Exp Appl Acarol DOI 10.1007/s10493-016-0019-4
Ticks associated with domestic dogs and cats in Florida, USA Jennifer E. Burroughs1,5 • J. Alex Thomasson2 • Rosanna Marsella3 • Ellis C. Greiner1 • Sandra A. Allan4
Received: 15 September 2015 / Accepted: 7 February 2016 Ó Springer International Publishing Switzerland (outside the USA) 2016
Abstract Voluntary collections of ticks from domestic dogs and cats by veterinary practitioners across Florida, USA, were conducted over a 10 month period. Of the 1337 ticks submitted, five species of ixodid ticks were identified and included Rhipicephalus sanguineus, Amblyomma americanum, A. maculatum, Dermacentor variabilis, and Ixodes scapularis. Most ticks were collected from dogs (98.4 %) with the most predominant species being R. sanguineus (94.3 %). Of the ticks collected from cats (1.6 %), A. americanum were the most common (74 %). Only R. sanguineus were collected throughout the state, with the other species collected only in central and north Florida. The tick species collected from dogs and cats represent a risk to these domestic species as well as associated humans for a range of tick-borne diseases in Florida. Keywords
Ticks Dog Cat Rhipicephalus Amblyomma Ixodes Florida
& Sandra A. Allan [email protected] 1
Department of Infectious Diseases and Pathology, College of Veterinary Medicine, University of Florida, Gainesville, FL 32607, USA
2
Field Veterinary Services, Merial Ltd, Duluth, GA 30096, USA
3
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32607, USA
4
Center for Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service (ARS), USDA, Gainesville, FL 32608, USA
5
U.S. Army Medical Command, Carlisle, PA 17013, USA
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Introduction Tick-borne diseases affect numerous dogs and cats in North America each year and many of these diseases are zoonotic. Common bacterial tick-borne diseases include borreliosis, rickettsiosis, ehrlichiosis, and anaplasmosis. Lyme borreliosis is caused by the spirochete Borrelia burgdorferi and most commonly transmitted by Ixodes spp. (Shaw et al. 2001a, b; Fritz and Kjemtrup 2003; Bowman et al. 2009). While clinical disease has been characterized in dogs (Fritz and Kjemtrup 2003), contradictory information exists for clinical symptoms in cats which remain uncharacterized (Shaw et al. 2001a, b; Fritz and Kjemtrup 2003). In a recent national serologic survey, 0.5 % of dogs (256/54,982) examined in Florida were positive for Lyme borreliosis (Bowman et al. 2009). In a study by Little et al. (2014) antibody presence in dogs in the US varied from 0.1 to 5 % depending on county. Exposure of cats to Borrelia in Florida remains unknown. Canine rickettsiosis results from infection with Rickettsia rickettsii primarily transmitted by Dermacentor variabilis and D. andersoni (Shaw et al. 2001a, b) with recent implication of Rhipicephalus sanguineus as a vector in Arizona (Green 2011). Dogs are susceptible to R. rickettsii with clinical disease characterized (Shaw et al. 2001a, b). While cats have been reported with exposure to R. rickettsii (Greene and Breitschwerdt 1998), clinical disease has not been documented (Shaw et al. 2001a, b). Exposure levels of dogs and cats in Florida to Rickettsia remains unclear. Ehrlichiosis may be caused by several species of Ehrlichia with different tick vectors. Dogs are susceptible to infection with Ehrlichia chaffeensis and E. ewingii, both of which are transmitted by Amblyomma americanum (Shaw et al. 2001a, b; Bowman et al. 2009) and with implicated transmission by R. sanguineus (Ndip et al. 2007, 2010). Additionally, R. sanguineus is the main effective vector of E. canis (Shaw et al. 2001a, b). In an extensive serosurvey examining 8662 dog blood samples across southern and central states, an overall seroprevalence of 2.8, 5.1 and 0.8 % was obtained for E. chaffeensis, E. ewingii, and E. canis, respectively (Beall et al. 2012). In Florida, seroprevalence was 1.2, 2.6 and 0.5 % for the three species, respectively. In national serosurveys Bowman et al. (2009) reported that 0.8 % of dog samples from Florida were positive for erhlichiosis and Little et al. (2014) reported 3.2 % seropositive dogs in the southeastern US with counties ranging from 0.1 to over 5 %. While feline ehrlichiosis has been the reported result of infection with Ehrlichia equi (Shaw et al. 2001a, b), E. canis (Breitschwerdt et al. 2001), and E. risticii (Stubbs et al. 1998), several studies (Lappin et al. 2005; Eberhardt et al. 2006) including a recent study on feral cats in Florida, reported no detectable exposure to Ehrlichia spp. (Luria et al. 2004). Anaplasmosis has been reported from both dogs and cats and caused by Anaplasma phagocytophilum transmitted by Ixodes ticks (most commonly Ixodes scapularis and I. pacificus) (Bowman et al. 2009). In a recent serosurvey, 0.5 % of dog blood samples at both a national level and within Florida were positive for exposure to Anaplasma (Bowman et al. 2009). Similar low levels of 0.9 % in southeastern states were reported by Little et al. (2014). While domestic cats can be infected with A. phagocytophilum (Shaw et al. 2001a, b), a recent study examining sera from 553 feral cats in northern Florida revealed no evidence of exposure (Luria et al. 2004). The most common tick-borne protozoan diseases of dogs and cats in North America include babesiosis, cytauxzoonosis, and hepatozoonsis. Babesiosis in dogs in North America is associated with infections with Babesia canis (now considered B. canis voegli (Zahler et al. 1998) and B. gibsoni vectored by R. sanguineus (Shaw et al. 2001a, b; Green
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2011). High levels of infection have been reported in kennels in North Carolina and Florida (Taboada et al. 1991; Kordick et al. 1999). Feline babesiosis in North America has been only reported once from cougars in Florida (Yabsley et al. 2006). Infections of domestic cats with the highly fatal Cytauxzoon felis occurs through tick bites generally from D. variabilis or A. americanum (Blouin et al. 1984; Reichard et al. 2009). These infections often occur in the vicinity of low residential areas in the presence of multiple land use cover types (Reichard et al. 2008). In Florida, bobcats and Florida panthers appear to serve as reservoirs with occasional cases reported from feral and domestic cats (Butt et al. 1991; Rotstein et al. 1999; Yabsley et al. 2006) and serve as hosts for the same tick species (Wehinger et al. 1995). Recent evidence of 6.2 % infection of healthy domestic cats with C. felis in southcentral US states appears to indicate that these chronically infected cats may serve as reservoirs for infection for naı¨ve cats (Rizzi et al. 2015). Hepatozoonosis is a tick-transmitted canine disease caused by ingestion of Hepatozoon americanum –infected Amblyomma maculatum ticks (Shaw et al. 2001a, b). This recently discovered disease is closely associated with the geographic distribution of the tick vector and reported in the southern United States, particularly along the gulf coast (Ewing and Panciera 2003). Clearly, tick-borne diseases could present a significant health risk to small animals in Florida with the zoonotic potential raising additional concern for animal owners. Better knowledge of the distribution of tick species in Florida as well as a clear understanding of the tick-host interaction can provide a foundation for enhanced disease detection and mitigation of risks of infection. A recent survey of feral cats in north central Florida provided some information on the interaction of feral cats and ticks (Akucewich et al. 2002). In this study, ticks were detected on only 5/200 cats with a total of nine ticks recovered. To date, no surveys have been conducted on the presence of ticks on domestic cats or dogs in Florida. To better evaluate the risk of tick borne disease, it is important to know the tick species present in a geographical area. Our objective in this study was to investigate the geographic distribution of tick species found on domestic dogs and cats throughout Florida.
Materials and methods Collections of ticks were obtained on a voluntary basis from veterinary small animal practitioners across Florida, from July 2008 through May 2009. Florida veterinary practices were contacted with a request to participate in the study, and those agreeing to participate were sent collection forms and instructions for submitting tick samples from dog and cat patients brought to the practice during the sample period. The reason for the visit to the practice did not have to be the presence of ticks or tick-borne disease symptoms. Collection forms included questions on the medical history of the animal relevant to tick transmitted diseases, the number of ticks observed during the visit, and whether animals were maintained indoors, outdoors, or both. Ticks received from the participating veterinary practices were sorted by life stage and sex, identified using keys (Keirans and Litwak 1989; Keirans and Durden 1998; Clifford and Anastos 1960), and stored in vials containing 70 % ethanol. Species identification data were reported to the participating practitioners via email or fax.
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Results The survey resulted in 1337 ticks from 189 submissions from veterinary practices. Dogs were hosts for 95.2 % of the submissions and contributed 98.4 % of ticks collected. Cats were hosts for 4.8 % of the submissions and 1.6 % of ticks collected. Five species of ixodid ticks were recovered from dogs and/or cats in this study and included R. sanguineus, A. americanum, A. maculatum, D. variabilis, and I. scapularis (Table 1). Overall, the predominant tick species collected was R. sanguineus (93.0 %) and the least common tick species was A. maculatum (0.3 %). From the collections submitted from dogs, R. sanguineus was the most commonly collected tick species (94.3 %), followed by A. americanum (2.7 %), I. scapularis (1.8 %) and A. maculatum and D. variabilis contributed *1 % of the rest of the collections (Table 1). For dogs, an average of 8.4 R. sanguineus ticks were collected per dog with a maximum of 132 ticks (all adults except one larva) collected on one dog. Average infestations on dogs across all tick species ranged between 2.0 and 2.4 ticks per dogs with a maximum infestation of 8 ticks per dog. The most common tick collected on cats was A. americanum (71 %) (Table 1) and average infestations were 3.7 ticks per cat. The highest infestation was a collection of 11 ticks from a cat that consisted of 9 larvae and 2 nymphs. Only a few cats were infested with I. scapularis and A. americanum (Table 1) with average infestations of 1.2 and 1 tick per cat, respectively. Few immatures were collected by veterinarians which is not atypical of volunteer collections that tend to focus on macroscopic examination and overlook smaller larvae and nymphs (Foldvari and Farkas 2005). Florida has 67 counties of which 22 were represented in the survey (Fig. 1). Of these counties, R. sanguineus were identified from 81.8 % of the counties. Counties reporting ticks other than R. sanguineus had samples of 6 or fewer ticks. Counties comprising over 5 % of the total tick collection included Marion County (41.7 %), Leon County (51.2 %), Brevard County (9.9 %) and Lake County (7.9 %). Several counties (Citrus, Duval, and Flagler) only had one submission. While submissions did not represent all of the counties, R. sanguineus were present throughout the state. Only 47 ticks were collected from south Florida (Miami-Dade, Collier, and Hendry Counties) and these were exclusively R. sanguineus. Of the 121 dogs in the survey, only 44 included information on whether the animal lives inside, outside, or both. Of the dogs reported as inside dogs, 90.9 % were infested with R. sanguineus, 9.0 % A. americanum, and 2.2 % with I. scapularis ticks. Of the dogs described as outdoor dogs, 83 % were infested with R. sanguineus. Of the 15 cats
Table 1 Identification of ticks collected from dogs and cats in Florida Tick species
Number collected (% of total)
Mean number on animal (SE) (range)
Dog
Cat
Dog
Cat
Amblyomma americanum
36 (2.7)
15 (71)
2.2 (0.6) (1–8)
3.7 (2.4) (1–11)
Amblyomma maculatum
4 (0.3)
Dermacentor variabilis
10 (0.8)
Ixodes scapularis
24 (1.8)
5 (24)
2.4 (0.6) (1–7)
Rhipicephalus sanguineus
1242 (94.4)
1 (5)
8.4 (1.5) (1–132)
Total
1316
21
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2.0 (0.0) (2) 2.0 (0.7) (1–5) 1.2 (0.2) (1–2) 1 (0) (1)
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Fig. 1 Map of Florida showing distribution of tick species collected on dogs and cats in the sampled counties
in the survey, only 5 included information on whether they lived indoors, outdoors, or both. Of the 5 cats, one cat with both indoor and outdoor habits was infested with R. sanguineus. Animals with diagnoses or suspected diagnoses of tick-borne disease represented 5.1 % of the submissions. Two dogs, one with a total of 126 R. sanguineus ticks (24 females and 102 males) and the other with a single R. sanguineus tick, were suspected to have tick paralysis. One dog with an attached A. americanum tick tested positive for Ehrlichia and one dog with 3 R. sanguineus ticks tested positive for borreliosis. A cat with 11 A. americanum ticks had a suspected diagnosis of hemobartonellosis.
Discussion In the present study, the majority of ticks submitted from dogs were R. sanguineus (94.3 %), likely reflecting the affinity for this species to infest indoors. Their ability to infest outdoors in warm climates further complicates control efforts (Dantas-Torres 2008,
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Diniz et al. 2010). Conditions supporting development of high R. sanguineus populations in conjunction with high tick and dog contact likely contribute to their widespread presence through Florida. The average infestation level of about 8.4 ticks/dog suggests that infestations are not incidental and are well established. Infestation rates of R. sanguineus on dogs have been reported for Georgia (US) (3.8 ticks/dog, Goldberg et al. 2002), Brazil (5.4, Dantas-Torres et al. 2009), and Italy (39.4, Otranto et al. 2005). The average number of R. sanguineus ticks/dog reported in southeastern Oklahoma and northwestern Arkansas was 53.6 with greatest infestations from July–September (Koch 1982). While infestation levels were not presented, Clark et al. (1996) reported that R. sanguineus was the third most common species collected from dogs in South Carolina. The establishment and maintenance of these tick populations peridomestically (Dantas-Torres et al. 2009) can contribute to sustained populations even in the event of control efforts directed toward dogs and facilities. The presence of insecticide resistance to permethrin and fipronil further complicates effective control of this species (Eiden et al. 2015). High infestation levels of dogs with R. sanguineus presumably increases risk of contracting babesiosis or ehrlichiosis. The other four species collected from dogs, A. americanum, A. maculatum, D. variabilis, and I. scapularis, are relatively common (average of 2.0–2.4 ticks/dog) ticks that live exclusively outdoors and are documented in previous surveys of ticks on wild animals in Florida (Greiner et al. 1984; Forrester et al. 1996; Allan et al. 2001). The presence of these species may reflect risk of ehrlichiosis, babesiosis, Lyme disease, rickettsiosis, anaplasmosis, and hepatozoonosis in dogs. The infestation rates of these four species on dogs in the present study contrast with rates found on dogs in previous studies in southeast US states or neighboring regions. In a survey of ticks infesting dogs in northwestern Georgia, A. americanum and D. variabilis were collected from dogs with a range of 2.1–2.4 ticks per dog (Goldberg et al. 2002). While A. maculatum, I. scapularis, and I. cookei were also collected from dogs, these were collected in low numbers (1–3 ticks per dog) (Goldberg et al. 2002). In Arkansas and Oklahoma, A. americanum were collected at high levels (30.7 ticks/dog) with low numbers of I. scapularis, D. variabilis, A. americanum, and I. cookei also collected (Koch 1982). In contrast to the above studies D. variabilis and A. maculatum were the most common species collected from dogs in South Carolina (Clark et al. 1996). Relatively few tick collections were obtained from cats, suggesting that ticks are not a significant risk for US domestic cats in the sampled region. Of the few ticks identified from cats in the survey, most were A. americanum and I. scapularis, both species found exclusively outside homes and posing a risk of tick-borne disease to cats, primarily cytauxzoonosis, ehrlichiosis, and anaplasmosis. Only one R. sanguineus tick was collected from cats, which resonates with other previous studies suggesting that though this species will feed on cats it does so at much lower levels than on dogs (Lappin et al. 2005; Eberhardt et al. 2006). Lower levels of tick infestation on cats compared to dogs in the current study could result from differences in grooming or host preference. In an earlier study in Florida, Akucewich et al. (2002) reported that 2.5 % of feral cats examined were infested with ticks which consisted of two A. americanum, five D. variabilis, one I. scapularis, and one R. sanguineus. In surveys conducted in countries with low R. sanguineus populations such as Germany (Beichel et al. 1996) and Great Britain and Ireland (Ogden et al. 2000), cats were infested with Ixodes spp. only; however, in Japan the most common ticks were Haemaphysalis as well as Ixodes spp. (Shimada et al. 2003). In a recent study on bloodmeal sources of A. americanum in Tennessee, 4/422 ticks were collected from domestic cats. In contrast, in a tropical climate in Brazil, the only ticks
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collected from an urban cat population were R. sanguineus (1.4 %) (Mendes-de-Almeida et al. 2011). Although ticks were obtained from veterinary practices across a variety of ecological regions of Florida in this study, only one-third of Florida counties was represented. Additionally, the veterinary practices participating in the survey did not equally provide submissions to the study, which further geographically biased sample rates for the tick species found in this study. Despite these limitations, however, patterns of geographic distributions of the sampled tick species do emerge. Clearly, R. sanguineus are present throughout the sampled Florida counties and probably the entire state, which reflects that the distribution of this species is known to match the presence of domestic dogs (DantasTorres 2008). Previous studies reported distribution of this tick throughout Florida, however collections were not specifically from dogs (Bishopp and Trembley 1945; Taylor 1951). Previous studies have indicated the scarcity of A. americanum in southern Florida (Bishopp and Trembley 1945; Taylor 1951; Smith 1977; Allan et al. 2001), and no A. americanum was reported in south Florida from the present study. In contrast, I. scapularis were reported from dogs or cats in 7 of the 22 participating counties, yet a previous detailed survey of Florida reported collections of I. scapularis from 57/67 counties with established populations in all regions of the state (Dennis et al. 1998) and previous studies indicated this species throughout the state (Taylor 1951; Smith 1977; Allan et al. 2001). Also in contrast, both A. maculatum and D. variabilis were only reported in 4 and 2 counties, respectively, yet A. maculatum (Bishopp and Trembley 1945) and D. variabilis (Bishopp and Trembley 1945; Taylor 1951; Allan et al. 2001) are present throughout the state, with higher numbers of A. maculatum collected from south Florida compared to northern Florida, and D. variabilis collections in south Florida appearing to be low. In the current study, only R. sanguineus were collected in south Florida, possibly indicating a scarcity of the other tick species, differences in host preference, a lack of overlap of habitat between wild hosts and domestic cats and dogs, or insufficient sampling. Additional studies in south Florida could provide valuable information concerning the presence and distribution of these tick species. Our survey provides valuable data on tick species on domestic dogs and cats throughout the state, which should aid practitioners in their ability to diagnose, treat, and manage tick-borne disease cases and enable them to more effectively advise pet owners on regionally-specific tick prevention measures. Acknowledgments The authors would like to thank participating veterinary practitioners and their staff for tick collection and submission, Merial, Inc., for assistance in distribution of the survey, and Toni McIntosh for her assistance in tick identification.
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Ticks associated with domestic dogs and cats in Florida, USA Jennifer E. Burroughs1,5 • J. Alex Thomasson2 • Rosanna Marsella3 • Ellis C. Greiner1 • Sandra A. Allan4
Received: 15 September 2015 / Accepted: 7 February 2016 Ó Springer International Publishing Switzerland (outside the USA) 2016
Abstract Voluntary collections of ticks from domestic dogs and cats by veterinary practitioners across Florida, USA, were conducted over a 10 month period. Of the 1337 ticks submitted, five species of ixodid ticks were identified and included Rhipicephalus sanguineus, Amblyomma americanum, A. maculatum, Dermacentor variabilis, and Ixodes scapularis. Most ticks were collected from dogs (98.4 %) with the most predominant species being R. sanguineus (94.3 %). Of the ticks collected from cats (1.6 %), A. americanum were the most common (74 %). Only R. sanguineus were collected throughout the state, with the other species collected only in central and north Florida. The tick species collected from dogs and cats represent a risk to these domestic species as well as associated humans for a range of tick-borne diseases in Florida. Keywords
Ticks Dog Cat Rhipicephalus Amblyomma Ixodes Florida
& Sandra A. Allan [email protected] 1
Department of Infectious Diseases and Pathology, College of Veterinary Medicine, University of Florida, Gainesville, FL 32607, USA
2
Field Veterinary Services, Merial Ltd, Duluth, GA 30096, USA
3
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32607, USA
4
Center for Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service (ARS), USDA, Gainesville, FL 32608, USA
5
U.S. Army Medical Command, Carlisle, PA 17013, USA
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Introduction Tick-borne diseases affect numerous dogs and cats in North America each year and many of these diseases are zoonotic. Common bacterial tick-borne diseases include borreliosis, rickettsiosis, ehrlichiosis, and anaplasmosis. Lyme borreliosis is caused by the spirochete Borrelia burgdorferi and most commonly transmitted by Ixodes spp. (Shaw et al. 2001a, b; Fritz and Kjemtrup 2003; Bowman et al. 2009). While clinical disease has been characterized in dogs (Fritz and Kjemtrup 2003), contradictory information exists for clinical symptoms in cats which remain uncharacterized (Shaw et al. 2001a, b; Fritz and Kjemtrup 2003). In a recent national serologic survey, 0.5 % of dogs (256/54,982) examined in Florida were positive for Lyme borreliosis (Bowman et al. 2009). In a study by Little et al. (2014) antibody presence in dogs in the US varied from 0.1 to 5 % depending on county. Exposure of cats to Borrelia in Florida remains unknown. Canine rickettsiosis results from infection with Rickettsia rickettsii primarily transmitted by Dermacentor variabilis and D. andersoni (Shaw et al. 2001a, b) with recent implication of Rhipicephalus sanguineus as a vector in Arizona (Green 2011). Dogs are susceptible to R. rickettsii with clinical disease characterized (Shaw et al. 2001a, b). While cats have been reported with exposure to R. rickettsii (Greene and Breitschwerdt 1998), clinical disease has not been documented (Shaw et al. 2001a, b). Exposure levels of dogs and cats in Florida to Rickettsia remains unclear. Ehrlichiosis may be caused by several species of Ehrlichia with different tick vectors. Dogs are susceptible to infection with Ehrlichia chaffeensis and E. ewingii, both of which are transmitted by Amblyomma americanum (Shaw et al. 2001a, b; Bowman et al. 2009) and with implicated transmission by R. sanguineus (Ndip et al. 2007, 2010). Additionally, R. sanguineus is the main effective vector of E. canis (Shaw et al. 2001a, b). In an extensive serosurvey examining 8662 dog blood samples across southern and central states, an overall seroprevalence of 2.8, 5.1 and 0.8 % was obtained for E. chaffeensis, E. ewingii, and E. canis, respectively (Beall et al. 2012). In Florida, seroprevalence was 1.2, 2.6 and 0.5 % for the three species, respectively. In national serosurveys Bowman et al. (2009) reported that 0.8 % of dog samples from Florida were positive for erhlichiosis and Little et al. (2014) reported 3.2 % seropositive dogs in the southeastern US with counties ranging from 0.1 to over 5 %. While feline ehrlichiosis has been the reported result of infection with Ehrlichia equi (Shaw et al. 2001a, b), E. canis (Breitschwerdt et al. 2001), and E. risticii (Stubbs et al. 1998), several studies (Lappin et al. 2005; Eberhardt et al. 2006) including a recent study on feral cats in Florida, reported no detectable exposure to Ehrlichia spp. (Luria et al. 2004). Anaplasmosis has been reported from both dogs and cats and caused by Anaplasma phagocytophilum transmitted by Ixodes ticks (most commonly Ixodes scapularis and I. pacificus) (Bowman et al. 2009). In a recent serosurvey, 0.5 % of dog blood samples at both a national level and within Florida were positive for exposure to Anaplasma (Bowman et al. 2009). Similar low levels of 0.9 % in southeastern states were reported by Little et al. (2014). While domestic cats can be infected with A. phagocytophilum (Shaw et al. 2001a, b), a recent study examining sera from 553 feral cats in northern Florida revealed no evidence of exposure (Luria et al. 2004). The most common tick-borne protozoan diseases of dogs and cats in North America include babesiosis, cytauxzoonosis, and hepatozoonsis. Babesiosis in dogs in North America is associated with infections with Babesia canis (now considered B. canis voegli (Zahler et al. 1998) and B. gibsoni vectored by R. sanguineus (Shaw et al. 2001a, b; Green
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2011). High levels of infection have been reported in kennels in North Carolina and Florida (Taboada et al. 1991; Kordick et al. 1999). Feline babesiosis in North America has been only reported once from cougars in Florida (Yabsley et al. 2006). Infections of domestic cats with the highly fatal Cytauxzoon felis occurs through tick bites generally from D. variabilis or A. americanum (Blouin et al. 1984; Reichard et al. 2009). These infections often occur in the vicinity of low residential areas in the presence of multiple land use cover types (Reichard et al. 2008). In Florida, bobcats and Florida panthers appear to serve as reservoirs with occasional cases reported from feral and domestic cats (Butt et al. 1991; Rotstein et al. 1999; Yabsley et al. 2006) and serve as hosts for the same tick species (Wehinger et al. 1995). Recent evidence of 6.2 % infection of healthy domestic cats with C. felis in southcentral US states appears to indicate that these chronically infected cats may serve as reservoirs for infection for naı¨ve cats (Rizzi et al. 2015). Hepatozoonosis is a tick-transmitted canine disease caused by ingestion of Hepatozoon americanum –infected Amblyomma maculatum ticks (Shaw et al. 2001a, b). This recently discovered disease is closely associated with the geographic distribution of the tick vector and reported in the southern United States, particularly along the gulf coast (Ewing and Panciera 2003). Clearly, tick-borne diseases could present a significant health risk to small animals in Florida with the zoonotic potential raising additional concern for animal owners. Better knowledge of the distribution of tick species in Florida as well as a clear understanding of the tick-host interaction can provide a foundation for enhanced disease detection and mitigation of risks of infection. A recent survey of feral cats in north central Florida provided some information on the interaction of feral cats and ticks (Akucewich et al. 2002). In this study, ticks were detected on only 5/200 cats with a total of nine ticks recovered. To date, no surveys have been conducted on the presence of ticks on domestic cats or dogs in Florida. To better evaluate the risk of tick borne disease, it is important to know the tick species present in a geographical area. Our objective in this study was to investigate the geographic distribution of tick species found on domestic dogs and cats throughout Florida.
Materials and methods Collections of ticks were obtained on a voluntary basis from veterinary small animal practitioners across Florida, from July 2008 through May 2009. Florida veterinary practices were contacted with a request to participate in the study, and those agreeing to participate were sent collection forms and instructions for submitting tick samples from dog and cat patients brought to the practice during the sample period. The reason for the visit to the practice did not have to be the presence of ticks or tick-borne disease symptoms. Collection forms included questions on the medical history of the animal relevant to tick transmitted diseases, the number of ticks observed during the visit, and whether animals were maintained indoors, outdoors, or both. Ticks received from the participating veterinary practices were sorted by life stage and sex, identified using keys (Keirans and Litwak 1989; Keirans and Durden 1998; Clifford and Anastos 1960), and stored in vials containing 70 % ethanol. Species identification data were reported to the participating practitioners via email or fax.
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Results The survey resulted in 1337 ticks from 189 submissions from veterinary practices. Dogs were hosts for 95.2 % of the submissions and contributed 98.4 % of ticks collected. Cats were hosts for 4.8 % of the submissions and 1.6 % of ticks collected. Five species of ixodid ticks were recovered from dogs and/or cats in this study and included R. sanguineus, A. americanum, A. maculatum, D. variabilis, and I. scapularis (Table 1). Overall, the predominant tick species collected was R. sanguineus (93.0 %) and the least common tick species was A. maculatum (0.3 %). From the collections submitted from dogs, R. sanguineus was the most commonly collected tick species (94.3 %), followed by A. americanum (2.7 %), I. scapularis (1.8 %) and A. maculatum and D. variabilis contributed *1 % of the rest of the collections (Table 1). For dogs, an average of 8.4 R. sanguineus ticks were collected per dog with a maximum of 132 ticks (all adults except one larva) collected on one dog. Average infestations on dogs across all tick species ranged between 2.0 and 2.4 ticks per dogs with a maximum infestation of 8 ticks per dog. The most common tick collected on cats was A. americanum (71 %) (Table 1) and average infestations were 3.7 ticks per cat. The highest infestation was a collection of 11 ticks from a cat that consisted of 9 larvae and 2 nymphs. Only a few cats were infested with I. scapularis and A. americanum (Table 1) with average infestations of 1.2 and 1 tick per cat, respectively. Few immatures were collected by veterinarians which is not atypical of volunteer collections that tend to focus on macroscopic examination and overlook smaller larvae and nymphs (Foldvari and Farkas 2005). Florida has 67 counties of which 22 were represented in the survey (Fig. 1). Of these counties, R. sanguineus were identified from 81.8 % of the counties. Counties reporting ticks other than R. sanguineus had samples of 6 or fewer ticks. Counties comprising over 5 % of the total tick collection included Marion County (41.7 %), Leon County (51.2 %), Brevard County (9.9 %) and Lake County (7.9 %). Several counties (Citrus, Duval, and Flagler) only had one submission. While submissions did not represent all of the counties, R. sanguineus were present throughout the state. Only 47 ticks were collected from south Florida (Miami-Dade, Collier, and Hendry Counties) and these were exclusively R. sanguineus. Of the 121 dogs in the survey, only 44 included information on whether the animal lives inside, outside, or both. Of the dogs reported as inside dogs, 90.9 % were infested with R. sanguineus, 9.0 % A. americanum, and 2.2 % with I. scapularis ticks. Of the dogs described as outdoor dogs, 83 % were infested with R. sanguineus. Of the 15 cats
Table 1 Identification of ticks collected from dogs and cats in Florida Tick species
Number collected (% of total)
Mean number on animal (SE) (range)
Dog
Cat
Dog
Cat
Amblyomma americanum
36 (2.7)
15 (71)
2.2 (0.6) (1–8)
3.7 (2.4) (1–11)
Amblyomma maculatum
4 (0.3)
Dermacentor variabilis
10 (0.8)
Ixodes scapularis
24 (1.8)
5 (24)
2.4 (0.6) (1–7)
Rhipicephalus sanguineus
1242 (94.4)
1 (5)
8.4 (1.5) (1–132)
Total
1316
21
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2.0 (0.0) (2) 2.0 (0.7) (1–5) 1.2 (0.2) (1–2) 1 (0) (1)
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Fig. 1 Map of Florida showing distribution of tick species collected on dogs and cats in the sampled counties
in the survey, only 5 included information on whether they lived indoors, outdoors, or both. Of the 5 cats, one cat with both indoor and outdoor habits was infested with R. sanguineus. Animals with diagnoses or suspected diagnoses of tick-borne disease represented 5.1 % of the submissions. Two dogs, one with a total of 126 R. sanguineus ticks (24 females and 102 males) and the other with a single R. sanguineus tick, were suspected to have tick paralysis. One dog with an attached A. americanum tick tested positive for Ehrlichia and one dog with 3 R. sanguineus ticks tested positive for borreliosis. A cat with 11 A. americanum ticks had a suspected diagnosis of hemobartonellosis.
Discussion In the present study, the majority of ticks submitted from dogs were R. sanguineus (94.3 %), likely reflecting the affinity for this species to infest indoors. Their ability to infest outdoors in warm climates further complicates control efforts (Dantas-Torres 2008,
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Diniz et al. 2010). Conditions supporting development of high R. sanguineus populations in conjunction with high tick and dog contact likely contribute to their widespread presence through Florida. The average infestation level of about 8.4 ticks/dog suggests that infestations are not incidental and are well established. Infestation rates of R. sanguineus on dogs have been reported for Georgia (US) (3.8 ticks/dog, Goldberg et al. 2002), Brazil (5.4, Dantas-Torres et al. 2009), and Italy (39.4, Otranto et al. 2005). The average number of R. sanguineus ticks/dog reported in southeastern Oklahoma and northwestern Arkansas was 53.6 with greatest infestations from July–September (Koch 1982). While infestation levels were not presented, Clark et al. (1996) reported that R. sanguineus was the third most common species collected from dogs in South Carolina. The establishment and maintenance of these tick populations peridomestically (Dantas-Torres et al. 2009) can contribute to sustained populations even in the event of control efforts directed toward dogs and facilities. The presence of insecticide resistance to permethrin and fipronil further complicates effective control of this species (Eiden et al. 2015). High infestation levels of dogs with R. sanguineus presumably increases risk of contracting babesiosis or ehrlichiosis. The other four species collected from dogs, A. americanum, A. maculatum, D. variabilis, and I. scapularis, are relatively common (average of 2.0–2.4 ticks/dog) ticks that live exclusively outdoors and are documented in previous surveys of ticks on wild animals in Florida (Greiner et al. 1984; Forrester et al. 1996; Allan et al. 2001). The presence of these species may reflect risk of ehrlichiosis, babesiosis, Lyme disease, rickettsiosis, anaplasmosis, and hepatozoonosis in dogs. The infestation rates of these four species on dogs in the present study contrast with rates found on dogs in previous studies in southeast US states or neighboring regions. In a survey of ticks infesting dogs in northwestern Georgia, A. americanum and D. variabilis were collected from dogs with a range of 2.1–2.4 ticks per dog (Goldberg et al. 2002). While A. maculatum, I. scapularis, and I. cookei were also collected from dogs, these were collected in low numbers (1–3 ticks per dog) (Goldberg et al. 2002). In Arkansas and Oklahoma, A. americanum were collected at high levels (30.7 ticks/dog) with low numbers of I. scapularis, D. variabilis, A. americanum, and I. cookei also collected (Koch 1982). In contrast to the above studies D. variabilis and A. maculatum were the most common species collected from dogs in South Carolina (Clark et al. 1996). Relatively few tick collections were obtained from cats, suggesting that ticks are not a significant risk for US domestic cats in the sampled region. Of the few ticks identified from cats in the survey, most were A. americanum and I. scapularis, both species found exclusively outside homes and posing a risk of tick-borne disease to cats, primarily cytauxzoonosis, ehrlichiosis, and anaplasmosis. Only one R. sanguineus tick was collected from cats, which resonates with other previous studies suggesting that though this species will feed on cats it does so at much lower levels than on dogs (Lappin et al. 2005; Eberhardt et al. 2006). Lower levels of tick infestation on cats compared to dogs in the current study could result from differences in grooming or host preference. In an earlier study in Florida, Akucewich et al. (2002) reported that 2.5 % of feral cats examined were infested with ticks which consisted of two A. americanum, five D. variabilis, one I. scapularis, and one R. sanguineus. In surveys conducted in countries with low R. sanguineus populations such as Germany (Beichel et al. 1996) and Great Britain and Ireland (Ogden et al. 2000), cats were infested with Ixodes spp. only; however, in Japan the most common ticks were Haemaphysalis as well as Ixodes spp. (Shimada et al. 2003). In a recent study on bloodmeal sources of A. americanum in Tennessee, 4/422 ticks were collected from domestic cats. In contrast, in a tropical climate in Brazil, the only ticks
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collected from an urban cat population were R. sanguineus (1.4 %) (Mendes-de-Almeida et al. 2011). Although ticks were obtained from veterinary practices across a variety of ecological regions of Florida in this study, only one-third of Florida counties was represented. Additionally, the veterinary practices participating in the survey did not equally provide submissions to the study, which further geographically biased sample rates for the tick species found in this study. Despite these limitations, however, patterns of geographic distributions of the sampled tick species do emerge. Clearly, R. sanguineus are present throughout the sampled Florida counties and probably the entire state, which reflects that the distribution of this species is known to match the presence of domestic dogs (DantasTorres 2008). Previous studies reported distribution of this tick throughout Florida, however collections were not specifically from dogs (Bishopp and Trembley 1945; Taylor 1951). Previous studies have indicated the scarcity of A. americanum in southern Florida (Bishopp and Trembley 1945; Taylor 1951; Smith 1977; Allan et al. 2001), and no A. americanum was reported in south Florida from the present study. In contrast, I. scapularis were reported from dogs or cats in 7 of the 22 participating counties, yet a previous detailed survey of Florida reported collections of I. scapularis from 57/67 counties with established populations in all regions of the state (Dennis et al. 1998) and previous studies indicated this species throughout the state (Taylor 1951; Smith 1977; Allan et al. 2001). Also in contrast, both A. maculatum and D. variabilis were only reported in 4 and 2 counties, respectively, yet A. maculatum (Bishopp and Trembley 1945) and D. variabilis (Bishopp and Trembley 1945; Taylor 1951; Allan et al. 2001) are present throughout the state, with higher numbers of A. maculatum collected from south Florida compared to northern Florida, and D. variabilis collections in south Florida appearing to be low. In the current study, only R. sanguineus were collected in south Florida, possibly indicating a scarcity of the other tick species, differences in host preference, a lack of overlap of habitat between wild hosts and domestic cats and dogs, or insufficient sampling. Additional studies in south Florida could provide valuable information concerning the presence and distribution of these tick species. Our survey provides valuable data on tick species on domestic dogs and cats throughout the state, which should aid practitioners in their ability to diagnose, treat, and manage tick-borne disease cases and enable them to more effectively advise pet owners on regionally-specific tick prevention measures. Acknowledgments The authors would like to thank participating veterinary practitioners and their staff for tick collection and submission, Merial, Inc., for assistance in distribution of the survey, and Toni McIntosh for her assistance in tick identification.
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