Kemp, D.H.

St. George, T. D

University of Queensland eSpace

Paper 1.6
The isolation of arboviruses including a new flavivirus and a new
bunyavirus from Ixodes (Ceratixoides) uriae (Ixodoidea: Ixodlidae) collected
at Macquarie Island, Australia, 1975-1979.
American Journal of Tropical Medicine and Hygiene 34: 406-412 (1985)
by
St. George, T.D., Doherty, R.L., Carley, J.G., Filippich, C Brescia, A., Gasals, J
Kemp, D.H. and Brothers, N
I initiated the project to isolate more viruses from Antarctic bird ticks. r~igel Brothers
, collected the ticks and supplied supporting data. Dr D.J. Griffiths, Dr f\~.M. Bryden,
" Dr G. W. Johnstone and Dr Ian Morgan also collected and transported ticks. The ticks
" were prepared for inoculation into mice by Neville Hunt and Steven Davis. I substituted
" the inoculation of tissue cultures for virus isolation for the traditional mouse brain
" isolation as a much more economical technique. Dr D.H. Kemp identified the ticks. The
" initial identification procedures were carried out at the Queensland Institute of Medical
" Research.
" The "new" virus identifications were carried out at the Yale Arbovirus R~esearch Unit.
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Ticks and arboviruses in Australia and its territories
The Postgraduate Committee in Veterinary Science, University of Sydney,
Proceedings No. 66 (1982) pp. 129-134.
St. George, T.D. and Kemp, D.H.
I contributed the expertise on ticks and their biology and Table 1. The balance of the
research came from Dr St.George's group who were responsible for the rest.
"
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D.H. : v~~. ~~
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T.D.
78.
Paper 1.6
THE UNIVERSITY OF SYDNEY
THE POST-GRADUATE COMMITTEE IN VETERINARY SCIENCE
( ,
REFRESHER COURSE FOR VETERINARIANS
PROCEEDINGS No. 60
COURSE ONREFRESHER
AD V ANCES IN VETERINARY
198217-21,May
Paper 1.6
60:130
T.O. St.George
barely out of water.
The few arboviruses that have been isolated are Upolu, Johnston Atoll and Saumarez Reef
and these have come from O. capensis. There have been reports of this tick attaching to humans,
as does ~ loculosum. It-rs quite uncertain whether the illness associated with the attachment
Paper 1.6
60:129
TlCKS AND ARBOVIRUSES IN AUSTRALIA AND ITS TERRITORIES
~ T .0. ST .GEORGE and D.H. KEr~p
INTRODUCTION: The normal concept of Australia is of a large mainland with an island
state, Tasmania,.t~ the south o~ th~ e~ster~ side. This view requires a considerable expansion
as much of the 11m1ted success 1n f1nd1ng V1ruses carried by ticks has been with ticks co11-
~cted outside this limited area. None of Australia's states are landlocked and all have
ls1ands c~ose offshore. Queensland especially has numerous islands extending in a broad zone
be'.(ond thlS out to the edge of the continental shelf, and to the waters close to Papua-New
Gu1nea. Two s~ates own islands even further out, Lord Howe Island (N.S.W.), and Macquarie
Island (Tasmanla). The Commonwealth has taken possession of various islets and cays in the
Coral Sea among them Cato Island, Saumarez Reef, Frederick Reef, and in the Indian Ocean vari-
ous reefs (e.g. Ashmore Reef),p1us Cocos and Keeling Islands and Christmas Island, and in the
Southern Ocean, Heard and MacDonald Islands; plus a large piece of the Antarctic mainland.
Many of these possessions are uninhabited and unused. Others have manned, or unmanned weather
stations. Very commonly seabirds use the islands for resting or nesting sites, and various
migratory species of birds make use of them or pass by them. These islands will be referred to
later.
On the mainland the cattle tick (Boochi1us microc1us) has attracted most attention because
of its economic effect. It has not been found to carry arboviruses and is the least suitable
species of tick of the numerous Australian tick species to do so, as it is a one host tick. An
arbovirus would need to be transmitted transovaria11y to pass from cow to cow via B. microc1us.
There is the odd transfer of ticks from cow to cow with transmission of Anac1asma Tn this way
but it is probably too infrequent for maintaining virus transmission. There are a variety of
other ticks which attach to vertebrates, in their larval, nymphal and adult stages. Thus, in
addition to the possibility of transovaria1 transmission they can transmit viruses in success-
ive development stages on different hosts of the same, or different species. A selection of
Australian ticks is listed in Table 1.
The duration of the life cycle of a particular tick species depends on the species of
tick, the availability of vertebrates to provide a blood meal, and climate. In tropical areas,
a tick can complete its life cycle in weeks, or months. At the other extreme an arctic tick's
life cycle may extend over several years and some Ornithodoros ticks may survive for 6-7 years
before finding another host. In either instance, the tick provides an excellent mechanism
whereby an arbovirus can be carried over from one season to another, and to a new generation of
vertebrate hosts. In other parts of the world, arboviruses are maintained in overwintering
ticks which transmit them to a vertebrate in the following spring. Until the next following
winter in addition to tick transmission there is major spread via mosquitoes. These mosquitoes
die out in the autumn, leaving the tick to maintain the virus again.
The Australian ticks belong to two families and a number of genera. Their principal
vertebrate hosts range widely through mammals, birds and reptiles. Some ticks are very speci-
alized, such as B. microclus, others will attach to a range of vertebrates, e.g. Ixodes ho10-
~. Man and-rhe domestic animals can be major hosts, or sometimes are quite accidentaJly
attacked and are not necessarily useful to the tick to complete its lire cycle. The tick can
damage its host in various ways; the bite can be painful; the blood meals taken in by a heavy
infestation can cause anaemia; some ticks excrete toxins in their saliva which are injected
into the wound made by the ticks' mouthparts; ticks can transmit protozoa, rickettsiae or
viruses. Only arboviruses and certain species or tick will be the subject of further consider-
ation. There are other species of tick additional to those in Table 1, which may be found in
usual or unusual hosts, but most, if not all, viruses known to be associated with those ticks
have been listed. There is no known association with a virus for most species of ticks on the
list. Bird associated ticks form most of the substance of this article.
An arbovirus is a virus which replicates in a vertebrate and an invertebrate host. The
~ormal cycle is vertebrate-invertebrate-vertebrate. This is distinct from viruses like myxo-
~~tosis which are moved mechanically from one vertebrate host to another on biting mouthparts,
I/:thout replication. The "arbo" in the name arbovirus is an abbreviation for "arthropod borne"
l':rus.
..TICKS OF THE CORAL SEA: The important species of ticks here are Ornithodoros caoensis and
~~ loculosum. These ticks live on various cays and islets that sea birds use. The tick
Paper 1.6
60:131
-T.D. St.George -
of such ticks is due to a toxic effect, or an infectious agent carried by the tick. Undoubted-
ly technicians building and servicing automated weather stations on these cays have been ill
following an attack by ticks. Saumarez Reef virus is a flavivirus (older synonym "group B"),
which is a group of viruses with many members pathogenic for man so human infection is quite
possible.
It is also quite uncertain whether the die-back that occurs in sea birds on some cays has
an'.! relevance to the ticks, or the as~ociated arboviruses. Small serological surveys have
shown that seabirds do become infected by the viruses so infection certainly occurs. There is
scope for more work. With the development of national parks in the area, reports of attachment
of ticks to man and his companion animals will increase.
TASMANIAN SEA BIRD TICKS: The distance from Saumarez Reef to Tasmania is approximately
2500 km. There is a link between the two areas via sea birds. Saumarez Reef virus (a flavi-
virus) was isolated from Ixodes eudyptidis ticks collected from two dead Silver gulls (~
novaehollandiae) collected by Mr. R.H. Green of the Queen Victoria Museum, Launceston, about
the same time as the ticks of a different species, and family, from which the same virus came
were collected in the Coral Sea. Four of 14 sera from silver gulls in the Launceston area had
neutralising antibodies in their sera. Thus again there was a link between the virus and the
gull populations, but again, there is no direct evidence to connect the virus, or the ticks,
with the deaths of the gulls.
THE ANTARCTIC TERRITORIES: The interest in the ticks and possible viruses in the Antarc-
tic region was stimulated by a visit to Australia of Professor D.K. Lvov, of the Ivanovsky
Institute, Moscow. He described the very high infection rate of viruses in ticks of the Behring
Strait birds. It seemed that an analagous situation should exist in the Antarctic. According-
ly, with the cooperation of various scientific visitors to Macquarie Island, ticks were coll-
ected from numerous sites on the island between 1972 and 1979. All the ticks were or the
species Ixodes uriae, most from habitats of Royal, Rockhopper or King Penguins. The viruses
isolated~N~, Taggert and flaviviruses. The rate of inrection of the ticks was high.
The e'/idence that the viruses actually infected Penguins came from neutralisation tests on
Penguin sera collected on Macquarie Island. Such serological surveying that has been done was
quite inadequate to determine what birds, other than Penguins, were infected. Tests on.ser~ of
members of an Antarctic expedition who suffered a febrile illness were negative for ant1bod1es
to Nugget and Taggert virus. Thus, these two viruses have not been linked to a human infection.
The really significant part of the story is that both the ticks and the arboviruses on
Macquarie Island have close relatives in the a~ctic regions, but ~ot in th~ tro~ics.and.sub~ro-
pics. The tick Ixodes~ certainly occurs 1n the northern ~em1sph~re, 1ts.d1str1b~t10n 1~
circumpolar, and it is recorded under another name, ~~, 1n RUSS1a. It ~s assoc1a~ed w1th
sea birds. The viruses Nugget and Taggert, belong to t.~e Kemerovo and Sakhal1n serologlcal
groups respectively. As these names suggest, related viruses occur in Russia. The link be-
tween Macquarie Island Penguins and sea birds of the subarctic cannot be a very direct one..
Penguins, with perhaps the exception of one species in the Galapagos Islands, do not °7c~r 1n
the northern hemisphere. Some of the migratory birds which travel to the northern Pac1f1c do
not touch land there. The distribution of these two viruses, and the flaviviruses of Macquarie
Island in the Antarctic is not really known, so speculation without further information is not
really profitable. The close relationship of both viruses and ticks does suggest that exchange
of genetic material must occur.
LAND BIRD TICKS: The only isolations of viruses from ticks collected on the mainland.were
from bird rookeries near Brisbane and Dar'liin. The rookery near Brisbane was clearly assoc1ated
with land birds.
CSIRO 704 VIRUS: This virus was isolated from ~ robertsi ticks collected in a cattle
egret (Ardeola~) colony about 100 km west of Br~sbane. The.ticks wer~ plentiful un?er bark
of trees and debris, and were also found on young b1rds. The v1rus was 11nked to the b1rds by
finding antibodies to it in 8 nestlings. The virus is being classified at present at the Yale
Arbovirus Research Unit in New Haven, Connecticut.
The cattle egret is a large white bird often seen feeding near cattle. It has an inter-
esting, if uncertain, history. It is a comparative newcomer to most or Australia. The uncer-
Paper 1.6
60:l32
-T.D. St.George -
TABLE 1
A Selected List of Ticks Found in Australia or its Territories
3 Bandicoot (possum, dog, cattle,
sheep, horse, human)
Nil
3 Many native animals (dog, sheep,
horse)
Many seabirds
[xodes holocyclus
TAUStral~ysis tick)(CSIRQ Handbook of Co"",on
Names)
Ixodes tasmani
TEOiiiiiOn Marsup-i a1 Ti ck)
~~ 3
3 Penguins (many seabirds)
Nii
Nugget, Taggert
CSIRQ 122
Saumarez Reef
3 Penguin (other seabirds, man) Nil
3
3
Seabirds and land birds.
Bats
Nil
Nil
1 Cattle (deer, sheep) Nil
Dogs (man)3 Nil
3 Nil
3 Nil
3
Kangaroo (cattle, sheep, horses,
dogs, man)
Pig (man, immatures on birds and
rodents)
Sea birds (man) rlj 1
3 Cattle (sheep, horses, dogs, man) Nil
3 Especially ground dwelling birds Nil
3+ Saumarez Reef, Opulu,
Johnston Atoll
Nil3+
Gulls, penguins, terns and other
seabirds
Kangaroos (horses, dogs, man)
3+ Stork, Egret, Cormorant
(domestic poultry)
Domestic poultry
Kao Shuan, CSIRO 704
Ixodes eudyptidis
~ealand seabird tick)
Ixodes kohlsi
TKO"iil's -s-e-abi rd tic k )
~ auritulus
Ixodes simolex
"'{"6"attick)
Booohilus microolus
(Cattle tick)
Rh i oi ceDha 1us s an~ ineus
(Brown dog tick).
Amblyonma triguttatum
(Ornate Kangaroo Tick)
~blyonma cyprium
(Feral pig tick)
~blyonma loculosum
(Seaoird tick)
~~emaohysa1is longicornis(bush tick)
HaemaDhysalis doenitzi
(Doenitzl Oriental-Australian
bird haemaphysalid)
Ornithodoros caoensis
(Seabird soft tick)
Ornithodoros gurneyi
(Inornate Kangaroo Tick)
~ robertsi
(Rooertls bird tick)
~ persicus
(fowl tick)
3+ Nii
* Occasional host records shown in brackets.
Paper 1.6
60:133
-T.D. St.George -
tainty is whether it arrived as a migrant, via the islands to the north, or is descended from
18 egrets imported to the Kimberleys from India by graziers in 1933 to control cattle ticks
(unsuccessfully) or perhaps both ways. The birds range as far south as Tasmania in the east
and the south west of Western Australia, on the other side of the continent.
Mortalities do occur in egret colonies (Niel McKilligan, unpublished data), but nothing is
known of the pathogenicity of the virus CSIRO 704. Since A. robertsi sometimes invades back-
yard poultry houses, infection of domestic poultry is theor;tically possible.
Kao Shaun virus, a virus which belongs to the Deri Ghanzi Khan serological group was
isolated from this same species of tick, ~ robertsi, collected by H. Hoogstraal in a large
rookery in mangroves near Darwin. This particular rookery was used as a nesting place or
visited by a variety of bird species including cormorants, ibis and egrets, so has land and sea
associations. ~ robertsi is widespread in south east Asia. The finding of this tick on a
lighthouse beacon on Young Reef, Great Barrier Reef has interesting implications for introduc-
tion of the tick and its viruses to Australia. Most, but not all, of the other viruses of the
Deri Ghanzi Khan group in other parts of the world are associated with bird ticks.
POTENTIAL FOR THE FUTURE: The very few isolations of arboviruses from Australian ticks
gives perhaps a false idea of the potential for them to act as vectors. The ticks from sea
birds or their habitats has been most productive in relation to the small effort that has been
invested by investigators, whose main line of work is concerned with viruses carried by mos-
quitoes or culicoides. In recent years, very little has been done to investigate whether ticks
of livestock, marsupials or reptiles carry arboviruses. It is hard to imagine that this eco-
logical niche is not occupied, as it is on other continents.
The first problem is to obtain ticks for virus isolation, than to have them identified.
Ticks can be sent to Dr. D.H. Kemp of CSIRO Long Pocket Laboratories, P.B. No.3, P.O., Indoor-
oopilly, Queensland 4068. A large representative collection of Australian Ticks was prepared
by Dr. F.H.S. Roberts, and is maintained at these laboratories. Ticks, other than cattle ticks
which are in good order can be sent alive to the above address. They should be in a container
with a small amount of moisture on a Kleenex tissue. They should not be crowded as their
metabolT;;byproducts will otherwise over~helm them in transit. Data on where, when, and by
whom they were collected will assist considerably. The host, or habitat, from which they came
should also be stated. After identification suitable specimens can be processed for virus
isolation.
If the viability of the tick is uncertain, it should be preserved in alcohol and for~arded
for identification with the same data relating to origin. Due care should be taken that the
alcohol will not leak in transit.
In contrast to many other viral topics dealt with in this refresher course, most of the
basic work is yet to be done. What has been described here represents only a small start. In
the near future, further work on the bird ticks, especially ~ auritulus, ~~,
Amblyomma loculosum and ~ robertsi, looks the most promising.
The ~ robertsi infestation of cattle ~grets was discovere~ by Dr. .Neil Mc~illigan ?f
the Darling Downs Institute of Advanced Educatl0n and we are grateful to hlm for hlS help wlth
this work.
SELECTED REFERENCES
BOURNE. W.R.P., BOGA~I. J.A.. BULLOCK. D.. DIAMOND, A.W. and FEARE. C.J. (1977). Abnormal
terns. sick sea and shore birds. organochlorines and arboviruses in the Indian Ocean.
Mar. Pollut. Bull. B: 154-158.
CONVE~~HO~RAAL. H.. MOUSSA. M.I.. KAISER. M.~I.. CASALS. J. and FEARE. C.J. (1976).
Aride virus, a new ungrouped arbovirus infecting Amblyomma loculosum ticks from roseate
terns in the Seychelles. Archs Virol. 50: 237-240.
DOHERTY, R.L.. WHITEHEAD, R.H.,~E~J~-and JOHNSON. H.N. (1969). Isolation of viruses
from Ornithodoros cacens;s Neumann from a tern colony on the Great Barrier Reef, NorthQueensland. ~ ~ ~ ~!: 363-364.
Paper 1.6
60:134
-T.D. 5t.George -
DOHERTY, R.L., CARLEY, J.G., MURRAY, M.D., MAIN, A.J.Jr., KAY, B.H. and DOMROW, R. (1975).
Isolation of arboviruses (Kemerovo group, Sakhalin group) from Ixodes uriae collected at
Macquarie Island, Southern Ocean. ~ ~ ~ ~ ~ ~~: 521=526 HOOGSTRAAL, H., KAISER, M.N. and McCLURE, H.E. (1974). The subgenus Persicarqas (Ixodoidea:
Argasidae:~) 20. A. (P.) robertsi parasitizing nesting and wading birds and domestic
chickens in the AustraTran-and Oriental regions, viral infections, and host migration. J.med. Ent. 11: 513-524. --
HOOGS~L-:1l:,-wASSEF, H.Y., CONVERSE, J.D., KEIRANS, J.E., CLIFFORD, C.M. and FEARE, C.J.
(1976). Amblyomma 10culosum (Ixodoidea: Ixodidae): identity, marine bird and human
hosts, virus infection and distribution in the southern oceans. Ann. ent. Soc. Am. 62:
3-14. READER'S DIGEST. (1977). Complete~Qf Australian~. Reader's Digest Services, Sydney.
ROBERTS, F.H.S. (1970). Australian Ticks. CSIRO, Australia.
5T.GEORGE, T.D., STANDFAST, H.A., DOHEJrrf, R.L., CARLEY, J.G., FILLIPICH, C. and BRANDSMA, J.
(1977). The isolation of Saumarez Reef virus, a new flavivirus, from bird ticks Ornitho-
~ capensis and Ixodes eudyptidis in Australia. ~ ~ ~ ~ ~ ~ ~§:
493-499.


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