2009, Vol. 4 No. 1, Article 31
Biological Control of Helminth
Parasites by Predatory Fungi
S. De and P. K. Sanyal*
Department of Parasitology,
College of Veterinary Science & Animal Husbandry
Agricultural University Anjora, Durg-491 001, Chhattisgarh
Biological control of animal parasites could become a strong arm for
Integrated Parasite Control in the very near future. Though various
nematode-destroying fungi received attention, predominantly on
academic interest, from the 18th Century in Scandinavian countries,
work on their application to control animal parasites gathered
momentum from 1990's. The philosophy behind biological control is to
utilise one or more of the natural enemies of the nematodes, making
it possible to reduce the infection on pasture to a level where
grazing animals can avoid both clinical and subclinical effects of
the parasitic nematodes. The important requirement is the presence
of the fungi in the faecal pats where the development of the
pre-parasitic larvae takes place. Therefore, to be effective, the
fungi should pass through the gastrointestinal tract of the host
without loss of viability. The fungi, Duddingtonia flagrans and
Verticillium chlamydosporium, which can be isolated from organic
environment of India produces thick walled chlamydospores, the stage
responsible for their survival during passage through the gut of
ruminants following oral administration. The results had indicated
survival of the fungus during gastrointestinal transit in grazing
animals and successful reduction of numbers of parasitic nematode
larvae on pasture. The dose of fungal spores to be given to an
animal and the time of administration for effective parasite control
has been standardised. The fungus behaves in density dependent
manner and appears to be environment-friendly. The challenge lies
ahead in its field application.
Biological control, Helminth,
During the last 10-15 years there has been
an increasing emphasis on the need of development of new alternative to
or supplements for chemical control of parasitic nematodes in grazing
livestock. The background for this interest is multi-factorial but the
major reason is the serious development of anthelmintic resistance in
parasitic populations. Anthelmintic resistance involving particularly
the gastrointestinal nematodes of small ruminants is escalating globally
and is the single most important concern of parasitologists around the
world since it threatens the survivability of small ruminant farming as
well as the helminthologists. The problem is most severe in the
countries of southern hemisphere like South Africa (Van Wyk et al.,
1997), Australia (Waller et al., 1995a), New Zealand (Kettle et al.,
1983) and many other Latin American countries (Waller et al., 1995b).
India is slowly and steadily emerging as the resistance epicenter of
South Asia (Sanyal, 1998). The global tempo of development and extent of
anthelmintic resistance in helminths of small ruminants in particular,
indicates that the numerous anthelmintics and strategies developed and
implemented over the period of last 40-50 years have been incorrectly
applied (Van Wyk, 2001). Other reasons include handling of parasite
problems in the organic livestock production, regulation of conventional
drug use by legislation, political and consumer pressure for reduced
chemical residues in products. Sutherst (1986), among others, has talked
about the importance of implementing integrated parasite control based
upon host resistance, immunization and non-living vaccines to reduce the
use of chemotherapy. To become sustainable, parasite control schemes
need to be based on the principles of integrated pest management
(Waller, 1993). Towards this objective, significant advances have
recently been made in the development of worm vaccines (Emery, 1996;
Smith, 1997), in the breeding of animals for parasite resistance (Woolaston
and Baker, 1996) and biological control exploiting predacious fungi
PARASITE CONTROL MEASURES
Gronvold et al. (1996) have suggested two major groups of control
measures that are in use and would be tried in future.
Spraying of Poison
Use of Repellants
Selection for Host Resistance
Use of Pheromones
Sterile Male Technique
Present Status of Different Control Strategies
Three crucial reasons for opting alternative parasite control
strategies including biological control are drug resistance,
residues on food and environmental degradation. Frequent and
haphazard use, over-reliance on chemicals are the causes of the drug
resistance. As resistance to newer anthelmintics develops, there is
a need for control measures alternative to chemotherapy. Chemical
residues in foods are now a major concern and a strong driving force
for reduced chemical inputs in agriculture. Consumers increasingly
demand that food supply should be free from contaminants of all
kinds. Unlike organochlorine ectoparasiticides, residues are not a
major problem for anthelmintics. The benzimidazoles and their
prodrugs are subjected to close scrutiny because some are known
teratogens. The environmental impact of anthelmintics has been
generally regarded as un-important. Levamisole and the benzimidazoles
pose little cause of concern, but there is greater worry regarding
the avermectins. There is evidence of adverse effects on a variety
of dung colonizing insects.
Within the last decade, much effort has been directed at the
development of a vaccine especially against Haemonchus contortus,
either based upon naturally exposed or hidden antigens (Smith,
1997). Despite promising results and mass appraisal over the years,
a commercial product is still to be released. Dictol, based on
infective Dictyocaulus viviparous larvae attenuated by
irradiation, is the only marketed vaccine against GI nematodes but
it has only a very limited distribution.
strategies have been demonstrated to be useful to alleviate the
impact of GI nematodes in livestock (Barger, 1999; Stromberg &
Averbeck, 1999). Unfortunately, these strategies have not been
adopted to their full extent, perhaps due to the ease for the farmer
to use drugs and secondly, the increased demand for land, which
makes this proposition less likely in many intensive livestock
systems. Where it is used it is often in combination with
chemotherapy. In organic livestock production these strategies are
widely used, but are primarily based upon the availability of
herbage rather than an active measure to control problems with GI
nematodes (Thamsborg et al 1999). Breeding for Resistant Host
Breeding for resistance in host animals to GI nematodes has been
attempted with some success (Kloosterman et al 1992; Woolaston &
Baker, 1996; Gray, 1997), but although breeding programmes are
promoted and adopted based upon these principles (e.g. Nemesis in
Australia, Worm FEC in New Zealand), they are far from widely
This is now a
well-established fact that supplementation of the diet with
additional protein does not appear to affect initial establishment
of nematode infection but the patho-physiological consequences are
generally more severe on lower planes of protein nutrition. The main
effect of protein supplementation is to increase the rate of
acquisition of immunity and increase resistance to re-infection and
this has been associated with an enhanced cellular immune response
in the gastro-intestinal mucosa. Studies on the influence of
nutrition on the expression of genotype have shown that the benefits
of a superior genotype are not lost on a low protein diet whereas a
high protein diet can partially ameliorate the disadvantages of an
inferior genotype (Coop and Holmes, 1996). Although many aspects of
the interaction between nutrition and helminth parasites have been
established many features remain to be examined. It has now largely
been acknowledged that parasite control cannot be achieved by a
single method. The available classical and alternate technologies
should properly be integrated similar to those practiced in the
integrated pest control in agriculture. Biological control seems to
be one of such alternate control strategy.
Concept of Biological Control
This area of research has attracted increasing attention, especially
within the last 10-12 years. Biological control is defined as the
action of natural enemies which maintain a host population at levels
lower than would occur in the absence of enemies. This not only
includes classical un-exploited organisms but also those that are
genetically modified to enhance these properties (Waller and Faedo,
1996). Biological control is divided into two major categories,
viz., natural and applied. Natural biological control is affected by
native or co-evolved natural enemies in the environment without
Within the environment, the pre-parasitic stages of nematodes are subjected
to a variety of both abiotic and biotic factors that can profoundly
influence their development and survival. The most important abiotic
factors are temperature; humidity and oxygen-extremes in these can
be lethal on the free-living stages. In regard to biotic factors,
there exists a vast assemblage of living organisms that can affect
the success of worm eggs developing larvae. From these may emerge
candidate(s) for biological control of worm parasites. By
definition, biological does not assume to be a substitute for
chemotherapy, where the expectation, if not the reality, is that
parasites may be eradicated by frequent use of drugs with efficacies
approaching 100%. Biological control agents really eliminate the
target organism, but reduce the number of expectable levels and
maintain a balance between the pathogen and the antagonist. In
contrast to chemical control of nematode parasites, which is
directed entirely at the parasitic stage within the host, biological
control will almost certainly be focused on the free-living stages
of parasites on pasture.
The intention of using biological
control methods is to lower the density of pest population below the
clinical level and perhaps below the economic threshold above which
production losses are obvious owing to a high parasitic population
Agents for Biological Control
All gastro-intestinal nematode parasites of livestock have a
life-cycle which involves not only the parasitic stage within the
host, but also a free-living or pre-parasitic stage on pasture. The
pre-parasitic stages on the pasture are potentially vulnerable to
attack by biological control agents. A number of organisms have been
identified to exploit the free-living stages of parasites as food
source and are likely to be commercially exploited in the near
future. These organisms include micro-arthropods, protozoa,
predacious nematodes, virus, bacteria and fungi. Although the all
are of intrinsic interest, it is from the last group of organism
that breakthroughs in biological control of nematode parasites of
livestock are likely to emerge.
Fungi as Biological Control Tool
Fungi that exhibit anti-nematode properties have been known for a
long time. They consist of a great variety of species characterized
by their ability to capture and exploit nematodes either as the main
source of nutrients or supplementary to a saprophytic existence.
They are divided into three major groups based on their morphology
and types of nematode-destroying apparatus (Barron, 1997; Nordbring-Hertz,
specialized nematode-trapping structures (adhesive knobs, networks,
rings etc.) on the mycelium. The idea of possibly using predacious
micro-fungi to control animal nematodes arose in the 1930’s. It was
not until the mid 1980s before thorough and systematic
investigations were undertaken and since then, two lines of work can
be clearly distinguished.
Trials performed with mainly with Arthobotrys spp. (A.
Monacrosporium spp. as biological control agents. A group
of Danish researchers, testing the effect of fungus
A. oligospora primarily against parasitic nematodes in
cattle but also in other livestock species. Testing different doses
of spores mixed into faeces, 250 and 2500 conidia per gm of faeces
was found to significantly lower the number (70 & 99% reduction,
respectively) of developing
C. oncophora larvae in faecal cultures (Gronvold et al.
1985). The trapping activity of the fungus was influenced by the
motility of the infective larvae & there is no specificity for the
parasitic species (Nansen et al. 1996). Unfortunately various trials
performed to test
A. oligospora mycelium and conidia failed due to the
destruction of these structures in the GI tract of the host animals
(reported in Gronvold et al. 1993 a, b). A high dose (between 470 &
680 gm of fungal material on millet) of one of the three different
fungal species (A. musiformis, A. tortur, Dactylaria candida)
was fed to housed lambs, harboring a mono infection of either
H. contortus or O. circumcincta. This subsequently
led to survival of
A. tortur through the GI tract at a level high enough to
significantly reduce the number of
H. contortus in faecal cultures.
The other line of research is with Duddingtonia flagrans.
This predacious fungus produces three dimensional, sticky networks
on its growing hyphae. It also produces an abundance of intercalary
thick walled resting spores, chlamydospores. This fungus is
relatively slow growing and as with other predacious fungi growth is
strongly influenced by temperature (Fernandez et al. 1999e). Many
other species of predacious fungi are fast growing but the spores of
these fungi are much more sensitive to the stress of the GI tract
than that of the chlamydospores of
D. flagrans. In plot trials D. flagrans have shown
good reduction of free living larval stages of parasitic nematodes
of cattle (Gronvold et al. 1993a, b), sheep (Peloille, 1991) and
horses (Fernandez et al. 1997, 1999a; Baudena et al. 1999). These
field trials shown that daily feeding of fungal spores to grazing
animals for 3-4 months prevents build-up of dangerous levels of
infective larvae on the pasture. In an Australian study Knox and
Faedo (2001) found that sheep feed supplement containing
D. flagrans chlamydospores had lower egg counts and
improved liveweight gains compared to untreated animals.
These invade nematodes either by penetration of cuticle from sticky
spores adhering to the cuticle or following ingestion of spores
which lodged in the gut. This type of fungi is obligate parasite of
nematodes, with very limited capacity to develop outside the prey
and density dependent (Jaffe et al, 1993). This has led researchers
to believe that there might be better or stronger BC candidate
against pest nematodes.
Drechmeria coniospora is a fungus producing sticky drops on
very small conidia, which adhere to the cuticle of the nematode,
penetrate the cuticle and destroy the victim. By applying a very
high dose (108 conidia per gm of faeces) to faecal cultures, Santos
& Charles (1995) found that only infective third stage parasite
larvae stripped of the protective extra (second stage) cuticle,
became infected by the fungus. Another endoparasitic fungus,
Harposporium anguillulae produce very small, half moon
shaped conidia which lodge in the digestive tract of the feeding
nematode and after germination totally digest the victim before
finally breaking through the cuticle to produce new conidia on the
short conidiophores. In a laboratory study it was found that at a
dose of 3 lakh conidia/ gm faeces, the number of
H. contortus larvae recovered was significantly reduced
(Charles et al, 1996). The requirement of spore dispersion or
infection to be more or less directly from one infected individual
to the next, severely limits or almost excludes the use of this
group of fungi as practical BC agents.
These have the ability to attack the egg stage and may have a role
in the control of animal parasites which have a long development
and/or survival time in the egg stage in the environment outside
Ascaris, Fasciola spp., amphistomes etc.
Eggs of Ascaris lumbricoides collected from naturally infected pigs
were used to test the effect of mainly the fungus
Verticillium chlamydosporium but also other
Verticillium spp. the fungus was shown to be able to degrade
the egg shell enzymatically and infect the eggs (Lysek & Krajci,
1987; Lysek & Sterba, 1991; Kunert, 1992). Short exposure to high
temperature or UV- irradiation rendered the eggs more susceptible to
fungal attack (Lysek & Bacovsky, 1979). In the USA, Chien and
colleagues have shown that V. chlamydosporium attacked and
destroyed eggs of
Ascaridia galli and Parascaris equorum but only
Trichuris suis. In Denmark works were done on the
Arthobotrys spp. and egg parasitic fungi Paecilomyces
lilacinus for activity against eggs of
T. canis. P. lilacinus showed
some activity (16% eggs infected after 7 days) but the predacious
species did not attack the eggs.
Present Global Status
As a result of renewed interest and intensified research in
biological control during the last 15 years, a convincing amount of
evidence on the potential of this principle has been gathered
(Larsen, 2002). Most of this work has been carried out in Europe
(Denmark, Sweden, UK and France) and Australia and recently
initiated in USA, Latin America, Africa, South-east Asia and Far
East. Among the nematode trapping fungi,
Duddingtonia flagrans has displayed superior abilities with
respect to survival through gastro-intestinal transit as well as
subsequent destruction of parasitic larvae in faecal pats (Larsen,
2002). Danish scientists first demonstrated through laboratory and
field trials, that biological control against pre-parasitic stages
of nematodes could be achieved by feeding chlamydospores of this
fungus to cattle (Gronvold et al., 1993), horses (Fernandez et al.,
1997), pigs (Nansen et al., 1996) and sheep (Githigia et al., 1997).
Successful pilot scale trials with
D. flagrans chlamydospores through feed supplement (Knox
and Faedo, 2001), feed blocks (Waller et al., 2001a) and slow
release devices (Waller et al., 2001b) provide sufficient euphoria
for commercial exploitation of fungal delivery devices in future
integrated parasite control programmes. Besides being safe for
animals and man, it is imperative that new technologies dealing with
BC need to be of no negative impact to the grazing environment.
Short time impact studies have shown no negative effect of the
fungus on earthworms (Gronvold et al., 2000) and on soil nematodes (Yeates
et al.1997; Faedo, 2001). The future appears to be very promising in
early outcome of a bio-control product to control nematode parasite
Present Indian Status
India initiated the work on biological control of animal nematode
parasites using mycological means in 1998 and two species of
nematode-trapping fungi, viz.,
Arthrobotrys oligospora and D. flagrans and two
species of egg parasitic fungi, viz.,
Paecilomyces lilacinus and Verticillium chlamydosporium
were isolated from organic environment of Gujarat and Chhattisgarh (Sanyal,
2005; Sanyal et al., in press). They were subjected to stringent
screening for their suitability as biocontrol agents against
nematode parasites of ruminants using growth assay, predatory
activity, germination potential and ability to survive ruminant gut
passage. The study indicated that the isolates of
D. flagrans and V. chlamydosporium fulfilled all
the possible criteria. A strategy is formulated for application of
nematode-trapping fungi to control gastrointestinal nematodosis of
ruminants (Sanyal et al., 2005).
There is an increasing awareness that in
future the parasitic control programme should reduce reliance on
chemical anthelmintics. Compared to the other non-chemotherapeutic
approaches to parasitic control in ruminant livestock, use of nematode
trapping fungi has shown promising results in Denmark, Australia &
India. This has been well exemplified through both in vitro and in vivo
studies resulting in reduced translation of larvae to the herbage from
faecal pats and reduced worm burdens in livestock. As integrated
sustainable control strategies would be the modus operandi to control
the parasitic gastro-enteritis in livestock both in conventional and
organic farming system, mycological control would be arm for integration
with both non-chemical and chemical means.
Barger, I.A. 1999. The role of
epidemiological knowledge and grazing management for helminth
control in small ruminants. International Journal for
Parasitology 29, 41-48.
Barron, G.L. 1977. The
nematode-destroying fungi. Topics in Mycology No. 1. Canadian
Biological Publications Ltd., Guelph, Ontario, Canada.
Baudena, M.A., Chapman, M.E.,
Larsen, M. & Klei, T.R. 2000. Seasonal efficacy of nematophagous
fungus Duddingtonia flagrans in reducing numbers of
equine Cyathostome larvae on pasture in southern Lousiana.
Veterinary Parasitology (In press).
Charles, T.P., Rouque, M.V.C. &
Santos, C.DE P. 1996. Reduction of Haemonchus contortus
infective larvae by Harposporium anguillulae in sheep
faecal cultures. International Journal for Parasitology 26,
Coop and Holmes, 1996. Nutrition
and Parasite Interaction. International Journal for
Parasitology, 26, 951-962. Emery, D.L. 1996. Vaccination against
worm parasites of animals. Veterinary Parasitology 64 : 31-45.
Faedo, M. 2001. Growth, trapping
and genetic diversity of Duddingtonia flagrans a
biological control agent of free-living larval stages of
ruminant parasitic nematodes. Ph.D. Thesis. Danish Centre for
Experimental Parasitology, The Royal Veterinary and Agricultural
University, Copenhagen, Denmark.
Fernandez, A.S., Henningsen, E.,
Larsen, M., Nansen, P., Gronvold, J. & Sondergaard, J. 1999a.
Anew isolate of the nematode trapping fungus Duddingtonia
fagrans biological control agent against free-living larvae
of horse Strongyles. Equine Veterinary Journal 31, 488-491.
Fernandez, A.S., Henningsen, E.,
Larsen, M., Nansen, P., Gronvold, J., Henriksen, S.A. & Wolstrup,
J. 1997. Effect of the nematode-trapping fungus Duddingtonia
flagrans on the free-living stages of horse parasitic
nematodes: a plot study. Veterinary Parasitology 73, 257-266.
Fernandez, A.S., Henningsen, E.,
Larsen, M., Nansen, P., Gronvold, J. & Bjorn, H. 1999b. Growth
rate and trapping efficacy of nematode-trapping fungi under
constant and fluctuating temperatures. Parasitology Research 85,
Gary, G.D. 1997. The use of
genetically resistant sheep to control nematode parasitism.
Veterinary Parasitology 72, 345-366.
Githigia, S.M., Thamsborg, S.M.,
Larsen, M., Kyvsgaard, N.C. and Nansen, P. 1997. The preventive
effect of the fungus Duddingtonia flagrans on
trichostrongyle infections of lambs on pasture. International
Journal for Parasitology 27 : 931-939.
Gronvold, J., Henriksen, S.A.,
Larsen, M., Nansen, P. & Wolstrup, J. 1996. Biological control:
Aspects of biological control- with special reference to
arthropods, protozoans and helminthes of domesticated livestock.
Veterinary Parasitology 64: 47-64.
Gronvold, J., Nansen, P.,
Henriksen, S.A., Larsen, M., Wolstrup, J. & Fribert, L. 1996.
Induction of traps by Ostertagia ostertagi larvae,
chlamydospore production and growth rates in the
nematode-trapping fungus Duddingtonia flagrans. Journal
of Helminthology 61, 65-71.
Gronvold, J., Korsholm, H.,
Wolstrup, J., Nansen, P. & Henriksen, S.A. 1985. Laboratory
experiments to evaluate the ability of Arthobotrys
oligospora to destroy infective larvae of Cooperia
species and to investigate the effect of physical factors on the
growth of the fungus. Journal of Helminthology 59, 119-126.
Gronvold, J., H., Wolstrup, J.,
Nansen, P., Henriksen, S.A, Larsen, M. & Bresciani, J. 1993.
Biological control of nematode parasites in cattle with
nematode-trapping fungi- a survey of Danish studies. Veterinary
Parasitology 48, 311-325.
Gronvold, J., Wolstrup, J.,
Larsen, M., Henriksen, S.A. and Nansen, P. 2000. Absence of
obvious short-term impact of the nematode-trapping fungus
Duddingtonia flagrans on survival and growth of the
earthworm Aporrectodea longa. Acta Veterinaria
Scandanavia 41 : 147-151.
Jaffee, B.A., Tedford, E.C. &
Muldoon, A.E. 1993. Tests for density-dependent parasitism of
nematodes by nematode-trapping and end-parasitic fungi.
Biological Control 3, 329-336.
Kettle, P.R. Vlassoff, A., Reid,
T.C. and Horton, C.T. 1983. A survey of nematode control
measures used by milking goat farmers and of anthelmintic
resistance on their farms. New Zealand Veterinary Journal 31:
Kloosterman, A., Parmentier, H.K.
& Ploeger, H.W. 1992. Breeding cattle and sheep for resistance
to gastro-intestinal nematodes. Parasitology Today 8, 330-335.
Knox, M.R. and Faedo, M. 2001.
Biological control of field infections of nematode parasites of
young sheep with Duddingtonia flagrans. Veterinary
Parasitology 101 : 155-160.
Kunert, J. 1992. On the mechanism
of penetration of ovicidal fungi through egg shells of parasitic
nematodes. Decomposition of chitinous and ascaroside layers.
Folia Parasitologica 39, 61-66.
Larsen, M. 2002. Biological
control in a global perspective – A review with emphasis on
Duddingtonia flagrans. In Biological control of nematode
parasites of small ruminants in Asia, FAO Animal Production and
Health Paper, pp. 19-37.
Lysek, H. and Bacovsky, J. 1979.
Penetration of ovicidal fungi into altered eggs of Ascaris
lumbricoides. Folia Parasitologica 26, 139-142.
Lysek, H. & krajci, D. (1987).
Penetration of ovicidal fungus Verticillium chlamydosporium
through the Ascaris lumbricoides egg-shells. Folia
Parasitologica 34, 57-60.
Lysek, H. & Sterba, J. 1991.
Colonization of Ascaris lumbricoides eggs by the fungus
Verticillium chlamydosporium Goddard. Folia
Parasitologica 38, 255-259.
Nansen, P., Larsen, M.,
Roepstorff, A., Gronvold, J., Wolstrup, J. and Henriksen, S.A.
1996. Control of Oesophagostomum dentatum and
Hyostrongylus rubidus in outdoor reared pigs by daily
feeding with the microfungus Duddingtonia flagrans.
Parasitology Research 82 : 580-584.
Nordbring-Hertz, B. 1988.
Nematophagous fungi : strategies for nematode exploitation
and for survival. Microbiological Sciences 5 : 108-116.
Peloille M. 1991. Selection of
nematode-trapping fungi for use in biological control. In :
Working group on integrated control of soil pests, Methods for
studying Nematophagous Fungi, International Union of
Biological Sciences, Bulletin of West Paleartic Regional Section
14 : 13-17.
Sanyal, P.K. 1998. Integrated
parasite management in ruminants in India: A concept note.
Biological of gastro-intestinal parasites of ruminants using
predacious fungi, FAO Animal Production and Health Paper 141,
FAO, Rome, pp.54-65.
Sanyal, P.K. 2005. Mycological
control of nematode parasites of livestock : from academic
interest to reality. Proceedings of National Academy of
Sciences, India 75 (B)-Special Issue : 263-271.
Sanyal, P.K., Sarkar, A.K.,
Patel, N.K., Mandal, S.C. and Pal, S. 2008. Formulation of a
strategy for the application of Duddingtonia flagrans
to control caprine parasitic gastroenteritis. Journal of
Helminthology 82 : 169-164.
Sanyal, P.K., De, S., Sarkar,
A.K., Patel, N.K., S.C. Mandal and S. Pal. Isolation of egg
parasitic fungi from Chhattisgarh plain. Journal of Veterinary
Parasitology (in press).
Santos, C.P. & Charles, T.P.
1995. Effetio da aplicacao de conidios de Drechmeria
coniospora em cultivos de fezes contendo ovos de
Haemonchus contortus (Effect of an endo-parasitic fungus,
Drechmeria coniospora, in faecal cultures containing
eggs of Haemonchus contortus). Arquivo Brasileiro de
Medicina Veterinaria et Zootecnia 47, 123-128.
Smith, W.D. 1990. Prospects for
vaccines of helminth parasites of grazing ruminants.
International journal for Parasitology 29, 17-24.
Smith, W.D. 1997. Prospects for
vaccines against gastrointestinal helminth parasites of
ruminants. In : Managing Anthelmintic Resistance in
Endoparasites. Workshop held at the 16th International Congress
of the World Association for the Advancement of Veterinary
Parasitology (eds. J.A. Van Wyk and P.C. Van Schalkwyk) Sun
City, South Africa, pp. 6-12.
Stromberg, B.E. & Averbeck, G.A.
1999. The role of parasite epidemiology in the management of
grazing cattle. International journal for Parasitology 29,
Sutherst, R.W. 1986.
Epidemiological concepts and strategies for parasites control:
What changes are likely to occur? In Parasitology-Quo Vadit,
Proceedings of the 6th International Congress of Parasitology
(ed. Howel, M.J.), pp. 721-729. Australian Academy of Sciences.
Thamsborg, S.M., Roepstorff, A. &
Larsen, M. 1999. Integrated and biological control of parasites
in organic and conventional production systems. Veterinary
Parasitology 84, 169-186.
Van Wyk, J.A. 2001. Refugia-
overlooked as perhaps the most potent factor concerning the
development of anthelmintic resistance. Onderstepoort Journal of
Veterinary Reseach 68: 55-67.
Van Wyk, J.A., Malan, F.S. and
Randles, J.L. 1997. How long before resistance makes it possible
to control some field strains of Haemonchus contortus
in South Africa with any of the anthelmintics. Veterinary
Parasitology 70: 111-122.
Van Wyk, J.A., Coles, G.C. and
Krecek, R.C. 2002. Can we slow the development of anthelmintic
resistance? An electronic debate. Trends in Parasitology 18:
Waller, P.J. 1997. Sustainable
helminth control of ruminants in developing countries.
Veterinary Parasitology 71 : 195-207.
Waller, P.J. and Faedo, M. 1996.
The prospects for biological control of the free-living stages
of nematode parasites of livestock. International Journal for
Parasitology 26 : 915-925.
Waller, P.J., Dash. K.M., Barger,
I.A., Le Jambre, L.F. and Plant, J. 1995a. Anthelmintic
resistance in nematode parasites of sheep: learning from the
Australian experience. Veterinary Record 136: 411-413.
Waller, P.J., evarria, F.,
Eddi, C., Maciel, S., Nari, S. and Hansen, J.W. 1995b.
Anthelmintic resistance in nematode parasites of sheep flocks in
South America. Veterinary Record 136: 620.
Woolaston, R.R. & Baker, R.L.
1996. Prospects for breeding for parasite resistance.
International Journal for Parasitology 26, 845-855.
Yeates, G.W., Waller, P.J. and
King, K.L. 1997. Soil nematodes as indicators of the effect of
management of grasslands in the New England Tablelands (NSW):
Effect of measures for control of parasites of sheep.
Pedobiologia 41: 537-548.