Content uploaded by Naresh Magan
Author content
All content in this area was uploaded by Naresh Magan on Dec 29, 2017
Content may be subject to copyright.
European Journal of Plant Pathology 109: 723–730, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
Post-harvest fungal ecology: Impact of fungal growth and
mycotoxin accumulation in stored grain
Naresh Magan, Russell Hope, Victoria Cairns and David Aldred
Applied Mycology Group, Biotechnology Centre, Cranfield University, Silsoe, Bedford MK45 5DT, UK
(Fax: +44 1525 863540; E-mail: n.magan@cranfield.ac.uk)
Key words: ecology, biotic, abiotic factors, fungal interactions, niche occupation, mycotoxins, insects
Abstract
Grain quality after harvest is influenced by a wide variety of abiotic and biotic factors and has been studied as
a stored grain ecosystem. Important factors include grain and contaminant mould respiration, insects and mites,
and the key environmental factors of water availability and temperature. Interactions between these factors influ-
ence the dominance of fungi, particularly mycotoxigenic species. Studies have shown that growth, mycotoxin
production, competitiveness and niche occupation by mycotoxigenic species are influenced by the presence of
other contaminant moulds and environmental factors. This has been demonstrated for both Fusarium culmorum
and deoxynivalenol production, Aspergillus ochraceus/Penicillium verruscosum and ochratoxin production and
Fusarium section Liseola and fumonisin production. Interactions between mycotoxigenic spoilage fungi and insects
do occur but have not been studied thoroughly. Some insects disseminate mycotoxigenic species, others are known
to use spoilage moulds as a food source, while others avoid certain fungal species. Thus, a more holistic eco-
logical view is needed when considering management approaches to long-term-safe storage of cereal grains after
harvest.
Stored grain as an ecosystem
Grain entering store carries a wide range of microor-
ganisms including bacteria, yeasts and filamentous
fungi, the population structure being dependent on field
climatic conditions and harvesting processes (Magan
and Lacey, 1986; Lacey and Magan, 1991). Poor post-
harvest management can lead to rapid deterioration in
grain quality, severely decreasing germinability and
nutritional value of stored grain. Fungal activity can
cause undesirable effects in grain including discoloura-
tion, contribute to heating and losses in nutritional
value, produce off-odours, losses in germination, dete-
rioration in baking and milling quality, and can result
in contamination with mycotoxins.
Wallace and Sinha (1981) were the first to con-
sider stored grain as a man-made ecosystem and use
multivariate statistics to examine the complex inter-
actions between abiotic and biotic factors to identify
key parameters for safe storage. They believed that
unless this more holistic and ecological approach was
adopted it was not possible to understand the processes
occurring and thus improve post-harvest management
of stored grain. Factors such as grain type and quality,
fungal population and community structure, mycotoxin
production and pest infestation were all interlinked
(Figure 1). The key environmental factors of tempera-
ture, water availability and gas composition influence
both the rate of fungal spoilage and the production of
mycotoxins.
Generally, provided grain is stored at a moisture
content equivalent to ≤0.70 water activity (aw) then
no spoilage will occur. However, since grain is often
traded on a wet weight basis, inefficient drying systems
can lead to fungal activity and concomitant myco-
toxin production which renders grain useless for food
or feed. During initial storage, fungal inoculum can
become redistributed in grain. Mechanical damage is
also conducive to entry of spoilage fungi in insuffi-
ciently dried grain. It must also be remembered that
724
Figure 1. Diagrammatic representation of interactions between
biotic and abiotic factors in stored grain ecosystems (adapted from
Sinha, 1995).
stored grain ecosystems offer an excellent but finite
nutritional substrate for spoilage fungi.
Ecological considerations of interactions
between spoilage fungi post-harvest
Fungi seldom occur on grains in isolation, but usu-
ally as a mixed consortium of bacteria, yeasts and
filamentous fungi. It is thus inevitable that interspe-
cific and intraspecific interactions will occur depend-
ing on the nutritional status of the grain and the
prevailing environmental conditions. Indeed, envi-
ronmental factors may exert a selective pressure
influencing community structure and dominance of
individual species, especially mycotoxigenic species.
Figure 2 shows the effect of awon respiration of sin-
gle spoilage fungi (e.g. Eurotium amstelodami and
Penicillium aurantiogriseum) when grown individually
or co-inoculated on wheat grain using an automated
electrolytic respirometer system (Willcock and Magan,
2001). Respiration of co-inoculated species was less
than additive especially at intermediate awconditions
after 7 days. After 14 days, patterns changed again
when total O2utilisation was considered (Hamer and
Magan, unpublished data). This is indicative of com-
petition between species. The situation becomes even
more complex when a mixture of species colonising
cereal substrates is considered.
From an ecophysiological point of view, it has to be
remembered that spoilage fungi colonising grain use
different primary and secondary strategies to occupy
the niche. They may have combative (C-selected),
Figure 2. Measurement of the total respiratory activity of
E. amstelodami (Ea), P. auratiogriseum (Pa) or a mixture of
the two (mixture) at 0.85 and 0.90 water activity after 7 and
14 days incubation (Magan, unpublished data). Bar indicates least
significant difference (P=0.05) between treatments.
stress (S-selected) or ruderal (R-selected) strategies or
merged secondary strategies (C–R, S–R, C–S, C–S–R;
Cooke and Whipps, 1993). Primary resource capture
of grain is influenced by the germination rate, growth
rate, enzyme production and the capacity for sporula-
tion. Subsequent interactions between spoilage fungi
result in combat, antagonism and niche overlap which
all influence secondary resource capture.
We will consider two approaches which have been
used to understand the type of interactions which occur
between fungi under different environmental regimes
in grain to enable better prediction of not just domi-
nance by key spoilage fungi, but also the potential for
production of mycotoxins. Magan and Lacey (1984,
1985) used categories of mutual intermingling (1/1),
antagonism (2/2; 3/3) on contact or at a distance
respectively, and dominance on contact or at a dis-
tance (4/0; 5/0). By giving a higher numerical score
to fungi able to dominate in vitro rather than antago-
nism and adding the scores for each species, an Index
of Dominance (ID) was developed to assist with inter-
preting patterns of colonisation and dominance in grain
ecosystems. The IDwas found to significantly change
with awand temperature, and with grain substrate.
Of 15 species, the most competitive species in wheat
grain in the United Kingdom were P. brevicompactum,
725
P. hordei,P. roqueforti,Aspergillus fumigatus and
A. nidulans. Decreasing the awled to conditions
increased competitiveness of P. brevicompactum. Only
Fusarium culmorum could compete with storage
moulds, at >0.93–0.95 aw. Interestingly, the rate of
growth was not related to dominance. Previously,
studies by Ayerst (1969) had suggested that speed
of germination and growth were key determinants
of colonisation of nutrient-rich matrices, such as
grain.
Table 1 shows the effect of interactions between
a mycotoxigenic strain of F. culmorum and other
species in relation to water availability on wheat
grain using the IDscoring system. It is interesting to
note that F. graminearum is more competitive than
F. culmorum, regardless of temperature or water avail-
ability. F. culmorum is, however, dominant against
Table 1.F. culmorum interaction and IDdetermined after 30 day
incubation at 15 or 25 ◦C on irradiated wheat grain adjusted to
different awlevels (Hope and Magan, unpublished data)
awSpeciesaTemperature ID
15 ◦C25
◦C
0.995 F.c: F.g 0b/4c0/4 0/8
F.c: F.p 2/2 1/1 3/3
F.c: A.t 4/0 4/0 8/0
F.c: C.h 4/0 4/0 8/0
F.c: M.n 2/2 4/0 6/2
F.c: M.m 2/2 4/0 6/2
F.c: P.v 4/0 2/2 6/2
ID16/10 19/7 35/17
0.955 F.c: F.g 0/4 0/4 0/8
F.c: F.p 0/4 2/2 2/6
F.c: A.t 4/0 4/0 8/0
F.c: C.h 4/0 4/0 8/0
F.c: M.n 4/0 4/0 8/0
F.c: M.m 0/4 4/0 4/4
F.c: P.v 2/2 4/0 6/2
ID14/14 20/6 34/20
aF.c., Fusarium culmorum; F.g., Fusarium graminearum; F.p.,
Fusarium paoe; A.t., Alternaria tenuissima; C.h., Cladosporium
herbarum; M.n., Microdochium nivale; M.m; M. nivale var.
majus; P.v., Penicillium verrucosum.
bRefers to interaction score for first species only.
cRefers to interaction score for second species only.
IDrefers to total addition of scores for an individual species com-
peting with a range of other species based on the interaction scores
for each species of 1 : 1 (mutual intermingling), 2 : 2 (mutual
antagonism on contact), 3 : 3 (mutual antagonism at a distance),
4 :0 (first species dominant over the other on contact), 5 : 0 (first
species dominant at a distance over the other; from Magan and
Lacey, 1984).
other grain fungi including Microdochium nivale.
This is indicative of why F. culmorum has become such
an important pre- and post-harvest pathogen of temper-
ate cereals and also indicates that F. graminearum is
more competitive when both colonise grain. Thus inter-
actions can change with different abiotic factors and
with interacting species. Table 2 gives an example for
an ochratoxin (OTA)-producing strain of A. ochraceus
and other species, both in vitro and on maize grain at
two different temperatures. A. ochraceus is domi-
nant against A. candidus and A. flavus at 18 ◦C, but
not against the latter at 30 ◦Cin situ.
More recently, alternative approaches were utilised
to understand the relative competitiveness of different
species within fungal communities colonising grain.
Wilson and Lindow (1994a,b), working with bio-
control systems, suggested that the co-existence of
microorganisms particularly on plant surfaces may be
mediated by nutritional resource partitioning. Thus
in vitro carbon utilisation patterns (Niche size) could
be used to determine Niche overlap indices (NOI)
and thus the level of ecological similarity. Based on
the ratio of the number of similar C-sources utilised
and those unique to an individual isolate or species,
a value between 0 and 1 was obtained. NOI of >0.9
were indicative of co-existence between species in an
ecological niche, while scores of <0.9 represented
occupation of separate niches. This approach was mod-
ified by Marin et al. (1998a) and Lee and Magan
(1999) for a multifactorial approach by including
water availability and temperature into the system.
This demonstrated that based on utilisation of maize
C-sources, the NOIs for fumonisin-producing strains
of F. verticillioides and F. proliferatum were >0.90 at
>0.96 awat 25 and 30 ◦C, indicative of co-existence
with other fungi such as Penicillium species, A. flavus
and A. ochraceus. However, for some species, pairing
with F. verticillioides resulted in NOI values <0.80
indicating occupation of different niches. Figure 3
shows a diagrammatic example of the impact that envi-
ronmental factors and interaction have on Niche size
and NOI for A. ochraceus against Alternaria alternata.
This shows how interactions may change with environ-
ment. Table 3 shows results for interactions between an
OTA-producing P. verrucosum strain and a Eurotioum
species at 15 and 25 ◦C. These results suggest that
Niche overlap is in a state of flux and significantly
influenced by both temperature and water availabil-
ity. Nutrient status is very important. Lee and Magan
(1999) demonstrated that comparison of C-sources in a
standard BIOLOG test plate (95 carbon sources) with
726
Table 2.In vitro and in situ interaction scores and IDbetween A. ochraceus and other
species in relation to environmental factors (adapted from Lee and Magan, 2000a,b)
awSpeciesaIn vitro In situ
18 ◦C30
◦C18
◦C30
◦C
0.95 A. ochraceus :A. candidus 4b/0c5/0 4/0 4/0
A. ochraceus :A. flavus 4/0 4/0 4/0 0/4
A. ochraceus :A. niger 4/0 0/4 0/4 0/4
A. ochraceus :E. amstelodami 2/2 2/2 0/4 0/4
Index of Dominanced14/2 11/6 8/8 4/12
aInteracting fungal species.
bRefers to interaction score for A. ochraceus only.
cRefers to interaction score for interacting species only.
dRefers to total addition of scores for an individual species competing with a range of
other species based on the interaction scores for each species of 1 :1 (mutual intermin-
gling), 2 : 2 (mutual antagonism on contact), 3 : 3 (mutual antagonism at a distance),
4 :0 (first species dominant over the other on contact), 5 : 0 (first species dominant at a
distance over the other; from Magan and Lacey, 1984).
Figure 3. Diagrammatic representation of the Niche size and
NOI for A. ochraceus when interacting with A. alternata at
different temperatures and water activity levels (adapted from
Lee and Magan, 1999). aNumber of C-sources utilised out
of 95; NOIoch, number of C-sources in common divided by
total number utilised by A. ochraceus; NOIstr, number of C-
sources utilised in common divided by the number utilised by
A. alternata.
those only relevant to maize grain (18 carbon sources)
gave very different results in terms of Niche size and
NOI under different environmental conditions. This
approach confirms that interactions and dominance are
dynamic, not static, and emphasises the importance
of taking account of such fluxes in any integrated
approach to understanding and controlling the activity
of mycotoxigenic spoilage moulds in the stored grain
ecosystem.
Table 3. Example of impact of environmental factors on Niche
size and NOI between P. verrucosum and other spoilage fungi
(Cairns and Magan, unpublished data)
Water activity 0.995 0.93
Niche NOIPv/ Niche NOIPv/
sizeaNOISp size NOISp
15 ◦C
P. verrucosum 92 74
A. ochraceus 71 0.71/0.92 52 0.50/0.74
F. culmorum 90 0.88/0.92 63 0.58/0.74
P. aurantiogriseum 90 0.78/0.92 75 0.69/0.74
25 ◦C
P. verrucosum 85 69
A. ochraceus 88 0.84/0.85 63 0.55/0.69
F. culmorum 89 0.82/0.85 51 0.45/0.69
P. aurantiogriseum 74 0.84/0.85 64 0.59/0.60
aNiche size, the total number of carbon sources utilised by a
species based on Biolog GN plate of 95 Carbon sources.
NOIpv, total number of carbon sources utilised in common divided
by the total number utilised by P. verrucosum only, under each
set of conditions.
NOIsp, total number of carbon sources utilised in common,
divided by the total utilised by the competitor, under each set of
conditions.
Effect of interactions on growth and
mycotoxin production
Figure 4 shows effects of fungal interactions and awon
growth of F. culmorum on layers of irradiated wheat
grain at two different awlevels. The results show that
when interacting with some species, e.g. M. nivale or
727
Figure 4. Effect of environmental factors on relative growth (diametric extension±SE) of F. culmorum when paired with other interacting
fungi on wheat grain at 0.995 and 0.955 water activities and 25 ◦C. Growth rates are means of five replicates per treatment. Key to fungi:
F.c., Fusarium culmorum; F.g., Fusarium graminearum; F.p., Fusarium paoe; A.t., Alternaria tenuissima; C.h., Cladosporium herbarum;
M.n., Microdochium nivale; M.m.; M. nivale var. majus; P.v., Penicillium verrucosum (Hope and Magan, unpublished data).
P. verrucosum, growth of F. culmorum is significantly
faster than when growing alone on grain. Similar effects
on growth and on OTA production were observed for
A. ochraceus on maize grain (Lee and Magan, 2000b).
The question arises whether such effects on growth
also influence mycotoxin production in poorly stored
grain. In vitro and in situ studies have previously
suggested that interaction between some species can
result in a significant accumulation of mycotoxins,
while in other cases an inhibition of mycotoxin pro-
duction is observed. For example, interactions between
section Liseola Fusarium species with A. niger resulted
in a tenfold increase in fumonisin production espe-
cially at 0.98 aw, although under drier conditions no
increase in fumonsin occurred on maize grain (Marin
et al., 1998b). Also in maize, A. flavus,A. niger and
E. amsteladami all significantly inhibited OTA produc-
tion by A. ochraceus (Figure 5; Lee and Magan, 2000b).
Recent studies with F. culmorum show that interaction
with M. nivale stimulated DON production on wheat
grain with freely available water (=0.995 aw),
while under drier conditions (0.955 aw) interaction
with A. tenuissima,Cladosporium herbarum and
P. verrucosum reduced DON production (Table 4, Hope
and Magan, unpublished data). OTA production by
P. verrucosum was also influenced by competition with
other spoilage fungi on wheat grain (Table 5).
Relationship between insects and mycotoxin
producing fungi in stored grain
It is important to remember that insect pests are a
common problem in stored grain ecosystems. They
grow and multiply at water availabilities much drier
than those allowing fungal growth. Insects can produce
728
Figure 5. Effect of temperature and water activity on relative ochratoxin production by A. ochraceus when interacting with other fungi on
maize grain at 18 and 30 ◦C when compared to A. ochraceus colonisation alone. Key to fungi: Ao, Aspergillus ochraceus; Ac, Aspergillus
candidus; An, Aspergillus niger;Aa, Alternaria alternata; Ea, Eurotium amstelodami (adapted from Lee and Magan, 2000b). ∗Indicates
significant differences from the control (P=0.05).
Table 4. Effect of interactions between F. culmorum and
other species on deoxynivalenol and nivalenol (ng g−1
grain) production on irradiated wheat grain at two water
activity levels at 25◦C (Hope and Magan, unpublished
data)
Mycotoxin
Deoxynivalenol Nivalenol
Water activity 0.995 0.955 0.995 0.955
F. culmorum 7669 447 289 298
F. culmorum +C. herbarum 634 0 316 412
F. culmorum +A. tenuissima 459 444 0 288
F. culmorum +M. nivale 451 600 868 0
F. culmorum +M. majus 0 440 292 0
F. culmorum +P. verrucosum 3264 450 0 0
LSD (P=0.05): DON =180.5: NIV =123.2.
Key to fungi: F, Fusarium; A, Alternaria;M,Microdochium;
M. majus,M. nivale var. majus;P,Penicillium verrucosum.
metabolic heat which generates water via condensa-
tion on surfaces due to temperature differentials and
develop classic hot spots which can quickly result
in heating and complete spoilage. Pre-harvest insect
infection can lead to increased post-harvest production
of aflatoxin in maize (Sauer et al., 1984).
Some storage insects are disseminators of storage
fungi, while others are exterminators (Sinha, 1971).
Some storage fungi attract insects as food sources
and promote population increases. Some fungi pro-
duce metabolites which repel insects. Indeed, loss in
calorific value is due to the combined effects of spoilage
fungi and insects. These interactions have often been
neglected, although they are important. Physiological
and biochemical similarities between fungi and
early developmental stages of insects mean that
potential exists for combined insecticidal/fungicidal
control.
729
Table 5. Effect of interactions between P. verrucosum and two other mycotoxigenic Fusarium species
(F. culmorum,F. poae) on ochratoxin production (ng g−1±SE) on wheat-based medium under different
water activity and temperature conditions after 56 days incubation
Water activity Temperature (◦C)
15 25
0.99 0.95 0.99 0.95
P. verrucosum alone 3000 ±327 1800 ±645 150 ±36 3600 ±409
P. verrucosum +F. culmorum 010±70 0
P. verrucosum +F. poae 60 200 ±18 0 0
There are no recent studies of interactions between
insects and mycotoxigenic fungi. Dix (1984) found
that Penicillium spp. and A. flavus were associated
with Sitophilus zeamais. As adults they carried a
high density of spores without succumbing to afla-
toxicoses. Earlier Eugenio et al. (1970) showed that
the lesser mealworm and the confused flour beetle
retained zearelenone (ZEA) through metamorphoses
from larvae to adult. Wright (1973) found that neither
ZEA or T-2 toxin produced by F. graminearum and
F. tricinctum, respectively, caused any mortality in the
life-cycle of Tribolium confusum. Since this insect also
feeds on these fungi, it may be a non-propagative vector
or disperser of these fungal metabolites.
Dunkel (1988) carried out elegant studies to exam-
ine the efficacy of different concentrations of OTA,
citrinin, rubratoxin B and patulin on larval weights
and development time of three different insect species
at between 0 and 1000 ppm concentrations. Larval
weight of T. confusum was only significantly affected
by citrinin, rubratoxin B and patulin at 1000 ppm con-
centration, with little effect on adult emergence. Of the
three insect pests examined, only Attagenus megatoma
was significantly affected at 100–1000 ppm of the
mycotoxins. Surprisingly, no studies have been con-
ducted with regard to fumonsins, DON or nivalenol.
Such studies are necessary to evaluate the interactions
which might occur between insect pests and spoilage
moulds in stored grain ecosystems.
Conclusions
The activity of mycotoxigenic fungi in stored
grain must be examined in the context of the
ecosystem as a whole in order to understand the
dominance of certain species under certain environ-
mental conditions. Interactions between these fungi
and other contaminants are complex and are signifi-
cantly affected by the prevailing and changing envi-
ronmental factors. Niche overlap and dominance of
mycotoxigenic species have been shown to fluctuate
with environmental factors. Studies in vitro and in situ
suggest that interactions between toxigenic species and
other spoilage fungi markedly influence mycotoxin
production, with some species stimulating and others
inhibiting production. The role of insect pests should
not be neglected as they may be integrally involved in
the dominance of mycotoxigenic species by helping
in dispersal and acting as vectors and carriers of the
toxin through grain. Overall, conditions in stored grain
are not in a steady state and thus the dynamics of the
system will vary over time. This needs to be taken into
account in determining safe storage times for cereals
without risks of spoilage and mycotoxin contamina-
tion. Any decision support system must take all these
factors into account for the effective development of
good management systems post-harvest.
Acknowledgements
Parts of this research were funded by the European
Commission, Quality of Life and Management of
Living Resources Programme (QOL), Key Action 1 on
Food, Nutrition and Health, Contract Nos. QLK1-CT-
1999-00433 and QLK1-CT-1999-00996.
References
Ayerst G (1969) The effects of moisture and temperature on
growth and spore germination in some fungi. Journal of Stored
Product Research 5: 127–141
Cooke R and Whipps J (1993) Ecophysiology of Fungi.
Blackwell, Oxford
Dix DE (1984) Interactive binomics of the maize weevil,
Sitophilus zeamais Motchulsky, and Aspergillus flavus Link.
Ph.D. Thesis, University of Georgia, Athens, GA, USA,
129 pp
Dunkel F (1988) The relationship of insects to deteriora-
tion of stored grain by fungi. International Journal of Food
Microbiology 7: 227–244
730
Eugenio C, Delas Casas E, Harein PK and Mirocha CJ (1970)
Detection of the mycotoxins F-2 in the confused flour beetle
and the lesser mealworm. Journal of Economic Entomology
63: 412–415
Lacey J and Magan N (1991) Fungi colonising cereal grain:
Their occurrence and water and temperature relationships.
In: Chelkowski J (ed) Cereal Grain – Mycotoxins, Fungi
and Quality in Storage, Chapter 5 (pp 77–118) Elsevier,
Amsterdam
Lee HB and Magan N (1999) Environmental factors and nutri-
tional utlization patterns affect niche overlap indices between
Aspergillus ochraceus and other spoilage fungi. Letters in
Applied Microbiology 28: 300–304
Lee HB and Magan N (2000a) Environmental influences on in
vitro interspecific interactions between A. ochraceus and other
maize spoilage fungi on growth and ochratoxin production.
Mycopathologia 146: 43–47
Lee HB and Magan N (2000b) Impact of environment and inter-
specific interactions between spoilage fungi and Aspergillus
ochraceus and ochratoxin production on maize. International
Journal of Food Microbiology 61: 11–16
Magan N and Lacey J (1984) The effect of water activity, temper-
ature and substrate on interactions between field and storage
fungi. Transactions of the British Mycological Society 82:
83–93
Magan N and Lacey J (1985) Interactions between field and
storage fungi on wheat grain. Transactions of the British
Mycological Society 85: 29–37
Magan N and Lacey J (1986) The phylloplane microbial popula-
tions of wheat and effect of late fungicide applications. Annals
of Applied Biology 109: 117–128
Marin S, Sanchis V, Ramos AG and Magan N (1998a)
Environmental factors, interspecific interactions, and niche
overlap between Fusarium moniliforme and F. proliferatum
and Fusarium graminearum,Aspergillus and Penicillium spp.
isolated from maize Mycological Research 102: 831–837
Marin S, Sanchis V, Rull F, Ramos AJ and Magan N
(1998b) Colonisation of maize grain by F. moniliforme and
F. proliferatum in the presence of competing fungi and their
impact on fumonisin production. Journal of Food Protection
61: 1489–1496
Sauer DB, Storey CL and Walker DE (1984) Fungal populations
in US farming-stored grain and their relationship to moisture,
storage time, regions and insect infestation. Phytopathology
74: 1050–1053
Sinha RN (1971) Fungus as food for some stored product insects.
Journal of Economic Entomology 64: 3–6
Sinha, RN (1995) The stored-grain ecosystem. In: Jayas DS,
White NDG and Muir WE (eds) Stored Grain Ecosystems.
Marcell Dekker, New York, USA
Wallace HAH and Sinha RN (1981) Causal factors oper-
ative in distributional patterns and abundance of fungi:
A multivariate study; In: Wicklow DT and Carroll GC
(eds) The Fungal Community– Its Organisation and
Role in Ecosystems (pp 233–247) Marcell Dekker Inc.,
New York, USA
Willcock J and Magan N (2001) Impact of environmental fac-
tors on fungal respiration and dry matter losses in wheat straw.
Journal of Stored Product Research 37: 35–45
Wilson M and Lindow S (1994a) Coexistence among epiphytic
bacterial populations mediated through nutritional resource
partitioning. Applied and Environmental Microbiology 60:
4468–4477
Wilson M and Lindow S (1994b) Ecological similarity and
co-existence of epiphytic ice-nucleating (Ice+)Pseudomonas
syringae strains and a non-ice nucleating (Ice−) biological
control agent. Applied and Environmental Microbiology 60:
3128–3137
Wright (1973) A model to study the effects of mycotoxins on
insects utilizing Tribolium confusum DuVal and metabolites
of Fusarium species. M.Sc. Thesis, University of Minnesota,
Minneapolis, MN, USA, 70 pp
