Ecological Research (1998) 13, 7±15
Spore dispersal of Dictyophora fungi (Phallaceae)
by ¯ies
NOBUKO TUNO*
Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, 606-01, Kitasirakawa
Oiwake, Sakyou-ku, Kyoto, Japan
The composition and food habits of insects visiting fungi of two Dictyophora species, D. indusiata (Vent.
& Pers.) and D. duplicata Fisch, were examined in Furano, northern Japan, and in Kyoto, central Japan.
As well as ®eld work being carried out, the quantity and the viability of spores in the recta of
drosophilid and muscid ¯ies were examined in vitro. Although the composition of insects varied locally
and temporally, most of the insects were observed to feed on gleba, which contains spores. Among the
insect assemblies, a few insects were specialized for mycophagy but most were secondarily or not at all
mycophagous. Although Dictyophora-feeders rarely attached the spores on their body surfaces, they
contained a quantity of spores in their gut, which was estimated to be about 35 000±240 000 for
drosophilids and about 1.7 million for muscids. Those spores showed high germination rates, which
were not signi®cantly different from the intact spores. Thus, spores of Dictyophora are dispersed as
excrement through the gut of Dictyophora-feeding insects but not as adherers on the insect body.
Key words: Dictyophora; Drosophilidae; mycophagy; Phallaceae; spore-dispersal.
INTRODUCTION
Insect±fungus relationships are a major part of
biological interactions in biological communities
(Crowson 1984; Newton 1984; Pirozynski &
Malloch 1988; Hammond & Lawrence 1989). In
spite of the importance of this relationship,
however, the nature of spore dispersal by insects
still remains poorly explored compared with
pollen dispersal by insects (Pyrozynski & Malloch
1988). To date, some mutualistic associations
between fungi and their insect vectors have been
described, such as cecidomyiid midges with speci®c fungi in ambrosia galls (Bissett & Borkent
1988), wood wasps, some coleopteran beetles or
fungus-growing termites and wood-rotting fungi
(Gilbertson 1984; Beaver 1989; Berryman 1989;
*Present address: Department of Medical Entomology, Institute for Tropical Medicine, Nagasaki
University, 1-12-4 Sakamotomachi, Nagasaki 852,
Japan.
Received 26 March 1997.
Accepted 10 September 1997.
Redfern 1989; Webber & Gibbs 1989; Wood &
Thomas 1989). Moreover, among adult females
of midges and wasps, morphological adaptations
for storing and transporting spores, known as
mycangia (Batra 1963), have developed. These
associations between the fungi and the insect
visitors are characterized as tight and speciesspeci®c ones lasting the entire life history of the
insect. The tight and species-speci®c associations
are certainly biologically interesting; however,
most insect±fungi relationships are diffused and
loose (Hackmann & Meinander 1979; Lacy 1984;
Hanski 1989; Courtney et al. 1990). To understand insect±fungus relationships comprehensively, such diffused and loose relationships are
of critical importance.
The stinkhorn fungi (Phallales) attracts various
insects with its characteristic strong odour
(Ramsbottom 1953; Imazeki & Hongo 1957;
Ogawa 1983; Hanski 1989). The biological process of spore dispersal, however, has been little
uncovered, and there are contradicting views for
the process of spore dispersal: spores of a phalloid fungus are not digested but possibly dispersed through the digestive tract of dipteran ¯ies
8
N. Tuno
(Cobb 1906, quoted in Ramsbottom 1953 and
Hanski 1989; Beppu 1994), whereas Imazeki and
Hongo (1957) and Ogawa (1983) suggested that
insects disperse spores attaching on the body
surface since phalloid spores within gleba are
extremely sticky. However, no further evidence is
available to inform us of the nature of the spore
dispersal process of phalloids.
This paper reports the composition and food
habits of insects visiting fungi of two Dictyophora
species, D. indusiata and D. duplicata. In addition,
as the ®rst step in documenting the process of
spore dispersal by insects, the quantity and the
viability of spores in the rectum of insects were
examined in vitro.
METHODS
Field observation and insect collection
Insect assemblies gathering at sporocarps of
Dictyophora spp. were observed and sampled four
times during 1990±1996: at sporocarps of
D. duplicata in Furano Experimental Forest of the
University of Tokyo, Hokkaido in September
1990, and at those of D. indusiata and D. duplicata
in the Botanical Garden of the Faculty of Science, Kyoto University in July 1991, and in July
and October 1996, respectively (Table 1). In
Furano, D. duplicata occurred at mixed coniferous
and deciduous forest dominated by Abies sachaliensis (Fr. Schmidt) Masters. In Kyoto, the study
Table 1
site is surrounded by human domesticated area.
Dictyophora indusiata occurred at bamboo vegetation, whereas D. duplicata occurred where Camellia
japonica L. dominated, near the bamboo area.
A Dictyophora sporocarp matures at night. A
young sporocarp looks spherical, containing
gleba inside, but a mature one consists of a cap,
stalk and volva. The cap is covered with olive
green mucus and the stalk is spongy and hollow.
Both of them are quite ephemeral, lasting for 1±3
days. Insect assemblies may change as the
sporocarps grow. Among the insect assemblies,
only those gathering at the mature stage of the
sporocarps are the potential spore dispersers.
Thus, observation and collection of insects were
made only at the mature sporocarps having
spores in order to exclude mere consumers or
decomposers, which hardly play a role as spore
dispersers. Insects visiting the sporocarps were
®rst observed for their behavior and then collected with a net and an aspirator. Collection of
all insects present there was usually accomplished
within 15 min. In case there were too many insects to collect all of them, sampling was broken
off at 15 min.
All insects collected were identi®ed at least to
the family level, referring to Ito et al. (1977) and
MacAlpine et al. (1981, 1987) for diptera, and
Kurosawa et al. (1985), Morimoto and Hayasi
(1986) and Ueno et al. (1985) for coleoptera. In
particular, drosophilids were identi®ed to species
referring to Okada (1988) and Grimaldi (1990).
Data of insect samplings from sporocarps of Dictyophora spp.
Abbreviation
F1
K1
K2
K3
Study site
Main vegetation
Furanoa
Mixed coniferous
and deciduous forest
Abies sachalinensis
dominated
D. duplicata
31 Aug. (9:00, 16:00)
Kyotob
Bamboo
Kyotob
Broad-leaved
evergreen forest
Camellia japonica
dominated
D. duplicata
3 July (15:00)
Kyotob
Broad-leaved evergreen
forest
Camellia japonica
dominated
D. duplicata
29 Oct. (9:00, 12:00, 16:00)
4 July
(9:00, 12:00, 16:00)
5 July
(9:00, 12:00, 16:00)
30 Oct (9:00, 12:00, 16:00)
Host species
Date (time) of
sampling
1 Sep. (9:00, 16:00)
D. indusiata
9 July (14:00, 17:00)
10 July
(9:00, 12:00, 17:00)
11 July (8:00, 12:00)
a
Furano Experimental Forest of the University of Tokyo (43°N, 142°E).
University (35°N, 135°E).
b
Botanical Garden of Faculty of Science, Kyoto
Spore dispersal of Dictyophora fungi
The drosophilids were ecologically categorized
into three feeding-habit groups: mycophagous
(M); secondarily mycophagous (MS); and nonmycophagous (S). Here, secondarily mycophagous insects refers to those feeding both on
mushrooms and other materials to various degrees. The feeding habit of drosophilids has been
categorized by several researchers (Okada 1954;
Toda et al. 1972; Kimura 1976; Beppu et al. 1977;
Kimura et al. 1977; Minami et al. 1978). These
categorizations are quite similar but different in
detail. I followed the categorization by Minami
et al. (1978). For the drosophilid species not
categorized by Minami et al. (1978), I followed
Beppu et al. (1977), except for D. sternopleuralis
Okada & Kurokawa. The other drosophilids
(D. albomicans Duda and D. annulipes Duda) and
D. sternopleuralis were categorized based on my
personal observation.
Examination of spores on the body surface
and in the recta of insects and spore viability
At the same time as identi®cation of specimens,
they were examined under a stereomicroscope to
see whether gleba were attached on them.
In order to investigate the possibility that insects disperse Dictyophora spores through their
gut, the following experiment was conducted.
Insect specimens used for this experiment were
collected from sporocarps of D. duplicata that
occurred on 3 July 1996 in the Botanical Garden
of Kyoto University. After collection, the insects
were left in a plastic container supplied with only
a piece of water-containing cotton for 24 h under
the condition of 25°C and 16 h daylight in order
to clean out their gut. Then, a mature sporocarp
of D. duplicata was provided for them in the
container. The insects were allowed to feed on it
for 24 h. After this treatment, the following tests
were applied.
Number of spores contained in the rectum
The specimens were ®rst dipped into 70% ethanol for 10 s to sterilize their bodies, and then
dissected under a stereomicroscope to take out
the recta. The extracted recta were sterilized, only
outside, again with 70% ethanol, and then ground
with 100 ll sterilized water, individually. The
9
homogenized suspension of the rectum was
examined for the density of spores with a hemocytometer. The total number of spores contained
in the rectum was estimated from the density.
Viability of spores in the rectum
The rectal suspension used for the determination
of spore density was also used to examine the
germination ability of spores. Ten microliters of
the rectal suspension was inoculated on PDA
medium (39 g potato-dextrose agar in 1 l distilled
water) in a petri dish (90 mm ´ 15 mm). In addition, the medium was inoculated with a spore
suspension made from the fungus itself as a control, after determining the spore density. Three
replicates were made from each rectal suspension
and the control. All procedures were conducted on
a clean bench to avoid contamination with other
molds. The petri dish was incubated at 25°C in
16 h daylight. Colonies of the fungus that occurred in the cultures were identi®ed by comparing
species-speci®c colony shapes with those in the
control culture. The proportion of germinated
spores in each petri dish was examined with a
hemocytometer 3 and 5 days after incubation,
based only on contamination-free samples.
RESULTS
Insect assemblies visiting Dictyophora
sporocarps
Table 2 summarizes the composition of insect
families captured at Dictyophora sporocarps. Except for a parasitoid wasp, all the insects collected
were observed to feed on the fungus in the following three ways: (i) a few individuals of
Macrodorcus recta (Motschulsky) (Lucidae, Coleoptera) and Onthophagus sp. (Scarabaeidae, Coleoptera) fed on whole sporocarps; (ii) individuals
of Carpophilus sp. and Haptoncus ocularis (Fairmaire) (Nitidulidae, Coleoptera) fed on stems and
caps; and (iii) the rest fed only on gleba. Only the
beetles, which fed on whole sporocarps, were
observed to attach some spores on their body
surfaces. Although the species composition of
Dictyophora visitors varied spatiotemporally, the
Drosophilidae was always predominant (22.2±
85.3%) among assemblies.
10
N. Tuno
Table 2
Composition of insect families captured at sporocarps of Dictyophora spp. in Furano (F1) and Kyoto (K1, K2, K3)
Order
Family
Coleoptera
Nitidulidae
Scaphidiidae
Scarabaeidae
Staphylinidae
Lucidae
Calliphoridae
Cecidomyiidae
Chloropidae
Drosophilidae
Dryomyzidae
Heleomyzidae
Lauxaniidae
Muscidae
Phoridae
Psychodidae
Sciaridae
Sphaeroceridae
Formicidae
Ichneumonidae
Sminthuridae
Diptera
Hymenoptera
Colembora
Spores
Feeding type
On body
Stem
Gleba
Whole
Gleba
Whole
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Gleba
Parasitoid
Gleba
Total number of individuals
Relative proportions of drosophilid species and
their feeding-habit groups are shown in Tables 3
and 4, respectively. Compositions of drosophilid
assemblies were different between Furano and
Kyoto: Drosophila immigrans, D. lutescens, D. auraria
complex and Scaptodrosophila coracina were dominant in Kyoto, but in Furano D. histrio was
dominant. However, it is dif®cult to draw any
conclusion due to the small sample size. By
contrast, the composition of feeding-habit groups
were similar between the two localities, both
being dominated by non-obligate fungivors, MS
and S (99±100%).
Number and viability of spores
in the recta of insects
Insects that fed on the sporocarps of Dictyophora contained a quantity of spores, but no cell
wall fragments were found. These results strongly
suggest that the insects do not digest the spores.
The quantity of spores in the rectum was estimated to be approximately 35 000±240 000 for
drosophilids and approximately 1 680 000 for
No
No
Yes
No
Yes
No
No
No
No
No
No
No
No
No
No
No
No
No
No
No
F1…%†
K1…%†
±
±
±
2.8
±
±
2.8
±
22.2
±
5.6
±
16.7
±
±
±
±
27.7
±
22.2
41.4
0.4
0.9
4.3
±
1.3
0.4
0.4
45.4
±
±
±
1.7
±
±
0.4
0.4
3.0
±
±
36
232
K2…%†
K3…%†
9.6
±
±
±
0.3
±
±
±
76.5
0.3
±
±
1.7
±
1.7
±
0.6
9.0
0.3
±
±
±
±
±
±
±
±
±
85.3
6.9
±
0.9
±
1.7
±
2.6
1.7
0.9
±
±
354
116
muscids (Table 5). Those spores showed high
germination rates if incubated on PDA medium,
approximately 80% on the third day and 90% on
the ®fth day, which were not signi®cantly different from the control. Every combination of
species/sex was also not signi®cantly different
(P > 0.05, post hoc test, ScheffeÂ's F-test).
DISCUSSION
Most of the insects attracted to Dictyophora
sporocarps were observed to feed only on gleba.
Among these insect assemblies, the Drosophilidae was usually a major component, although the
composition of insect families varied locally and
temporally. The drosophilid assemblies were
dominated by the D. immigrans and/or the
D. melanogaster species groups in the study cases in
Kyoto, both of which are known to feed on
basically decayed plants and/or fermented fruit
(Okada 1962; Toda et al. 1972; Beppu et al. 1977;
Kimura et al. 1977; Minami et al. 1978). These
results suggest non-obligate mycophagous
Spore dispersal of Dictyophora fungi
Table 3
11
Relative proportions of drosophilid species collected at sporocarps of Dictyophora spp.
Genus
(subgenus)
Species
group
Drosophila (D.)
bizonata
Species
histrio
immigrans
testacea
quinaria
D. (Sophophora)
melanogaster
D. (Dorsilopha)
Scaptodrosophila
Hirtodrosophila
Mycodrosophila
D. bizonata Kikkawa
& Peng
D. sternopleuralis
Okada & Kurokawa
D. histrio Meigen
D. albomicans Duda
D. annulipes Duda
D. curviceps
Okada & Kurokawa
D. immigrans Sturtevant
D. orientacea Grimaldi
D. brachynephros Okada
D. nigromaculata
Kikkawa & Peng
D. simulans Sturtevant
D. melanogaster Meigen
D. lutescens Okada
D. suzukii Matsumura
D. auraria Peng
D. biauraria Bock & Wheeler
D. triauraria Bock & Wheeler
D. rufa Kikkawa & Peng
D. busckii Coquilett
Sd. coracina Kikkawa
& Peng
Hi. confusa Staeger
My. gratiosa (de Meijere)
Total number of individuals
Mycophagous (M)
Secondarily
mycophagous (MS)
Non-mycophagous (S)
F1…%†
K1…%†
MS
±
±
0.4
15.2
MS
±
±
0.4
±
MS
S
S
S
37.5
±
±
±
±
±
7.6
±
±
±
±
±
1.0
2.0
±
4.0
MS
MS
MS
S
±
25.0
12.5
±
24.8
±
±
1.0
83.4
±
±
±
19.2
±
1.0
±
S
S
S
S
S
S
S
S
S
MS
±
±
±
±
12.5
±
±
±
±
±
±
±
2.9
1.0
29.5
±
1.0
4.8
±
26.7
±
±
1.5
±
5.2
0.4
3.3
±
4.1
1.5
16.2
4.0
19.2
4.0
±
3.0
5.1
2.0
±
4.0
MS
M
12.5
±
±
1.0
±
±
±
±
8
Table 4 Relative proportions of the three food-habit
groups of drosophilid ¯ies
Feeding habit*
Feeding
habit
F1…%† K1…%† K2…%† K3…%†
±
87.5
1.0
51.4
±
85.6
±
40.4
12.5
47.6
14.4
59.6
*See text.
insects, in particular some drosophilids play a key
role for spore dispersal or spore consumption.
The spore-feeding experiment revealed that a
large number of undigested spores of Dictyophora
were present in the recta of the insects, but no
cell walls were found. This con®rms that drosophilid and muscid ¯ies do not digest Dictyophora
spores. The spores in the recta retained their
105
K2…%†
271
K3…%†
99
germination ability as high as the control. Thus,
only mucus but not spores of gleba was consumed by insects that were opportunistically attracted to Dictyophora sporocarps but were not
obligate fungivorous. In spite of the sticky nature
of gleba, it was rarely observed being attached on
the insect body surface. Beppu (1994) hypothesized that Dictyophora spores are dispersed
through the guts of the insect visitors as the excrement rather than as the adherer on the insect
bodies. However, no further lines of evidence
have been available until now. This study presents for the ®rst time strong evidence for Beppu's hypothesis.
Dictyophora sporocarps are quite ephemeral,
lasting only for 1±3 days. It is dif®cult for
consumers to specialize to such an ephemeral
and unpredictable resource (Jaenike 1978;
12
Table 5
control)
N. Tuno
Germination rates of Dictyophora duplicata spores extracted from recta of ¯ies or from a sporocarp (as the
Family
Drosophilidae
Muscidae
Control
Species
Sex
No.
specimens
examined
D. lutescens
D. busckii
D. immigrans
D. immigrans
spp.
F
F
F
M
F
2
2
3
8
3
No. spores in a rectum
(Mean ‹ SD)
35 840 ‹ 27 955
102 400 ‹ 74 218
240 640 ‹ 135 765
152 000 ‹ 102 596
1 681 920 ‹ 460 231
Germination rate (n)
On the 3rd day
On the 5th day
0.79
0.87
0.85
0.87
0.74
0.81
‹
‹
‹
‹
‹
‹
0.03
0.06
0.12
0.08
0.06
0.03
(585)
(436)
(1507)
(1521)
(526)
(227)
0.89
0.99
0.95
0.87
0.95
‹
‹
‹
‹
‹
±
0.04
0.02
0.07
0.09
0.03
(893)
(4219)
(1835)
(236)
(562)
Every combination is not signi®cantly different (P > 0.05, post hoc test, ScheffeÂ's F method).
Hanski 1989), the condition of which has obliged
Dictyophora to recruit opportunistic insects that are
usually dependent on other resources. On the
other hand, tight and species-speci®c relationships
exist between wood-rotting fungi and wood wasps
(Gilbertson 1984) and between fungi-growing
termites and Macrotermitinae (Wood & Thomas
1989). These fungi persist all the year round,
thereby possibly providing stable food resources
to those insects. The stable coexistence of fungi
and insects may be the ®rst step to mutualistic
coevolution. Tight and species-speci®c relationships are restricted to these persisting fungi. This
can explain why such relationships have hardly coevolved between ephemeral Dictyophora fungi and
those non-obligatory mycophagous insects. How
can Dictyophora fungi recruit those non-obligatory
mycophagous insects then?
Dictyophora sporocarps produce strong odour
from gleba. Although most mature mushrooms
have an odour to some extent, the odours of
phalloid sporocarps including Dictyophora are
peculiar and noteworthy (Imazeki & Hongo
1957, 1987; Imazeki et al. 1988). Although the
chemical components of the odour of Dictyophora
are not known yet, it smells like decayed fallen
fruit. The smell possibly attracts generalist decomposers that basically feed on such resources.
In addition to drosophilids, Haptoncus ocularis
(Nitidulidae, Coleoptera), which is known to
swarm on fallen fruits (Kurosawa et al. 1985),
was abundant in the two insect assemblies observed in Kyoto (K1 and K2 in Table 2). Insect
swarms around Dictyophora sporocarps are attracted by a certain cue, probably by the peculiar
odour. This is partly supported by the fact that
the three insect assemblies observed on the
Dictyophora sporocarps in Kyoto (K1, K2, K3)
resembled one another in composition, but were
quite different from those at other sympatric
fungi (N. Tuno, unpubl. obs.).
In addition, the physical nature of Dictyophora's
mucilaginous gleba looks quite similar to decayed
material. This may allow the Drosophilids to
consume the gleba more easily. In general, to
digest fungi is potentially dif®cult even for mycophagous insects since the physical nature of
fungi requires special digestive adaptations. Thus,
mycophagous beetles have developed speci®c
morphological adaptations to digest various
kinds of substrates that fungi produce (Crowson
1984; Newton 1984; Lawrence 1989). Among
mushroom-feeding Drosophilidae, the larval
dentition of mouth hooks, which are homologous to the mandible or maxilla, are developed in
relation to the increasing hardness of mushrooms consumed (Okada 1968). By contrast,
generalist drosophilids have another type of
mouth hooks with undeveloped dentition. To
recruit generalist drosophilids as spore dispersers, the mushrooms should provide a food reward that is easy to digest. The mucilaginous
gleba of Dictyophora may be such an easily digestible reward.
The composition of insect assemblies for Dictyophora sporocarps seemed to differ between
Kyoto and Furano, suggesting general attractiveness of the fungi for a wide range of insects.
The fungi may recruit some generalist mycophagous insects as potential spore dispersers depending on time and place. To con®rm this,
further detailed study should be carried out.
Spore dispersal of Dictyophora fungi
In summary, Dictyophora fungi use the following
strategy for spore dispersal. The fungi attract a
wide range of generalist mycophagous insects by
their strong odour similar to that of decaying
plants or fruit. The attracted insects can easily
feed on gleba, which is physically similar to their
own food resources. Since the attracted insects
are not specialized enough in mycophagy to digest spores ef®ciently, they excrete a quantity of
viable spores. Thus, instead of establishing a tight
relationship with specialists, Dictyophora fungi recruit temporally passing insects as spore dispersers, paying the cost of the odour and
mucilaginous gleba which is provided to the insects as a reward. It is still unknown whether the
specialist dispersers are fairly restricted, as long as
their densities are quite low.
ACKNOWLEDGEMENTS
I would like to thank Drs E. Kuno, M. J. Toda,
T. Nishida, K. Beppu and K. Futai for their
useful suggestions and revision of the manuscript. Thanks are also offered to Drs K. Kanmiya, T. Okadome and M. J. Toda for their help
in identi®cation of the dipteran insects.
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