Sci. Rep. Kanazawa Univ.
Vol. 60, pp. 1–10, 2016

Fungal defense against mycophagy in milk caps
Ira TASKIRAWATI and Nobuko T UNO⇤
Graduate School of Natural Science and Technology
Kanazawa University, Kanazawa 920-1192, Japan(Received February 9, 2016 and accepted in revised form February 25, 2016)

Abstract Some Basidiomycetes exude latex, but very little is known about the nature offungal latex. In this study, we examined the nature of latex in Lactarius Pers. 1797 spp.
to clarify the role on fungivorous predation. In the field, we compared the degree of predation on taxonomically closely related latex-exuding Lactarius spp. and latex-non-exuding
Russula Pers. 1796 spp. (Russulaceae) at developmental stages of sporocarps. We clarified
that Russula spp. suffered more infestation than did Lactarius spp. at young and maturedevelopmental stages, whereas Lactarius spp. did only at decaying stages. We measured
the amount of latex exuded varied according to developmental stage and sporocarps parts in
Lactarius spp.: mature sporocarps exuded more latex than did younger ones, while decaying
sporocarps exuded the least, and the same patterns were observed at sporocarps parts: theamount of latex was more intense at hymenophore and cap than at stripe. At feeding experiments, three-band garden slugs Ambigolimax valentianus Férussac, 1822 avoided feedingon sporophores of Lactarius spp. when they exuded latex, but fed on them when they did
not. Our observations suggest that fungivores generally escape higher density of the latex at
feeding using signs volatized by sporophores with exuding latex.
Key words.

Lactarius, Russula, mycophagy, slug, latex

Introduction
Fruit bodies of several Lactarius species (Russulaceae; Russulales), i.e., Lactarius volemus,
Lactarius hygrophoroides Berk. & Curt.1859,
Lactarius corrugis Peck 1879, Lactarius akahatsu Nobuj. Tanaka 1890, Lactarius hatsudake Nobuj. Tanaka 1890, and Lactarius laeticolorus, (S. Imai) Imazeki ex Hongo 1960 are
appreciated in Japan, where they are considered to be delicious mushrooms. There are also
pungent tasting species; however, a characteristic common to all species in the genus is thatthey exude milk or latex when the sporocarps⇤ Corresponding author

are damaged. The milk exudes from lactiferous
hyphae distributed under the surface of the entire fruit body. The main content of the milk
in L. volemus has been identified as polyisoprene, which is the same compound found in therubber that exudes from the rubber tree, Hevea
brasiliensis (Ohya et al. 1998).
Several species of rubber trees (Euphorbiaceae: Euphorbiales) that have been planted
to produce rubber are well-known to yield latex
from bruised leaves, although the physiological
function and ecological significance of this phenomenon has been subject to scant study (Lightand Dennis 1989). This phenomenon is not ex-

Email: tuno@staff.kanazawa-u.ac.jp

2

Fungal defense against mycophagy in milk caps

clusive to rubber trees; in angiosperms, 10 % ofplant species (> 20, 000 species among 40 families in multiple lineages) exude latex upon tissue
damage; this latex has no known function in the
primary metabolism (Farrell et al. 1991; Hunter
1994; Lewinsohn 1991). Historically, several
types of evidence have implied that the latex
acts as a potent plant defense against herbivores(Fellows et al. 1986; Hartmann 1991). In thepast two decades, increasing numbers of studies
have emerged on latex, its biochemistry, and its
ecological and evolutionary consequences, withspecial reference made to plant-herbivore interactions (e.g., Konno et al. 2004; Konno et al.
2006; Agrawal and Konno 2009). To date, nostudy has explored the ecological role of latex
in fungal sporocarps during fungi-fungivory interactions. We adapt the comparative ecologicalapproach to clarify the role of latex in Lactarius
spp. on the interaction between the sporocarpsof the genus Lactarius and Russula, mainly due
to that 1) the sporocarps of Lacrarius exudes
latex, whereas those of Russula do not, and 2)
these two genera are taxonomically closely related in family Russulaceae (Miller et al. 2006),
and 3) their habitats are often largely overlappedin a field. Additionally, many characteristic
feeding marks by slugs were often observed on
the Russula sporocarps in a field. However, no
study clarifies the feeding behaviours of slugs
on fungi except for Worthen (1988).
In this study, we examined the animalcommunity, mainly focused on arthropods andslugs, on Lactarius spp. and sympatric Russula
spp. in relation to the developmental stages (i.e.,
young, mature, and decaying stage) of sporocarp in a field. Furthermore we investigated theamount of latex in relation to the developmental
stages and the sporocarp parts (i.e., cap surface,
hymenophore, and stipe). Additionally, we performed feeding experiments using slugs to confirm the role of latex on the fungivorous predation.

Materials and Methods
Field sampling

We collected species of Lactarius and Russula sporocarps in various broad-leaf and coniferous forests (136 330 137 450 E, 36 250
37 180 N, altitude ca. 50 1000m) locatedin Ishikawa and Toyama prefectures of western Japan, from July to November in 2013.
The collected sporocarps were brought back to
the laboratory, in a cool box to avoid desiccation, for further analysis. We recorded fungal species (Ikeda 2005, 2013), developmental
stage (young: cap is undeveloped; mature: cap
is developed; decaying: flesh has started to deteriorate), and the presence of any trace of predation in the respective sporocarps. We also
recorded for feeding marks on the sporocarps in
the field. The round-shaped feeding marks canbe identified by characteristic signs of scraping
by slugs. We collected insects that had gatheredaround sporocarps using an aspirator, with theaid of a hand net, and kept them in ethanol for
identification at the genus or species level (Uenoet al. 1985; Okada and Suzuki 1988; Disney
et al. 2014) under a microscope in the laboratory. Insect specimens that we were unable toidentify were sent to specialists for identification (specialists are named in the Acknowledgements section). To check for the presence of
breeding insects within sporocarps, fungal samples were weighed and placed on moist vermiculite, in containers of an appropriate size, at
23 ± 1 C under 14-h light/10-h dark photoperiod conditions. Each container lid had a holeplugged with cotton wool to ensure adequate air
exchange. The sporophores were misted withwater to maintain sufficiently high humidity.
The containers were checked for emerging insects every 1 or 2 days, for at least 1 month after
sporophore collection. The collected emerged
insects were identified as described above.
Quantification of latex in sporocarps of Lactarius spp.
We quantified the amounts of latex exuded
from three parts of the collected Lactarius
sporocarps: the cap, hymenophore, and stipe.
On each part, we cut a slash (1-cm length, 0.5cm depth, 0.1-mm width) in a flawless section

Ira TASKIRAWATI and Nobuko T UNO

using a blade (FA-10, Feather Safety Razor Co.,
Ltd. Osaka, Japan) to quantify the exuded latex using a microcapillary tube (Accu-Fill 90
Mi-cropet, Clay Adams Co., Ltd., New York,NJ, USA). The angles of the slashes were vertical from top to the bottom (hymenophore) in
the cap, vertical and across at right angles tolamella in the hymenophore, and horizontal in
the stipe (Figure 1). Slashes were made threetimes and exuded latex was averaged in eachpart. We measured exuded latex in the young,mature, and decaying stages of sporophores.

Cap:%ver)cal%cut%

1cm%width,%
5mm%depth,%
0.1mm%

Hymenophore:%ver)cal%cut%
S)pe:%horizontal%cut%

Fig.%1.%%Figure 1. Cut angle in Lactarius sporocarps formeasuring the volume of latex exuded.
Feeding experiments by slugs
To observe their feeding behaviour, we collected wild three-band garden slugs Ambigolimax valentianus Férussac, 1822 (Limacidae,
Stylommatophora, Gastropoda, Mollusca), in
October 2013 from the Kanazawa University
campus. We observed their feeding behaviour
via the following two groups of experiments ina laboratory:

3

Group A: Mature sporocarps of Lactarius akahatsu, L. hatsudake, L. chrysorrheus Fr. 1838
and Russula pseudointegra Arnould & Goris
1907 were collected in October 2013. Two
sporocarps of one of the three Lactarius species
and two of R. pseudointegra were placed individually in plastic petri dishes (four dishes in total, each 9 cm in diameter), which were then laid
equidistantly in a plastic case (35 ⇥ 25 ⇥ 19.5
cm in height) with a plastic mesh ridge to allow air exchange. Five slugs were introduced
and allowed to feed on the sporocarps, and wet
tissue was laid in the bottom of the case to facilitate the slugs movement. This set-up was replicated for each of the three Lactarius species, sothat six Lactarius and six R. pseudointegra were
tested with 15 slugs simultaneously. The cases
were placed in an incubator (22 C, 14 hours
light/10 hours dark), and the slugs’feeding waschecked and recorded every 8 hours, for a totalof nine times over the first 72 hours after introduction.
Group B: The basic set-up was the same as
for Group A, with each of the three Lactarius
species plus R. pseudointegra. However, we
made a 2-cm-wide by 0.5-cm-deep incision into
the cap, hymenophore, and stipe of all Lactarius
sporocarps using a sharp blade to allow latex toooze out.

Results
Arthropod community on Lactarius spp. and
Russula spp.
We collected 300 sporocarps from 30
species in the Russulaceae. Of these, we collected 874 arthropods from 24 of 78 Russula
sporocarps and 45 of 222 Lactarius sporocarps.
Mobile arthropods collected at various stages ofsporocarp maturity and senescence are shownin Table 1. In young sporocarps, we found noarthropod from Lactarius spp. and only fivefrom Russula spp. (Table 1). In mature sporocarps, we again found no arthropods from Lactarius, but collected 279 from Russula (Table 1).
The dominant groups included four species of4

Fungal defense against mycophagy in milk caps

Table 1. Taxonomic groups of arthropods collected from young, mature, and decaying Lactarius(L) and Russula (R) sporocarps in the fieldyoung
Order Family Species
L
R
Blattodea
Coleoptera
Leiodidae
Cyrtusa japonica Champion, 1925
Pseudocolenis strigosulus (Portevin 1905)
Staphylinidae
Acidota crenata (Fabricius 1792)
Atheta weisei Bernhauer 1907
Gyrophaena nipponensis Cameron 1933
Oxyporus sp.
Priochirus japonicus Sharp 1889
DipteraCecidomyiidae
Chironomidae
Chloropidae
Clusiidae
Drosophilidae
Drosophila angularis Okada 1956
Drosophila bizonata Kikkawa & Peng 193
Drosophila brachynephros Okada 1956
Hirtodrosophila sexvittata Okada 1956
Muscidae
Muscina angustifrons (Loew 1858)
1
Mycetophilidae
Exechia arisaemae Sasakawa 1993
1
Otitidae
PhoridaeMegaselia flava (Fallen 1823)
M. gotoi Disney 1989
3
M. kanekoi Disney 1989
M. donaldsonae Disney et al. 2014
Megaselia sp.
Sciaridae
Sphaeroceridae
Hymenoptera
Formicidae
Parasitoidic wasp
Collembora
Hypogastruridae
Ceratophysella cf. horrida
Ceratophysella denisana (Yosii 1956)
Ceratophysella denticulta (Bagnall 1941)
Ceratophysella pilosa (Yosii 1956)
Pseudoscorpionida
Total number of individual
05Number of sporocarps
41 23
Density per sporocarp
0 0.2

matureLR

decaying
L
R
1

22
1
1
3
171
1
1
1
1
1

1

2
3
1
3

27
9
15
6

1
12
15
11
1
5

1
2
1
2
3
1

3

2

2
2
1
1
4

3
3

31
67
101
21
0 279
60 25
0 11.2

23
71
153
2
463
21
22.0

31
22

127
30
4.2

5

Ira TASKIRAWATI and Nobuko T UNO

Table 2. Composition of insects emerged from Lactarius (L) and Russula (R) sporocarps

young
Order Family Species
L
R
DipteraChloropidae
Drosophilidae
Drosophila angularis
D. bizonata
D. brachynephros
D. unispina Okada 1956
Hirtodrosophila alboralis (Momma & Takada 1954)
H. histrioides Okada & Kurokawa 1957
H. sexvittata
Mycodrosophila gratiosa
M. poecilogastra (Loew 1874)
Lonchaeidae
Muscidae
Muscina angustifrons
Mycetophilidae
PhoridaeMegaselia sp.
M. donaldsonae
M. flava
Psychodidae
Sphaeroceridae
TiplidaeHymenoptera
not identified (Parasitoidic wasp)
Total number of individual00Number of sporocarps
41
23
Density per sporocarp
00collembola (78.9% of the 279-individual total), four species of drosophilid (14.0%), fivespecies of phorid (3.2 %), and Muscina angustifrons (Loew, 1858) (1.8%) (Table 1). In
decaying sporocarps, we found 463 arthropods
from Lactarius, dominated by collembola (53.3%) and beetle species (leodids and staphylinids, 43.0 %), while 127 were collected from
Russula, dominated by drosophilids (44.9 %),collembola (41.7 %), and phorids (6.3 %) (Table1). Larval species composition is represented as emerged adults, and summarised inTable 2. Mycophagous dipteran larvae normally grow within the sporocarp until emergence. Therefore, insect fauna of sporocarp
is characterised by lower mobility. No adultemerged from young sporocarps of either genus(Table 2). In mature Lactarius, M. angus-

matureLR

decaying
L
R
2

1

17
10

104

229

1

1

2
40
6
2
1
296
4
27
23
14

1

30
1

38
1

2
2
5
2
7

133
60
2.2

230
25
9.2

2
466
21
22.2

3
1

1

5

52
30
1.7

tifrons was most abundant (78.2 % of 133 individuals) followed by Hirtodrosophila histrioides Okada & Kurokawa 1957 (12.8 %) andMycodrosophila gratiosa (Meijere 1911) (7.5%), while M. angustifrons dominated in Russula(99.6 % of 230 individuals). Diverse dipteraninsects (eight families, nine drosophilid species,
and three Megaselia spp.) emerged from decaying Lactarius, of which drosophilids (86.1% of 466 individuals) and M. angustifrons (6.4%) were most abundant, while in Russula, lessdiverse diptera (six families, four drosophilid
species, and one Megaselia sp.) emerged andwere dominated by M. angustifrons (73.1 % of
52 individuals). Sporocarps of the two generawith all types of feeding marks and with onlyslug-derived marks are summarised in Table 3.
We found no feeding marks in young sporocarps

6

Fungal defense against mycophagy in milk caps

3. Percentage
of Lactarius(L)(L)andand Russula
Russula (R)withanimalfeeding
Table Table
3. Percentage(%)(%)of Lactarius(R)sporocarps
sporocarps
withanimalfeeding marks
marks
(all
kinds
of
animalor
slugs
alone)
intheyoung,
mature,anddecaying
stages.
(all kinds of animal or slugs alone) in the young, mature, and decaying stages.
developing stage
Number of sporocarp

young
L

R

14

6

mature
P

L

R

200

decaying
P

L

R

44

73

56

P

All kind of feeding mark 22% 50%

NS

9%50% <0.01

32%

68%

<0.01

Feeding marks of slugNS3%

21% <0.01

18%

43%

<0.01

0%

0%

Table 4. Amount of latex exuding from caps, hymenophores, and stipes in the Lactarius species
Table 4. Amount of latex exuding from caps, hymenophores, and stipes in the Lactarius species sampled.
sampled
Mean±SE (!l)

speciesNumber of
sporocarp

Cap

Hymenophore

Stipe

Lactarius akahatsu Nobuj. Tanaka 189060.10±0.00

0.10±0.00

0.10±0.00

L. chrysorrheus Fr. 183876.86±2.38

16.86±4.70

3.79±1.75

L. lividatusBerk. & M.A. Curtis 18603

0.10±0.00

0.10±0.00

0.100±0.00

L. subvellereus Peck 1898

1

1

1

2

L. piperatus (L.) Pers. 17973

2.33±0.88

4.67±0.67

1.00±0.58

L. quietus (Fr.) Fr. 183828

1.81±0.56

5.53±1.37

1.19±0.47

L. subpiperatusHongo 196412

3.28±1.55

3.87±1.55

1.45±0.60

L. volemus(Fr.) Fr. 1838118

10.16±1.31

18.39±1.99

7.59±1.32

Lactarius sp.1

1

5

17

0

Lactarius sp.2

2

0

0.05

0

of either genus (Table 3). In mature and decaying sporocarps, we found fewer feeding marks
in Lactarius for all animals and for slugs alone(Fishers exact test for no. of sporocarps withmarks, P < 0.01, Table 3).
Quantification of latex
We quantified the exuded latex of 181 sporocarps from 10 species (Table 4). In general,hymenophores exuded the most latex among
the three parts incised (Table 4). We statistically compared the volume of latex in reference
to the sporocarp only for the two most abundant species, L. volemus and L. quietus. Latex volumes varied among sporocarps depend-ing on environment, and we expressed the volumes as proportions of the volume of latex fromthe stipe to that from the respective sporocarp(Fig. 2A). We found a significant differencein latex volume among parts of mature sporocarps, wherein hymenophores exuded the most,
followed by caps, and finally stipes (N = 64,
Kurskal-Wallis nonparametric test with SteelDwass test, P < 0.05, Fig. 2A) in L. volemus.
Hymenophores exuded more latex than stipes inmature L. quietus (N = 13, P < 0.05, Fig. 2A).
In L. volemus, more latex was exuded from hymenophores in mature and young stages than in
the decaying stage (N = 119, P < 0.05, Fig. 2B).

7

Ira TASKIRAWATI and Nobuko T UNO

      

A.#Lactarius)volemus)(pale#bar)#and#L.)
quietus)(dark#bar),#mature#stage
9"
8"

A

7"
6"

B

5"
4"
3"

ab

2"
1"

C

b

0"
Cap"

20"

S0pe"

Hymenophore"

B.#Lactarius)volemus,)hymenophore
A

18"

A

16"

  

a

14"
12"
10"
8"

B

6"
4"
2"
0"
young"

mature"decaying"

Figure 2. Comparative latex volume in different parts of mature Lactarius volemus and L. quietus(Fr.) Fr. Fig."21838 (2A) and different developmental stages in L. volemus hymenophores (2B). Different letters indicate statistical significance (P < 0.05) in respective species between different parts
or different developmental stages.

Feeding experiments by slugs
Group A: All Lactarius species exuded latex
within 16 hours of feeding by slugs and were
not fed on again for at least 48 hours. One L.
hatsudake that stopped exuding after 64 hours
was later fed on by one slug in the stipe (at 64
hours) and a further two slugs in the stipe andhymenophore (at 72 hours). Five sporocarps –the other L. hatsudake, two L. akahatsu, and two
L. chrysorrheus – were not fed on after the first
feeding and were still exuding at the end of observations, 72 hours later. Contrary, all six R.
pseudointegra were fed on by at least one offive slugs (two slugs in one case) over the threedays. Feeding marks were observed on every
part of the sporocarp: hymenophore, cap, andstipe. All R. pseudointegra appeared to be in
the mature stage without desiccating or decaying by the end of observation.
Group B: All sporocarps were incised to makethe Lactarius exude before exposure to slugs.
All but two Lactarius were free from feeding
marks for 72 hours, and were still exuding 72
hours later. One L. akahatsu was fed on, andone L. chrysorrheus had gained marks in thestipe at 64 hours and in the hymenophore at 72

8

Fungal defense against mycophagy in milk caps

hours. Due to desiccation, neither was exuding latex at the end of observations. All six R.
pseudointegra had feeding marks on their hymenophores, caps, and stipes. All R. pseudointegra appeared to be in the mature stage without
desiccation or decay by the end of the observation period.

Discussion
We found less infestation in Lactarius sporocarps than in sympatric Russula, another member of the Russulaceae. In field observations, wefound few arthropods visiting mature Lactarius
sporocarps. The lack of arthropods visiting or
emerging from the young stages of both Lactarius and Russula may be due to the relatively
short exposure time, or some type of repellent
effect. While few or no arthropods visited or
emerged from mature Lactarius, many collembola and flies visited mature Russula. By contrast, we found more collembola and beetles
on, and more diverse flies emerging from, decaying Lactarius. These differences could be
due to physical features: most decaying Lactarius sporocarps were dry, whereas most decaying Russula ones were sludgy inside andmisshapen. Because collembola and beetles
feed mainly on surfaces, the most abundantgroup on decaying Lactarius sporocarps wasbeetles, whose mandibles enable them to scrape
the desiccated surfaces of the sporocarps. The
most abundant among larvae were a diverse
group comprising Hirtodrosophila and Mycodrosophila spp. These two genera are known
to feed and breed more on the comparatively
hard sporocarps of the Pleurotaceae and Polyporaceae than other mycophagous drosophilids(Tuno 1998, 1999, 2001; Toda et al. 1999;
Takahashi et al. 2005). Interestingly, themost common species in mature and decaying
Russula was Muscina angustifrons (Muscidae,
Diptera), an opportunistic predatory species that
feeds on dipteran larvae within the same sporocarp (Akaishi and Nakamura 2015). Perhaps
this predator prefers laying eggs on Russula
over Lactarius, and this difference may con-tribute to the diverse and abundant dipteran flies
emerging from decaying Lactarius sporocarps.
In this study, the ratio of wild sporocarps
with feeding marks was also significantly lower
in mature and decaying stages of Lactarius but
was not significant in the immature stage withrespect to feeding marks caused by all animals,
or by slugs alone. Latex oozing was generally
higher in the young and mature stages than in
the decaying stage for all species, and in hymenophores and caps than in stipes. Our predation avoidance by latex hypothesis predicts
that latex abundance may vary among mature
stages and fruit body parts in a manner consistent with relative contribution to fitness. For example, fruit bodies of Amanita muscaria (L.)
Lam. (1783) contain ibotenic acid which islethal to flies. The highest concentration of
ibotenic acid was detected in the caps that produce spores in the immature stages (Tsunoda etal. 1993). Similar result of amanitin has beenreported in lethal mushroom, Amanita exitialis
Yang and Li 2001 (Hu et al. 2012). Theseobservations suggest that lethal toxins are produced selectively and distributed specifically in
the immature stages and in the caps as a defense
against predation. That more latex oozing wasobserved in the young and mature stages, and in
hymenophores and caps, is consistent with the
predation avoidance hypothesis.
In feeding experiments, it was clear thatslugs, Ambigolimax valentianus, avoided feeding on Lactarius sporocarps when they exuded latex. Thus, milk caps apparently receive slug predation only when they are intact
or degraded but not exuding latex. To thisend, we have rarely come across flies around
Lactarius species in the field, though we haveseen many gathered around sympatric Russula
sporocarps. Therefore, we assume that Lactarius spp. release volatiles that repel a wide rangeof arthropods and slugs when they are exuding. Various mushroom-characteristic volatiles,
such as 1-octen-3-ol and lenthionine, are known
to science (Maga 1981). It has been reported
that 1-octen-3-ol is increasingly released upontissue damage to sporocarps, and repels slugs

Ira TASKIRAWATI and Nobuko T UNO

and collembola (Sawahata et al. 2008; Woodet al. 2001). Though volatiles have beenreported in some Lactarius species (Pyysalo
1976), we have not detected their characteristic strong odour in the field or in the laboratory. Poly-isoprene, the main constituentof L. volmes emulsion, initiates a condensation reaction when in contact with air, releasing volatiles such as lactone (Morand 1977).
As this condensation reaction progresses polyisoprene indurates, and the sporocarp hardens.
Therefore, old and hard sporocarps will not release volatiles of sub-products of the condensation reaction. Further biochemical studies areneeded to test our hypothesis: we must identify
volatile variation relating to sporocarp development and bioassay them to determine their ecological functions against diverse mycophagous
animals.

Acknowledgements
We deeply thank Drs. Kenkichi Kanmiya,
Jostein Kjaerandsen, Hiromu Kurahashi, andTaizo Nakamori for their supports for the insect
identification.

References
Akaishi D and Nakamura K. 2015. Omnivorous and predaceous larval habits of Muscina angustifrons (Loew)(Diptera, Muscidae). Med Entomol Zool 56: 195-199.
Agrawal A and Konno K. 2009. Latex: a model for understanding mechanisms, ecology, and evolution of plant
defense against herbivory. Ann Rev Ecol Evol Syst 40:
311-331.
Disney RHL, Nitta M, Kobayashi M, Tuno N. 2014.
New records of Megaselia (Diptera: Phoridae) reared
from fungus sporophores in Japan, including five new
species. Appl Entomol Zool 49: 541-552.
Farrell BD, Dussourd DE, Mitter C. 1991. Escalation ofplant defense: Do latex and resin canals spur plant diversification. Am Nat 138: 881-900.
Fellows LE, Kite GC, Nash RJ, Bell EA. 1986. Polyhydroxy plant alkaloid as glycosidase inhibitors andtheir possible ecological role. In: Green MB and
Hedin PA (eds) Natural Resistance of plants to pests,
ACS Symposium Ser 296: 72-78, American Chemical
Society, Washington DC.
Hartmann T. 1991. Alkaloids. In: Rosenthal GA andBerenbausm MR (eds) Herbivores: their interaction

9with secondary plant metabolites Vol I, The chemical
participants, 2nd ed, pp 33-85. Academic Press, San
Diego.
Hu JS, Zhang P, Zeng J, Chen ZH. 2012. Determination of
amatoxins in different tissues and development stagesof Amanita exitialis. J Sci Food Agri 92: 2664-2667.
Hunter J. 1994. Reconsidering the functions of latex.
Trees-Struct Funct 9: 1-5.
Ikeda Y. 2005. Mushroom in Hokuriku area. Hashimotokakubundo Publishing Co. Ltd, Kanazawa (inJapanese).
Ikeda Y. 2013. New edition of Mushroom in Hokuriku
area. Hashimoto kakubundo Publishing Co Ltd,
Kanazawa (in Japanese).
Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura
Y, Hattori M, Kohno K. 2004. Papain protects papaya
trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37: 370-378.
Konno K, Ono H, Nakamura M, Tateishi K, Hirayama
C, Tamura Y, Kohno K. 2006. Mulberry latex rich inantidiabetic sugar-mimic alkaloids forces dieting on
caterpillars. Proc Nat Acad Sci USA 103: 1337-1341.
Lewinsohn TM. 1991. The geographical distribution ofplant latex. Chemoecology 2: 64 – 68.
Light DR and Dennis MS. 1989. Purification of a prenyltransferase that elongates cis-polyisoprene rubberfrom the latex of Hevea brasiliensis. J Biol Chem 264:
18589-18597.
Maga JA. 1981. Mushroom flavor. J Agri Food Chem 29:
1-4.
Miller SL, Larssen E., Larsson K-H, Verbeken A, Nuytinck J. 1981. Perspective in the new Russulales. Mycologia 98: 960-970.
Morand JL. 1977. Chain scission in the oxidation of polyisoprene. Rub Chem Tech 50: 373-396.
Ohya N, Takizawa J, Kawahara S, Tanaka Y. 1998. Molecular weight distribution of polyisoprene from Lactarius volemus. Phytochem 48: 781-786.
Okada T and Suzuki K. 1988. Selected Papers by Dr. Toyohi Okada, 1936-1988. Published by The associationof the memorial issue of Dr. Toyohi Okada, Toyama(in Japanese).
Pyysalo H. 1976. Identification of volatile compounds inseven edible fresh mushrooms. Acta Chem Scand B
30: 235-244.
Sawahata T, Shimano S, Suzuki M. 2008. Tricholoma matsutake 1-Ocen-3-ol and methyl cinnamate repel mycophagous Proisotoma minuta (Collembola: Insecta).
Mycorrhiza 18: 111-114.
Takahashi KH, Tuno N, Kagaya T. 2005. The relative importance of spatial aggregation and resource partitioning on the coexistence of mycophagous insects. Oikos
109: 125-134.
Toda MJ, Kimura MT, Tuno N. 1999. Coexistence mechanisms of mycophagous drosophilids on multi-species
fungal hosts: Aggregation and resource partitioning. J
Anim Ecol 68: 794-803.
Tsunoda K, Inoue N, Aoyagi Y, Sugahara T. 1993.

10

Fungal defense against mycophagy in milk caps

Changes in concentration of ibotenic acid and muscimol in the fruit body of Amanita muscaria during the
reproduction stage. Food hygienic studies of toxigenic
basidiomycotina II 34: 18-24.
Tuno N. 1998. Spore dispersal of Dictyophora fungi (Phallaceae) by Flies. Ecol Res 13: 7-15.
Tuno N. 1999. Insects feeding on spores of a bracket fungus, Elfvingia appalata (Pers.) Karst. (Ganodermataceae, Aphyllophorales). Ecol Res 14: 97-103.

Tuno N. 2001. Community structure of mycophagous insect assembly in Kyoto, Japan. Jpn J Ecol 51: 73-86(in Japanese).
Ueno S, Kurosawa Y, Sato M. 1985. The Coleoptera inJapan in color Vol. 2. Hoikusha Publishing Co Ltd,
Osaka (in Japanese).
Wood WF, Archer CL, Largent DL. 2001. 1-Octen-3-ol, abanana slug x antifeedant from mushrooms. Biochem
Syst Ecol 29: 531-533.