Mycol. Res. 105 (5) : 515–523 (May 2001). Printed in the United Kingdom.

515

Species richness, abundance, and phenology of fungal fruit

bodies over 21 years in a Swiss forest plot

Gerben STRAATSMA1*, François AYER2 and Simon EGLI2

" Applied Plant Research, Mushroom Research Unit, Postbus 6042, 5960 AA Horst, The Netherlands.
# Swiss Federal Research Institute WSL, Zuercherstrasse 111, CH-8903 Birmensdorf, Switzerland.
E-mail : g.straatsma!ppo.dlo.nl.

Received 25 July 2000 ; accepted 17 January 2001.

Fungal fruit bodies were surveyed on a plot area of 1500 m# from 1975–99 (excluding 1980–83) in the fungal reserve La Chaneaz in
western Switzerland. Fruit bodies were identified and counted on a weekly basis. Species richness and abundances varied strongly
between years. More than 400 species were encountered. Many species were transient ; particularly rich years showed species
occurring for only one year. This indicates that the number of species will substantially increase if the survey is continued. Within
years, the species richness, abundances and periods of fruiting were tightly correlated. The abundance data of species within a year
seemed symmetrically distributed over their fruiting period. The relation between species richness and abundances within years was
studied by fitting species-abundance plots, known from numerical ecology. The surface area under the curves was taken as a
parameter for ecological\fungal diversity. Productivity was correlated with the precipitation from June until October. The time of
fruit body appearance was correlated with the temperatures in July and August. As groups, mycorrhizal and saprotrophic species
behaved similarly over the years. The productivity of species was compared with their distribution in The Netherlands indicating a
correlation between the level of local abundance and the geographic range of species.

INTRODUCTION conclusions on the occurrence and the behaviour of fruit

bodies, as affected by environmental conditions, such as
Data sets on fungal fruit bodies are special, they only partially
temperature and precipitation. Important are the number of
represent the fungi living in the substrate. Several reasons
years of the survey, the protocols for the area to be studied,
exist to study fruit bodies rather than mycelia. Fruit bodies are
and the time frequency of recording. Many surveys have
immediately visible and attract much more attention than
already been done. Vogt et al. (1992) give an overview of
mycelia. People are attracted by the sudden appaerance of
sampling designs and methods used. In some studies transects
fruit bodies and their ephemeral beauty. In many countries
were used (Wilkins, Ellis & Harley 1937, Ohenoja 1984), in
edible species are picked for food or as a delicacy. Therefore
others permanent plots, with or without subplots. Sampling
fruit bodies, more than mycelia in general, are important in the
frequency varied from one observation per year (Parker-
context of nature conservation and management. Of course,
Rhodes 1951) to a weekly interval (Vogt, Edmonds & Grier,
fruit bodies have specific functional role(s) : (1) in the
1981). Egli, Ayer & Chatelain (1997) quantified the loss of
dissemination of spores for the establishment of new mycelia,
recorded species caused by a reduction of the sampling
or perhaps for the genetic adaptation of existing ones or even
frequency from weekly to monthly intervals. For some
for the prevention of gene flow (Fries 1981, Gregory 1984) ;
purposes 1 yr of sampling is enough, but most questions need
(2) on micro- and macrofauna due to their food value (Avila,
longer periods of investigation (Vogt et al. 1992). Many
Johanson & Bergstrom 1999, North, Trappe & Franklin 1997) ;
studies were focussed on the coherence of the fungal
and (3) maybe on soil mineralisation if developmentally
assemblage, the mycocoenosis, and the vegetation. Studies
regulated extracellular enzyme systems and differential
examining the influence of environmental factors on fruit
resource utilisation as in Agaricus bisporus and Lentinula edodes
body production have been conducted since the 1930s (Vogt
(Turner et al. 1975, Wood & Goodenough 1977, Ohga et al.
et al. 1992). Rainfall and temperature are generally recognized
2000) are common.
as important factors, but quantifications have hardly been
Elaborate and long-term data sets are required to draw any
made. The present data set is suited for studying these
questions because it is based on a long-term study with a strict
* Corresponding author. and steady protocol. Data were collected in permanent (sub)
Fruit bodies in a Swiss forest 516

plots and a monitoring frequency of 1 week. The data set is distance of the fungus reserve. Temperature data represent
the result of a broader myco-ecological study in the fungus monthly mean values, precipitation data are monthly sums.
reserve La Chaneaz in western Switzerland. Topics of the
study are the effects of mushroom picking (Egli, Ayer &
Chatelain 1990), forest management (Egli & Ayer 1997) and Mathematical
microclimate (Ka$ lin & Ayer 1983, Ayer 1990). Structure of the data set
The present analysis describes the coherent structure of the The data set was structured into records, entries, and fruit
data set, and considers species richness, abundance, and body numbers. A record represents a species in a year ; it holds
phenology. Data on individual species are hardly given but data entries for the weeks with fruiting, and the entries hold
species were grouped in two ways, according to their the fruit body numbers (Table 1).
mycorrhizal versus saprotrophic status and according to their
yearly frequency. The relationships with meteorological data
are described. Further, an example is given of a comparison Log-transformation
with quite another data set : the productivity of species was
compared with distribution data of the same species in The Log-transformation of biological variables often results in
Netherlands (Arnolds, Dam & Dam-Elings 1995) to test an better correlations with other variables (Burton 1998). Also, in
ecological ‘ law ’ that the local abundance of species is related statistical analysis, normal distributions and homogeneous
to the size of their geographic range (Johnson 1998). variance of variables are often required which perhaps can be
met by log-transformation. PivotTables were made containing
a column with all species and columns for the years of the
MATERIAL AND METHODS study holding either fruit body numbers or week (entry)
Survey numbers. Averages, variances and medians were calculated for
species. Average fruit body numbers were higher than
Mycological data were collected in the 75 ha fungus reserve medians. Re-transformed averages of log fruit body numbers
La Chaneaz in western Switzerland, established in 1975. It is were quite similar to the medians. For the period of fruiting
located 600 m above sea level in a typical mixed forest, with (entries with week numbers) the trend was similar but the
deciduous and coniferous tree species, such as Fagus sylvatica, effect of log transformation was small. In both cases variances
Quercus petraea, Picea abies, Pseudotsuga menziesii, Pinus silvestris, of log transformed data were more homogeneous than of non
P. strobus, and Larix decidua. The plant community (Galio transformed data. When fruit body numbers within records
odorati-Fagetum) represents a dominating forest type in the were studied (phenology), the untransformed numbers in the
Swiss Mittelland and an important and highly frequented entries were used.
habitat for picking mushrooms, especially in the recreational
areas around urban regions.
The data set is based on 5 observation plots each of Yearly frequency
300 m#, distributed within the reserve, and surrounded by 2 m
high fences to avoid all inconvenient influences by mushroom Yearly frequency of species is a parameter that it is easy to
pickers and large forest animals. From May to November understand and relatively easy to determine in a data set. The
(weeks 21 to 50) all the epigeous fruiting bodies of whole range of species was grouped according to the 21
macromycetes were identified and counted at weekly intervals. frequency classes. The disadvantages of this parameter are
To avoid multiple counting of the same fruit bodies, fruit that : (1) its unit, year, is specific for the data set being studied ;
bodies were marked with methylene blue at their first and (2) it provides for a short discontinous range of numbers
encounter. Voucher specimens of all the fungal species found between a discrete minimum of 1 and a discrete maximum that
within this study area are deposited in the mycoherbarium of equals the total number of years of the survey.
the Swiss Federal Research Institute WSL.
The survey spanned 25 years, from 1975–99. In 1980–83,
Diversity, productivity
as the consequence of a rationalization effort that we now
regret, only the edible species were recorded. Thus only 21 Species-abundance relations can be described in several ways
years are considered in the detailed analysis. (Magurran 1988). Rather than using or elaborating existing
Climatic data were registered by the automatic surface biological models (Preston 1948, Rosenzweig 1995, Harte,
network of the SMI–MeteoSwiss (Payerne station), in 5 km Kinzig & Green 1999) we, pragmatically, tried to apply a

Table 1. Structure of the data set ; illustration of records, entries and numbers. Two records of Russula ochroleuca in a poor (1989) and in a rich (1992)
year.

Weighted
Fruit appearance,
Year Week number bodies Entries week number

21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50
1989 1 1 1 41n0
1992 1 2 3 2 15 28 22 78 68 20 12 6 257 12 43n9
G. Straatsma, F. Ayer and S. Egli 517

Table 2. Diversity, abundance and phenology data over the years of the study.

Species richness Abundance Phenology Meteorology

1 2A 2B 2C 3A 3B 3C 4A 4B 5A 5B
Number of Number of Number of Number of Week number Precipitation
species mycorrhizal saprotrophic Number of Mycorrhizal Saprotrophic entries with most Temperature months 6–10,
Year (records) species species fruit bodies fruit bodies fruit bodies (weeks) fruit bodies month 8 mC mm

75 81 54 25 1891 1682 194 221 38 18n0 401n3

76 40 26 13 266 161 98 75 38 16n2 326n4
77 88 61 24 1954 1649 299 251 34 16n1 446n2
78 72 47 22 1253 846 404 238 35 15n7 328n0
79 119 76 37 3802 2478 951 392 37 16n1 319n6
84 38 31 7 668 341 327 125 40 17n1 462n3
85 40 32 8 633 327 306 120 38 17n2 285n5
86 68 46 19 1914 1313 546 245 39 17n4 360n5
87 65 41 22 2251 1109 1106 268 43 17n8 636n3
88 71 48 23 2875 2050 825 273 40 18n4 471n9
89 18 10 8 182 58 124 45 41 18n2 244n8
90 95 64 27 4012 2769 1031 336 40 19n0 468n7
91 55 38 17 830 322 508 145 44 19n7 393n4
92 194 125 60 6006 3861 2080 603 41 20n6 472n4
93 179 119 51 8467 5559 2783 583 40 18n3 609n4
94 162 107 47 8047 4624 3353 472 39 19n6 515n9
95 141 96 41 5972 3362 2529 371 39 18n0 396n1
96 142 88 50 4974 2231 2686 352 41 16n6 412n8
97 157 101 50 5879 2609 2965 459 42 19n3 458n2
98 137 84 50 4507 2079 2397 294 41 18n8 422n1
99 157 98 56 4839 2220 2604 523 43 18n4 544n3

simple statistical model. For all years 5 abundance classes (log number before the maximum (front), the maximum number,
values, from minimum to maximum abundances) were applied. and the number after the maximum (tail). Only records with
The corresponding numbers of species were counted and fruit bodies in 2 or more weeks and with only one maximum
expressed as log’s. Linear regression of log-transformed were suited for this analysis (1075 out of 2119). Alternatively,
species numbers (y) on log-abundance classes (x ; y l AjB*x) the entries and their fruit body numbers were taken and the
resulted in adequate fits. Fitted A and B values were used to ‘ weighted week number of appearance ’ was calculated of all
calculate the surface area under the fitted curve. This value 2119 records : the sum of the products of week numbers and
was taken for both ‘ diversity ’ as well as ‘ productivity ’. The fruit body numbers divided by the total number of fruit
frequently used Shannon index of diversity (Magurran 1988) bodies. For the 1075 records, the weighted appearance was
was calculated for comparison. almost equal to the week number in which the maximum
With mycorrhizal species as a (sub)assemblage, the same number of fruit bodies occurred.
calculations could be made. The saprotrophic assemblage
consisted of too few species to obtain satisfactory species- RESULTS
abundance curves ; some abundance classes did not contain
any species and in several plots the points were scattered During 21 years, numbers of fruit bodies per mushroom
irregularly. A productivity parameter was required for species were counted on a weekly basis. A total of 71 222 fruit
saprotrophs for an analysis of the trend seen in Table 2 bodies belonging to 408 species were seen on the observed
columns 2B, 2C, 3B and 3C that the number of fruit bodies of area of totally 1500 m#. Only 8 species were found in all years,
saprotrophs, not that of species, increased in time. An estimate 6 being mycorrhizal : Lactarius blennius, Russula cyanoxantha, R.
was improvised. After preparing the tables required for any fellea, R. fageticola, R. ochroleuca, and Xerocomus badius ; and 2
species-abundance curve, the sums of the abundance columns being saprotrophic : Collybia butyracea var. asema and C.
were taken, rather than the area under the (incomplete) species- dryophila. The average number of fruit bodies per species and
abundance curves. In addition the average abundance was year (per record) equals 71222\2119 l 33n6. Few records
calculated of all saprotrophic species, of the two species that with high numbers contribute strongly to this average. Not
were present in all years, of the 7 most abundant species (7 surprisingly, the median value is low, it equals 6. If 10-
being the lowest number of species present in 1984) and the logarithms of the numbers in the records are taken, the
maximum abundance of any species (these parameters were average equals 0.860, and, re-transformed it equals 10!n)'! l
progressively better correlated with year number). 7n3, quite similar to the median. Log transformation was quite
often applied, as described above.
Species richness, abundances and periods of fruiting vary
Distribution of fruit body numbers (entries) in records, phenology
over the years (Table 2 columns 2A, 3A and 4A, respectively)
For a straight on analysis of as many records as possible, the and seem correlated. This gives the impression that merely
numbers in the records were divided into three parts, the one phenomenon is encountered : productivity.
Fruit bodies in a Swiss forest 518

Table 3. Yearly frequency of species.

1 2 3 4 5 6
Time of weighted
Number of Number of Number of species appearance, averaged
Frequency Number of mycorrhizal saprotrophic with most fruit bodies over species,
group species species species before week 36 week number

1 150 102 42 28 38n8

2 53 34 13 2 40n5
3 32 15 17 7 38n6
4 18 14 4 0 39n2
5 23 15 7 6 38n0
6 13 8 5 0 38n9
7 12 8 3 1 38n8
8 20 12 8 2 39n2
9 14 9 3 2 38n8
10 8 5 2 2 37n6
11 7 5 2 1 39n0
12 4 1 2 0 38n5
13 6 2 4 1 36n4
14 7 4 3 1 37n4
15 1 1 0 0 42n3
16 10 7 3 0 39n4
17 4 4 0 0 39n7
18 6 4 2 2 37n2
19 8 7 1 0 38n0
20 4 2 2 0 39n2
21 8 6 2 1 38n3

2·5
Species richness and yearly frequency
The numbers of species in the years are given in Table 2 2·0
column 2A. In 1989 only 18 species were found and in 1992
log number of species

the number was as high as 194. The richnesses of the two 1·5
major ecological groups, mycorrhizal and saprotrophic species,
is given in columns 2B and 2C. The number of mycorrhizal
species is about twice as high as the number of saprotrophs. 1·0
‘ Species-time ’ curves show the total number of species in the
course of the years (Rosenzweig 1995, Watling 1995, Tofts & 0·5
Orton 1998). We prefer to give the number of species
appearing for the first time in the observation period (Table 4 0·0
column 2A). One would expect that this number levels off in 0·5 1·0 1·5 2·0 2·5 2·5
time. This is not the case. The number of ‘ first ’ species is first Abundance, log number of fruit bodies
of all correlated with ‘ productivity ’ of years, less so with year Fig. 1. Species-abundance curve of the rich year 1992. Five
number. abundance classes were taken, the highest class until the abundance
The number of years that species fruited were counted and of the most abundant species (Table 4 column 3B). The surface area
species were grouped according to their yearly frequency. The under the curve (Table 4 column 3E) is taken as a parameter for
number of species in each frequency group is given in Table diversity and productivity.
3 column 2. The number of species with a frequency of 1 is
high and holds the majority of species identified to genus only
Abundance, diversity and productivity
(a total of 64 species, 48 belonging to Cortinarius). As groups,
the mycorrhizal and saprotrophic species showed similar The easy to understand productivity parameter ‘ number of
patterns (Table 3 columns 3 and 4). The group of species often fruit bodies per species per year ’ is ambiguous because the
showing most of their fruit bodies in early summer (Table 3 species composition varies over the years. Moreover, each
column 5 ; phenology section) also showed this common year shows many species with low numbers. These low
pattern. The log number of species can be plotted against numbers tend to obscure the differences in productivity
frequency, as done for a grassland\disturbance study of Glenn between years. This matter has been solved elegantly in
& Collins (in Collins & Benning 1996). Such a plot gradually biodiversity research where species richness and species
falls to a level of 0n7 (of 10!n( l 5 species) for frequencies abundances are both taken into account in species-abundance
above 10. curves (Magurran 1988). Typical species-abundance curves
G. Straatsma, F. Ayer and S. Egli 519

Table 4. Detailed parameters over the years of the study ; extension of Table 2.

Species richness Diversity\productivity Phenology

1 2A 2B 3A 3B 3C 3D 3E 3F 4A 4B 4C
Difference in
Number Number Log number Log number A value B value Area under Number of appearance
of species of species of species of maximum of fitted of fitted fitted species with Weighted (weeks) :
appearing occurring with a abundance species- species- species- Shannon fruit week saprotrophic–
for first only in single fruit of any abundance abundance abundance index of bodies before number of mycorrhizal
Year year 1 year body species curve curve curve diversity week 36 appearance species

75 81 1 1n204 2n646 1n846 k0n484 3n19 3n095 18 38n1 0n3

76 13 3 1n301 1n643 1n232 k0n481 1n37 2n857 11 37n9 k1n5
77 29 7 1n255 2n685 1n909 k0n505 3n31 3n129 72 34n2 1n3
78 8 0 1n255 2n212 1n623 k0n405 2n60 3n318 49 35n5 k2n0
79 29 7 1n301 2n725 1n916 k0n389 3n78 3n513 33 38n5 0n2
84 2 0 0n954 2n079 1n226 k0n317 1n86 2n686 13 39n0 k2n9
85 1 0 0n954 2n292 1n46 k0n480 2n09 2n631 20 36n6 k2n7
86 3 1 1n146 2n489 1n516 k0n289 2n88 3n164 35 36n8 k1n0
87 5 2 1n041 2n558 1n461 k0n252 2n91 3n116 29 38n8 1n5
88 7 3 1n041 2n698 1n586 k0n308 3n16 3n042 30 38n4 0n8
89 1 1 0n602 1n826 0n954 k0n476 0n95 2n133 4 40n4 2n8
90 18 2 1n255 2n805 1n708 k0n289 3n65 3n348 25 39n1 0n6
91 4 0 1n000 2n356 1n61 k0n480 2n46 2n923 18 39n8 2n9
92 74 33 1n633 2n870 2n192 k0n429 4n52 3n800 55 40n1 0n2
93 33 20 1n602 3n162 2n282 k0n471 4n86 3n516 55 37n7 0n4
94 16 9 1n255 3n046 2n138 k0n420 4n56 3n441 30 39n6 0n7
95 15 10 1n398 2n991 2n058 k0n408 4n33 3n444 18 39n1 k1n2
96 17 8 1n491 2n876 2n093 k0n450 4n16 3n322 40 39n0 0n5
97 22 15 1n477 3n173 2n311 k0n540 4n61 3n307 71 38n9 0n8
98 11 9 1n301 2n880 2n037 k0n418 4n13 3n563 15 40n9 0n0
99 19 19 1n301 2n870 2n144 k0n453 4n29 3n730 76 38n2 1n8

2·0 The abundances vary strongly among species. If species are

grouped to yearly frequency and the abundances averaged
Abundance per year, log number

accordingly, a clear relationship is seen between abundance

1·5 and frequency (Fig. 2). Thus yearly frequency can be used to
express the productivity of species.
The number of fruit bodies of mycorrhizal species and of
1·0
saprotrophs are given in Table 2 columns 3B and 3C. The
abundance per mycorrhizal species was a bit lower than per
saprotrophic species (not shown). In the lasts years of the
survey the total numbers of fruit bodies of saprotrophs were
0·5
higher than those of mycorrhizal species (see Time course
below).
0 5 10 15 20
Yearly frequency of species
Fig. 2. Relation between the number of fruit bodies (averaged over Phenology
years) and yearly frequency of species (the number of species Fruiting bodies were monitored between week numbers 21
involved is given in Table 3 column 2).
and 50, the ends of months 5 and 12. The start of fruiting
varied strongly over the years and over species. The longest
were obtained ; Fig. 1 shows the curve of a rich year. Columns period of fruiting of any species in any year showed Russula
3A and 3B in Table 4 give an impression of the left and right cyanoxantha in 1992. It fruited from week numbers 26 to 45
side borders of the curves : column 3A contains the number of (20 weeks) but it showed no fruiting in week numbers 36 and
species with only one fruit body (being the smallest abundance) 37, thus the number of weeks with fruiting was 18 (being the
and column 3B contains the number of fruit bodies of the most number of entries in that record). The overall information on
abundant species (in all years this value belonged to a single the duration of fruiting in the years (total number of entries)
species only). Fitted values of the species-abundance curves is given in Table 2 column 4A. On average, week number 40
are given in Table 4 columns 3C and 3D. The surface area at the end of month 9, showed the highest numbers of fruit
under the fitted curve (column 3E) was taken to characterize bodies.
the curve with a single parameter only. The Shannon index of The number of species fruiting in each week of the years
diversity is given in column 3F. were counted (data not shown). Some years had a ‘ pre-
Fruit bodies in a Swiss forest 520

42

(area under fitted species-abundance curve)

Time of weighted fruit body appearance,
5

40

Diversity/productivity
4
week number
38 3

2
36

1
34
0
15 16 17 18 19 20 21 300 400 500 600
Temperature in August, °C Precipitation from June until October, mm
Fig. 3. Relation between the temperature in August and the Fig. 4. Relation between the precipitation from June until October
weighted time of appearance of fruit bodies (Table 4 column 4B). and the parameter for diversity and productivity (the area under the
fitted species-abundance curve, Table 4 column 3E).
summer ’ peak, lasting maximally until week 35. Then a dip
occurred and the ‘ autumn ’ peak appeared. Most years did not Relations with meteorological data
show a typical pre-summer peak. The number of species Monthly temperatures show a cyclic patterns over the year. A
(partly) fruiting up and until week 35 (Table 4 column 4A) was Gaussian curve fits well to the data, its peak of 19n6 mC lies at
determined. Year 1977 was exceptional ; 80 % of all species month 7n1 (week 27). This is 12 weeks before the peak of
appeared in pre-summer and the distribution in the autumn fruiting (Table 2 column 4B, Table 4 column 4B). Estimating
was irregular. Overall, the pre-summer peak is not very that the development of fruit bodies takes about 2 weeks, the
important : (1) the total number of fruit bodies until week 35 fruiting peak may be the respons to the temperature in week
is 10 886, being only 15 % of the total ; and (2) the species 37, when it drops below about 14 mC. This temperature level
in column 4A may well have most of their numbers in the is crossed the other way in spring in week 21, when the first
autumn. fruit bodies (erratically) appear.
A ‘ weighted ’ week number of fruit body appearance is The ‘ weighted ’ appearance of fruit bodies (Table 4 column
presented in Table 4 column 4B. For many records, the 4B) correlates with the temperatures (Table 2 column 5A) in
weighted appearance is very much in between the first and months 7 and in month 8 (Fig. 3). An increase of 1 m coincides
last appearance and similar to the appearance of the highest with a delay of fruiting of almost 1 week. Cantharellus cibarius
number of fruit bodies in any week. On average the numbers and Lactarius volemus were exceptions, they were negatively
within a record for front, maximum and tail were 12, 33 and correlated with the temperatures. Not a delay in fruiting, but
17, respectively. The three parameters were positively a full stop was found at high temperatures. On average this
correlated over the records. Distributions within records seem resulted in an early appearance time. The ‘ negative ’ effect of
quite regular. It is characterized by the total number of fruit temperature on fruiting is not quite apparent in the numbers
bodies, a maximum number in the middle of the distribution of species, or in ‘ productivity ’. As groups mycorrhizal and
and a time span for fruiting. Two of the three characteristics saprotrophic species seem to behave differently : mycorrhizal
largely determine the distribution. Some abundant and species fruit earlier (Table 4 column 4C, section Time course
frequent species showed almost ‘ normal ’ distributions. below) when summer temperatures are high.
Exceptions were Mycena pura and Russula cyanoxantha, that Monthly precipitations show a weak cyclic pattern ; the
showed two peaks in several years. It was impossible to variation over the years is high and the summer peak is less
characterize all species ; infrequent and unproductive species than twice the winter low. Species richness, overall abundances
do not show enough data for entries and fruit bodies. and periods of fruiting (log values of Table 2 columns 2A, 3A
The number of species was counted that showed most of and 4A), the average frequency of species (not shown), and
their fruit bodies in pre-summer in most of the years (Table 3 diversity parameters (Table 4 columns 3E and 3F) are all
column 5). Early fruiting species occurred in all frequency correlated weakly with the precipitations of months 10, 8 and
groups ; an example is Collybia dryophila, one of the 8 species 6 (months given in order of impact). Correlation existed also
that was present in all 21 years. The week numbers with most with the total precipitation of months 6 to 10 (Table 2 column
species fruiting, the week numbers with most fruit bodies and 5B). With the total precipitation, all parameters leveled off at
the weighted appearances of individual species were compared. a precipitation of about 550 mm (Fig. 4). At this level
The difference in appearance of mycorrhizal and saprotrophic productivity\diversity is maximal.
species is given in Table 4 column 4C. Negative values
indicate that mycorrhizal species fruited earlier than sapro-
Time course
trophic species. Over the years many species showed positive
correlations with the parameters of appearance in general. Over the years, the temperature in month 8 increased and the
This indicates that species showed quite the same sequence of precipitation of months 6–10 showed a tendency to increase.
appearance over the years. This climate change is typical for the central European region
G. Straatsma, F. Ayer and S. Egli 521

species are infrequent and have low abundancies in our

8 present study.

Distribution in the Netherlands,

9 classes of grid numbers
6 DISCUSSION
The data set is highly structured : species richness, abundance,
4 and the length of the fruiting period in a year, are tightly
correlated. This coincides with : (1) the symmetrical distribution
of abundance data of species over their fruiting periods ; and
2
(2) regular species-abundance distributions over the years (Fig.
1). Regular species-abundance relations are found in all sorts
of assemblages, for example of diatoms, higher plants,
0 5 10 15 20
Yearly frequency of species
butterflies etc (Magurran 1988). We assume that, even after
21 yr, the whole spectrum of species richness has not been
Fig. 5. Relation between the distribution of species in The seen. Many new species may be expected in additional
Netherlands and the yearly frequency, as parameter for abundance, in ‘ productive ’ years. These years provide for infrequent and
this study. unique species (Table 4 column 2B). It was not surprising to
find that ‘ species richness estimators ’ (Schmit, Murphy &
Mueller 1999) did not stabilize to a definite maximum (results
(Rebetez & Beniston 1998). The weighted times of fruiting not shown).
(Table 4 column 4B) correlated with the year numbers of the Productivity varies over the years and probably shows a
survey. However, this correlation was weaker than that continuous range of values between its minimum and
between time of fruiting and the temperature in month 8. maximum (both unknown). One may consider that the species
Probably the time course of the survey itself has no effect on of the mushroom assemblage form a continuous range of
the shift in time of fruiting. Similarly, the shift in appearance (potential) productivities. It is not that simple. The least and
of saprotrophic versus mycorrhizal species (Table 4 column most productive years are 1989 and 1992, respectively. Given
4C) correlates with year number, but less so than with the a continuous range of productivities, the 18 species of 1989
temperature of month 8. Productivity parameters were would be present in all other years and the number of species
correlated with year number. This was analyzed in detail in with a frequency of one would be 194–179 (being the
multiple regressions on year number, temperature in month 8 difference in species of 1992 and the second species rich year
and the precipitation of months 6–10. Precipitation had the 1993). Also, the total number of species in the survey would
highest impact, the influence of year number was small and not exceed the number of 194 in 1992. However, almost each
that of temperature not important. Analyzing the groups of year showed unique species (Table 4 column 2B). Many
saprotrophic versus mycorrhizal species showed that sapro- species are transient ; unique species are not the only transient
trophic species reacted to year number in particular and ones. Species may be transient because : (1) they establish
mycorrhizal species much less so. The abundance of themselves for a certain number of years and then disappear
saprotrophic species increased with time ; not the number of from the plot ; and (2) their mycelial biomass and the amount
species. of resource they captured fluctuates over the years, in-
dependent from the ‘ productivity ’ level. Of course our data
relate to fruit bodies, not to mycelia, and the mycelia need
Relation with distribution data from The Netherlands
not be transient at all.
Of the 408 species of this study, 326 have been fully identified For mycorrhizal fungi, the correspondance between fruit
and 82 are identified to genus but not (yet) to species (mainly body occurrence and mycelia occurrence in the soil can be
Cortinarius spp.). Of the fully identified species, 257 are measured on the basis of mycorrhizas by molecular methods.
mentioned in a list of Dutch wild mushrooms by Arnolds, The species composition of fruit bodies reflects poorly that of
Dam & Dam-Elings (1995). The list provides distribution data mycorrhizas on the same plot (Gardes & Bruns 1996, Jonsson
for all species : a virtual grid is laid over The Netherlands and et al. 1999). Many mycorrhizal species do not form fruit
the presence of species is counted in each grid number. Counts bodies or form inconspicuous (Thelephoraceae and Corticiaceae)
are given on an (almost) exponential scale of 1 to 9. All or invisible (‘ Tuberales ’) ones. Dahlberg, Jonsson & Nylund
frequent species in the present study occur in The Netherlands. (1997) and Peter, Ayer & Egli (2001) found that about half of
Infrequent species are present in the Netherlands to a lesser the abundance of the ectomycorrhizas was accounted for by
extent, the overlap being 70 % or higher. Fig. 5 shows the species that did not produce conspicuous epigeous fruit
relationship between Dutch distributions and the frequencies bodies.
in the present study. Of all Dutch species, 2475 ‘ sufficiently A rather adequate and simple parameter for the expression
documented ’ species were considered for the establishment of of productivity is the number of species. This parameter
a red list (Arnolds & van Ommering 1996). Of ‘ our ’ fully requires less effort to be measured than the accurate counting
identified species, 122 fall within one of the categories of the of numbers of (identified) fruit bodies and a strict periodical
Dutch red list : susceptible, vulnerable, threatened, seriously visit of the study site. If this holds for other data sets as well,
threatened, and disappeared (12 species). On average these a quick (re-)analysis of those data can be done because the
Fruit bodies in a Swiss forest 522

accurate identification of species and a list or table showing the amount of substrate for these species. Perhaps soil organic
the presence of species over the years of a study will probably matter is accumulating, or, as Arnolds (1991) found, a general
be basic to that study. The best conceivable parameter should nutrient enrichment by atmospheric deposition, in particular
characterize the species-abundance relations, for instance the that of nitrogen, facilitates the fruiting of saprotrophs.
area under the fitted curve (Table 4 column 3E). Compared Knowledge of fruit body productivity is of ecological
with other productivity parameters (log numbers of species or relevance because of the functional role(s) of fruit bodies. The
of fruit bodies), the area under the curve shows a relatively results are also relevant in a conservational context. Absence
long range of values, providing for much ‘ resolution ’. in productive years is more alarming than in poor years ; this
However, the length of this range should not be surprising, is important for the selection of species for ‘ red ’ lists. The
because the area under the fitted curve is an expression of results are also interesting for those trying to manipulate the
species richness and of species abundances, two parameters yield of edible mushrooms in forests and in tree plantations of
with independent ranges. truffles and of other species.
To our knowledge, the correlation of the summer Fruiting starts with the formation of primordia (Cle! mençon
temperature with one aspect of phenology, the time of 1997) or primordial undifferentiated stages (Umar & van
fruiting, has not been found previously. High temperatures in Griensven 1997). Very little is known about this process in the
full summer seem to delay fruiting. Temperature is related to field. In Agaricus bisporus, the formation of the total number of
the evaporative power of air ; the capacity of air to carry water primordia is fixed before any fruit body is visible (Flegg 1979).
doubles at a temperature increase of 10 mC. Mushroom tissue If this phenomenon is common, it is easy to understand that
will desiccate more easily at a high temperature and perhaps the appearance of fruit bodies is quite independent from their
this vulnerability causes a delay to the autumn in the numbers and that numbers are regularly distributed over the
development of fruit body initials or their growth into mature, period of appearance. In the field, fairy ring-forming fungi
and visible, fruit bodies. We suggest that the species in the may be suited to study the occurrence of this phenomenon ;
assemblage react in a continuous range to temperature for the position of emerging mushrooms and thus of their
fruit body development and (or) growth. The correlation of primordia can be predicted by observations on fruit body
precipitation data with productivity parameters has also been positions in previous years. This offers the possibility of
demonstrated in other studies (Wilkins & Harris 1946, selecting sites for observations. ‘ Mycelium ’ mapping and
Wasterlund & Ingelog 1981, Agerer 1985). Fungal species analysis of such data would help in studying the species
composition seems to be strongly determined by soil chemical dynamics in the soil. Primary data related to the present data
properties (Ruehling & Tyler 1990) and vegetation type set await analysis. Experimental field studies have been
(Runge 1964). Other factors are the structure and age of the concentrated on edible mycorrhizal species unsuitable for
forest stand (Dighton & Mason 1985, Vogt et al. 1981), and cultivation, such as truffles (Singer 1965, Rebiere 1967, Hall &
even the host genotype in the case of mycorrhizal species Wang 1998), and on ‘ environmental ’ effects of fertilization,
(Last & Fleming 1985). acid rain, etc. (Jonsson et al. 1999). Watering of plots can be
The correlation of Swiss ‘ productivity ’ data with Dutch used to study the effect of precipitation. Perhaps field
‘ distribution ’ data (Fig. 5) supports the biological ‘ law ’ of the experiments can be extended by applying airconditioning in
abundance-distribution relation of species (Johnson 1998). ‘ greenhouses ’ on site to study the effect of temperature and
Rare species seem to be threatened with extinction on a the moisture contents of air. Saprotrophic species could be
(sub)evolutionary time scale. Few data exist for rare species selected for experimental studies. They can often be cultivated
because of their rarity. It is difficult to distinghuish between a (Flegg, Spencer & Wood 1985, Poppe & Heungens 1991) and
specific and a general threat for rare species. Thus, the thus could serve as models in the laboratory and (or) field. The
establishment of red lists is difficult. Such lists will easily over- cultivated white button mushroom, Agaricus bisporus, seems to
concentrate on rather abundant and frequent species and will react to temperature and moisture (Flegg et al. 1985) quite
probably be too short. similarly to the assemblage in our plot.
Mycorrhizal and saprotrophic groups of species behaved
similarly. A difference was found with regard to the time of
appearance of fruit bodies. In years with high summer A C K N O W L E D G E M E N TS
temperatures the saprotrophic species reacted with a later G. S. thanks L. J. L. D. van Griensven for his encouragement and critically
appearance (Table 4 column 4C). Another difference was the reading the draft, and thanks J. T. N. M. Thissen and Thomas W. Kuyper for
relatively higher number of fruit bodies of saprotrophs in the discussions.
later years of the study. The substrates of both groups are
quite different. Saprotrophs require litter from (the) previous
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