Ticks (Acari: Ixodoidea: Argasidae, Ixodidae) of China

Ze Chen • Xiaojun Yang • Fengju Bu • Xiaohong Yang •

Xiaolong Yang • Jingze Liu

Received: 2 September 2009 / Accepted: 9 January 2010 / Published online: 27 January 2010� Springer Science+Business Media B.V. 2010

Abstract This paper presents results of an investigation and listing of tick species found

in China during a survey in all 28 provinces. This will be a step towards a definitive list of

tick species and their distribution. To date, the tick fauna of this area consists of 117

species in the following families: Argasidae-Argas (7 species), Carios (4 species) and

Ornithodoros (2 species); Ixodidae-Amblyomma (8 species), Anomalohimalaya (2 species),

Dermacentor (12 species), Haemaphysalis (44 species), Hyalomma (6 species), Ixodes (24

species) and Rhipicephalus (8 species). Some well known ticks carrying and transmitting

many infectious agents to man and domestic animals are also found in China. These

include Ixodes persulcatus, Haemaphysalis longicornis, Rhipicephalus sanguineus,

R. (Boophilus) microplus and Hyalomma asiaticum. It is worth mentioning that Ixodesrangtangensis Teng and Haemaphysalis xinjiangensis Teng should be relegated to a

synonym of I. moschiferi and Hae. danieli, respectively. The distribution of ticks over the

provinces of China is also discussed. The information on ticks in some areas such as Henan

is not exhaustive.

Keywords China � Geographical distribution � Haemaphysalis xinjiangensis �Ixodes rangtangensis � Ixodoidea

Introduction

Ticks are obligatory blood-feeding arthropods, which are currently considered to be second

only to mosquitoes as vectors of disease-causing agents to humans, and the most important

arthropods capable of carrying and transmitting pathogens to animals (Coddingtonja and

Colwell 2001). They transmit a great variety of pathogens, including bacteria, viruses,

blood protozoans, spirochetes, rickettsiales etc., which can cause many diseases like Lyme

disease, babesiosis, human granulocytic ehrlichiosis (HGE), forest encephalitis, spotted

Z. Chen � X. Yang � F. Bu � X. Yang � X. Yang � J. Liu (&)College of Life Sciences, Hebei Normal University, 050016 Shijiazhuang, Chinae-mail: jzliu21@heinfo.net

123

Exp Appl Acarol (2010) 51:393–404DOI 10.1007/s10493-010-9335-2

fever, Q fever and anaplasmosis by the bite of infected ticks (Gong and Zhou 2005). Ticks

can also cause direct parasitic damage due to paralyses and toxicoses, irritation, and

allergy. Ticks and tick-borne diseases cause significant losses to the livestock industry by

decreasing milk production, effecting weight loss, and increasing risk for bacterial, viral,

and fungal infections (Ahmed et al. 2007). Recent outbreaks of tick-transmitted human

granulocytic anaplasmosis (HGA) in many areas especially in China have generated widely

interest in ticks as vectors of human disease (Dumler et al. 2005; Zhang et al. 2008). The

bacterium of this disease is maintained in a transmission cycle with Ixodes persulcatuscomplex ticks (Dumler et al. 2005), and I. persulcatus is a common species in China.

Considering its significant medical and veterinary importance, the knowledge of species

present in a given area is important to physicians, veterinarians, wildlife biologists, and

farmers of livestock.

Shen Xu was acknowledged as the first person who described the tick in the book ‘‘Shuo

Wen Jie Zi’’ in the year 121 AD of the later Han dynasty in China. Afterwards, many

people became interested in this animal group. However, in the 19th and early 20th

centuries, China was beset by civil unrest, major famines, military defeats and foreign

occupation, which seriously hampered the development of the natural sciences. After

liberation in the year 1949, researches on acarology developed rapidly, and many

researchers were hence famous for their achievements in ticks, such as Guofan Teng, Xin

Yu, Kejun Huang, Lanzhou Feng, Baolin Lu, Weijun Wu, Zaijie Jiang (Teng and Jiang

1991). The late Guofan Teng was the expert on tick taxonomy. However, it is a pity that

few studies about ticks were conducted after him. Only some people who are interested in

parasites have paid a little attention to this filed. His last major species names and bio-

geograhical review of the hard and soft ticks of China is now almost 30 years old (Teng

1978). In addition, this book and some other monographs of incomplete distribution or

families of Chinese ticks (Teng and Jiang 1991; Yu et al. 1997), have numerous dis-

crepancies against each other when critically compared. Based on the concerns above, it is

imperative to renew the old lists of Chinese tick fauna and its biogeographical distribution.

Geographically, China is located in the southeastern part of vast Eurasia continent, in

the eastern part of Asia, on the west coast of the Pacific Ocean (between latitudes 4�N–

53�N and longitudes 73�E–135�E). It covers a land area of about 9.6 million square

kilometers, and is bordered by twelve countries: Korea, Russian, Mongolia, India, Paki-

stan, Bhutan, Nepal, Burma, Laos and Vietnam. The complexity and variety of geomor-

phological types existing in China are unique in the world (Wan and Liu 1994), so the tick

of China is also diversity (about 13% species of the world). However, so far many foreign

researchers have not understood the detail information about ticks in China. Fortunately,

we have the opportunity to collect many specimens and informations about this group, so

herein we attempt a revision of Chinese tick species. Finally, information on the distri-

bution of ticks is also included. Figure 1 shows the administrative divisions (province) and

biogeographical divisions of China.

Materials and methods

From September 2004 to November 2008, ticks were collected from vegetation and ani-

mals (mainly domestic animals and some field rodents) in different regions of China. The

collected tick specimens were transported alive or preserved in 75% alcohol to our labo-

ratory for taxonomic identification. When possible, live immature specimens were reared

to the adult stage in the laboratory for identification (Chen et al. 2009). Tick specimens

394 Exp Appl Acarol (2010) 51:393–404

123

were identified morphologically and sometimes molecularly by comparing their 16S

ribosomal DNA and ITS2 (internal transcribed spacer 2) gene sequences to homologous

sequences deposited in GenBank. The collected ticks were deposited in the tick collection

of College of Life Sciences, Hebei Normal University. Additional data were obtained from

the tick cllection of the Academy of Military Medical Sciences, some researchers’ personal

tick cllections, and from previous published data of ticks in China (Teng 1978; Yao 1984;

Li 1987; Kang et al. 1991; Teng and Jiang 1991; Zhu and Zheng, 1994; Bai et al. 1995;

Liao and Lai 1995; Liao and Yu 1995; Xu et al. 1995; Liu et al. 1996; Sun et al. 1996;

Huang et al. 1997; Shen and Shen 1997; Yu et al. 1997; Li et al. 1998, 2002; Sun et al.

1998; Ma et al. 1999; Gong et al. 2001; Liu and Yang 2001; Lu 2004; Shi et al. 2004; Chen

et al. 2006; Yang et al. 2008a, b). Moreover, much valuable information is also doubtless

stored away in the minds and collections of the many entomologists (such as Xin Yu; Wei

Li; Jiagang Sun; Yi Sun; Jinlin Zhou; Yujiang Zhang et al.) who have worked on the tick

occurrence for a long time, but have lacked the time or the interest to publish their findings.

Thus we consulted them, and got much important information.

The phylogenies followed for the present article were those of Barker and Murrell

(2004) for the family Ixodidae and Argasidae.

Fig. 1 The administrative and biogeographical divisions of China

Exp Appl Acarol (2010) 51:393–404 395

123

Results

The primary functions of this work are to show the currently valid tick species and their

distributions in China. A total of 117 tick species have been confirmed as occurring

definitely in China (13% of world tick species). The checklist of these species and their

occurrence in different province of China is presented in Table 1.

The argasid tick fauna of China consists of 13 species from 3 genera, Argas (7 species),

Carios (4 species) and Ornithodoros (2 species), and the ixodid tick fauna comprises 104

species from 7 genera, Amblyomma (8 species), Anomalohimalaya (2 species), Derma-centor (12 species), Haemaphysalis (44 species), Hyalomma (6 species), Ixodes (24 spe-

cies) and Rhipicephalus (8 species).

Discussion

The present study reports 117 tick species for China, representing 13% of tick species that

occur in the world. All of the species names have been checked for accuracy in the ‘‘world

list of valid tick names’’ fields (Horak et al. 2002; Barker and Murrell 2004, 2008; Kolonin

2009). However, there exist several taxonomic problems. The tick species Ixodes rang-tangensis Teng (1973) described by Teng (1973) was based on one female collected on a

forest musk deer Moschus berezovskii from Sichuan of China and compared with its most

similar species I. acutitarsus. However, after he examined the type again several years

later, Teng proposed that I. rangtangensis should be classified as a junior subjective

synonym of I. moschiferi (Teng 1986; Teng and Jiang 1991). Haemaphysalis xinjiangensisTeng, 1980 was also described by Teng (1980), some of which were collected in alpine

pasture and some collected off wild goats from the southern part of Xinjiang. In 1991,

he suggested this species should be relegated to a synonym of Hae. danieli. Since

I. moschiferi and Hae. danieli has page priority over I. rangtangensis and Hae. xinji-angensis, respectively, the latters should be deleted from the list of valid tick species (Teng

1986; Teng and Jiang 1991). I. rangtangensis as a synonym of I. moschiferi was commonly

recognized by Robbins and Robbins (2003), Guglielmone et al. (2009), and Kolonin

(2009), and Hae. xinjiangensis was considered invalid and suggested to be a synonym of

Hae. pospelovashtromae by Kolonin (2009). Since Kolonin did not compared the speci-

mens of these species, only compared the description and figures which were incompletion

in Teng (1980). Thus we selected the suggestion of Teng and Jiang (1991) that Hae.xinjiangensis is a synonym of Hae. danieli. However, Horak et al. (2002), Barker and

Murrell (2004) and also Barker and Murrell (2008) included both I. rangtangensis and

Hae. xinjiangensis as valid tick species names.

From the Table 1 we can see that the distribution of ticks in China appeared as spot or

belt. Ticks are abundant in Yunnan, Gansu, Xinjiang, Taiwan, Tibet and Fujian (about 30–

40 species), but are much less common in Henan and Jiangxi (4 and 6 species, respec-

tively). While many factors influence distribution of ticks (topography, climate, vegetation,

host distribution and density, and land use patterns by humans), there appears to be

incomplete investigation in some areas. Such as Henan which located at the juncture of the

Palaearctic and Oriental realm, with abundant propagation resources, but only a small

number of tick species reported (4 species). Thus a further investigation is needed in

these areas.

Spot distribution. Some species only occurr in a single province, such as Argas assimilis(Guangxi), A. beijingensis (Hebei), Carios sinensis (Sichuan), Ixodes spinicoxalis (Fujian),

396 Exp Appl Acarol (2010) 51:393–404

123

Tab

le1

Tic

kfa

una

acco

rdin

gto

pro

vin

ces

inC

hin

a

No

.S

pec

ies

Pro

vin

ce

Heb

Sd

Hen

Ah

JsZ

jJx

Fj

Tw

Gd

Gx

Han

Hn

Hb

Sx

Sax

Nx

Gz

Yn

Sc

Qh

Tb

Xj

Gs

ImH

lJl

Ln

Arg

as(7

)

1A

.a

ssim

ilis

?

2A

.b

eiji

ng

ensi

s?

?

3A

.ja

pon

icu

s?

??

4A

.la

hore

nsi

s?

?

5A

.p

ersi

cus

??

??

??

??

??

??

??

??

?

6A

.ro

ber

tsi

?

7A

.vu

lga

ris

??

??

??

?

Car

ios

(4)

8C

.ca

pen

sis

?

9C

.p

usi

llu

s?

10

C.

sin

ensi

s?

11

C.

vesp

erti

lioni

s?

??

??

??

??

?

Orn

ith

od

oro

s(2

)

12

O.

tart

ako

vsky

i?

?

13

O.

tho

loza

ni

??

Ixod

es(2

4)

14

I.a

cum

ina

tus

?

15

I.a

cuti

tars

us?

??

??

16

I.a

rbo

rico

la?

??

?

17

I.b

erle

sei

?

18

I.cr

enula

tus

??

??

??

??

??

19

I.g

ran

ula

tus

??

??

??

??

??

?

20

I.h

yatt

i?

??

?

Exp Appl Acarol (2010) 51:393–404 397

123

Tab

le1

con

tin

ued

No

.S

pec

ies

Pro

vin

ce

Heb

Sd

Hen

Ah

JsZ

jJx

Fj

Tw

Gd

Gx

Han

Hn

Hb

Sx

Sax

Nx

Gz

Yn

Sc

Qh

Tb

Xj

Gs

ImH

lJl

Ln

21

I.ka

sch

mir

icu

s?

22

I.ka

zaks

tani

?

23

I.ku

ntz

i?

?

24

I.m

osc

har

ius

?

25

I.m

osc

hif

eria

??

?

26

I.m

yosp

ala

cis

??

??

27

I.n

ipp

one

nsi

s?

28

I.n

utt

all

ian

us

??

??

29

I.o

vatu

s?

??

??

??

??

??

??

30

I.p

ersu

lca

tus

??

??

??

??

??

??

?

31

I.p

om

eran

zevi

??

??

??

32

I.se

men

ovi

?

33

I.si

mp

lex

??

?

34

I.si

nen

sis

??

??

??

?

35

I.sp

inic

oxa

lis

?

36

I.ta

nu

ki?

?

37

I.ve

sper

tili

onis

??

??

??

??

??

Am

bly

om

ma

(8)

38

Am

.co

rdif

erum

?

39

Am

.cr

ass

ipes

??

40

Am

.g

eoem

yda

e?

?

41

Am

.h

elvo

lum

??

42

Am

.ja

van

ense

??

??

?

43

Am

.p

att

on

i?

?

398 Exp Appl Acarol (2010) 51:393–404

123

Ta

ble

1co

nti

nu

ed

No

.S

pec

ies

Pro

vin

ce

Heb

Sd

Hen

Ah

JsZ

jJx

Fj

Tw

Gd

Gx

Han

Hn

Hb

Sx

Sax

Nx

Gz

Yn

Sc

Qh

Tb

Xj

Gs

ImH

lJl

Ln

44

Am

.te

stu

din

ari

um

??

??

??

??

45

Am

.va

rane

nse

??

Ha

ema

ph

ysa

lis

(44

)

46

Ha

e.a

bo

ren

sis

?

47

Ha

e.a

no

mal

oce

raea

?

48

Ha

e.a

po

no

mm

oid

es?

??

49

Ha

e.a

sia

tica

??

?

50

Ha

e.b

an

dic

ota

?

51

Ha

e.b

irm

an

iae

??

?

52

Ha

e.b

isp

ino

sa?

??

??

53

Ha

e.ca

mp

anu

lata

??

??

??

??

??

54

Ha

e.ca

nes

trin

ii?

??

55

Ha

e.co

nci

nn

a?

??

??

??

??

??

?

56

Ha

e.co

rnig

era

??

??

??

57

Ha

e.d

an

ieli

*?

??

58

Ha

e.d

oen

itzi

??

??

59

Ha

e.er

ina

cei

??

??

60

Ha

e.fl

ava

??

??

??

?

61

Ha

e.fo

rmo

sen

sis

??

??

62

Ha

e.g

arh

wal

ensi

s?

63

Ha

e.g

ora

l?

64

Ha

e.h

ystr

icis

??

??

??

?

65

Ha

e.ja

po

nic

a?

??

??

??

??

??

66

Ha

e.ki

tao

kai

??

??

?

Exp Appl Acarol (2010) 51:393–404 399

123

Ta

ble

1co

nti

nu

ed

No

.S

pec

ies

Pro

vin

ce

Heb

Sd

Hen

Ah

JsZ

jJx

Fj

Tw

Gd

Gx

Han

Hn

Hb

Sx

Sax

Nx

Gz

Yn

Sc

Qh

Tb

Xj

Gs

ImH

lJl

Ln

67

Ha

e.la

gra

ng

ei?

68

Ha

e.lo

ngic

orn

is?

??

??

??

??

??

??

??

??

??

69

Ha

e.m

ag

eshi

ma

ensi

s?

??

70

Ha

e.m

ega

spin

osa

??

71

Ha

e.m

eng

laen

sis

?

72

Ha

e.m

on

tgo

mer

yi?

??

?

73

Ha

e.m

osc

his

ug

a?

??

??

74

Ha

e.n

epa

len

sis

??

75

Ha

e.o

rnit

ho

ph

ila

??

??

76

Ha

e.p

ha

sia

na

??

??

77

Ha

e.p

rim

itiv

a?

?

78

Ha

e.p

un

cta

ta?

??

?

79

Ha

e.q

ing

ha

ien

sis

??

??

??

80

Ha

e.si

nen

sis

??

81

Ha

e.sp

inig

era

??

??

82

Ha

e.su

lca

ta?

83

Ha

e.ta

iwa

na

??

??

?

84

Ha

e.ti

bet

ensi

s?

??

85

Ha

e.ve

rtic

ali

s?

??

??

??

??

?

86

Hae.

viet

nam

ensi

s?

??

?

87

Ha

e.w

arb

urt

oni

??

?

88

Ha

e.w

elli

ng

ton

i?

?

89

Ha

e.ye

ni

??

??

??

400 Exp Appl Acarol (2010) 51:393–404

123

Ta

ble

1co

nti

nu

ed

No

.S

pec

ies

Pro

vin

ce

Heb

Sd

Hen

Ah

JsZ

jJx

Fj

Tw

Gd

Gx

Han

Hn

Hb

Sx

Sax

Nx

Gz

Yn

Sc

Qh

Tb

Xj

Gs

ImH

lJl

Ln

Hya

lom

ma

(6)

90

Hy.

an

ato

licu

m?

?

91

Hy.

asi

ati

cum

??

??

??

?

92

Hy.

dro

med

ari

i?

??

93

Hy.

isa

aci

??

??

94

Hy.

scupen

se?

??

??

??

??

??

??

??

95

Hy.

rufi

pes

??

??

??

?

An

om

alo

him

ala

ya(2

)

96

An

.la

mai

?

97

An

.lo

tozk

yi?

Der

ma

cen

tor

(12

)

98

D.

ab

aen

sis

??

?

99

D.

au

ratu

s?

??

??

??

10

0D

.ev

eres

tianus

??

10

1D

.m

arg

ina

tus

??

?

10

2D

.m

on

tan

us?

10

3D

.n

iveu

s?

??

??

?

10

4D

.n

utt

all

i?

??

??

??

??

??

10

5D

.p

avl

ovs

kyi

?

10

6D

.re

ticu

latu

s?

??

10

7D

.si

lva

rum

??

??

??

??

??

?

10

8D

.si

nicu

s?

??

??

??

??

10

9D

.ta

iwa

nen

sis

??

Exp Appl Acarol (2010) 51:393–404 401

123

Ta

ble

1co

nti

nu

ed

No

.S

pec

ies

Pro

vin

ce

Heb

Sd

Hen

Ah

JsZ

jJx

Fj

Tw

Gd

Gx

Han

Hn

Hb

Sx

Sax

Nx

Gz

Yn

Sc

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ImH

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Rh

ipic

eph

alu

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)

11

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.(B

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a?

?

11

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aem

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ysa

loid

es?

??

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??

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??

11

3R

.p

um

ilio

??

?

11

4R

.ro

ssic

us

?

11

5R

.sa

ng

uin

eus

??

??

??

??

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??

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??

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??

11

6R

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hu

lzei

?

11

7R

.tu

ran

icu

s?

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m1

99

41

31

28

63

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91

41

51

71

02

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92

51

81

23

82

42

52

83

93

31

91

21

31

6

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An

hu

i,F

jF

uji

an,

Gd

Gu

ang

do

ng

,G

sG

ansu

,G

xG

uan

gxi,

Gz

Gu

izho

u,

Heb

Heb

ei,

Hb

Hu

bei

,H

lH

eilo

ng

jian

g,

Ha

nH

ain

an,

Hen

Hen

an,

Hn

Hu

nan

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Inn

erM

ong

oli

a,Jl

Jili

n,

JsJi

ang

su,

JxJi

angx

i,L

nL

iao

nin

g,

Nx

Nin

gx

ia,

Qh

Qin

gh

ai,

Sa

xS

haa

nx

i,S

cS

ich

uan

,S

dS

han

do

ng

,S

xS

han

xi,

Tb

Tib

et,

Tw

Tai

wan

,X

jX

inji

ang

,Y

nY

un

nan

,Z

jZ

hej

ian

ga

I.ra

ngt

an

gen

sis

Ten

g(1

97

3)

and

Ha

e.xi

nji

ang

ensi

sT

eng

(19

80)

wh

ich

wer

est

ill

list

edto

be

val

idsp

ecie

sn

ames

(Ho

rak

etal

.2

00

2;

Bar

ker

and

Murr

ell

20

04,

20

08)

had

bee

nal

read

yre

legat

edto

asy

nonym

of

I.m

osc

hif

eri

and

Ha

e.d

an

ieli

,re

spec

tivel

y(T

eng

19

86;

Ten

gan

dJi

ang

19

91;

Rob

bin

san

dR

ob

bin

s2

00

3;

Gu

gli

elm

on

eet

al.

20

09;

Ko

lon

in2

00

9)

402 Exp Appl Acarol (2010) 51:393–404

123

Haemaphysalis megaspinosa (Gansu), Haemaphysalis garhwalensis (Ningxia), Haema-physalis goral (Zhejiang). Argas robertsi, C. capensis, C. pusillus, Amblyomma cordife-rum, Ixodes semenovi and Haemaphysalis bandicota are only found in Taiwan,

Ornithodoros tartakovskyi, Ixodes acuminatus, Ixodes berlesei, Ixodes kazakstani,An. lotozkyi, D. pavlovskyi, D. montanus, Rhipicephalus rossicus and Rhipicephalusschulzei only occurr in Xinjiang. Ixodes kaschmiricus, Ixodes moscharius, Haemaphysalistibetensis and An. lamai are only found in Tibet. Haemaphysalis menglaensis and

Haemaphysalis anomaloceraea are only found in Yunan. Some also can be found in

adjacent regions, such as A. japonicus (Jilin, Liaoning, Hebei), A. vulgaris (Ningxia,

Gansu, Xinjiang, Heilongjiang) etc. These endemic species are rich and account for

69.75% of ticks in China.

Belt distribution. Based on the results it is concluded that Haemaphysalis longicornis,

R. (Boophilus) microplus, R. haemaphysaloides and R. sanguineus are dominant tick

species in China and should be noted for their ability in transmission of infectious agents.

Argas persicus is distributed in belt from northeast to northwest, dispersing itself to

adjacent regions from north to south. These ticks called universal species were about

30.25%.

Acknowledgments This project was supported by National Natural Science Foundation of China(30670259) and Natural Science Foundation of Hebei province of China (C2007000266). We thank Xin Yu,Jiagang Sun, Jinlin Zhou, Yujiang Zhang et al. for specimens and Yi Sun kindly provided data on collectionsdeposited in the museum of the Academy of Military Medical Sciences. We also thank Dr Haining Yu andNeville Sevicke Jones for the manuscript revision.

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