Introduction

Zoonotic infections are a major global public health issue [1, 2]. The majority of human infections have originated from non-human animals [3], and it is recognised that many emerging infectious diseases come from various animals including wildlife and livestock [4, 5]. Most studies on emerging zoonotic infections have focused on mammals as potential sources of zoonoses [6, 7] for two key reasons: (1) Since humans are also mammals, the phylogenetic affinities and thus physiological similarities to other mammals mean that there is greater likelihood of successful host-jump event from such animals [8]. And (2) since many domestic pets and livestock are also mammals, there are more opportunities for humans to come into contact with them and their parasites [9].

In contrast, the phylogenetic distance and physiological dissimilarity between reptiles and humans would seemingly mean that there are less overlaps in their respective parasite communities. However, because many reptiles predate upon mammals, some of their parasites also use mammals as intermediate hosts. Thus, such parasites may present some element of infection risk to humans. Compared with mammals, humans interact less frequently with reptiles, as they are considered to be of relatively low economic or veterinary importance, and accordingly, there has been comparatively less research interest in the parasite communities of reptiles. Though, this may change in the future with increasing popularity of reptiles as companion animals [10, 11],

Living (non-avian) reptiles are an extremely diverse and species-rich class with over 11,000 known living species [12]. They play important ecological roles in a wide variety of habitats [13,14,15], and this diversity in terms of sheer number of species as well as ecological breadth means they are host to a wide variety of parasites. The parasite communities of reptiles were traditionally considered to be relatively depauperate [16], and the parasite fauna of reptiles is not as well-studied as those of other vertebrate classes such as mammals, birds, and fishes. While studies on the parasite communities of reptiles have increased over the last few decades, the life cycles and ecology of many of those reptile parasites, along with their zoonotic potential, remains unknown.

While zoonoses from reptiles are not as common as those from mammals, there are still some very notable examples [17••] which are of public health concern. Reptiles are known to be host to various serotypes of Salmonella bacteria, which are common among captive reptiles [18, 19], as well as a range of other lesser-known zoonotic bacteria [20]. Reptiles can also serve as potential reservoirs for a range of zoonotic arboviruses [21,22,23]. But this review will be focusing on groups which fall under the traditional definition of “parasites”—helminths, arthropods and “protozoans” (unicellular eukaryotes excluding fungi). The review will be providing an overview of zoonotic and potentially zoonotic parasites found in reptiles, and then it will be turning its focus on the diverse reptile fauna of Australia to discuss the potential zoonoses which may be found in their parasite communities.

Zoonotic Parasites of Reptiles

Reptiles are host to a range of potentially zoonotic parasites from many different taxa [17••] which can be broadly divided into three categories: helminths, arthropods, and protozoans.

Helminths

Trematodes

Of the many taxa of trematodes known from reptiles, the main group of zoonotic concern is species in the genus Alaria, which commonly uses snakes as paratenic hosts [24]. These flukes have a three-host life cycle, with carnivorous mammals serving as the definitive host, aquatic snails as the first intermediate host and a wide range of different animals as the second intermediate and paratenic hosts including frogs, snakes, rodents and boars [25]. Inside the second intermediate or paratenic host, the fluke develops into the mesocercaria stage, and humans can become infected through eating raw or undercooked intermediate or paratenic hosts [25]. The mesocercariae can cause high pathogenicity as they migrate into various different organs and tissues, causing lesions and haemorrhages, anaphylaxis or even fatality in the case of heavy infections [25].

Cestodes

Reptiles are host to a wide range of cestodes both as intermediate/paratenic hosts and as definitive hosts. However, the species of reptile-borne cestodes which are of zoonotic and public health significance are those in the genus Spirometra. Spirometra is a genus of cestodes which has a worldwide distribution [26]. There are four recognised species of Spirometra, and their plerocercoid stages are associated with the larva migrans disease sparganosis [27]. This parasite’s life cycle involves three hosts, with cats or canids serving as the definitive hosts for the adult tapeworm, copepods as the first intermediate host, and a wide range of vertebrate animals can act as the second intermediate host including fish, amphibians, reptiles, various mammals and birds [26]. In the second intermediate host, Spirometra develops into a plerocercoid, which is the stage commonly associated with sparganosis [28].

Inside a human host, the plerocercoid invades various parts of the body including subcutaneous tissue, the central nervous system and visceral organs and in some cases starts budding and proliferating progeny plerocercoids [28]. Sparganosis has been reported from many parts of the world, though most cases are from mainland China and East Asia [29, 30]. The most common infection route is through eating raw or undercooked frogs or snakes [31, 32], or drinking water contaminated with infected copepods [29]. Spirometra plerocercoids are particularly prevalent in snakes [33] and have been found to be common in snakes sold at markets for food [32] or the exotic pet trade [34].

Nematodes

A wide variety of nematode parasites are found in reptiles, but only a handful of reptile-borne nematodes are known to be potential zoonoses. It must be noted that this is not necessarily reflective of the actual zoonotic potential of nematodes from reptiles, but rather the current state of scientific knowledge as there have been relatively few studies on the zoonotic potential of reptile nematodes, especially when compared with nematodes from other vertebrate classes. Of those reptile-borne nematodes, three genera stand out as particularly notable zoonotic parasites: Angiostrongylus, Gnathostoma and Trichinella.

Angiostrongylus is a genus of nematode with 21 recognised species around the world [35]. The species most commonly associated with disease in humans is Angiostrongylus cantonensis. Its definitive host are rats, with snails serving as intermediate hosts, while a wide variety of other invertebrates and vertebrates can function as paratenic hosts [36]. When humans become accidentally infected, usually through ingestion of infected intermediate or paratenic hosts, the nematode migrates to the central nervous system where it can cause an inflammatory reaction that manifests as eosinophilic meningitis, which can lead to paralysis, coma or death [36]. Angiostrongylus cantonensis has been reported to use lizards as paratenic hosts [37, 38•] and there have been recorded cases of Angiostrongylus infections resulting from consumption of raw or undercooked monitor lizard (Varanus spp.) meat [38•, 39].

Gnathostoma is also a foodborne zoonosis; there are 12 species in the genus, and five are known to be zoonotic [40]. Since humans are accidental hosts, the pathologies induced by Gnathostoma results from the mechanical damage caused to tissues and internal organs by the larvae’s migratory tracks through the body, as well as inflammatory and immunological reactions induced by the larvae’s presence and secretions [41]. The primary route of zoonotic infection is through ingesting infected intermediate or paratenic hosts such as fish, snakes, frogs, and poultry [40]. Gnathostoma larvae have been reported from various species of snakes [42,43,44], and while usually associated with consumption of raw or undercooked fish [41], there is a recorded case of gnathostomiasis resulting from consumption of raw snake [45], and there are likely other unreported cases in areas where consumption of snakes is more common.

Trichinella is another genus of concern which has some rather unique aspects to its biology as it uses the same host individual as both the definitive and intermediate host in its life cycle. Hosts become infected via ingesting muscle cells containing Trichinella larvae; these worms then grow to sexual maturity in the intestinal mucosa and produce larvae that are carried by the lymphatic and circulatory systems to striated muscle cells which they infect and encyst, awaiting ingestion by the next host [46].

There are two species which are known to infect reptiles, T. papuae and T. zimbabwensis, both of which are also capable of infecting and circulating in mammalian hosts [47, 48]. Trichinella papuae has been found in farmed crocodiles [48], while among wild reptiles, T. zimbabwensis has mostly been found in crocodiles and monitor lizards [49]. Experimental infections have shown that both T. papuae and T. zimbabwensis are also capable of infecting other reptiles including pythons and turtles [50]. As the consumption of crocodile meat becomes more popular in various parts of the world, those Trichinella species could present a significant public health risk [48]. Furthermore, there has been a documented case of T. papuae infection resulting from eating raw soft-shelled turtles [51], showing that crocodilian meat is not the only reptilian source of Trichinella infection.

There are also other reptile-borne nematodes which are not usually known to be zoonotic, but may potentially become zoonotic under certain circumstances. Nematodes from the Ascaridida order are of particular concern due to aspects of their life cycles and life histories. Many of them have complex life cycles that involve vertebrate intermediate hosts [52] and can potentially be zoonotic when humans become accidental intermediate or paratenic hosts. For example, experimental infection has shown that Hexametra larvae can successfully infect primates, which indicates it may potentially infect humans [53]. Furthermore, a recent case of an Ophidascaris robertsi larva causing human visceral and neural larva migrans [54•] raises further questions about the zoonotic potential of these reptile ascarids and the pathologies they may cause.

Arthropods

Pentastomida

Pentastomids are highly derived parasitic crustaceans [55], and they have a complex life cycle with the adult living in the respiratory system of their tetrapod vertebrate definitive hosts (mostly reptiles) and can infect a variety of both invertebrates and vertebrate animals as intermediate and paratenic hosts [56]. For reptile pentastomids, humans usually serve as accidental paratenic hosts, in which the larval stage (nymphs) migrates to various parts of the body, causing visceral pentastomiasis [57]. While the infection can often be asymptomatic, ocular pentastomiasis, where the nymphs migrate into the eyes [58], can cause permanent vision loss, and on rare occasions, high-intensity infection may result in death [59].

Of the reptile pentastomids, species from the genus Armillifer are most commonly associated with zoonoses. Armillifer has been reported in snakes sold for human consumption [60, 61], and human pentastomiasis is most common in parts of West Africa, Central Africa, and Malaysia [57] where consumption of undercooked snakes is relatively common. In those cases, infection can result from consumption of meat which has been contaminated with the eggs of pentastomes during the butchering process [61], or the incidental consumption of the gravid adult pentastome itself [59]. Armillifer and other pentastomids have also been found in captive reptiles that are kept as pets [62] which can present a zoonotic risk, as accidental ingestion of pentastome eggs in secretion or faeces from infected reptile may also be a potential infection route [63].

Ticks

There are a number of tick species that can feed across different vertebrate classes, parasitising both reptiles and mammals at various stages of their life cycles [64, 65]. Additionally, some tick species that predominately parasitise reptiles have also been documented to occasionally bite humans [e.g. 66, 67]. While the impact of each individual tick feeding is negligible, they can act as vectors for a variety of infectious agents which circulate in reptiles and other animals that they bite. For example, Rickettsia has been detected from Amblyomma dissimile [68], and the tortoise tick Hyalomma aegyptium can carry the pathogens that cause granulocytic anaplasmosis and Q fever [69], as well as Crimean-Congo haemorrhagic fever virus [70•]. Considering that a wide range of ticks are commonly found on reptiles in the international reptile trade [65, 71], reptile ticks and the infectious agents they carry should be a key zoonotic concern.

Mites

Reptiles are host to a wide range of mites [72], some of which can potentially infect humans [17••, 23]. For example, the snake mite Ophionyssus natricis is commonly found in captive reptiles [73], and it has been recorded to infest humans, causing pruritic dermatitis [74, 75]. More recently, Hirstiella, a genus of lizard mite, has also been recorded to cause papular dermatitis in the owner of a captive green iguana (Iguana iguana) which was heavily infested with mites [76]. And much like ticks, those mites can also serve as potential vectors for various pathogens such as Rickettsia [77]. It is notable those recorded cases usually involve captive reptiles, kept either privately or in a zoo, showing that frequent contacts with captive reptiles can lead to infestation by reptile mites.

Protozoans

Reptiles are host to a variety of blood-borne pathogens, some of which may have zoonotic significance. Lizards have been found to be reservoirs for a variety of Trypanosoma [78] including human-infecting species such as T. brucei [79] and T. cruzi [80]. Reptiles are also host to a range of enteric protozoans that can potentially be zoonotic. Sarcocystis is a genus of intracellular parasite with a two-host life cycle—a prey intermediate host and a predatory definitive host, and two species, S. hominis and S. suihominis, are known to infect humans as the definitive host [81]. However, S. nesbitti, a species which uses snake as its definitive host, has been found to infect humans as intermediate host, causing relapsing fever and myalgia [82, 83]. Additionally, Cryptosporidium and Giardia have also been reported from pet reptiles [84]. While reptiles seem to have their own specific species of Giardia [e.g. 85], the zoonotic species Giardia duodenalis has also been detected in free-living lizards [86]. Cryptosporidium has also been reported from many different species of reptiles, and while reptile-specific species of Cryptosporidium are usually not considered to be infectious to mammals [87], human-infecting species of Cryptosporidium such as C. parvum have also been detected from captive reptiles [88,89,90], possibly due to captive conditions with humans exposing them to C. parvum via their food and surroundings.

Zoonotic Parasites in Australian Reptiles

Australia is home to about 14% of the world’s total reptile diversity with over 1100 known reptile species, composing of all major groups of living non-avian reptiles aside from Rhynchocephalia (more commonly known as Tuatara) [91]. While many aspects of these reptiles have been extensively studied [91], knowledge about their parasite communities has lagged behind in comparison. In a summary of helminth parasites in Australian reptiles by Pichelin, Thomas, and Hutchinson [92], they listed about 230 helminth taxa from 180 host taxa. Since then, a handful of dedicated workers have added more taxa to that list (see [93] for details), but the sum knowledge of sampled host taxa represents only a small fraction of Australia’s reptile fauna.

The zoonotic reptile parasites of Australia consist of a mix of both invasive and native species. While some of the invasive parasites are well-known as zoonoses elsewhere in the world, the zoonotic potential of many Australian native reptile parasites is poorly understood.

Cestodes

The sole species of Spirometra recorded in Australia is S. erinacei [94]. Also known as “zipperworms”, S. erinacei is the most commonly found helminth in feral cats along eastern Australia [95], which play a crucial role in the dissemination and transmission of S. erinacei in Australia. Spirometra plerocercoids have been recorded from various snakes in Australia [94, 96], with Stephanson [96] finding between 12 and 28% prevalence in Australian snakes, but very little is known about the prevalence and abundance of plerocercoids in other Australian reptiles. The first case of human sparganosis in Australia was reported in 1905 [97], and while human infection by Spirometra is relatively rare in Australia when compared to other parts of the world, they are possibly under-recognised as these parasites have a long incubation period and presents a diagnostic challenge [97].

Nematodes

While both Angiostrongylus and Gnathostoma are commonly present as potential foodborne reptile zoonoses in other parts of the world, zoonotic cases involving those parasites are rare in Australia, and the prevalence of those nematodes in Australian reptiles is unknown. While Angiostrongylus is well-established in Australia, cases of human infection have been rare and sporadic, and are usually associated with incidental ingestion of infected snails or contaminated vegetables [98]. Gnathostoma is considered to be an uncommon zoonotic infection in Australia associated with consuming raw or undercooked fish [99], though some diagnosis of gnathostomiasis attributed to Gnathostoma in Australia may in fact be caused by a different genus of gnathostomatid nematode, Echinocephalus [100].

In contrast to those introduced species, there are a number of native reptile-borne nematodes which may have greater zoonotic significance in the Australian environment. As mentioned in the previous section, reptile ascarids can be potentially zoonotic, and they are found among many species of Australian reptiles, mostly in large snakes [92]. The health risk they pose can be seen with a recent case of Ophidascaris robertsi causing visceral and neural larva migrans, in a patient who may have accidentally ingested O. robertsi eggs via contaminated vegetation or kitchen equipment [54•]. The eggs of O. robertsi are resistant to desiccation [101], and the larvae have been recorded to use many different species of native Australian mammals as their intermediate hosts [102,103,104]. While O. robertsi larvae have been found to develop poorly in introduced mammals such as guinea pigs and rabbits, and not at all in cats, dogs or sheep [102], the case reported by Hossain et al. [54•] shows that a larva can develop into a full-size L3 inside a human host. The potential for Ophidascaris zoonoses has previously been raised [e.g. 105], but usually in the context of bush meat and direct human consumption of the snake definitive host. The findings by Hossain et al. [54•] highlight the need to consider other routes of infection which are less direct and not as immediately apparent.

In addition to ascarid nematodes, Australian reptiles are also host to a range of physalopterid nematodes [106], some of which may present an infection risk for humans [107]. While human infections with physalopterid nematodes have been in dramatic decline throughout modern time [108], there has been a reported case in Australia of an infant suffering from gangrene in the small bowel due to being infected with physalopterid nematodes [109]. Studies on the life cycles of physalopterids from Australian reptiles found that the larvae parasitise arthropod intermediate hosts [107], which means human infection may result from accidental ingestion of infected insects. Given the ubiquity of physalopterids in Australian reptiles [106], it would be worthwhile to investigate their zoonotic potential.

Pentastomids

Pentastomids are common among Australian snakes [110], but the life cycle of most pentastomids in Australia is poorly known. The nymphs of Alofia merki, a crocodile pentastomid, have been found in two species of marine and brackish water fish [111], which may present a potential risk as a foodborne zoonosis. However, the genus most usually associated with visceral pentastomiasis in human infection is Armillifer [112], and there are two species of Armillifer which have been described from Australian snakes—A. australis and A. arborealis [112], but the zoonotic potentials of these Australian species are unknown.

Ticks

There are 12 species of ticks in Australia which are considered as reptile ticks [113], and while many of them feed only on reptiles, some are also known to feed on humans. For example, Amblyomma moreliae feeds on a wide range of reptiles, but has also been reported to bite various mammalian hosts, including humans [65]. Similarly, Bothriocroton hydrosauri, the southern reptile tick, can feed on livestock and humans, even though it is usually associated with the stump-tailed lizard Tiliqua rugosa and other reptiles [65]. More recently, the reptile tick Amblyomma albolimbatum has also been recorded biting a human [114]. Some of those ticks can also harbour various tick-borne infections. For example, the aforementioned B. hydrosauri has been found to harbour bacteria from the genus Rickettsia, in particular, R. bonei, which causes Flinders Island spotted fever [115].

Mites

There are over 20 species of reptile mites known in Australia [116,117,118,119], composing of both native and introduced species. However, the mite fauna of Australian reptiles is not as well documented as those of Australian birds and mammals [116, 117], so there may be many more undescribed reptile mite species. Of the mites reported from Australian reptiles, the species that are known to be zoonotic are actually the introduced species such as Ophionyssus natricis and mites in the genus Hirstiella [119, 120], both of which, as previous discussed, can infect and cause dermatitis in humans [74,75,76]. Worryingly, some introduced mite species have taken readily to infecting Australian native reptiles, which have facilitated their propagation and spread in the wild [119,120,121]. There may be native reptile mites which are potentially zoonotic, but as Spratt and Beveridge [93] noted, there is currently limited taxonomic capacity in Australia for identifying and describing new species of mites due to the lack of sustained research interest. Thus, there may be other species of potentially zoonotic mites on reptiles and other Australian wildlife which are currently undocumented.

Protozoans

There is evidence to indicate that Sarcocystis nesbitti is present in Australian scrub pythons, Simalia amethistina [122]. This parasite was responsible for an outbreak of muscular sarcocystosis in Malaysia in 2012 [82, 83]. The main concern relating to this parasite is for potential contamination of the water supplies with faeces from infected snakes, as the sporocysts are somewhat resistant to chlorination, and infection may occur from drinking contaminated water or eating uncooked food which have been washed with contaminated water [83].

Captive Reptiles as a Potential Pathway for Zoonoses

Due to local dietary habits, consumption of reptiles is much less common in Australia in comparison with other parts of the world, which means many foodborne parasites from reptiles which are common in other regions are far less prevalent in Australia. Nevertheless, there are some sections of the population which could be at risk of such zoonoses. Reptiles such as snakes, goannas, crocodiles, and turtles are regularly consumed by some Australian Indigenous communities [123], which may put them at risk of those reptile-borne parasites. Additionally, the rise in consumption of crocodile meat may also be a concern. While commercially sold crocodile meat usually comes from farmed or ranched crocodiles which are regularly monitored and inspected for parasites, wild-harvested crocodiles are often included in meat made available for human consumption [124]. Thus, there are some reptile parasites that are potential foodborne zoonoses in Australia. However, a more common source of zoonotic infections from reptiles in Australia may actually come from inadvertent contact with the infective stages of their parasites, through shared environment and cohabitation. This includes reptiles that are kept as pets.

According to a report by Animal Medicines Australia, as of 2022, there are an estimated 538,000 reptiles kept as pets across Australia, with 41% of the reptile-owning household having two or more reptiles, and snakes appear to be the most popular pet reptile [125]. Ethical and animal welfare concerns have been raised regarding the trade and private keeping of reptiles as “pets” [126], as well its impact on wild populations, especially of threatened or range-restricted species [127]. While Australian reptiles are protected in their range and export is technically prohibited, due to the lack of international protection for those species, Australian reptiles are common on the global exotic pet market, bred in captivity from parental stocks that were initially smuggled out of the country [11]. Additionally, there are persistent efforts at smuggling highly invasive exotic reptiles into Australia for the pet trade [128, 129]. Illegal wildlife trade is recognised as a pathway for the spread of various parasites and pathogens across the world [130••], and even among legal trade, parasites are common, showing that quarantine procedures are lacking [65, 131]. Considering the very low to negligible host specificity of helminths from Australian lizards [132], this can lead to parasite exchange between Australian lizards and introduced reptiles.

Private keeping of captive reptiles provides opportunities for direct contact between humans and reptile parasites. Unfortunately, a significant number of owners lack basic understanding of the requirements for keeping their reptiles in captive conditions [133], let alone awareness of any zoonotic parasites that their pets may potentially harbour. Thus, captive reptiles may become a key source of emerging zoonoses as they can harbour a wide range of parasites with varying degrees of zoonotic potential [134, 135].

Captive conditions which place many different species of animals in shared enclosures can also provide opportunities for parasite transmission and exchange. For example, a group of crested geckoes, Correlophus ciliatus, at a theme park in Hong Kong developed heavy infections of Hexametra angusticaecoides after they were kept in an enclosure which had previously housed wild-caught Madagascan mossy geckoes, Uroplatus sikorae [136•]. Additionally, exposure to and transmission of reptile parasites can also occur during various stages of the trade chain. For example, the case of a captive-bred sugar glider, Petaurus breviceps, which was infected with the nematode Ophidascaris robertsi, may have resulted from being exposed to the parasite while being held in a store that also housed pythons [104]. Considering the increasing interest in reptile pets, there is a need to monitor the parasite communities of captive reptiles, especially for potentially zoonotic species.

Conclusion

Much like reptiles elsewhere in the world, Australian reptiles are host to a wide range of taxonomically diverse parasites, some of which have varying degrees of zoonotic potential. These consist of both well-known zoonoses which were introduced and have become established in various Australian ecosystems, as well as native species for which very little is known about their ecologies or zoonotic potential. There is generally paucity in knowledge about the parasites (zoonotic or otherwise) of Australian reptiles. To fill in this gap, there needs to be more studies on the ecologies and life cycles of parasites in both native and invasive reptiles of Australia.

The increasing popularity of reptiles as exotic pets will bring more people into contact with reptile parasites. Furthermore, the international trade in reptiles is enabling the spread and exchange of various reptile-borne infections across the globe. Compared with other classes of vertebrate animals, reptiles are generally overlooked as potential sources of zoonoses. But as more people interact with reptiles as pets, subjects for tourism, or food, it is necessary for us to recognise that reptiles can also be host to parasites which have significant public health ramifications.