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Tuatara: Volume 29, Issues 1 and 2, August 1987
A Review of the Origins and Zoogeography of Tick-Borne Disease in New Zealand
A Review of the Origins and Zoogeography of Tick-Borne Disease in New Zealand
Abstract
By comparison with the global scene, New Zealand has only a very small proportion of the total number of tick-borne diseases known. The New Zealand tick fauna, although small, includes two species with worldwide disbribution (Ixodes uriae; Ornithodoros capensis) and already established as hosts of many viruses, some of which produce illness in man. Regular visits from migratory sea-birds could see the gradual accumulation of organisms, and particularly viruses, which at present are known only from the Northern Hemisphere.
Key words: Ticks, tick-borne disease, viruses, sea-birds, zoogeography, New Zealand.
Introduction
Ticks have been unwelcome associates of man and his livestock for centuries, yet less than one century has passed since a tick (Boophilus annulatus) was first shown to transmit a disease (Texas fever, caused by Babesia bigemina) (Smith, 1889; Smith and Kilborne, 1893).
Subsequently, numerous protozoa, rickettsias, bacteria (spirochaetes) and viruses have been shown to have tick vectors, and the majority of these discoveries have been in the last 25 years (Chamberlain, 1982).
In the unaltered habitat (the “wild”), ticks and organisms they harbour are part of a self-sustaining vertebrate-arthropod ecosystem. All is not peaceful coexistence however, as disease does frequently occur (Duffy, 1983; Morgan et. al. 1981, Smith, 1982). When man impinges upon these habitats generally benign tick-borne infections of wildlife can become more or less serious zoonoses (in the sense of a disease of an animal transmitted to man) or diseases of livestock (Hoogstraal, 1981; Hoogstraal et. al. 1970).
This paper will explore the relationships between New Zealand's tick fauna and tick-borne diseases in the Pacific basin and other parts of the world.
New Zealand and Its Tick Fauna
According to the hypothesis of continental drift, New Zealand's isolation from the primordial southern continent of Gondwanaland started in the Upper Cretaceous (70 million years ago) and from this time onward, the opportunities for land organisms to reach New Zealand decreased as the country became more isolated (Fleming, 1975).
At the end of the Cretaceous, isolation for land vertebrates would have been complete (Fleming, 1975), but there was no barrier to sea-birds, and it is these hosts that harbour the majority of tick-borne diseases both in New Zealand and elsewhere.
The long period of isolation from neighbouring continents after the Cretaceous could explain why there is not a large variety of tick-borne diseases in New Zealand. With a greater number of tick species and a wider diversity of genera; with a wide variety of small mammals and a more diverse range of habitats, New Zealand may have become home to a moderate selection of tick-borne diseases. Indeed, this is the case today in other countries with a Marine West Coast climate similar to that of New Zealand's, such as the United Kingdom (Arthur, 1963), page 20 or S.E. Australian coast (Roberts, 1970). Thus our climate is not necessarily a barrier to arthropod-borne disease, although it seems to be true as far as malaria is concerned. Alternative explanations for the paucity of disease may be either the absence of suitable vectors or that many exotic diseases have not yet had the chance to reach our shores.
New Zealand Ticks
New Zealand has only nine named species of ticks (Heath, 1977, Table 1).
Aponomma sphenodonti may act as the occasional vector of a haemogregarine that occurs rarely in the tuatara (Desser. 1978), but the other endemic species, Ixodes anatis and I. jacksoni, harbour no known disease. Similarly, the indigenous species I. pterodromae and I. auritulus are virgin vectors. The bipolar I. uriae (Fig. 1) the cosmopolitan Ornithodoros capensis (Fig. 2) and the indigenous I. eudyptidis (Fig. 1) are all vectors of viruses (Hoogstraal, 1973) and the Western Pacific's Haemaphysalis longicornis is a vector of protozoa, rickettsias and viruses (Hoogstraal et. al. 1968; Roberts, 1970). Ornithodoros capensis is known from many species of sea-birds that either live in New Zealand or frequent our shores (Heath. 1977). Similarly, Ixodes uriae is another tick with a wide sea-bird host range. It has been taken from Puffinits griseus, the sooty shearwater (Heath, unpublished), a transequatorial migrant to New Zealand waters, and the only such long-distance flier reaching New Zealand from which I. uriae has been taken to date.
Ixodes eudyptidis is shared with Australia and may be one of our exports to that country (Heath. 1977). Haemaphysalis longicornis occasionally infests terrestrial birds but it appears that its movement around the Pacific (Fig. 1) has been mainly on the back of cattle (Hoogstraal et. al. 1968).
Diseases
Protozoa, Rickettsias and Spirochaetes
As far as is known, there is only one pathogenic protozoan in New Zealand capable of being transmitted by ticks (James et. al. 1984) but no rickettsias or spirochaetes. Some of the cellular components of tick haemolymph have caused an occasional scare as they are remarkably like rickettsias. However, indications are that probably all of the debilitating effects of our only “economic” tick, H. longicornis are caused by the tick's feeding actions and/or salivary components.
Haemaphysalis longicornis was originally thought to be a vector of Theileria sergenti, a protozoan that is extremely pathogenic to cattle in Korea and Japan (25% mortality and up to 100% morbidity) but apparently non-pathogenic in Europe and Australlia (Purnell, 1980). Earlier workers classified the European and Australian Theileria as T. mutans (now established as an African species) and this seemed reasonable on the basis of pathogenicity (Purnell, 1980). However, it has been established that the species transmitted by Haemaphysalis ticks is T. orientalis (James et. al. 1984). There is no evidence of any severe disease in New Zealand, although heavily infected or splenectomised animals may develop severe anaemia (James et. al. 1984).
There is evidence that H. longicornis is capable of transmitting Babesia gibsoni (Otsuka. 1974), but incapable of transmitting other Babesia spp. (Seddon, 1968) page 21 or Anaplasma spp. (Connell, 1978) although the tick is an experimental vector of Q fever (Smith. 1942), a rickettsial disease that affects livestock and man in Australia. It is likely though that the ticks are only a rare source of human infestation as the latter disease can be caught by inhaling infected dust or drinking infected milk.
Experiments are in progress in the U.K. in an effort to determine whether H. longicornis is a possible vector of Babesia major (Heath, unpublished). This protozoan is not common in the UK but the likelihood of its introduction into New Zealand has been questioned and its transmission by a Haemaphysalis species in the UK has justified the experiment, considering that we do occasionally import British cattle.
Both B. divergens and B. bovis have caused fatal infections in splenectomised men in the UK (Cox, 1980).
There are no records of New Zealand tick species being capable of. or implicated in, the transmission of spirochaetes.
Viruses
The last 25 years have seen the isolation of more than 80% of the nearly 400 arthropod-borne viruses registered worldwide (Chamberlain, 1982). About 80 of these viruses are tick-borne (Hoogstraal, 1973) and 37 have been isolated from 4 tick species that occur in New Zealand (Tables 2, 3 and 4), although only 3 tick-borne viruses have been isolated specifically from New Zealand (Austin, 1984).
The 4 tick species involved are I. uriae, I. eudyptidis, Q. capensis and H. longicornis.
Tables 2, 3 and 4 show the viruses isolated from these ticks, the country of isolation and an indication as to whether the viruses affect man. Ixodes eudyptidis is the only species not recorded as biting man, but it will feed on mice in the laboratory (Heath, unpublished).
Ornithodoros capensis and H. longicornis bite man readily (Roberts, 1970) but I. uriae is less likely to (Doherty et. al. 1975). An endemic New Zealand virus (Whataroa) was originally isolated from mosquitoes (Ross et. al. 1964) but has been shown to survive in O. capensis in the laboratory (Ross, 1971).
Infections of man with tick-borne viruses normally cycling in closed bird-tick-virus-island ecosystems, have occurred (Converse et. al. 1975; Converse et. al. 1976; Hoogstraal et. al. 1970; Yunker, 1975). In fact humans can be regularly attacked by ticks on islands (Hoogstraal, et. al. 1976b, c). but there has been only occasional viral infection (Hoogstraal et. al. 1970) despite the presence of viruses in the ticks and bird hosts.
Johnson Atoll Virus
This virus was recorded from New Zealand in 1978 (Austin, 1978) and is worthy of special mention because it is the first tick-borne arbovirus known from this country. It was isolated from O. capensis collected near gannets (Sula bassana serrator) in the Cape Kidnappers sanctuary and extends the range of Johnson Atoll Virus (JAV) from the tropics into the temperate zone. It was originally known from islands in the North Pacific and in Australia (Clifford et. al. 1968; page 22 Doherty et. al. 1969; Yunker, 1975). JAV has not been associated with disease in man, but the other two members of the the Quaranfil group to which JAV belongs have been isolated from individuals with a febrile illness (Austin, 1978).
Saumarez Reef Virus
This virus was originally isolated from O. capensis and I. eudyptidis ticks taken respectively from Sooty Terns (Sterna fuscata) and red-billed gulls (Larus nova-ehollandiae) in Australia (St. George et. al. 1977). So far in New Zealand Saumarez Reef Virus has only been isolated from a mixed gull (L. novaehollandiae scopulinus and white-fronted tern (Sterna striata) colony at Kaikoura (Austin, 1984).
Hughes Group Viruses
This virus group was first described from O. denmarki in North America (Hoog-straal, 1973). A number of strains of virus belonging to this group have been isolated from O. capensis collected at Cape Kidnappers (Austin, 1984). Here they were associated with the Australian gannet. S. b. serrator. Other isolations have been from ticks (O. capensis) in colonies of red-billed gulls (L. n. scopulinus) and white-fronted terns (S. strauta) from Kaikoura, Sumner and Karitane (Austin, 1984).
Origins of Virus Infestations
At first sight, it seems almost axiomatic that migratory birds have spread bird-adapted tick-borne viruses around the world and the concept has its supporters (Kemp et. al. 1982; St. George et. al. 1977; 1985). However there is some reluctance to accept that the interchange of viruses between subarctic and subantarctic could occur simply by dispersal of ticks (e.g. I. uriae) on transequatorial, viremic birds (Doherty et. al. 1975). These doubts are expressed despite the fact that antigeni-cally-related viruses have been isolated from I. uriae in both the subarctic and the subantarctic (Hoogstraal, 1973; Doherty et. al. 1975; St. George et. al. 1985).
The opposition is based on the fact that migrating birds such as shear-waters are said to settle on land only when they return to their breeding places and not in their northern latitude dispersal and feeding grounds. As an alternative, Doherty et. al. (1975) suggested that other species of Ixodes, parasitising sea-birds, may form a chain on islands between the northern and southern distribution of I. uriae and may carry viruses related to those in I. uriae. These, if found, may show that there is a gradual antigenic change between the northern and southern viruses; (this seems to indicate that these workers accept a limited amount of island-hopping by birds other than the transequatorial migrants). If such connecting links are not found, then the present distribution of I. uriae and its viruses may need to be explained in terms of plate tectonics or some other yet to be understood evolutionary forces. It is not such a large step however from accepting the circumpolar dissemination of ticks by sea-birds (Doherty et. al. 1975; Heath, 1977) to agreeing to their transequatorial carriage by the same means. The present distribution of O. capensis (Fig. 2) serves as a good model of a bird-distributed tick (Health, 1977) as there appears to be no other way in which it could have attained localities in both hemispheres. Furthermore, there are two species of birds in addition to page 23 P. griseus (Wilson's Storm Petrel, Oceanites oceanicus and Arctic Tern, Sterna paradisaea) which are transequatorial and could fill the role of disseminators of I. uriae (St George et. al. 1985).
Despite such arguments, there is evidence that some sea-bird ticks, and particularly I. eudyplidis, cause varying degrees of paralysis in their hosts (Heath. unpublished). Such a condition would restrict their flying ability and perhaps force them to land, when they otherwise would not voluntarily do so. This phenomenon would help explain the distribution of antigenically-related viruses on not-too-distant islands and other land areas without involving visits by migratory birds. Nevertheless, an ill (viremic or tick-infested) transequatorial migrant bird could also make an unscheduled landing and so disseminate viruses and/or ticks.
It has been found that deaths and nest-desertion occur among bird colonies where virus-infested ticks have been present in large numbers, or even in the absence of a virus (Duffy, 1983: Feare, 1976; Johnstone et. al. 1975; King et. al. 1977). It seems likely that birds leaving such areas would land on nearby islands and help spread ticks and viruses. What is certain is that their movements could not happen at a better time for the ticks and their viruses.
Conclusions
From the evidence presented it is apparant that tick-borne viruses and other organisms have potential as zoonotic agents in New Zealand should they reach here. It is also certain that a considerable amount of survey work has yet to be done before it can be established that no more than three tick-borne viruses occur in this country. It is likely that many of the viruses isolated from O. capensis in other parts of the world could find their way to New Zealand and viruses unique to the New Zealand or subantarctic regions may yet be found. Furthermore, even though the known tick-borne diseases in New Zealand are few, our tick fauna, limited as it appears to be, still has a vector-potential that justifies a rigid quarantine system.
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| Tick | Distribution |
| Aponomma sphenodonti | New Zealand |
| Ixodes anatis | New Zealand |
| I. jacksoni | New Zealand |
| I. eudyptidis | New Zealaad, Australia |
| I. auritulus zealandicus | New Zealand |
| I. pterodromae | New Zealand, Australia, Sub-Antarctic |
| I. uriae | Bipolar |
| Haemaphysalis longicornis | Western Pacific |
| Ornithodoros capensis | Cosmopolitan |
| Virus Group | Virus | Origin | Disease | References | |
|---|---|---|---|---|---|
| Ixodes Eudyptidis | |||||
| B | Saumarez Reef | Australia; New Zealand | ± | Austin (1978): St George (1978): St George et. al. 1977 | |
| HAEMAPHYSALIS LONGICORNIS | |||||
| Ungrouped | Coxsackie A-like | Fiji | + | Hoogstraal (1973) | |
| Khasan | USSR | ? | Lvov et. al. (1978) | ||
| B | Russian Spring- | USSR | + | Hoogstraal (1973) | |
| Summer Encephalitis | ” | ” | ” | ||
| Powassan Encephalitis | Korea | + | Hoogstraal (1981) | ||
| + = causes disease | |||||
| ± = posssibly causes disease | |||||
| ? = not known if causes disease |
| Virus Group | Virus | Origin | Disease | Reference |
|---|---|---|---|---|
| B | Tyuleniy | USSR; USA; Norway | + | Hoogstraal (1973); Lvov et. al. (1972); Saikku et. al. (1980) Thomas et. al. (1973) |
| Gadgets Gully | Australia | ? | St. George et. al. (1985) | |
| Kemorovo | Yaquina Head | USA | ? | Hoogstraal (1973); Yunker et. al. (1973) |
| Great Island | Canada | ? | Hoogstraal (1973) | |
| Bauline | Canada | ? | Hoogstraal (1973) | |
| Nugget | Australia | ? | Doherty et. al. (1975) | |
| Okhotskiy | USSR | ? | Lvov et. al. (1973) | |
| Cape Wrath | UK | ? | Main et. al. (1976); Nuttall et. al. (1982) | |
| Poovoot | USA | + | Yunker (1975) | |
| Unnamed | UK | ? | Nuttall et. al. (1984) | |
| Unnamed | Norway | ? | Saikku et. al. (1980) | |
| Unnamed | USA | ? | thomas et. al. (1973) | |
| Sakhalin | Sakhalin | USSR; USA | ? | Hoogstraal (1973); Lvov et. al. (1972) |
| Taggert | Australia | ? | Doherty et. al. (1975) | |
| Avalon | Canada | ? | Main et. al. (1976) | |
| Clomor | UK | ? | Main et. al. (1976); Nuttall et. al. (1982) | |
| Unnamed | USA | ? | Thomas et. al. (1973) | |
| Uukuniemi | Uukuniemi | USSR; USA; UK | ? | Nuttall et. al. (1984) |
| Zaliv Terpeniya | USSR | ? | Lvov et. al. (1973) | |
| Precarious Point | Australia | ? | St. George et. al. (1985) | |
| Unnamed | Norway | ? | Saikku et. al. (1980) | |
| Unnamed | USA | ? | Thomas et. al. (1973) | |
| Ungrouped | Paramushir | USSR | ? | Lvov et. al. (1976) |
| + = causes disease | ||||
| ? = not known if causes disease |
| Virus Group | Virus | Origin | Disease | References |
|---|---|---|---|---|
| Hughes | Solado | Ethiopia: Seychelles: | ± | Connverse et. al. (1975); Hoogstraal (1973): Hoogstraal et. al. (1976a): Main et. al. (1980) |
| Unnamed | New Zealand, UK | ± | Austin (1984); Nuttall et. al. (1984) | |
| Quaranfil | Johnson Atoll | Australia; New Zealand; Pacific | ? | Austin (1978); Clifford et. al. (1968); Hoogstraal (1973) |
| Abal | Australia | ? | Hoogstraal (1973) | |
| B | West Nile | USSR | ? | Gromashevsky et. al. (1973) |
| Saumarez Reef | Australia | ± | St George et. al. (1977) | |
| Sakhalin | Caspiy | USSR | ? | Lvov et. al. (1975) |
| Kemerovo | Baku | USSR | ? | Gromashevsky et. al. (1973) |
| Upolu | Upolu | Australia | ? | Doherty et. al. (1969); Hoogstraal (1973) |
| Aransas | USA | ? | Yunker et. al. (1979) | |
| Nyamanini | Midway | Midway Island | ? | Hoogstraal (1973) |
| A | Whataroa | New Zealand | ? | Ross (1971); Ross et. al. (1964) |
| = causes disease | ||||
| = possibly causes disease | ||||
| not known if causes diseases | ||||
| Mosquito-borne; survives in, and transmitted by O. capensis in laboratory |
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Fig. 1. Distribution of Ixodes uriae, Ixodes eudyptidis and Haemaphysalis longicornis
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Fig. 2. Distribution of Ornithodoros capensis