japan. ' National Institute of Hygiene and Epidemiology. as well as the current distribution ofthe 2 species in Vietnam. Yersin 1, Hanoi, Vietnam.
I

INTRODUCTION

2 Table I. Period December 7-16. 2006 March 17-20, 2(X)7 May 15-20, 2007 July 1-12, 2007 January 7-16, 2008

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Regional location and season of larval collection from used tires in Vietnam. Region Central and a part of the north (far south of" Hanoi) North (far north of Hanoi) South and mountainous Central and a part of the north (far south of Hanoi) South and mountainous Season Dry Dry Wet Wet Dry

MATERIALS AND METHODS Larval collections Using the mosquito-collection method of Kawada et al. (2009), mosquito larvae were collected from used tires along the national road from the north end of Vietnam to the Mekong Delta. During the 5 larval collections, the region far north of Hanoi was visited once in the dry season; every other region was visited twice (Table 1). Whenever we encountered used tires, most of which were found around repair shops for vehicles, while driving along a systematically deterniitied route, the geographical position (with a global positioting system [GPS]), number of tires, presence of water, and presence of mosquito larvae in the tires were recorded. The degree of urbanization at each collection site was determined on the basis of the distribution of houses (continuously distributed or gaps with vegetated areas between houses), road conditions (asphaltsurfaced, paved road), and traffic lights, indicating frequent transportation in the area. Each area was classified as urban (hou.ses continuously distributed, asphalt-surfaced road, and traffic light present), transition (usually a little gaps with vegetated sites between houses, paved road, no traffic light), or rural (gaps with vegetated sites between houses, unpaved road, and no traffic light). Larvae were collected from 527 sites throughout Vietnam (Fig. 1). Mosquito larvae were collected from tires (6-20 tires per site, depending on desiccation) by netting (5 times per tire). The collected larvae were placed in 1.5-ml plastic vials containing absolute ethanol solution and were taken to the laboratory for identification. All late instars (3rd and 4th) collected were carefully identified to species under a microscope, using identification keys of Stojanovich and Scott (1966) and Rattanarithikul et al. (2005a, 2005b). The number and species of mosquito larvae from each tire were recorded. Due to identification dilTiculty, the early instars and pupae were not included in our analyses. Statistical analysis The mosquito density was calculated as the number of larvae per tire. The frequency of tires containing Ac. acgypti, or Ac. alhopictus^ or both species, was calculated as the number of tires

positive for Ae. aegypti, or for Ae. Albopidus. or both divided by the number of tires positive for water. On the basis of latitude and elevation, which were good parameters for division of geographical zones and climates, the country was divided into 4 regions for subsequent analyses: the northern region, the central regioti. the mountainous regions., and the southern region. The effect of regions, seasons, and degree of urbanization on the density of Ae aegypti and Ae. alhopictus was analyzed by analysis of variance (ANOVA). The frequency of the presence of Ae. aegypti, or Ae. alhopiclus. or both species, according to regions, seasons, and the degree of urbanization, was tested as presence or

Khanh Hoa

Fig. I. Location of the mosquito collection from used tires in Vietnam.

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DISTRIBUTION OF DENGUE VECTORS IN VIETNAM

absence by logistic regression analysis. The JMP 8 software was used for all statistical tests and models (SAS 209).
RESULTS (icngraphical distribution of mosquito species

Used tires are extensively and commonly distributed throughout the country (Fig. 1). Of the lotiU of 24.8% (4.757/19,188) of all tires sampled, 51.9% (2.468) contained water. In total, ^4.5% (852) tires contained larval mosquitoes, of which 26.5% (653) had Ae. iic^ypii and/or Ae. alhopicius. In total, 8,771 Ae. acgypti and 5,916 Ac. cilhiipiciiis larvae were collected, which accounted for 54.5% of all late instars collected from used tires. Non-dengue vectors collected trom used tires included Cuk'.x quinc/ue/asciafus Say (11,356), Cule.x pallidothora.x Thcohal (327), C'ute.x tritiieniorhymhii.s Giles ( 158), Armigeres sp.. Anopheles sp., To.xor/iyiuhiii's sp.. and i'ranohicnia sp. In the northern part of Vietnam. Ae. alhopictus was dominant, and this dominance gradually reduced toward the south (Fig. 2). Aedcs aegypti was dominant in the southern area, whereas in the coastal areas far south of Khanh Hoa province, most of the larvae collected were those o\' Ac. acgypfi. However, in the mountainous areas with forest vegetation, the proportion of Ae. albopiciiis was higher, indicating that each species is affected ditlerently between the northsouth and coastal-mountainous areas. Aedes iilhopUtus individuals were collected from used tires in Ho Chi Minh City and Vinh Long. Soc Trang. and Ca Mau provinces in the southern Vietnam.
FfTect of the regions, seasons, and urbanization on mosquito density

i.e., high density in urban and transition areas. In mountainous areas, the density of Ae. alhopictus was high in rural as well as urban areas (Fig. 3). The eiects of the region X season, region X urbanization, and region X season x urbanization interactions were statistically significant (P < 0.0001, P - 0.0006, and P - 0.0049, respectively), indicating that the seasons and the degree of urbanization affected the density difTerently. The analyses revealed that the effect of region, season, and urbanization was greater on the density of Ae. albopictus than that of Ae. aegypti. The densities of Ac. aegypti and Ae. albopietus according to the regions, seasons, and urbanization (Fig. 3) were negatively eorrelated, suggesting adverse distributions of dengue vectors in Vietnam (Spearman rank order test: p = -0.4235, P = 0.0392).
Effect of regions, seasoas, and urbanization on tbe frequency of occurrence

The density of Ae. aegypti was significantly higher in the southern region and lower in the norlhcrn region, thus exhibiting a strong elTect of the geographical regions on the density (P < O.OOI) (Fig. 3 and Table 2). Moreover. Ac. aegypti predominated over Ae. albopictu.s throughout urban-rural areas in the southern region (Fig. 3). Although the density of Ae. acgypti tended to be high in urban and transition areas, the effects of region and urbanization interactions were statistically significant (P = 0.0197), indicating that the effect of the degree of urbanization on density was not the same among the regions. For Ae. albopietus, the density was high in the northern region and low in the DISCUSSION southern region. Aedes alhopictus was likely to predominate over Ac. aegypii throughout urbanThe present study clearly showed the difference Miral areas in the northern region (Fig. 3); in the spatial distributions between Ac. aegypti however, urbanization strongly alTected density and Ac. albopicius in the north-south and coastalwhen entire regions were considered (P = 0.0157) mountainous areas; the former seemed to have

As shown in Figure 4 and Table 3. Ae. aegypti was rare in the northern region, especially during the dry season. Its frequency of occurrence gradually increased from the northem to the southern regions. The effects of the regions, urbanization, and region x season X urbanization interaction on the freqtiency of occurrence of only Ae. acgvpti were statistically significant [P < 0.0001, P - 0.0112, and /'-0.0444. respectively), indicating that the frequency varied greatly according to the regions and the degree of urbanization. In contrast to the case of Ae. aegypii., Ac. albopictus was frequent in the northern region throughout urban-rural areas, especially in the wet season, and its frequency decreased dramatically in the central and southern regions (Fig. 4). The effects of seasons and urbanization on the frequency of occurrence of this species were not statistically significant. However, significant effects on the frequency were indicated by the region X season interaction (P = 0.0008). The frequency of co-occurrence of both species was high in the central and mountainous regions (Fig. 4). and the elTect of the region X urbanization interaction on the frequency was significant, indicating that the degree of urbanization differently aTected the frequency (P ^ 0.0051). The frequencies of occurrence of both species according to the regions, seasons, and urbanization (Fig. 4) were negatively correlated (Spearman rank order test: p = -0.6111, P = 0.0015).

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Northern region

Hanoi

( J

Aedes aegypti Aedes alhopictus

Central region

Mountainous region Khanh Hoa

Southern region HoChiMinhCity Vinh Long Soc Trang

the most significant etTect on the distribution of the dengue vectors. However, the effect of urbanization on the spatial distribution was rather unclear and not consistent throughout the regions.

In general, Ae. aegypti moves short distances, prefers dark places, is anthropophilic, cndophagous. and endophilic, and favors urbanized environments {Christophers I960, Service 1993. Kuno 1997, Kawada et al. 2005b). On the other

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20 IK 16 14

Aedes aefivpti

12 10 8
6 4 2 0

20 18

Aedes alhopictus

+ 1

16 14 12 10

8
6 4 2 0

dry North Fig. 3. The number of Aedes aegypii and Aedes albopictus collected from tiscd tires in

hand, Ae. alhopictus travels longer distances than .*. ac^ypti. prefers vegetated environments . is an opportunistic feeder, and is exophagous and cxophilic (Hawley 1988., Niebylski and Craig 1994. Niebylski et al. 1994. Higa et al. 2001). These characteristics imply that the latter species lias a wider activity range and can adapt more easily to outdoor environments than the former species. The ditTerences between the adult niches of At: (iffypi and Ac. albopictus were related to difierent responses to environments; this partially explained the difference in their spatial distribution between the urban-rural and coastal-mountainous environments and seemed to contribute lo the coexistence within a region (Ishak et al. 1997. Maciel-de-Freitas et al. 2006. Tsuda et al. 2006). In Vietnam, the effect of the north-south geographical dilference on the spatial distributions of ^i'. acgypii and Ac. alhopictus indicated that the distribution of these mosquitoes was strongly affected by climatic factors e.g.. temperature, humidity, and precipitation. In the region where 1 species dominates over the other, climatic conditions would highly favor the former species.

For example. Ae. alhopictus is distributed in temperate regions as well as tropical region.s, and thus, it is more adaptive to cooler climates than Ae. aegypti; while the eggs and adults of Ae. aegypti are more resistant to desiccation than those of Ae. alhopictus. and thus. At: ucgypti is more adaptive to hot and dry environments thiin Ae, alhopicius (Hawley 1988. Sota and Mogi 1992. Sota 1993. Juliano et al. 2002). The meteorological data of the average temperature and precipitation in Vietnam over the last half century seemed appropriate for explaining this phenomenon (Weatherbase 2009). The average temperature was below 20 C from December to March in the northern region and In January in the mountainous region. On the other hand, the temperature was above 24 C throughout the year in the southern region. The average lowest temperature, which inlluenced the distribution o Ae, 7eg>7//(Christophers 1960). was different among the regions; it was less than 15 C from December to February in the northern region and December in the mountainous regions, while it was more than 15 C throughout the year in the central and southern regions. The monthly

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Table 2. Analysis of variance (ANOVA) table for the effects of region, season, and the degree of urbanization on density of Aedes aegypti and Aedes alhopictus collected from used tires in Vietniim. Species Ae. aegypti Source Model Region Season Urbanization Region X season Region X urbanization Season X urbanization Region X season x urbanization Error C. total Model Region Season Urbanization Region X season Region X urbanization Season X urbanization Region X season x urbanization Error C. total

dr
23 3

F value 11.9579 25.3033 2.1323 0.9860 1.9880 2.5169 0.9364 0.8284 7.0427 14.2588 3.7348 4.1618 11.6485 3.9928 0.4031 3.1115

1
2 3

6 2
6

<0.0001* <0.0001* 0.1444 0.3732 0.1137 0.0197* 0.3922 0.5478 <0.O0OI* <0.0001* 0.0534 0.0157* <O.OOOI* 0.0(X)6* 0.6683 0.0049*

2,439 2.462
23 3

Ae. albopictus

1 2 3 6 2
6

2,439 2,462

Statistically significant.

average precipitation was high i.e., >I80 mm, in the mountainous region. In other regions, the monthly average precipitation was 160 mm. not markedly different; however, the dry period, which was characterized by precipitation below 30 mm, was longer in the southern region (3 months long, from January to March) than in the northem region ( I month long, in January). These parameters were intermediate in the central region. The sequential change of responses to climatic conditions was possibly one of the

factors for the difference in infestation of Ae. aegypti and Ae. alhopictu.s along the north-sotith geographical divide in Vietnam. On the othei" hand, in the region where both Ac. aegypti and Ae. alhopictus breed, climates may be moderate for both species, and neither one would dominate the other. In such regions, habitat heterogeneity along the urban-rural gradient and interspecific interaction were considered to be more important than climate for spatial distribution. From previous studies, it is assumed that the former
aegypti only atbopictus only co-occurcnce

Fig. 4. Frequency distribution of the number of iarvae-positive tires in Vietnam. Each frequency was for .4edes aegypti, or Aedes albopictus, or both.

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Table 3. Logistic regression table for the effects of region, season, and the degree of urbanization on frequency of Aedes aegypti. Aedes alhopictus. and co-occurrence from used tires in Vietnam. Species Only Ac. aegypti Source Region Season Urbanization Region X season Region X urbanization Season x urbanization Region X season x urbanization Region Season Urbanization Region X season Region X urbanization Season x urbanization Region X season X urbanization Region Season Urbanization Region X season Region X urbanization Season X urbanization Region X season x urbanization
df

Chi square 68.3594 0.0005 8.9801 3.7457 6.5404 2.0122 12.9149 58.3860 0.1065 1.7815 16.8306 7.7256 2.7792 9.7126 60.7649 0.5983 1.3989 7.8274 18.5210 1.2738 7.2661 <0.0001* 0.9823 0.0112* 0.2903 0.3654 0.3656 0.0444' <O.OOOI* 0.7442 0.4103 0.0008* 0.2589 0.2492 0.1373 <0.000I* 0.4392 0.4969 0.0497* 0.051* 0.5289 0.2969

I
2 3 6 2 6

Only Ae. albopictus

3 1 2
3 6 2 6 3

Co-occurrence

1 2 3 6 2
6

Statistically significant.

Species may be abundant in urban areas., and the latter in the rural areas, according to the differences in the preferred sites of Ae. acgypti and Ac. alhopiciu.s for resting, feeding, oviposition, and breeding. Habitat segregation between the urban-rural areas would play an important role lor the coexistence of the 2 species within the region, even if the larvae have similar habitat requirements {Chan et al. 1971a, 1971b; Hawley 1988). In that case, the frequency of larval cooccurrence may be high at intermediate sites such as transition areas. However, although Ae. acgypti and Ac. albopictu.s coexisted in the central region of Vietnam, the high frequency of cooccurrence through urban to rural areas suggested that there was no obvious habitat segregation between the urban-rural areas in our study. This may be explained as follows. First, because we collected larvae along roads, the environments might not be too heterogeneous to exhibit a significant difference along the urban-rural gradient as compared to the environments inside villages, towns, and cities. Second, although our larval collections were limited to used tires, the higher density and frequency of ^i'. alhopictu.s in urban and transition areas than rural sites suggested an increase in the abundance of the species in domestic environments in Vietnam. This may suggest the abundance of dengue mosquitoes is changing to some extent in Vietnam. Braks et al. (2003) mentioned that the coexistence of the 2 species seems to be possible when the local environment favors a nonaquatic stage of I species and larval competition favors the other. Further study concerning both larvae

and adults is needed to examine habitat segregation of these 2 species along the urban-rural griidicnt in central Vietnam. The dilTerence in spatial distribution of Ae. aegypti and Ae. albopictus seems to be significant for dengue occurrence in Vietnam. Out of 25.269 234.920 annual dengue cases froml996 to 2000, 50.8-75.6% were reported from southern Vietnam (Ministry of Health 2001 ). incriminating Ae. aegypti as a major vector and a priority for vector control in Vietnam. Although Ae. aegypti was not collected from used tires in northern Vietnam, the species was observed in urbanized cities such as Hanoi city and Hai Phong Province of northern Vietnam (Vu et al. 1998, Kawada et al. 2005a). where dengue cases were still reported. Therefore, it should be important to monitor the infestation of Ae. aegypti and Ae. albopictus for potential of dengue outbreaks. Tires provide habitats to various containerinhabiting mosquitoes, including the dengue vectors (Roiz et al. 2007, Yee 2008). The aquatic environment for larvae basically originated from rainfall; therefore, water qualities contained in tires did not fluctuate throughout the study areas. indicating that tires would be undisturbed and would serve as a relatively stable environment for mosquito larvae without severe prdation pressure in Vietnam (Higa et al., unpublished data). The sequential difference in the spatial distribution of Ac. aegypti and Ac. albopidus indicates that larval collection from used tires i.s a reliable way to assess the distribution of dengue vectors. The newly established method in the present study makes it possible to rapidly investigate the

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current nationwide distributions of vectors, especially mosquitoes breeding in artificial containers, and apply the results to geographic information systems (GIS) (Kawada et al. 2009).

Hawley WA. 1988. The biology of Aedes albopictm.

Higa Y, Tsuda Y. Tuno N. Takagi M. 2001. Preliminary field experiments on exophagy of Aedes alhopictus (Diptera: Culicidae) in peridomestic habitat. Med Entomol Zool 52:105-116. Ishak H, Miyagi I, Toma T, Kamimura K. 1997. ACKNO^VLEDGME^^^S Breeding habitats of Aedes aegypii (L) and Aeiies alhopicius (Skuse) in villages of Barru, South We are grateful to the stafT of the Department Sulawesi, Indonesia. Southeast Asian J Trop Mvd of Medical Entomology and Animals, National Puhlie Health 28:844-850. Institute of Hygiene and Epidemiology (NIHE), Juliano SA. O'Mearii GF, Morrill JR. Cutwa MM. for their assistance during the study period. 2002. Desiccation and thermal tolerance of eggs and Further, we would also like to thank J. Sakemoto the coexistence of competing mosquitoes. Oecologia and T. Ueno, Department of Vector Ecology and 130:458^69. Environment, Institute of Tropical Medicine Kavt'ada H, Higa Y. Nguyen TY. Tran HS, Nguyen (NEKKEN), Nagasaki University, for their TH. Takagi M. 2009. Nationwide investigation of the pyrethroid susceptibility of mosquito larvae collected encouragement. This study was based on a from used tires in Vietnam. PLuS Negl Trop Dis scientific program "The Collaborative Study on 3:e39l. Emerging and Re-emerging Infectious Diseases in Kawada H, Nguyen TY, Nguyen TH. Truong MS. Vietnam: Enhancement of Research Capacity" of Nguyen VD, Takagi M. 2(K)5a. Field evaluation ol' Nagasaki University, Japan, in collaboration spatial rcpellency of meioriuthrin impregnated plastic with the National Institute of Hygiene and strips against mosquittws in Hai Phong city, Vietnam, Epidemiology, Vietnam, since 2005, and was Am J Trap Meil Hyg 73:350-353. funded by The Ministry of Education, Culture, Kawada H. Takemitra S, Arikawa K, Takagi M. 2005b. Sports. Science and Technology, Japan (MEXT) Comparative study on nocturnal behavior of Aedes and Core University Program of Japan Society aegvpti and Aedes alhopictus. J Med Entomol for the Promotion of Science (JSPS). 42:312 318. Kuno G. 1997. Factors inlluencing the transmission o" dengue viruses. In: Gubler DJ, Kuno G, eds. Dengue and dengue hemorrhagic fever. New York: CAB REFERENCES CITED International, p 61-88. Bagny L. Delattc H. Eiissa N, Quilici S, Fontenille D. Maciel-de-Freitas R. Neto RB. Gonalves JM, Codeo 2009. Ac'Je.'i (Diptera: Culicidae) vectors of arboviCT. Loiireno-De-Oliveira R. 2(X)6. Movement of ruses in Mayotte (Indian Ocean): distribution area dengue vectors between the human modified enviand larva! habitats. J Med Entomol 46:198-207. ronment and an urban forest in Rio de Janeiro. J Med Braks MH. Honorio NA. Lourenco-De-Oliveira R, Entomol 43:\\\2 1120. Juliano SA, Lounibos LP. 2003. Convergent habitat Ministry of Health. 2001. .4nalysis of vomnmnicahle segregation of Aedes aegypti and Aede.s tilhopicfu.-i di.sease data In Vietnam 996-2(H)0. Hanoi. 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Dengue and dengue hemorrhagic lever: its history and resurgence as a global public Rattanarithikul R, Harrison BA, Panlhusiri P. Colehealth problem. In: Gubler DJ, Kiino G, eds. Dengue mean RE. 2005b. Illustrated keys to the mosquitoes and dengue hemorrhagic fever. New York: CAB of Thailand I. Background; geographic distribution: Intemational, p 1-22. lists of genera, subgenera, and sf)ecies; and a key to

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