HOST SEX AND ECTOPARASITE INFECTIONS OF PLATEAU PIKA ...

POLISH JOURNAL OF ECOLOGY
(Pol. J. Ecol.)
56 3 535–539 2008
Short research contribution
Haixin CI 1, 2 , Gonghua LIN 1, 2 , Jianping SU 1 , Yifan CAO 1
1
Key laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology,
Chinese Academy of Sciences, Xining 810001, China, e-mail: jpsu@nwipb.ac.cn (corresponding author)
2
Graduate School of Chinese Academy of Sciences, Beijing 100049, China,
e-mails*: haixinci@gmail.com, lingonghua05@mails.gucas.ac.cn
HOST SEX AND ECTOPARASITE INFECTIONS
OF PLATEAU PIKA (OCHOTONA CURZONIAE, HODGSON)
ON THE QINGHAI-TIBETAN PLATEAU
ABSTRACT: A total of 449 plateau pika
(Ochotona curzoniae Hudgson) individuals were
sampled with rattraps from 21 plots (size 1 ha)
randomly scattered over the area of the species
distribution at the altitude 3275–4807 m a.s.l. in
the Qinghai-Tibetan Plateau (West China). Two
main ectoparasite species Hypoderma satyrus
Brauer and Ixodes crenulatus Neumann of plateau
pika were surveyed, and the relations between
host sex and parasitism were analyzed. The results
were: (i) although not significantly, the infection
rate of female young was close to zero and lower
than that of male young (6%), while the infection
rate of female sub-adults (19%) was contrarily
– higher than that of male sub-adults (11%);
adult females had significantly higher (41%) infection
rate than that of males (18%) (P

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Haixin Ci et al.
Fig. 1. Sampling locations on Qinghai-Tibetan Plateau (West China )
as parasite taxon and age of hosts might also
affect the sex-specific host-parasite relations
(Amundsen et al. 1997, S chalk and
Forbes 1997, Moore and Wilson 2002).
The various factors and their interrelations
make situations complex (Krasnov et al.
2005), and more data are needed to elucidate
the problems about SBP.
Plateau pika (Ochotona curzoniae
Hudson)is a keystone species on the Qinghai-Tibetan
Plateau, and plays an important
role for biodiversity in the ecosystem (Smith
and Foggin 1999). Several studies have paid
attention to the parasite infections of plateau
pika (Zhang 1991, Cao and Ye 1998, Ding
et al. 1999, Wang et al. 2003). To our knowledge,
however, no studies focused on sex-specific
differences in the parasitism. Since there
are ecological differences e.g. in growth rate
(Zhou et al. 1987) and spacial territory between
male and female plateau pika (Qu et
al. 2007), we suggest there is also SBP in this
species. During July of 2006, when a sampling
aimed to analyze phylogeographic structure
of plateau pika on the Qinghai-Tibetan Plateau
was executed, at the same time we surveyed
the parasite infections in this species
and then investigated the relations between
parasite infections and host sex. The relationship
between sex-specific parasitism and age
of animal was also investigated.
Sampling was conducted in July 2006, at
the annual peak of abundance of plateau pika
(Liang and Qi 1989), in order to increase
trapping efficiency. Pika trappings were carried
out on 21 plots of 1 ha size that were randomly
selected on the plateau, on the area of
the species distribution at altitude 3275–4807
m a.s.l. (Fig. 1). Each plot was sampled in
the day time with ~30 rattraps placed at the
entrances of their burrows. Animals were
decollated by hand immediately after trapping,
and parasite infections and other biological
characters including gender, body
weight, body length, reproduction condition
were measured before tissue for DNA extrac-
journal 15.indb 536 2008-09-23 10:56:07

Host sex and ectoparasite infections of plateau pika
537
Table 1. Total sample size (N), average body mass (M±SD) and infection rate (R) of males and females
in each age-group.
Males
Females
young sub-adults adults young sub-adults adults
N 82 71 114 27 53 102
M (g)
57.12
±13.32
104.06
±10.65
151.07
±22.63
53.30
±16.91
105.17
±10.59
162.19
±30.58
R (%) 6 11 18 0 19 41
tion was collected. The longitude, latitude
and altitude at the centre of each sampling
plot were measured using an Etrex GPS unit
(Garmin, Taiwan).
Although there are many kinds of ectoparasites
and endoparasites in plateau pika
(Ding et al. 1999, Wang et al. 2003), only
two ectoparasite species that could be easily
identified were surveyed in this work since
(i) the parasitism survey was a byproduct
of a sampling aimed to analyze phylogeographic
structure of plateau pika and (ii)
the work conditions in the field on the plateau
was pretty difficult. The ectoparasite
species included in the study – Hypoderma
satyrus Brauer (1858) and Ixodes crenulatus
Neumann (1904) are two most common
parasite species of plateau pika. The maggot
of Hypoderma satyrus usually adheres
to endermic of the back and outboard limbs
(Ding et al. 1999), and could be found by
carefully searching the pika skin. Ixodes
crenulatus individuals usually attach at auricle,
eyelid, cheek, nose lid, inboard foreleg
(Ding et al. 1999) of pikas, and could be
easily identified in these positions. Due to
the relatively low infection rates of either
Hypoderma satyrus or Ixodes crenulatus
alone, the infection data of these two parasites
were combined i.e. pika individuals infected
by either of the two parasite species
were recorded as ‘infected’.
Individuals were grouped according to
their weight and gender in each plot. Three
age-groups were determined based on present
studies both in the field and under the
condition of artificial feeding (Zhou et al.
1987, Ye and Liang 1989): (i) young – no
more than 80g ,(ii) sub-adult – between 80g
and 120g, (iii) adult – more than 120g. Infection
rates of males as well as females were
calculated for each age-group based on all
samplings. Sex-specific parasite infection
rate and related factors were analyzed. The
Independent-Sample T Test was used to test
the differences of body mass between males
and females of each age group. For the comparison
of infection rates among groups with
different gender and age, the small sample
data in each plot were combined and a Crosstabs
analysis was used. All statistical analyses
were executed using SPSS 13.0 for Windows
(SPSS Inc., Chicago, IL, USA).
A total of 449 individuals were sampled
from 21 plots randomly scattered on the Qinghai-Tibetan
Plateau (including Qinghai, Tibet
and Sichuan Province) (Fig. 1). The sampling
covered almost the entire geographical
distribution of the species. The average body
mass and the infection rate of each group are
listed in Table 1. Crosstabs analysis did not
show significant differences between the infection
rates of young and sub-adult males
and females however the respective data were
lower for female young than for male young
(df = 1, P = 0.189), and higher – for female
sub-adults than that for male sub-adults (df =
1, P = 0.235) (Table 1). In adult group, infection
rate of females was significantly higher
than that of males (Crosstabs analysis, df = 1,
P

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Haixin Ci et al.
Recent related reviews generally emphasized
male biases in parasitism (Poulin
1996, S chalk and Forbes 1997, Wedekind
and Jakobsen 1998, Acuna-S oto
et al. 2000). However, our analysis on adult
age-group showed female biases in ectoparasite
infections. There are two major classes of
hypotheses for the proximate control of SBP.
One claims that males are envisaged to suffer
a sex-specific handicap because of a mechanism
called immunodepressive effect (Klein
2000), while another class of hypotheses suggests
that it is body size per se that is important
in generating SBP either because the larger
sex is exposed more to infection, or because
of the balance of energy investment between
somatic growth and immune function, that
is, the enhanced growth of larger sex reduced
the energy investment on their immune system
and consequently makes them more
susceptible to parasites (Moore and Wilson
2002). We suggest that, in our study, the
biological differences e.g. in body mass and
growth rate had caused the SBP of plateau
pika at different age stages, which is consisted
with Moore and Wilson (2002) findings.
Although not significantly, the weights
of female young were a little lower than male
young (Independent-Sample T Test, df = 107,
P = 0.290) while female sub-adults were a
little heavier than male sub-adults, however
without significance (Independent-Sample
T Test, df = 122, P = 0.565). Moreover, the
growth rate of female pika is lower at young
stage but higher at juvenile (sub-adult) stage
than that of the males (Zhou et al. 1987).
As to the adults, female adults (including 31
pregnant individuals) were also significantly
heavier than male adults (df = 214, P

Host sex and ectoparasite infections of plateau pika
539
Amundsen P.A., Kristoffersen R., Knudsen
R ., Klemetsen A. 1997 – Infection
of Salmincola edwardsii (Copepoda: Lernaeopodidae)
in an age-structured population of
Arctic charr – a long-term study – J. Fish Biol.
51: 1033–1046.
Brei B., Fish D. 2003 – Comment on “Parasites
as a viability cost of sexual selection in
natural populations of mammals” – Science,
300: 55a.
Cao Y.F., Ye R .R . 1998 – Survey of helminthes
parasitism of plateau pika – Chin. J. Vet. Sci.
Tech. 28 (5): 14–15 (in Chinese with English
abstract).
Ding X.T., He X.Q., Cao Y.Q., Dai L.
1999 – Reports on parasite infections on plateau
pika – Sichuan J. Zool. 18 (1): 34–43 (in
Chinese).
Klein S.L. 2000 – The effects of hormones on
sex differences in infection: from genes to
behavior – Neurosci. Biobehav. Rev. 24: 627–
638.
Krasnov B.R., Morand S., Hawlena H.,
Khokhlova I.S., Shenbrot G.I. 2005 –
Sex-biased parasitism, seasonality and sexual
size dimorphism in desert rodents – Oecologia,
146: 209–217.
Liang J.R., Qi G.X. 1989 – The population
age structure and dynamics of the plateau
pika (Ochotona curzoniae) – Acta Theriol.
Sin. 9 (3): 228–230 (in Chinese).
McCurdy D.G., Shutler D., Mullie A.,
Forbes M.R . 1998–Sex-biased parasitism
of avian hosts: relations to blood parasite taxon
and mating system–Oikos, 82: 303–312.
Moore S.L., Wilson K. 2002–Parasites as
a viability cost of sexual selection in natural
populations of mammals–Science, 297: 2015–
2018.
Poulin R. 1996–Sexual inequalities in helminth
infections: A Cost of Being a Male?–Amer.
Naturalist. 147 (2): 287–295.
Poulin R., Curtis M.A., Rau M.E. 1991–
Size, behaviour, and acquisition of ectoparasitic
copepods by brook trout, Salvelinus fontinalis
– Oikos, 61: 169–174.
Qu J.P., Li K.X., Yang M., Li W.J., Zhang
Y.M., Smith A.T. 2007–Seasonal dynamic
pattern of spacial territory in social groups
of plateau pikas (Ochotona curzoniae) – Acta
Theriol. Sin. 27(3): 215–220 (in Chinese with
English abstract).
Reimchen T.E., Nosil P. 2001 – Ecological
causes of sex-biased parasitism in threespine
stickleback – Biol. J. Linn. Soc. 73: 51–63.
Schalk G., Forbes M.R. 1997 – Male biases
in parasitism of mammals: effects of study
type, host age, and parasite taxon – Oikos, 78:
67–74.
Smith A.T., Foggin J.M. 1999–The plateau
pika (Ochotona curzoniae) is a keystone species
for biodiversity on the Tibetan plateau
– Anim. Conserv. 2: 235–240.
Wan X.R., Liu W., Zhao T.B., Jing Y.,
Guo P.F., Shi Y.S., Wang G.H. 2007
– Relationship between the infective characters
of Capillaria hepatica and the body mass
of the Brandt’s vole (Lasiopodomys brandtii)
– Acta Theriol. Sin. 27 (2): 165–169 (in Chinese
with English abstract).
Wang Z.D., Fang W., Ma J., Zhang Y., Cai
J.F., Han D.H., Lv R ., Zhong X.Y. 2003
– Effectiveness of Expelling Endoparasiteand
Ectoparasite of wild plateau pika – Chin. Qinghai
J. Anim. Vet. Sci. 33 (6): 22–23.
Wedekind C., Jakobsen P.J. 1998 – Malebiased
susceptibility to helminth infection: an
experimental test with a copepod – Oikos, 81:
458–462.
Wilson K., Moore S.L., Owens I.P.F. 2003
– Response to Comment on “Parasites as a
Viability Cost of Sexual Selection in Natural
Populations of Mammals” – Science, 300: 55b
Ye R.R., Liang J.X. 1989 – Study on the
growth and development of plateau pika under
the condition of artificial feeding – Acta
Theriol. Sin. 9 (2): 110–118 (in Chinese with
English abstract).
Zhang G.D. 1991 – Fleas, ticks and mites in
plateau pika in Qinghai – Chin. J. Vect. Biol.
Contr. 2: 131–133 (in Chinese).
Zhou L., Liu J.K., Liu Y. 1987 – Studies on
population productivity ecology of the plateau
pika (I). A dynamic model of growth of
body weight in the plateau pika – Acta Theriol.
Sin. 7 (1): 67–78 (in Chinese with English
abstract).
Zuk M., Mckean K.A. 1996 – Sex differences
in parasite infections: patterns and process
– Int. J. Parasitol. 26: 1009–1024.
Received after revising March 2008
journal 15.indb 539 2008-09-23 10:56:09