FIBRA DE ABACÁ

F-LARGE 0.7632 0.2307 -0.0677 0.0791 F-SMALL 0.4165 -0.6945 -0.4820 -0.1398 PALMS -0.8854 -0.2460 -0.2240 -0.0945 HUMUS -0.8230 0.2619 -0.1168 0.4211 PH 0.7605 0.4280 0.3173 -0.1996

small wood was, however, somewhat weakly correlated with axis 2, being also

negatively correlated with soil humus depth.

The results showed that palm density, soil humus depth, and the strongly

negatively correlated soil pH, were the most important factors determining variation in

species composition of the termite assemblage across the 13 sites. Greater density of

palms and soil humus depth were associated with the species compositions of two

large island transects (T8 and T2) and three medium sized island transects (T9, T5 and

TIO), whereas low palm density and soil humus depth were associated with the

species composition of transects from two mainland (T1 and T13) and two small

island sites (T6 and T il). Logio (distance to forest edge), as represented by the second

axis, was still shown to have a significant effect on species composition, with the

result that the two mainland transects furthest from the forest edge (T1 and T13)

showed greatest compositional differences with the four smallest islands (T3, T7, T6

and T il).

The partial RDA for soil feeding species only, showed almost identical results

to those for the complete assemblage, because the latter was in any case dominated by

soil feeding species. For this reason, only the resulting RDA bi-plot is presented

of the bi-plot was divided into quarters, each corresponding (approximately) to the

zone in which species vectors are most closely positively associated with one of the

four main environmental conditions: high palm density, low soil pH; low palm

density, high soil pH; large edge distance (and fragment area); and short edge distance

(and small fragment area). This revealed a clear difference in the environmental

conditions most favourable to two taxonomic sub-divisions of the soil feeder

assemblage. The great majority of Apicotermitinae (which make up 47% of all soil

feeding species found) were negatively associated with palm density (15 species)

rather than positively associated (three species). The remaining soil feeding species

(belonging to two further termite subfamilies, the Termitinae and Nasutitermitinae)

showed a slightly smaller imbalance, but tended to favour areas of high palm density

(15 species vs. nine species). The dichotomy in the division of species associations

between larger and smaller fragment size, and edge distance, was much less apparent.

The only difference was that more species of Apicotermitinae were associated with

smaller rather than larger fragment size and edge distance (nine species vs. five

species).

The partial RDA for wood and leaf litter feeders, however, showed that

environmental variables associated most closely with fragmentation, rather than other

factors, were having the greatest influence on species composition. Specifically,

forward selection showed that volume of standing dead wood had greatest marginal

significance in explaining variation in species composition, followed by soil moisture

and soil pH (Table 4.6). Again, the eigenvalues for the partial RDA (0.16, 0.12, 0.07,

and 0.13, for axes 1-4, respectively) were not markedly lower than those for the partial

LO L G E D G E JL L arger f r a g m e n ts Ap: 8 spp. N on-A p: 5sp p . P H ' S "N Ap: 15 sp p > N on-A p: 9 spp. P A L M S Ap: 3 sp p . N on-A p: 15 sp p . S m a ll e r f r a g m e n ts Ap: 8 sp p . N o n -A p : Sspp. LT) 1 . 5 + 1 . 5

Figure 4.13. Ordination bi-plot for partial RDA o f soil feeder species data and environmental variables, with season (wet and dry) entered as nominal categorical covariables. Centroids for sites have been removed for clarity. Axes 1 and 2 ordination space is divided into quadrants (by thick dashed line), corresponding to zones o f association with parts o f environmental gradients. Numbers o f species o f Apicotermitinae (Ap) and Non-Apicotermitinae (Non-Ap) associated with each quadrant are indicated. Species arrows are coded as follows: solid = Apicotermitinae species; dashed = Non-Apicotermitinae species (i.e. Termitinae,

Nasutitermitinae, see Appendix 4.2). (Environmental variable abbreviations are as for Figure 4.7).

Table 4.6. Results of partial RDA forward selection procedure, showing environmental variables explaining significant variance in termite wood and leaf litter species composition across 13 transect sites. À] = eigenvalue (fit) for each variable on its own; = increase in eigenvalue (additional fit); £Aa = cumulative total of eigenvalues Aa',P = significance level of effect, as obtained with a Monte Carlo permutation test under the null model with 999 random permutations conditioned on the covariables.

Marginal Effects Variable _M P Conditional Effects Variable _h. P EA,2 V-STAND 0.15 0.012 V-STAND 0.15 0.012 0.15 MOISTURE 0.14 0.002 PH 0.11 0.035 0.26 PH 0.12 0.038

environment correlations were high (0.978, 0.972, and 0.842, for axes 1-3,

repectively). A notable feature of the resulting bi-plot (Figure 4.14), in which only

significant marginal variables were included, was that the four smallest islands

showed the greatest differences in species composition, as indicated by the relatively

wide spacing of their centroids across axes 1 and 2 ordination space (T3, T6, T7 and

T il). In particular, the centroid for T6 from the smallest island, was most closely

associated with those for mainland and large island transects (Tl, T13 and T4).

Notable also, was the strong association between the centroids for transects (T il and

T7) from the second and third smallest islands, respectively, and species of

Cornitermes. This genus is known to inhabit hard epigeal soil mounds which are likely

to protect resident colonies from the microclimatic harshness that are a feature of drier

o Glypto A T4 T13 Het tenu IndKA Rugi A Ns guay MOISTURE

Ns oct Cor pug

V-STAND

Cyl parv

112 IndKB Cor web

N s J /j g Ns D

Ns gai _{Dol long}

T11 Ac sub Ns suri 18 Vel beeb Ns sim Syn spin T3 Ns bank LO 1 . 0 + 2 . 0

Figure 4.14. Ordination bi-plot for partial RDA o f wood and leaf litter feeder species data and environmental variables, with season (wet and dry) entered as nominal categorical co variables. Circles representing centroids for transects are coded as: white = small islands (<1 ha); light grey = medium islands (1-10 ha); dark grey = large islands (10-100 ha); and black = mainland (1000 ha). Abbreviated species names are as follows: Ac sub, Acorhinotermes subjus ci ceps'.

Cor A, Cornitermes sp. A nr. cumulons'. Cor pug, Cornitermes pugnax'. Cor web, Cornitermes

weberi', Cyl parv, Cylindrotermes parvignathus', Dol long, Dolichorhinotermes longilabius',

Glypto A, Glyptotermes sp. A nr. guianensis', Het tenu, Heterotermes tenuis', IndK A ,

Indeterminate Kalotermitidae sp. A; IndK B, Indeterminate Kalotermitidae sp. B; Ns bank, Nasutitermes banksr, Ns gai, Nasutitermes gaigev, Ns guy, Nasutitermes guayanae', Ns oct, Nasutitermes octopilus', Ns sim, Nasutitermes similis', Ns suri, Nasutitermes surinamensis', Ns

D, Nasutitermessp. D; N sJ , Nasutitermessp. J; Rugi A, Rugitermessp. A; Syn spin,

Syntermes spinosus', Syn A, Syntermessp. A nr. longiceps', Vel beeb, Velocitermes beebei.

Ordinations to assess spatial autocorrelation.

The forward selection procedure for the partial RDA of the complete species datatset

across all 13 terrestrial sites, and the 9-term spatial matrix, indicated that three terms

(x, y, and xy) showed significant marginal effects (i.e. when each variable was tested

on its own) upon variation in species composition (Table 4.7) indicating significant

spatial autocorrelation in the species composition data. With these spatial terms

entered as covariables, together with season, a further partial RDA of the complete

species data and measured environmental variables revealed that only soil moisture

showed marginal significance in explaining the variance in species composition.

Nevertheless, soil moisture is strongly correlated with distance to the forest edge i.e.

forest fragmentation.

Table 4.7. Results of partial RDA forward selection procedure, showing spatial positioning terms explaining significant variance in termite species composition across 13 transect sites.

= eigenvalue (fit) for each variable on its own; = increase in eigenvalue (additional fit); IÀq, = cumulative total of eigenvalues ^ , P = significance level of effect, as obtained with a

Monte Carlo permutation test under the null model with 999 random permutations conditioned on the covariables. Marginal Effects Variable P Conditional Effects Variable _^2 P IÀ2 y 0.12 0.008 y 0.12 0.013 0.12 xy 0.12 0.022 X 0.12 0.028

Partitioning of the variation in species composition revealed that 32.6% of the

total variance in species composition was spatially structured, of which over a third

(9.1% of total variance) was spatially structured environmental variation, the

44.9% o f total variation w as due to non-spatial environm ental variation, leaving 22.6% as unexplained variation. Again, as soil feeders make up the majority o f sp ecies, the results o f an analysis for soil feeders alone w ere very sim ilar to th ose for the overall assem blage. A n alysis o f w oo d and le a f litter feed ers only, revealed a sm aller spatially structured com ponent o f variation (21.3% o f total) including considerably less spatially structured environm ental variation (just 3.0% o f total).

0) u c re "C re > re o •*-> 0) O) re -4-J c re e re Q . 2 3.1% 4 3.5% 2 1 .2 % 23.5% 11.7% 4 4.9% 44.0% 35.1%

Total W ood Soil

I I U n d e t e r m i n e d # # S p a c e ■ ■ S p a c e + e n v

E n v i r o n m e n t

Figure 4.15. Variance partitioning o f the termite species data across 13 terrestrial forest transects for; the total assemblage (total); for wood and leaf litter feeders (wood); and for soil feeders (soil), calculated from the results o f partial RDAs following Borcard e( a l (1992). Percentage variances for each component o f total variation are given inside white boxes. Abbreviations for variance components are as follows: undetermined, undetermined variance; space, spatially structured variance; space + env, spatially structured environmental variance; environment, non-spatially structured environmental variance.

4.4. Discussion

Overview o f main environmental and spatial effects upon assemblage composition.

Four years after the original inundation events, the effects of forest fragmentation

upon the total assemblage, and upon soil feeders in particular, were subordinate to the

influence of forest understory palm density, and the closely associated gradients of soil

humus depth and soil pH. Moreover, changes in these three variables were found to be

uncorrelated with any fragmentation gradient, and to largely account for the

component of spatially structured environmental variation detected in the species

composition data. Nevertheless, forest fragmentation appeared to be having a

significant effect on changes in termite species composition across the St. Eugène

study site. The validity of this result was brought into question by the finding that the

fragmentation gradient was partially confounded by spatial positioning of sites, when

considering variation in the complete assemblage. However, the significant influence

of soil moisture upon the wood and leaf-litter feeding sub-assemblage (when

controlling for spatial position) suggested a real effect of fragmentation. Further

indirect support for this species level fragmentation effect came from a feeding group

level analysis of the same dataset (see Chapter 5) showing that fragmentation has also

resulted in a clear shift in the relative encounters between wood and soil feeding

termites. In addition to the influence of palm density and fragmentation upon species

composition, purely spatial variation was clearly also influencing /^-diversity changes

The role o f forest palms in structuring termite assemblage composition from soil to understory.

The spatial heterogeneity in distribution of forest palms almost certainly pre­

dated the inundation events that created forest islands. This is indirectly supported by

the findings of Scariot (1999) from the BDFFP site in Brazil showing that, between 10

and 15 years following habitat fragmentation, species richness of adult and juvenile

palms (but not seedlings) was unaffected by fragmentation, and that there was no

evidence of differential adult mortality. Increasing evidence points to the ubiquity of

edaphically-related spatial heterogeneity in plant community structure in old-growth

tropical wet forests, across scales ranging from 0.5 -10^ ha (Clark et al. 1995). Soil

drainage, topography, and forest architecture are all considered to be important in

influencing palm distributions in Amazonian terre firme forests (Kahn and de

Granville 1992). Although the relationship between palm density and soil pH has not

been reported previously, a Costa Rican study showed that lowest palm species

richness occurred on the soil type (alluvium) with highest fertility and pH (Clark et al.

1995). In Amazonian palm communities of terre firme forests, most species are small

or medium in size with 99% of individuals being under 10-m tall, with the result that

palms dominate the understory plant community (Kahn and de Granville 1992). The

funnel-like form of many adult understory palms with large leaves leads to

concentration of falling canopy leaf-litter and small woody debris towards their stems

(Kahn and de Granville 1992). This canopy litter can remain suspended in the crowns

of the palms themselves or become caught on above-ground stems, particularly in

Figure 4.16. Canopy litter and humus accumulations, and termite nest, between the armed petioles o f an understory palm with a single erect stem.

species, debris often accumulates in conspicuous raised piles at the bases of palms

(Figure 4.17). This feature almost certainly explains the positive correlation between

palm density and soil humus depth observed in the present study.

The palm community of upper slopes and ridge crests at St. Eugène, hence that which

coincided with termite transect sampling, is dominated by the arborescent species

Jessenia bataua (Martius), and the understory species Bactris oligocarpa Barbosa

Figure 4.17. Understory palm with funnel-like crown o f large leaves showing conspicuous pile o f accumulated leaf-litter around the base.

1996). The last two species are known to accumulate canopy leaf-litter (de Granville

1977). Their structural form, their potential as a food source, and their associated

accumulations of canopy litter, make palms important habitats for a wide diversity of

vertebrate and invertebrate forest fauna. The present study demonstrates the

importance of understory forest palms and their associated humus accumulations as

key micro-sites for termites. Moreover, this is the first study to have shown the direct

levels in Amazonian tropical forests. In addition to those found on the above-ground

structures of understory palms, suspended litter and humus accumulations also occur

high in forest canopies, especially in association with epiphytes. However, we predict

that termite assemblages associated with canopy soils will share few species in

common with (or be a depauperate subset of) those of understory palms, due to the

much harsher micro-climatic conditions of the canopy. For a particular subset of the

termite assemblage, understory palms represent suspended humus and litter

accumulations that are well-drained, and yet in a microclimatically favourable stratum

of the forest, making them ideal sites for foraging and nesting that are not as

abundantly replicated by other components of above-ground forest architecture.

The results of ordinations analyses revealed that the primary influence of palm

density and associated environmental gradients was upon soil feeders rather than wood

feeders. This is partly due to the rich accumulations of humus, both suspended and at

ground-level, that are associated with many palms. However, there was a lower

diversity of soil feeding termites associated with high, as opposed to low, palm

density, suggesting that below-ground soil conditions in the vicinity of palms are less

favourable to soil feeders. This effect is likely to be at least as important as the

positive effect of palms as termite microsites. The reason for it remains uncertain, but

may be linked to the lower soil pH associated with high palm densities. Termites

actively increase the pH inside their guts to facilitate digestion of food substrates

(Bignell and Eggleton 1995). Palms may themselves be directly contributing to the

acidity of their associated soils in some way, or the palm community overall may

thrive in more acid soils and hence achieve higher densities under such conditions.

and soil feeder diversity. The most likely reason for the taxonomic bias in species that

are associated with palms, and those that are not, concerns the level of humification of

food substrates. Most species of Apicotermitinae are feeding on more humified

substrates in the soil, than the majority of soil feeding Nasutitermitinae or Termitinae.

Forest fragmentation effects and the influence o f the ghost forest/canopy assemblage.

Species composition of wood and leaf-litter feeders was shown to be under greater

influence from fi’agmentation-associated environmental variables (volume of standing

dead wood and soil moisture) than from others, even after removing any influence of

ghost forest species. In most studies where invertebrate abundance and diversity have

been found to increase close to forest edges or in smaller fragments, the most plausible

explanation has been an increase in abundance of gap- or disturbance-adapted species

and/or species influx from surrounding matrix habitat (Didham 1997). However, in the

present study, this appeared not to be so and the nearest savannas or open, human-

impacted terrestrial areas were at least 50 km away. Instead, it appears that species

that were most abundant in the ghost forest and littoral zone were relatively rare at or

near ground-level in terrestrial forest sites and were probably a relict canopy-adapted

assemblage. Other invertebrate studies have shown that communities encountered near

ground-level at forest edges showed more in common with those of forest canopies

than of forest interiors (Toda 1992, Malcolm 1997). However, only one additional

species which was known to occur in the canopy, but was not known from the ghost

forest, was found on terrestrial transects. This soil feeding species, Anoplotermes

and edge distance, and was the only soil feeder to be found during limited casual

sampling from epiphyte-associated humus suspended high in mainland forest canopy

at the study site.

Species richness, similarity and evenness.

The results of species compositional similarity comparisons within and between

categories of fragments of different sizes (Figure 4.10) resembled those of a study on

beetle responses to tropical forest fragmentation at the BDFFP (Didham et a l 1998) in

which there was no indication that highly disturbed sites shared a common beetle

fauna. Moreover, in the present study, mean similarity among small island transects

was not only lower than mean similarity among mainland forest transects, but was also

lower than that between small island and mainland transects. Together with the finding

of insignificant differences in evenness across fragment size categories, the latter

result is in accordance with the conclusion that small islands have not been colonized

by generalist disturbance-adapted species from more open habitats elsewhere.

An alternative explanation for the observed similarities between small islands

is that transects were sampling from a moderately large pool of disturbance-adapted

species that was present within the original forest assemblage, although with

apparently rather low occurrence at or near ground-level in mainland forest.

Specifically, these disturbance-adapted species are likely to be canopy-, forest edge-,

or treefall-gap-adapted. The inherent patchiness of edge-, canopy- or treefall-gap-

associated termite food resources in a relatively undisturbed tropical forest, could be

In document Obtención y Caracterización de Materiales Compuestos Híbridos de Matriz (página 48-52)