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Veterinary Parasitology
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Raquel Sobrino a , Javier Millán b , Álvaro Oleaga c , Christian Gortázar c , José de la Fuente c,d , Francisco Ruiz-Fons c,∗ a
Università degli Studio di Torino, Facoltà di Medicina Veterinária, Dipartimento di Produzioni Animali, Epidemiologia ed Ecologia, Vía L. Da Vinci, 44,
Q2 Grugliasco, Torino, Italy
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b Servei d‘Ecopatologia de Fauna Salvatge (SEFaS) (Wildlife Diseases Research Group), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain c Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Animal Health Dept., Ronda de Toledo s/n, 13005 Ciudad Real, Spain d Dept. of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, USA
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Article history: Received 30 June 2011 Received in revised form 26 August 2011 Accepted 5 September 2011
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Keywords: Behaviour Climate Ecology Endophilic Exophilic Mediterranean Tick
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Ticks parasitizing wild carnivores and the tick-borne pathogens (TBPs) that they transmit may affect domestic carnivores and humans. Thus, investigating the role of wild carnivores as tick hosts is of relevance for understanding the life cycle of ticks in natural foci and the epidemiology of TBPs shared with domestic animals and humans. Therefore, the main objective of this study was to determine the ixodid tick fauna of wild carnivores in Peninsular Spain and the environmental factors driving the risk of wild carnivores to be parasitized by ixodid ticks. We hypothesized that the adaptation of tick species to differing climatic conditions may be reflected in a similar parasitization risk of wild carnivores by ticks between bioclimatic regions in our study area. To test this, we surveyed ixodid ticks in wild carnivores in oceanic, continental-Mediterranean, and thermo-Mediterranean bioclimatic regions of Peninsular Spain. We analyzed the influence of environmental factors on the risk of wild carnivores to be parasitized by ticks by performing logistic regression models. Models were separately performed for exophilic and endophilic ticks under the expected differing influence of environmental conditions on their life cycle. We found differences in the composition of the tick community parasitizing wild carnivores from different bioclimatic regions. Modelling results partially confirmed our null hypothesis because bioclimatic region was not a relevant factor influencing the risk of wild carnivores to be parasitized by exophilic ticks. Bioclimatic region was however a factor driving the risk of wild carnivores to be parasitized by endophilic ticks. Spanish wild carnivores are hosts to a relevant number of tick species, some of them being potential vectors of pathogens causing serious animal and human diseases. Information provided herein can be of help to understand tick ecology in Spanish wildlife, the epidemiology of tick-borne diseases, and to prevent the risks of TBPs for wildlife, domestic animals, and humans. © 2011 Published by Elsevier B.V.
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Ecological preferences of exophilic and endophilic ticks (Acari: Ixodidae) parasitizing wild carnivores in the Iberian Peninsula
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∗ Corresponding author. Tel.: +34 926295450; fax: +34 926295451. E-mail addresses:
[email protected],
[email protected] (F. Ruiz-Fons).
1. Introduction
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Ticks are obligate blood-sucking arthropods that parasitize vertebrates worldwide (Sonenshine et al., 2002). As a consequence of their blood-feeding lifestyle, ticks are able to get infected, replicate, and maintain active
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0304-4017/$ – see front matter © 2011 Published by Elsevier B.V. doi:10.1016/j.vetpar.2011.09.003
Please cite this article in press as: Sobrino, R., et al., Ecological preferences of exophilic and endophilic ticks (Acari: Ixodidae) parasitizing wild carnivores in the Iberian Peninsula. Vet. Parasitol. (2011), doi:10.1016/j.vetpar.2011.09.003
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in the family Ixodidae – those of interest in this work – may follow both strategies. Many ixodid ticks follow only exophilic or endophilic strategies across their complete life-cycle, but some exophilic species may follow a pseudo-endophilic strategy because particular instars of the species remain on the host for more than one developmental stage (Klompen, 2005). As an example, some species in the genera Hyalomma, Rhipicephalus, and Dermacentor quest as larvae and adults in the vegetation looking for hosts while nymphs remain in the host (two-host cycle). As a consequence, endophilic and exophilic ticks differ in their exposure to environmental conditions due to their differing host-seeking behaviour. While endophilic ticks remain better protected from environmental changes and hosts are easily accessible, exophilic ticks are highly exposed to environmental conditions and the accessibility to the host is also dependent on host ecology and population dynamics (Wilson et al., 1990; Ruiz-Fons and Gilbert, 2010). Additionally, the ecology of certain tick species is influenced by climatic and meteorological conditions (Sonenshine, 1993) and by host population and host individual factors such as host abundance, host community composition, sex, age, and physical condition as well (LoGiudice et al., 2008; Alzaga et al., 2009; Vor et al., 2010). Most wild carnivores are widely distributed in Spain (Palomo et al., 2007) and they occupy from natural to humanized biotopes (Palomo and Gisbert, 2002). Wild and domestic carnivores may be parasitized by the same tick species and wild species such as the red fox (Vulpes vulpes) are peridomestic animals (Palomo and Gisbert, 2002) increasing the risk of indirect contacts with domestic animals through ticks. This wildlife–domestic connection may have consequences for human health as many pathogens shared by foxes and dogs may be transmitted to humans (Márquez and Millán, 2009). Information on the ticks parasitizing wild carnivores in Spain is scarce and most of the Spanish mainland has not been surveyed before, especially most of the Atlantic regions and continental inner areas of mainland Spain. Wild carnivores in Spain have been found to host different endophilic species such as Ixodes hexagonus, Ixodes canisuga, Ixodes trianguliceps, Ixodes ventalloi, Riphicephalus sanguineus, Riphicephalus pusillus, Haemaphysalis hispanica and exophilic ticks such as I. ricinus, Haemaphysalis punctata, Haemaphysalis concinna, Riphicephalus turanicus, Hyalomma spp., and adult Dermacentor reticulatus (Encinas Grandes, 1986; Domínguez, 2004; Martínez- Q3 Carrasco et al., 2007; Millán et al., 2007; Gerrikagoitia, 2010). Q4 The important gap in the knowledge about ticks parasitizing wild carnivores in some areas of their distribution in Spain led us to this study. We hypothesize that in spite of big climatic variations across different bioclimatic areas in mainland Spain, the risk of animals to be parasitized by ticks would remain constant due to adaptations of the different tick species present in these areas to the predominant environmental conditions. This study adds information on the distribution, host range, and life-cycle of ixodid ticks in the Iberian Peninsula.
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pathogens that can be later transmitted to susceptible vertebrate hosts. Ticks are vectors of a wide range of pathogens such as viruses, bacteria, and protozoa that cause diseases to humans and animals (Sonenshine et al., 2002; Jongejan and Uilenberg, 2004). Tick-borne pathogens (TBPs) life cycle is highly dependent on tick ecology which is one of the most important factors driving the epidemiology of tick-borne diseases (Randolph, 2009). Most of the emergent tick-borne diseases in the world emerge from the wild reservoir (Daszak et al., 2001). Thus, preventing emergence of tick-borne diseases includes determining the role of wildlife as tick hosts and their role in the life cycle of TBPs. Some tick species may be generalists and may feed on different vertebrate species depending on their availability and abundance (Wilson et al., 1984) whereas other species may be more specific and use a narrow host range (Sonenshine et al., 2002). Many ticks parasitize domestic animals but few ticks feed exclusively on them and most tick species may also parasitize wild animals. Wild and domestic cycles are often complementary. Immature tick stages that parasitize wild and peridomestic animals can feed later as adults on domestic animals. Thus, investigating the role of wildlife species as tick hosts is of great relevance for understanding the life cycle of ticks and the epidemiology of tick-borne diseases shared with domestic animals and humans (Ruiz-Fons et al., 2006; Ruiz-Fons and Gilbert, 2010). Among the wide range of wildlife hosts of ticks, wild carnivores are important hosts to endophilic ixodid ticks because they spend many daily hours in burrows, nests or caves where ticks remain active. Wild carnivores are also hosts for some instars of exophilic tick species such as larvae and nymphs of Ixodes ricinus (Santos-Silva et al., in press). I. ricinus is the main European vector of Borrelia burgdorferi sensu lato – the causal agent of Lyme disease – for which wild carnivores are good sentinels (Sobrino and Gortázar, 2008). Another important group of pathogens transmitted by ticks hosted by carnivores is the order Rickettsiales. In Spain, Rickettsia monacensis, Rickettsia helvetica, and Rickettsia massiliae have been recently detected in wild carnivores (Márquez and Millán, 2009), all of them with demonstrated zoonotic character (Parola et al., 2005). Anaplasma phagocytophilum and Ehrlichia spp. have also been detected by molecular and serological techniques in European wild carnivores (Petrovec et al., 2002; Ryser-Degiorgis et al., 2005; Millán et al., 2009). Nonetheless, the role of wild carnivores in the epidemiology of Rickettsia spp., A. phagocytophilum, and other TBPs such as Ehrlichia canis and A. platys is poorly understood. Across their evolutionary history, ticks have diversified from their ancestors allowing them to colonize very different biotopes, adapting their life cycle to the environment (Black and Kondratieff, 2004). Ticks have developed two different feeding strategies, an endophilic strategy in which ticks adopt a nidicolous lifestyle remaining in burrows, nests, hollows or craks near resting or breeding places of hosts, and an exophilic strategy in which ticks must search for their hosts. Ticks in the family Argasidae follow an endophilic strategy whereas ticks
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2.2. Study areas
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Due to the opportunistic nature of the data collected due to difficulties in sampling wild carnivores in such a wide land surface (Sobrino and Gortázar, 2008), sampling sites were grouped into three main biogeographic areas (Fig. 1) according to gross climatic differences: (i) an Atlantic area in the northern third of mainland Spain; (ii) a continental-Mediterranean area in inland Spain; and (iii) a thermo-Mediterranean area in the south-west coast of Spain. The Atlantic area is dominated by an oceanic climate with year-round persistent rains (above 1000 mm), mild winters and slightly warm summers. The continental area is under the Mediterranean influence but characterized by extreme weather conditions with cold winters and very hot summers. Rains range 300–800 mm annually and are under a Mediterranean influence and thus highly seasonal – concentrated mainly in autumn and spring. The thermo-Mediterranean area is characterized by mild winters and hot summers with also a Mediterranean influence on rains (ranging 700–1000 mm in a year). Red foxes, genets, polecats, and European badgers were surveyed in the three bioclimatic areas. Iberian wolves, pine martens, the stoat, and the weasel were collected only in Atlantic areas. Finally, stone martens and wild cats were collected only from the Atlantic and continentalMediterranean regions meanwhile Egyptian mongooses were only surveyed in the continental-Mediterranean and thermo-Mediterranean regions.
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2. Material and methods
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2.1. Sampling wild carnivores and ticks
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Two hundred and four wild carnivores were surveyed for ticks from 2003 to 2010 in different geographic areas in mainland Spain (Fig. 1). Our survey approach was based on the collection of ticks on experimentally live-trapped wild carnivores and the collection of wild carnivore carcasses, both animals shot (red fox (V. vulpes) by hunters and Iberian wolf (Canis lupus signatus) by gamekeepers) or found dead. A total of 88 red foxes, 14 Iberian wolves, 15 stone martens (Martes foina), eight pine martens (Martes martes), 17 common genets (Genetta genetta), 26 Eurasian badgers (Meles meles), 23 Egyptian mongooses (Herpestes ichneumon), seven polecats (Mustela putorius), one stoat (Mustela erminea), one weasel (Mustela nivalis) and four wildcats (Felis silvestris) were surveyed for ticks. Live animals were anesthetized before inspection according to the protocol reported elsewhere (Millán et al., 2007). Live carnivores were visually inspected for tick detection and ticks were collected in tubes containing 70% ethanol. Shot carnivores were preserved in sealed plastic bags and transported to the laboratory. Sealed plastic bags impeded ticks detaching from the carcass to escape. Animals found dead were also transported to the laboratory in sealed plastic bags. Dead animals and container plastic bags were thoroughly inspected in the laboratory for ticks. Sampled animals were sexed and age was estimated by dentition and size (Saénz de Buruaga et al., 1991). Date of collection was recorded from several animals although it was not available for most of them (64.7%). Every tick collected from dead animals was stored at −20 ◦ C Q5 until identification (Gil Collado et al., 1979; Manilla, 1998; ˜ et al., 2004b). Some immature ticks could not Estrada-Pena be identified to species level due to the damage suffered during collection. Description of ticks collected in wild carnivores from southern Spain has been formerly reported
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Fig. 1. Map of Peninsular Spain showing the bioclimatic areas where the wild carnivore survey for ticks was carried out (A: Atlantic bioclimatic area; C: continental-Mediterranean bioclimatic area, and T: thermoMediterranean bioclimatic area).
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(Millán et al., 2007) and these data were herein used only to test the influence of environmental factors on tick prevalence. Each tick was classified according to its behavioural pattern in two classes: exophilic and endophilic. As different stages of the same tick species may show variations in their feeding strategy, the classification of ticks as exophilic or endophilic was done at the developmental stage level. By doing this, those stages of exophilic ticks that remained on the host after feeding and molting were considered as endophilic. We classified as exophilic every stage in the species I. ricinus and adult Hyalomma marginatum, Riphicephalus bursa, R. turanicus, and D. reticulatus. Every stage of I. ricinus is known to quest in the vegetation (e.g., RuizFons and Gilbert, 2010) and adult Hyalomma marginatum and R. turanicus are usually found parasitizing ungulates on which no immature stages are found (Pegram et al., 1987; Ruiz-Fons et al., 2006). Adult D. reticulatus and R. bursa ticks are frequently collected from the vegetation (Bullová et al., 2009; the authors, unpublished). Every stage in the species R. sanguineus, R. pusillus, I. hexagonus, I. canisuga, and I. ventalloi were considered as endophilic as they are not commonly found questing in the vegetation in our study areas (unpublished results). R. sanguineus can be occasionally collected outside houses, cracks or crevices (Barandika et al., 2006; Ruiz-Fons et al., 2006) but it is considered a true endophilic species (Danta-Torres, 2010). In contrast, R. turanicus frequently parasitizes ungulates ˜ et al., 2004a), which suggests an endophilic (Estrada-Pena behaviour.
Please cite this article in press as: Sobrino, R., et al., Ecological preferences of exophilic and endophilic ticks (Acari: Ixodidae) parasitizing wild carnivores in the Iberian Peninsula. Vet. Parasitol. (2011), doi:10.1016/j.vetpar.2011.09.003
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We wanted to test the hypothesis that the risk of wild carnivores to be parasitized by ticks would remain constant across bioclimatic area in spite of the differences in the composition of the community of ticks in these areas. For this purpose, every sampled animal was categorized according to the presence/absence (0 and 1, respectively) of exophilic and endophilic ticks. Using sampled wild carnivores in which every data of interest in the statistical approach was collected (n = 138), we performed logistic binomial regression (binomial distribution and logistic link function) considering the presence/absence of ticks as the response variable and sampling area (categorical, three classes; Fig. 1), season (categorical, four classes) and the interactions between taxonomic family and area and taxonomic family and season as environmental predictor variables. Sampling area was considered as a proxy of the predominant macroclimatic conditions, season as a proxy of tick activity and interactions of taxonomic family with area and season as a proxy of eco-environmental features of individuals influencing exposure to ticks. We measured the proportion of individuals sampled after being trapped or surveyed immediately after being hunted and the proportion of individuals found dead in each taxonomic family. We found statistically significant differences between taxonomic families (Chi-square = 27.3, df = 3, p < 0.001) and this was the reason for not considering this variable as a pure effect in the models. We assumed the influence of environmental factors on the prevalence of ticks in wild carnivores would vary according to their host-seeking behaviour, being exophilic ticks more exposed to the environment than endophilic ones. Therefore logistic models were performed for exophilic and endophilic ticks in separate. For details about the modelling approach see Ruiz-Fons et al. (2008). We studied the particular case of the red fox separately from the rest of wild carnivores because red fox is the most abundant wild carnivore in Spain and thus accounted for the majority of our samples (Palomo et al., 2007). We aimed to test in foxes the same hypothesis tested
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3. Results
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A total of 475 ixodid ticks were collected during the sampled period (393 adults and 82 immatures) in the three bioclimatic areas. No ticks were collected from the stoat, weasel, polecats, and pine martens surveyed. Forty-five of 88 red foxes (51.1 ± 10.4%), 13 of 14 Iberian wolves (92.9 ± 13.5%), 9 of 26 European badgers (34.6 ± 18.3%), 12 of 23 Egyptian mongooses (52.2 ± 13.4%), 3 of 15 stone martens (20 ± 20.2%), 1 of 4 wild cats (25 ± 42.4%), and 3 of 17 genets (17.7 ± 18.1%) were parasitized by ticks. Species of ticks identified in the different bioclimatic areas by carnivore species are shown in Table 1. I. ricinus was the predominant species in wild carnivores from Atlantic areas, where it was detected in almost every sampling site. I. ricinus was rarely found in Mediterranean areas where it was present only in a reduced number of sites. I. canisuga and D. reticulatus were found only in Atlantic areas. I. hexagonus was together with I. ricinus the most distributed tick species in the different bioclimatic areas (Table 1). We collected mainly adult stages of I. hexagonus and a small number of nymphs. In contrast, R. pusillus, R. sanguineus, R. turanicus, and R. bursa were found in carnivores from Mediterranean areas but not in Atlantic areas (Table 1). I. ventalloi was collected only in wild carnivores from thermo-Mediterranean areas. Ticks of the genus Hyalomma were collected in Mediterranean areas in low numbers while they were not collected in Atlantic areas. The prevalence of exophilic and endophilic ticks in the examined wild carnivores was 19.1 ± 5.2% and 29.4 ± 6.1% respectively. Twenty-six (29.5 ± 9.2%) and 29 (32.9 ± 9.8%)
Table 1 Tick species and developmental stages parasitizing wild carnivores through host species and bioclimatic area. Host
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for the entire carnivore taxa surveyed. Therefore, logistic binomial regression was performed with bioclimatic area, season and two additional host individual variables, sex and age. The interaction between sex and age was also considered in the models. Model performance followed the same approach described above. Statistical uncertainty of the calculated tick prevalences was assessed by calculating the 95% confidence interval for each of the proportions according to the expression C.I.95% = 1.96[p(1 − p)/n]1/2 .
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2.3. Statistical analyses
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Iberian wolf (Canis lupus signatus) Red fox (Vulpes vulpes)
Stone marten (Martes foina)
European badger (Meles meles) Genet (Genetta genetta)
Wild cat (Felis silvestris) Egyptian mongoose (Herpestes ichneumon)
Bioclimatic area (No. of parasitized)
Tick species and stages
Atlantic (13) Atlantic (6) Continental (11) Thermo-Mediterranean (19)a Continental (2) Atlantic (3) Continental (5) Thermo-Mediterranean (1)a Continental (1) Thermo-Mediterranean (2)a Continental (1) Continental (1) Thermo-Mediterranean (10)a
Ir (A), I. spp. (A, N), Dr (A) Ir (A), Ih (A, N), Ic (A), I. spp. (A, N), Dr (A) Ir (A, N, L), Ih (A), I. spp. (A, N), Hm (A), Hy. spp. (N), Rs (A), Rp (A) Ir (A), Iv (A), Rp (A), Rt (A), R. spp. (A) Ih (N), R. spp. (A) Ir (A), Ih (A), Dr (A) Ih (A), Ic (A), I. spp. (N), Rs (A), Rb (A) Rp (A) I. spp. (L) I. spp. (N), Rp (A) Rs (A), Rp (A) Ih (A) Ih (A), Iv (A), I. spp. (A, N), Hy. spp. (A), Rp (A), Rt (A), R. spp. (A)
Abbreviations: Ir: Ixodes ricinus; Ih: I. hexagonus; Ic: I. canisuga; Iv: I. ventalloi; I. spp.: Ixodes genus; Hm: Hyalomma marginatum; Hy. spp.: Hyalomma genus; Rb: Rhipicephalus bursa; Rs: R. sanguineus; Rp: R. pusillus; Rt: R. turanicus; R. spp.: Rhipicephalus genus; Dr: Dermacentor reticulatus; A: adult; N: nymph; L: larva. a Information reported by Millán et al. (2007).
Please cite this article in press as: Sobrino, R., et al., Ecological preferences of exophilic and endophilic ticks (Acari: Ixodidae) parasitizing wild carnivores in the Iberian Peninsula. Vet. Parasitol. (2011), doi:10.1016/j.vetpar.2011.09.003
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To the best of our knowledge this is the first study addressing the ecological determinants of ticks parasitizing wild carnivores in Spain according to their different
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4.1. Methodological considerations
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Ticks are expected to detach from animals after death in a variable time lapse. Shot animals were collected immediately after death and ticks had no chance to escape from the sealed plastic bag in which they were placed. The rest of carnivore carcasses surveyed were collected after being found death. Hence, we ignore the time between death and sampling. We only selected those animals whose condition was good enough to be necropsied, normally before 24 h after death. Thus, in order to avoid any confusing effect of the sampling approach on our findings, we estimated the percentage of animals properly sampled for ticks and those found dead in any of the surveyed regions, season, and families. There were no statistically significant (Chi-square = 1.4, df = 2, p > 0.05) differences in the proportion of animals sampled alive or immediately after death between bioclimatic areas (27.3%, 29.6%, and 37.3% in Atlantic, continental-Mediterranean, and thermoMediterranean bioclimatic areas, respectively) and this pattern was similar for the different seasons (data not shown). We expected a lower influence of climatic conditions on endophilic than on exophilic ticks due to the buffering microclimate provided by nests, burrows, caves or crevices which endophilic ticks inhabit. However, endophilic tick activity is influenced by the predominant climatic conditions such as seasonal changes in temperature and ˜ et al., 1992) and season may hence humidity (Estrada-Pena influence its prevalence on hosts as well. This gross classification does not consider particular differences within endophilic or exophilic tick species. A good example of
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life cycles, contributing to our knowledge on the ecology of ticks in wildlife in the Iberian Peninsula. Our hypothesis was partially confirmed as no statistically significant differences in the prevalence throughout bioclimatic areas were evidenced for exophilic ticks. However, the prevalence of endophilic ticks statistically differed between bioclimatic areas, suggesting the influence of macroclimatic conditions on the risk of wild carnivores to be parasitized by endophilic ticks. This finding may nonetheless be modulated by tick host population dynamics that may vary between the considered bioclimatic areas. Thus, confirming the effect of climate would need further research. Our results are a preliminary approach to understand the epidemiology of tick-borne pathogens transmitted by the tick species that parasitize wild carnivores.
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of 88 red foxes, 6 (42.8 ± 25.4%) and 8 (57.1 ± 25.4) of 14 Iberian wolves, 3 (11.5 ± 12.1) and 7 (26.9 ± 16.8%) of 26 European badgers, 4 (17.3 ± 15.2%) and 10 (43.4 ± 19.6%) of 23 Egyptian mongooses, 0 and 3 (17.6 ± 17.4%) of 17 genets, 0 and 2 (13.3 ± 17.1%) of 15 stone martens and 0 and 1 (25 ± 41.9%) of 4 wild cats were parasitized by exophilic and endophilic ticks, respectively. The best model showed that none of the variables had a statistically significant influence on the risk of wild carnivores to be parasitized by exophilic ticks (Table 2). Nonetheless, we observed that the risk of wild carnivores to be parasitized by exophilic ticks in thermo-Mediterranean areas was three times higher (31.3 ± 11.1%, n = 67) than in the rest of the areas (11.4 ± 9.4%, n = 44; and 7.4 ± 9.8%, n = 27 for Atlantic and continental areas, respectively). Prevalence of exophilic ticks peaked in summer in Atlantic and continental areas while the peak in the thermoMediterranean area took place in spring (Table 3). The final model for endophilic ticks showed a statistically significant influence of bioclimatic area and season on the risk of wild carnivores to be parasitized (Table 2). The prevalence in continental areas was higher than that found in Atlantic and thermo-Mediterranean areas (Table 3). Prevalence was observed to peak in spring (44.2 ± 13.4%, n = 52) meanwhile lower prevalence values were observed in summer (18.2 ± 16.1%, n = 22), autumn (19.0 ± 16.7%, n = 21) and winter (18.6 ± 11.6%, n = 43). Prevalence peaked in spring in the three bioclimatic areas (Table 3). None of the factors considered was statistically significant in the final models for endophilic and exophilic ticks in foxes. However, we observed differences in the prevalence in the thermo-Mediterranean area (51.5 ± 17.1%, n = 33) and in the Atlantic area (7.1 ± 13.4%, n = 14). The prevalence peaked in spring in thermo-Mediterranean areas while it peaked in summer in Atlantic areas. In the case of endophilic ticks, the final model also showed that none of the considered factors influenced the risk of foxes to be parasitized. However, the prevalence was also higher in thermo-Mediterranean (27.3 ± 15.2%, n = 33) than in Atlantic (14.3 ± 18.3%, n = 14) areas and the prevalence peaked in spring in both thermo-Mediterranean and Atlantic areas.
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Table 2 Model statistics (Wald Chi-square statistic value, degrees of freedom (df) and the P-value) for the final binomial regression models (binomial distribution and a logistic link function) of endophilic and exophilic ticks. Models were carried in a separate way for of all of the carnivores surveyed and for red foxes only. Host
Tick class Exophilic
Wild carnivores
Endophilic
Red fox
Exophilic Endophilic
Variable
Wald
Intercept Family × Season Intercept Area Season
0.000 13.59 18.77 17.89 9.89
Intercept Intercept
3.81 12.12
df 1 16 1 2 3 1 1
P-value 0.999 0.629
