Age-related crown thinning: common but not universal

in tropical and temperate forest trees

by

Eadaoin Maria Ines Quinn

A thesis submitted in conformity with the requirements

for the degree of Master of Science in Forestry

Faculty of Forestry

University of Toronto

© Copyright by Eadaoin Maria Ines Quinn

ii

Age-related crown thinning: common but not universal in tropical and

temperate forest trees

Eadaoin Maria Ines Quinn

Master of Science in Forestry 2013

Faculty of Forestry

University of Toronto

Abstract

Gap dynamics theory proposes that forest canopy gaps provide the high light levels needed

for regeneration. Little attention has been given to more gradual alternatives; however, recent

studies have demonstrated declines in within-crown leaf area index with tree size in

temperate forest trees. Our project builds on this previous research by assessing the

prevalence of this age-related crown thinning phenomenon. We quantified crown openness

for 18 dominant tree species in temperate and tropical forests (n = 1786 trees). Separate

pooled groupings of tropical and temperate species showed significantly positive

relationships between openness and DBH (p<0.001). Of the 9 sampled species showing

positive relationships, significance (p< 0.05) was detected in 3 out of 10 tropical species and

1 out of 8 temperate species. Two temperate species showed significantly reduced canopy

openness with size. These trends highlight the role that very large trees play in influencing

light availability for understorey regeneration.

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Acknowledgments

I am deeply grateful for all those who helped me write this thesis. I would like to express a

special thanks to my supervisor Dr. Sean Thomas for his guidance and encouragement to

look at the bigger picture, committee members Dr. Sandy Smith and Dr. Jay Malcolm for

their insight and flexibility, labmate Laura Fernandez for those early morning boat rides and

wet afternoons in the rainforest, staff at Barro Colorado Island and El Verde Field Stations

for providing supportive working environments, and previous supervisors Dr. Jess

Zimmerman and Dr. Wayne Sousa for giving me the opportunity to assist with their field

work. This study would not have been possible without the financial support of the Natural

Sciences and Engineering Research Council of Canada and the Center for Tropical Forest

Science. While data collection, analysis, and writing were the obvious challenges of this

thesis, I would like to thank the people closest to me for personal support: my parents

Thomas and Maria Jose Quinn for continuous love and understanding and my partner Derek

Wolf for having confidence in me in moments of doubt.

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Table of Contents

Abstract ........................................................................................................................................... ii Acknowledgments.......................................................................................................................... iii

Table of Contents ........................................................................................................................... iv List of Tables ................................................................................................................................. vi List of Figures ............................................................................................................................... vii List of Appendices ......................................................................................................................... ix Chapter 1 – Framework and intention of study ...............................................................................1

1.1 Forest regeneration, gap dynamics theory, and alternative mechanisms .............................1 1.2 Age-related crown thinning .................................................................................................3

1.2.1 Potential causes of age-related crown thinning .......................................................3

1.2.2 Processes offsetting age-related crown thinning ......................................................6 1.3 Scope of work ......................................................................................................................7

Chapter 2 – Age-related crown thinning: common but not universal in temperate and

tropical forest trees ......................................................................................................................8

2.1 Introduction ..........................................................................................................................8 2.2 Methods..............................................................................................................................12

2.2.1 Study sites ..............................................................................................................12 2.2.1.2 Temperate sites ......................................................................................................12 2.2.1.3 Tropical sites ..........................................................................................................13

2.2.2 Sampling design .....................................................................................................14 2.2.2.1 Moosehorn densiometer .........................................................................................14

2.2.2.2 Measurements ........................................................................................................15 2.2.2.1 Power analysis and measurement validation .........................................................18

2.2.3 Canopy openness estimation ..................................................................................20 2.2.3.1 Observed total openness ........................................................................................20

2.2.3.2 Overlap-corrected openness ...................................................................................20 2.2.4.1 Linear and nonlinear regression analysis ...............................................................22 2.2.4.3 Comparison of functional groups using species as unit of analysis.......................22

2.2.4.4 Mean crown openness and confidence intervals ....................................................23 2.2.4.5 ANCOVA analyses ................................................................................................23

2.3 Results ................................................................................................................................24

2.3.1 Linear and nonlinear regressions of openness-DBH relationships .......................24 2.3.4 ANCOVA analysis................................................................................................35

2.4 Discussion ..........................................................................................................................37 2.4.1 Age-related crown thinning as a general phenomenon .........................................37

2.4.2 Species-specific patterns in age-related crown thinning .......................................38 2.4.3 Biome-specific patterns in age-related crown thinning ........................................41 2.4.4 Review of methods and future work .....................................................................42

2.4.1 Conclusion ............................................................................................................43 Chapter 3 – Discussion, implications, and future work .................................................................44

3.1 Overview of results, sources of error, and statistically significant effects ........................44 3.1.1 Overview of results ...............................................................................................44 3.1.1 Sources of error .....................................................................................................45

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3.1.1 Statistically significant effects ..............................................................................45

3.2 Potential explanations for observations, implications, and future work ............................46 3.2.1 Decreased crown openness with age and the Janzen-Connell hypothesis ............46 3.2.2 Liana loading ........................................................................................................48

3.2.3 Crown thinning and reproductive allocations .......................................................50 3.2.4 Physical and environmental explanations .............................................................51 3.2.5 Alternative methods in future work ......................................................................52

3.3 Concluding remarks ...........................................................................................................54 Literature Cited ..............................................................................................................................55

Appendices .....................................................................................................................................64

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List of Tables

Table 2.1: Summary of ANCOVA results for pooled data for ten tropical species sampled at

Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and

2011, and for eight temperate species sampled at Haliburton Forest, Ontario, and Koeffler

Science Reserve, Ontario, in 2009 and 2010. For each grouping, sample size (n), R2, and p-

value are shown. ..........................................................................................................................36

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List of Figures

Figure 1.1: Potential causes of age-related crown thinning .............................................................4

Figure 2.1: Power analysis of A. saccharum. Random sample with replacement from

entire data set, n = 646. Data collected at Haliburton Forest, Ontario, and Koeffler

Science Reserve, Ontario, in 2009 and 2010 ............................................................................19

Figure 2.2: Linear and nonlinear regressions for eight temperate species sampled at

Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010.

Each data point is the average of three openness readings taken on one tree. X- and y-

axes are log-transformed ...........................................................................................................25

Figure 2.3: Linear and nonlinear regressions for ten tropical species sampled at Barro

Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010

and 2011. Each data point is the average of three openness readings taken on one tree.

X- and y-axes are log-transformed ............................................................................................26

Figure 2.4: Linear regressions for eight temperate species sampled at Haliburton Forest,

Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical

species sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics

Plot, Puerto Rico, in 2010 and 2011. Each data point is the average of three openness

readings taken on one tree. X- and y-axes are log-transformed ................................................28

Figure 2.5: Linear regressions for pioneer and climax species sampled at Haliburton

Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten

tropical species sampled at Barro Colorado Island, Panama, and Luquillo Forest

Dynamics Plot, Puerto Rico, in 2010 and 2011. Each data point is the average of three

openness readings taken on one tree. X- and y-axes are log-transformed . ..............................29

Figure 2.6: Linear regressions for deciduous/semi-deciduous and evergreen species

sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009

and 2010, and ten tropical species sampled at Barro Colorado Island, Panama, and

Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011. Each data point is the

average of three openness readings taken on one tree. X- and y-axes are log-

transformed ...............................................................................................................................29

Figure 2.7: Average slopes of the relationship between crown openness and DBH for

functional groups of eighteen species sampled at Haliburton Forest, Ontario, and

Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical species sampled

at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in

2010 and 2011. Each data point is the average of three openness readings taken on one

tree. X- and y-axes are log-transformed and 95% confidence intervals are shown.. ................31

Figure 2.8: Mean crown openness with 95% confidence intervals for eight temperate

species sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario,

in 2009 and 2010. Species codes defined as ACSA = A. saccharum, FAGR = F.

grandifolia, PIST = P. strobus, QURU = Q. rubra, BEAL = B. alleghaniensis, FRAM

= F. americana, PRSE = P. serotina, and TSCA = T. canadensis. ..........................................32

Figure 2.9: Mean crown openness with 95% confidence intervals for ten tropical species

sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot,

Puerto Rico, in 2010 and 2011. Species codes defined as ALSEBL = A. blackania,

BEILPE = B. pendula, JACACO = J. copaia, PRIOCO = P. copaiferia, QUARAS =

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Q. asterolepis, TABEAR = T. arborea, TETRPA = T. panamensis, TRICTU = T.

tuberculata, BUCTET = B. tetraphylla, and MANBID = M. bidentata. ..................................33

Figure 2.10: Mean crown openness with 95% confidence intervals for ten tropical species

sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot,

Puerto Rico, in 2010 and 2011, and for eight temperate species sampled at Haliburton

Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010. ............................33

Figure 2.11: Crown openness by size class for ten tropical species sampled at Barro

Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010

and 2011. Each species was divided into two groups: one group with trees below the

median DBH and one group above the third quartile in DBH. 95% confidence

intervals are shown. Species codes defined as ALSEBL = A. blackania, BEILPE = B.

pendula, JACACO = J. copaia, PRIOCO = P. copaiferia, QUARAS = Q. asterolepis,

TABEAR = T. arborea, TETRPA = T. panamensis, TRICTU = T. tuberculata,

BUCTET = B. tetraphylla, and MANBID = M. bidentata. ......................................................34

Figure 2.12: Crown openness by size class for temperate species for eight temperate

species sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario,

in 2009 and 2010. Each species was divided into two groups: one group with trees

below the median DBH and one group above the third quartile in DBH. 95%

confidence intervals are shown. Species codes defined as ACSA = A. saccharum,

FAGR = F. grandifolia, PIST = P. strobus, QURU = Q. rubra, BEAL = B.

alleghaniensis, FRAM = F. americana, PRSE = P. serotina, and TSCA = T.

canadensis. ................................................................................................................................35

Figure 2.13: Average Crown Illumination Index and average liana scores for ten tropical

species sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics

Plot, Puerto Rico, in 2010 and 2011. Species codes defined as ALSEBL = A.

blackania, BEILPE = B. pendula, JACACO = J. copaia, PRIOCO = P. copaiferia,

QUARAS = Q. asterolepis, TABEAR = T. arborea, TETRPA = T. panamensis,

TRICTU = T. tuberculata, BUCTET = B. tetraphylla, and MANBID = M. bidentata. ...........37

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List of Appendices

Appendix 2.1: Summary of regression results between direct crown openness and DBH

for eight temperate species sampled at Haliburton Forest, Ontario, and Koeffler

Science Reserve, Ontario, in 2009 and 2010, and ten tropical species sampled at Barro

Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010

and 2011. All x- and y-axes are log-transformed. Additional linear regressions include:

overlap-corrected openness vs. DBH, openness vs. height, and openness vs. crown

depth. Average Crown Illumination Index (CII) and average liana scores (LS) also

provided for each species ..........................................................................................................64

Appendix 2.2: Summary of linear regression results for pooled data for eight temperate

species sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario,

in 2009 and 2010, and ten tropical species sampled at Barro Colorado Island, Panama,

and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011. All x- and y-axes

are log-transformed ...................................................................................................................65

Appendix 3.1: Basic life history traits for eight temperate species sampled at Haliburton

Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten

tropical species sampled at Barro Colorado Island, Panama, and Luquillo Forest

Dynamics Plot, Puerto Rico, in 2010 and 2011 ........................................................................66

1

Chapter 1 – Framework and intention of study

1.1 Forest regeneration, gap dynamics theory, and alternative

mechanisms

As soon as seeds are released from their parent tree, their fight for survival begins.

Whether they are dispersed by a gust of wind or buried in a rodent’s den, they are thrust into

the competitive dynamics of the forest ecosystem. Nutrient limitation, light exposure, water

access, stem density and exposure to herbivory are among many factors that could reduce

fitness from the moment of germination (Lutz and Halpern 2006). The race to the canopy is a

critical period during a tree’s life where a change in any one factor could mean death. As

would be expected, these early stages of tree development are intensively studied across

many biomes and forest types (Kubota and Hara 1995, Ricard et al. 2003, Schnitzer et al.

2005). Trees that have reached apparent stability after reaching canopy-level are studied

much less frequently (Kolb and Matyssek 2001). While there are many practical reasons that

later life stages of trees would receive less attention (challenge accessing large tree crowns,

difficult to follow trees through a multi-century life span, etc.), there is good reason to

believe that very large trees play a significant role in forest regeneration processes.

Gap dynamics theory posits that treefall events drive regeneration processes. These

events cause large gaps in the canopy which increase light transmittance into the understorey

to foster regeneration (March and Skeen 1976, Whitmore 1978, and Canham et al. 1990).

Aubreville (1938) was one of the first to describe the process of gap dynamics, documenting

its occurrence in the tropical forests of Cote d’Ivoire. Instead of a stable, climax tree

community that was often attributed to temperate forests at the time, Aubreville described

2

tropical forest regeneration as a cyclical, shifting mosaic. When a tree or group of trees died,

the space they leave in the canopy will be filled by pioneer trees. After the gap has been

closed, the climax tree species will then begin to outcompete the pioneer trees. Although this

theory of gap-phase regeneration can be traced back to the 1800s, it gained prominence in the

1980s (Brokaw 1982, Chazdon and Fletcher 1984, Swaine et al. 1987, Canham 1988,

Hartshorn 1989). It is now widely regarded as the primary mechanism for forest regeneration

in both temperate and tropical forests (McCarthy 2001, Gravel et al. 2010).

Tree mortality through windthrow results in an abrupt change in canopy conditions.

However, there are potentially more gradual processes influencing light transmittance and

regeneration that relate to canopy dominant trees (“very large trees”). For instance, Gandolfi

et al. (2007) noted how seasonal leaf shedding in the canopy of deciduous/semi-deciduous

forests led to gradual changes in light transmission. Putz et al. (1984) found that crown

abrasion between crowns led to the formation of inter-crown gaps. Clark and Clark (1991)

showed how small-scale losses of crown biomass in individual trees resulting from physical

damage affected light heterogeneity in the understorey. These smaller, more gradual changes

in light transmission to the understorey over time could have an effect on regeneration

processes that are not considered in the standard gap-phase model. It is apparent that

understorey light conditions fall along a continuum, rather than a neat dichotomy. Canopy

gaps and canopy closures are ubiquitous throughout the forest, but so are sun flecks and gaps

smaller than individual tree crowns (Lieberman et al. 1989). In the tightly budgeted economy

of the forest, that light is surely not being wasted. Multiple studies have documented this

continuum in light environments and the continuous nature of tree responses to this variation

3

(Canham et al. 1994, Kobe 1999, King 1999; Montgomery and Chazdon 2002, Poorter 1999,

Baltzer and Thomas 2007ab).

1.2 Age-related crown thinning

There has been little research into the idea that crowns of individual trees may

actually be thinning as they age and that the altered light conditions that result may be

affecting regeneration processes. Nock et al. (2008) made the case that the leaf area index

(LAI) declines could be happening within each aging tree, LAI being a measure of leaf area

per unit ground area, closely related to canopy openness and light transmission. They

recorded the LAI in two temperate species (Acer saccharum and Betula allegheniensis) and

detected declines in LAI with increasing tree size. To my knowledge, no other studies have

examined intra-crown age-related thinning; however, increase canopy openness during

reproduction has been noted (Innes 1994).

1.2.1 Potential causes of age-related crown thinning

Although literature on this subject is relatively sparse, there are a number of processes

known to occur that we can expect to give rise to crown thinning as trees age (Figure 1.1).

While in the understorey, a tree’s primary objective is to reach canopy level. In order to reach

this height, trees must allocate most available resources to vegetative growth to strengthen

the stem, expand branches, and flush leaves. After achieving canopy status, resources once

used to produce and maintain somatic structures, such as photosynthate, mineral nutrients,

and water, will be dedicated towards reproduction (see Thomas 2011 review). Trees will

begin shifting resources towards energy intensive reproductive events and producing more

reproductive structures, such as flowers and fruits (Thomas and LaFrankie 1993, Acosta

4

1997). Monocarpic species, which only have one reproductive event in their lifetimes,

demonstrate an extreme example of this trade-off between vegetative growth and

reproduction. Monocarpic trees spend the majority of their life using all their resources to

reach the canopy and maintain their somatic structures. As they approach the end of their life,

suddenly these trees shift their focus to create reproductive structures. They bloom and then

die shortly after. This is a common approach in herbaceous plant forms, but it is also a

strategy used by at least 100 long-lived woody perennial species (Thomas 2011). Crown

thinning could occur as a result of resources being devoted to future generations rather than

maintaining crown leaves and branches in a senescent tree.

Figure 1.1: Potential causes of age-related crown thinning.

Reaching the co-dominant level of the canopy allows the tree to receive direct

radiation to the top of the crown. However, it is only when trees reach up and over the

canopy that the crown can receive radiation from sides of the crown as well. In both

Age-related crown-

thinning mechanisms

Allocation of resources to reproductive

structures

Hydraulic limitations

Soil nutrient limitations

Gradual increase in pathogen

infestation

Periodic stressors and

damaging events

5

temperate and tropical forests, canopy heights can reach elevations over 60m (Lefsky

2010).Trees that reach dominant stature are no longer only competing against other plants for

nutrients, but they are now also fighting against physical forces resisting water transport. The

hydraulic limitation hypothesis is proposed as one of the most important mechanisms for

age-related crown declines (Ryan and Yoder 1997). This biophysical restriction results when

trees reach a height above which the transpiration-cohesion-tension mechanism can no longer

overcome the forces of gravity and frictional resistance to water movement through the

xylem. With a lack of resources reaching the tops of the canopies of tall trees, it would be

difficult for the tree to continuing producing leaves in those stressed areas. While this

hypothesis has been linked to size dependent declines, such as reduced leaf turgor (Ryan et

al. 2006, Woodruff et al. 2004, Woodruff and Meinzer 2011), it has not been demonstrated

that these declines will contribute to an increased crown openness with age.

In addition to these physiological and biophysical processes, external environmental

factors can also contribute to crown thinning. Towards the end of the long life of a canopy

dominant tree, its vast spread of roots have been penetrating the same plot of land searching

for mineral nutrients for decades or centuries. The process of growing and maintaining a

large canopy tree could on some sites drain the soil of nutrients over time (Ryan et al. 1997).

A tree that is lacking mineral nutrients will begin to experience physical declines. Physical

accumulation of damage is another means by which crown thinning can occur. Broken

branches due to storm events or animal inhabitation are to be expected regularly throughout a

tree’s life (Aide 1987). Even though trees can resprout branches, too much damage to one

side of a tree can put a disproportionate amount of strain on the tree. Trees lacking in

symmetry are more likely to experience decline than a balanced crown (Young and Hubbell

6

1991). Even if a tree does not lose a major branch, smaller scale damage can expose the tree

to pathogens. A small cut in the bark will not kill a tree, but it does provide an entry point for

fungus or an insect into the tree’s vascular system or internal cavity. Older trees that have

been subjected to wind, frost, and other stressors for relatively long periods of time may be at

particular risk of pathogens. A tree would likely continue to have a healthy crown when

exposed to any one of these mechanisms; however, an interaction of multiple stressors could

lead to rapid crown decline. There is recent evidence that older trees show both increased

rates of internode dieback and reduced regrowth capacity (Hossain and Caspersen 2012).

1.2.2 Processes offsetting age-related crown thinning

It is important to note that there are also processes that can lead to age-related

increases in crown biomass and subsequent decreases in canopy openness. These processes

could serve to offset crown thinning trends. Lianas are woody climbing plants that depend on

trees for the structural support to reach higher regions of the canopy, where they overtop and

intermingle their foliage with tree crowns. Ubiquitous in tropical climes, lianas have a strong

effect on understorey light conditions (Clark and Clark 1990, Schnitzer et al. 2000).

Schnitzer and Bongers (2002) even go as far to say that liana presence is the single largest

difference between temperate and tropical forests. Another potential mechanism by which

canopy openness declines with age is epicormic branching, which is known to increase in

response to damage and increases in light levels (Miller 1996, Ishii and McDowell 2002).

Epicormic branches sprout from dormant buds of stems that have grown during previous

growth periods (Meier et al. 2012). The increased light levels experienced by canopy

dominant trees may trigger epicormic growth, thereby neutralizing the canopy thinning effect

or contributing to crown closure.

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1.3 Scope of work

This thesis explores age-related crown thinning trends for a variety of species over

two biomes. The empirical study, presented in Chapter 2, employed the use of a moosehorn

densiometer to compare canopy openness values of individual trees with tree size. Eighteen

species from four sites in temperate and tropical biomes were included in the study. The

results, which include testing of species and biome effects, are discussed. Chapter 3

concludes by summarizing results with reference to the literature and providing

recommendations for the scope and methods of future research.

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Chapter 2 – Age-related crown thinning: common but not universal in

temperate and tropical forest trees

2.1 Introduction

Gap-phase regeneration theory provides an important framework for understanding

forest dynamics. The theory proposes that gaps in the forest canopy caused by treefall events

provide the high light levels needed for understorey regeneration (Watt 1947, Whitmore

1978, White 1979, Brokaw 1985). Pioneer species colonize these openings and climax (or

late-successional) species eventually out-compete the pioneers; non-pioneer light-demanding

species may regenerate in the understorey but require canopy gaps to reach maturity (Fayolle

et al. 2012). While these ebbs and flows are widely accepted as the main driver of

regeneration dynamics seen in most forest types throughout the world (Swaine et al.

1987,Yamamoto 2000, Kathke 2009), it is important not to overlook more gradual

mechanisms of light penetration occurring concurrently that may affect regeneration. There

are two assumptions of the theory that should be examined more closely: 1) that trees die in

sudden events and 2) that light conditions in a forest can be categorized as either a gap or

closed canopy.

The first assumption suggests that light floods into the understorey at the moment a

tree falls to the ground and dies. Many tree deaths occur due to wind, lightning, rain, or

snow; however, not all tree deaths occur so suddenly. When a tree falls to the ground, it is

often be the culmination of years of decline, a result of physiological, physical, and

environmental factors. As with any biological organism, trees follow a sigmoidal cumulative

growth curve (Verhulst 1839). Trees have a long juvenile period (Harper and White 1974),

9

during which accelerating growth occurs. Throughout maturity, during which trees spend the

majority of their lives, there is generally a constant rate of growth. Then during senescence,

there is a decelerating rate of growth. These age-related growth patterns could be manifested

in structural changes that could include declines in crown biomass (leaves and branches),

resulting in more subtle or gradual changes in light transmittance to the understorey over

time. Likewise, environmental factors that lead to losses in crown biomass, such as wind

damage, snow damage, crown abrasion, etc. are also known to occur. These processes could

create moderate light environments that may be best suited to tree species that are

outcompeted in either very bright or very dark conditions.

A number of studies have documented age-related changes in crown biomass and

structure. For example, Thomas and Ickes (1995) recorded leaf size reduction for 51 species

in tropical rain forest trees with increasing tree size, and for two intensively studied species

noted a unimodal relationship between leaf size and tree diameter, which has also been noted

in other systems (Thomas 2010, Panditharathna et al. 2010). Kenzo et al. (2006) quantified

an increase in leaf blade thickness and leaf mass per area with tree height for 65 individuals

ranging from seedlings to mature trees; and Ishii and McDowell (2002) found a decrease in

branch density when comparing recently mature Pseudotsuga menziesii trees with very old

size classes (~450 years old). Even studies that were not originally linked to age-related

changes provide relevant context for ageing crowns. Many surrounding environmental

factors can contribute to cumulative degradation of the crown. With regards to environmental

causes, studies have quantified small-scale crown structural changes such as broken branches

(Clark and Clark 1991), spaces between crowns due to crown abrasion (Putz et al. 1984), and

Kainer et al.(2006) described an increase in liana loads with increasing tree size. These

10

studies are just a small sampling of work that has shown that trees in a larger size class,

whether it be due to age or biophysical limitations, exhibit patterns unique to this life stage.

Age-related declines in crown biomass could lead to more light passing through the

canopies of aging trees, creating moderate light conditions beneath otherwise closed

canopies. At the stand level, it is widely accepted that an older forest will be less productive

(Gower et al. 1996) and allow more light through the canopy, i.e. have a lower leaf area

index (LAI) (Smith and Long 2001). At the individual tree level, there is much less evidence

supporting the idea of increased canopy openness as trees age. Based on detailed within-

canopy measurements, Nock et al. 2008 showed that two temperate tree species experience

large decreases in leaf area index with tree age and size, allowing more light through the

crowns of older trees.

There is a need in the literature to explore crown thinning dynamics further. For

instance, there is reason to believe that age-related crown thinning dynamics/patterns will

differ between temperate and tropical tree species. Specifically, the tropics have higher light

and water availability. For example, our temperate forest sites have annual precipitation in

the range of 800 cm to 1,100 cm, while our tropical forest sites have more than double the

amount of precipitation, with a range of 2,600 cm to 3,500 cm. Light availability, as

measured in terms of photosynthetically active radiation (PAR), has also been shown to reach

near twice the amount in tropical forests (Canham et al. 1990). Given that water and light are

the two most important factors in tree growth, the abundance of these two resources might

alleviate some of the stress that could be contributing to age-related declines.

Furthermore, with less pronounced growing seasons in the tropics, it would not be

surprising to find a significantly different senescence pattern. Most temperate species

11

(excluding evergreen conifers) must use stored energy throughout the winter, while most

tropical species have nearly continuous leaf coverage throughout the year, which allows them

to produce energy consistently throughout most of the year. Annual abscission and regrowth

of leaves is energy intensive and therefore one might expect crown thinning to be greater in

temperate species. Potentially more important than energy (i.e. carbon) loss is mineral

nutrient loss. Deciduous species are generally adapted to higher resource levels than

evergreen species (Aerts 1995, Reich et al. 1995, Aerts and Chapin 2000, Catovsky and

Bazzazz 2002), which may predispose deciduous species to larger ontogenetic declines as

their environment changes through development.

We were also interested in exploring age-related differences in pioneer and climax

successional types, which are commonly used in gap dynamics theory to dichotomize life

history strategies. Pioneer species are defined as fast-growing species that are able to take

advantage of disturbances (e.g. canopy gaps formed by tree fall events). Climax species are

slower growing species, often more shade tolerant, that eventually out-compete pioneer

species for canopy position. These differences in regeneration strategies, while broad, may

manifest in unique ontogenetic patterns.

In the present study we employed “low tech” methods that could be easily replicated

on many trees at multiple sites without the aid of canopy access techniques to assess the

generality of the phenomenon of age-related crown thinning in forest trees. We used DBH as

a proxy for age (O’Brien et al. 1995), and measured canopy openness with a “moosehorn”

densiometer (Garrison 1949). We examined the following hypotheses: (1) canopy trees in

general will show age-related crown thinning, as indicated by increased gap fraction with

increasing size; (2) age-related crown thinning patterns will vary significantly among

12

species; (3) age-related crown thinning patterns will vary significantly among biomes

(temperate and tropical).

2.2 Methods

2.2.1 Study sites

2.2.1.2 Temperate sites

Haliburton Forest and Wildlife Reserve, Ontario – The majority of the temperate data

was collected at the privately-owned 25,000-ha the Haliburton Forest and Wildlife Research

(HF) (45˚15’N, 78˚34’W) in the Great-Lakes-St Lawrence region of south central Ontario.

This tolerant hardwood forest is dominated by Acer saccharum, Fagus grandifolia, Tsuga

canadensis, and Betula alleghaniensis. The daily average temperature is -10.9˚C for January

and 18.9˚C for July, the annual precipitation level of 1008 mm (Environment Canada 1971-

1992), and forest canopy heights of 20-25 m (Nock et al. 2008). Sampling of the area was

conducted in the summer 2009, summer 2010, and fall 2010, primarily on the large mapped

HF “Megaplot” located in primary forest.

Koffler Scientific Reserve, Ontario – Additional temperate data was gathered from

the Koffler Scientific Reserve (KSR), which is owned and maintained by the University of

Toronto as a conservation and research area. The 350-ha reserve (44˚2’N, 79˚32’W) is

situated on the Oak Ridges Moraine near King Township, Ontario. KSR consists of open

habitats as well as primary and secondary forests that are dominated by A. saccharum, F.

grandifolia, T. canadensis, and Pinus strobus. The daily average temperature ranges from -

7.9˚C in January to 20.5˚C in July, and the area receives 849 mm of precipitation annually

(Environment Canada, 1974-2000). Due to the warmer climate at KSR compared to HF, we

13

were able to sample this area in the fall 2010 after most trees had already begun to lose their

leaves at HF.

2.2.1.3 Tropical sites

Barro Colorado Island, Panama – Most of the tropical data collection was conducted

at the 50-ha Plot on Barro Colorado Island (BCI) (9˚10’N, 79˚50’W), which is a forested

hilltop island located midway between the Caribbean Sea and the Pacific Ocean in the

Panama Canal Waterway. The southwest of the island has remained mostly uncleared since

the Spanish conquest of Panama, while the rest of the island was deforested in the 1880s

when the French attempted to build the canal (Croat 1978). Since 1923, the seasonally

tropical moist lowland forest on the island has been maintained as a biological reserve

(Foster and Brokaw 1996). With canopy heights of 35-40 m, this forest has an average

annual temperature of 27.0˚C and receives an annual precipitation of 2,600 mm. Data were

collected during the wet season (Jun.-Sept.) 2010.

Luquillo Forest Dynamics Plot, Puerto Rico – Data for two more tropical species

were collected from the 16-ha Luquillo Forest Dynamics Plot (LFDP) (18˚19’N, 65˚49’W)

near the El Verde Field Station in Luquillo mountains in northeastern Puerto Rico. The

LFDP has the typical vegetation and environment of a “tabonuco forest,” named after the

presence of Dacryodes excelsa (Odum 1970). Until the 1930s, the northern area of the plot

was regularly clear-cut for timber and agriculture (e.g. coffee plantations). The southern area

of the plot was never cleared, but selective logging occurred in the 1930s and 1940s.

Hurricanes also caused major disturbances in the plot, primarily in the northern area, in 1928,

1932, 1989, and 1998. This subtropical wet montane forest receives 3,500 mm of

14

precipitation annually, has an average temperature of 22.8˚C, and has an average canopy

height of 20-30 m (Weaver and Murphy 1990). Sampling occurred in Feb. 2011.

2.2.2 Sampling design

2.2.2.1 Moosehorn densiometer

There are many methods for assessing leaf area and light transmittance at the

individual tree level, including sub-sampling of fisheye photographs (e.g., Astrup and Larson

2006), narrow-angle lens photographs (e.g., Beaudet et al. 2002), the line drop method

(Thomas and Winner 2002), and the moosehorn densiometer (Garrison 1941). In attempts to

quantify age-related crown thinning as a general trend that occurs in numerous species, our

study made use of a quick, low-tech method: the moosehorn densiometer. This is in contrast

to a study by Nock et al. (2008), which showed a significant crown thinning trends for A.

saccharum and B. alleghaniensis through meticulous, time-consuming line-drop

measurements from within the canopy (n = 49). Photographic methods also serve to limit

sample size because photographs can only be taken near dawn and dusk when the sun is not

overhead. In contrast, moosehorn measurements are not limited by sky conditions and can be

taken at any time of day – even during moderate precipitation. A major advantage for using

the moosehorn is the ability to distinguish tree leaves from liana leaves or sub-canopy

vegetation. The moosehorn is used in conjunction with binoculars that allow the viewer to

verify, while in the field, what exactly is being observed. Our decision to use the moosehorn

allowed us to expand the scope of their findings by taking on-the-ground readings of a large

sample of trees across as many species as possible (n = 1786).

15

The moosehorn densiometer is used to estimate canopy openness (or gap fraction)

(Garrison 1941). It consists of an L-shaped PVC tube that has a mirror placed at the joint. It

is distinct from the typical densiometer used to estimate stand-level canopy cover in that it

uses a flat mirror instead of concave, allowing for focus on individual crowns. A bubble level

is attached to the eyepiece to ensure that the viewer is observing the crown at zenith. The

moosehorn’s self-leveling eyepiece is attached to the 25cm neck with a 5 cm opening, which

gives it an 11.4 degree angle of view. As a person looks through the lower horizontal portion

of the moosehorn, they will see a reflected image of the tree crown above. The top of the tube

has a 5×5 grid printed on plexi-glass so that when one looks through the moosehorn the grid

and the canopy are visible on the mirror. Each square on the 5x5 grid represents 4% of the

total view. To read the measurement, each cell is scored from 0-4. Going from left to right

and top to bottom, the scores are added for each cell. A tree with a very dense canopy might

get a score of 2%, whereas a tree with a sparse canopy might get a score of 40%.

2.2.2.2 Measurements

At each site, we selected common canopy tree species for study, making moosehorn

densiometer measurements on individuals with crowns located at or above the main forest

canopy. The moosehorn densiometer measurements involved assessing the percentage of the

total view that was open sky to estimate observed total openness (see below). At the tropical

sites, additional measurements were taken to estimate overlap-corrected openness (see

below). At all sites, three measurements were taken for each tree at three separate locations

below the respective tree crown, and the average of these measurements was used. The

location of each reading was determined using a semi-random sampling method. We would

begin at the north side of the base of the tree. If we could see into the canopy from that point

16

we would take our first sample at that location. If not, we would begin to walk clockwise in a

spiral direction around the tree until we found a suitable, representative area to measure. We

did not take measurements of areas that extended beyond the crown edge or that included

gaps within the canopy, i.e. gaps caused by a large branch fall event.

For each tree, we measured the DBH with a diameter measuring tape at all sites

except for BCI, where we were able to use the data from the census collected in the same

year (Hubbell et al. 2010). We also measured tree height, height to live crown, crown radius,

and Crown Illumination Index (CII: Clark and Clark 1992). Heights and crown radii were

measured using a laser rangefinder (Laser Technology TruPulse 200) and binoculars. The CII

describes the crown’s social position. A score of 5 is given to an emergent canopy tree, 4 is

given to a canopy-level co-dominant tree, 3 is given to a canopy that is overtopped slightly

by another tree, and 2 is given to a tree that is completely overtopped by the canopy. We did

not use any trees that had a value lower than 3.

At the temperate sites (HF and KSR), we took measurements without a tripod on trees

with a DBH greater than 25 cm from eight species: Acer saccharum Marsh., Fagus

grandifolia Ehrh., Pinus strobus L., Quercus rubra L., Betula alleghaniensis Britt., Fraxinus

americana L., Prunus serotina Ehrh., and Tsuga canadensis (L.) Carrière. A. saccharum was

sampled intensively, as it is the regional dominant species and had been assessed to show a

crown thinning pattern in a prior study in the region (Nock et al. 2008).

At the tropical sites (BCI and LFPD), measurement methods differed slightly from

those taken at the temperate sites in that a tripod was used to deal with the greater complexity

of tree crown structure and also to enable assessment of non-tree objects in the canopy (see

below). At BCI, we sampled from eight species: Alseis blackania Hemsl., Beilschmiedia

17

pendula (Sw.) Hemsl., Jacaranda copaia (Aubl.) D. Don, Prioria copaifera Griseb.,

Quararibea asterolepis Pittier, Tabernaemontana arborea Rose, Tetragastris panamensis

(Engl.) Kuntze, and Trichilia tuberculata (Triana & Planch.) C. DC. At LFPD, we chose to

focus on just two species: Buchenavia tetraphylla (Aubl.) R. Howard and Manilkara

bidentata (A. DC.) Chev. The two species from LFPD were chosen because they are

common, are known to have low liana loads, and have easily distinguishable leaves. At each

site, using census maps, we went to areas of the plots that had high concentrations of the

desired species in order to maximize sampling efficiency. In those areas where

concentrations of desired species were highest, we examined all trees of the selected species

that we encountered that had a DBH greater than or equal to 30 cm. If the crown was co-

dominant or dominant, and if leaves of lianas did not exceed 50% of the visible canopy

foliage, we would then take measurements with the moosehorn densiometer.

The moosehorn densiometer readings taken at the tropical sites involved not only

assessment of the percentage of the total view that was open sky (observed total openness),

but also the percentage of the total view that was occupied by lianas, epiphytes, other trees,

or any other objects that did not belong to the subject tree that happened to be in the view

(e.g. nests, animals, large dead leaves, etc.). We later factored out these other objects in the

canopies using an overlap-corrected openness metric that is described below. This approach

was taken because a major hindrance to our ability to accurately assess crown openness is the

existence of other objects within the circumference of the crown (e.g. overlapping tree

crowns, dead branches, nests, epiphytes, lianas, etc.). We expected this to especially be a

challenge in tropical forests where lianas play such a prominent role in forest ecology

(Schnitzer and Bongers 2002). The purpose of calculating the overlap-corrected openness

18

metric was to mathematically approximate the tree’s crown openness value by excluding

“other objects” that exist in the canopy. These data were also used to calculate a Liana Score

between 0 and 4. A score of 0 means that no lianas were present in the tree’s crown, 1 means

0-25% liana coverage, 2 means 25-50% liana coverage, 3 means 50-75% liana coverage, and

4 means 75%-100% (Schnitzer 2000).

2.2.2.1 Power analysis and measurement validation

Before beginning research at our tropical study sites, we oversampled A. saccharum

(n > 600) to determine the minimum sample size needed in order to detect a thinning trend.

Figure 2.1 shows the results of a power analysis using A. saccharum, where the points in the

graph were generated through randomly sampling with replacement from the entire data set.

This graph demonstrates that we needed to sample at least 60 trees from each species in order

to have a 50% chance of detecting a significant trend.

19

Figure 2.1 Power analysis of A. saccharum. Random sample with replacement from entire data set, n

= 646. Data collected at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009

and 2010.

To validate measurements, we took repeat measurements of moosehorn readings at

BCI for a subsample of trees to assess the moosehorn’s accuracy. We compared the average

of three moosehorn readings the first time we went to a tree compared to the average of the

three readings on the second time we went to a tree later in the summer of 2010 (about two

months later). These points were used to construct a linear regression equation that predicted

the second moosehorn reading from the first. With a sample size of 77, we found a weak

(R2=0.46), yet highly significant relationship (p<0.001). The repeat measurements were

taken nearly 3 months after the first readings were taken by a different observer. Aside from

20

observer variation, the low R2

may reflect real temporal variation in canopy gap fraction as

well as error (Chen 1996).

2.2.3 Canopy openness estimation

Once the moosehorn data had been collected, canopy openness was estimated using

two different procedures.

2.2.3.1 Observed total openness

The observed total openness describes the percent of the moosehorn view that is open

sky. This value was used in all subsequent analyses. This value does not correct for instances

when something other than the canopy biomass (leaves and branches) of the tree of interest is

blocking the view (e.g. lianas). This value was assumed to be best suited for the temperate

forest because the canopy biomass of the tree of interest would typically be the only object

attenuating light. In the tropical forest, the observed total openness value is expected to tell

us less about the specific tree of interest because it is common in tropical forests to encounter

lianas, epiphytes, and understorey trees blocking much of the light in the view. The direct

percent open value is still valuable for the tropical data for purposes of comparison with the

temperate data.

2.2.3.2 Overlap-corrected openness

This is used to get better estimates of crown thinning for trees by factoring out non-

tree objects. This overlap value separates the crown projected area of the tree of interest from

that of lianas, other trees, and other objects not belonging to the tree of interest (e.g.

epiphytes, nests). We could not merely subtract the percentage of the total view that was

covered by other biomass because that would assume that there were no leaves or branches

21

of the tree of interest above the non-tree object. To account for this potential overlap effect,

we assumed that the non-tree objects were distributed randomly throughout the crown. We

calculated a proportional overlap value that reflects what the openness would have been if the

objects not belonging to the tree of interest (lianas, other trees, epiphytes, etc.) were not

present. Specifically, we estimated the proportion of the horizontal area above non-tree

objects that was occupied by the crown biomass of the tree of interest (b). This was achieved

by assuming that b was related to the fraction of the moosehorn view covered by non-tree

biomass (x + y + m).

The overlap-adjusted openness (c) is calculated in the following way. Using the

equation:

Where L represents the direct reading of open sky that we measured using the

moosehorn; x represents lianas; y represents the crowns of other trees; and m represents all

other objects that blocked light from passing through the tree crown (e.g. epiphytes, nests,

etc.). The b variable that we are solving for is the fraction of the moosehorn view that is

covered by biomass (i.e. leaves and branches) of the tree of interest. To solve for b, the

equation is rearranged to the form:

Once we account for all other objects in the view by solving for b, we are able to

subtract b from 1 to arrive at c. This final variable, c, represents a value for crown openness

22

that may more accurately represent the openness of the tree if the other objects present in the

canopy were removed.

2.2.4 Statistical analysis

2.2.4.1 Linear and nonlinear regression analysis

For each species, we conducted a linear regression analysis to assess the strength of

the relationship between observed total openness (“openness”) and DBH. To reduce

heteroskedasticity and improve linearity, we took the log of both dependent and independent

variables. Linear regressions were performed on all the data pooled together, on life history

groupings (leaf periodicity and successional strategy), and also by biome groups (temperate

and tropical). In addition, linear regressions were performed on the overlap-corrected

openness values from the tropical sites and DBH for all species, as well as openness and

height. Before performing the linear regressions, we tested the significance of a second order

(quadratic) polynomial model. If significant, we fit a locally weighted scatterplot smoothing

(LOWESS) curve to the data.

2.2.4.3 Comparison of functional groups using species as unit of analysis

When we compared functional groups using linear regressions, we used individual

tree crowns as the unit of analysis. Each individual tree crown is a representative from the

three groupings we examined (biome, successional status, or leaf periodicity), and valuable

information can be garnered about functional group trends. However, it is possible that our

analysis could be skewed by the variable sample sizes for each species – namely, the very

high sample size we collected on A. saccharum. To minimize the effect oversampled species

23

would have the linear regressions of pooled groups, we also conducted an analysis that

compared functional groups based on the slope of the relationship between openness and

DBH of each species. This meant that each species was weighted equally. In addition to the

three original functional groupings, we also explored how the trends may have differed

between species with crowns that tend to be sub-canopy, canopy, or emergent. We plotted

the average slope of the graphs with 95% confidence intervals. We then conducted ANOVAs

on all four groupings, again using slopes as the unit of analysis. Sample size was used as a

weighting factor for these ANOVA analyses.

2.2.4.4 Mean crown openness and confidence intervals

As our most basic analysis, we looked for differences in crown openness means

among species. We plotted the mean openness for each species with 95% confidence

intervals. Additionally, we plotted pooled means and confidence intervals for tropical and

temperate species to assess how widely the mean openness varied between biomes. To help

visualize the size-dependent trends occurring, we separated each species into two groups:

recently mature canopy trees (DBH below the median of our sample) and very large trees

(DBH above the 3rd

quartile of our sample). We then plotted and compared the mean of each

group with 95% confidence intervals.

2.2.4.5 ANCOVA analyses

Three sets of ANCOVA analyses were performed. The first was performed to assess

heterogeneity of slopes of crown openness vs. DBH among all species, temperate species,

and tropical species. The second was performed to assess species effects, namely to

determine how life history traits including successional status and leaf periodicity affected

24

the relationship between openness and DBH. Finally, the third assessed the effect of biome

on the relationship between openness and DBH. All statistical analyses were performed in R

(2008).

2.3 Results

2.3.1 Linear and nonlinear regressions of openness-DBH relationships

The linear regression relationships had relatively weak R2

values; all were below 0.2.

Of the eight temperate species studied, only one species showed a significant positive

relationship: A. saccharum (p < 0.001). Two of the temperate species showed significant

negative relationships: Q. rubra (p<0.01) and T. canadensis (p<0.05) (Figure 2.2). Of the ten

tropical species studied, three species showed significant positive relationships between

direct crown openness and DBH: B. pendula (p<0.01), J. copaia (p<0.05), and P. copaifera

(p<0.05) (Figure 2.3). No tropical species showed a significant negative relationship.

Significant non-linear relationships were also detected in three species: T. panamensis

(p<0.05), P. serotina (p<0.001), and F. americana (p<0.001). For each species-specific

relationship, the sample size, intercept, R2

value, and p-value are reported in the Appendix

2.1.

25

Figure 2.2: Linear and nonlinear regressions for eight temperate species sampled at Haliburton Forest, Ontario, and Koeffler Science

Reserve, Ontario, in 2009 and 2010. Each data point is the average of three openness readings taken on one tree. X- and y-axes are

log-transformed.

26

Figure 2.3: Linear and nonlinear regressions for ten tropical species sampled at Barro Colorado Island, Panama, and Luquillo Forest

Dynamics Plot, Puerto Rico, in 2010 and 2011. Each data point is the average of three openness readings taken on one tree. X- and y-

axes are log-transformed.

27

For tropical species, the overlap-corrected value for crown openness – which

attempted to provide an improved estimate of openness by factoring out those objects that

were not part of the tree’s crown – yielded weaker and less significant relationships to DBH.

Using this openness metric, nine out of the ten tropical species had lower R2

values compared

to the relationships using observed total openness. However, two of the ten species still

displayed a significant positive relationship: B. pendula (p<0.05) and P. copaifera (p<0.05).

In order to assess the relationship between crown openness and DBH on a more

general scale, we tested the relationship for our sampled trees in three larger categories:

tropical trees, temperate trees, and all trees. Tropical trees and temperate trees both showed

significant positive relationships (p<0.001) (Figure 2.4). These relationships seem to imply

that across all studied species, there is a general trend of increasing openness with increasing

DBH, although these trends again had consistently low R2 values (Appendix 2.2).

28

Figure 2.4: Linear regressions for eight temperate species sampled at Haliburton Forest, Ontario, and

Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical species sampled at Barro

Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011. Each

data point is the average of three openness readings taken on one tree. X- and y-axes are log-

transformed.

Aside from grouping by biomes, we also performed linear regressions on species

grouped by two life history traits: successional strategy and leaf periodicity. Pioneer species

and climax species did not have significant relationships between openness and DBH when

plotted separately (p>0.05) (Figure 2.5). Evergreen species also did not show a significant

relationship (p>0.05), however, deciduous and semi-deciduous did show a significantly

positive relationship (p<0.001) (Figure 2.6).

29

Figure 2.5: Linear regressions for pioneer and climax species sampled at Haliburton Forest,

Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical species

sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico,

in 2010 and 2011. Each data point is the average of three openness readings taken on one

tree. X- and y-axes are log-transformed.

Figure 2.6: Linear regressions for deciduous/semi-deciduous and evergreen species sampled at

Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical

species sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico,

in 2010 and 2011. Each data point is the average of three openness readings taken on one tree. X- and

y-axes are log-transformed.

30

2.3.2 Comparisons with species as unit of analysis

The three previous comparisons of pooled functional groups (biomes, successional

status, and leaf periodicity) use individual tree crowns as the unit of analysis. Given our large

sample size of A. saccharum (n=646) in comparison to other species (n ranging from 35 to 91

individuals), it is important to also consider species as the unit of analysis rather than just the

individual. In Figure 2.7, we plotted the average slope of the species within four functional

groups: biomes, leaf periodicity, shade-tolerance, and canopy position. Although there are no

significant differences between and among groupings, nine out of ten groupings show

positive slopes between openness and DBH. The one grouping to show a negative slope was

the sub-canopy species A. blackania. The ANOVA analyses to compare the categories within

these groupings were all insignificant (p>0.05).

31

Figure 2.7: Average slopes of the relationship between crown openness and DBH for functional

groups of eighteen species sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve,

Ontario, in 2009 and 2010, and ten tropical species sampled at Barro Colorado Island, Panama, and

Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011. Each data point is the average of three

openness readings taken on one tree. X- and y-axes are log-transformed and 95% confidence intervals

are shown. (“decid” = deciduous; “intol” = shade intolerant; “mid” = mid-tolerant; “tol” = shade

tolerant; “1.sub” = subcanopy; “2.can” = canopy; “3.emerg” = emergent).

32

2.3.3 Mean crown openness and confidence intervals

The mean crown openness ranged from 6.5-14.0% for temperate species (Figure 2.8)

and ranged from 2.8-10.9% in tropical species (Figure 2.9). F. americana and B. tetraphylla

were the only two species to show significantly different means from all of the other sampled

species in their respective biomes. The pooled results of temperate and tropical species

clearly show that the two groups have significantly different means, 9.7% (σ = 0.7%) and

4.7% (σ = 0.3%) (Figure 2.10).

Figure 2.8: Mean crown openness with 95% confidence intervals for eight temperate species sampled

at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010. Species

codes defined as ACSA = A. saccharum, FAGR = F. grandifolia, PIST = P. strobus, QURU = Q.

rubra, BEAL = B. alleghaniensis, FRAM = F. americana, PRSE = P. serotina, and TSCA = T.

canadensis.

33

Figure 2.9: Mean crown openness with 95% confidence intervals for ten tropical species sampled at

Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011.

Species codes defined as ALSEBL = A. blackania, BEILPE = B. pendula, JACACO = J. copaia,

PRIOCO = P. copaiferia, QUARAS = Q. asterolepis, TABEAR = T. arborea, TETRPA = T.

panamensis, TRICTU = T. tuberculata, BUCTET = B. tetraphylla, and MANBID = M. bidentata.

Figure 2.10: Mean crown openness with 95% confidence intervals for ten tropical species sampled at

Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011,

and for eight temperate species sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve,

Ontario, in 2009 and 2010.

34

In order to gauge how tree size influences openness values within species, we

separated the openness values into two distinct size classes: trees with DBH below the

median, representing recently mature trees, and trees with a DBH greater than the third

quartile, representing large old trees. This division shows that the large size classes of the

tropical species B. pendula, J. copaia, and P. copaifera have significantly higher openness

values than recently matured trees of the same species (Figure 2.11). Likewise, the temperate

graph shows that old A. saccharum trees have higher crown openness than recently matured

conspecifics; whereas old Q. rubra trees have significantly less crown openness than trees

that have recently reached the canopy (Figure 2.12).

Figure 2.11: Crown openness by size class for ten tropical species sampled at Barro Colorado Island,

Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011. Each species was

divided into two groups: one group with trees below the median DBH and one group above the third

quartile in DBH. 95% confidence intervals are shown. Species codes defined as ALSEBL = A.

blackania, BEILPE = B. pendula, JACACO = J. copaia, PRIOCO = P. copaiferia, QUARAS = Q.

asterolepis, TABEAR = T. arborea, TETRPA = T. panamensis, TRICTU = T. tuberculata, BUCTET

= B. tetraphylla, and MANBID = M. bidentata.

35

Figure 2.12: Crown openness by size class for temperate species for eight temperate species sampled

at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010. Each species

was divided into two groups: one group with trees below the median DBH and one group above the

third quartile in DBH. 95% confidence intervals are shown. Species codes defined as ACSA = A.

saccharum, FAGR = F. grandifolia, PIST = P. strobus, QURU = Q. rubra, BEAL = B.

alleghaniensis, FRAM = F. americana, PRSE = P. serotina, and TSCA = T. canadensis.

2.3.4 ANCOVA analysis

The ANCOVAs testing for heterogeneity of slopes for all species (p<0.001),

temperate species (p<0.05), and tropical species (p<0.001) detected statistically significant

differences in the relationship between openness and DBH. For life history effects,

ANCOVA comparisons of pioneer vs. climax species and deciduous vs. non-deciduous

species also yielded significant p-values (p<0.001 for both). Finally, the ANCOVA of

temperate vs. tropical species was statistically significant (p<0.001). The results of these

ANCOVAs are in Table 2.1.

36

Table 2.1: Summary of ANCOVA results for pooled data for ten tropical species sampled at Barro

Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011, and for

eight temperate species sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve,

Ontario, in 2009 and 2010. For each grouping, sample size (n), R2, and p-value are shown.

Sample size (n) R2 value p-value

Tests for

heterogeneity of

slopes

All species 1786 0.270 <0.001

Temperate

species

974 0.014 <0.05

Tropical species 812 0.046 <0.001

Tests between

functional groups

Temperate vs.

tropical species

1786 0.083 <0.001

Pioneer vs.

climax species

1786 0.024 <0.001

Deciduous/semi-

deciduous vs.

evergreen species

1786 0.030 <0.001

2.3.5 Crown illumination indices and liana scores

Crown Illumination Index (CII) scores were given to each tree crown sampled at

tropical sites. As seen in Figure 2.13, four species had an average score of 4 and above: B.

pendula, J. copaia, P. copaifera, and B. tetraphylla. High CII scores means that the crown is

dominant and receives direct sunlight from multiple angles. None of the average scores are

below 3 because we actively skipped trees that were below canopy-level. Liana scores (LS)

represented the percentage of the individual crowns covered by lianas (Figure 2.11). We

avoided taking measurements on trees with too many lianas. J. copaia had the lowest average

LS, while B. tetraphylla had the highest average LS.

37

Figure 2.13: Average Crown Illumination Index and average liana scores for ten tropical species

sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010

and 2011. Species codes defined as ALSEBL = A. blackania, BEILPE = B. pendula, JACACO = J.

copaia, PRIOCO = P. copaiferia, QUARAS = Q. asterolepis, TABEAR = T. arborea, TETRPA = T.

panamensis, TRICTU = T. tuberculata, BUCTET = B. tetraphylla, and MANBID = M. bidentata.

2.4 Discussion

The goal of this study was to test three hypotheses related to age-related changes in

crown thinning: (1) age-related crown thinning occurs as a general phenomenon; (2) age-

related crown thinning patterns are species-specific; and (3) age-related crown thinning

patterns vary between temperate and tropical biomes.

2.4.1 Age-related crown thinning as a general phenomenon

With regards to hypothesis 1, that age-related crown thinning is a general

phenomenon, our study failed to detect age-related crown thinning as a pervasive cross-

species, cross-biome phenomenon. Instead, the relationship between tree size and crown

thinning varied widely among species: some species showed crown thinning with increasing

size, some show crown closure with increasing size, and some show no discernible trend.

Considering only one-third of the species sampled that had statistically significant

38

relationships between openness and tree size, patterns varied: A. saccharum and three

tropical species, B.pendula, J. copaia, and P. copaifera, showed positive significant

relationships, while two temperate species, Q. rubra and T. canadensis, showed negative

significant relationships.

The fact that we did not detect a significant relationship between openness and DBH

for the majority of tested species is likely explained in part by our relatively low sample size.

For example, A. saccharum – which had more than seven times the sample size of any other

temperate species (n=646) – had a positive slope that was highly significantly different from

zero (p<0.001), corroborating results from Nock et al. (2008). None of the other temperate

species – which had samples sizes below 60 – had statistically significant positive slopes.

With a much higher sample size, we may have seen more significant trends in the other

temperate species. In a post-hoc power analysis of the A. saccharum data (Appendix 2.6),

we found that a sample size of at least 110 trees would have been needed for each species to

achieve a statistical power of 0.8 (80% chance of detecting a trend at p<0.05), and a sample

size of 52 trees needed to achieve a statistical power of 0.5. The significance of openness-

size relationships of the grouped temperate and tropical data is further indication that the

increase in statistical power afforded by a sufficient sample size could detect the

hypothesized age-related trend.

2.4.2 Species-specific patterns in age-related crown thinning

Our tests for heterogeneity of slopes (for all species, temperate species, and tropical

species) all demonstrated that within each of these pooled groups, at least one of the species

had a statistically significant different slope from the rest. This result of heterogeneity is

expected given the observed variability in slopes among species. It also demonstrates that

39

the relationship between openness and DBH is not happening in all species nor necessarily

occurring at the same rate in the species experiencing crown thinning. The relationship

between DBH and openness is dependent on many factors and is highly species specific.

We were interested to assess if important life history characteristics (such as

successional stages and leaf periodicity) would affect the relationship between openness and

DBH. The significantly different trends found in ANCOVA analyses of the relationship

between openness and DBH in pioneer and climax species highlight that differences in

growth patterns and light tolerances may be relevant in later life stages. Related work has

also shown that tree species of differing life-history strategies show pronounced differences

in canopy openness, which is generally higher in more light-demanding species (Canham et

al. 1994). We found this to be true with F. americana and P. serotina, which are relatively

light-demanding species that had a significantly higher mean crown openness than all the

other temperate species (Figure 2.6).

However, when linear regressions for both pioneer species and climax species were

considered independently, they did not yield significant relationships. Therefore, we cannot

describe the directionality of these differences based on our study. When deciduous and

semi-deciduous species were grouped together and compared to evergreen species, the

ANCOVA analysis also detected a significant difference. This could be explained by the

results of the linear regressions between openness and DBH: the liner regression for all

evergreen species does not show a significant trend, while the linear regression for deciduous

and semi-deciduous species does show a significantly positive relationship. One explanation

for this is that losing all leaves at some point throughout the year will create conditions that

40

affect the relationship between openness and DBH – namely, it is possible that deciduous

trees are more likely to experience crown thinning.

Although it is not a significant trend, it is interesting that A. blackania is the only

tropical species examined to show a negative relationship between openness and DBH. This

species is known to have a peculiar life history as a shade-tolerant pioneer tree (Dalling

2001). Many A. blackania actually decrease in height once they have reached maturity, yet

they continue to exhibit high resprouting. A. blackania was also the most common species to

have high liana loads. The high presence of lianas might have made it difficult to detect what

was actually occurring within the crown of interest. Lianas present a unique challenge to

assessing age-related crown thinning in the tropics. As trees and forests get older, their liana

loads also increase (DeWalt et al. 2000). This correlation makes it more difficult to assess the

openness of old tropical trees and has obvious implications to light penetration in likely

offsetting trends of age-dependent crown thinning. While focusing on tree species known to

have low liana loads would allow a more accurate assessment of the individual tree crowns, it

will not help evaluate a more general, cross-species trend. It may be that trees with highest

liana loads are the ones experiencing highest crown thinning.

T. canadensis and Q. rubra showed significant negative relationships, implying

crown closure with increasing DBH. Both of these temperate species, as well as the species

with the next most negative relationship (P. strobus), are all relatively long-living (Burns and

Honkala 1990). It is possible that this negative trend reflects a lack of many very old

individuals in the sample. Another likely explanation is that T. canadensis and P. strobus –

evergreen species – do not undergo seasonal foliage shedding. Instead of using limited

resources to flush all new leaves each year, the evergreens can increase their crown density

41

by maintaining leaves and producing just a few more. This conservative approach could

delay the onset of crown thinning, which might have been felt earlier if each year they had to

dedicate so many nutrients and resources towards new leaf production. Q. rubra and P.

strobus also share the trait of commonly producing epicormic branches (Sanchez et al. 1996,

Ward 1966, respectively). Epicormic buds lie dormant below the bark, but can become active

when higher parts of the tree are damaged or light levels increase (Miller 1996). The ability

or tendency to produce epicormic branches that could fill small gaps in the canopy due to leaf

loss or branch damage may be an important predictor of crown transparency through

ontogeny (Ishii and McDowell 2002).

2.4.3 Biome-specific patterns in age-related crown thinning

Linear regressions for pooled temperate and tropical species yielded statistically

significant positive slopes. For the temperate data, while two of the temperate species

showed significantly negative trends, the temperate pattern was dictated by A. saccharum,

which represented more than two-thirds of all trees in the temperate data set. A. saccharum

has a highly significant positive relationship that is able to outweigh the other negative

significant relationships in the temperate pool with a much smaller sample size. For tropical

data, there was a general positive directionality of crown thinning with age, as 90% of the

sampled species had positive slopes, three of which were significant. The results of the

ANCOVA comparing all temperate species with all tropical species showed that the two

groups, while both exhibiting positive trends, had significantly different slopes (p<0.001).

This indicates that biome-specific factors may be at play. Furthermore, according to our

moosehorn direct openness values, the openness of the temperate species averaged 9.7% (σ =

42

0.7%) whereas the openness of the tropical species averaged 4.8% (σ = 0.3%), suggesting

unique biome-related causes.

2.4.4 Review of methods and future work

We sampled a wide range of tree sizes above certain threshold sizes, without

oversampling any size class. It is possible that the process of age-related crown thinning only

begins at much later stages of ontogeny and occurs at a relatively fast pace, brought on by

pathogen invasion (Castello 1995), large fruiting events (Innes 1994), or hydraulic limitation

(Ryan 1997, Hubbard et al. 1999). In this case, detection of significant declines in crown

thinning may be possible with a sampling regime that focuses attention on much larger size

class. For example, Nock et al. (2008) were able to detect strong crown thinning relationships

in two temperate species by over-sampling the very largest and oldest trees available.

However, these trees are rare, and may play a minor role in overall forest regeneration

patterns.

A methodological explanation for our inability to detect significant changes in crown

thinning with age is our sampling methodology, which relied on the moosehorn densiometer.

Visual assessment of the number of boxes in the 5x5 viewing grid that contain open space

and the various obstructions to light transmittance (e.g. canopy biomass, lianas, epiphytes,

etc.) is vulnerable to human error in identification of barriers and subjective decisions (e.g.

whether a particular grid box contains more openness than biomass). Our assessment of the

accuracy of the moosehorn readings calculated an R2 of only 0.46, indicating that

measurement error could be largely affecting our results. However, it is important to note that

the relatively low R2

value could also be due to environmental variability. Whether it is

seasonal fluctuation in light transmittance or simply movement of the crown, the light

43

conditions below a crown could be a real variation over time. To counter this potential

inconsistency that exists in natural settings, future studies that use the moosehorn

densiometer should focus on large samples (>110 individuals).

2.4.1 Conclusion

The ultimate purpose of the present study is to explore more gradual mechanisms of

light penetration to the understorey over time. By sampling from a large number of species

across two biomes, the present study confirmed that such processes occur while also

detecting species-specific and biome-specific patterns. At a stand level, patterns of

regeneration will be determined by the relative abundances of species, spatial distribution of

species, and the strength of species-specific closure and thinning trends. For example, the

observed increases in crown thinning with age of A. saccharum are likely to play a driving

role in light availability in the understorey. A. saccharum is a predominant and

homogenously distributed species in the northern hardwood forest of North America. Under

the crowns of ageing A. saccharum, we might expect to find a species composition unique to

moderate light environments. Taken as a whole, this study provides further evidence that

gap-phase dynamics in forest ecosystems are likely moderated by age-related changes

occurring within individual crowns. Further study is needed to better understand the role of

large canopy dominant trees in the light regime of tropical and temperate forests – not only

the gaps they create in the moment they die, but also the moderate light levels that gradually

increase for years.

44

Chapter 3 – Discussion, implications, and future work

The study of age-related changes in tree structure and function is confounded by the

very long lifespans of trees. The most direct way to assess age-related processes would be to

follow a cohort of saplings through their ~200 year development. Given the difficulties of

this approach, most studies take samples from different size classes (a proxy of age) at a

given point in time and compare attributes of interest. As reviewed in the previous chapters,

many such studies have found evidence of distinct changes that occur throughout a tree’s life

resulting from physiological, physical, and environmental origins (Yoder et al. 1994, Sterck

and Bonger 1998, Cavender-Bares and Bazzazz 2000, Smith and Long 2001, Boege et al.

2007, Matinez-Villata 2007). In this final chapter, I provide a recap of the results of Chapter

2 in relation to the relevant literature, with a focus on possible explanations for the observed

results and possible directions for future work.

3.1 Overview of results, sources of error, and statistically

significant effects

3.1.1 Overview of results

Our study aimed to contribute to the understanding of age-related changes by

quantifying canopy openness over a range of species and for two biomes (temperate and

tropical). We measured canopy openness of individual trees using a moosehorn densiometer,

which allowed us to measure over 1,780 individuals of eighteen species in temperate and

tropical forests. Results indicate species-specific relationships between openness and size,

with some species showing significant crown thinning with age, some showing significant

crown-closure with age, and some species showing no discernible trend. This observed inter-

45

specific variability – which occurred across and within biomes – can be explained by

measurement error and sample error, and/or actual species-specific patterns.

3.1.1 Sources of error

Although we attempted to minimize measurement error by taking multiple samples at

each location for each tree crown and, in the tropical system, used a tripod, the moosehorn

method has a degree of subjectivity. Our assessment of the accuracy of the moosehorn

readings calculated an R2 of only 0.46, which may indicate an underlying sampling

inaccuracy, but could also be a true reflection of dynamic conditions of light below canopy

dominant trees. The low reproducibility of the moosehorn led to a loss of precision, while

allowing for greater sampling intensity, and was judged to be appropriate given the research

objectives. With regards to sample size, post-hoc power analysis of A. saccharum (the

species for which we collected the highest sample size, 646 individuals) found that the

minimum sample size should have been at least 110 to achieve a statistical power of 0.8.

Seventeen of the eighteen species considered in this study had sample sizes below this

threshold.

3.1.1 Statistically significant effects

While there are significant sources of measurement error and sampling error in the

study, statistical evidence for species effects emerged when species were pooled by life

history attributes (pioneer vs. climax; deciduous vs. coniferous) and subjected to ANCOVA

analysis. Pioneer species and climax species are expected to have differences because of

differential growth patterns and light tolerance, for instance. Likewise, deciduous/semi-

deciduous species and coniferous species are expected to have differences because deciduous

leaf flushing is energy intensive.

46

3.2 Potential explanations for observations, implications, and future

work

Life history traits, including those related to both physiological and physical factors

can frequently provide useful groupings for understanding complex ecosystem processes.

Our analysis indicates that life history traits such as successional status and leaf periodicity

can have a significant effect on the relationship between canopy openness and DBH.

Examination of these functional groupings and their relationship with age-related canopy

thinning could define key objectives for future studies. Appendix 3.1 highlights some basic

life history traits that we suspected might influence the relationship between canopy

openness and tree size: successional category, shade tolerance, dispersal agent, leaf

periodicity, and sexual strategy, some of which were discussed in Chapter 2. These life

history traits, and environmental factors, are discussed in more detail below in relation to our

results and the literature. It must be remembered that life history traits are coarse groupings

that do not always apply throughout a tree’s life cycle (Clark and Clark 1992). A tree species

may start out in one category as a seedling but then change course throughout its lifetime,

like A. blackania’s successional approach (Dalling et al. 2001).

3.2.1 Decreased crown openness with age and the Janzen-Connell hypothesis

Our analysis detected a trend in some species that was opposite what we expected

from our hypothesis. With increasing age, Q. rubra and T. canadensis showed statistically

significant increases in crown closure (p < 0.01 and p < 0.05, respectively). Both being

relatively long-lived species (Burns and Honkala 1990), it is interesting that they demonstrate

a negative relationship between openness and tree size (DBH). It is also worthy to note that

47

temperate species P. strobus and F. grandifolia showed negative trends, although they were

statistically non-significant (low sample size).

Given that both temperate conifers (T. canadensis and P. strobus) displayed a

negative relationship between openness and DBH (although P. strobus did not show a

significant relationship), there is a plausible explanation for this pattern. As evergreens, these

two species do not have to invest energy in entirely replacing their leaves each year. Leaf

replacement in evergreens is a constant, continuous process whereas deciduous trees replace

leaves seasonally. During these seasonal flushes, deciduous trees may be particularly

vulnerable to environmental stress (Cavender-Bares and Holbrook 2001). If a drought strikes

or fungus blight spreads at the time of year when a tree replaces its fallen leaves, the tree

might find itself unable to produce as many leaves as the year before. Evergreens avoid this

vulnerability by shedding and growing leaves evenly throughout the year. Furthermore, the

long-lived evergreen leaves require less nutrient input (Monk 1966). This could prove

beneficial in retaining foliage mass into later stages of ontogeny given the local nature of tree

nutrient uptake and the finite nature of soil nutrient pools. Other explanations for the negative

relationship between openness and DBH in the studied conifers include restricted crown

extension and the high frequency of epicormic branching.

Although the Janzen-Connell hypothesis proposes that seedlings fare better when they

germinate farther from the parent tree (Janzen 1970, Connell 1971), the potential for a parent

tree to create favorable light conditions for its progeny should not be discarded. For

example, T. canadensis is a very shade-tolerant climax species, which tends to grow dense

stands that can nearly eliminate the presence of an understorey (Godman and Lancaster

48

1990). The significant trend of crown closure that we found in our study could demonstrate a

mechanism for creating these dark stands that are less hospitable to shade-intolerant species.

P. copaifera also exhibit clumped distribution, yet its openness-DBH relationship

followed a positive significant relationship. Age-related crown density patterns (positive and

negative alike) could play a role in maintaining light conditions best-suited for conspecifics.

P. copaifera are generally considered shade-tolerant, so the small increase in light

availability provided through crown-thinning could be enough to initiate regeneration. Being

that P. copaifera (which is commonly called el cativo) is one of the most commonly

harvested trees in the Darien region of Panama, it is important to consider how P. copaifera

will regenerate if light conditions provide by mature trees is removed. This is especially of

concern since el cativo is often harvested by clear-cutting its patches, known as cativules. If

these older cohorts of these stands are removed, the moderate light conditions that they

created in the understorey will also be removed. Along with over-harvesting, a lack of

consideration for how this thinning trend affects the regeneration of P. copaifera seedlings

could have contributed to the rapid decline of P. copaifera in neighboring Costa Rica, where

P. copaifera is now considered a threatened species. While pioneers depend on gaps in the

forest for regeneration, shade-tolerant climax species might be more dependent on the

specific light conditions create by parent trees.

3.2.2 Liana loading

The three species that demonstrated age-related crown thinning were noted in field

work to have relatively low liana loads. These three species may be more able to resist lianas,

a capacity that is known to be species-specific (Putz 1983). In species that are susceptible to

liana colonization, it is common for liana loads to increase with age (Kainer et al. 2006).

49

Thus, even if crown thinning was occurring in trees with high liana loads, the thinning trend

might not be apparent. Lianas tend to display their leaves above the leaves of their tree hosts

in order to intercept the light (Schnitzer 2000). Due to this tendency, distinguishing lianas

from tree crowns can be very challenging.

One species that appeared to demonstrate the effect of high liana loads is A.

blackania. During field work, we frequently skipped A. blackania individuals because a high

percentage of their crown was covered by lianas. This species was the only tropical species

studied to show a trend toward an increase in crown density with age. As said before, it is

hard to distinguish whether this crown closure is caused by the lianas on the tree or the leaves

of the tree itself. Therefore, it is not surprising that A. blackania is the one species to show a

negative relationship between openness and tree size. In multiple ways, A. blackania has a

unique life history. Its most unique characteristic is that it can persist in the understorey in

low light levels for years but exhibits growth traits typical of pioneer species when a gap

opens in the canopy (Dalling et al. 2001). A. blackania does not rely on animals to disperse

its seedlings – most will germinate near the parent tree. In this respect, the crown closure

with age might create a darker light environment below its crown where seedlings of its

species can grow, just as in temperate species like T. canadensis (Bourdeau and Laverick

1958). It has the unique ability to persist in the understorey along with the seedlings of

climax species which are shade-tolerant throughout their life history. When a gap opens, A.

blackania can out-compete the climax species to reach the canopy. Although its crown-

closure trend is not statistically significant, it would be worth investigating further because of

A. blackania’s unique life history traits (Appendix 3.1).

50

3.2.3 Crown thinning and reproductive allocations

One potential mechanism for age-related crown thinning involves an allocation of

resources away from structural tissue (leaves and branches) to sexual organs once trees reach

maturity (Obeso 2002). While the majority of the studied species had both sexual structures

present on each tree (were monoecious or hermaphroditic), four species were dioecious. We

can expect by chance that half of the individuals sampled from these four species were male,

without the capability to produce fruit, and therefore without the potential for reproduction-

related crown thinning, presuming the fruit, and not flower, production is of importance in

this regard. It is noteworthy that three of the four dioecious species studied did not display a

significant trend. If we had recorded which trees were male and female (and collected a

higher sample size of each), we might have been able to pull out two separate openness vs.

tree size trends within each species.

A related life history pattern of interest was how the specific seed sizes would relate

to the crown openness trends. Although the typical dispersal agent does not necessarily

dictate average seed size (Howe and Smallwood 1982), a species that disperses its seeds

through the wind will generally have smaller seeds than a species that depends on animal

dispersal. Of the fourteen species studied that showed positive trends between openness and

DBH, nine species are known to have relatively large animal-dispersed seeds. For instance,

the temperate deciduous species with animal dispersed seeds (F. americana, P. serotina, and

Q. rubra) bear large edible fruits (and seeds). It is possible that the higher energy costs

associated with producing larger seeds could have contributed to higher prevalence of age-

related crown thinning in these species. Monocarpic trees, such as BCI’s Tachigalia

versicolor, which have their one and only fruit production event before death (Loveless et al.

51

1998), would be ideal candidates to evaluate how allocation of resources towards

reproductive structures effect the overall health of the tree leading up to the masting event.

3.2.4 Physical and environmental explanations

Only three of the ten tropical species had significant positive relationships: J. copaia

(p < 0.01), B. pendula (p < 0.05), and P. copaifera (p < 0.05). These three species are also the

species that we found to have the highest Crown Illumination Index (CII) of the species

sampled on Barro Colorado Island. This index describes the social position of the crowns: a

reading of “5” given to trees whose crowns are entirely above the canopy and a “1” given to

tree crowns that are completely below the canopy and are not receiving direct sunlight. Being

above the canopy, these three species would have been exposed to excessive levels of solar

radiation, wind, and storms. These stressors can lead to mortality, such as crown breakage

(Clark and Clark 1991) or crown abrasion (Putz et al. 1984).

The hydraulic limitation hypothesis also applies as a biomechanical explanation for

the pronounced canopy thinning in the three sampled dominants. The hydraulic limitation

hypothesis states that as trees grow into the very high levels of the canopy, the tree’s vascular

system needs more pressure to overcome the forces of gravity. At the heights of the crowns,

trees might not be able to maintain adequate cell turgor in the leaves. The presence of lower

hydraulic conductivity in older trees compared to recently mature trees has been found in

multiple studies (Ryan and Yoder 1997, Hubbard et al. 1999, Ryan et al. 2006). Although our

study did show some significant trends correlating crown openness and tree size, we did not

find significant relationships between crown openness and tree height, which would have

provided some backing for the hydraulic limitation hypothesis (Appendix 2.1). It would be

interesting if further studies found the same. This distinction could mean that crown density

52

changes that occur later in tree ontogeny could be more closely associated with the internal

physiological state of the tree rather than the physical position and exposure of its crown.

3.2.5 Alternative methods in future work

There are a few other changes in approach to this study that could improve our

understanding of how crown openness changes throughout a tree’s life. For example, it

would be informative to also look at tree growth rates. It is known that trees grow more

slowly before dying (Ruger et al. 2011). Whether growth rates were quantified over five

years or just one year, this dynamic measurement would provide more insight into the current

health status of the tree. The DBH shows evidence of a lifetime of growth but does not depict

which trees are becoming stronger or are on the decline. Data from repeated censuses could

provide insight into whether crown thinning is associated with tree mortality.

Another area of the study that should be altered going forward is our approach to

collecting moosehorn crown openness readings. While valid inferences can be drawn from

our data set as is, it is important to acknowledge and address the shortcomings of our

methods. When repeat moosehorn measurements were taken on 77 trees, we found a

correlation coefficient of only 0.46 (p <0.001). Although the linear regression of the repeat

measurements is highly statistically significant, this low correlation means that

measurements taken of the same tree can yield very different results. One way to combat this

discrepancy would be to take more readings at each tree to ensure that a true representation

of the crown is captured in the average value. With such a low R2

value, doubling the

samples per tree (six readings instead of three) would seem appropriate. Unfortunately,

doubling the time spent at each tree would contradict the initial draw to using the moosehorn:

the ability to take quick readings and attain large sample sizes at reasonable cost.

53

Nevertheless, fast data collection is not the only advantage to using a moosehorn. Along with

being simple and cheap to make from scratch, moosehorns are durable in any climate. If

sampling size per tree were increased, moosehorns could continue to be a valuable tool used

by scientists with limited resources.

For researchers with access to state-of-the-art technologies, LiDAR could become an

important tool for understanding both forest and tree structure. LiDAR uses laser pulses to

determine topographical structure of the forest canopy. LiDAR is unique from other aerial

imaging because the laser pulses can penetrate the canopy to provide a 3-D representation of

the forest below the top of the canopy. LiDAR could be used to observe the crown openness

by assessing the crown density in the footprint area of the tree of interest. Further, there is a

great deal of research being done to identify tree species using LiDAR alone (Magnussen and

Boudewyn 1998, Naesset and Okland 2002). An ability to determine tree species and crown

density from one data set could allow researchers to look at the trend across a very large area.

Instead of spending months collecting data, researchers would be able to use a LiDAR data

set collected by plane within a few hours. Especially for a study of this sort, where we are

looking for a general trend across multiple species, there is considerable potential for LiDAR

to contribute to the continued advancement of forest science, including our knowledge of

age-related patterns in crown openness (e.g. Thomas et al. 2006). Although technologies

continue to improve, LiDAR might not be best suited for the detection of small-scale crown

thinning. The spread of the laser would generally make only large canopy openings visible if

fixed-wing aircrafts are used. While the dominance of LiDAR for large-scale or global

projects continues to grow (Simard et al. 2011, LeToan et al. 2011), crown level assessment

using LiDAR must still be honed.

54

While assessing crown thinning trends using LiDAR might still present some

technological obstacles, other forms of forest modeling could readily make use of data

presented in this study. The relationships between openness and DBH could be used to

provide parameters that could be put into a model like SORTIE (Murphy 2008). In all studied

species showing significantly positive relationships, the regressions indicate that there should

be more than a two-fold increase in openness between recently mature trees and very old

trees. Specifically, Figure 2.2 and Figure 2.3 show A. saccharum following a trend from 4%

openness in recently mature trees ranging to a 20% in the largest sampled trees; B. pendula:

2% to 7%; J. copaia: 4% to 8%, and P. copaifera: 1%-3%. Most models of forest dynamics

consider variation in gap openness size but do not consider the heterogeneity that exists in

non-gap areas. These data could be incorporated into models to capture additional levels of

complexity that clearly exist in forest systems.

3.3 Concluding remarks

Our study has not determined a general, cross-species trend for age-related crown

openness changes; however, it has highlighted the vast differences in growth strategies that

exist even within functional groups and biomes. Despite the variation in results, the six

species that show significance in the relationship between openness and tree age demonstrate

that this concept is worthy of further investigation. Through an increase in sample size, a

focus on larger size classes, and a more accurate assessment of openness, these trends might

be found to be more pronounced and widespread. In a field where age-related changes are

difficult to detect, these results provide examples of traits that shift throughout the tree’s later

life stages. These age-related changes contribute to a slow and constant flux of light into the

understorey that can go unnoticed in comparison to a gap creation’s flood of light.

55

Literature Cited

Acosta FJ, Delgado JA, Lopez F, Serrano JM. 1997. Functional features and ontogenetic

changes in reproductive allocation and partitioning strategies of plant modules. Plant

Ecology 132: 71-76.

Aerts R. 1995. The advantages of being evergreen. Trends in Ecology and Evolution 10:

402–407.

Aerts R, Chapin FS. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of

processes and patterns. Advances in Ecological Research 30:1–67.

Aide TM. 1987. Limbfalls: a major cause of sapling mortality for tropical forest plants.

Biotropica 19: 284-285.

Astrup R, Larson BC. 2006. Regional variability of species-specific crown openness for

aspen and spruce in western boreal Canada. Forest ecology and management. 228(1):

241-250.

Aubreville A. 1938. La foret coloniale; les forets de l’Afrique occidentale francais. Annales

Academie Sciences Coloniale 9: 1–245.

Baltzer JL, Thomas SC. 2007a. Physiological and morphological correlates of whole plant

light compensation point in temperate deciduous tree seedlings. Oecologia 153: 209-

223.

Baltzer JL, Thomas SC. 2007b. Determinants of whole plant light requirements in Bornean

rain forest trees. Journal of Ecology 95: 1208-1221.

Beaudet M, Messier C, Canham CD. 2002. Predictions of understorey light conditions in

northern hardwood forests following parameterization, sensitivity analysis, and tests

of the SORTIE light model. Forest Ecology and Management 165(1): 235-248.

Boege K, Dirzo R, Siemens D, Brown P. 2007. Ontogenetic switches from plant resistance to

tolerance: minimizing costs with age? Ecology Letters 10(3):177-187.

Boege K, Marquis RJ. 2005. Facing herbivory as you grow up: the ontogeny of resistance in

plants. Trends in Ecology and Evolution 20: 441-449.

Bohlman S, O’Brien S. 2006. Allometry, adult stature and regeneration requirement of 65

tree species on Barro Colorado Island, Panama. Journal of Tropical Ecology 22: 123-

136.

Bourdeau PF, Laverick ML. 1958. Tolerant and photosynthetic adaptability to light intensity

in white pine, red pine, hemlock, and Ailanthus seedlings. Forest Science 4: 196-202.

56

Brokaw NVL. 1982. The definition of treefall gap and its effect on measures of forest

dynamics. Biotropica 11: 158–160.

Brokaw NVL. 1985. Gap-phase regeneration in a tropical forest. Ecology 66(3): 682-687.

Brokaw NVL. 1987. Gap-phase regeneration of three pioneer tree species in a tropical forest.

Journal of Ecology 75: 9-19.

Burns RM, Honkala BH. 1990. Silvics of North America: Volume 1, Conifers & Volume 2,

Hardwoods. Forest Service. United States Department of Agriculture, Washington,

D.C.

Canham CD. 1988. An index for understory light levels in and around canopy gaps. Ecology

69:1634-1638.

Canham CD, Burbank DH. 1994. Causes and consequences of resource heterogeneity in

forests: interspecific variation in light transmission by canopy trees. Canadian Journal

of Forest Research 24: 337-349.

Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS. 1990. Light regimes

beneath closed canopies and tree-fall gaps in temperate and tropical forests. Canadian

Journal of Forest Research 20(5): 620-631.

Castello JD, Leopold DJ, Smallidge PJ. 1995. Pathogens, patterns, and processes in forest

ecosystems. BioScience 45(1):16-24.

Catovsky S, Bazzaz FA. 2002. Nitrogen availability influences regeneration of temperate tree

species in the understorey seedling bank. Ecological Applications 12(4): 1056-1070.

Cavender-Bares J, Bazzaz FA. 2000. Changes in drought response strategies with ontogeny

in Quercus rubra: implications for scaling from seedlings to mature trees. Oecologia

124(1): 8-18.

Cavender-Bares J, Holbrook NM. 2001. Hydraulic properties and freezing-induced cavitation

in sympatric evergreen and deciduous oaks with contrasting habitats. Plant, Cell and

Environment 24: 1243-1256.

Chazdon RL, Fletcher N. 1984. Light environments of tropical forests. In: Medina E,

Monney HA, Vasquez-Yanes C, editors. Physiological ecology of plants of the wet

tropics. The Hague, Netherlands: W. Junk Publishers. p 27-36.

Chen JM. 1996. Optically-based methods for measuring seasonal variation of leaf area index

in boreal conifer stands. Agricultural and Forest Meteorology 80(2): 135-163.

Clark DB, Clark DA. 1990. Distribution and effects on tree growth of lianas and woody

hemiepiphytes in a Costa Rican tropical wet forest. Journal of Tropical Ecology 6:

321-331.

57

Clark DB, Clark DA. 1991. The impact of physical damage on canopy tree regeneration in

tropical rain forest. Journal of Ecology 79: 447-457.

Clark DA, Clark DB. 1992. Life history diversity of canopy and emergent trees in a

neotropical rain forest. Ecological Monographs 62(3): 315-344.

Clark DB, Clark DA. 1996. Abundance, growth and mortality of very large trees in

neotropical lowland rain forest. Forest Ecology and Management 80: 235-244.

Clark DB, Olivas PC, Oberbauer SF, Clark DA, Ryan G. 2008. First direct landscape-scale

measurement of tropical rain forest Leaf Area Index, a key driver of global primary

productivity. Ecology Letters 11: 163-172.

Connell JH. 1971. On the role of natural enemies in preventing competitive exclusion in

some marine animals and in rain forest trees. In: den Boer PJ, Gradwell GR, editors.

Dynamics of populations. Proceedings of the Advanced Study Institute on Dynamics

of numbers in populations. Oosterbeek, Netherlands: Centre for Agricultural

Publishing and Documentation. p 298-310

Crawley MJ. 2005. Statistics: An Introduction Using R. Exercise 6: Ancova. Imperial

College London. Available at

<http://www.bio.ic.ac.uk/research/crawley/statistics/exercises.htm>.

Croat TB. 1978. Flora of Barro Colorado Island. Stanford University Press.

Dalling JW, Winter K, Nason JD, Hubbell SP, Murawski DA, Hamrick JL. 2001. The

unusual life history of Alseis blackiana: a shade-persistent pioneer tree? Ecology

82(4): 933-945.

Dewalt SJ, Schnitzer SA, Denslow JS. 2000. Density and diversity of lianas along a

chronosequence in a central Panamanian lowland forest. Journal of Tropical

Ecology 16(1): 1-19.

Foster RB, Brokaw N. 1996. Structure and history of the vegetation of Barro Colorado

Island. In: Leigh EG, Rand AS, Windsor DM, editors. The ecology of a tropical forest

seasonal rhythms and long-term changes. 2nd

ed. Washington, DC: Smithsonian

Institution Press. p 67-82.

Gandolfi S, Joly CA, Rodrigues RR. 2007. Permeability - impermeability: canopy trees as

biodiversity filters. Scientia Agricola. 64 (4): 433-438.

Garrison GA. 1949. Uses and modifications for the ‘Moosehorn' crown closure estimator.

Journal of Forestry 47: 733-735.

Givnish TJ. 2002. Adaptive significance of evergreen vs. deciduous leaves: solving the triple

paradox. Silva Fennica 36(3): 703-743.

58

Godman RM, Lancaster K. 1990. Eastern Hemlock. In: Burns, Russell M., and Barbara H.

Honkala, editors. 1990. Silvics of North America: 1. Conifers; 2. Hardwoods.

Agriculture Handbook. Washington, DC: U.S. Department of Agriculture, Forest

Service.

Gove JH, Fairweather SE. 1988. Tree-ring analysis of a 500-year old hemlock in central

Pennsylvania. U.S. Forest Service General Technical Report NC 120 (1): 483-489.

Gower ST, McMurtie RE, Murty D. 1996. Aboveground net primary production decline with

stand age: potential causes. Tree 11(9): 378-382.

Gravel D, Canham CD, Beaudet M, Messier C. 2010. Shade tolerance, canopy gaps and

mechanisms of coexistence of forest trees. Oikos 119(3): 475-484.

Gross HL. 1972. Crown deterioration and reduced growth associated with excessive seed

production by birch. Canadian Journal of Botany 50: 2431-2437.

Harper JL, White J. 1974. The demography of plants. Annual Review of Ecology and

Systematics. 5: 419-463.

Hartshorn GS. 1989. Application of gap theory to tropical forest management: natural

regeneration in strip clearcuts in the Peruvian Amazon. Ecology 70: 567–569.

Hossain SMY, Caspersen JP. 2012. In-situ measurement of twig dieback and regrowth in

mature Acer saccharum trees. Forest Ecology and Management 270: 183-188.

Howe HF, Smallwood J. 1982. Ecology of seed dispersal. Annual Review of Ecology and

Systematics 13: 201-228.

Hubbard RM, Bond BJ, Ryan MG. 1999. Evidence that hydraulic conductance limits

photosynthesis in old Pinus ponderosa trees. Tree Physiology 19:165-172.

Hubbell SP. 1979. Tree dispersion, abundance, and diversity in a tropical dry forest. Science

203(4387): 1299-1309.

Ingwell LI, Wright SJ, Becklund KK, Hubbell SP, Schnitzer SA. 2010. The impact of lianas

on 10 years of tree growth and mortality on Barro Coloardo Island, Panama. Journal

of Ecology 98: 879-887.

Innes JL. 1994. The occurrence of flowering and fruiting on individual trees over 3 years and

their effects on subsequent crown condition. Trees 8: 139–150.

Ishii H, McDowell N. 2002. Age-related development of crown structure in coastal Douglas-

fir trees. Forest Ecology and Management 169: 257-270.

Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. American

Naturalist. 104: 501-528.

59

Kainer KA, Wadt LHO, Gomes-Silva DAP, Capanu M. 2006. Liana loads and their

association with Bertholletia excelsa fruit and nut production, diameter growth and

crown attributes. Journal of Tropical Ecology. 22: 147–154.

Kathke S, Bruelheide H. 2009. Gap dynamics in a near-natural spruce forest at Mt. Brocken,

Germany. Forest Ecology and Management 259: 624-632.

Kato S, Komiyama A. 2002. Spatial and seasonal heterogeneity in understorey light

conditions caused by different leaf flushing of deciduous overstory trees. Ecological

Research 17: 687-693.

Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T. 2006. Changes in

photosynthesis and leaf characteristics with tree height in five dipterocarp species in a

tropical rain forest. Tree Physiology 26: 865-873.

Kobe RK. 1999. Light gradient partitioning among tropical tree species through differential

seedling mortality and growth. Ecology 80(1): 187-201

Kolb TE, Matyssek R. 2001. Limitations and perspectives about scaling ozone impacts in

trees. Environmental Pollutions 115(3): 373-393.

Kubota Y, Hara T. 1996. Allometry and competition between saplings of Picea jezoensis and

Abies sachalinensis in a sub-boreal coniferous forest, northern Japan. Annals of

Botany 77(5): 529-538.

Lefsky MA. 2010. A global forest canopy height map from the Moderate Resolution Imaging

Spectroradiometer and the Geoscience Laser Altimeter System. Geophysical

Research Letters 37(15): 1-5.

Le Toan T, Quegan S, Davidson MWJ, Balzter H, Paillou P, Papathanassiou K, Ulander L.

2011. The BIOMASS mission: Mapping global forest biomass to better understand

the terrestrial carbon cycle. Remote sensing of environment 115(11): 2850-2860.

Lieberman M, Lieberman D, Peralta R. 1989. Forests are not just swiss cheese: canopy

stereogeometry of non-gaps in tropical forests. Ecology 70:550–555.

Loveless MD, Hamrick JL, Fosters RB. 1998. Population structure and mating system in

Tachigali versicolor, a monocarpic neotropical tree. Heredity 81: 134-143.

Lutz JA, Halpern CB. 2006. Tree mortality during early forest development: A long-term

study of rates, causes, and consequences. Ecological Monographs 76: 257-275.

Magnussen S, Boudewyn P. 1998. Derivations of stand heights from airborne laser scanner

data with canopy-based quantile estimators. Canadian Journal of Forest Research 28:

1016-1031.

March WJ, Skeen JN. 1976. Global radiation beneath the canopy and in a clearing of

suburban hardwood forest. Agricultural Meterology 16: 321-327.

60

Martinez-Vilalta J, Vanderklein D, Mencuccini M. 2007. Tree height and age-related decline

in growth in Scots pine (Pinus sylvestris L.). Ecophysiology 150: 529-544.

McCarthy J. 2001. Gap dynamics of forest trees: A review with particular attention to boreal

forests. Environmental Reviews 9 (1): 1-59.

Meier AR, Saunders MR, Michler CH. 2012. Epicormic buds in trees: a review of bud

establishment, development and dormancy release. Tree physiology 32(5): 565-584.

Miller GW. 1996. Epicormic branching on Central Appalachian Hardwoods 10 years after

deferment cutting.USDA Forest Service. Research Paper NE-702.

Monk CD. 1966. An ecological significance of evergreenness. Ecology 47: 504-505.

Montgomery RA, Chazdon RL. 2002. Light gradient partitioning by tropical tree seedlings in

the absence of canopy gaps. Oecologia 131: 165-174.

Murphy LE. 2008. SORTIE-ND User Manual, Version 6.09. Millbrook, New York: Institute

of Ecosystem Studies. Available online: <www.sortie-nd.org>.

Naesset E, Okland T. 2002. Estimating tree height and tree crown properties using airborne

scanning laser in a boreal nature reserve. Remote Sensing of Environment. 79: 105-

115.

Nock CA, Caspersen JP, Thomas SC. 2008. Large ontogenetic declines in intra-crown leaf

area index in two temperate deciduous tree species. Ecology 89(3): 744-753.

Obeso JR. 2002. The costs of reproduction in plants. New Phytol. 155: 321-348.

O’Brien ST, Hubbell SP, Spiro P, Condit R, Foster RB. 1995. Diameter, Height, Crown, and

Age Relationships in Eight Neotropical Tree Species. Ecology 76 (6): 1926.

Panditharathna PAKAK, Singhakumara BMP, Griscom HP, Ashton MS. 2008. Change in

leaf structure in relation to crown position and size class for tree species within a Sri

Lankan tropical rain forest. Botany 86(6): 633-640.

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.

Putz FE. 1983. Liana biomass and leaf area of a “Tierra Firme” forest in the Rio Negra

Basin, Venezuela. Biotropica 15(3): 185-189.

Putz FE, Parker GG, Archibald RM. 1984. Mechanical abrasion and intercrown spacing.

American Midland Naturalist 112(1): 24-28.

61

R Development Core Team. 2008. R: A language and environment for statistical

computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-

900051-07-0. Available at <http://www.R-project.org>.

Reich PB, Walters MB, Kloeppel BD, Ellsworth DS. 1995. Different photosynthesis-nitrogen

relations in deciduous hardwood and evergreen coniferous tree species. Oecologia,

104(1): 24-30.

Ricard JP, Messier C, Delagrange S, Beaudet M. 2003. Do understorey sapling respond to

both light and below-ground competition?: a field experiment in a north-eastern

American hardwood forest and a literature review. Annals of Forest Science 60(8):

749-756.

Ruger N, Huth A, Hubbell SP, Condit R. 2011. Determinants of mortality across a tropical

lowland rainforest community. Oikos 120: 1047-1056.

Ryan MG, Yoder BJ. 1997. Hydraulic limits to tree height and tree growth. Bioscience 47:

235-242.

Ryan MG, Binkley D, Fownes JH. 1997. Age-related decline in forest productivity: patterns

and processes. Advances in Ecological Research 27: 214-262.

Ryan MG, Phillips N, Bond BJ. 2006. The hydraulic limitation hypothesis revisited. Plant,

Cell and Environment 29: 367-381.

Sanchez MC, San-Jose MC, Ballester A, Vieitez AM. 1996. Requirements for in vitro

rooting of Quercus robur and Q. rubra shoots derived from mature trees. Tree

Physiology 16 (8): 673-680.

Schnitzer SA, Bongers F. 2002. The ecology of lianas and their role in forests. TRENDS in

Ecology & Evolution 17(5): 223-230.

Schnitzer SA, Kuzee ME, Bongers F. 2005. Disentangling above‐and below‐ground

competition between lianas and trees in a tropical forest. Journal of Ecology 93(6):

1115-1125.

Simard M, Pinto N, Fisher JB, Baccini A. 2011. Mapping forest canopy height globally with

spaceborne lidar. Journal of Geophysical Research: Biogeosciences (2005–

2012), 116(G4).

Smith FW, Long JN. 2001. Age-related decline in forest growth: an emergent property.

Forest Ecology and Management 144: 175-181.

Souza RP, Valio IFM. 2001. Seed size, seed germination and seedling survival of Brazilian

tropical tree species differing in successional status. Biotropica 33: 447-457.

Swaine MD, Lieberman D, Putz FE. 1987. The dynamics of tree populations in tropical

forest: a review. Journal of Tropical Ecology 3(4): 359-366.

62

Sterck FJ, Bongers F. 1998. Ontogenetic changes in size, allometry, and mechanical design

of tropical rain forest trees. American Journal of Botany 85(2): 266-272.

Thomas SC. 2010. Photosynthetic capacity peaks at intermediate size in temperate deciduous

trees. Tree physiology 30(5): 555-573.

Thomas SC. 2011. Age-related changes in tree growth and functional biology: the role of

reproduction. Invited chapter for “Size- and Age-Related Changes in Tree Structure

and Function”, Meinzer FC, Dawson T, Lachenbruch BJ, editors. Springer-Verlag

Tree Physiology Series. p 33-64.

Thomas SC, Ickes K. 1995. Ontogenetic changes in leaf size in Malaysian rain forest trees.

Biotropica 27(4): 427-434.

Thomas SC, LaFrankie JV. 1993. Sex, size, and inter-year variation in flowering among

dioecious trees of the Malayan rainforest understorey. Ecology 74: 1529-1537.

Thomas SC, Sztaba AJ, Smith SM. 2010. Herbivory patterns in mature sugar maple:

variation with vertical canopy strata and tree ontogeny. Ecological Entomology 35: 1-

8.

Thomas SC, Winner WE. 2000. Leaf area index of an old-growth Douglas-fir forest

estimated from direct structural measurements in the canopy. Canadian Journal of

Forest Research 30(12): 1922-1930.

Thomas SC, Winner WE. 2002. Photosynthetic differences between saplings and adult trees:

an integration of field results by meta-analysis. Tree Physiology 22: 117-127.

Thomas V, Trietz P, McCaughey JH, Morrison I. 2006. Mapping stand-level forest

biophysical variables for a mixedwood boreal forest using lidar: an examination of

scanning density. Canadian Journal of Forest Research 36: 34-47.

Verhulst PF. 1838. Notice sur la loi que la population poursuit dans son accroissement.

Correspondance mathématique et physique 10: 113–121.

Ward WW. 1966. Epicormic branching of black and white oaks. Forest Science 12(3): 290-

296.

Watt AS. 1947. Pattern and process in the plant community. Journal of Ecology 35:1-22.

Weaver PL, Murphy PG. 1990. Forest structure and productivity in Puerto Rico's Luquillo

Mountains. Biotropica 22(1): 69-82.

Whitmore TC. 1978. Gaps in the forest canopy. In: Tomlinson PB, Zimmerman MH, editors.

Tropical Trees as Living Systems. London: Cambridge University Press. p 639-655.

Whitmore TC. 1990. An introduction to tropical rain forests. Oxford, UK: Oxford University

Press.

63

White PS. 1979. Pattern, process, and natural disturbance in vegetation. Botanical Review.

45: 229-299.

Whitney GG. 1982. A demographic analysis of the leaves of open and shade grown Pinus

strobus L. and Tsuga canadensis (L.) Carr. New Phytologist. 90: 447-453.

Woodruff DR, Bond BJ, Meinzer FC. 2004. Does turgor limit growth in tall trees? Plant,

Cell & Environment 27(2): 229-236.

Woodruff DR, Meinzer FC. 2011. Size-dependent changes in biophysical control of tree

growth: the role of turgor. In: Size-and age-related changes in tree structure and

function. Netherlands: Springer. p 363-384.

Yamamoto S. 2000. Forest gap dynamics and tree regeneration. Journal of Forest Research 5

(4): 223-229.

Young TP, Hubbell SP. 1991. Crown asymmetry, treefalls, and repeat disturbance of broad-

leaved forest. Ecology 72(4): 1464-1471.

Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR. 1994. Evidence of

Reduced Photosynthetic Rates in Old Trees. Forest Science 40(3):514-527.

64

Appendices

Appendix 2.1: Summary of regression results between direct crown openness and DBH for eight temperate species sampled at Haliburton Forest, Ontario, and

Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical species sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot,

Puerto Rico, in 2010 and 2011. All x- and y-axes are log-transformed. Additional linear regressions include: overlap-corrected openness vs. DBH, openness vs.

height, and openness vs. crown depth. Average Crown Illumination Index (CII) and average liana scores (LS) also provided for each species.

n Log direct open vs Log DBH Log overlap vs Log DBH Log direct open vs. Log

Height

Log direct open vs. Log

Depth

Avg.

CII

Avg.

LS Intercept R2 p-value Int R2 P Int R2 p Int R2 p

Tropical species 814 0.397 0.024 1.0e-05

***

Alseis blackania 85 -0.527 0.026 0.14 0.578 0.041 0.061 -0.079 0.0004 0.86 -0.278 0.0172 0.23 3.49 1.82

Beilschmiedia pendula 76 1.06 0.103 0.005 1.089 0.084 0.010

*

0.332 0.007 0.47 -0.463 0.0581 0.035 4.00 1.13

Jacaranda copaia 83 0.647 0.071 0.014 0.268 0.019 0.209 0.126 0.004 0.58 0.110 0.0123 0.32 4.80 0.26

Prioria copaifera 87 0.665 0.071 0.013 0.147 0.069 0.014

*

-0.609 0.020 0.19 -0.185 0.0095 0.37 4.14 1.60

Quararibea asterolepis 91 -13.4 0.059 0.064 -0.417 2.37e-8 0.999 0.434 0.020 0.18 -0.257 0.0202 0.17 3.94 0.54

Tabernaemontana

arborea

76 0.699 0.042 0.067 0.404 0.042 0.074 -0.286 0.011 0.35 -0.0038 4.3e-6 0.99 3.37 1.99

Tetragastris panamensis 75 -22.7 0.11 0.012 0.838 0.023 0.190 0.319 0.015 0.30 -0.0542 9.5e-4 0.80 3.67 1.92

Trichilia tuberculata 76 0.408 0.008 0.440 0.572 0.006 0.519 0.355 0.011 0.37 -0.0570 8.2e-4 0.80 3.73 1.35

Buchenavia tetraphylla 64 0.038 0.001 0.800 -0.165 0.0001 0.929 0.158 0.007 0.53 -0.192 0.0589 0.051 4.54 2.03

Manilkara bidentata 85 0.343 0.025 0.140 0.145 0.024 0.158 0.034 0.0001 0.95 0.114 0.0064 0.46 3.86 1.59

Temperate species 972 0.459 0.013 0.0003

***

- Positive significant relationships

- Negative significant relationships

- Non-linear significant relationships

Acer saccharum 646 1.380 0.079 3.3e-13

*** Betula alleghaniensis 35 0.663 0.042 0.230

Fagus grandifolia 38 -0.143 0.00183 0.80

Fraxinus americana 46 -71.1 0.29 0.0004

Pinus strobus 52 -0.368 0.015 0.380

Prunus serotina 38 -64.5 0.34 0.0005

Quercus rubra 52 -1.000 0.192 0.0010

** Tsuga canadensis 58 -1.050 0.070 0.044

All Species 1786 0.035 0.0001 0.640

65

Appendix 2.2: Summary of linear regression results for pooled data for eight temperate species

sampled at Haliburton Forest, Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and

ten tropical species sampled at Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot,

Puerto Rico, in 2010 and 2011. All x- and y-axes are log-transformed.

Sample size (n) R2 value p-value

All species 1786 0.0001 >0.1

Biome Temperate

species

972 0.013 <0.001

Tropical species 814 0.024 <0.001

Successional

strategy

Pioneer species 398 0.010 <0.1

Climax species 1388 0.001 >0.1

Leaf periodicity Deciduous/semi-

deciduous species

1418 0.010 <0.001

Evergreen species 368 0.002 >0.1

66

Appendix 3.1: Basic life history traits for eight temperate species sampled at Haliburton Forest,

Ontario, and Koeffler Science Reserve, Ontario, in 2009 and 2010, and ten tropical species sampled at

Barro Colorado Island, Panama, and Luquillo Forest Dynamics Plot, Puerto Rico, in 2010 and 2011.