Carnivora, Bowdich, 1821

Seguel, Mauricio & Gottdenker, Nicole, 2017, The diversity and impact of hookworm infections in wildlife, International Journal for Parasitology: Parasites and Wildlife 6 (3), pp. 177-194 : 179-185

4.1. Carnivora

4.1.1. Canidae

Nine hookworm species have been described in canids, all of them members of the Ancylostoma , Uncinaria and Arthrostoma genera ( Table 1). Among canids, the best studied species are the red fox ( Vulpes vulpes ) and coyotes ( Canis latrans ), probably related to their widespread distribution and because they are commonly hunted/culled.

In Asia, the native hookworms Arthrostoma miyazakiense and Ancylostoma kusimaense are the most common gastrointestinal nematodes of native (raccoon dogs, Nyctereutes procyonoides ) and introduced canids (red foxes) (Sato et al., 2006; Shin et al., 2007). Interestingly, introduced raccoon dogs in Denmark lack their native Asian hookworms but are infected with U. stenocephala (48.5% prevalence), a very common parasite of red foxes in that region ( Al-Sabi et al., 2013), highlighting the potential of canine hookworms to infect multiple species (see Table 1).

Many common canine hookworms such U. stenocephala , A. caninum and A. ceylanicum are important zoonotic pathogens, especially in Australia and Southeast Asia ( Smout et al., 2013).

4.1.2. Felidae

Twelve species of hookworms within the Ancylostoma , Uncinaria , Galoncus and Arthrostoma genera have been described in wild felids ( Table 2). Despite the significant diversity of hookworm species within felines, and the vulnerable conservation status of many of them, considerably less research has been performed on hookworm parasites in felids compared to canids, and many aspects of their hookworms' biology are unknown.

The dog hookworm A. caninum infects felids in many areas where wild cats are sympatric with domestic or wild canids, such as the southeastern United States ( Miller and Harkema, 1968; Little et al., 1971; Mitchell and Beasom, 1974). In other areas, however, the domestic cat hookworms, A. tubaeforme and A. braziliense , are the predominant species in wild felids ( Waid and Pence, 1988; Pence et al., 2003; Smith and Kok, 2006), and in some occasions these wildlife infections are most likely because of spillover from feral domestic cats (Milĺan and Basco-Costa, 2012).

In Asia, Uncinaria felidis and Uncinaria maya are the most common hookworms of native felids such as the leopard ( Prionailurus bengalensis ) and Iriomote cats ( Prionailurus iriomotensis ) ( Hasegawa, 1989; Yasuda et al., 1993; Shimono et al., 2012). Although apparently rare, the nematode Arthrostoma hunanensis infects the bile duct of leopard cats in some areas ( Yasuda et al., 1993).

4.1.3. Otariidae

Four Uncinaria species have been described in eared seals (otariids); however, molecular analyses suggest that there are at least 5 additional undescribed Uncinaria species ( Nadler et al., 2013; Seguel et al., 2017) ( Table 3).

4.1.4. Procyonidae

Six species of hookworms within the Necator , Arthrocephalus , Ancylostoma , Arthrostoma and Uncinaria genera have been described in procyonids ( Table 4). Most studies in procyonids have been conducted in raccoons ( Procyon lotor ), which in their native North America are infected with Arthrocephalus lotoris ; however, in Japan, where they have been introduced, raccoons are infected with the native raccoon dog hookworms Ancylostoma kusimaense and Arthrostoma miyazakiense ( Matoba et al., 2006; Sato and Suzuki, 2006).

4.1.5. Mustelidae

Four species of hookworms within the Uncinaria and Tetragomphius genera and at least one unknown species within the Ancylostoma genus have been described in mustelids ( Table 5). The most studied host species is the European badger ( Meles meles ), which is usually infected with Uncinaria criniformis , and in Korea Tetragomphius procyonis has been described in the Asian badger

Host Species Hookworm References species

Crab-eating raccoon ( Procyon Necator urichi Cameron 1936

cancrivorus) Uncinaria Vicente et al., 1997

maxillaris

Uncinaria bidens Vicente et al., 1997

Coati (Nasua nasua) Uncinaria bidens Duarte 2016

Raccoon ( Procyon lotor ) Arthrocephalus Dikmans and Goldberg 1949 , Jordan and Hayes 1959, Gupta 1961, Balasingam 1964, Snyder and Fitzgerald 1985, Cole lotoris and Shoop 1987, Yabsley and Noblet 1999, Ching et al., 2000, Kresta et al., 2009

Ancylostoma spp Popiołek et al., 2011

Ancylostoma Matoba et al., 2006 , Sato and Suzuki 2006

kusimaense

Arthrostoma Sato and Suzuki 2006

miyazakiense

( Meles leucurus ) ( Son et al., 2009).

In Europe, pine martens ( Martes martes ) are infected with Uncinaria sp. , U. criniformis and an Ancylostoma sp. ( Segovia et al., 2007; Borecka et al., 2013).

4.1.6. Ursidae

Six species of hookworms within the Ancylostoma , Arthrocephalus and Uncinaria genera have been described in bears ( Table 6). The most important hookworm species in black bears is Uncinaria rauschi , which can reach up to 72% prevalence in some areas of Canada ( Catalano et al., 2015a,b). Uncinaria yukonenesis is more common in brown bears in North America, while in Japan brown bears are infected with Ancylostoma malayanum ( Catalano et al., 2015a,b; Asakawa et al., 2006). The canine hookworm, A. caninum , and the raccoon hookworm, A. lotoris , infect black bears in the southeastern United States; however, the mean intensities are usually low (<15 nematodes per animal) ( Crum et al., 1978; Foster et al., 2011).

4.1.7. Mephtididae, Herpestidae , Phocidae , Hyenidae and Viverridae

There are few studies reporting hookworm infections in the Mephitidae (skunks), Herpestidae (mongoose), Phocidae (true seals), Hyenidae (hyenas) and Viverridae (civets) families ( Table 7). Skunks can be infected with the raccoon hookworm A. lotoris in North America ( Dikmans and Goldberg, 1949), while in South America the native skunk, Conepatus chinga , harbor its own hookworm, Ancylostoma conepati (Ib́anez ̃, 1968). In Taiwan a few individuals of Arthrostoma vampire were found in the Palawan stink badger ( Mydaus marchei ) ( Schmidt and Kuntz, 1968). Arthrocephalus gambiensi has been described in herpestids inhabiting Gambia and Taiwan ( Ortlepp, 1925; Myers and Kuntz, 1964). Compared to their otariid relatives, hookworms have been rarely described in phocids; however, the description of Uncinaria sp. in Southern elephant seals ( Mirounga leonina ) from Antarctica ( Ramos et al., 2013) highlights the extreme adaptability of some hookworm species. The human hookworm, Ancylostoma duodenale , has been found in low numbers (n = 7) in spotted hyenas ( Crocuta crocuta ) in Ethiopia ( Graber and Blanc,1979), and in other study in Kenya up to 90% of hyenas harbored an Ancylostoma sp. (Engh et al., 2003). The Malay civet ( Viverra tangalunga ) in Borneo harbors the zoonotic hookworm, Ancylostoma ceylanicum , in low prevalence (3%); however, they are more commonly infected (33% prevalence) with a different Ancylostoma sp. ( Colon and Patton, 2012).