Vulpes vulpes, Linnaeus, 1758

Holland, Celia V., 2023, A walk on the wild side: A review of the epidemiology of Toxocara canis and Toxocara cati in wild hosts, International Journal for Parasitology: Parasites and Wildlife 22, pp. 216-228 : 217-220

2.1. Red fox ( Vulpes vulpes )

A total of 10 species of fox are listed in Table 1 as hosts of T. canis detected by either eggs, worms or both. This group of hosts are, therefore, the most frequently listed in Table S1. These are Red fox ( Vulpes vulpes ), Arctic fox ( Vulpes lagopus ) (Myˇskova´et al., 2019), Swift fox ( Vulpes velox ) (Criffield et al., 2009), Darwin’ s fox ( Lycalopex fulvipes ) (Jim´enez et al., 2012), Japanese red fox ( Vulpes vulpes japonica ) (Sato et al., 1999), Kit fox ( Vulpes macrotis ) (Ubelaker et al., 2014), Andean fox ( Lycalopex culpaeus ) (Vega et al., 2021), Pampas fox ( Lycalopex gymnocercus ) ( Moleon et al., 2015), Crab-eating fox (Cerdocyonthous cerdocyon) (Santos et al., 2012) and Gray fox ( Urocyon cinereoargenteus ) (Hern´andez-Camacho et al., 2011).

As a definitive host of T. canis , the red fox has received the most attention in the published literature. Red foxes are the most widespread wild carnivores in the world. They are highly adaptable to a range of habitats due to their opportunistic feeding behaviour and are found in almost all regions of the northern hemisphere ( Hoffmann and Sillero-Zubiri, 2016). Red fox density has increased in many European countries, a trend that is attributable principally to the impact of a successful rabies vaccination campaign of wild animals, an increase in anthropogenic food sources, and the impact of environmental factors ( Gloor et al., 2001).

Factors that influence the importance of red foxes as sources of pathogen spillover, include the increased population density of foxes, their susceptibility to pathogens that can also infect domestic animals and humans (such as T. canis ), their hunting preference for small

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mammals and their wide distribution and close proximity to human settlements ( Duscher et al., 2015). In peri-urban and urban areas of Estonia, Plumer et al. (2014) detailed how contact between red foxes, pets and humans has changed from sporadic to constant, thereby enhancing the risk of successful parasite transmission. Otranto et al. (2015) have emphasised how the predominance of small mammals and birds in the diet of red foxes, all of which may act as paratenic hosts for Toxocara spp. , may impact upon the epidemiology of T. canis .

Publications from 31 countries, published between 1973 and 2022, are listed in Table 2 and full details of each paper surveyed are included in Table S1. Unlike some other wild hosts, prevalences in red foxes have fluctuated quite considerably with values as low as 4% in Spain (Criado-Fornelio et al., 2000) (but with two other studies recording prevalences of 23% and 45% respectively) to as high as 74% in the Netherlands (Borgsteede, 1984). However, the majority of studies record moderate to high prevalences. Even within a single country, prevalences can fluctuate quite markedly. For example, three Canadian studies recorded prevalences of 11, 25 and 70% respectively. In terms of abundance, an epidemiologically more robust measure of helminth population dynamics, figures rarely exceed an average of 10 with the exception of studies by Willingham et al. (1996) from Denmark (17.1) and a Polish study by Tylkowska et al. (2021) (12.1). Ranges and values of k demonstrate aggregation with several concordant values of 0.2 (see Table 2).

A number of studies have compared the efficacy of detection using egg counts versus worm counts and not surprisingly, have demonstrated the reduced efficacy of egg counts as a measure of prevalence. For example, Martinez-Carrasco et al. (2007) recorded prevalences of 12.5% by egg count versus 45.5% by worm count and Saeed and Kapel (2006) recorded prevalence based on eggs as 41%, but that based on worms as 76%. In a recent comprehensive study, Marchiori et al. (2023) compared copromiscroscopy utilising a classical flotation technique (FT) using a zinc chloride solution to a scraping filtration and counting technique (SFCT) in 150 red foxes from Poland. Both T. canis and Toxascaris leonina were combined as ascarids in their analysis. Concordance values were 62.7% and sensitivity was 36.3% but increased to 46.1% after the exclusion of single-sex infections and infections solely by immature worms.

In a novel approach based on a large sample of Polish red foxes, Tylkowska et al. (2021) divided the intestine into three sections and found a statistically significantly lower prevalence in the ileum (10.3%)

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versus the duodenum (20.7%) and the jejunum (26%) based upon worm counts at autopsy.

Several studies have provided particularly comprehensive data sets on the epidemiology of T. canis in red foxes. Richards et al. (1993) recorded higher prevalences of T. canis among male versus female red foxes and juvenile versus adult red foxes. Aggregation was pronounced with k values of 0.328 in males and 0.223 in females and variance to mean ratios of 16.03 and 14.26 respectively. In Denmark, Saeed et al., (2006) recorded a high prevalence of 59% among over 1000 red foxes. Mirroring the results of Richards and colleagues, prevalence and abundance of T. canis was higher in male versus females red foxes and in cubs versus older animals. In addition, T. canis was more prevalent and abundant in red foxes sampled from rural versus urban areas. In a very detailed study that included an analysis of worm fecundity, Saeed and Kapel, 2006 revealed that female worm fecundity was lower in female compared to male red foxes, higher in cubs versus young and adults and higher in summer compared to other seasons. In an extensive study of over 600 red foxes from Northern Italy, Di Cerbo et al. (2008) explored the contribution of environmental variables and the structure of the red fox population on the composition of the intestinal helminth community. With a prevalence of 54.4% and a mean abundance of 9.3 worms, T. canis was a dominant parasite that was geographically widespread and abundant. Prevalence and abundance of T. canis demonstrated high spatial variability with a peak prevalence and abundance of 71% and 10.4 respectively in the Aosta region.

In Switzerland, Koller et al. (2019) employed a standardised sampling scheme based on the collection of red fox faecal samples along transects in 1-km 2 grid cells dispersed over the whole country and found that the prevalence of T. canis was significantly lower south of the Alps. The authors advocated the use of such a standardized method, that allows for follow-up surveys of red fox scats without culling interventions, a useful procedure for assessing and monitoring on a large scale and over time the infection pressure on dog populations.

In Australia, the red fox is an invasive species (Bezerra-Santos et al., 2023) that was introduced for sport and to control rabbits ( Mackenstedt et al., 2015). Australian red foxes are now known to be infected with T. canis as shown by Dybing et al. (2013) who recorded a prevalence of 15% in 147 foxes sampled. In contrast to many other parts of the world, T. canis in domestic dogs is more effectively controlled in Australia (Thompson, 2023) and environmental contamination is low (see Massetti et al., 2022). The red fox is now considered to be a potentially important reservoir that may contribute to spillover of infection to both domestic dogs and humans (Bezerra-Santos et al., 2023).

To conclude, the wide distribution of red foxes coupled with their ecological plasticity enabling them to live successfully in a variety of contrasting environments, enhances their importance as potential transmitters of T. canis to both domestic dogs and humans. Clearly further studies are needed, that incorporate the one health approach, in order to successfully implement surveillance and risk assessment of wildlife parasite spillover (Waindock et al., 2021).