SELECTING LATE-SUCCESSIONAL TREES FOR TROPICAL

SELECTING LATE-SUCCESSIONAL TREES FOR TROPICAL FOREST
RESTORATION
BY
CRISTINA MARTÍNEZ-GARZA
B.S., National University of Mexico (UNAM), 1996
THESIS
Submitted as partial fulfillment of the requirements
for the degree of Doctor of Philosophy in Liberal Arts and Sciences
in the Graduate College of the
University of Illinois at Chicago, 2003
Chicago, Illinois
iii
This thesis is dedicated to the Martínez and Garza families, with special thanks to the
Martínez-Garza family, José Martínez, Magdalena Garza, José de Jesus, Silvia, Miguel
Angel, Clara, Alejandro, Carlos, and to my husband Raúl Díaz-Heredia.
iv
ACKNOWLEDGMENTS
I would like to thank my thesis committee, Hormoz BassiriRad, Joel S. Brown, Robin B.
Foster, Henry F. Howe and Martin Ricker, for their support and assistance. I especially
thank Hank Howe for his advice and friendship. I also thank my colleagues from UIC,
especially Norbert Cordeiro, Elaine Hooper, Malu Jorge, Maria Miriti, Gaby Nuñez,
Manuel Pacheco, Sonali Saha (and Amartya), Amy Sullivan, Barbara Zorn-Arnold and,
in Mexico, Reyna A. Castillo, Cecilia Sánchez, Juan Fornoni and Fernando Pacheco, all
of them were a constant source of technical and emotional support.
I thank all my brothers and sisters, especially Clara (and Gil), Alejandro, Miguel
(and Frederike) and Silvia for all their help in the fieldwork. I am grateful to my husband
Raul for his help through everything, life, the fieldwork and the writing of the thesis. I
infinitely thank my parents and my grandmother (Esperanza Portillo) for their love and
support that always accompany me.
Finally, I thank the staff of the Los Tuxtlas Biological Station where the fieldwork
was conducted. Financial support was provided by the National Council of Science and
Technology of Mexico (CONACyT) and The Lincoln Park Zoo Neotropic Foundation of
Chicago.
CMG
v
TABLE OF CONTENTS
CHAPTER
1.
PAGE
GENERAL INTRODUCTION
1.1 Introduction……………………………………………………
1.2 Restoration objectives…………………………………………
1.3 Conceptual Framework………………………………………..
1.3.1 Leaf Traits of Tropical tree species………………..
1.4 Literature Cited……………………………………..………….
2.
RESTORING TROPICAL DIVERSITY: BEATING THE TIME TAX
ON SPECIES LOSS
2.1 Abstract………………………………………………………..
2.2 Introduction……………………………………………………
2.3 Natural succession…………………………………………….
2.4 Arriving and surviving in unnatural landscapes………………
2.5 Attrition of species from fragments in alien matrices………...
2.6 Restoring the matrix: beating the time tax in diversity……….
2.7 Synthesis and Applications……………………………………
2.8 Acknowledgment……………………………………………...
2.9 Literature Cited………………………………………………..
3.
1
2
3
4
7
11
12
13
14
17
19
24
25
26
ONTOGENY OF SUN AND SHADE LEAVES OF EIGHT NONPIONEER TROPICAL TREE SPECIES
3.1 Abstract……………………………………………………….
3.2 Introduction…………………………………………………...
3.3 Material and methods…………………………………………
3.3.1 Study site………………………………………….
3.3.2 Sampling………………………………………….
3.3.3 Data Analysis……………………………………..
3.4 Results…………………………………………………………
3.4.1 Effects of species and ontogenetic stage on leaf
traits………………………………………………..
3.4.1.1.Leaf State………………………………….
3.4.1.2.Leaf Flexibility……………………………
3.4.2 Ontogenetic leaf variability and maximal height
species…………………………………………….
3.5 Discussion…………………………………………………….
3.6 Acknowledgment……………………………………………..
3.7 Literature Cited………………………………………………..
31
32
36
36
36
40
41
41
41
44
46
51
53
54
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TABLE OF CONTENTS (continued)
CHAPTER
4.
PAGE
RESTORING BIODIVERSITY: PREDICTING SURVIVAL AND
GROWTH OF LATE-SUCCESSIONAL TREE SPECIES IN EARLY
SUCCESSIONAL ECOSYSTEMS
4.1 Abstract………………………………………………………..
4.2 Introduction……………………………………………………
4.3 Methods……………………………………………………….
4.3.1 Study site………………………………………….
4.3.2 Land use history and Experimental planting……..
4.3.3 Data analysis………………………………………
4.4 Results…………………………………………………………
4.4.1 CV of Leaf traits and Survival…………………….
4.4.2 CV of Leaf traits and Increments in height and
Diameter…………………………………………..
4.4.3 Maximal tree height…….………………………….
4.5 Discussion…………………………………………………….
4.6 Conclusions……………………………………………………
4.7 Acknowledgment………………………………………………
4.8 Literature Cited…………………………………………………
5.
58
59
62
62
62
66
68
68
68
73
73
76
77
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PREDICTING SURVIVAL AND GROWTH RATES OF LATESUCCESSIONAL TREE SPECIES IN ABANDONED PASTURES
5.1 Abstract……………………………………………………….
5.2 Introduction…………………………………………………..
5.3 Methods………………………………………………………
5.3.1 Study Site…………………………………………
5.3.2 Land use and Experimental Plantation……………
5.3.3 Data analysis………………………………………
5.4 Results…………………………………………………………
5.4.1 Survival……………………………………………
5.4.2 Increments in Height and Diameter……………….
5.4.3 Leaf Traits…………………………………………
5.4.3.1. Leaf size…………………………………..
5.4.3.2. SLM………………………………………
5.4.3.3. Leaf Water Content………………………
5.4.3.4. Leaf Density………………………………
5.4.4 Leaf traits and performance in secondary forest and
Pastures……………………………………………
82
83
86
86
86
89
91
91
91
92
93
93
95
95
96
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TABLE OF CONTENTS (continued)
CHAPTER
PAGE
5.4.5
6.
CV of leaf traits and performance in secondary
forest and Pastures…………………………………
5.5 Discussion……………………………………………………..
5.6 Conclusions……………………………………………………
5.7 Literature Cited………………………………………………..
103
108
110
110
SYNTHESIS AND IMPLICATIONS…………………………….
6.1. Literature Cited……………………………………………….
113
123
APPENDICES
Appendix A……………………………………………………….
Appendix B……………………………………………………….
Appendix C……………………………………………………….
Appendix D……….………………………………………………
Appendix E……………………………………………………….
Appendix F……………………………………….………………
Appendix G………………………………………………………
Appendix H………………………………………………………
Appendix I……………………………………………………….
Appendix J……………………………………………………….
Appendix K………………………………………………………
Appendix L………………………………………………………
Appendix M………………………………………………………
Appendix N……………………………………………………….
Appendix O……………………………………………………….
Appendix P………………………………………………………..
128
129
130
131
132
133
134
136
137
138
139
140
141
142
143
144
VITA……………………………………………………………….. ……
145
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LIST OF TABLES
TABLE
I.
PAGE
VARIABLES ASSESSED IN EIGHT TROPICAL
NON-PIONEER TREE SPECIES……………………………….
35
SPECIES, AUTHORITIES AND RANGE OF STATURE
OF EIGHT TROPICAL NON-PIONEER TREE SPECIES…….
37
LEAF TRAITS MEASURED IN EIGHT TROPICAL TREE
SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO.............
39
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE
OF LEAF TRAITS MEASURED IN EIGHT TROPICAL TREE
SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO…………
41
UNIVARIATE ANALYSIS OF VARIANCE OF LEAF TRAITS
AT EACH ONTOGENETIC STAGE OF EIGHT TROPICAL
TREE SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO…
43
UNIVARIATE ANALYSIS OF VARIANCE OF LEAF TARITS
FOR EACH LEAF ENVIRONMENT OF EIGHT TROPICAL
TREE SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO…
43
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE
OF LEAF FLEXIBILITIES MEASURED IN EIGHT TROPICAL
TREE SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO…
45
UNIVARIATE ANALYSIS OF VARIANCE OF LEAF
FLEXIBILITY FOR EACH ONTOGENETIC STAGE OF
EIGHT TROPICAL TREE SPECIES IN LOS TUXTLAS,
VERACRUZ, MEXICO…………………………………………..
46
PHOTON FLUX DENSITY (PFD), GRAVIMETRIC SOIL
MOISTURE AND BULK DENSITY AT DIFFERENT LEVELS
OF CROWN ILLUMINATION INDEX…………………………
64
FAMILY, FRUIT TYPE AND RANGE OF HEIGHT OF 23
LATE-SUCCESSIONAL TROPICAL TREE SPECIES…………
67
XI.
CORRELATIONS AMONG LEAF TRAITS……………………
67
XII.
PHOTON FLUX DENSITY (PFD), GRAVIMETRIC SOIL
MOISTURE AND BULK DENSITY IN SECONDARY FOREST
AND PASTURES…………………………………………………
89
II.
III.
IV.
V.
VI.
VII.
VIII.
IX.
X.
ix
LIST OF TABLES (continued)
TABLE
XIII.
PAGE
FAMILY, FRUIT TYPE AND RANGE OF MAXIMAL TREE
HEIGHT OF 12 LATE-SUCCESSIONAL TROPICAL TREE
SPECIES………………………………………………………….
XIV. SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE
OF INCREMENTS IN HEIGHT AND DIAMETER MEASURED
IN 12 TROPICAL TREE SPECIES IN LOS TUXTLAS,
VERACRUZ, MEXICO.............………………………………….
XV.
90
92
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE
OF LEAF TRAITS MEASURED IN 12 TROPICAL
TREE SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO…
95
XVI. LEAF SIZE MEASURED IN EIGHT TROPICAL TREE
SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO..............................................
127
XVII. SLM MEASURED IN EIGHT TROPICAL TREE SPECIES
AT THREE ONTOGENETIC STAGES IN LOS TUXTLAS,
VERACRUZ, MEXICO…………………………………………..
128
XVIII. LEAF DENSITY MEASURED IN EIGHT TROPICAL TREE
SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO.............................................
129
XIX. LEAF TOUGHNESS MEASURED IN EIGHT TROPICAL TREE
SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO.............................................
130
XX.
LEAF WATER CONTENT MEASURED IN EIGHT TROPICAL
TREE SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO..............................................
131
XXI. UNIVARIATE ANALYSIS OF VARIANCE OF FOLIAR
FLEXIBILITY OF EIGHT TROPICAL NON-PIONEER TREE
SPECIES IN LOS TUXTLAS, VERACRUZ, MEXICO………...
132
XXII. FAMILY, COEFFICIENT OF VARIATION OF LEAF TRAITS
AND SAMPLE SIZE OF 23 LATE-SUCCESSIONAL TROPICAL
TREE SPECIES…………………………………………………...
133
XXIII. SURVIVAL OF 12 LATE-SUCCESSIONAL TROPICAL TREE
SPECIES IN PASTURES AND SECONDARY FORESTS……..
136
x
LIST OF TABLES (continued)
TABLE
PAGE
XXIV. LEAF TRAITS AND TOTAL NUMBER OF INDIVIDUALS
SAMPLED OF 12 LATE-SUCCESSIONAL TROPICAL TREE
SPECIES………………………………………………………….
137
XXV. PEARSON CORRELATION AMONG LEAF TRAITS
MEASURED IN PASTURES AND SECONDARY FOREST
FOR 12 TREE SPECIES AT LOS TUXTLAS, MEXICO………
138
XXVI. SUMMARY OF UNIVARIATE ANALYSIS OF VARIANCE
OF INCREMENTS IN HEGHT FOR BROSIMUM
ALICASTRUM AND POUTERIA CAMPECHIANA FROM A
GREENHOUS EEXPERIMENT…………………………………
139
XXVII. SUMMARY OF MULTIVARIATE ANALYSIS OF
VARIANCE OF LEAF TRAITS OF BROSIMUM
ALICASTRUM AND POUTERIA CAMPECHIANA
GROWING IN A GREENHOUSE EXPERIMENT AT
THREE LIGHT LEVELS AND TWO WATER
LEVELS…………………………………………………………..
141
XXVIII. LEAF TRAITS OF BROSIMUM ALICASTRUM AND
POUTERIA CAMPECHIANA GROWING IN A GREENHOUSE
EXPERIMENT AT THREE LIGHT LEVELS AND TWO WATER
LEVELS…………………………………………………………..
142
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LIST OF FIGURES
FIGURE
1.
2.
3.
4.
5.
6.
PAGE
Correlation between ontogenetic leaf variability and the
maximal height of species for eight non-pioneer tropical
tree species from Los Tuxtlas, Veracruz, Mexico. A) Leaf
size from juveniles to adults, B) SLM from seedlings to
juveniles, C) SLM from seedlings to adults. The key for
the species follows Table II……………………………………….
48
Regression of 4-year survivorship percentage on the
coefficient of variation of SLM of 23 non-pioneer tropical tree
species growing in an experimental planting in the Cooperative
of Lázaro Cárdenas, Los Tuxtlas, Mexico. Open circles
correspond to canopy and emergent species (> 25 m) and filled
circles to understory species. The key for the species follows
Table X……………………………………………………………
69
Regression of the Incremental growth in basal diameter on
the coefficient of variation of SLM of 23 non-pioneer tropical
tree species growing in an experimental planting in the
Cooperative of Lazaro Cárdenas, Los Tuxtlas, Mexico. Open
circles correspond to canopy and emergent species (> 25 m)
and filled circles to understory species. The key for the species
follows Table X…………………………………………………..
71
Regression of the Incremental growth in height on the
coefficient of variation of SLM of 23 non-pioneer tropical tree
species growing in an experimental planting in the Cooperative
of Lazaro Cárdenas, Los Tuxtlas, Mexico. Open circles
correspond to canopy and emergent species (> 25 m) and filled
circles to understory species. The key for the species follows
Table X……………………………………………………………
72
Regression of the Coefficient of variation of SLM on the
maximal tree height of 23 non-pioneer tropical tree species
growing in an experimental planting in the Cooperative of Lazaro
Cárdenas, Los Tuxtlas, Mexico. The key for the species follows
Table X……………………………………………………………
74
Log Increment of diameter of 12 late-successional tropical tree
species Key for species follows Table XIII. Asterisks over bars
represent significant differences between secondary forest and
pasture tested with Pos Hoc Tuke Test…………………………...
94
xii
LIST OF FIGURES (continued)
FIGURE
7.
8.
9.
10.
11.
12.
13.
PAGE
Regression of 17-month survivorship percentage on the
Leaf size of 11 non-pioneer tropical tree species growing in an
experimental planting in the Cooperative of Lázaro Cárdenas,
Los Tuxtlas, Mexico. The key for the species follows Table XIII.
97
Regression of Log of monthly increment in diameter of
individuals growing in pasture on log of SLM of conspecific
growing in the secondary forest for 12 late-successional tropical
tree species in the Cooperative of Lázaro Cárdenas, Los Tuxtlas,
Mexico. The key for the species follows Table XIII……………..
99
Regression of Log Increment in diameter on log of SLM of
individuals growing in the pasture for 12 late-successional
tropical tree species in the Cooperative of Lázaro Cárdenas,
Los Tuxtlas, Mexico. The key for the species follows Table XIII.
100
Regression of Log Increment in diameter of individuals growing
in pasture on Log of Leaf Density of conspecific growing in the
secondary forest for 12 late-successional tropical tree species in
the Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The
key for the species follows Table XIII…..………………………..
101
Regression of 17-months survivorship of individuals growing
in pastures on Log Increment in height for 12 late-successional
tropical tree species in the Cooperative of Lázaro Cárdenas,
Los Tuxtlas, Mexico. The key for the species follows Table XIII.
102
Regression of 17-month survivorship in secondary forests on
the coefficient of variation of Water Content of 12 non-pioneer
tropical tree species growing in an experimental planting in the
Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The key
for the species follows Table XXIII……………………………….
104
Regression of the increments in height in secondary forests on the
Coefficient of variation of Water Content of 12 non-pioneer
tropical tree species growing in an experimental planting in the
Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The key
for the species follows Table XXIII………………………………
105
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LIST OF FIGURES (continued)
FIGURE
14.
15.
16.
17.
18.
PAGE
Regression of the increments in height in secondary forests on
the Coefficient of variation of Leaf Density of 12 non-pioneer
tropical tree species growing in an experimental planting in the
Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The key
for the species follows Table XXIII………………………….……
106
Regression of the increments in height in pastures on the
Coefficient of variation of Leaf Density of 12 non-pioneer
tropical tree species growing in an experimental planting in the
Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The key
for the species follows Table XXIII……………………………....
107
Regressions of Log of monthly Increment in height on the
coefficient of variation of SLM for canopy and understory species
growing in an experimental planting in the Cooperative of Lazaro
Cárdenas, Los Tuxtlas, Mexico……………………………………
135
Log increments in Height measured in Brosimum alicastrum and
Pouteria campechiana individuals growing in a greenhouse
experiment at three light levels and two water levels…………….
140
Regression of Log increment in height and Log of SLM for
Brosimum alicastrum (bold letters) and Pouteria campechiana.
Each point represent mean Log increment in height and mean
Log of SLM for a combination of light levels (HL, high light
levels [100 %], ML, medium [50 %] and LL, low light [30 %],
and water availability (HW, high water availability [70 %], LW,
low water [50 %])…………………………………………………
143
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LIST OF ABBREVIATIONS
ANOVA
Analysis of Variance
CV
Coefficient of Variation
Env
Environment
LTBS
Los Tuxtlas Biological Station
Leaf E
Leaf Environment
MANOVA
Multivariate Analysis of Variance
Ontogenetic S
Ontogenetic Stage
P
Pasture
PFD
Photon Flux Density (µmol /m2 s)
SLM
Specific Leaf Mass
SF
Secondary Forest
Sec For
Secondary Forest
WC
Leaf Water Content
xv
SUMMARY
Planting seedlings of interior forest species after land abandonment could sharply
accelerate the process of re-vegetation of complex communities. Pioneer stands or
monocultural plantations may be enriched with seedlings of late-successional animaldispersed trees, or initial plantings could be mixes of late-successional and pioneer
species. This thesis sets criteria for selecting species for enrichments and in some cases
for overstories. My main hypothesis is that those species with leaf traits associated to
high light levels and/or higher ability to adjust leaf traits to different light levels and
water availability, will survive and grow better in environmental conditions typical of
early successional environments (i.e., abandoned pastures, secondary forest). Further, tall
species (canopy and emergent) experience a vertical gradient in light levels and water
availability from their seedling stage in the shade understory to the bright canopy.
Therefore, I expect tall species to show leaf traits related to high light levels and higher
ability to adjust leaf traits to different environmental conditions, reflected by higher
intraspecific variation in leaf traits measured across various microhabitats.
From 23 late-successional tree species evaluated, those with high intraspecific
variability in leaf mass per unit leaf area (specific leaf mass; SLM) showed higher
survival and growth rates across different microhabitats of early successional
environments than species with low variability in SLM, while for thwelve latesuccessional tree species evaluated, those species with low mean SLM measured in sun
(pastures) or shade (secondary forest) leaves showed higher growth rates in height when
growing in abandoned pastures with long-lasting high light conditions. Maximal tree
xvi
SUMMARY (continued)
height was related to variation in SLM but it was not correlated to survival and growth
rates in early successional ecosystems and neither in pastures. Leaf traits offer easily
measurable variables that may provide criteria for selection of species for planting mixed
species stands. This alleviates the need to individually screen large numbers of latesuccessional species for performance in different scenarios of restoration (i.e. early
successional ecosystems, pastures).
1. GENERAL INTRODUCTION
1.1
Introduction
It is widely recognized that deforestation of tropical habitats is occurring at a
rapid and in many places accelerating pace (Bawa and Dayanandan, 1997); what is less
appreciated is that tens of thousands of hectares of denuded land are abandoned annually
to succession back to forest (Moran et al., 1994). The normal process of secondary
succession in neotropical habitats involves initial colonization by early successional fastgrowing species, which occupy sites for up to 15 years or more before a mixture of them
and a species-poor cohort of long-lived tree species is established for up to several
decades (e.g., Denslow, 1985; Uhl et al., 1988; Guariguata et al., 1997). This early to
mid-successional forest may not resemble the original forest for a long time, if ever.
Restoration efforts frequently aim to recover ecosystem function as soon as
possible; therefore, usually exotic or native fast growing species are used when planting
is necessary. If exotic fast growing species are used, they may invade other natural areas
and displace native species (Fine, 2002). Native fast growing species, “pioneers”,
represent only 20 % of the diversity in the tropical forest (Gómez-Popma and VázquezYanes, 1981). This and both, high initial mortality and establishment of low-diversity
stands for decades reduce the desirability of reforestation with pioneers alone.
The objective of this thesis is to presents new criteria to choose late-successional
tropical tree species to restore biodiversity in early successional environments, based
1
2
on vegetative traits that predict species survival and growth rates. The restoration of
biodiversity and the subsequent recovery of many plant-animal interactions has been one
overlooked objectives of restoration. In the next section I present some of the general
objectives of restoration:
1.2
Restoration objectives
Restoration projects aim to start or accelerate successional process to achieve
ecological fidelity by combining i) structural replication, ii) restoration of ecosystem
function, and iii) durability in time (Higgs, 1997; Lamb, 1998). From this it follows that
the most simple restoration effort is based on the removal of the perturbation (i.e. cattle,
agriculture, logging) and the hope that natural succession progresses to create a forest
similar to the original one.
Many barriers to natural regeneration have been identified and procedures to
overcome them have been suggested (Nepstad et al., 1990; Holl, 1999; Ashton et al.,
2001). Among these barriers, dispersal limitation of deep forest species in early
successional environments is a key phenomenon that deserves more attention. A general
consequence of dispersal limitation is that secondary forest lack deep forest species for
many years. Here, “letting nature takes its course” encourages continuing random species
loss from primary forest remnants during what could be recovery of floristic and faunistic
diversity in and near forest fragments (see Janzen, 1988). A second general consequence
is that this usual process of secondary succession precludes recovery of biotic diversity
representative of either forests prior to deforestation, or of remaining fragments, for
decades.
3
Managed succession may have a variety of objectives (Parker, 1997; also Howe
1994, 1999). Restoration of gross ecosystem functions, such as material retention and
loss, energy inputs and outputs, and the outlines of food-web structure, may require only
a small subset of the 30 to 100 tree species/ ha representative of forest structure (see
Ehrenfeld and Toth, 1997; Palmer et al., 1997), but establishing methods for successfully
accelerating the recovery of diversity of mid-and late-successional trees will be necessary
for slowing the loss of diversity from remnants and restoring floristic and faunistic
interactions and dependencies. How should this be done, with passive secondary
succession, somewhat facilitated natural succession, consciously enriched succession, or
manipulated succession under exotic monocultures? These issues are reviewed in Chapter
2. Restoration efforts benefit from the knowledge of the natural dynamics in mature
forest, to study this dynamic, tropical tree species have been classified in functional
groups. This is reviewed in the following section.
1.3
Conceptual Framework
Rain forest tree species are classified into two big groups pioneer and non-
pioneers using as criterion demography as well as the requirements of seed and seedling
(Martínez-Ramos, 1985; Swaine and Whitmore, 1988). Early successional or pioneer
species have small seeds, long-distance dispersal capacity, long persistence in the seed
bank, and ability to colonize gaps within the forest. These canopy gaps receive higher
light levels than the understory, have lower humidity at the soil surface, and in some
cases a temporal release of nutrients (Bazzaz and Wayne 1994). Pioneer species are
known to respond immediately to environmental factors of canopy gaps that give them an
4
advantage over non-pioneer species in this particular habitat. These species have short
life spans (Martínez-Ramos, 1985), often senescing or dying in 15-30 years.
Non-pioneer species represent the remaining 80 % of tropical tree species
(Martínez-Ramos, 1985). Non-pioneers may germinate and establish inside the forest in
shade (Swaine and Whitmore, 1988). For this study, non-pioneer species and long-lived
species are considered as the same group of late-successional species, although there are
many exceptions in more species-rich tropical forests (Martínez-Ramos, 1985; Foster et
al., 1986). The late-successional group may be further subdivided on the basis of
maximal height of adults as emergent and canopy (tall species) and understory categories
(short species). Certain species may be exposed to less environmental heterogeneity
during most of their life cycle. For example pioneer species may germinate, establish and
reach the canopy always experiencing high light level while short statured tree species
may germinate and inhabite always the dark forest understory. On the other hand,
emergent and canopy late-sucessional species depend on eventual opening of gaps to
reach the canopy, therefore they are exposed to higher environmental heterogeneity
during their lives. The environmental conditions that species experience for the most part
of their lives is related to morphological and functional plant characteristics, for example,
leaf traits, which will be reviewed in the next section.
1.3.1. Leaf traits of tropical tree species
Late-successional tree species show substantial phenotypic plasticity (sensu
Bradshaw, 1965): they can function in a range of environments. As adults, they have sun
leaves at the top of their crown and shade leaves at the bottom of the crown. Shade
5
leaves have lower specific leaf mass (SLM; leaf dry weight/ leaf area, g m -2), lower leaf
water content (WC: fresh leaf weight-dry leaf weight/ leaf area, g m-2) and thinner leaves,
and higher stomatal density in comparison with sun leaves within an individual crown
(Popma et al., 1992; Oberbauer and Strain, 1986, Pearcy and Sims, 1994). These traits
increase whole-plant productivity by maximizing photosynthesis and minimizing loss of
water (Björkman, 1981; Bongers and Popma, 1988; Popma et al., 1992). Reduction in
leaf area and increase in leaf thickness in sun conditions alleviates heat load and
decreases loss of water (Chiariello,1984). On the other hand, shade leaves have larger
leaves for light capture and maximization of sunfleck use. How light heterogeneity, that
different species experiences through their ontogeny, affects their leaf traits is shown in
Chapter 3 for eight late-successional species with a maximal tree height ranging from 8 to
40 m.
Leaf area represents the available photosynthetic area for light harvesting events.
A minimum total leaf area on a per plant basis should be maintained at any set of
conditions to ensure survival (Kohyama, 1987). This may be accomplished through leaf
production and leaf life span (King, 1994). Short leaf life span is considered an
adaptation for rapid growth rate and drought-avoidance (Reich et al., 1991), generally
attributed to pioneer species (Coley, 1988). Under shade conditions, pioneer species are
unable to maintain their leaf area, due to short life span and lack of resources for high leaf
production. In contrast, at similar light levels, emergent and canopy species have long
leaf life span and lower leaf production (King, 1994). In Panama, survival of two herb
species with different dependence on gaps was positively related to intrinsic leaf
longevity (Mulkey et al., 1991). For 142 tropical tree species at different DBH classes
6
survival was negatively correlated with growth rates in the forest (Condit et al., 1995). It
appears that the ability to function in a range of environments might be at least as well
predicted by functional and demographic features than by physiological traits alone
(Mulkey et al., 1991), particularly in field situations where physiological work is
difficult.
Determinations of which traits predict species survival and growth in restoration
planting have been done for grassland (Pywell et al., 2003), whilet this essential
information is not available for tropical forest. Chapter 4 shows a study of the variation in
leaf traits that predict survival and growth rates of 23 late-successional species growing
in the different microhabitats of early successional ecosystems. In this plantation the
natural arrival of pioneer species lead to rapid changes in microenvironmental conditions
as it may happen in restoration projects that are located close to sources of pioneer seeds.
However, not all restoration projects will be carried out in such environments. Chapter 5
reports results from the first 17 months of 12 mid-successional and late- successional
species growing in a plantation that mimics the environmental conditions of a pasture
without natural arrival of pioneer species. In this plantation leaf traits that predict
performance were also evaluated.
Restoration projects aim to recover former forests, including the high biodiversity
typical of mature forests; consequently the planting of late-successional species is
necessary. However the lack of information about species establishment requirements
makes it easier to use few species with high growth rates and survival in early
successional environments. Determination of which trait(s) best predict(s) latesuccessional species survival in different scenarios of restoration (i.e. early successional
7
ecosystems, pastures) will obviate the need to test all tropical tree species (about 300
species at the Los Tuxtlas) individually to decide which of them to plant. Maximizing
survival per planted seedling reduces the cost of nursery maintenance and replanting in
restoration projects. By resolving which traits are better predictors of species growth rates
in adverse conditions of tropical pastures, we will minimize the time needed to regenerate
a forest of high structural and species diversity.
1.4
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Bazzaz, F. A. and Wayne, P. M. 1994. Coping with environmental heterogeneity: The
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Björkman, O. and Demmig-Adams, B. 1994. Regulation of Photosynthetic Light Energy
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Bongers, F. and J.Popma. 1988. Is exposure-related variation in leaf characteristic of
tropical rain forest adaptive? Plant form and vegetation structure (eds. M. J. A.
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Academic Publishing, The Netherlands.
Bradshaw, A. D. 1965. Evolutionary significance of phenotypic plasticity in plants.
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Press, New York, USA.
Chiariello, N. 1984. Leaf energy balance in the wet lowland tropics. Physiological
ecology of plants of the wet tropics (eds. E. Medina, H. A. Mooney and C.
Vázquez-Yanes), 85-98. Dr. Junk Publishers, The Netherlands.
8
Coley, P. D. 1988. Herbivory and defensive characteristics of tree species in a lowland
tropical forest. Ecological Monographs, 53, 209-229.
Condit, R., Hubbell, S. P. and Foster, R. B. 1995. Mortality-Rates of 205 Neotropical
Tree and Shrub Species and the Impact of a Severe Drought. Ecological
Monographs, 65, 419-439.
Denslow, J. S. 1985. Disturbance-mediated coexistence of species. The Ecology of
Natural Disturbance and patch dynamics (eds. S. T. A. Pickett and P. S. White),
307-323. Academic Press, Inc, USA.
Ehrenfeld, J. G. and Toth, L. A. 1997. Restoration ecology and the ecosystem
perspective. Restoration Ecology, 5, 307-317.
Fine, P. V. A. 2002. The invasibility of tropical forests by exotic plants. Journal of
Tropical Ecology, 18, 687-705.
Foster, R. B., J. Arce B., and T. Wachter.1986. Dispersal and the sequential plant
communities in Amazonian Peru floodplain. Frugivores and Seed Dispersal (eds.
A. Estrada and T.H. Fleming), 357-370. W. Junk Publishers, Dordrecht,
Netherlands.
Gómez-Pompa, A. and C. Vázquez-Yanes. 1981. Sucessional Studies of a rain forest in
México. Forest Sucession Concepts and Application (eds. D. C. West, H. H.
Shugart and D. B. Butkin), 246-266. Springer-Verlag, New York, USA.
Guariguata, M. R., Chazdon, R. L., Denslow, J. S., Dupuy, J. M. and Anderson, L. 1997.
Structure and floristics of secondary and old-growth forest stands in lowland
Costa Rica. Vegetation, 132, 107-120.
Higgs, E. S. 1997. What is good ecological restoration? Conservation Biology, 11, 338
-348.
Holl, K. D. 1999. Factors limiting tropical rain forest regeneration in abandoned pasture:
Seed rain, seed germination, microclimate, and soil. Biotropica, 31, 229-242.
Howe, H. F. 1994. Managing Species-Diversity in Tallgrass Prairie - Assumptions and
Implications. Conservation Biology, 8, 691-704.
Howe, H. F. 1999. Dominance, Diversity and Grazing in Tallgrass Restoration.
Ecological Restoration, 17, 59-66.
Itoh, A., Yamakura, T., Ogino, K., lee, H. S. and Ashton, P. S. 1997. Spatial distribution
patterns of two predominant emergent trees in a tropical rainforest in Sarawak,
Malaysia. Vegetation, 132, 121-136.
9
Janzen, D. H. 1988. Tropical Ecological and Biocultural Restoration. Science, 239, 243244.
King, D. A. 1994. Influence of light on the growth and morphology of saplings in a
Panamanian forest. American Journal of Botany, 81, 948-957.
Kohyama, T. 1987. Significance of architecture and allometry in saplings. Functional
Ecology, 1, 399-404.
Lamb, D. 1998. Large-scale ecological restoration of degraded tropical forest lands: The
potential role of timber plantations. Restoration Ecology, 6, 271-279.
Lovelock, C. E., Jebb, M. and Osmond, C. B. 1994. Photoinhibition and Recovery in
Tropical Plant-Species - Response to Disturbance. Oecologia, 97, 297-307.
Lugo, A. E. 1997. The apparent paradox of reestablishing species richness on degraded
lands with tree monocultures. Forest Ecology and Management, 99, 9-19.
Martínez-Ramos, M. 1985. Claros, ciclos vitales de los arboles tropicales y
regeneración natural de las selvas altas perennifolias. Investigaciones sobre la
Regeneración de selvas altas en Veracruz, México. (eds. A. Gómez-Pompa and S.
Del Amo), 191-240. Alhambra Mexicana, Mexico.
Martínez-Ramos, M. 1994. Regeneración natural y diversidad de especies arboreas en
selvas humedas. Boletin de la Sociedad Botánica de México, 54, 179-224.
Moran, E. F., Brondizio, E., Mausel, P. and Wu, Y. 1994. Integrating Amazonian
Vegetation, Land-Use, and Satellite Data. Bioscience, 44, 329-338.
Mulkey, S. S., Smith, A. P. and Wright, S. J. 1991. Comparative Life-History and
Physiology of 2 Understory Neotropical Herbs. Oecologia, 88, 263-273.
Nepstad, D., Ch.Uhl and A.E.Serrao. 1990. Surmounting barriers to forest regeneration in
abandoned highly degraded pastures: a case study from Paragominas, Pará,
Brazil. Alternatives to deforestation: steps toward sustainable use of the amazon
rain forest (ed. A. B. Anderson), 215-229. Columbia University Press, New York,
USA.
Oberbauer, S. F. and Strain, B. R. 1986. Effect of canopy position and irradiance on the
leaf physiology and morphology on Pentaclethra macroloba (Mimosaceae).
American Journal of Botany, 73, 409-416.
Palmer, M. A., Ambrose, R. F. and Poff, N. L. 1997. Ecological theory and community
restoration ecology. Restoration Ecology, 5, 291-300.
10
Parker, V. T. 1997. The scale of successional models and restoration objectives.
Restoration Ecology, 5, 301-306.
Pearcy, R. W. and Sims, D. A. 1994. Photosynthetic Acclimation to Changing Light
Environments: Scaling from the Leaf to the Whole Plant. Exploitations of
Environmental Heterogeneity by Plants. Ecophysiological Processes Above-and
Belowground (eds. M. M. Caldwell and Pearcy, R.W.), 145-173. Academic Press:
Harcourt Brace & Company, USA.
Poorter, L. 1999. Growth responses of 15 rain-forest tree species to a light gradient: the
relative importance of morphological and physiological traits. Functional
Ecology, 13, 396-410.
Popma, J. and Bongers, F. 1991. Acclimation of seedlings of three Mexican tropical rain
forest tree species to a change in light availability. Journal of Tropical Ecology, 7,
85-97.
Popma, J., Bongers, F. and Werger, J. A. 1992. Gap-dependence and leaf characteristics
of trees in a tropical lowloand rain forest in México. Oikos, 63, 207-214.
Pywell, R. F., J.M. Bullock, D.B. Roy, LIZ Warman, K.J. Walker and P. Rothery. 2003.
Plant traits as predictors of performance in ecological restoration. Journal of
Applied Ecology, 40, 65-77.
Reich, P. B., Uhl, C., Walters, M. B. and Ellsworth, D. S. 1991. Leaf Life-Span as a
Determinant of Leaf Structure and Function among 23 Amazonian Tree Species.
Oecologia, 86, 16-24.
Ricker, M. 1998. Enriching the tropical rain forest with native fruit trees: a biological and
economic analysis in Los Tuxtlas (Veracruz, Mexico). PhD. Dissertation. 262 pp.
Yale University, USA.
Swaine, M. D. and Whitmore, T. C. 1988. On the Definition of Ecological Species
Groups in Tropical Rain Forests. Vegetatio, 75, 81-86.
Uhl, C., Buschbacher, R. and Serrao, E. A. S. 1988. Abandoned Pastures in Eastern
Amazonia .1. Patterns of Plant Succession. Journal of Ecology, 76, 663-681.
Welden, C. W., Hewett, S. W., Hubbell, S. P. and Foster, R. B. 1991. Sapling Survival,
Growth, and Recruitment - Relationship to Canopy Height in a Neotropical
Forest. Ecology, 72, 35-50.
2. RESTORING TROPICAL DIVERSITY: BEATING THE TIME TAX ON
SPECIES LOSS
2. 1
Abstract
Fragmentation of tropical forest is accelerating, at the same time that already
cleared land reverts to second growth. Fragments inexorably lose deep forest species to
local extinction while embedded in low-diversity stands of early successional pioneer
trees. Pasture matrices undergoing passive secondary succession become a “pioneer
desert” from the vantage of remnant immigration, imposing a “time tax” of loss of deepforest plants from forest fragments. If seeds of deep-forest trees find pastures, or
seedlings are planted there, many prosper. Bypassing early domination of pioneer trees
in regenerating matrices, or enriching matrices with animal-dispersed forest trees, may
stem loss of species from forest fragments and accelerate succession far from edges of
old forest. Planting disperser-limited trees that establish in open ground may bypass 3070 years of species attrition in isolated remnants by attracting animals that encourage
normal processes of seed dispersal into and out of the fragments. Development of criteria
for selection of persistent, reasonably rapidly growing animal-dispersed species that are
mixed with planted or naturally-arriving pioneers will be an important component of
enrichment planting.
11
12
2. 2
Introduction
In vast areas of the tropics, forest has been displaced by crops and commercial
cattle grazing, leaving land devoid of natural vegetation and the soil seed banks, seedling
cohorts, and suppressed saplings of mature forest trees that might restore it (QuintanaAscencio et al., 1996; Miller, 1999). Often forest nuclei remain, but as fragments of a few
hectares that inexorably lose species to local extinction (Turner, 1996). Where intensive
crop production or cattle ranching is unprofitable, restoration of biological diversity in
regenerating matrices between fragments has the potential to stem the loss of species
from relict forests, and may actually facilitate restoration of natural metapopulation
dynamics. How should this be done, with passive secondary succession, somewhat
facilitated natural succession, consciously enriched succession, or manipulated
succession under exotic monocultures?
I argue that in restoration of biological diversity between forest remnants, the
vegetation matrix matters. The matrix influences rates of accumulation of organic matter
and nutrients (Lugo, 1997), and the population and community dynamics of species in the
remnants which the matrix surrounds (Vandermeer and Carvajal, 2001). Almost any
vegetation adds organic matter and nutrients, and retains water, to a greater extend than
barren land. However, loss of species from remnants may not be stemmed if land is
quickly occupied by one or a few early successional species, followed by what I call the
“pioneer desert” of early and late pioneers that retard influx of disperser-limited deepforest trees for a century or more (Finegan, 1996). If intensive land use imposes a “time
tax” of soil degradation (Lugo, 1988), the 100+ year pioneer matrix imposes another
13
“time tax” of species loss from remnants, a lost opportunity cost which may be
irredeemable.
Loss of mutualists and herbivores may accelerate plant extinctions in forest
fragments. A disproportioante share of tropical trees require insects, bats or birds for
pollination, and bats, birds, or terrestrial or arboreal mammals for seed dissemination
(Howe and Westley, 1997), and the diversity of recruiting cohorts of seedlings is
maintained by thinning by ground-foraging mammals (Dirzo and Miranda, 1991). An
immense array of ecological disruptions occurs if herbivores, predators, dispersal agents,
and pollinators lack access to forest patches for long intervals (Cordeiro and Howe, 2001;
Terborgh et al., 2001; Wright and Duber, 2001; Tewksbury et al., 2002). A matrix that
accelerates the influx of frugivores and herbivores is an overlooked but needed
component of forest regeneration.
I argue that loss of tree species continues unabated from forest remnants
embedded in a matrix of pioneer species, imposing a time tax of local extinction that will
impede future restoration efforts. A remedy is the creation of matrices enriched with
large-seeded, animal-dispersed trees which attract dispersal agents that accelerate
succession to mature forest, mediate immigration of forest species back into remnant
fragments, and augment emigration of trees of relict forests into regenerating matrices.
2. 3
Natural succession
In rainforests, natural disturbances vary in scale, intensity, and frequency, and
trigger a variety of successional processes. Most disturbances are small branchfalls and
treefalls that form canopy gaps of 50-1000 m2 and close within a few years (e.g. Fig. 1,
14
Howe, 1990), usually filled by deep-forest species already present as seeds, seedlings,
saplings, re-sprouts, or overhanging canopy trees (Brokaw and Scheiner, 1989). Even
extensive hurricane blow-downs yield to tree-species already present as suppressed plants
in the understorey or stumps capable of re-sprouting after damage (Boucher et al., 2001).
Most natural regeneration in rainforests free from human disturbance comes from
established plants, the species composition of which roughly reflects the pre-disturbance
community.
Nature can favour immense stands of early pioneer trees, but the circumstances
are limited and rare. Massive mudslides following earthquakes or volcanism are closed
by small-seeded pioneer species with high dispersal capacity (e.g. Thebaud and
Strasberg, 1997). For instance, Garwood and colleagues (1979) reported that an
earthquake in eastern Panama sloughed an entire watershed into the sea. Much like a
large anthropogenic disturbance, the exposed earth was quickly choked with saplings of
invasive bird-dispersed Trema (Ulmaceae), a common early successional tree that
produced fruits within four years. Large natural disturbances that remove vegetation over
several to hundreds of hectares involve quite different processes of succession than
simple closure of canopy gaps, or even re-vegetation after damage by wind or fire that
leaves many seeds, seedlings, and older plants alive and ready to respond to increased
light and soil resources.
2.4
Arriving and surviving in unnatural landscapes
Landscape features influence the arrival and survival of tree species after major
disturbances (e.g. Tewksbury et al., 2002). In the tropics, abandoned croplands and
15
pastures do not have seed banks of forest species, nor are there seedling or sapling
cohorts waiting to respond to opportunity. Low rates of colonization and emergence, and
high mortality of seeds and seedlings, result in low densities and diversities of tree
juveniles and saplings (Uhl et al., 1988; Nepstad et al., 1996; Zimmerman et al., 2000).
Under such conditions, dispersal becomes a limiting factor in the rate of forest
regeneration (Quintana-Ascencio et al., 1996; Holl, 1999; Miller, 1999), and the size and
distribution of remnant sources of forest seeds becomes an important determinant of seed
dispersal and seedling recruitment. Even when small pastures experience substantial seed
rain from late-successional trees in nearby mature forest, they always receive different
seed input than small gaps in within the mature rainforest (see Purata, 1986; MartínezGarza and Montagut, 1999; 2002). It is not realistic to expect early large-scale
colonization of open land by large-seeded bird, bat, or primate-dispersed tree species
even tens of meters, much less hundreds of meters, from a forest edge (e.g. see Hooper et
al., 2002; Ingle, 2003). Unsuccessful intensive farming and ranching have made such
large tracts of thoroughly disturbed land commonplace, and have coincidently made the
dispersal limitation that is characteristic of such situations the rule rather than the
exception throughout much of the Neo- and Paleotropics. Only part of the problem is
what can establish and grow under the canopy of such pioneers; much of the problem is
what can get there.
Examples from the Neotropics illustrate the issues. A few early pioneers such as
Cecropia (Moraceae [Cecropiaceae]), Croton (Euphorbiaceae), Trema (Ulmaceae), and
Vismia (Guttiferae [Clusiaceae]) hold ground for 20 - 30 years, to be replaced by such
longer-lived late pioneers as Cordia (Boraginaceae), Goupia (Goupiaceae
16
[Celastraceae]), Guazuma (Sterculiaceae), Laetia (Flacourtiaceae), Rollinia
(Annonaceae), Spondias (Anacardiaceae), Stryphnodendron (Fabaceae) and Vochysia
(Vochysiaceae) (Uhl and Jordan, 1984; Finegan, 1996; Mesquita et al., 2001). In a mix
of successional forests, species richness and diversity may approach that of mature forest
in 100 years, but species composition does not resemble mature forest; dominants of
primary forest, if present, are rare (Finegan, 1996; Aide et al., 2000). A century of revegetation after intensive grazing or farming produces forests that restore most ecosystem
function, but the new forests do not have - for many years, if ever - the same species of
trees that were present before the cow or plough. Such a “pioneer desert” does not
supply stands of remnant mature forest with propagules of deep forest species, nor
provide genetic diversity from pollen for isolated relict trees, for at least several decades.
Ecosystem function may return, but much of the biological function of a mature forest
does not.
A useful irony is that many disperser-limited deep forest species do well in open
pastures, if they get there. In Panama, Hooper and colleagues (2002) find > 70% survival
of large-seeded, shade-tolerant tree seedlings in pastures, where per-capita survival of
seedlings of pioneers is < 0.1%. In Costa Rica, seedlings of large-seeded Octoea
glaucosericea, O. whitei (Lauraceae), and Calophyllum brasiliense Cambess. (Guttiferae
[Clusiaceae]) have greater than 50% survival when planted in pastures (Loik and Holl,
1999), while this Calophyllum and deep-forest trees Virola koshnyi Warb.
(Myristicaceae), Dipteryx panamensis (Pittier) Record & Mell [D. oleifera Benth],
Pithecellobium elegans ([Albizia elegans]; Fabaceae), and Genipa americana L.
(Rubiaceae) experience 60-98 % survival when planted as seedlings in other abandoned
17
pastures (Montagnini et al., 1995). Evidence is mounting that many deep-forest species
survive in pastures.
Similar success occurs in the Old World. Hardwick and her colleagues (1997) find
that in abandoned agricultural land in northern Thailand, seedlings of animal-dispersed
Beilschmiedia spp. (Lauraceae) with large seeds (6-7 g) and Prunus cerasoides D. Don
(Rosaceae) with seeds of moderate size (0.23 g) have survival in weedy pastures of 93%
and 70%, respectively. Pioneers colonize pastures, but only because small (< 10 mg)
seeds are present in immense numbers. Far from a forest edge, even pioneer arrival may
be very slow. However, if deep-forest trees with large seeds find pastures, or are planted
there, seedlings of many species prosper.
2.5
Attrition of species from fragments in alien matrices
Forest fragments excised from continuous forest and imbedded in alien matrices
lose many species of animals and plants over 20 - 100 years (Turner, 1996). Proximity of
fragments to sources of dispersal agents influence which species are vulnerable to local
extinction in remnants. The landscape of sources, and the quality of surrounding
matrices, will likely determine which species are most vulnerable in a given area.
Very low densities of most species make tropical forest fragments especially
vulnerable to high rates of local extinction (e.g. Maina and Howe, 2000). Species number
is positively associated with size of habitat patches, while population densities of all but
the dominants are inversely correlated with richness (Preston, 1948; MacArthur, 1972).
Recent studies show that seedlings and juveniles of many rainforest species suffer
declines in fragments (Cordeiro and Howe, 2001; Githiru et al., 2002), and some island
18
communities show dramatic losses through older juvenile and sapling stages (see Leigh et
al., 1993). With adult tropical trees dying at a rate of roughly 1% per year in mature
forest (Brokaw, 1985; Sukumar et al., 1998), the less representative the matrix is of
mature forest, the more rapidly small populations of dispersal agents and trees with
reduced recruitment will be lost from remnants. Maina and Howe (2000) argue that tree
species most vulnerable to local extinction from small forest remnants are those at the
moderately abundant to rare end of the species abundance distribution that lose
pollinators or dispersal agents in small fragments, while those most likely to persist are
highly vagile weeds, augmented by successional pioneer deserts, and “always rare”
species that function as successful metapopulations.
Records from old fragments in East Africa have borne out these expectations
(Cordeiro and Howe, 2001). In the East Usambara Mountains of Tanzania, a rainforest
of largely animal-dispersed trees (23% endemic) was fragmented into <1-600 ha patches
around a remnant of 3500 ha, within a matrix of tea plantations 60-90 years old. Interior
forest bird and primate populations disappeared or were much reduced in small
fragments. Preliminary censuses showed that densities of seedlings and juveniles of 31
animal-dispersed tree species were more than three times greater in continuous forest and
in large (> 30 ha) than small (< 10 ha) forest fragments, whereas recruitment of eight
wind- and gravity-dispersed trees of the forest interior was unaffected. Recruitment of 10
endemic, animal-dispersed tree species was 40 times lower in small fragments than in
continuous forest or large fragments. Even in this system, with far fewer species than
many forests of South America or East Asia, many tree species were represented by 1-5
19
adult individuals per fragment, far fewer than necessary to maintain viable populations.
In such situations, restoration of the matrix is a race.
2.6
Restoring the matrix: beating the time tax on diversity
Restoring matrix diversity encourages natural processes of immigration and
integration among nuclei of forest remnants. One measure is planting buffers, corridors,
and stepping stone stands around and between remnants (Janzen, 1988; Lamb et al.,
1997; Tewksbury et al., 2002). Another measure after release from intensive agriculture
is to upgrade or eliminate the 100 year pioneer desert by encouraging late-successional
trees long before they would passively arrive of their own accord. This in turn should
attract vertebrate dispersal agents that accelerate the process of seed dispersal into and
out of forest fragments. A question is, are some means of encouragement more effective
than others?
In general, in forest regeneration of large areas of abandoned agricultural land or
pasture, passive succession cannot stem the loss of species from forest remnants. Isolated
trees that attract dispersal agents or artificially positioned perches that do the same
increase seed rain of animal-dispersed species (Guevara et al., 1991; Miriti, 1998), but
recruitment is slow and remains unrepresentative of mature forest (Holl, 1999). I doubt
that passive succession, or succession encouraged with perches, will effectively counter
the time tax of loss from remnants, except for edges close to mature forest. Encouraging
disperser activity in this minimal way may be more appropriate for buffering edges of
remnants (e.g., Janzen, 1988) than for bypassing the pioneer desert.
20
I suggest that beating the time tax on biodiversity is possible if successions of
pioneers are actively enriched with plantings of late-successional and deep forest animaldispersed tree species. Pioneers arrive of their own accord close to forest edges, or may
be planted far from edges in the largest deforestations. In some cases valuable timber
species may be mixed in plantings for later commercial harvest, a conservation measure
that as has been attempted in Australia (Lamb and Lawrence, 1993). I suggest that
criteria should include a mix capable of growing in xeric conditions of open ground,
capable of growing under exotic grasses, capable of establishing under the inevitable
pioneer canopy, and when mature capable of attracting animate dispersal agents that
accelerate the process. Tucker and Murphy (1997) demonstrate enhanced regeneration
of animal-dispersed species in enriched successions in tropical Queensland, where
dispersal agents and the trees that they use are far more common with plantings of latesuccessional trees than in control plots of the pioneer matrix. Criteria for selection of
those late-successional species most likely to accelerate succession to complex forests
should become an important facet of enrichment plantings.
At some sites, exotic plantation monocultures may admit deep forest species
native to surrounding forests. Lugo (1997) makes the interesting point that plantation
monocultures of some short-lived exotics cast enough shade to suppress pioneers, but
admit invasion by deep-forest species at least as well as pioneers and better than other
plantation crops. This variation on passive succession would permit a cash crop, and cost
little. Whether such a method would create unintended consequences, be a superior
strategy to enrichment of early and late pioneer stands, or simply be the only option in
regions used for plantation crops, should be a matter of debate.
21
The evidence indicates that the feasibility of using plantations of exotic
monocultures to promote late-successional indigenous species depends on the species
used and the location. In Brasil, Leucaena leucocephala (Lam.) De Wit (Fabaceae)
plantations admitted more native forest species than Casuarina plantations (Parrotta
1995). In Hawaii, plantations of Eucalyptus saligna Sm. (Myrtaceae) and Flindersia
brayleyana F. V. Muell. (Rutaceae) from Australia and Fraxinus uhdei (Wenzig)
Lingelsh (Oleaceae) from Mexico established in the 1950s and 1960s fostered very
different regeneration pathways (Harrington and Ewel, 1997). E. saligna strongly
favored exotics and F. braylenana replaced itself, while F. uhdei favoured two dominants
of surrounding mature forest, Cibotium glaucum (Sm.) Hook. and Arnott (Dicksoniaceae)
and Metrosideros polymorpha Gaud. (Myrtaceae). Various pines and eucalypts in South
Africa admitted a few common animal- and wind-dispersed forest canopy species, which
appear to represent late pioneer species (see Geldenhuys, 1997). In the Congo, eucalypt
plantations admit a number of native forest species, especially close (< 50 m) to the forest
edge, with strong representation by wind-dispersed species that show especially rapid regrowth after clear-cutting of the plantation crop (Loumeto and Huttel, 1997). With some
exceptions, such as Leucanea in Brazil and Fraxinus in Hawaii, forests developing under
plantation monocultures resemble pioneer desert produced by passive regeneration of
unnaturally extensive abandoned agricultural land, or admit even fewer species than
natural successions if exotics replace themselves.
Another option might be the planting of native monocultures or mixed stands
(Guariguata et al., 1995; Haggar et al., 1997; Murcia, 1997). Monocultures or mixed
stands of native species admit the invasion of other native species, but success also
22
depends on which species are planted and the objectives of restoration. For instance in
Costa Rica, establishment of forest trees is favored under monocultures of Vochysia
guatemalensis (Donn.Sm.) Standl. (Vochysiaseae), but plant growth is slower than under
Jacaranda copaia (Aubl.) D. Donn. (Bignoniaceae) monocultures (Guariguata et al.,
1995). In the Colombian Andes, recruitment of forest species is lower in plantations of
Alnus acuminata (Kunth) Kuntze (Betulaceae) than in the natural regenerated forest
(Murcia, 1997). As in natural successions, few of the species that recruit under the
plantations belong to the mature forest (Murcia, 1997; Haggar et al., 1997). These
planted overstorey trees are wind-dispersed, which would not draw dispersal agents as
effectively as animal-dispersed species In summary, enrichment of successional plots
with seedlings of a variety of animal-dispersed tree species would appear to be the most
feasible means of beating the time tax on species loss from remnants embedded in
secondary successions (see Tucker and Murphy, 1997). Variations on passive succession,
unattended or under overstories of exotic or native trees, may offer a means of restoring
ecosystem function, but they do not avoid the equivalent of the pioneer desert: forest
remnants remain surrounded by low-diversity matrix. Adding perches may or may not
speed succession near forest edges, and planting animal-dispersed monocultures might
accelerate attraction of birds and mammals that eat fruits and disperse other seeds in the
process. The risk in any variation of passive succession is embedding remnant forests in
alien matrices for unnecessarily long times. In our view, useful factors to consider as
criteria for enrichment plantings of late successional trees include both attributes of
growth and survival of the tree species, and their role in dispersal dynamics.
23
Not all deep-forest species can survive in xeric pasture conditions, or prosper
under thick cover of exotic grasses or exotic or native weeds. Some deep forest species
are more likely to survive in the open than others, and some species grow more rapidly
than others (e.g., Hooper et al., 2002). High mortality and very slow growth could admit
weedy herbaceous grasses and forbs, thereby setting back succession. Pioneer trees will
arrive of their own accord near forest edges (e.g., Martínez-Garza and Montagut, 1999;
2002; Ingle, 2002), but animal-dispersed pioneers such as Cecropia, Cordia, Ficus, and
Trema could be gainfully planted far (> 100 m) from source forests edges to secure soil,
provide shade, and initiate the process of frugivore assembly. Maury-Lechon (1993) has
found that growth plasticity of juvenile stages of trees is a predictor of growth rate in
secondary succession. I found that variation (coefficient of variation) in an easilymeasured leaf character, specific leaf weight, is a reasonable predictor of growth rate and
survival of deep forest trees in one five-year-old planting in southern Mexico (see
Chapter 4). Given a pool of dozens to hundreds of moderate- to large-seeded species in
the vicinity of almost any tropical forest, the high survival rate of those mature forest
species that have been planted in open pastures, and the evolving understanding of easily
detected attributes that are correlated with high growth rates and persistence, I am
confident that plant functioning will not limit enrichment.
Besides capacity for survival, species used in enrichment plantings should also
serve other purposes. Species chosen might represent rare species logged out of many
remnants, and therefore serve a conservation function (e.g., Lamb and Lawrence, 1993).
A more general tactic is to select those species that, once mature, will attract birds,
primates, bats, or other fruit-eating animals that accelerate seed dispersal of late-
24
successional species into and out of forest remnants. Because the greater majority of tree
species in many tropical forests bear fruits adapted for animal dispersal (Howe and
Westley, 1997), a wide range of species appealing to generalist and specialist species is
likely to be available, and otherwise suitable for planting as seedlings. With refined
criteria for inclusion of components of the mature forest community, Tucker and
Murphy’s (1997) approach could be the basis for a model for effective re-vegetation in
most tropical regions of the world.
2.7
Synthesis and Applications
Planting seedlings of interior forest species after land abandonment should sharply
accelerate the process of re-vegetation of complex communities. Two to 10 years may be
lost in slower growth of some trees, but decades saved in total community recovery.
Bypassing acute dispersal limitation with plantings that accelerate re-occupation of land
far from remnants by herbivorous and fruit-eating animals may subtract 30-100 years of
the time tax on diversity imposed by a low-diversity pioneer matrices. Effects of
enrichment between forest remnants will be strongest where matrices are dominated by
wind-dispersed trees, where plantation exotics self-seed easily, and in deforested areas far
(> 100 m) from forest edges. Pioneer stands or plantation monocultures may be enriched
with seeds or better with seedlings of late-successional animal-dispersed trees, or initial
plantings could be mixes of late-successional and pioneer species. Whatever enrichment
is used will almost certainly do more to beat the time tax on species loss from remnants
than passive secondary succession or minimal encouragement with perches.
25
Active enrichment of successions or plantations with a variety of animal-dispersed
species appears to be the best method of recruiting a variety of mature forest trees in and
from remnants, with some care to selection of trees bearing fruits for consumption and
dispersal by different animal guilds. Enrichment of plantations, when possible by
animal-dispersed species, has the advantage of adjusting overstorey densities enough to
suppress pioneers but not so much as to suppress mature-forest species planted
underneath. A challenge will be to establish criteria for selecting candidates for
enrichments and in some cases for overstories. The mix should include species that are
able to grow in xeric open pastures in some cases, under shade of trees or grasses in
others (e.g., Hooper et al., 2002). Species should be animal-dispersed to most effectively
harness natural processes of dissemination into and out of remnant forests, and should
represent a variety of fruit sizes and attractiveness to the birds, primates, bats, and other
arboreal and terrestrial mammals that will mediate the process.
2.8
Acknowledgments
I am grateful to N. Cordeiro, P. Fine, B. Finegan, H.F. Howe, N. Ingle, J. Klock,
G. Nuñez, S. Saha, A. Sullivan, B. Zorn-Arnold and one anonymous reviewer for
comments on the manuscript, and to the Lincoln Park Zoo Neotropic Foundation,
CONACyT of Mexico for support of research leading to these insights.
26
2.9
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30
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3. ONTOGENY OF SUN AND SHADE LEAVES OF EIGHT NONPIONEER TROPICAL TREE SPECIES
3.1
Abstract
I asked whether the ability of individual plants to adjust leaf traits during ontogeny
reflected an immediate morphological means of responding to current light availability,
or was consistent with a strategic change to meet predictable future light conditions. Leaf
size, leaf mass per unit area (SLM), leaf density, toughness and water content of eight
non-pioneer tropical tree species of different maximal height (8 to 40 m) were determined
within three ontogenetic stages (seedling, juvenile and adult). Immediate responses to
environmental conditions are reported as the mean values of leaf traits (leaf state) in sun
and shade environments and the degree of change from sun to shade environments (leaf
flexibility) while strategic changes for future light levels are reported as the correlation
between maximal height of species and the direction and magnitude of the change in leaf
traits (ontogenetic leaf variability) for the following ontogenetic transitions: from
seedlings to adults, from seedlings to juveniles and from juveniles to adults. Seedlings,
juveniles and adults of all species showed similar degree of immediate response to
environmental conditions (leaf flexibility) irrespective of their maximal height for leaf
size, SLM and toughness. Tall species showed greater change in leaf size and SLM from
seedling to adult stage than short species as might be expected of species that experience
varied light environments in life. These results show that all leaf traits change through
31
32
ontogeny, and that the magnitude and direction of this change (ontogenetic leaf
variability) is determined by species maximal height. Still, leaf traits change in respond to
current light levels (leaf flexibility) but this response is limited by current ontogenetic
stage and the future habitat of individuals as adults.
3.2. Introduction
Measurements of a variety of leaf traits of tropical tree species change during
ontogenetic development, coinciding with increases in light availability as individuals
increase in size (Coleman et al., 1994; Davies et al., 1998). Seedlings and juveniles of the
shaded understory undergo morphological and physiological adjustments when gaps
created by treefalls or branchfalls suddenly expose them to increased light levels
(Bongers et al., 1988a; Agyeman, 1999; Poorter, 2001). Plants in high light conditions
have smaller leaves with higher leaf mass per unit area (Specific leaf mass, SLM), dry
mass per unit volume (leaf density) and toughness than plants in low-light environments
(Parkhurst and Loucks, 1972; Bongers and Popma, 1988; Witkowski and Lamont, 1991;
Pearcy and Sims, 1994). Quantitative changes in leaf characters are in part responsible
for increased growth rates under higher light levels (King et al., 1997). Few studies,
however, explore the changes in leaf traits that result from the interaction of ontogeny,
current light availability and potential light availability that species are likely to
experience as adults (Thomas and Bazzaz, 1999; Rijkers et al., 2000). An open question
is whether changes in dimensions of leaf traits reflect an immediate adjustment to current
conditions, or a strategic adjustment that anticipates the future conditions likely to be
encountered during the ontogeny of a tree.
33
Plants may adjust leaf traits of photosynthetic importance to the light conditions
that individual trees experience as they grow, or changes may be strategic, increasing the
chance that individuals can adjust, if necessary, to conditions that they are likely to
experience for most of their lives. As an example of a phenotypic response to
contemporary conditions, Pearcy and Sims (1994) showed for the tropical herb Alocasia
macrorrhiza (L.) G. Don that SLM doubled in contrasting light levels (15 to 700 µmol
/m2 s ). In addition, comparative evidence suggests that tree species of different maximal
heights modulate leaf characters (magnitude and direction of change) as part of
ontogenetic development, what I term ontogenetic leaf variability. For example, in
Malaysia, juveniles of tall species (canopy and emergent) have larger leaves than
conspecific adults, while juveniles of short species (understory) have smaller leaves than
conspecific adults (Thomas and Ickes, 1995; N=51 species). Within this sample, short
species show less change in SLM from juvenile to adult than tall species (Thomas and
Bazzaz, 1999; N=28 species), perhaps reflecting the more similar light environments
shared by juveniles and adults of short species as compared with juveniles and adults of
tall species. What remains to be tested is if these and other adjustments are immediate
phenotypic responses to light environments of a given ontogenetic stages or strategic
changes to face future light environment.
Here I ask whether seedlings, juveniles and adults of eight late-successional tree
species change their leaf traits in response to immediate light level (sun or shade) or if
this response depends in the maximal height of these species that range from 8 to 40 m.
Immediate responses to environmental conditions are reported as the mean values of five
leaf traits (leaf size, SLM, leaf toughness, leaf density and water content; leaf state) and
34
the degree of change in leaf traits at contrasting leaf environments: sun and shade (leaf
flexibility), while strategic changes for future light levels are evaluated as the correlation
between maximal height of species and the direction and magnitude of the change in leaf
state for three ontogenetic transitions: from seedlings to adults, from seedlings to
juveniles and from juveniles to adults (ontogenetic leaf variability, Table I). I reason that
all forest tree species regardless of their maximal height encounter variable light levels in
their transitions from seedling to adult and are able to adjust their leaf traits to immediate
conditions. This hypothesis will be supported if all species show (1) difference in leaf
state between sun and shade leaf environments: leaves in sun conditions will show lower
leaf size and higher SLM, toughness, leaf density and water content than leaves in shade
conditions; (2) similar degree of change between contrasting leaf environments (leaf
flexibility) for all leaf traits and, (3) similar magnitude and direction of change in leaf
traits (ontogenetic leaf variability) in the three ontogenetic transitions: from seedlings to
juveniles, from juveniles to adults and from seedlings to adults, irrespective of maximal
height. Adults are expected to develop larger and heavier leaves than seedlings
(Oberbauer and Strain, 1986; Kitajima, 1994) and the degree of this change should be
similar for all species.
Alternatively, leaf state, leaf flexibility and ontogenetic leaf variability may reflect
fixed functional strategies of species, which differ by maximal height. In this scenario,
(4) ability to show differences in leaf state between leaf environments (sun and shade) for
each ontogenetic stages, (5) the degree of change between contrasting leaf environments
(leaf flexibility) and, (6) the magnitude and direction of change in the three transitions
(ontogenetic leaf variability) will depend on the maximal height of species. Taller species
35
experience a much greater range of light environments though ontogeny that goes from
the dark understory to the bright canopy. Therefore, they are expected to show higher leaf
flexibility than short species and smaller and heavier leaves at adult stage than at
seedlings stage (direction of change) (Thomas and Ickes 1995, Thomas and Bazzaz
1999), in response to increases in light levels. For short species the opposite trend is
expected, seedlings are expected to show smaller and lighter leaves than adults (direction
of change) and, the magnitude of this change is expected to be smaller than that of tall
species. Short species encounter less light variability from seedlings to adult stage,
therefore, lower leaf flexibility and less ontogenetic leaf variability are needed or are
likely to be expressed.
TABLE I
VARIABLES ASSESSED IN EIGHT TROPICAL NON-PIONEER TREE SPECIES
Variable
Definition
Leaf State
Mean of the measured leaf characteristic in a given leaf
environment (sun or shade in a given ontogenetic stage).
Leaf Flexibility
Ratios of measures of leaf traits in sun as contrasted
with shade environments within an ontogenetic stage.
Leaf state in sun environment divided by leaf state in
shade environment.
Ontogenetic Variability
Ratio of measurements among ontogenetic stages. Three
measures include: mean leaf state pooled for both
environments (sun and shade) of i) seedlings over
adults, ii) seedlings over juveniles, and iii) juveniles
over adults
36
3.3
Materials and Methods
3.3.1
Study site
This study was conducted in an experimental plantation located in the
Cooperative of Lázaro Cárdenas, and at Los Tuxtlas Biological Station (LTBS) in the
State of Veracruz, southeast Mexico (18 º 30’ N and 95º 03’ W). LTBS lies within a
reserve of 640 ha of lowland tropical rain forest that constitutes the northernmost rain
forest in the Neotropics, the Cooperative of Lázaro Cárdenas is located in the southwest
corner of the reserve. Soils are sandy loams, classified as vitric andosols (FAO/UN 1975
in Soto-Esparza, 1976). Mean annual temperature is 27º C and mean annual rainfall is
4900 mm. The dry season extends from March to May, and a rainy season from June to
February. The forest has a 35 m tall closed canopy. Nectandra ambigens (Blake) C.K.
Allen (Lauraceae) is the most common species in the canopy while Pseudolmedia
oxyphyllaria Donn. Sm. (Moraceae) and Astrocaryum mexicanum Liebm. (Palmae) are
abundant in the mid-canopy and understory respectively (Bongers et al. 1988b). Field
crops, pastures and small forest remnants surround this forest reserve.
3.3.2. Sampling
In 1999, eight non-pioneer tree species with different maximal height were chosen
from an experimental plantation created in 1997 in former pastures and secondary
vegetation close to the Cooperative of Lazaro Cárdenas (Table II). The experimental
plantation is located within a 25 ha parcel of former forest that was felled in 1978, used
as agricultural land for 4 years and for cattle ranching for 15 years. The secondary forest
has a 15 m tall canopy of pioneer species: Cecropia obtusifolia Bertol. (Moraceae),
37
Heliocarpuss appendiculatus Turcz. (Tiliaceae), Bursera simaruba (L.) Sarg.
(Burceraceae) and Cedrela odorata L. (Meliaceae). Photon flux density (PFD) was
measured in the dry season at midday (Light Meter Li-cor LI-189 quantum sensor) in
pastures and secondary vegetation. In the understory of the secondary forest,
instantaneous measurement of PFD was 22.53 ± 9.04 µmol/ m2 s (N=75; max 50 and
min.10), while in the open pasture PFD was 1947.7 ± 218.78 µmol/ m2 s (N=11; max
2227 and min 1730). Species used in this study were chosen from the experimental
plantation depending in the availability of seedlings under contrasting light levels
(pasture area and secondary vegetation) that refers to leaf environment.
TABLE II
SPECIES, AUTHORITIES AND RANGE OF STATURE OF EIGHT TROPICAL
NON-PIONEER TREE SPECIES
Species 1
Height (m)1
Family
Key
Nectandra ambigens (S.F. Blake) C.K. Allen
Lauraceae
Nect
20-40
Brosimum alicastrum Sw.
Moraceae
Bros
20-30
Calophyllum brasiliense Cambess.
Clusiaceae
Call
20-30
Pimenta dioica (L.) Merr.
Myrtaceae
Pimi
8-30
Eugenia inirebensis P.E. Sánchez
Myrtaceae
Euge
8-15
Licaria velutina van der Werff
Lauraceae
Lica
10-15
Amphitecna tuxtlensis A.H. Gentry
Pouteria rhynchocarpa T.D. Penn.
1
Bignonaceae Amph
Sapotaceae
From Ibarra-Manriquez and Sinaca (1995, 1996, 1996a)
Pout
3-10
3- 8
38
Fully expanded undamaged sun and shade leaves of the eight non-pioneer species
in three ontogenetic stages (seedling, juvenile and adult) were sampled in November
1999; six individuals at the seedling and juvenile stages and three individuals at the adult
stage of each species. Seedlings were < 1.3 cm diameter at the base and < 1.0 m high
(except Licaria velutina van der Werff, ≤ 1.21 m height), juveniles were < 3.5 cm DBH
and 2.5 m tall except Nectandra ambigens (S.F. Blake) C.K. Allen (≤ 8.9 cm DBH and 4
m tall), while adults were reproductive individuals > 3.5 cm DBH (Diameter at Breast
Height; BH=1.5 m). Paucity of smaller seedlings of Licania and Nectandra required the
larger cut-offs, which I also expect reflected reality of high growth rates in these species
since all individuals in the plantation have the same age.
Adults and juveniles of all species were located in the LTBS reserve. Ten to 20
leaves of adult trees were taken from the most exposed part of the canopy (sun leaves)
and at the very bottom of the same crown (shade leaves). Three to five leaves were taken
from each selected branch. To produce comparable leaf ages among life stages, leaves
were sampled just behind the new leaves. Juveniles were located in the understory (shade
environment) and in canopy gaps with full vertical illumination (sun environment) inside
the reserve. Measures of leaf traits were taken on these different plants to associate leaf
characters with low and high light environments (hereafter leaf environments). Ten
leaves of each juvenile individual (N=3 for each species) and five leaves of each seedling
(N=3 for each species) were sampled in each light environment (sun and shade, total N=
6 per species).
Leaves were measured within 2 hr of collection. Leaf fresh mass was measured
with a balance Pocket Pro 250-B (readability of 0.1 g) while fresh leaf size was measured
39
by drawing the leaf perimeter on paper and determining area with a Leaf area meter (Li3100, LiCor, Inc. Lincoln Nebraska USA). Leaves were oven dried to constant mass at
100 ° C and weighed to the nearest 0.01 g. With these measurements I calculated the
following leaf traits (Table III): Specific Leaf Mass (SLM; inverse of Specific Leaf Area)
is the leaf dry mass per unit fresh leaf area. Leaf Water content (WC), that is the
difference of fresh leaf mass less leaf dry mass per unit area. I also report the ratio of leaf
fresh mass over leaf dry mass often thought of as “leaf density” (Rascio et al., 1990;
Garnier and Laurent, 1994). This leaf density reflects the amount of cytoplasm versus
hemicellulose and cellulose in plant tissues. A penetrometer was constructed to measure
toughness (Choong et al. 1992). Sand could be added to a pan above a punch head of 1
mm diameter to force it down; a reading was grams of sand needed to produce failure
(Choong et al. 1992).
TABLE III
LEAF TRAITS MEASURED IN EIGHT TROPICAL TREE SPECIES IN LOS
TUXTLAS, VERACRUZ, MEXICO.
LEAF TRAITS
DEFINITION OR FORMULA
REFERENCES
LEAF SIZE
Fresh leaf lamina projection and petiole
Westoby 1998,
Weiher 1999
SLM
Dry mass of the leaf in relation with its area (g m -2)
Reich et al 1992
DENSITY
Dry mass to saturated leaf mass ratio
Garnier and Laurent 1994
TOUGHNESS
The grams of sand needed to make a hole of 1 mm
Choong et al. 1992
diameter through a leaf (g)
WATER
CONTENT
Fresh mass – dry mass /leaf area (g m -2)
Popma et al. 1992
40
3.3.3. Data analysis
To test for the effect of species, leaf environment and ontogenetic stage in leaf
traits (leaf size, SLM, leaf density, toughness and water content) multivariate analysis of
variance (MANOVA) was used. The mean of each leaf characteristic for 5-20 leaves for
each individual was used in all analyses. To calculate leaf flexibility (the ratio of leaf
state in sun divided by that in shade) three pairs of individuals for each ontogenetic stage
for species were used. To test for the effect of species and ontogenetic stage on leaf
flexibility of leaf size, SLM, leaf density, toughness and water content, MANOVA was
also used. To test differences within ontogenetic stages for leaf state or flexibility Tukey
post hoc comparisons were used. Leaf state and leaf flexibility for all leaf traits were logtransformed to satisfy MANOVA assumptions. The mean leaf state from both leaf
environments (sun and shade) of six individuals for each ontogenetic stage and for each
species was used in the calculations of ontogenetic variability for three transitions: 1)
from seedlings to adults, 2) from seedlings to juveniles, and 3) from juveniles to adults.
To test the association of these three ratios with the maximal height of species, Spearman
rank correlations were performed. Finally, leaf state from both leaf environments (sun
and shade) and leaf flexibility for each species was correlated with the maximal height of
species. Species are referred by genus only. Means are accompanied of standard errors
trough all. All test were performed with STATISTICA 5.1 (StatSoft, 1998).
41
3.4
Results
3.4.1
Effects of species and ontogenetic stage on leaf traits
3.4.1.1. Leaf state
The mean leaf size for the eight species, at both leaf environment and for the three
ontogenetic stages was 51.59 ± 3.1 cm2, mean SLM was 76.49 ± 2.2 g/m2, mean leaf
density was 0.46 ± 0.01, mean toughness was 120.4 ± 2.0 g and mean water content was
98.7 ± 3.3 g/m2. MANOVA showed that species, ontogenetic stage and leaf environment
had large effects on leaf traits: the interaction of species, ontogenetic stage and leaf
environment was also significant (Table IV).
TABLE IV
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE OF LEAF TRAITS
MEASURED IN EIGHT TROPICAL TREE SPECIES IN LOS TUXTLAS,
VERACRUZ, MEXICO
MAIN FACTOR
DF 1
P<
WILKS ‘ LAMBDA
RAO ‘S
Species
0.01
24.2
35, 480 0.00001
Ontogenetic Stages
0.37
13.4
10, 480 0.00001
Leaf Environment
0.75
6.7
5, 480 0.00005
Species * Ontogenetic Stage
0.18
3.1
70, 480 0.00001
Species * Leaf Env
0.50
2.3
35,480 0.00010
Ontogenetic S * Leaf Env
0.87
1.4
10,480 0.23000
Species* Ontogenetic S * Leaf E
0.41
1.5
70,480 0.01000
1
Note that the degrees of freedom for MANOVA are multiplied for the number of
dependent variables used, in this case, five variables.
42
The univariate test at species level showed significant differences in all leaf traits
among species. Leaf size ranged from 31.45 cm2 (Pouteria) to 144.51 cm2 (Licaria) (F 7,
96=
56.16, P<< 0.00001); SLM ranged from 54.86 (Amphitecna) to 102.22 (Pimenta) (F 7,
96=
23.75, P<< 0.00001); Leaf density ranged from 0.35 (Calophyllum) to 0.61 (Pouteria)
(F 7, 96= 27.31, P<< 0.00001); toughness ranged from 98.67 (Brosimum) to 141.5
(Amphitecna) (F 7, 96= 13.61, P<< 0.00001); water content ranged from 51.63 (Pouteria)
to 129.81 (Pimenta) (F 7, 96= 25.65, P<< 0.00001). Tables XVI-XX in Appendices A-E
show leaf traits per species, ontogenetic stage and leaf environment.
Ontogenetic stages differed substantially in leaf traits. Adults showed from 1.1 to
1.4 times higher SLM, toughness, and water content than seedlings, while juveniles were
intermediate. Juveniles showed 1.2 times higher leaf area than adults and seedlings.
Seedlings showed the highest leaf density, while adults and juveniles showed similar
values of leaf density (Table V).
Overall, sun leaves were significantly tougher, with higher SLM and water
content than shade leaves, while leaf size and density were similar in both leaf
environments (Table VI).
43
TABLE V
UNIVARIATE ANALYSIS OF VARIANCE OF LEAF TRAITS AT EACH
ONTOGENETIC STAGE OF EIGHT TROPICAL TREE SPECIES IN LOS TUXTLAS,
VERACRUZ, MEXICO.
ONTOGENETIC STAGE 1, 2
LEAF TRAITS
F (2, 96)
LEAF SIZE (cm2)
8.18***
46.4 ± 5.2 ac
59.9 ± 5.6 b
51.5 ± 5.1 a
SLM (g m-2)
36.48****
64.8 ± 2.5 c
72.3 ± 4.1 bc
89.9 ± 3.6 a
DENSITY
4.67**
0.4 ± 0.1 a
0.5 ± 0.1 a
113.3 ± 3.6 bc
117.9 ± 3.8 b
128.6 ± 2.7 a
79.4 ± 5.1 c
97.1 ± 6.4 b
116.2 ± 4.3 a
TOUGHNESS (g) 8.69***
-2
WC (g m )
23.77****
SEEDLINGS
JUVENILES
0.5 ± 0.1 b
ADULTS
1
Means ± standard errors (SE) are reported.
Different superscripts within a row indicate that means are significantly different with a
post hoc Tukey test. ** P < 0.01, *** P < 0.005, **** P < 0.0001
2
TABLE VI
UNIVARIATE ANALYSIS OF VARIANCE OF LEAF TRAITS FOR EACH LEAF
ENVIRONMENT OF EIGHT TROPICAL TREE SPECIES IN LOS TUXTLAS,
VERACRUZ, MEXICO
LEAF ENVIRONMENT 1
LEAF TRAITS
LEAF SIZE (cm2)
SLM (g m-2)
F (1, 109)
0.25
30.47****
SUN
SHADE
52.9 ± 5.2
50.7 ± 3.6
85.2 ± 3.6
68.9 ± 2.3
0.5 ± 0.1
0.5 ± 0.1
DENSITY
1.90
TOUGHNESS (g)
8.32***
125.4 ± 2.8
116.3 ± 2.9
WC (g m-2)
8.22***
104.5 ± 5.3
93.3 ± 3.9
1
Means ± standard errors are reported. Analyses were performed on Log transformed
data.
*** P < 0.005, **** P < 0.0001
44
The significant interaction of species and ontogenetic stage revealed the
differences in the magnitude and direction of the ontogenetic change in leaf traits at the
species level (see ontogenetic leaf variability below). The significant interaction of
species and leaf environment revealed that leaves of Pouteria showed significantly higher
leaf density in sun environment and that this pattern was reversed for Amphitecna that
showed significantly higher leaf density in shade environment. Pimenta showed
significantly higher SLM in sun than those in shade. All species showed similar leaf
toughness, leaf size and water content in sun and shade leaf environments. The
interaction of ontogenetic stage and leaf environment was not significant. No correlations
were found among leaf state and the maximal height of species. No correlations were
found among mean leaf state for both leaf environments (sun and shade) at all
ontogenetic stages and the maximal height of species. However, when the tallest species
(Nectandra ambigens) was excluded, leaf density and maximal height of species were
negatively correlated (Spearman rs = - 0.85, P <0.01).
3.4.1.2
Leaf Flexibility.
MANOVA showed that species and ontogenetic stage showed significant
differences in the flexibility of all leaf traits (Table VII). The univariate test at the species
level showed significant differences in the leaf flexibility of all leaf traits among species
(Table XXI, Appendix F). No correlations were found among flexibility in leaf traits and
the maximal height of species.
45
TABLE VII
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE OF LEAF
FLEXIBILITIES MEASURED IN EIGHT TROPICAL TREE SPECIES IN LOS
TUXTLAS, VERACRUZ, MEXICO
WILKS ‘ LAMBDA
RAO ‘S
DF 1
P<
Species
0.24
4.20
35, 240
.00001
Ontogenetic Stages
0.37
13.40
10, 240
.00001
Species * Ontogenetic Stage
0.18
3.11
35, 240
.00001
MAIN FACTOR
1
Note that the degrees of freedom for MANOVA are multiplied for the number of
dependent variables used, in this case, five variables.
Univariate test for ontogenetic stages showed that the flexibility in leaf density
and water content were significantly different at each ontogenetic stage. Adults showed
significantly higher flexibility in leaf density than juveniles and seedlings and lower
flexibility in water content than seedlings (Table VIII).
The interaction of species and ontogenetic stage was significant. This reflected
differences in leaf flexibility for two species: seedlings of Amphitecna showed
significantly lower flexibility in leaf density than conspecific adults (Tukey pos hoc P <
0.005), while juveniles of Pimenta showed higher flexibility in SLM than conspecific
adults (Tukey post hoc P < 0.05). No correlations were found between leaf flexibility and
the maximal height of species.
46
TABLE VIII
UNIVARIATE ANALYSIS OF VARIANCE OF LEAF FLEXIBILITY FOR EACH
ONTOGENETIC STAGE OF EIGHT TROPICAL TREE SPECIES IN LOS TUXTLAS,
VERACRUZ, MEXICO.
ONTOGENETIC STAGE 1, 2
LEAF FLEXIBILITY
F (2, 48)
SEEDLINGS
JUVENILES
ADULTS
LEAF SIZE
2.93
1.19 ± 0.14
1.12 ± 0.10
0.87 ± 0.06
SLM
1.68
1.19 ± 0.07
1.28 ± 0.11
1.24 ± 0.04
DENSITY
3.60*
1.05 ± 0.07b
1.03 ± 0.04b
1.13 ± 0.03a
TOUGHNESS
0.34
1.17 ± 0.09
1.12 ± 0.06
1.06 ± 0.02
WC
3.59*
1.34 ± 0.18b
1.26 ± 0.11ab
1.03 ± 0.04a
1
Means ± standard errors (SE) are reported.
Different superscripts within a row indicate that means are significantly different with a
post hoc Tukey test.
** P < 0.01, *** P < 0.005, **** P < 0.0001.
2
3.4.2
Ontogenetic leaf variability and maximal tree height
Ontogenetic variability in leaf size from juveniles to adults was highly correlated
with maximal tree height (Spearman rank correlation rs = 0.92, P < 0.005; Figure 1A).
The ontogenetic variability in leaf size from juveniles to adults was greater for tall
species than for short species. Ontogenetic variability of SLM from seedling to juveniles
was negatively correlated with maximal tree height (Spearman rank correlation rs = 0.75, P < 0.05; Figure 1B), as it was ontogenetic variability of SLM from seedling to
adults and the maximal tree height (Spearman rank correlation rs = - 0.92, P < 0.001;
47
Figure 1C). The ontogenetic variability of SLM from seedlings to juveniles and from
seedlings to adults is greater for tall specie (ratios far from one) than for short species.
The transition among ontogenetic stages for leaf toughness, leaf density and water
content were not correlated to the maximal tree height.
48
Figure 1. Correlation between ontogenetic leaf variability and the maximal height of
species for eight non-pioneer tropical tree species from Los Tuxtlas, Veracruz,
Mexico. A) Leaf size from juveniles to adults, B) SLM from seedlings to
juveniles, C) SLM from seedlings to adults. Spearman Rank correlation was
performed with the ratio of leaf trait between ontogenetic stages and maximal
height of species transformed into ranks. Ratios closer to 1 refer to small change
(magnitude) in mean leaf traits between ontogenetic stages. Ratios over 1 refer to
early ontogenetic stages showing higher mean leaf trait than conspecific adults
(direction of change). The key for the species follows Table II.
49
Ratio of leaf size of juveniles / leaf size of adults
A)
2.4
2.2
rs = 0.92
P < 0.005
Nect
2.0
1.8
1.6
Bros
1.4
Pimi
1.2
Euge
1.0
0.8
PoutAmph
Call
Lica
10
20
30
40
50
Species Maximal Height (m)
B)
1.04
SLM of seedlings/ SLM juveniles
1.00
Pout
Amph
Euge
Bros
0.96
rs= - 0.75
P < 0.05
Lica
Call
0.92
0.88
0.84
Nect
0.80
0.76
0.72
Pimi
10
20
30
Species Maximal Height (m)
40
50
50
C)
Ratio of SLM of seedlings / SLM of adults
1.00
rs = - 0.92
P < 0.001
0.96
0.92
0.88
Pout
0.84
Amph
0.80
Lica
0.76
Bros
Euge
0.72
Pimi
0.68
Call
Nect
0.64
5
10
15
20
25
30
Species Maximal Height (m)
35
40
45
51
3.5.
Discussion
The ability of tropical tree species to adjust functional leaf characteristics to
different light levels is widely recognized (Popma and Bongers, 1991; Popma et al.,
1992; King, 1994; Still, 1996). However, their capacity for changing leaf traits during
ontogeny has been less studied (Sterck and Bongers, 2001). These results show that leaf
traits differ at each ontogenetic stage, and that the magnitude and direction of this change
(ontogenetic leaf variability) depends on species maximal height. The limits within which
individuals change their leaf traits due to contemporary light levels (leaf flexibility) may
be set by current ontogenetic stage and the future habitat of individuals as adults.
Individuals of all tree species are overtopped and released many times before they
reach their maximal height (Whitmore, 1996), therefore similar leaf flexibilities at all
ontogenetic stages support that they adjust leaf traits to contrasting light levels at early
ontogenetic stages to respond to gaps in the canopy and at adult stage to cope with the
heterogeneity in light levels from the bottom to the top of the canopy (vertical
heterogeneity).
Ontogenetic constraints in carbon allocation limit seedlings to have large and
heavy leaves, like adults (Oberbauer and Strain, 1986; Kitajima, 1994). According with
this, in this study, seedlings showed 1.4 times lower SLM than adults. However,
seedlings showed higher leaf density than juveniles and adults. Leaf density represents
the amount of cytoplasm relative to the amount of cell wall material. Under water stress
hemicelluloses accumulates, thereby increasing leaf density and the water-holding
capacity of leaves (Rascio et al., 1990; Garnier and Laurent, 1994). Seedlings in this
52
study might have experienced higher water stress than juveniles and adults due to the
conditions in the experimental planting.
On the other hand, seedlings may have intrinsic high leaf densities that allow them
to tolerate low water availability. For example, in a study in Singapore, it was shown that
seedlings of three species were able to tolerate low soil water availability when grown in
pots under low light availability (Burslem, 1996) while in open areas in Costa Rica
seedlings of 16 tree species were not moisture-limited (Holl, 1999). Seedlings of nopioneer species that are usually large and show low growth rates, may have an
intrinsically high water-holding capacity that may allow them to survive the low humidity
conditions of gaps inside the forest or in pastures.
Leaf density was negatively associated with maximal height of species when the
tallest species Nectandra was excluded. In this scenario, short species had higher leaf
density than tall species. Shade-tolerant species may tolerant dry conditions (Nepstad et
al., 1990; Hardwick et al., 1997) probably because they allocate more resources to root
than to aboveground biomass. The high leaf density of short species may contribute to
this drough-tolerance.
Ontogenetic leaf variability was related to the maximal height of species. Tall
species show higher ontogenetic leaf variability than short species. Short species
germinate and establish inside the forest, the environment they inhabit as adults is similar
to the environment that they experience as seedlings or juveniles. Tall species inhabit the
forest understory as seedlings, but occupy an increased bright environment as adults.
Hence, their leaf size and SLM change more from seedling to adult to fill their adult
niche. These results are supported by other studies in Malaysia (Thomas and Bazzaz,
53
1999; Thomas and Ickes, 1995). Besides, other traits not measured here like allometry
and mechanical design were also related to species maximal height for three species in
French Guiana (Sterck and Bongers, 1998).
In conclusion, those species that inhabit the understory all of their lives show high
leaf density related to water-holding capacity and lower ability of changing leaf traits
through ontogeny (ontogenetic leaf variability) than those species that inhabit the canopy.
Tall species show higher ontogenetic variability in SLM and leaf size from early to late
ontogenetic stages. High ontogenetic variability in leaf traits allows tall species to endure
the changes in light and water availability on their way to the canopy.
Variability in leaf traits has implications for restoration and forest regeneration.
Leaf flexibility and ontogenetic leaf variability may help to predict which forest species
perform best in habitats outside the forest, and therefore which are best suited for
restoration projects. For instance, if high flexibility in SLM is associated with high
growth rates and survival in early successional environments, species in other forests
(Reich et al., 1999) with high SLM or high flexibility in SLM may be better candidates
for restoring forest diversity than either a random pick of forest plants, or short-lived
pioneers (see Chapter 2). These traits offer easily measured variables that may provide
criteria for selection of species for planting mixed species stands.
3.6
Acknowledgment
I thank the staff of the Los Tuxtlas Biological Station, J. Nuñez from the Institute
of Ecology (UNAM), and R. Bye from the Botanical Garden (UNAM) for their support. I
am grateful to N. Cordeiro, P. Fine, J. Fornoni, N. Ingle, M. Jorge, J. Klock, S. Russo, S.
54
Saha, A. Sullivan, B. Zorn-Arnold and two anonymous reviewers for comments on the
manuscript. CONACyT of Mexico and the Lincoln Park Zoo of Chicago supported this
study.
3.7
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4. RESTORING TROPICAL BIODIVERSITY: PREDICTING SURVIVAL AND
GROWTH OF LATE-SUCCESSIONAL TREE SPECIES IN EARLY
SUCCESSIONAL ENVIRONMENTS
4.1
Abstract
Natural succession after abandonment of degraded land often results in a low
diversity secondary forest that may persist for decades. Planting of late-successional
species in early successional environments may help to bypass this low diversity stage.
Early successional environments include microhabitats that range from the shaded
understory of a secondary forest to sunny abandoned land with no tree canopy. To
identify which plant traits will predict survival and growth rates of late-successional
species growing in early successional environments I evaluated morphological and
functional leaf traits and maximal height of 24 tropical tree species that grow in an early
successional environments close to Los Tuxtlas Biological Station in Veracruz, Southeast
Mexico. I measured the intraspecific variation in leaf traits across these microhabitats to
predict survival and growth rates. Species with high intraspecific variation in leaf mass
per unit area (SLM) showed better performance as judged by high survival and growth
rates in height and basal diameter in early successional environments. Tall species
showed higher intraspecific variation in SLM, yet no correlation was found between
maximal stature of species and performance. Variation in SLM may be predicted by
maximal stature. Further, variation in SLM will enable identification of species most
appropriate to increase biodiversity in early successional environments.
58
59
4.2
Introduction
Large areas of forest are now being lost to agriculture or cattle ranching, while
remaining fragments of forest show a reduction in biodiversity (Turner, 1996). At the
same time, tens of thousands of hectares of denuded land are abandoned annually to
succession back to forest (Moran et al., 1994). Early successional environments resulting
from agriculture or cattle ranching progress back to forest very slowly because of the low
arrival of forest seeds, and subsequent low plant colonization and establishment rates
(Whitmore, 1989; Finegan, 1996). In large deforested areas, trees and shrubs that do
arrive on their own are early successional pioneer species.
To speed up succession, commercial tree plantations are increasingly used as
synthetic forest matrices (Lugo, 1997; Lamb, 1998; Parrotta and Knowles, 1999). The
input of seeds of native species to plantations is higher than to pastures or agricultural
lands; many seeds germinate and establish in the understories of plantations, eventually
increasing the canopy biodiversity at these sites where immigrants are allowed to mature
(Lugo, 1992, 1997). Plantations of few species and new forests under plantations
canopies are enough to stop erosion, but these depauperate communities do not resemble
the former forest for many years, if ever.
The rate of forest regeneration depends partly on the species that arrive on their
own or are planted. Where time is at a premium, native early successional trees with high
growth rates are often used (e.g. 5 m per year for Cecropia obstusifolia, Gómez-Pompa
and Vazquez-Yanes, 1981; see Whitmore, 1989). In the tropics this amounts to
encouraging occupation of large areas with a small proportion (< 20%) of forest biota that
is virtually certain to arrive anyway (e.g. Martínez-Garza and Montagut, 1999). Late-
60
successional species provide much of the structural diversity in the mature forest, as well
as food resources for fruit- and seed-eating animals (see Welden et al., 1991; MartínezRamos, 1994). Planting late-successional species that are so dispersal-limited that they do
not arrive for a long time, if ever, is a preferable reforestation tactic than to reliance on a
low-diversity pioneer matrix (see Chapter 2). To establish, a species-rich and structurally
diverse forest, over a shorter time frame than by natural means, the planting of latesuccessional species in early successional habitats is a valuable option. What is unknown
is which late-successional species are able to endure the variable abiotic conditions of
early successional environments.
A number of studies evaluate the survival and growth rates of tropical tree species
in early successional habitats (i.e., abandoned pastures; Montagnini et al., 1995; Haggar
et al., 1998; Loik and Holl, 1999; Leopold et al., 2001; Hooper et al., 2002). Given the
high biodiversity in tropical ecosystems, it is impractical to hope to test more than a small
fraction of individual species under conditions common in regenerating agricultural
lands. One approach is to determine vegetative traits that predict success in survival and
growth of trees under the stressful conditions of open pasture or recently abandoned
cropland, and then use those traits as criteria for selection of species to enrich or
dominate forest restorations.
Trade-offs between species leaf traits (leaf size, photosynthetic capacity) and leaf
longevity result in different growth rates. Species with big leaves and high photosynthetic
capacity have high growth rates but low leaf longevity (Reich et al., 1999).
Morphological and functional leaf traits that affect growth rates are brought together in
the dry leaf weight per unit leaf area (Specific Leaf Mass; SLM). SLM is negatively
61
related to growth rates (e.g. Grime et al., 1997; Reich et al., 1998; Westoby, 1998). In
general, those species with larger leaves and low SLM show higher growth rates than
species with smaller leaves and high SLM. SLM also varies within a species. Plants in
high light conditions have smaller leaves with higher leaf mass per unit area (Specific
leaf mass, SLM), dry mass per unit volume (leaf density) and toughness than plants in
low-light environments (Parkhurst and Loucks, 1972; Bongers and Popma, 1988;
Witkowski and Lamont, 1991; Pearcy and Sims, 1994). Quantitative changes in leaf
characters are in part responsible for growth rates under different light levels (King et al.,
1997). I hypothesize that the variability of leaf traits, such as leaf size, SLM, leaf density
and water content reflects the ability of a species to adjust leaf traits to different
microhabitats of an early successional environment, and therefore should predict their
survival and growth rates across those microhabitats.
Variability in leaf traits should also correlate with maximal tree height. Tall
species experience lower light levels as seedlings or juveniles, but higher light levels
when they reach the canopy. Further they experience higher heterogeneity in light levels
within their crown than short species spending most of their lives in the shaded
understory (Thomas and Bazzaz, 1999; see Chapter 3). For tall tree species, labile leaf
traits (i.e., leaf size, SLM, leaf density and leaf water content) may provide the functional
means of adjusting easily to the changing environmental conditions of early successional
environments. I asked if the intraspecific variation in leaf traits of late-successional
species, measured as the coefficient of variation (CV) of leaf traits, across different
microhabitats of early successional environments (i.e. pastures, edge and secondary
62
forest), can predict species performance (i.e. survival and growth rates), and if this
intraspecific variation is related to the maximal height of species.
4.3
Methods
4.3.1
Study site
This study was conducted in a large experimental planting in the Cooperative of
Lázaro Cárdenas at approximately 6 km from Los Tuxtlas Biological Station (LTBS) in
the state of Veracruz, southeast Mexico (18 º 30’ and 18º 40’ N, 95º 03’ and 95º 10’ W).
The LTBS lies within a reserve of 640 ha of lowland tropical rain forest that is the
northernmost rain forest in the neotropics. The forest has a closed canopy about 35 m
high. Nectandra ambigens (Blake) C.K. Allen (Lauraceae) is the most common species in
the canopy while Pseudolmedia oxyphyllaria Donn. Sm. (Moraceae) and Astrocaryum
mexicanum Liebm. (Arecaceae) are abundant in the mid-canopy and understory,
respectively (Bongers et al., 1988). Soil is sandy loam classified as vitric andosols
(FAO/UN 1975 in Soto-Esparza, 1976). Annual mean maximum temperature and mean
annual rainfall are 28º C and 4500 mm, respectively. A dry season extends from March to
May, and a rainy season from June to February.
4.3.2
Land use history and Experimental Planting
The study area is located within a 25 ha parcel of former forest land that was
deforested in 1968, and used as crop land for 4 years and for cattle ranching for 15 years.
It has been undergoing natural regeneration since abandonment in 1987. This early
successional environment has three distinct microhabitats: (1) secondary forest with a 15
63
m tall canopy of pioneer species: Cecropia obtusifolia Bertol. (Moraceae), Heliocarpus
appendiculatus Turcz. (Tiliaceae), Bursera simaruba (L.) Sarg. (Burseraceae) and
Cedrela odorata L. (Meliaceae); (2) open area of approximately 3 ha remains covered
with the exotic grass Cynodon plectostachyus (K. Schum.) Pilg. up to 1.5 m high in the
wet season; and (3) low and broken canopy of 2 to 4 m.
In August-December 1996, seeds of 45 tropical species of all life forms were
collected from the LTBS and germinated (100 individuals per species, on average; total
of N= 5000 individuals, Table XXII, Appendix G) under shade in a nursery. During
January-March 1997, a grid of 5000 squares of 2 X 2 m of area covering the field was
marked, including each of the designated microhabitats of the early successional
environment. Seedlings approximately 4 months old were planted as mixed stands, one
seedling in the middle of each square.
The microhabitat that each experimental individual inhabited was described with
respect to crown illumination index (Table IX; see Dawkins and Field, 1978 in Clark and
Clark, 1992). This index goes from 1 to 5, with 1 representing the dark understory of the
secondary forest (no direct light reaching individual) and 5 the sunny pasture (individuals
totally exposed to light). In addition, light levels (Photon Flux Density, PFD) and soil
characteristics (i.e. soil moisture and bulk density) were measured in the different levels
of crown illumination index (microhabitats) for a sub-sample of individuals. Photon-flux
density was measured with a Light Meter Li-cor LI-189 quantum sensor. Gravimetric soil
moisture and bulk density were measured following Chapman (1976). Bulk density
estimates soil compaction. Photon-flux density and gravimetric soil moisture were
64
significantly different at the different levels of crown illumination index while soil bulk
density was not (Table IX).
TABLE IX
PHOTON FLUX DENSITY (PFD), GRAVIMETRIC SOIL MOISTURE AND BULK
DENSITY AT DIFFERENT LEVELS OF SEEDLINGS CROWN ILLUMINATION
INDEX.
CROWN ILLUMINATION INDEX
PFD 1
(µmol /m2 s)
Soil Moisture 2 BulkDensity2
(ml/g)
(g/cm3)
1 No direct light
20
0.45 ± 0.01 a 3
0.67 ± 0.02
2 Lit from the side
25
0.45 ± 0.02 a
0.66 ± 0.01
3 Partial vertical illumination (10-90 %)
33
0.42 ± 0.01ab
0.67 ± 0.02
4 Full vertical illumination
80
0.44 ± 0.01ab
0.67 ± 0.01
1730
0.40 ± 0.01 b
0.66 ± 0.01
5 Crown fully exposed
1
Median, N=500
Mean ± SE, N=120
3
Different letters after mean ± SE indicate significant differences at P < 0.05 tested with
a Tukey HSD post-hoc test.
2
Twenty-four tree species from 15 families were used to represent the variety of
fruit types and maximal heights of late-successional trees in the area (Table X). Maximal
height is the tallest published stature for adults of a given species in the LTBS (IbarraManríquez and Sinaca, 1995, 1996, 1996a). To calculate growth rates, seedling heights
and diameters at the stem base were measured on April 1998, October 1998, April 1999
and April 2001. Grasses and herbs were removed 50 cm around individuals at the time of
65
measurement, but the canopy over each experimental plant was left untouched.
Increments of growth rates in heights (height t2-height t1/ time) and in diameter at the
stem base (hereafter diameter) were calculated for the three periods between censuses.
The survival rate for the species was calculated as the number of individuals surviving
from 1997 to 2001, divided by the number of individuals present in 1997. Seven species
that experience some losses of seedlings during a small accidental fire in 1998 were
omitted from the analysis of survival.
To measure the intraspecific variation in leaf traits, three leaves from one
individual per species in each microhabitat for a total of 5 individuals per species were
taken. For those species with compound leaves, one leaflet at the same position was taken
from three leaves. Leaves were taken from different branches sampled just behind the
new leaves to work with comparable leaf ages. Leaf size (leaf area meter: Ci-202, CID,
Inc. Camas, WA, USA) and leaf fresh weight (FW; balance Pocket Pro 250-B; readability
of 0.1 g) were measured within 2 hours of collection. Leaves were oven dried to constant
mass at 100 ° C and weighed to the nearest 0.01 g. Leaf mass per unit area [SLM= (DW/
LS)] was calculated from leaf dry weight (DW), and leaf size (LS). Leaf density [Leaf
density= FW / DW] as measured in this study, reflects the amount of cytoplasm versus
hemicellulose and cellulose in plant tissues (Rascio et al., 1990; Garnier and Laurent,
1994). Leaf water content [WC=FW-DW/LS] was calculated as the difference between
FW and DW per unit leaf area (LS). The intraspecific variation for each leaf trait is
reported as its coefficient of variation (hereafter CV) = Standard Deviation of given leaf
trait * 100 / Mean of given trait across all microhabitats, and it was corrected for sample
size (Sokal and Rohlf, 2003).
66
4.3.3
Data Analysis
Linear regressions were performed for survival and increments in height and in
diameter on the intraspecific variation for each leaf trait (CV of leaf size, SLM, leaf
density and leaf water content). The mean increment for species in the three periods of
time between censuses and across all habitats was used for regressions. Increments in
height and diameter were log transformed to satisfy regression assumptions. No multiple
regressions were performed with the four variables due to the high correlation among
them (Sokal and Rohlf 1981; Table XI). All statistical analyses were performed in Systat
9.0.
67
TABLE X
FAMILY, FRUIT TYPE AND RANGE OF HEIGHT OF 23 LATE-SUCCESSIONAL
TROPICAL TREE SPECIES
Ulmaceae
Amho
Bignoniaceae
Amtu
Clusiaceae
Cabr
Bombacaceae
Cepe
Sapotaceae
Chve
Mimosaceae
Coar
Boraginaceae
Come
Boraginaceae
Cost
Chrysobalanaceae Copo
Myrtaceae
Euin
Meliaceae
Gugr
Chrysobalanaceae Hitr
Mimosaceae
Insi
Lauraceae
Live
Fabaceae
Locr
Lauraceae
Neam
Lauraceae
Pesc
Myrtaceae
Pidi
Moraceae
Poar
Sapotaceae
Porh
Green Drupes
Green Berry
Green Drupes
Brown Capsules
Brown spherical Berry
Red Legume
Brown drupes
Red Drupes
Orange Drupes
Yellow Drupes
Brown or Orange Capsule
Purple Berries
Hairy Brown Legume
Black Drupes with Red cap
Black legume
Black Drupes with Red cap
Green Drupes
Black Berry
Brown greenish multifruit
Yellow Drupes
HEIGH2
(M)
15-30
3-10
20-30
20-40
5-20
15-25
20-35
10-25
15-25
8-15
20-30
15-20
6-20
10-15
15-25
20-40
12-20
8-30
20-40
3-8
Clusiaceae
Rhed
Sapindus saponaria
Sapindaceae
Sasa
Trichilia havanensis
Meliaceae
Trha
Virola guatemalensis
Myristicaceae
Vigu
1, 2
From Ibarra-Manriquez and Sinaca (1995, 1996, 1996a)
Yellow Berry
Green Berry
Green Capsule
Capsule with arrillate seed
5-15
20-30
6-10
20-30
SPECIES
FAMILY
Ampelocera hottlei
Amphitecna tuxtlensis
Calophyllum brasiliense
Ceiba petandra
Chrysophyllum venezuelanense
Cojoba arborea
Cordia megalantha
Cordia stellifera
Couepia polyandra
Eugenia inirebensis
Guarea grandifolia
Hirtella triandra
Inga sinacae
Licaria velutina
Lonchocarpus cruentus
Nectandra ambigens
Persea schiedeana
Pimenta dioica
Poulsenia armata
Pouteria rhynchocarpa
Rheedia edulis
KEY
[Garcinia intermedia]
FRUIT TYPE 1
TABLE XI
CORRELATIONS AMONG LEAF TRAITS 1,2
CV of SLM
CV of Leaf size CV of Water Content
CV of SLM
1.00
CV of Leaf size
0.38 *
1.00
CV of Water Content
0.38 *
0.57 ***
1.00
CV of Density
0.70 ***
0.57 ***
0.80 ****
1
Pearson correlation and Bonferroni probabilities
2
* P < 0.05, *** P < 0.001, ****P < 0.0001
68
4.4
Results
4.4.1
CV of leaf traits and Survival
The mean percentage of 4-year survivorship for the 16 species analyzed was 74.4
+ 5.5 (SE) %. Eugenia inirebensis P.E. Sánchez, an understory tree, showed the lowest
survival (32.2 %) while Sapindus saponaria L., a canopy tree, had the highest survival
(96.8 %). Mean CV of leaf size was 34.1 ± 4.0 %, mean CV of SLM was 17.4 + 2.1 %,
mean CV of leaf density was 14.4 ± 2.1 % and mean CV of leaf water content was 24.6 ±
4.1 %. As expected, the CV of SLM predicted 4-year survivorship of late-successional
tree species growing in the various microhabitats of an early successional ecosystem (4year survivorship % = 47.0 + 1.6 CV of SLM, R2= 0.24, P< 0.05; N= 16, Figure 2). The
other three leaf traits did not have predictive power for 4-year survivorship (leaf size,
F=0.01, P > 0.9; leaf density, F=3.43, P> 0.05; leaf water content, F=1.21, P > 0.1).
4.4.2
CV of leaf traits and Increments in height and diameter
The mean percentage of incremental growth was 2.6 + 0.4 cm/month in height
and 0.5 + 0.3 cm/month in diameter. Mean CV of leaf size was 35.7 ± 3.1 %, mean CV of
SLM was 18.2 + 1.5 %, mean CV of leaf density was 14.4 ± 1.5 % and mean CV of leaf
water content was 23.3 ± 2.9 %. Rheedia edulis (Seems.) Planch. & Triana [Garcinia
intermedia], a mid-canopy tree, had the lowest incremental growth in height (0.6 + 0.8
cm/month) while Trichilia havanensis Jacq., an understory tree, had the highest (6.5 +
3.0 cm/month). Eugenia inirebensis showed the lowest incremental growth in diameter
(0.03 + 0.04 cm/month), while Ceiba pentandra (L.) Gaertn., a canopy tree, had the
69
highest incremental growth in diameter (1.4 + 1.1 cm/month). CVs of each leaf trait per
species are in Table XXII, Appendix G.
100
Sasa
Neam
Amtu
4-year Survivorship (%)
Porh
Live
Insi
Cost
80
Coar
Copo
Amho
Vigu
Pidi
60
Rhed
40
Cabr
Chve
Euin
20
2
6
4-year Survivorship % = 45 +1.61 CV of SLM
2
R = 0.24, P< 0.05, N=16
10
14
18
22
26
30
34
Coefficient of Variation of SLM (%)
Figure 2. Regression of the percentages of survival on the coefficient of variation
of SLM of 23 non-pioneer tropical tree species growing in an experimental
planting in the Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. Survival
was calculated as the number of individuals present in 2001, divided by the
number of individuals planted in 1997. Open circles correspond to canopy and
emergent species (> 25 m) and filled circles to understory species. The key for the
species follows Table X.
70
Regression of incremental growth in height and diameter on CV of leaf size
(F=1.7, P > 0.2; F=0.5, P > 0.4), CV of leaf density (F=0.9, P > 0.4; F=0.7, P > 0.4), and
CV of leaf water content (F=0.6, P > 0.4; F=0.8, P > 0.4) were not significant.
As predicted, regressions of incremental growth in diameter on CV of SLM (Log
Increment in diameter= -2.1 + 0.04 CV of SLM, R2= 0.34, P<0.005; Figure 3) and on
height (Log Increment in height= -0.16 + 0.03 CV of SLM, R2= 0.35, P<0.001; Figure 4)
were positive and significant; higher incremental growth in height and in diameter in latesuccessional tree species were associated with higher intraspecific variation in SLM.
One outlier, Lonchocarpus cruentus Lundell, was removed from the analysis.
Regressions including L. cruentus were significant, but the slope was uncharacteristically
steep due to a remarkably high increment in height (9.5 ± 5.5 cm/month).
When regressions were partitioned by canopy and understorey status, similar
regression were found for incremental growth in height (Log Increment in height
(Canopy)= - 0.22 + 0.04 CV of SLM, R2= 0.37, P<0.05, N=10, and Log Increment in
height (Understorey)= - 0.19 + 0.03 CV of SLM, R2= 0.35, P<0.05, N=13; Figure 16,
Appendix H), but regressions for incremental growth in diameter on the CV of SLM were
not significant for either category.
71
Log of Increment in Diameter (cm / month)
-0.6
Cepe
Coar
-1.0
Insi
Trhe
Pesc
Chve
Cost
Come
Poar
Sasa
Gugr
Live
-1.4
Vigu
Copo
Neam
Cabr
PidiAmtu
Rhed
-1.8
Amho
Porh
Hitr
-2.2
Log Increment Diameter = - 2.09 + 0.036 CV of SLM
2
R = 0.34, P< 0.005
Euin
-2.6
2
6
10
14
18
22
26
30
34
Coefficient of Variation of SLM (%)
Figure 3.Regression of the Log of monthly Increment in basal diameter on the
coefficient of variation of SLM of 23 non-pioneer tropical tree species growing in
an experimental planting in the Cooperative of Lázaro Cárdenas, Los Tuxtlas,
Mexico. Incremental growth refers to one mean of three periods of growth from
1998 to 2001. Open circles correspond to canopy and emergent species (> 25 m)
and filled circles to understory species. The key for the species follows Table X.
72
Log Increment in Height (cm / month)
1.0
Trhe
0.8
Insi
0.6
Cepe
Coar
Pesc
Live
Sasa
0.4
Vigu
Poar
Chve
0.2
Cost
Copo
Neam
Pidi Come
Cabr
Porh
Gugr
Hitr
Amtu
0.0
Euin
Amho
-0.2
-0.4
2
6
Log Increment in Height = -0.155 + 0.029 CV of SLM
2
R = 0.35, P< 0.005
Rhed
10
14
18
22
26
30
34
Coefficient of Variation of SLM (%)
Figure 4. Regression of the Log of monthly Increment in height on the coefficient
of variation of SLM of 23 non-pioneer tropical tree species growing in an
experimental planting in the Cooperative of Lázaro Cárdenas, Los Tuxtlas,
Mexico. Incremental growth refers to one mean of three periods of growth from
1998 to 2001. Open circles correspond to canopy and emergent species (> 25 m)
and filled circles to understory species. The key for the species follows Table X.
73
4.4.3
Maximal tree height
The mean maximal tree height of the 24 species studied was 24.9 + 2.1 m, ranging
from 8 m for Pouteria rhynchocarpa T.D. Penn. to 40 m for Poulsenia armata (Miq.)
Standl. and Nectandra ambigens. Maximal tree height did not predict CV of leaf size (F
= 0.7, P > 0.4), neither CV of leaf density (F = 0.1, P > 0.8) nor CV of leaf water content
(F = 0.6, P > 0.5).
As expected, maximal tree height predicted the CV of SLM (CV of SLM= 8.64 +
0.31 Maximal Tree Height, R2= 0.18, P < 0.05; Figure 5). Tall species had higher
intraspecific variation in SLM than short species.
No significant regressions were found of survival on the maximal tree height (F =
0.09, P > 0.7, N=16) neither for the increments in diameter (F= 2.03, P > 0.1) and height
(F = 0.27, P > 0.6) on maximal tree height.
4.5
Discussion
These results show that an easily-measured leaf traits (CV of SLM) predicts the
performance of late-successional tree species growing in different microhabitats of early
successional environments, allowing a criterion for selection of species suitable for
planting in abandoned pastures and agricultural fields. Species most capable of adjusting
SLM to different microhabitats of early successional environments (high CV of SLM)
had higher survival and growth rates in that environment than species with less
capability. Planting late-successional species in early successional environments, where
pioneer species arrive by unassisted dispersal, helps bypass low-diversity forests
(“pioneer desert” of Chapter 2) that may persist for decades.
74
34
CV of SLM = 8.64 + 0.31 Maximal Tree Height
2
R = 0.18, P< 0.05
Coefficient of variation of SLM (%)
30
Pesc
Neam
Coar
Cepe
26
Insi
22
Amtu
Cost
Copo
Come
Cabr Pidi
Poar
Vigu
18
Trhe
14
Live
Gugr
Hitr
Sasa
Porh
10
Rhed
Chve
6
2
Amho
Euin
5
10
15
20
25
30
35
40
45
Maximal Tree Height (m)
Figure 5. Regression of the Coefficient of variation of SLM on maximal tree height
of 23 non-pioneer tropical tree species growing in an experimental planting in the
Cooperative of Lazaro Cárdenas, Los Tuxtlas, Mexico. The key for the species
follows Table X.
There are good reasons why variation in SLM is a suitable indicator of growth in
varied conditions. A trade-off exists between growth potential and adaptation to adverse
conditions (Lambers and Poorter, 1992). Those species adapted to harsh environments
grow more slowly than those species growing in high-quality sites. In addition, trade-offs
between species leaf traits (leaf area, photosynthetic capacity) and leaf longevity result in
75
different growth rates. The dry leaf weight per unit area (SLM) is a measure of allocation
strategy (Wright and Westoby, 1999). In general, those species with low SLM show
higher growth rates than species with high SLM when growing under optimal conditions,
and this correlation holds for many species of different life forms in various ecosystems
(Poorter and Remkes, 1990; Walters et al., 1993; Huante et al., 1995; Cornelissen et al.,
1996; Grime et al., 1997; Reich et al., 1998; Westoby, 1998). Further, SLM varies within
a species when individuals grow under different abiotic conditions. Plants in high-light
conditions have smaller leaves with higher SLM than plants in low-light environments
(Parkhurst and Loucks 1972; Bongers and Popma, 1988; Witkowski and Lamont, 1991;
Pearcy and Sims, 1994). Given that quantitative changes in leaf traits in response to
variable light levels are in part responsible for different growth rates (King et al., 1997)
different abilities of species to adjust leaf traits to different microhabitats of an early
successional environment predict their growth rates.
Intraspecific variation in SLM results from adjusting leaf traits to different light
and water availability levels. In the mature forest, seedlings growing in the dark and
humid environment of the forest floor adjust their leaf traits to high light levels when
canopy gaps open over them. By adjusting their leaf traits (i.e. leaf size) to the new
conditions, they optimize light harvesting, thereby increasing their growth rates.
However, not all species have the same ability to adjust leaf traits to new abiotic
conditions. They still may tolerate the new environmental conditions but they are not able
to efficiently use the new resources. Other attributes of species might serve as predictors
of growth and survival.
76
Maximal tree height is associated with the plasticity of leaf traits (Niinemets,
1996; Thomas and Bazzaz, 1999). Tall species reach the canopy and develop two kinds
of leaves within the same crown to cope with high light levels at the top of the crown and
low light levels at the bottom (Popma et al., 1992). These “sun” and “shade” leaves may
differ only in quantitative traits, or may differ markedly in structure and shape (Popma et
al., 1992). Therefore, tall species have the ability to adjust leaf traits to different light
levels and this might provide the functional means of adjusting well to the different
microhabitats of early successional environments, resulting in higher survival and growth
rates. This study did not support this prediction. Even when intraspecific variation in
SLM was positively associated with maximal tree height, and the variation of SLM was
related to growth rate and survival, maximal tree height did not predict performance.
Selection of tall species from a little-studied sample for planting abandoned agricultural
land, without evidence of ability to grow and survive, might not succeed. Of several leaf
characters surveyed (Table XXII, Appendix G) all of them highly correlated to each
other, coefficient of variation of SLM was the best predictor of growth and survival in
early successional habitats.
4.6
Conclusions
Late-successional tropical tree species represent > 80% of rain forest tree species
in undisturbed habitats, and provide much of the structural diversity as well as food
resources for fruit- and seed-eating animals. For places where natural regeneration takes
place, the species that are present in the old growth forest require many years to arrive by
themselves (i.e. dispersal limitation exists). The planting of late-successional species is a
77
viable means of restoring diversity much more rapidly than natural regeneration (see
Chapter 2). Here I show that tree species with high intraspecific variability in SLM will
grow and survive better across different microhabitats of early successional environments
than species with low variability in SLM. Use of variation in SLM and potentially other
indices that predict performance may alleviate the need to individually screen large
numbers of late-successional species for performance in restoration projects, allowing for
more time and money to be used to evaluate other criteria for combinations of species
that will generate desired restored forest.
4.7
Acknowledgments
I thank the staff of the Los Tuxtlas Biological Station, Dr. R. Bye from the
Botanical Garden (UNAM) and Dr. Kumiko Shimada, Institute of Geology (UNAM) for
their support, Miguel Sinaca and Jose Luis Paxtian for field assistance. I am grateful to N.
Cordeiro, J. Fornoni, M. Jorge, S. Saha, A. Sullivan, and B. Zorn-Arnold for comments
on the manuscript. This study was supported by CONACyT of Mexico and the Lincoln
Park Zoo of Chicago.
4.8
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81
Thomas, S.C., Bazzaz, F.A., 1999. Asymptotic height as a predictor of photosynthetic
characteristic in Malaysian rain forest trees. Ecology, 80, 1607-1622
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gradients. Journal of Ecology, 87, 85-97.
5. PREDICTING SURVIVAL AND GROWTH OF LATE-SUCCESSIONAL TREE
SPECIES IN ABANDONED PASTURES
5.1
Abstract
In the middle of large deforested areas or in sites far from a forest, dispersal of
forest seeds may be low or nil; abandoned lands may remain with no forest cover for a
long time. In such cases, erosion degrades land quickly, making future restoration efforts
difficult. Here I ask which average or variations in leaf traits predict higher survival and
growth rates in sites with no incoming natural regeneration. I evaluate leaf size, leaf mass
per unit area (SLM), leaf density and leaf water content and, maximal tree height of 12
tropical tree species grown for 17 months in pastures and secondary forests close to Los
Tuxtlas Biological Station in Veracruz, Southeast Mexico.
Incoming vegetation was cut once a month in pasture conditions to mimic
abandoned pastures with no natural regeneration. Even when survival of latesuccessional species was higher under secondary forest (88 %) than in pastures, overall
survival in pastures was high (70 %). All species showed similar increments in height in
pasture and secondary forest while only two species (Omphalea and Sideroxylum)
showed higher increments in diameter in pasture than in secondary forest. Leaf traits
changed in response to contrasting light levels in pastures and secondary forest:
individuals growing in pasture showed lower water content and higher SLM and density
than individuals growing in the secondary forest. Survival of species in pastures was
predicted by increments in height (R2 = 0.28). Mean leaf density or SLM measured in
82
83
individuals growing in secondary forest, and mean SLM measured in individuals growing
in pastures predicted the increments in diameter of individuals growing in pastures.
Those species with lower mean SLM or leaf density measured in secondary forest
showed higher increments in diameter in pasture conditions (R2= 0.39 and R2= 0.45
respectively). By measuring mean SLM or leaf density in individuals growing in
understory conditions, it is possible to predict which species will perform better in
abandoned pastures with no input of pioneer species that develop a canopy over them. By
planting these species it is possible to increase biodiversity in abandoned pastures that
otherwise will remain as low diversity environments for long time.
5.2
Introduction
After former agricultural or pasturelands are abandoned, the only source of seeds
for forest regeneration comes from dispersal events (Gómez-Pompa and Vázquez-Yanes,
1981; Finegan, 1996). In the middle of large deforested areas or in sites far from the
forest, dispersal of forest seeds may be low or nil (Martínez-Garza and GonzálezMontagut, 1999; Hooper et al., 2002; Ingle, 2003). Even the small, highly vagile seeds of
early successional species may not arrive. Abandoned lands may remain with no forest
cover for years to decades while erosion degrades land quickly, making future restoration
efforts difficult.
Planting early successional species (pioneers) with high growth rates will only
encourage the occupation of large areas with a small proportion (< 20%) of forest biota.
Planting late-successional species that are so dispersal-limited that they do not arrive for
a long time, if ever, is a preferable reforestation tactic than to create a low-diversity
84
pioneer matrix. Highly diverse mature forest is composed of late-successional species
that provide much of the structural diversity and the food resources for fruit- and seedeating animals (see Welden et al., 1991; Martínez-Ramos, 1994). The planting of midand late-successional species, together with pioneer species, is a valuable option to
establish a species-rich and structurally diverse forest in places where succession has
been arrested. What is unknown is which mid- and late-successional species best endure
the harsh conditions of abandoned lands with no woody regeneration.
A previous study (Chapter 4) showed that of 23 late-successional species, those
with higher variation in leaf mass per unit area (SLM) showed higher survival and growth
rates across the microhabitats of early successional ecosystems (secondary forest, edge
and open pastures). This high variation corresponds to an adjustment of leaf traits, (i.e.,
leaf size and weight) to different microhabitats of early successional environments. Here
I ask which leaf traits or their variation predict higher survival and growth rates in
abandoned pastures where all incoming vegetation was cut once a month to mimic
abandoned pastures without natural succession. Further, I compare survival and growth
rates of mid- and late-successional species in pasture conditions and in the secondary
forest.
Even if some species benefit from higher light levels when a gap opens over them
in the forest, I expect late-successional species will show lower survival and growth rates
in the long-lasting high light levels and low water availability typical of pastures than in
the secondary forest (a habitat more similar to the mature forest). Leaf traits change in
response to light and water levels. Therefore I expect individuals in long-lasting pasture
condition to show leaf traits typical of individuals growing under high light levels and
85
low water availability. This in turn results in smaller leaves and lower water content and
higher leaf density and SLM than individuals growing in the shade of secondary forest.
Species adjust leaf traits in response to light and water levels, and these changes are in
part responsible for higher growth rates. Therefore, mean leaf traits have been found to
predict species growth rates under optimal conditions: those species with large leaves and
low SLM show higher growth rates (Grime et al., 1997; Reich et al., 1998; Westoby,
1998). In agreement with this, the intraspecific variation in leaf mass per unit area (SLM)
predicts species growth rates across microhabitats of early successional environments
(Chapter 4). But which leaf traits will predict survival and growth rates in persistant
adverse conditions like pastures with no input of pioneer species? I expect that those
species with larger leaves and lower SLM show higher survival and growth rates in
pasture while the opposite may be true for secondary forest.
Previous studies showed that maximal tree height predicts the direction and
magnitude of change in leaf traits through ontogeny for eight late-successional tree
species (Chapter 3) and also predicted the intraspecific variation in SLM for 23 latesuccessional tree species (Chapter 4). Besides, in a study in Malaysia mean SLM was
positively correlated to asymptotic tree height of 28 species (Thomas and Bazzaz, 1999).
Tall species experience low light levels as seedlings or juveniles, but high light levels
when they reach the canopy. They experience more heterogeneity in light levels during
their lives than short species that spend more of their lives in a more homogeneous
habitat, the shaded understory. Therefore, seedlings of tall species show larger leaf size
and lower SLM than conspecific adults while the pattern is reversed for short species
(Chapter 3). I expect tall species to show overall smaller leaves and higher SLM than
86
short species. However even with higher SLM, tall species may show higher survival and
growth rates in pastures due to their higher variability in leaf traits.
5.3
Methods
5.3.1
Study site
This study was conducted in a experimental planting in the Cooperative of Lázaro
Cárdenas at approximately 6 km from Los Tuxtlas Biological Station (LTBS) in the state
of Veracruz, southeast Mexico (18 º 30’ and 18º 40’ N, 95º 03’ and 95º 10’ W). The
LTBS lies within a reserve of 640 ha of lowland tropical rain forest that is the
northernmost rain forest in the neotropics. The forest has a closed canopy of about 35 m
high. Nectandra ambigens (Blake) C.K. Allen (Lauraceae) is the most common species in
the canopy, while Pseudolmedia oxyphyllaria Donn. Sm. (Moraceae) and Astrocaryum
mexicanum Liebm. (Arecaceae) are abundant in the mid-canopy and understory,
respectively (Bongers et al., 1988). Soil is sandy loam classified as vitric andosols
(FAU/UN 1975 in Soto-Esparza, 1976). Mean annual temperature and mean annual
rainfall are 27º C and 4900 mm, respectively. A dry season extends from March to May,
and a rainy season from June to February.
5.3.2
Land use history and Experimental Planting
The study area is located within a 25 ha parcel of former forest land that was
deforested in 1968, and used as crop land for 4 years and for cattle ranching for 15 years.
It has been undergoing natural regeneration since abandonment in 1987. This early
successional environment has three distinct microhabitats: (1) area covered by grasses,
87
(2) secondary forest and, (3) low and broken canopy of 2 to 4 m. From these three, two
microhabitats were used: (1) open area of approximately 3 ha covered with the exotic
grass Cynodon plectostachyus (K. Schum.) Pilg. up to 1.5 m high in the wet season, and
(2) the closest secondary forest with a 15 m tall canopy of pioneer species: Cecropia
obtusifolia Bertol. (Moraceae), Heliocarpus appendiculatus Turcz. (Tiliaceae), Bursera
simaruba (L.) Sarg. (Burseraceae) and Cedrela odorata L. (Meliaceae).
From August to December 2000, seeds of 12 mid and late-successional tree
species (Martínez-Ramos, 1985) were collected from the LTBS and germinated (100
individuals per species N= 1200 individuals) under shade in a nursery. Numbers of
individuals per species are unequal due to differential seed germination, and seedling
survival and mortality during transplantation (Table XXIII, Appendix I). On March 2001,
I marked a grid of 1200 squares of 2 X 2 m covering the field, including open pasture and
the closest secondary forest. In August 2001, seedlings of approximately 4 months old
were planted, one seedling in the middle of each square. Seedlings of all species were
systematically randomized in the grid to guarantee interspersion.
Light levels (Photon Flux Density, PFD) and soil characteristics (i.e. soil moisture
and bulk density) were measured in the pastures and secondary vegetation for a subsample of individuals. Photon-flux density was measured with a Light Meter Li-cor LI189 quantum sensor. Gravimetric soil moisture and bulk density were measured
following Chapman (1976). Bulk density estimates soil compaction. Photon-flux density
and gravimetric soil moisture were significantly different in the two habitats (MannWhitney U test (1,262) =31.6 P< 0.0001; F(1,52)=4.1, P < 0.05, respectively) while bulk
density was not (F(1,54)=0.02, P > 0.9; Table XII).
88
Twelve tree species from nine families were used to represent the variety of
maximal tree heights and fruits that attract different frugivorous animals in the area
(Table XIII). Maximal tree height is the tallest published stature for adults of a given
species in the LTBS (Ibarra-Manríquez and Sinaca, 1995; 1996; 1996a). To calculate
growth rates, seedling heights and diameters at the stem base were measured in August
2001, February 2002, April 2002 and January 2003. Grasses and herbs were removed 50
cm around individuals at the time of measurement. To mimic abandoned pastures without
natural regeneration, incoming plants growing in the pasture were cut once a month to
ensure homogeneous high light conditions. Increments of growth rates in heights (height
t2-height t1/
time) and in diameter at the stem base (hereafter diameter) were calculated for
the three periods between censuses. The survival rate of each species was calculated as
the number of individuals surviving from 2001 to 2003, divided by the number of
individuals present in 2001.
One to three fully expanded undamaged leaves were collected from individuals
displaying more than 10 leaves (see Table XXIV, Appendix J). Leaves were measured
within 2 hr of collection. Leaf fresh weight (FW) was measured with a balance Pocket
Pro 250-B (readability of 0.1 g) while fresh leaf size (LS) was measured with a leaf area
meter (Ci-202, CID, Inc. Camas, WA, USA). Leaves were oven dried to constant weight
at 100 ° C and weighed to the nearest 0.01 g (DW). Specific Leaf Mass (SLM; inverse of
Specific Leaf Area) is the leaf dry weight per unit fresh leaf area (=DW/LS). I also report
the ratio of leaf fresh weight over leaf dry weight often thought of as “leaf density”
(=FW/DW; Rascio et al., 1990; Garnier and Laurent, 1994). This leaf density reflects the
amount of cytoplasm versus hemicellulose and cellulose in plant tissues. I also report leaf
89
water content that is the difference between leaf fresh weight and leaf dry weight per unit
leaf area (=FW-DW/LS).
TABLE XII
PHOTON FLUX DENSITY (PFD), GRAVIMETRIC SOIL MOISTURE AND BULK
DENSITY IN SECONDARY FOREST AND PASTURES
Habitat
Secondary Forest
Pasture
1
Median, N=500
2
Mean ± SE, N=120
PFD 1
Soil Moisture 2
BulkDensity2
(µmol -2 s -1)
(mL g -1)
(g cm -3)
20
0.43 ± 0.01
0.67 ± 0.02
1730
0.39 ± 0.01
0.64 ± 0.01
The intraspecific variation in leaf traits is reported as its coefficient of variation
(hereafter CV) = Standard Deviation of leaf traits * 100 / Mean leaf traits for the two
habitats, and it was corrected for sample size (Sokal and Rohlf, 2003).
5.3.3
Data Analysis
T-tests were used to test for survival differences between habitats overall the 12
species. Multivariate Analysis of Variance (MANOVA) tested the effects of species and
habitat (pasture and secondary forest) on increments in height and diameter at the base of
the stem. The mean increment in height and diameter for the three periods of time
90
between the censuses during which an individual was alive was used for MANOVA
analysis. Individuals that showed a mean negative increment (died back) were not
included in MANOVA analysis since increments were log transformed. However, mean
individual negative increments are included when means and standard Errors (SE) of
increments are shown for each species. Increments and leaf traits were log transformed to
satisfy MANOVA assumptions.
TABLE XIII
FAMILY, FRUIT TYPE AND RANGE OF MAXIMAL TREE HEIGHT OF 12 LATESUCCESSIONAL TROPICAL TREE SPECIES
SPECIES
FAMILY
KEY
FRUIT TYPE 1
HEIGHT (m) 1
Amphitecna tuxtlensis
Bignoniaceae
Amtu
Green berry
3-10
Calophyllum brasiliense
Clusiaceae
Cabr
Green drupes
20-30
Coccoloba hondurensis
Polygonaceae
Coho
Red or black drupes
15-20
Chrysophyllum mexicanum
Sapotaceae
Chme
Red or black berry
10-20
Cymbopetalum baillonii
Annonaceae
Cyba
Capsule with arrillate seeds
8-25
Diospyros digyna
Ebenaceae
Didi
Green berry with black arill
20-25
Guarea grandifolia
Meliaceae
Gugr
Brown capsule
20-30
Nectandra ambigens
Lauraceae
Neam
Black drupe with red cap
20-40
Omphalea oleifera
Euphorbiaceae
Omol
Green berry
15-30
Pouteria campechiana
Sapotaceae
Poca
Brown drupe
15-20
[Garcinia intermedia]
Clusiaceae
Rhed
Yellow berry
5-15
Sideroxylon portoricense
Sapotaceae
Sipo
Brown berry
20-35
Rheedia edulis
1
From Ibarra-Manriquez and Sinaca 1995, 1996, 1996a.
To find out which traits may predict survival and growth rates of mid and latesuccessional species, linear regressions were performed for survival and increments
91
separated for the two microhabitats used on all leaf traits and their variation (CV). The
mean increment for species in the three periods of time between censuses and across all
habitats was used for regressions. Regressions are used to explore data; for regression
with data measured in two habitats causal relationships are not implied. Increments in
height and diameter were log transformed to satisfy regression assumptions. All statistical
analyses were performed in STATISTICA 4.0
5.4
Results
5.4.1
Survival
Mean 17-month survivorship % for 12 species was significantly higher in the
secondary forest (88 ± 1.7 %) than in the pasture (69 ± 4.8 %, t-test (1, 11) =3.22, P<
0.005). Cymbopetalum showed the lowest survival in the secondary forest and pastures
(77 and 39 % respectively) while Chrysophyllum showed the highest survival in the
secondary forest (97 %), and Coccoloba in the pasture (100 %; Table XXIII, Appendix
I).
5.4.2
Increments in height and diameter
Mean increment in height for the twelve species was 1.17 ± 0.05 cm / month.
Guarea grandifolia showed the lowest increment in height (0.34 ± 0.01 cm / month),
while Calophyllum brasiliense showed the highest (2.86 ± 0.51 cm / month). Nectandra
ambigens showed the lowest increment in diameter (0.01 ± 0.005 cm / month), while
Cymbopetalum baillonii showed the highest increment in diameter (0.07 ± 0.01 cm /
92
month). MANOVA revealed that overall species and habitat showed differences in
increments in height and diameter. The interaction of species and habitat was significant
(Table XIV) revealing that only two species (Omphalea oleifera and Sideroxylum
portoricense) showed significately higher increments in diameter in open pasture than in
secondary forest (Figure 6). All species showed similar increments in height in pasture
and secondary forest.
TABLE XIV
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE OF INCREMENTS
IN HEIGHT AND DIAMETER MEASURED IN 12 TROPICAL TREE SPECIES IN
LOS TUXTLAS, VERACRUZ, MEXICO
MAIN FACTOR
WILKS ‘
RAO ‘S
DF 1
P<
LAMBDA
Species
0.86
3.79
22, 1080
0.00001
Habitat
0.96
10.17
2, 1080
0.00005
Species * Habitat
0.93
1.66
22,1080
0.05000
1
Note that the degrees of freedom for MANOVA are multiplied for the number of
dependent variables used, in this case, five variables.
93
5.4.3
Leaf Traits
Species identity and habitat affected leaf traits, while the interaction of species and
habitat was not significant (Table XV). Univariate analyses are shown per leaf traits for
significant MANOVA tests.
5.4.3.1 Leaf size
Univariate analysis of variance showed that species significantly differ in leaf
sizes (F= 58.3, P (11, 399) < 0.00001). Omphalea showed the largest leaf size (177.0 ± 14
cm2) while Chrysophyllum showed the smallest leaf size (14.4 ± 1 cm2 ; Table XXIV,
Appendix J). Habitat (secondary forest vs. pasture) did not affect leaf size (F= 1.2, P(1, 399)
> 0.2).
4.4.3.2 SLM
Species differed in SLM (F= 69.1, P(11, 399) < 0.00001), and habitat had large effect
on this leaf trait (F= 174.0, P(1, 399) < 0.00001). Rheedia showed the highest SLM (115.6
± 4.3 g m-2) while Omphalea showed the lowest SLM (36.4 ± 2.6 g m-2; Table XXIV,
Appendix J). Individuals in the pasture showed 1.4 times higher SLM than those in the
secondary forest (86 ± 1.6 g/m2 and 62 ± 1.5 g/m2 respectively).
94
Log Increment Diameter (cm / month)
-0.8
*
Secondary Forest
Pasture
-1.2
*
-1.6
-2.0
-2.4
-2.8
Amtu Rhed Chme Coho
Poca
Cyba
Didi
Gugr
Omol
Cabr
Sipo
Neam
Species
Figure 6. Log Increment of diameter at the base of the stem of 12 late-successional
tropical tree species Key for species follows Table XIII, species are arranged by
increasing maximal tree height from left to right. Asterisks over bars represent
significant differences between secondary forest and pasture tested with Post Hoc
Tukey Test after Univariate tests were performed.
95
TABLE XV
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE OF LEAF TRAITS
MEASURED IN 12 TROPICAL TREE SPECIES IN LOS TUXTLAS, VERACRUZ,
MEXICO
WILKS ‘ LAMBDA
RAO ‘S
DF 1
P<
Species
0.09
29.10
44, 1596
0.00001
Habitat
0.96
10.17
4, 1596
0.00001
Species * Habitat
0.93
1.66
22, 1596
0.10000
MAIN FACTOR
1
Note that the degrees of freedom for MANOVA are multiplied for the number of
dependent variables used, in this case, five variables.
5.4.3.3 Leaf Water Content
Species showed different leaf water content (F= 10.3, P(11, 386) < 0.00001), and
habitat affected leaf water content (F= 6.5, P(1, 386) < 0.01). Calophyllum showed the
highest water content (152.6 ± 11.3 g/m2) while Amphitecna showed the smallest leaf
water content (81.5 ± 5.3 g/m2; Table XXIV, Appendix J). Individuals in the pasture
showed 1.1 times higher water content than those in the secondary forest (105.8 ± 2.7
g/m2 and 118.8 ± 3.7 g/m2 respectively).
5.4.3.4 Leaf Density
Species showed different leaf density (F= 43.3, P(11, 391) < 0.00001) and habitat
had large effect on leaf density (F= 15.2, P(1, 391) < 0.00001). Rheedia showed the highest
leaf density (0.54 ± 0.03) while Cymbopetalum showed the lowest leaf density (0.31 ±
96
0.02, Table XXIV, Appendix J). Individuals in the pasture showed 1.4 times higher leaf
density than those in the secondary forest (86 ± 1.6 and 62 ± 1.5 respectively).
5.4.4
Leaf traits and performance in secondary forest and pastures
Species survival after 17 months in pastures was partially predicted by leaf area
measured in secondary forest (F= 4.0, P (1,10)= 0.07); Omphalea was an outlier for leaf
size (see above), when this species was not included, 17-month survivorship in the
pasture was predicted by leaf size measured in secondary forests (Figure 7): those species
with larger leaves under secondary forest conditions showed higher survival when
growing in pastures.
Monthly increments in height were not predicted by leaf traits.
The increment in diameter for plants in pastures was predicted by mean SLM of
conspecific individuals growing in either secondary forest (Log Increment Diameter =
0.69 - 1.27 Log of SLM, R2=0.39, P < 0.05; Figure 8) or in the pasture (Log Increment
Diameter = 1.36 - 1.52 Log of SLM, R2 = 0.37, P < 0.05; Figure 9) as predicted. Those
species with higher mean SLM measured in secondary forests or pastures showed lower
increments in diameter when growing in the pasture. Leaf density measured in
individuals growing in the secondary forest also predicted increments in diameter for
plants growing in the pasture (Log increment Diameter = -2.39 -1.87 Log Leaf Density,
R2 = 0.45, P < 0.05; Figure 10).
97
17-months survivorship in Pastures (%)
1.1
1.0
17-month survivorship = 0.04 + 0.45 * Log leaf size
2
R = 0.30 P < 0.05
Coho
0.9
0.8
Neam
Chme
Poca
0.7
Cabr
Didi
Amtu
Rhed
0.6
Sipo
0.5
Gugr
0.4
0.3
1.1
Cyba
1.2
1.3
1.4
1.5
1.6
1.7
1.8
1.9
2
Log of Leaf size in Secondary Forests (cm )
Figure 7. Regression of 17-month survivorship percentage on Leaf size of 11
non-pioneer tropical tree species growing in an experimental planting in the
Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The key for the species
follows Table XIII.
98
Maximal tree height did not predict survival, growth increments, nor leaf traits. Leaf
traits measured in pastures were highly correlated with those measured in secondary
forest. Mean SLM measured in pastures was highly correlated to all other leaf traits
measured in secondary forest or in pastures, except leaf size (Table XXV, Appendix K).
The 17-month survivorship in pasture conditions was predicted by the increments
in height there, those species with higher increments in height showed higher survival in
the pasture (17-month survivorship = 0.64 + 0.2 Log Leaf Density, R2 = 0.45, P < 0.05;
Figure 11).
Log Increment in Diameter in Pastures (cm / month)
99
-0.8
-1.0
Log Increment Diameter in Pastures = 0.69 - 1.27 Log SLM in Sec For
2
R =0.39 P < 0.05
Cyba
Omol
-1.2
-1.4
Coho
Amtu
-1.6
PocaSipo
Chme
Rhed
Cabr
Neam
Didi
-1.8
Gugr
-2.0
1.35
1.45
1.55
1.65
1.75
1.85
1.95
2.05
2
Log of SLM in Secondary Forests (g / m )
Figure 8. Regression of Log of monthly increment in diameter of individuals growing in
pasture on log of SLM of conspecific growing in the secondary forest for 12 latesuccessional tropical tree species in the Cooperative of Lázaro Cárdenas, Los
Tuxtlas, Mexico. The key for the species follows Table XIII.
Log Increment in Diameter in Pastures (cm / month)
100
-0.8
-1.0
Log Increment Diameter in Pastures = 1.36 - 1.52 Log SLM in Pastures
2
R = 0.37 P < 0.05
Cyba
Omol
-1.2
-1.4
Coho
-1.6
Chme
Poca
Sipo
Amtu
Rhed
Cabr
Neam
Didi
-1.8
Gugr
-2.0
1.6
1.7
1.8
1.9
2.0
2.1
2.2
2
Log SLM in Pastures ( g / m )
Figure 9. Regression of Log Increment in diameter on log of SLM of individuals growing
in pastures for 12 late-successional tropical tree species in the Cooperative of
Lázaro Cárdenas, Los Tuxtlas, Mexico. The key for the species follows Table
XIII.
Log Increment Diameter in Pastures (cm / month)
101
-0.8
-1.0
Log increment Diameter in Pastures = -2.39 - 1.87 Log Density in Sec For
2
R = 0.45 P < 0.05
Cyba
Omol
-1.2
-1.4
Coho
Amtu
-1.6
Cabr
Chme
Poca
Neam
Rhed
Sipo
Didi
-1.8
Gugr
-2.0
-0.8
-0.7
-0.6
-0.5
-0.4
-0.3
Log Density in Secondary Forests
Figure 10. Regression of Log Increment in diameter of individuals growing in pasture on
Log of Leaf Density of conspecific growing in the secondary forest for 12 latesuccessional tropical tree species in the Cooperative of Lázaro Cárdenas, Los
Tuxtlas, Mexico. The key for the species follows Table XIII.
102
17-month Survivorship % in Pastures
110
100
17-month survivorship % = 64 + 20 Log Increment Height
R 2 = 0.28, P < 0.05
Chme
90
Coho
80
Poca
Neam
Omol
Didi
70
Amtu
Rhed
60
Cabr
Rhed
50
Gugr
Cyba
40
30
-1.0
-0.6
-0.2
0.2
0.6
1.0
Log Increment in Height in Pastures (cm / month)
Figure 11. Regression of 17-months survivorship of individuals growing in
pastures on Log Increment in height for 12 late-successional tropical tree species
in the Cooperative of Lázaro Cárdenas, Los Tuxtlas, Mexico. The key for the
species follows Table XIII
103
5.4.5. CV of leaf traits and performance of in secondary forest and pastures
Mean CV of leaf size was 49.98 ± 2.30 %, mean CV of SLM was 57.87 + 2.69 %,
mean CV of leaf density was 27.48 ± 2.90 % and mean CV of leaf water content was
35.29 ± 2.70 %. The CV of Water content predicted 17-month survivorship of latesuccessional tree species growing in secondary forests (17-month survivorship % = 0.75
+ 0.004 CV of Water Content, R2= 0.29, P< 0.05; N= 12, Figure 12). The variation of the
other three leaf traits did not have predictive power for 17-month survivorship in
secondary forest (leaf size, F=3.2, P > 0.1; SLM, F=0.8, P > 0.7; leaf density, F=0.2, P>
0.6) and, neither of them had predictive power for the survival in pastures (leaf size,
F=2.43, P > 0.1; SLM, F=0.12, P > 0.7; leaf density, F=1.79, P> 0.2; leaf water content,
F=0.05, P > 0.8).
The species growth increments in diameter in secondary forest were not predicted
by the variation in leaf traits while the increment in diameter in pastures was partially
predicted by the coefficient of variation of SLM (F= 4.42, P < 0.06). The species
increments in height in the secondary forest were predicted by the CV of Water Content
(Log Increment in height = 1.47 - 0.05 CV of WC; R2 = 0.42, P < 0.01; Figure 13) and
the CV of leaf density (Log Increment in height = 0.79 - 0.04 CV of Density; R2 = 0.30, P
< 0.05; Figure 14), while CV of leaf size (F = 0.38, P > 0.5) and CV of SLM (F=0.18, P >
0.6) did not have predictive power. The increment in height for individuals growing in
pastures was predicted only by the Coefficient of Variation in Leaf density (Log
Increment in height = 1.01 - 0.03 CV of Density; R2 = 0.27, P < 0.05; Figure 15), the
remaining leaf traits did not have predictive power (leaf size, F = 0.5, P > 0.5; SLM,
F=0.49, P > 0.5; leaf water content, F = 1.39, P > 0.2).
104
17-month survivorship in Sec Forests (%)
1.02
0.98
17-month survivorship in Sec For = 0.75 + 0.003 * CV of W C
2
R = 0.30, P < 0.05
Neam
0.94
Coho
Chme
Amtu
Poca
Rhed
Omol
0.90
0.86
Didi
Gugr
Sipo
Cabr
0.82
0.78
0.74
10
Cyba
15
20
25
30
35
40
45
50
55
Coefficient of Variation of Water Content (%)
Figure 12. Regression of 17-month survivorship in secondary forests on the
coefficient of variation of Water Content of 12 non-pioneer tropical tree species
growing in an experimental planting in the Cooperative of Lázaro Cárdenas, Los
Tuxtlas, Mexico. The key for the species follows Table XIII
Log Increment in Height in Sec For (cm / month)
105
0.6
Didi
Cabr
Neam
0.2
Omol
Cyba
Chme
-0.2
Poca
Coho
-0.6
Amtu
Sipo
-1.0
Gugr
-1.4
-1.8
-2.2
-2.6
10
Rhed
Log Increment in Height in Sec Forest = 1.47 - 0.05 CV of W C
2
R = 0.42, P < 0.01
15
20
25
30
35
40
45
50
55
Coefficient of Variation of Water Content (%)
Figure 13.Regression of the increments in height in secondary forests on the
Coefficient of variation of Water Content of 12 non-pioneer tropical tree species
growing in an experimental planting in the Cooperative of Lázaro Cárdenas, Los
Tuxtlas, Mexico. The key for the species follows Table XIII
Lof of Increment in Height in Sec For (cm / month)
106
0.6
Neam
Cabr
Didi
0.2
Omol
Cyba
Chme
-0.2
Poca
Amtu
Coho
Sipo
-0.6
-1.0
Gugr
-1.4
-1.8
Log of Increment in Height in Sec For = 0.79 - 0.04 CV of Leaf Density
2
R = 0.30 P < 0.05
Rhed
-2.2
-2.6
10
15
20
25
30
35
40
45
50
55
Coefficient of Variation of Leaf Density (%)
Figure 14.Regression of the increments in height in secondary forests on the
Coefficient of variation of Leaf Density of 12 non-pioneer tropical tree species
growing in an experimental planting in the Cooperative of Lázaro Cárdenas, Los
Tuxtlas, Mexico. The key for the species follows Table XIII.
Log of Increment in Height in pastures (cm / month)
107
1.0
0.6
Cabr
Amtu
Didi Omol
Neam
Coho
Chme
Poca
0.2
Cyba
-0.2
Sipo
Rhed
-0.6
Log Increment in Height in pastures = 1.01 - 0.03 CV of Density
2
R = 0.27, P < 0.05
-1.0
10
15
20
25
30
35
40
Gugr
45
50
55
Coefficient of Variation of Leaf Density (%)
Figure 15.Regression of the increments in height in pastures on the Coefficient of
variation of Leaf Density of 12 non-pioneer tropical tree species growing in an
experimental planting in the Cooperative of Lázaro Cárdenas, Los Tuxtlas,
Mexico. The key for the species follows Table XIII.
108
5.5
Discussion
In deforested areas far from sources of seed to start regeneration, natural
succession may be delayed many years or not start (Finegan 1996). Planting a mix of
fast-growing, early-successional species along with mid- and late-successional tree
species may fulfill many important restoration goals in such sites. Pioneer species may
immediately stop erosion, providing a highly desired ecosystem function, while mid- and
late-successional species generate a high diversity forest. However, the high number of
species in the mature tropical forest precludes testing all of them in pastures to screen
which ones show high survival and growth rates in these environments.
Functional leaf traits, like SLM or leaf density are useful for predicting survival
and growth rate of late-successional species when planted in adverse conditions (i.e.,
abandoned pastures). Further, these leaf traits may be measured in pastures or in the
shaded conditions of the secondary forest, and still predict growth rates of species
growing in pastures. Light conditions in the secondary forest are as low as those
prevailing in the mature forest, therefore, by measuring leaf traits under those conditions,
it is possible to predict the performance of species in another set of very adverse
environmental conditions (pastures). This alleviates the need to individually screen large
numbers of late-successional species for restoration projects, allowing for more time and
money to be used to evaluate other criteria for combinations of species that will generate
desired restored forest.
That survival of late-successional species was higher under secondary forest than
in pastures is an anticipated result, since these species usually establish in the dark humid
understory of the forest. On the other hand, that all species showed similar increments in
109
height in pasture and secondary forest was surprising. Even when late successional
species respond to sudden high light conditions caused by formation of gaps in the
canopy (Popma and Bongers, 1991), their growth may decrease at extremely high light
levels (Ricker, 1998; Poorter, 1999). Especially tall species are known to increase their
height when gaps open, which is confirmed by the presence of juveniles and subcanopy
size classes preferentially in forest gap or building phases (Clark and Clark, 1992). Two
canopy species (Omphalea and Sideroxylum) showed significantly higher increments in
diameter in pasture than in the secondary forest, these two species are those with the
highest increments in height and in diameter (Figure 6). However, increments in height
and diameter were not predicted by maximal tree height at least in the first 17 months;
perhaps differences in growth rates will be noticeable later on.
In a previous study, survival of late-succesional tree species across various
microhabitats of an early successional environment was predicted by the variation in
SLM. These different microhabitats result from natural regeneration events, then
individuals are exposed to changing light and water levels due to the natural input of
pioneer species (Chapter 4). In places where pioneers species do not arrive due to
dispersal limitation (long-lasting pasture conditions), the variability in the leaf density
that species display in pastures and secondary forest explain their increments in height in
pasture (Figure 15). Leaf density represents the amount of cytoplasm relative to the
amount of cell wall material. Under water stress, hemicellulose accumulates, thereby
increasing leaf density and the water-holding capacity of leaves (Rascio et al., 1990;
Garnier and Laurent, 1994). Those mid and late-successional species able to adjust leaf
110
density (water-holding capacity) showed higher increments in height in an environment
with very low water availability, as they are pastures.
5.6
Conclusions
Late-successional tropical tree species represent > 80% of rain forest tree species
in undisturbed habitats, and provide much of the structural diversity as well as food
resources for fruit- and seed-eating animals.
For places where natural regeneration does not take place the planting of a mix of
early and late-successional species is a viable means of restoring diversity much more
rapidly than waiting for natural regeneration to occur. Mean SLM and leaf density
measured in the forest understory of mature forest may be used to predict performance of
mid and late-successional species in long-lasting harsh conditions (i.e. pastures with not
natural regeneration). This may alleviate the need to individually screen large numbers of
species for survival and growth rates in restoration projects, allowing for more time and
money to be used to evaluate other criteria for combinations of species that will generate
desired restored forest.
5.7
Literature Cited
Bongers, F., Popma, J., Meave del Castillo, J., Carabias, J., 1988. Structure and floristic
composition on the lowland rain forest of Los Tuxtlas, Mexico. Plant Ecology,
74, 55-80.
Chapman, S.B., 1976. Methods in Ecology. Blackwell Science Pub, USA.
Finegan, B., 1996. Pattern and process in neotropical secondary rain forest: the first 100
years of succesion. Trends in Ecology and Evolution, 11, 119-124.
111
Gómez-Pompa, A., Vazquez-Yanes, C., 1981. Sucessional studies of a rain forest in
Mexico. In: West, D. C., H. H. Shugart, D. B. Butkin (Eds.), Forest Sucession
Concepts and Application, Springer-Verlag, USA, pp. 246-266.
Grime, J. P., Thompson, K., Hunt, R., Hodgson, J.G., Cornelissen, J.H.C., Rorison, I.H.,
Hendry, G.A.F., other 28 authors, 1997. Integrated screening validates primary
axes of specialization in plants. Oikos, 79, 259-281.
Hooper, E., Condit, R., Legendre, P., 2002. Responses of 20 native tree species to
reforestation strategies for abandoned pastures in Panama. Ecological
Applications, 12, 1626-1641.
Ibarra-Manríquez, G., Sinaca, S., 1995. Lista florística comentada de la Estación de
Biología Tropical “Los Tuxtlas”, Veracruz, México. Revista de Biologia Tropical,
43, 75-115.
Ibarra-Manríquez, G., Sinaca, S.,1996. Lista florística comentada de la Estación de
Biología Tropical “Los Tuxtlas”, Veracruz, México (Mimosaceae a Verbenaceae).
Revista de Biologia Tropical, 44, 41-60.
Ibarra-Manríquez, G., Sinaca, S.,1996a. Lista florística comentada de la Estación de
Biología Tropical “Los Tuxtlas”, Veracruz, México (Violaceae a Zingiberaceae).
Revista de Biologia Tropical, 44, 427-447.
Martínez-Ramos, M. 1985. Claros, ciclos vitales de los arboles tropicales y regeneración
natural de las selvas altas perennifolias. Investigaciones sobre la Regeneración de
selvas altas en Veracruz, México. (eds. A. Gómez-Pompa and S. Del-Amo), 191240. Alhambra Mexicana S.A. de C.V., Mexico.
Martínez-Ramos, M., 1994. Regeneracion natural y diversidad de especies arboreas en
selvas humedas. Boletin de la Sociedad Botanica de Mexico, 54, 179-224.
Parkhurst, D.F., Loucks, O.L., 1972. Optimal leaf size in relation to environment. Journal
of Ecology, 60, 505-537.
Pearcy, R.W., Sims, D.S., 1994. Photosynthetic acclimation to changing light
environments: scaling from the leaf to the whole plant. In: Caldwell, M.M.,
Pearcy, R.W. (Eds.), Exploitation of environmental heterogeneity by plants,
Academic Press, USA, pp. 145-173.
Poorter, H., Remkes, C., 1990. Leaf-area ratio and net assimilation rate of 24 wild
-species differing in relative growth-rate. Oecologia, 83, 553-559.
112
Ricker, M., Siebe, C., Sánchez, S., Shimada, K., Larson, B.C., Martínez-Ramos, M.,
Montaginini, F., 2000. Optimising seedling management: Pouteria sapota,
Diospyros digyna, and Cedrela odorata in a Mexican rainforest. Forest Ecology
and Management, 139, 63-77.
Sokal, R.R., Rohlf, F.J., 2003. Biometry: The principles and practice of statistics in
Biological Research. Third edition. W. H. Freeman and Company, New York.
Soto-Esparza, M., 1976. Algunos aspectos climaticos de la región de Los Tuxtlas. In:
Gómez-Pompa, A., C.Vázquez-Yanes, S., Del Amo, R., Butanda, C. A. (Eds.),
Investigaciones sobre la Regeneración de Selvas altas en Veracruz, México,
CECSA, Mexico, pp. 70-111.
Thomas, S. C. and Bazzaz, F. A. 1999. Asymptotic height as a predictor of
photosynthetic characteristics in Malaysian rain forest trees. Ecology, 80, 16071622.
Walters, M.B., Kruger, E.L., Reich, P.B., 1993. Relative growth-rate in relation to
physiological and morphological traits for northern hardwood tree seedlings species, light environment and ontogenic considerations. Oecologia, 96, 219-231.
Welden, C.W., Hewett, S.W., Hubbell, S.P., Foster, R.B., 1991. Sapling survival, growth,
and recruitment - relationship to canopy height in a Neotropical forest. Ecology,
72, 35-50.
Whitmore, T.C., 1989. Canopy gaps and the two major groups of forest trees. Ecology,
70, 536-538.
6. SYNTHESIS AND IMPLICATIONS
Deforestation of tropical habitats is occurring at a rapid and in many places
accelerating pace (Bawa and Dayanandan, 1997). Conservation efforts only may not be
enough to preserve the forest, given the inevitable lost of species in fragmented forest
(Turner, 1996). However, at the same time that deforestation is taking place, tens of
thousands of hectares of denuded land are annually abandoned to succession back to
forest (Moran et al., 1994). Restoration around forest remnants, abandoned land
undergoing secondary succession, and open areas is urgently needed to decrease the
impact of fragmentation in border areas and to protect the remaining core forest.
Restoration ecology uses natural succession as basic tool; this managed
succession may have a variety of objectives (Higgs, 1997, Parker 1997; also Howe 1994,
1999). Recovery of gross ecosystem functions, such as material retention and loss, energy
inputs and outputs, and the outlines of food-web structure may require only a small
subset of the 30 to 100 tree species ha-1 representative of forest structure in tropical
Mexico (see Ehrenfeld and Toft, 1997, Palmer et al., 1997). To recover and maintain the
high biodiversity of the tropical forest characterized by myriads of plant-animal
interactions, many more species are needed.
Which species should be chosen to start restoration projects depends on particular
circumstances. Land is abandoned in different degrees of perturbation; a gradient of
perturbation may go from little in small clearings of different size surrounded by mature
113
114
forest to highly degraded abandoned land covered by exotic grasses. In most of the cases,
small seeded, highly vagile pioneer species are in the soil bank or arrive by dispersal
events; they establish first after a perturbations occur, growing fast under high light
levels.
Abandoned lands far from the sources of forest seeds may remain under “arrested
succession” as grasslands for long time (Zanne and Chapman, 2001). In these places
succession does not start because of the lack of seeds of pioneer species (Nepstad et al.,
1990, Holl, 1999). If and when pioneer trees do arrive, they soon provide a canopy that
shades and kills grasses, thereby immediately improving the micronenvironmental
conditions required by other tree species for germination and establishment. In places
under arrested succession, the planting of pioneer species is mandatory, they will restore
ecosystem function in a short time, and if trees bearing fleshy fruits are planted, birds and
bats will be attracted, and they will further increase biodiversity by dropping seeds of
other species.
However, the planting of only pioneer species in restoration projects is not totally
desirable. During the normal process of secondary succession in neotropical habitats, a
mixture of fast growing pioneer species and a species-poor cohort of long-lived tree
species establish for up to several decades (e.g., Denslow, 1985, Uhl et al., 1988,
Guariguata et al., 1997). Pioneer species show low survival per capita and low diversity
as a group (González-Montagut, 1996; Martínez-Ramos, 1985), therefore, few pioneer
species dominate perturbed areas. This pioneer forest will not resemble the original
forest for a long time, if ever.
115
A pioneer forest may provide ecological services (i.e. forest cover, soil retention),
however, some biological function will not be there. Once a canopy of pioneer species
exists, species diversity may keep increasing due to input of seeds brought by birds and
bats attracted to these places. However, the intrinsic low dispersal ability of most deepforest, non-pioneer species may preclude their presence in extensive second-growth
forests far from large remnants for many decades to centuries.
A general consequence of natural or human-induced secondary succession with
dispersal limitation of deep forest species is that isolated forest remnants may be
surrounded for decades by species-poor assemblages of a subset of local early
successional trees which overall comprise ≤ 20% of tropical tree species (MartínezRamos, 1994, Welden et al., 1991). Here, “letting nature takes its course” encourages
continuing random species loss from primary forest remnants during what could be
recovery of floristic and faunistic diversity in and near forest fragments (see Janzen,
1988). A second general consequence is that this usual process of secondary succession
precludes recovery of biotic diversity representative of either forests prior to
deforestation, or of remaining fragments, for decades. Restoration efforts in these places
should ecourage the increase of biodiversity of deep forest species with low dispersal
ability that otherwise may reach the secondary forest very slowly, if at all.
Most tree species in the highly diverse mature forest are deep-forest, non-pioneer
species (80 %, Martínez-Ramos, 1985). They germinate and establish inside the forest in
shade (Swaine and Whitmore, 1988) and are usually long-lived species, although there
are many exceptions in more species-rich tropical forests (Foster et al., 1986). Even when
these species are those that sustain the highly diverse myriad of biological interactions,
116
they are not used in restoration projects for a number of reasons: non-pioneer species
show lower growth rates than pioneer species (Swaine and Whitmore, 1988), therefore,
planting only these species will delay the recovery of highly desired ecosystem functions
(i.e., soil retention). More important, the little knowledge about non-pioneers survival and
growth outside the forest preclude their use in restoration porjects. Given that nonpioneer tropical tree species provide much of the structural diversity as well as food
resources for fruit- and seed-eating animals, they should be used to increase biodiversity
in early successional ecosystems and planted as mixed stands with pioneer species in
places under arrested succession. These plantings should sharply accelerate the process of
re-vegetation of complex communities. Two to 10 years may be lost in slower growth of
some trees, but decades saved in total community recovery.
Dozens of non-pioneer species have been evaluated for survival and growth rates
in abandoned pastures (Haggar et al., 1998, Leopold et al., 2001), while no information
exist on their performance in places undergoing secondary succession. Given the high
biodiversity in tropical ecosystems, it is impractical to hope to test more than a small
fraction of individual species under certain conditions. One approach is to determine
vegetative characteristics that predict success in survival and growth of trees under the
stressful conditions of open pasture or abandoned land undergoing secondary succession,
and then use those characteristics as criteria for selection of species to enrich or dominate
forest restorations.
Determination of which trait or traits best predict(s) species survival and growth
in different scenarios of restoration (i.e. early successional ecosystems, pastures) will
obviate the need to test all tropical tree species individually to decide which of them to
117
use. Maximizing survival per planted seedling reduce the cost of nursery maintenance
and replanting in restoration projects. By resolving which trait is a better predictor of
species growth rates in in different restoration scenarios we will minimize the time
needed to regenerate a forest of high structural and species diversity.
How can one predict survival and growth rates of tropical tree species under
different scenarios of restoration? To survive, plants need to display a minimum leaf area
(Kohyama 1987); to grow, photosynthetic products should be sufficient to maintain and
increase shoot and root biomass. Morphological and physiological adjustments in plant
traits to different microenvironmental conditions that occur within the forest are in part
responsible of the higher survival and growth of individuals in variable environments
(King, 1994). This phenotypic plasticity allow plants to survive and grow in a wide range
of environmental conditions
The phenotypic plasticity in leaf traits shows predictable behavior for different
levels of light and water. Individuals exposed to sun conditions develop leaves with
higher leaf mass per unit area (specific leaf mass; SLM), higher leaf water content (WC:
fresh leaf weight-dry leaf weight/ leaf area, g m-2) and thicker leaves, and lower stomatal
density in comparison with shade leaves (Popma et al., 1992, Oberbauer and Strain,
1986, Pearcy and Sims, 1994). These traits increase whole-plant productivity by
maximizing photosynthesis and minimizing loss of water (Björkman, 1981, Bongers and
Popma, 1988, Popma et al., 1992). Reduction in leaf area and increase in thickness in sun
conditions alleviates heat load and decreases loss of water (Chiariello, 1984). On the
other hand, plants in shade have larger leaves for light capture and maximization of
sunfleck use.
118
The amount of phenotypic plasticity that a species displays may depend on the
environmental heterogeneity that it has to endure through its ontogenetic development
and to the most prevalent environmental conditions that it experiences. At Los Tuxtlas,
Veracruz, Mexico, I measured leaf traits in eight late-successional tree species at three
ontogenetic stages (seedlings, juveniles and adults) and at contrasting light levels (sun vs.
shade). I found that seedlings, juveniles and adults showed similar phenotypic plasticity
in leaf traits (leaf flexibility; the ratio of sun and shade measurement in leaf traits) for leaf
size, SLM, leaf density, water content and toughness, though higher leaf flexibility in
thickness and physiological attributes were found for adults compared to juveniles in the
ivy, Hedera helix for contrasting light levels (Hoflacher and Bauer, 1982). Individuals of
tropical tree species are exposed to horizontal and vertical light gradient inside the forest
and they are able to adjust their leaf traits at all ontogenetic stages perhaps better than
species in other ecosystems with less environmental heterogeneity.
The most prevalent environmental conditions that a tree species experiences for
most of its life may be represented by its height (Thomas, 1996, Westoby, 1998). For 36
Malaysian tropical tree species, it was found that leaf size, measured in adults fallen
leaves and juveniles freshly leaves, decrease from juveniles to adult stage for tall species
while short species show the opposite trend (Thomas and Ickes, 1995). For 28 Malaysian
tropical tree species, it was found for SLM, that taller species showed higher SLM at
adult stage than conspecific juveniles and the direction of this change was similar for
short species but the magnitude of this change was higher for taller species (Thomas and
Bazzaz, 1999). For eight late-successional species which maximal tree height that ranges
from 8 to 40 m, I found that taller species show higher change in leaf size and SLM in
119
different ontogenetic transitions (ontogenetic leaf variability) than short species, which
agrees with the previous studies even when a different measure of tree height was used.
The best measure of tree height is the average final height of a population of a
given species; this is called asymptotic tree height (Thomas, 1996). For my study, longterm growth records were not available, only range of maximal tree height. Maximal tree
height refers to “champion trees”, for which final size is affected by environmental and
genetic variation. For Los Tuxtlas, this data was taken from Ibarra-Manriquez and Sinaca
(1995, 1996, 1996a). Therefore, even when caution in using “champion tree” data is
mandatory (Thomas, 1996), existing data of maximal tree height is a useful first
approach.
Non-pioneer species that reach the canopy (tall species) are exposed to a higher
heterogeneity in light levels and water availability than short species during their
expansion to attain the canopy, but once there, they experience the highest light levels in
the upper part of their crown. Those species that inhabit the understory all of their lives
show lower ability of changing leaf traits through ontogeny given that they may remain in
the dark understory from seedlings to adult stages. How will the variability in leaf traits,
related to prevalent habitat that adults experience aid to predict performance of species in
different scenarios of restoration?
In extensive abandoned pastures, where no natural regeneration is taking place,
high light conditions and low water availability are the prevalent environmental
conditions. Therefore, leaf traits related to high light conditions might provide the means
to better survive and grow there, and taller species are expected to show those leaf traits.
From all leaf traits previously mentioned, SLM have been found to better correlate with
120
growth rates for many species in many ecosystems (e.g. Grime et al., 1997; Reich et al.,
1998; Westoby, 1998). For twelve late-successional tree species growing in pastures
where incoming vegetation was cut once a month to mimic arrested succession, I found
that, mean SLM measured in individuals growing in pastures (high light levels), or mean
SLM and mean Leaf density measured in the closest secondary forest (lower light levels),
to some extent predict growth rates in diameter for individuals growing in pasture
environments. Those species that show lower mean SLM show higher growth rates than
those species with higher mean SLM, with regressions coefficient (R2) that range from
0.27 to 0.45. This agrees with previous studies done under controlled conditions, for
example Grime and 28 colleagues (1997) found a Spearman rank correlation coefficient
of - 0.50 of growth rates with SLM, while Reich and colleagues (1998) found a Pearson
correlation coefficient of - 0.90 for growth of nine boreal species with their SLM. The
lower regression coefficient that I found are possible due to the error components
associated to measurements in the field: unknown environmental conditions during the
development of leaves and the genetic variation in leaf traits independent of
environmental conditions.
A greenhouse experiment with two late-successional tree species further supports
my results from the field. Brosimum alicastrum and Pouteria campechiana were grown
in pots under three light levels (30, 50 and 100 % availability) and two water
availabilities (50 and 70 % of field capacity) during 6 months. Pouteria showed higher
increments in height than Brosimum (3.76 ± 0.1 and 1.06 ± 0.01 cm / month
respectively). The significant interaction between species and light levels (Table XXVI,
Appendix L) revealed that Brosimum showed significantly higher increments in height at
121
30 % of light than at 100 % while Pouteria showed similar increments in height at all
light levels (Figure 17, Appendix M). Species identity and light levels significantly
affected leaf traits (Table XXVII, Appendix N and Table XXVIII, Appendix O). The
regression of Log of Increments in height on mean SLM per each combination of light
and water availability (Figure 18, Appendix P) showed the same pattern observed in field
conditions: those individuals and species with low mean SLM show higher growth rates.
Secondary forest has become a large portion of tropical forests (Moran et al.,
1994). The increase of plant biodiversity with species that show very high dispersal
limitation is mandatory if lost animal diversity is to eventually recover. If mean leaf traits
(specifically leaf density and SLM) predicted increments in height for plants growing
under one set of environmental conditions, the variation of leaf traits might explain the
survival and growth rates of late-successional species growing in the different
microhabitats of an early successional environment (i.e., secondary forest, edge and open
pastures). For 23 late-successional tropical tree species I found that the intraspecific
variation in SLM (measured as the coefficient of variation of SLM) explained survival
and growth of individuals in early successional environments. Those species with higher
variation in SLM showed higher mean increments in height and in diameter across the
different microhabitats of an early successional environment.
Maximal tree height was not correlated with survival and growth in early
successional ecosystems in this study, as was expected. Thomas (1996), found that
asymptotic maximal tree height predicted growth rates for adults and saplings of 28
Malaysian tree species. I did not find these correlations perhaps because I used maximal
122
tree height that refers to “champion trees” (trees favored by genetic and particular
environments; Thomas 1996), instead of asymptotic tree height.
Mean SLM and its variation offer easily-measured variables that may provide two
of several criteria for selection of species for planting mixed species stands. For example,
if a site far from sources of forest seeds is to be restored, a mix of pioneer and nonpioneer species should be planted there. Samples of leaves of as many as possible nonpioneer species from the region should be taken and evaluated for leaf traits. Three to five
leaves from at least three individuals per species in only one microhabitat (sun or shade
conditions) and one ontogenetic stage (saplings or adults) should be taken. Data about
tree height and fruit type should be gathered when possible. Those non-pioneer species
with lower mean SLM or leaf density will show higher survival and growth rates in longlasting high light conditions. A mix of those species and all known pioneer species
should be planted. A high number of seeds of pioneer species will be needed because of
their high initial mortality. Further selection of non-pioneer species may be done by fruit
type, seed size, attractiveness to particular animal dispersal agents, and other desired
criteria.
For places alredy undergoing secondary succession, pioneer species might already
be there. In this case, samples of leaves of as many as possible non-pioneer species,
preferably those with the lowest dispersal ability should be evaluated for leaf traits. Three
to five leaves per individual per species in different microhabitats should be evaluated:
understory, gaps or borders and open areas when possible. Only one ontogenetic stage
should be used, if adults are sampled, then, sun leaves at the top of the crown and shade
leaves from the bottom of the crown can be used to evaluate variation in leaf traits. Also,
123
since variation in leaf traits is related to maximal tree height, tall trees may be choosen
for further evaluation of leaf traits. A mix of as many non-pioneer species as possible
should be planted, if necessary pioneer individuals should be cut or they canopy reduced.
Further selection of species by local use or fruit type can be done to generate the desired
restored forest.
6.1
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APPENDICES
127
128
APPENDIX A
TABLE XVI
LEAF SIZE MEASURED IN EIGHT TROPICAL TREE SPECIES AT THREE ONTOGENETIC STAGES IN LOS TUXTLAS,
VERACRUZ, MEXICO 1
ONTOGENETIC STAGE
ADULT
JUVENILE
SEEDLING
HABITAT
SUN
SHADE
SUN
SHADE
SUN
SHADE
Calophyllum brasiliense
30.9 ± 1.7
36.3 ± 1.3
34.1 ± 2.7
33.3 ± 2.8
39.3 ± 2.3
35.1 ± 3.1
Brosimum alicastrum
51.8 ± 2.4
51.8 ± 2.6
77.9 ± 4.8
62.4 ± 3.6
29.0 ± 2.8
28.1 ± 3.7
Eugenia inirebensis
23.5 ± 1.0
21.6 ± 0.7
25.2 ± 1.5
22.7 ± 2.1
37.3 ± 3.6
27.9 ± 1.7
Pouteria rhynchocarpa
24.9 ± 0.8
33.7 ± 0.9
28.6 ± 1.3
27.6 ± 1.4
26.5 ± 2.7
47.2 ± 3.0
Licaria velutina
152.1 ± 4.3
149.7 ± 6.2
175.7 ± 6.5
127.4 ± 4.8
Pimenta dioica
39.1 ± 1.8
60.1 ± 2.5
53.1 ± 3.0
62.2 ± 6.7
28.9 ± 1.3
37.4 ± 4.5
Amphitecna tuxtlensis
43.7 ± 2.1
41.6 ± 1.7
40.0 ± 2.5
41.3 ± 2.1
37.1 ± 2.4
31.6 ± 2.8
Nectandra ambigens
26.8 ± 1.4
39.9 ± 2.2
58.9 ± 3.1
83.3 ± 6.7
42.7 ± 3.9
38.4 ± 2.8
SPECIES
1 Means and standard errors of Leaf size (cm2)
168.9 ± 14
87.0 ± 6.4
129
APPENDIX B
TABLE XVII
SLM MEASURED IN EIGHT TROPICAL TREE SPECIES AT THREE ONTOGENETIC STAGES IN LOS TUXTLAS,
VERACRUZ, MEXICO 1
ONTOGENETIC STAGE
ADULT
JUVENILE
SEEDLING
HABITAT
SUN
SHADE
SUN
SHADE
SUN
SHADE
Calophyllum brasiliense
85.6 ± 2.9
70.5 ± 1.6
64.2 ± 1.4
54.9 ± 1.4
57.2 ± 5.5
55.7 ± 3.6
Brosimum alicastrum
80.0 ± 2.5
61.2 ± 1.4
47.2 ± 1.0
58.3 ± 1.3
61.1 ± 1.9
40.3 ± 1.1
112.1 ± 4.8
82.8 ± 2.6
69.6 ± 2.2
68.5 ± 1.5
66.3 ± 3.1
72.8 ± 4.3
92.5 ± 1.1
71.4 ± 1.5
81.3 ± 2.9
55.1 ± 1.1
76.5 ± 3.1
60.7 ± 1.9
Licaria velutina
111.8 ± 4.2
103. 9 ± 3.8
97.6 ± 2.2
77.8 ± 2.0
99.5 ± 3.8
64.9 ± 1.2
Pimenta dioica
125.8 ± 3.2
100.0 ± 3.9
138.8 ± 13.3
76.5 ± 7.4
96.3 ± 2.7
67.5 ± 1.9
Amphitecna tuxtlensis
67.7 ± 1.6
56.5 ± 0.8
51.2 ± 2.2
51.4 ± 1.6
43.3 ± 3.0
59.7 ± 2.9
Nectandra ambigens
110.7 ± 2.9
91.5 ± 2.0
92.2 ± 1.6
71.0 ± 1.3
64.5 ± 3.2
67.2 ± 1.5
SPECIES
Eugenia inirebensis
Pouteria rhynchocarpa
1
Mean ± standard error of specific leaf mass (g m-2)
130
APPENDIX C
TABLE XVIII
LEAF DENSITY MEASURED IN EIGHT TROPICAL TREE SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO 1
ONTOGENETIC STAGE
ADULT
JUVENILE
SEEDLING
HABITAT
SUN
SHADE
SUN
SHADE
SUN
SHADE
Calophyllum brasiliense
0.36 ± 0.01
0.33 ± 0.01
0.35 ± 0.01
0.40 ± 0.02
0.31 ± 0.03
0.36 ± 0.02
Brosimum alicastrum
0.45 ± 0.01
0.45 ± 0.01
0.43 ± 0.01
0.43 ± 0.01
0.40 ± 0.01
0.48 ± 0.02
Eugenia inirebensis
0.52 ± 0.02
0.41 ± 0.01
0.41 ± 0.02
0.48 ± 0.03
0.33 ± 0.01
0.34 ± 0.02
Pouteria rhynchocarpa
0.64 ± 0.01
0.54 ± 0.01
0.58 ± 0.02
0.53 ± 0.02
0.73 ± 0.04
0.53 ± 0.02
Licaria velutina
0.44 ± 0.01
0.43 ± 0.01
0.44 ± 0.01
0.41 ± 0.01
0.53 ± 0.02
0.50 ± 0.02
Pimenta dioica
0.47 ± 0.01
0.41 ± 0.01
0.42 ± 0.01
0.39 ± 0.03
0.5 ± 0.02
0.41 ± 0.01
Amphitecna tuxtlensis
0.39 ± 0.01
0.36 ± 0.01
0.37 ± 0.01
0.45 ± 0.02
0.41 ± 0.04
0.83 ± 0.05
Nectandra ambigens
0.55 ± 0.01
0.47 ± 0.01
0.52 ± 0.02
0.41 ± 0.01
0.65 ± 0.04
0.60 ± 0.03
SPECIES
1
Mean ± standard error of Leaf Density
131
APPENDIX D
TABLE XIX
LEAF TOUGHNESS MEASURED IN EIGHT TROPICAL TREE SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO 1
ONTOGENETIC STAGE
ADULT
JUVENILE
SEEDLING
HABITAT
SUN
SHADE
SUN
SHADE
SUN
SHADE
Calophyllum brasiliense
127.1 ± 2.4
122.1 ± 2.2
101.8 ± 2.3
101.2 ± 4.1
Brosimum alicastrum
115.2 ± 3.6
97.7 ± 4.0
93.6 ± 5.4
100.4 ± 4.8
Eugenia inirebensis
115.6 ± 2.7
121.0 ± 3.9
98.99 ± 5.4
97.7 ± 7.1
126.1 ± 8.7 118.8 ± 7.5
Pouteria rhynchocarpa
115.6 ± 3.9
106.8 ± 2.8
120.7 ± 4.4
102.1 ± 4.4
130.6 ± 6.3 113.3 ± 4.6
Licaria velutina
132.4 ± 4.3
130.1 ± 3.4
123.9 ± 6.2
117.9 ± 4.3
107.5 ± 6.3
78.3 ± 3.8
Pimenta dioica
147.2 ± 3.6
142.6 ± 2.5
151.2 ± 2.2
90.2 ± 3.5
151.8 ± 5.7
139.5 ± 4.1
Amphitecna tuxtlensis
158.0 ± 2.1
152.4 ± 2.2
141.6 ± 5.2
160.9 ± 2.6
114.7 ± 12.8 115.1 ± 8.2
Nectandra ambigens
144.5 ± 2.8
144.8 ± 2.3
140.3 ± 3.5
135.5 ± 3.8
122.6 ± 3.1 123.0 ± 4.2
SPECIES
1
Mean ± Standard Errors of Toughness (g)
98.5 ± 8.2 106.1 ± 6.6
117.5 ± 9.5
68.2 ± 5.3
132
APPENDIX E
TABLE XX
LEAF WATER CONTENT MEASURED IN EIGHT TROPICAL TREE SPECIES AT THREE ONTOGENETIC STAGES IN LOS
TUXTLAS, VERACRUZ, MEXICO 1
ONTOGENETIC STAGE
ADULT
JUVENILE
SEEDLING
HABITAT
SUN
SHADE
SUN
SHADE
SUN
SHADE
Calophyllum brasiliense
149.2 ± 2.9
141.5 ± 2.7
123.7 ± 5.4
90.6 ± 5.1
131.0 ± 7.1
97.3 ± 4.7
Brosimum alicastrum
103.0 ± 4.5
77.6 ± 2.9
62.7 ± 2.1
79.7 ± 3.7
91.6 ± 3.7
46.2 ± 3.7
Eugenia inirebensis
102.6 ± 4.8
118.1 ± 3.2
109.1 ± 7.3
85.3 ± 6.9
131.9 ± 4.9
140.5 ± 6.7
55.2 ± 2.7
64.7 ± 2.5
60.4 ± 3.6
53.3 ± 4.0
31.9 ± 6.1
55.4 ± 4.1
Licaria velutina
140.4 ± 5.6
135.1 ± 2.1
127.1 ± 3.5
110.8 ± 3.2
88.0 ± 5.1
66.5 ± 4.4
Pimenta dioica
145.1 ± 3.8
139.2 ± 2.5
195.5 ± 19.8
128.1 ± 16.3
96.5 ± 5.1
99.4 ± 5.4
Amphitecna tuxtlensis
107.9 ± 2.6
102.1 ± 2.3
89.3 ± 3.9
68.9 ± 4.0
66.5 ± 5.6
30.1 ± 5.6
Nectandra ambigens
93.5 ± 3.8
106.2 ± 3.1
94.3 ± 5.9
104.6 ± 2.8
41.2 ± 5.5
47.8 ± 5.3
SPECIES
Pouteria rhynchocarpa
1
Mean ± standard errors of Water Content (g m-2)
133
APPENDIX F
TABLE XXI
UNIVARIATE ANALYSIS OF VARIANCE OF FOLIAR FLEXIBILITY OF EIGHT TROPICAL NON-PIONEER TREE SPECIES
IN LOS TUXTLAS, VERACRUZ, MEXICO 1
SPECIES
FOLIAR FLEXIBILITY
LEAF SIZE
SLM
LEAF DENSITY
TOUGHNESS
WATER CONTENT
F (7,56) = 2.7*
F (7,56) = 4.4***
F (7,56) = 9.3****
F (7,56) = 3.23*
F (7,56) = 8.19***
Nectandra ambigens
0.99 ± 0.02
1.18 ± 0.10
1.00 ± 0.05
1.01 ± 0.04
1.23 ± 0.07
Brosinum alicastrum
1.17 ± 0.10
1.21 ± 0.10
0.94 ± 0.02
1.30 ± 0.15
1.43 ± 0.15
Calophyllum brasiliense
1.14 ± 0.10
1.10 ± 0.10
1.03 ± 0.06
1.01 ± 0.04
1.01 ± 0.07
Pimenta dioica
0.80 ± 0.10
1.35 ± 0.10
1.31 ± 0.10
1.14 ± 0.04
0.80 ± 0.12
Eugenia inirebensis
1.53 ± 0.20
1.31 ± 0.10
1.05 ± 0.02
1.16 ± 0.07
1.17 ± 0.07
Licaria velutina
0.81 ± 0.10
1.55 ± 0.20
1.14 ± 0.05
1.29 ± 0.12
1.28 ± 0.24
Amphitecna tuxtlensis
1.10 ± 0.10
0.97 ± 0.10
0.79 ± 0.10
0.98 ± 0.10
1.71 ± 0.36
Pouteria rhynchocarpa
0.86 ± 0.10
1.16 ± 0.10
1.25 ± 0.01
1.01 ± 0.02
0.90 ± 0.06
1
Flexibility is the ratio of sun over shade value in leaf characteristics for pairs of individuals growing under contrasting light levels.
Means ± standard errores are reported. * P < 0.05, *** P < 0.0005, **** P < 0.0001
134
APPENDIX G
TABLE XXII
FAMILY, COEFFICIENT OF VARIATION OF LEAF TRAITS AND SAMPLE SIZE OF 23 LATE-SUCCESSIONAL TROPICAL
TREE SPECIES
Species
Family
CV Leaf size
CV SLM
CV Leaf density
CV Water Content
N
Ampelocera hottlei
Ulmaceae
29.08
6.82
11.76
22.14
89
Amphitecna tuxtlensis
Bignoniaceae
14.65
21.02
20.4
18.79
83
Calophyllum brasiliense
Clusiaceae
22.64
27.60
6.97
15.37
66
Ceiba petandra
Bombacaceae
34.88
26.66
8.3
14.27
9
venezuelanense
Sapotaceae
30.07
7.30
14.17
25.85
47
Cojoba arborea
Mimosaceae
43.13
27.30
19.61
44.67
62
Cordia megalantha
Boraginaceae
49.04
24.09
17.27
26.27
50
Cordia stellifera
Boraginaceae
17.41
29.47
8.35
16.00
149
Couepia polyandra
Chrysobalanaceae
33.71
16.62
15.63
23.06
47
Eugenia inirebensis
Myrtaceae
26.51
6.57
3.22
6.94
38
Guarea grandifolia
Meliaceae
34.01
15.48
11.64
11.79
32
Hirtella triandra
Chrysobalanaceae
56.38
14.49
17.11
28.00
13
Inga sinacae
Mimosaceae
52.40
25.11
13.25
19.05
64
Chrysophyllum
135
TABLE XXII (continued)
Species
Family
CV Leaf size
CV SLM
CV Leaf density
CV Water Content
N
Licaria velutina
Lauraceae
29.88
15.30
7.2
9.15
115
Lonchocarpus cruentus
Fabaceae
57.59
51.49
30.56
41.84
112
Nectandra ambigens
Lauraceae
31.64
20.0
14.93
11.37
125
Persea schiedeana
Lauraceae
35.43
27.74
13.1
14.93
9
Pimenta dioica
Myrtaceae
33.33
21.08
15.4
25.41
55
Poulsenia armata
Moraceae
20.49
18.40
6.63
22.36
12
Pouteria rhynchocarpa
Sapotaceae
21.17
10.63
13.15
22.79
105
Rheedia edulis [Garcinia intermedia] Clusiaceae
24.41
8.49
2.12
9.02
31
Sapindus saponaria
Sapindaceae
40.68
12.28
30.93
63.27
90
Trichilia havanensis
Meliaceae
43.69
14.23
11.58
13.16
38
Virola guatemalensis
Myristicaceae
38.74
19.63
6.81
12.74
235
136
APPENDIX H
Log Increment Height (understory) = -0.22 + 0.04 CV SLM
2
R = 0.37, P< 0.05 N=10
Log of Increment in Height
1.0
Trhe
0.8
0.6
Insi
Cepe
Coar
Pesc
Live
Sasa
0.4
Vigu
Poar
Chve
0.2
Cost
Copo
Neam
Pidi Come
Cabr
Porh
Gugr
Hitr
Amtu
0.0
Euin
Amho
-0.2
-0.4
2
6
Log Increment Height (canopy) = -0.195 + 0.03 CV SLM
2
R = 0.35, P< 0.05, N=13
Rhed
10
14
18
22
26
30
34
Coefficient of Variation of SLM
Figure 16. Regressions of the Log of monthly Increment in height on the
coefficient of variation of SLM for canopy and understory species growing in an
experimental planting in the Cooperative of Lazaro Cárdenas, Los Tuxtlas,
Mexico. Incremental growth refers to one mean of three periods of growth from
1998 to 2001. Open circles and thick line correspond to canopy and emergent
species (> 25 m). Filled circles and thin line correspond to understory species.
The key for the species follows Table X.
137
APPENDIX I
TABLE XXIII
SURVIVAL OF 12 LATE-SUCCESSIONAL TROPICAL TREE SPECIES IN
PASTURES AND SECONDARY FORESTS
Species
Family
N
Survival %
Survival %
Secondary
Pasture
Forest
Amphitecna tuxtlensis
Bignoniaceae
106
94
65
Calophyllum brasiliense
Clusiaceae
21
83
73
Chrysophyllum mexicanum
Sapotaceae
87
90
100
Coccoloba hondurensis
Polygonaceae
83
96
80
Cymbopetalum baillonii
Annonaceae
63
77
39
Diospyros digyna
Ebenaceae
49
85
72
Guarea grandifolia
Meliaceae
37
84
44
Nectandra ambigens
Lauraceae
65
94
81
Omphalea oleifera
Euphorbiaceae
94
91
78
Pouteria campechiana
Sapotaceae
59
93
76
Rheedia edulis [Garcinia intermedia] Clusiaceae
72
93
63
Sapotaceae
68
83
56
Sideroxylon portoricense
138
APPENDIX J
TABLE XXIV
LEAF TRAITS AND TOTAL NUMBER OF INDIVIDUALS SAMPLED OF 12 LATESUCCESSIONAL TROPICAL TREE SPECIES
Species
N
Leaf size1
SLM (g /m2) WaterContent2 Leaf density
Amphitecna tuxtlensis
54
21.9 ± 1.5
71.8 ± 2.8
81.5 ± 5.3
0.50 ± 0.02
Calophyllum brasiliense
13
35.1 ± 3.3
109.8 ± 4.1
152.6 ± 11.3
0.43 ± 0.03
Chrysophyllum mexicanum
50
15.2 ± 0.9
74.7 ± 2.1
99.0 ± 6.4
0.47 ± 0.02
Coccoloba hondurensis
50
64.7 ± 4.6
71.4 ± 2.2
131.2 ± 5.7
0.36 ± 0.01
Cymbopetalum baillonii
22
19.8 ± 2.6
50.0 ± 2.2
116.6 ± 6.9
0.31 ± 0.02
Diospyros digyna
34
42.1 ± 3.6
85.6 ± 1.9
114.1 ± 3.3
0.43 ± 0.01
Guarea grandifolia
11
32.8 ± 4.9
59.1 ± 3.2
149.9 ± 16.2
0.32 ± 0.05
Nectandra ambigens
37
61.1 ± 4.2
87.7 ± 2.5
123.32 ± 6.2
0.43 ± 0.02
Omphalea oleifera
42
176.9 ± 13.9
36.4 ± 2.6
146.3 ± 7.9
0.20 ± 0.01
Pouteria campechiana
33
32.2 ± 2.5
68.3 ± 2.9
82.7 ± 5.1
0.46 ± 0.02
[Garcinia intermedia]
35
14.5 ± 0.8
115.7 ± 4.3
116.4 ± 9.9
0.54 ± 0.03
Sideroxylon portoricense
34
24.2 ± 2.7
70.9 ± 3.5
89.0 ± 5.5
0.45 ± 0.01
Rheedia edulis
1
cm2
2
g /m2
139
APPENDIX K
TABLE XXV
PEARSON CORRELATION AMONG LEAF TRAITS MEASURED IN PASTURES AND SECONDARY FOREST FOR 12 TREE
SPECIES AT LOS TUXTLAS, VERACRUZ, MEXICO1,2
Leaf size S F 3
Leaf size Sec Forest
1.00
Leaf size Pasture
0.98****
Leaf size P
SLM Sec For
SLM P4
WC Sec Forest
-0.40
-0.48
1.00
SLM Pasture
-0.43
-0.50
0.96****
1.00
Water Content S F
0.45
0.44
0.27
0.38 *
1.00
Water Content P
0.42
0.52
-0.27
0.38 *
0.57 ***
Leaf Density S F
0.68*
1
-0.53
1.00
-0.75**
0.79**
0.82**
-0.35
-0.65*
1.00
-0.64*
0.74**
0.81**
-0.25
-0.83**
0.91***
Pearson correlation and Bonferroni probabilities
* P < 0.05, *** P < 0.001, ****P < 0.0001
3
Secondary Forest
4
Pastures
2
L Density S F
1.00
SLM Sec Forest
Leaf Density P
Water C P
140
APPENDIX L
TABLE XXVI
SUMMARY OF UNIVARIATE ANALYSIS OF VARIANCE OF INCREMENTS IN
HEGHT FOR BROSIMUM ALICASTRUM AND POUTERIA CAMPECHIANA
FROM A GREENHOUSE EXPERIMENT
MAIN FACTOR
DF
F
P<
Species
1, 97
159.6
0.00001
Light Levels
2,97
2.2
0.10000
Water Availability
1,97
0.5
0.40000
Species * Light Levels
2,97
6.7
0.00100
Species * Water availability
1,97
0.1
0.70000
Light levels * Water availability
2,97
0.3
0.90000
Species * Light * Water
2,97
0.5
0.50000
141
APPENDIX M
0.7
Log of Increment in Height
0.5
d
100 %
50 %
30 %
d
d
0.3
b
0.1
a
-0.1
-0.3
ab
Brosimum
Pouteria
Species
Figure 17. Log increments in Height measured in Brosimum alicastrum and Pouteria
campechiana individuals growing in a greenhouse experiment at three light levels
(30, 50 and 100 % of availability) and two water levels (50 and 70 % of field
capacity).
142
APPENDIX N
TABLE XXVII
SUMMARY OF MULTIVARIATE ANALYSIS OF VARIANCE OF LEAF TRAITS
OF BROSIMUM ALICASTRUM AND POUTERIA CAMPECHIANA GROWING IN
A GREENHOUSE EXPERIMENT AT THREE LIGHT LEVELS (30, 50 AND 100 %
OF AVAILABILITY) AND TWO WATER LEVELS (50 AND 70 % OF FIELD
CAPACITY).
WILKS ‘ LAMBDA
RAO ‘S
DF 1
P<
Species
.21
66.9
4, 148
.00001
Light availability
.32
14.1
8, 148
.00001
Water availability
.93
1.2
4, 148
.20000
Species * Light
.59
2.4
8, 148
.00005
Species * Water
.96
0.7
4,148
.60000
Light * Water
.84
1.5
8,148
.10000
Species * Light * Water
.89
1.0
8,148
.40000
MAIN FACTOR
1
Note that the degrees of freedom for MANOVA are multiplied for the number of
dependent variables used, in this case, four variables.
143
APPENDIX 0
TABLE XXVIII.
LEAF TRAIST OF BROSIMUM ALICASTRUM AND POUTERIA CAMPECHIANA GROWING IN A GREENHOUSE
EXPERIMENT AT THREE LIGHT LEVELS (30, 50 AND 100 % OF AVAILABILITY) AND TWO WATER LEVELS (50 AND
70 % OF FIELD CAPACITY).
Brosimum alicastrum
Pouteria campechiana
High Light 100 %
Medium 50 %
Low Light 30 %
High Light 100 %
Medium 50 %
Low Light 30 %
Traits
HW
HW
LW
HW
HW
HW
LW
HW
LW
L size
16 ± 1
23 ± 2
25 ± 12
25 ± 10
55 ± 2
36 ± 7
76 ± 10
92 ± 9
106 ± 9
121 ± 13
118 ± 9
105 ± 9
SLM
68 ± 8
62 ± 6
59 ± 7
55 ± 3
45 ± 1
49 ± 1
71 ± 2
70 ± 1
56 ± 1
56 ± 2
45 ± 1
47 ± 2
WC
89 ± 7
101 ± 2
97 ± 5
105 ± 6
89 ± 2
94 ± 1
131 ± 2
136 ± 2
112 ± 3
106 ± 3
95 ± 2
103 ± 5
Density
0.4 ± 0
0.4 ± 0
0.4 ± 0
0.3± 0
0.3 ± 0
0.3 ± 0
0.4 ± 0
0.4 ± 0
0.3 ± 0
0.3 ± 0
0.3 ± 0
0.3 ± 0
LW
LW
LW
144
APPENDIX P
0.7
ML HW
HL HW
ML LW
Log of Increment in Height
0.5
LL LW
LL HW
HL LW
0.3
LL HW
LL LW
0.1
HL LW
HL HW
-0.1
ML HW
Log Increment in Height = 4.5 - 2.4 * Log SLM
2
R = 0.37, P < 0.05
-0.3
1.58
1.62
1.66
1.70
1.74
1.78
ML LW
1.82
1.86
Log of SLM
Figure 18. Regression of Log increment in height on the Log of SLM for Brosimum
alicastrum (bold letters) and Pouteria campechiana. Each point represent mean
Log increment in height and mean Log of SLM for a combination of light levels
(HL, high light levels [100 %], ML, medium [50 %] and LL, low light [30 %],
and water availability (HW, high water availability [70 %], LW, low water
[50 %]).
VITA
NAME:
Cristina Martínez-Garza
EDUCATION:
B.A., B.S., National University of Mexico (UNAM), 1996
Ph.D., Ecology and Evolution, University of Illinois at Chicago,
Chicago, Illinois, 2003
TEACHING
EXPERIENCE:
Department of Biological Sciences, UIC
Biology of populations and communities
Human Development and Reproduction
HONORS:
Ph.D. fellowship from the National Council of Science and
Technology of Mexico (1997-2002)
Lincoln Park Zoo Grant (2001, 2002)
PROFESSIONAL
MEMBERSHIPS:
PUBLICATIONS:
Botanical Society of America
Martínez-Garza, C. and R. González-Montagut. 1999. Seed rain
from forest fragment into tropical pastures in Los Tuxtlas, Mexico.
Plant Ecology, 145, 255-265
Martínez-Garza, C. and R. González-Montagut. 2002. Spatial
distribution of seed dispersed by bats into tropical pastures in Los
Tuxtlas, Mexico. Journal of Tropical Ecology, 18, 457-462
Martínez-Garza C. and H.F. Howe. Restoring tropical diversity:
beating the time tax on species loss. Journal of Applied Ecology, in
press.
Martínez-Garza, C., J. Brown and H.F. Howe. Vole effects on two
established forbs in tallgrass plantings. Ecological restoration, in
press.
Martínez-Garza C. and H.F. Howe. Inmediate and strategic
changes in leaf traits of tropical tree species. American Journal of
Botany, in review.
145
146
Martínez-Garza, C., H. F. Howe, V. Peña, M. Ricker and A.
Campos. Restoring tropical biodiversity: Predicting survival and
grow of late-successional tree species in early successional
environments. Forest Ecology and Management, in review.
Martínez-Garza, C., H. F. Howe, S. Saha, V. Torres and J. S.
Brown. Size distribution of four dicots in synthetic tallgrass
communities. Oecologia, in review.
Martínez-Garza, C., H. F. Howe, V. Peña, M. Ricker y A. Campos.
Restoring forest in sites under arrested succession: Predicting
survival and growth of late-successional tree species in longlasting pastures. In prep.
Martínez-Garza, C. Effect of light levels and water availability in
leaf characteristics of seedlings of two non-pioneer tropical tree
species. In prep.
Martínez-Garza, C. and M. Ricker. Establishment of gapdependent species in a microenvironmental gradient in pastures of
Los Tuxtlas, Veracruz, Mexico. In prep.