Are Worms Affected by Host Ecology? a Perspective from Mudumalai Wildlife Sanctuary, Southern India

2004·2.4 MB·

by  Guha Dharmarajan

,
Journal of the Bombay Natural History Society, 101 (3), Sep-Dec 2004 399-402
ARE WORMS AFFECTED BY HOST ECOLOGY? A PERSPECTIVE FROM
MUDUMALA1 WILDLIFE SANCTUARY, SOUTHERN INDIA
1
Guha Dharmarajan2 M. Raman3 and MathewC. John4
,
'Accepted May, 2002
2Centre for Ecological Sciences, Indian Institute ofScience,Bangalore 560 012, Karnataka, India. Email:guha_d@yahoocom
’Department of Parasitology, Madras Veterinary College, Chennai 600 007, Tamil Nadu, India.
4Department ofWildlife Science, Madras Veterinary College, Chennai 600 007, Tamil Nadu, India
Interspecific comparisons ofhelminth loads, using helminth eggs per gram offaeces as an index, were done in the
Mudumalai Wildlife Sanctuary between May and August, 1999. The host species sampled were chital (Axis axis),
sambar Cervusunicolor),gaur(Bosgaums),elephant(Elephasmaximus)anddomesticcattle. Helminthdistributions
(
inallthespecieswerehighlyoverdispersedandexceptinthecaseofgaurthenegativebinomialdistributiongavegood
fitstotheobserveddata. Ingeneral, itwasfoundthattheelephantandgaurhadhigherloadsthanthecervids, probably
duetotheirlargerbody size.Amongthecervids, sambarhad lowerloadsthan chital probablybecausetheyaremixed
feedersasopposedtochital, which aremainlygrazers. Cattlehadthehighestloadsandprevalenceofparasitesamong
allthe speciesstudied, probablyduetotheeffectsofdomestication and poorhygiene. Helminth communitystructure
and species diversity was related to the taxonomic distinctivenessofthe host. It isthus likely that many interspecific
differences in helminth loadscan beexplained bytheexistinghypothesesrelatedto hostecology.
Key words: Helminths,Axisaxis, Cervus unicolor.Bosgaurus,Elephasmaximus cattle
INTRODUCTION decrease inrainfall fromthewestern side(1,800 mm/year)to
theeasternside(600 mm/year).Ahighdiversityofvegetation
Wildlife conservation, with population health as an types has been observed (Sukumar et al. 1992).
important component, has emerged as one of the greatest
challenges ofourtime. However, the existing knowledge on MATERIALAND METHODS
wildlifedisease isoflittlehelpwhendealingwith population
health, as most ofthis information has accumulated through Hosts sampled: Species ofhost included were chital
“investigation ofindividualanimalsratherthan populations” (Axis axis), sambar (Cervus unicolor), gaur (Bos gaurus),
(Spalding and Forrester 1993). In spite ofthis, there have elephant (Elephas maximus) and forest grazing domestic
beenonlyafewstudies(Aroraetal. 1985, Watve 1992, Bhatt cattle.
1994), in India, on helminths in free-ranging wildlife Coprologicalstudy: Helmintheggspergramoffaeces
populations. This according to Davis and Anderson (1971) (epg) have been used as an index of helminth load. A
could be because “itwas a common theme that the parasites representative sample ofapproximately 2 gm was collected
ofwild animals were so perfectly adapted to their host that fromclearlydemarcated,freshdungpilesvoidedbythetarget
under natural conditions they would not cause disease.” species. Samples were collected in labelled, pre-weighed
However, research has shown that this premise is not true containers with 10 ml of 10% formalin between 0700 and
with parasite affecting the survival of their host directly 0900 hrs daily. The exact weight of faeces collected was
(Choudhary etal. 1987,Nudds 1990)or indirectly(Freeland calculated by subtracting the weight of the container with
1981,Schall 1983,Rau 1984,Saumieretal. 1986).Foraclearer formalin fromtheweightofthecontainercontainingthedung
picture of helminth epidemiology in wild herbivores, it is sample in formalin. The intensity ofhelminth infection was
essential to understand the ecological factors that affect the determined by the quantitative Sedimentation-floatation
magnitude ofinfection in the host species. Technique developed and standardized by Watve (1992).
Prevalence of strongyle genera were calculated using data
STUDY AREA
obtainedfrom larval cultures. Samplesforlarval cultureswere
collectedseparately in cloth bags, keptmoist,andcultured in
The study area comprises the Mudumalai Wildlife the laboratory within 12-15 hours after collection. Larval
Sanctuary and National Park, and the Sigur Reserve Forest, culturesforthirdstage(infective)strongyle larvaeweredone
situated between 1 1° 32'-1 1° 93’ N and 76° 22'-76° 43' E. asperRobertsandO’Sullivan(1949). Larvaewere identified
Elevations vary between 900-1,000 m above msl. There is a with the help of keys provided by Davies (1984). Larvae
1
EFFECTS OF HOST ECOLOGY ON HELMINTH LOADS
Table 1 Distribution of helminth eggs in selected species ofwild herbivores and domestic cattle
attheMudumalaiWildlifeSanctuary,TamilNadu
Host Species Samplesize % Infected Median Mean Variance Index of d-statistic Negative
Load (epg) Load (epg) Dispersion Binomial
Parameters
k X2
Chital 214 74.77 2 3 88 191 53 49 32 124 34* 0.76 198 ns
Gaur 54 85 19 3 11 93 684 82 57 42 67.77* 0.64 40 47*
Elephant 34 85 29 3.5 4 15 45.04 10.86 18.71* 1.38 724ns
Sambar 36 58 34 1 1.22 11 49 9 40 17.35* 1.38 3 51ns
Cattle 56 91.07 5.5 7 84 156 35 19 95 36 4* 1.19 12-52ns
epg-eggs per gram of faeces; *- Statistically significant, ns- not significant (see text for details)
culturedfromelephantdungwere identifiedbymeasurements species (parasite species richness) in the study animals. The
given by Raman(Unpubl. Data). median egg load was chosen in preference to the mean
Terminology: Helminth loads have been expressed in because in over-dispersed populations a few outlying
termsofeggspergramoffaeces(epg). In thisstudy,theterm individuals can drastically affect the latter. The parasites
has been broadened to include larvae of lungworms also. identified in the hosts showed that most host species, with
Theterm“species”hasbeenused looselytodescribedistinct the exception of elephants, had similar parasitic genera
groups of parasites. Thus, for example all fluke eggs are (Table2).
classifiedasasingle ‘species’. Thoughtheterm ‘Operational
Taxonomic Unit' as used by Watve (1992) is more accurate,
the term species is retained because offamiliarity in usage. Table 2 Helminth species identified in the hosts sampled
The total number of such “species” has been used as an
Host Parasite species identified Parasitic
indexof“Parasitediversity” in thehost community. Because diversity
of the methodology used, definitions of some terms used
here are different from Margolis et al. (1982). The term Chital Trichostrongylus sp , 16 species
Oesophagostomum sp
‘prevalence’ indicates percentage of samples found to be Haemonchus sp Mecis,tocirrus sp.,
,
positive forhelminth eggsand/or larvae. Theterm sympatric Cooperia sp., hookworm, Muellerius sp.,
isdefinedas(ofbiological speciationorspecies)takingplace Dicrocoelium sp., Cotylophoron sp.,
Nematodirussp trichurid, fluke,
or existing in the same or overlapping geographic areas ascarid, strongylo,id, anoplocephalid and
(Hanks 1979). This term has been used synonymously with spirurid
co-grazing.
Sambar* strongyle, fluke, Muelleriussp and 4 species
StatisticalAnalyses: Calculationofindexofdispersion, strongyloid
d-statistic and fitting of the negative binomial distribution
has been done as per Ludwig and Reynolds (1988). The Gaur Trichostrongylus sp , 12 species
Oesophagostomum sp., Haemonchus sp
d-statisticwastermedsignificant if>1.96.All otherstatistics Mecistocirrus sp hookworm, ,
,
weretested ata probability level of5%. Muellerius sp fluke, protostrongylus,
,
strongyloid, anoplocephalid, trichurid and
spirurid
RESULTS
Elephant Murshidia sp Quilonia sp 7 species
, ,
The distribution of helminths in all host species Decrusia sp , Bathmostomum sp,,
fluke, spirurid and anoplocephalid
sampled was highly non-random or over-dispersed as the d-
statistic was >1.96 (Table 1). The negative binomial Cattle Trichostrongylus sp , 13 species
Oesophagostomum sp
distribution in general gave good fits to the observed data in Haemonchus sp Mecis,tocirrus sp.,
the case ofall the species studied, with the exception ofgaur Cooperia sp hoo,kworm, fluke, ascarid,
,
(Table 1). Interspecific comparisons ofhelminth loads were strongyloid, Moniezia sp , trichurid,
Dicrocoelium sp and Nematodirus sp
carried out using three main parameters. These parameters
were the prevalence of infection (Percentage of animals
infected),medianeggload(inepg)andtotal numberofparasite * Larval culture data not obtained for host species
400 J. Bombay Nat. Hist. Soc., 101 (3), Sep-Dec 2004
EFFECTS OF HOST ECOLOGY ON HELMINTH LOADS
DISCUSSION Cattlewerefound tohavethehighest levelsofparasite
prevalence(91.07)aswell asmedianegg loads(5.5 epg)and
Inthis study, eggpergram offaeces (epg)wasused as this could be due to two reasons. Firstly, it has been
an index ofhelminth load in the host. Though this method hypothesised that domestication tends to tilt the “natural
has limitations as pointed out by Foreyt and Trainer(1980), balance” in favourofparasites(Gordon 1948). Secondly,the
faecal examination is non-invasiveand thus hasgreat appeal cattlegrazingin Mudumalai arekeptin pensduringthenight.
especially in wild animals. Because ofpositive correlation The high levels of crowding in these pens will create an
between worm size and egg output (Skorping et al. 1991), environmentthat isconducive forthe increasedtransmission
egg outputs can be considered to be an accurate indicator of ratesofparasites(Solomon 1965). Poorhygiene inthepensis
parasite biomass, ifnot numbers. Faecal eggcounts can thus likely to exacerbate these high transmission rates, and thus
give very valuable assistance in studies concerninghelminth contribute both to the high parasite prevalence rates and
populations(Robertsetal. 1951). helminth loads observed in cattle.
Prevalenceofinfection and median eggloads: Itwas Parasite species richness: The richness of parasite
found that the two larger herbivores sampled, namely fauna varied widely among different species of host.
elephants and gaur, had the highest prevalence ofinfection Taxonomically related host species tend to share parasite
(85.29%and85.19%respectively)and medianloads—(3.5 and species (Cameron 1964, Segun 1971), which may be due to
3 epg respectively), as compared to that ofcervids chital immunological reasons (Freeland 1983). Thus, host species
andsambar.Thiscouldbeduetothreemajorreasons. Firstly, withalargenumberofrelatedspecies inthesameareacanbe
larger animals tend to consume large quantities offood and expected to have high parasite species richness. This was so
water, and thus have greater chances ofpicking up infective in our findings, with chital having the greatest parasite
parasitic stages (Kennedy et al. 1986). Secondly, as larger diversity (16 parasite species) followed by gaur(12 species)
animals have larger gastrointestinal tracts, the “crowding andforestgrazingcattle( 13 species). Elephantswith noclose
effect” as described by Read (1951) is less likely to be of relativeshadthe lowestspeciesdiversity(7 species). Sambar
importance, thus allowing these animals to support larger was not considered forcomparison, as larval culturedatafor
numbers ofparasites without reductions in parasite size and this species could not be obtained. Using larval culture data,
fecundity. Thirdly, as body size increases there is a decrease which allows identification ofstrongyles up to the generic
in predatory pressures. In Mudumalai, sambar and chital are level, itwasfoundthattheruminants(chital,gaur,cattle)had
preyed uponby leopards, tigers and wild dogs, while gaur is very similar parasitic genera. This is well in agreement with
mostlypreyed uponbytiger. Elephantsdonotform theusual Horak(1981). Elephants,whichwerephylogeneticallydistinct
prey base ofany carnivore. Since parasites can decrease the fromotherherbivores,werefoundtohaveadistinctivestrongyle
ability of animals to escape predation either directly, by communitystructurecomposedofMurshidiasp.,Decrusiasp.,
reducingrunningstamina(Schall etal. 1982)or indirectly,by Quiloniasp.andBathmostomum sp.Genericlevelidentification
causingdebility (Soulsby 1982), animals like deerwith high ofotherparasiteswasonlypossible in a fewcaseswherein the
predatory pressures are likely to evolve higher resistance to eggmorphologywasvery distinct (e.g. Trichurissp.).
infection by way of natural selection. Additionally, if From the management point of view, the fact that
carnivoresselectpreywithpoorbodycondition(Kruuk 1972) the cattle entering the Sanctuary have the highest worm
theymayselectivelyremoveanimalswithhigh parasite loads loads among the herbivores, and also have many parasitic
fromthepopulation,thusreducingamajorsourceofinfection genera in common with the wild herbivores, should be
tootheranimals. viewed with concern. Dharmarajan et al. (2003a, b) shows
Among the cervids studied, sambar had lower thatsuchcattlemayhaveadverseeffectsonchital populations.
prevalence of infection and median egg loads (58.34% In conclusion, it may be stated that differences in
and 1 epgrespectively)as compared to chital (74.77%and2 parasite loads and helminth community structure between
epg). Ithasbeenobservedthatsambarisamixed feeder,both differentspeciesofwildlifeand forestgrazingdomesticcattle
grazing and browsing, as compared to chital which is in Mudumalai can be explained by the existing ecological
predominantlyagrazer(Schaller 1967). Sincebrowserstend hypotheses. The majorparameters are likelytobe species of
to have lower loads of parasites (Horak 1984), mainly host, phylogenetic distinctiveness, feeding habits and
as a result of less contact with the infective stages of the domestication. Morework is required to identify therelative
helminths, which are found mainly in the soil or on grass, importanceofthevarious factors influencingthedistribution
the higher helminth load in chital can be attributed to this ofhelminths within and between populations ofhost species
reason. studied in Mudumalai.
1 Bombay Nat. Hist. Soc., 101 (3), Sep-Dec 2004 401
EFFECTS OF HOST ECOLOGY ON HELMINTH LOADS
ACKNOWLEDGEMENTS Mr. S. Swaminathan (Bombay Natural Flistory Society);
Dr. R. Sukumar, Dr. N.V. Joshi (Centre for Ecological
We thank the Tamil Nadu Forest Department, Sciences); Dr. G. Rajavelu, Dr. S. Ramesh, Dr. M.G.
Mr. A. Udhayan, IFS; Dr. V. Krishnamurthy (retd. Forest Jayathangaraj (Madras Veterinary College) and Mr. Sachin
Veterinarian); Mr. A.A. Desai, Dr. N. Baskaran, Ranade.
REFERENCES
Arora, B.M., P.N. Bhat & K. Ramaswamy (1985): Survey of Ludwig, J.A. & J.F. Reynolds (1988): Statistical ecology: A primer.
gastrointestinalparasiticinfectionsinfreewildmammals.FAO John Wiley & Sons, Inc., NewYork. 337 pp.
fielddocumentNo. 5:Proceedingsoftheworkshopon“Wildlife Margolis, L., GW. Esch, J.C. Holmes, A.M. Kuris & G.A. Schad
health for Veterinarians”. Wildlife Institute of India, Dehra (1982): The use ofecological terms inparasitology (Reportof
Dun. 90 pp. an ad-hoc committee of the American Society of
Bhatt, N. (1994): Disease profile in wild herbivores. M.V.Sc. Thesis Parasitologists). J. Parasitol. 66: 131-133.
submitted to Tamil Nadu Veterinary & Animal Sciences Nudds, T.D. (1990): Retroductive logic in retrospect: The ecological
University, Chennai, Tamil Nadu. 78 pp. effectsofmeningeal worms.J. Wildl. Manage. 54: 396-402.
Cameron, T.W.M. (1964): Host specificity and the evolution of Rau,M.E.(1984):L,ossofbehaviouraldominanceinmalemiceinfected
helminth parasites. Adv. Parasitol. 2: 1-34. with Trichinellaspiralis. Parasitology88: 371-373.
Choudhary, C., B. Narasimhaswamy, V. Shivasankar, M R. Read, C.P. (1951): The “crowding effect” in tapeworm infections.
Krishnamohan Rao & J.H. Das (1987): Hydatidosis in lungs J. Parasitol. 37: 174-178.
and liver ofan American bison (Bison bison). Ind. Vet. J. 64: Roberts,F.H.S.& P.J.O’Sullivan(1949): Methodsforeggcountsand
713-714. larvalculturesforstrongylesinfectingthegastro-intestinaltract
Davies, E.T. (Ed.) (1984): Manual ofveterinary investigation. 3rd ofcattle. Aust. J. Agri. Res. 1: 99-103. (Original notseen)
edn. Volume2. MinistryofAgriculture, Fisheries& Food, Her Roberts,F.H.S.,P.J.O’Sullivan&R.F.Rieck(1951):Thesignificance
Majesty’s Stationary Office, London. Pp. 173-175. ofegg counts in diagnosis ofparasitic enteritis in cattle. Aust.
Davis,J.W.& R.C.Anderson(Eds.)(1971): Parasiticdiseasesofwild Vet. J. 278: 16-21.
mammals. 1st edn. Iowa State University Press, Ames. Iowa. Saumier,M.D.,M.E.Rau&D.M. Bird(1986):TheeffectofTrichinella
364 pp. pseudospiralisinfectiononthereproductivesuccessofcaptive
Dharmarajan, G, M. Raman & M.C. John (2003a): The effects of Americankestrels (Falcosparverius). Can. J. Zool. 64: 2123-
cattlegrazingandhabitatonhelminthloadsinchital(Axisaxis) 2125.
intheMudumalaiWildlifeSanctuary,SouthernIndia.J. Bombay Schall,J.J.(1983):Lizardmalaria:costtovertebratehostsreproductive
Nat. Hist. Soc. 100: 58-64. success.Parasitology87: 1-6.
Dharmarajan, G, M. Raman & M.C. John (2003b): Effect ofcattle Schall,J.J.,A.F. Benett& R.W. Patman(1982):Lizardsinfectedwith
and habitat on helminth community structure of chital. Ind. malaria: Physiological and behavioural consequences. Science
Vet. J. 80: 984-987. 217: 1057-1059.
Foreyt, W.J. & D.O. Trainer (1980): Seasonal parasitism changes in Schaller, GB. (1967): The deer and the tiger: a study ofwildlife in
two populations ofwhite-tailed deer in Wisconsin. J. Wildl. India. University ofChicago Press, Chicago. 384 pp. —
Manage. 44: 758-764. Segun, A.O. (1971): Acephaline gregarines ofBritish earthworms
Freeland,W.J. (1981): Parasitismandbehavioural dominanceamong their possible host specificity. Parasitology 62: 389-399.
male mice. Science 213: 461-462. Skorping,A.,A.F.Reed&A.E.Keymer(1991): Lifehistorycovariation
Freeland, W.J. (1983): Parasites and the co-evolution ofanimal host in intestinal nematodes of mammals. Oikos 60: 365-672.
species. Am. Nat. 121: 223-236. (Original not seen)
Gordon, H.M. (1948): The epidemiology ofparasitic diseases, with Solomon, M.E. (1965): Analysis of processes in control of insects.
special reference to studies with nematode parasites ofsheep. Adv. Ecol. Res. 2: 49.
Aust. Vet. J 24: 17-45. Soulsby,E.J.L.(1982):Helminth,arthropodsandprotozoaofdomestic
Hanks, P. (Ed.) (1979): Collins Dictionary ofEnglish Usage. Collins, animals. 7thedn. BaillerieTindall Co., UK. 824 pp.
London, pp. 1472. Spalding, M.G & DonaldJ. Forrester(1993): Diseasemonitoringof
Horak, 1.G (1981): Hostspecificity& thedistributionofthehelminth free-ranging and released wildlife. J. Zoo. & Wildl. Med. 24:
parasites of sheep, cattle, impala and blesbok according to 271-280.
climate.J. SouthAfrican Vet. Assoc. 52: 201-20—6. Sukumar, R., H.S. Dattaraja, H.S. Suresh, J. Radhakrishnan,
Horak, I.G (1984): Cattle, wild animals & parasites Epizootic or R. Vasudevan, S. Nirmala & N.V. Joshi (1992): Long
delicatelybalancedecosystem. 13thWorldCongressondisease term monitoring of vegetation in a tropical deciduous
ofcattle, Durban, Sept. 1989, pp. 390-393. forest in Mudumalai, Southern India. Curr. Sci. 62:
Kennedy, C.R., A.O. Bush & J.M. Aho (1986): Patterns in helminth 608-616.
communities: Why are birds and fish different? Parasitology Watve, M.G (1992): Ecology ofhost-parasite interactions in a wild
93: 205-215. mammalian host community in Mudumalai, Southern India,
Kruuk. H. (1972): Thespotted hyena.Astudyofpredation and social Ph.D.ThesissubmittedtoIndianInstituteofScience,Bangalore.
behaviour.ChicagoUniversityPress,Chicago(Originalnotseen) 114 pp.
402 J. Bombay Nat. Hist. Soc., 101 (3), Sep-Dec 2004