ACAROLOGIA
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THE HY ALOM.lviA TICKS
(IXODOIDEA, IXODIDAE) OF PAKISTAN,
INDIA, AND CEYLON, WITH KEYS TO SUBGENERA AND SPECIES
1
BY
Makram N. KAISER and Harry HooGSTRAAL
(Department of Afedical Zoology, United States Naval Medical
Research Unit Number Three, Cairo, Egypt, U.A .R.)
The Hyalomma tick fauna of the Indian area is characterized by the presence
of several distinct, endemie species as well as by the small size of individual ticks
in local populations of species widely distributed in this area and elsewhere in
Asia, Africa, and southern Europt. The geographie range of Indian Hyalomma
is south of U.S.S.R. and the crests of the Himalayas, from Pakistan in the west
to Bengal and Assam in the cast and Ceylan in the south. Certain members of
this fauna also penetrate into Afghanistan, Tibet, and Nepal.
Hyamomma ticks in general are exceptionally versatile and efficient reservoirs
and vcctors of a variety of pathogens causing human and animal diseases. The
relationships of the Indian Hyalomma fauna to dissemination of diseases are,
however, almost entirely unstudied. Biological and ecological data concerning
these ticks are conspicuous by their extreme dearth. Taxonomically, the endemie
species have been inadequately described and delineated. Geographie variation
in size and shape of Hyalomma species encroaching this geographie area from
elsewhere has not previously been reported and the taxonomie, biological, and
applied significance of this phenomenon continues to be unknown.
This preliminary review is intended to outline the basic features of the Indian
Hyalomma fauna and to stimulate research on the biology of these parasites and
their medical and veterinary relationships. Comparative data and materials for
this genus which have accumulated in our files and collections during the past
ten years are considerably more extensive in variety and quantity than have preI. From Research Project MRoo5.09-1402.3, Bureau of Medicine and Surgery, Navy
Department, Washington 25, D.C.
The opinions and assertions contained herein are the private ones of the authors and are
not to be construed as official or reflecting the views of the ?\avy Department of the naval
service at large.
Acarologia, t. VI, fasc.
2,
1964.
-258viously been available. They remain, however, quite inadequate for any practical
economie applicability in this geographie area.
For reviews of Hyalomma ticks in areas adjacent to that discussed here, see
ABBASSIAN-LINTZEN (1960, 1961) for Iran, KAISER and HooGSTRAAL (1963) for
Afghanistan, and POMERANTZEV (1950) and SERDYUKOVA (1956) for U.S.S.R.
The following abbreviations are used in recording depositories of materials
examined : BM(NH), British Museum (Natural History) ; RML, Rocky Mountain
Laboratory, Hamilton, Montana ; and VRC, Virus Research Centre, Poona. Most
other specimens are in the Hoogstraal collection at NAMRU-3, Cairo.
Subgenera of Hyalomma
Species in the genus Hyalomma fall into three natural and distinct groups that
can quite convcniently be considered as subgenera. In this paper, wc have retained
the frcguently accepted thought moot names Hyalommina, Hyalommasta, and
Hyalomma for these subgenera. It will obviously be sorne time before subgeneric
designations of Hyalomma are settled to the full satisfaction of taxonomie purists.
In brief, NEUMANN (1901), SALMON and STILES (1901), NuTTALL and WARBURTON
(19n), and Opinion 73 of the International Rules of Nomenclature have considerecl
H. aegyptium to be the type species of the genus. H. aegyptium therefore shoulcl
be the type specics of the subgenus Hyalomma. However, the subgcnus Hyalommasta was erectecl by ScHULZE (1930) for H. aegyptium. Other workers, especially the Russian school reprcsentecl by PoMERANTZEV (1950), as weil as SAl'iTOS
DIAS (1956), consider H. dromedarii to be the type species of the genus. If this
opinion were acceptecl, the cliscrepencies noted above coulcl be more easily rcsolved.
The subgenus Hyalommina is cgually troublesome, having been erected by ScHULZE
(1919) for H. rhipicephaloides, a specics based on imperfectly formed specimens
and a synonym of H. anatolicum, a typical representative of the subgenus Hyalomma
(see HooGSTRAAL, 1956, pp. 447-8, 520-2, and HooGsTRAAL and KAISER, 1959).
SANTOS DIAS (1956) namecl a new subgenus, Delpyiella, to replace Hyalommina.
FELD!\IAX-MUHSAM (1957), however, not only maintainecl that H. rhipicephaloides
is a valid species but also considerecl Hyalommina as a full generic catagory.
KEY TO
HY ALOMMA
SUBGENERA (ADULTS)
r. Basis capituli ventrally with lateral projections. Adana! shields very broad. Subanal
shields absent. (Endemie in Indian Subregion)... . . . . .
Subgenus Hyalommina
Basis capituli lacking ventral lateral projections. Adanal shields elongate. Subanal
shields present (absent in atypical specimens)... . . . . . . . . . . . . . . . . . . . . . . . . . . .
2
2. Coxa I with two equal, weil separated spurs.
Subanal shields rudimentary, sornetimes absent (H. aegyptium, Mediterranean basin to West Pakistan) ............. .
Subgenus Hyalommasta
-259Coxa I deeply divided into narrow external spur and wider internai spur. Subanal
shields weil developed. (Asia, southern Europe, Africa). . . . . .
Subgenus Hyalomma
HY ALOMMINA
SuBGENUS
Males
r. Lateral grcoves superficial, long, short, or absent. Punctations shallow. Tarsus IV
humped. Scutum, legs, capitulum and ventral shields yellowish brown (Afghanistan
to Assam, Nepal, ? Tibet)............................................
lmmari
Lateral grooves distinct and long. Punctations discrete Tarsus IV fiat or slightly
humped. Scutum, legs, capitulum, and Yentral shields reddish brown. . . . . . . .
z
z. Punctations large, few, widely scattered. Median and paramedian grooves deep and
distinct. Spiracular plates elongate oval (Pakistan, India, Burma).......
hussaini
Punctations small, moderately numerous adjacent to lateral grooves and posteriorly.
Median and parameclian grooves less distinct. Spiracular plates comma-shape (Pakistan, India). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
brevip~mctata
Females
r. Operculum ( ~' genital apron) profile slightly bulging ; outline elongately oval. Scutum, legs, and capitulum pale yellowish brown. Tarsus IV humped....
kumari
Operculum profile bulging anteriorly, depressed or sloping posteriorly. Scutum, legs,
and capitulum recldish brown. Tarsus IV fiat of slightly humped. . . . . . . . . . . .
z
z. Operculum wide, surface somevvhat dcpresscd mcdiopostcriorly. Punctations large,
very few in median field. Cervical grooves distinct . . . . . . . . . . . . . . . . . . . .
hussaini
Operculum an elongate oval, surface not depressed medioposteriorly. Punctations
fine, numerous in lateral and cervical fields, more wiclely scattered posteriorly. Cervical groo\·es poorly developed. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
brevipunctata
SUBGENUS
HY AMOMMA
Males
r. Lateral grooves short, not reaching central third of scutum. Punctations few on
central scutum..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
z
Lateral grooves reaching beyond posterior third of scutum. Punctations variable.
3
z. Subanal shields situated exterior to axis of adanal shields. Adana! shields often
curvcd posteriorly towards each other. Posteromedian groove reaching parma.
(Pakistan, northern India, U.S.S.R. to Africa). . . . . . . . . . . . . . . . . . . . . .
dromedarii
Subanal shields situated on the axis of the adanals (unengorged specimens). Adanal
shields straight. Posteromedian groove not reaching parma. [Cervical grooves
shallow, short, not reaching mid-scutum. Basis capituli dorsally with slightly concave
posterior margin, never angular
1].
26o(Pakistan, India, U.S.S.R. to Africa) ........ .
a. anatolicum
3· Scutum brown. Punctations numerous. Lateral, median, and paramedian grooves
not pronounced. (Pakistan, India, U.S.S.R. to Africa)....
marginatum turanicum
Scutum dark glossy brown. Punctations few, scattered, large. Lateral, median and
paramedian grooves weil developed. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4
4· With a (usually white) parma. Leg segments with dorsal white stripe. Cervical
grooves shallow (Pakistan, India, G.S.S.R. to Africa).... . . . . . . . . . . . . . .
detritum
Without parma. Leg segments with sharply defined rings on joints. Cervical grooves
marginatum isaaci
deep. (Pakistan, India, Ceylon). . . . . . . . . . . . . . . . . . . . . . . . . . . .
Females
r. Operculum (= " genital apron ") profile gradually depressed posteriorly ; outline
triangular. Scutum with few large puncatations. . . . . . . . . . . . . . . . . . . . . . . . . . . .
2
Operculum profile flat or bulging ; outline variable. Scutum with variable punctations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3
2. Operculum narrowly triangular (V shaped).
Legs usually ringed....
dromedarii
Operculum widely triangular, approximately equilaterally so. Leg segments usually
with white stripe dorsally. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
detritum . ..
3· Operculum short, small (knoblike). Scutum light brown with shallow cervical grooves.
a. anatolicum
Legs usually lacking rings. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Operculum widely triangular. Scutum brown to dark brown. Legs with rings or
strips . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4
4· Scutum dark glossy brown with few, scattered, large punctations ; cervical grooves
well developed. Legs with white, narrow, sharply defined rings. Operculum profile
slightly bulging.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
marginatum isaaci
Scutum brown with many punctations ; cervical grooves less pronounced. Legs with
less contras ting white rings or stripes. Operculum profile bulging ............... .
marginatum turanicum
SUBGENUS HYALOMMASTA
Hyalomma aegyptium (Linnaeus, 1758)
The Tortoise Hyalomma
(Figure 39)
Record.
PAKISTAN. Quetta (SHARIF, 1928, as H. syriacum).
Other records.
Other records of " H. aegyptium " from Pakistan, India, and
Ceylon (SHARIF, 1928) refer to H. a. anatolicum, H. dromedarii, and H. marginatum
subsp.
r. The details in brackets differentiate H. a. anatolicum from H. asiaticum (which may
occur in northern Pakistan), in which the deep, long, cervical grooves extend to the midscutum and the postcrior margin of the basis capituli dorsally is deeply concave and usually
angular. In the female JI. asiaticum, the cervical grooves are also deep, the operculum is
longitudinally oval, and the legs have white or yellowish rings.
-
26r-
H. aegyptium was revicwed and illustrated by PmiERA:\TZEV (rgso, pp. rg3-195)
and HoOGSTRAAL (rgs6, pp. sr::;-sr6).
Hasts and Distribution. Tortoiscs arc the chief hosts of ali stages. Hedgchogs
are secondary hosts of adults ; other mammals arc rarely parasitizecl by this stage.
Immature stages also feed on a Yariety of small reptiles, birds, and mammals.
H. aegyptium is clistributed in parts of the l\Iediterrancan basin, castvvard through
southern U.S.S.R. (as far as Taclzhikistan), through Afghanistan, and (SHARIF, rg28)
into \Vest Pakistan (Quetta). ABBASSIAK-LI:\TZEN (rg6o) stated that H. aegyptium
is common on tortoiscs in northwcstcrn Iran, but rcported none from east of the
Ca-;pian Sea. Specimens from Afghanistan have bccn noted by ILusER and
HooGSTRAAL (rg63).
Diagnosis. Both sexes arc casily recognized by the two equal, \Yell separated
spurs of coxa I. The male scutum is smooth and shiny, with few scattcred, large
punctations ; festoons arc unfusccl ; lateral grooves and a caudal depression are
lacking. Adana! shields arc very large but subanal shields arc very small or sornetimes lacking.
The fcmale scutum is shiny and smooth with fcw, scattercd, large decp punctations. The operculum is a flat, widcly triangular shield that becomes greatly
depressed postcriorly upon engorgement. The form of the mounted genital area
is illustrated in fig. 39·
Although the sizc range of H. aegyptium is variable, most specimens are comparatively large. The few from Afghanistan arc the smallest specimens of this
spccies that we have sccn.
St'BGE:\CS HY ALOMJv[ A
Hyalonmza kumari Sharif, rg28
The Indian Goat Hyalomma
(Figures r to g, 40)
Hyalomma (Hyalommina) l<umari sp. nov., SHARIF, 1928, pp. 319, 320, fig. 40
and Plate IX.
Cotypes in Indian Museum (
2
~; 3\
from wild goat (or .Nilgiri Thar),
Hemitragus hylocrius (OGILBY), Parambikulam, altitude r,JOO to 3,200 feet, Cochin
(now Kerala State). (The type locality is uncertain; no such place is now known
in the area of old Cochin State. There is a place called " Perumakulam " in Trivandrum District. The type specimens were collected on r6 September 1924
by F. H. GRAVELY; 2 c)c), 2 c;2c;2 of cotype series are now in BM(.NH)).
A carola gia, t. VI, fasc.
2,
r964.
I7
-262-
Hyalomma excavatum Koch, r844; DELPY, 1949, p. 488, synonymized H. kumari.
Hyalommina kumari Sharif, 1928 ; FELDMAN-MUI-ISAM, 1957, pp. 53-56, figs 9-rr,
d' and Cf! redescribed and illustrated; NAGAR, 1962, p. 6r, stated agreement.
lYiaterial examined. PAKISTAN. r d' r Cf!, domestic goat, Nagar Parkar, in the
Great Rann, near the Indian border, 4 February 1963, Vincent McCARTHY (RH 3692);
thesc specimens differ slightly from those of India ; sec Identification below.
lNDIA. Kerala (sec note above) : 2 d'd', 2 Cf!Cf!, cotype series, data as above,
Nuttall collection No. 3659, BM(NH). Uttar Pradesh : r d', 2 Cf!Cf!, goat, Haldwani,
2 June 1905, R. E. Montgomery (" Hyalomma n. sp." on label), BM(NH). 15 d'd',
goats, Agra, 27 July 1909, F. H. HANKΠ(on labels : "Hyalomma n. sp., note
tarsus, seen by L. E. ROBINSON) "), NGTTALL no. 759, BM(NH). 9 d'd', goat,
Izatnagar, Bareilly, February, 1946 (RML 22400). Bihar : 2 Cf!~, black goat,
Jahanabad, Gaya (HH 2745). PunJ·ab : r Cf!, sheep, Capt. H. E. Cross, Nuttall
no. 3552, BM(NH). Delhi: r ~' goat, Bajhghera (NAGAR collection). Note absence
of material of this species from Maharashtra State in VRC collections.
NEPAL. r d', Tibetan sheep at Kathmandu market, November, 1959, R. L. Fleming (HH 2746).
AFGHANISTAN. 3 d'd', Bashgul Valley, rroo and r2oo meters altitude, Nuristan,
April, 1953 (HH 2737, 2738, 2739) (reported as H. excavatum by ANASTOS, 1956;
see also KAISER and HooGsTRAAL, 1963).
Other records. AssA~I : Goalpara District (SHARIF, 1928). lNDIA : SHARIF
(1928) listed a number of collections from Bihar, Orissa, Uttar Pradesh, Madhya
Pradesh, and Punjab (Faridkot District). PAKISTAN. Sialkot (fmmerly Punjab)
(SHARIF, 1928).
Hasts and distribution. H. kumari appcars to parasitizc chiefty wild and
domcstic goats. It also infests domestic sheep, dogs, cattle, and horses. Sharif's
specimen from Assam was from a tiger. Hosts of immature stages are unknown.
This species is widely distributed from northcastern Pakistan to Madras in the
south and Assam in the east. The specimen from Tibetan sheep in the market
at Kathmandu, Nepal, suggests that H. kumari may also occur in Tibet. We have
not seen other specimens of this specics among large collections of ticks from
Nepal, though several records from Uttar Pradesh are from localities close to the
western border of Nepal. The exact relationships of the three somewhat atypical
Afghanistan males to H. kumari of India cannot be determined at the present
time (KAISER and HooGSTRAAL, 1963). The ecological situations inhabited by
this species are unknown.
Identification. The basis capituli is narrow dorsally and has anterior lateral
projections ventrally; subanal shields are lacking (Subgenus Hyalommina). The
FIGS. r,
FIG. r to 4· Hyalomma kumari, Jahanabad, Gaya, Bihar, India (HH 2745).
male, dorsal and ventral views. - FrGs. 3, 4, female, dorsal and ventral views.
2,
male, measuring from 3·3 to 3.8 mm. in length and from r.5 to r.8 mm. in width,
has a pale or transparent yellowish to light brown scutum with few large and
medium size, shallow punctations, which are somewhat more numerous laterally
and posteriorly. The more or less distinct, shallow lateral grooves may be short,
long, or absent, and contain large and medium size punctations which are usually
contiguous posteriorly. The shallow cervical grooves arise from deep cervical pits
and extend posterior of the eyes. The posteromedian and paramedian grooves
are shallow and indistinct. The venter is whitish or pale yellow and the spiracular
plates (fig. 8) have a unique form. The large, broadly rectangular adanal shields
are almost contiguous; subanals are lacking. Legs are yellowish brown, not ornamented. Tarsi are short ; IV (and sometimes others) is humped.
The female operculum is longitudinally oval and slightly bulging in profile ;
3
3
6
7
FIGS. 5 to g. Hyalomma kumari, Jahanabad, Gaya, Bihar, India (HH 2745).- FIG. 5, female
operculum in profile. - FIG. 6, female operculum and genital area. - FIG. 7, female
spiracular plate. -FIG. 8, male spiracular plate. -FIG. g, male tarsi I to IV, lateral view.
-265when mounted, a distinctive rounded eup is seen surrounding the orifice posteriorly
(fig. 40). Body and leg colors are like those of the male. The scutum, somewhat
longer than wide, is smooth posteriorly but bas wide, long cervical grooves containing
large punctations and other large punctations are present in the anteromedian field.
The Pakistan male and female collected from a wild goat by Mr. V. McCARTHY
(HH 3692) differ slightly in that the ventral lateral projections of the basis capituli
are more blunt than in those from India. More material is necessary to determine
the importance of this variation.
Hyalomma brevipunctata Sharif, 1928
Sharif's Indian Haylomma
(Figures 10-18, 41)
Hyalomma (Hyalommina) hussaini var. brevipunctata nov., SHARIF, 1928, p. 318.
Cotypes in Indian Museum \ ~~) from domestic dog, Anantapur, Madras (now
Andhra Pradesh State).
Hyalomma excavatum Koch, 1844; DELPY, 1949, p. 488, synonymized H. hussaini
(and var. brevipunctata by implication).
Hyalomma hussaini Sharif, 1928 ; SANTOS DIAS, 1954, p. 379, synonymized
H. brevipunctata.
Species inquirenda; FELDMAN-lVIUHSAM, 1957, p. 58.
NAGAR, 1962, did not consider this species in his revision of Hyalomma from
In dia.
Hyalomma brevipunctata Sharif, 1928 ; KAISER and HooGSTRAAL, 1963, new
combination.
""faterial examined : PAKISTAN.
(HH 2732).
1
<3',
human,
Karachi,
January,
1944
INDIA. Gujerat : (Saurashtra District, January ,1958) : 1 <3', bullock; 5 <3'<3',
2 <fl<fl, buffalo, Barda Hills (2 <fl<fl HH 2729). rr d'd', goats, Ranawo. (Junagadh
District) : 1 <3', bullock; 1 <3', goat, Dolatpara. (Gohilwad District, October,
1959) : 5 d'd', 6 <fl<fl, cattle, Sanosara. (Sorath District, October, 1959) :
2 d'd', cattle, Kutiyana. (Kutch District, March, 196o) : 34 d'd', 37 <fl<fl, cattle,
Durbana (z8 d'd', 20 <fl<fl, HH 2727, 2728). 1 <fl, human; 4 d'd', 2 <fl<fl, cattle; Kuar-Bet.
1 <3', 1 <fl, Khauyda, horse.
1 <3', 2 <fl<fl, camel, Dhori. (Jura, District March, 1961) :
2 d'd', 1 <fl, camels, Wadi Jat Ali Mohamed. AU VRC. Madhya Pradesh : (Indore
District, December, 1958) : 54 d'd', 14 <fl<fl, cattle, Bhaironghata. 1 <3', 1 <fl, cattle,
Bai. Both VRC. 1 <3', 1 <fl, Blue Bull (Nilgai Antelope, Boselaphus tragocamelus
-
z66-
FrGs. ro to 13. Hyalomma brevipunctata, Durbana, Kutch, Gujerat, India (HH 2728).
FrGs. ro, II, male, dorsal and ventral views.- FrGs. 12, 13, female, dorsal and ventral views.
-267(Pallas, 1766)), within 50 miles of Raipur, Nilghac, 4 August 1950 (HH 2733).
Delhi : 1 Cjl, calf, Vinay (Nagar collection). Mysore : 5 ({({, cattle, Mysore,
24 August 1945 (HH 2731). Bihar : 1 Cjl, bullock, Gaya, February, 1926 (RML).
Madras : 5 CjlCjl, Madras, October, 1909, Nuttall collection no. 906 b, BM(NH)
(HH 2730).
I
,
~4
TI
~
3
3
15
16
17
FrGs. 14 to r8. Hyalomma brevipunctata, Durbana, Kutch, Gujerat, India (HH 2728). FrG. J4, female operculum in profile. - FIG. rs, female operculum and genital area. FrG. r6, female spiracular plate. -FIG. 17, male spiracular plate. - FrG. r8, male tarsi I
to IV, lateral view.
Other records. lNDIA. SHARIF (1928) listed localities, mostly in central and
eastern India, in Madhya Pradesh, Andrha Pradesh, Maharashtra, Bihar, Orissa,
and Bengal States.
Hasts and distribution. Hosts of adults are domestic cattle, goats, buffalo,
dogs, and camels. A human was host of the specimen from Karachi and a "wild
-268blue bull" for those from Nilghac. In Bengal, SHARIF (1928), reported the Sambar
Deer, Cervus unicolor niger Blainville, and the Chital or Spotted Deer, Axis a. axis
(Erxleben), as hosts. Animais parasitized by immature stages are unknown.
Ecologically H. brevipunctata has been recorded from situations as variable as
Kutch desert:; and Bcngal jungles, geographically from Karachi in Pakistan to
near Calcutta in Bcngal.
Identification. The basis capituli is broader than long and has anterior lateral
projections, adanal shields are broad and contiguous, and subanal shields arc
lacking (Subgcnus Hyalommina). The male (mcasuring from J.O to J.C) mm in
length and I.5 to 1.9 mm in width) has a light brown scutum with fevv punctations
in the céntral arca and modcratc numbcrs of small and medium sizc punctations
posteriorly and bordering the lateral grooves. The deep, distinct lateral grooves,
which réach the level of the eyes, are dotted with hcavy, usually contiguous punctations. The cervical groovcs are merely deep, short pits. In the caudal arca,
threc clcep, longitudinal, heavily punctatc depressions represcnt the postcromedian
and paramedian groovcs. The ventral shields are like thosc of H. lmmari. The
spiracular plates are as illustrated (fig. 17). The tarsi arc longer than those of
H. kumari and lcss humped or flat topped.
The female operculum is elongatc oval in outlinc (fig. r5) ; in profile it is gradually slanted posteriorly (fig. 14). \"'hen mounted (fig. 41), the postcrior margin
of the operculum is broad and truncatc and the eup surrounding the orifice is
triangular. The operculum has a minute, membranous posteromedian 1ip (indicated by small paler area in fig. r5) that is not clearly characterizcd in mounted
speCimens. The light brown scutum is slightly longer than wide and smooth
posteriorly. Large punctations are present in the shallow, wide cervical grooves
and in the anteromedian field.
Hyalomma hussaini Sharif, 1928
Hussain's Indian Hyalomma
(Figures 19-26, 42)
Hyalomma (Hyalommina) hussaini (forma typica) sp. nov., SrrARIF, 1928,
pp. 314-3I8, fig. 39 and Plate IX.
Cotypes in Indian Museum
(~~)
from bullock,
.\kola, Central Provinces (now Madhya Pradesh).
Hyalomma (Delpyiella) hussaini Sharif, rgz8; SAJ\iTOS DIAS, 1956, p. 459,
designated H. hussaini as type species of subgenus Delpyiella nov.
Hyalomma hussaini Sharif, 1928 ; HoocsTRAAL, 1956, pp. 519, 523, figs 198-zor ;
figs 200 ande represent a dry specimen of H. brevipunctata mistaken for H. hussaini.
wi. · 0/ Qi
a
\
b
\
c \
FrGs. rg to 22. Hyalomma hussaini. - FrGs. 19, 20, male, dorsal and ventral views, Daya,
Bihar, India (HH 2787).- Frc;s. 21, 22, female, dorsal and ventral views, Kutiyana, Sorath,
Gujerat, India (HH 2750). a, b, c, fcmale opercula, outlines and profiles.
-270Hyalommina hussaini Sharif, 1928; FELDMAN-MUHSAM, 1957, pp. 52, 53, figs 6-8,
d' and s;2 redescribed and illustrated; NAGAR, 1962, p. 61, stated agreement.
Material examined. PAKISTAN. 1 s;2, sheep, locality illegible (RML). lNDIA.
Gujerat : 2 66, goat; 1 s;2, sheep (HH 2789), 6 66, 1 s;2, buffalo (HH 2750, 2788),
3 66, cattle (HH 2748), aU Kutiyana, Sorath District, September and October, 1959
3
3
23
26
24
25
FIGS. 23 to 26. Hyalomma hussaini. -- FIG. 23, female genital area.
FIGS. 24, 25, female and male spiracular plates. ~ FIG. 26, male tarsi I to IV, lateral view.
(VRC). Maharashtra : 6 66. cattle, Mulshi, Pirangut, Poona District, April, 1960
(VRC) (2 66, HH 2749). Bihar : 4 66. 3 s;2s;2, bullock, Gaya, February, 1926
(HH 2787).
Other records. SHARIF (1928) listed a large number of specimens from localities
in Bihar, Orissa, Madhya Pradesh, Madras, and Maharashtra States. SANTOS
DIAS (1954) reported a few specimens from domestic mammals from Goa; sorne
of these may have been H. brevipunctata, which he considered to be a synonym
of H. hussaini.
-271-
Hasts and distribution. Adults of H. hussaini have been recorded from domestic
cattle, buffalo, camels, horses, and dogs, but favorite hosts are unknown. Hosts
of immature stages are unknown. This specics is widely distributed in India and
occurs in Pakistan, but the ecological situations in which it exists remain to be
studied.
Identification. The basis capituli is broader than long dorsally and has anterior
lateral projections vcntrally. Adanal shields are broad and contiguous, and subanal
shields are absent (Subgenus Hyalommina). The male (measuring approximately
3-3 mm in length and r.8 in width) has a smooth, glossy, reddish brown scutum
with rare punctations in the central and caudal areas and moderate numbers
in the scapular and cervical areac;. The deep, distinct lateral grooves extend almost
to the level of the eyes. The shallow, smoothly rounded cervical grooves extend
from the deep cervical pits almost to the scutal midlength. The posteromedian
groovc is deep, long, and narrow and reaches the midfcstoon. The paramedian
groovcs are wider and shortcr and separated from the festoons by a narrow area
of smooth integument. Two narrow, convex, very shallow, sublateral depressions
are usually present on the posterior half of the scutum. The ventral shields are
like those of H. kumari. The spiracular plates are as illustrated (fig. 25). The
tarsi arc like thosc of H. brevipunctata.
The femalc operculum (figs 22 a, b, c, 23) is widely subrectangular or shieldshape
and its surface is usually somewhat deprcssed medioposteriorly ; in profile it is
gradually slanted. When mounted (fig. 42) the genital arca shows a wide, funnellike eup opcning into a narrow vaginal tube. The scutum is slightly longer than
wide, smooth and glossy, with few scattered, large, shallow punctations, especially
in scapular and cervical areas ; the cervical grooves are smooth and shallow.
SUBGENUS HY ALOM MA
Hyalomma anatolicum anatolicum Koch, 1844
The Small Anatolian Hyalomma
(Fig. 43)
Material examined. PAKISTAN. 125 c)'ê, 125 ~~ (approx.), sheep; 3 c)'c)', 2 ~~'
goats ; 10 c)'c)', 5 ~~' horses ; varions localities in general area of Lahore. 7 c)'c)', 5 ~~'
bullock, Nowshera, April, 1907, NuTTALL no. 256, BM(NH). 1 c)', goat, Rawalpindi. 7 c)'c)', 1 ~' sheep, Jhelum. 4 c)'c)', 2 ~~' cattle, Setharja (HH 1582). 6 c)'c)',
1 ~' 2 NN, cattle (HH 1579, 3645) ; 14 c)'c)', 10 ~~' sheep (HH 1583) ; 33 c)'c)', 31 ~~'
horses (HH 1580, 1581); 14 c)'c)', 3 ~~'buffalo (HH 1585); 6 c)'c)', 4 ~~' goat (HH3642);
Khairpur. 16 c)'c)', I I ~~' Tando Musti Khan (HH 1578). 8 c)'c)', 4 ~~, buffalo,
-272Gumbat (HH 1584).
Sukkur.
5 d'd', 7 ~~. bullock (HH 3643) ; 8 66, 16
~~.
horse (HH 3644);
INDIA. Delhi (localities in and near New Delhi, .t\agar collection) : 76 d'd',
24 ~~' cattle ; 1 ~' buffalo ; 12 d'd', camels ; 6 d'd', 5 ~~'mules ; 62 d'd', 20 ~~' horses ;
40 d'd', 1 ~' pigs ; 2 d'd', 6 ~~' goats. Himachal Pradesh : 1 d', cattle, near Simla,
BM(NH). Gujerat : (Sorath District, September-October, 1959) : 10 d'd', 5 ~~'
cattle; 1 d', buffalo ; Kutiyana. 2 d'd', bull, Mohabatpura. (Gohilwad District,
October ,1959) : 1 d', cow, Sanosara. (Junagadh District, January, 1958) : 7 66,
bullock; 8 66, 1 ~. buffalo; Dolatpara. (Saurashtra District, January, 1958) :
7 d'd', 1 ~' camel (HH 1421) ; 1 ~' buffalo; 12 d'd', 3 ~~' bullock; Barda Hills.
(Kutch District, l\Iarch and May, 1958, 1960) ; 3 ~~. camel, Dhori. 1 ~. goat,
Khavada (HH 1422). 8 66, 1 ~' goats; 2 ~~' cattle (HH 1423) ; Kakar-Khavada.
All VRC. .Madhya Pradesh: 1 d', 1 ~' cow, Bhaironghata, Indore District, December, 1958. VRC. Andhra Pradesh : 2 d'd', Donga pony; 3 66, 8 ~~. bullock
(HH 1424) ; Secunderabad; :\!lay and June, 1906, Nuttall nos. II2 and II7 Bl\l(NH).
1 ~' horse; 4 d'd', 2 ~~' no host listed; Hyderabad, January, 1906 and 1913,
NUTTALL nos. 34 and 1990 a, BM(NH).
Other records. For a review of this tick, see Hooc;sTRAAL (1956, pp. 435-451,
as H. excavatum) and ANASTOS (1957, pp. 149-152). The definitive work is that
of HOOGSTRAAL and KAISER (1959).
Hasts and distribution. Adults of H. a. anatolicum feed on all domestic animais
and immature stages usually feed on the same hosts as adults. This is one of the
most widely distributed ticks in the genus Hyalomma, ranging from the Canary
Islands and northwestern Africa through Arabia, the .t\ear and Middle East and
southern U.S.S.R. to Afghanistan, Pakistan, and northern India, at least far south
and east as Secunderabad and Hyderabad.
Identification. The male is a small, narrow, yellowish brown tick with a con v ex,
lightly punctated scutum (less than 3.85 mm in length) ; very short but distinct
lateral grooves ; a depressed, punctate caudal field between two smooth ridges ;
a pronounced posteromedian groovc not reaching the parma; small subanal shields
directly posterior of the adanals ; legs yellowish, unstriped, rarely with faint pale
markings, but not marbled when dry (for typical and variable specimens, see
HooGSTRAAL and KAISER, 1959, figs 1, 2, 5-IZ).
The female (loc. cit., figs 3, 4) has a bulging, small, knoblike genital operculum
which in outline is usually circular but may be traingular. The genital area in
a mounted specimen is illustrated in fig. 43· The scutum is usually longer than
wide with a narrowly rounded posterior margin, a few large punctations in the central
field and scapular areas, and a variable number of very fine, superficial punctations
ovcr much of the surface.
Taxonomy. FELDMAN-MUHSAM (1962) refers to H. a. anatolicum as H. excavatum
and to H. anatolicum excavatum as H. anatolic~tm species inquirenda. In so doing,
-273she overlooks the neotype already designated for the former form and that much
data has been presented to show that the existing type specimen of excavatum
Koch, r844, from Egypt, which she bad earlier (r954) very usefully redescribed,
represents a distinctivic taxon, recognized by structural and biological characteristics
in Egypt and elsewhere in ~orth Africa and western Asia (HoocsTRAAL and KAISER,
1959). Following one of two Soviet schools, FELDI\IAN-MUHSAl\1 considers both
subspecies as one polymorphie species, yet she redcfined H. anatolicum excavatum
as a separatc taxon (H. anatolicum) and calls it "species inquirenda ". She fails
to state that not ali Russian workers are in agreement on this subject. She stresses
the light yellow color on the anterior scutum of her " species inquirenda " ; this
is often useful as a distinctly secondary character but shades of scutal coloration
are biologically and taxonomically unsound primary criteria on which to differentia te
Hyalomma taxa. Although our colleague disputes that H. anatolicum excavatum
occurs in Russia, numerous specimens identified as such and conforming to the
physical characteristics of this form outside of Russia have been presented to us
by Russian workers. FELDMAX-NlUHSAM states that in Russia the form excavatum
does not show the yellowish color on the anterior scutum; however those in our
collection do have this color.
The decision to lump these two forms as one (PERVOMAISKY, 1954) was based
on a single study of laboratory-reared ticks. Useful and important as this technique
is, it is also a two-edged sword. vVe have indicated earlier, regarding a tropical
African Hyalomma species that FELDMAX-MUHSA:VI had incorrectly defined (HooGSTIU\AL, 1956, pp. 501-2), that while the laboratory environment may provide a
certain range of optimal conditions, if often permits survival of larger numbers
of stunted, atypical specimens thau may be normally found in nature. ~umerous
workers (among them, SHATAS, rg56) have reported atypical laboratory-rearcd
ticks where few occur in field collections. Owing to the toughness of Hyalomma
ticks, sorne misformed individuals survive in nature ; these are always confusing
but must be recognized as such. Stunted specimens are morphologically atypical ;
they do not otherwise alter thE basic biological or taxonomie patterns of the forms
they reprcsent.
Ample morphological, biological, and ecological evidence bas been prcsented
to show the distinctness of the forms anatolicum and excavatum. The question
of whether these should be considered as subspecies or as full species revolves
around a perplexing procedural problem that is one of the most controversial in
modern biology. Within our conceptual framework, these are subspecies. This
view is enhanced by similarity of female opercula of the two forms. vVe recognizc
that sorne taxonomists analyzing the same biological and structural detail, might,
with much reason, cali these forms separate species. However, a few convenient
samples cannot be forced into simple structural categories A and B while ignoring
the wealth of supporting biological data as well as the range of structural variation
in any single population in nature.
The anatolicum complex requires a large amount of continuing cooperative
-274research in many scientific disciplines and in an extensive geographie area ; these
prcblems will only be solved by this approach. Until meaningful studies can be
accomplished, two or possibly even more schools of thought concerning the anatolicum complex will persist. Unfortunately for the many workers in public health,
veterinary medicine, and microbiology who frequently must refer to these forms,
there is little hope for early seUlement of these questions owing to the vast and
difficult terrain in whi.ch these ticks exist, as well as to the long period necessary
for adequate study, the extensive field and laboratory facilities required, the political
aspects that make cooperative scientific efforts difficult in this area, and the number
of highly qualified researchers who must cooperatively undertake this research.
Hyalomma dromedarii Koch, 1844
The Camel Hyalomma
(Fig. 44)
Material examined. PAKISTAN. 7 é{é{, 1 C(, cattle, Rawalpindi, May, 1959
(RML 35662). 32 é{é{, 27 C(C(, camels, Bahawalpur, January, 1955 (HH 85). 1 é{,
camel, Lahore, February, 1953. 5 é{é{, buffalo, Shahzada, near Lahore, 6 September 1962 (HH 3639). 10 é{é{, 24 C(C(, camel, Lahore, October, 1912, Nuttall no. 3425,
BM(NH). 7 é{é{, 5 C(C(, Kamar Mashasse, February, 1955. 23 é{é{, 3 C(C(, camel,
Karriar Markani, May, 1955. 3 é{é{, 2 C(C(, cow, Choa, May, 1956 (HH 84). 3 é{é{,
sheep, Dina. 1 C(, cow, Tando Musti Khan (HH 1586).
INDIA. Gujerat : (Kutch District, March, 1960) : 271 é{é{, 128 C(C(, camels,
Dhori. 37 é{é{, I I C(C(, cattle, Durbana. 3 é{é{, 3 C(C( horse; 1 é{, goat; 2 é{é{,
3 C(C(, cattle; Kuar Bet (HH 17). 1 é{, camel; 1 é{, goat; Wad-Wali-Wai. (Sorath
District, October, 1959) : 1 é{, camel, Porbander (Saurashtra District, January,
1960) : 6 é{é{, 3 C(C(, camels, Barda Hills. All VRC. Andhra Pradesh: 1 é{, pony;
18 é{é{, !9 C(C(, bullock; Secunderabad; May and June, 1906, Nuttall nos. rr2
and rr7, BM(NH). Delhi (localities in and near New Delhi; Nagar collection) :
5 é{é{, 4 C(C(, cattle; 3 é{é{, buffalo; 38 é{é{, camels; 1 é{, 1 C(, horse; 1 C(, goat.
Other records. For a review of H. dromedarii, see HooGSTRAAL (1956, pp. 420-435)
and ANASTOS (1957, pp. 143-148).
Hasts and distrib~ttion. Adults of Hyalomma dromedarii attack all domestic
animais. This species is almost entirely restricted to areas in which the camel,
its chief host, occurs. Larvae and nymphs parasitize rodents, hares, and hedgehogs,
and sometimes lizards and birds. This tick ranges through desert and steppe
lands across northem Africa as far south as northem Kenya, through Arabia,
and Near and Middle East, and southern U.S.S.R. to Tadzhikistan and Uzbekistan.
It is apparently common in Afghanistan, Pakistan, and north western India.
-2751dentification. :Males are usually largcr than th ose of H. anatolicum. Their
subanal shields arc displaced laterally and their lateral grooves are limited to the
posterior third of the scutum. A few large shallow punctations are scattered over
the scutum, other punctations are rare or absent. The posteromedian groove is
deep and narrow ; it cxtends from the distinct parma to the scutal midlength and
is bounded by converging ridges and deep, rugose paramedian grooves.
The fcmale genital operculum, elongately triangular in outline and gradually
dcpressed in profile, is surrounded by a narrow, raised integumental fold. In
mountcd specimens, the genital arca appears as in fig. 44· The scutal lengthwidth ratio is approximatcly equal; scutal punctations are few and large ; and
the surface is frcquently rugose.
Hyalomma detritum Schulze, 1919
The Shiny Hyalomma
(Fig. 45)
Hyalomma aegyptium subsp. ferozedini nov. ; SHARIF, 1928, pp. 310, 311, fig. 37.
Cot~pc
(~~J
in Indian Museum
Ind1a.
from cattle, Sasaram, Shahabad District, Bihar,
1
DELPY, 1949, pp. 471 and 485, and NAGAR, 1962, p. 6r, considered Sharif's
subspecies ferozedini and isaaci to be synonyms of H. detritum.
Material examined. PAKISTAN. 2 JJ, sheep, Punjab (HH 1361). 3 JJ, 6 ~~'
cattle and goats, Muree and Gholi (HH 1362). r J, r ~' Goat, Khairpur, Gumbat,
ro Septembcr 1962 (HH 3641).
INDIA.
Delhi : 3 JJ,
I
~'
calf, Vinay (HH 1338).
Other records. H. detritum was reviewed by HooGSTRAAL (1956, pp. 403-419)
and ANASTOS (1957, pp. 132-142). SHARIF's (1928) apparently synonymous
H. aegyptium ferozedini was recorded from Bihar and Orissa.
H osts and Distribution. Domestic cattle and horses are the chief hosts of
H. detritum. All stages feed on the same kind of animal. Sheep and goats, and
any other domestic animal, as well as humans and wild hares and ungulates may
also be parasitized. H. detritum is localized in specialized ecological zones in
northwestern Africa and other areas of the Mediterranean Basin, the Near East,
and southern Russia. In Afghanistan, Pakistan, and India, H. detritum is known
by very few specimens.
1dentification. The male su banals lie directly posterior to the adanal shields
and the cleanly eut lateral grooves reach the level of the eyes. The bright, glossy,
reddish to dark brown, arched scutum has rare, superficial punctations; a narrow,
-276long posteromedian groove extending from the parma to the scutal midlength ;
and pronounced though variable paramedian groovcs. The legs are reddish or
yellowish brown and may have pale, poorly contrasting rings. Among Pakistani
samples of this species (HH 3641) are specimens equalling the maximum size that
this species reaches elsewhere.
The female genital operculum is equilaterally triangular with slightly convex
margins, a rounded or truncate (not narrowly rounded) posterior juncture, and
a gradually depressed profile. When mounted, the genital area appears as in fig. 45·
The shieldshape scutum is longer than wide, smooth and shiny, with no or rare
punctations.
Hyalomma marginatum isaaci Sharif, 1928
Isaac's Indian Hyalomma
(Figures 27-30, 46)
Hyalomma aegyptium subsp. isaaci nov. ; SHARIF, 1928, pp. 307-310, fig. 36 and
Plate IX.
Cotypes in Indian
~Iuseum (~g)
from buffalo, Kandeli, Hoshangabad
District, Central Province (now Madhya Pradesh), India.
Hyalomma detritum Schulze, 1919 ; DELPY, 1949, p. 485, and NAGAR, 1962,
p. 61, synonymized this form under H. detritum.
Hyalomma marginatum isaaci Sharif, 1928; new combination, KAISER and
HOOGSTRAAL (1963).
Material examined.
(HH 2771, 2773). 1
collection.
cr,
cr,
CEYLON. 1
1 ~ ,goat, Nikaweratiya, April, 1959
buffalo, Batticaloa, April, 1959 (HH 2772) ; Seneviratna
crcr,
PAKISTAN, 3
2 ~~' sheep, Buchal Kalan (HH 2791).
Rawalpindi, September, 1917, Nuttall no. 2465, BM(NH).
Khairpur, Gumbat (HH 3648).
cr,
crcr,
cr,
9
2
crcr,
crcr,
1 ~' buffalo,
3 ~~' goat,
cr cr,
INDIA: Delhi: 1
1 ~'buffalo ; 1 1 ~' sheep; 3
5 ~~'calf, Nagar collection.
Uttar Pradesh : 4
sheep, Madanpur. Madhya Pradesh: 2 ~~' Lepus nigricollis,
Balaghat, Suphkar, 10 March 1959 (VRC-A22775). ]\;[aharashtra : 2
cattle,
Pirangut, Poona District, April, 1960 (VRC). 2 ~~' Lepus nigricollis, Tulsi, Bombay, Salsette Island, 14 April 1962 (VRC-A 34044). Gujerat : (Saurashtra District,
January, 1958) : 1
camel; 1
1 ~' buffalo (HH 2782) ; Barda Hills. 35
13 ~~,buffalo, Gir Forest. (Gohilwad District, October, 1959 and January, 1960) :
29
2 ~~, cattle, Sanosara (HH 2776, 2785). (Sorath District, October, 1959) :
3
camel, 1 ~' human ; Kutiyana. (Kutch District, March, 1960) : 12
6 ~~' camel, Dhori (HH 2781). 27
14 ~~' cattle, Durbana (HH 2775). 1 ~'
goat, Kakar-Khavada (HH 2780). 2
goats, Wad-Wali-Wai. 2
1 ~'
cr,
crcr,
crcr,
crcr,
cr,
crcr,
crcr,
crcr,
crcr,
crcr,
-277Lepus dayanus, Kuar-Bet. 1 Cj2, collected as fed nymph off Passer domesticus
(SS zog), Bhuj, 9 September 1959 (HH 2784). Ail VRC.
KASHMIR. 1 Cj2, rea red from nymph from Blue Rock Thrush (AI onticola solitaria
pandoo), Sajapur, approximately, 6,ooo feet altitude, Kashmir Valley, 7 May 1959,
M. G. R. Varma (VRC-A 21794) (HH 2774) (see remarks under hosts and distribution, below). 2 cjcj, cattle, Muzaffarabad, July, 1951 (HH 2790).
No LOCALITY : 1 cj, hare, October, 1912, Nuttall no. 3423, BM(NH). 2 cjcj,
2 Cj2Cj2, laboratory reared, Armed Forces Medical College, Poona, from Miss U. Rau
(HH 3640).
Other records. lNDIA. Numerous collections from many localities in Bihar,
Orissa, Uttar Pradesh, Madhya Pradesh, Madras, and Maharashtra States were
reported by SHARIF (1928). PAKISTAX. SHARIF's (1928) records from Jhelum
and Dera Ghazi Khan, formerly Punjab, apply to Pakistan. NEPAL. A single CJ2
from the Red Deer or Shou, Cervus elaphus wallichi Cuvier (= Cervus affinis),
at Kota was listed by SHARIF.
Hosts and distribution. The above records of nymphs of this tick from a Blue
Rock Trush in Kashmir and from a Domestic Sparrow in Kutch conform to the
immature-stage host pattern of the H. marginatum complex, which includes a very
large variety of ground-feeding birds and hares. Hasts of larvae and nymphs
of this form have not previously been recorded. Adults of the subspecies isaaci
have been taken from domestic cattle, buffalo, camels, horses, dogs, sheep, and
goats, as well as from several hares and a human.
This form, widely distributed in India, also occurs in Ceylon and Pakistan.
The single Afghanistan sample may represent specimens introduced on camels
from Pakistan. \Ve consider the Nepal record as tentative since we have not
seen representatives of this species among large collections of ticks from wild and
domestic animais inN epal. The specimens of H. marginatum isaaci from a migra ting
bird and from cattle at Muzaffarabad are the only hyalommas known from Jamma
and Kashmir. No others were collected there during the Virus Research Centre
Expedition to Kashmir. The bird host of the Kashmir nymph, taken on the VRC
expedition in May, 1959, had probably recently migrated from the plains of India.
Life cycle. RAu (1963) reared this subspecies in the laboratory as a two-host
tick with immature stages feeding on guinea pigs and adults on rabbits. Heavy
mortality occurred when larvae fed on rabbits. Adults were as large as those
from camels and cattle in nature.
Identification (figs 27-30, 46). The male scutum, dark glossy brown with few
large, scattered punctations, is quite straight posteriorly. Lateral grooves are
long, distinct, and deep posteriorly. The pronounced posteromedian and paramedian grooves extend to the festoons in a distinctive fashion and the smoothly
rounded cervical grooves extend to the anterior third of the scutal length. Additional depressions are one medially and one on each side tending to link the cervical
Acarologia, t. VI, fasc. z, 1964.
r8
-278-
Frcs. 27 to 30. Hyalomma marginatum isaaci. - Frcs. 27, 28, male, dorsal and ventral views,
Barda Hills, Saurashtra, Gujerat, India (RH 2782). - Frcs. 29, 30, female, dorsal and
ventral views, Kakar Khavada, Kutch, Gujerat (RH 2780).- Frcs. a and b, female and
male spiracular areas. - FrGs. c and d, female genital area and profile of operculum.
-279and paramedian grooves. Adanal shields are large and their inner margins lack
median projections posterior of the anus. The small subanals are situated on the
midaxis of the adanals. The integumental area around the spiracular plates is
somewhat pilose, and the plates have a moderately thick tail. The legs have irregular, contrasting white rings near the joints.
The female operculum is widely triangular and rounded posteriorly ; in profile
it is slightly bulging. The scutal color and punctation are as in the male. The
scutum is slightly longer than wide with deep, smoothly rounded cervical grooves
extending to and breaking the posterior margin.
Hyalomma marginatum turanicum Pomerantzev, 1946
The Turanian Hyalomma
(Figures 31-38, 47)
1v1aterial examined: PAKISTAN. 1 J', on acacia tree, Kohi-i-Murad, near Turbat,
Mekra (HH 2375) ; 1 <jl, on ground, Little Kapoto, 10 miles south of Kalat (HH 2792) ;
both March, 1955, Henry Field legit.
lNDIA. Gujerat : 2 d'd', cattle, Durbana, Kutch District (HH 2332).
camel, Dhori, Kutch District (HH 2333) ; both March, 1960, VRC.
1 <jl,
Other records. For reviews of H. marginatum turanicum, see PoMERANTZEV
(1950, pp. 216-218), SERDYUKOVA (1956), and HOOGSTRAAL (1956, pp. 528-532).
Subsequent records are from Iraq (HooGSTRAAL and KAISER, 1958), Iran (ABASSIANLINTZEN, 1961), and Afghanistan (KAISER and HooGSTRAAL, 1963). This subspecies
is further reviewed in our forthcoming report on the H. marginatum complex.
H osts and distribution. Hosts of adults are chie fly cattle, horses, and camels.
Larvae and nymphs parasitize a variety of birds. This form is widely distributed
in southern U.S.S.R. and from India to northern Africa, at least as far south as
Aden and northern Sudan and as far west as Libya.
Identification (figs 31-38, 47). The brown male scutum has dense, noncontiguous punctations that are more regular and deeper laterally than elsewhere.
The lateral grooves are long, seldom obscured by punctations. Cervical grooves
reach posteriorly beyond the eyes. Posteromedian and paramedian grooves are
more or less distinct ; a parma is absent. Adanal shields usually lack a medially
directed projection posterior of the anus ; subanals are situated on the midaxis
of the adanals. The integument around the spiracular plates is usually pilose
and these plates have thin to moderately thick tails. The legs are usually ringed
and striped dorsally.
The female operculum is widely triangular in outline and bulging in profile.
The scutum is as long as wide, with coloration and punctation as in the male. The
scapular areas are usually darker and have deeper punctations than the cervical areas.
-280-
FrGs. 31 to 34· Hyalomma marginatum turanicum, Chahbahar (Gulf of Oman), Iran (HH 2353).
- FrGs. 31, 32, male, dorsal and ventral views. - FrGs. 33, 34, iemale, dorsal and ventral
VleWS.
·- z8r-
SUMMARY
Species in the genus Hyalomma fall into three distinct, natural subgeneric groups,
but the names for these divisions remain moot.
Hyalomma ticks endemie in the Indian Subregion are H. kumari Sharif (Afghanistan, Pakistan, In dia to Assam, N epal, ? Tibet), H. hussaini Sharif (Pakistan, In dia,
Burma), H. brevipunctata Sharif (Pakistan, India), and H. marginatum isaaci Sharif
(Pakistan, India, Ceylon). The first three of these are in the subgenus Hyalommina,
l
3
3
36
FrGs. 35 to 38. Hyalomma marginatum turanicum. -FIG. 35, female genital area. - FIG. 36,
female operculum, in profile.- FIGS. 37, 38, spiracular plates and surrounding integumental
area, male and female.
the fourth in the subgenus Hyalomma. Adults of each species parasitize chiefiy
domestic animais; H. kumari appears to have a predilection for wild and domestic
goats. Hosts of immature stages are unknown, except that adults of H. marginatum isaaci have been reared from nymphs taken from birds. Adults of the
subspecies isaaci have been collected from wild hares on several occasions ; this
immature and adult stage hostpattern conforms to that of other members of the
marginatum complex elsewhere.
A number of African-Asiatic species encroach sorne distance into the Indian
Subregion. H. (Hyalommasta) aegyptium is known here only from Quetta, near
~
co
~
FIGS. 39 to 47· Photomicrographs of mounteù and cleared female genital areas. Each photograph at same
scale.- FIG. 39, H. aeg;•ptium (Bitlis, Turkey, HH 22I6).- FIG. 40, H. kumari (Bihar, India, HH 2745).FIG. 41, H. brevipunctata (Gujerat, India, HH 2727).- FIG. 42, H hussaini (Gujerat, India, HH 2750).FIG. 43, H. a. anatolicum (Andrha Pradesh, India, HH 1424). - FIG. 44, H. drornedarii (Gujerat, India,
HH I6). - FIG. 45, H. detriturn (Muree, Pakistan, HH 1362).- FIG. 46, H. marginatum isaaci (Gujerat,
India, HH 2786).- FIG. 47, H. rnarginatum turanicum (Charikar, Afghanistan, HH 227I).
The measurement of each division of the scale in the lower right corner, at the size originally photographeù is .oor mm.
the Pakistani-Afghanistan frontier. All remaining speCles are m the subgenus
Hyalomma. H. a. anatolicum Koch is the most common hyalomma in Pakistan
and northern India and H. dromedarii Koch is common in this area wherever camels
occur. A few records of H. marginatum turanicum Pomerantzev are from southern
C
H
1
B
B
E
N
N
A
G
A
y
A
TONY
Frc. 48. l\Iap of the Indian Faunal Subregion to show countries, states, and most districts
and collecting localities mentioned in the text.
Pakistan and Gujerat State, India, and a few specimens of H. detritum Schulze
are known from northern Pakistan and Delhi, India.
The overall size, and sometimes the body outline, of most specimens of the
non-endemie species in the Indian Subregion is generally smaller or narrower than
in samples from western Asia and Africa (KAISER and HooGSTRAAL, 1963). This
is especially true of H. a. anatolicum, H. dromedarii, and H. aegyptium. The systematic importance, if any, of this phenomenon rema.ins to be determined.
The biology and ecology, as well as the medical and veterinary importance
of ail Hyalomma ticks in the Indian Subregion, is insufficiently known.
ACKNOWLEDGEMENTS
Materials from India and Pakistan in collections of the British Museum (Natural
History) and Rocky Mountain Laboratory, sent to us for identification by
Dr. G. OwEN-EVANS and Mr. Glen M. KoHLS respectively, have been particularly
useful for this study. A valuable collection, chiefly from Gujerat State, India,
was forwarded by Drs. Harold TRAPIDO and M. G. R. V ARMA of the Virus Research
Centre, Poona. Dr. TRAPIDO and Dr. T. RAMACHANDRA RAo, Director of the VRC,
also kindly assisted in correlation of certain Indian localities and the States in which
they are presently situated. Specimens from Delhi State were sent for identification by Dr. S. K. NAGAR of Delhi University. Dr. Henry FIELD, of Coconut
Grove, Florida, Dr. Ahmed MoHIUDDIN of Sind University, Jamshoro, and
Dr. Vincent McCARTHY of the Pakistan Medical Research Centre, Lahore, contributed specimens from Pakistan and Dr. McCARTHY assisted with the spelling
and location of collecting localities in this country. Dr. P. SENEVIRATNA of the
University of Ceylon generously provided specimens from Ceylon. Dr. McCARTHY,
and Mr. M. J. REBELLO of the Virus Research Centre, Poona, critically read the
manuscript and checked out the keys. To each of these colleagues, we are most
grateful.
ADDENDUM
After this paper went to press, Dr. Vincent McCARTHY furnished several
collections that contribute to knowledge of the Hyalomma fauna of Pakistan.
Sorne highlights in this material are the following. H. schulzei was taken from
camels at Dalbandin, 170 miles southwest of Quetta and 40 miles south of the
Afghanistan border on 2 April rg63. Characters to differentiate this species from
H. dromedarii can be found in HooGSTRAAL (rg56). Another group of camels
at Chaman, 6o miles north-northwest of Quetta, yielded H. a. asiaticum, H. a. anatolicum, H. dromedarii, and H. marginatum turanicum. Key characters for distinguishing H. a. asiaticum are provided in a footnote to the key in the present
paper, and a diagnosis and illustrations of this species are included in our recent
report on Hyalomma ticks of Afghanistan (KAISER and HoocsTRAAL, rg63). A third
lot, from sheep at Bhootan (r4 miles south east of Yazmaa) on 23 J anuary rg63,
consists of a male and female, both very tiny specimens, that can be referred
only to H. impeltatum, a species also listed in the rg63 report on Afghanistan
hyalommas. We are additionally grateful to Dr. McCARTHY for these samples,
-
z8s
which show that H. a. asiaticum and H. schulzei range into the mountains of
Pakistan near Afghanistan, and that H. impeltatum may possibly also occur m
this country.
In January, 1964, Dr. R. B. GRIFFITHS, FAO Regional Veterinarian for the
Far East, generously sent us a collection of ticks taken from cattle from Thazi, in
the dry zone of B UR:\IA, in N ovember, 1961. A number of H yalomma hussaini were
represented in these collections, together with Boophilus microplus and Rhipicephalus haemaphysaloides. Annual rainfall in this area is 31.60 inches. The ticks
were taken at the end of the wet season, when 3 or were found on each animal.
Ticks are said to be absent on animais here during the dry season.
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ANASTOS (G.), I957·- The ticks, or ixodides, of the U.S.S.R. A review of the literature.
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DELPY (L. P.), I949· -Essai critique de synonymie du genre Hyalomma C. L. Koch r844
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FELDMAN-MUHSAM (B.), I957· - Revision of the genus Hyalomma. II. The subgenus Hyalommina. Parasitology, 47 (r-z) : 46-59.
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PERVOMAISKY (G. S.), 1954. - Variability of pasture ticks (Acarina, Ixodidae), and
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-286PoMERANTZEV (B.), 1950.- Arachnida. Ixodid ticks (Ixodidae). In: Fauna of U.S.S.R.,
4 (2) : 223 pp. (In Russian, AIBS translation).
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