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Vertical Stratification of Rainforest Collembolan (Collembola: Insecta) Assemblages:Description of Ecological Patterns and Hypotheses concerning Their GenerationAuthor(s): D. J. Rodgers and R. L. KitchingReviewed work(s):Source: Ecography, Vol. 21, No. 4 (Aug., 1998), pp. 392-400Published by: Blackwell Publishing on behalf of Nordic Society OikosStable URL: http://www.jstor.org/stable/3683174 .Accessed: 18/01/2012 16:10

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ECOGRAPHY 21: 392-400. Copenhagen 1998

Vertical stratification of rainforest collembolan (Collembola: Insecta) assemblages: description of ecological patterns and hypotheses concerning their generation

D. J. Rodgers and R. L. Kitching

Rodgers, D. J. and Kitching, R. L. 1998. Vertical stratification of rainforest collem- bolan (Collembola: Insecta) assemblages: description of ecological patterns and hypotheses concerning their generation. - Ecography 21: 392-400.

We describe a complex vertical stratification of collembolan assemblages from rainforest leaf litter samples and identify distinct assemblages associated with forest floor, lower canopy and upper canopy samples. Leaf litter samples were collected from the forest floor and deposits of leaf litter suspended in epiphytes in the canopy of a subtropical rainforest site at Lamington National Park in southeast Queensland. The patterns of relationship among assemblages of Collembola extracted from these samples were examined using a variety of analyses of a matrix of similarities between samples. The results of ANOSIM analyses showed that forest floor, lower canopy and upper canopy samples formed discrete groups. These results permit a discussion of these groups as three distinct collembolan assemblages. Analysis of the dissimilar- ities between these assemblages revealed a gradient of similarity from the forest floor through the lower to the upper canopy. This gradient represents a more complex vertical stratification than has previously been identified in rainforest canopy arthropods. We suggest that limitations on the dispersal of some forest floor species into the canopy may be responsible for this pattern. We also identify a second gradient of similarities among these assemblages. We show that dissimilarity among samples from forest floor is significantly lower than dissimilarity among samples from within the lower canopy, and that the level of dissimilarity between samples from within the upper canopy is significantly higher again. We suggest that dispersal barriers and higher probabilities of extinction in upper canopy collembolan colonies may be responsible for higher heterogeneity of species composition and abundance among samples from the upper canopy. We outline a number of testable hypotheses aimed at determining the importance of these processes in producing the patterns we have observed.

D. J. Rodgers and R. L. Kitching, Cooperative Research Centre for Tropical Rainforest Ecology and Management, Griffith Univ., Nathan, Qld, 4111 Australia.

It is now generally accepted that the canopies of rain- forests 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). Al- though the task of survey and inventory of these organ- isms 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 rain- forests 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 homoge- neous habitat. Many separate components of the canopy ecosystem exist and arthropod assemblages

Accepted 30 October 1997 Copyright C ECOGRAPHY 1998 ISSN 0906-7590 Printed in Ireland - all rights reserved

392 ECOGRAPHY 21:4 (1998)

reflect this heterogeneity. Any process-oriented under- standing of canopy diversity must include a close exam- ination of the common habitat components within the canopy. Epiphytes are one of the distinguishing charac- teristics of rainforests in general and the arboreal an- giosperms, ferns, bryophytes, lichens and fungi may play important roles in determining and maintaining arthropod diversity. Few of these components have been studied in this context (but see references below).

The subtropical rainforests of southeast Queensland have a rich epiphyte flora often dominated by broad- leaved ferns such as Asplenium australasicum (J.Sm.) Hook. The present paper focuses on collembolan as- semblages in leaf litter suspended A. australasicum in the rainforest canopy and leaf litter on the forest floor. While the Collembola are not among the most speciose of rainforest arthropod orders, they have been shown to dominate rainforest arthropod faunas in terms of abundance (e.g. Stork 1988, Kitching et al. 1993, Guilbert et al. 1995). Stork (1988) has shown that, numerically, Collembola made up almost half of an estimated 42.3 million arthropods in a single hectare of Seram rainforest. Collembola were also found in all rainforest biotopes examined by Stork (1988), i.e. canopy, ground vegetation, tree trunks, leaf litter and soil.

There have been a limited number of previous studies of invertebrate communities associated with leaf litter suspended in epiphytes. Longino and Nadkarni (1990) found a clear distinction between the ant species assem- blage in leaf litter on the forest floor and that sus- pended in rainforest canopy epiphytes. In a study of the ant fauna associated with leaf litter suspended in Asple- nium nidus on boulders, Floater (1995) found that only five of nine species found in ground litter were found in suspended litter. Since no additional species were found in epiphytic litter, the epiphytic fauna represent a sim- ple subset of the ground fauna. Floater (1995) sampled epiphytic litter only from epiphytes on boulders and only to a height of 2.5 m; accordingly, his study is of limited value as a comparison to that of Longino and Nadkarni (1990). Nadkarni and Longino (1990) have shown a fundamental similarity in the structure of assemblages of arthropods associated with rainforest canopy leaf litter and those in leaf litter on the forest floor. This similarity was based on the ordinal signa- tures of the assemblages and was not observed when a species level analysis was carried out on a more exten- sive set of samples from the same site (e.g. Longino and Nadkarni 1990). Most recently Fragoso and Rojas- FernAndez (1996) have shown evidence of canopy/ ground habitat specialisation among earthworms in southeastern Mexican rainforests, with three species occurring almost exclusively in ground litter and decay- ing logs and one almost exclusively in epiphytic brome- liads.

The results of a comparative study of epiphytic and forest floor soil fauna by Paoletti et al. (1991) are difficult to interpret. The authors state that their sam- ples could only be separated consistently to family or sub-order level, yet draw conclusions regarding differ- ences in species composition between arboreal and ter- restrial soil fauna. In the absence of a clearer description of methods such conclusions cannot be evaluated with respect to their relevance to the present study. These authors also state that species level analy- ses must await the description of all species. We dis- agree with this perspective and follow earlier canopy workers and New (1996) in analysing the fauna follow- ing sorting to recognisable biological units ('morpho- species').

One clear trend emerges from this limited literature: the detection of ecological pattern at a scale as fine as the contrast between ground and canopy arthropod faunas requires species level data (e.g. Longino and Nadkarni 1990, Fragoso and Rojas-Fernandez 1996). Analyses at higher taxonomic levels may detect ecologi- cal pattern at a coarser scale such as that between forests (e.g. Kitching et al. 1997), but often fail to do so at a finer scale (e.g. Nadkarni and Longino 1990, Paoletti et al. 1991).

In this study we tested a number of hypotheses regarding ecological distinctions between assemblages of Collembola associated with leaf litter on the forest floor and suspended in epiphytes in the canopy of a subtropical rainforest. The first hypothesis was that a clear distinction between ground and canopy collem- bolan assemblages would exist, either in terms of spe- cies composition or in the abundance of shared species. The existence of similar distinctions between assem- blages in upper and lower canopy litter deposits, and large versus small litter deposits was also hypothesised.

Methods Site description, sampling design, field and laboratory methods Our study site was a 1 ha plot of subtropical rainforest within Lamington National Park in southeast Queens- land (28'15'00"S, 153008'50"E). The vegetation of this area is complex notophyll vine forest (Webb et al. 1976), and described by Floyd (1990) as subtropical rainforest, Argyrodendron actinophyllum alliance, subal- liance 11 (Caldcluvia - Crytocarya erytroxylon - Orites - Melicope octandra - Acmena ingens). Canopy height on the site averaged ca 35 m.

We sampled canopy leaf litter from a single epiphyte species, Asplenium australasicum. This is a common epiphytic pteridophyte in tropical and subtropical rain- forests of eastern Australia, and western Pacific islands. Asplenium australasicum grows commonly on boulders,

ECOGRAPHY 21:4 (1998) 393

Table 1. A systematic list of collembolan species collected, with total abundance, rank abundance and proportions of each species found in the canopy and on the forest floor.

Species Total Rank Ground Canopy abundance abundance % %

Entomobryidae Acanthocyrtus spinosus (Sch6tt, 1917) 112 9 15.2 84.8 Ascocyrtus cinctus (Schiffer, 1898) 1005 1 98.2 1.8 Entomobrya sp. Rondani, 1861 32 21 0.0 100.0 Epimetrura rostrata Greenslade and Sutrisno, 1994 1 35 0.0 100.0 Lepidosira (Lepidosira) australica australica (Sch6tt, 1917) 28 22 82.1 17.9 Lepidosira sp. 2 Sch6tt, 1925 87 12 0.0 100.0 Lepidobrya sp. Womersley, 1937 35 19 0.0 100.0 Lepidocyrtoides sp. 1 Sch6tt, 1917 ' 2 30 50.0 50.0 Lepidocyrtoides sp. 2 T 4 28 100.0 0.0 Sinella termitum Sch6tt, 1917 45 18 100.0 0.0 Paronellidae Pseudoparonella queenslandica (Sch6tt, 1917) 559 4 32.0 68.0 Pseudoparonella sp. 2 Handschin, 1925 f 92 11 96.7 3.3 Pseudoparonella sp. 3 f 1 33 0.0 100.0

Tomoceridae Lepidophorella sp. Schaffer, 1897 9 26 100.0 0.0

Isotomidae Folsomides sp. Stach, 1922 150 7 100.0 0.0 Folsomina onychiurina Denis, 1931 48 16 60.4 39.6 Isotoma (Parisotoma) sp. Bagnall, 1940 963 2 10.9 89.1 Isotoma (Isotoma) sp. Bourlet, 1893 72 13 66.7 33.0 Subisotoma sp. Stach, 1947 794 3 5.0 95.0

Neanuridae Acanthanura sp. B6rner, 1906 1 34 100.0 0.0 Australonura quarta Greenslade and Deharveng, 1990 52 15 100.0 0.0 Ceratrimeria sp. B6rner, 1906 262 6 13.7 86.3 Hemilobella sp. (cf. rounsvelli) Deharveng and Greenslade, 1992(p 46 17 13.0 87.0 Pseudachorutella sp. Stacjh. 1949 12 25 100.0 0.0

Brachystomellidae Brachystomella sp. Agren, 1903 296 5 46.6 53.4

Onychiuridae Tullbergia sp. Lubbock, 1876 3 29 100.0 0.0

Sminthuridae Arrhopalites sp. B6rner, 1906 2 32 100.0 0.0 Katianna sp. B6rner, 1906 9 27 55.6 44.4 Neosminthurus sp. Mills, 1944 20 24 100.0 0.0 Pseudokatianna sp. Salmon, 1944 93 10 65.6 34.4 Sphaeridia sp. Linnanieme, 1912 35 20 22.9 77.1 Sminthurinus sp. B6rner, 1901 145 8 10.3 89.7

Dicyrtomidae Clavatomina sp. Yosii, 1966 2 31 100.0 0.0

Neelidae Neelides sp. Caroli, 1912 22 23 4.5 95.5 Megalothorax sp. Willem, 1990 55 14 29.1 70.9

T Lepidocyrtoides spp. 1 and 2 are distinguished by the presence of three teeth on the inner margin of the mesotibiotarsal claw in sp. 1, and one tooth in this position in sp. 2. fPseudoparonella spp. 2 and 3 are distinguished by the presence two rows of spines extending along the full length of the dens in sp. 2, and the absence of dental spines in sp. 3. 500 mm di- ameter) and small (

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 speci- mens 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

Lower Upper canopy canopy

2.5

--e* -o 2

0 1.5

0.5

U Ground Small litter deposits ] Canopy 1 Large litter deposits

Fig. 1. Mean collembolan abundance in ground, canopy (pooled), and large and small litter deposits in the lower and upper canopy (error bars are standard deviations).

1 5 Lower Upper 14 - 4 3 canopy canopy 13 12 11 10

o 9 8

,

7 6 5 a

- 0 4 3 2 I

0

Ground Small litter deposits l Canopy I Large litter deposits

Fig. 2. Mean species richness in ground, canopy (pooled), and large and small litter deposits in the lower and upper canopy (error bars are standard deviations).

0

A * 0

N [3

Am . 0

AA A A

A

*A 0

e

A. A

SA A

* *

Ordination axis 1 (Variance = 18.58)

Fig. 3. Ordination in three dimensions of all leaf litter samples. * Ground litter samples, 0 Lower canopy small litter deposit samples, Ol Lower canopy large litter deposit samples, A Upper canopy small litter deposit samples, A Upper canopy large litter deposit samples. (Ordination stress = 0.18).

was determined. Where this was not sufficient to dis- criminate between morphospecies (i.e. in the case of congeners) morphological characters of established tax- onomic value were used to discriminate between spe- cies.

Univariate statistics All species abundance data were log(x + 1) transformed before analysis. This transformation stabilised variances to some degree, but in many cases homoscedasticity was not achieved. Where homoscedasticity cannot be relied upon randomisation tests offer superior statistical

ECOGRAPHY 21:4 (1998) 395

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

Multivariate statistics The Bray-Curtis dissimilarity measure was used to pro- duce a sample dissimilarity matrix. The Bray-Curtis dissimilarity measure was chosen from a number of

Table 2. ANOSIM results, statistic value, number of permuta- tions and significance level of all pairwise comparisons. Comparison Significance level %

Ground/Canopy 0.000 Upper/Lower canopy 1.5 Large/Small litter deposits 13.4 Lower canopy, small/Lower canopy

large litter deposits 27.9 Lower canopy, small/Upper canopy

small litter deposits 1.5 Lower canopy, small/Upper canopy

large litter deposits 3.2 Lower canopy, large/Upper canopy

small litter deposits 0.9 Lower canopy, large/Upper canopy

large litter deposits 9.5 Upper canopy, small/Upper canopy

large litter deposits 16.2 * 10 000 was used as the default number of permutations unless the number of possible permutations was

Table 3. Species contributing most substantially to the significant differences between assemblages as per ANOSIM results. (For each comparison the species listed are the first five from a ranked list of contributions to average dissimilarities between groups). Groups compared Species Average Average Average % contribution to (Group 1/Group 2) abundance abundance dissimilarity between

Group 1 Group 2 groups

Ground/Canopy Ascocyrtus cinctus 41.13 0.75 12.92 Isotoma (Parisotoma) sp. 4.38 35.75 8.05 Subisotoma sp. 1.67 31.42 6.83 Brachystomella sp. 5.75 6.58 6.00 Pseudoparonella queenslandica 7.46 15.83 5.24

Upper canopy/Lower canopy Subisotoma sp. 27.42 35.42 11.79 Isotoma (Parisotoma) sp. 25.08 46.42 9.54 Pseudoparonella queenslandica 18.00 13.67 9.19 Sminthurinus sp. 9.92 0.92 9.18 Acanthocyrtus spinosus 1.42 6.50 6.38

Upper canopy, small/Lower canopy Subisotoma sp. 4.83 50.6 11.64 small litter deposits Isotoma (Parisotoma) sp. 7.83 23.83 10.07

Acanthocyrtus spinosus 0.17 12.00 9.06 Sminthurinus sp. 11.50 1.33 8.88 Pseudoparonella queenslandica 7.67 8.67 8.50

Upper canopy, small/Lower canopy Pseudoparonella queenslandica 7.67 18.67 11.51 large litter deposits Isotoma (Parisotoma) sp. 7.83 69.00 11.04

Sminthurinus sp. 11.5 0.50 10.82 Subisotoma sp. 4.83 20.17 9.44 Brachystomella sp. 0.17 22.67 8.37

Upper canopy, large/Lower canopy Subisotoma sp. 50.00 50.67 13.48 small litter deposits Acanthocyrtus spinosus 2.67 12.00 9.09

Sminthurinus sp. 8.33 1.33 7.95 Pseudoparonella queenslandica 28.33 8.67 7.61 Isotoma (Parisotoma) sp. 42.33 23.83 7.12

wise comparisons. Clarke and Warwick (1994) point out that there is no procedure to protect these pair- wise comparisons from an accumulation of the proba- bility 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 struc- ture of canopy collembolan assemblages using ANOSIM for the two-way crossed design with the two factors, litter deposit height and size (no interac- tion 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 lit- ter deposits.

In addition to ANOSIM analyses based on the ra- tios of within and between group dissimilarities, we have analysed within and between group dissimilari- ties separately. The rationale for these separate analy- ses 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 mea-

sure of the impact of pollutants on aquatic inverte- brate communities. The separate analysis of multi- variate 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 in- volved 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. Randomi- sation 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 be- tween assemblages. The identification of these dis- criminating 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 sam- ples (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.

ECOGRAPHY 21:4 (1998) 397

Results Thirty-five morphospecies of Collembola were iden- tified from the samples (Table 1). A total of 5094 individuals were found in the samples. The total abun- dance of Collembola did not differ significantly be- tween 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 signifi- cantly 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 ordi- nation 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 multi- ple 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 de- posits in the upper canopy was also significantly differ- ent 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

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 randomisa- tion 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 dissimi- larities between canopy and ground samples showed significant effects of both upper/lower canopy and large/small deposit factors, with no significant interac- tion. 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 be- tween ground and canopy litter samples, with an aver- age 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 (Pariso- toma) sp. ranked second among species contributing to the distinction between ground and canopy litter sam- ples contributing 8.05% of total dissimilarity between these groups. In contrast to A. cinctus, Isotoma (Pariso- toma) 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

398 ECOGRAPHY 21:4 (1998)

27.42 and 25.08 in the upper canopy respectively. Con- versely, Pseudoparonella queenslandica (Sch6tt 1917) and Sminthurinus sp. 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 signifi- cantly different groups as shown in Table 3.

Discussion The ANOSIM results establish a clear distinction be- tween the forest floor, lower and upper canopy collem- bolan 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 inter- mediate 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 dissimi- larity of samples within assemblages from the lower to the upper canopy and from large to small litter de- posits. 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 Nad- karni (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 dif- ferent 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 inter- connected islands. The two major processes generating the peculiar biogeographic patterns found among is- lands 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

scale, may play a significant role in producing the patterns of relationship among these collembolan as- semblages. 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 sev- eral 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 rain- forest microclimates. Microclimatic conditions in sus- pended 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, characteris- tics 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 de- posits in the upper canopy might therefore be extin- guished more frequently than colonies in lower or larger deposits. If recolonisation of upper canopy litter deposits was also limited by the dryness of the sur- rounding environment, then the outcome would be very similar to the patterns of stratification we have ob- served. An unpredictable outcome of such processes in terms of the species composition of assemblages is consistent with Higvar's (1995) results and would ex- plain 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 de- termining 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 con- sider 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

ECOGRAPHY 21:4 (1998) 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.

Acknowledgements - Financial support for this research was provided by the Cooperative Research Centre for Tropical Rainforest Ecology and Management. We also thank P. Greenslade for her assistance with the identification of several specimens.

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400 ECOGRAPHY 21:4 (1998)

Article Contentsp. 392p. 393p. 394p. 395p. 396p. 397p. 398p. 399p. 400

Issue Table of ContentsEcography, Vol. 21, No. 4 (Aug., 1998), pp. 337-446Front MatterTopographical Constraints and Home Range Quality [pp. 337-341]Global Patterns in Species Richness of Pelagic Seabirds: The Procellariiformes [pp. 342-350]An Isozyme Study of Clone Diversity and Relative Importance of Sexual and Vegetative Recruitment in the Grass Brachypodium pinnatum [pp. 351-360]Species-Range Size Distributions in Britain [pp. 361-370]Biogeographical Regions of the Iberian Peninsula Based on Freshwater Fish and Amphibian Distributions [pp. 371-382]Forest Fragmentation and Colony Performance of Forest Tent Caterpillar [pp. 383-391]Vertical Stratification of Rainforest Collembolan (Collembola: Insecta) Assemblages: Description of Ecological Patterns and Hypotheses concerning Their Generation [pp. 392-400]The Effects of Scale and Sample Size on the Accuracy of Spatial Predictions of Tiger Beetle (Cicindelidae) Species Richness [pp. 401-414]The Effect of Depletion and Predictability of Distinct Food Patches on the Timing of Aggression in Red Deer Stags [pp. 415-422]Testing for Spatial Autocorrelation in Ecological Studies [pp. 423-429]A Re-Examination of Geographical Variation in Nepenthes Food Webs [pp. 430-436]ForumThe Historical Assembly of Continental Biotas: Late Quaternary Range-Shifting, Areas of Endemism, and Biogeographic Structure in the North American Mammal Fauna [pp. 437-446]

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