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Vertical Stratification of Rainforest Collembolan (Collembola: Insecta) Assemblages:

Description of Ecological Patterns and Hypotheses concerning Their Generation
Author(s): D. J. Rodgers and R. L. Kitching
Reviewed work(s):
Source: Ecography, Vol. 21, No. 4 (Aug., 1998), pp. 392-400
Published by: Blackwell Publishing on behalf of Nordic Society Oikos
Stable URL: http://www.jstor.org/stable/3683174 .
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ECOGRAPHY21: 392-400. Copenhagen1998

Vertical stratificationof rainforestcollembolan

(Collembola:Insecta) assemblages:descriptionof ecological
patterns and hypothesesconcerningtheir generation
D. J. Rodgers and R. L. Kitching

Rodgers,D. J. and Kitching,R. L. 1998.Verticalstratificationof rainforestcollembolan (Collembola:Insecta) assemblages:descriptionof ecological patterns and
hypothesesconcerningtheir generation.- Ecography21: 392-400.
We describe a complex vertical stratificationof collembolan assemblagesfrom
rainforestleaf littersamplesand identifydistinctassemblagesassociatedwith forest
floor, lower canopy and upper canopy samples.Leaf litter sampleswere collected
fromthe forestfloor and depositsof leaf littersuspendedin epiphytesin the canopy
of a subtropicalrainforestsite at LamingtonNationalParkin southeastQueensland.
The patternsof relationshipamongassemblagesof Collembolaextractedfrom these
sampleswereexaminedusinga varietyof analysesof a matrixof similaritiesbetween
samples.The resultsof ANOSIM analysesshowed that forest floor, lower canopy
and uppercanopysamplesformeddiscretegroups.Theseresultspermita discussion
of these groupsas threedistinctcollembolanassemblages.Analysisof the dissimilarities betweentheseassemblagesrevealeda gradientof similarityfromthe forestfloor
throughthe lower to the upper canopy. This gradientrepresentsa more complex
vertical stratificationthan has previously been identified in rainforestcanopy
arthropods.We suggestthat limitationson the dispersalof some forestfloor species
into the canopy may be responsiblefor this pattern. We also identify a second
gradientof similaritiesamongthese assemblages.We show that dissimilarityamong
samplesfromforestflooris significantlylowerthandissimilarityamongsamplesfrom
within the lower canopy, and that the level of dissimilaritybetweensamplesfrom
within the upper canopy is significantlyhigher again. We suggest that dispersal
barriersand higherprobabilitiesof extinctionin uppercanopycollembolancolonies
may be responsiblefor higherheterogeneityof speciescompositionand abundance
among samplesfrom the uppercanopy.We outlinea numberof testablehypotheses
aimedat determiningthe importanceof theseprocessesin producingthe patternswe
have observed.
D. J. Rodgers and R. L. Kitching, CooperativeResearch Centrefor TropicalRainforest
Ecology and Management, Griffith Univ., Nathan, Qld, 4111 Australia.

It is now generally accepted that the canopies of rainforests in various parts of the world are extremely rich
in arthropod species (Stork 1987a,b, Basset 1991, Erwin
1991, Kitching et al. 1993, Guilbert et al. 1995). Although the task of survey and inventory of these organisms will continue more or less indefinitely, the
attention of ecologists is now being focussed on the
underlying mechanisms which generate and maintain

this diversity and the patterns we observe within it

(Kitching et al. 1997, Stork et al. 1997).
Studies of the canopy faunas of Australian rainforests have been in progress since 1988 (Kitching et al.
1993). As our knowledge of these systems has grown, it
has become clear that the canopy is a far from homogeneous habitat. Many separate components of the
canopy ecosystem exist and arthropod assemblages

Accepted30 October1997
CopyrightC ECOGRAPHY1998
ISSN 0906-7590
Printedin Ireland- all rightsreserved
392

ECOGRAPHY 21:4 (1998)

The results of a comparative study of epiphytic and

reflect this heterogeneity. Any process-oriented understanding of canopy diversity must include a close exam- forest floor soil fauna by Paoletti et al. (1991) are
ination of the common habitat components within the difficult to interpret. The authors state that their samcanopy. Epiphytes are one of the distinguishing charac- ples could only be separated consistently to family or
teristics of rainforests in general and the arboreal an- sub-order level, yet draw conclusions regarding differgiosperms, ferns, bryophytes, lichens and fungi may ences in species composition between arboreal and terplay important roles in determining and maintaining restrial soil fauna. In the absence of a clearer
arthropod diversity. Few of these components have description of methods such conclusions cannot be
been studied in this context (but see references below). evaluated with respect to their relevance to the present
The subtropical rainforests of southeast Queensland study. These authors also state that species level analyhave a rich epiphyte flora often dominated by broad- ses must await the description of all species. We disleaved ferns such as Asplenium australasicum (J.Sm.) agree with this perspective and follow earlier canopy
Hook. The present paper focuses on collembolan as- workers and New (1996) in analysing the fauna followto recognisable biological units ('morphosemblages in leaf litter suspended A. australasicum ing sorting
in the rainforest canopy and leaf litter on the forest species').
One clear trend emerges from this limited literature:
floor. While the Collembola are not among the most
the
detection of ecological pattern at a scale as fine as
speciose of rainforest arthropod orders, they have been
the
contrast between ground and canopy arthropod
shown to dominate rainforest arthropod faunas in
faunas
requires species level data (e.g. Longino and
terms of abundance (e.g. Stork 1988, Kitching et al.
Nadkarni
1990, Fragoso and Rojas-Fernandez 1996).
1993, Guilbert et al. 1995). Stork (1988) has shown
at higher taxonomic levels may detect ecologiAnalyses
almost
half
of
Collembola
made
that, numerically,
up
an estimated 42.3 million arthropods in a single hectare cal pattern at a coarser scale such as that between
forests (e.g. Kitching et al. 1997), but often fail to do so
of Seram rainforest. Collembola were also found in all
at a finer scale (e.g. Nadkarni and Longino 1990,
rainforest biotopes examined by Stork (1988), i.e.
Paoletti et al. 1991).
canopy, ground vegetation, tree trunks, leaf litter and
In this study we tested a number of hypotheses
soil.
regarding
ecological distinctions between assemblages
There have been a limited number of previous studies
of Collembola associated with leaf litter on the forest
of invertebrate communities associated with leaf litter
floor and suspended in epiphytes in the canopy of a
suspended in epiphytes. Longino and Nadkarni (1990)
rainforest. The first hypothesis was that a
found a clear distinction between the ant species assem- subtropical
clear distinction between ground and canopy collemblage in leaf litter on the forest floor and that sus- bolan
assemblages would exist, either in terms of spepended in rainforest canopy epiphytes. In a study of the cies
or in the abundance of shared species.
composition
ant fauna associated with leaf litter suspended in AspleThe existence of similar distinctions between assemnium nidus on boulders, Floater (1995) found that only
blages in upper and lower canopy litter deposits, and
five of nine species found in ground litter were found in
large versus small litter deposits was also hypothesised.
suspended litter. Since no additional species were found
in epiphytic litter, the epiphytic fauna represent a simple subset of the ground fauna. Floater (1995) sampled
epiphytic litter only from epiphytes on boulders and Methods
only to a height of 2.5 m; accordingly, his study is of
limited value as a comparison to that of Longino and Site description, sampling design, field and
Nadkarni (1990). Nadkarni and Longino (1990) have laboratory methods
shown a fundamental similarity in the structure of Our study site was a 1 ha
plot of subtropical rainforest
assemblages of arthropods associated with rainforest within Lamington National Park in southeast Queenscanopy leaf litter and those in leaf litter on the forest land (28'15'00"S, 153008'50"E). The vegetation of this
floor. This similarity was based on the ordinal signa- area is complex notophyll vine forest (Webb et al.
tures of the assemblages and was not observed when a 1976), and described by Floyd (1990) as subtropical
species level analysis was carried out on a more exten- rainforest, Argyrodendronactinophyllumalliance, subalsive set of samples from the same site (e.g. Longino and liance 11 (Caldcluvia - Crytocarya erytroxylon - Orites
Nadkarni 1990). Most recently Fragoso and Rojas- - Melicope octandra - Acmena ingens). Canopy height
FernAndez (1996) have shown evidence of canopy/ on the site averaged ca 35 m.
ground habitat specialisation among earthworms in
We sampled canopy leaf litter from a single epiphyte
southeastern Mexican rainforests, with three species species, Asplenium australasicum. This is a common
occurring almost exclusively in ground litter and decay- epiphytic pteridophyte in tropical and subtropical raining logs and one almost exclusively in epiphytic brome- forests of eastern Australia, and western Pacific islands.
liads.
Asplenium australasicum grows commonly on boulders,
ECOGRAPHY 21:4 (1998)

393

Table 1. A systematiclist of collembolanspeciescollected,with total abundance,rank abundanceand proportionsof each

speciesfound in the canopy and on the forestfloor.
Total
abundance

Species
Entomobryidae
Acanthocyrtus spinosus (Sch6tt, 1917)

Ascocyrtuscinctus(Schiffer, 1898)

Rank
Ground
abundance
%

Canopy
%

112

15.2

1005

98.2

1.8

21

0.0

100.0

84.8

Entomobrya sp. Rondani, 1861

32

35

0.0

100.0

Lepidosira (Lepidosira) australica australica (Sch6tt, 1917)

Lepidosira sp. 2 Sch6tt, 1925
Lepidobrya sp. Womersley, 1937

28
87
35

22
12
19

82.1
0.0
0.0

17.9
100.0
100.0

30

50.0

50.0

Lepidocyrtoides sp. 2
Sinella termitum Sch6tt, 1917

4
45

28
18

100.0
100.0

0.0
0.0

559
92
1

4
11
33

32.0
96.7
0.0

68.0
3.3
100.0

26

100.0

0.0

150
48

7
16

100.0
60.4

0.0
39.6

rostrataGreensladeand Sutrisno,1994
Epimetrura

Lepidocyrtoides
sp. 1 Sch6tt, 1917

'

Paronellidae

Pseudoparonella queenslandica(Sch6tt, 1917)

Pseudoparonella sp. 2 Handschin, 1925
Pseudoparonella sp. 3
f

Tomoceridae
Lepidophorella
sp. Schaffer,1897
Isotomidae

Folsomides sp. Stach, 1922

Folsomina onychiurina Denis, 1931

Isotoma(Parisotoma)sp. Bagnall,1940

Isotoma (Isotoma) sp. Bourlet, 1893

Subisotoma sp. Stach, 1947
Neanuridae

Acanthanura
sp. B6rner,1906

Australonuraquarta Greenslade and Deharveng, 1990

Ceratrimeria
sp. B6rner,1906
Hemilobellasp. (cf. rounsvelli)Deharvengand Greenslade,1992(p
Pseudachorutella sp. Stacjh. 1949

Brachystomellidae

Brachystomella sp. Agren, 1903

Onychiuridae
Tullbergiasp. Lubbock,1876
Sminthuridae
Arrhopalites sp. B6rner, 1906
Katianna sp. B6rner, 1906
Neosminthurus sp. Mills, 1944
Pseudokatianna sp. Salmon, 1944
Sphaeridia sp. Linnanieme, 1912
Sminthurinussp. B6rner, 1901
Dicyrtomidae
Clavatomina sp. Yosii, 1966
Neelidae
Neelides sp. Caroli, 1912
Megalothorax sp. Willem, 1990

963

10.9

89.1

72
794

13
3

66.7
5.0

33.0
95.0

34

100.0

52

15

100.0

0.0

262
46

6
17

13.7
13.0

86.3
87.0

12

25

100.0

0.0

296

46.6

53.4

29

100.0

0.0

2
9
20
93
35
145

32
27
24
10
20
8

100.0
55.6
100.0
65.6
22.9
10.3

0.0
44.4
0.0
34.4
77.1
89.7

31

100.0

0.0

22
55

23
14

4.5
29.1

95.5
70.9

0.0

spp. 1 and 2 are distinguishedby the presenceof threeteeth on the innermarginof the mesotibiotarsalclaw
T Lepidocyrtoides
in sp. 1, and one tooth in this position in sp. 2.

fPseudoparonellaspp. 2 and 3 are distinguishedby the presencetwo rows of spinesextendingalong the full lengthof the dens
in sp. 2, and the absenceof dentalspinesin sp. 3.
<pHemilobellasp. differsfrom H. rounsvelliin having reducedthoracicand abdominaldorsal chaetotaxyand is thought to
representan undescribedspecies.
trees and lianas, rarely in full sun, and almost never in
the mineral soil. Its vertical distribution extends from
immediately below the uppermost canopy leaves to just
above the forest floor. Large specimens of A. australasicum can reach 3 m in diameter with individual fronds
up to a metre in length. We estimate that such specimens contain up to 40 1 of leaf litter in the bowl-like
crown of the plant, which itself reaches ca 1 m in
diameter.
We took 24 random samples of ground litter and 24
of canopy litter. Independence of the canopy samples
394

was maintained by sampling only a single epiphyte in

any given tree. Stratified random sampling of canopy
litter was carried out using to a two-way crossed design.
The two factors included in this design were the height
and size of the canopy litter deposit with two levels for
each factor. The two levels of the height factor adopted
were high (14-21 m) and low (0-7 m). The two levels
of the size factor were based on the surface diameter of
the litter deposit and defined as large (>500 mm diameter) and small (<300 mm diameter). All leaf litter
samples were 1 1 in volume. Arthropods were extracted
ECOGRAPHY 21:4 (1998)

from the samples in an array of Tullgren funnels and

preserved in 95% ethanol. Canopy access was achieved
using single rope techniques (e.g. see Perry 1978).
Following sorting and counting, representative specimens of all morphospecies were cleared in Nesbitt's
solution and slide mounted in Hoyer's medium. The
identification of all specimens was carried out by DJR
using a variety of keys and original species descriptions
where available. In the situation where morphospecies
could not be recognised as described species their genus

0
0

A *

Am
AA

SA
Lower
canopy

Upper
canopy

A [3
N

A
A.

A
A

2.5
-o

--e* 2

1.5

*A

0.5
*

U Ground
] Canopy 1

Smalllitterdeposits

Largelitterdeposits

Fig. 1. Mean collembolan abundance in ground, canopy

(pooled),and large and small litter depositsin the lower and
uppercanopy (errorbars are standarddeviations).
15
14 -

4
133

Lower

Upper

canopy

canopy

12

11

Ordinationaxis 1 (Variance = 18.58)

Fig. 3. Ordinationin threedimensionsof all leaf littersamples.

* Groundlittersamples,0 Lowercanopysmalllitterdeposit
samples, Ol Lower canopy large litter deposit samples, A
Upper canopy small litter deposit samples, A Upper canopy
large litter deposit samples.(Ordinationstress= 0.18).

10

9
8

was determined. Where this was not sufficient to discriminate between morphospecies (i.e. in the case of
congeners) morphological characters of established taxonomic value were used to discriminate between species.

7
,

6
5a

3
2
I

Ground

Smalllitterdeposits
Largelitterdeposits

Univariatestatistics

All species abundance data were log(x + 1) transformed

before analysis. This transformation stabilised variances
to some degree, but in many cases homoscedasticity
Fig. 2. Mean speciesrichnessin ground,canopy(pooled),and was not achieved. Where
homoscedasticity cannot be
and
small
litter
in
the
lower
and
large
deposits
uppercanopy
relied upon randomisation tests offer superior statistical
(errorbars are standarddeviations).

l Canopy

ECOGRAPHY 21:4 (1998)

395

power to standard non-parametric and parametric procedures, and are generally at least as powerful as equivalent parametric tests when the assumptions of the
latter are met (Manly 1991). Rather than using a mixture of parametric and non-parametric procedures with
variable comparability between results, we used randomisation tests for all analyses of variance and pairwise comparisons of means. The statistical software
used for randomisation tests was 'RT' (Manly 1996).

Lower
canopy

0 .-9

Upper
canopy

0.8
0.7

.-..
,
o

.6

0.5

0.4

0.3
0.1

Multivariate statistics

The Bray-Curtis dissimilarity measure was used to produce a sample dissimilarity matrix. The Bray-Curtis
dissimilarity measure was chosen from a number of

SSmalllitterdeposits

11Largelitterdeposits

Fig. 5. Meandissimilaritybetweencanopygroupsand ground

Table2. ANOSIMresults,statisticvalue,numberof permuta- for and largeand smalllitterdepositsin the lower and upper
tions and significancelevel of all pairwisecomparisons.
canopy (errorbars are standarddeviations).
Significancelevel %

Comparison

0.000
Ground/Canopy
1.5
Upper/Lowercanopy
13.4
Large/Smalllitter deposits
Lowercanopy, small/Lowercanopy
27.9
large litter deposits
Lowercanopy, small/Uppercanopy
small litter deposits
1.5
Lowercanopy, small/Uppercanopy
3.2
large litter deposits
Lowercanopy,large/Uppercanopy
small litter deposits
0.9
Lowercanopy,large/Uppercanopy
9.5
large litter deposits
Upper canopy, small/Uppercanopy
16.2
largelitter deposits
* 10000 was used as the default number of permutations
unless the numberof possiblepermutationswas <10 000. In
all such cases the numberof permutationsused representsa
full randomisationof the data (i.e. all possiblepermutations
were used).

0.9
0.8

Lower
canopy

0 .7

Upper
canopy

such measures because it captures differences in assemblage structure due to differences in both the abundance of shared species and species composition and is
among the most robust of such measures of ecological
distance (Faith et al. 1987). Accordingly, we use the
terms dissimilarity and difference in assemblage structure somewhat interchangeably in our interpretation of
our results. Based on this dissimilarity matrix, a threedimensional ordination plot was produced using semistrong hybrid multidimensional scaling (Belbin 1991).
Both the dissimilarity matrix and the ordination were
produced using the PATN pattern analysis package
(Belbin 1995).
The fundamental hypotheses of our study were tested
using the ANOSIM procedure first outlined by Clarke
and Green (1988). This procedure is based upon the
concept that if the dissimilarities between a priori
groups of samples are greater than the dissimilarities
within these groups of samples, then the groups are
likely to be discrete or have little overlap. In the
PRIMER (Anon. 1996) package which was used for
these analyses, the ANOSIM test statistic is calculated
as:

0 .6
R = (rB- rw)/(M/2)

o 0.5

0 .4

where rB and rw are the averages of all rank similarities

between and within a priori groups respectively, and
0 .2
M = n(n - 1)/2, where n is the total number of samples
0.1
under consideration (Clarke and Warwick 1994).
The significance of this statistic is determined by
0
comparing it with the distribution of the same statistic
Ground
Small litter deposits
when recomputed from the similarity matrix under
11Largelitterdeposits
Canopy
multiple random permutations of the sample (row)
labels (Clarke and Warwick 1994). Within PRIMER,
Fig. 4. Meanwithingroupdissimilarity(D) in ground,canopy ANOSIM
analyses can accommodate one-way and
(pooled),and large and small litter depositsin the lower and
uppercanopy (errorbars are standarddeviations).
two-way sampling designs as well as subsequent pair0.3

396

ECOGRAPHY 21:4 (1998)

Table3. Speciescontributingmost substantiallyto the significantdifferencesbetweenassemblagesas per ANOSIMresults.(For

betweengroups).
eachcomparisonthe specieslistedare the firstfive froma rankedlist of contributionsto averagedissimilarities
Average
Average Average% contributionto
abundance abundance
dissimilaritybetween
groups
Group 2
Group 1

Groupscompared
(Group 1/Group2)

Species

Ground/Canopy

Ascocyrtus cinctus
Isotoma (Parisotoma) sp.

41.13
4.38

Brachystomella sp.
Pseudoparonella queenslandica
Subisotoma sp.
Isotoma (Parisotoma) sp.
Pseudoparonella queenslandica
Sminthurinussp.
Acanthocyrtus spinosus

0.75
35.75

12.92
8.05

1.67

31.42

6.83

5.75
7.46
27.42
25.08
18.00
9.92
1.42

6.58
15.83
35.42
46.42
13.67
0.92
6.50

6.00
5.24
11.79
9.54
9.19
9.18
6.38

4.83
7.83

50.6
23.83

11.64
10.07

Acanthocyrtus spinosus
Sminthurinussp.
Pseudoparonella queenslandica
Pseudoparonella queenslandica

0.17
11.50
7.67
7.67

12.00
1.33
8.67
18.67

9.06
8.88
8.50
11.51

7.83

69.00

11.04

Sminthurinussp.

11.5

0.50

10.82

4.83

20.17

9.44

0.17

22.67

8.37

50.00

50.67

13.48

2.67
8.33
28.33
42.33

12.00
1.33
8.67
23.83

9.09
7.95
7.61
7.12

Subisotomasp.

Upper canopy/Lower canopy

Upper canopy, small/Lowercanopy Subisotomasp.

Isotoma(Parisotoma)sp.
small litter deposits

Upper canopy, small/Lower canopy

large litter deposits

Isotoma(Parisotoma)sp.
Subisotomasp.

Brachystomella sp.

Upper canopy,large/Lowercanopy Subisotomasp.

small litter deposits

Acanthocyrtus spinosus
Sminthurinussp.
Pseudoparonella queenslandica
Isotoma (Parisotoma) sp.

wise comparisons. Clarke and Warwick (1994) point

out that there is no procedure to protect these pairwise comparisons from an accumulation of the probability of type I errors, and simply advise caution in
interpreting the results of these tests.
We performed these analyses sequentially, such that
we first tested for differences between the structure of
ground and canopy assemblages in a simple one-way
ANOSIM. We then tested for differences in the structure of canopy collembolan assemblages using
ANOSIM for the two-way crossed design with the
two factors, litter deposit height and size (no interaction term is available in ANOSIM as in an analogous
two-way ANOVA). This was followed by pairwise
comparisons of the four groups of canopy samples,
i.e. low-small, low-large, high-small and high-large litter deposits.
In addition to ANOSIM analyses based on the ratios of within and between group dissimilarities, we
have analysed within and between group dissimilarities separately. The rationale for these separate analyses lies in the potential they provide for extended
ecological interpretation of the data. Analyses of the
relative magnitude of dissimilarities between a priori
groups of samples reveal which assemblages are most
closely and which most distantly related, as well as
gradients of relationship between them. Faith et al.
(1995) have for example used such analyses as a meaECOGRAPHY 21:4 (1998)

sure of the impact of pollutants on aquatic invertebrate communities. The separate analysis of multivariate dissimilarity within such groups provides a
comparison of their internal structure. For example, a
relatively high level of dissimilarity between samples
within a group is indicative of more heterogeneous
species composition and/or more variable abundance
among common species.
Our methods of analysis for these comparisons involved two simple stages. The first stage of data
preparation required extraction of the relevant blocks
of data from the dissimilarity matrix and conversion
of the extracted blocks of data to vectors. Randomisation methods were then used to test for significant
differences among the means of these vectors, either
pairwise or with two-way crossed designs.
The final stage of our analyses was to establish
which species were responsible for any distinction between assemblages. The identification of these discriminating species was achieved using the SIMPER
procedure in PRIMER, which performs a calculation
of the average contribution of each species to the
overall dissimilarity between any two groups of samples (Clarke and Warwick 1994).
In the following section the probability level used
in determining the significance of all statistical results
was 95%. Means, standard deviations and n are given
in the format (mean + SD(n)), unless otherwise stated.
397

Results
Thirty-five morphospecies of Collembola were identified from the samples (Table 1). A total of 5094
individuals were found in the samples. The total abundance of Collembola did not differ significantly between any of the components of the system (Fig. 1).
Species richness per sample was significantly higher in
litter samples from the forest floor (12.08 + 2.8 (24))
than in canopy litter samples (7.92 + 2.95 (24)). Species
richness per sample was also significantly lower in the
upper canopy (3.04 - 1.11 (12)) than in the lower
canopy (4.34 + 1.76 (12)), but did not differ significantly between large (8.08 + 3.12 (12)) and small
(7.75 + 2.89 (12)) litter deposits in the canopy, and
there was no significant interaction between these two
effects (Fig. 2). It should be noted that this does not
imply that the collembolan fauna of the forest floor is
significantly more speciose that that of the canopy. A
total of 28 species were found on the forest floor and 24
in the canopy (Table 1). The proportions of the total
abundance of each species found in the canopy and on
the forest floor show clearly that the canopy fauna was
not a simple subset of the ground fauna. For example,
Australonura quarta Greenslade and Deharveng 1990,
and Folsomides sp. were found exclusively in forest
floor litter while Lepidosira sp. 2 and Lepidobrya sp.
were found exclusively in canopy litter.
The results below provide a description of significant
relationships between sampling groups as objects in a
multivariate (multispecies) space. While these results
are reflected in the ordination plot (Fig. 3) they are
derived from analyses of the sample similarity matrix
they are not dependent upon the ordination. The ordination plot shown in Fig. 3, is provided as broadly
illustrative of all of the multivariate results outlined
below rather than their basis.
The results of a one-way ANOSIM comparison
showed a significant difference between forest floor and
canopy samples (Table 2, Fig. 3). A two factor
ANOSIM comparison of samples from within the
canopy showed a significant effect of height and no
significant effect of deposit size (Table 2). Lower and
upper canopy samples therefore formed significantly
different groups, while large and small litter deposits in
the canopy did not (Fig. 3). Subsequent one-way multiple comparisons of sample groups within the canopy
give some indication of the nature of these differences.
The collembolan assemblage in small litter deposits in
the upper canopy was also significantly different from
those in both large and small litter deposits in the lower
canopy (Table 2). The assemblage in large litter deposits in the upper canopy was also significantly different from that in small deposits in the lower canopy
(Table 2, Fig. 3). Although the significance of any
interaction between upper/lower canopy and large/
small litter deposit effects remains undetermined, the
398

results of these one-way multiple comparisons give a

strong indication of a significant interaction between
the effects of these two factors. Separate analyses of
both within group and between group dissimilarities
gave further evidence of significant differences between
these groups of samples.
There appears to be less dissimilarity among samples
from the forest floor (0.46 +_0.1 (276)) than among
samples from within the canopy (0.62 + 0.13 (276))
(Figs 3 and 4). A one-way randomisation test of these
within group dissimilarities showed that this difference
was significant. A two-way ANOVA using randomisation of dissimilarities within canopy groups showed no
significant effect of either the upper/lower canopy or
large/small deposit factors, but a significant interaction
of these effects. Subsequent one-way comparisons
showed that dissimilarities between samples from small
litter deposits in the upper canopy (0.69 + 0.12 (15))
were significantly higher than those between samples
from small litter deposits in the lower canopy (0.52 +
0.12 (15)) and large litter deposits in the upper canopy
(0.62 + 0.11 (15)). Dissimilarities between samples from
small litter deposits in the lower canopy (0.52 + 0.12
(15)) were also significantly lower than those between
large deposits in the lower canopy (0.62 + 0.11 (15))
(see Figs 3 and 4).
A two-way ANOVA using randomisation of dissimilarities between canopy and ground samples showed
significant effects of both upper/lower canopy and
large/small deposit factors, with no significant interaction. The nature of these differences was such that
lower canopy samples were significantly less dissimilar
with (0.71 + 0.1 (288)) forest floor samples than were
upper canopy samples (0.81 + 0.1 (288)) (Figs 3 and 5).
Large litter deposits within the canopy (0.74 + 0.09
(288)) were also significantly more closely related to
those from the forest floor than were those from small
litter deposits (0.75 + 0.09 (288)) (Figs 3 and 5).
Ascocyrtus cinctus (Schiffer 1898) is clearly the most
important species contributing to the distinction between ground and canopy litter samples, with an average abundance in ground litter samples of 41.13 and
only 0.75 in canopy litter samples, and contributed
12.92% of the total dissimilarity between ground and
canopy litter samples (see Table 3). Isotoma (Parisotoma) sp. ranked second among species contributing to
the distinction between ground and canopy litter samples contributing 8.05% of total dissimilarity between
these groups. In contrast to A. cinctus, Isotoma (Parisotoma) sp. was clearly a canopy species with an average
abundance of 35.75 in canopy litter samples and 4.38 in
ground litter samples.
The distinction between upper and lower canopy
litter samples was most substantially due to species with
higher abundances in the lower canopy. Subisotoma sp.
and Isotoma (Parisotoma) sp. for example had average
abundances of 35.42 and 46.42 in the lower canopy and
ECOGRAPHY 21:4 (1998)

27.42 and 25.08 in the upper canopy respectively. Conversely, Pseudoparonella queenslandica (Sch6tt 1917)
and Sminthurinussp. were more abundant in the upper
than the lower canopy with average abundances of
18.0, 9.92 and 13.67 and 0.92 in the upper and lower
canopy respectively (Table 3).
Pseudoparonella queenslandica, Subisotoma sp. and
Isotoma (Parisotoma) sp. also feature consistently and
prominently in the distinction between other significantly different groups as shown in Table 3.

Discussion
The ANOSIM results establish a clear distinction between the forest floor, lower and upper canopy collembolan assemblages. Our separate analyses of within and
between group dissimilarities have revealed gradients of
similarity among these assemblages of two distinct
forms. The first gradient is related to the level of
dissimilarity between assemblages. The lower canopy
assemblage is more closely related to the forest floor
assemblage than is the upper canopy assemblage. The
lower canopy assemblage therefore occupies an intermediate position between the upper canopy and the
forest floor assemblages. This first gradient is explained
by the occurrence of several species which are common
on the forest floor, in suspended litter deposits in the
lower canopy but not in the upper canopy. The second
gradient we have observed is an increase in the dissimilarity of samples within assemblages from the lower to
the upper canopy and from large to small litter deposits. Within the canopy, species composition is more
heterogeneous among small litter deposits than among
large deposits and more heterogeneous among upper
canopy deposits than among lower canopy deposits.
This represents a vertical stratification of a more
complex form than that reported by Longino and Nadkarni (1990). While their results show a clear distinction
between the ant species assemblages in leaf litter on the
forest floor and that suspended in rainforest canopy,
they did not distinguish between samples taken at different heights within the canopy and show no evidence
of a gradient similar to that which we have observed.
Although habitat specialisation would be sufficient to
explain the occurrence of distinct ground and canopy
assemblages, the complexity of the patterns we have
described suggests that they are the outcome of more
complex ecological processes. We agree with Paoletti et
al. (1991) that epiphytic plants and their associated soils
can be likened to a three-dimensional matrix of interconnected islands. The two major processes generating
the peculiar biogeographic patterns found among islands are: limited dispersal of fauna to islands and the
extinction of colonising species. We suggest that these
processes, operating at a very fine spatial and temporal
ECOGRAPHY 21:4 (1998)

scale, may play a significant role in producing the

patterns of relationship among these collembolan assemblages. The impact of some of these processes on
the structure of collembolan assemblages has been
demonstrated in both field and laboratory studies.
Hertzberg et al. (1994) have shown an increase in
demographic heterogeneity with patch isolation in several collembolan species among tussocks of Carex
ursina. Laboratory experiments by Haigvar (1995) have
also shown that a predictable decline in species richness
leads unpredictable changes in the species composition
in small isolated communities of Collembola.
An important characteristic of rainforest canopies,
with some potential limit the dispersal of Collembola
and cause the extinction of colonies in suspended litter
deposits, is the well-documented stratification of rainforest microclimates. Microclimatic conditions in suspended litter deposits would be expected to track those
in the surrounding air and vapour pressure deficits are
commonly higher in the upper canopy than on the
forest floor and in the lower canopy (e.g. Parker 1995).
Coupled with the sensitivity to desiccation, characteristics of many collembolan species (e.g. Butcher et al.
1971), microclimatic stratification could give rise to a
gradient in the extinction probabilities for Collembola
colonising canopy litter deposits. Small litter deposits
might also be expected to dry out more quickly than
large deposits. Collembolan colonies in small litter deposits in the upper canopy might therefore be extinguished more frequently than colonies in lower or
larger deposits. If recolonisation of upper canopy litter
deposits was also limited by the dryness of the surrounding environment, then the outcome would be very
similar to the patterns of stratification we have observed. An unpredictable outcome of such processes in
terms of the species composition of assemblages is
consistent with Higvar's (1995) results and would explain the high level of dissimilarity we observed among
samples from the upper canopy. We also suggest that
although the timescale over which these processes might
operate is unknown, it is possible that this system is
extremely dynamic and that colonies of some species
might be extinguished and re-established several times
within a month.
We do not overextend these hypotheses to include all
rainforest canopy arthropods. Although dispersal and
extinction probabilities undoubtedly play a role in determining the composition of assemblages in groups
such as the Coleoptera and Lepidoptera, it is possible
that among pterygote insects these processes act at very
different spatial and temporal scales to those we consider above.
Several questions requiring further research emerge
from our results and hypotheses. In the first instance,
our study should be replicated to assess the consistency
of these patterns on other rainforest sites and in winter
and summer. The extent to which other taxa show
399

similar patterns of stratification also requires study.

The suggestion of Paoletti et al. (1991) that suspended
litter deposits are akin to a matrix of interconnected
islands also requires further investigation. This would
be a more powerful analogy if it was shown that there
was little overlap in the species composition of the
fauna of tree trunks and suspended litter deposits.
- Financialsupportfor this researchwas
Acknowledgements
providedby the CooperativeResearchCentre for Tropical
Rainforest Ecology and Management.We also thank P.
Greensladefor her assistancewith the identificationof several
specimens.

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