Ixodid ticks on white-tailed deer and feral swine in Florida

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1 June, 2001 Journal of Vector Ecology 93 Ixodid ticks on white-tailed deer and feral swine in Florida Sandra A. Allan, Leigh-Anne Simmons and Michael J. Burridge Department of Pathobiology P.O. Box , College of Veterinary Medicine University of Florida,Gainesville, Florida Received 20 August 2000; Accepted 30 January 2001 ABSTRACT: A state-wide survey was conducted in Florida during the hunting seasons to examine white-tailed deer (Odocoileus virginianus) and feral swine (Sus scrofa) for potential indigenous vectors of the rickettsial agent of heartwater, Cowdria ruminantium. A total of 504 white-tailed deer and 166 feral swine was examined from 30 wildlife management areas across the state. Amblyomma maculatum, an experimental vector of C. ruminantium, was common on both deer and feral swine throughout the state. Of the collection of 3,169 ticks, 34.5% were Ixodes scapularis Say, 34.0% Amblyomma americanum (L.), 25.5% Amblyomma maculatum Koch, 5.8% Dermacentor variabilis (Say), 0.4% Ixodes affinis Neumann, 0.03% Rhipicephalus sanguineus (Latreille) and 0.01% Amblyomma auricularium (Conil). The only exotic tick collected was A. auricularium, which is found on armadillos in Central and South America and is not known to be associated with any disease. Overall, the most prevalent species on deer were I. scapularis (51.1%) and A. maculatum (35.8%), with A. americanum less prevalent (16.0%) and D. variabilis (3.0%) and I. affinis (1.9%) rare. On feral swine, the most prevalent species were I. scapularis (69.7%) and D. variabilis (56.9%), with A. maculatum (16.2%) and A. americanum (4.6%) less common. The geographic distribution of ticks differed significantly throughout the state. Both A. maculatum and Dermacentor variabilis were more prevalent on deer from southern Florida compared to northern and central Florida. In contrast, A. americanum were more prevalent in northern and central Florida but rare in southern Florida, and I. scapularis were more common in southern compared to northern Florida. These geographic differences may reflect differences in the risk of tick-borne diseases to domestic animals, wildlife and humans within Florida. Journal of Vector Ecology 26(1): Keyword index: Ticks, Florida, wildlife, deer, swine, Ixodes, Amblyomma, Dermacentor INTRODUCTION The introduction and possible establishment of foreign animal diseases is an issue of increasing concern in view of numerous recent reports of the detection of exotic ticks on birds, reptiles and mammals imported into the United States (Wilson and Barnard 1985, Mertins and Schlater 1991, Clark and Doten 1995, Burridge et al. 2000a). The accidental introduction of nonindigenous tropical ticks is of particular concern due to the subtropical climate of Florida, which may be conducive to survival of these species. Of the diseases potentially carried by imported tick vectors, heartwater may have the most serious ramifications on the US livestock industry (Burridge 1997, Bram and George 2000). In addition to potentially devastating the cattle industry, heartwater may decimate indigenous wildlife including white-tailed deer (Odocoileus virginianus)(burridge 1997). This rickettsial disease, caused by Cowdria ruminantium, occurs in sub-saharan Africa and the eastern Caribbean and is exclusively transmitted by ticks belonging to the genus Amblyomma. Competent tick vectors such as Amblyomma variegatum (Fabricius) and Amblyomma hebraeum Koch are not established in North America, but have been reported on imported wildlife species (Clark and Doten 1995, Burridge et al. 2000a). Other related species of Amblyomma also have been associated with heartwater (Hoogstraal 1956) and recently the African tortoise tick, Amblyomma marmoreum Koch, was demonstrated to be an effective experimental vector of C. ruminantium (Peter et al. 2000). The establishment of this species on a reptile facility in central Florida (Allan et al. 1998) underscores the potential for disease introduction. Recently, Amblyomma sparsum Neumann and A. variegatum as well as seven other exotic tick species were collected in a survey of captive reptile facilities in Florida (Burridge et al. 2000b). If established, these ticks could spread onto wildlife species throughout the state. Moreover, the recent

2 94 Journal of Vector Ecology June, 2001 discovery of the heartwater agent in A. sparsum in Florida (Burridge et al. 2000b) prompted Florida to issue an emergency ban on importation of any African spurred tortoises or leopard tortoises (Florida Fish and Wildlife Commission 1999) and the restriction of importation of certain animals capable of carrying the disease agent or tick vectors (Florida Department of Agriculture and Consumer Services 1999). The Gulf Coast tick, Amblyomma maculatum, is indigenous to the United States and a competent experimental vector of C. ruminantium (Uilenberg 1982, Mahan et al. 2000) comparable to A. variegatum (Mahan et al. 2000). With the potential for accidental importation of heartwater into Florida, it is important to determine the distribution of A. maculatum in Florida. Both white- tailed deer and feral swine (Sus scrofa) are common hosts of this tick in Florida (Greiner et al. 1984, Forrester et al. 1996), however, the geographic distribution of this species throughout the state is unclear. This study was undertaken to investigate the importance of white-tailed deer and feral swine as hosts in Florida of Amblyomma that could potentially serve as vectors of C. ruminantium. MATERIALS AND METHODS A survey of ticks from hunter-killed white-tailed deer and feral swine was conducted during the hunting seasons (September- April) in and on wildlife management areas (WMAs) representing 34 counties in Florida (Figure 1). In the hunting seasons, localized collections were made from WMAs primarily in southern and central Florida, with additional collections from a public park (Duette Park, Collier Co.) and private lands (Charlotte, Manatee and Osceola counties). Deer and swine were examined at hunter check stations, with collections focussed on ear, head, neck and brisket regions where ticks most frequently attach (Bloemer et al. 1988, Schmidtmann et al. 1998). Ticks were removed with forceps and placed in vials containing 70% ethanol for storage until identified. Information on date, county, and host species of the collection was recorded. Ticks were identified using standard keys, and representative specimens were deposited in the U.S. National Tick Collection, Georgia Southern University, Statesboro, Georgia; Florida State Collection of Arthropods, Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Gainesville, Florida; and National Veterinary Services Laboratory, Ames, Iowa. Tick collections across Florida were grouped into 3 geographic regions (north, central and southern) (Figure 1)(based on Myers and Ewel 1990) to determine if patterns of distribution existed. The northern region consists of Apalachicola delta, Dougherty karst district, Tifton upland district and southern pine hills. Vegetation is mostly mixed pine and hardwood forests, pine flatlands, mixed hardwood swamps, salt marshes, sandhills and dunes (Myers and Ewel 1990). The central region of Florida consists of the central lake district, Ocala uplift district and Sea Island district, with areas of vegetation consisting of pine flatwoods, mixed hardwood forest, sand pine scrub dunes, salt marshes, and sandhills. The southern region consists of the Gold Coast-Florida Bay district and southern portions of the Eastern and southwestern flatland districts consisting of sawgrass and other marshes, dwarf cypress, prairies, calcareous rockland, mangroves, pine flatlands, cypress domes, and dunes (Myers and Ewel 1990). Prevalence of adult ticks was estimated following Bush et al. (1977). Prevalence was calculated as the number of individuals of a host species infested by ticks divided by the number of host species examined. In some instances, ticks collected from different individual animals were combined in one vial and these data were excluded from calculations of prevalence. Prevalence data were analyzed using X 2 analysis. Determination of a significant difference in occurrence of tick species by region was evaluated using a R x C G-test of independence (Sokal and Rohlf 1995). Because different individuals collected ticks from deer, intensity of tick infestations on deer was not calculated. RESULTS One exotic tick species, Amblyomma auricularium (Conil), was collected. A single male was collected from a feral hog in Collier County. A total of 3,169 ticks comprising seven species was collected from 504 deer and 166 wild swine (Table 1). Of the hosts examined, 75.2% were white-tailed deer and 24.8% were feral swine. Collections of A. maculatum from deer and swine were common, accounting for 58.6% of all ticks collected from deer and 41.4% of ticks collected from feral swine. Despite the fact that three time more deer than swine were examined, almost half of the specimens of I. scapularis were collected from swine. Moreover, more D. variabilis were collected from swine (84.2%) than from deer (15.8%). Deer were the primary hosts for A. americanum (98.9%). Collections of Rhipicephalus sanguineus and Amblyomma auricularium were rare (Table 1). Tick collections consisted of both adult ticks and immatures. All A. maculatum collected were adults (63.7% males and 36.1% females) except for one nymph.

3 June, 2001 Journal of Vector Ecology 95 Figure 1. Wildlife management areas (countries) in Florida where white-tailed deer and feral swine were xamined for ticks during the hunting seasons in and Numbers indicate location of wildlife management areas.

4 96 Journal of Vector Ecology June, 2001 Table. 1. Relative occurrence of ticks collected from white-tailed deer (504) and feral swine (166) during the hunting seasons ( and ) in Florida. % collected by host Species No. ticks collected Deer Swine Amblyomma americanum Amblyomma auricularium Amblyomma maculatum Dermacentor variabilis Ixodes affinis Ixodes scapularis Rhipicephalus sanguineus Most of the A. americanum collected were immatures (86.3%), with only 6.7% and 6.0% of the collections male and female, respectively. Collections of immatures consisted of nymphs (61.0% in one large collection) and larvae (25.3%). One collection in Hamilton Co. in October 1997 consisted of 414 larvae and 209 nymphs. Larvae of A. americanum were present in collections from October (Hamilton, Marion and Sumter Co.), November (Marion Co.) and December (Citrus Co.). Nymphs were present in collections from October (Hamilton, Marion and Sumter Co.) and January (Sumter Co.). Collections of males and females were almost equivalent for D. variabilis (51.4% males, 48.6% females) and I. affinis (46.2% males, 53.8% females) but not for I. scapularis (28.7% males, 71.3% females). No immatures were collected for the three latter species. Clear patterns in the species composition and relative abundance of ticks were apparent for some species when collections were grouped by geographic region (Table 2). Tick species abundance was not independent of region for white-tailed deer (G = 118.5, df = 6, P = 0.05) or feral swine (G = , df = 6, P = 0.05). Over 81% of ticks collected from deer in southern Florida were A. maculatum, whereas this species only represented 10-12% of collections from the northern and central regions. Amblyomma americanum were scarce in collections of ticks from deer and swine in the southern (0 and 1.5% of collections, respectively). In collections from central Florida, A. americanum were more abundant on deer (47.9%) than swine (0.6%) and in northern Florida, A. americanum were relatively common and over twice as abundant in collections from deer (56.9%) than from swine (27.3%). Few D. variabilis were represented in tick collections from deer across the state ( %), with collections from swine containing more D. variabilis ( %) in northern and central Florida than in southern Florida (0%). Tick collections throughout the state were comprised of similar proportions of I. scapularis, with % in collections from deer and % in collections from swine. Collections of I. affinis were rare and only from deer in central and southern Florida. Only one collection of R. sanguineus was made from deer in central Florida. Between geographic regions in Florida there were clear differences in prevalence of ticks on white-tailed deer but not feral swine (Table 3). Because some collections of ticks from individual hosts were combined by site and date, only a portion of the tick collection could be used to calculate prevalence. Of the overall collections on deer, the prevalence of I. scapularis was highest (51.1%), followed by A. maculatum (35.8%), A. americanum (16.0%), D. variabilis (3.0%) and I. affinis (1.9%) (Table 3). Over half of the feral swine examined in this study were infested with I. scapularis (69.7%) and D. variabilis (56.9%) with prevalence lower for A. maculatum (16.2%) and A. americanum (4.6%) (Table 3). Prevalences of A. maculatum and D. variabilis on deer were significantly higher in southern Florida compared to northern and central Florida (Table 3). In contrast, prevalence of I. scapularis on deer was significantly higher in northern Florida than in southern Florida. Ixodes affinis was not common, with a prevalence of 3.7% on deer in central Florida and 1.2 % in southern Florida. Amblyomma americanum was absent from collections from deer in southern Florida and only one feral swine was infested in southern Florida. Prevalence of tick species did not differ between central and south Florida on feral swine. DISCUSSION Amblyomma maculatum was the only tick species collected in Florida with potential to be a vector of the

5 June, 2001 Journal of Vector Ecology 97 Table 2. Regional distribution of ticks collected from deer and feral swine in Florida during the and hunting seasons. % species composition of each region Host Region No. of hosts No. of ticks A. A. A. D. I. I. R. sampled collected americanum auricularium maculatum variabilis affinis scapularis sanguineus Deer North Central South Swine North Central South Table 3. Prevalence of ixodid ticks collected from deer and feral swine in different regions of Florida during the and hunting seasons. % hosts infested by tick species Host Region No. of hosts A. americanum A. maculatum D. variabilis I. affinis I. scapularis Deer North a 27.3a 1.4a 0.0a 75.7 a Central a 29.4a 0.9a 3.7a 51.4ab South b 60.2b 9.4b 1.2a 30.5a Combined Swine North Central a 15.7a 57.8a 0.0a 57.8a South a 19.8a 54.1a 0.0a 79.1a Combined Numbers with the same column and host followed by the same letter at not significantly different (X 2, P > 0.05) 2 No tick collections from individual feral swine.

6 98 Journal of Vector Ecology June, 2001 rickettsial agent of heartwater (Uilenberg 1982, Mahan et al. 2000). Across the state, this species was widespread in distribution and present commonly on deer in relatively high numbers during the fall and winter when hosts were sampled. Should heartwater be accidentally introduced into the United States, A. maculatum has the capability of playing a role in the establishment of this disease in wildlife and livestock populations. The average prevalence on deer (35.8%) was similar to a previous report of 32% across Florida (Smith 1977), and greater than reports of 18% in southern Texas (Samuel and Trainer 1970) and 1% in Alabama (Durden et al. 1991). The prevalence in south Florida (60.2%) was also greater than that reported in southern Florida (10%) by Forrester et al. (1996). There was a clear pattern in geographic distribution of A. maculatum in Florida, with more specimens present on deer in southern Florida compared to the northern and central regions of the state. Additionally, this was the most common tick collected from deer in southern Florida (81.6% of all ticks). Feral swine were also important hosts for Amblyomma maculatum. Over 16% of swine across the state were infested with this species, making it the third most abundant tick on these animals. No A. maculatum were collected from swine in northern Florida and moderate numbers were collected in central and southern Florida. In southern Florida A. maculatum represented 14.6% of the ticks collected from feral swine. Previous reports indicated that 85.9% of feral swine sampled during late summer in southern Florida (Greiner et al. 1984) and 7 and 1 % of Florida panthers (Felis concolor coryi) and bobcats (Felis rufus floridana), respectively, collected across Florida (Wehinger et al. 1995) were infested with A. maculatum. In the current study, the lower prevalence (16%) presumably reflects collection from a later time of year (fall and winter). Adult ticks were collected throughout the fall and winter months in our study. Adult A. maculatum have been reported to be active in northern Florida from June to September, with some present in December (Rogers 1953) or August and September (Cilek and Olsen 2000). The only exotic tick collected in this study was a single specimen of A. auricularium collected from a feral swine. This common parasite of armadillos in South and Central America (Fairchild et al. 1966, Jones et al. 1972) has not been reported in the United States. Although A. auricularium has been collected from Collier Co. (this study) and Glades Co. (Lord and Day 2000), it was not reported from earlier surveys of armadillos throughout Florida (summarized in Forrester 1992) and the extent to which A. auricularium is established in Florida is unknown. Hosts of this species include a variety of other mammals, with a report of collection from a domestic hog in Panama (Fairchild et al. 1966). While our collections were limited to wildlife management areas during the fall and winter, it is possible that other exotic ticks might be present in sites not sampled or during other times of the year. Our collections, however, do provide baseline information for the wildlife management areas involved. Future surveys for exotic ticks should focus on collections of ticks from both reptiles and mammals in the proximity of locations where exotic ticks have been reported (Burridge et al. 2000a,b). The climate in Florida is conducive to the establishment of exotic tropical and subtropical tick species on wildlife. The iguana tick, Amblyomma dissimile Koch, a native of central and south America has been reported in Florida on captive animals (Bishopp and Trembly 1945) and indigenous species of snakes (Bequaert 1932, 1945, Keirans and Durden 1998). Another exotic tick species recently reported in Florida as established on the marine toad (Bufo marinus) is Amblyomma rotundatum (Oliver et al. 1993b). The lone star tick, A. americanum, does not appear to be a competent vector of C. ruminantium, with no evidence of transmission under experimental conditions in a recent study by (Mahan et al. 2000). It feeds readily on humans (Felz et al. 1996) and is implicated as a vector of Ehrlichia chaffeensis (Anderson et al. 1993). This species was relatively abundant in northern and central Florida, but rare in southern Florida, with only one adult collected in this study in Palm Beach County. Previous reports of A. americanum in southern Florida include those collected from Glades Co. (Greiner et al. 1984)(3 ticks from 453 feral swine) and Dade Co. (Taylor 1951). Smith (1977) collected A. americanum from white-tailed deer in central and northern Florida, but not in southern Florida. Smith et al. (1982) also did not collect this species from feral swine in Florida north of Glades Co. Amblyomma americanum was only reported from central Florida northward by Taylor (1951) and Wehinger et al. (1995). The southernmost collection of A. americanum from Florida panthers and bobcats was from central Florida (Highlands Co.)(Wehinger et al. 1995). The reason for the low prevalence of this species in southern Florida is not known, and possible factors may include climate, vegetation and host availability. Adult A. americanum were collected during fall and winter in Florida as reported previously (Rogers, 1953, Greiner et al. 1984). While peak adult activity of A. americanum in northern Florida is March, adults have been collected year round (Rogers 1953). Our collection of larvae and nymphs in the fall is similar to that of Rogers (1953) who reported peak abundance of

7 June, 2001 Journal of Vector Ecology 99 immatures during spring and summer with nymphs active year round and larvae active in all but the coldest months. Deer appear to be more common hosts of lone star ticks than feral swine, with over 98% of this species collected from deer. Prevalence of lone star ticks on deer (16.0%) was more than three times greater than that on feral swine (4.6%). In other studies, prevalence of lone star ticks on deer ranged from 10% in Texas (Samuel and Trainer 1970), 11% in Alabama (Durden et al. 1991), 26% across northern and central Florida (Smith 1977), 53% in North Carolina (Apperson et al. 1990) to 59-81% throughout Mississippi (Demarais et al. 1987). The prevalence of A. americanum on feral swine was <1% in southern Florida (Greiner et al. (1984) and 35% from the southeastern states (Smith 1981). In the latter study, however, no ticks were collected in Florida. Reasons for the higher prevalence of lone star ticks on deer compared to feral swine are not known. As indicated in our study and by others (Smith 1977, Apperson et al. 1990, Durden et al. 1991, Luckhardt et al. 1991), one of the most common tick species on deer in southeastern North America is Ixodes scapularis. This species was collected during the peak of seasonal activity which is the fall and winter in the southeast (Rogers 1953, Clark et al. 1998). The state-wide prevalence of Ixodes scapularis on deer in our study was 51.1%, similar to reports from North Carolina (46%) (Apperson et al. 1990) and Alabama (54%) (Durden et al. 1991). The prevalence on deer in southern Florida (30.5%) was similar to reported by Forrester et al. (1996)(26%). The prevalence of Ixodes scapularis on feral swine (69.7%) was higher than previous reports from southern Florida (1%) (Greiner et al. 1984) and southeastern states (7%) (Smith et al. 1982). The difference in prevalence of I. scapularis between these studies may reflect different habitats utilized by swine. In addition to white-tailed deer and feral swine, 15 other mammal species have been reported as hosts of this species in Florida (Forrester 1992). The spirochete causing Lyme disease, Borrelia burgdorferi, has been isolated from I. scapularis collected in southeastern states (Oliver et al. 1993a, Oliver 1996). Ixodes affinis is a relatively rare tick reported from deer throughout parts of Florida, Georgia and South Carolina (Oliver et al. 1987, Clark et al. 1998, Lavender and Oliver 1996). Adults of I. affinis are present from spring to fall with a peak in summer (Oliver et al. 1987, Clark et al. 1998) and may therefore have been less abundant in our study because collections were primarily from fall and winter. In this study I. affinis was reported from 1.9% of deer. Previously this species has been reported from 8% of deer in southern Florida (Forrester et al. 1996), and from 32% of Florida panthers and 13% of bobcats in Florida (Wehinger et al. 1995). These studies, however, involved tick collections throughout the year, not just during the fall and winter as in this study. Isolates of B. burgdorferi have also been obtained from this species in Georgia and South Carolina (Clark et al. 1998). Dermacentor variabilis is a vector of Rickettsia rickettsii, the causal agent of Rocky Mountain spotted fever (Schreifer and Azad 1994). Similar to previous reports, this tick was relatively uncommon on deer during the fall and winter (Rogers 1953, Kellogg et al. 1971, Smith 1977, Durden et al. 1991, Forrester et al. 1996). This species, however, was relatively common on feral swine collected from the same time period and areas. This is consistent with reports from southern Florida of high prevalence on feral swine (Greiner et al. 1984) and bobcats and Florida panthers (Wehinger et al. 1995). The greatest seasonal activity of adult D. variabilis is during the summer in Florida, with adults present on hosts year round (Rogers 1953). No immature stages were collected in this study, although immatures have been reported from rodents during the fall and winter in Florida (Rogers 1953). While only 24.7% of the hosts sampled in this study were swine, more than 84% of the D. variabilis collected were from swine. Similarly, there was a higher prevalence of this species on swine (56.9%) than on deer (3.0%). The differences in prevalence were similar between years, and similar patterns of infestation were seen when collections were subdivided by geographic region of Florida. In southern Florida, Greiner et al. (1984) reported D. variabilis from 99.6% of the swine examined in Glades County, while Forrester et al. (1996) reported 1% prevalence on deer in southern Florida (Collier, Monroe and Dade counties). The prevalence of D. variabilis reported from Florida panthers and bobcats was 92% and 66%, respectively, from southern Florida (Wehinger et al. 1995). In Tennessee, 30% of feral swine were infested with D. variabilis (Henry and Conley 1970). Differences in prevalence of this tick species between deer and swine may result from factors such as host preference, difference in habitat utilization or size of home range. Although there have been previous reports of D. variabilis from white-tailed deer or feral swine in Florida, this is the first direct comparison of prevalence, intensity and abundance of these ticks on different hosts. Only two R. sanguineus were collected in this study, both from deer. This tick has previously been reported from white-tailed deer in Florida (Forrester 1992). There were clear geographic differences in the presence of different tick species from northern to southern Florida. Intensity of infestations of A. americanum, A. maculatum

8 100 Journal of Vector Ecology June, 2001 and I. scapularis on deer differed significantly with geographic region with infestations of A. americanum and I. scapularis being significantly lower in southern Florida and infestations of A. maculatum significantly higher. Differences in distribution across geographic region have been reported previously for I. scapularis (North Carolina (Apperson et al. 1990), Tennessee (Kollars 1996), Missouri ( Kollars et al. 1997), Alabama (Durden et al. 1991) and A. americanum (North Carolina (Apperson et al. 1990), Alabama (Durden et al.1991) but not for A. maculatum. These tick species are all competent vectors of a variety of pathogens affecting wildlife, livestock and humans. Differences in geographic distribution of vectors in Florida potentially represents differences in disease risk throughout the state. Acknowledgments Thanks to R. E. Vanderhoof, N. Bates, N. Barnes, W. Chandler, R. Crawford, J. Garrison, M. Holmes, D. C. Hunt, J. King,, B. Marchinton, G. Marsh, B. Mitchell, D. R. Munyan, G. C. Platt, B. Reynolds, B. Schumate, R. Sconiers, M. R. Spires, A. Stockle, R. Uherka,, T. Walker, L.G. Warden, W. K. Weems, and M. Wefer of the Florida Fish and Wildlife Conservation Commission and USDA/APHIS for collection of ticks. Thanks are also extended to D. Forrester and E. Greiner for their thoughtful comments. This paper is published as Florida Agricultural Experiment Stations Journal Series No. R REFERENCES CITED Allan, S. A., L. A. Simmons, and M. J. Burridge Establishment of the tortoise tick, Amblyomma marmoreum (Acari: Ixodidae) on a reptile-breeding facility in Florida. J. Med. Entomol. 35: Anderson, B. E., K. G. Sims, J. G. Olson, J. E. Childs, J. F. Piesman, C. M. Happ, G. O. Maupin, and B. J. B. Johnson Amblyomma americanum: a potential vector of human ehrlichiosis. Am. J. Trop. Med. Hyg. 49: Apperson, C. S., J. F. Levine, and W. L. Nicholson Geographic occurrence of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) infesting white-tailed deer in North Carolina. J. Wild. Dis. 26: Bequaert, J Amblyomma dissimile Koch, a tick indigenous to the United States (Acarina: Ixodidae). Psyche 39: Bequaert, J Further records of the snake tick, Amblyomma dissimile Koch in Florida. Bull. Brooklyn Entomol. Soc. 40: 129. Bishopp, F. C. and H. L. Trembley Distribution and hosts of certain North American ticks. J. Parasitol. 31: Bloemer, S. R., R. H. Zimmerman, and K. Fairbanks Abundance, attachment sites, and density estimators of lone star ticks (Acari: Ixodidae) infesting white-tailed deer. J. Med. Entomol. 25: Bram, R. A. and J. E. George Introduction of nonindigenous arthropods pests of animals. J. Med. Entomol. 37: 1-8. Burridge, M. J Heartwater: an increasingly serious threat to the livestock and deer populations of the United States, pp In Proceedings the 101st Annual Meeting of United States Animal Health Association, Louisville, KY Spectrum Press, Richmond, VA. Burridge, M. J., L. A. Simmons, and S. A. Allan. 2000a. Introduction of potential heartwater vectors and other exotic ticks into Florida on imported reptiles. J. Parasitol. 86: Burridge, M. J., L. A. Simmons, B. H. Simbi, T. F. Peter and S. M. Mahan. 2000b. Evidence of Cowdria ruminantium infection (heartwater) in Amblyomma sparsum ticks found on tortoises imported into Florida. J. Parasitol. 56: Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W. Shostak Parasitology meets ecology on its own terms. Margolis et al. Revisited. J. Parasitol. 83: Cilek, J. E. and M. A. Olsen Seasonal distribution and abundance of ticks (Acari: Ixodidae) in northwestern Florida. J. Med. Entomol. 37: Clark, L. G. and E. H. Doten Ticks on imported reptiles, Miami International Airport November 1994 through January In Proceedings, 1995 Veterinary Epidemiology and Economics Symposium, College Station, TX. Clark, K. L., J. H. Oliver, Jr., D. B. McKechnie and D. C. Williams Distribution, abundance, and seasonal activities of ticks collected from rodents and vegetation in South Carolina. J. Vect. Ecol. 23: Demarais, S., H. A. Jacobson, and D. C. Guynn Effects of season and area on ectoparasites of whitetailed deer (Odocoileus virginianus) in Mississippi. J. Wild. Dis. 23: Durden, L.A., S. Luckhardt, G. R. Mullen, and S. Smith Tick infestations of white-tailed deer in Alabama. J. Wild. Dis. 27: Fairchild, G. B., G. M. Kohls, and V. J. Tipton

9 June, 2001 Journal of Vector Ecology 101 The ticks of Panama (Acarina: Ixodoidea). In: Ectoparasites of Panama, R. L. Wenzel and V.J. Tipton (eds.) Field Museum of Natural History. Chicago, Illinois. Felz, M. W., L. A. Durden and J. H. Oliver, Jr Ticks parasitizing humans in Georgia and South Carolina. J. Parasitol. 82: Florida Department of Agriculture and Consumer Services C-ER Temporary restrictions on importation of animals. Tallahassee, FL. Florida Fish and Wildlife Conservation Commission A-ER Emergency prohibition against importation of certain African tortoises. Tallahassee, FL. Forrester, D. J Parasites and diseases of wild mammals in Florida. University Press of Florida, Gainesville. Forrester, D. J., G. S. McLaughlin, S.R. Telford, Jr., G. W. Foster, and J. W. McCown Ectoparasites (Acari, Mallophaga, Anoplura, Diptera) of whitetailed deer, Odocoileus virginianus, from southern Florida. J. Med. Entomol. 33: Greiner, E. C., P. P. Humphrey, R. C. Belden, W. B. Frankenberger, D. H. Austin, and E. P. J. Gibbs Ixodid ticks on feral swine in Florida. J. Wild. Dis. 20: Henry, V. G. and R. H. Conley Some parasites of European wild hogs in the southern Appalachians. J. Wildl. Manag. 34: Hoogstraal, H African Ixodoidea. 1. Ticks of the Sudan (with special reference to Equatoria Province and with preliminary reviews of genera Boophilus, Margaropus and Hyalomma. Res. Rep. N. M U.S. Govt. Dept. Navy, Bur. Med. Surg., Washington, D.C. Jones, E. K., C. M. Clifford, J. E. Keirans, and G. M. Kohls The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the western hemisphere. Brigham Young Univ. Science Bulletin 17. Keirans, J. E. and L. A. Durden Illustrated key to nymphs of the ticks genus Amblyomma (Acari: Ixodidae) found in the United States. J. Med. Entomol. 35: Kellogg, F. E., T. P. Kistner, R. K. Stickland, and R. R. Gerrish Arthropod parasites collected from white-tailed deer. J. Med. Entomol. 8: Kollars, T. M Variation in infestation by Ixodes scapularis (Acari: Ixodidae) between adjacent upland and lowland populations of Odocoileus virginianus (Mammalies: Cervidae) in western Tennessee. J. Entomol. Sci. 31: Kollars, T. M., Jr., L. A. Durden, E. J. Masters and J. H. Oliver, Jr Some factors affecting infestations of white-tailed deer by black-legged ticks (Acari: Ixodidae) in southeastern Missouri. J. Med. Entomol. 34: Lavender, D. R. and J. H. Oliver, Jr Ticks (Acari: Ixodidae) in Bulloch County, Georgia. J. Med. Entomol. 33: Lord, C. C. and J. F. Day First record of Amblyomma auricularium (Acari: Ixodidae) in the United States. J. Med. Entomol. 37: Luckhardt, S., G. R. Mullen, and J. C. Wright Etiologic agent of Lyme disease, Borrelia burgdorferi, detected in ticks (Acari: Ixodidae) collected at a focus in Alablama. J. Med. Entomol. 28: Mahan, S. M., T. F. Peter, B. H. Simbi, K. Kocan, E. Camus, A. F. Barbet, and M.J. Burridge Comparison of the efficacy of American and African Amblyomma ticks as vectors of heartwater (Cowdria ruminantium) infection by molecular analyses and transmission trials. J. Parasitol. 86: Mertins, J. W. and J. L. Schlater Exotic ectoparasites of ostriches recently imported into the United States. J. Wildl. Dis. 27: Myers, R. L. and J. J. Ewel. (Eds) Ecosystems of Florida. University of Central Florida Press, Orlando, FL. Oliver, J. H., Jr., J. E. Keirans, D. R. Lavender, and H. J. Hutcheson Ixodes affinis Neumann (Acari: Ixodidae): New host and distribution records, description of immatures, seasonal activities in Georgia and laboratory rearing. J. Parasitol. 73: Oliver, J. H., Jr., F. W. Chandler, M. P. Luttrell, A. M. James, D. E. Stallkneckt, B. S. McGuire, H. J. Hutcheson, G. A. Cummins and R. S. Lane Isolation and transmission of the Lyme disease spirochete from the southeastern United States. Proc. Natl. Acad. Sci. 90: Oliver, J. H., Jr., M. P. Hayes, J. E. Keirans, and D. R. Lavender. 1993b. Establishment of the foreign parthenogenic tick Amblyomma rotundatum (Acari: Ixodidae) in Florida. J. Parasitol. 79: Oliver, J. H., Jr Lyme borreliosis in the southern United States: a review. J. Parasitol Peter, T. F., M. J. Burridge and Suman M. Mahan Competence of the African Tortoise tick, Amblyomma marmoreum (Acari: Ixodidae), as a vector of the agent of heartwater (Cowdria ruminantium). J. Parasitol. 86: Rogers, A. J A study of the ixodid ticks of

10 102 Journal of Vector Ecology June, 2001 Northern Florida, including the biology and life history of Ixodes scapularis Say (Ixodidae: Acarina). University of Florida, M.S. thesis. Samuel, W. M. and D. O. Trainer Amblyomma (Acarina: Ixodidae) on white-tailed deer, Odocoileus virginianus (Zimmermann), from south Texas with implications for theileriasis. J. Med. Entomol. 7: Schmidtmann, E. T. J., F. Carroll and D. W. Watson Attachment-site patterns of adult blacklegged ticks (Acari: Ixodidae) on white-tailed deer and horses. J. Med. Entomol. 35: Schreifer, M. E. and A. F. Azad Changing ecology of Rocky Mountain Spotted Fever. pp In Ecological dynamics of tick-borne zoonoses. D. E. Sonenshine and T. N. Mather (eds.) Oxford University Press, NY. Sokal, R. R. and F. J. Rohlf Biometry: the principles and practice of statistics in biological research, 3rd. Ed., Freeman, NY. Smith, H. M., Jr Parasites of wild swine (Sus scrofa) in the southern United States. M.S. thesis, University of Georgia. Smith, H. M., W. R. Davidson, V. F. Nettles, and R. R. Gerrish Parasitisms among wild swine in southeastern United States. J. Am. Vet. Med. Assoc. 181: Smith, J. S A survey of ticks infesting whitetailed deer in 12 southeastern states. M.S. thesis, University of Georgia, Athens. Taylor, D. J The distribution of ticks in Florida. University of Florida, M.S. thesis. Uilenberg, G Experimental transmission of Cowdria ruminantium by the Gulf Coast tick Amblyomma maculatum: Danger of itnroducing heartwater and benign African theileriasis onto the American mainland. Am. J. Vet. Res. 43: Wehinger, K. A., M. E. Roelke, and E. C. Greiner Ixodid ticks from panthers and bobcats in Florida. J. Wildl. Dis. 31: Wilson, N. and S. M. Barnard Three species of Aponomma (Acari: Ixodidae) collected from imported reptiles in the United States. Florida Entomol. 68:

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