Front Cover

Group Title: Reptile tick Aponomma gervaisi (FLMNH Bulletin v.35, no.1)
Title: The Reptile tick Aponomma gervaisi
Full Citation
Permanent Link: http://ufdc.ufl.edu/UF00099067/00001
 Material Information
Title: The Reptile tick Aponomma gervaisi (Acarina : Ixodidae) as a parasite of monitor lizards in Pakistan and India
Physical Description: p. 1-34 : ill. ; 23 cm.
Language: English
Creator: Auffenberg, Walter
Auffenberg, Troy
Donor: unknown ( endowment )
Publisher: University of Fla.
Place of Publication: Gainesville, Fla.
Publication Date: 1990
Copyright Date: 1990
Subject: Ticks   ( lcsh )
Monitor lizards -- Parasites -- Pakistan   ( lcsh )
Monitor lizards -- Parasites -- India   ( lcsh )
Genre: bibliography   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
non-fiction   ( marcgt )
Spatial Coverage: Pakistan
Bibliography: Includes bibliographical references (p. 33-34).
General Note: Cover title.
General Note: Abstracts in English and Spanish.
General Note: Bulletin of the Florida Museum of Natural History, volume 35, number 1, pp. 1-34
Statement of Responsibility: Walter Auffenberg, Troy Auffenberg.
 Record Information
Bibliographic ID: UF00099067
Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: oclc - 22416439
issn - 0071-6154 ;

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Full Text

of the



Walter Auffenberg
Troy Auffenberg

Biological Sciences. Volume 35. Number 1. Do. 1-34





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ISSN: 0071-6154


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Walter Auffenberg and Troy Auffenberg*


The common tick of monitor lizards (Varanus) in Pakistan, India, and Sri Lanka is
Aponomma gervaisi. In nature it occurs on only one of three native varanid species (V.
bengalensis), in spite of the fact that both remaining varanid species in the main area investigated
(V. griseus and V. flavescens) are ecologically and geographically syntopic with Varanus
bengalensis at the two extreme ecological conditions in which the latter is found. Individuals of
Aponomma gervaisi do not use their major host (Varanus bengalensis) at random. The level of
infestation varies between different localities, between different seasons of the year, and between
hosts of different sizes.
Attachment sites of adult male and female Aponomma gervaisi are very specific. Males
occur mainly on the lateral surfaces of the tail and/or in a shallow, medioventral depression
immediately behind the cloaca; adult females are usually attached in the axillary or a nearby
region. Larval and nymphal site preferences are less distinct than those of the adults, and
attachment is probably partly determined by competitive factors. Breeding takes place at the
adult female attachment sites.
It is suggested that there is an advantage in adult male ticks aggregating in specific small
areas due to the proportionally greater effect of several closely packed individuals on the hosts
immune response system, particularly in reference to lymphoid cell density. These cells and body
fluids seem to comprise the main food of the males. Male attachment sites are often located in
areas of high potential abrasion. Females tend to attach in protected sites. Since females are
mainly blood-sucking, there is probably an advantage in dispersed attachment patterns.
Haemaphysalis sindensis Bilques and Masood is placed in the synonomy of Aponomma

* Walter Auffenberg is Curator of Herpetology, Florida Museum Natural History, University of Florida, Gamesville FL 32611;
his son Troy Auffenberg is a graduate student at the Department of Microbiology and Immunology, College of Medicine,
University of Kentucky, Lexington, KY 40536-0084.

AUFFENBERG, W., and T. AUFFENBERG. 1990. The reptile tick Aponomma gervaisi
(Acarina: Ixodidae) as a parasite of monitor lizards in Pakistan and India. Bull. Florida Museum
Natural History, Biol. Sci. 35(1):1-34.



La garrapata comuin de los lagartos monitors (Varanus) en Pakist6n, India y Sri
Lanka es Aponomma gervaisi. En condiciones naturales se le encuentra s61o en una de las tres
species nativas de varanos (V. bengalensis), a pesar de que las otras dos species que existen en
el area estudiada son sint6picas ecol6gica y geogrAficamente con Varanus bengalensis en los dos
extremos de condiciones ecol6gicas en los que esta uiltima especie habitat. Los individuos de
Aponomma gervaisi no utilizan a su hudsped primario (Varanus bengalensis) al azar. El nivel de
infestaci6n varia entire localidades diferentes, entire estaciones del afio, y entire hu6spedes de
diferentes tamahios.
Los sitios de fijaci6n de las hembras y machos adults de Aponomma gervaisi son muy
especificos. Los machos se encuentran principalmente en las superficies laterales de la cola y/o
en una depresi6n medioventral superficial inmediatamente detrAs de la cloaca; las hembras
adults usualmente se encuentran fijadas en o cerca de la regi6n axilar. Los sitios preferidos por
las larvas y ninfas son menos definidos que los de los adults, y la fijaci6n esti en parte
probablemente determinada por factors competitivos. El apareamiento ocurre en los sitios de
fijaci6n de las hembras adults.
Se sugiere que existe una ventaja en que los machos adults formen agregaciones en
areas especificas pequefias, debido al efecto proporcionalmente mayor de various individuos
agregados cerca unos de otros sobre el sistema de respuesta inmune del hudsped,
particularmente en referencia a la densidad de c6lulas linfoides. Estas c6lulas y fluidos
corporales parecen representar el principal alimento de los machos. Los sitios de fijaci6n de los
machos estan frecuentemente localizados en areas de alto potential de abrasi6n. Las hembras
tienden a fijarse en sitios protegidos. Debido a que las hembras son principalmente chupadoras
de sangre, probablemente es ventajoso el fijarse en patrons dispersos.
Se coloca a Haemaphysalis sindensis Bilques y Masood en la sinonimia de Aponomma


Introduction........................................... .............................................................. 3
A cknowledgem ents.......................................................................................... 7
M methods ............................................................ ................................................................................ 7
R esults.............................................................................. ...................................................................... ... 9
.......Identity of T icks ........................................................................................................................ 9
.......Percent Infestation................... ................................................................................................. 10
.......N um ber T icks/H ost............... ................................................................................................... 13
.......Size and C olor ................................................................................ ........................................... 15
.......Patterns of Site A ttachm ent............................................................................. ....................... 18
.....Subsurface Attachment Details................... ........................................................... 22
.......Seasonal Patterns of Infestation.................... ............................................................. 25
.......L ife H history ...................................................................................................... .......................... 27
Conclusions and D iscussion.......................................................... .................................................. 28
Literature C ited ............................................................................................... ............................ 33



In spite of the fact that ticks are commonly encountered on reptiles,
relatively little work has been conducted on the attachment site preferences of
the species that prefer these hosts. The fairly recent contributions of such
workers as C. M. Bull, R. H. Andrews, T. N. Petney, and their associates attest
to the fertility and importance of this field of investigation. However, most of
these papers address the question of the role of competition in host attachment
sites of parapatric ixodid tick species (i.e. Bull, Sharrad, and Petney 1981;
Andrews and Petney 1981; Andrews, Petney, and Bull 1982). The question of
site attachment specificity within members of a single tick species has been
addressed less often. Of particular importance is the recent documentation of
sexual separation on reptilian hosts among a very few species of the ixodid
genera Aponomma and Hyalomma (one species each, see Petney and Al-
Yaman 1985) and Amblyomma (one species, T. Auffenberg 1988). The
conclusion in both these studies was that adult female ticks attach in the
anterior part of the body and adult males on the posterior part.
Of particular interest is the work on Amblyomma helvolum (T.
Auffenberg 1988), for site attachment analyses included two sympatric varanid
lizard species (Varanus olivaceus [as V grayi in the publication] and V. salvator,
both in southern Luzon, Philippine Islands). Several important conclusions
were drawn regarding host site attachment preferences of this ectoparasite (an
Aponomma-like species of eastern India, Southeast Asia and the Indo-
Australasian Archipelago); namely, Amblyomma helvolum is apparently a
varanid lizard specialist, for this parasitic species is common only on species of
this lizard family, and only on varanids is a definite site attachment pattern
discernible. The attachment pattern is one in which male Amblyomma
helvolum are located more posteriorly on the host than female ticks of the
same species. More intriguing is that, while female ticks are most often
attached in the axillary region of both host species investigated, the males are
mainly attached at the base of the claws on the hind feet of the host Varanus
olivaceus, and on the median part of the chest and in a medioventral
depression at the base of the tail on V salvator. Thus, the host species seems
to determine what particular area of the posterior part of the body will be
infested with adult male Amblyomma helvolum.
More recently we had an opportunity to study the site attachment
patterns of several other species of geographically sympatric varanid lizards in
India and Pakistan during the senior author's work on the behavioral ecology
of local monitor lizards. None of these varanids represented the same species
as the Philippine ones, nor was the parasite congeneric to that in the earlier
study. Here then was an opportunity to examine spatial distribution of still
another reptile tick on the skin surfaces of three congeneric sympatric hosts.


The tick we studied was Aponomma gervaisi (Lucas 1847). This ixodid
species has a geographic range from Yeman to the southern tropical parts of
Nepal and south through all of the Indian Peninsula to Sri Lanka (more
eastern localities in the early literature seem to be misidentifications, as are
early records from Africa). We found it at elevations from nearly sea level to
700 m; the highest elevational record we have found in the literature is 1000 m
(southern India, Siddappaji and Channabasavanna 1981). The distribution
(Fig. 1) reflects a common zoogeographic pattern among faunal elements
associated with Afro-Indian tropical deciduous forests.
In Pakistan and most of India, Aponomma gervaisi is geographically
sympatric (Figs. 1, 2) with three species of varanid lizards, i.e. the Bengal
monitor Varanus bengalensis, desert monitor V. griseus, and yellow-headed
monitor V. flavescens. These three lizard species are sympatric in at least parts
of their respective geographic ranges. However, V. griseus and V. flavescens
occur in ecologically divergent habitats. The former lives mainly in arid sandy
places (Auffenberg et al. in press a) and the latter in marshes (Auffenberg et
al, in press b). V. bengalensis is found in both of these habitats, though less in
desertic situations. However, if the sandy tracts are within several hundred
meters from water, V. bengalensis also occurs there. Thus V bengalensis is
ecologically sympatric at opposite ends of its environmental spectrum
(Auffenberg MS ) with each of the remaining species (Fig. 3). It is also
sympatric with Varanus salvator, which ranges from northeastern India
eastward through all of Southeast Asia and most of the Indo-Australian
The few references to Aponomma gervaisi on the Indian subcontinent
have all been short, stressing geographic range, morphology, or host species.
No detailed work has been published on parasite density or seasonal
abundance. The only previous mention of any reptile ticks in Pakistan is by
Bilques and Masood (1973), who described a new species, Haemaphysalis
sindensis, from a single individual of Varanus monitor (= V. bengalensis in
current usage) from Sind Province.
The genus Aponomma is a member of the family Ixodidae, currently
believed to be comprised of about 630 species, and the subfamily
Amblyomminae, of 126 species (Aponomma and Amblyomma only). The
subfamily parasitizes mainly reptiles. The genus Aponomma is comprised of
24 species. Of these, 22 can be placed in the < strict-total> type of tick-host
specificity, as defined by Hoogstraal and Aeschlimann (1982), being found
primarily on reptiles; in Asia the hosts are large snakes and varanid lizards.
Several Aponomma species have been reported to parasitize Varanus
bengalensis (including the subspecies V b. nebulosus). These are A. varanensis,
A. gervaisi, and A. laeve. The latter is a tick of generally mesic forest habitats
of the western Ghats of India and Sri Lanka, Aponomma varanensis occurs in
evergreen to deciduous forests from Sri Lanka and eastern India through


Figure 1. Geographic location of specimens of Aponommna gervaisi examined during this study
(dots). The general distribution of Aponomma varanensis is shown as a cross-hatched area.

Figure 2. The general geographic ranges of Varanus bengalensis bengalensis (cross-hatched) and
V. b. nebulosius (dots) on the Asian mainland.




Figure 3. The general habitat relationship of the three varanid lizards within the range of
Aponomma gervaisi.

Southeast Asia to the Indonesian Archipelago. A. varanensis is found primarily
on land turtles and varanid lizards. Aponomma gervaisi is a reptile tick of
generally xeric habitats on the basis of available locality records--usually Acacia
and other deciduous forests (Yeman to and including southern Nepal, the
Indian peninsula, and Sri Lanka). It characteristically parasitizes mainly
Varanus bengalensis.1 Both A. gervaisi and A. varanensis have been most
commonly and consistently associated with Varanus bengalensis bengalensis and
Varanus bengalensis nebulosus respectively. The borders of the ranges of both
the ticks and the lizards are more or less coincident (compare Figs. 1 and 2).
Previously Aponomma gervaisi has been reported from Varanus
bengalensis by Sharif (1928) from several localities throughout peninsular India
and Ceylon, Bhat and Sreenivasan (1981) in western peninsular India,
Hoogstraal and Rack (1967) and Nagar et al. (1977), in northern India,
Siddappaji and Channabasavanna (1981), Stephan and Rao (1979) in southern
India, Warburton (1910) in eastern India. and Deraniyagala (1953) and
Seneviratna (1985) in Sri Lanka. Haemaphysalis sindensis, described as a new
species by Bilques and Masood (1973), was found on an individual of Varanus
bengalensis from near Karachi, Pakistan. This name should be referred to the
synonomy of Aponomma gervaisi (see below). Other species reported as
(occasional) hosts of A. gervaisi are provided in Table 1. These comprise only
one species of lizard and several of rather large snakes.

1 A. varanensis has been called A. quadratum, A. barbouri, A lucasi, and as a variety of A. gervaisi
in the older literature. A. varanensis and A. gervaisi are possibly subspecifically related, though
this and other nomenclatorial questions will have to await future study of material from many
localities. As Hoogstraal and Rack have stressed (1967), the Asiatic species of Aponomma are in
need of critical study. The most recent taxonomic review of the entire genus is by Kaufman


Table 1. Hosts (excluding Varanus bengalensis = V. cepidianus]) from which Aponomma gervaisi
has been reported.

Host Source

Indian Garden Lizard, Calotes versicolor Warburton 1910

"snake" Nagar et al. 1977
Rock python (Python molurus) Wall 1921, Seneviratna 1985
Dhaman, Ptyas mucosus Warburton 1910 (as Zamenis mucosus)
Common Cobra, Naja naja Sharif 1928; Warburton 1910;
(= N. tripudians) Siddappaji and Channabasavanna 1981
Seneviratna 1985.
King Cobra, Ophiophaga hannah Bhat and Sreenivasan 1981;
Stephan and Rao 1979

The present study was undertaken mainly to determine whether in
Aponomma gervaisi there is (1) a different pattern in site attachment of adult
males and females that is consistent with that found with Amblyomma
helvolum (i.e. females anterior, males posterior) and, (2) whether the
preferred attachment sites of this tick also vary with different host varanid


We are grateful to the following staff members of the Zoological Survey of Pakistan,
Karachi, for the tabulation of data from the Pakistan hosts: Hafizuur Rahman, Fatima Iffat and
Zahida Perveen. James E. Keirans, Medical Entomology, Smithsonian Institution, Washington
was helpful in providing the latest information on distribution boundaries of several tick species.
Elliot Jacobson, School of Veterinary Medicine, University of Florida, made the technicians of
his laboratory available for histological preparations, which was much appreciated.
The major funding for the work on the behavioral ecology of monitor lizards in India and
Pakistan was provided by the United States Fish and Wildlife Service through it's foreign
currency accounts. Earlier travel and study in Southeast Asia and Sri Lanka were made possible
through the support of the Animal Conservation Department, New York Zoological Society.


A total of 381 monitor lizards were examined during this study, as follows: 73 Varanus
griseus, 90 V flavescens, and 218 Varanus bengalensis (79 Pakistan, 120 India, 19 Sri Lanka). Most
host specimens were seen alive and the ticks sexed and counted on different parts of the body;,


some preserved museum specimens are included in the analyses for months in which field
samples were insufficient in number (the ticks rarely detach themselves from the skin when the
lizards are preserved). Selected samples of ticks were preserved and later studied in detail under
magnification at the Florida Museum of Natural History.
Designated parts of the body for which total ticks/host were indicated each time in the
field are shown in Figure 4. Of special significance is a shallow somewhat longitudinal depression
on the ventral side of the tail base, hereafter called the "pit," in which ticks are often attached.
The total area of exposed skin in each of the designated sample areas was calculated by
first skinning an adult V. bengalensis and then cutting out each of the sample areas. These fresh
pieces of skin were then placed on a sheet of 1 X 1 mm graph paper. Each representative skin
sample was carefully traced and the surface area calculated by counting the 1 mm2 squares in
each tracing (see Table 2).

Table 2. Skin area and frequency of attachment by adult males and females, and by nymphs of
Aponomma gervaisi.

Males Females Nymphs
Skin Area (N = 909) (N = 420) (N = 439)
(% of total area) (% of total) (% of total) (% of total)

Pit 0.04 41.0 0.4 0.5
Deltoid 0.12 0.1 9.7 0.2
Fingers* 0.13 0.0 0.0 8.0

Toes** 0.16 0.1 0.5 0.9
Posting. 0.20 0.0 0.0 16.9
Cloaca 0.39 0.4 1.5 8.4

Axilla 0.47 0.7 60.4 15.5
Inguinal 0.58 0.3 0.3 8.0
Head 1.67 0.3 2.0 0.0

Chin 1.90 0.0 2.3 0.0
Throat 2.36 0.0 6.6 3.9
Arm 3.54 0.0 8.1 12.3

Leg 5.12 0.0 0.7 8.4
Neck 5.91 0.0 3.2 0.0
Chest 8.70 <0.1 3.0 0.0

Lateral 14.56 0.7 0.5 13.4
Tail 16.39 50.4 0.0 1.4
Belly 17.30 0.3 1.0 2.1
Dorsal 20.46 0.4 0.0 0.2

* Between fingers
** Between toes


Figure 4. Tick attachment site classification used in this paper. Top, dorsal and lateral surfaces:
bottom, ventral surface. Abbreviations: A=axillary; B=belly; Bk, back; Bl=back leg;
Bt=between hind toes; Ch=chin; Cl=cloacal periphery; Clw = base of claws; Ct=chest;
D= deltoid; Fl= front leg; Ft between front toes; H= top and sides of head; I= inguinal; N= nape;
P= pit; Pi = post-inguinal; Sb= side of body; Ta= sides of tail; Th= throat.

All host animals were sexed, weighed (to nearest g), and measured (standard lizard snout-
vent length = SVL below, to nearest mm). Field aspects of the study were conducted during all
months of the year, from June 1984 through September 1987, in order to obtain information on
seasonal aspects of tick infestation.


Identity of Ticks

All ticks examined during this study were identified as Aponomma
gervaisi. This includes material from Sind Province, Pakistan, from where
Haemaphysalis sindensis was described by Bilques and Masood (1973) from a


single adult Varanus bengalensis. Haemaphysalis is a common mammalian
ectoparasite but rarely found on reptiles. No Haemaphysalis species have been
reported from any Oriental reptiles to date (see Hoogstraal and Rack 1969 for
discussion of Asiatic members of this genus). This fact, plus our consistent
identification of all Sindhi reptile ticks as Aponomma gervaisi during the course
of the study, leads us to the conclusion that the holotype of Haemaphysalis
sindensis should be referred to the genus Aponomma (which is normally
restricted to reptilian hosts). We base this on a number of salient characters
mentioned in the holotype description. These are (1) the distinctive color
pattern, (2) the shape of the coxal spurs, and (3) the appearance of the
festoons on the idiosoma. Unfortunately the presence of eyes could not be
determined in view of the unavailability of the holotype.2 When placed in the
correct genus, it becomes clear that Haemaphysalis sindensis Bilques and
Masood 1973 is a synonym of Aponomma gervaisi Lucas 1847. The latter is the
most common ixodid tick parasitizing Varanus bengalensis throughout the
western half of its range.
In southern India and Sri Lanka, A. laeve occasionally infests Varanus
bengalensis, but it is apparently found mainly on large snakes. In Southeast
Asia, A. varanensis is the common tick of Varanus bengalensis, though in the
same area Amblyomma helvolum is the the most frequent tick species
parasitizing other varanids (i.e. Varanus salvator). Indeed, T. Auffenberg
(1988) has shown that this tick seems specifically adapted to this varanid host.
Because Aponomma gervaisi has not previously been adequately
illustrated, we include appropriate drawings in Figures 5 and 6.

Percent Infestation

Nagar et al. (1977) show that in the New Delhi area only 5.2 percent of all
snakes they examined were infested by Aponomma gervaisi, whereas 21.4
percent of all Bengal monitor lizards in the same area were infested. These
data originate from small samples. No other appropriate data occur in the
literature. Our work in Pakistan shows that the tick is only a rare snake
parasite (< 2.0 %, N= 56), and then only in larger, terrestrial (nonfossorial)
species. Furthermore, the extensive present data provide a basis for analyzing
the extent of both seasonal and geographic infection levels in Bengal monitors.
In a random sample of 58 adult Varanus bengalensis from Sind Province,
Pakistan, 92% were infested; 90 % of a sample of 70 adults from the

2 The University of Karachi was closed due to political disturbances during a trip made
specifically to examine the type.



Figure 5. Aponomma gervaisi Thatta, Sind Province, Pakistan. A, Adult male, dorsal and ventral
views. B, Adult female, dorsal and ventral views.






<11 iz I

Figure 6. Enlarged views of anatomical parts ofAponomma gervaisi, Thatta, Sind Prov., Pakistan.
Male A-M; (A) hypostome, ventral view; (B) shape of genital aperture; (C) capitulum, dorsal
view; (D) same, ventral view; (E) spiracle; (F-J) terminal part of legs I-IV respectively; (K-M)
coxae I-IV respectively, showing shape of the coxal spurs. Female, N-Z; (N) hypostome, ventral
view; (0) shape of genital aperture; (p) spiracle; (Q) capitulum, dorsal view; (R) same, ventral
view; (S-V) terminal part of legs I-IV respectively, (W-Z) coxae I-IV, showing shape of coxal





















State of Uttar Pradesh, India; and 77% of a sample of 38 adults from Sri
Lanka. The desert region of Gujarat and Rajasthan States in India had the
lowest infestation percentage we found throughout the range of this tick; only
32 percent of a sample of 38 adults were infested. It is clear that while some
geographic variation in infestation percentage does seem to occur, the
infestation rate of adult Varanus bengalensis is high throughout the entire
range of this tick species. There is no other reptile species in Pakistan-India
that can be demonstrated to have an infestation rate even one sixth as great
(see below for other varanid species in Indo-Pakistan area). We conclude that
this species of varanid lizard is a major host ofAponomma gervaisi.

Number Ticks/Host

No wild caught Varanus griseus or V. flavescens had any ticks,
regardless of geographic origin of the host, time of year, or host size.
However, if adults of either monitor species were placed in confinement where
V. bengalensis had been kept earlier, Aponomma gervaisi nymphs and adults of
both sexes attached themselves to a few of these captive lizards. This was
noted in three V. flavescens (1 nymph in the axilla of one host lizard, 2 nymphs
in the axilla of another, and 3 adult females in the axilla and 2 adult males on
the belly of the third). Ticks also attached themselves to three captive V
griseus (1 male in the medioventral caudal pit of one host, 1 male in the pit and
7 nymphs near the cloaca on another host, and a single male in the pit of the
last host). We conclude that (1) Aponomma gervaisi is rarely (ever ?) a natural
parasite of Varanus griseus and V flavescens, and (2), when it does attach to
them (in captivity), it does so in a pattern more or less consistent with that
demonstrated for its major host, Varanus bengalensis (see below).
Only three Aponomma gervaisi were found on any of the 382
individuals of 53 other species of terrestrial reptiles collected in Pakistan and
northern India (including snakes and lizards of several families, but no land
tortoises). However in the same places and during the same times, 1509
individuals of Aponomma gervaisi were found on 218 individuals of Varanus
Overall, 87 percent of all adult Varanus bengalensis examined in the
field throughout that part of its range coincident with that of Aponomma
gervaisi carried at least one adult tick; most had many more. The most we
counted in the field/host was 103 (host SVL 372 mm), but in captivity one
large male (SVL 536 mm) carried 416 adult ticks (though appeared listless and
stopped eating, presumably as a result of the heavy infection). The overall
average number of adult ticks per V. bengalensis was 10.8 10.5. The large
standard deviation reflects the great variation in number of adult ticks per host.


There is no statistically significant difference in the number of ticks found
on male and female monitor lizards. However, statistically significant positive
correlations (<5%) can be demonstrated between the number of adult
ticks/host and host SVL in all the populations studied (r = 0.63 for populations
from Northern India [N = 70], 0.64 for Southern India [N = 39], 0.75 for Sri
Lanka [N = 38], and 0.50 for Pakistan [N = 58]). An analysis of R2 (coefficient
of determination) demonstrates that in populations from northern India, 40%
of the total variation in number of ticks/host is associated with the regression;
41% in southern India, 56% in Sri Lanka and 25% in Pakistan. Individuals
with SVL < 260 mm never had any ticks. Since hosts of this size are known to
be in their second year of life (Auffenberg MS), it follows that neither nymphs
nor adult ticks attach themselves to V. bengalensis during the lizards first year
of life. This is probably partly related to the fact that during the first year,
juveniles over most of the species' range spend much of their active time in the
trees. This does not however, account for the fact that juveniles in relatively
treeless parts of Pakistan also lack ticks. The entire matter of the
circumstances under which monitor lizards acquire their tick loads needs
additional study.
Nymphal ticks were found on 22.9 percent of all V. bengalensis examined.
The average number of nymphs/host was 14.3; the maximum number recorded
is by Nagar et al. (1977), who report 254 from one individual captured near
New Delhi.
Larval forms are much less frequently seen. The average was 2.3/host,
but we have found as many as 21 on a single host. The relative rarity of larval
stages (at least one larva occurs on only 3.3 percent of all adult monitors
collected) suggests that this life stage will be found to parasitize other host
species as well. Of the total infected hosts, 46 percent possessed only adult
ticks, 30 percent had adults and nymphs, and only 2.9 percent carried only
nymphal ticks.
Within the range ofAponomma gervaisi, the infestation patterns of adult
male and female ticks over four geographic samples covering large areas
(Pakistan, northern India, southern India, and Sri Lanka) are statistically
homogeneous (Kruskal and Wallis ANOVA [one way] test: X23 = 1.04, not
significantly different). However, some spatial heterogeneity of infestation
patterns can be demonstrated over even shorter distances. The best example is
drawn from data within the Pakistan sample. Here a series of 61 monitor
lizards from a southern Pakistan subset (Sind Province) has a significantly
lower mean number of ticks/host than a series of 32 similar sized monitors
from the north (Punjab Province); mean south 3.9 male and 2.0 female
ticks/host, mean north 13.8 and 6.6/host respectively, students t-test 2.65, df
91, with a probability < 0.01. Results are provided in Table 3. Bull (1978)
obtained similar results in infestation rates of adult ticks from different
localities on Australian lizards.


Figure 7. Varanus b. bengalensis inguinal skin surface, showing general similarity of large scales
and surrounding "scalettes" to the adult tick carapace and its festoons.

In Pakistan, 71.3 percent of all adult ticks on the hosts are males (sex
ratio 7.1 males per 2.9 females). In India and Sri Lanka, (no significant
differences between them), male ticks comprise 60.0 percent of the adult
population on the hosts (6.0 males per 4.0 females). The difference between
the Pakistan and India-Sri Lanka sex ratios is not, however, statistically
significant at the 5 percent level.

Size and Color

Our results show statistically significant correlation between tick and scale
size in geographically disparate populations of both Aponomma ticks and
Varanus bengalensis.
In general, the combination of body shape and color pattern of the
scutum, particularly in male ticks of the subfamily Amblyomminae, are
remarkably similar to the general scale morphology of varanid lizards (first
pointed out by Flower 1896 and Deraniyagala 1953). On close inspection, the
skin of varanid lizards is very different from that of any other Asian


Table 3. Mean number of individuals of Aponomma gervaisi per Varanus bengalensis host in
northern (Punjab Province) and southern (Sind Province) Pakistan during the same months of
the year. M = males, F = females, N = number host examined.

Sind Province Punjab Province

Month M F N M F N

March 4.2 2.1 23 8.7 15.5 6
July 3.3 3.2 9 10.8 6.4 16
August 4.2 0.7 29 20.2 2.3 10
Overall mean 3.9 2.0 61 13.8 6.6 32

reptile group. There is a dominant, large central scale, surrounded, usually at
one end only, by much smaller "scalettes" (Fig. 7). The combination of tick
color pattern and the presence of festoons combine to make the males
inconspicuous when attached between the body scales (scale morphology varies
over the surface of the body, legs, and tail). However, this generality becomes
more striking when combined with color and size details of those ticks most
frequently found on Varanus bengalensis.
Varanus bengalensis is currently considered as composed of two
geographic races (Mertens 1959). Analysis of considerably larger sample sizes
than were available to earlier workers have corroborated this conclusion (W.
Auffenberg MS). The eastern subspecies, V. b. nebulosus, is distributed from
Java to Burma (Fig. 2). There is then a zone of intergradation extending
westward through Bangladesh and West Bengal, in which the characters slowly
merge with those of the western geographic race, V. b. bengalensis. The latter
is found throughout the Gangetic Plain and all of peninsular India, including
Sri Lanka, extending into the Indus Valley in Pakistan (Fig. 2). Here it follows
the Kabul River to near that city itself; along the southern Mekkran Coast it
extends through the basin and range part of southeastern Iran (Seistan). The
combined range of these two subspecies is almost exactly coincident with the
combined ranges of the tick species Aponomma gervaisi and A. varanensis (Fig.
The varanid subspecies are distinguished by certain features of their color
pattern and scalation. In general, adults of the eastern subspecies Varanus b.
nebulosus are dark, having much black pigment in the dorsal ground color.
This is punctuated with numerous scattered yellow and green spots. This
subspecies also has relatively few scale rows encircling the midbody and along
the ventral midline (scalation means for various populations vary from 76 to 83


from 76 to 83 and 123 to 133 respectively, based on 384 specimens from
scattered localities throughout Southeast Asia; see Mertens 1942 for scale
counting method). On the other hand, the dorsal ground color of adult
Varanus b. bengalensis is dominated by light brown. There is little yellow,
black, or green in the scheme. The series of both longitudinal ventral scale
rows and those encircling the body have higher mean numbers of scales (84-
108 and 135-148 respectively). Because body proportions are identical in both
subspecies, this means that the scales are smaller in the western race of V.
bengalensis and larger in the eastern one. A t-test shows the differences to be
statistically significant (t = < 2.58, p = < .005, df 386). The reasons for this
may be related to problems of water loss in drier, very hot habitats in the
western parts of the geographic range of this lizard, where water can be
expected to be in shorter supply. Soule and Kerfoot (1972) have shown that
there is a positive correlation between high evaporation rate and scale size in at
least some iguanine lizards. If the same explanation pertains to varanid scales,
then it follows that those populations of V. bengalensis in the driest parts of its
range with the smallest scales have the lowest rate of evaporation from the skin
The tick that is most often found on V. bengalensis in the deciduous
forests of Southeast Asia is Aponomma varanensis (W. A. data unpubl.). The
scutum diameter of male A. varanensis varies from 2.12 to 3.03 mm, X 2.55
0.25 mm. For Aponomma gervaisi the scutum diameter of males varies from
1.90 to 2.41 mm, with a X 2.15 0.24 mm. The mean difference between them
is 0.40 mm 0.32. A t-test shows that this difference is statistically significant
with p < .01 (t = 2.45, df = 31). Thus it is possible that male tick size is
related to "grain" size of the substrate. There is no clear relationship between
female tick capitulum and monitor scale sizes. In general, females attach in
more protected places on the body than males (this study, Table 2, and T.
Auffenberg 1988).
Several workers have shown that some predators attack and eat reptile
ticks on the ground. Tick predators reported are ants and spiders (Wilkinson
1970), mice (Bull and Sharrad 1981), chickens and the hoopoo bird (Nagar et
al. 1977). Though birds are sometimes known to remove ticks from
mammalian hosts, there is no evidence that any predators remove ticks from
monitor lizards. Of those predators listed above, all are regularly eaten by
Varanus bengalensis adults. Tick parasites are also potentially important in
depressing reptile tick populations on the host. The chalcid mite Hunterella
hooker is a common tick parasite in India and is sometimes found on
Aponomma gervaisi (Soni and Srivastava 1957). However, one cannot imagine
that the cryptic morphology and color pattern of Aponomma gervaisi is related
to such parasitism.
On rare occasions, almost intact, undigested adult ticks have been
found in the feces of long-term captive monitor lizards (Lederer 1942), after


they were evidently found and eaten on the floor of the pen. Vogel (1979)
believes that some of the scratching he observed in wild Varanus salvator was
related to removing ticks from themselves. Having removed many ticks from
monitors we do not believe this is very likely, as they are decidedly firmly
attached. Furthermore, during the dissection of over a thousand monitor
lizards from a number of Asiatic species, both in museums and in the wild, we
have never found any ticks in the stomachs. Thus, if monitors eat them, it is
indeed very rare. We are left with the problem of why particularly the male
ticks are so obviously cryptic on monitor lizards. Furthermore, there is no
relationship between male tick-size or color-pattern and the places they
normally attach (pit and lateral tail surfaces). Thus, if predation is important,
it is only so during the time when the male ticks leave these sites to move over
the dorsal skin to find receptive females (see below).

Patterns of Site Attachment

Siddappaji and Channabasavanna (1981) suggested (on the basis of
only a few observations) that males of Aponomma gervaisi tend to be on the
"tail region" and females "on the body." Our observations corroborate their
conclusions and add important details to this generality.
Table 4 provides data on attachment sites for this species. For adult
male ticks, 97.0 percent are found on the tail (posterior to the level of the tail);
of these, 46.6 percent are clustered in the pit. In no other part of the body are
either males or females so tightly packed (Fig. 8). As stated above, a
depressed rather narrow groove on the midventral surface of the tail base is
present in almost all monitors (Fig. 4). When ticks attach here they modify the
shape of the groove, so that it becomes more depressed, with clear, rather
acute borders and a scaleless bottom, comprised of what appears to be scar
tissue that extends around the often more or less vertical walls of the pit as
well. On the pit walls, the acute upper pit boundary, and the pit bottom, the
surfaces are often provided with smaller pit-like depressions. These fit the
shape and size of the adult male ticks so that many of the resident males are
located in separate small superficial dimples (Fig. 10). The tissue lining the pit
is highly modified and lacks the many small blood vessels often associated with
new scar tissue. On all parts of the host's body, ticks are always attached in the
skin between the scales. However, even here adult males (but not females)
modify the immediate area by their presence, eroding or forcing the tissues
from around the tick in such a way that a small pit-like depression is formed,
even tough caudal scales are minutely, but plainly misshapen at male
attachment sites (Fig. 9). This suggests that males either remain in the same
site for a long period of time, or that specific sites are repeatedly revisited by


Table 4. Percent of total male (= M) and female (= F) Apononmmna genvaisi attached in different
parts of the body.

Pakistan India Sri Lanka Overall


Axillary 1.9 78.4 <0.1 42.0 <0.1 60.8 0.7 60.4
Shoulder 0.0 5.8 0.2 11.2 <0.1 12.0 0.1 9.7
Throat 0.0 2.6 0.0 9.8 0.0 7.3 0.0 6.6

Arm 0.0 2.6 0.0 11.0 0.0 9.2 0.0 8.1
Chin 0.0 2.6 0.0 2.0 0.0 2.4 0.0 2.3
Belly 0.8 2.1 <0.1 1.0 0.0 0.0 0.3 1.0

Chest 0.0 1.0 0.2 8.0 <0.1 0.0 <0.1 3.0
Neck 0.0 1.6 <0.1 4.6 0.0 3.3 0.0 3.2
Cloaca 1.1 1.6 0.2 2.0 0.0 1.0 0.4 1.5

Head 0.0 0.5 1.0 3.2 <0.1 2.2 0.3 2.0
Lateral 0.03 0.5 <0.1 0.5 2.0 1.0 0.0 0.0
Toes* 0.3 0.0 0.0 1.0 0.0 0.6 0.1 0.54

Dorsal 1.1 0.0 <0.1 0.0 <0.1 0.0 0.4 0.0
Tail 29.1 0.0 51.0 0.0 71.0 0.0 50.4 0.0
Pit 66.0 0.0 43.1 1.2 14.2 0.0 41.0 0.4

Hind leg 0.0 0.0 0.0 1.0 0.0 1.2 0.0 0.7
Inguinal 0.0 0.0 <0.0 0.0 0.0 0.0 0.3 0.3
Posting. 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Fingers** 0.0 0.0 <0.1 0.0 0.0 0.0 0.0 0.0

* Skin between hind toes.
** Skin between front fingers.

the same, or other males, over a long period of time (clearly years in the case
of the pit).
Even those adult males attached in areas other than the pit tend to be
found on the posterior part of the body (Table 2, 4). The exception is in the
axilla. It is here where most adult females are attached (60.4%). Of 909 males
found, 15 were in the axilla, with 4 of these not attached, but walking about the
area, and 5 were found on females in a copulatory position, mounted venter to
venter; the remainder were attached in the area (temporarily ?). Therefore, it
is likely that most or all of .the males in the axilla are there because of the


Figure 8. A pit on the ventral surface of the base of the tail of Varanus bengalensis is regularly
used by adult males ofAponomma gervaisi, where they are often densely aggregated.


Figure 9. Edges of scales of the lateral surface of the tail of Varanus b. bengalensis modified by
male ticks after frequent attachment at the same site.

-,- : ... 6

Figure 10. Generalized cross-section of area where mouth parts of adult male tick are inserted
into skin of Varanus b. bengalensis. (A-B) recently abandoned attachment sites; (C) cementum;
(E) epidermis; (K1) keratin alpha layer; (K2) keratin beta layer; (M) zone of macrophage
concentration; (P) mouth parts; (S) zone of streaming cellular remains; (U) unaffected dermis.


frequency with which females occur in the same place. Apparently some males
leave the posterior part of the body and move anteriorly to mate with sexually
active females. The method by which the presence of reproductively receptive
females is communicated to males remains unknown (see below).
Females tend to be found in the anterior part of the body; 65.5 percent
are associated with the insertion of the front leg axillaa 60.4%, deltoid 8.0%
and upper arm 7.1%).
Ticks also occur in large numbers on wounds, sometimes located outside
the normal attachment sites, or in numbers considered abnormal for that site.
However, in no instance was any female found to be attached to a wound area.
The reasons for this may be related to a probable different dietary source of
adult males and females (see below).
There is no correlation between the mean size of the sample skin area on
adult lizard hosts and the mean number of ticks in each ((Table 2). Certain
areas are favored as attachment sites, regardless of their surface extent. Thus
the pit, which is extremely small when compared to the remainder of the
surface available, is a preferred site of attachment for males, just as the
relatively small axillary area is the preferred attachment site of the adult

Subsurface Attachment Details

Female Aponomma gervaisi attach in highly vascularized areas of
relatively thin skin with little cornification. Here they certainly engorge on
blood from the numerous capillaries found. The situation in adult males is less
clear, as they often attach on the edges of old wounds, or in heavily cornified
tissues on the tail, and particularly in the pit at the base of the ventral caudal
surface. Because of this, several histological sections were prepared and
stained to obtain information on feeding and tissue details. The following is
based on slides prepared from male attachment sites on the lateral surfaces of
the tail and the pit.
The tissue surrounding these sites under normal conditions is a thick,
irregular, moderately dense to loose connective type, with coarse, irregularly
oriented collagen bundles. In these areas there are only small amounts of
serious exudate (ground substance) between the bundles. It contains freely
floating macrophages and small lymphocytes. During inflammatory conditions,
the latter become exceptionally numerous and change to macrophages.
Eosinophilic leucocytes (uncommon in normal dermal connective tissue of
monitors) become very numerous during inflammatory reactions of several
types. The large numbers of eosinophils attracted to the affected area


area probably phagotize and destroy immune complexes introduced by the tick
mouth parts.
Examination of tissue near the introduced mouth parts of the attached
male shows that in the dermis, deeper than the mouth parts, the collagen fiber
bundle organization is broken down. In the immediate area there are many
larger cells, which become more densely packed the closer one moves to the
inflammation center (Fig. 10, M). These appear to be mast and macrophage
cells. The closer to the mouth parts one goes, the more abundant a serious,
probably mucoid, exudate (ground substance) becomes. In this area,
orientation of the cells suggests they are being drawn to the mouth parts, for
most of them are aligned longitudinally (parallel) to it, in "flow-lines." There is
a fairly sharp differentiation in the highly stained ground material near the
mouth parts in the closest, most densely packed zone of the macrophages.
Beyond this zone, the ground material is open and clear. Furthermore, the
densely packed macrophage zone changes rather quickly to a less dense one.
Only the fibroblasts (and leucocytes?) seem to extend beyond this last zone as
any indication of tissue inflammation. Immediately surrounding the hypostome
is a clear zone of cementum exuded by the tick into the host tissues, apparently
to help keep the mouth parts inserted in the skin.
The material in the gut of the tick is also composed of the stained
mucoidd?) ground material, as well as what appear to be granules and perhaps
even complete nuclei of the cells being drawn into the mouth parts. None of
the ingested cells is entire, but such cells are rare near the chelicae in the tissue
anyway. The cells seem dissolved, and the contents, as well as the mucoid
substance, are being drawn into the mouth parts. Cell wall destruction
probably takes place at the macrophage zone, and the difference in ground
substance staining is probably due to the cell contents spilling out in that area.
In summary, the feeding male ticks start by lysing the epidermal layer.
Feeding occurs by the tick pumping saliva into the tissues through its mouth
parts. This causes the cells to break down and the ticks then suck up the
resultant broth of lymph and cell debris. However, it is probably the
introduction of foreign proteins in the form of the lysing saliva that is most
important in this process, for it attracts lymphoid cells towards the hypostome.
These lymphoid cells are in turn broken down and ingested. Thus the immune
response caused by the saliva produces a steady stream of food material in the
form of body fluids and particularly lymphoid cells. There is thus little
profitability in changing attachment position, for a flow of nutrients is assured
as long as saliva is regularly introduced into the tissues.
This feeding strategy probably explains why male reptile ticks are so often
in such dense aggregations. Several males injecting saliva in a small area
should produce a proportionately much greater immune response on the part
of the host, sending proportionately more lymphoid cells and fluids to the
affected area than to an equal number of scattered male parasites. Thus, there


is probably a very distinct advantage for male attachment sites to be clustered.
Those sites with the greatest potential for habitat abrasion and injury (ventral
body surface, lateral tail surfaces, etc.) may have a higher resident population
of lymphoids and may explain why male attachment clusters of the varanid
ticks studied so far are often located in those parts of the body where abrasion
is expected to be high. It may, as a matter of fact, explain why male
Amblyomma helvolun prefers the base of the claws as an attachment site in
the monitor lizard Varanus olivaceus, for this is a species that spends much
time in the trees. When climbing, varanids depend entirely on their claws for
purchase. Thus the base of the claws is exactly where one would expect much
abrasion and stress, and thus probably high densities of resident lymphoid cells.
On the other hand, the terrestrial monitor in the same area, Varanus salvator,
infected by the same tick species would be expected to suffer the greatest
abrasion on the median ventral body and tail surface, and this is exactly where
the males tend to aggregate. Varanus bengalensis is primarily a terrestrial
species, and this may explain why one of the major male aggregation sites is
also on the ventral surface.
At the same time, this feeding strategy also explains the tendency for male
reptile ticks to accumulate on wound edges. Additionally, it explains why they
tend to restrict the attachment sites to relatively small parts of the body and
why some sites are repeatedly used by a succession of ticks. Such repeated use
of the same site produces a pit-like depression with a raised, highly keratinized
anterior margin (Fig. 9). The shape of these depressions is such that
succeeding resident ticks tend to lie in it in exactly the same way, assuring the
new resident that the mouth parts will be inserted in almost the same place as
was that of the last resident. Arnold (1986) has postulated that mite pockets in
the skin of many lizard species are a way of ameliorating the effects of mite
infestations, since he believed they tend to concentrate such infestations to
certain parts of the body where they will not disrupt normal cutaneous
function. There is no evidence suggesting that this is the case in varanid lizards
and their tick parasites. Research is needed to prove whether the lymphoid
cells are concentrated in the specific attachment sites even without the
parasitizing ticks, or whether they become concentrated only after injection of
saliva from the mouth parts.
The situation in female reptile ticks is entirely different from that of the
males. Females apparently feed entirely on blood, drawing their high nutrient
food from a capillary bed. Blood supply to any specific dermal area is largely
dependent on the capillary density of the immediate area. This being the case,
there is probably a distinct advantage in the females dispersing themselves over
an appropriate protected site, rather than forming the dense concentrations of
lymphoid-feeding males.


Seasonal Patterns of Infestation

The most complete records of seasonal abundance of ticks on Varanus
bengalensis exist for Pakistan, and this area is used as a guide to what is
presumed to be happening seasonally throughout the range of Aponomma
gervaisi. These data are presented in Figure 11, which shows a strong pattern
of seasonal differences in tick frequency on the host animals. The annual
pattern is slightly different for male and female ticks. Males clearly show two
peaks, one during the winter (December through February) and the other
during the monsoon withdrawal phase (September and October). That the
frequency of ticks is not entirely related to seasonal difference in monitor
activity is demonstrated by the fact that during the winter peak the monitors
are inactive--usually brumating in burrows in which they spend the coolest
months of the year (Auffenberg, MS). The second male peak (September-
October) is during a period of increased monitor foraging activity, when food
abundance (primarily insects) is high and lizard fat bodies are enlarging in
response to reproductive and reduced food resources during the cool winter
and the hot dry spring months of the following year. Though less defined, this
is also the time of year when monitors have the most female ticks/host. This
correlates with the onset of the cloudy weather and cooler temperatures during
the premonsoon of Pakistan's Indus Valley (where most of the specimens of
lizards in this study originated).
The lowest monthly mean number of male ticks/host occurs during May,
which is also the hottest part of the year in Pakistan and the peak of the dry
season. This more or less corresponds with the period of fewest female ticks
on V. bengalensis (April-June). Our studies on monitor lizards at Bharatpur,
India, make it clear that this dry season reduction in number of ticks per lizard
is correlated with the appearance of many individuals of Aponomma gervaisi in
crevices in the parched earth and in and on walls and ceilings of burrows
regularly inhabited by large reptiles (i.e. pythons and monitor lizards). Thus
the dry season seems to be a period of quiescence for ticks of both sexes.
We know that breeding between male and female Aponomma gervaisi
takes place on the host. Because of both the number of males and females on
the host at this time of year, and the dates of breeding observed on them, we
conclude that all breeding takes place during the summer monsoon. The
reduction of females on the hosts immediately after July suggests that it is at
this time when eggs are laid (generally true of many insect groups in eastern
Pakistan and western India, W. Auffenberg MS). The females apparently lay
their eggs in the soil (of mainly reptile burrows?). All female hard ticks die
after the eggs are laid, and it is presumed that those of Aponomma gervaisi do
so as well. Thus, it is the male ticks that provide the genetic continuity from




L 6

z 3
2 Females
w 2


Figure 11. Mean monthly frequency of adult male and female Aponomma gervaisi ticks attached
to all Varanus b. bengalensis collected during the study; the middle graph is the same for nymphs
and larvae.

one breeding population to the next. We assume the winter increase in
numbers of both male and female ticks is associated with the fact that the
lizards are spending much more time in burrows (W. Auffenberg MS), where
the ticks are also known to congregate (see above). Table. 1 suggests there may
also be some geographic variation in seasonal abundance patterns, though the
data are too scattered to be completely reliable.
During a year-long study of movement and growth patterns in Varanus
bengalensis at Haliji Lake, Pakistan, the senior author and the Zoological
Survey Department staff captured and marked 61 adults. As part of the study
the tick loads of each were tabulated. Of these, 12 individuals were
subsequently recaptured (some several times), with the days between varying
from 14 to 282. Upon recapture the tick loads were again counted. As a
result, data are available on the change in number of ticks/host/season for a
series of adult animals in one small area.
These data corroborate what is surmised from Figure 11, namely that it is
during the dry season when most ticks leave their hosts. Additionally, the data
also show that significant changes in tick number/host may take place over
periods as short as 2 weeks. They also indicate that males, females, and
nymphs are all affected the same way during the same time of year, either
leaving or assembling on individual host lizards at the same time. This is even
more interesting when one realizes that on some hosts the ticks of both sexes


and both nymphal and adult life stages may be in a leaving phase and that on
other hosts captured and recaptured during the same time, the ticks are in an
aggregation phase. The proportions of males, females, and nymphs involved in
these movements reflect the ratios in which these categories are expected to
occur. We have no idea what triggers these movement patterns, but the fact
that they sometimes produce opposite results on different hosts at the same
time suggests that it may be related to the host as much as to general climatic
conditions. However the results may also reflect a statistical artifact depending
on the dispersion of ticks on the ground.

Life History

Larvae of Aponomma gervaisi moult on the host Varanus bengalensis. It
is here that the nymphs also remain, attached in the same general area as the
larvae. Active periods of the larval and nymphal stages in three northern
Indian and Pakistan sites probably occur only during the warmer months, as
other Aponomma species living in seasonally cool areas are inactive during
winter (i.e. A. hydrosauri, Australia, Bull and Sharrad 1980). Thus we presume
that in northern Pakistan and India both larvae and nymphs are active on the
host for about eight months and inactive about four months. In seasonally less
variable parts of the range (central India to Sri Lanka) we expect they would
remain active throughout the year. Adult Varanus bengalensis taken from their
burrows at this time of year have both nymphs and adult ticks attached to
them, suggesting that neither leave their hosts during the cool, quiescent
Molting of the nymphs undoubtedly takes place in the burrows of Varanus
bengalensis, mainly during the May-June dry season. This is based on the fact
that by July thousands of adults may be found in some burrows in Pakistan and
northwestern India habitually used by monitors (and an adult, brooding Python
molurus in one instance). These are positioned in small crevices and holes in
the walls and ceiling of the primary burrow, where they hang upside down.
Any slight physical disturbance arouses the apparently quiescent adults, and
the walls and ceilings of the burrow become completely covered with moving
ticks, which rapidly transfer themselves onto any object moving within the
burrow. Downes (1984) has demonstrated the same behavior for quiescent
nymphs of Aponomma hydrosauri (not in host burrows) and the behavior is
probably characteristic of quiescent nymphs of A. gervaisi in reptile burrows as
well. Active nymphs may be attracted to the host by its odor, as Downes has
shown for A. hydrosauri. Active adults probably depend on actual contact with
the host for transfer within the host burrows.


Adult Aponomma gervaisi apparently attach themselves to their hosts
mainly during the monsoon season (July and August). We base this on the
significant increase in number of adult ticks during this time of the year (Fig.
11). The increase is correlated with an increase in the activity level of the
monitor lizards. During this time of year they are active for a longer part of
the day and move over greater distances than during any other season (W.
Auffenberg, MS). There is thus a greater chance of ticks coming into contact
with monitor lizards during this time of year than any other.
Breeding takes place on the host (suggested earlier by Siddappaji and
Channabasavanna 1981 on basis of a single observation), when one or more
males leave their more posterior attachment positions and move anteriorly.
Not all males do so, suggesting that either some males have not received
whatever information is transmitted from the ovulating female, have ignored
the signal, or are not sexually ready to breed at that time. During breeding a
single male is mounted venter to venter on the still attached female. Females
drop off their host in significantly large numbers during the cool months
(December-January, Fig. 11), presumably to lay their eggs in the soil of the
monitor lizard burrows.


During the course of study regarding the behavioral ecology of Varanus
bengalensis, 381 individuals of this species of varanid lizard were examined for
ticks in Pakistan, India, and Sri Lanka. None of the ticks could be assigned to
any species other than Aponomma gervaisi. Thus, the Indo-Gangetic Plain
probably has only one species of reptile tick.
We have shown that 91.4 percent of all adult males of Aponomma gervaisi
are found on only 16.3 percent of the body surface, whereas 93.3 percent of the
adult females are found on 23 percent of the host's body surface. The males
are found in more posterior and more extensively keratinized sites than those
in which the females occur. These male attachment sites are regularly used by
a series of transient adult male ticks. Such regular, sustained attack, produces
a depressed, scar-like, inflammatory area from which the males derive their
nutrients, which appears to be mainly digested cellular matter, rather than
blood. Males are also commonly found in scar tissue in other areas of the
body, and it is on such sites where they are sometimes found on other reptilian
hosts. On the other hand, adult females are located in highly vascularized sites
that have thin, easily penetrated skin (such as the axillary area). Here the
females are apparently able to ingest the large supply of highly nutritious blood
that is needed for egg production. After mating, females may increase to as
much as five times their unmated size, and are thus more susceptible than the


much smaller males to disturbance by host movement through the environment
(Smyth 1973; Andrews and Bull 1980, Andrews and Petney 1981). Of the sites
on which the females are generally found, the most protected is the inguinal
area, being located on the posterior part of the insertion of the upper arm and
protected from being brushed off by the limb itself.
Only 0.4 percent of all females observed were found in any of the
"preferred male sites," and 0.8 percent of the males were found in "preferred
female sites." The higher percentage for the males is the result of their moving
to presumably sexually mature females, where breeding takes place. Not all
males move forward at the same time, suggesting that not all receive the
message, and/or that not all males are ready to mate at the same time.
Communication from the female to the male is undoubtedly chemical in
nature, and in other ticks it has been suggested to be a pheromone moving
posteriorly across the host surface (Andrews and Bull 1981). If this were the
case, it would seem advantageous for the males to be located closer to the
females. But in each species of Varanus we have studied so far, we have found
that the adult males are always located some distance from the females. Males
of the tick Amblyomma helvolum attach mainly on the median ventral surface
of both the chest and the base of the tail (= the pit in this report) on Varanus
salvator, while in Varanus olivaceus they attach mainly to the base of the claws.
In Varanus bengalensis the adult males are located both in the pit and on the
lateral surface of the basal half of the tail. Thus, at least among varanid
lizards, a surface-moving pheromone seems a remote possibility (T.
Auffenberg 1988), though an airborne one is likely. Such a pheromone has
been shown to be operative in A. hydrosauri, Andrews 1982, Andrews and Bull,
1982a, b, and Andrews et al. 1982a. Only an airborne pheromone would be
able to be perceived and interpreted over the large area represented in order
to attract respondent males to receptive females in the anterior part of the
In any event, what is significant in the current tick species is that males
are always located posteriorly, and secondly, that they are located in such
distinctly different parts of the hosts posterior anatomy. Aponomma gervaisi
males are never found on the chest, and rarely on the hind feet. On the other
hand, the tick Amblyomma helvolum is characteristically found on the chest
and the base of the claws on Varanus salvator and V. olivaceus respectively.
This attachment site specificity is apparently based on differences in the
epidermal/dermal microhabitat. These differences are most likely of a
chemical nature and ultimately related to tissue-mediated immune responses.
Male ticks of both Amblyomma helvolum and Aponomma gervaisi are probably
reacting to chemical differences and not to feeding ease or the degree of
protection offered by the sites selected on different hosts.
While the pit is clearly an area protected from abrasion (depressed), it is
on the ventral surface, where most abrasion probably occurs. The lateral tail


surfaces are also areas where abrasion is very high, for during locomotion, the
tail of varanid lizards is constantly undulated from side to side. In fact, that
part of the tail which tends to be most abraded from this movement is just
where male ticks are most commonly attached. Even on Varanus olivaceus,
where male ticks are most often found at the base of the hind claws, the
preferred site is one of high abrasion. In Varanus salvator, the preferred
median chest area is another zone of high abrasion. Presented with these
distributional facts, we conclude that adult males of these tick species
deliberately seek sites regularly and generously abraded. On the other hand,
females are obviously responding to an entirely different cue common to all
host monitor species and resulting in the same distribution of attachment sites
in all host species. While the reasons for this are rather clear in the females,
with their relatively larger size resulting from engorgement and their need for a
ready supply of blood, it is not at all clear for males of both tick genera. Site
selection among males may be the most critical factor from the standpoint of
male-female competition and may be related to the ability of members of this
sex to remain with the host in the face of particularly difficult environmental
pressures to sweep them off (T. Auffenberg 1988).
It is clear that what is needed is a series of carefully controlled
experiments under laboratory conditions in which the biochemical and
histological aspects of the microenvironment are carefully investigated during
initial attachment and later movements on the host, as well as when leaving it.
This work serves to again focus attention on that need, as was demonstrated in
the earlier work of the junior author on other species of varanid hosts and a
different genus of reptile tick.
It has been shown that the life history of this tick is intimately associated
with major climatic cycles. This is particularly true in the more xeric parts of
the range. Here the immature and mature ticks tend to leave their hosts
during the driest parts of the year. Such hot, dry conditions have been shown
to lead to rapid water loss and death in other tick species (Bull and Smyth
1973) and is expected to be similarly important inApononmma gervaisi. During
this time it enters crevices and burrows in the earth, particularly those regularly
used as refuges by its major host Varanus bengalensis. Though this monitor
species uses these burrows throughout the year (W. Auffenberg 1983), it is
during the dry season when the ticks move into the same burrows. Data
available for other tick species (Wilkinson 1961, Owen 1975) suggest that they
do not disperse when in a refuge. This is suggested for Aponomma gervaisi as
well, for during this time of year hundreds may be found infecting a single
burrow. Presumably, engorged and detached adult females also lay their eggs
in the refuges, so that large numbers of larvae may often be found in some
burrows during this time of year. When the monitors become particularly
active during and immediately following the wet season, the ticks have moulted
and reinfested the lizards. On the basis of similar data, Bull (1978) suggested


that this refusing behavior of ticks during the dry season best explains their
distribution on the Australian scincid lizard Trachydosaurus nigosus. The
concentrations of moulting and waiting ticks in some burrows explains why
certain monitor lizards are so heavily parasitized and others are not. It also
explains why juvenile monitors have fewer, or no ticks (depending on size), for
it is known that Bengal monitor lizards in the first year of life spend much time
in the trees (W. Auffenberg MS).
The closely related Apononmmna varanensis parasitizes the same species of
lizard in less seasonally affected forests of Southeast Asia, suggesting that this
tick species may have a somewhat different seasonal life history pattern than
Aponommn a gervaisi. This is further complicated by the fact that the more
eastern populations of Varanus bengalensis are much more arboreal than their
western conspecifics (W. Auffenberg MS). One would thus expect adults of
the eastern monitor populations to have fewer ticks. This is substantiated by
our data on regional infestation levels between populations of Varanus
bengalensis. However, our samples from the eastern extremes of the
geographic range are considerably smaller than those from the western
sections used in the current study, and we are less confident of our analysis of
tick data originating in Southeast Asia. Additionally, it is important to point
out that monitor burrows may not be necessary in the life history of monitor
lizard ticks. For example, in T. Auffenberg's study of infestation of the
Philippine Varanus olivaceus, he found approximately the same level of
infestation in this non-burrowing species as in the burrow-utilizing V.
bengalensis bengalensis.
Based on what we now know of the life history of Aponomma gervaisi,
one would conclude that it is an endophilic species, i.e. all the developmental
stages periodically inhabit the same shelter type (Varanus burrows). This is
reflected in the fact that the hosts of both the immature and mature ticks of
this species have the same narrow host specificity (Varanus bengalensis). From
an evolutionary standpoint, single-host tick species are generally believed to be
advanced (Hoogstraal 1978).
Hoogstraal and Aeschlimann (1982) have challenged what they describe
as "a common assertion that ticks lack host-specificity", pointing out that a
number of tick species are reptile-specialists. We suggest that some of these
reptile specialists prefer either turtle, snake, or lizard hosts; those falling into
the latter category are frequently specialists on the lizard family Varanidae
(Aponomma gervaisi and Amblyomma helvoluni). Not only are these tick
species host-specific, but site-specific as well, more so for the adult males.
Varanid lizards have a long fossil history, extending back to the Lower
Cretaceous. Because the Superfamily Ixodoidea is believed to have arisen as
an obligate parasite of Reptilia during the late Paleozoic or early Mesozoic
(Hoogstraal and Aeschlimann 1982), one supposes a long association between
ticks and varanid lizards. This may explain the high degree of site attachment


preferences among the varanid tick specialists. It remains to be seen if the
high degree of host-site specificity demonstrated on the Asian mainland is also
true of reptile ticks in Australia, where varanid lizard diversification
(presumably during the mid-Tertiary, W. Auffenberg 1980) is particularly
As is typical for ixodoidid ticks, all female Aponomma gervaisi both
oviposit and die on the ground, rather than on the host. Bull and Sharrad
(1980) have shown that unfed adult A. hydrosauri can live for as long as two
years without food, and there is no reason to believe that A. gervaisi cannot do
the same.
The food sources of adult male and female Aponomma gervaisi are
apparently different. Egg production in females demands an abundant, highly
nutritious source, which is satisfied by blood. Adult males digest cellular
material associated with immune responses of the host in areas of
inflammation. This, as well as the distribution patterns of both males and
females on the hosts, suggests there is no site competition between the sexes.
On the other hand, there must be intrasexual competition among both males
and females for sites appropriate to their particular feeding type. Some of
these sites are obviously better than others. For females this means a
protected site in the anterior part of the body provided with thin, highly
vascularized skin. The ideal location is apparently in and near the axillary
region. For males, the lateral surfaces of the tail and the pit seem ideal. The
latter is apparently somewhat more preferred, for the ticks are more regularly
found there and are frequently also packed remarkably tight. It is obvious that
first-comers achieve an attachment site in the pit, those arriving later will not
be able to find a place. In time this crowding tends to enlarge and deepen the
pit, so that it holds proportionately more male ticks as the monitor lizards
become larger (older). The lateral surface of the tail is a large area, and space
is always available for many more males than are attached there.
It is not clear why Aponomma gervaisi never occur on the two other
syntopic monitor species in Pakistan and northern India (V. griseus and V.
flavescens). Parallel situations can be demonstrated in the mesic forests of
Southeast Asia, where Amblyomma helvolum is regularly found on the semi-
aquatic V salvator, yet absent on the similarly semi-aquatic V dumerili living in
the same area (T. Auffenberg notes). Of those varanid species that are
regularly infested, the pattern of female attachment sites remains the same,
centered on the axillary area. This is true even across tick genera
(Amblyonumma and Aponomma). For the adult male ticks, the site attachment
pattern is distinctly different for each host, even within the same tick species.
This has now been demonstrated for Amblyomma helvolun and Aponomma
gervaisi. Thus the males are host-species site-specific.



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