Reprinted from Australian Zoologist Volume 19 (1) 1976
Mosquitoes Feeding on Ectothermic Vertebrates:
A Review and New Data
HAROlDHEA
TWOlE and RICHARD SHINE'
Department of Zoology, University of New England, Armidale, N.S.W. 2351.
Australia
I
ABSTRACT
The literature on feeding by mosquitoes on ectothermic vertebrates is reviewed.
Original observations of the feeding of Uranotaenia argyrotarsis on Rana daemelii
on Cape York Peninsula are presented.
LITERATURE REVIEW
Gilett (1971) in a review of mosquito biology lists lizards, snakes and frogs
as hosts of filarial parasites transmitted by Anopheles quadrimaculatus and Aedes
taeniarhynchus, mentions a trematode lung fluke of frogs which is transmitted from
snails via larvae of Anopheles maculipennis to frogs (mosquito perhaps eaten by
frog), and indicates that lizards and frogs are known to have non-human
Plasmodium malarias which are presumably transmitted by mosquitoes. He also
mentions that Culex tarsalis feeds on snakes and cites his personal observations of
Coquillettidia fuscopennata feeding on a variety of vertebrates including frogs and
toads. Some species of Culex feed exclusively on ectotherms (Woke, 1937a).
I
Aedes aegypti has frequently been observed to feed on ectotherms. Yuill
( 1964) developed the ingenious technique of using individuals of this species as
micro-syringes for withdrawing small blood samples from Thailand geckos (Hemidactylus frenatus and Platyurus platyurus) for viraemia determinations of Japanese
encephalitis; in the laboratory this same species fed on two species of Puerto
Rican lizards, Anolis cristatellus and Anolis pulchellus (Fox and Bayona, 1964),
and on the Oriental lizards Gecko verticillata and Calotes sp. (ToumanofI, 1949);
the latter reported that Aedes albopictus also feed on G. verticillata and Calotes.
Woke (1937a, b) records A. aegypti feeding on a turtle (Terrapene carolina) and
on a frog (Rana clamitans). Gordon and Lumsden (1939) induced this species
to feed on frogs (Rana sphenocephala) but could not get Anopheles maculipennis
1. Present address: Dept. Biology, University of Utah, Salt Lake City. Utah, U.S.A.
Aust. Zool. 19(1), 1976
69
r;
HAROLD
HEATWOLE
and
RICHARD
SHINE
Fig. 1. Uranotaenia argyrotarsis feeding on Rana daemelii in the field. Note blood-engorged
mosquito piercing upper eyelid and the swollen appearance of the eyelid.
70
Aust. Zool. 19(1), 1976
MOSQUITOES FEEDING ON FROGS
or Culex molestus to do so. Although A. aegypti obviously has wide food
preferences, it does not feed on all species of ectothermic vertebrates, as in their
literature review of this species, Fox and Bayona (1964) mention reports of failure
to induce it to bite the lizard Urocentron azureum and some Brazilian geckos. Woke
( 1937a) also reports this species rejecting a lizard.
1
There
ectotherms
ectotherm
Toumanoff
than those
is disagreement as to the relative nutritive value of the blood of
and homeotherms for this species. Woke (1937a, b) found that
blood was equal or superior to that of some homeotherms whereas
(1949) found that A. aegypti feeding on lizards matured fewer eggs
feeding on humans.
Thomas and Ekland (1960) found that garter snakes (T hamnophis sirtalis
parietalis and T. ordinoides vagrans) experimentally infected with western equine
encephalitis virus could transmit it to a mosquito vector of the disease (Culex
tarsalis) even after having overwintered under artificial conditions subsequent to
infection with the virus. Gebhardt et al. (1964) further showed that at least four
species of snakes (Thamnophis elegans vagrans, T. sirtalis, Pituophis catenifer and
Coluber constrictor) served as natural overwintering hosts for the virus. Under
certain climatic conditions (especially high per cent of available sunshine in late
spring or early summer), favourable both for large mosquito hatches and viraemia
in infected snakes, epidemics resulting from transmission to warm-blooded hosts
might result.
Craighead et al. ( 1962) suggest that lizards (Ameiva, Cnemidophorus,
Basiliscus, Iguana) may play a role in the natural history of eastern equine
encephalitis in Panama. A number of papers have recently indicated that a number
of snakes, lizards and turtles can be experimentally infected by Japanese encephalitis virus or by western equine encephalitis virus and that natural reptilian
populations often have high levels of antibodies to such viruses (see review by
Shortridge et al. 1975). Hoff and Trainer (1973) in a review list 7 species
of Aedes, 6 species of Culex, 2 of Culiseta, and Mansonia perturbans and
Anopheles quadrimaculatus having been reported to feed on lizards, turtles and
snakes. To the above records Tempelis and Galindo (1975) recently added 4
species of Culex that feed predominantly on reptiles and mention that some
Deinocerites feed preferentially on ectotherms. Pinger and Rowley (1975) additionally record Aedes trivittatus as sometimes feeding on amphibians and reptiles.
,I(
..
The genus Uranotaenia seems to have a predilection for amphibian hosts.
Remington (1945) records Uranotaenia lowii feeding on the frog Rana sphenocephala, the tree frog Hyla cinerea, and the toad Bufo valliceps in the field, and
upon H. cinerea, B. valliceps, B. woodhousii fowleri and the salamander Desmognathus fuscus auriculatus in the laboratory; only the salamander reacted to the
bites. In laboratory tests, this mosquito rejected box turtles, two species of lizards,
and humans; it seems to be largely restricted to amphibians.
Aust. Zool. 19(1), 1976
71
----
-e
HAROLD
HEATWOLE
and
RICHARD
SHINE
.~
,
t
'\
I
,
L_,
Fig. 2. Uranotaenia argyrotarsis piercing the eyelid of Rana daemelii
whitish swelling on the frog's right eyelid.
72
in the field. Note the
Aust. Zoo!. 19(1), 1976
MOSQUITOES FEEDING ON FROGS
Marks (1960) records Uranotaenia albescens and Culex (Lophoceraomyia) sp.
biting the hylid frog Litoria caeruleaj this frog harbors a hemogregarine parasite
in its blood and Marks suggested these mosquitoes may act as the invertebrate host.
Her observations represent the only previous record of mosquitos feeding on
ectothermic vertebrates in the Australian region.
OBSERVATIONS AND DISCUSSION
I
\
I
\
The present paper reports still another species of Uranotaenia feeding on
amphibians, again from Australia. While collecting frogs at night along a small
stream 16 km north-west of Iron Range, Queensland, on 6 September 1972, we
noticed that a number of Rana daemelii were being bitten by mosquitoes. Many
of the mosquitoes were observed to be blood-filled. Nine mosquitoes were collected
and subsequently proved to be female Uranotaenia argyrotarsis Leceister. No other
species was observed on the frogs. We subsequently approached the frogs cautiously
using flashlights. The frogs remained motionless as long as the light was kept upon
them and they could be closely observed. Of the 12 specimens captured and about
three times that number observed but unmolested, nearly all were being bitten by at
least one mosquito (Fig. 1) and some had as many as six biting simultaneously.
The site of biting was always on the head. especially the upper eyelids, while no
mosquitoes were observed biting the body or legs although these areas were
exposed. The bites resulted in raised whitish swellings (Fig. 2). On no occasion
did any frog give evidence of being irritated by the insects or in fact to be even
aware of their presence.
We do not know how host-specific these mosquitoes are. However, we did
not observe them biting any other species of frog in the area and they did not
attempt to bite us although we were in close proximity to them for the several
hours we observed the frogs. It is certain that they are not restricted to R. daemelii
however, as the mosquito's geographic range is much wider than that of the frog.
U. argyrotarsis occurs in Malaya, the Moluccas, the Philippines, New Guinea, the
Solomon Islands and in Australia in the Northern Territory and north Queensland
(Marks, pers. comm.). R. daemelii is found only on Cape York Peninsula, Australia. Some herpetologists consider R. daemelii as a subspecies of Rana papua.
Even the range of R. papua in this broad sense is much smaller than the range of
the mosquito, encompassing only New Guinea and Cape York.
We had the opportunity to collect R. daemelii at a different locality. On 7
September 1972, 24 km east of Iron Range, we obtained frogs from around small
ponds and found that frogs are attacked in this area also. The swelling caused by
mosquito bites are ephemeral except on the eyelids where they persist for some
time, even in preservative. The preserved collections from the two sites were
Aust. Zoo!. 19(1), 1976
73
'I.
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HAROLD HEATWOLE and RICHARD SHINE
examined in November 1975. On the 12 frogs collected on the 6th, 5 (45%) had
one or both eyelids swollen; the corresponding value for the 40 collected by a
pond on the 7th was 18 (45%). Thus, the incidence of biting seems to be
similar in both localities. However, at the time of collection, no mosquitoes were
seen on the frogs in the second area despite the fact that the collection was made
at approximately the same time of evening as before. Weather conditions were
probably responsible. The 6th was a calm night and no wind was noticeable. The
7th was windy and this may have inhibited mosquito activity.
Our observations in conjunction with similar ones from the literature suggest
that feeding of mosquitoes on ectothermic vertebrates may be more common. than
generally realised. There may be economic and! or medical implications. A possible
benefit which might accrue from examination of mosquito-transmitted diseases to
amphibians could be the selective control of introduced amphibian pests in
Australia
such as the cane toad (Bufo
marinus).
Studies are badly needed which survey (1) the range of hosts attacked by
different species of mosquitoes, (2) the range of mosquito species biting particular
species of amphibians and reptiles, (3) the diseases and! or parasites transmissible
between mosquitoes and ectotherms, and (4) the environmental factors related to
such transmission. Also studies evaluating ectotherms as potential reservoirs of
viral or other mosquito-borne diseases attacking man, domestic animals or wildlife
would be extremely valuable.
"ACKNOWLEDGEMENTS
We are grateful
support of part of
to Miguel Heatwole
of the mosquitoes,
tions, and to Audry
to the Department of Za,ology, University of New England, for financial
the Cape York Expedition during which these observations were made,
and Alana Young for assistance, to Dr. E. N. Marks for identification
to Professor A. F. O'Farrell and J. Parmenter for criticism and suggesHeatwole for aid in preparation of the manuscript.
REFERENCES
CRAIGHEAD,
host
for
J.E., A. SHELOKOV
eastern
equine
The lizard: a possible
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A iides aegypti feeds on lizards in Puerto Rico. J. Econ.
encephalitis
& P. H. PERALTA
virus
in Panama.
(1962).
Amer.
J. Hygiene
FOX, l. & l. G. BA YONA (1964).
Ent. 57, 417-418.
GEBHARDT,
L. P., G. J. STANTON, D. W. HILL & G. C. COLLETT (1964). Natural
overwintering hosts of the virus of western equine encephalitis. New England J. Med.
271, 172-177.
GlLETT, J. D. (1971). Mosquitoes. Weidenfeld & Nicholson, London, 274 pp.
GORDON,
R. M. & W. H. R. LUMSDEN
(1939). A study of the behaviour of the
mouth-parts
of mosquitoes when taking up blood from living tissue; together with
some observations
on the ingestion of microfilariae.
Ann. Trap. Med. Parasit. 33,
259-278.
74
Aust. Zool. 19(1), 1976
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MOSQUITOES FEEDING ON FROGS
HOFF, G. & D. O. TRAINER (1973). Arboviruses in reptiles: isolation of a Bunyammera
group virus from a naturally infected turtle. J. Herpetology 7, 55-62.
MARKS, E. N. (1960). Mosquitoes biting frogs. Aust. J. Sci. 23, 89.
PINGER, R. R. & W. A. ROWLEY (1975). Host preference of Aedes trivittatus (Diptera:
Culicidae) in central Iowa. Amer. J. Trop. Med. Hygiene 24, 889-893.
REMINGTON, C. L (1945). The feeding habits of Uranotaenia lowii Theobald (Diptera:
Culicidae). Ent. News 56, 32-68.
TEMPELIS, C. H. & P. GALINDO
(1975). Host-feeding patterns of Culex (Melano
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TOUMANOFF,
C. (1949) . L'hemophagie variee et l'activite reprodllctrice chez A fides
aegypti L. et Aedes albopictus Skuse. Bull. Soc. Pathol. Exotique 42, 466-470.
THOMAS, LA. & C. M. EKLUND
(1960). Overwintering of western equine encephalomyelitis virus in experimentally infected garter snakes and transmission to mosquitoes.
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WOKE. P.A. (1937b). Comparative studies of the blood of different species of vertebrates
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