Biohgicalj’oumal ofthe Linnean Sociep (1997), 62: 111-131.

With 3 figures

Stability, ephemerality and dispersal ability:

microarthropod assemblages on hngal

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sporophores

TADHG O’CONNELL AND THOMAS BOLGER

Department of <oolo~, Universtp College Dublin, Beyield, Dublin 4, Ireland

Received 22 May 1996; acceptedfor publication 13 February 1997

A comprehensive analysis of the microarthropod fauna from fungal sporophores revealed a

series of recurrent patterns demonstrating the non-random structure of these assemblages.
Despite the existence of a strong species-area relationship from sporophores of certain fungi,
particularly among perennial species, several small sporophores always maintained a more
diverse microarthropod fauna than fewer large sporophores of equivalent total area. A
consistently high degree of overlap in microarthropod species occurrence between larger and
smaller sporophores was indicated by the presence of highly significantnested subset structure.
The fauna from Heternbasidion annosum sporophores was the most nested, followed by Hypholoma
facicukzre and a collection of pooled agarics, respectively. When the fauna was split into
functional groups, microphytophages were always significantly nested in their distributions
but, when significant, macrophytophages and panphytophages had stronger nested hier-
archies. Non-random organization was least evident among predatory species. Micro-
arthropods had significantly ordered distributions on sporophores of various fungi. Many
species occurred on perennial H . annosum sporophores of all sizes while others had more
restricted distributions. Most species from very ephemeral agarics, including those which
were widely distributed on H. nnnosum, were restricted to a small number of larger sporophores.
The pattern from H. fascicukzn was intermediate; most species had narrow distributions and
were present only on larger sporophores, except a small number of more widely distributed
species.
0 1997 The Iinnean Society of London

ADDITIONAL KEY WORDS4iversity - dividedness - functional groups - hierarchy -

incidence functions - nestedness - Acari - Collembola.

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . . . . . 1 12
Samples and sites . . . . . . . . . . . . . . . . . . . . . 113
Analysis . . . . . . . . . . . . . . . . . . . . . . . . 114
Cumulative species-area curves . . . . . . . . . . . . . . . . . 115
Nestedness . . . . . . . . . . . . . . . . . . . . . . . 117
Incidence functions and Mann-Whitney tests . . . . . . . . . . . . 119

Correspondence to T. O’ConneU. email: Tadhg-O’Connell@cbtsys.com

111
0024-4066/97/0901 I I C211 $25.00/O/hj970144 0 1997 The Linnean Society of London
112 T. O’CONNELL AND T. BOLGER

Habitat dividedness and ‘temporal stability’ . . . . . . . . . . . . 122

Implications . . . . . . . . . . . . . . . . . . . . . 122
The paradox . . . . . . . . . . . . . . . . . . . . . 123
Sporophores as ‘islands’ . . . . . . . . . . . . . . . . . 123
Hierarchical structure . . . . . . . . . . . . . . . . . . . . 124
Why a nested hierarchy? . . . . . . . . . . . . . . . . . 125
The evidence from incidence . . . . . . . . . . . . . . . . . 125
Conclusions . . . . . . . . . . . . . . . . . . . . . . . 127
Acknowledgements . . . . . . . . . . . . . . . . . . . . 127

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References . . . . . . . . . . . . . . . . . . . . . . . 127
Appendix. . . . . . . . . . . . . . . . . . . . . . . . 130

INTRODUCTION

Historically, studies of the fauna of fungal sporophores have focused almost

exclusively on the Diptera and Coleoptera (Weiss & West, 1920; Scheerpeltz &
HBfler, 1948; Wilding et al., 1989). Prior to Graves (1960) the diversity of the
microarthropod fauna was not appreciated and since then has been largely ignored
(but see Pielou & Verma, 1968; Matthewman & Pielou, 1971). However, the
Acari and Collembola are the most numerous inhabitants of sporophores in the
Aphyllophorales (Graves, 1960) and have very diverse assemblages in other species
of fungi. In a recent survey a total of 323 species were identified from approximately
65,000 microarthropods collected from the fructifications of 38 species of fungi
(O’Connell, 1994).
Patterns and processes must be investigated at several spatial and temporal scales
and fungal sporophores are unrivalled as resources or habitats encompassing broad
heterogeneity at several spatial, and especially temporal, scales (Hanski, 1989). The
existence of pattern in natural communities has often been used as evidence of
structure (Strong et al., 1984; Schoener, 1986) and the search for pattern in the
distribution and abundance of species has been one of the central themes of ecology
(Hutchinson, 1959; Diamond, 1975). Many previous studies were based upon the
tenets of island biogeographic theory and have investigated its associated species-
area relationship (Connor & McCoy, 1979; McGuinness, 1984; but see Coleman et
al., 1982; Boecklen & Gotelli, 1984 for a critique). Drawing a parallel between
oceanic archipelagoes and fungal sporophores as habitat patches in a ‘sea of
woodland’, O’Connell (1994) successfdy applied the classic species-area model of
island biogeography (MacArthur & Wilson, 1967) to analyses of the microarthropod
fauna of fungal sporophores. This study demonstrates a significant relationship
between the species richness of the fauna and the weight of sporophores for the
perennial bracket fungus, Hehobasidion annosum (Fr.) Bref., and the ephemeral agaric,
ClitocybeJlaccidu (Sow. ex Fr.) Kummer. However, the spatial and temporal patterns
of distribution of ephemeral habitats impose severe constraints on the types and
identities of the organisms which colonize and consume them, while the structural
complexity of the habitat is a major influence on the species diversity of these
assemblages (Doube, 1987).
The studies of Graves (1960) and Matthewman & Pielou (197 1) noted that certain
microarthropod species were present in great abundance in the fruiting bodies of
bracket fungi (10‘- 1O4 individuals) and that often all life-history stages (egg-adult)
were present. This observation was reaffirmed in the survey of O’Connell (1994).
The majority of microarthropods comprising these assemblages were fungal feeders.
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 113

The microscopic size (200-800 pm) of many microphytophagous (fungivorous) and

certain specialist predatory species (Graves, 1960; Lindquist, 1970; OConnor, 1984)
enables them to forage among the layers of spore tubes and structural and generative
hyphae which constitute fungal sporophores. Although generation times for micro-
arthropods are extremely variable and sensitive to environmental factors such as
temperature, moisture content and type of substrate, some fungivorous species have
very short developmental times ranging from 1.5 to 35 days (Butcher, Snider &
Snider, 1971; Luxton, 1981; Walsh & Bolger, 1990; Norton et al., 1993). These

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traits allied to parthenogenetic reproductive strategies, with or without r-type
demographic strategies, colonizing life-styles, continuous year-round breeding, and
phoretic associations with fungivorous insects (Butcher et al., 1971; Luxton, 1981;
Lebrun et al., 1991) may facilitate the development of abundant and diverse
fungus-microarthropod assemblages in the face of extreme habitat spatio-temporal
heterogeneity (O'Connell, 1994). However, many of the oribatids collected from
fungi appear to contradict this scenario since they are often characterised by typically
K-selected life-history strategies (Norton, 1994).
In this paper, the previously established species-area relationship (O'Connell,
1994) serves as the starting point for a further investigation of patterns in species
distribution and abundance in fungus-microarthropod assemblages. Using theory
derived from the fields of conservation biology, island biogeography and meta-
population studies, three specific issues are addressed. Firstly, the relative contribution
of dividedness and structural complexity in determining the species richness of
microarthropod assemblages associated with fungi is examined. This is tested by
determiningwhether single large sporophores contain a more diverse microarthropod
fauna than several smaller sporophores of equivalent total size. Secondly, the
assemblages are examined to determine whether the fauna of smaller sporophores
are nested subsets of those present on larger sporophores. Thirdly, the incidence of
individual microarthropod species are described, statistically assessed and considered
with reference to data for the complete fauna of fungal sporophores.

SAMPLES AND SITES

Sporophores of Heterobasidion annosum, a perennial bracket species, were collected

from the bases of infected trees. All sampling sites were located in mature woodland
in south-east Ireland. They consisted of a mixed woodland dominated in different
areas by beech (Fagw sylvatica L.) and Sitka spruce ( f i e a s i h h Z r (Bong.) Carri6re)
{labelled Mix 1 : 52"44'N, 6" 1OW}, two adjacent stands of Sitka spruce (labelled
Ss3 and Ss4: 53"01'N, 6"lO'W) and a pure stand each of Norway spruce ( f i e a abies
(L.) Karsten) {labelledNs: 52"43'N, 6'38'W) and Western hemlock (Tsuga hetmp@lZa
(Rafin.) Sarg.) {labelled Hem: 52"46'N, 6'38W).
A large variety of ephemeral agaric species, with a mean sporophore longevity
of 4-21 days, were also collected in south-east Ireland. All were collected from the
litter layer. The sampling sites consisted of two pure stands of Scots pine (Pinus
sylvestris L.) {Spl: 53"05'N, 6"09W and Sp2: 53"05'N, 6"14W} and Sitka spruce
(Ssl: 53"01'N, 6"lOW and Ss2: 53"00'N, 6"09'W), two mixed beech-Sitka spruce
stands (Mixl: 52"44'N, 6"lOW and Mix2: 53"05'N, 6"09'W), and a pure stand of
Norway spruce (Ns: 52"43'N, 6'38'W) and birch (Betula pubescens Ehrh.) {Bir:
114 T. O’CONNELL AND T. BOLGER

53”00’N, 6’21’W). Alone among the agarics, sporophores of Hypholorna fasciculare

(Huds. ex Fr.) Kummer were always found in very dense aggregations and appeared
relatively stable, remaining intact for several weeks. The annual bracket fungus,
plptopoms betulinus (Bull. ex Fr.) Karst., was also collected at the Bir site. In this case,
sporophores were collected at a height of one to two metres up infected tree trunks.
All sporophores were placed in brown paper bags and returned to the laboratory.
Larger ones were split into several sections and the microarthropods extracted using
Tullgren funnels. Following extraction the dry weight of sporophoreswere measured.

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Dry weight was the chosen index of sporophore size as it is easily converted to a
measure of area given a linear functional relationship between log of area and log
of weight, i.e. the power hnction. The abundance and diversity of the fauna from
sporophores collected at different sites and of variable weight were compared by
O’Connell(l994) using rarefaction curves based on the method of Simberloff (1 978).
This demonstrated that samples from different sites and of different sizes accumulated
species at an equivalent rate and that there was no artifactual effect of habitat or
size.

ANALYSIS

The question of whether larger sporophores are more structurally complex was
examined using the cumulative species-area analysis described by Quinn & Harrison
(1988). Three data sets, reflecting resources differing strongly in their temporal
stability, were analysed: the fauna of the pooled perennial sporophores of Hehbasidion
annosum (n = 55), the pooled ephemeral sporophores of Hypholma fasciculare (n = 29)
and the pooled sporophores of a variety of very ephemeral agaric species (n= 181).
Sporophores were ranked according to dry weight and curves were plotted of
cumulative species richness against area (as weight) (i) beginning with the smallest
sporophore and adding successively heavier sporophores (the small-to-large curve),
and (ii) beginning with the heaviest sporophore and adding successively lighter ones
(the large-to-small curve). This produces a comparison between a curve which
maximizes subdivision or dividedness and minimizes mean sporophore weight or
size (the small-to-large curve), with a curve which maximizes mean sporophore
weight (size) and minimizes subdivision (the large-to-small curve), for each dataset.
A difference between the two curves indicatesthat random placement is not occurring
and that ‘fragmentation effects’ are present (Douglas & Lake, 1994).
Nestedness of species assemblages occurs when the biotas of sites with fewer
species are subsets of the biotas at richer sites (Wright & Reeves, 1992). In the
extreme, species assemblages at a cluster of sites may be perfect subsets of the fauna
at the richest site. Thus, nestedness measures the degree of relative overlap or
coincidence in species distributions across sites (or samples). If nestedness is strong,
the few species present in small islands (or habitat patches) will be those with the
widest regional distribution, whereas only larger or richer sites will support the more
uncommon or ‘rarer’ species (Patterson, 1990).
Statistically significant nested patterns are one example of non-random species
distributions (Schoener & Schoener, 1983; Bolger, Alberts & Soulk, 1991; Patterson
& Brown, 1991). In this study the degree of nestedness was estimated using the
method of Wright & Reeves (1992). This protocol avails of a new measurement of
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 115

nestedness, Nc, based upon counting the number of times a species’ presence at a
site correctly predicted its presence at a richer site, and then summing the counts
across species and sites. Cochran’s Q statistic was then used to estimate the
significance of this nestedness metric. This new metric can also be standardized to
provide a measurement of the relative degree of nestedness, i.e. an index which is
independent of the size of the species presence-absence matrix. This standardized
index of nestedness, called ‘C’, is given by :

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C= Nc-E P C I
max P C I -E ”J
where E”c] is the expected value and max[Nc] is the value it would take if the
matrix was perfectly nested (Wright & Reeves, 1992). The great advantage in using
the C-index is that it allows comparison between data sets with different numbers
of species and sites. The index varies from small negative values-which indicate a
matrix less nested than would be expected at random-to C = 1.0, for a perfectly
nested data set.
Statisticallysignificant nestedness in the fauna of fungal sporophores would indicate
non-random patterns of distribution at the level of microarthropod assemblages. Non-
randomness in individual microarthropod species distributions was assessed using
incidence functions (Diamond, 1975) and the Mann-Whitney U statistic. Incidence
functions describe the probability of a species’ presence on an island or habitat
fragment (Taylor, 1991).They were constructed by ranking sporophores by increasing
species richness and grouping these data into a number of classes of species richness.
The number of occurrences (the incidence) of a species within a class is then plotted
against the mean species richness for each sporophore class. The Mann-Whitney U
statistic was then used to determine whether a given species’ distribution was
significantly ordered on sporophores, which again, were ranked according to in-
creasing species richness. The significant ordering of a species’ distribution was
estimated by comparing the ranks of sporophores where the species occurred with
those where it was absent. Incidence functions have been used to infer the potential
dispersal and/or colonization ability of individual species and Peltonen & Hanski
(1991) demonstrated empirically that incidence functions provide good estimates of
a species’ observed colonization and extinction rate. In this analysis Mann-Whitney
tests were used to provide a statistical basis for grouping species with the same or
similar patterns of incidence into incidence categories s m u Diamond (1975).

CUMULATIVE SPECIES-AREA CURVES

The cumulative species-area curves for Heterobasidion annosum, Hypholoma fasciculare,

and the pooled agarics (all other agarics in this study) are presented in Fig. 1 (A-C).
All three data sets display a similar pattern, with the small-to-large curve rising
more steeply than the corresponding large-to-small curve. This indicates that the
curve saturates more quickly with additional microarthropod species when the
smallest sporophores are added together first and implies that, for any value of
cumulative area, a greater number of small sporophores will encompass a higher
species diversity than a lesser number of larger sporophores.
116 T. O'CONNELL AND T. BOLGER

250
A
200

160

100

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b b
0 1000 2000 3000 4000 6( 00
160
B
140
I120
.r(

100
.g 80
s
'3 60
8 40
/
20
I I I I I I
0 100 200 300 400 600 600 700

0 200 400 600 800 1000

Cwk&&ive area (weight)

Figure 1, Cumulative Species-Area (Weight) curves for (A)H e t n o b d w n annosurn, (B) H y k h o l mfmciculare
and (C) the pooled agarics. (0)Small-to-large and (0)Large-to-small sporophones.

The,slopes of the small-to-large curves are very similar for the three datasets.
However, the slopes become progressively less steep from the curve representing
greatest habitat dividedness (the small-to-large curve of the agarics) to that rep-
resenting the large-to-small sporophores of H. unnosum. In fact, the large-to-small
curve of H. unnosum accumulates species at a much slower rate. This curve represents
minimum habitat dividedness for this dataset implying that cumulative species
diversity was reduced as sporophore size increased and relative dividedness was
 MICROARTHROPOD ASSEMBLAGES O N FUNGAL SPOROPHORES 1 I7

TABLE 1. Nestedness of the fauna from Hekmbasidion annosum sporophores

at five sites, pooled Hypholoma fasciculare, and Hypholoma fasciculare at four
sites. (* R0.05; ** RO.01; *** RO.001)
~____

Dataset Cochran’s Q C-Index of nestedness

Hem H. anno.wm 1452.51 *** 0.5796

Ss3 H. anno.wm 463.61 *** 0.4622
Ss4 H. annosum 67.15 N.S. 0.1176
Mix1 H. annosum 72.26 N.S. 0.0851

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Ns H. annosum 154.17 *** 0.2379
Ssl H . JarCiulare 48.32 ** 0.1279
Ss2 H. faciruh 13.11 N.S. 0.4622
M i 2 H.faciculare 87.19 * 0.1140
sp2 H.facicuhre 95.98 N.S. 0.1321
Pooled H. fm6culare 658.52 *** 0.2714

C>O.G-High relative nestedness

0.3<C<O.6-Medium relative nestedness
C<O.S--LOw relative nestedness
(After Wright & Reeves 1992)

reduced. The largest sporophores of H. annosum were, however, the most species
rich and thus habitat subdivision (or dividedness) was a crucial factor in this
cumulative species-area relationship.

NESTEDNESS

The microarthropod fauna of H. annosum, at three out of five sites, were significantly
nested (Table 1). The entire fauna of H. annosum from the Hem and Ss3 sites were
very significantlynested (P<<O.OO1) with C-values indicating medium levels of relative
nestedness (Table 1 ) . Only four samples were collected at the Ns site but most were
very species rich with between 43 and 75 species. The fauna was significantly nested,
yet the C-index was low (C =0.2379) relative to the Hem and Ss3 samples. At Ss4
the fauna was not significantly nested but this may have been a result of the lower
species richness of oribatid mites recorded at this site (O’Connell, 1994). A small
number of samples (n=4) were collected at Mix1 and the fauna here, also, was not
significantly nested.
The results of the nestedness analysis for the fauna of H. farciulare are also
presented in Table 1. Sporophores from both the Ss 1 and Mix2 sites had significantly
nested faunas while samples collected at Ss2 and Sp2 were not significantly nested.
A small number of samples at Sp2 and small species-poor sporophores at Ss2
probably account for the non-significant results at these sites. Although the fauna
of the H.fmciculare sporophores at Ss 1 and Mix2 were significantly nested, the relative
nestedness was low (C =0.1279 and C = 0.1 140, respectively).When sporophores of
H. fasciculare from all sites were pooled together the fauna was very significantly
nested (P<< 0.001) yet the index still remained relatively low (C = 0.27 14).
Thirty-four microarthropod taxa, from a total of 103, were found exclusively on
H. fmciculare sporophores at the Mix2 site. Therefore, in order to gauge the degree
of relative nestedness (i.e. overlap) in the fauna of the smaller sporophores, a
comparison was made between the fauna of the agarics including and excluding
I18 T. O’CONNELL AND T. BOLGER

TABLE 2. Nestedness of the fauna from four sites with pooled agarics and
the Bir-Piploporus betulinw site (* -0.05; ** -0.01; *** RO.001).
Dataset Cochran’s Q C-Index of nestedness

Pooled Ns agarics 255.81 *** 0.2397

Ns agarics (except H. fmhlurc) 112.78 *** 0.1574
Pooled Mix2 agarics 329.21 *** 0.2419
Mix2 agarics (except H.fnrcinrlan) 132.01 *** 0.1073
Pooled Spl agarics 276.45 *** 0.1513

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Spl agarics (except H. farciculan) 198.80 *** 0.1 157
Pooled Sp2 agarics 590.45 *** 0.2433
Sp2 agarics (except H. fmciculaw) 362.09 *** 0.1746
Pooled Bir fungi 145.66 *** 0.0760
Pipkrporus betalinus only 134.44 *** 0.1224

the H. fmciculure samples at this site and three other sites where H. fmcicuhre alone
accounted for a large number of taxa. These results are presented in Table 2. The
faunas of all sites were very significantly nested (P<<
0.00 1) whether the H.fmciculure
sporophores were included or not. Removal of the H. fmciculure samples was most
notable in producing a concomitant reduction in the already low relative value of
the nestedness index. Hence removal of the most species rich samples was not
enough to break down this apparently robust pattern of species distribution, but it
noticeably suppressed the value of the C-index.
The results of the nestedness analysis for the Bir site are also presented in Table
2. Here the nestedness of the fauna of Piptopom betulinus sporophores was contrasted
with the nestedness of the fauna of the pooled fungi at this site. Both faunas were
very significantly nested (P<<O.OOl)but the fauna of the pooled fungi had very low
relative nestedness (C =0.0760).
The nestedness analysis was extended to search for patterns of nested distributions
among the microarthropod functional groups. The complete faunas from the three
datasets were subdivided into four functional groups based on the major feeding
preferences of the constituent species. The results for the microphytophage (feeding
on microflora), macrophytophage (feeding on deadldecaying higher plant material),
panphytophage (non-selective feeders) and predator groups collected from spo-
rophores of (i) H. annosum at the Hem and Ss3 sites; (ii) the pooled H. fmciculure
sporophores; and (iii) the pooled agarics (excluding H. fmciculure) at the Mix2, Sp 1,
Sp2 and Ns sites are presented in Table 3. A highly non-random nested pattern

TABLE
3. Relative nestedness of the fungal fauna after division into its constituent functional groups
Dataset Micro- Macro- Pan- Predators
phytophages PhytOPhageS phytophagcs
C Prob. C Prob. C Prob. C Prob.

Hem H. annosam 0.6005 RO.001 0.6686 RO.001 0.6616 RO.001 0.5259 RO.001
Ss3 H. annosum 0.4495 RO.001 0.9390 RO.0OI 0.4522 RO.001 0.4465 RO.001
Pooled H. f u k u h m 0.2406 RO.001 0.3862 RO.001 0.5794 RO.001 0.1672 R0.001
Pooled Ns agarics 0.1878 RO.001 0.2443 R0.05 0.1579 R0.05 -0.290 N.S.
Pooled Mix2 agarics 0.1557 RO.001 0.0943 N.S. 0.0689 N.S. 0.0121 N.S.
Pooled Spl agarics 0.1325 RO.001 0.1063 N.S. 0.2831 RO.001 -0.046 N.S.
Pooled Sp2 agarics 0.2010 RO.001 -0.041 N.S. 0.0472 N.S. -0.099 N.S.
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 119

(P<<O.OOl) was detected for all four functional groups in the H. annosum samples
and for three of the four groups in the H. fmdculare samples. The micro-, pan-, and
macrophytophagegroups from H. annosum at Hem were in the high relative nestedness
category (see also Table 1) of the standardized C-index, with the macrophytophages
and panphytophages having the highest index values, respectively. A similar pattern
emerged for the groups at Ss3 but only the macrophytophages were in the high
nestedness category (C = 0.9390). There was greater variation in the C-index for
the functional groups on H. fmciculare and all groups except the panphytophages

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were highly nested (p<O.OOl). Predators were the only functional group not sig-
nificantly nested in the pooled agarics from the Ns site but relative nestedness
was always low. In contrast, only the microphytophages had consistently nested
distributions in the pooled agarics at the other three sites, although the. pan-
phytophages at Spl were also significantly nested, and again the index of relative
nestedness was low.

INCIDENCE FUNCTIONS AND MA"-WHITNEY TESTS

Species whose occurrence in fungal sporophores was not significantly ordered in

relation to the richness of the fauna were interpreted as being B-tramps s m
Diamond (1975). Extension of this method to include the entire fauna, suggests that
species with significant differences in their distribution and which were found
predominantly on sporophores with high average rank were A-tramps. Species with
a significant difference in their distribution but which were absent only from a small
number of sporophores of low average rank were C-tramps, while species present
on all or all but one sporophore were D-tramps. At the opposite end of the
continuum, species present only on the highest ranked sporophores were considered
equivalent to Diamond's High-S species.
Forty-one species, chosen as a representative sample of the microarthropod fauna
of fungal sporophores, were investigated according to these criteria. The incidence
functions (Figs 2 and 3) illustrate a variety of patterns for some of these species. For
most species examined there was agreement between the Mann-Whitney test and
the shape of the incidence functions, e.g. most C- and D-tramps had very similar
incidence functions (Fig. 2A). On H. annosum, for example, the C-tramps C e p k
latus C.L.K. and Chamobates cuspidatus (Mich.) had similar incidence functions as did
the A-tramps Pugamasus runciger (Berl.) and ,@coonopsis remiger (Kr.) (Fig. 2B). For some
species the incidence functions remained the same irrespective of site or species of
fungus (Fig. 3A), but for others they changed. The most striking differences were
usually between a species on H. annosum and the same species collected from one
of the various agarics, e.g. Pla&othrus peltfir C.L.K. (Fig. 3B). The results for the
entire 40 species are presented in the Appendix.
The fauna of H. annosum at the Hem and Ss3 sites had microarthropod species
in each of the five incidence categories described above with C-tramps comprising
the single largest category in the fauna at this site (see Appendix). In stark contrast,
the majority of species were considered A- or B-tramps at all other sites and no C-
or D-tramps were found in the pooled agarics from the Ns, Mix2, Spl , or Sp2 sites.
The H. fasciculure assemblages contained only two C-tramp species but there was
evidence of a strong site effect in these samples.
120 T.O'CONTVELL AND T. BOLGER

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0.1 -

0.0

S (speciesrichness)

t
0.9 -

0.8 -
0 Rrunciger

V R lapponicus
A Zremiger
"I
0.7 -
-# 0.6 -
3
.s
v
CJ
0.5
-

0.4 -

0.3 -

0.2 -

0.1 -

0.0 I-
90 100
S (species richness)
Figure 2. Incidence functions of (A) C- and D-tramp and (B) A-tramp microarthropods from H.
annosum at the Hem site.
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 121

:::I
1.01A
7

0.7
0 Mix2

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Spl
A Ns
v sp2

% 0.4 1 +
+
H. fasciculare
Heannosus

o.21
0.1

0.0 L- -0 10 20 30 40 50 60 70 80 90 100
S (species richness)

-2
v
TJ
0.8

0.7

0.6
a.i0.5
0.4
x V H. fasciculare
+ H.annosus
0.3

0.2

0.1

0.0

S (species richness)

Figure 3. Incidence functions for (A) Oppia obsoleta and (B) Plapwthtus pelti& at different sites.
I22 T. O’CONNELL AND T. BOLGER

Individuals of 0pp;ella nova (Oudms.) and Tarsomus talpae Schaarschmidt were

present in every sporophore of H. annosum collected at the Hem site and Oppk
obsohtu (Paoli)was present in all but one of these samples. In total, 20 microarthropod
species were found in at least half of the sporophores collected at this site. Cepheus
latus, Ohdiscus minima (Kr.), and Schwiebaa sp. Oudms. were present in all but one of
the H. annosum sporophores collected at the Ss3 site with a total of 17 species found
in at least half of the samples. Only 0. obsohtu and Isotoma notabilis SchafX were
present in 50% or more of the H. f a k u l a r e samples. No microarthropod species

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were found in more than half of the pooled agaric samples at the other four sites,
although individuals of T. talpae were present in half of the sporophores collected at
the Ns site. In general, 0. obsohta and T. talpae were the most frequently collected
microarthropods from sporophores in the dataset.
Considering microphytophages comprised the single largest functional group on
most sporophores, it was not surprising that most C- and D-tramps were also
microphytophages, although C. htus and C. cuspidatus were notable exceptions (on
H. annosum)in the Appendix. High-S species, A- and B-tramps were disproportionately
represented by predators and to a lesser extent by macrophytophages. Nevertheless,
there were notable exceptions such as the aforementioned C. latus and Viaia
nemorm-is (Koch)-a C-tramp-on H. annosum.

HABITAT DMDEDNESS AND ‘TEMPORAL STABILITY’

The hypothesis that increased resource dividedness (or patchiness) promotes

species coexistence and diversity has been explored extensively both theoretically,
experimentally, and in the field (Atkinson & Shorrocks, 1981; Kneidel, 1985;
Rosewell, Shorrocks & Edwards, 1990). It has been demonstrated that increasing
resource dividedness (up to a critical level) facilitates coexistence of potentially
competing species and elevates species diversity, as vacant resource patches can
serve as ‘probabilistic niches’ for inferior cmpetitors. In patchy environments,
species richness is expected to accumulate with numbers of habitat patches. The
cumulative species-area analysis of faunas from the bracket fungus H. annosum, H.
fasicuhre and the other pooled ‘mushroom-type’ agarics, consistently demonstrated
that several small sporophores maintained a greater cumulative microarthropod
I

species diversity than a lesser number of larger sporophores of equivalent total area
(Fig. 1). The curve representing maximum sporophore dividedness (or patchiness)
and minimum size-the small-to-large curve of the ‘mushroom-type’ agarics-is
also the curve accumulating species at the greatest rate. The slopes of the remaining
curves become progressively less steep, accumulating species at a slower rate, as
habitat dividedness is decreased. The curve minimizing sporophore dividedness and
maximizing size accumulated species at the slowest rate despite the fact that it
contains the most species rich samples, i.e. the, large-to-small curve of H. annosum.

Implications

The question of whether single large or several small (SLOSS) habitats of

equivalent total area maintain the greatest species diversity is one of the vexed
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 123

contributions of community ecology to the field of conservation biology (Diamond

& May, 1976; Simberloff & Abele, 1982). Simberloff & Abele (1982) noted that
evidence cited supporting either side of the debate was often anecdotal or equivocal,
but where clear cases have been established they almost always demonstrated that
several small areas maintain greater species richness, e.g. 29 out of 30 cases in one
study (Quinn & Harrison, 1988). The data from this study conclusively illustrate
that several small sporophores, on average, encompass greater species diversity than
a single large sporophore. The key point is, however, that the curve representing

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the greatest cumulative diversity (for all datasets) is composed entirely of very
ephemeral (mostly small) habitat patches whereas the curve accumulating diversity
at the slowest rate represents much larger stable and essentially perennial habitat
patches. The idea that ephemeral habitats promote high species diversity is not,
however, new (Elton, 1927).

irhe paradox

Edge effects, habitat diversity, disturbance, and interspecific variation in dispersal

abilities, colonization and extinction rates are factors which may account for the
difference between the large-to-small and small-to-large curves (Quinn 8z Harrison,
1988). Many microarthropods in litter and soil are associated with microbial and
vegetational transitions and since the relative perimeter of habitats increases with
increasing subdivision, ‘edge species’ may elevate the species diversity of groups of
small sporophores relative to that of fewer large sporophores of equivalent area. At
the scale of individual fungus fructifications, complex patterns of sporophore growth
and development (e.g. larger, often older, sporophores of H. annosum potentially
encompass greater habitat diversity with areas of old ‘woody’ tissue and ‘fresh’ newly
developing layers of spore tubes) present a potentially confusing scenario where it is
possible to imagine, paradoxically, collections of both larger and smaller sporophores
having the greatest species richness. Larger islands may be less susceptible to
environmental disturbance than smaller islands (MacArthur & Wilson, 1967) and
greater disturbance levels among smaller sporophores (e.g. fructifications in the field
which are partially consumed by slugs etc.) may promote the diversity of the entire
fungal fauna. The greater perimeter of multiple small sporophores and increased
spatial heterogeneity of highly divided resources increases their statistical likelihood
of being encountered by potential colonists with high dispersal and colonization
rates. This pattern of habitat invasion can also produce significantly nested species
distributions (Bolger et al., 1991).

Spomphores as ‘islands’

Fungal sporophores, from the point-of-view of microarthropod colonists, may be

more accurately described as patchy (often ephemeral) habitats in an extremely
heterogeneous environmental mosaic rather than as ‘islands’in the true sense of the
word. Also, fungal patches tend to be in intimate contact with the source area of
the potential colonists-humus, litter, decaying wood, and arboreal habitats-
unlike true (e.g. oceanic) islands. Although a specificity for fungal tissue has been
described for some microarthropods collected during this study (Graves, 1960;
I24 T. OCONNELL AND T. BOLGER

OConnor, 1984),there was no evidence of a tight coupling between fungi and any
microarthropods in this dataset, except perhaps for Dinychus sp. and Ganodma
sporophores (O’Connell, 1994). This study, nevertheless, has demonstrated the
heuristic value of considering fungal sporophores as ‘islands’ despite the potential
oversimplification of this system that this may entail.

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HIERARCHICAL STRUCTURE

Nested patterns are one example of non-random species distribution and in recent
years they have been found to characterize the distribution of a wide variety of taxa
-plants, mammals, birds, reptiles and beetles-in a variety of different habitats,
e.g. oceanic and landbridge islands as well as various terrestrial habitat isolates
(Patterson & Brown, 1991; Wright & Reeves, 1992). This study has demonstrated
that the species distribution of microarthropods on fungal sporophores is also highly
nested (see Tables 1-3). The fungal faunas from H. annosum had the highest levels
of relative nestedness followed by H. fmciculure, P betulinus and the pooled agarics,
respectively. The trend of decreasing nestedness from the fauna of perennial (H.
annosum) sporophores to those of very ephemeral sporophores suggests a gradient of
decreasing relative nestedness with decreasing temporal stability.
The study of Wright & Reeves (1992) noted that all datasets in the high relative
nestedness category were systems dominated by extinction, such as landbridge islands
with ‘relaxing’faunas or the ‘relict’ faunas of terrestrial habitat isolates. In contrast,
systems in the low nestedness category had faunas very influenced by dispersal, e.g.
deepwater islands or oceanic archipelagoes. It was suggested that, over time, species-
specific extinction rates may produce highly nested deterministic faunas as species
go extinct in a predictable sequence while immigration may obscure this pattern by
enabling species which were extinct to re-establish themselves. Conversely, Patterson
(1990) found strong patterns of nestedness in systems dominated by immigration
due to consistent species-specific ordering of colonization, while Ryti & Gilpin (1987)
observed a strong correlation between colonization ability and non-randomness
(nestedness) among species presence-absence matrices. The agarics and P betulinus
shared a number of important characteristics; relatively impoverished and un-
predictable faunas with low numbers of individuals and species (O’Connell, 1994)
and a low relative index of nestedness. The ephemerality of the agarics and the
position of betulinus sporophores high up on birch trunks suggests the primacy of
dispersal ability (vagility) for species exploiting these habitats, while the temporal
‘remoteness’ of the agarics along with the spatial ‘remoteness’ of r! betulinus may be
an important parallel between these systems and remote oceanic archipelagoes with
which they share low relative nestedness. The variance of stochastic processes
changes inversely with population size while colonizing species with low population
number immediately face a very high risk of extinction (Patterson, 1990), thus
immigration-driven systems with small populations are more likely to behave
stochastically than systems with large populations and a ‘relaxing’ fauna or the
slowly dwindling relict faunas of some terrestrial habitat isolates.
The H. annosum faunas were, in contrast, characterized by abundant and diverse
assemblages and their perennial sporophores are always found at the base of the
trunks of infected trees, surrounded by leaf litter. They may be more akin to ‘patches
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 125

of more favourable habitat’ for microarthropods than real habitat islands and high
immigration rates from the surrounding litter are to be expected. The durational
stability of these sporophores will facilitate true colonization-stablishing and
maintaining a stable population-as distinct from simple dispersal (Patterson, 1990).
Predictable species-specific immigration rates with or without the life-history at-
tributes often necessary for colonization, particularly among species such as the
oppiids and tarsonemids (Norton et al., 1993), appear responsible for the patterns of
strong nestedness in the faunas of H. annosum. The low relative nestedness typical

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of the dispersal-driven systems of the pooled agarics and 2 betulinus suggests the
primacy of stochastic dispersal (with or without persistence) for these faunas.

Why a nested hierarchy?

Factors producing nested subset structure are those which control species incidence
over habitat patches, i.e. individual species immigration and extinction rates (Peltonen
& Hanski, 1991) and these processes are currently receiving much attention with
the development of metapopulation theory (Gilpin & Hanski, 1991). Nestedness
among species within a single guild or functional group depends on hierarchical
ecological relationships among species, causing some to be more restricted in their
distribution and perhaps more specialized in their ecological requirements than
others (Patterson & Brown, 1991). The faunas of H. annosum, H. fmciculare and the
pooled agarics when divided into functional groups again produced very significant
patterns of nestedness (Table 3) in all datasets. Microphytophages were always
significantly nested and had highly non-random distributions on all sporophores.
Macrophytophages and panphytophages, when significantly nested, had higher
relative nestedness while predators either were not significantly nested (in the agarics)
or had low relative nestedness. The functional groups from H. annosum had the
greatest relative nestedness followed by H. fmciculare and the agarics, respectively.
This suggests that the structure of whole faunas (Tables 1-3) are driven by highly
non-random distributions of species within functional groups (Table 3) and that
faunas of individual sporophores could be modelled by assembly rules based on
functional groups, e.g. the model of Fox & Brown (1993). Graded differences in
vagility coupled perhaps with other biotic and abiotic factors (location in the litter
or fungal associations, for example) appear to be the processes underlying this
consistent pattern of distribution across fungus species, samples and sites and this is
of particular importance in the context of metapopulation studies. Drake et al. (1 993)
described how assembly processes operating in an artificial system of patches can
produce differences in structure among interconnected patches owing to interspecific
differences in invasion success and persistence.

THE EVIDENCE FROM INCIDENCE

Schoener & Schoener (1983) used Mann-Whitney tests to demonstrate that a

large number of lizard, spider and bird species distributions were highly non-
randomly related to island characteristics in the Bahamian island system. In this
study, Mann-Whitney tests (Appendix) and the consistency of incidence functions
126 T. O’CONNELL AND T. BOLGER

for species in the same incidence category (Fig. 2), or for a given species at different
sites or from different species of fungi (Fig. 3A), have together demonstrated that
many microarthropod species have highly non-random distributions among the
fungal assemblages at each site. Incidence functions provide good estimates of
species’ observed colonization and extinction rates (Peltonen & Hanski, 1991).Larger
sporophores of Heterobdwn annosum hosted very abundant and diverse communities
(O’Connell, 1994)with faunas which included many C- and D-tramps as well as B-
tramps and significant numbers of ‘rarer’A-tramp and High-S species, e.g. Phthiracaw

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and Pegamasus species, which by definition have relatively narrow distributions
(generally macrophytophages and predators). In fact, Phthirucam species are pref-
erentially xylophages (feeding on woody tissues), so their abundance in the larger
H. annosum sporophores appears to confirm the suggestion that these are the oldest
sporophores. Typically, faunas of small H. anmsum sporophores comprised several
C- and D-tramp species, i.e. ‘common’ species with high dispersal rates and wide
distributions(mostlymicrophytophages).The H.annosum microarthropod assemblages
bear the hallmarks of an equilibrial community s m u Gee & Giller (1987) and
potentially rapid colonization of these stable, perennial, high quality resources by
highly mobile species in the surrounding litter may make this system the obverse of
the highly nested ‘relict’ and ‘relaxing’ faunas of Wright & Reeves (1992).
Conversely, sporophores of the pooled agarics and I? betulinus are characterized
by low abundance and diversity (O’Connell, 1994), with most species found only
on larger sporophores even among those previously categorized as C- or D-tramps
on H. annosum. Nevertheless, the species with the highest incidence on these
sporophores were the C- and D-tramps from H. annosum, e.g. various oppiid species,
Chamobates cuspidatus, C e p h latu.s, Paradamam clavapes (Herm.) and Tarsonemus tulpae.
Greater unpredictability of their occurrence among the pooled agarics has resulted
in their incidence categories being shifted back towards the more restricted dis-
tributions of A- and B-tramp species, a pattern identical to the ‘inter-archipelagal
shifts in incidence category’ described by Diamond & Marshall (197 7). They observed
conspicuous differences in the distribution of species among incidence categories for
bird species found in common between two or three oceanic archipelagoes differing
in ‘remoteness’ from the source of colonists, with some species shifting at least two
categories in the direction of D-tramps towards High-S species. These species may
be the ‘core species’ of Hanski (1982) which remain dominant over space and time
despite constant variation in species composition in non-equilibrium environments
(Gee & Giller, 1987).
The great ephemerality of agaric sporophoresand the extreme spatial heterogeneity
of sporophore distribution suggests that environmental stochasticity and interspecilk
variation in immigration (and possibly extinction) probabilities (Hanski, 1991) may
be the primary factors structuring these fungus-microarthropod assemblages. The
pattern of species distribution on sporophores of H. faciculare appeared to be
somewhat intermediate between that of H.annosum and the agarics, as some species
were found consistently in significant numbers-mainly C- and D- tramps of H.
annosum-while most species had ‘narrow’ distributions (A-tramps). Stanton &
Tepedino (1977) studying microarthropod communities in soil habitat isolates also
found species diversity increasing with increased number of resource patches and
concluded that these habitat ‘islands’ were undergoing constant colonization and
extinction.
 MICROARTHROPOD ASSEMBLAGES ON FUNGAL SPOROPHORES 127

CONCLUSIONS

How environmental conditions and life-history processes determine patterns of

species abundance and distribution has long been a central problem of ecology and
biogeography (Andrewartha & Birch, 1954; Hutchinson, 1959; Norton et al., 1993).
This study illustrates that coordinated analyses at the level of populations, functional
groups and individual species can provide greater insight into the factors driving
patterns of species distribution and abundance. Crucially, it is demonstrated here

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that the degree of ephemerality of resource patches (on a scale from highly
ephemeral to essentially perennial) and species-specificdispersal rates are vital factors
determining the structure, dynamics and composition of the attendant fauna. Gee
& Giller (1987) identified the equilibrium-nonequilibrium continuum and scale as
the two recurring themes in an investigation of a wide range of natural communities.
The study emphasises the key importance of these concepts.

ACKNOWLEDGEMENTS

We thank Jack Lennon for reading this manuscript and suggesting improvements,
Lucy Hammond for help with the figures, and all in the Terrestrial Ecology Unit,
University College, Dublin and the Population Biology Unit, b e d s University for
their advice and encouragement. In particular, we would like to thank three
anonymous referees for their assistance, great insight, and advice on improving this
manuscript.

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