Palms, peccaries and perturbations: widespread
effects of small-scale disturbance in tropical
forests
Queenborough et al.
Queenborough et al. BMC Ecology 2012, 12:3
http://www.biomedcentral.com/1472-6785/12/3 (19 March 2012)
R E S E A R C H A R T I C L E Open Acces s
Palms, peccaries and perturbations: widespread
effects of small-scale disturbance in tropical
forests
Simon A Queenborough 1* , Margaret R Metz 2 , Thorsten Wiegand 3 and Renato Valencia 4
Abs tract
Background: Disturbance is an important process structuring ecosystems worldwide and has long been thought
to be a significant driver of diversity and dynamics. In forests, most studies of dis turbance have focused on large-
scale disturbance such as hurricanes or tree-falls. However, sm aller sub-canopy disturbances could also have
significant imp acts on community structure. One such sub-canopy disturbance in tropical forests is abscising leaves
of large arborescent palm (Arececeae) trees. These leaves can weigh up to 15 kg and cause physic al damage and
mortal ity to juvenile plants. Previous studies examining this question suffered from the use of static data at small
spa tial scales. Here we use data from a large permanent forest plot combined with dynamic data on the survival
and growth of > 66,000 individuals over a seven-year period to address whether falling palm fronds do impact
neighboring seedling and sapling communities, or whether there is an interaction between the palms and
peccaries rooting for fallen palm fruit in the same area as falling leaves. We tested the wider generalisation of
these hypotheses by comparing seedling and sap ling survival under fruiting and non-fruiting trees in another
fami ly, the Myristi caceae.
Results: We found a spa tially-restricted but significant effect of large arborescent fruiting palms on the spatial
structure, population dynamics and species diversity of neighbouring sapling and seedling communities. However,
these effects were not found around slightly sm aller non-fruiting palm trees, suggesting it is seed predators such
as peccaries rather than falling leaves that impact on the communities around palm trees. Conversely, this
hypothesis was not supported in dat a from other edible species, such as those in the family Myristi caceae.
Conclusions: Given the abundance of arborescent pa lm trees in Amazonian forests , it is reasonable to conclude
that their presence does have a significant, if spatial ly-restricted, impact on juvenile plants, most likely on the
surviv al and growth of seedlings and saplings damaged by foraging peccaries. Given the abundance of fruit
produced by each palm, the widespread effects of these small-scale disturbances ap pear, over long time-sc ales, to
cause directional changes in community structure at larger scales.
Back ground
Disturbances are an important process structuring for-
ests worldwide and have long been considered as signifi-
cant drivers of dynamics and diversity [1-3]. In tropical
forests, disturbances such as hurricanes and tree-falls
from lightning or wind events create a mosaic of forest
patches of different microhabitats at varying stages of
succession [4-6] superimposed upon background
topographical and soil variation. If niche partitioning
permits coexistence along the axis of tolerance to distur-
bance, different species should be selected by such dis-
turbances, and we would expect to find predictable
suites of species associated with different disturbance
regimes [7]. This is indeed the case. Because of a trade-
off between growth and survival, fast-growing pioneer
species occur predictably in tree-fall gaps. Conversely,
slow-growing shade-tolerant species survive well in
closed canopy forest [8-10]. Furthermore, resprouting of
trees is high in areas affected by hurricanes [11]. These
large-scale disturbances are obvious in the forest and
* Correspondence: queenborough.1@osu.edu
1 Department of Evolution, Ecology and Organismal Biology, The Ohio State
University, Columbus, OH 43210, USA
Full list of author information is available at the end of the article
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? 2 0 1 2 Queenborough et al; li censee BioMed Central L td. Thi s is an Open Access art ic le dis tributed under the terms of the Creati ve
Commons At tribution Li cense (http :/ /creat ivecommons.org/l icenses/by/ 2.0 ) , which permi ts unrestri cted use, di stribution, and
reproduct ion in any medium, provi ded the original work i s properly c ited.
are important mechanisms of species coexistence and
community structure [4,12]. However, the contribution
of gaps and their associated pioneer flora to species
coexistence is likely to be limited, because full tree-fall
gaps are relatively infrequent in lowland rain forest [13]
and most pioneer species occur at low abundance [12].
Are there other kinds of disturbance in tropical forests
affecting far wider areas of forest that influence species
composition and community dynamics?
Several authors have suggested that smaller distur-
bances such as branch-falls have a greater and more
widespread effect on forest dynamics and composition
than might be apparent at first glance [13-15]. In the
absence of large canopy-opening disturbances, mortality
in sub-canopy layers can increase light availability, free
up resources and lead to faster sapling growth [16,17].
Furthermore, these sub-canopy gaps occupy large pro-
portions of forest [13]. Sub-canopy openings occur from
a variety of processes, including the death of sub-canopy
trees, large branch falls, or in-filling of canopy gaps by
trees in middle forest strata [14]. In addition to freeing
resources, these events may cause disturbances to
younger life stages, such as branch-falls affecting the
survival and growth of seedlings and saplings [18-21].
Falling branches are heavy and can kill or physically
damage small plants [22]. If these branch-falls were pre-
valent enough of a selective force, species intolerant of
this damage could be selected against in areas of high
branch-fall. Peters et al. [15] extend this argument to
apply to arborescent palm leaves, which are heavy
enough to physically damage anything underneath (> 15
kg dry mass and several metres in length [23]). Given
the ubiquity of large palms in western Amazonian for-
ests (densities often exceeding 60 palms > 10 cm dbh
ha-1 [24-29]), these authors suggested that falling leaves
could select for species adapted to withstand this distur-
bance impact, such as those with storage organs or coty-
ledons that could easily resprout following damage.
Indeed, Peters et al. [15] found differences in sapling
(0.5-2.5 m in height) communities in areas close to large
arborescent palms compared to those with no influence
of palm leaf fall. Although theirs was only a small study
over 2.25 ha, it would seem that falling palm leaves
could have a large effect on the species composition of
forest communities.
However, falling branches and leaf fronds are not the
only widespread small-scale disturbances in forests.
Large frugivores such as tapirs and peccaries are known
to cause heavy localised disturbance, dramatically
increase mortality of seedlings and saplings [30-33], and
consume and disperse seeds [34,35]. Peccaries also con-
sume palm fruit [33] and in a repeat study of Peters et
al. [15], Beck et al. [36] showed that sapling commu-
nities were impacted by the presence of palms in forest
containing peccaries, but not in forest where they had
been hunted out. Beck et al. [36] attributed the relation-
ship between palms and saplings to peccaries rooting
around palms and not to falling palm fronds. However,
both studies [15,36] suffered from using only static data,
examining distributions of palms relative to other spe-
cies without the ability to test how these distributions
develop through differential growth or mortality.
Whatever the mechanism (falling fronds or rooting
peccaries), the disturbance around palms should cause
differences in seedling and sapling density, growth, mor-
tality, and/or re-sprouting close to palms compared to
areas further away. If falling fronds are the cause, there
should be similar effects in the neighbourhoods of large,
fruiting palms as well as large, but non-fruiting palms.
Alternatively, if the disturbance is caused by peccaries,
we would not expect an effect by non-fruiting palms. In
addition, although palms are a common food source,
many other species of large-fruited tree are also con-
sumed by peccaries [33]. Therefore, we would also
expect an effect on the seedling and sapling commu-
nities around other large fruit-bearing tree species simi-
larly eaten by peccaries. In this latter case, the effect of
these small-scale disturbances may be even more wide-
spread than Peters et al. [15] envisaged.
We should also consider that palms may have positive
effects on some species. Evidence gathered by Connell
et al. [13] showed that smaller sub-canopy disturbances
led to faster growth of understorey saplings, presumably
because of increased light penetration or freed-up
resources from the death of a sub-canopy individual.
These sub-canopy gaps (without complete opening of
the forest canopy) were very common in the forest (cov-
ering up to about 48% of forest). Falling palm fronds
likely create such sub-canopy gaps and seedlings that
survive palm or peccary damage may benefit from hav-
ing (i) fewer competitors (seen in the lower local densi-
ties of seedlings and saplings), (ii) more light (because
palms have a less dense canopy than other trees and
because the falling fronds knock other branches down)
and, (iii) more soil resources (for the same reasons).
Ultimately, this increased availability of resources adja-
cent to palms could lead to higher growth or survival of
saplings of some species.
In this study we use spatially-explicit data from long-
term monitoring of seedlings, saplings in the neighbour-
hoods of large arborescent Arecaceae (mostly Iriartea
deltoidea) and reproductive Myristicaceae trees in a
large forest dynamics plot in western Amazonia to
examine the potential structuring effect of falling leaves
and branches on tropical forest communities. We aim
to test (i) whether large palms and other fruiting trees
appear to impact seedling and sapling dynamics and dis-
tributions and (ii) whether any difference is due to the
Queenborough et al. BMC Ecology 2012, 12:3
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trees themselves or an interaction with large frugivores.
We extend previous studies of these phenomena in two
key areas. First, we use dynamic data to understand the
processes that lead to the patterns observed in static
data in previous studies. Second, we consider that small-
scale disturbances and/or interactions with frugivores
must also apply to other fruiting trees. In this case, we
examined seedlings and saplings in the neighbourhood
of fruiting adults in a common dioecious family at our
site, the Myristicaceae, fruits of which are also often
consumed by peccaries [33]. The Myristicaceae have
been studied here for 10 years, and detailed information
is available on the sex of each reproductive tree. Com-
paring the sapling communities around male (non-fruit-
ing) and female (fruiting) trees allows a rigorous
comparison of fruit-eating by peccaries, and a counter-
point to understanding the impacts of disturbances asso-
ciated with arborescent palms.
Resu lts
A total of 1,673 mature arborescent palms (? 15 cm
dbh) were recorded in the 25 ha Yasun? FDP in the
initial census (a mean of 67 ha-1, Table 1). Exactly 309
large arborescent palms in the size class 10-15 cm dbh
were recorded. These palms were presumed to be
immature (i.e. non-fruiting) but still with large leaves
capable of causing physical damage to seedlings and
saplings beneath. A total of 54,406 non-palm saplings
(1-2 cm dbh) were recorded on the plot and 46,853 of
these survived to the next census. A total of 12,309 new
seedling recruits were recorded in the 339 seedling plots
from 2003 to 2007. Fewer than half of these (4,480) sur-
vived to the next year.
Spatial patterns of distribution and density
In initial neighbourhood analyses using a bivariate form
of the O-ring statistic with a homogeneous Poisson null
model we found a significant large-scale effect, indicating
that large palms are located in areas of somewhat lower
sapling density (data not shown). When we corrected for
this effect using the heterogeneous Poisson null model,
randomly displacing palms within a 30 m neighbour-
hood, we found, as expected, notable small-scale repul-
sion of saplings from mature palms at distances < 3 m
(Figure 1A). Considering immature palms, the large scale
effect with respect to saplings existed as a tendency but
was not significant and there were no significant small-
scale effects (Figure 1B). Saplings were neither repulsed
from or attracted to immature palm trees. When we
extended these analyses to other fruiting trees, contrary
to our predictions, there was no significant repulsion or
attraction of saplings from neither male nor female Myr-
isticaceae trees and the observed O-ring values remained
within the simulation envelopes (Figure 1C and 1D).
Spatial patterns of community structure
A total of 1,471 5 ? 5 m quadrats contained or were
adjacent to a quadrat containing a mature palm (?palm
quadrats?) and the remaining 8,301 quadrats were
defined as uninfluenced by mature palms (?non-palm
quadrats?, Figure 2). Both stem density and species rich-
ness were lower in palm quadrats, by about 0.5 of a
stem/species. When we accounted for stem density, rar-
efied species richness was equivalent between palm and
non-palm quadrats, indicating that the lower observed
species riches in palm quadrats was primarily caused by
a fewer individuals.
Testing for differences in community composition at
the quadrat scale, we found a significant difference
between palm and non-palm quadrats (adonis, df = 1,
SS = 3.40, MSS = 3.40, F = 7.46, R2 = 0.001, P < 0.001),
indicating that the assemblages of species in the neigh-
borhoods of palms differed significantly from non-palm
neighborhoods, despite similar levels of diversity. How-
ever, the amount of variation explained was very low,
with an R2 of 0.001. A comparison of the abundance of
species within palm and non-palm quadrats indicated
that only a minority of the over 1,000 species in the plot
showed a significant response to palms (Table 2). Ten
species were more abundant than expected in palm
quadrats, and 25 species were more abundant than
expected in non-palm quadrats.
These results were confirmed in ISAR neighbourhood
analyses, were we found a significant repelling effect of
large arborescent mature palms on surrounding species at
distances < 5 m (Figure 3A). This result implies that
mature palms have a limited direct negative effect on the
diversity of surrounding sapling species. In contrast, imma-
ture arborescent palms had no such effect on surrounding
species diversity, and the observed ISAR values for the null
model generally remained within the simulation envelopes,
indicating a significant but very small repelling effect at
only one distance category (3 m, Figure 3B).
Dynamic demographic effects of large trees on seedlings
As expected, one-yr survival of new seedlings near (< 10
m) to mature palms was significantly lower than survival of
seedlings far (> 10 m) from mature and immature palms
Table 1 Abundances of the four arborescent palm species
on the Yasun? FDP in the first census
Species DBH class (cm)
1-10 10-15 ? 15
Iriartea deltoidea Ruiz & Pav. 493 292 1520
Astrocaryum chambira Burret 0 3 94
Oenocarpus bataua Mart. 0 3 98
Socratea exorrhiza (Mart.) H. Wendl. 15 11 3
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(Figure 4). Survival of new seedlings near to immature
palms was also significantly lower, but only when also near
mature palms. However, unexpectedly, survival of new
seedlings near to male and far from female Myristicaceae
trees was significantly lower than survival of seedlings far
from from sexes (Figure 4), survival of new seedlings near
female trees was not significantly lower (although in these
cases our analyses suffer from small sample sizes).
Dynamic demographic effects of large trees on saplings
There were some significant effects of palm and Myristi-
caceae trees on sapling dynamics. Contrary to our
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Distance from focal species (m)
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Figure 1 Spatial pattern analysis of non-palm saplings compared to palm trees and Myristicaceae trees. Results of bivariate point pattern
analyses between mature ( A, > 15 cm dbh) or immature ( B, non-fruiting, 10-15 cm dbh) large arborescent palms, and non-palm saplings (1-2
cm dbh), and female ( C, fruiting) or male ( D, non-fruiting) Myristicaceae and non-palm saplings in the 25 ha Yasun? FDP. In each case we
randomised the focal individuals (palms or Myristicaceae) with a heterogeneous Poisson distribution (20 m). Each pane shows the O-ring statistic
(circles, O 12 (r) ), giving the local neighborhood density of the pattern at scale r. Simulation envelopes (dashed lines) are the 5th highest and
lowest O(r) of 199 randomizations of the pattern over the study region. Points lying outside of the confidence envelope (filled circles) indicate
significant attraction (above) or repulsion (below) of saplings relative to palms.
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predictions, saplings showed no significant difference in
the probability of survival in areas near to (< 10 m) or
far from (? 10 m) large arborescent palms, mature or
not (Figure 5A, blue circles), and the probability of
negative growth of saplings near to immature palms was
greater than that of saplings far from either mature or
immature palms (Figure 5B, blue circles). In accordance
with our predictions, resprouting rates were higher in
saplings near to palm trees compared to areas far from
both immature and mature palms (Figure 5C, blue
circles).
When we looked at the effects of mature Myristica-
ceae trees on sapling dynamics, we found fewer signifi-
cant effects. Sapling survival near to male but far from
female Myrsticaceae trees was significantly higher com-
pared to saplings far from both sexes (Figure 5A, red
squares). However, these same saplings also had a signif-
icantly higher probability of negative growth (Figure 5B,
red squares). There was no effect of Myristicaceae trees
on resprouting rates (Figure 5C).
Disc ussion
Using a combination of spatially-explicit static and popu-
lation dynamic data, we conducted multiple tests to
examine hypotheses that falling palm fronds and/or pecc-
aries are major structuring forces of lowland Neotropical
rain forests [15,36]. We found a restricted but significant
direct effect of large arborescent mature fruiting palms
on the spatial structure and species diversity of neigh-
bouring sapling and seedling communities. There was
also a strong and consistent larger-scale environmental
effect of large palms being located in areas of lower
neighbourhood density and diversity of saplings. Further,
these patterns were corroborated by process in that we
also found significant differences in the population
dynamics of saplings (reduced growth and increased
resprouting) and seedlings (lower survival) in the vicinity
of mature palms. Evidence such as this was taken by pre-
vious authors to implicate falling palm fronds as major
causal agents of mortality and selection in tropical forests
[15]. However, when we attempted to exclude the con-
founding effects of frugivores by analysing still-large but
immature (ie. non-fruiting) palm trees, we found no sig-
nificant spatial signature, although there is some evidence
of reduced growth of neighbouring saplings. This would
suggest that large frugivores such as peccaries, and not
falling fronds, are the more important cause of physical
damage and mortality of seedlings and saplings in the
vicinity of mature palms as they root around for fruit
[36], because we would expect falling fronds to have an
equal effect around mature and immature palm trees.
We then tested these potential effects of peccaries by
examining the spatial structure and population dynamics
of seedlings and saplings around another important food
source, the Myristicaceae. Most species of this family are
large canopy trees [54] and produce abundant crops of
fruit that are eaten by peccaries [33] among other frugi-
vores [37,38]. Unlike palms though, these trees do not
have large heavy leaves that could damage seedlings and
saplings beneath the canopy. Furthermore, the family is
dioecious and so we could compare fruiting female trees
with non-fruiting male trees. However, we found no
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Species number
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Quadrat State
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pe
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F i g u r e 2 Comparison of sapling communities in areas
influenced and not influenced by large arborescent palm trees.
We show the sapling density (stem density 25 m -2 ), observed
number of species (species number 25 m -2 ), and rarefied species
richness (species per two individuals) for 5 ? 5m quadrats that
contain or are adjacent to a large palm (N = 1,471), and quadrats
that are > 1 quadrat from a palm quadrat (N = 8,301). We show the
mean ? SE.
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convincing evidence that the seedling and sapling commu-
nities near female Myristicaceae were structured at all, and
the significant population dynamic results we did find
were in the opposite direction to that hypothesized.
Why did we find these conflicting results? One possibi-
lity is that peccaries are not large consumers of Myristi-
caceae fruit. It is known that peccaries consume a wide
variety of species in tropical forests [33]. However, the
abundance of each species in peccary diets is less well
known [33]. Peccaries may focus largely on palms and eat
other fruit as and when they happen upon it [32,39].
Arboreal frugivores such as toucans and primates will
also likely have a large effect on the availability of fruit on
the ground. Further data on peccary and other frugivore
diets are required. In addition, palm seeds likely remain
attractive to peccaries (if not viable) long after abscission
because of their hard seed coat. Myristicaceae seeds are
not protected in this way and quickly decompose.
Alternatively, there may be a difference in the pattern
of abscission of palm and Myrsticaceae fruit and the seed
shadows these generate. Palm fruits are held in a single
infructescence at the top of the tree. These fruit then fall
in rapid succession, creating a very dense carpet of fruit
around the tree with a short dispersal tail [34]. Animals
Table 2 Abundances of tree species with significantly high or low relative abundances in areas influenced by large
arborescent palms on the Yasun? FDP in the first census
Abundance in quadrats:
Species Non-palm Palm Proportion in non-palm
Acalypha cuneata 252 64 0.80
Acidoton nicaraguensis 862 117 0.88
Aniba guianensis 40 14 0.74
Bertiera guianensis 5 4 0.56
Calyptranthes bipennis 66 4 0.94
Calyptranthes sedosa 66 4 0.94
Discophora guianensis 64 3 0.96
Endlicheria ? dori ? 74 4 0.95
Eugenia pusilliflora 216 18 0.92
Garcinia brasiliensis 40 0 1.00
Geonoma aspidiifolia 721 71 0.91
Guarea fistulosa 349 37 0.90
Guatteria scalarinervia 95 7 0.93
Hyospathe elegans 120 11 0.92
Inga auristellae 635 86 0.88
Leonia glycycarpa 173 15 0.92
Licania nervifina 65 3 0.96
Lacistema nena 41 0 1.00
Matisia oblongifolia 1537 322 0.83
Miconia multispicata 36 16 0.69
Miconia tipica 204 54 0.79
Mollinedia killipii 89 4 0.96
Neea ?bajio ? 197 14 0.93
Otoba glycycarpa 44 16 0.73
Pentagonia spathicalyx 28 12 0.70
Picramnia ? mini ? 30 0 1.00
Piper ?obchic ? 1702 183 0.90
Pourouma bicolor 550 67 0.89
Pouteria trilocularis 45 1 0.98
Sorocea muriculata 262 26 0.91
Tococa guianensis 1 6 0.14
Unonopsis veneficiorum 330 33 0.91
Hippocrateaceae ?atenumembra ? 179 18 0.91
Eugenia ? smedcomun ? 195 20 0.91
Solanaceae ?plata? 3 4 0.43
Species in bold are those with more individuals than expected in quadrats close to palm trees. All other species have more individuals than expected in quadrats
far from palm trees.
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rooting around in this small area will likely have a big
impact on the juvenile plants growing there [40]. Myristi-
caceae trees, on the other hand, have a much larger
canopy, the fruit carpet is thinner and more spread out.
Animals foraging for fruit here will likely have a lower
impact on juvenile plants.
A final possibility is our assumption that the fronds of
mature and immature palms are equivalent does not hold,
and that immature palm trees have lighter and/or smaller
leaves that cause less damage to seedlings and saplings
when they fall. We were not able to compare leaves from
both types of palm trees to verify this, although Iriartea
leaves do change morphology throughout their life cycle
[23,41]. Furthermore, leaves falling from shorter immature
palms will have lower velocity and might do less damage
than leaves falling from the greater height of mature
palms. Finally, the size cut-offs determined by Iriartea for
mature and immature individuals might be different for
other species. However, these species are much less abun-
dant than Iriartea and are unlikely to significantly influ-
ence our results.
Implications for forest diversity and community structure
Given the difficulties of reliably measuring seedling
growth, it was not possible to repeat all three tests of
dynamic data in both seedlings and saplings. Growth and
resprouting were analysed solely in saplings. However, it
seems that significant mortality of seedlings occurs in the
vicinity of palm trees, but that saplings can generally
withstand physical damage caused by peccaries and/or
palm fronds, and rather suffer reduced growth and can
potentially resprout. This difference in mortality implies
that different mechanisms are at work at different life
history stages and that if seedlings can grow large
enough, their fate is more secure [42]. The differences in
spatial structure and sapling density around palms are
therefore more likely to be formed at the seedling stage
than the sapling stage. The small-scale repulsion of sap-
lings (Figure 1B) may be a consequence of the immediate
negative effect of large palms on seedlings (falling palm
fronds cause increased mortality and stem breakage in
neighboring saplings) and the large-scale effects (Figure
1A) could be a long-term cumulative population
dynamics effect that results from many generations of
palms having a negative impact on nearby seedlings.
The impacts of palms on the forest structure are of
smaller spatial scale than that hypthesized by Peters et al.
[15], who suggested that the effect of palms extended out
to 7 m and that at least a quarter of lowland forest could
be impacted by falling palms fronds per year. We found
significant negative effects of palm trees out to only 3 m
(in terms of over-dispersion of saplings [spatial pattern])
and 5 m (in terms of species repelled [ISAR]). Given the
spatial pattern and density of palm trees in our plot, the
0 5 10 15 20
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Distance from focal species (m)
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Figu re 3 Spatial analysis of the species diversity around large palm trees. Indi vidual species area relationship (ISAR ) for arborescent palm s
in the Yasun? FDP from the first census. We used a heterogeneous Poisson null model which accounts for some degree of aggregation in the
focal species. We show ISARs for ( A) mature large palms and ( B) immature large palms. Each pane shows the ISAR statistic for each distance
(circles). Confidence envelopes are the 5th highest and lowest ISAR of 199 randomizations of the patterns over the study region. Points lying
outside of the confidence envelope (filled circles) indicate significant ?diversity accumulator ? (above) or ? diversity repeller ? (below) with respect to
the number of neighbouring sapling species.
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0.0 0.5 1.0 1.5
?
?
?
?
79
10
185
65
N
537
27
34
2
Far
Far
Near
Near
Female
Mature
Far
Near
Far
Near
Male
Immature
Odds Ratio of Survival
Se
ed
lin
g L
oc
ati
on
Myrist.:
Palm:
Fi gu r e 4 Seedling survival around large palm trees. The odds ra t ios of seedling surviv a l near (< 10 m) and f ar (> 10 m) from ma ture and
immature large palm trees (indicated by blue circles), and female and male Myristicaceae (indicated by red squares). Each odds ratio is indicated
by a point with SE error bars. Significant differences in survival of seedlings far from both classes of focal tree (far-far, indicated by a vertical
dashed line) are indicated by filled points ( P < 0.05), non-significant differences by empty points.
5.0 6.0 7.0 8.0
?
?
?
?
10109
2344
28869
13049
N
43654
4923
4802
992
Far
Far
Near
Near
Female
Mature
Far
Near
Far
Near
Male
Immature
A) Survival
Sa
pli
ng
 Lo
ca
tio
n
Myrist.:
Palm:
0.10 0.14 0.18
?
?
?
?
7598
1706
21373
9630
N
32278
3725
3567
737
Odds Ratio
B) Negative Growth
0.12 0.14 0.16 0.18 0.20
?
?
?
?
7598
1706
21373
9630
N
43654
4923
4802
992
C) Resprouting
F i gu r e 5 Dynamics of saplings around large palm trees and large Myristicaceae trees. The odds ra t ios of sa p l ing survi v a l (A ) , negat i ve
growth ( B) and resprouting ( C) near (< 10 m) and far (> 10 m) from mature and immature large palm trees (indicated by blue circles) and
female and male Myristicaceae (indicated by red squares). Each odds ratio is indicated by a point with SE error bars. Significant differences in the
response of seedlings far from both classes of focal tree (far-far) are indicated with solid points ( P < 0.05). The vertical dashed line indicates the
coefficient estimate for the baseline state (far-far).
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area of forest predicted to be directly affected by this pro-
cess is therefore reduced to 17%, although we noted
above that these effects could multiply over generations
leading to large areas of lower sapling density.
The negative impacts identified above appear limited
to large palms and do not involve other fruiting trees
such as the Myristicaceae. We would conclude therefore
that this process is not a disturbance that affects large
swathes of forest (or everywhere there is a tree that pro-
duces large peccary-consumed fruit). If the effect is lim-
ited to the environment of palms, this creates
heterogeneity in the forest, which may lead to a wide
variety of regeneration niches for species that can with-
stand the effects of falling leaves, fruit and rooting frugi-
vores [43]. Once established, however, these individuals
may have better access to light and soil resources, given
the diffuse nature of palm canopies and the large
amounts of decaying fruit and animal faeces that likely
accumulate around the base of palm trees. The stilt-
roots of many arborescent palms probably increase
nutrient availability by trapping leaves and organic
matter.
This kind of widespread small-scale disturbance cre-
ates heterogeneity in regeneration niches in both space
and time. Fruiting and frugivory by peccaries is episodic,
and palms generally mature one infructescence at a
time. Furthermore, in the aseasonal forest of Yasun?,
Iriartea fruit production is not confined to a few
months of the year (Nancy Garwood, unpublished data).
Confoundingly, palm fronds are also produced regularly
throughout the year. Beck et al. [36] found no difference
in leaf-fall rates between two widely separated forests in
Peru. In seasonal sites such as Yasun?, therefore, where
seedling germination takes place throughout the year,
some individuals may escape damage simply by growing
enough before the next frond or infructescence falls. In
more seasonal forests where germination is often
restricted to short periods, individuals are of similar
ages and/or vulnerabilities and so may suffer greater
impact. A further test of our hypotheses could take
place in seasonal forest and examine if seedlings and
saplings suffer greater mortality during the fruiting sea-
son (therefore more likely caused by peccaries) or dur-
ing the non-fruiting season (more likely leaf-fall).
The ubiquitous nature of the palm family in Neotropi-
cal forests implies that given some effect, palm trees
could be a powerful force structuring these forests [15].
Several species of tree dominate large areas of lowland
forests in western Amazonia, and arborescent palms
such as Iriartea are among this ?oligarch? group
[24,26,28]. Widespread small-scale mosaics created by
these palms may affect the composition of advanced
regeneration for when a larger canopy gap does open.
However, we note that peccaries are among the first
large mammals to be hunted out of forest near to
human habitation. Hunting will likely have dramatic
effects on forest structure [32].
If reduced survival and growth around palms is pre-
dictable and selective, what can we hypothesize about
species that occur in the neighbourhood of palms? Spe-
cies that are better able to survive damage by falling
fronds or rooting peccaries would be more likely to sur-
vive in areas close to palm trees. From our community-
level analyses we cannot identify traits of individual spe-
cies. However, species with underground storage organs
or cotyledons might find an advantage in germinating
near to a large palm because of their increased resource
availability allowing resprouting following damage [15].
We identified a number of species that had significantly
higher or lower abundance around palms - identification
of key functional traits of these species implicated by
this pattern would be useful. An advantage might even
apply to the seedlings of arborescent palm trees them-
selves, if they can survive predation and falling fronds.
Iriartea is one of the most widespread and abundant
tree species in western Amazonia. If Iriartea seedlings
can survive better in the adult zone of influence than
the majority of non-palm species, this may go some way
to explaining how such abundant populations can be
maintained. Future work should therefore look for more
evidence of selection potential of the process that Peters
et al. [15], Beck et al. [36] and we have identified. What
species are selected for? Does species diversity change
predictably from seedlings to saplings? Are there species
that appear more frequently together in proximity to
palms than in other parts of the forest? Furthermore, a
broader-scale comparison with other forests may be
helpful. For example, the forests of SE Asia are not
dominated by palms as are Neotropical ones, and yet
peccaries have a significant impact on seedling and sap-
ling communities [31].
Palms themselves are not immune to the effects of
branch falls [44] and suffer negative density dependence
[45], caused by falling fronds [22,46-48], peccaries
[32,34], and pathogenic fungi [49]. Although palm trees
significantly impact non-palms, the combination of fall-
ing fronds and peccary seed predation and fungal attack
inhibit population growth such that palms may currently
be at maximum density in the forest.
Conc lusions
On a much larger scale then previously tested, we exam-
ined hypotheses that peccaries and/or falling palm
fronds are major structuring forces of lowland Neotropi-
cal rain forests. We found a restricted but significant
direct effect of large arborescent mature fruiting palms
on the spatial structure, population dynamics and spe-
cies diversity of neighbouring sapling and seedling
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communities. These effects were not found in smaller
non-fruiting palm trees. However, this evidence of a pri-
mary effect of peccaries on the seedling and sapling
communities around palms was not supported in data
from other edible species in the Myristicaceae.
Given the abundance of arborescent palm trees in
Amazonian forests, it is reasonable to conclude that
their presence does have a significant, if spatially-
restricted, impact on juvenile plants. The widespread
effects of these small-scale disturbances appear, over
long time-scales, to cause directional changes in com-
munity structure. However, the population growth of
large arborescent palms themselves is very likely limited
by the very same two factors that impact their sur-
rounding juvenile plant communities.
Me thods
Tree and sapling data
A 25-ha permanent forest dynamics plot (FDP; http://
www.ctfs.si.edu) is located inside Yasun? National Park
(0?41S, 76?24W; [50]), a still largely wilderness, tropical
lowland aseasonal rain forest in eastern Ecuador [51].
Mean annual rainfall is approximately 2800 mm and
total monthly rainfall is almost never ? 100 mm. Mean
monthly temperature is 25-27?C [50]. The FDP ranges
from 216 to 248 m a.s.l: it includes two ridges and an
intervening valley that floods for brief periods. From
1995-1999, all freestanding stems ? 1 cm diameter at
breast height (dbh at 1.3 m), excluding lianas, were
tagged, mapped and identified [50]. In the first census,
1104 morph species were recorded, comprising 151,230
individual trees [50]. The FDP was recensused in 2002-
2003 [52].
There are four species of arborescent palm in the
Yasun? FDP: Astrocaryum chambira Burret, Iriartea del-
toidea Ruiz & Pav., Oenocarpus bataua Mart., and
Socratea exorrhiza (Mart.) H. Wendl. The majority of
individuals are Iriartea (Table 1). Although the relation-
ship between stem diameter and height in palms is not
as robust as that in dicotyledon trees, Iriartea generally
reaches maturity around 15 cm dbh [53]. Because the
height of palms is not measured on the FDP, we took
this diameter as the cut-off between mature and imma-
ture large palms. In order to examine the interaction
between frugivory and leaf-falls, we compared mature
fruiting palms (> 15 cm dbh) to large palms without
fruit, being those 10-15 cm dbh.
The size at which tropical trees mature is difficult to
examine and often unknown for many species and can
depend on a number of factors such as light availability,
nutrient and water resources. However, the Myristica-
ceae at Yasun? have been studied intensively for the pre-
vious 10 years, and trees have been visited multiple
times to look for signs of reproduction. The family is
dioecious and all reproductive (ie. mature) male and
female trees have been identified and sexed from flowers
and/or fruit [54-58]). The environment below a male
and female Myristicaceae adult should be qualitatively
similar, allowing the separation of the effect of fruit
crop and associated frugivores from the effects of light
availability or habitat quality on the performance of
seedlings and saplings.
Seedling data
Within the 25-ha FDP, 339 1 m2 seedling plots were
established along trails in 2002 [59]. They were arranged
around seed traps in sets of three as part of a long-term
community phenology study. Survival, growth and
recruitment are monitored every year and we use data
from 2003 to 2008.
Data analysis
We conducted two sets of analyses. First we looked at
the static spatial patterns of saplings and trees in the
FDP. Second we examined the demographic rates of
seedlings and saplings to understand the causes of these
patterns. In all analyses, we tested the previously identi-
fied potential drivers of spatial patterns and demogra-
phy. These were (i) large mature arborescent palms > 15
cm dbh, (ii) smaller, immature arborescent palms 10-15
cm dbh, (iii) large mature female Myristicaceae trees,
(iv) large mature male Myristicaceae trees. In compari-
sons examining palms, differential responses based on
proximity to larger or smaller palms are likely due to
the effects of fruiting, while similar responses could be
attributed to large, falling fronds common to both
groups. Comparisons between male and female Myristi-
caceae isolate the effects of a large fruit crop and may
generalize impacts of peccaries, if any exist, of the large
palms. Unless otherwise stated, all analyses were con-
ducted with R [60].
Spatial patterns of distribution and density
In order to examine patterns of attraction and repulsion
between two sets of spatially-explicit points, we used an
extension of the O-ring statistic for bivariate patterns
[61] to test, for example, the density of saplings (1-2 cm
dbh) at various distances r around large palms (> 15 cm
dbh). More formally, the O-ring statistic O12(r) for a
bivariate pattern composed of type 1 and type 2 points
yields the average density of type 2 point within rings of
radius r and width dr around the points of pattern 1.
The O12(r) is also called neighbourhood density function
and is closely related to the pair correlation function g12
(r), i.e., O12(r) = l2g12(r) [61,62] where l2 is the average
density of type 2 points in the plot.
To find out if the distribution of saplings in the neigh-
bourhood of palms or Myristicaceae trees is different
from a distribution expected by chance for each of these
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analyses we initially tested two different null models of
spatial distribution. The first null model retained the
spatial distribution of saplings and assumed a random
distribution of palms (i.e., a homogenous Poisson null
model [61]). This null model therefore compares the
observed neighbourhood density of saplings around
palms with sapling densities in random locations. If the
neighbourhood density of saplings around focal trees is
smaller (or larger) than expected for randomly relocated
focal trees we can infer a negative (or positive) impact
of focal trees on saplings. However, we could observe
the same pattern if (larger-scale) environmental hetero-
geneity acted such that the focal trees were located in
areas of higher or lower overall sapling density. We
therefore used a second null model that approximately
factors out such larger-scale environmental variability
and reveals the ?pure? smaller-scale effects of focal trees
on saplings (e.g. [63-65]). The second test also assumed
a random distribution of palms, but the palms were
only displaced within a given neighborhood of 30 m.
The neighborhood of 30 m is somewhat larger than the
expected range of direct interactions between focal trees
(i.e., palms and adult Myristicaceae trees) and saplings
(< 10 m based on ePeters2004). Technically, this null
model was implemented as a heterogeneous Poisson
process with a non-parametric kernel estimate of the
intensity function l1(x) of the focal trees (for details see
[64]).
We made these comparisons for (i): non-palm sapling
distributions versus mature and immature palms and (ii)
non-palm sapling distributions versus male and female
Myristicaceae. All analyses were run for 199 simulations
and 95% simulation envelopes were calculated. These
analyses were conducted using the Programita software
package [61].
Spatial patterns of community structure
While the previous analysis focused on overall sapling
density we also carried out tests where we compared the
species diversity of sapling communities that were influ-
enced by palms to sapling communities that were not.
For the first two tests we compared sapling (1-2 cm
dbh) communities in 5 ? 5 m quadrats that either con-
tained ? 1 palm or were adjacent to a quadrat contain-
ing a palm to quadrats that were > 1 quadrat distant
from a palm-quadrat. This accounted for the up to 10
m distance over which palm fronds fall. In the third
test, we examined the individual species-area relation-
ships between palms and saplings.
First, we tested whether sapling density, species rich-
ness and rarefied species richness per two individuals
were lower in quadrats influenced by palms, using the
?vegan? R package [66]. This provided a basic description
of the community spatial structure with minimal consid-
eration of species identity.
Second, we compared the community composition of
saplings in quadrats using a multiple response permuta-
tion procedure (adonis), in ?vegan? [66]. This method is
analogous to a multivariate analysis of variance and pro-
vides a robust test of whether there is a significant dif-
ference between the species composition of palm and
non-palm quadrats. Palm and non-palm quadrats may
have equivalent species richness yet these species need
not be identical. We also compared the abundance of
every species in the plot in palm and non-palm quadrats
using a proportion test, with the expected relative abun-
dance set to 85% of individuals in non-palm quadrats
(the proportion of all quadrats that were non-palm).
Species with significantly higher or lower abundances
than expected (P < 0.05) were identified.
Third, we examined the individual species area rela-
tionships (ISAR; [64]) for neighbourhoods around indi-
vidual large palms. The ISAR unites spatial patterns and
species identity. It allows for a much subtler assessment
of species effects on local diversity with respect to their
interactions with plants of other species than the two
previous methods because it considers each interspecific
interaction rather than the focal species versus all spe-
cies pooled. The ISAR(r) function is the expected num-
ber of species within radius r around an arbitrary
individual of a target species. Technically, the ISAR
function can be expressed for a given focal species f as
sum of nearest neighbor distribution functions Dfi(r)
because the probability that a given individual of species
i is within distance r of an individual of the focal species
f is given as 1-Dfi(r):
ISARf (r) =
S
?
i=1
(1? Dfi(r)) (1)
ISAR is a statistic to analyse the spatial diversity struc-
ture in forest ecosystems and reconciles common species
area relationships [67-69] and the individual perspective
of point-pattern analysis [63,70]. The ISAR allows for a
subtle assessment of the effect of palms (or adult Myristi-
caceae) trees on the non-palm sapling diversity in their
neighbourhood. If negative interactions of the focal spe-
cies on saplings dominate, the target species would
decrease the proportion of species in its neighborhood (i.
e., a diversity repeller). Conversely, if the target species
exerts positive interactions to non-palm saplings, the tar-
get species would accumulate and maintain an over-
representative proportion of sapling diversity in its proxi-
mity (i.e., being a diversity accumulator). Finally, if posi-
tive and negative interactions are weak or even out, the
focal species would behave neutrally.
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Similar to the case of the neighbourhood density
described above, environmental heterogeneity may cause
repeller or accumulator effects in the absence of species
interactions if the focal species is predominantly located
in areas of low or high sapling diversity. We therefore
contrasted the observed ISAR(r) function to that of the
same null models as for the analyses of neighbourhood
density. In the first null model we distributed individuals
of palms randomly over the entire plot. The second test
also assumed a random distribution of palms, but the
palms were only displaced within a given neighborhood
of 30 m to remove in the null model potential interac-
tions with saplings and to guarantee that the displaced
palms will be as well located in areas with low sapling
density. The neighborhood of 30 m is somewhat larger
than the expected range of direct interactions between
focal trees. These analyses were conducted in Progra-
mita, for more details of ISAR, see Wiegand et al. [64].
We hypothesize that large palms are a diversity repel-
ler because of the disturbance effects of falling fronds or
rooting damage by palm fruit consumers in the vicinity
of palms. Only a subset of species would have the traits
necessary for resprouting and continued growth follow-
ing damage from nearby palms.
Dynamic demographic effects of large trees on seedlings
To examine the effects of proximity to large palms and
Myristicaceae on seedling survival, for each of the 339
seedling plots located in the FDP we calculated the total
number of new recruits of all species between 2003 and
2007. We then calculated the number of each cohort
surviving one year. We modelled the proportion of sur-
vivors in each plot as a function of location relative to
mature and immature large trees with a generalised lin-
ear model with binomial errors as above.
Dynamic demographic effects of large trees on saplings
We examined the survival, growth and resprouting of
saplings 1-2 cm dbh from the first to the second plot
census as a function of whether the sapling was near to
(within 10 m) or far from (> 10 m) focal trees (palm or
Myristicaceae). First, we modelled the probability of sur-
vival to the second census of all saplings alive in the
first census. Second, we modelled the probability of
each sapling resprouting (new sprouts growing up and
out from damaged or broken stems). Third, growth rate
for each sapling from the first census to the second cen-
sus was calculated as growth = (dbh1 dbh0)/(time1
time0) and divided into negative (1) or ? zero growth
(0). We modelled the probability of a negative growth
rate between censuses. In all three cases we used a gen-
eralised linear model with binomial errors. We modelled
survival (or growth or resprouting, all binary response
variables) as a function of proximity to the nearest focal
tree (mature and immature palm or male and female
Myristicaceae): survival ~ mature palms * immature
palms. We coded each sapling as near or far (</> 10 m)
from focal trees. We included the interaction term
because saplings could be near to a mature palm but far
from an immature palm, for example.
Acknowledgements
We thank two reviewers for their comments that improved the manuscript.
The Forest Dynamics Plot of Yasun? National Park has been made possible
through the generous support of the Pontifical Catholic Universi ty of
Ecuador funds of donaciones del impuesto a la renta , the government of
Ecuador, the US National Science Foundation, the Andrew W. Mellon
Foundation, the Smi thsonian Tropical Research Institute, and the University
of Aarhus of Denmark. The Yasun? Forest Dynamics Plot is associated to the
Center for Tropical Forest Science, a global network of large-scale
demographic tree plots.
Author details
1 Department of Evolution, Ecology and Organismal Biology, The Ohio State
University, Columbus, OH 43210, USA. 2 Department of Plant Pa thology,
University of California, Davis, CA 95616, USA. 3 Department of Ecological
Modelling, UFZ Helmholtz Centre for Environmental Research-UFZ, PF
500136, D-04301 Leipzig, Germany. 4 Laboratory of Plant Ecology, School of
Biological Sciences, Pontifi cal Catholic University of Ecuador, Quito, Ecuador.
Authors? contributions
SAQ conceived the study, carried out the statistical analyses and drafted the
manuscript. MRM participa ted in the design of the study and helped draft
the manuscript. TW oversaw the spatial analyses and interpretation. RV
helped conceive and design the study. All authors contributed to, read, and
approved the final manuscript.
Received: 19 October 2011 Accepted: 19 March 2012
Published: 19 March 2012
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doi:10.1186/1472-6785-12-3
Cite this article as: Queenborough et al.: Palms, peccaries and
perturbations: widespread effects of small-scale disturbance in tropical
forests. BMC Ecology 20 12 12 :3.
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