Prevalence of intestinal parasites
among captive Asian Elephants Elephas maximus: effect of season, host
demography, and management systems in Tamil Nadu, India
V. Vanitha1, K. Thiyagesan2& N. Baskaran3
1,2Postgraduate and Research Department of Zoology and Wildlife Biology, A.V.C.
College, Mannampandal, Mayiladuthurai, Tamil Nadu 609305, India.
3 Asian Nature Conservation Foundation, Innovation Centre, Indian Institute of Science, Bengaluru, Karnataka 560012 India.
Present address: 1 D.G.
Government Arts College (Women), Mayiladuthurai, Tamil Nadu 609001, India.
Email: 1 vanithabaskar@rediffmail.com (corresponding author), 2 kthiyagesan1@rediffmail.com, 3 baskar@ces.iisc.ernet.in
Date of publication (online): 26 February 2011
Date of publication (print): 26 February 2011
ISSN 0974-7907 (online) | 0974-7893 (print)
Editor: Heidi S.
Riddle
Manuscript
details:
Ms #
o2488
Received
21 June 2010
Final
received 02 January 2011
Finally
accepted 17 January 2011
Citation: Vanitha, V.,
K. Thiyagesan & N. Baskaran (2011). Prevalence
of intestinal parasites among captive Asian Elephants Elephas maximus:
effect of season, host demography, and management systems in Tamil Nadu, India.Journal of
Threatened Taxa 3(2): 1527-1534.
Copyright: © V. Vanitha,
K. Thiyagesan & N. Baskaran 2011. Creative Commons Attribution 3.0 Unported
License. JoTT allows unrestricted use of this article in any medium for
non-profit purposes, reproduction and distribution by providing adequate credit
to the authors and the source of publication.
Author detail: Dr. V. Vanitha is presently an assistant
professor in zoology. She obtained
her PhD in 2008 for the study on ‘Status and management of captive Asian
Elephants in Tamil Nadu, India from Bharathidasan University,
Tiruchirapalli. Dr. K. Thiyagesan is an associate
professor, working on ornithology and is the research adviser to number of PhD
students. Dr. N. Baskaran is a
scientist at the Asian Elephant Research and Conservation Centre, working on
wild Asian Elephants across Eastern, and Western Ghats and Eastern Himalaya for
more than two decades. His
research interest includes behavioural ecology of various mammalian fauna, and
assessment of population, habitats, biodiversity and impact of development
activities.
Author
contribution: VV designed and conducted the present study as a part of her Doctor of
Philosophy Research Degree. KT and
NB supervised the research work with technical inputs as research advisers.
Acknowledgements: We thank the
Tamil Nadu Forest Department, Hindu Religious Endowment Charity and private
elephant owners for permitting this study and providing access to the register
of records maintained for the captive elephants. We also thank AVC College for providing laboratory for
analyzing the dung samples. We
acknowledge the critical comments and inputs by Dr. Guha Dharmarajan, Purdue
University, Indiana, U.S.A. and Susan Mikota, DVM, Elephant Care International,
Hohenwald, TN, U.S.A. that shaped this manuscript significantly.
Abstract:Maintenance of wild animals in captivity is fraught with
numerous challenges, including the control of disease. This study evaluates the effect of season,
host demography (age-sex), and differing management systems on the prevalence
of intestinal parasites among elephants managed in three captive systems:
temple, private, and forest department, in Tamil Nadu. In addition, the study also assessed
the availability of veterinary care for elephants in these systems. The parasitic prevalence was evaluated
by direct microscopic identification of helminth eggs in faecal samples (n =
115) collected from different age/sex classes of elephants. Of the 115 elephants examined, 37%
showed positive results, being infected only with Strongyles sp. The prevalence rate varied significantly across seasons,
with the highest rate during summer (49%) followed by monsoon (41%) and the
lowest rate during winter (15%). While males had a significantly lower parasite prevalence compared to
females (29% vs. 40%), age classes showed no significant difference. Despite the fact that the proportion of
animals receiving veterinary care was higher under the forest department system
(100%) compared to the private system (26%), parasite prevalence was
significantly higher under the former (48%) than the latter (31%) system. The difference in the proportion of
animals with parasitic prevalence among the three systems could be due to differing
management practices (i.e. in solitary versus groups) and the details are
discussed.
Keywords:
Captive Asian Elephants, forest department, intestinal parasite, management
prevalence, private, Temple.
INTRODUCTION
Most
free-living organisms harbour parasites of several species (Begon & Bowers
1995), which can adversely affect host health, fecundity and foraging, and may
also modify host behaviour to facilitate parasite transmission (Wesenberg-Lund
1931; Holmes & Bethel 1972; Moore 1984). Parasitism has been shown to directly affect both the
evolution and ecology of hosts through processes such as sexual selection
(Hamilton & Zuk 1982) or parasite-mediated competition, which can lead to a
reduction in population size, or the extinction of one host (Price et al.
1986). Asian Elephants Elephas
maximus are susceptible
to gastrointestinal parasitic infection in the wild (Watve 1995; Dharmarajan
2000; Vidya & Sukumar 2002) and in captivity are often confined to small
enclosures and/or maintained in isolation (Vanitha 2007) in damp unhygienic
conditions that may result in enhanced susceptibility to parasitic disease
(Dhungel et al. 1990; Chandrasekaran et al. 1995; Suresh et al. 2001).
Tamil
Nadu, a southern state of India, manages approximately 150 captive elephants
under three different management systems: private, temple and forest department
(Vanitha 2007; Vanitha et al. 2010). The captive elephants in the temple system are managed with very limited
mobility and are used mainly for religious and cultural ceremonies in Hindu
temples, while private elephants are used for commercial purposes such as in
films and in VIP programmes with extensive travel, in addition to cultural and
religious ceremonies in Hindu temples that do not own an elephant. In contrast, captive elephants in the
Tamil Nadu forest department are managed mostly in semi-wild conditions at
forest camps located in Mudumalai and Anamalai wildlife sanctuaries (presently
tiger reserves). While originally
used for timber logging, captive elephants under the forest department
management are presently used predominantly for ecotourism. Additionally, on a rotational basis, a
few elephants from the timber camps are placed by the forest department at the
Arignar Anna Zoological Park, Chennai, for education and entertainment (Vanitha
et al. 2010).
Given
the widely differing husbandry conditions in which elephants are managed under
the three systems (Vanitha 2007; Vanitha et al. 2008, 2009), it is meaningful
to ask whether there is variability in the prevalence of parasites in the
different management systems. There have been studies on the prevalence of parasitic infection in
captive elephants managed in nature reserves (Arunachalam et al. 2007),
zoological gardens (Suresh et al. 2001) and Hindu temples (Saseedran et al.
2003). This paper presents data
comparing the occurrence of intestinal parasites among captive elephants in
three management systems during various seasons and among various age–sex
classes in Tamil Nadu.
MATERIALS AND METHODS
Study animals and sampling
procedures: Between 2003
and 2005, faecal samples (one/individual) were collected from 115 captive
elephants managed by: (i) the Tamil Nadu Forest Department at the elephant
camps in Mudumalai and Anamalai wildlife sanctuaries, and Arignar Anna
Zoological Park, Vandalur (n = 42), (ii) temples (n = 38: Appendix 1), and
(iii) private owners (n = 35: Appendix 2). Dung samples were collected within a few hours of defecation
and stored in 10% formalin. From
each dung pile, a representative sample was collected from the outer and inner
parts of different boli; parts in contact with soil were avoided. Details of the age and sex of the study
animals were recorded by interviewing the mahouts (keepers) as well as by
verifying the studbook or register of records. Where proper age records were not available, as in the
case of animals caught/rescued from the wild by the forest department or those
bought from other states by private and temple authorities, age was estimated
by employing the shoulder height method of Sukumar et al. (1988). Considering the diverse climatic
conditions that prevail across the study area: the Western Ghats, where the
forest department manages most of its captive elephants, and the plains, where
the private and temple systems manage their elephants, the year was divided
into three seasons - summer, monsoon, and winter and designated according to
similarities in climate. For the
timber camps of the forest department, the period from February to April was
treated as summer, May to November as monsoon, and December to January as
winter. In the case of private,
temple and Arignar Anna Zoological Park elephants, March to July was classified
as summer, August to November as monsoon, and December to February as winter.
Parasite prevalence appraisal: The prevalence of intestinal parasites
among captive elephants was assessed through coprological analysis using direct
microscopic examination, and the sedimentation floatation methods following
Watve (1992, 1995), Vidya & Sukumar (2002), and the sedimentation technique
standardized by Monson-Bhar & Bell (1982). In the sedimentation floatation method, a known weight of
dung sample (in 10% formalin) was strained to remove the coarse debris and the
filtrate was centrifuged. The dung
that sedimented was dissolved in 10ml of saturated zinc sulphate solution
(specific gravity 1.8%) and centrifuged again. In the first centrifugation,
nematode eggs sink with the faecal matter. Nevertheless, in the second round they float to the surface
due to the high specific gravity of zinc sulphate. Six loopfuls of the solution were removed from the surface
using a wire-loop of 5mm diameter and the solution was examined to record
presence or absence of eggs. If no
eggs were found in a sample, 12 more loopfuls of the solution (six at a time)
were scanned for eggs to confirm the absence of parasite infection. In the sedimentation technique
(Monson-Bhar & Bell 1982), a small amount of faecal sample was emulsified
with 10ml of water in a centrifuge tube and was centrifuged for two minutes at
3000rpm. The supernatant was
poured off carefully and a drop of the sediment was placed on a slide and
examined under the microscope.
Veterinary care: The availability of professional
veterinary care for the elephants in the three management systems was evaluated
through a questionnaire survey with the concerned authorities, and also by
scrutinizing the register (medical) records of the elephants. Information such as presence or absence
of periodic medical check-ups by veterinarians, and the number of medical
check-ups per year were obtained for each elephant.
Analysis: The prevalence of parasitic infection
among captive elephants in three management systems, three seasons, and
different sex and age-classes was determined by the presence or absence of data
on parasitic infection of individual elephants. Statistical significance for the proportion of elephants
infected with parasites out of the total number of individuals examined was
tested using the proportion test. A
logistic regression analysis using presence or absence of parasites (coded as 1
or 0) at the individual level as the independent variable, and the management
system (private, temple, forest department), season (monsoon, summer, winter),
age class (calf & juvenile (0-5 yr), sub-adult (5-15 yr), adult (15 yr and
above)) and sex (male, female), as dependent variables were coded as 1 to 2 or
3 according to number of categories. Data on the proportion of elephants with periodic medical check-ups in
the three management systems was tested using the proportions test.
RESULTS
Intestinal
parasite prevalence
Overall
and among seasons: Out of 115
individuals examined for intestinal parasite prevalence, 43 (37%) individuals
were found positive (Table 1). All
the positive cases were infected only with helminthic parasites (Strongyles sp.). Both eggs and worms of Strongyles sp. were
identified from the infected individuals. The eggs were found in all infected
cases and worms were found only in one case. The proportion of elephants (43 out of 115) infected with
intestinal parasites was significantly lower than uninfected individuals
(χ2 = 6.817, df = 1, p = 0.009). Parasite prevalence was
significantly different in three seasons (Wald = 9.681, p <0.01) (Table 2),
with the highest infection rate found during summer (19 out of 39 or 49%),
followed by monsoon (23 out of 61 or 38%), and the lowest infection rate during
winter (1 out of 15 or 7%). The
rate of infection between monsoon and winter did not vary significantly (B ± SE
= 2.089 ± 1.147, Wald = 3.315, p > 0.05), while the infection rate between
summer and winter varied statistically (B ± SE = 3.238 ± 1.169, Wald = 7.670, p
< 0.01), indicating parasite prevalence was more common during summer.
Prevalence
among three management systems: The
occurrence of intestinal parasites varied significantly among the three
management systems (Wald = 8.753, p = 0.01) with the prevalence of parasite
infection being higher among captive elephants in the forest department (20 out
of 42 or 48%) system than in temple (12 out of 38 or 32%) and private (11 out
of 35 or 31%) systems (Table 1). The proportion of infected individuals between the private and forest
department systems was not significantly different (B ± SE = -1.300 ± 0.697,
Wald = 3.483, p > 0.05) (Table 2), while the infection rate observed between
the temple and forest department systems showed a significant difference (B ±
SE = - 2.239 ± 0.757, Wald = 8.750, p < 0.01) indicating a higher
susceptibility to parasitic diseases for elephants in the forest department
system.
Prevalence
between sex and among age–classes: Among
the 31 males and 84 females sampled, the prevalence of helminthic infection was
significantly higher in females (34 out of 84 or 40%) than in males (9 out of
31 or 29%), (B ± SE = - 1.693 ± 0.649, Wald = 6.811, p < 0.01) (Table 2)
suggesting that females are more prone to helminthic infection under captive
conditions than males. Among the three major age classes of elephants tested,
the prevalence of intestinal parasites was not significantly different (Wald =
1.221, p > 0.05) with 41% individuals in adult class, 29% of individuals in
sub–adult class, and 25% of juvenile and calves being infected.
Periodic
medical care: The data on the
veterinary care in the three captive management systems reveal that only
one-fourth (26%) of the elephants in the private system, and three-fourths
(75%) in the temple system had periodic medical examinations. All the elephants (100%) in the forest
department system were checked periodically by veterinarians. A proportions test on the percentage of
elephants with periodical medical check-ups in the three systems reveal that
the observed difference was statistically significant (Z = -2.54; p < 0.01)
indicating that in Tamil Nadu elephants managed in the private system had
significantly less access to veterinary care than elephants in the other two
systems.
DISCUSSION AND CONCLUSIONS
In general, macroparasites (i.e. parasitic species
where reproduction usually occurs via transmission of free-living infective
stages that passes from one host to the next) aggregate across their host
population with most individuals harbouring low number of parasites, but a few
individuals play host to higher parasitic burdens (Shaw & Dobson
1995). Such heterogeneity is
generated due to variation between individuals in their exposure to infective
stages and differences in their susceptibility (Wilson et al. 2002). The intestinal parasite Strongyle sp. was prevalent among 37% of the captive elephants
monitored across three management systems in Tamil Nadu during 2003-2005. This parasite infection rate is similar
to the prevalence rate of 36% reported for Mudumalai timber camp elephants
(Arunachalam et al. 2007), and lower than that reported (majority of the 245
cases) among the captive elephants in Kerala (Chandrasekharan et al.
1995). However, the present estimate
was considerably higher than the 10% parasite infection reported for the
Guruvayoor Temple elephants (Saseedaran et al. 2004). Such differences among different elephant populations could
be attributed to variable treatment levels, husbandry practices, sampling
season, and age-sex classes.
Among the three management systems studied, the
parasite prevalence was higher in the captive elephants of the forest
department system compared to temple and private systems, while the elephants
in the former facility had a higher level of medical attention than those in
the latter two systems. In the forest department system, over 90% of the
captive elephants are managed at the timber camps in social groups, sharing the
natural habitat of wild elephants which are known to have a high parasite
prevalence (Watve 1995; Dharmarajan 2000; Vidya & Sukumar 2002). The social life style, along with the
semi-natural environment shared by wild elephants is likely to enhance
susceptibility to parasitism from conspecifics both within the system as well
as from the wild. In support of
this, at the Anamalai timber camp, 14 of the 16 forest department elephants
examined for parasites showed positive results. Most of the private and temple elephants are managed in
solitary conditions or in small groups, and provided with Astasooranam, a traditional herbal medicine prepared by mahouts, at periodic intervals for digestive ailments (Vanitha
2007). In addition, regular
vaccinations and de-worming activities organised by the Tamil Nadu government
during the special rejuvenation camps for the temple and private elephants
coinciding with this study (2003-2005) may have contributed to the lower
prevalence of intestinal parasites among the private and temple elephants. The
higher prevalence of helminthic parasite infection during summer and early
monsoon could be due to the prevalence of ideal climatic conditions
(temperature & humidity) for faster rates of egg hatching and rapid
development to the infective stage as reported elsewhere (English 1979), and
due to poor hygienic conditions of the resources such as shelter, food and
water. Further, the nutritional state of the host is known to affect
immuno-competence (Rolston 1992; Lyles & Dobson 1993), and as the rainy
season progresses, the increased vegetation growth could reduce nutritional
stress and thus improve overall resistance to helminth infection (Dharmarajan
et al. 2005).
The present study and that from the Nehru Zoological
Park, Hyderabad (Suresh et al. 2001) show the prevalence of intestinal
parasites was higher in females than males, contradicting the general trend
reported for mammals (Poulin 1996; Schalk & Forbes 1997). Such trends among captive elephants
could be related to the more social nature of females with frequent physical
contacts to various age-sex classes compared to males, and hence more
susceptibility to parasitic infection. Besides the above reason, the lesser mobility of female elephants
compared to males, observed during the course of grazing in natural habitats at
the timber camps in the forest department system (Vanitha 2007), resulted in
the same space being more frequently used by females than males. In comparison to free ranging
elephants, such a constraint imposed by captivity could also contribute to the
higher prevalence of parasitic infection among females. The observed higher (80%) proportion of
females with parasitic prevalence at timber camps is in line with the above
statement.
In general, wildlife medicine has received less
interest in India when compared to the western world, and the situation is the
same with regard to captive elephant health care (Krishnamurthy & Wemmer
1995; Bist 2002; Vanitha 2007). Lack of clinical facilities with appropriate equipment and financial
constraints contribute to inadequate veterinary care in all the captive elephant
management systems. The situation
is more prominent in private and temple systems, as shown by data on the
proportion of elephants receiving veterinary care in the three systems in this
study, and elsewhere (Krishnamurthy 1998; Bist et al. 2002; Vanitha 2007). Therefore, due to a lack of exercise,
quality and quantity of food, and other appropriate husbandry practices along
with inadequately trained veterinary support, elephants in the temple and private
systems experience more major health problems (like arthritis, foot rot, skin
diseases, overweight and underweight) than the elephants in the forest
department system (Vanitha 2007), and this needs immediate redressal. Overall, the study shows that the
prevalence of intestinal parasites is higher (i) in cases of captive elephants
managed by the forest department in social groups within natural habitats
shared with wild conspecifics than those solitarily managed in private and
temple facilities, (ii) during summer and monsoon when compared to the winter
season, and (iii) among females than males. Therefore, the study suggests more
frequent diagnosis and deworming for the forest department captive elephants,
especially those managed at the timber camps of Mudumalai and Anamalai wildlife
sanctuaries, during summer and monsoon seasons.
REFERENCES
Arunachalam, K., M. Raman
& T.J. Harikrishnan (2007). Incidence
of helminth ova in Indian elephants Elephas maximus at
Theppakadu Nilgiris, Tamil Nadu. Zoos’ Print Journal22(11): 2898–2899.
Begon, M.
& R.G. Bowers (1995). Beyond
host-pathogen dynamics, pp. 478-509. In: Grenfell, B.T. & A.P. Dobson,
(eds.). Ecology
of Infectious Diseases in Natural Populations. Cambridge, Cambridge University Press.
Bist, S.S. (2002). An overview
of elephant conservation in India. Indian Forester128(2): 121-136.
Bist,
S.S., J.V. Cheeran, S. Choudhury, P. Barua & M.K. Misra (2002). The domesticated Asian Elephants in
India, pp. 129-148. In: Giant in our Hands. Proceedings of the International
workshop on the domesticated Asian Elephants. Bangkok, Thailand, February
2001.
Chandrasekharan,
K., K. Radhakrishnan, J.V. Cheeran, K.N. Muraleedharan & T. Prabhakaran
(1995). Review of the
incidence, ecology and control of common diseases of Asian Elephants with
special reference to Kerala, pp. 439–449. In: Daniel, J.C. & H.S.
Datye (eds.). A Week with Elephants:
Proceedings of the International Seminar on the Conservation of Asian Elephant.
June 1993; Oxford University Press, Oxford.
Dharmarajan,
G. (2000). Epidemiology
in wild and domestic herbivores at the Mudumalai Wildlife Sanctuary, Tamil
Nadu. M.V.Sc Thesis submitted to Tamil Nadu University of Veterinary and Animal
Sciences, Chennai, Tamil Nadu, 75pp.
Dharmarajan, G., M. Raman
& M.C. John (2005).Effect of season on helminth loads of wild herbivores and cattle in the
Mudumalai Wildlife Sanctuary, southern India. Zoos’ Print Journal 20(2): 1766-1769.
Dhungel,
S., C. Browner & S. Yoder (1990). Elephant training and management in Nepal. Tigerpaper 17:1-6.
English,
A.W. (1979). The epidemiology of
equine Strongylosis in southern Queensland 1. The Bionomics of the Free-Living
Stages in Faeces and on Pasture. Australian Veterinary Journal 55(7): 299-305.
Hamilton,
D.G. & M. Zuk (1982). Heritable
true fitness and bright birds: a role for parasites? Science 218: 384-387.
Holmes, J.C. & W.M. Bethel
(1972). Modification of
intermediate host behaviour by parasites. Zoological Jounral of the
Linnean Societysupplemnt 1: 123-149
Krishnamurthy, V. (1998). Captive elephant management in India
under different systems: Present trends. Zoos’ Print 13: 1-4.
Krishnamurthy, V. & C. Wemmer
(1995). Veterinary care
of Asian timber elephants: Historical accounts and current observations. Zoo
Biology 14: 123-133.
Lyles, A.M. & A.B. Dobson
(1993). Infectious
disease and intensive management: population dynamics, threatened hosts and
their parasites. Journal
of Zoo Wildlife Medicine24: 315–326.
Monson–Bhar,
P.E.C. & D.R. Bell (1982). Manson’s
Tropical Diseases. English language
book society/Bailliere, Tindall, London, xvii+1557pp.
Moore, J.
(1984). Parasites that change the
behaviour of the hosts. Scientific
American 250: 108–115.
Price,
P.W., M. Westoby, B. Rice, P.R. Atsatt, R.S. Fritz & J.N. Thomson (1986). Parasite mediation in ecological interaction. Annual
Review of Ecology and Systematics 17:
487-505.
Poulin, R.
(1996). Sexual inequalities in
helminthic infections: a cost of being male? American Naturalist147: 287-295.
Rolston,
H. (1992). Ethical responsibilities
towards wildlife.Journal of American Veterinary Association200: 618-622.
Saseedran, P.C., S.
Rajendran, H. Subramanian, M. Sasikumar, G. Vivek & K.S. Anil (2003). Incidence of helminthic infection among
annually de-wormed captive elephants. Zoos’ Print Journal 19(3):
1422.
Schalk, G.
& M.R. Forbes (1997). Male biases
of parasitism in mammals: effects of study type, host age and parasite taxon. Oikos 78: 67-74.
Shaw, D.J.
& A.P. Dobson (1995). Patterns of
macro-parasite abundance and aggregation in wildlife populations: a
quantitative review. Parasitology 111: 111-133.
Sukumar, R., N.V. Joshi & V.
Krishnamurthy (1988).Growth in the Asian Elephants. Proceeding of the Indian Academy
of Science. (Animal
Science) 97(6): 561-571.
Suresh, K.P., C. Choudhuri,
K. Nalini Kumari, Md. Hafeez &
P.A. Hamza (2001). Epidemiological
and clinico-therapeutic studies of strongylosis in elephants. Zoos’
Print Journal 16(7): 539-540.
Vanitha,
V. (2007). Studies on
the status and management of captive Asian Elephants (Elephas
maximus) at Tamil Nadu
in southern India. PhD Thesis. Bharathidasan University, Tiruchirapalli, India,
130+xpp.
Vanitha,
V., K. Thiyagesan & N. Baskaran (2008).Food and feeding of captive Asian Elephants (Elephas maximus) in
the three management facilities at Tamil Nadu, south India. Journal
of Scientific Transactions in Environment and Technovation 2(2): 87–97.
Vanitha,
V., K. Thiyagesan & N. Baskaran (2009). Socio-economic
status of elephant keepers and human–captive elephant conflict: A case
study from three management systems from Tamil Nadu, southern India. Gajah 30: 8–12.
Vanitha,
V., K. Thiyagesan & N. Baskaran (2010).Demography of captive Asian Elephants (Elephas maximus) in
three management systems in Tamil Nadu, India. Journal of the Bombay Natural History Society 107(1): 30-37.
Vidya,
T.N.C. & R. Sukumar (2002). The
effect of some ecological factors on the intestinal parasite loads of the Asian
Elephant (Elephas
maximus) in southern
India. Journal
of Bioscience 27:
521–528.
Watve,
M.G. (1992). Ecology of
host-parasite interactions in wild mammalian host community in Mudumalai,
southern India. PhD Thesis. Indian Institute of Science, Bangalore, India.
Watve,
M.G. (1995). Helminthes
parasites of elephant’s ecological aspects, pp. 289-295. In: Daniel, J.C. &
H.S. Daty (eds.). A week with elephants: Proceedings of the International
Seminar on the Conservation of Asian Elephants. June 1993; Oxford University
Press, New Delhi.
Wesenberg–Lund,
C. (1931). Contributions to the
development of the Trematoda Digenea. Part I. The biology of the Leucochloridium
paradoxum. Kongelige
Danske Videnskabernes Biology Selskab4: 89–142.
Wilson, K., O.N. Bjornstad, A.P. Dobson, S. Merler, G. Poglayen, S.E. Randolph, A.F. Read & A. Skorping (2002). Heterogeneities in macro-parasite infections: patterns and processes, pp. 6-44. In: Hudson, P.J., A. Rizzoli, B.T. Grenfell, H. Heesterbeek & A.P. Dobson (eds.).The Ecology of Wildlife Diseases.Oxford University Press, New York, United States, xii+197pp.