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LSU Master's Theses
Graduate School
2011
Seed rain and advance regeneration in secondary
succession in the Brazilian Amazon
Lindsay Michelle Wieland
Louisiana State University and Agricultural and Mechanical College, [email protected]
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SEED RAIN AND ADVANCE REGENERATION IN SECONDARY SUCCESSION
IN THE BRAZILIAN AMAZON
A Thesis
Submitted to the Graduate Faculty of the
Louisiana State University and
Agricultural and Mechanical College
in partial fulfillment of the
requirements for the degree of
Master of Science
in
The Department of Biological Sciences
By
Lindsay M. Wieland
B. S. Dickinson College, 2004
May 2011
ii
Acknowledgements
There is no doubt in my mind that without my advisor, Dr. G. Bruce Williamson,
this project would not have turned out the way it did. From the moment we decided to
work together, his dedication to the project and to me as his graduate student went
beyond my expectations. Throughout many challenges, Bruce has been available to
discuss my ecological questions or to talk about life in general; always in an enthusiastic
and down to earth manner. For this, I can‟t thank him enough.
I thank my committee, Richard Stevens and Phil Stouffer who provided guidance
and feedback on this research. Rita Mesquita and Paulo Estefano Bobrowiec were
invaluable counterparts, without whom I would never have obtained visas to work in
Brazil. I am especially grateful to Paulo, who bent over backwards to help me get
permits, clear up logistical issues and for discussions on bat behavior and seed dispersal.
Thanks to all of the staff at the Biological Dynamics of Forest Fragments Project
for their support. In particular, I‟d like to thank M. Rosely C. Hipólito and Ary Jorge C.
Ferreira for helping organize field logistics; Cleucilene da Silva, Adriane Pantoja and
Angela Midori Furuya Pacheco for helping me navigate the bureaucracy of doing
research in Brazil; Mirtes Silva Bernardes for always lighting up my day with her smile;
and especially José Luís Camargo, for logistical support and advice. Both Mario CohnHaft and Phil Stouffer lent me mist nets, helping me keep a reasonable research budget.
There are no words to express my gratitude to Tony Vizcarra Bentos for his help
with botanical identification, enlightening discussions on forest succession and for his
friendship whether I was working in the field, in Manaus or thousands of kilometers
ii
away in Baton Rouge. Catarina Jakovac helped me with my initial site selection and
introduced me to land-owners along ZF7. My connection with the land-owners was only
possible due to the pre-existing relationships between them and the “Pioneiras” research
team, namely Rita Mesquita, Tony Vizcarra Bentos and Catarina Jakovac.
I owe a debt of gratitude to all of the people who helped me in the field. Thanks to
my field assistants: Gisiane Rodrigues Lima, Manoel do Silvo e Silvo, Antonio Darlion
and particularly Alaercio (Leo) Marajó dos Reis with whom I spent countless hours
collecting fecal samples and listening to World Cup games. I‟d also like to thank Luiz
Raimundo Queiroz for driving me from site to site.
Financial support came from a generous grant from the Conservation, Food &
Health Foundation, the National Science Foundation (DEB-0639114), and BioGrads
supplements from Louisiana State University. The Lowy Bernard Fund supported me on
an Organization for Tropical Studies field course.
There are many people in the Department of Biological Sciences at Louisiana
State University who have helped me throughout this process. In particular, Prissy
Milligan helped with logistical issues; Chimene Williams and Jill Atwood have made
sure I was reimbursed in a timely manner. My lab-mate and friends have been an integral
part of my experience in Baton Rouge. They include, but are in no way limited to: Meche
Gavilanez, Lorelei Patrick, Verity Mathis, Amanda Accamando, Jessica Deichmann and
Adriana Bravo. I also want to thank Melanie Driscoll for caring for Wilson and
MacArthur during the months I was away.
iii
My family has always been incredibly supportive during the varied adventures I
have chosen to embark on. Their love and encouragement has allowed me to travel the
world pursuing my dreams. Thank you Gary and Mary Wieland, Courtney and Sohail
Jarrahian, Jess and Andy Smith, and Wilson and MacArthur - I love you all.
Finally, I am indebted to the land-owners and their families who were gracious
enough to allow me to tromp on their land collecting seeds. Thank you to the families of
David, Odete, Mauro, Carlito, Zezito, Raimundo, Daniel and Ivo. I thank all the people
living along ZF7 for creating a great community in which to work, for always being
friendly and for sharing their fruit with me. I am particularly grateful to Carlito and
Ivonette for opening up their home to me. I shared countless laughs, and watched hours
upon hours of quality telenovelas. Muito obrigada!
iv
Table of Contents
ACKNOWLEDGEMENTS …………….…………………………..…………………….ii
LIST OF TABLES ………...……….……………………..…………………….……….vi
LIST OF FIGURES ….…………….…………………….………………..……….…...viii
ABSTRACT ……………………………………………………………………….…….ix
CHAPTER 1: INTRODUCTION…………………………………………………….…. 1
CHAPTER 2: METHODS
Study Sites ………………………………………………………………………..6
Re-sprouting …………….………………………………………………………...9
Seed Traps ………………………………………………………………………...9
Mist Nets ……………………………………………………………………...…12
CHAPTER 3: RESULTS
Study Sites …………………………………………….………………………...15
Re-sprouting …………….…………………………………………………….…21
Seed Traps …………………………………………………………………….…22
Mist Nets ……………………………………………………………………...…29
CHAPTER 4: DISCUSSION & CONCLUSIONS
Site Characteristics ………………………………………………………………31
Re-sprouting …………….…………………………………….…...…….………32
Seed Dispersal ………………………………………………….………….…….33
Mist Nets ……………...…………………………………………………………36
Arrested Succession ……………...…………………………….………………. 37
Management Implications …………………………………………………….…39
LITERATURE CITED …………….………………………………….………….……. 42
APPENDIX : SPECIES LISTS
A. Second Growth Stand Vegetation ……………………………………………50
B. Daily Seed Trap Collection …………………………………………………..57
C. Monthly Seed Trap Collection ……………………………………………….58
D. Mist-netting: Bat and Bat-dispersed Seed Species Richness and
Abundances…………………………………...………………………………59
E. Mist-netting: Bird Species Richness and Abundances ……………………….60
F. Bird-dispersed Seeds Species Richness and Abundances ………………..…. 62
VITA …………………………………...…………………………………………….… 63
v
List of Tables
Table 1.
Stand descriptions and land-use history as recorded by land-owners ….…8
Table 2.
Density and basal area, based on all stems ≥ 3 cm dbh, for Vismia and
Cecropia second growth stands.…………………..……………….…….15
Table 3.
Mean ± SD and results of ANOVA testing number and proportion of all
Vismia, Cecropia and other species in Vismia and Cecropia stands ……16
Table 4.
Pair-wise comparisons of Sørensen‟s modified index of similarity for
relative abundance and basal area in each of eight second growth stands.
Dark grey represents Cecropia-Cecropia comparisons, light grey
represents Vismia-Vismia comparisons, and white represents
Cecropia-Vismia comparisons …………………………………………..19
Table 5.
Mean ± SD and results of ANOVA testing the total number and proportion
of stems originating as resprouts of Vismia, Cecropia and other species
found in Vismia and Cecropia stands. Significant values in bold ………21
Table 6.
Total trap hours, number of feces and seeds collected in second growth
traps, diversity indexes, species richness and evenness values for seeds
dispersed into each site by second growth type ……….….…………..…23
Table 7.
Diversity indexes, species richness and evenness values for seeds
dispersed into each site by second growth type excluding rare genera such
as Clidemia, Lantana and Phytolacca. Significant values in bold …..….24
Table 8.
Number (N) and percent of total seeds collected in seed traps within each
stand type during the two time periods (day and night) …………………24
Table 9.
The effect of disperser and stand type on the number of seeds dispersed
into seed-traps for eight genera. Dispersers are birds and bats. Stand types
are Cecropia and Vismia. Significant values in bold ….…………...……26
Table 10.
Abundance of seeds month-1 stand-1 (Mean ± SD) collected in Cecropia,
Vismia and mature forest including Tukey‟s adjusted P-value for all pairwise comparisons of seeds dispersed into each stand type: VismiaCecropia second growth (V-C), Vismia-Mature forest (V-M), and
Cecropia-Mature forest (C-M). “Unknown” seeds include all seeds from
the 35 morpho-taxa not identifiable to genus. Seed numbers were logtransformed before performing the ANOVA. Significant values in
bold ……………………………………………………………………..28
vi
Table 11.
Abundance of seeds month-1 stand-1 (Mean ± SD) in different size classes
collected in Cecropia stands, Vismia stands, and mature forest including
Tukey‟s adjusted P-value for pair-wise differences in seed sizes dispersed
into each stand type: Vismia-Cecropia second growth (V-C), VismiaMature forest (V-M), and Cecropia-Mature forest (C-M). Tiny: <0.5 cm,
Small: 0.5-0.99 cm, Medium: 1.0-1.99 cm, Large: >2.0 cm. Significant
values in bold ............................................................................................28
Table 12.
Total weeks traps were open, seeds collected in monthly traps, diversity
indexes, species richness and evenness values for seeds dispersed into
each stand type. Species evenness was calculated using the ShannonWiener diversity index …………………………………………………..29
Table 13.
Abundance of seeds (Mean ± SD) collected per bird capture in Cecropia
and Vismia stands and ANOVA test results for differences in seeds
dispersed into each stand type …………………..……………….………30
vii
List of Figures
Figure 1.
Map of South America showing approximate location of field sites with
inset of a satellite image of Vismia (V1-V5), Cecropia (C1-C3) and
mature forest (M1-M5) stands .…….…….……………………….………7
Figure 2.
Seeds were collected twice a day in seed-traps assembled in Cecropiadominated second growth (shown) as well as in Vismia-dominated second
growth ……………………………….…….……………………….……11
Figure 3.
Comparison of generic dominance (≥3 cm d.b.h.) based on mean density
(A) and basal area (B) in Cecropia and Vismia dominated second growth
stands (Mean ± SD) …………………………………………………….17
Figure 4.
Non-metric multi-dimensional scaling (NMDS) ordination of the modified
Sørensen‟s index of similarity values for relative abundance (A) and
relative basal area (B) for three Cecropia and five Vismia stands. Cecropia
stands are: C1, C2, and C3. Vismia stands are: V1, V2, V3, V4,
and V5……………………………………………………………………20
Figure 5.
Species accumulation curves with 95% confidence intervals for seeds
collected in Cecropia stands (black lines) and Vismia stands
(gray lines) ………………………………....……………….…………...25
viii
Abstract
Forest regeneration on abandoned land in the Brazilian Amazon depends first and
foremost on prior land-use history. Abandoned clearcuts become dominated by Cecropia
trees, but contain a rich mix of other arboreal genera and succession proceeds rapidly to a
diverse forest. In contrast, abandoned land that has been burned repeatedly for pastures
becomes dominated almost completely by Vismia trees and remains in monogeneric
stands gaining few new genera over the same time interval. I tested the hypothesis that
areas with repeated burns would have more re-sprouts, particularly Vismia re-sprouts. I
also predicted that in monogeneric Vismia stands, seed dispersal would be limited to few
bat-dispersed genera while there would be more diverse seed rain in Cecropia,
particularly from bird dispersers.
In order to test these hypotheses, stands with different land-use histories were
evaluated in terms of tree, palm, shrub and liana abundance and diversity, as well as
whether they germinated from seed or grew as re-sprouts from the root. I found that
Vismia stems were one hundred percent re-sprouts in Vismia stands. In Cecropia stands,
93% of Vismia stems germinated from seed. There were no significant differences in the
abundance of re-sprouts by Cecropia and all other species, regardless of stand type.
To test how seed dispersal in Cecropia and Vismia stands differs, I collected seeds
fallen into seed traps by bird and bat dispersers as well as from fecal samples collected
principally from mist netted birds. I found that both bird and bat dispersers deposited a
more diverse seed assemblage into Vismia stands than Cecropia stands. Overall, bats
ix
disperse more Vismia seeds while birds disperse more Miconia seeds, regardless of stand
type.
My results suggest that seed dispersal does not drive the differences in succession
found in Cecropia and Vismia second growth. However, the capability of seeds to
germinate and recruit in Vismia stands warrants further investigation. I suggest that the
use of repeated fire should be limited as much as possible due to the long term effects on
succession after site abandonment.
x
Chapter 1: Introduction
Species composition of a regenerating forest is the result of the germination of
propagules present in the soil at the time of disturbance and those arriving early in the
successional process (Egler 1954) as well as those re-sprouting from primary forest
stumps and roots (advance regeneration). In this model, vegetation composition of
successional stages changes over time due to differences in growth rate, shade tolerance,
longevity and size at maturity (Finegan 1984, 1996). Aspects of the theory have been
supported by a number of studies in boreal (Chapin et. al. 2006), temperate (Oliver 1981;
Turner and Franz 1985), as well as tropical systems (Finegan, 1996; Hooper et. al. 2004).
However, forest regeneration following anthropogenic disturbances such as
clearcutting and use for agriculture or pasture follows a different pattern. In
anthropogenically disturbed landscapes in the Neotropics, succession may be retarded or
arrested due to the absence of disperser-limited mature forest trees (Finegan 1996;
Martínez-Garza and Howe 2003) and the dominance of early successional genera
(Nepstad et al. 1990, 1996; Schnitzer et al. 2000, Mesquita et al. 2001, Schnitzer and
Bongers 2001, Hooper et al. 2004). In the Brazilian Amazon, regeneration on abandoned
land depends first and foremost on prior land-use history (Mesquita et al. 2001).
Abandoned clearcuts become dominated by Cecropia trees, but contain a rich mix of
other arboreal genera. In contrast, abandoned pastures become dominated, almost
completely, by Vismia trees. In fact, the number of tree species found under Cecropia
canopies is twice the number found under Vismia (Mesquita et al. 2001). Furthermore,
Cecropia second growth succeeds rapidly to a diverse mixed forest within 20 years,
1
whereas Vismia second growth remains in pure stands with few new genera over the
same time interval.
Several processes that may explain the relatively quick succession that occurs in a
Cecropia forest compared to a Vismia forest (Williamson et al. 1998). First, the pioneer
genus Vismia, which has the ability to re-sprout from below ground by differentiating
shoots from root tissue, is a prolific source of re-sprouting in the study system. In fact,
the Vismia individuals dominating second growth plots, following heavy land-use, are
assumed to be re-sprouts (Bentos, T., pers. comm.). Conversely, Cecropia spp. do not
commonly re-sprout after pasture fires, but persist in second growth due to the presence
of large quantities of long-lived propagules in the seed bank (Uhl and Clark 1983,
Kauffman 1991).
Secondly, there is a positive correlation between distance to primary forest and
the species richness of the seed rain (Mesquita et al. 2001). This implies that for
succession of either forest type, seed dispersal into young second growth also limits plant
recruitment. Vertebrate frugivores are the principle seed vectors in tropical rain forests
(Terborgh 1990). Cecropia stands produce fruits dispersed by bats, birds and terrestrial
mammals, so they attract a broader set of dispersers that could bring a broader array of
seeds into the second growth. In contrast, Vismia produces fruits consumed mostly by
bats which potentially bring a limited subset of forest species into Vismia second growth
(Medellin and Gaona 1999).
Finally, Vismia is not a successional facilitator (sensu Connell and Slayter 1977)
and may inhibit the regeneration of mature forest whereas Cecropia promotes
2
diversification, apparently facilitating the establishment of mature forest species. Several
mechanisms have been proposed, pending field confirmations. However, Vismia species
have been found to delay the regeneration of primary forest species under their crowns,
perhaps due to a change in soil condition caused by the leaf litter (Saldarriaga 1985;
Saldarriaga and Uhl 1991). Soil conditions that assist in the growth of primary forest
species are created in Cecropia litter, and the well-shaded habitat under a Cecropia
canopy may create conditions in which shade-tolerant primary forest seeds can germinate
(Maury-Lechon 1991).
Delayed or arrested succession is a common result of heavy or repetitive
anthropogenic disturbances (Griscom and Ashton 2003; Acácio et al. 2007). In such
circumstances, both the accumulation of species and the accumulation of biomass is
hindered by seed limitation, frequent fire and disturbed or compacted soils from grazing
or bulldozers (Hjerpe et al. 2001, Chinea 2002, Fine 2002, Zarin et al. 2005). Vismia
second growth may be an example of arrested succession driven by limited seed dispersal
and dominance by a persistent pioneer.
Here, I am interested in exploring how two mechanisms, advance regeneration
and seed dispersal, impact young secondary forest succession in central Amazonia. The
low diversity and slower succession in Vismia stands may be a result of the rapid
vegetative re-growth found in the Vismia genus. Williamson and Mesquita (unpublished
data) have documented the ability of Vismia to differentiate shoots from root tissue, and
here I will explore the relative prevalence of re-sprouting by Vismia versus other genera
3
in the initial stages of succession for the two second growth types. The first two
hypotheses to explain the difference in succession are:
I.
Individuals in the genus Vismia exhibit re-sprouting following disturbance
more often than individuals in other genera.
II.
Re-sprouting from Vismia roots in different plots reflects their land-use
histories – i.e., the proportion of Vismia stems originating as re-sprouts is
higher in areas subjected to repeated burns.
There is a positive correlation between distance to primary forest and the species
richness of the seed rain (Mesquita et al. 2001). This implies that for succession of either
forest type, seed dispersal into young second growth also limits plant recruitment. While
the tree species in this region have seeds dispersed by birds, bats, as well as other
mammals, in this study I will focus on the role of bird and bat seed dispersal in the
process of forest regeneration.
Behavioral, biological and physical processes affect the significance of these
animals in dispersing seeds into Cecropia and Vismia stands. For example, bats can travel
long distances when changing feeding areas and when moving to and from day roosts
(Bernard and Fenton 2002). Therefore, they may transport seeds long distances and are
less likely than birds to defecate all seeds in foraging areas (Fleming and Williams 1990).
Physical processes linked to forest structure and canopy height can affect where faunal
species forage. Vismia stands generate a microclimate that is hotter, drier and more
illuminated than Cecropia stands (Didham 1999), a difference which may alter some of
the faunal species behavior and therefore seed dispersal processes. However, Bobrowiec
4
(2003) found little difference in the seeds dispersed by bats in Cecropia and Vismiadominated second growth.
Avian community composition is affected by forest type, height and presence of a
complex canopy. While the species richness of birds and number of frugivorous and
omnivorous bird species in Cecropia stands is not significantly different from that of
Vismia stands, there is a significantly higher abundance of birds in Cecropia stands
(Borges and Stouffer 1999). With a higher abundance of birds in Cecropia stands, I can
expect a greater abundance of seeds and possibly a more diverse seed rain in young
Cecropia stands compared to young Vismia stands. Therefore, the next hypotheses of this
study are:
III.
Cecropia second growth seed rain contains a greater diversity of seeds than
Vismia second growth seed rain.
IV.
Seed rain from bird dispersers is more diverse than the seed rain from bat
dispersers regardless of stand type.
Although the ecological importance and conservation benefits of understanding
forest regeneration have been recognized at local, regional and global levels (Richards
1979; Gomez-Pompa and Vasquez-Yanes 1981; West et al. 1981; Finegan 1984, 1992,
1996; Dourojeanni 1987; Brown and Lugo 1990, Chazdon 2008), the mechanisms of
regeneration in response to anthropogenic disturbances are still poorly understood. This
thesis seeks to better understand some of the mechanisms behind forest succession in
central Amazonia, specifically, the degree of re-sprouting by plants and the input from
seed dispersal by bats and birds in young second growth.
5
Chapter 2: Methods
Study Sites
The study area is located 80 km north of Manaus in the state of Amazonas, Brazil
(2º 29‟ S, 59º 41‟ W, 54 m – 132 m elevation). The region is dominated by dense
evergreen terra firme forest with a mean annual temperature of 26º C (Bruna 2002). The
climate is type Am in the Köppen (1936) system: tropical humid with excessive rain in
some months and an occasional month of less than 100 mm precipitation. The average
annual rainfall is between 2,200 and 2,700 mm (Gascon and Bierregaard 2001; Radtke et
al. 2007) with a dry season from June to October. The predominant soils are nutrient
poor, clay-rich oxisols with yellow latosols and red-yellow podzols (Ranzani 1980).
Study sites were established in young secondary forest on land owned by farmers
along Zona Franca 7 (ZF7), a two-lane dirt road north-east of the small town of Rio Preto
da Eva. Private lots on ZF7 measure 250 m by 1,000 m with the shorter length fronting
on the road (Fig. 1). Land-owners in this area are not subsistence or swidden-farmers,
who clear portions of their land to plant cassava and fruit trees, and harvest wood for
charcoal production.
To determine the effect of land-use history on seed rain, eight second growth
stands between 3 and 15 years after abandonment with different land-use histories were
selected (Table 1). These stands were roughly 2 km distant from adjacent stands to ensure
independence of sampling. In each stand, one 100 m by 10 m transect was established
and all trees, palms, vines and shrubs ≥ 3 cm diameter at breast height (dbh) were
recorded to species. Stands were classified as Vismia-dominated or Cecropia6
2
2mikm
M2
V1
M1
C1
V2
V3 M3
V4 M4
C2
V5
M5
C3
Figure 1. Map of South America showing approximate location of field sites with inset of
a satellite image of Vismia (V1-V5), Cecropia (C1-C3) and mature forest (M1-M5)
stands.
7
dominated based on a subjective assessment of current vegetation. Five stands were
Vismia-dominated and three were Cecropia-dominated. Second-growth ages ranged
from 3-15 years since abandonment with only one site over 10 years of age at the
beginning of the study. Stands conformed to the findings of Mesquita et al. (2001) that
Cecropia dominated areas are burned 0-1 times while Vismia dominated areas are burned
twice or more.
Table 1. Stand descriptions and land-use history as recorded by land-owners
2nd Growth
Years since
Stand Size
C1
Type
Cecropia
Abandonment
8
(m2)
10,000
C2
Cecropia
4
7,500
Cleared & abandoned
C3
Cecropia
15
250,000
Cleared & abandoned
V1
Vismia
4
15,000
Orange grove
V2
Vismia
3
3,750
Cassava
V3
Vismia
8
1,875
Cassava, fruit trees
V4
Vismia
8
2,500
Cassava, guarana trees
V5
Vismia
3
4,000
Charcoal
Site Name
Land-use History
Agriculture < 5 yrs
Sørensen‟s index of similarity was calculated for the vegetation in each pair of
stands to determine similarity in community composition between stands (Bray and
Curtis 1957; Southwood and Henderson 2000). This index was selected because of its
sensitivity to heterogeneous datasets and because it places little importance on outliers.
Sørensen‟s index was calculated separately based on basal area and relative abundance
(proportion) of stems in each site. Non-metric multidimensional scaling (NMDS) was
8
used to ordinate the indices for the eight transects in order to visualize plant community
differences among stands. Wilcoxon rank sum tests were conducted to test for differences
in stand vegetation similarities between like stands (Cecropia-Cecropia and VismiaVismia) and different stands (Cecropia-Vismia). All statistical tests were performed in
SAS (SAS, Version 9.1.3, 2004).
Re-sprouting
Along the established 100 m by 10 m transect in each second growth stand, I
examined each stem of trees, palms, shrubs and lianas over 3 cm dbh to determine if it
originated from seed or as a re-sprout. Stems were considered re-sprouts when they were
visibly growing out of a remnant stump or shared remnants of other stems that had died.
The latter condition indicated that there had been multiple re-sprouts, but that by canopy
closure usually only one stem had survived. ANOVA tests were used to test for
significant differences in the numbers and proportions of Vismia, Cecropia, and all other
stems that originated as seedlings or as re-sprouts in Cecropia and Vismia stands.
Seed Traps
Daily Seed Traps
To determine the composition of seed rain in Cecropia and Vismia stands, eleven
1 m2 seed traps were assembled at 10 m intervals along the established 100 m transect,
with 10 m between traps and at least 10 m from the edge of the stand. Seed traps (Fig 2)
were constructed of 1 m tall PVC pipe frames which supported 1 mm nylon mesh
9
suspended concavely to prevent seeds from bouncing or being washed out of the trap
(Cramer et al. 2003; Clark et al. 2001; Smythe 1970; Zhang 1995). There were 11 traps
on each transect for a total of 55 in Vismia stands and 33 in Cecropia stands. Each trap
was considered one replicate of the site. Sites were sampled from June through August
2010.
All seeds collected from traps at dawn (6:00 am) were assumed to have been
dispersed by bats and those at dusk (6:00 pm) to have been dispersed by birds. To ensure
that the seeds counted were those that had been handled by frugivores and not simply
fruit fallen directly from the tree, only seeds with attached fecal matter were counted.
For all seeds collected in seed traps, the following diversity metrics were
calculated: Simpson‟s diversity index, Shannon-Wiener diversity index, species richness
and species evenness from the Shannon-Wiener diversity index. Estimate S was used to
determine individual based species accumulation curves with 95% confidence intervals
for seeds collected in Vismia stands and Cecropia stands separately (Colwell 2009). For
bird-dispersed seeds, bat-dispersed seeds, as well as all seeds combined, I performed
ANOVAs on all diversity metrics to determine differences by stand type Vismia or
Cecropia. Two-factor ANOVAs were used on seed species abundances from the traps to
determine differences caused by second growth type and disperser type. Abundances
were log10 transformed before performing the ANOVA.
10
Monthly Seed Traps
In addition to the eight second growth stands, five mature forest sites were
located, four within 100 m of Vismia stands and one within 100 m of Cecropia stands.
Eleven seed traps were established along transects within each of the five mature forest
sites, with 22 traps located within one plot for a total of 66 traps in mature forest; 55 near
Vismia stands and 11 near Cecropia stands.
Figure 2. Seeds were collected twice a day in seed-traps assembled in Cecropia-dominated
second growth (shown) as well as in Vismia-dominated second growth
11
Mature forest and second growth seed rain traps were emptied at approximately
monthly intervals between January and May 2010 on a rotating basis. Half the sites were
sampled in January (14 days), February (28 days) and April (30 days), while the
remaining sites were sampled in March (31 days) and May (31 days). All seeds, fruits
and feces containing seeds were dried, counted and identified to lowest practical taxon,
usually to genus (Cornejo and Janovec 2010). Some of the uncommon seeds could not be
identified and were grouped by morpho-taxa based on size, shape and color.
I performed an ANOVA on the number of seeds stand -1 month-1 deposited in each
of the three stand types (Cecropia, Vismia and mature forest) to determine differences
caused by stand type. A second ANOVA on the size classes of seeds stand -1 month-1
collected in the three stand types to determine the differences caused by stand type. For
both ANOVAs, numbers of seeds were log10 transformed and individual treatment means
were compared via LSMEANS with Tukey's adjustment for multiple comparisons. Size
classes were assigned as follows: “Tiny”: <0.5 cm at greatest length, “Small”: 0.5-0.99
cm, “Medium”: 1.0-1.99 cm, and “Large” : >2.0 cm.
Mist Nets
Bird Captures
Bird presence was determined by mist net captures. Six 12-m mist nets were used
to capture birds in the eight second growth stands where seed traps were placed. Nets
were open in one site for two consecutive mornings, returning to each site after all other
sites had been sampled for an average of 20.05 (±5.95 SD) mist net hours. Intervals
12
between mist netting at each site varied over the course of the sampling period, but
generally consisted of one two-day sampling period per month from June through
August, 2010.
Feces were recovered from captured birds using two methods. First, the ground
below the bird‟s point of capture in the net was searched for feces. Birds that had not
defecated while in the mist net were retained in a cloth bag for 30 minutes until they
defecated. Some of the individuals that were known to be strict insectivores were
identified and subsequently released without collecting a fecal sample in order to
maintain an efficient processing time when capture rate was high. Bird species found in
each transect, as well as the seeds they deposited, were identified to lowest taxon
possible.
Bird species were grouped by guild (frugivore, insectivore, omnivore or
nectarivore/insectivore) following the designations suggested by Karr et al. (1990),
Stouffer and Bierregard (1995) and Powell (1989). Bird guilds were then compared by
stand type, Cecropia and Vismia. The number of seeds collected from captured birds was
analyzed by species with an ANOVA to test for an effect of stand type on seed genera
dispersed by birds.
Bat Captures
Mist netting for bats was limited to 7:00 pm to 11:00 pm on two consecutive
nights for a total of 9 mist netting hours in a Vismia-dominated plot. Feces were
13
collected from bats either by looking below the net or by retaining the bat in a cloth bag
for 30 minutes. Bat species and seed genera were identified to lowest taxon possible.
14
Chapter 3: Results
Study Sites
The five stands classified a priori as Vismia-dominated had in fact, a significantly
higher number of Vismia stems than stems of any other genera and included individuals
of genera such as Cecropia, Bellucia and Miconia. Vismia transects had an average of 36
species whereas the three Cecropia stands had an average of 70 species per plot (Table 2,
Appendix A).
While stem density was similar in Vismia and Cecropia stands, the mean basal
area was almost 60% greater in Cecropia second growth (Table 2). Because stand C3 was
the oldest at 15 years, stem densities for Cecropia stands, C1 and C2, which are close in
age to the average age of Vismia stands, are shown separately (Table 2).
Table 2. Density and basal area, based on all stems ≥ 3 cm dbh, for Vismia and Cecropia
second growth stands.
Vismia stands All Cecropia stands C1 and C2 stands
Mean ± SD
Mean ± SD
Mean ± SD
Number of stands
5
3
2
Age of stands
5.2 ± 2.59
9 ± 5.57
6 ± 2.83
No. of trees ≥ 3 cm (dbh) ha -1
246 ± 20
248 ± 4.2
250 ± 1.4
Basal area (m2) ha-1
19 ± 2.7
30 ± 1.6
28.6 ± 0.32
Species richness
36.4 ± 11.2
70.3 ± 9.5
71 ± 7.1
Mean density of Vismia stems and basal area of Vismia stems were significantly higher in
Vismia stands than Cecropia stands (Fig. 3). There was no significant difference in the
mean density of Cecropia stems in the two stand types; however, Cecropia exhibited
greater basal area in Cecropia stands than in Vismia stands (Fig. 3). For other common
genera, the mean density and mean basal area were not significantly different based on
15
stand dominance, however there was a higher density of “other” species in Cecropia
stands (Fig. 3).
The ANOVA test revealed that the average number of Vismia stems was higher in
Vismia stands (127 ± 32.15, mean ± SD) than in Cecropia stands (13.67 ± 5.86;
F1,6=34.38, P=0.0011, Table 3). The proportion of all stems that were Vismia was higher
in Vismia stands compared to Cecropia stands (0.32 ± 0.067 in Vismia stands and 0.047 ±
0.017 in Cecropia stands, F1,6=43.71, P=0.0006).
Table 3. Mean ± SD and results of ANOVA testing the total number and proportion of all
Vismia, Cecropia and other species found in Vismia and Cecropia stands. Significant
values in bold.
Vismia Stands
Cecropia Stands
Mean
SD
Mean
SD
DF
F
P
Total Number
Vismia stems
127
32.15
13.67
5.86
6
34.38 0.0011
Cecropia stems
21.80
21.00
48.33
12.70
6
3.79
0.099
Other stems
119
47.41
234
8.54
6
16.28 0.0068
Proportion
Vismia stems
0.94
0.24
0.06
0.02
6
38.49 0.0008
Cecropia stems
0.06
0.06
0.17
0.02
6
10.06 0.019
Other stems
0.43
0.13
0.82
0.10
6
19.89 0.0043
The total number of Cecropia stems in Cecropia stands (48.3 ± 12.7, mean ± SD)
was twice that found in Vismia stands (21.8 ± 21) (F1,6=3.79, P=0.099, Table 3), although
these differences were not significant. The proportion of all stems that were Cecropia in
Cecropia stands (0.17 ± 0.019) was significantly higher than in Vismia (0.057 ± 0.057)
(F1,6=10.06, P=0.019). The number and proportion of “other” stems found in Cecropia
stands were double the number and proportion in Vismia stands (total number: 234 ±
8.54, mean ± SD in Cecropia stands and 119 ± 47.41 in Vismia stands, F1,6=16.28,
16
A
Cecropia Stands
Mean density of stems per stand
70
Vismia Stands
60
50
40
30
20
10
0
Vismia
Cecropia
Bellucia
Laetia
Miconia
Other
B
Average basal area per stand
70
Cecropia Stands
60
Vismia Stands
50
40
30
20
10
0
Vismia
Cecropia
Bellucia
Laetia
Miconia
Other
Figure 3. Comparison of generic dominance (≥3 cm d.b.h.) of five most common secondgrowth genera based on mean density (A) and basal area (B) in Cecropia (N=3) and
Vismia (N=5) dominated second growth stands (Mean ± SD).
17
P=0.0068; proportion: 0.67 ± 0.16 in Cecropia stands and 0.25 ± 0.09 in Vismia stands,
F1,6=22.51, P=0.0032).
The Sørensen‟s modified index, based on species‟ relative abundance and basal
areas, generally supported the classification of stands into Vismia-dominated and
Cecropia-dominated (Table 4). The relative abundance similarity indices for CecropiaCecropia were significantly lower than the indices for Vismia-Vismia (Mann-Whitney
U=3.0, P=0.049), although the magnitude of the difference was small (Table 4). In
contrast, Cecropia-Cecropia similarities were much larger than Cecropia-Vismia
similarities (Mann-Whitney U=8.3, P=0.027), and Vismia-Vismia similarities were much
larger than Cecropia-Vismia similarities (Mann-Whitney U= 8.1, P>0.0001).
For basal area comparisons, the similarity indices were not different between
Cecropia-Cecropia and Vismia-Vismia comparisons (Mann-Whitney U=6.8, P=0.81),
whereas Cecropia-Cecropia similarities were significantly larger than Cecropia-Vismia
(Mann-Whitney U=8.0, P=0.0025) and Vismia-Vismia similarities were significantly
larger than Cecropia-Vismia (Mann-Whitney U=8.5, P<0.0001).
In the NMDS ordination, the three Cecropia stands clustered together but the five
Vismia stands were widely dispersed (Fig. 4). This disparity occurred in both relative
abundance and basal area ordinations. One Vismia stand, “V3”, was located in the middle
of the Cecropia stands by both ordinations, but its similarity indicated proximity to other
Vismia stands, not Cecropia stands.
18
Table 4. Pair-wise comparisons of Sørensen‟s modified index of similarity for relative
abundance and basal area in each of eight second growth stands. Dark grey represents
Cecropia-Cecropia comparisons, light grey represents Vismia-Vismia comparisons, and
white represents Cecropia-Vismia comparisons.
Relative Abundance
C1
C2
C3
V1
V2
V3
V4
V5
C1
0.34
0.39
0.36
0.23
0.11
0.24
0.08
C1
C2
C3
V1
V2
V3
V4
V5
C1
0.38
0.5
0.35
0.25
0.11
0.21
0.08
C2
C3
V1
V2
V3
V4
V5
0.4
0.4
0.2
0.11
0.28
0.05
0.35
0.18
0.13
0.28
0.09
0.51
0.46
0.56
0.44
0.38
0.41
0.5
0.4
0.39
0.51
-
C2
C3
V1
V2
V3
V4
V5
0.49
0.36
0.22
0.09
0.23
0.05
0.37
0.2
0.12
0.29
0.08
0.5
0.39
0.51
0.39
0.31
0.39
0.47
0.36
0.33
0.52
-
Basal Area
Basal Area
Relative Abundance
Comparison
Average ± SD
Average ± SD
Vismia-Vismia
0.42 ± 0.078
0.46 ± 0.06
Cecropia-Cecropia 0.46 ± 0.064
0.38 ± 0.03
Cecropia-Vismia
0.20 ± 0.11
0.21 ± 0.11
19
0.4
A
0.3
V2
0.2
C3
Dimension 2
0.1
V1
V4
0
V3
C1
-0.1
C2
V5
-0.2
-0.3
-0.4
-0.4
-0.3
-0.2
-0.1
0
0.1
0.2
0.3
0.4
Dimension 1
0.4
B
0.3
V4
0.2
C1
Dimension 2
0.1
V1
C2
0
-0.1
V3
V5
V2
-0.2
C3
-0.3
-0.4
-0.4
-0.3
-0.2
-0.1
0
0.1
0.2
0.3
0.4
Dimension 1
Figure 4. Non-metric multi-dimensional scaling (NMDS) ordination of the modified
Sørensen‟s index of similarity values for relative abundance (A) and relative basal area
(B) for three Cecropia and five Vismia stands. Cecropia stands are: C1, C2, and C3.
Vismia stands are: V1, V2, V3, V4, and V5.
20
Re-sprouting
Two-way ANOVA tests revealed differences in the proportion of Vismia,
Cecropia and „Other‟ stems that originated as re-sprouts in Cecropia and Vismia stands.
The proportion of Vismia stems that were re-sprouts (100%) was higher in Vismia stands
(0.32 ± 0.067, mean ± SD, Table 5) than Cecropia stands (9.5%; 0.0073 ± 0.0041;
F1,6=59.1, P=0.0003), while the proportions of Cecropia and „Other‟ species that were resprouts were not different by stand type (F1,6=0.77, P=0.41 and F1,6=1.01, P=0.35
respectively).
A similar pattern was observed in the numbers of Vismia, Cecropia and „Other‟
re-sprouts in each stand type. A total of 127 Vismia stems were re-sprouts in Vismia
stands, only 2 individuals were re-sprouts in Cecropia (F1,6=42.5, P=0.0006; Table 5).
The total number of Cecropia re-sprouts and „Other‟ re-sprouts were not significantly
different by stand type (F1, 6=0.79, P=0.41 and F1,6 = 0.43, P=0.54, respectively).
Table 5. Mean ± SD and results of ANOVA testing the total number and proportion of
stems originating as re-sprouts of Vismia, Cecropia and other species found in Vismia
and Cecropia stands. Significant values in bold.
Vismia Stands
Cecropia Stands
Mean
SD
Mean
SD
DF
F
P
Total Number
Vismia re-sprouts
127
32.15
2
1
6
42.50 0.0006
Cecropia re-sprouts
2.20
3.49
0.33
0.58
6
0.79
0.41
Other re-sprouts
22.4
10.83
36.33
47.86
6
0.43
0.54
Proportion
Vismia re-sprouts
1.00
0.00
0.18
0.12
6
286.16 <0.0001
Cecropia re-sprouts
0.11
0.21
0.01
0.01
6
0.67
0.44
Other re-sprouts
0.24
0.14
0.22
0.30
6
0.03
0.88
21
Seed Traps
Daily Seed Traps
Seed traps were open in both Cecropia and Vismia stands for a total of 2,028 h
overnight and 1,848 h during the day. Fecal samples collected in traps contained a total of
6,443 seeds. All seeds were identified to genus. Samples without seeds (38.1% of all
fecal samples collected) contained insect parts, fruit pulp or unidentified organic material.
Seed traps in Cecropia stands yielded 177 fecal samples from 33 seed traps over
1,308 h of sampling (Table 6). From these fecal samples, 922 seeds were collected while
the traps were open during the day (bird-dispersed), and 857 seeds were collected
overnight (bat-dispersed, Table 8). Of the seeds dispersed by birds in Cecropia stands,
97.8% were in the genus Miconia. Bat-dispersed seeds were predominantly in the genera
Vismia (67.7%) and Miconia (24.9%).
Seed traps in Vismia stands yielded 313 fecal samples from 55 seed traps over the
2,568 h of sampling (Table 6). From these fecal samples, 1,178 seeds were birddispersed, and 3,529 seeds were bat-dispersed (Table 8). The majority of seeds dispersed
by birds were in the genus Miconia (82.0%) and the majority of bat-dispersed seeds were
Vismia (73.0%) and Miconia (13.3%). When rare seed genera (present in less than 5 fecal
samples) were removed from the analysis, there were no changes in significance in the
ANOVA results (Table 7).
Seed species richness was higher in Vismia stands (4.00 ± 1.00, mean ± SD) than
in Cecropia stands (2.33 ± 0.58; F1,6=6.70, P=0.04). ANOVAs comparing the seeds
collected by birds versus bats and stand type revealed no significant differences in
species richness of seeds or species evenness (Table 6).
22
Table 6. Total trap hours, number of feces and seeds collected in second growth traps,
diversity indexes, species richness and evenness values for seeds dispersed into each site
by second growth type. Factorial ANOVA values shown. Significant values in bold.
Vismia stands
Cecropia stands
Total trap hours
2,568
1,308
Total fecal samples
312
177
-1
Total fecal samples week
20.41
22.25
Fecal samples with seeds
210
97
Total seeds
4,707
1,779
Total seeds trap-1 week-1
61.50
76.17
Mean ± SD
Mean ± SD
df
F
P
Trap hours
513 ± 187.71
436 ± 159.35
6
0.35 0.57
Fecal samples
62.40 ± 29.04
59.00 ± 35.68
6
0.02 0.89
Fecal samples week-1
20.36 ± 8.45
22.03 ± 8.02
6
0.08 0.79
Fecal samples with seeds
42.00 ± 25.62
32.33 ± 28.43
6
0.25 0.64
Seeds
940 ± 769.80
593 ± 521.60
6
0.46 0.52
-1
-1
Seeds trap week
59.88 ± 55.68
68.62 ± 48.45
6
0.05 0.83
Simpson‟s Index
Bird-dispersed
0.47 ± 0.27
Bat-dispersed
0.76 ± 0.42
All seeds
0.86 ± 0.18
Shannon-Wiener
Bird-dispersed
0.98 ± 0.60
Bat-dispersed
2.61 ± 1.47
All seeds
2.84 ± 1.06
Species Richness
Bird-dispersed
3.20 ± 1.48
Bat-dispersed
3.00 ± 1.58
All seeds
4.00 ± 1.00
Species Evenness
Bird-dispersed
0.43 ± 0.10
Bat-dispersed
0.57 ± 0.25
All seeds
0.55 ± 0.02
Note: Rare genera such as Clidemia, Lantana and
the end of the sampling period.
23
0.42 ± 0.39
0.73 ± 0.21
0.81 ± 0.18
6
6
6
0.03
0.01
0.14
0.87
0.92
0.73
0.83 ± 0.91
2.20 ± 1.31
2.48 ± 1.17
6
6
6
0.08
0.16
0.20
0.78
0.71
0.67
1.67 ± 1.53
2.00 ± 0.00
2.33 ± 0.58
6
6
6
1.93
1.12
6.70
0.21
0.33
0.04
0.50 ± 0.41
6
0.11 0.75
0.68 ± 0.45
6
0.12 0.76
0.76 ± 0.22
6
3.88 0.10
Phytolacca were only detected towards
Table 7. Diversity indexes, species richness and evenness values for seeds dispersed into
each site by second growth type excluding rare genera such as Clidemia, Lantana and
Phytolacca. Significant values in bold.
Vismia stands
Cecropia stands
Mean ± SD
Mean ± SD
df
F
P
Simpson‟s Index
Bird-dispersed
0.45 ± 0.26
0.43 ± 0.40
6
0.01 0.92
Bat-dispersed
0.76 ± 0.42
0.73 ± 0.21
6
0.01 0.92
All seeds
0.86 ± 0.18
0.81 ± 0.18
6
0.13 0.73
Shannon-Wiener
Bird-dispersed
0.93 ± 0.60
0.83 ± 0.90
6
0.04 0.85
Bat-dispersed
2.61 ± 1.47
2.20 ± 1.31
6
0.15 0.71
All seeds
2.82 ± 1.05
2.48 ± 1.17
6
0.19 0.68
Species Richness
Bird-dispersed
2.80 ± 1.30
1.33 ± 1.16
6
2.56 0.16
Bat-dispersed
2.80 ± 1.48
2.00 ± 0
6
0.82 0.40
All seeds
3.40 ± 0.55
2.00 ± 0
6
18.37 0.005
Species Evenness
Bird-dispersed
0.50 ± 0.17
0.53 ± 0.38
6
0.02 0.90
Bat-dispersed
0.69 ± 0.37
0.68 ± 0.45
6
0.52 0.52
All seeds
0.54 ± 0.02
0.75 ± 0.22
6
3.88 0.11
Table 8. Number (N) and percent of total seeds collected in seed traps within each stand
type during the two time periods (day and night).
Vismia Stands
Cecropia Stands
Day
Night
Day
Night
Seed Genera
N
%
N
%
N
%
N
%
Cecropia
1
0.08
105
2.98
57
6.65
Vismia
43
3.65 2,577 73.02
15
1.63
580 67.68
Miconia
966 82.00 470 13.32
902 97.83 214 24.97
Piper
76
6.45
230
6.52
6
0.70
Solanum
46
3.90
133
3.77
4
0.43
Phytolacca
14
0.40
Lantana
1
0.11
Clidemia
46
3.90
Total seeds
1,178 100% 3,529 100%
922 100% 857 100%
24
9
Number of species
8
7
6
5
4
3
2
1
0
0
1000
2000
3000
4000
5000
Number of individuals
Figure 5. Species accumulation curves with 95% confidence intervals for seeds collected
in Cecropia stands (black lines) and Vismia stands (gray lines).
Species accumulation curves did not show a significant difference in seed species
richness between Cecropia and Vismia stands as there was considerable overlap of their
95% confidence intervals (Fig 5).
A two-way ANOVA was used to test for differences in the seed genera dispersed
by birds and bats in the two stand types (Table 9). For the total number of Cecropia,
Solanum, Clidemia, Lantana, and Phytolacca seeds dispersed, there were no significant
disperser, stand or disperser-by-stand effects (Table 9). Vismia seeds had a significant
disperser effect (F1,12=8.53, P=0.013)--namely, bats and birds deposited a significantly
different number of Vismia seeds in Vismia stands (0.022 and 0.0007 seeds per trap day-1,
respectively) and Cecropia stands (0.01 and 0.0004 seeds per trap day-1, respectively).
Miconia seeds also had a significant disperser effect (F1,12=4.89, P=0.05) where birds
25
dispersed more Miconia seeds than bats in Vismia stands (0.006 and 0.003 seeds per trap
day-1, respectively) and in Cecropia stands (0.01 and 0.002 seeds per trap day-1,
respectively).
Table 9. The effect of disperser and stand type on the number of seeds dispersed into
seed-traps for eight genera. Dispersers are birds and bats. Stand types are Cecropia and
Vismia. Significant values in bold.
Vismia
Cecropia
Miconia
Piper
Independent Variable d.f.
F
P
F
P
F
P
F
P
Disperser
12 8.53 0.01
2.21
0.16
4.89 0.047
1.01 0.33
Stand
12 0.63 0.44
0.87
0.37
0.03 0.86
3.59 0.08
Disperser x Stand
12 0.92 0.36
0.95
0.35
0.48 0.50
1.01 0.33
Independent Variable d.f.
Disperser
12
Stand
12
Disperser x Stand
12
Solanum
F
P
0.40 0.54
0.00 0.97
0.38 0.55
Lantana
F
P
2.16
0.17
0.08
0.79
2.16
0.17
Clidemia
F
P
0.62 0.45
0.62 0.45
0.62 0.45
Phytolacca
F
P
0.42 0.53
0.42 0.53
0.42 0.53
For Piper, the difference in number of seeds dispersed by bats in the two stand
types was not significant (F1,12=3.59, P=0.08), more Piper seeds being dispersed in
Vismia stands (0.008 seeds per trap day-1) than in Cecropia stands (0.003 seeds per trap
day-1). There were only four Piper trees (>3cm dbh) in the study plots, all recorded in
Vismia stands, and some Piper noted in the understory of Vismia plots.
Monthly Seed Traps
The monthly collection of seeds in Vismia stands contained eight genera. Every
month, traps collected an average of 13,000 (± 23,000) seeds from four tiny seeded (<0.5
cm) pioneer genera and an average of 0.43 (± 0.50) small seeds (0.5-0.99 cm) and
26
medium seeds (1.00-1.99 cm) from four unknown genera. Two unknown large seeds (>2
cm) were collected. The four common seed genera found in Vismia stands were Vismia,
Cecropia, Solanum and Piper.
Seeds collected monthly in the Cecropia stands were from eight genera. Each
month, traps collected over 1,900 (±570) seeds of Cecropia, Vismia, Miconia, and
Croton. Of these genera, Cecropia, Vismia and Miconia are common in the canopy of
Cecropia stands. Four seeds from two small-seeded (0.5–0.99 cm) unknown species and
one unknown medium seed (1.0-1.99 cm) were collected. Seed traps in mature forest
yielded seeds ranging in size from tiny (<0.5 cm) Cecropia seeds to large (>2 cm)
Mauritia seeds. An average of fifty-six medium and large seeds was collected monthly
from 29 unknown morpho-taxa.
Tukey‟s multiple comparisons was used to determine if there were more seeds
month-1 stand-1 collected in Cecropia, Vismia or mature forest stands (Table 10). Results
showed significantly more Vismia seeds month-1 stand-1 were collected in Vismia stands
than Cecropia stands (t10=-6.71, Tukey adj. P=0.0001). There were more Cecropia seeds
month-1 stand-1 collected in Cecropia stands (t10=-0.79, Tukey adj. P=0.01) and more
unknown seeds month-1 stand-1 collected in mature forest stands (t 10=-3.72, Tukey adj.
P=0.01).
Tukey‟s multiple comparisons was used to compare size classes of seeds month-1
stand-1 collected in the three stand types (Table 11). Significant differences were detected
for the number of tiny seeds: more tiny seeds month-1 stand-1 collected in Vismia stands
than mature forest (t10=-7.39, Tukey adj. P<0.0001), and more tiny seeds month-1 stand-1
27
collected in Cecropia stands than mature forest (t 10=3.72, Tukey adj. P=0.01).
Conversely, there were more medium seeds month-1 stand-1 collected in mature forest
than Vismia stands (t10=5.30, Tukey adj. P=0.001), and more medium seeds month-1
stand-1 collected in mature forest than in Cecropia stands (t10=-4.59, Tukey adj.
P=0.003). Diversity of seeds, species richness and evenness were highest in mature forest
and lowest in Vismia stands (Table 12).
Table 10. Abundance of seeds month-1 stand-1 (Mean ± SD) collected in Cecropia,
Vismia and mature forest including Tukey‟s adjusted P-value for all pair-wise
comparisons of seeds dispersed into each stand type: Vismia-Cecropia second growth (VC), Vismia-Mature forest (V-M), and Cecropia-Mature forest (C-M). “Unknown” seeds
include all seeds from the 35 morpho-taxa not identifiable to genus. Seed numbers were
log-transformed before performing the ANOVA. Significant values in bold.
Tukey adj. P
Seeds
Vismia stands
Cecropia stands Mature forest
V-C
V-M
C-M
Vismia
707.91 ± 6143.58
0.25 ± 2.67
0
0.0001
Cecropia
1.13 ± 13.11
13.95 ± 140.07
0.15 ± 2.20
0.14
0.22
0.01
Solanum
0.39 ± 4.06
0
0
Piper
0.92 ± 13.22
0
0
Croton
0
0.79 ± 8.91
0
Miconia
0
0.14 ± 1.6
0
Unknown
0
0.03 ± 0.36
0.16 ± 1.25
0.01
Total
29,977.80 ± 29,849.52 638.00 ± 810. 12 26.80 ± 30.10
0.09
0.04 0.003
Table 11. Abundance of seeds month-1 stand-1 (Mean ± SD) in different size classes
collected in Cecropia stands, Vismia stands, and mature forest including Tukey‟s
adjusted P-value for pair-wise differences in seed sizes dispersed into each stand type:
Vismia-Cecropia second growth (V-C), Vismia-Mature forest (V-M), and CecropiaMature forest (C-M). Tiny: <0.5 cm, Small: 0.5-0.99 cm, Medium: 1.0-1.99 cm, Large:
>2.0 cm. Significant values in bold.
Tukey adj. P
Size class
Vismia stands
Cecropia stands
Mature forest V-C
V-M
C-M
Tiny
29,976 ± 29,850
636.33 ± 811.24
6.40 ± 14.31 0.06 <0.0001
0.01
Small
0.20 ± 0.45
1.33 ± 2.31
0
0.23 Medium
0.40 ± 0.55
0.33 ± 0.58
17.80 ± 17.74 1.00 0.001
0.003
Large
0.40 ± 0.89
0
2.60 ± 2.19
0.08
28
Table 12. Total weeks traps were open, seeds collected in monthly traps, diversity
indexes, species richness and evenness values for seeds dispersed into each stand type.
Species evenness was calculated using the Shannon-Wiener diversity index.
Vismia stands
Cecropia stands
Mature forest
Total trapping time (wks)
Total seeds
Total seeds week-1
Simpson‟s Index
Shannon-Wiener
Species Richness
Species Evenness
46
149,889
3258.46
0.03
0.08
9
0.29
26
1,913
73.58
0.36
0.59
7
0.59
36
134
3.72
0.70
1.4
30
0.75
Mist Nets
Bird Captures
Capture data comparisons were based on mist netting effort. A total of 164 birds
from 44 species were captured in three Cecropia stands (62.7 mist net hours) and in five
Vismia stands (97.7 mist net hours; for a list of species captured see Appendix). In
Cecropia stands, 35 birds from 15 species were captured. In these stands, 57.1% of bird
captures were frugivores or omnivores while 42.9% of captures were insectivores. In
Vismia stands, 129 birds from 41 species were captured, and 56.6% of the captures were
frugivores or omnivores, whereas 39.5% of captures were insectivores.
A total of 4,711 seeds from 47 seed-containing fecal samples were collected
during the sampling period. Eight different seed species were detected, with Miconia sp.
being the most abundant. An ANOVA revealed no statistically significant differences
between stand types in the abundance of seeds, tested separately for each seed genus
(Table 13).
29
Table 13. Abundance of seeds (Mean ± SD) collected per bird capture in Cecropia and
Vismia stands and ANOVA test results for differences in seeds dispersed into each stand
type.
Seeds
Vismia stands
Cecropia stands
DF
F
P
Vismia
1.08 ± 6.53
0.46 ± 3.37
7
1.52
0.26
Cecropia
0.05 ± 0.30
0
Miconia
4.67 ± 6.98
3.59 ± 4.90
7
0.23
0.64
Solanum
0.03 ± 0.12
0.004 ± 0.01
7
0.43
0.53
Trema
0.003 ± 0.02
0
Phytolacca
0.01 ± 0.04
0
-
Bat Captures
Mist nets were opened from 7:00 pm to 11:30 pm on two consecutive nights for a
total of nine mist netting hours. From the 34 bats of three species netted (Carollia
perspicillata, Artibeus jamaicensis and Sturnira lilium), 24 provided fecal samples. Only
18 of these fecal samples contained seeds, the majority of which were Vismia seeds
(83%); however seeds from the genera Piper and Solanum were also collected.
30
Chapter 4: Discussion & Conclusions
Natural disturbances in rain forests are variable in intensity, scale and frequency.
Most natural disturbances are small-scale treefalls or branchfalls and create 50-1,000 m2
gaps that close within a few years (Howe 1990). Forest regeneration following such
natural disturbances typically originates from germination of seeds from the soil seed
bank, seedling growth, and re-sprouting of mature forest trees (Brokaw and Scheiner
1989; Quintana-Ascencio et al. 1996; Miller 1999). When all of these sources are intact,
species composition in the second growth is similar to the pre-disturbance community
(Martínez-Garza and Howe 2003).
Regeneration following anthropogenic disturbances such as clearcutting and
conversion to agriculture or pasture follows a different pattern. In these landscapes,
succession is retarded due to the absence of disperser-limited mature forest trees (Finegan
1996; Martínez-Garza and Howe 2003) and the dominance of early successional species
(Nepstad et al. 1990, 1996; Schnitzer et al. 2000, Mesquita et al. 2001, Schnitzer and
Bongers 2001, Hooper et al. 2004). How succession proceeds in these anthropogenically
disturbed areas is largely unknown. Here, I explored two components of succession,
specifically how advance regeneration and seed dispersal impact secondary forest
succession in central Amazonia.
Stand Characteristics
Stand composition reflected the land-use history in a manner similar to that
described in Mesquita et al. (2001). Areas that were used for short-term agriculture or
31
that were abandoned shortly after being cleared had a diverse species composition and
were dominated by individuals in the genus Cecropia. In contrast, areas used for crops or
for charcoal production, and thus repeatedly burned prior to abandonment, were
dominated by Vismia. The two stand types had a similar density of trees ≥ 3 cm (dbh) ha 1
; however the basal area in Vismia stands was much lower, indicating smaller overall
stem size. These differences were still apparent after excluding the older Cecropia site
(C3), which indicates a true difference in stem size that is not based on stand age.
Comparing similarity of stand types revealed an interesting pattern. The Cecropia
stands were more similar to each other than the Vismia stands were to other Vismia
stands. All Vismia stands were very different for both relative abundance as well as basal
area comparisons. The NMDS ordination showed that one Vismia stand, “V3”, appeared
to be more similar to the three Cecropia stands than the other Vismia stands. However,
this may reflect the two-dimensional ordination rather than a true similarity between
“V3” and Cecropia stands. Comparing the Sørensen‟s modified index of similarity values
show that “V3” is, in fact, more similar to Vismia stands than Cecropia stands.
Re-sprouting
I found that individuals in the genus Vismia were much more likely to have resprouted than any other pioneer species. This was particularly apparent in areas where the
land-use history included intense and repeated burnings for the creation of agricultural
plots and charcoal. Other studies in the Neotropics also report a lack of re-sprouts
following fire for species capable of re-sprouting vegetatively (Uhl et al. 1990; Kauffman
32
1991; Sampaio et al. 1993; Miller and Kauffman 1998; Hooper et al. 2004). This is the
first study to explore the re-sprouting ability of the genus Vismia, which is apparently not
killed by successive burns.
This study shows that the ability of Vismia roots to re-sprout contributes to Vismia
monogeneric dominance. In Cecropia stands, only 9.5% of Vismia stems were re-sprouts,
whereas Vismia stands were comprised mainly of Vismia stems, all of which re-sprouted
from pre-existing root systems as opposed to germinating directly from seed. Abandoned
land that has been burned repeatedly for pastures becomes dominated almost completely
by Vismia trees, while abandoned clearcuts become dominated by Cecropia.
Cecropia and all other non-Vismia species do not show a higher propensity to resprout in one stand type over the other. Thus, the prevalence of Vismia re-sprouts in
Vismia stands suggests that other sources of regeneration, such as germination from seed
and growth of the existing seedling bank have been removed in areas with repeated fire.
The loss of the seed and seedling bank has negative repercussions for the diversity of
recruiting vegetation, leading to retarded or arrested succession. This result has important
implications for forest regeneration and management in central Amazonia where
repeatedly burning tracts of land is common.
Seed Dispersal
My second set of hypotheses considered the importance of seed dispersal as a
means of regeneration in secondary forests. I predicted that Cecropia stands would
receive more diverse seed rain; however, I found almost no differences between stands in
33
various diversity measures. While individual based species accumulation curves with
95% CIs did not indicate a significant difference in seed species richness between Vismia
and Cecropia stands, absolute species richness was statistically higher in Vismia stands
than in Cecropia stands. However, seed rain in both stand types was relatively species
poor. The diversity and abundance of seeds dispersed in Vismia stands was higher than
that in Cecropia stands. This may be a reflection of the higher capture rate of birds in
Vismia stands. Miconia seeds were over-represented in the seed rain, relative to the
presence of Miconia trees in the canopy. There were few Cecropia seeds collected in
either stand type which may reflect the lack of fruiting observed in the second growth
during sampling. C. sciadophylla and C. purpurascens typically have ripe infructescences
from late August through November, after the sampling period was completed (Bentos
2006). Some Vismia species fruit during the sampling period (Bentos 2006), which may
be why Vismia fruits were observed in high abundances in Vismia stands.
I predicted that the seed input from bird dispersers would be more diverse than
that from bats due to their consumption of a more diverse array of fruit species. However,
I found only slight differences in dispersal by birds and bats. In both stand types, birds
consumed mostly Miconia seeds and bats consumed mostly Vismia seeds; however, both
seed genera were found in fecal samples from both disperser types. Moreover, while
birds and bats specialize on different genera of seeds (Fleming and Willams 1990,
Gorchov et al. 1993), the array of seed species that they transport in second growth is
virtually the same. Birds often forage in high numbers in fruiting trees, particularly in the
Cecropia spp. canopy, where seed rain abundance and diversity can be high (Rosenberg
34
1990, Saracco et al. 2004). However, in this experiment, traps were placed randomly in
second growth stands and may have missed the seed input from this source.
The majority of seeds collected in seed traps were pioneer species commonly
found as adults in the second growth in which they were collected. The absence of mature
forest species in the seed rain may reflect the abundance of fruit produced by pioneer
species in Vismia and Cecropia second growth and that dispersers in second growth are
eating seeds in second growth rather than moving between mature forest and second
growth stands. For birds, this was expected as they often drop seeds in the same location
where they forage (Fleming and Williams 1990). Bats may travel long distances between
a foraging area and a night roost (Heithaus and Fleming 1978, Morrison 1980), making
them more likely to disperse seeds into other second growth stands. However, the results
suggest that in this time period, bats were not transporting mature forest seeds into
second growth.
Finally, there was no interaction effect between stand type and seed disperser in
terms of seed dispersal. Considering my original hypotheses, I expected that birds would
contribute a greater diversity of seeds in Cecropia stands, due to the higher plant species
and structural diversity as well as the behavior and biology of birds. I did not find this
pattern. Instead, birds and bats contributed a similar diversity of seeds in both stand
types. As such, the original hypotheses about seed dispersal were not supported in this
study.
Monthly seed rain yield was very different in Vismia, Cecropia and mature forest
stands with more tiny seeds in second growth and more medium-sized seeds in mature
35
forest. Seed traps in Vismia stands collected the highest number of seeds, the majority of
which were Vismia and reflect the monogeneric dominance of Vismia in these stands as
well as the prolific fruiting by this pioneer genus. Cecropia stands had fewer seeds than
Vismia stands; however, there was also an abundance of pioneer seeds. There were
significantly more Cecropia seeds in Cecropia stands reflecting the Cecropia dominance
of those sites. As previously stated, few Cecropia seeds were collected in daily seed rain
from birds and bats from June through August, perhaps due to the lack of fruiting by
Cecropia spp. during that time period (Bentos 2006). However, Cecropia sciadophylla
has ripe fruits during the monthly seed collections (January through May) when they
were detected in Cecropia stands (Bentos 2006).
In both second growth stand types there were few mature forest seeds despite
their proximity to mature forest stands. Seed rain into traps in mature forest stands was
much richer than that in second growth stands, despite the lower number of seeds
collected. This can be explained by the higher diversity of adult trees in mature forest.
The seeds collected by monthly seed collections probably reflect the stand composition in
terms of species richness and fruiting phenology.
Mist nets
Vismia stands had higher abundance and diversity of birds with over four times
the number of captures and almost three times as many species as Cecropia stands. This
was contrary to my expectations and differed from the study conducted by Borges and
Stouffer (1999) where more individuals and more species were captured in Cecropia
36
stands. It is unclear whether the differences between my results and those of Borges and
Stouffer (1999) are due the biases of mist netting (Remsen and Good 1996), the limited
time spent mist netting at these sites or are an accurate reflection of the differences in bird
activity. The use of mist net data for relative abundance comparisons of mobile animals is
biased due to the effects of net spacing as well as variety in flight distance and flight
frequency of the target animals (Remsen and Good 1996). While both this study and
Borges and Stouffer (1999) used mist nets to calculate bird relative abundance, the net
spacing and time spent netting were different. Future studies of bird density and diversity
should include point counts in order to avoid these biases (Reynolds et al. 1980).
Arrested Succession
In some anthropogenically altered landscapes, the dominance of grasses, lianas
and shrubs have been shown to significantly repress tree regeneration for decades after
disturbance (Pinard, Howlett and Davidson 1996, Chapman and Chapman 1997,
Sarmiento 1997, Chapman et al. 1999). Three major drivers of arrested succession are
outlined below.
The first is the absence of disperser-limited mature forest trees (Uhl et al. 1988,
Aide and Cavelier 1994, Finegan 1996, Holl 1999, Wijdeven and Kuzee 2000,
Zimmerman et al. 2000 Martínez-Garza and Howe 2003). Dispersal limitation into
cleared land such as abandoned pastures is a common factor that inhibits forest
regeneration following agriculture. In Costa Rica, three forces work together to retard
forest recovery: a depleted seed bank, limited seed rain, and abundant seed predation
37
(Wijdeven and Kuzee 2001). In the central Amazon, dispersal limitation is evident in
young second growth, particularly second growth dominated by Vismia (Mesquita et al.
2001, Monaco et al. 2003).
The second mechanism found to inhibit succession is liana dominance (Schnitzer
et al. 2000, Schnitzer and Bongers 2001). Lianas are commonly found during gap-phase
regeneration, as they take advantage of high light levels and relatively low canopy
heights(Schnitzer et al. 2000, Schnitzer and Bongers 2001). In at least one case however,
liana dominance has been associated with pioneer tree survival while inhibiting nonpioneer trees, thus stalling succession (Schnitzer, Dalling and Walter 2000).
Finally, the dominance by grasses, sometimes in association with fire has been
shown to delay succession (Nepstad et al. 1990, 1996; Hooper et al. 2004). Grasses
dominate abandoned lands where fire is commonly used for agricultural purposes
(Nepstad et al. 1990, 1996; Hooper et al. 2004). In Panama, the invasive Saccharum
spontaneum dominates landscapes and reduces species richness due to fire-induced
changes in site conditions (Hooper et al. 2004). Fire kills re-sprouts and germinating
seedlings of many tree species, while light-dependent wind-dispersed grasses are capable
of re-establishing quickly (Hooper et al. 2004).
Drivers of succession are complex and multiple factors may be responsible for the
arrested state of Vismia second growth. In the central Amazon, the slow turnover rate in
Vismia second growth stands makes this an exemplary case of arrested succession
(Williamson and Mesquita 1998, Mesquita et al. 2001, Feldpausch et al. 2007, Norden et
al. 2010). Mesquita et al. (2001) showed that as distance to primary forest increases,
38
species richness declines, indicating that seed dispersal limits plant recruitment in young
second growth. My results support this hypothesis, in that very few mature forest species
are dispersed in second growth seed rain.
My results also show that a high level of self-replacement occurs in Vismia stands
where 100% of Vismia stems re-sprout from root tissue. This self-replacement occurs in
response to fire and retards the re-establishment of tree species diversity by perpetuating
Vismia in the canopy. The long-term dominance of Vismia in the canopy may be
attributed to seed limitation, the repeated burning of the site, the failure of Vismia to
create environmental changes or competitive inhibition by Vismia, particularly in the
extensive growth of roots.
Management Implications
While this study examined the effects of small-scale anthropogenic disturbances,
my findings can be applied to conservation management on a variety of scales. High
intensity land-use has been linked to Vismia-dominated successional forests throughout
the Neotropics, in Brazil (Uhl et al. 1988, Nepstad et al. 1990, Parrotta et al. 1997,
Williamson and Mesquita 2001), French Guiana (Maury-Lechon 1991), and Colombia
(Uhl 1987). As previously mentioned, secondary succession on these abandoned lands
depends on land-use history, dispersal from the nearest seed sources (Mesquita et al.
2001) and the ability of forest species to re-sprout.
Repeatedly burning a site retards succession by reducing the presence of seed and
seedling banks and by killing mature forest speciesre-sprouts. However, because re39
sprouting by the pioneer genus Vismia is prolific, a mono-generic second growth stand
succeeds slowly towards mature forest composition. In contrast, the presence of a diverse
seed bank, seedling bank and ability of mature forest species to re-sprout adds to the
diversity of flora found in Cecropia second growth stands, permitting a more rapid return
to mature forest.
I suggest that repeated burns should be limited as much as possible due to the
long term effects on succession after abandonment. Enrichment planting in successional
plots may be useful in restoring species composition of secondary forests (Tucker and
Murphy 1997), although initial attempts in Vismia stands have generally failed (Jakovac
pers. com.). Animal-dispersed pioneer and mature forest species should be used in order
to facilitate the return of disperser-limited deep-forest species (Martínez-Garza and Howe
2003). There is increasing evidence that seedlings of large seeded, shade-tolerant mature
forest species are, in fact, capable of surviving in pastures (Montagnini et al. 1995; Loik
and Holl 1999; Hooper, Condit and Legendre 2002),and therefore they should be used in
enrichment planting to mitigate species loss in secondary forests (Tucker and Murphy
1997). Alternatively, constructing bat houses within abandoned pastures and young
second growth may increase bat activity and seed dispersal by bats, as suggested by
Tuttle and Hensley (2000).
Another strategy for management of successional forests is the presence of
isolated trees which provide perches attracting potentially seed-dispersing birds and bats;
this has been shown to increase seed rain in pasture matrices (Guevara et al. 1991; Miriti
1998). In Vismia stands where succession is delayed, the proximity of seed sources is
40
critical to the restoration of diverse seed rain (Monaco et al. 2003). Previous studies have
shown that as distance from edge increases, seed dispersal decreases (Thomas et al. 1988;
Willson and Crome 1989; Gorchov et al.1993; Aide and Cavelier 1994; Duncan and
Duncan 2000; Mesquita et al. 2001); thus, I recommend planting buffers, corridors or
stepping-stone stands in the vicinity of patches of second growth (Janzen 1988; Lamb et
al. 1997; Tewksbury et al. 2002) so that dispersal of mature forest seeds is possible.
Additionally, seed traps placed directly under fruiting Cecropia would capture seed rain
from the diverse frugivore assemblage foraging in the Cecropia canopy which is a source
that was unaccounted for in this study.
Corridors that provide landscape and habitat connectivity between second growth
and mature forests is critical for maintenance of diversity (Saunders and Hobbs 1991;
Lindenmayer and Nix 1993). In this system, I encourage the use of Cecropia as the
dominant genus of these corridors because the complexity ofCecropia second growth has
been found to be more attractive for mature forest birds (Borges and Stouffer 1999); it
provides sufficient shade to eliminate grasses and weeds and has fruits that are attractive
to a wide range of potentially seed-dispersing animals (Lamb et al. 1997).
Conservation of primary forest reserves in Amazonia requires the maintenance of
functional, sustainable secondary forests to meet the needs of anthropogenic
development. Otherwise, primary forest reserves will succumb to anthropogenic needs.
Managing (manipulating ecologically) secondary forests is becoming an increasingly
important aspect of conservation in the Amazon.
41
Literature Cited
Acácio, V., M. Holmgren, P.A. Jansen, and O. Shrotte. 2007. Multiple recruitment
limitation causes arrested succession in Mediterranean cork oak systems.
Ecosystems 10:1220–1230.
Aide, T. M., and J. Cavelier.1994. Barriers to lowland tropical forest restoration in the
Sierra Nevada de Santa Marta, Colombia. Restoration Ecology 2:219-229.
Bentos, T. V. 2006. Estratégias reprodutivas de espécies pioneiras na Amazônia central:
Fenologia e sucesso no establecimento de plantas. Manaus: INPA.
Bernard, E. and M. B. Fenton. 2003. Bat mobility and roosts in a fragmented landscape
in central Amazonia, Brazil. Biotropica 35:262–277.
Bobriowiec, P. E. D. 2003. Chuva de sementes por morcegos e aves sob árvores isoladas
em pastos abandonados da Amazônia central. Manaus: INPA.
Borges, S.H. 1995. Comunidade de aves em dois tipos de vegetação secundária da
Amazônia central. Manaus: INPA/FUA.
Borges, S.H. and P.C. Stouffer. 1999. Bird communities in two types of anthropogenic
successional vegetation in central Amazonia. The Condor 101:529-536.
Bray, J. R. and T. Curtis. 1957. An ordination of the upland forest communities of
southern Wisconsin. Ecological Monographs 27:326-349.
Brown, S. and A. E. Lugo. 1990. Tropical secondary forests. Journal of Tropical
Ecology 6: l-32.
Bruna, E. M. 2002. Effects of forest fragmentation on Heliconia acuminata seedling
recruitment in central Amazonia. Oecologia 132:235-243.
Chapin, F. S., III, T. Hollingsworth, D. F. Murray, L. A. Viereck, and M. D. Walker.
2006. Floristic diversity and vegetation distribution in the Alaskan boreal forest.
Pages 81–99 in F. S. Chapin, III, M.W. Oswood, K. Van Cleve, L.A. Viereck, and
D.L Verbyla, editors. Alaska‟s changing boreal forest. Oxford University Press,
New York.
Chapman, C.A. and L. J. Chapman. 1997. Forest regeneration in logged and unlogged
areas of Kibale National Park, Uganda. Biotropica 29:396–412.
42
Chapman, C.A., L. J. Chapman, L. Kaufman, and A. E. Zanne. 1999. Potential causes of
arrested succession in Kibale National Park, Uganda: growth and mortality of
seedlings. African Journal of Ecology 37:81–92.
Chazdon, R. L. 2008. Beyond Deforestation: Restoring Forests and Ecosystem Services
on Degraded Lands. Science 320:1458-1460.
Chinea J. D. 2002. Tropical forest succession on abandoned farms in the Humacao
municipality of eastern Puerto Rico. Forest Ecology Management 167:195–207.
Clark, C. J., J. R. Poulsen, and V. T. Parker. 2001. The role of arboreal seed dispersal
groups on the seed rain of a lowland tropical forest. Biotropica 33:606-620.
Connell, J. H. and R. O. Slayter. 1977. Mechanisms of succession in natural communities
and their role in community stability and organization. American Naturalist
111:1119-1144.
Colwell, R. K. 2009. EstimateS: Statistical estimation of species richness and shared
species from samples. Version 8.2. User's Guide and application published at:
http://purl.oclc.org/estimates.
Cornejo, F. and J. Janovec. 2010. Seeds of Amazonian plants. Princeton University Press,
Princeton, NJ.
Cramer, J. M., R. C. G. Mesquita, and G. B. Williamson. 2007. Differential effects of
forest fragmentation on seed dispersal: A case study of two Central Amazon trees
with contrasting dispersal syndromes. Biological Conservation 137:415-423.
Didham, R. K, J. H. Lawton. 1999. Edge structure determines the magnitude of
changes in microclimate and vegetation structure in tropical forest fragments.
Biotropica 31:17-30.
Dourojeanni, M. 1987. Aprovechamiento del barbecho forestal en areas de agricultura
migratória en la Amazonía Peruana. Revista Forestal de1 Perú 14:15-61.
Duncan R. S. and V. E. Duncan. 2000. Forest succession and distance from forest edge
in an Afro-Tropical grassland. Biotropica 32:33-41.
Egler F. E. 1954. Vegetation science concepts I. Initial floristic composition – a factor in
old-field vegetation development. Vegetatio 4:412-417.
Fine P. V. A. 2002. The invasibility of tropical forests by exotic plants. Journal of
Tropical Ecology 18:687–705.
43
Finegan, B. 1984. Forest succession. Nature 312:109–114.
Finegan, B. 1992. The management potential of Neotropical secondary lowland rain
forest. Forest Ecology and Management 47:295-321.
Finegan, B. 1996. Pattern and process in Neotropical secondary rain forests: The first 100
years of succession. Trends in Ecology and Evolution 11:119–124.
Fleming, T. H. and C. F. Williams. 1990. Phenology, seed dispersal, and recruitment in
Cecropia peltata (Moraceae) in Costa Rican tropical dry forest. Journal of
Tropical Ecology 6:163-178.
Gascon, C., and R. O. Bierregaard, Jr. 2001. The Biological Dynamics of Forest
Fragmentation Project: The study site, experimental design, and research activity
in R. O. Bierregaard, Jr., C. Gascon, T. E. Lovejoy, and R. Mesquita, editors.
Lessons from Amazonia. Yale University Press, New Haven, CT.
Gonçalves, J. H. C. 1991. Fitocenoses espontâneas dos sobreirais alentejanos: factores
ambientais e dinâmica da vegetação associada a condições de mortalidade das
árvores. Relatório final do curso de engenheiro silvicultor. Lisboa: Instituto
Superior de Agronomia, Universidade Técnica de Lisboa. 133p.
Gorchov, D. L., F. Cornejo, C. Ascorra and M. Jaramillo. 1993. The role of seed
dispersal in the natural regeneration of rain forest after strip-cutting in the
Peruvian Amazon. Vegetatio 107/108:339-349.
Griscom, B.W., and P. M. S. Ashton. 2003. Bamboo control of forest succession: Guadua
sarcocarpa in Southeastern Peru. Forest Ecology Management 175:445–454.
Guevara, S., M. del Castillo, Jr., P. Moreno-Casasola, and J. Laborde. 1991. Floristic
composition and structure of vegetation under isolated trees in Neotropical
pastures. Journal of Vegetation Science 3:655–664.
Heithaus, E. R. and T. H. Fleming. 1978. Foraging movements of a frugivorous bat,
Carollia perspicillata (Phyllostomidae). Ecological Monographs 48:127-143.
Hjerpe J., H. Hedenas and T. Elmqvist. 2001. Tropical rain forest recovery from cyclone
damage and fire in Samoa. Biotropica 33:249–259.
Hooper, E., R. Condit, and P. Legendre. 2002. Responses of 20 native tree species to
reforestation strategies for abandoned farmland in Panama. Ecological
Applications 12:1626–1641.
44
Hooper, E.R., P. Legendre, and R. Condit. 2004. Factors affecting community
composition of forest regeneration in deforested, abandoned land in Panama.
Ecology 85:3313–3326.
Howe, H. F. 1990. Seedling survival in a Central American tree (Virola surinamensis):
Effects of herbivory and canopy closure. Journal of Tropical Ecology 6:259–280.
Janzen, D. H. 1988. Management of habitat fragments in a tropical dry forest: growth.
Annals of the Missouri Botanic Garden 75:105–116.
Karr, J. R., S. J. Robinson, J. G. Blake and R. O. Bierregaard. 1990. Birds of four
Neotropical forests in A. H. Gentry, editor. Four Neotropical rainforests. Pages
237-269. Yale University Press, New Haven, CT.
Kauffman, J. B. 1991. Survival by sprouting in the tropical forests of the Eastern
Amazon. Biotropica 23:219-224.
Köppen, W. 1936. Das geographische System der Klimate in W. Köppen and R. Geiger,
editors. Handbuch der Klimatologie. Pages C1-C44. Gerbrüder Bornträger,
Berlin.
Lamb, D., J. Parrotta, R. Keenan, and N. Tucker. 1997. Rejoining habitat remnants
restoring degraded rainforest land in W. F. Laurance and R. O. Bierregaard, Jr.,
editors. Tropical Forest Remnants. Pages 366–385. University of Chicago Press,
Chicago, IL.
Lindernmayer D. B., and H. A. Nix. 1993. Ecological principles for design of wildlife
corridors. Conservation Biology. 7:627-360.
Loik, M. E. and K, D. Holl. 1999. Photosynthetic responses to light for rainforest
seedlings planted in abandoned pasture, Costa Rica. Restoration
Ecology 7:382–391.
Martinez-Garza, C. and H. F. Howe. 2003. Restoring tropical diversity: beating the time
tax on species loss. Journal of Applied Ecology 40:423–429.
Maury-Lechon, G. 1991. Comparative dynamics of tropical rain forest regeneration in
French Guyana in J. N. R. Jeffers, editor. Rainforest Regeneration and
Management. Pages 285-293. MAB Series, v. 6 UNESCO, Paris.
Medellin, R. A. and O. Gaona. 1999. Seed dispersal by bats and birds in forest and
disturbed habitats of Chiapas, Mexico. Biotropica 31:478–485.
45
Mesquita, R. C. G., K. Ickes, G. Ganade, and G. B. Williamson. 2001. Alternative
successional pathways in the Amazon basin. The Journal of Ecology 89:528-537.
Miller, P. M. 1999. Effects of deforestation on seed banks in a tropical deciduous forest
of eastern Mexico. Journal of Tropical Ecology 15:179–188.
Miller P. M., and J. B. Kauffman. 1998. Effects of slash and burn agriculture on species
abundance and composition of a tropical deciduous forest. Forest Ecology and
Management 103:191-201.
Miriti, M. N. 1998. Regeneração florestal em pastagens abandonadas na Amazônia
Central: competição, predação, e dispersão de sementes in C. Gascon, D. Nepstad
and P. Moutinho, editors. Floresta Amazônica: Dinâmica, regeneração e manejo.
Pages 179–191. Instituto Nacional de Pesquisa da Amazonia, Manaus, Brazil.
Monaco, L. M., R. C. G. Mesquita and G. B. Williamson. Banco de sementes de uma
floresta secundária Amazônica dominada por Vismia. 2003. Acta Amazônica
33:41-52.
Montagnini, F., E. González, C. Porras, and R. Rheingans. 1995. Mixed and pure forest
plantations in the humid Neotropics: A comparison of early growth, pest damage
and establishment costs. Commonwealth Forest Review 74:306–314.
Montero, G., E. Torres, I. Cañellas. 1994. Regeneración de alcornocales. Síntesis
Bibliográfica Ecología 8:271–83.
Morrison, D. W. 1980. Foraging and day-roost dynamics of canopy fruit bats in Panama.
Journal of Mammalogy 62: 20-29.
Natividade, J. V. 1950. Subericultura. Lisboa: Ministério da Agricultura, Pescas e
Alimentação, Direcção-Geral das Florestas. p. 387.
Norden, N., R. C. G. Mesquita, T. V. Bentos, R. L. Chazdon, and G. B. Williamson.
2011. Contrasting community compensatory trends in alternative successional
pathways in central Amazonia. Oikos 120:143–151.
Oliver, C. D. 1981. Forest development in North America following major disturbances.
Forest Ecology and Management 3:153-168.
Powell, G. V. N. 1989. On the possible contribution of mixed species flocks to species
richness in Neotropical avifaunas. Behavioral Ecology and Sociobiology
24:387-393.
46
Quintana-Ascencio, P. F., M. Gonzales-Espinoza, N. RamírezMarcial, G. DominguezVázquez, and M. Martínez-Icó. 1996. Soil seed banks and regeneration of
tropical rain forest from milpa fields at the Selva Lacandona, Chiapas, Mexico.
Biotropica 28:192–209.
Radtke, M. G., C. R. V. da Fonseca, and G. B. Williamson. 2007. The old and young
Amazon: dung beetle biomass, abundance and species diversity. Biotropica
39:725-730.
Ranzani, G., 1980. Indentificação e caracterização de alguns solos da Estação
Experimental de Silvicultura Tropical do INPA. Acta Amazônica 10:7–41.
Richards, P. W. The Tropical Rain Forest. Cambridge University Press, 1976.
Rivas-Martínez S, M. Lousa, T. E. Díz, F. Fernández-González, J. C. Costa. 1990. La
vegetación del sur de Portugal (Sado, Alentejo y Algarve). Itinera Geobotanica
3:5–126.
Remsen, J. V., D. A. Good. 1996. Misuse of data from mist net captures to assess relative
abundance in bird populations. Auk 113:81–398.
Reynolds, R. T., J. M. Scott, and R. A. Nussbaum. 1980. A variable circular-plot method
for estimating bird numbers. Condor 82:309-313.
Rosenberg, G. H. 1990. Habitat specialization and foraging behavior by birds of
Amazonian river islands in Northeastern Peru. The Condor 92:427-443.
Saldarriaga, J. G. 1985. Forest succession in the upper Rio Negro of Colombia and
Venezuela. Doctoral thesis, University of Tennessee, Knoxville.
Saldarriaga, J. G. and C. Uhl. 1991. Recovery of forest vegetation following slash-andburn agriculture in the upper Rio Negro in A. Gomes-Pompa, T.C. Whitmore and
M. Hadley, editors. Rain Forest Regeneration and Management. MAB, 6. Pages
285-293. UNESCO, Paris.
Sampaio, E. V. S. B., I. H. Salcedo, and J. B. Kauffman. 1993. Effect of different fire
severities on coppicing of Caatinga vegetation in Serra Talhado, PE, Brazil.
Biotropica 25: 452–460.
Saracco, J. F., J. A. Collazo, and M. J. Groom. 2004. How do frugivores track resources?
Insights from spatial analyses of bird foraging in a tropical forest. Oecologia
139:235-245.
47
Sarmiento, F. O. 1997. Arrested succession in pastures hinders regeneration of
Tropandean forests and shreds mountain landscapes. Environmental Conservation
24:14–23.
SAS software, Version 9.1.3, 2004. SAS Institute Inc., Cary, NC.
Saunders, D. A. and R. J. Hobbs, editors. 1991. Nature conservation 2: The role of
corridors. Surrey Beatty and Sons, Chipping Norton, Australia.
Smythe, N. 1970. Relationships between fruiting seasons and seed dispersal methods
in a Neotropical forest. The American Naturalist 104:25-35.
Southwood, T. R. E. and P. A. Henderson. 2000. Ecological Methods. Blackwell Science,
Oxford.
Stouffer, P. C. and R. O. Bierregaard, Jr. 1995. Use of Amazonian forest fragments by
understory insectivorous birds. Ecology 76:2429-2445.
Terborgh, J. 1990. Seed and fruit dispersal-commentary in K. S. Bawa and M. Handley,
editors. Reproductive ecology of tropical forest plants. Man and the Biosphere
Series. Pages 181-190. The Parthenon Publishing Group, Paris, France.
Tewksbury, J. J., D. J. Levey, N. M. Haddad, S. Sargent, J. L. Orrock, A. Weldon, B.J.
Danielson, J. Brinkerhoff, E. I. Damschen, and P. Townsend. 2002. Corridors
affect plants, animals, and their interactions in fragmented landscapes.
Proceedings of the National Academy of Sciences, USA, 99:12923–12926.
Thomas, D.W., D. Cloutier, M. Provencher, and C. Houle. 1988. The shape of bird- and
bat-generated seed shadows around a tropical fruiting tree. Biotropica
20:347–348.
Tucker, N. I. J.,and T. M. Murphy. 1997. The effects of ecological rehabilitation on
vegetation recruitment: Some observations from the wet tropics of North
Queensland. Forest Ecology and Management 99:133–152.
Turner, I. M. 1996. Species loss in fragments of tropical rain forests: A review of the
evidence. Journal of Applied Ecology 33:200–209.
Tuttle, M. D., and L, Hensley. 2000 The Bat House Builder‟s Handbook. University of
Texas Press, Austin, TX.
Uhl, C, and R. Clark. 1983. Seed ecology of selected Amazon Basin successional species.
Botanical Gazette 144:419- 425.
48
Uhl, C., D. Nepstad, R. Buschbacher, K. Clark, B. Kauffman, and S. Subler. 1990.
Studies of ecosystem response to natural and anthropogenic disturbance provide
guidelines for designing sustainable land-use systems in Amazonia. A. B.
Anderson, editor. Alternatives to Deforestation: Steps Toward Sustainable Use of
the Amazon Rain Forest. Pages 24–42. Columbia University Press, New York,
NY.
West, D. C., H. H. Shugart, and D. B. Botkin, editors. 1981. Forest succession: Concepts
and applications. Springer-Verlag, NY.
Wijdeven, S. M. J. and M. E. Kuzee. 2000. Seed availability as a limiting factor in forest
recovery processes in Costa Rica. Restoration Ecology 8:414–424.
Williamson, G. B., R. C. G. Mesquita, K. Ickes and G. Ganade. 1998. Estratégias de
árvores pioneiras nos Neotrópicos in C. Gascon and P. Moutinho, editors. Floresta
Amazônica: dinâmica, regeneração e manejo. Pages 131-144. Instituto Nacional
de Pesquisas da Amazônia, Manaus, Brazil.
Zarin D. J., E. A. Davidson, E. Brondizio, I. C. G Vieira, T. Sá, T. Feldpausch, E. A. G.
Schuur, R. C. G. Mesquita, E. Moran, P. Delamonica, M. J. Ducey, G. C. Hurtt,
C. Salimon, and M. Denich. 2005. Legacy of fire slows carbon accumulation in
Amazonian forest regrowth. Frontiers in Ecology and the Environment
3:365–369.
Zhang, S. Y. and L. X. Wang. 1995. Comparison of three fruit census methods in
French Guiana. Journal of Tropical Ecology 11:281-294.
49
Appendix 1. Species Lists
Appendix 1A. Second Growth Stand Vegetation
Abundance of each species of tree, palm, shrub and liana (>3 cm d.b.h.) recorded in Cecropia stands
(C1-C3) and Vismia stands (V1-V5). Numbers represent the quantity of each species that were found
and numbers in bold are those that were found to re-sprout.
Cecropia Stands
Vismia Stands
Genus
Species
C1 C2
C3
V1 V2 V3 V4 V5
Abarema
adenophora
1
1
Abarema
jubumba
1
Alchorneopsis
floribunda
1
3
1
Alchornia
discolor
1
Aniba
terminalis
2
Anisophilium
manauensis
1
Aparicium
cordatum
1
1
1
Apeiba
equinata
1
1
1
Argofilae
integrifolia
1
1
12
Astrocaryum
genicanthus
2
1
4
Bellucia
imperialis
1
6
6
19
2
Bellucia
grossularioides
5
9
4
6
Bocageopsis
multiflora
2
2
6
Brachium
palidum
1
Brosimum
acutifolium
4
Brosimum
guianense
1
1
1
Brosimum
potabile
1
Brosimum
rubescens
1
Bucheriarea
congesta
1
Byrsonima
crispa
1
Byrsonima
duckeana
8
1
8
3
Capsoneura
ule
1
50
Cariocar
Casearia
Casearia
Casearia
Casearia
Casearia
Casearia
Cecropia
Cecropia
Cecropia
Chimarres
Chrysophyllum
Chrysophyllum
Conceveiba
Cordia
Cordia
Cordia
Coussopoa
Crepidospermum
Croton
Cupania
Cupania
Dialium
Diplotropis
Dipteryx
Dulacea
Duroia
Duroia
Elioteca
Enterolobium
Eperua
viloso
arborea
duckeana
grandiflora
jabutensis
silvatica
vitensis
sciadophylla
concolor
purpurascens
duckeana
sanguinodentum
pomiferum
guianensis
falax
hirta
sagotiana
asperifolia
ramiflorum
lanjouwensis
hispida
scrobiculata
guianensis
triloba
odorato
candida
longifolia
macrophylla
globosa
eschamburque
glabiflora
6
9
1
1
1
6
2
1
1
1
1
1
3
41
1
40
1
1
2
1
63
35
21
30
1
4
1
1
16
1
1
2
1
1
1
2
6
1
1
1
8
1
1
1
1
1
1
2
1
1
1
1
2
1
1
2
8
2
3
1
2
51
1
4
2
Epinusa
Erichtroxilium
Eschweilera
Eschweilera
Eschweilera
Eschweilera
Eugenia
Eugenia
Euterpe
Ficus
Ficus
Ficus
Garcinia
Goupia
Guarea
Guarea
Guatteria
Guatteria
Guatteria
Guatteria
Heliocostylis
Heliocostylis
Heliotropium
Hervia
Hiania
Himatanthus
Iminea
Inga
Inga
Inga
Inga
guianensis
macronatum
coriacea
truncata
roraimensis
wachenheimii
cupulata
patricia
precatoria
duckeana
guianensis
trigonum
madruna
glabra
gidonea
transifolia
foliosa
olivacea
picophylla
sitophila
scabra
tomentosa
sitiofolium
brasilensis
espesciosa
sucuuba
corbadium
umbelifora
cayennensis
estipulares
grandifolia
1
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
1
40
8
4
5
1
1
7
7
5
5
5
1
1
1
1
1
1
9
1
7
7
7
14
2
3
2
2
1
1
1
1
1
2
2
1
2
2
1
52
1
Inga
Inga
Inga
Inga
Inga
Inga
Inga
Inga
Jacaranda
Laetia
Lasistema
Lasistema
Lecitis
Licania
Loreya
Mabia
Mabia
Mabia
Mapira
Maquira
Miconia
Miconia
Miconia
Miconia
Miconia
Miconia
Miconia
Miconia
Miconia
Miconia
Miconia
huberi
laterifolia
leocalicina
obedensis
rubiginosa
species
tibauiana
umbractica
copaia
procera
agregatum
grandifolia
barnade
gracilipes
spruceana
acutifolia
angularis
caudata
guianensis
calophyllum
microphylla
pyrifolia
burchelli
argiofilae
dispar
fenestrata
gratissima
lepitoptera
regelli
testrapernoides
tomentosa
1
1
1
1
1
1
1
2
1
1
2
31
1
2
2
8
4
1
14
8
1
2
1
9
2
1
1
1
1
2
1
2
5
1
1
1
2
1
1
3
37
2
15
21
1
16
1
1
4
37
1
1
2
4
3
2
1
7
2
1
1
27
3
1
1
1
10
2
53
3
Micrandropsis
Microphylens
Microphyllus
Milicia
Myrcia
Myrcia
Myrcia
Myrcia
Myrcia
Myrcia
Ocotea
Ocotea
Ocotea
Ocotea
Oonocarpus
Ormosia
Paliculia
Paliculia
Paraicornia
Parkia
Piper
Pogonotola
Poterium
Protium
Protium
Protium
Psidium
Psodomedia
Pterocarpus
Rauvolfia
Rhodostenophne
scleroxylon
gruquensis
casiquicarensis
excelsa
species
bracteata
falax
fenestrata
magnifolia
paiva
Amazônica
negrensis
santodora
tabacifolia
bacaba
paraensis
guianensis
columbifera
fasciculatum
multijuga
aduncum
eschumurquiana
hispida
gigantum
grandifolium
trifoliolatum
guajava
laeves
rohrii
sprucei
sordida
1
1
1
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
3
1
3
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
54
1
3
Rinorea
Rinorea
Rinorea
Rollinia
Ruisterania
Sacoglotis
Santoxilum
Sapium
Simaba
Siparuna
Siparuna
Sloania
Solanum
Solanum
Solocea
Sterculia
Stryphnodendron
Stryphnodendron
Stryphnodendron
Swartzia
Swartzia
Swartzia
Swartzia
Swartzia
Syagrus
Taberna
Tachigali
Tagichali
Tapirira
Tapirira
Taulisia
falcata
rasenosa
species
insignis
albifloria
ceratocarpus
dejaubatistae
glandulatum
polyfila
desipins
guianensis
eschomburke
crinitum
rugosum
guiliminama
pruriens
guianense
burcheremo
pulcherrimum
longifolia
reticulata
arborescens
corrugata
cuspidata
comosus
emotania
myrmecophila
rolifolium
guianensis
obtusa
pulvinata
1
3
1
1
2
3
1
1
1
1
1
1
1
2
1
11
2
1
2
2
3
21
3
1
1
1
1
1
7
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
2
1
6
3
1
2
2
2
1
55
Teobroma
Tetagrassus
Toulicia
Toulicia
Trattinnickia
Trema
Tsirorium
Virola
Virola
Virola
Vismia
Vismia
Vismia
Vismia
Vismia
Voarana
Vuceriavia
Xilopia
Xilopia
silvestre
panamensis
guianensis
pulvinata
burserifolia
micrantha
epussanium
caducifolia
calophylla
mollissima
guianensis
japurensis
cayennenis
gracilis
sandwithii
guianensis
grandes
nitida
ventane
1
1
1
6
1
1
5
1
4
21
1
4
4
35
71
2
1
20
58
6
3
88
41
6
18
17
88
2
1
2
17
1
1
1
2
7
5
1
1
1
1
4
1
2
1
4
3
11
4
24
1
4
56
3
24
139
Appendix 1B. Daily Seed Trap Collection
Abundance of seeds and fecal samples collected in seed traps at each site. Cecropia stands (C1-C3), and Vismia stands (V1-V5). No.= Total number of
seeds collected; Feces No.= Number of fecal samples collected; Other= Samples containing fruit pulp, fibrousand other organic materials
Cecropia stands
Vismia stands
C1
C2
C3
V1
V2
V3
V4
V5
Fecal content
No. Feces No. Feces No. Feces No. Feces No. Feces No. Feces No. Feces No.
Feces
Vismia spp.
91
2
453
62
50
7
644
51
559
29
1014
47
4
1
399
26
Cecropia spp.
57
7
104
3
2
2
Miconia spp.
1116
16
12
1
110
1
903
11
10
1
401
5
Piper spp.
48
1
133
5
33
2
57
4
Solanum spp.
10
2
122
7
57
9
Clidemia spp.
2
1
44
1
Phytolacca spp.
7
1
Lantana spp.
1
1
Insect
4
4
14
4
10
10
3
2
Other
15
30
17
17
15
15
13
15
57
Appendix 1C. Monthly Seed Trap Collection
Abundance of seeds (total number) collected in seed traps at monthly intervals in Cecropia stands (C1-C3), Vismia stands (V1-V5) and mature forest
(M1-M5). Mature forest stands were located within 100 m of second growth stands. Pairs of proximate second growth – mature forest sites are: M1C1, M2-V1, M3-V3, M4-V4, M5-V5
Cecropia stands
Vismia stands
Mature forest stands
Size Class
C1
C2
C3
V1
V2
V3
V4
V5
M1 M2 M3 M4 M5
Species
Tiny (0.0-0.5cm)
1
30
19,689 16,782 33,792
235
78,871
Vismia spp.
40
188
17
9
25
32
Cecropia spp. 1,566 152
49
33
Solanum spp.
192
2
Piper spp.
100
Croton spp.
18
Miconia spp.
2
Unknown
Small (0.5-0.99cm)
Unknown
4
1
Medium (1.0-1.99cm)
Unknown
1
1
1
43
6
30
2
7
Large (>2.0cm)
Mauritia spp.
1
Unknown
2
2
2
7
2
58
Appendix 1D. Mist-netting: Bat and Bat-dispersed Seeds Species Richness and Abundances
Number of bats captured in the Vismia stand “V3” and the abundance of seeds and seed-containing
fecal samples collected from each species.
Vismia
Piper
Solanum
Insect
Other
Total
No. Feces No. Feces No. Feces Feces
Feces
Bat species
captures
3
5
1
2
Artibeus jamaicensis
29
751
12
77
2
5
1
1
13
Carollia perspicillata
2
199
1
1
Sturnira lilium
59
Appendix 1E. Mist-netting: Bird Species Richness and Abundances
Species of birds captured in each stand type and total number captured. Guild assignments follow the
designations suggested by Karr et al. (1990), Stouffer and Bierregard (1995) and Powell (1989).
Individuals not identified to species are not included in this table.
Species
In
In
Total
Bird species
Code
Guild
Vismia Cecropia
No.
Automolus ochrolaemus
AUOC
I
x
1
Camptostoma obsoletum
CAOB
I/F
x
2
Cercomacra tyrannina
CETY
I
x
10
Columbina passerina
COPA
F
x
x
5
Columbina talpacoti
COTA
F
x
1
Corapipo guttaralis
COGU
F
x
1
Cyanocompsa cyanoides
CYCY
F
x
2
Cyclarhis gujanensis
CYGU
I
x
2
Dendrocincla fuliginosa
DEFU
I
x
x
5
Gallbula albirostris
GAAL
I
x
x
4
Geotrygon montana
GEMO
F
x
1
Gymnopithys rufigula
GYRU
I
x
5
Hypocnemis cantator
HYCA
I
x
1
Lepidothrix serena
LESE
F
x
x
5
Leptotila verreauxi
LEVE
F
x
2
Lophotrichus galeatus
LOGA
I
x
2
Manacus manacus
MAMA
F
x
12
Mionectes macconnelli
MIMA
I/F
x
x
21
Myiarchus ferox
MYFE
I
x
2
Myiarchus swainsoni
MYSW
I
x
1
Myiarchus tuberculifer
MYTU
I/F
x
2
Myrmeciza atrothorax
SCLE
I
x
2
Myrmotherula axillaris
MYAX
I
x
2
Myrmotherula longipennis
MYLO
I
x
2
Oryzoborus angolensis
ORAN
F
x
3
60
Pachyramphus rufus
Pernocstola rufifrons
Phaethornis ruber
Phaethornis supercilious
Picumnus exilis
Pipra pipra
Pithys albifrons
Platyrinchus coronatus
Ramphocelus carbo
Saltator maximus
Selenidera culik
Tachyphonus surinamus
Terenotriccus erythrurus
Thamnophilis murinis
Thraupis episcopus
Thraupis palmarum
Pheugopedius coraya
Tolmomyias policephalus
Trogon rufus
Vireo olivaceus
PARU
PERU
PHRU
PHSU
PIEX
PIPI
PIAL
PLCO
RACA
SAMA
SECU
TASU
TEER
THMU
THEP
THPA
THCO
TOPO
TRRU
VIOL
I
I
N/I
N/I
I
F
I
I
F
F
F
F
I
I
F
F
I
I
I/F
I
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
2
3
1
2
1
16
4
1
13
1
1
2
1
2
1
3
3
2
1
3
x
x
x
x
x
x
x
61
Appendix 1F. Bird-dispersed Seeds Species Richness and Abundances
Abundance of seeds and seed-containing fecal samples collected in Cecropia and Vismia stands by bird species. Species codes are listed in
Appendix E following the designations suggested by Karr et al. (1990), Stouffer and Bierregard (1995) and Powell (1989).
Species
CETY
DEFU
LESE
MIMA
Cecropia
PIPI
Stands
RACA
SAMA
THMU
Total
COGU
CYGU
LESE
MAMA
MIMA
Vismia
PIPI
Stands
RACA
TASU
THEP
THPA
UNUN
Total
Vismia
Cecropia
Miconia
Solanum
No. Feces
No. Feces
No.
Feces No. Feces
306
106
22
300
168
1
1
1
1
4
1
8
8
1
1
4
1
0
46
4
1
46
0
1
1
902
88
8
1
63
304
165
280
2613
5
1
4
3
4
8
1
73
1
105 2
3696 26
Clidemia
Phytolacca
Lantana
Trema
No. Feces
No. Feces
No. Feces
No.
Feces
0
0
0
0
0
2
1
3
1
3
1
1
1
1
14
1
1
1
1
1
3
1
9
10
8
0
2
1
1
32
3
62
3
1
9
2
4
6
1
2
Vita
Lindsay Michelle Wieland, born on April 8, 1982 to Gary and Mary Wieland, was
raised in Norwich, Vermont, along with her sisters Courtney and Jessica. Her
experiences while growing up in a house full of pets nestled in the forest of the Green
Mountains nourished her love for nature and animals. She pursued her interests in
ecology while completing a bachelor of science degree in biology at Dickinson College.
During her undergraduate studies, she furthered her interests in ecology while exploring
her desire to travel, by spending one semester abroad in at the University of Queensland
in Brisbane, Australia, and one semester with the School for Field Studies Center for
Wildlife Management Studies in Kenya. Following the completion of her Bachelor‟s
degree in 2004, Lindsay went on to spend two years in the United States Peace Corps. As
an education volunteer, Lindsay taught biology to pre-university students at the Escola
Secundária de Cambine in Cambine, Mozambique. Her desire to continue living abroad
while pursuing a career in ecology and conservation led her to return to the School for
Field Studies at the Center for Sustainable Development Studies in Atenas, Costa Rica.
This experience brought her to a brief stint as assistant data manager at the South Florida
Caribbean Network of the National Park Service, in Miami, Florida. In the summer of
2008, she moved to Baton Rouge, Louisiana, to pursue a Master‟s degree in the
Department of Biological Sciences at Louisiana State University, joining the lab of Dr. G.
Bruce Williamson. In the future, she plans to bring together her interests in science and
international travel in her professional life, while continuing to admire and work to
protect the natural world.
63