Larval Mosquitoes in Abandoned Tire Pile Sites from West Virginia

Journal of the American Mosquito Control Association, 2O(l):12-17,2OO4 Copyright @ 2004 by the American Mosquito Control Association, Inc.

LARVAL MOSQUITOES IN ABANDONED TIRE PILE SITES FROM WEST VIRGINIA

JAMES E. JOY

Department of Biological Sciences, Marshall University, Huntington, WV 25755

ABSTRACT. Larvae of l3 mosquito species were collected from abandoned tire piles at peridomestic and nonperidomestic sites in 3 south-central West Virginia counties from May through September 2OO2. Ochlerotatus triseriatus was the most frequently collected species from May through August, whereas Aedes albopictus and Ochlerotatus japonicus were more prevalent in September. Prevalence of Oc. triseriatus and Culex restuans declined throughout the study period. Conversely, prevalences ofAe. alhopictus, Oc. japonicus, Culex territans, and Toxorhynchites rutilus increased during the same period. Ochlerotatus atropalpus was significantly more likely to be encountered at nonperidomestic sites. None of the other species exhibited a significant predisposition for either peridomestic or nonperidomestic sites.

KEY WORDS Arboviruses, Ochlerotatus triseriatus, Ochlerotatus japonicus, Aedes albopictus, invasive species

INTRODUCTION on native forms, the confluence of Ae. albopictus, Oc. japonicus, and Oc. triseriatus in West Virginia Nasci et al. (2000) acknowledged that the influ- at this time highlights the desirability of continued ence of habitat on the transmission cycle of the La surveillance activity on these 3 species. Crosse encephalitis virus (LAC) was not fully un- Nicholas County was once considered the en- derstood. Work by those investigators in Nicholas demic focus for LAC, but Fayette and Raleigh County, West Virginia, in 1996 indicated that La counties, located immediately to the south of Nich- Crosse encephalitis cases and the presence of LAC olas County, are now experiencing comparable in Ochlerotatus triseriatus (Say) were associated numbers of cases annually (West Virginia Depart- with a variety of habitat types, leading to the con- ment of Health and Human Resources, unpublished clusion that the dynamics of enzootic LAC trans- data 2OO2). Joy et al. (2003) reported on monthly mission by this vector species were very complex. surveillance results of tire-breeding species in Ultimately, those investigators found no clear set of Nicholas County based on collections made in habitat parameters that could be used as predictors 2001, but as a result of the more recent LAC re- for the presence or absence of LAC in a particular porting data in Fayette and Raleigh counties, the area of Nicholas County. focus of the present surveillance work has been ex- Two Asian mosquito species have been intro- tended geographically to those latter counties. duced into West Virginia since that 1996 study by Nasci et al. (2000): Aedes albopiaus (Skuse) in 1998, and Ochlerotatus japonicus (Theobald) in MATERIALS AND METHODS 2O02. Introductions of these exotic species may have made the dynamics of LAC transmission even Study area: Nicholas, Fayette, and Raleigh more complex for 2 reasons. First, the Asian spe- counties, with a combined population of 153,000, cies may compete wrtl:. Oc. triseriatus for space and are located in south-central West Virginia approx- fbod resources, thus altering-i11 sn[nsr67n ways- imately between latitudes 37'30' and 38'30'N and population structure of the native LAC vector. The longitudes 80'30' and 8l'30'W. introduction of Oc. japonicas is too recent to have Site characteriz.ation and collection procedure: produced any relevant data on this subject, but Ae. A total of 112 abandoned tire pile sites were iden- albopictus is thought by some workers (Ho et al. tified in the 3-county target area from May through 1989, Livdahl and Willey 1991, Edgerly et al. September 2OO2. Each of those sites was placed 1993) to be capable of competing effectively with into I of 2 categories (peridomestic or nonperi- Oc. triseriatus and perhaps even displacing over the domestic) based on the proximity of the tire habitat long-term. Second, with the isolation of LAC from to human hosts. Fifty-seven peridomestic sites had naturally infected Ae. albopictus in Tennessee, Ger- tires located in areas where humans were readily hardt et al. (2001) established thar the Asian tiger available to mosquitoes. These sites were business- mosquito may serve as an accessory LAC vector. es that offered automobile tire replacement services The possibility that Oc. japonicu.s might become and were located within 100 m of homes, motor- involved in LAC transmission as well cannot be cycle or go-cart race tracks, and convenience ruled out. stores. Additionally, 55 nonperidomestic sites (i.e., So, from the standpoint of both a public health sites >100 m distant from areas of human activity) perspective and an investigation of competitive were examined. These sites were generally along pressures that introduced species may bring to bear rural roads where illegal dumping occurred. Tire- LARVAL MosQUIToEs Fnou Wrsr VIRGINIA 13

Table 1. Frequencies (percent of visits positive) of larval mosquito species colonizing waste tire piles in south- centraf West Viiginia (e.g., larval Aedes aTbopictls were collected from 123, ot36.6Vo, of the 336 total site visits). Number of visits is given in parentheses.

NonPeri- Total Peridomestic domestic Species (336) (167) (l6e) X'(l df)

Aedes aLbopictzs (Skuse) 36.6 32.9 40.2 r.628 Anophe le s barb eri (Coquillett) 1.2 0 L.+ Ano phe le s puncti pe nni s (S ay) 3.9 2.4 5.3 r.231 Anophele s quadrimaculatus Say 1.5 1.2 1.8 Culex pipiens Linnaeus 6.O 6.6 5-3 0.163 Cuiex restuans Theobald +J.Z 46.1 40.2 0.953 Culex territans Walker 27.1 30.5 z-). I 1.675 Ochle rotatus at ropalpus (Coquillett) 17.0 71.4 z3- | 6-056r Ochlerotatus canadensis (Theobald) 5.4 4.8 5.9 o.o47 Ochle rotatus j aponicus (Theobald) 31.5 -J-). -t 27.8 1.864 Ochlerotatus trise riatus (SaY) 62.5 57.5 67.5 3.150 O nhopodomyia si gnife ra (Coquillett) z-+ 1.8 3-0 Toxo rhynchites rutilus septentrionalis (Coquillett) 19.6 19.8 19.5 o.007 'P < 0.05. inhabiting mosquitoes at nonperidomestic sites did to 112 tire dump sites in Fayette, Nicholas, and not have ready access to humans as a blood-meal Raleigh counties of West Virginia from May source. Many sites were visited on more than I through September 2OO2 (Table l). Overall fre- occasion, but no site was visited more than once in quency of occurrence was high (>5OVo of the site the same month. visits) for Oc. triseriatus; moderate (>2O-5OVo) for ja- Tires were sampled by repeatedly sweeping a Culex restuans (Theobald), Ae. albopictus, Oc. (>5- handheld strainer with a mesh size of approximate- ponicus, and Culex territans (Walker); low ly 1.0 mm through the water and leafy substrate. 2OVo) for Toxorhynchites rutilus (Coqtillet)' Och- Larvae collected in the strainer were removed with lerotatus atropalpus (Coquillet), Culex pipiens L-, jeweler's forceps and placed in 30-ml bottles, ap- and Ochlerotatus canadensis (Theobald); and rare propriately labeled with a site number and date of (<57o) for Anopheles punctipennrs (say), Ortho- collection, containing 957o ethanoL Larvae were podomy ia si gnife ra (Coquillet), Anophele s quadri- identified with the aid of a Zeiss stereomicroscope maculatus Say, and Anopheles barberi (Coquillet). at 60X. If identification was questionable, larvae were dehydrated to 99Eo ethanol, cleared in xylene, Larval presence bY site category and mounted in Permount@ (Fisher Scientiflc, Pitts- burgh, PA) for examination under a compound mi- Larval colonization frequency patterns by site croscope at greater magnification. Keys by Means category varied according to species, with 5 species (1979), Darsie and Ward (1981), and Darsie (1986) more often found at peridomestic sites, and 8 at were consulted for larval identifications. In addi- nonperidomestic sites. However, no species was tion, Oc. japonicus was identified from the key significantly more likely to be encountered at per- made available by Rutgers University (2003). idomestic sites, and only a single species, Oc. atro- Data analysis.' A chi-square 2 x 2 table was palpus, was significantly more likely to be ob- used to test for statistical significance for larval served at nonperidomestic tire habitats (Table 1). species at peridomestic vs. nonperidomestic sites, whereas the chi-square test of equality of propor- presence by month of collection tions (SAS Institute 1989) was employed to eval- Larval uate temporal distribution for each of the 7 most Ochlerotatus triseriatus was the most frequently commonly encountered species. Levels of proba- collected species from May through August (Table bility are given in the narrative or tables as appro- 2). Both Ae. albopict r.t and Oc. japonicus were priate. more frequently collected than Oc. triseriatus in September, but only the higher prevalence of 65-7Vo RESULTS for Ae. albopictus (vs. 4O.OVofor Oc. triseriatus) was significant (X' : 8.284; I df; P < 0.05). General findings Prevalence (i.e., percent of visits positive in Ta- Thirteen species of mosquito larvae were iden- ble 2) of 2 species, Oc. triseriatu,t and C.r. restuans, tified in 336 visits (167 and 169 visits to peri- gradually declined throughout the study period, domestic and nonperidomestic sites, respectively) whereas the reverse was true for Ae. albopictus, Oc. l4 JounNer- oF THE AMERrcal Mosquno CoNrnoL Assocraltorl VoL. 20, No. I

Table 2- Larval distribution, by month of collection, for the 7 species in tire pile habitats where valid chr-square tests can be made. The negative (Neg.) and positive (Pos.) visiis for each species total to the number of visits (shown in parentheses) for each month (total collections, all months : 336). The null hypothesis is that the proportion positives of is the same for each month for any given species. The null hypotheiis is rejected for every "Wrt* "-..pt Orhl"r"r*", "r,

Oc. triseridtus Cx. restuans Ae. albopictus

Neg. Neg. Neg Pos. May 9 49 z) 35 50 8 (58) 15.5 84.5 39.1 60.3 86.2 13.8 7.4'7 4.49 3.O2 4.76 8.25 June 26 46 30 42 63 9 (72) 36.1 63.9 4r.7 58.3 87.5 12.5 0.04 0.o2 2.92 3.84 6.60 11.43 July ZJ 43 33 JJ 40 26 (66) 34.8 65.2 s0.0 50.0 60.6 39.4 o.t2 o.o7 o.54 o.72 0.08 0.14 Aug. 26 44 54 16 36 34 (70) 5t-l 62.9 77.1 22.9 51.4 48.6 0.o0 0.00 5.O7 6.69 1.58 2.74 11 Sept. 28 51 t9 24 46 (70) 60.0 40.0 72.9 27.1 34.3 65.7 9.45 5.6'7 3.16 4.16 9.36 16.20 (336) 126 2lo 191 145 2t3 I z-) : xt 27.34;df 4; 34.08;df : 4; 61.13;dt : 4; P < 0.0001 P < 0.0001 P < 0.0001 I oc', Ochlerotatusi Cx.' Culex; Ae., Aedes; Tx., Toxorhynchit€r. Numbers in each of the 35 cells (as depicted in the I st cell) represent (from top to bottom): number of visits negative or positive for mosquito lmae, percent of visits negative or positive for lffiae, and negative or positive cell contribution to tlle total chi-square value. Nbte: 7 mosquito species x 5 monthty catelories : 35 cells, with each cell having a negative and positive component. japonicus, prevalence Cx. territans, and Tx. rutilus. The possibility that residenr populations of Oc. of Oc. atropalpus was relatively consistent over the triseriatus could be displaced by the invasive Ae. colfection period. Collections of Cx. pipiens, Oc. albopictus has been suggested by several investi- canadensis, and Or. signffiera, as well as the 3 gators (Ho et al. 1989, Livdahl and Willey 1991, anopheline species, were too few to determine Edgerly et al. 1993), although Livdahl and Willey monthly distributions. (1991) cautioned that the predatory Tx. rutilus could influence the outcome of any Ae. albopictus DISCUSSION invasion. Moore (1999) also questioned the ability of the Asian tiger mosquito to compete with resi- The 13 species of mosquitoes using abandoned dent species in natural conditions, citing the relative tires as larval habitats in 3 counties of south-central scarcity of Ae. albopictus in the northeastern United West Virginia compares favorably with the 12 spe- States. Another impediment to the displacement of cies reported from tires in West Virginia (Joy et al. Oc. triseriatus by Ae. albopictus is that the former 2003), the I 1 species reported from containers species exhibits a superior cold hardiness over the (mostly tires) in North Carolina (Szumlas et al. latter (Hanson and Craig 1995). Evidence for this 1996), and the 14 species collected from tires in cold tolerance is seen in the very high prevalence Michigan (Wilmot et al. 1992) and Illinois (Novak of Oc. triseriatus in April and May (Joy et al. 1995). Ochlerotatus japonicus was lst reported in 2OO3), a phenomenon supported by the present West Virginia early in 2OO2 (James Amrine, per- study where the chi-square cell contribution for lar- sonal communication), and this introduced species val presence of Oc. triseriatus in May alone made was well represented in our 2002 summer collec- up 44Vo of the total chi-square value (Table 2). (Table tions l). Conversely, larval collections of Ae. albopictus Ochlerotatu.s triseriatus was the dominant spe- were highest in September, with the chi-square cell cies encountered in all months except September, contribution for that I month contributing approx- when it was supplanted by both Ae. albopictus and imately 427o of the total chi-square value (Table 2). Oc. japonicus. However, only the higher prevalence These findings :re in agreement with those of observed for Ae. albopictus vis-i-vis Oc. triseriatus Lampman et aI. (1997), who noted that Ae. albo- in September was significant. This was in contrast pictus was a major late-season species. Although to the results of Joy et al. (2003), who noted that examination of our data ('Iable 2) indicates that Ae. prevalence of Ae. albopictus never reached levels albopictus may be present in higher frequencies (in attained by Oc. tiseriatus in later months of 2001. northeastern states such as West Virginia) than pre- MARCH 2004 LARVAL MosQutroEs FROMWEsr VInctNta

Table 2. Extended.

Oc. japonicus Cx. territans Tx' rutilus Oc' atropalpus Pos' Neg. Pos. Neg. Pos. Neg' Pos' Neg'

580508580526 10'3 100 0 86.2 13.8 100 0 89'7 8.43 18.30 1.4r 3.78 2.79 ll.4 0'31 l'so 53 19 55 1,7 67 5 56 16 22'2 73.6 26.4 76.4 23.6 93.1 6.9 77'8 | '17 0.28 0.61 0.12 0.32 r.45 5.91 0'24 3729442255115214 21'2 56.1 43.g 66.7 33.3 83.3 16.7 78'8 1.48 3.21 0.35 0.95 0-07 0.30 0'14 0'70 41 29 52 18 44 26 57 13 58.6 41.4 74.3 25.7 62.9 37.1 8l'5 l8'3 LOO 2.17 0.02 0.05 2.67 10.91 0'o2 0'l I 412944264624628 65.'7 34.3 88.6 rr'4 58.6 41.4 62.9 37.r '7.64 1.00 2.r'7 0.97 2.62 1.87 0.26 1'27 230 106 245 gl 270 66 279 s7 = 38.64;df = 4: 10.59;df : 4; 44.99: df : 4; 5'71; df 4; P<0.00Or P=O.O3|6 P<0'0001 P=0'2216

viously thought, this species does not overlap tem- States. The peak in recorded La Crosse encephalitis porally with the resident Oc. triseriatus. cases (1995-2001) for West Virginia occurs in Au- The monthly occulrence pattern for Oc. iaponi- gust (West Virginia Department of Health and Hu- crs was more closely related to that of Ae. albo- man Services, unpublished data); thus, it could be pictus than Oc. triseriatus (Table 2), but because postulated that the temporal extension of Ae. al' the bionomics of Oc. japonicus in the USA are bopictus evident in this study could result in the largely unknown (Sardelis and Turell 2001), and increased incidence and distribution of La Crosse this species is such a recent introduction to West encephalitis cases as well. Such a proposition is Virginia, evaluation of its monthly distribution is strengthened by the findings of Grimstad et al. premature. lf Oc. iaponicas becomes well estab- (1989), who, in working on LAC-competent vec- lished in West Virginia, it could be a significant tors under laboratory conditions, concluded that in- ". competitor with Oc. triseriatus because it has a Pa- troduced Ae. albopictus populations: . . must be learctic distribution (Peyton et aI. 1999) and has considered potentially able to transmit LACV as (Ka- been reported as numerous in the early spring efficiently as fresh Ae. triseriatus field popula- of Oc. mimura 1968). The public health importance tions." detail, japonicus in the USA has not been studied in A monthly decline in larval populations of Oc. japonicus is an efficient laboratory vector bttt Oc. triseriatus in West Virginia has been observed by West Nile virus (WN), and may serve as an ideal of Joy et al. (2003). That decline was corroborated in bridge vector between birds and horses or humans the present study, where May was the most impor- (Tirrell et al. 2001). tant month for larval presence, and September was Continued monitoring of the 2 introduced Asian the least important, as indicated by the chi-square species is desirable for 2 reasons: lst, we are pre- test of equality of proportions, where high chi- sented with an opportunity to study the effect(s) of square cell contributions for those months account- invasive species on resident forms; and 2nd, the ed for most of the total chi-square value (Table 2). Asian species represent potential new vector op- monthly prevalences of the 2 Asian portunities for viral pathogens. The latter issue is Conversely, and the particularly relevant to public health officials in species, Ae. albopictus and Oc. iaponicus, increased throughout the West Virginia because LAC is highly endemic to predatory Tx. rutilus, prevalence for the Asian the state (McJunkin et al. 2001), and LAC has been summer. The increase in it clearly found in wild populations of Ae. albopictus (Ger- tiger mosquito was so pronounced that hardt et al. 2001). These latter workers speculated became the dominant species in September collec- that the continued range extension ofAe. albopictus tions. These findings suggest that a competitive could result in an increase in both incidence and pressure is being exerted upon larval populations distribution of LAC in the southeastern United of the resident Oc. triseriatus by invasive species l6 JounNel oF THE AMERTcaN Mosqurro CoNrnol AssocrlrroN Vol. 20, No. I

(and possibly by the predatory activities of Tx. ru- prevalence of 55Va for this species in tire samples tilus) over the breeding season. from Connecticut. Culex restuans also appeared early and exhibited In summary, the numbers of larval mosquito spe- a gradual decline in larval frequency throughout the cies in tires compared favorably with those found 2001 breeding (Joy season et al.2OO3). This pattern in previous investigations. Ochlerotatus triseriatus was repeated in 2OO2 collections, as evidenced by was clearly the dominant larval species in tire hab- the high proportion of positive collections in May itats, but apparent predation by Ti. rutitus and com- and June, coupled with low positive collections in petition by 2 introduced Asian species may con- August and September (Table 2). This pattern is tribute to lowered prevalences of Oc. triseriatus different from that observed by Andreadis (l9gg), later in the summer. The desirability for continued who noted that Cx. restuans showed no sisns of monitoring of LAC and WN vectors is discussed such a decline, and remained the dominant"Culex because of the potential for increased disease trans- species throughout the summer and fall. mission, and the effect(s) of introduced species on The role of Cx. territanJ as a competitor species resident forms. is less clear. This species has been reported as an infrequent colonizer of tire habitats (Wilmot et al. ACKNOWLEDGMENTS 1992, Jamieson et al. 1994, Szumlas et al. 1996), or absent altogether (Lee and Rowley 2000). Con- I thank Jason Godby and Brooke Kennedy for versely, Joy et al. (2OO3) noted that larvae of Cx. their help with collections, and Stuart Thomas for territans were the 3rd most commonly encountered his advice on statistical analyses. I am also indebted forms in West Virginia tire habitats in collections to Jamesina Scott for her helpful comments regard- from 2001, although the total positive encounters ing larval populations of Oc. japonlczs. This re- (-26Eo) for Cx. territans in 2OOl was comparable search was sponsored by a grant from the Rahall to that (-277o) recorded for 2OO2 (present study). Appalachian Transportation Institute, Marshall Uni- These prevalences for Cx. territans were compa- versity, under contract ATI TRP 99-08/298024. rable to the 28Vo reported for tire dumps in Con- necticut (Andreadis 1988). REFERENCES CITED Lampman et al. (1997) noted that Cx. territans was rare in early season collections, and Means AndreadisTG. 1988.A surveyof mosquitoesbreeding rn usedtire stockpilesin Connecticut. (1987) added that larval abundance of this species J Am Mosq Control Assoc 4:256-260. in New York increased through mid-July and re- DarsieRE 1986.The identificationof Aedesalbopictus n mained stable through late August. Results from the Nearctic region. .I Am Mosq Control Assoc 2:336- both of those studies were corroborated by the pre- 340. sent work, as evidenced by the fact that the sum of DarsieRII Ward RA. 1981.Identification and geographi- chi-square cell contributions for the months of May cal distribution of the mosquitoes of North America, and September made up approximately 83%oof the North of Mexico. J Am Mosq Control Assoc Mosq Syst total chi-square value (Table 2). 1(Supplt):l-313. 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This is a somewhat States:potential vector of La Crossevirrrs (Bunyaviri- different outcome than that observed bv Jov et al. dae: California serogroup).J Am Mosq Control Assoc 5:422-427. (2003), who found that larvae of Oc.- atopalpus HansonSM, Craig GB Jr. 1995.Aedes albopioas (Dip- were evenly distributed across both habitat types. tera:Culicidae) eggs: field survivorshipduring northern Remaining species were encountered too infre- Indianawinters. J Med Entomol 32:599-6O4. quently to provide valid statistical inferences in Ho BC, Ewert A, Chew L. 1989.lnterspecific competition terms of their temporal distribution. Still, because amongAedes aegypti, Ae. albopictus, and Ae. triseria- of its potential role in the transmission of West Nile las (Diptera: Culicidae):larval developmentin mixed virus, Cx. pipiens should be considered for contin- cuftures.J Med Enromol26:615-623. ued monitoring. 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