Norval, Gerrut¹ ; Sharrad, Robert D.² and Gardner, Michael G.³

¹✉ College of Science and Engineering, Flinders University, Adelaide 5042, South Australia, Australia.
²College of Science and Engineering, Flinders University, Adelaide 5042, South Australia, Australia.
³College of Science and Engineering, Flinders University, Adelaide 5042, South Australia, Australia & Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide 5000, South Australia, Australia.

2020 - Volume: 60 Issue: 3 pages: 607-611

Short note

Keywords

Abstract

Ticks are parasitic arthropods that are generally haematophagous in all three active life stages; larval, nymphal and adult instars (Oliver, 1989). Although the males of some Ixodes species may occasionally parasitize engorged conspecific females (Moorhouse and Heath, 1975; Ntiamoa-Baidu, 1986; Durden et al., 2018), ticks are primarily parasites of all vertebrate groups, except fish (Oliver, 1989).

Tick species exhibit degrees of host specificity due to various morphological adaptations and behaviours to locate hosts and feed efficiently (Oliver, 1989; McCoy et al., 2013). Some species, such as Haemaphysalis longicornis Neumann, 1901, will parasitize a large variety of host species (Hoogstraal et al., 1968; Barker and Walker, 2014). Other tick species tend to favour different host types at different stages of their life cycle. For instance, Amblyomma longirostre (Koch, 1844) has only been recorded to parasitize birds during the larval stage, but nymphs will also infest some mammals, and adults primarily parasitize particular rodent species (Nava et al., 2010). Several species tend to parasitize only certain vertebrate classes or orders such as Amblyomma helvolum Koch, 1844, which only exploit reptiles (Simmons et al., 2002). Others are very host specific and usually will only parasitize one or a small number of similar host species. Thus, Argas (Microargas) transversus Banks, 1902, only feeds on Galapagos giant tortoises (Hoogstraal and Kohls, 1966; Hoogstraal et al., 1973). However, apparently host-specific species are still occasionally collected from atypical hosts, such as Amblyomma (formerly classified as Aponomma) sphenodonti (Dunmbleton 1943) that almost exclusively parasitizes tuataras, Sphenodon punctatus (Gray, 1842), but is occasionally also found on other sympatric reptiles (Heath, 2006b). Herein, we report three instances of human parasitism by ticks that usually infest reptiles.

• Case 1 On November 6^th, 1972, upon concluding fieldwork at Mt Mary in the Mid North region of South Australia, RDS found a male of an ixodid attached to the inside of his left elbow. The tick was left in place for observation, but it was removed approximately 24 hours later on November 7^th as the attachment site had become inflamed and painful. RDS had also developed a headache, although it cannot be confirmed that it was related to the tick bite. The attachment site remained inflamed for another two days. Using the keys in Roberts (1970), the tick was identified as a male of Amblyomma limbatum Neumann, 1899. The tick specimen was subsequently lost and therefore could not be deposited in a museum collection.

• Case 2 On November 9^th, 2017, a day after returning from a study site near Mt Mary, GN found a nymphal tick attached to the dorsal aspect of the first segment of his left big toe. The tick was removed and preserved in 70% ethanol. There were signs of localized minor inflammation (red skin discoloration and tenderness) at the site of the bite, which persisted for three days. Using the keys and descriptions in Roberts (1970) and Andrews et al. (2006), the tick was identified as a nymph of Bothriocroton hydrosauri (Denny, 1843), formerly classified as Aponomma hydrosauri, and was subsequently deposited in the parasites collection of South Australian Museum, Adelaide, South Australia (voucher number J 21395).

• Case 3 On November 9^th, 2019, a resident of Bower, a small town near Mt Mary, noticed some discomfort on the inside of the right foot just below the ankle, and closer inspection revealed that it was a tick. She removed the tick and sent it to the South Australian Museum for species identification. There were signs of localized minor inflammation at the site of the bite, which persisted for ten days. Using the keys and descriptions in Roberts (1970) and Andrews et al. (2006), the tick was identified as an un-engorged female of B. hydrosauri and was subsequently deposited in the parasites collection of South Australian Museum, Adelaide, South Australia (voucher number J 21415).

Amblyomma limbatum and B. hydrosauri are reptile ticks with parapatric distributions; the former occurs throughout the arid and semi-arid parts of Australia, whereas the latter is restricted to the wetter parts of southern New South Wales, Victoria, Tasmania, southeastern South Australia and parts of southwestern Western Australia (Smyth, 1973; Barker and Walker, 2014). Our observations not only confirm that A. limbatum and B. hydrosauri will parasitize humans, but we also provide new information about life stages and attachment sites. Both these tick species have previously been reported to occasionally parasitize humans (Table 1), but as stated by Guglielmone and Robbins (2018), little information was provided, so it is not clear which life stages were involved nor where they attached. The risk of transmission of tick-borne pathogens can increase the longer an infected tick remains attached (e.g. Eisen, 2018). As a result, immature life stages, which may not initially be detected due to their small size, and/or ticks attached on parts of the body where they are not easily noticed can be more likely to infect the host with tick-borne pathogens. In this way, information about life stages and attachment sites are vital for establishing prevention strategies and should be systematically reported.

Although ticks may occasionally attach and attempt to feed on atypical hosts, this does not necessarily mean they can successfully engorge and survive. For instance, larvae, nymphs and adults of the seabird tick, Ixodes laridis Heath & Palma, 2017 (reported as Ixodes eudyptidis), were fed on laboratory white mice, and although not all individuals survived, some did and one female even produced fertile eggs (Heath, 2006a). However, less than 1% of the larvae of the echidna tick, Bothriocroton tachyglossi Roberts, 1953, attached when they were experimentally exposed to sleepy lizards, Tiliqua rugosa (Gray, 1825), and none successfully engorged (Andrews et al., 2006). In two of the instances described herein, the ticks survived for at least a day, and all the indications were that they were feeding successfully. Amblyomma limbatum and B. hydrosauri are primarily reptile ticks, and even though the latter species has been reported to parasitize horses, Equus caballus Linnaeus, 1758, and domestic cattle, Bos taurus Linnaeus, 1758, these records are more likely attributable to B. tachyglossi (Roberts, 1953; Andrews et al., 2006; Barker and Walker, 2014; Barker et al., 2014). The prevalence of parasitism on mammalian hosts by A. limbatum and B. hydrosauri therefore appears to be rare and are likely instances of accidental host use.

In addition to anemia and other conditions such as dermatosis, tick may also cause tick paralysis and/or otoacariasis in their hosts. However, their main risk to public health and agriculture stems from their role as vectors of various bacterial, filarial, fungal, protozoan and viral pathogens (Lapage, 1963; Hoogstraal, 1985; Roberts and Janovy, 2005). Amblyomma limbatum and B. hydrosauri are both known vectors for the haemogregarine parasite Hemolivia mariae Smallridge and Paperna, 1997 (Smallridge and Paperna, 1997). Both the Flinders Island spotted fever agent, Rickettsia honei Stenos, Roux, Walker, and Raoult, 1998, and an undescribed Rickettsia species, which is present in the Mt Mary region (Staines et al., 2020), have been detected in B. hydrosauri (Stenos et al., 2003; Whiley et al., 2016), making this tick species of particular public health concern (Stenos et al., 1998; Stenos et al., 2003).

In order to gain a better understanding of tick host specialization, it is necessary to shift from merely recording the variety of hosts utilized by a tick species throughout its geographic range, to reporting host use on a more localized scale (McCoy et al., 2013). Such information can be instrumental in highlighting localities where particular tick species pose a risk to public health and/or livestock. Here, we described instances of A. limbatum and B. hydrosauri parasitizing humans. However, in order to determine whether these were merely accidental host choices, additional information is required. Empirical studies related to the prevalence of parasitism of mammalian hosts by the different life stages of A. limbatum and B. hydrosauri and their ability to use these hosts to complete their life cycles are warranted. Finally, we encourage the reporting and submission of tick specimens found on atypical hosts to academic institutions or museums for species verification and for improving our knowledge on host specialization in this group of parasites.

Acknowledgements

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. The observations presented herein were made by RDS while a PhD student at the University of Adelaide, and GN while conducting research for his current PhD studies at Flinders University. GN's research in 2017 was partly funded by a grant from the Royal Society of South Australia. We would like to thank Jae Dalgleish and Dr. Matthew Shaw (South Australian Museum) for providing information about case 3, and Dr. Allen C.G. Heath for the addition pertaining to the tick bite record from New Zealand.

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