ELSEVIER International Journal for Parasitology 29 (1999) 139-146

Biological control of helminths

M. Larsen*
Danish Cer~rc for E.uprrimenfal Parasitology, Rowl Vrtrrinar~ ami .4gricultural Uniwrsit~. 3 Rideehanrwj,
DK-1870 Frederiksherg C, Dennmrk

Received 1 June 1998: accepted 24 September I998

Abstract

As a potential component in future integrated parasite-control strategies, biological control by means of predacious
fungi seems to be moving from a promising possibility toward becoming a reality, and the netforming nematode-
destroying fungus Dlrddingtoniu,pug~ans appears to be the candidate of choice. Not only has this fungus been found in,
and isolated from. fresh sheep, cattle and horse faeces, but it also appears to be the only fungus that is able to consistently
and significantly reduce the number of infective trichostrongyle larvae in faeces from animals fed fungal spores. Results
from the last few years have shown that D. ,flagrans is able to trap and destroy free-living stages of the most important
and common trichostrongylid larvae with very similar external life-cycles, as well as larvae of parasites with a slightly
different transmission biology (Nenmrodirus spp., Dict.vocau/us civiparus). The introduction of microfungi for biological
control could be as part of a feed supplement or incorporated in feed-blocks presented to animals which are raised
under relatively intensive conditions and constant surveillance. Apart from the special niche for organic farmers, such
a product would be suited for horses. small ruminants (as either milking herds or housed daily for other reasons), cattle
in special situations and free-roaming pigs. The most important constraint, still, for a major breakthrough in biological
control in the latter is the lack of good antagonists against the long-lived and rather resistant infective stages of parasites,
being transmitted as larvae inside the egg. Since the first Conference on Novel Approaches to the Control of Helminth
Parasites of Livestock in Armidale, Australia, 1995, there has been a steady evolution within the area of biological
control of parasitic nematodes. Today this principle is being exploited and tested out in almost all parts of the world,
under various climatic conditions and production systems. Where, in the past. a large part of the work focused on cattle
and to a lesser degree horse and sheep parasites, the focus of the research in many of the newly involved countries is on
small ruminants, because of their importance to primarily small-scale farmers in local communities. Today research and
trials are either on-going or being planned in many developing countries, as well as in countries in transition. The
involvement of multinational agencies in addition to national and industrial interests is very welcome and should increase
the chances and keep up the momentum for development and implementation of biological control in future animal
production around the world. s(_‘,1998 Australian Society for Parasitology. Published by Elsevier Science Ltd. All rights
reserved.

Kr~uvrds: Biological control; Livestock; Parasitic nematodes: Nematode-destroying fungi; Duridiil~tonia,f~fi~~~

*Tel: 45 3528 2794; Fax: 45 3528 2774: e-mail: mila(a kvl.dk

0020-7519/98/S - see front matter i;, 1998 Australian Society for Parasitology. Published by Elsevier Science Ltd. All rights reserved.
PII:s00’0-7519(98)00185-4
140 M. Larser~llr~trunational Jourual,for Purasitology 29 / 1999) 139-146

1. Introduction to have been serious attempts to pursue the possi-

bility of using bacteria, in particular Bacillus
Within the last 5-10 years there has been a steady, thuringiensis, as biological control agents. Since
increasing interest and involvement in research on Ciordia and Bizzell [l l] showed that B. thuringiensis
biological control of animal parasitic nematodes toxin could affect free-living stages of some cattle
of grazing livestock. During this period, biological parasitic nematodes, detailed studies by Bone et al.
control of nematodes has gone from being some- [12-141 and Bottjer et al. [15, 161 showed that eggs
thing considered to be a novelty of mainly basic and larvae of Trichostrongylus colubrifbrnzis could
research interest to an area of applied research with be killed by B. thuringiensis israelensis toxin.
the potential of becoming an important, integrated Unfortunately, there appears to have been no fur-
element in developing new, sustainable strategies ther development in this area within the last 5
to control parasitic nematodes in livestock. The years.
urgency of developing and implementing these new Predation on soil nematodes by mites, Turbel-
strategies stems primarily from the severe problems larians, tardigrades, or predacious nematodes, plus
of anthelmintic-resistant worm populations the influence of earthworm or dung-beetle activity
developing and spreading across the world, in par- on allocation of nematodes into soil, indicates that
ticular in the small ruminants, sheep and goats [lL the various naturally occurring mortality factors in
41. The means of fighting this problem are likely the pasture environment might, to a certain extent,
to encompass a restricted and more clever use of be able to reduce the number of free-living stages
anthelmintics [5], grazing-management strategies of parasitic nematodes in dung and surrounding
[6-81 with or without animals bred for worm resist- soil. Since the activity and subsequent influence
ance or tolerance [9]. preventive use of biological of many of these natural enemies are affected by
control agents and, possibly, vaccines. It is very changes in the environment, it is likely that through
important in this context to stress that, besides a manipulation of the environment it will be possible
few exceptional situations [lo], biological control to increase the number of nematode antagonists
should be used as a prophylactic measure and not and, thereby, potentially further reduce the survival
be looked upon as a single alternative solution to of animal parasitic nematode larvae in the system
the traditional use of chemicals. Instead, biological [17, 181. The existence of the so-called suppressive
control is likely to become a major, integrated soils, where naturally occurring enemies appear to
element in strategies which could provide reliable increase in intensive monocultures of cultivars,
and sustainable solutions to integrated parasite seems to support this natural control concept. Simi-
management in the future. lar controlling mechanisms could be expected to be
The whole philosophy of using a biological con- stimulated on organic farms, where a rich nematode
trol agent against animal parasitic nematodes is to population would trigger increase of the number of
significantly reduce the number of infective stages enemies, such as nematode-destroying fungi.
available to be picked up by grazing susceptible Nematode-destroying fungi exist as a natural part
individuals of the different species of livestock. This of the soil microflora, and they have also been iso-
reduction in infective stages on herbage will sub- lated from old [19, 201 and fresh faeces [21-231. In
sequently prevent the build-up of worm burdens in a recent study from New Zealand [19] it was shown
hosts, which otherwise would cause subclinical or that nematode-destroying fungi are quickly intro-
clinical responses, in particular in young animals. duced into freshly deposited sheep dung, where they
In the past, several natural enemies of nematodes, could contribute to the destruction of larvae of
such as, e.g., earthworms, collembolans, mites, parasitic nematodes. This invasion by nem-
predatory nematodes, viruses and bacteria, have atophagous fungi, most likely carried by already
repeatedly been suggested as potential candidates infected, but surviving soil nematodes, is antici-
as biological control agents. When we look on what pated to take place in other types of dung and in
has actually evolved, apart from the work on the other parts of the world. Invasion and dis-
nematode-destroying microfungi, there appear only semination of fungal material in this way would
 M. Larse,ilIntevnational Journdfor Parasitology 29 (1999) 139-146 141

contribute to a natural biological control of para- that are efficient BC agents [25,45]. In fresh faeces,
sitic larvae on permanent pastures. fungi belonging to several genera have been
A steadily increasing number of review articles isolated, predominantly predatory fungi forming
have been published within the last 4-5 years on the three-dimensional networks. Endoparasitic fungal
subject of potential biological control of helminths, species are never or very rarely isolated from fresh
as well as possibilities for the various elements in faeces.
integrated control strategies 124-361. The present,
short overview will focus on some of the trials and
experiments which have been carried out over the 3. Biological control experiments-laboratory
past decade involving biological control of animal and in-vivo trial
parasitic nematodes by the use of nematophagous
microfungi. Although some fungi which attack eggs The types of experiments that have been per-
of plant-parasitic nematodes have also been formed to test the potential biological control fungi
described, the only fungi dealt with here will be can be divided into two categories:
those capable of trapping or infecting free-living
larval stages of animal parasitic nematodes. 1. Laboratory experiments observing the pre-
dacious capacity of pure fungal cultures on agar
plates or in faecal-culture assays.
2. Fungal candidates for biological control of 2. In-vivo experiments where fungal material is
animal parasitic nematodes either mixed into faeces of parasitised animals
and subsequently deposited on pasture (plot tri-
Experience has shown that it is clearly not als) or experiments where fungal material is
sufficient just to find and isolate fungi with the given per OSto the host and the subsequent effect
capacity to trap nematodes. As the whole idea of on the developing free-living stages of the para-
biological control (BC) of animal parasitic nema- site in the faecal environment is monitored.
todes relies on preventive reduction of infective These tests could be either plot or full-scale graz-
stages on the pasture, it is necessary for a good BC ing experiments.
candidate to survive passage through the gas-
trointestinal tract (GIT) of the animals for sub- 3.1. Laborator), e.uperiments
sequently being voided with the parasite eggs in the
fresh faeces, where it should be able to germinate, The often voracious activity of many different
grow, trap and destroy parasite larvae. fungal species against almost any kind of bait nema-
In the quest for good BC candidates, researchers tode (numerous important species of cattle, sheep,
have tested fungal isolates from culture collections horse and pig parasitic nematodes) has been studied
125, 37, 381 or isolates obtained from various natu- on petri dishes with various agar media [4659].
ral sources, such as soil, old and fresh faeces [lo, These studies have involved a range of different
19,20,22,23,39-44]. To be sure of their real poten- fungal species from collections or newly isolated
tial as BC candidates, isolates from both collections from soil or faeces. Often, the conclusions of such
as well as soil and old faeces have to go through a studies have been very favourable with regard to
number of laboratory and in-door tests (passage the potential of the investigated fungi as BC agents
tests through housed animals). On the other hand, against animal parasitic larvae, but a solution of
fungi found in, and isolated from fresh, per rectum- how to implement this in practice is most often
collected faeces have already proven their capacity missing. By definition, there exist several hundred
to survive through the GIT of the host animals we species of nematophagous fungi [60-621, many of
are interested in. Therefore, it is anticipated that which would be able to infect and destroy the free-
such fungi will have a greater potential as BC agents living stages of parasitic nematodes when tested in
compared with collection isolates. As it also has these simple laboratory tests. Some work indicates
been shown, it is not all fungi surviving the GIT that the endoparasitic group of fungi, infecting their
142 M. Larsmllnterrlational Journal,for Parasitology 29 (1999) 139-146

victims by means of either small spores which lodge icles have clearly demonstrated that it is possible
in the oesophagus/gut of the feeding nematodes or to reduce both the amount of infective larvae on
by small, adhesive spores sticking to the nematode herbage and subsequently the number of nematodes
cuticle, subsequently penetrating and destroying establishing in the grazing animals [44, 64701.
the nematode, may be less likely to produce good Most of the work performed to date has involved
candidates due to a reduced effect against the free- animals infected with Ostertagiu ostertagi and
living stages of animal parasitic nematodes, and in Cooperia oncophora, the most common parasites in
particular the infective third stage. cattle in the Northern Europe. Recent work on the
It is clear that attempts to draw firm conclusions effect of D.jugrans against another very important
as to whether one fungus or another would be suited cattle pathogen, Dictyocaulus viviparus, have shown
as a potential biological control agent against ani- that this fungus is also able to control lungworms
mal parasitic nematodes cannot be justified on sim- [71] when tested in faecal assay in the laboratory as
ple laboratory tests alone. This being said, it has well as in a plot study. Also, there has been a report
also been shown that if faecal cultures are used in of control of Strongyloides papillosus by an Arthro-
a sequence of events of stress-selection of fungi [40, botrys oligospora in faecal cultures [lo]. Both of
41, 631, simulating GIT passage, the data from the these parasites have previously been considered
laboratory assays are very good predictors of which difficult to control by the same fungus as used
fungal isolates/species would have a good in-vivo against the most common trichostrongyloids, due
potential for survival through the GIT and sub- to the different transmission biology of the former
sequently be highly efficient against developing two, but the present data seem to indicate that the
parasite larvae in the faecal environment. fungi will also be able to control these parasites.
In sheep, nematophagous fungi have been iso-
3.2. In-vivo experiments lated from fresh faecal pellets of grazing sheep [22].
Various passage experiments have confirmed that
Today, there is good evidence showing that in only a limited number of fungal species are able to
the field under natural or experimental conditions, survive passage through the GIT in sufficiently high
species of the nematophagous fungi serve as good numbers to subsequently reduce the number of
BC agents. Using this approach, it has been shown developing parasite larvae [21, 22, 63, 72, 731. As
that virtually all the important nematode parasites before, D. flagruns isolates are the most consistent
of all species of livestock can be successfully performers, showing high survival and reduction
controlled. As mentioned above, examination of capacity. With respect to testing BC agents against
fresh faeces from cattle, sheep and horses has shown sheep parasitic nematodes in field situations, we
that there is a low, natural excretion of fungal have yet only relatively limited, but very encour-
spores [20, 22, 271. The fungi have been found in aging data [42,74]. One study [74] performed under
less than 5% of the samples examined. The vast Danish conditions showed that D. flagruns could
majority of the fungi belong to the predacious significantly reduce worm burdens in lambs on pas-
group and are very often of the type forming three- ture and, surprisingly, was capable of also reducing
dimensional, sticky network. In subsequent tests the number of Nematodirus spathiger and Nem-
for the capability of such fungal isolates to survive atodirus battus in the small intestine, in addition to
GIT passage, one species appears to rank above the Ostertagia spp. and Trichostrongylus spp. in the
rest Duddingtoniaflagrans, producing many resist- abomasum. In Fiji [42], some preliminary work
ant, thick-walled resting spores, chlamydospores. with sheep in pens also indicates that supplementing
This special feature seems to be what makes the sheep on pasture with D. jlagrans chlamydospores
difference between successful passage and survival would provide control of H. contortus and other
compared to those producing many thin-walled important sheep parasitic nematodes. By employ-
conidia. ing mathematical modelling to BC of worms in
With regard to the effect of nematophagous fungi sheep, it has been suggested that a 75% reduction
against cattle parasitic nematodes, numerous art- in larval yield for at least 60 days will provide equal
 M. Larsetlilnternationrrl Jownal,for Parasitology 29 (1999) 139-146 143

or better control than three doses of anthelmintics nematodes (e.g., D. tkiparus and Nematodirus spp.)
in the chosen scenario [24]. with a transmission biology which is different from
With regard to horse parasites, besides some lab- the general pattern for trichostrongyloids.
oratory studies [38, 75, 761, only a limited number Ongoing work indicates that apart from using
of passage, plot or field experiments have been car- fungi as BC agents given to the animals in feed
ried out [77779]. Larsen et al. [78] found that D. supplements, it is feasible to consider incorporation
Ragrans was able to survive passage through the of fungi into blocks or mineral salt mixes. Although
alimentary tract of horses and subsequently destroy preliminary Slow Release Device techniques have
free-living stages of cyathostomes in faecal cultures. been investigated, there are still many unanswered
In a subsequent field trial, Larsen et al. [79] dem- questions and unsolved technological problems to
onstrated that D.jagrans significantly reduced both attend to before this latter option becomes an econ-
the number of infective strongyle larvae on pasture omical feasible option. The first introduction of
and the acquired worm burden in tracer foals. The microfungi for BC could be as part of a feed sup-
highly significant capacity to reduce herbage infec- plement or incorporated into various kinds of feed-
tivity has recently been confirmed in a plot study blocks presented to animals, raised under relatively
[77] under Danish conditions and preliminary intensive conditions and constant surveillance.
results from a plot study performed in Louisiana, Apart from the special niche for organic farmers,
USA, indicate that this fungus will also be able to one could consider a product for horses, small rumi-
grow and control horse parasitic strongyles in a nants (as either milking herds or for other reasons
warm and moist climate. housed daily), cattle in special situations and free-
Finally, a single report [SO] has shown that the roaming pigs. The most important constraint, still,
free-living stages of parasitic nematodes in free- for a major breakthrough in the latter is the lack of
roaming pigs could also be controlled by D. Jag- good antagonists against the long-lived and rather
rans. The worm burdens of Oesophagostomum resistant infective stages of parasites (e.g., Ascaris
dentatum and Hyostrongylus rubidus in tracer pigs suum) being transmitted as larvae inside the egg.
on a pasture, where animals had been fed sup- One major task in the future will be to test the
plement containing D. jlagrans chlamydospores, effect of D.3agran.s when BC is integrated in differ-
were significantly lower compared to those of tra- ent integrated parasite control strategies. If we look
cers on untreated, control pasture. Results from at some of the other potential elements in an inte-
an unpublished study where the fungus was tested grated control strategy, then much progress has
against 0. dentatum larvae in faecal cultures, also been made towards novel and restricted use of
showed that diet might have some influence on the anthelmintics, exploitation of resistant animals, as
development of the parasite larvae, but not on the well as documented positive effects of implementing
high nematode-reducing activity of the fungus. various grazing managements. In traditional ani-
mal production systems, it should be possible for
BC to play a part to further reduce or, perhaps in
4. Conclusion and future outlook periods of a grazing season, eliminate the use of
anthelmintics. On organic farms, where medication
Today, substantial evidence supports the use of is strictly limited to curative use, BC would be
D. jagrans as a BC agent against the free-living expected to play a bigger role. In both systems,
larval stages of many of the most important animal diet may also influence the level of parasitism and
parasitic nematodes. The bulk of the work per- deserves further attention.
formed has been in temperate climates and there- The effect of using a cocktail of fungal biological
fore further work is needed to investigate the control agents with different mechanisms of action
efficacy of the fungus against parasites like H. con- as well as requirements for growth and survival will
tortus in subtropical/tropical environments. Fur- be one of the areas of focused attention. Irrespective
ther research is needed to confirm initial findings of use of just one pure species, or a cocktail of
on the effect of D.,flagrans on some of the parasitic species, yet another important task ahead is to
144 M. Lars~r~ll~~terrtational Journrrl,fbr Purasitology 29 (1999) 139%146

understand and monitor impact of the fungal ruminants without the recourse to anthelmintics:
approaches, experiences and prospects. Int J Parasitol
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