Heliconia Acuminata: Habitat Fragmentation and The Demographic Structure of An Amazonian Understory Herb
Heliconia Acuminata: Habitat Fragmentation and The Demographic Structure of An Amazonian Understory Herb
Heliconia Acuminata: Habitat Fragmentation and The Demographic Structure of An Amazonian Understory Herb
Abstract: Little is known about the demographic consequences of fragmentation for plant populations. By
assessing the population structure of a common herb ( Heliconia acuminata) in an experimentally fragmented
landscape in the central Amazon, we tested the predictions that fragmentation could reduce population den-
sity, alter population structure, and reduce reproductive effort. Population density in continuous forest var-
ied six-fold, some areas having high density and others low density. Population density in small fragments
and on the edges of large fragments was often low, but it was within the range of densities found in continu-
ous forest, and the difference between locations was not significant. Heliconia populations in forest fragments
were skewed toward smaller demographic size classes, however. Because reproduction in H. acuminata is pos-
itively correlated with plant size, these shifts were predicted to result in fewer flowering plants in forest frag-
ments. The proportion of the population flowering in forest fragments and continuous forest was not signifi-
cantly different, although there was a trend toward proportionately greater flowering in continuous forest.
For plants that did flower, per-individual reproductive success (measured as developing fruit set) was the
same in forest fragments and continuous forests. Our results suggest that per-individual and population-level
reproduction by understory herbs in tropical forest fragments may be resistant to the detrimental conse-
quences of fragment isolation. Our study also highlights the need to consider how fragmentation influences
aspects of population structure and demography beyond abundance and fruit production, because these al-
ternative measures of population structure can be modified in forest fragments in subtle, unexpected ways.
Fragmentación del Hábitat y la Estructura Demográfica de una Hierba (Heliconia acuminata) del Sotobosque
Amazónico
Resumen: Se conoce poco de las consecuencias demográficas de la fragmentación sobre poblaciones vege-
tales. Probamos las predicciones de que la fragmentación puede reducir la densidad poblacional, alterar la
estructura de la población y reducir el esfuerzo reproductivo, evaluamos la estructura poblacional de una hi-
erba común ( Heliconia acuminata) en un paisaje experimentalmente fragmentado en la Amazonía central,
La densidad poblacional en bosque continuo varió hasta seis veces, con algunas áreas con alta densidad y
otras con baja densidad. La densidad poblacional en fragmentos pequeños y en los bordes de fragmentos
grandes a menudo fue baja, pero estaba en el rango de las densidades encontradas en el bosque continuo, y
la diferencia entre localidades no fue significativa. Sin embargo, las poblaciones de Heliconia en los fragmen-
tos de bosque estaban sesgadas hacia las clases de tamaño demográfico más pequeñas. Debido a que la re-
§ Current address: Department of Wildlife Ecology and Conservation, University of Florida, PO Box 110430, Gainesville, FL, 32611, U.S.A.,
email brunae@wec.ufl.edu
Paper submitted October 28, 1999; revised manuscript accepted November 28, 2001.
1256
producción en H. acuminata esta positivamente correlacionada con el tamaño de la planta, se predijo que es-
tos cambios resultarían en menos plantas florecientes en los fragmentos de bosque. La proporción de la
población floreciente en los fragmentos de bosque y en el bosque continuo no fue significativamente difer-
ente, aunque hubo una tendencia hacia una mayor proporción de plantas florecientes en el bosque con-
tinuo. Para plantas que florecieron, el éxito reproductivo por individuo (medido como el desarrollo de fru-
tos) fue igual en fragmentos de bosque que en bosques continuos. Nuestros resultados sugieren que la
reproducción, por individuo y al nivel poblacional, de hierbas del sotobosque en fragmentos de bosque tropi-
cal puede ser resistente a las consecuencias perjudiciales del aislamiento por fragmentación. Nuestro estudio
también resalta la necesidad de considerar como la fragmentación influye sobre aspectos de la estructura po-
blacional y la demografía más allá de la abundancia y producción de frutos, debido a que estas medidas de
estructura poblacional alternativas pueden ser modificadas de manera sutil e inesperada en los fragmentos
de bosque.
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1258 Fragmentation and Plant Population Structure Bruna & Kress
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Bruna & Kress Fragmentation and Plant Population Structure 1259
Table 1. Biological Dynamics of Forest Fragments Project reserves in which H. acuminata demographic plots were established,
their year of isolation, and attributes of plant populations measured.a
Straight-billed Hermit (P. bourcieri ) as its primary polli- marked demographic plots 50 100 m in size. Six plots
nators in our study sites (Stouffer & Bierregaard 1995; were in continuous forest (CF 1–6), four were in 1-ha
Bruna 2001). fragments (FF 1–4), and three were in 10-ha fragments
Heliconia acuminata is a self-incompatible hermaph- (FF 5–7) ( Table 1). Demographic plots in 1-ha fragments
roditic perennial with limited vegetative reproduction were established at random on either side of the frag-
( E.M.B and W.J.K., unpublished data). Flowering begins ment, plots in 10-ha fragments were established in the
in late January and continues through April. Most repro- fragment center, and plots in continuous-forest sites
ductive plants have one inflorescence with a total of 20– were haphazardly placed at locations 500–4000 m from
25 flowers (Bruna 2001). Each flower is open for 1 day, borders of secondary and mature forest.
after which the perianth and the style abscise. Each fruit In January 1998, we marked all the H. acuminata
produces a maximum of three seeds (mean number of plants in the seven demographic plots in forest frag-
seeds/fruit 1.9 .027 SE, n 873 fruits), and mature ments and three of the continuous-forest plots (CF 1–3).
fruits are dispersed by birds (Kress 1983). Each plant was marked with a stake to which we at-
Heliconia acuminata can be long-lived (20 years; tached an individually numbered aluminum tag. For
W.J.K., personal observation), as is the case for many each plant we counted the number of vegetative shoots
other tropical understory herbs ( Horvitz & Schemske and measured the height by the distance from the base
1995). As a result, it is probable that many of the individ- to its highest point above the ground. During the 1998
uals currently found in forest fragments were alive when reproductive season, we regularly surveyed the 10 estab-
fragments were initially isolated. This assumption is sup- lished plots and recorded which individuals were flow-
ported by ongoing demographic censuses that indicate ering, how many flowers each produced, and the num-
high survivorship of established plants ( Bruna 2001). ber of flowers developing into fruits.
In August 1998, we established plots in three addi-
tional continuous-forest sites (CF 4–6) and measured
Demographic Plots and Censuses
plants as before. Because previous research at the BD-
As part of a long-term study of the population dynamics FFP has demonstrated the importance of edge effects for
of H. acuminata , we established 13 permanently plants in medium-size fragments ( Benitez-Malvido 1998;
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1260 Fragmentation and Plant Population Structure Bruna & Kress
Laurance et al. 1998), we also surveyed (but did not Analyses of Reproductive Characteristics
mark or measure) all the plants in identical 50 100 m
plots on a randomly selected edge and corner of the To determine if the proportion of the population that was
10-ha fragments in which demographic plots were lo- reproductive differed among fragments and continuous for-
cated. In 1999 we returned to survey all 13 demographic est, we used Kruskal-Wallis tests. These analyses were con-
plots and recorded reproduction as in the previous year. ducted on both the 1998 and 1999 survey results. We also
plotted the proportion of individuals flowering in each de-
mographic size classes for populations in each habitat type.
To calculate female reproductive success for individuals
Analyses of Plant Density that did flower, we divided the total number of developing
To test the hypothesis that plant density is reduced in fruits on each plant by the number of flowers it produced.
forest fragments, we compared the total number of plants The fruit-set percentages in forest plots were then com-
found in demographic plots located in continuous forest, pared to the values from 1-ha and 10-ha fragments with
1-ha fragments, 10-ha fragment corners, 10-ha fragment Kruskal-Wallis tests. Plants from different plots within the
edges, and 10-ha fragment centers. To conduct this analy- same habitat type (i.e., 1-ha and 10-ha fragments and con-
sis, we used the August 1998 surveys of plant density tinuous forest) were pooled because of limited sample
conducted in 10-ha fragment edges and corners and the sizes in some fragments. This analysis was done for both
January 1999 survey results from plots in the remaining the 1998 and 1999 flowering seasons.
locations. Because the number of plots located in the dif-
ferent habitat types was limited, we could not examine
the distributional assumptions of parametric tests. We Results
therefore used the nonparametric Kruskal-Wallis test for
Plant Density
this analysis.
Heliconia acuminata density ranged from 112 to 753
individuals per plot ( Table 1). Although the rank order
Analyses of Vegetative Characteristics
and Demographic Structure
To compare the demographic structure of Heliconia
populations in continuous forests and forest fragments,
we used log-linear modeling. We first placed plants into
six size classes based on height (0–15, 15–30, 30–45,
45–60, 60–75, and 75 cm). We used height because
age is usually impossible to determine in tropical herba-
ceous taxa; furthermore, size is usually a better predic-
tor of reproductive potential and plant fate ( Horvitz &
Schemske 1995). Height and shoot number were strongly
positively correlated in this system (n 4326, 0.716,
p 0.0001), and results were similar for analyses based
on shoot number. We therefore present comparisons of
population structure based on height only.
Our null hypothesis was that the number of plants in
each demographic size class was independent of both
habitat type (i.e., 1-ha fragment, 10-ha fragment, and
continuous forest) and plot identity (i.e., FF 1–7, CF1–
6). To determine the importance of habitat type for pre-
dicting the number of plants in each size class, we com-
pared the goodness of fit to the observed data of the null Figure 2. Density of plants per demographic plot in
model with that of models including habitat type. Two each habitat type: 1-ha fragments, 10-ha fragment
models testing the importance of habitat type were edges, 10-ha fragment corners, 10-ha fragment centers,
used, one that included and one that excluded plot iden- and continuous forest. The upper and lower limits of
tity. Similarly, the importance of plot identity was tested the box represent the seventy-fifth and twenty-fifth per-
with models that both included and excluded habitat centiles, respectively. The line through the box is the
type. Finally, the goodness of fit of a saturated model median value. Marks beyond the error bars represent
was used to test the importance of the interaction be- outliers less than or greater than the tenth and nineti-
tween habitat type and plot location. eth percentiles.
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Bruna & Kress Fragmentation and Plant Population Structure 1261
Reproductive Characteristics
Differences in the proportion of the population that
flowered in 1-ha fragments, 10-ha fragments, and continu-
ous forests were only marginally significant in 1998 (H
5.0, p 0.08) and not significant in 1999 (H 4.34,
p 0. 11), although in both years there was a trend to-
ward a greater proportion of the population flowering in
continuous forest sites ( Fig. 4).
As might be expected, the probability that an H. acumi-
nata individual would flower increased with plant size
( Fig. 5). Although the proportion of individuals that flow-
ered in each demographic size class often varied substan-
tially from plot to plot, the proportion flowering in each
size class was similar for populations in 1-ha fragments,
10-ha fragments, and continuous forest ( Fig. 5).
Median fruit set was not significantly different in for-
Figure 3. Proportion of plants (mean 1 SD) found ests and fragments in either year (1998: H 2.103, p
in each of six height-based size classes in continuous 0.3411; 1999: H 0.842, p 0.6558). In 1998, how-
forest, 1-ha fragments, and 10-ha fragments. ever, plants in 1- and 10-ha fragments produced slightly
more fruit than those in forests (29.3% and 29.0% devel-
oping fruit set vs. 23.5%, respectively, Fig. 6).
Table 2. Results of log-linear analysis comparing the effects of habitat type (H), (i.e., 1-ha or 10-ha fragment or continuous forest), plot (P),
(i.e., FF 1–7 and CF 1–6), and their interaction for predicting the number of H. acuminata individuals in each demographic size class (S).a
Effect Contrast b
G2
df p
Habitat HP, S vs. HP, HS 141.25 10 0.001
Plot HP, S vs. HP, PS 212.78 25 0.001
Habitat, given plot HP, PS vs. HP, PS, HS 72.01 10 0.001
Plot, given habitat HP, HS vs. HP, PS, HS 143.53 25 0.001
Plot habitat size class PS, HS, HP vs. PSH 95.61 25 0.001
a
Analyses were conducted for densities recorded in the 1999 survey.
b
Notation follows Caswell (2001) and Horvitz and Schemske (1995) for denoting hierarchical models, such that all terms containing that inter-
action or lower-order interactions are included. The significance of each factor is determined by examining the change in G2 (i.e.,
G2) when a
factor is removed from a model that includes it. A constant of 0.5 was added to all cells prior to analysis (Caswell 2001).
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1262 Fragmentation and Plant Population Structure Bruna & Kress
Heliconia acuminata Density in Forest Fragments Figure 5. Proportion of plants (mean 1 SD) that
Given the broad range of densities in continuous forest were reproductive in each demographic size class in
and the lack of prefragmentation data, it is impossible to (a) 1998 and ( b) 1999.
exclude the possibility that the densities observed in for-
est fragments reflect preexisting spatial variation. This re-
sult contrasts with the findings of several other studies, in CF plots 4–6) and others at much higher density
conducted at the BDFFP and in other systems, demon- (551–749 in CF plots 1–3). Interpopulation differences
strating that populations of plants on fragment edges in abundance are not necessarily unexpected, because
are those most at risk from environmental perturbations they are the natural result of changes in demographic
(e.g., Didham 1997; Jules 1998; Laurance et al. 1998; and environmental conditions across sites (Horvitz &
Gehlhausen et al. 2000). For example, in a study con- Schemske 1995). The factors responsible for the six-fold
ducted in several of the same reserves, Benitez-Malvido range in abundance observed in our study are unclear,
(1998) found that the density of seedlings of canopy however. Although none of the continuous-forest sites
trees was lower in fragments than in continuous forest. were noticeably different in forest structure or distur-
She also found that the density of seedlings on edges of bance history, variation in both of these factors could be
large fragments was lower than in fragment interiors, al- partly responsible for the observed differences. Varia-
though the pattern was not consistent across all frag- tion in soil chemistry or texture may also influence Heli-
ments. Interestingly, H. acuminata density in two of conia density. Plots with reduced abundance may be lo-
three 10-ha fragments was lower on the edges or cor- cated in areas with sandy soils, a lower concentration of
ners than in fragment centers ( FF-6 and FF-7), whereas nitrogen, less organic matter, or higher aluminum satura-
in the other 10-ha fragment density was similar in all lo- tion, all of which might influence Heliconia growth and
cations ( FF-5; Table 1; Fig. 2). abundance. In continuous-forest sites nearby, these chem-
The density of Heliconia acuminata plants in the ical and textural parameters explain over 30% of the vari-
BDFFP’s continuous-forest reserves was highly variable, ation in the biomass of living trees (Laurance et al.
with some populations at low density (112–235 plants 1999), indicating that even in the universally weathered
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Volume 16, No. 5, October 2002
Bruna & Kress Fragmentation and Plant Population Structure 1263
Figure 6. Map of the Biological Dynamics of Forest Fragments Project and location of demographic plots. White ar-
eas are continuous forest, shaded areas represent pasture and clearings surrounding fragments, and dark lines
represent roads. See Table 1 for plot descriptions. Abbreviations: CF, continuous-forest plot; FF, forest-fragment plot.
and acidic soils characterizing our study sites, the conse- Several nonmutually exclusive mechanisms could be
quences for plant populations of small-scale variation in responsible for the observed pattern. First, large plants
soil chemistry can be significant. in fragments could have been susceptible to increased
mortality following fragment isolation, causing the pro-
portion of the population made up of the largest individ-
uals to decrease. Second, there could be a flush of post-
Demographic Structure of Heliconia acuminata Populations
isolation recruitment in forest fragments, resulting in
Although the isolation of fragments does not appear to overrepresentation of the smallest size classes. This re-
have acted consistently to reduce density in the BDFFP cruitment could be from either rhizomes that have lost
fragments, there appears to have been a shift in the de- all aboveground tissue following fragment isolation or
mographic structure of Heliconia acuminata popula- newly germinating seeds. Finally, individuals could have
tions found there. Log-linear modeling indicated that the survived in forest fragments but shifted from larger size
proportion of individuals in each demographic size class classes to smaller ones following isolation.
was not independent of habitat type, despite the signifi- Elevated mortality of large plants and proportionately
cant variation among plots. Populations in the fragments greater recruitment in fragments are almost certainly not
studied were skewed more toward smaller size classes, the mechanisms responsible for the observed demo-
with proportionately more small individuals and fewer graphic shift. Current mortality rates of plants with three
large ones than in continuous-forest plots. Individuals in or more shoots are extremely low in all locations, and
the two largest size classes (60–75 cm and 75 cm tall) they are almost identical in forest fragments and contin-
made up approximately 20% of the populations in con- uous forest ( Bruna 2001). Furthermore, Heliconia seed
tinuous forest, whereas in 1-ha fragments these individu- germination and seedling survival are three to seven
als comprised only about 8% of populations. Heliconia times lower in 1- and 10-ha fragments than they are in
populations found in the interiors of 10-ha fragments continuous forest ( Bruna 1999, 2002), and the absolute
also appeared to have been affected, although not to the number of seedlings recruited into fragments was con-
extent of those in small fragments. In the larger isolates, siderably lower than in continuous forest (17.25 15.0
the two largest size classes represented 15% of the total SD vs. 38.33 30.21 SD). The per capita rate of recruit-
population ( Fig. 3). ment, which would include both new seedlings and re-
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1264 Fragmentation and Plant Population Structure Bruna & Kress
cruits growing back from rhizomes, was similar in all Heliconia of a given size are as likely to flower in for-
habitat types in 1999 ( Bruna 2001). est fragments as they are in continuous forest ( Fig. 5 ),
Instead, the observed shift is probably due to past and suggesting that environmental cues used to initiate flow-
ongoing reductions in the number of plants in larger size ering are not altered in forest fragments. In addition,
classes. Plants that survived the slash-and-burn tech- fruit production by plants that did flower was not signif-
niques used to isolate these fragments may have done so icantly different in the different habitat types. Although
by shedding shoots and leaves, a pattern seen in other several studies have shown that fruit production by
long-lived perennials exposed to harsh conditions such plants can decrease in forest fragments as a result of re-
as drought and water stress ( Hsaio 1973; Wright 1996). duced pollen deposition or decreased pollinator visita-
Recent experimental evidence supports this hypothesis. tion rates (Aizen & Feinsinger 1994; Cunningham 2000a,
One year after Heliconia plants were reciprocally trans- 2000b; Parra-Tabla et al. 2000), our results are similar to
planted between 1-ha fragments and continuous forest, those from other studies which found that fruit produc-
plants in continuous forest grew into larger size classes, tion remained constant or actually increased in fragmented
whereas plants in fragments shrank into smaller ones areas (e.g., Aizen & Feinsinger 1994; Dick 2001). This is
( Bruna et al. 2002). If these reductions in size continue because both species of hummingbird that pollinate H.
over multiple seasons, then the size distribution of pop- acuminata at our sites appear to be resistant to the ef-
ulations in fragments could be shifted toward smaller fects of fragmentation. Results from a 12-year study doc-
size classes. The strength of these effects would proba- umenting the abundance of Phaethornis superciliosus
bly be ameliorated by the structure and species compo- and P. bourcieri in the BDFFP reserves suggest that they
sition of the surrounding forest ( Mesquita et al. 1999), move easily through the secondary growth surrounding
which can buffer plants from adverse environmental these fragments (Stouffer & Bierregaard 1995, 1996),
conditions. This may explain why size structures for and the more common of the two species (P. supercilio-
plots in 10-ha fragments, which were more protected sus) actually increases dramatically in abundance in frag-
from edge effects as a result of their location in the frag- ments during the rainy season (Stouffer & Bierregaard
ment’s core, were similar to those in continuous-forest 1996), when H. acuminata is flowering. Although hum-
locations. mingbirds are rarely species-specific ( Feinsinger 1987),
Although no comparable studies have been conducted other flowering plants in the understory of these frag-
in tropical systems, at least one analysis of plant popula- ments are rare during the rainy season (Gentry & Em-
tion structure has been conducted in temperate-forest mons 1987; E.M.B. & J.W.K., personal observation). Hel-
fragments. By taking advantage of the ability to age plant iconia acuminata is therefore the primary source of
rhizomes, Jules (1998) was able to estimate the pre- and nectar for hummingbirds moving through fragments,
post-isolation recruitment and mortality of Trillium ova- and flowering plants in fragments probably receive fre-
tum found in fragments of old-growth forest in the quent visits.
northwestern United States. In contrast to our results, Despite proportionately similar levels of reproduction
Jules found that populations that were close to clearcuts in fragments and continuous forest, however, popula-
and edges had substantially fewer seedlings and juvenile tions in 1-ha fragments could still be vulnerable to repro-
plants, whereas older age classes of Trillium were not as ductive failure in some years because the absolute num-
strongly affected by edge creation. ber of plants reproducing in them was extremely low
(Table 1). Demographic plots 0.5 ha in size located in
1-ha fragments had as few as one or two flowering
plants in them (1998: mean 4.00 2.94 SD; 1999:
H. acuminata Reproduction in Forest Fragments
mean 4.25 1.50 SD), whereas flowering plants in
Heliconia reproduction does not appear to have been analogous continuous-forest plots were 5–10 times more
compromised in the forest fragments we studied, either abundant (1998 mean 52.67 32.39 SD; 1999 mean
at the population or the individual level. Although there 26.00 26.96 SD).
was a trend toward a greater proportion of the popula- As a result of lower absolute numbers of flowering
tion flowering in continuous forest than in forest frag- plants in fragments and low developing fruit sets (Fig.
ments in both years, this difference was only marginally 6), the total number of seeds produced in fragments is
significant in 1998 and not significant in 1999 (when probably very limited. Populations in fragments may
low-density continuous-forest sites were included in the therefore depend primarily on nearby continuous-forest
analysis). The proportion of the population flowering areas for seed dispersal. Although low-density popula-
was low in all locations, ranging in 1998 from 0.7% in tions in continuous-forest also had low flowering-plant
FF-1 to 13.0% in CF-1. This is consistent with previous abundances, and hence produced few seeds, they were
studies conducted in the region in which the density of not isolated from source populations by matrix habitat
flowering and fruiting plants was found to be extremely through which frugivores may not easily disperse ( Renjifo
low (Gentry & Emmons 1987 ). 1999; Tabarelli et al. 1999). In addition to reductions in
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Volume 16, No. 5, October 2002
Bruna & Kress Fragmentation and Plant Population Structure 1265
seed availability, the lower numbers of reproductive plants Alvarez-Buylla, E. R. 1994. Density dependence and patch dynamics in
in fragments could also cause a substantial increase in in- tropical rain forests: matrix models and applications to a tree spe-
cies. The American Naturalist 143:155–191.
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fragments is limited ( Young et al. 1996). ruption and stochastic biodiversity losses. Pages 281–291 in W. F.
Our results suggest that populations of Heliconia and Laurance and R. O. Bierregaard Jr., editors. Tropical forest rem-
other tropical understory herbs may be resistant to re- nants: ecology, management, and conservation of fragmented com-
ductions in population density and the disruptions of re- munities. University of Chicago Press, Chicago.
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