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This is to certify that the
dissertation entitled

MULTIPLE SCALE PATTERNS IN GROWTH AND
STRUCTURE OF SUBTROPICAL DRY FORESTS: SOILS,
TREES, AND HURRICANES

presented by

Skip Judson Van Bloem

has been accepted towards fulﬁllment
of the requirements for the

Doctoral degree in Botany and Plant Pathology
and Program in Ecology,
Evolutionary Biology and
Behavior

 

 

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MULTIPLE SCALE PATTERNS IN GROWTH AND STRUCTURE OF
SUBTROPICAL DRY FORESTS: SOILS, TREES, AND HURRICAN ES

by

Skip judson Van Bloem

A DISSERTATION

Submitted to
Michigan State University

in partial fulﬁllment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Botany and Plant Pathology
and Program in Ecology, Evolutionary Biology and Behavior

2004

ABSTRACT

MULTIPLE SCALE PATTERNS IN GROWTH AND STRUCTURE OF
SUBTROPICAL DRY FORESTS: SOILS, TREES, AND HURRICANES

by

Skip judson Van Bloem

Compared to dry forests found in other tropical locations, those in the West Indies have a
unique structure — with higher stem density, a larger proportion of multiple stemmed trees,
and less basal area at maturity. The primary goal of this dissertation is to identify factors that
lead to the unique structure of West Indian dry forest, using Guanica Forest, Puerto Rico, as
a representative example. This dissertation addresses two potential mechanisms for the
unique structure of West Indian dry forest: nutrient limitation and hurricane disturbance.

I assessed forest maturity by resampling trees from plots within a research site 18
years after site establishment. Basal area increased by 7.3% while stem density increased by
<1%. Mortality equaled in-growth. Nutrient pools remained constant. Without the effects
of the hurricane, the forest would appear to be aggrading, with increases of 11% in stem
density and 26% in basal area since 1981. Species composition changed little, but putative
pioneer species decreased in importance.

The size and distribution of nutrient pools were analyzed using geostatistical
methods in four research sites in Guanica Forest. Nutrient limitation was assessed by
comparing species distribution and tree growth rates to nutrient gradients and by
manipulating nutrient concentrations in root in-growth cores. Nutrient patch size ranged
from 17-25 m. Spatial distributions of nitrogen and organic matter were similar among and
within sites. Although calcium binds with phosphorus at the high pH (7.8) found in

Guanica soils, there were no strong correlations between pool sizes and spatial distributions

for pH, Ca, and P. Soil nutrients were greatest where litter accumulated, either in small
depressions or crevices between outcrops. Individuals of common tree species were present
across the entire breadth of each nutrient gradient, suggesting that these species distributions
were not limited by nutrient pool size. Nutrient pools inﬂuence the growth of basal sprouts,
but were not associated with the growth of mature trees. Root growth in cores treated with
N exceeded that in control or P treatments but was greatest in the NP-combined treatment,
indicating co-limitation of root growth. Guanica Forest had higher values of soil pH and
larger pools of organic matter (OM), N, and total P than reported for other dry forests.

The effects of hurricane disturbance were determined following Hurricane Georges
in 1998. Over 3000 stems were assessed for damage, mortality, and sprouting in 33 different
plots within Guanica Forest and nearby in 19 forest fragments. Hurricane winds damaged
only 12.4% of stems but damage was biased toward larger-diameter stems. Stem mortality
was only 2% and not associated with size class. Damage was greatest in exposed sites and
was caused by the storm’s strongest winds. Leaf litterfall was about half that of average
annual levels, but nutrient return in leaf litterfall equaled or surpassed annual averages. Basal
sprouting following the hurricane was tenfold greater than pre-hurricane levels (3.5%).
Sprouting was not related to the severity of stem damage or defoliation.

Overall, hurricanes appear to have a greater inﬂuence on the structure of Guanica
Forest than do nutrient pools. Hurricane Georges damaged large stems and caused basal
area losses equaling decades of growth. Furthermore, the hurricane resulted in a widespread
sprouting response that could increase stem density and the proportion of multi—stemmed
trees as sprouts mature into stems. Soil nutrient content most inﬂuenced growth and
survival of basal sprouts. Although other mechanisms may exist, hurricanes play a central

role in determining the structure of West Indian dry forest.

Copyright By
SKIP JUDSON VAN BLOEM
2004

ACKNOWLEDGMENTS

I would never have been able to wade through the reams of data and hours of lab
work necessary to complete this project without the professional and personal assistance of
many individuals.

Ariel Lugo provided cheerful advice, support and encouragement, as well as helping
to identify other useful opportunities for my research and career development. He and Fred
Scatena allowed me to use the facilities of the soil nutrient labs at the USDA Forest Service,
International Institute of Tropical Forestry. Under a co-operative agreement with the Forest
Service (IITF-98-CA-006), funding was provided to ﬁnance my ﬁeld trips to Puerto Rico
and to allow the lab staff of Mary Jeane Sanchez, Edwin Nunez, and Maribelis Santiago to
help analyze my nutrient samples. Their careful attention to detail and helpful advice were
indispensable. Having worked with them, it is easy to understand why the IITF soils lab has
such a good reputation. In addition, Carlos Rodriguez provided GPS equipment and
processed data, making many of the spatial analyses performed herein possible.

Miguel Canals and the staff of the Bosque Seco de Guanica supplied me with useful
observations, insight into site selection, and background into local history and contacts of
others doing research in the forest. Their speed in re-opening the forest after Hurricane
Georges made timely observations possible. I am grateful for Sr. Canals' trust in my pursuits.

Field work in Puerto Rico was fantastic. Much of my success and satisfaction in PR
can be traced to the other MSU folks doing research in Guanica Forest and sharing summer
quarters with me. I had the good fortune of spending my ﬁrst two ﬁeld seasons with John
Genet, Kristen Genet and Ian Ramjohn. Field hands were numerous and all did a ﬁne job

helping with research and providing friendship. Thanks to Christa Jen, Alan Talhelm, Adam

LaVoy, Joe Harsh, Katie Donaghue, Arecelis Tirado, Daniel Colon, Joseanibal Colon, and
Kathleen Shearman. Christa, Alan, Katie, and Allen Dawson helped explore some ideas
growing out of this dissertation in undergraduate thesis projects at MSU.

My sister, Nikki Van Bloem, has spent substantial portions of her winter vacations
entering data, grinding litter, and processing root in-growth cores. I don’t think the
experience will convince her to begin a new career in science, but I appreciate her help and
cheerful approach to some of my more tedious tasks.

Frank Telewski brought me up to speed on the role of hormones in regulating
sprouting response. His insight was crucial in interpreting post-hurricane sprouting patterns.
Elvira Cuevas loaned root in-growth baskets to me and convinced me of the utility of this
method. Becky Ostertag and Ivelisse Ruiz helped reﬁne hurricane assessment and
contributed to Chapter Five. Martin Quigley provided information on the Honda site,
which he had set up for another project. Sergeant Daniel Martinez helped steer me through
licensing procedures necessary to obtain ammonium nitrate legally (being from the state of
Michigan did not help in this regard). Ochoa provided fertilizer gratis. Augusto Carvajal
harvested root in growth cores. Nina Consolatti dove in at a critical time to help with the
root in-growth core analysis. Pete Hinson, Irma Hinson, and Chao Martinez provide safe
harbor and support during the hurricane. Special thanks to Christa Jen, who helped in the
lab for three years and cheerfully sorted leaf litter to species. Amy Vance, Christa Jen,
Jonathan Crawford, and Will Keusch also sorted litter, the height of tedium.

Numerous folks have reviewed portions of this research, including Richard Thomas,
Clint Springer, Gera jochum,]ohn Genet, Kristen Genet, Phil Sollins, Pamela Hall, Ian
Ramjohn, and four anonymous reviewers. Murphy Lab denizens and “frequenters”

including Lissa Leege, Kurt Stanley, Ian Ramjohn, Joe Harsh, Erica McConnell, Khara

vi

Greiger, Jason Kilgore, and Bob Hollister have contributed to my sanity, and when
appropriate, to some insanity. Their patience, useful comments, and friendship has been
greatly appreciated.

I have had excellent support from my doctoral committee: G. Philip Robertson,
Frank W. Ewers, and Patrick Webber. I appreciate Dr. Robertson’s willingness to sponsor
my residence at the Kellogg Biological Station, providing me with a second home and lab, as
well as thoughtful insight into nutrient dynamics and geostatistics. Dr. Webber graciously
granted me with leave from TA responsibilities for part of the Fall 1998 semester so that I
could follow up on the effects of Hurricane Georges. Without that time, this dissertation
would be much different. Dr. Ewers’ support for my teaching efforts in Ecology while
serving as Department Chairman of Plant Biology has proven invaluable in helping me to
gain important experience to move on with my career in academics.

One’s advisor inevitably plays a major role in one’s satisfaction with their research
and their motivation and desire to continue a career in science. This inﬂuence can be
positive or negative. Peter G. Murphy, my advisor, has been a ﬁne guide. I appreciate his
candor, his ability to ask to the right questions to guide the research, and the excitement he
shows when discussing research and reviewing results. Pete has the uncanny ability to be
realistic without being discouraging. I hope that I can follow his example in my future
interactions with graduate advisees.

Finally, to my wife and fellow Ph.D., Stefanie Whitmire, thanks for your patience,
support, and volunteering to go to Puerto Rico with me on a lark. Of all the discoveries I

have made while in graduate school, you are the best.

vii

TABLE OF CONTENTS

LIST OF TABLES .................................................................................... x
LIST OF FIGURES ................................................................................. xiii
CHAPTER 1. INTRODUCTION TO THE DISSERTATION ............................... 1
A brief history of research in Guanica Forest ............................................. 2
Motivation for this research .................................................................. 4
Lay—out of this dissertation .................................................................. 6
Site descriptions .............................................................................. 7

CHAPTER 2. DYNAMICS OF FOREST STRUCTURE AND NUTRIENT POOLS IN
MATURE SUBTROPICAL DRY FOREST: A LONG-TERM REASSESSMENT OF

GUANICA FOREST (1981-1999) ................................................................. 13
Methods ...................................................................................... 1 5
Results ........................................................................................ 17
Discussion .................................................................................... 20

CHAPTER 3. HETEROGENEITY OF SOIL NUTRIENTS IN SUBTROPICAL DRY

FOREST .............................................................................................. 36
Methods ....................................................................................... 40
Results ........................................................................................ 45
Discussion .................................................................................... 49
Conclusions .................................................................................. 56

CHAPTER 4. TREE GROWTH PATTERNS IN THE TROPICAL DRY FOREST OF

GUANICA, PUERTO RICO: INFLUENCE OF NUTRIENT POOLS ................... 77
Methods ...................................................................................... 80
Results ....................................................................................... 84
Discussion ................................................................................... 86
Conclusions ................................................................................. 89

CHAPTER 5. THE INFLUENCE OF HURRICANE WINDS ON CARIBBEAN DRY

FOREST STRUCTURE AND NUTRIENT POOLS .......................................... 94
Introduction ................................................................................. 95
Materials and Methods ..................................................................... 97
Results ....................................................................................... 104
Discussion ................................................................................. .1 08

CHAPTER 6. SUBTROPICAL DRY FOREST TREES WITH NO APPARENT

DAMAGE SPROUT FOLLOWING A HURRICANE ....................................... 128
Introduction ................................................................................ 130
Methods .................................................................................... 131
Results ....................................................................................... 1 32

viii

Discussion .................................................................................. 1 33

Conclusions ................................................................................. 1 34
CHAPTER 7. OVERALL CONCLUSIONS ................................................... 138
Nutrient Effects ........................................................................... 139
Hurricane Effects .......................................................................... 141
Long-term Growth Patterns .............................................................. 142
Future Research ........................................................................... 143
APPENDICES
1. Full site descriptions ................................................................... 145
2. Properties of soil nutrients not discussed in Chapter Three ........................ 150
3. Literature Cited ......................................................................... 152

LIST OF TABLES

Table 1-1. Characteristics of the three sites used for the majority of research reported in this
dissertation ............................................................................................ 10

Table 2-1. Importance values (IV) of species with dbh 22.5 cm in the main site in 1981,
adapted from Murphy & Lugo (1986b). I.V. is the sum of relative frequency (RF), relative
density (RD), and relative dominance (RBA; basal area) ......................................... 26

Table 2-2. Comparison of structural features of Guanica Forest from 1981 to 1999 using
trees with minimum dbh of 2.5 cm ................................................................. 27

Table 2—3. Importance values for stems 22.5 cm in Guanica Forest in 1999. See Table 2-1
for abbreviations. .................................................................................... 28

Table 2-4. Comparison of soil chemistry in the Main site from 1981-83 and 1999 ........... 29

Table 2-5. Comparison of soil nutrient content and pH from various dry forests. Ranges
reported below reﬂect values from multiple sites in a study ..................................... 30

Table 3-1. Sampling points, lag classes, and intervals used for geostatistical analysis of soil
data. Horizontal precision is the measurement error for X'Y locations measured by the GPS
unit. .................................................................................................... 58

Table 3-2. Means of elevation (m above sea level) and soil properties of four sites in
Guanica Forest. Means across sites were different unless indicated with the same letter.
ND: Not determined ................................................................................ 59

Table 3-3. Parameters for variogram models of soil nutrient concentrations. PSV is the
proportion of structural variance (C / (C+ Co)) where C is structure and Co is nugget variance.
......................................................................................................... 60

Table 3-4. Parameters for variogram models for litter depth, pH, elevation, and nutrient
ratios. PSV is the proportion of structural variance (C / (C+ Co)) ............................... 61

Table 3-5. Pearson correlation coefﬁcients among soil nutrients and between soil nutrient
concentrations and elevation, litter depth, and acidity at the Main and satellite sites in
Guanica Forest. Elevation was not correlated with either pH or litter depth at any site.
Litter depth and pH were weakly correlated at the Main site (r = -0.35, p < 0.0005). . . . . 62

Table 4-1. Correlation between sprout development and soil nutrient pools or nutrient pool
ratios for ﬁve commonly sprouting species. No correlations were found between nutrient
pools and other common species (see Chapter 2 for species composition) or between these
ﬁve species and other nutrients, pH, or organic matter .......................................... 90

Table 4-2: Results of AN OVA for root growth. Root length was normally distributed. . 91

Table 5-1. Description of sites in SW Puerto Rico used to assess hurricane effects. All sites
except the fragments were in Guanica Forest ................................................... 115

Table 5-2. Hurricane effects on representative tree species in Guanica Forest. Defoliation
was assessed in native-south forests and mahogany plantations within two weeks for species
with 225 total trees. Median defoliation rate was 50%. Damage was assessed in all forest
types for species with 225 total stems. Average damage rate was 12.4%. Designation of
species as evergreen, deciduous, and pioneer from Little and Wadsworth (1964), Little at al.
(1974), and Molina Colon (1998) .................................................................. 116

Table 5-3. Biomass and nutrient content of litterfall and standing litter in the 1.44~ha native-
south forest plot. Mass values of standing litter are expressed as means (standard errors) and
are corrected for ash-free dry mass ............................................................... 117

Table 5-4. Hurricane-related mortality of trees and stems 22.5 cm DBH in four types of
forest in Guanica Forest 9 mo after Hurricane Georges ........................................ 118

Table 5-5. Percent stem mortality by size class for height and DBH for all stems in native-
north, native-south, ridgetop, and Leucaena plots. Mortality was not assessed in mahogany
plantations ............................................................................................ 1 19

Table 5-6. Comparison of mortality and structural damage caused by hurricanes in various
tropical forests ...................................................................................... 120

Table 6-1. Sprouting in Guanica Forest, Puerto Rico. Pre-hurricane sprouts were counted
on 451 stems. Post-hurricane sprouts were counted on 1407 stems pooled from ﬁve plots.
Only sprouts developing below breast height (1.4 m) were counted. A sprout was deﬁned as
any woody twig with an orientation greater than 45° relative to the ground. Post hurricane
sprouts compared against pre-hurricane sprouts using 2 or t tests as appropriate ........... 133

Table 6-2: Percentage of post-hurricane sprouts arising from trunks or roots. Sample size is
number of stems sprouting ........................................................................ 133

Table 6-3: Species effects in proportion of stems sprouting, sprout rates and sprout length
for species with at least 10 individuals sampled. All sprouts are post-hurricane. Some

individual trees were multi-stemmed, but only one stem per tree was sampled for sprouts.
........................................................................................................ 134

Table A-1. Importance values for stems 22.5 cm at the Main site in Guanica Forest in 1999.
I.V. is the sum of relative frequency (RF), relative density (RD), and relative dominance
(RBA; basal area) ................................................................................... 147

Table A-2. Importance values for plant species having dbh 22.5 cm in nine 10 x 10 m
blocks in the Lluberas site in 1998. See Table A-1 for abbreviations .......................... 148

xi

Table A-3. Importance values for plant species having dbh 22.5 cm in nine 10 x 10 m
blocks in the Ventana site in 1998. See Table A-1 for abbreviations ......................... 149

Table A-4. Means of elevation (m above sea level) and soil properties of four sites in
Guénica Forest. Means across sites were different unless indicated with the same letter.
Samples were analyzed as described in Chapter Three. Subscripts av and to refer to available
and total forms of elements. All concentrations are in mg/ g unless speciﬁed ............... 150

Table A-5. Parameters for variogram models of soil C, available Ca, available K, and total K.
Spatial analyses were performed as described in Chapter Three ............................... 151

xii

LIST OF FIGURES

Figure 1-1. Map of Guanica Forest showing study site locations ............................... 11

Figure 1-2. Topography of the Main and satellite study sites. Contour lines are 2 m intervals
above sea level (m.a.s.l.) as labeled around maps. Boxes on Lluberas and Ventana sites
indicate 30 x 30 m plots where soil sampling occurred ........................................... 12

Figure 2-1. Map of Main site in Guanica Forest. Areas that are not designated Draw or Flat
are rocky slopes ....................................................................................... 31

Figure 2-2. Mortality and in-growth of stems 22.5 cm in the Main site of Guanica Forest
from 1981 to 1999 .................................................................................... 32

Figure 2-3. Mortality and in-growth as basal area (top) and stem density (bottom) of stems
22.5 cm by species in the Main site of Guanica Forest from 1981 to 1999 .................... 33

Figure 24. Average change in height and basal area (top) and average percent change

(bottom) by species for stems 22.5 cm dbh that carried over from 1981 to 1999 in the Main
site in Guanica Forest ............................................................................... 34

Figure 2-5. Leaf and wood litter production from thirty 0.35-m2 litter baskets in Guanica
Forest. Daily rates are from the previous collection period. Traps were placed on August
20, 1998. Black bars are average leaf-litter-fall values for the time period between
collections, based on 3 years of monthly sampling from 1981-83 (Murphy et a1. 1995).
Hurricane Georges occurred one day after the initial sample was taken. Hurricane litter
production was not included in the data for the second collection period ..................... 35

Figure 3-1. Elevation maps of experimental sites in Guanica Forest, Puerto Rico. Contour
bands are at 2 m intervals ........................................................................... 63

Figure 3-2. Soil sampling and mapping locations in Guanica Forest: (A) Main site, (B) at the
base of trees in the Main site and (C) general scheme for satellite sites using Lluberas as an
example. The higher density of soil samples along six transects in the main site reﬂect
locations of trees measured for growth and phenology for the last 4-20 years ................ 64

Figure 3-3. A) A generalized semivariogram, showing nugget variance. The sill is the total
amount of variability within the sample. Structure is the amount of variability explained by
spatial autocorrelation. Random variability, sampling or measurement error, and variability
attributable to spatial scales smaller than the smallest lag interval make up nugget variance.
The range is the distance where the values measured at two points are completely
independent — the distance where spatial structure ceases. When no spatial structure is
present, the nugget equals the sill. As the distance between sampling points increases,
structure decreases. B) Nested structure in spatial autocorrelation caused by three
hypothetical inﬂuences operating at different spatial scales ...................................... 65

xiii

Figure 3-4. Variograms for soil nutrient concentrations at the Main site. Dotted lines are
sample variance (sz). Parameters for each model are listed in Table 3-3. Left panel in each
case is at 150 m interval, right panel is 32 m interval ............................................. 66

Figure 3-5. Isopleths of soil chemical properties at the Main site derived by 2x2 m block
kriging. The site measures 120 m on each side. Table with legend gives levels for each color
band ................................................................................................... 69

Figure 3-6. Isopleths of soil chemical properties at the Lluberas site derived by 2x2 m block
kriging. The site measures 30 m on each side. Table with legend gives levels for each color
band ................................................................................................... 71

Figure 3-7. Isopleths of soil chemical properties at the Ventana site derived by 2x2 m block
kriging. The site measures 30 m on each side. Table with legend gives levels for each color
band ................................................................................................... 73

Figure 3- 8. Isopleths of soil chemical properties at the Honda site derived by 2x2 m block
kriging. The site measures 25 m on each side. Table with legend gives levels for each color
band .................................................................................................... 75

Figure 4-1. Occurrence of tree species along gradients of soil nutrient pools and pH. Box
plots immediately above axes (in grey) represent distributions of the entire gradient for a
given nutrient or pH from soil samples at the Main site (n = 623). Box plots in black
represent soil nutrient values for samples taken beneath the 6 most numerous species in the
sample (n = 37 to 72). Boxes are the middle 50% of values, whiskers (lines) extending from
the boxes include z 90% of the data, and lines dividing boxes are sample medians. Barrera,
Examine, and Pictetia are pioneer species. Differences in species dist'dbutions across a
gradient are signiﬁed using the rame letter. ........................................................ 92

Figure 4-2. Box plots of treatment means for root length from in-growth cores. Dots
represent individual cores. Nitrogen increased root length (F =18.199, p<0.0005, see Table
4—2) and there was a signiﬁcant interaction with P (F = 5.241, p=0.027). Treatments with the
ram letters are signiﬁcantly different based on post-hoe Tukey tests for multiple
comparisons. Although phosphorus cores had two groups of similar values, neither group
was concentrated along a particular transect ...................................................... 93

Figure 5-1. Hurricane tracks with year of occurrence of the 15 storms most likely to have
affected Guanica Forest. Hurricane Georges is the thickest line across the center. Bolded
years are hurricanes likely to have had the strongest effects on Guanica Forest. Solid lines
are known hurricane tracks. Dashed lines are best-estimate trajectories based on Salivia
(1972), Neuman at a]. (1993), and Miner-Sola (1996). Hortense was a low-level storm that,
according to local reports, had little impact on the forest. Luquillo Forest and Hurricane
Hugo included for reference ...................................................................... 121

xiv

Figure 5-2. Locations of study plots in Guanica Forest and nearby fragments (inset) in
southwestern Puerto Rico. Forest types indicated by symbols in legend. Numbers next to
symbols denote multiple plots of a type in the area ............................................. 122

Figure 5-3. Hurricane effects on stems for different forest types within Guénica Forest,
Puerto Rico. Structural damage includes uprooting, snapping, breakage of large branches, or
leaning. “Undetermined” refers to stems that lacked structural damage but were sampled
after signiﬁcant refoliation had occurred. Most of the stems in this category probably had
been defoliated. Numbers below forest type labels indicate the total number of stems
sampled in each forest type. “All forests” is pooled data for the ﬁve forest types .......... 123

Figure 5-4. Stem density of various modes of structural damage in different stands of Puerto
Rican dry forest. Sample included all stems 22.5 cm DBH. Numbers below forest type
labels indicate total stem density of each forest type. *Branch loss not estimated for native-
north or Leucaena sites, structural damage densities are therefore underestimated ......... 124

Figure 5-5. (A) Proportion of structural damage incurred by stems within diameter classes
for three forest types in Guanica Forest. Broken branches not assessed in native-north or
Leucaena forests. (B) Stems incurring various modes of structural damage as a proportion
of all stems in each diameter or height class. Data included stems only from native-south,
mahogany, and ridgetop sites because broken branches were not assessed for native-north or
Leucaena forest ..................................................................................... 125

Figure 5-6. Stem-fall directions of snapped, uprooted, and leaning stems in Guanica Forest
and nearby forest fragments. Totals are pooled from both Guanica Forest and the
fragments. Strongest winds from Hurricane Georges came from the southeast. The radial
scale is number of stems. The direction of fall was measured for 259 fallen stems in total;
119 from Guanica Forest and 140 from fragments ............................................. 126

Figure 5-7. The relationship between sprouting and structural damage to stems in Guanica
Forest as a result of hurricane winds. Structural damage includes uprooting, snapped stems,
breakage of large branches, and leaning. Only living tagged stems were surveyed for
sprouting. Each point represents a site. All sites are located in mature native-south (S) or
ridgetop (R) forests. Note that in all sites, the percentage of stems with new sprouts exceeds
the percentage of stems with structural damage reﬂecting sprouting on defoliated and
unaffected stems. Sprouting rates and structural damage rates are correlated (r = 0.94; P =
0.017). Pre-hurricane sprouting rates were 3.5% ................................................ 127

Figure 6-1. Percent of stems in Guanica Forest incurring structural damage and with new
sprouts relative to wind exposure. Sprouting data are from four months after Hurricane
Georges. Structural damage includes snapping, permanent bending, uprooting, or loss of
large branches. Exposure is determined by elevation and slope based on wind speeds and
directions reported after Hurricane Georges (Bennett, 1998), all plots face south. Exposure
1 is most protected at low elevation and a level slope. Exposures 4 8t 5 are at the highest
elevations, 5 has the steepest slope. Both damage and sprouting are greater at higher

exposures (x2 tests: p=0.016, p < 0.00001 respectively) ........................................ 132

XV

Figure 62 Trends in proportion of sprouting stems or sprouting rate with defoliation
severity in Guanica Forest following Hurricane Georges. Bars are one standard error of the
mean. Pre-hurricane sprouting shown in Table 1. Severity of defoliation is not related to
sprouting response. X2 tests: p=0.60 for percent of stems sprouting; p=0.92 for sprouts per
stem .................................................................................................. 1 33

Figure 6-3. The median length of the longest sprouts on stems in 16 species of dry forest
trees is related to the number of stems of each tree. (p=0.012) Median sprout length is
similarly related to the percent of multi-stemmed trees (p=0.018) The data are from species
with at least 20 trees in our plots. Each point represents a tree species ...................... 134

xvi

CHAPTER ONE

INTRODUCTION TO THE DISSERTATION

If tropical forests were human societies, dry forests would be the proletariat —
overlooked despite being widespread and exploited with little return. Dry forests cover the
most land area (42%) of any tropical forest type (Murphy and Lugo 1986a) and are found in
nearly every tropical country (Bullock et al. 1995, Van Bloem et al. 2004). Dry forests have
been extensively cleared for agriculture and human settlements because their soils are less
leached than in wet zones and the climate provides seasonal respite from humidity, pests,
and disease. As a result, only about 5% of dry forests worldwide are protected in parks and
reserves (Van Bloem et al. 2004). While tropical rainforests have experienced rapid and
recent expansions of human disturbance (N epstad et al. 2002), human conversion of dry
forests has a much longer history that may have caused these forests to be under-appreciated
by the research community. For example, since 1970, only approximately 30% of scientiﬁc
journal articles on tropical forests have focused on dry forests, with the balance discussing
moist, wet, or rain forests (metadata analysis by Skip Van Bloem using Science Citation
Index ®).

Across their geographical distribution, mature dry forests show a large range in
structure and function. Stem density (minimum 2.5 cm diameter at breast height, this criteria
is used throughout the dissertation) varies from about 650 to 12000 stems / ha, height ranges
from 8 to 30 m, and basal area from 18 to 49 m2/ ha (Murphy and Lugo 1990, Van Bloem et
al. 2004). Tree growth in diameter averages from 0.3 to 4.7 m/ y (Dunphy et al. in prep).

Annual litter production varies from 1.5 to 12.6 Mg ha"yr" (Martinez-Yrizar 1995), while

nutrient use efﬁciency varies about two-fold for nitrogen (44-97 g/ g) and six-fold for
phosphorus (926-6056 g/ g; Van Bloem et al. 2004). Among dry forests, those in the West
Indies tend to exhibit the most extreme characteristics, with the greatest stem density
(>10,000 stems/ ha) and P-use efﬁciency (up to 6000 g/ g), and the lowest basal area (17.8
mz/ ha), height (9 m), and tree growth rate (3 mm/ yr) (Lugo and Murphy 1986, Murphy and
Lugo 1986b, Dunphy et al. in prep). These characteristics lead to a unique forest
physiognomy with a short, shrubby growth form, many (>40%) multiple-stemrned trees, and
an even forest canopy without emergent trees. Despite the unusual physiognomy, the
climate of Caribbean dry forests is not extreme in comparison to other dry forest areas
(Murphy and Lugo 1986a). For example, the climate of Guanica Forest, Puerto Rico, which
is considered among the best preserved tracts of Caribbean dry forest (Ewel and Whitmore
1973), consists of average annual rainfall of 860 mm, 25.1°C mean annual temperature, and
temperature to precipitation ratio of 2.9. These values all fall near or slightly above median
values for dry forests worldwide (Murphy and Lugo 1986a, Van Bloem et al. 2004). Thus,
although Caribbean dry forests are among the densest, shortest, and have the most multi—
stemmed trees, they are not the driest or hottest, suggesting that other factors interact with
climate to generate the physiognomy of the region. Broadly, the overall objective of this
dissertation is to identify factors and mechanisms which lead to the unique structure of West

Indian dry forest, using dry forests of Puerto Rico as a representative example.

A BRIEF HISTORY OF RESEARCH IN GUANICA FOREST
An explanation for the unique structure of West Indian dry forests has been elusive.
A single, overriding factor is unlikely to exist as the forests must respond to various climatic,

biological, and human stresses. Fortunately, a long record of research in permanent plots in

Guanica Forest, Puerto Rico, has helped to identify and evaluate possible explanations. This
dissertation adds to previous research efforts in Guanica Forest in an attempt to further our
understanding of the uniqueness of West Indian dry forests and the structure and function
of dry forests in general.

Guanica Forest was originally protected by the US government in 1917 with major
additions of land area occurring in the late 19303 and from 2000-2004. The forest now
includes over 4500 ha. Initial descriptions of plant communities and succession were made
in the 19205 by Gleason and Cook (1927). Experiments determining the suitability of
mahogany plantations in the forest and early analysis of hurricane effects on forest structure
were performed from 1940-1957 (Wadsworth 1950, Wadsworth and Englerth 1959). Early
succession from an experimental clearcut established in 1969 was described by Ewel (1971)
and reassessed by Dunevitz (Dunevitz 1985). The abandonment of a small village within the
forest boundaries in the 19305 provided the opportunity to evaluate 60-yr patterns of
succession and the effects of land use (Molina Colén 1998). Studies describing
physiological, functional, and structural characteristics of the forest in detail have been
completed since 1978 (Lugo et al. 1978, Lugo and Murphy 1986, Murphy and Lugo 1986b,
Cintron and Lugo 1990, Medina and Cuevas 1990, Murphy and Lugo 1990, Famsworth
1993, Murphy et al. 1995, Quigley and Platt 2003). Many of these studies were conducted in
a 1.44 ha permanent site established by Peter G. Murphy and Ariel E. Lugo in 1981 (Murphy
and Lugo 1986b). These studies documented the unique structural and functional
characteristics of Guénica Forest highlighted above and suggested potential explanations for

these characteristics.

MOTIVATION FOR THIS RESEARCH

This dissertation addresses two potential explanations for the unique structure of
Caribbean dry forest: nutrient limitation and disturbance. However, it should be noted at
the outset that all dry forest dynamics occur within the context of seasonal drought and
unpredictable rainfall patterns. Annual rainfall limits productivity, however, rainfall appears
to be sufﬁcient during the growing season because dry forest productivity at that time
approaches that of rainforests (Murphy and Lugo 1986a). Tree growth and the phenology of
most tree species are tied to seasonal rains (Murphy et al. 1995). Severe drought during the
rainy season can lead to the death of terminal buds which could result in multiple stemmed
trees if they were to resprout from the base. However, within Guénica Forest, only one
species, Gymnant/m lucida, appears to incur top-kill and when this occurs the tree usually
resprouts above 1 m height (personal observations and Dunphy 1996). Therefore it appears
that water limitation does not explain the multi-stemmed growth form and, at least during
the rainy season, other conditions inﬂuence forest structure.

Previous research has identiﬁed important nutrient characteristics of Guanica Forest
that could inﬂuence its structure. Total soil P is relatively high (1820 kg/ ha) but only 1.3% is
bioavailable (Lugo and Murphy 1986). Leaf N:P ratios are high (21-38, Medina and Cuevas
1990) and phosphorus use efﬁciency (>6000) is the highest reported from the tropics
(V itousek 1984). The calcareous soil has a mean pH of 7.8, a level at which phosphorus
binds to calcium (Lugo and Murphy 1986). Leaves have a tendency to be sclerophyllous
(Murphy and Lugo 1995), which can be a sign of P limitation (Medina et al. 1990). Together,
these characteristics suggest potential nutrient limitation of forest productivity and structure,
primarily by P, although the short supply of P could be the result of insufﬁcient soil

moisture for P transport (Murphy et al. 1995). The possibility of P limitation motivated

some of the nutrient research within this dissertation, but another compelling reason was the
opportunity to compare 18 years of on-going tree-growth measurements to soil nutrient
pools in the permanent plot (Murphy et al. 1995, Dunphy et al. in prep).

Another key factor that may explain mature Caribbean dry forest structure is
disturbance — two types of which commonly occur. The ﬁrst is anthropogenic — primarily
cutting or clearing by humans. Until the 19305, some areas within Guanica Forest were
cleared for agriculture and housing while other areas were selectively cut for ﬁrewood and
small-scale charcoal production (Lugo et al. 1996, Molina Colon 1998). Regrowth on cleared
forest lands resulted in forests with lower stem density, more single-stemmed trees, and a
species assemblage dominated by exotics (Molina Colon 1998). Conversely, high stem
density and coppice clumps were common in former charcoal sites (Molina Colon 1998),
which makes cutting a reasonable explanation for Caribbean forest structure. However, it
now appears that a natural mechanism must exist which generates the Caribbean forest
structure because other studies have shown that stumps of main stems were absent on multi-
stemmed trees and that multi-stemmed trees were present in size classes that were too small
to have existed during fuel-wood harvests (Dunphy et al. 2000).

Hurricanes are another major disturbance type endemic to the Caribbean. They
strike Puerto Rico about once every nine or ten years (Weaver 1999), but the last major
hurricane to cross over Guénica Forest was in 1928 (Miner-Sola 1996). By luck rather than
by design, I arrived in Puerto Rico ﬁve days before Hurricane Georges in September, 1998,
and therefore was able to assess the effects of this “natural experiment” on the structure of

Caribbean dry forest.

LAY-OUT OF THE DISSERTATION

The dissertation contains ﬁve main chapters (2-6), each on a different aspect of the
relationship of forest growth and structure to soil nutrient content or hurricane disturbance.
Chapter Two evaluates structural changes in the permanent site (the Main site) 18 years after
it was established. As I discuss in the chapter, long term reassessments of permanent sites —
even if only 18 years - are rather uncommon in the dry tropics. Understanding change
provides a good context by which to address the role of nutrients and hurricanes in shaping
forest structure. Speciﬁc objectives of this chapter are to: 1) reassess forest structure,
species composition, soil nutrient pools, and litter fall; 2) assess mortality and in-growth
(recruitnrent into the minimum diameter class considered: 2.5 cm) during the 18-year period;
3) provide a baseline of natural variability in order to evaluate the effects of episodic
disturbance by hurricanes; and 4) describe dynamics of mature Caribbean dry forest to
improve our ability to compare against patterns from dry forests in other locations.

Chapters Three and Four address nutrient limitation in Guanica Forest. Chapter
Three provides extensive analysis of the quantity and distribution of soil nutrient pools
focusing on N, P, and Ca. Supplemental information for Chapter Three can be found in the
Appendix. The primary objective of this chapter is to describe spatial patterns of soil
nutrients and pH within and among four sites in Puerto Rican dry forest. Emphasis is given
to relationships between phosphorus and calcium, topography and nutrient contents, and
correspondence of nutrient patch size to tree crown diameter. Chapter Four compares
patterns of tree growth and distribution to soil nutrient content. The objectives of this
chapter are to: 1) determine whether common species in Guanica Forest were limited to

certain positions along gradients in soil fertility; 2) to determine if and which soil nutrients

limited growth; and 3) to evaluate whether N or P plays a greater role in nutrient limitation
on forest growth.

Evaluation of hurricane effects on dry forest structure is covered in Chapters Five
and Six. Chapter Five describes the immediate effects of a hurricane — damage, mortality,
and defoliation. The main objectives of this chapter are to: 1) provide a detailed
description of hun'icane effects on Puerto Rican dry forest; 2) compare effects of
hunicane winds in large tracts of forest with those in nearby forest fragments; 3) measure
short-tenn responses of trees to hurricane winds in terms of mortality; and 4) assess the
potential of hurricanes to maintain the unique forest structure of the West Indies. In
addition to the data I collected in mature, south-facing forest for Chapter Five, Dr. Sandra
Molina Colon and Ivelisse Ruiz Benard contributed data for forest plots with different
aspects and land use histories. This chapter has been accepted by Biotmpica. Chapter Six
assesses the response of the forest by sprouting and the ﬁrst two years of sprout growth
following the hurricane. This chapter has already been published in Tmpz'cal Ecology (Van
Bloem et al. 2003). The objectives of this chapter are to evaluate three predicted outcomes
of hurricane disturbance: 1) sprouting frequency would be higher on damaged stems; 2)
sprouting would be proportional to defoliation because sprouting response might be related
to biomass loss; and 3) a majority of sprouts produced after Hurricane Georges would die
after the ﬁrst or second dry season due to thinning of new sprouts as they competed for

resources.

SITE DESCRIPTIONS
The majority of the research presented here was performed in three sites in Guanica

Forest (Figure 1-1). The Main site was the 1.44-ha permanent plot established in 1981

(Murphy and Lugo 1986b). Two 1-ha “satellite” sites were established inJune, 1998:
Lluberas and Ventana. Each site was >2 km from the others (Figure 1-1). Structural
characteristics of the forest were measured in these sites and soils were sampled for spatial
analysis in portions of each sites. In addition to the Main site and satellite sites, some
additional sites were included to assess hurricane effects. These are described in Chapter
Five. Also, one 25 x 25 m site (Honda) was established in 1992 for a study of plant species
diversity along a latitudinal gradient of seasonal forests (Quigley and Platt 2003). I used this
site as part of the analysis of spatial patterns of soil nutrients. It is described in Chapter
Three. Some of the information here is repeated as needed for the context of each data
chapter. Complete details of each site can be found in Appendix 1.

The Main and satellite sites were all located in mature, semi-deciduous forest (as in
Lugo et al. 1978) consisting of native tree species. For stems 2 2.5 cm diam&er at breast
height (the minimum size class used for all analyses in this dissertation), 32-37 tree species
were present at each site, basal area ranged from 17.9-21.3 mz/ ha and stem density from
6,400 to 10,400 stems/ ha (Table 1-1). Human disturbance at each site has been minimal for
the last 70 years as veriﬁed by analysis of aerial photos taken since the 19305 (Lugo et al.
1996). The topography was hilly with rocky outcrops and soils derived from limestone
(calciustols). Where outcropping was prevalent, soil was only found at the surface in
crevices between rocks and plants rooted in loosely consolidated humus layers. The sites
were located between 23 and 150 m above sea level and elevation within each site varied
from 10-20 m (Figure 1-2).

Multiple sites were used for most analyses to ensure that patterns were consistent

across the forest and that results previously reported from the Main site were representative

of the forest in general. In addition, multiple sites provided better opportunity to study

spatial patterns of nutrient distribution and hurricane disturbance.

Table 1-1. Characteristics of the three sites used for the majority of research reported in this
dissertation.

 

Main Lluberas Ventana
Size (ha) {.44 1.0 1.0
Sampled area (m2) 690-1500 900 900
Mean elevation (m.a.s.l.) 129 147 25
Range of elevation (m) 20 9 14
Number of tree species* 37 33 32
Basal area (mz/ha)* 19.1 21.3 17.9
Stem density (ha")* 10,400 9,200 6,400
Previous land use** Mature Mature Mature

*minimum 2.5 cm diameter at breast height
**minor selective cutting prior to 1940 for ﬁrewood or charcoal production noted

10

Figure 1-1. Map of Guénica Forest showing study site locations.

Southwestern Puerto Rico 66°50’W
l

 

     
 
      
   
   
 
   
 
   
  

 

 

 

. YaUCO _ 18°N
M = Main
aribbean Sea L = Lluberas
W 17057, (V V = Ventana

H = Honda

North M

H
Guanica Forest (Eastern Portion)

  

Private
Land

1 km Caribbean Sea 66050,“,

11

Figure 1-2. Topography of the Main and satellite study sites. Contour lines are 2 m intervals
above sea level (m.a.s.l.) as labeled around maps. Boxes on Lluberas and Ventana sites
indicate 30 x 30 in plots where soil sampling occurred.

Main Site

Magnetic
Nonh

True North

“tritium

Hill in: "IIl

 

 

 

 

Lluberas Site Ventana Site

 

 

 

 

 

V 100 Ill >

CHAPTER TWO

DYNAMICS OF FOREST STRUCTURE AND NUTRIENT POOLS IN MATURE
SUBTROPICAL DRY FOREST: A LONG-TERM REASSESSMENT OF

GUANICA FOREST (1981-1999)

Succession theory suggests that a forest community will reach a dynamic equilibrium
or steady state at maturity. Mature forests would be expected to maintain stable size class
distributions, stem density, basal area, a balance between recruitment and mortality, and a
tree community without pioneers except in canopy gaps (Richards 1996). The time required
for a forest to regain mature status from a disturbance is typically greater than the time
available for most research projects and grants (3-5 y). Consequently, evaluation of maturity
and forest dynamics of mature forests is frequently achieved through modeling or the use of
forest plots along a chronosequence of successional age instead of long term monitoring.
Modeling and chronosequences have provided valuable evidence to shape ecological theory,
but are unable to directly evaluate dynamics of forest structure in mature systems. In
contrast, long-term permanent sampling plots allow for direct assessment of mature forests,
clarify whether short-term patterns are trends or ﬂuctuations (Sheil 1995), increase the
possibility that forest response to infrequent events can be studied (e.g. Crow 1980, Waide et
al. 1998, Burslem et al. 2000), and highlight information gaps or mistaken predictions from
theory (e.g. Sheil et al. 2000).

Long term (215 y) assessment of tropical forest dynamics in permanent plots has

largely conﬁrmed the predictions of succession theory (reviewed by Swaine et al. 1987, and

augmented by Burslem, et al. 2000, Taylor et al. 1996, Lwanga et al. 2000, Sheil et al. 2000,

13

Fashing et al. 2004). These studies have all taken place in moist-to-rain forest, including sites
in Puerto Rico (Crow 1980, Waide et al. 1998). Stands tend to be self-maintaining with
annual mortality of 1-2%. In Malaysia, trees that maintained positive growth rates from year
to year had lower mortality rates than those with negative growth rates or no growth increase
over a period of years (Manokaran and Kochummen 1987), a pattern recently documented
in Puerto Rican dry forest (Dunphy et al. in prep). Long term recruitment (or in-growth)
into minimum size classes balanced mortality in most sites, but this balance was often not
present within short periods (S 8 y) for studies where multiple enumerations of forest
populations occurred (Taylor et al. 1996, Burslem et al. 2000, Sheil et al. 2000). Distribution
of stems in size classes remained steady over time, as did basal area. A few studies have also
included long term measurements in plots which began in earlier successional stages due to
prior logging or clearing (Okali and Olaadams 1987, Richards 1996, Sheil et al. 2000, Fashing
et al. 2004). Even after 40 years, disturbed forests had yet to return to a mature forest
species composition, basal area or stem density.

In addition to attaining steady state in stand dynamics, mature forests may be
expected to have relatively constant nutrient pools over time (Sprugel 1985). Studies of long
term soil dynamics suggest that forest fallows, after clearing and burning, require at least 15-
30 years to rebuild soil nutrient pools (Maass 1995), while organic matter may take up to 60 y
to return to pre-disturbance levels (Aber and Melillo 1991). In dry forests of Puerto Rico,
soil nutrients in cleared sites had not returned to mature forest levels after 45 y, however soil
nutrients in selectively cut sites had recovered (Molina Colon 1998). The dry forest
environment responds quickly to highly variable rainfall (Lugo et al. 1978), so year-to-year

variability in litter fall, standing litter, productivity, and diameter growth can be high (Lugo

14

and Murphy 1986, Murphy and Lugo 1986b, Cintron and Lugo 1990, Murphy et al. 1995,
Dunphy et al. in prep), but can only be determined with long-term observations.

The conclusions of previously published long term permanent plot studies have been
successful in verifying many assumptions of mature forest dynamics and highlighting some
surprises (e.g., persistence of pioneer species in forest canopy; Sheil et al. 2000). Dry forests
may approach dynamic equilibrium at a different rate than wetter forests due to a longer
dormant season, lower annual tree growth rates, and lower biomass. The objectives of this
chapter are to: 1) assess forest structure, species composition, soil nutrient pools, and litter
fall after an 18 year period in a long-term permanent dry forest plot, 2) assess mortality and
in-growth during this period, 3) provide a baseline of natural variability in order to evaluate
the effects of infrequent disturbance by hurricanes (which are dealt with in Chapters Five
and Six), and 4) describe dynamics of mature Caribbean dry forest to improve our ability to

compare against patterns from dry forests in other locations.

METHODS
Fomt .rtmctzm

In 1981, a permanent 1.44-ha research site was established in Guénica Forest
(Murphy and Lugo 1986b), a state forest originally established in 1918 and expanded in the
19308. The site was considered to be mature forest but there was some evidence of selective
cutting for charcoal production from before the 19305 (Lugo et al. 1996). Cut areas were
localized, approximately 10-20 m in diameter, and covered less than 15% of the plot. Within
the site, ﬁfteen 10 x 10 m plots were censused in November, 1981 (Figure 2-1). The

diameter, height and species were recorded for all stems 2 5.0 cm diameter at breast height

(dbh). Within the SE quarter of each plot, these same data were recorded for stems 2 2.5

15

cm dbh. These plots were remeasured in the same manner in 1999 and the fate of individual
trees was determined based on precise locations recorded in 1981. Hurricane Georges
passed over the site in September, 1998. Some effects of the hurricane are reported here,
but details of data collection and overall effects are reported in Chapter 5. Original
structural data were reported in Murphy and Lugo (1986) (Table 2-1). Mortality, in-growth,
and changes in basal area, height, stem density, and species composition were determined by
comparing structural data from 1999 with those from 1981. Species were determined using
Little and Wadsworth (1964) and Little et al. (1974).

Because multiple-stemmed trees are the dominant growth form in the forest, data
were generally analyzed using stems instead of trees. When results refer to trees, this
includes single-stemmed individuals and an entire clumps of stems. When discussing

individual trunks, regardless of whether growing singly or clumped, I use “stern.”

Utterﬁll and rail nutrient:

In 1982, litter fall was collected monthly in thirty 50 x 70 cm wire mesh traps (Lugo
and Murphy 1986, Murphy and Lugo 1995). I collected litter fall from these same traps, in
different locations, eight times between August 1998 and August 2000. Litter fall was dried
to a constant weight to determine biomass. Nutrient content of litter fall was not analyzed
because collection intervals were greater than one month, a period during which some labile
nutrients would be lost (Cuevas and Medina 1986).

Soil nutrient content was originally analyzed from composites of 20 subsamples
taken from 0-5 cm depth in ﬁve plots in the main site on seven different dates (n=35) from
1981-1983 (Lugo and Murphy 1986) and from monoliths from four soil pits. In 1999, as

part of a study of spatial patterns in soil nutrient content (see Chapter 3), I collected 623 soil

16

samples from 0-10 cm depth along 6 transects. Total soil nitrogen was analyzed on 100-mg
soil subsamples using dry combustion in a LECO CNS (LECO Corp. St. Joseph, MI)
analyzer. Soil samples were combusted at 1450°C. Organic matter (OM) was measured as
loss on ignition by combusting samples in a mufﬂe furnace at 490°C. At this temperature,
loss on ignition does not include clay-bound water and therefore estimates OM well (Nelson
and Sommers 1996). Total concentrations of other elements (Cato, Km, Pm) were
determined by digesting 100-mg subsamples in nitric acid followed by hydrogen peroxide.
Using 5-g subsamples, available calcium (Caav) was extracted in 1.0 M KCl while available
phosphorus (Pay) and potassium (Kay) were extracted using a modiﬁed Olsen solution
(Wilde et al. 1979). Digested total and available element concentrations were determined
using an atonric-emission spectrometer. Measurement accuracy was maintained for each
analysis by verifying standards after every twenty samples and running duplicates of every

tenth sample. Bulk density was measured using intact cores of 10 cm soil depth.

RESULTS

Changes in structural characteristics of Guanica Forest over the 18-y period were
generally small, despite the occurrence of Hurricane Georges <1 y before the end of the
sampling period (Table 2-2). Three new species were present in the size classes of trees
measured: Colubrina arborvrcem, Eugenia rbombea, and Rgmorz'a andnata. Only E. r/Jombea has
not been recorded in the understory in 1981 (P.G. Murphy, unpublished data) and therefore
was assumed to be entirely new to the site. Elsewhere in Guanica Forest, this species is

common. No species were lost. Basal area of stems 22.5 cm dbh increased 7.3% while

overall stem density increased by <1%. The number of stems 2 5 cm dbh decreased 4.8%,

17

while stems 2.5-4.9 cm dbh increased 1.9%. The number of multiple-stemmed trees
increased by only 1%.

New stems added by in-growth totaled 26% of the stems present in 1981 and
accounted for 3.0 m2/ ha basal area. Annual in-growth rates were 1.4%, 149 stem/ ha, or
0.16 mz/ ha basal area. In—growth was most common in the smallest size classes measured
(2.5-4.0 cm) since larger trees would have been present in 1981 (Figure 2-2). Only 34% of
new stems were in clumps that had existed in 1981. Most new stems were from entirely new
trees, of these, 18% were multiple-stemmed. New stems came from 28 species (Figure 2-3).
Gymnantber lucida and Como/aha minutiae/ya accounted for the greatest inﬂux of stems and
increase in basal area, however, the two largest diameter stems added were 9-cm Pironia
a/bida.

Of the stems present in 1981, 25% died over the 18—y period, accounting for 4.3
m2/ ha of basal area. Thus the annual mortality rate was 1.4%, 144 stems / ha, or 0.24 mz/ ha.
Dead stems spanned all size classes from 2.5-17 cm dbh (Figure 2-2) and included 27 of the
original 34 species (Figure 2-3). Mortality was highest for onrtema caribaeum and Gymnant/Jer
lucida when measured by number of stems or basal area. The seven largest dead stems came
from Pirom'a albida, H ”be/ate tnfo/z'ata, Barrera rimaruba, and the cactus Pi/orocercar mjerrii. Of the
dead stems, 43% belonged to clumps that had living stems in 1999. The remaining dead
stems were primarily single-stemmed individuals — only 7% of dead trees were multiple-
stemmed. Of the species in the 1981 tally, ﬁve had neither mortality nor in-growth. These
species were among the six lowest in importance in 1981 (Table 2-1).

Hurricane Georges removed 9.4% of stems below breast height and 3.3 m2 / ha basal
area present in 1998 (Table 2-2). Subtracting these values from mortality data, mortality

would have accounted for losses of approximately 13% of stems and 1.0 m2/ ha basal area

18

without the hurricane. Including both mortality and in-growth there would have been an
11% increase in stem density and a 26% increase in basal area.

Among stems that carried over from 1981 to 1999, average height increased about 30
cm while average basal area increased 9.1 cm2. Most species showed an increase in both
height and basal area (Figure 2-4), despite the effects of the hurricane. The loss in basal area
for P. myenz'i was primarily due to Hurricane Georges breaking off large branches that arose
below breast height on trunks. Decreased basal area for the one individual of the palm
Tbrinax mania? was probably the result of petiole loss from the trunk resulting in a narrower
stem.

Community structure in terms of importance values changed little overall from 1981
to 1999, although some species’ ranks changed (T able 2-3). Comparing species populations
over time yielded a selection of response patterns. Some species declined, with lower
frequency, density, and basal area, including E. earibaenm, Erit/ra/irfmtieora, P. myenii, and
Canine :g/oearpa. Tboaz'nzaportorieennr stem density and basal area decreased, but frequency
remained the same, a result of clump thinning. Three species increased in basal area while
losing stems, indicating thinning of the population but continued growth of established trees
(Pironia albida, Antirr/Jea amtata and Krugz'odena’mnﬂmmn). Population growth was indicated by
increasing population density and basal area in H Zoe/ate tnfo/z'ata, Pietetz'a acn/eata, and
Izptoemn: quadrieortatnr. Gnettarda e/l'mtr'ea, C oeeo/oba mimrtae/pra, and Bonmvia mem/enta were
increasing both population size and frequency in the site while maintaining basal area. A
ﬁnal group of 20 species maintained their position in the community, keeping relatively
constant frequency, density, and basal area (e. g. Gynant/Jer lucida, Coeeoloba divernﬁ/ia, Barrera

damn/ha, Anya} elemifera, and Guettarda kmgz'z).

19

Total annual litter fall during the 2-y time period was 254 g/m2, of which 220 g/m2
(87%) consisted of leaves and reproductive parts. Non-hurricane leaf litter production
ﬂuctuated around the levels reported by Murphy et al. (1995) (Figure 2—5). Notable
deviations were found in November 1998 when leaf litter fall was twice the 1982 rate, May
1999 when it was reduced by nearly 400%, and February 2000 when it was reduced by about
300%. Wood litter production remained >0.3 g in2 day" from 1998-2000.

Soil nutrient pools in 1999 remained similar to those reported from 1981 (T able 2-4).
Organic matter, available P, and available cations were higher in 1999 while Total P and N

were lower, but none of these differences were statistically signiﬁcant.

DISCUSSION
Forest Structure

When Murphy and Lugo (1986) ﬁrst described the permanent research site in
Guénica Forest, they concluded that it had reached maturity. The results of this
reassessment of forest structure largely support their conclusion. In-growth equaled
mortality — a pattern typical for mature forest (Swaine et al. 1987) - and nutrient pools and
litter production appear to have reached a steady state. The nearly 5% decrease in larger
trees can be explained by Hurricane Georges preferentially removing larger stems (Chapter
Five). Hurricane disturbance appears to stimulate basal sprouting (Chapter Six), but sprouts
would not have had enough time (only 2 years) to grow into the size classes measured here.
Biomass and height were both increasing, despite disturbance by the hurricane, suggesting
that the forest may not yet have come to steady state in terms of biomass.

A notable structural feature of Guénica Forest in 1981 was the high proportion of

multiple-stemmed trees (Murphy and Lugo 1986b). This proportion was unchanged in 1999.

20

The survival of a tree was aided by having multiple stems, as only 7% of multistemmed trees
died. The origin of this growth habit has been a subject of speculation. Dunphy et al.
(2000) concluded that it was a natural occurrence for 7 of 10 common species, based on the
absence of cut trunks, the presence of original, intact stems on 20% of multistemmed trees,
and 23.3% of the smallest sized trees (<3.0 cm diameter at ground level) having multiple
stems. Of the ten species, Cocoa/05a kmgi, Gymnantber Incida, and Pietetz'a amleata had new
multi-stemmed trees in 1999. Dunphy et al. (2000) noted that 61% and 33% of small trees
of the ﬁrst two species were multi-stemmed, but found no small multi-stemmed individuals
for P. aar/eata. Since 1981, 18% of the ingrown trees were multiple stemmed, further
supporting the conclusion that neither cutting nor anthropogenic disturbance were needed
to generate the multi-stemmed growth form. These numbers, however, fall short of
explaining the overall proportion of multi-stemmed trees (43%) and the increasing
proportion of multi-stemmed trees with stem size (Dunphy et al. 2000), suggesting that there
is some mechanism which elicits growth of additional stems without removing the main
stem. In Chapter Six I propose that development of new stems is spurred by gravitational
displacement due to hurricane winds' causing sprouting — a thigmomorphogenetic response.

Guénica Forest contains 12 endemic and 14 endangered or threatened tree species
(Little et al. 1974, Quevedo et al. 1990). Of these, six were found in the main site: Pietetia
acn/eata, Tbonz'nz'a portorieeniir, Eugenia xemp/thz'ea, Rgrnoi‘ia guama, Linoeiem boldridgii, and the
cactus laptoeeren: quadrieortatar. Pietetz'a and Tbonz'nia were common (and remained so) while
only R. gnarna declined in population.

To the north of the main site, Molina Colon (1998) conducted a 5-y study on forest
development 45 years after the cessation of human disturbance. The disturbances included

stands which had been selectively cut and stands cleared for agriculture and housing. A

21

mature forest stand in a north-facing valley was included for comparison. Forest structure,
species composition, and soil nutrient content in the selectively cut sites had recovered to
mature forest levels — unlike the cleared sites. Stem density in Molina Colon’s mature forest
was lower than in my site, about 7000 stems / ha, while selectively cut sites had 7800

stems/ ha due to coppice growth, and the cleared sites 4000-6000 stems / ha. My site faced
south and was more exposed, which led to a shorter canopy and a relative abundance of
species common to drier, exposed areas (e. g. Gymnant/Jer, Pietetia, Canine, Cmrropeta/am)
compared to Molina Colon’s north-facing stands. Basal area (19 m2/ ha) and frequency of
multi-stemmed trees (43%) in Molina Colén’s mature stands matched that found here (Table
2-2). Both values were lower for younger forests (8-13 mz/ ha and 23-38%, respectively).
The results demonstrate that structural features and nutrient pools for mature forest are

largely comparable from place to place.

Utter fall and rail nutrient:

Annual litter fall in 1998-2000 was only 53% of that in 1982, but was 88% of litter
fall measured in another nearby mature forest stand in 1974-76 (Lugo et al. 1978, Cintron
and Lugo 1990). Leaf litter fall rates from 1998-2000 ﬂuctuated around levels measured in
the early 19805 (Lugo and Murphy 1986, Murphy et al. 1995). Some of the ﬂuctuation, at
least for 1998-99, can be explained by Hurricane Georges, which caused about 50%
defoliation (see Chapter 5) on September 21-22, 1998 (Figure 2—5). Following the hurricane,
trees continued to lose some damaged leaves at above-normal rates for about two months,
but subsequent leaf litter fall in the dry season was lower than measured in the 19805. Lower
litter fall rates could be explained by fewer leaves in the canopy because of incomplete

recovery following the hurricane, or lower inputs due to a large new ﬂush of leaves on

22

evergreen species, which typically remain on the trees for 2 1 yr before senescence (Olivares
and Medina 1992, Reich et al. 1992). The low litterfall in February 2000 was probably the
result of an unusually wet January (84 mm) delaying senescence. Leaf litterfall in Guénica
Forest during 1998-2000 was 30% lower than the median value in other dry forests (315
g/m2: Martinez-Yrizar 1995), but 33% higher than in 1982 (Lugo and Murphy 1986).
Constant levels of nutrient pools through time are another indication of forest
maturity. Conversion of dry forest to pasture or agricultural land is frequently accomplished
by clearing followed by burning (Maass 1995). In this process, a signiﬁcant nutrient pulse is
provided to forest soils, but these nutrients are lost rapidly due to leaching and erosion
(Adedeji 1984, Maass 1995). In Mexico and India, nutrient pools in dry forest soils had not
returned to original forest levels 10-15 years after clearing and burning (Maass 1995). Soil
nutrient pools in cleared sites from another study in Guanica Forest were still lower than in
mature sites after 60 years of succession (Molina Colon 1998). Soil chemistry reported here
fell within the range of values from the same site in 1981-83 (Table 2-4). The ratio of N to
Pay was much lower in 1999, a result of both higher Pay and lower N concentrations, but the
1981 value was close to that determined elsewhere in the forest (V entana site; see Chapter
Three). Although N was lower and available nutrients were higher in 1999, the differences
were not statistically signiﬁcant, supporting the conclusion that nutrient pools have remained
stable. The slight differences measured between sampling periods may result from both
methodological or environmental causes. The 1981-83 values were means from samples
taken quarterly over a two-year period while 1999 was sampled in July during the short dry
season, when plants and microbes would be less active and available nutrients would
accumulate in the soil (Davidson et al. 1993, Srivastava 1997, Campo et al. 1998).

Meanwhile, N supplies from through-fall would be lower (Campo et al. 2001). Available

23

nutrients may also have been elevated from the nutrient pulse created by fresh, mature leaves
being blown to the forest ﬂoor by Hurricane Georges in September 1998 (Lodge et al.
1994b). These leaves added relatively more phosphorus and potassium than nitrogen
(Chapter 5), because retranslocation was unable to occur and N is not conserved in Guanica
Forest trees (Lugo and Murphy 1986).

Guénica Forest soils generally were richer in organic matter and nutrients than soils
in other dry forests (Table 2-5). Guénica Forest had the highest amounts of N and organic
matter reported, as well as the most alkaline soils. Only dry forests in Belize had levels of
organic matter which approached those found in Guénica Forest. The high organic matter
in Guénica soils results from the forest having the highest litter turnover time reported (~3
y) for dry forests (median 1.2 y, Marﬁnez-Yrizar 1995) despite an annual aboveground NPP
of less than half that of other dry forests (Murphy and Lugo 1990). The calcareous origin of
Guénica soil resulted in its high pH, however, exchangeable Ca was nearly the lowest
reported. Only Ghanaian dry forests have soil N as high as the lowest values found in
Guénica Forest. Pay levels were equal or somewhat higher than found elsewhere, with the
exception of very P-rich soils in Brazil. CzN ratios were similar for all forests, but C:P and
N:P ratios were higher in Guénica Forest, reﬂecting high C and N concentrations found
there. With average amounts of phosphorus and high amounts of carbon and nitrogen in
the system (Table 2-4), P supplies could limit productivity in the system as suggested by the

high phosphorus use efﬁciency for the forest (V itousek 1984, Lugo and Murphy 1986).

Maturiy inforertr wit/J epirodic disturbance
Stability or dynamic equilibrium in most of the structural and functional traits

measured within the permanent research site indicated the forest had reached maturity.

24

Structurally, ingrowth balanced mortality and population and community structure showed
little change over the 18-y period (Table 2-2). Functionally, soil nutrient pools remained
constant and litter fall, while highly variable, oscillated within the range of previously
reported values. Only basal area and height increased over the 18-y period, despite losses
following Hurricane Georges (Table 2-2). Absent the hurricane, the forest would appear to
be aggrading. However, hurricanes are a regular part of the ecosystem, occurring multiple
times over the lifetime of mature trees, and thus would be expected to cause intermittent
losses. Hurricane Georges followed a 70-year period free of strong hurricanes, greater than
the average return interval of 43 y for Category 3 hurncanes (see Chapter 5). Potential
increases in basal area and stem density would therefore be lower between more frequent
hurricanes. Episodic disturbance by hurricanes may also help maintain individual
occurrences of pioneer species in mature forest. Despite the similarity of characteristics
from 1981 to 1999, the nature of the equilibrium in the forest was clearly dynamic, as
evidenced by a 25% turnover in stems, highly variable amounts of annual litter fall, and
episodic effects of hurricane winds on stem density and basal area.

Compared to mature tropical dry forests in areas less inﬂuenced by large, infrequent
disturbances such as hurricanes, the structure of Guénica Forest is shorter, with less basal
area and more multiple-stemmed trees. Even with this difference in appearance, Guénica
Forest, as a representative of Caribbean dry forest, exhibits many functional characteristics
similar to those found in other mature tropical forests (dry or wet), including: 1) annual
mortality ranging from 1-2%, 2) in-growth equaling mortality, 3) slowly increasing basal area,
4) low species turnover (in Guénica Forest species were maintained by sprouting), and 5)

relatively constant soil nutrient pools.

25

Table 2-1. Importance values (IV) of species with dbh 2 2.5 cm in the main site in 1981,

adapted from Murphy & Lugo (1986b).a I.V. is the sum of relative frequency (RF), relative
density (RD), and relative dominance (RBA; basal area).

 

 

% of

Species IV Total IV RF RD RBA

6123:5918“ lucida ' 43.58 ' 14.53 8.09 21.69 13.80
Exorterna caribeaum 25.38 8.46 8.67 7.59 9.11
T/Jouz'niaportoricenrir 21.10 7.03 4.62 1 1.52 4.96
Pironz'a albida 20.89 6.96 5.20 3.67 12.02
Pictetia aculeata 20.60 6.87 5.20 9.52 5.87
Cocco/oba miavttac/Jjadc lemgz'zb 20.07 6.69 5.78 8.43 5.86
Pilorocereu: rojeniz' 11.84 3.95 2.89 0.90 8.05
Bumra Jimaruba 11.57 3.86 5.20 1.09 5.27
Tabebuz'a betemp/y/la 10.29 3.43 4.05 3.35 2.90
Eritba/irﬁuticora 10.07 3.36 3.47 3.99 2.61
Coccoloba diverrzﬁ/ia 9.55 3.18 4.62 1.35 3.57
Canine egrlocarpa 8.94 2.98 3.47 2.90 2.58
Hype/ate tnfolz'ata 7.78 2.59 2.89 1.35 3.54
ngiodendmnﬁmurn 7.53 2.51 4.05 1.35 2.13
Bourrerz'a .rucculenta 7.48 2.49 4.05 1.74 1.69
Crrmopetalum niacorna 6.60 2.20 2.89 2.12 1.59
jacquinia berten'i 6.30 2.10 2.89 1.29 2.12
Antirbea acutata 6.19 2.06 1.73 2.90 1.56
Guettarda 1217431? 6.19 2.06 2.31 2.64 1.24
Anya} elemzfera 5.63 1.88 2.89 0.97 1.77
Guettarda ellmtz'ca 4.37 1.46 1.16 2.32 0.90
Eritbmagrlurn rotundzfo/r'urn 4.26 1.42 2.31 1.03 0.92
Eugenia foetz'da 3.51 1.17 2.31 0.64 0.55
Forertiera regregata 3.41 1 .14 1 .1 6 1.22 1 .04
Eugenia xemp/grtica 3.04 1.01 1.16 0.71 1.18
Izptocereur quadricortatu: 2. 81 0.94 1.16 0.71 0.94
Comocladia dodonaea 2.70 0.90 1.73 0.64 0.33
Linociera boldrz'dgii 2.33 0.78 0.58 1.03 0.72
Rg'non'aguatna 2.14 0.71 1.16 0.64 0.34
Plumm'a a/ba 1.11 0.37 0.58 0.32 0.21
Tbrinax monitii 1.00 0.33 0.58 0.06 0.36
Zantboaglutnﬂavurn 0.98 0.33 0.58 0.26 0.14
Rocbefortz'a acantbopbora 0.75 0.25 0.58 0.06 0.11

 

a. The ofiginal data were modiﬁed slightly to correct for a few misidentiﬁed trees and an
addition error that had increased the IV for G. ,érugii by 4.23.

b. Most of these stems were Cocco/oba mimrtac/Jja — subtracting C. krugz'i would not change
the order of importance.

26

Table 2-2. Comparison of structural features of Guénica Forest in 1981 and 1999 using
trees with minimum dbh of 2.5 cm.

 

' .' ' a P 1999 pre-Hurricane
Attribute 1981 1999

 

Georges

Tree species richness (0.15 ha) 34 37 37
Basal Area of trees (mz/ ha) 17.8 19.1 22.4
Stem Density: Total (n/ha) 10,360b 10,427 11,509

2.5 _ 5.0 cm dbh 8,347 b 8,507 9,359

2 5.0 cm dbh 2,013b 1,920 2,150
Multiple stemmed trees (%) 43 b 42 42
Average height (m) 4.2 4.5
Mortality (stems / ha) 2,593 1,51 1
In-growth (stems / ha) 2,680 3,762

 

a. data from (Murphy and Lugo 1986b)
b. data reﬁgured from that originally reported to match methods used in 1999.

27

Table 2-3. Importance values for stems 22.5 cm in Guénica Forest in 1999. See Table 2-1
for abbreviations.

 

 

1981 1999 % of
Order Order Species IV Total IV RF RD RC

1 i 1 Gymnant/Jer/ucida 48.45 16.15 8.38 25.38 14.68
6 2 Cocco/oba mimrtac/pra 23.38 7.79 7.26 8.57 7.55
5 3 Pictetia acu/eata 23.38 7.79 5.59 11.19 6.60
4 4 Pironz'a albida 21.56 7.19 5.03 2.75 13.78
3 5 Tbouiniaporton'cenn’r 17.76 5.92 5.03 8.95 3.78
2 6 Excite/71a caribeaum 15.88 5.29 7.26 3.77 4.84
8 7 Burrera nmaruba 10.83 3.61 5.03 1.02 4.78
15 8 Bourrerr'a .ruccu/enta 9.32 3.11 5.03 2.11 2.18
11 9 Cocco/oba divemfo/ia 9.21 3.07 4.47 1.34 3.39
9 1 0 Tabebuz'a betemp/gy/la 8.82 2.94 3.91 2.37 2.54
13 1 1 H Jpe/ate tnfo/z'ata 8.29 2.76 2.23 1.79 4.26
21 12 Guettarda e/lq'btica 7.53 2.51 2.23 3.58 1.72
7 13 Pi/orocereur mjenr'i 7.30 2.43 1.68 0.64 4.99
10 14 Eritba/irfmtz'cora 7.26 2.42 2.79 2.75 1.72
12 15 Canine ag/ocarpa 7.20 2.40 2.79 2.37 2.04
26 1 6 Leptocereur quadricortatur 7.12 2.37 1 .12 2.1 7 3. 83
14 17 Krugiodendmnﬁmum 7.10 2.37 3.91 0.83 2.35
17 18 [acquinia berten'i 6.76 2.25 3.35 1.28 2.13
18 19 Antir/rea acutata 6.15 2.05 1.68 2.56 1.92
19 20 Guettarda krugz'z' 5.53 1.84 2.23 2.17 1.12
20 21 .4221de elemifera 5.48 1.83 2.79 0.96 1.73
16 22 Cronopeta/urn r/racorna 5.31 1.77 2.23 1.85 1.22
22 23 Eritbmagllurn mtundzfo/ium 4.62 1.54 2.23 0.90 1.49
29? 24 Cocco/oba my“ 3.88 1.29 1.12 1.85 0.91
24 25 Forrrtiera regregata 3.76 1.25 1.12 1.85 0.79
25 26 Eugenia xemp/thica 3.70 1.23 1.68 0.96 1.07
28 27 Linociera bo/dridgz'i 2.43 0.81 0.56 1.02 0.85
27 28 Comoc/aa’ia dodonaea 1.95 0.65 1.12 0.58 0.26
29 29 Rgnoria guarna 1.73 0.58 1.12 0.38 0.23
30 30 Plunmia a/ba 1.64 0.55 1.12 0.32 0.21
31 Co/ubrina arborercenr 1.54 0.51 0.56 0.77 0.21

32 32 Zant/Joagr/urnﬂavum 1.01 0.34 0.56 0.26 0.19
23 33 Eugeniafoetz'da 0.93 0.31 0.56 0.26 0.12
34 Eugenia rbombea 0.89 0.30 0.56 0.26 0.07

31 35 T/m'nax Inom'riz' 0.83 0.28 0.56 0.06 0.21
33 36 Rocbefortia acantbop/Jora 0.75 0.25 0.56 0.06 0.13
37 Rgrnorz'a uncinata 0.71 0.24 0.56 0.06 0.09

 

a. originally reported with Cocco/oba mimrtac/Jja in 1981 (T ableV2-1). 1981 orderis estimated
from 1999 data.

28

Table 2-4. Comparison of soil chemistry in the Main site in 1981-83 and 1999.

 

 

 

1999 1981-1983"

mean SD n mean - 'SD W n
pH 7.91 0.16 614 7.8 0.1 33
0M(%) 29.08 13.32 623 23.2 10.65 38
N(°/o) 0.88 0.22 623 1.13 0.41 14
Pto(mg/g) 0.48 0.14 622 0.57 0.06 38
Pav(mg/g) 0.014 0.006 622 0.0074 NR NR
K.v(mg/g) 0.69 0.22 623 0.41 0.23 14
Caav(mg/g) 8.27 2.52 623 4.71 2.98 14
°/o Pay 2.9 1.3
%Kav 6.9 25
N/pto 28.3 6.5 19.8b
N/Pav 670 317 1525b
Bulk density 0.60 0.25 570 0.77 NR NR

 

No differences between means using t-tests at Ot=0.05.

NR = Not reported.

8Data collected from the top 5 cm of soil (Lugo and Murphy 1986).
bComputed from means above, not reported in Lugo and Murphy (1986).

29

 

 

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30

Figure 2—1. Map of Main site in Guanica Forest. Areas that are not designated Draw or Flat
are rocky slopes.

 

III-IIIIIIIIIIIIIIIIIIIIIIIIIIIIII .- ll... ....ll........... ..... l...
l I

FLAT

 

 

 

 

 

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\

 

 

 

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\‘

 

 

'- -- -- -- -- -- -- -\

 

 

\

 

 

 

 

 

 

 

 

 

 

 

 

 

 

' ' ' ' ' ' ' ' ' " Location of soil sampling transects —

N 20m

Bolded boxes are the 15 original plots used to describe forest structure.

31

Figure 2-2. Mortality and in-growth of stems 22.5 cm in the Main site of Guénica Forest
from 1981 to 1999.

 

 

Iln Growth
1300 - :5 Mortality
800 —
g 300 «
E
2
-200 - Fl? (i
-700 J;
i o
w ‘ .
‘ o o c Q o o o g [t
-12001<'.><rlr.> <9 '70? c? v.- a:
m o o q o o o o d
N ('0 V l!) (D B Q 0') v-

Stem diameter (cm)

32

I In Growth
I Mortality

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0.3 -
0.6 +
0.4 -
0.2 .
0.0 - _.
-0.2 -

Figure 2-3. Mortality and in-growth as basal area (top) and stem density (bottom) of stems

2.2.5 cm by species in the Main site of Guanica Forest from 1981 to 1999.

O
-200 a
.400 _

w
s

33

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(bottom) by species for stems 22.5 cm dbh that carried over from 1981 to 1999 in the Main

Figure 2-4. Average change in height and basal area (top) and average percent change
site in Guanica Forest.

 

A
54. s
00 n.v

AEV Ego: 3:20 on

34

Figure 2-5. Leaf and wood litter production from thirty 0.35—m2 litter baskets in Guanica
Forest. Daily rates are from the previous collection penod. Traps were placed on August
20, 1998. Black bars are average leaf-litter-fall values for the time period between
collections, based on 3 years of monthly sampling from 1981-83 (Murphy et al. 1995).
Hurricane Georges occurred one day after the initial sample was taken. Hurricane litter
production was not included in the data for the second collection period.

 

 

 

0 Leaves I Wood _ Average 1981-83 leaf litter fall
2.0 -
337‘
3g . _ _
E: 1.0 - . Q
g . —
s ’ _ O o
I — I__E__

 

 

20-Aug-98 19-Nov-98 18-Feb-99 20-May-99 19-Aug-99 18-Nov-99 17-Feb-OO 18-May—00 17-Aug-OO
Collection Date

 

Hurricane Georges:
Leaf litter fall = 239 g/m2
Wood litter fall = 510 g/m2

 

 

 

35

CHAPTER THREE

SPATIAL PATTERNS OF SOIL NUTRIENTS IN SUBTROPICAL DRY FOREST

Tropical dry forests hold the potential to evaluate questions about spatial patterns of
soil nutrients and carbon cycling. These forests have higher alpha diversity than seasonal
temperate forests (Bullock et al. 1995), providing the opportunity to evaluate tree species
effects on soil nutrient pools in systems with more complex species assemblage. In the dry
neotropics, litter turns over more slowly (1 -3 y, Martinez-Ynzar 1995) than in other tropical
forest systems or deciduous temperate forest systems (<1 y, Schlesinger 1997). The
accumulation of litter on the forest ﬂoor may subsequently increase the importance of
microbes, or lack of microbial activity, in determining spatial patterns of soil nutrients
(Binkley and Giardina 1998, Burghouts et al. 1998).

Spatial heterogeneity of soil resources can be inﬂuenced by plant growth (Day et al.
2003a, Day et al. 2003b), the strength and outcome of competition among plant species
(Reynolds et al. 1997, Fransen et al. 2001, Hodge 2003, Hutchings et al. 2003) and plant-
microbe interactions (Kinzig and Harte 1998, Ettema and Wardle 2002). Plants can strongly
affect nutrient content of underlying soil by nutrient uptake and nutrient return through
litter fall (Binkley and Giardina 1998). One trait common to plants growing in low-nutrient
environments is the retranslocation of the majority of a limiting nutrient from senescing
leaves, resulting in low-nutrient leaf litter (Boerner 1984, Vitousek 1984, Schlesinger 1997).
This creates a positive feedback where soil nutrients decrease as plants take up more
nutrients from the soil than they return via litterfall. Conversely, plants that retranslocate
fewer nutrients produce higher quality litter that can lead to comparatively nutrient-rich soil

patches (Schlesinger 1997). Plant-soil feedback can result in heterogeneous soil nutrient

36

pools with rich or poor patches roughly equal to the size of mature plants. Plant or plant-
population-sized patches of soil nutrients have been measured in desert (Schlesinger et al.
1996), grassland (Gallardo et al. 2000), old-ﬁeld (Robertson et al. 1988), temperate forest
(Boettcher and Kalisz 1990, Gross et al. 1995) and tropical forest locations (Dockersmith et
al. 1999). However, larger scale processes can also inﬂuence nutrient patch size. For
example, spatial heterogeneity has been shown to differ among forest stands within a
successional sequence (Gross et al. 1995) or with different disturbance histories (Hirobe et
al. 2003).

Spatial patterns of soil and litter nutrients interact with the activity and diversity of
soil microbial communities. Microbes decompose litter at lower rates as C:N ratios increase,
resulting in slow turnover of soil carbon and immobilization of soil nutrients. Spatial
patterns of microbial activity can therefore be inﬂuenced by the amount and quality of litter
produced by different tree species (Saetre 1999, Saetre and Baath 2000). Spatial patterns of
decomposition depend on particle size and distribution. Uniform distributions of same-
quality litter tend to decompose faster than patchy distributions and decomposition
progresses more quickly in smaller particles than larger ones because there is greater soil-
particle contact (Sorensen et al. 1996, Henriksen and Breland 2002). Smaller particles can
result in greater immobilization of nutrients as microbes are able to take advantage of larger
surface-area—to—volume ratios (Sorensen et al. 1996, Corbeels et al. 2003). However,
decomposition rates depend on initial litter quality and the amount of nitrogen available in
the soil for microbial uptake (Angers and Recous 1997). The diversity of microbial
communities decreases in low-carbon environments due to competition, but sites with high

organic matter maintain uniform microbial distributions and high diversity in space, possibly

37

because competition is reduced in an environment with a high diversity of carbon resources
(Zhou et al. 2002).

Parent material also inﬂuences patterns of nutrient availability. Soils developing
from limestone substrates will have higher pH and cation exchange capacity than those from
igneous substrates, which produce very acid soils in the tropics. Rainfall interacts with
parent material to increase weathering and leaching of nutrients. Tropical soils beneath dry
forests tend to be more fertile than those for wet forests when developed from similar
parent material, due to lower rates of leaching and lower decomposition rates. While the
high calcium content of calcareous soils maintains favorable cation exchange for plant
growth, it can decrease phosphorus availability by forming calcium phosphates at pH > 7.6
(Aber and Melillo 1991).

The amount of soil heterogeneity and correspondence of soil nutrient pools to plant
size has been assessed using geostatistics (Robertson 1987, Goovaerts 1998). Spatial
heterogeneity can be evaluated by the amount of variability that can be explained by spatial
autocorrelation, known as spatial structure. Patch size can be inferred from the range, or
distance, over which spatial autocorrelation exists. While most geostatistical studies focus on
a single plot or single plots within a series of treatments, this study uses four sites separated
by distances of at least 2 km in an effort to evaluate spatial heterogeneity not only within a

site, but among sites.

The primary objective of this research is to describe spatial patterns of soil nutrients
and pH within and among four sites in Puerto Rican dry forest. Within this objective,
special attention will be given to: 1) the association between soil Ca and available P, 2) the

potential for trees to determine spatial patterns of soil nutrients, and 3) the effects of local

38

topography on soil nutrient pools. Within these objectives, the following hypotheses were
considered:

i. Available phosphorus will be inversely related to calcium and pH. Soils in
Guanica Forest are calcareous in origin and have average pH > 7.6 (Lugo and Murphy
1986). Under these conditions, P is bound into calcium orthophosphates and becomes
unavailable for plant use.

ii. If individual trees have a strong effect on soil nutrient pools, then the range of
spatial autocorrelation will be similar to crown diameter. In temperate and tropical wet
forests, litter fall and tree productivity have been shown to have a greater inﬂuence on spatial
patterns of soil nutrients than did microbial activity, at least on scales > 1 m (Burghouts et al.
1998). If similar patterns hold for dry forests, then spatial autocorrelation should decline at
distances of 3-5 m.

iii. Soil organic matter, total N, and available P content will be lower in draws than
on slopes and ridges. The combined effects of deeper soils and greater soil moisture would
decrease soil carbon and nutrient levels due to greater leaching, decomposition by microbes,
and nutrient uptake by plants. Low soil nutrient pools in draws may occur despite higher
litter biomass or depth. Studies of topographic effects on soil nutrient pools in other dry
forests have generated conﬂicting results on this question. Raghubanshi (1992) measured
lower organic matter and nutrients on “hillbases” in Indian dry forests. In Mexico, organic
matter and total N content were lower in lowlands than adjacent uplands, but there were no
differences identiﬁed in N concentration ()aramillo et al. 2003). Finally, in another Indian
dry forest, troughs were found to have higher organic matter and nutrient concentrations
than ﬂats (Roy and Singh 1994). In this last case, low drainage from troughs appeared to

have concentrated leaf litter and nutrients.

39

METHODS
Site dcmiption

This study was conducted in Guanica Forest which is located in subtropical dry
forest in SW Puerto Rico on calcareous soils with limestone parent material. The soils are
classiﬁed as mollisols and have organic soil over clay extending to 70 cm depth. The
topography is hilly with rocky outcrops. Sampling occurred in a 1.4-ha Main site and in
three smaller satellite sites (Lluberas, Ventana, and Honda) located 1-5 km from the Main
site. Elevation of the sites ranged from 25-147 m above sea level (Figure 3-1). See the
Appendix for complete site descriptions.

The 1.4-ha Main site has been the subject of scientiﬁc study for over 20 years,
beginning in 1981 by Peter Murphy and Ariel Lugo (Murphy and Lugo 1986b). The
northeastern portion of the site is ﬂat with shallow litter layers and few outcrops. The
northwestern, center, and southern portions of the site are sloping and rocky with deep (>10
cm) litter layers. Frequently, soil was only found at the surface in crevices between rocks
and plants would root in loosely consolidated humus layers. The western side of the site
consists of a shallow draw which drains the northeast corner and most of the western half of
the site (Figure 3-1). Surface rocks are absent in the draw and the litter layer varies in
thickness, presumably accumulating in the bottom from transport from the sides and direct
deposition from trees overhead. The site had previously been used (before 1930) for non-
commercial charcoal production, where pits of 3-5 m diameter were dug, ﬁlled with wood
cut from nearby, lit on ﬁre, and covered with soil. The surfaces of the pits are now ﬂat. At
least three pits were located in the ﬂat, northeastern portion of the site and one in the draw.

There was no evidence of charcoal pits in sloped areas.

40

The Lluberas site is located in the original portion of the Commonwealth Forest, set
aside in 1919. The western third of the site follows the side of a very shallow draw located
further to the west (Figure 3-1) and has few outcrops. The eastern two-thirds of the site
were rocky with little surface soil. There were no signs of human use since 1930.

The Ventana site straddles a valley which runs from NW to SE. The soil surface is
rocky, resulting in rooting in the lower layers of litter. Of all the sites, Ventana is the most
open, having about 60% of the stem density found elsewhere. There have been no signs of
human use since 1930, but before 1920 there had been extensive ranching to the west of this
site and in the 16003 there was a Spanish outpost about 1.5 km west (M. Canals, personal
communication), so it is likely that the site has incurred some human disturbance in the past.

The Honda site is located just up the slope from a valley bottom. Outcrops are
absent. Mahogany (Swietem'a ma/Jagam) had been planted in the area in the 19303. The
mahogany was abandoned after planting and the area allowed to regrow without
intervention. Most of the mahogany trees were dead when the soil was sampled in March

2000.

Soil collection

Soil samples were collected for three objectives: 1) to determine spatial
autocorrelation among soil characteristics, 2) to map patterns of soil nutrients and pH across
the landscape, and 3) to relate nutrient content to growth of speciﬁc trees (Chapter 4).
Sampling locations were therefore established to optimize these objectives and differed
between the satellite sites and the Main site. To obtain an initial estimate of spatial
autocorrelation of soil properties, pH and soil moisture were determined from samples

collected at 1-m intervals along a 100-m transect on the west side of the Main site two days

41

after a soaking rainfall in June 1998. In July 1999, soil samples were collected around the
base of each of 475 trees that had been measured for 2-20 years previously for growth and
phenology. These trees were located 1-10 m from 6 transects which criss-cross the 1.44-ha
site (Figure 3-2A). For most locations, samples consisted of three bulked subsamples
collected in roughly equiangular locations 1 m from the trunk (Figure 3-2B). To improve
spatial analysis at short distances, some subsamples were analyzed separately instead of
bulked. Twenty additional samples were added at approximately 10 m intervals in areas
between transects to improve mapping. In total, there were 623 soil samples.

At the satellite sites, soils were collected to assess spatial distribution of nutrient
pools. The amount and placement of samples were determined in advance using GS+ 5.0
(Robertson 1998) to ensure sufﬁcient comparison pairs for geostatistical analyses. At the
Ventana and Lluberas satellite sites, 76 soil samples were collected from within a 30 x 30 m
block. Of these, 25 samples were uniformly spaced in a 7.5 m grid (Figure 3-2C). The
remainder were placed in a stratiﬁed random design, dividing the block into four quarters.
The Honda site was established by Martin Quigley (Quigley and Platt 2003) and measured 25
x 25 m, therefore only requiring 69 samples (25 in a 5 m grid, 44 random).

At each sampling point, the top 10 cm of soil (a volume of ~200 cm’) was collected
using a hammer corer or bulb planter. In approximately 10% of samples, where the rocky
soil or outcrops prevented collection to 10 cm depth, shallower depths or alternate sites
were used within 50 cm of the target location. As a coarse estimate of litter mass and
productivity, litter depth was measured to the nearest 0.5 cm at each soil sampling point
except at Ventana. Fresh soil samples were placed in clean cloth bags, kneaded to break up
clumps, and air dried at 40°C. (Cloth bags facilitate air drying and kneading without tearing.)

Dry soils were sieved with a #18 mesh for lab analysis. All sample locations were recorded

42

using a 12-channel Trimble Pro GPS system. The GPS data were differentially corrected
using the US State Plane 1927 coordinate system, PR&VI 5201 coordinate zone, and NAD
1927 (Puerto Rico) datum. Horizontal positions were precise to within 1 m (Table 3-1) and
elevation to 2 m. Sampling occurred in June 1999 for Lluberas and in March 2000 for

Ventana and Honda.

Laboratogt anabrz's

Total soil nitrogen was analyzed on 100-mg soil subsamples using dry combustion in
a LECO CNS analyzer with a thermal conductivity detector. Soil samples were combusted
at 1450°C. Organic matter (OM) was measured as loss on ignition by combusting samples
in a mufﬂe furnace at 490°C. At this temperature, loss on ignition does not include clay-
bound water and therefore estimates OM well (Nelson and Sommers 1996). Organic C was
estimated as 50% of OM. Total concentrations of calcium and total phosphorus (TP) were
determined by digesting 100-mg subsamples in nitric acid followed by hydrogen peroxide.
Using S-g subsamples, available phosphorus (Pay) was extracted using a modiﬁed Olsen
solution (Wilde et al. 1979). Digested total and available element concentrations were
determined using an atomic-emission spectrometer. Measurement accuracy was maintained
for each analysis by verifying standards after every twenty samples and running duplicates of

every tenth sample.

Statzlrtica/ rumba":
Differences in soil characteristics among sites were assessed using ANOVA with
Tukey tests for multiple comparisons. Trends in nutrient contents were compared using

multiple correlation with Bonferroni adjustments for p values. Strong correlation between

43

factors was indicated by |r| > 0.8, moderate correlation by 0.8 > | r| > 0.5, and weak
correlation by 0.5 > | r] > 0.3. Signiﬁcance levels were set at (1:005. Parametric analyses
were completed using SYSTAT 8. The amount of variability of soil properties within sites
was evaluated using coefﬁcients of variability (CV).

Patchiness of soil properties was determined by analysis of spatical autocorrelation
using semivariance. Semivariance models are developed by determining the amount of
dissimilarity of measured values (e.g. nutrient content) for each pair of data points sampled
within a given range of distances (lag interval). At greater distances, the similarity between
sampling points decreases and semivariance increases. Semivariance analysis provides four
statistics that are useful in describing spatial autocorrelation of a given property (Figure 3-
3A). The range (a) estimates the maximum distance between two samples that exhibits
spatial autocorrelation. Range therefore can estimate patch size for a soil property. Structure
(C) is the variance in a property (i.e., a soil nutrient) that can be explained by spatial
autocorrelation. Nugget variance (Co) is the variance that cannot be explained by spatial
autocorrelation. The sill (C + Co) is the amount of semivariance at its asymptote, which is
reached at the range. Theoretically, the nugget should be zero, but measurement error or
processes which occur at scales ﬁner than the smallest sampling interval result in nugget
variance. When structure accounts for a large proportion of sample variance (PSV), spatial
autocorrelation of the measured property is high. Theoretically, the sill equals the
population variance (:2) of the sample. If the sill is lower than population variance, spatial
structure exists at a distance greater than that modeled. Sometirnes this is the result of larger
scale processes (e.g. land use or topography) inﬂuencing patterns at distances greater than

the maximum interval sampled. These inﬂuences can lead to nested structure (Figure 3-3B).

44

Semivariance models were subsequently used to interpolate (krig) surface maps of
each soil characteristic. All geostatistical procedures were performed using GS+ 5.3a
software (Robertson 1998). A minimum of 30 pairs of data points were present in each lag
interval in order to assure valid estimates of semivariance. When necessary, raw values were
transformed prior to analysis because geostatistical methods require normally distributed
data. Data were back-transformed after kriging.

At all sites, the closest spacing of samples was 1 m, while the maximum spacing
varied from 35-168 m (Table 3-1). I used a minimum lag interval of 2 m for the main site,
corresponding to the measurement error of the GPS data, even though sufﬁcient pairs
existed for comparison at 1 m intervals. Wider intervals were used in the satellite sites to
satisfy minimum pair requirements. The maximum separation distance with sufﬁcient pairs
was 32 m for Ventana and Lluberas, 27 m for Honda, and 150 m for the Main site. Analyses
at the main site were also performed using a maximum separation distance of 32 m for
comparison to the satellite sites. At the main site, some soil nutrients exhibited different
levels of autocorrelation depending on spatial scale. In these cases, nested models were ﬁt

by analyzing spatial structure at varying lag distances.

RESULTS

Most soil properties differed among sites, indicating high variability across the
landscape (Table 3-2), including: pH (range 7.7-8.0), N (0.48-1.77%), Ca (53-260 mg/ g), and
N :Pav (400-1490). Average TP differed among three sites (range 0.48-0.96 mg/ g) The
proportion of TP that was in available forms ranged from 1.3-2.9°/o. On the other hand,

three soil properties showed few differences among sites. Three sites shared similar values

45

of Pay (13-14 mg/ kg) and N:TP (18-20). C:N was the same for Main and Honda (17-18) but
differed from Lluberas and Ventana (14).

Within sites, CVs for soil nutrient content and ratios were usually greatest at the
Main site, ranging from 29-61%, and lowest at Honda (9-38%). Ca and N were among the
more variable soil properties within each site (range of CVs for Ca: 40-73% excluding
Honda; and N: 21-53%) while pH, C:N, and TP varied little within sites (range of CV: 2-3%,
11-28%, 15-29%, respectively). Litter depth showed high variability among and within sites
(averages: 3.5-9.3 cm; CV 32-54%).

At the satellite sites spatial autocorrelation of soil nutrient content existed to a range
of 17-25 m (Table 3-3) with two exceptions at Lluberas, where TP was structured to only 7
m and Pay to 28 m. In addition, the limit of spatial structure was greater than the maximum
lag interval (27 m) for Ca at Honda, as indicated by a linear model. Despite these
exceptions, the similarity among ranges across nutrients and sites is noteworthy. Spatial
structure described at least 74% of sample variability, indicating strong autocorrelation for all
nutrient contents at each satellite site except for Pav at Lluberas (PSV 56%). Ranges of
spatial autocorrelation for nutrient ratios, pH, and litter depth were either <16 m or >25 m
(Table 3-4). limits to spatial autocorrelation were greater than maximum lag intervals for
N:TP at Ventana and litter depth at Honda and Lluberas. Spatial structure described 53-
100% of variability in nutrient ratios, litter depth, and pH at the satellite sites.

Ranges of spatial structure when analyzed over short distances at the Main site were
similar to those found at the satellite sites, with few exceptions (Tables 3-4). When
measured over short distances (32 m), pH, OM, N, Pay, and TP were spatially autocorrelated
to a range of 18—21 m. Spatial autocorrelation was indicated at ranges greater than 32 m for

Ca, greater than the ranges found for other soil nutrients or for Ca at the satellite sites. PSV

46

was only 66% for TP at Main, nearly 20% lower than at the next lowest site. Spatial
structure accounted for 77-100% of variability for all other soil nutrients and pH. Nutrient
ratios also showed a high degree of spatial structure (71-85%) with ranges from 10 to 27 m.
Litter depth and soil moisture were autocorrelated to a range of about 30 m but with only
50-58% of variability explained by structure.

In the Main site, all soil parameters with the exception of Ca exhibited nested spatial
structure when analyzed over 100 m (Figure 3-4) with a second level of structure developing
at 45-82 m (Table 3-3). Ca was structured to a range of 73 m, without nesting. Litter depth
was also nested, with the largest range of spatial structure at 112 m. The nested pattern of
nutrients is illustrated by the soil nutrient maps at the Main site (Figure 3-5). Within the
areas of higher N or OM (the second darkest color band), for example, exist smaller patches
containing the highest N or OM contents, indicating smaller-scale variability. Larger scale
trends are shown by higher N or OM near the center and east of the site grading to lower
contents in the north and west sides.

Soil N was strongly correlated with organic matter (r>0.8) at all sites, but
relationships between other combinations of soil properties were less consistent (Table 3-5).
Total and available forms of P showed no forest-wide patterns of association. Pay increased
with TP only at the Main and Ventana sites (r = 0.43, 0.67). At the main site Ca was
negatively correlated with the other nutrients, while TP and Pay increased with OM and N (r
= 0.60-0.72). Ca content increased with pH at Main and Ventana. No consistent patterns of
association existed among combinations of nutrients aside from OM and N at the satellite
sites. N and OM decreased with pH, but correlations were moderate to weak (r < 0.6).
Association between soil nutrients and litter depth were only apparent at the Main site.

Elevation had no effect on phosphorus or Ca, but weak positive correlations were present

47

for N and OM in two satellite sites (r < 0.4). Soil nutrient contents decreased as C:N
increased. N:P ratios were positively correlated with OM and N. N:Pav decreased as P
availability increased in soils.

Strong correlation between nutrients was evident by their similar spatial distributions.
At the Main site, high levels of OM, N, Pay, and N:TP were found on the slope forming the
east side of the draw and on the east side of the site, while low levels were found in the draw
and on the north side (Figure 3-5). These soil properties had the opposite pattern of Ca,
reﬂecting their negative correlations with Ca. With the exception of C:N, N :Pav, and litter
depth, soil characteristics appeared to track the draw on the west side. Locations of high N,
OM, and Pay also correspond to areas where rock outcrops were common as organic matter
was trapped in crevices.

At Lluberas, the general lack of correlation between soil properties was evident in the
dissimilarity among their spatial distributions (Figure 3-6). However, the strong correlation
between N, OM, and N:TP was reﬂected by all three properties having high values in a
patch in the NE quarter of the site, with decreasing values to the south and west. This patch
corresponds with the highest elevation at the site and the area with the most open canopy.
Properties with low range of structure (e.g., litter depth and TP) were illustrated by the
presence of many small patches and patches of high levels located near low level patches
(note high TP patches on west side of site within 10 m of low TP in the NE).

Soil nutrient contents at the Ventana site were greatest in the NE corner, which had
the highest elevation (Figure 3-7). Nutrient-poor areas were found in the NW and SE
corners. C:N ratios were highest in the area with both low OM and N. The similarity in
nutrient distributions reﬂected both the positive correlations and the consistent range

structure among all nutrients.

48

High OM, N, and TP were present in the north-central portion of the Honda site
(Figure 3-8). Low values of these nutrients were found at or near the lowest elevation of the
site, but high values were also found at intermediate elevations. The small range of spatial
autoconelation (5 m; Table 3-4) indicated by the patchiness of pH contrasted with the 18-

19 m ranges for OM, N, and Pav and the linear trends of Ca and litter depth across the site.

DISCUSSION
Among-site pattern; of rail nutrient:

Soil nutrient pools varied signiﬁcantly across the landscape, even though each site
had similar soil types and forest cover. The advantage of using multiple plots is that the
repeatability of patterns across the landscape can be assessed. For example, total soil
nutrient pools and pH differed among sites, while Pay remained constant. Some properties
maintained patch size from site to site (e.g., OM and N), while patch size varied among sites
for others (e.g. pH or C:N). In some locations, combinations of soil properties were
correlated while the same patterns were absent elsewhere (cg. contrasts for soil nutrients in
Ventana and Lluberas, Table 3-5). The high degree of variability among sites separated by
only a few kilometers indicates that extra care must be taken when interpreting results from
single plot studies. Using plots of different sizes also help to address issues of scale and
identify patterns that would otherwise be overlooked in smaller plots.

Despite the high variability of soil nutrients from site to site, some trends emerged.
Soil OM and N were always closely correlated in space and content. In addition, N generally
increased with TP and with decreasing pH. Thus, although each site varied from the other
in fertility, soil factors that contribute to fertility tended to vary in tandem within sites. The

association between OM, N, and TP may be the result of higher productivity. At the Main

49

site, litter depth increased at higher concentrations of TP, Pay, OM, and N and distributions
of OM, N, and Pav were also similar spatially. Considering previous indications that the
forest may be P-limited (e.g., PUE, high leaf and soil N:P ratios; Lugo and Murphy 1986),
one might expect P pools to be strongly correlated to CM and N pools, as higher P supplies
would result in greater productivity. However, the strength of correlation between P and
OM or N was always less than between OM and N alone. The weaker relationships between
P and OM than between OM and N probably result from two factors. First, trees in
Guénica Forest retranslocate a greater proportion of P than N from senescing leaves (Lugo
and Murphy 1986), so litter P would not be as closely tied to litter mass than litter N.
Second, while higher levels of soil P may alleviate some nutrient limitation, these P-rich
locations may not be in areas with favorable soil moisture. In addition, average C:N ratios
for each site were below 20 (Table 3—2), suggesting that N was in sufﬁcient supply for
microbial activity and unlikely to be immobilized (Paul and Clark 1996). As such, N would
be free to cycle through the system with OM. To adequately evaluate whether plant uptake
or microbial activity has the greatest effect on soil nutrient pools, nutrient ﬂux
measurements would need to be performed.

Of note are the high concentrations of OM found in Guénica Forest that tend to be
greater than those found in other dry forest locations (Chapter 2). High OM may minimize
microbial competition for carbon, thereby maintaining high diversity and size of microbial
populations (Zhou et al. 2002). Large, diverse communities may be more able to maintain

functionality during periods of stress and more efﬁciently cycle nutrients.

50

Pattern: qfcala'am, pH, and available p/Joipbomr

As expected based on previous studies (Lugo and Murphy 1986), levels of Ca and
pH were high at all sites in Guanica Forest while the percentage and quantity of Pay was low.
However, in contrast to expectations, there were no consistent spatial patterns or correlative
trends supporting direct control of Pay by Ca or pH. Nor were there consistent patterns
between TP and Pay. For example, at Ventana, Ca was strongly positively correlated with
Pay, while at Main there was a weak negative correlation. Spatial patterns of Pay and pH
differed at all sites, as did Pav from Ca and TP (except at Ventana). While it is apparent that
much of the TP was bound to Ca in the soil based on low %Pav, the difference in spatial
patterns of Pay from TP, Ca, and pH would be inﬂuenced by a variety factors. Geologic
sources of Pay include weathering of P-rich minerals and dissolution of clay- or calcium-
bound phosphates by carbonic or organic acids. Mycorrhizae and other fungi release
organic P for plant uptake (Allen 1991) and plants can acidify the rhizosphere to increase P
availability (Aber and Melillo 1991). Once available, P, as the potentially limiting nutrient in
the system, would be rapidly taken up by plants as long as sufﬁcient water was present to
transport P through the soil. Thus, multiple sources and sinks of Pav control its unique
distribution across the landscape and its lack of consistent association with other nutrients

from site to site.

Local maﬁa/pattern: (frail nutrient:

Patch sizes of soil nutrients (as inferred from the range of spatial autocorrelation)
measured 17—25 m, with few exceptions. Soil nutrient patches were at least threefold greater
in size than average crown diameter, contradicting the hypothesis that nutrient patch size

would equal tree crown diameter. Therefore there is no evidence of the tight tree-soil

51

nutrient feedbacks that have resulted in crown-sized patches of soil nutrient content noted in
other forested systems (Boettcher and Kalisz 1990, Gross et al. 1995, Dockersmith et al.
1999, Gallardo et al. 2000). In addition to being small in diameter, tree crowns and root
systems in Guénica Forest intermingle and leaf area index is low (~3, Murphy et al. 1995).
Tree species diversity is high and analysis of leaves in litter traps (personal observation)
shows that constant trade winds are able to transport leaves away from directly beneath their
trees. Therefore leaf litter is well mixed on the forest ﬂoor and the ability of single trees to
control patterns of soil nutrients is diminished.

At the Main site, nested spatial distribution of soil nutrients reﬂected multiple
inﬂuences operating at different scales (Figure 3-4). Larger scale trends were only
measurable at the Main site because more samples were taken over greater distances. The
northeast and a section of the west side of the site were used for charcoal production until
70 years ago. The southeast quarter of the site has numerous rock outcrops. It is probable
that both land use and topography have inﬂuenced soil properties in Guanica Forest at
scales >25 m, leading to nested spatial structure. Spatial patterns at scales < 25 m were
probably driven by the effects of litter on soil nutrients as mediated by plant production and
uptake, microbial decomposition, and transport by wind and water.

The large patch size of soil nutrient pools has several implications for carbon and
nutrient cycling. A well-mixed forest ﬂoor and large patches of nutrient pools may lower the
potential for hotspots of cycling to occur (Hutchings et al. 2003). Conversely, if hotspots
did develop, they could be larger than found in other forest systems, at least when water is
plentiful. At a centimeter scale, the mixing of leaf litter on the forest ﬂoor will bring
substrates of different qualities closer together, potentially increasing decomposition

compared to systems where nutrient patches are more discrete. More homogenous

52

collections of leaf litter or nutrient pools tend to result in faster decomposition and nutrient
turnover (Sorensen et al. 1996, Henriksen and Breland 2002). On the landscape level, the
intermingling of more nutrient-rich leaves with nutrient-poor leaves on the forest floor may
partially counteract the potential for dry forests to sequester carbon. However, the
overriding control of decomposition in these systems is water availability which has been
interpreted to result in long turnover times for leaf litter (Lugo and Murphy 1986, Martinez-
Ynzar 1995). The effects of water on nutrient cycling in dry forests is a question that

remains to be addressed, particularly as rainfall is highly variable within rainy seasons.

Eﬁctr of topograpb}

Large scale (i.e., 50 m) differences in elevation in Guanica Forest did not appear to
be related to soil properties (Table 3-2). While the highest site, Lluberas, had the greatest
amounts of OM, N, and TP, the second highest amounts of these nutrients were found at
the lowest elevation site, Ventana. This ﬁnding contrasts with results from Mexican dry
forests, where less OM was consistently found in sites at lower elevations (Jaramillo et al.
2003) due to loss by erosion and soil turnover.

In each of the four Guénica Forest sites, but particularly evident in the Main site,
microtopography affected soil properties. Higher concentrations of soil OM and N were
found at locally higher elevations. These locations were frequently covered by limestone
outcrops which trapped litter in crevices, retained less rainfall, and dried quickly, resulting in
slower decomposition and greater litter build up. OM accumulated in the crevices between
outcrops, increasing N and C concentrations, creating a thick humus layer, and resulting in
root development above the mineral soil, which was observed during sample collection.

Conversely, organic matter in areas with deeper soil and less outcropping (such as Honda

53

and the draw in the Main site) could decompose faster as a consequence of greater contact
with mineral soil (as opposed to rocks) and higher soil moisture. Honda had the lowest
average values of soil OM and N (Table 3-2), despite being the most productive site,
suggesting that decomposition rates are relatively fast. Ca was highest in deeper soils as a
consequence of being a major constituent of the mineral soil — as opposed to areas with
deeper humus between outcrops of limestone.

In an Indian dry forest, higher OM at higher elevations was associated with
microtopography, where small depressions in the terrain caught litter (Raghubanshi 1992),
similar to patterns found at the Main site. At another Indian forest, small troughs
concentrated litter, resulting in more OM and nutrients (Roy and Singh 1994). The patterns
in Indian dry forests complement the pattern found in Guénica Forest — where
microtopography is able to concentrate or trap litter, soil OM and nutrients increase,

regardless of elevation.

Spatial structure in Gua’m'ca Pom! compared to oI/Jerﬁrert:

Spatial patterns of soil properties have been analyzed with geostatistics in two other
tropical dry forests. On volcanic soils in St. Lucia, Gonzalez and Zak (1994) analyzed a 56 x
56 m plot with 4-m spacing between samples. They found spatial structure for pH, Pay, and
organic C at distances of 58 m, 48 m, and 71 m, respectively, indicating that spatial structure
was not related to crown diameter. Forest ﬂoor biomass and soil texture were structured to
ranges of 20-24 m. Their patterns for Pay and organic C appeared nested, with the ﬁrst
plateau occurring at about 24 m. Overall, the range of spatial structure on St. Lucia
corresponded well to Guénica Forest (Tables 3-3, 3-4), especially when comparing the

nested values for Pay and organic C. Conversely, the spatial structure explained less variation

54

in St. Lucia where PSVs (pH=58%, Pav=45%, organic C226%, forest floor biomass=29°/o)
were either at or below the lowest PSV for any site in Guénica Forest. The 4-m sampling
interval used in St. Lucia would have missed a notable amount of spatial structure, as
demonstrated for Guénica soils (Tables 3-3, 3—4, Figure 3-4). In a Thai dry forest (l-lirobe et
al. 2003), the range of soil moisture and inorganic forms of nitrogen decreased from 2 9.0 m
to 1-3 m as forests recovered from ﬁre. The smallest ranges were for forests ﬁre-free for 35
y, but model ﬁts were low (r2 < 0.5). The small scale at which this study was conducted (9
m) makes it difﬁcult to compare to patterns at Guinica Forest but does suggest that
individual trees may affect N mineralization and denitriﬁcation as the forest recovers from
ﬁre.

In other ecosystems, Gross et al. (1995) found spatial structure in soil moisture to 2
16 m in a mature temperate forest in Michigan and at ranges of 4-6 m (PSV 50—80%) in a soy
bean ﬁeld and an old ﬁeld. In these same sites, the range of soil N was greatest in the old
ﬁeld (15.6 m; PSV 63%) and less in the soy bean ﬁeld (2.5 m; PSV 33%) and forest (8.4 m;
PSV 35%). Compared to these locations, spatial patterns are stronger and exist over longer
distances in Guénica Forest. In an agricultural ﬁeld in Michigan, soil moisture, pH, C:N,
organic C, and inorganic P exhibited spatial structure from 45-63 m (Robertson et al. 1997).
Spatial variability explained most of the sample variability (PSV 76-93%) and a nested model
was computed for pH. Nesting was attributed to plant-soil interactions, soil development,
topography, and land use history as spatial scales increased. These results were very similar
to patterns found in the Main site at Guinica Forest, except that the smallest range of

nesting at ~20 m was absent, probably due to the homogenizing effects of cultivation.

55

CONCLUSIONS

Analysis of spatial patterns of soil properties in Guénica Forest reveals a landscape
with high variability among and within sites, but relatively large patch sizes when compared
to other forest types. Soil nutrient contents varied as much among sites as within sites.
Throughout the forest, levels of Ca, OM, and pH were high, and Pav was low. C:N ratios
were <20, suggesting that microbial immobilization of N was unlikely. OM and N were
greater in locations where microtopography tended to collect litter. Clear associations
between Pay and pH or Ca were absent, despite the potential for Ca to bind P at high pH,
suggesting that the distribution of Pa“, was controlled by both physical and biological activity,
rather than by soil chemistry alone. Patch sizes for most soil properties measured 17-25 m
with another level of spatial structure at 45-112 m. Pools of OM and N were strongly
correlated in space and size and, to a lesser degree, with P. The range of spatial structure for
most soil properties in Guénica Forest was comparable to dry forests in St. Lucia, but greater
than in other forest types where ranges tended to track aVerage crown diameter. Crown-
sized patches of soil nutrients in Guénica Forest were absent - likely the result of the forest’s
thin canopy and high stem density, which would intermingle crowns and roots and diminish
the localized inﬂuence of individual trees on soil nutrient pools. Thus, the diversity of trees
above ground was not translated below ground, because crown diameter did not correspond
to soil nutrient patch size.

Although this research identiﬁes clear trends in patch sizes of soil nutrient pools,
further research will be necessary to identify mechanisms that determine patch size. One
issue to be resolved would be whether patch sizes of soil nutrients are controlled more by

microbial decomposition of litter or the possibility of P limitation of plant productivity

56

indirectly inﬂuencing litter biomass. Some studies have suggested that plants will have a
greater inﬂuence on soil nutrient content via litterfall than microbes will by decomposition
(Burghouts et al. 1998). However, both productivity and decomposition appear to be
resource limited, possibly by P and certainly by water. A more direct method to measure
resource limitation of productivity would be to compare growth rates against soil nutrient
content. This is undertaken in Chapter Four. The information presented here on patch size
and spatial distribution of nutrient pools across the landscape should be a useful guide in
developing future projects to measure nutrient ﬂuxes in relation to decomposition or P

limitation of plant productivity.

57

Table 3-1. Sampling points, lag classes, and intervals used for geostatistical analysis of soil
data. Horizontal precision is the measurement error for XY locations measured by the GPS
unit.

Site Main Lluberas Ventana Honda
Sample points 623 76 76 69
Horizontal precision (m) 0.90 0.98 0.84 1.06
Uniform lag interval (m) 2 4 4 3
Maximum interval (m) 32 or 100 32 32 27
Pairs, 1’t interval 1207 101 106 63
Pairs, 2"d interval 1496 336 310 219

58

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59

Table 3-3. Parameters for variogram models of soil nutrient concentrations. PSV is the
proportion of structural variance (C/ (C+ Co)) where C is structure and Co is nugget variance.

 

Effective
% Site Max lag Model Rang (m) r2 PSV °/o
Organic Matter
Honda 27 spherical 18.9 0.92 83
Lluberas 32 spherical 24.0 0.97 74
Ventana 32 spherical 18.6 0.90 97
Main 32 spherical 21.4 0.95 100
Main 100 spherical 55.5 0.69 94
Nitrogen
Honda 27 spherical 19.3 0.94 82
Lluberas 32 spherical 25.0 0.96 82
Ventana 32 spherical 19.6 0.94 100
Main 32 spherical 19.1 0.94 100
Main 100 spherical 69.2 0.75 88
Available P
Honda 27 spherical 17.8 0.88 78
Lluberas 32 spherical 27.7 0.91 56
Ventana 32 spherical 1 7.4 0.68 98
Main 32 spherical 18.7 0.85 77
Main 100 spherical 62.2 0.72 67
Total P
Honda 27 spherical 22.9 0.95 100
Lluberas 32 exponential 7.0 0.63 85
Ventana 32 spherical 20.5 0.97 93
Main 32 spherical 20.7 0.77 66
Main 100 spherical 45.2 0.59 83
Total Ca
Honda 27 linear * 0.91
Lluberas 32 spherical 17.8 0.96 74
Ventana 32 spherical 1 8. 8 0.78 100
Main 32 linear * 0.97
Main 100 spherical 72.6 0.96 91

* greater than maximum lag interval

60

Table 3-4. Parameters for variogram models for litter depth, pH, elevation, and nutrient
ratios. PSV is the proportion of structural variance (C / (C+ Co)).

 

Site Max lag Model Effective r2 PSV
Range—(m) o/o

C:N
Honda 27 exponential 1 1.8 0.80 82
Lluberas 32 exponential 28.7 0.97 51
Ventana 32 spherical 15.1 0.88 95
Main 32 spherical 10.3 0.79 85
Main 100 spherical 81.5 0.80 57
N:TP
Honda 27 exponential 15.7 0.78 54
Lluberas 32 exponential 15.2 0.93 88
Ventana 32 linear * 0.96
Main 32 spherical 17.3 0.80 65
Main 100 spherical 61 .7 0. 89 70
N:P.v
Honda 27 spherical 8.5 0.82 84
Lluberas 32 exponential 48.5 0.92 53
Ventana 32 spherical 14.6 0.83 59
Main 32 spherical 19.5 0.96 72
Main 100 spherical 54.7 0.70 77
Litter Depth
Honda 27 linear * 0.91
Lluberas 32 exponential 4.4 0.43 96
Main 32 exponential 30.1 0.85 58
Main 100 linear * 0.83 87
pH
Honda 27 spherical 5 .0 0.31 100
Lluberas 32 spherical 15.1 0.75 80
Ventana 32 spherical 21 .6 0.59 58
Main 32 spherical 18.1 0.90 78
Main 100 spherical 64.6 0.75 68
Soil Moisture
Main 321 spherical 28. 8 0.95 50

* greater than maximum lag interval
1Estimated from a 100 m transect 2 d after a soaking rain.

61

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Figure 3-1. Elevation maps of experimental sites in Guanica Forest, Puerto Rico. Contour
bands are at 2 m intervals.

Main Lluberas

    
  
 

136

134

 

 

1 l11'1
”“1111” 1111mm; 1 2
;, "11mm!“ 111111l|.|.hm Ill u.
1 1‘1 1.
111111 1111111111111111111113 111111111111' Iwy1'1 1" 130
126
124
‘_120 m —> 4—30 m—>
Ventana Honda

 

 

63

Figure 3-2. Soil sampling and mapping locations in Guanica Forest: (A) Main site, (B) at the
base of trees in the Main site and (C) general scheme for satellite sites using Lluberas as an
example. The higher density of soil samples along six transects in the main site reﬂect
locations of trees measured for growth and phenology for the last 4-20 years.

OApproximate locations
of old charcoal nits

 

 

 

 

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630 680 730 780
MM
3 C Soil samples

 

 

 

 

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X(m)

64

Figure 3-3. A) A generalized semivariogram, showing nugget variance. The sill is the total
amount of variability within the sample. Structure is the amount of variability explained by
spatial autocorrelation. Random variability, sampling or measurement error, and variability
attributable to spatial scales smaller than the smallest lag interval make up nugget variance.
The range is the distance where the values measured at two points are completely
independent — the distance where spatial structure ceases. When no spatial structure is
present, the nugget equals the sill. As the distance between sampling points increases,
structure decreases. B) Nested structure in spatial autocorrelation caused by three
hypothetical inﬂuences operating at different spatial scales.

 

 

 

 

 

 

A
A Sill 0+ 00 z o ulation variance
3: Structure A ( 1 p p
g (C)
.9
a
.2
E
(‘3 Nugget variance (Co)
Distance (lag) interval (h)
Range (a)
B
4- Land use influence
8 <——— Topographic influence
a)
g A Local influence (tree,
'33 ‘ microtopography, etc.)
E
d)
a)

 

 

Distance (lag) interval (h)

65

Figure 3-4. Variograms for soil nutrient concentrations at the Main site. Dotted lines are
sample variance (3’). Parameters for each model are listed in Table 3. Left panel in each case
is at 150 m interval, right panel is 32 m interval.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Loss ON IGNITION
070 (155
I
046’ 036’ I
. I
I
023” 0J8’
QW' ' i . ¢ . c 0.00 v . . 4 ﬁ . - .
O 25 50 75 100 0 8 16 24 32
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U
é AVAILABLE PHOSPHORUS
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8 .

 

 

 

 

 

 

 

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TOTAL CALCIUM

8100‘

 

 

 

5400’

2700’

 

   

. U . . . . .
100 0 8 16 24 32

 

 

O 25 50 75
Distance Interval (m)

66

Semivariance

Figure 3-4. Continued

NITROGEN

 

 

 

0J4

0J0”

005

 

 

 

 

0.022L

 

 

0015”

 

 

 

 

 

 

 

 

0A7

 

031'

 

000 ' '
0 8 16 24 32
. 0019
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0.012 I...
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75 100 0 8 15 24 32
Q40

 

 

 

 

 

 

8 16 24 32

 

 

 

 

 

 

 

 

Qﬁﬁvv’ 000
o
N:PAV
003* 002
002
001
0.00w * v ' ' ' 000
0 25 50 75 100 0

Distance Interval (m)

67

Semivariance

Figure 3-4. Continued

 

 

 

 

 

 

 

 

 

8.5‘

64

21

SOIL MOISTURE

D

100

W

 

 

 

 

0.06

0.04 ’

0.02 '

 

 

 

0.00

 

0.61

0.41 ’

0.20 '

0.00

64

21

 

 

 

 

Distance Interval (m)

68

Figure 3- 5. Isopleths of soil chemical properties at the Main site derived by 2x2 m block
kriging. The site measures 120 m on each side. Table with legend gives levels for each color
band.

Organic Matter Nitrogen

 

 

 

 

 

 

 

 

 

42.8
32.7
22.5
12.4

 

69

Figure 36. continued

pH Litter Depth

 

 

 

   
  

    

ill”

I III”. my"

A y
- QQ- My.
3 . «km uny I u

, ‘1‘. "
111‘!ny lily’yylm

       

 

 

gled 1 AI‘J l l 1 l l l l

 

 

‘ Llwyyy -
N:Pav
PH Litter N:TP N:Pav
Depth
cm

 

1.42 17 31 1710
1.23 15 27 1436 -

0.84 9 19 887
0'64 6 14 613

 

 

 

 

70

Figure 3-6. Isopleths of soil chemical properties at the Lluberas site derived by 2x2 m block
kriging. The site measures 30 m on each side. Table with legend gives levels for each color

 

 

     

 

  

 

 

 

 

band.
Organic Matter Nitrogen
y " h I . y “ "yilgﬂhyyyfyyi:i
1’ I I A] 'l'l'y‘ ‘
" y
“""iimn 'ul
yyryy"iiiiiimumu1‘""'"i '
OM N TP Pav Ca
% % mg/sI mg/kg mg/g
67 2.6 152
60 2.3 1.2 15.8 128
52 1.9 1.1 14.3 104 '
44 1.6 1.0 12.9 79
36 1.3 0.9 11.4 55
29 0.9 0.8 10.0 31

 

71

 

Figure 3-6 continued

pH Litter Depth

 

 

 

 

"111ny

 

“my! 1
8.2 7.4 30.7 1670 14.9 yyI1.y.,y”"1111“:“""Nv
8.0 6.4 26.4 1510 14.5 - . 'y'yi‘f
7.8 5.4 22.0 1340 14.1 «

7.7 4.5 17.6 1180 13.7
7.5 3.5 13.2 1010 13.4
7.3 2.5 8.9 840 13.0

44

 

 

72

Figure 3- 7. Isopleths of soil chemical properties at the Ventana site derived by 2x2 m block
kriging. The site measures 30 m on each side. Table with legend gives levels for each color
band.

Organic Matter Nitrogen

 

 

 

 

 

 

4'—30m—>

73

Figure 3-7 continued

 

 

 

 

lyyull’ l‘r'!
I‘ll-iii I" l 11
:5 ‘i : 1,1.
1!? "H1111 " " "
11 . ii" " Willi" ., ..|i‘ L
.141‘1 11.11111:1111 "”1
I; ”my » "null” mull“ ’11th
pH N:TP N:Pav CN
1089 32 2110 17.9
932 28 1890 16.6
775 25 1670 15.4
619 22 1450 14.1
462 18 1220 12.9
306 15 1000 11.7

74

 

Litter Depth

(Not measured)

N:TP

 

 

 

Figure 3—8. Isopleths of soil chemical properties at the Honda site derived by 2x2 m block
kriging. The site measures 25 m on each side. Table with legend gives levels for each color

band.

Organic Matter

 

 

 

 

 

OM N TP Pav Ca
% % mg/g mglhq m9/9
21.8 0.67 1.02 15.3 296
19.4 0.61 0.90 13.6 283
17.9 0.54 0.78 11.9 269
16.5 0.48 0.66 10.2 255
15.1 0.41 0.54 8.5 241
13.6 0.34 0.42 6.9 227

 

Nitrogen

 

 

 

 

 

 

 

75

Figure 3-8 continued

pH Litter Depth

IIII' IIIIIIII1
IIII
114111, 41?:lenyny
IIIIIII . I.

IIIIIII‘ In 1
1I

 

 

 

 

pH Litter N:TP N:Pav CN
Depth
cm
8.18 5.5 8.6 556 19.5
8.11 4.8 8.0 487 18.7
8.03 4.1 7.5 432 18.0
7.92 3.4 7.0 384 17.3
7.77 2.7 6.5 345 16.6
7.54 2.0 6.0 311 15.9

 

 

 

76

CHAPTER FOUR

TREE GROWTH PATTERNS IN THE SUBTROPICAL DRY FOREST OF

GUANICA, PUERTO RICO: INFLUENCE OF NUTRIENT POOLS

In Guénica Forest, Puerto Rico, previous studies have indicated that phosphorus
may be a limiting factor to tree growth (Lugo and Murphy 1986, Murphy et al. 1995). The
limestone parent material beneath the forest produces soils with high pH (7 .8) and calcium
content (52 - 260 mg/ g) Phosphorus and calcium bind together to form insoluble calcium
phosphates, removing phosphorus from the available nutrient pool. While total P in the
soils is high (0.54-0.57 mg/ g), only 1.3% is extractable (Lugo and Murphy 1986). Nutrients
in leaves have a high N:P ratio (25, Lugo and Murphy 1986), which can identify a system as
P limited (Lathwell and Grove 1986). Another indicator of P-limitation is phosphorus use
efﬁciency (PUE), deﬁned as litterfall mass divided by P content in litter. PUE in Guanica
Forest has been reported at 6057g/ g, among the highest reported value for any system, most
of which range from 800 to 4000 (V itousek 1984). Nitrogen use efﬁciency was only 98, a
median value. Retranslocation of P before leaf fall has been estimated at 65% resulting in
only 0.71 kg P/ ha returned to the forest ﬂoor in leaf litter (Lugo and Murphy 1986). This
amount is lower than any value reported for mature forests of any type in multiple reviews
on the topic (V itousek 1984, Vitousek and Sanford 1986, Jaramillo and Sanford 1995).

In spite of the evidence suggesting P-limitation, Guanica Forest soils also have
attributes that could result in limitation by nitrogen. The soils are classiﬁed as mollisols,
which tend to support large microbial communities due to high carbon content (1 8-23°/o).

Total nitrogen in Guanica Forest averages 1.0-1.1% (Lugo and Murphy 1986). Microbes

77

generally out-compete plants for nitrogen, at least in the short term (Hodge et al. 2000).
Despite having high total nitrogen in the soils, a large proportion of the N could be
sequestered in the microbial community, rendering it unavailable for plants.

Nutrient limitation in forests is typically addressed by using indirect indicators (e.g.,
leaf N :P ratios or nutrient use efﬁciency). Some lack of attention to the topic in dry forests
can be explained by the fact that water is the factor most obviously limiting forest growth.
However, most dry forests have a season when water is not limiting and soils are saturated to
ﬁeld capacity. During these times, other factors including nutrients could become limiting to
forest growth as trees experience multiple resource limitations (Chapin 1980, Chapin et al.
1986). In addition, deciduous tree species may be dormant in the dry season, requiring little
or no nutrient inputs. The goal of this study is to assess nutrient limitation in Guénica
Forest using multiple techniques — including root in-growth cores and evaluation of
correlations between tree growth and soil nutrient content.

Nutrient cycling studies have demonstrated positive feedbacks between trees and
soils. Strong feedback suggests that soil nutrient pools should be correlated with tree
growth. Low-nutrient environments are maintained by trees with slow growth, high
retranslocation of nutrients, and low litter quality, while the opposite is true for more fertile
sites (Hobbie 1992). Cuevas and Lugo (1998) documented this pattern in moist forests of
Puerto Rico. Correlative studies have implicated nutrients as controls for the distribution of
tropical plant communities. For example, Australian rain forest species were shown to be
more tolerant of aridity than low soil P (Beadle 1966). Wet areas with low fertility were
dominated by sclerophyllous and xeromorphic species more typically found in dner,
nutrient-poor zones. Also in Australia, Adam (1989) found greater species diversity at lower

P concentrations in soils. Within wet forest, Gunatilleke (1997) found that different species

78

of Sborea grew differently across gradients of N, P, and Mg. Species which grew the most
when given extra nutrients tended to be found in more fertile locations in the ﬁeld, while
species with the smallest growth response were found on the poorest soils. In Mexico, dry
forest pioneer species require higher amounts of P and light for growth and survival than
mature forest species (Huante et al. 1995b). All species grew faster with increased P, but
pioneer growth was greater than that of mature species. Seedlings showed similar responses
to N, with pioneers increasing relative growth rate more than mature species (Huante et al.
19952). In dry montane systems in Mexico, deciduous species were found on richer soils
and evergreen species on more acidic soils, but the evergreens were able to grow on richer
sites (Goldberg 1982).

Some studies have attempted to identify limiting nutrients by adding fertilizer to
large plots of forest (at least 100m2, but often larger). (See Tanner et al. 1998, for review.)
In this way, Vitousek and Farrington (1997) reported P limitation in wet forests on old soils
in Hawaii, N limitation on young soils, and co-limitation of N and P on middle aged soils.
Similarly, N limitation was demonstrated in lower montane moist forests in Jamaica and
Venezuela (Tanner et al. 1990, Tanner et al. 1992). Large-plot fertilization additions have
not been attempted in dry forests where it is impractical for a number of reasons. The
response time to fertilization amendments can be quite long. In Venezuela, moist forests
took 2.6 years to respond to fertilizer treatments in diameter growth (Tanner et al. 1992).
Response in dry forests would be slower because the lack of water results in shorter growing
seasons and slower cycling of nutrients through the system. Dry forests can be very dense
(e.g., 10,000 stems/ ha in Guanica Forest) and therefore the fate of added nutrients would be
difﬁcult to follow. Fertilizing large plots permanently alters the characteristics and history of

the site.

79

Root in-growth cores have been shown to be an effective substitute for fertilization
plots in a variety of ecosystems, at least for evaluating treatment effects. In a series of soil
types within Venezuelan wet forest, Cuevas and Medina (1988) used root in-growth cores to
demonstrate that caatinga and bana forests were N limited and tierra ﬁrme were Ca limited.
Raich et al. (1994) used in-growth cores in Hawaii and reported the same results as the large
scale fertilization experiments (V itousek and F arrington 1997). More recently, Stewart
(2000) has used root in-growth cores to repeat N limitation ﬁndings from Jamaica (Tanner et
al. 1990). Root in-growth cores are good substitutes for large scale fertilization experiments
because roots are responsible for nutrient uptake, and thus are responsive to variations in
nutrient pools in soils. In addition, in-growth cores are simple to establish and add a
minimum of artiﬁcial nutrient to the system.

The objectives of this study were to: 1) determine whether common species in
Guanica Forest were limited to certain positions along gradients in soil fertility, 2) to
determine if and which soil nutrients limited growth, and 3) to evaluate whether N or P plays

a greater role in nutrient limitation of forest growth.

METHODS
Arrodah'om‘ (fine and guard growl/J wit/J soil nutrient:

Tree growth was assessed for 481 trees in the Main site. Of these trees, 270 had
been measured beginning as early as 1981 in previous studies (Murphy and Lugo 1986b,
1990, Murphy et al. 1995) and included 27 species. In 1998, I added 205 more trees to attain
sample sizes of 2 30 individuals for six species: Amyri: elemgﬁ’m, Barrera Iimamba, Eugenia
foetz'da, Gymnantber lua'da, Pictetia am/eata, and Exorfema can’baeum. Of these species, Burrera,

Exortema, and Pictetia are considered pioneers (Molina Colon 1998), Amyri: and GJMﬂaﬂf/R’J‘

80

are mid- to late successional species occupying canopy positions while Eugeniafoetz'da is a
mid-successional subcanopy species. The added trees were single-stemmed with few
exceptions. Diam&er measurements were taken at breast height (1.4 m; dbh) using a
diameter tape. To ensure consistency of measurement location, a chain was suspended from
a nail placed 2 30 cm above breast height. The chain was marked at 5 cm intervals
bracketing breast height, so that ﬁve diameters were measured on each stem. Growth was
determined by comparing averaged diameters from each time interval. This technique has
proven able to assess small differences in growth (Murphy and Lugo 1995, Dunphy et al. in
prep). Trees were divided into size classes for analysis based on diameter: <2.5 cm, 2.5-4.9
cm, 5.0-7.4 cm, and 27.5 cm. Diameters were converted to basal area. Growth rate analyses
were based on two-year averages, from May 1998 to May 2000.

In September, 1998, Hurricane Georges passed over Guanica Forest and was
followed by a flush of sprouts (see Chapter Six). The number of sprouts that developed
below breast height on the 481 trees were counted immediately after the hurricane, at the
end of the rainy season in January 1999, and in July 2000. Sprout initiation was assessed
using January 1999 data. Sprout mortality was determined by comparing data from 2000
with that from January 1999. The length of the longest sprout on each tree was measured to
the nearest cm inJuly 2000 to assess growth. More details on these measurements can be
found in Chapter Six. Analysis of sprout data only included those from defoliated or
undamaged stems. Sprouts from broken stems were excluded because broken stems would
be more likely to coppice, coppice sprouts would receive a greater proportion of nutrients
taken up by roots, and broken stems were a small percentage (<10°/o) of the total sample.

Growth rates were compared to levels of soil organic matter, total N, total and

available Ca (Cato and Caav), total and available P (P10 and Pay), and pH. Soil was collected

81

from the top 10 cm of the rooting zone at the base of each of the trees measured for
growth. Three subsamples were collected at l-m from the trunk, approximately evenly
spaced around the tree. Samples were air—dried, sieved using 1 mm mesh, and analyzed as
described in Chapter Three. Some subsamples were not bulked prior to analysis to facilitate
geostatistical analysis of nutrient pools (Chapter Three) but their values were averaged for

analyses here.

Root I ngmwt/J Com

Three 15-meter transects were installed running east—west off of the west edge of the
Main site in Guanica Forest (Murphy and Lugo 1986b). The transects were approximately 5
m apart and ran across a gentle slope on well-drained, relatively rock-free soils near a small
draw. Sixteen root in-growth cores (four from each of three treatments and control) were
placed at l-m intervals along each of the transects.

Baskets used for root in-growth cores were based on those used in Cuevas and
Medina (1988) and constructed from cylindrical high density polyethylene mesh tubing with
4 mm2 holes. Baskets were 7 cm in diameter, 10 cm high, and enclosed with nylon mesh on
the bottom. About 33% of the area on the sides of the baskets was open.

Baskets were ﬁlled with soil taken from near the beginning of each transect. Soil was
pooled, mixed thoroughly, and sieved to remove existing ﬁne roots. In previous studies
(Cuevas and Medina 1988, Raich et al. 1994), an inert medium was used to ﬁll the baskets
(e.g., vermiculite or calcined clay). In this study, native soil was used in this experiment to
maintain the microbial community, mycorrhizal innocula, and the natural geochemistry of
the ecosystem. After preparation, the soil was divided into four equal amounts for

treatment. The four treatments were N, P, NP combined, and a control of pooled, sieved

82

soil that received no nutrient amendment N was added as NH4NO3 and P as P205 in
granular form. Nutrients were added at a rate of 40 g/m2 of N or P. Baskets were ﬁlled
with treated soil and placed into 10-cm—deep cylindrical holes so that the top of the basket
was level with the top of the mineral soil surface. Gaps between the sides of the baskets and
the sides of the holes were ﬁlled with excess treated soil. Cores were covered with forest
ﬂoor litter which was set aside while making the holes.

Root in-growth cores were installed on June 30, 2000, which corresponds to a short,
but unpredictable, dry season in Puerto Rico. After 30 days, during which no rain fell, the
cores were inspected and no roots had grown into them. The cores were subsequently
harvested on Jan 15, 2001, after the primary rainy season. One core each from the N and
NP treatments was lost.

Cores were sieved though 0.5 mm mesh to remove roots from the majority of the
soil particles. Visual inspection revealed very little root loss into the <05 m fraction,
which was subsequently analyzed to determine whether fertilization affected pH. The
remaining soil particles and roots were separated using elutiiation (Smucker et al. 1982).
Root length was determined using a line-intercept method (T ennant 1975), with the root
mixture stirred into a sucrose solution (density 1.3) to separate roots from large sand
particles that were not completely separated during elutriation. Root length is considered a
better functional estimate of plant nutrient uptake than biomass because uptake is positively
associated with length and surface area, whereas biomass increases rapidly with root

diameter, but wider roots are less active in uptake.

83

Statistics

Species distributions across nutrient gradients were compared using Kolmogorov-
Smirnov (KS) two-sample tests, which compare similarity of distributions between samples.
Correlation was used for all comparisons between soil properties and growth rates.
Correlations by species or size class were only performed if sample sizes were 220.
Correlations between nutrient content and sprout initiation were performed on species with
210 individuals, and for sprout mortality and growth 2.10 sprouting individuals were
required. Root length data were analyzed using general linear models in Systat 8.0. Each
transect was treated as a block for statistical analysis. Tukey tests were used to make

multiple comparisons of treatment means. Signiﬁcance levels for all tests were set at

a=0.05.

RESULTS
Spedespresenee across nutrient gradients

The whiskers of each soil factor’s box plot (the grey boxes in Figure 4-1) included
approximately 90% of the values deﬁning the gradient for a particular factor. The ability of
a species to establish and survive to maturity across a soil nutrient gradient was indicated
when the species' entire box plot overlapped the whiskers of the pooled data for each factor.
Using this criterion, each of the six species’ were distributed across the majority of each soil
nutﬁent and pH gradient (Figure 4-1). For example, although the majority of Exosterna
individuals were found growing in areas of low Pav, at least four were found at the upper end
of the gradient at high Pay, suggesting that Exostema was not limited from growing at either

high or low nutrient levels.

84

Differences in species distributions were apparent across all soil gradients except for
Cato. Gymnantbes was usually the species occurring at the highest median level of available
soil nutrients, while Exosterna had the lowest median values. These two species were
involved in 26 of 28 signiﬁcantly different distributions among species within soil gradients
(Figure 4—1). The three pioneer species (Bursera, Exosterna, and Pictetia) sorted out together
only along the Pav gradient, although Exosterna and Pistetz'a also occupied the two lowest

positions for N and Caav and the two highest median pH values.

Eﬂi’ets of nutrient pools on tree and #977714! gran/ti)

No signiﬁcant correlations were found between soil nutrients or pH for the entire
sample of trees or for size classes of mature trees. The growth of one species, Bursera
simamba, responded to soil nutrients when divided by size class. The 5.0-7.4-cm Barrera
stems showed increased basal area growth with higher amounts of organic matter and N (r =
0.74 and 0.76 respectively, each p < 0.001), while 2.5-4.9-cm stems showed the same trend (r
= 0.76 and 0.70, p = 0.001 and 0.003) and also responded positively to Caav (r = 0.79, p <
0.001) and negatively to Cato (r = -O.80, p < 0.001). The largest size class of Bursera stems
showed no correlation between growth rates and soil nutrients.

Soil nutrient pools were related to the initiation, growth, and survival of ﬁve species’
sprouts that developed after Hurricane Georges (Table 4-1). Sprouting in Boumrz'a suesu/enta,
Cmssopeta/urn rbamrna, Eugenia foetida, and Pietetz'a acu/eata was facilitated by higher amounts of
P, alone or in relation to N or C. Sprout initiation and mortality of Exosterna earibeaurn

responded to C:N ratios.

85

Root gmwt/J

Root length varied among transects and was affected by a signiﬁcant interaction
between N and P (Table 4-2). Added N always produced greater root length (Figure 4-2). P
increased this effect in conjunction with N, but not when added alone. Treatment did not
affect the pH of the cores after harvest. Mean speciﬁc root length (total root length/ core
volume) was 4.3 cm/cm3 for P-treated cores, 6.7 cm/cm3 for the N treatment, 7.8 cm/cm’
for the NP treatment, and 5.7 cm/cm3 for the control in-growth cores. Root lengths were
higher than reported for temperate tree species (OZ-0.4 cm/cm’, Crookshanks et al. 1998),
coffee trees (2.1 cm/cm’, Nutrnan 1934), or tropical wet forests (0.4-0.7 cm/cm’, Ostertag
1998), but less than reported for grasslands (6.6-54.8 cm/cm’, Dittmer 1938). The values
reported here appear realistic considering higher root:shoot ratios of Guanica Forest

compared to other tropical forests (Murphy and Lugo 1986a).

DISCUSSION

Despite the indirect evidence (e.g. PUE and leaf N :P) suggesting that phosphorus
supplies could be limiting to tree growth, only a few weak relationships were found between
growth and P pool sizes (Table 4-1). More species’ sprouts responded to P than other
nutrients, basal area growth of small Barsera trees responded to N, while root growth was
most stimulated by combined NP additions. Differential response to nutrients among
tropical tree species in the same community has been shown elsewhere (Huante et al. 1995a,
Huante et al. 1995b, F etcher et al. 1996, Cuevas and Lugo 1998, Lawrence 2001, 2003).
Barrera is the fastest growing tree species in the sample (Dunphy, unpublished data). That it
would have greater growth at higher soil N reﬂects the feedback between fast-growing

species and soil nutrient pools discussed by Hobbie (1992). The response to soil N pools

86

ceased in the largest size class of Bursera, perhaps as a result of increased internal stores or
the attainment of equilibrium between large trees and soil nutrients. The lack of strong
patterns in relation to nutrient gradients may also reflect interspeciﬁc niche partitioning
among species based on root characteristics. Although the majority of ﬁne root biomass was
present in the top 10 cm of soil (Murphy et al. 1995), dry forest species elsewhere have
different patterns of root distribution in time and depth (Huante et al. 1995b). At this time,
little is known about rooting characteristics of individual species in Puerto Rican dry forest.
The soil sampling methods used here would not be able to resolve differences in temporal or
spatial responses among species’ roots within the in-growth cores. The ability of each
species to differentially respond to various resources, to acquire nutrients at different times
and locations in the soil, and potentially to maintain different relationships with microbes,
would seem to be a prerequisite to maintain the diversity of tree communities of Guénica
Forest.

Both ecological and methodological factors may explain the lack of a forest-wide P
response by trees. Lugo and Murphy (1986) found that retranslocation of P accounted for
65% of the annual P demand in Guanica Forest. With such a large proportion of P budget
accounted for internally, mature trees may not respond to soil P content. On the other
hand, sprouting trees would have a higher demand for external sources of P because
defoliation, decapitation, or root breakage would reduce internal P supplies — particularly
because defoliation during the hurricane would have occurred without retranslocation
(Waide et al. 1998). In addition, apparent P limitation may reﬂect the lack of water moving
P through the soil to roots, a frequent bottleneck for nutrient transport through the soil.
While soil nutrient content may appear high, if it is not reaching the rhizosphere then plants

will be unable to take up nutrients. Thus, soil nutrient content, as opposed to flux, is at best

87

a coarse way to estimate availability for plants, even when available forms of nutrients are
measured.

Competition between plants and microbes may also reduce the sensitivity of plant
growth to P pools. Microbes tend to be limited by N supplies when C:N ratios are 20-25
(Paul and Clark 1996) but soil bacteria can immobilize N at C:N ratios as low as 12.5 (Hodge
et al. 2000). The average C:N ratio in Guanica Forest ranges from 19-29 (Chapter 3 and
Lugo and Murphy 1986). During the rainy season, when the root in-growth cores were in
the ﬁeld and microbes would have been most active, they may have sequestered a sufﬁcient
amount of N to limit root growth. Roots therefore responded to N and NP additions,
which would have lowered C:N ratios and then provided additional P for growth. Assuming
that the high PUE and N:P ratios represent a real P deﬁcit, the N limitation may only be a
seasonal phenomenon relieved when pulses of N enter the system after drying and initial
wetting of soils (Davidson et al. 1993, Srivastava 1997) at a time when ﬁne root production
is at its highest (Kummerow et al. 1990, Kavanagh and Kellman 1992). Thus, the mature
trees may be integrating long term P limitation while the in~growth cores were only
measuring short-term response. On the other hand, the root response to added N and the
high PUE and leaf N:P ratios may signify multiple resource limitation.

Mycorrhizae undoubtedly play an important role in nutrient acquisition, but little is
known about their relationships to Guanica Forest trees. Vescicular-arbuscular (VA) types
are present in the forest and are known to infect at least ﬁve tree species, including
Gymnantbes and Exosterna (Dunevitz 1985). Plants and fungi respond to different
environmental factors (Allen 1991), so it may be that nutrient limitation is indirectly
regulated in trees by the needs of mycorrhizae. Considering that the fungi are typically

limited by carbon, production of sufﬁcient carbon by photosynthesis in host trees for use by

88

the fungi may be limited by N supply in the rainy season. Since mycorrhizae are able to help
diminish the effects of drought, they may be able to stretch the amount of time that a tree
can acquire P during the year (Allen 1991). Finally, an interesting phenomenon has been
noted in alkaline soils where bacteria are responsible for solubilizing P which is then taken
up by mycorrhizae for plant use (Azcon et al. 1976). Bacteria growing with limited N
supplies would thereby limit P supplies for the plant. In this case, increasing N supplies in
the iii-growth cores would result in more P released to plants and greater root growth in N

and NP treatments.

CONCLUSIONS

All common tree species appeared to be able to grow across the entire portion of
each nutrient gradient measured in Guanica Forest. The presence of some mature
individuals of each common species, even at the lowest end of a nutrient gradient, suggested
that all species were able to survive the most extreme nutrient conditions in the forest.

Nutrient limitation of tree growth appeared to result from both N and P, either
alone or in combination, and depended on the size and species of the tree and the time of
year. Despite measurements of potential long-term responses to nutrient supplies (e.g.,
nutrient use efﬁciencies, retranslocation estimates, and N:P ratios) indicating that P might
limit tree growth, nutrient limitation affected only smaller stems and sprouts. Growth or
survival of sprouts and smaller trees responded to nutrient pool sizes, most frequently to P,
but often in relation to OM or N. Root iii-growth cores indicated the growth may be co-
limited by both N and P, but there was no strong evidence for nutrient limitation on the

diameter growth of mature trees based on nutrient pool size.

89

Table 4.1. Correlation between sprout development and soil nutrient pools or nutrient pool
ratios for ﬁve more commonly sprouting species. No correlations were found between
nutrient pools and other common species (see Chapter Two for species composition) or
between these ﬁve species and other nutrients, pH, or organic matter.

 

 

Species Sprout Nutrient r p
- stage

Boarmia succulentaJacq. growth C:P .790 .039
Cmssopeta/urn r/Jacorna Crantz initiation Total P .889 .045
mortality Total P .919 .014
Eugenia foetida Pers initiation C:P .498 .041
°/o Available P .625 .001
mortality C:P .455 .046
"/0 Available P .570 .004
N:P .473 .033
Exosterna taribaeurn initiation C:N .495 .037
(J acq.) Roem. & Schult. mortality C:N .457 .039
Pietetz'a aea/eata (V ahl) Urb. initiation °/o Available P .826 .037

growth % Available P .939 .022

90

Table 4-2: Results of ANOVA for root growth. Root length was normally distributed.

Dependent variable: Root Length
N: 46 Multiple R: 0.668 Squared multiple R: 0.446

 

Source Sum-of-Squares df Mean-Square F -ratio P
BLOCK ' 4980000 2 2490000 ' 5.000 0.012
N 9070000 1 9070000 18.199 0.000
P 29700 1 29700 0.060 0.808
N*P 2610000 1 2610000 5.241 0.027
Error 9920000 40 49 8000

91

 

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92

Figure 4-2. Box plots of treatment means for root length from in-growth cores. Dots
represent individual cores. Nitrogen increased root length (F =18.199, p<0.0005, see Table
4-2) and there was a signiﬁcant interaction with P (F = 5.241, p=0.027). Treatments with the
mac letters are signiﬁcantly different based on post-hoe Tukey tests for multiple
comparisons. Although phosphorus cores had two groups of similar values, neither group
was concentrated along a particular transect.

 

   

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93

CHAPTER FIVE

THE INFLUENCE OF HURRICANE WINDS ON CARIBBEAN DRY FOREST

STRUCTURE AND NUTRIENT POOLS

Abstract: The inﬂuence of hurricanes on the structure of seasonal tropical forests is poorly
understood because there have been few opportunities to address this issue. In 1998, we
measured the effects of Hurricane Georges after it passed over long-term research sites in
Puerto Rican dry forest. Our primary objectives were to quantify hurricane effects on forest
structure, to compare effects in a large tract of forest versus a series of nearby forest
fragments, to evaluate short-term response to hurricane disturbance in terms of mortality
and sprouting, and to assess the ability of hurricanes to maintain forest structure. For stems
with 2.5 cm minimum diameter, 1004 stems/ ha (12.4%) suffered structural damage, while
69% of the undamaged stems were at least 50% defoliated. Basal area lost to structural
damage equaled 4.0 m2/ ha (22%) in south-facing native forests. Structural damage and
defoliation increased with stem diameter and were more common in certain dry forest
species. South—facing forests and those on ridgetops incurred more damage than north-
facing forests or those comprised primarily of introduced species. Stem mortality was only
2% of all stems after 9 mo. Structural damage did not necessarily result in stem mortality.
Hurricane-induced mortality was not associated with stem height or diameter, but was ten
times greater than background mortality. Basal sprouting was proportional to the amount of
structural damage incurred in a stand. Forest fragments experienced the same patterns of

hurricane effects as the reference forest. The low, dense structure of Caribbean dry forest

94

can be maintained by hurricanes damaging larger stems and inducing basal sprouting to

generate multi-stemmed trees.

INTRODUCTION

The structure of West Indian dry forests differs markedly from those elsewhere in
the neo-tropics. Compared to tropical dry forests or seasonal forests in temperate zones,
subtropical dry forests (sensu Holdridge 1967) have fewer canopy layers, no emergent trees,
and, especially in the West Indies, have high stem densities resulting from numerous multi-
stemmed trees (Murphy and Lugo 1986b, Dunphy et al. 2000, Quigley and Platt 2003).
Differences in structure among dry forests have been attributed to climatic factors such as
low annual rainfall and high potential evapotranspiration, as well as a suite of disturbances —
including human impacts such as grazing and cutting (Murphy and Lugo 1986b, Kelly et al.
1988, Murphy et al. 1995, Gonzalez and Zak 1996, Molina Colon 1998), and natural
disturbances such as salt spray (Smith and Vankat 1992), trade winds (Lawton 1982), and
hurricanes (Lugo et al. 1983, Kelly et a1. 1988, Reilly 1991). However, the difﬁculty in
teasing apart causal factors of forest structure after the fact is illustrated by studies in the
Solomon Islands, where species composition was initially attributed to hurricane disturbance
but, after further analysis, to logging by humans (Burslem et al. 2000). Although hurricanes
are common in the subtropics and widely studied in moist and wet forests (cf. Biotropica
23(4a) 1991 and recent reviews: Everham and Brokaw 1996, Whigham et al. 1999), their
effects have been less completely studied in dry forests. In this study, we report the effects
of Hurricane Georges on dry forests in southwestern Puerto Rico.

If climate alone determined forest structure, the driest forests (based on potential

evapotranspiration) would be expected to have the least basal area and biomass. Stem

95

density may also be higher in the driest forests if basal sprouting is caused by droughts killing
terminal buds. However, in independent projects, both Murphy and Lugo (1986b) and
Quigley and Platt (2003) found that Guanica Forest, Puerto Rico, had structural
characteristics that could not be explained by climate alone. Murphy and Lugo (1990)
reviewed the structure of 12 mature tropical and subtropical dry forests across a rainfall
gradient from 603—1800 mm/ yr. Of the 12 forests, Guanica Forest had the only ﬁfth
highest temperature to precipitation ratio (2.9; T:P ratio acts as a surrogate for potential
evapotranspiration, which is seldom reported), yet it was the shortest (9 m canopy height),
with the least aboveground biomass (53 Mg/ ha), and the second lowest basal area (17.8

mz/ ha). In Guanica Forest, 42% of all trees were multi—stemmed, leading to a stem density

of 12,000 stems/ ha (Murphy & Lugo 1986). Quigley and Platt (2003) compared structural

characteristics of seasonal forests from the equator to 40°N in the Western Hemisphere and

found that forests at 20-30°N, including those in Puerto Rico, had greater stem densities and
lower basal areas than those found elsewhere. These results suggest that other factors such
as hurricane disturbance supplement the effects of drought stress in structuring dry forest.
Aside from damaging stems, hurricanes can rapidly redistribute resources and alter
community composition and function. Hurricane winds lead to canopy thinning through
the loss of leaves — transferring substantial biomass and nutrients to the forest ﬂoor. In
Hawaii, hurricane litterfall was 1.4 times greater than normal annual levels (Herbert et al.
1999). In two wet forests and a cloud forest in Puerto Rico, hurricane litterfall ranged from

1.2—1.9 times greater than normal annual litterfall (Lodge et al. 1991). In Mexican dry

forests, hurricane litterfall was about 1.3-2.0 times as much as the average of the previous

96

four years (Whigham et al. 1991). These large inputs of litter change spatial and temporal
resources availability and serve as important nutrient pulses (Lodge et al. 1994a).

Another poorly understood aspect of hurricane disturbance is its interaction with
forest fragmentation. Fragmented forests have more edge to face hurricane winds than do
larger tracts of continuous forest and might therefore be more vulnerable to damage. Only
23.2% of the dry forest area of SW PR remains forested, contained in a collection of over
600 fragments (Ramjohn 2004). Therefore, the region provides a good location to evaluate
the effects of hurricanes on forest fragments.

The main objectives of this study were to: 1) provide a description of hurricane
effects on Puerto Rican dry forest, 2) compare effects of hurricane winds in a large tract of
forest with those in nearby forest fragments, 3) measure short-term responses of trees to
hurricane winds in terms of sprouting and mortality, and 4) assess the potential of hurricanes

to maintain the unique dry forest structure of the West Indies.

MATERIALS AND METHODS

DIE SITE AND THE EVENT.—Guanica Forest is located in SW Puerto Rico (17°58’N,

65°30’W). Rainfall averages 860 mm/ yr and mean annual temperature is 25.1°C (Murphy
and Lugo 1986b). The rainy season is bimodal, split between spring rains in March-Ade
and fall rains from August to December corresponding to the hurricane season. The
amount and disttibution of rains within years and seasons is highly variable (Murphy et al.
1995). The forest canopy reaches 5 m height on south-facing slopes and ridgetops (Murphy
and Lugo 1986b), and 9 m in valleys (Molina Colon 1998). Emergents are absent and taller
trees are always found in valley areas, leading to a more uniform canopy. Considered one of

the best preserved examples of Caribbean dry forest (Ewel and Whitmore 1973), Guanica

97

Forest has been extensively studied over the last 25 years (Lugo et al. 1978, Lugo and
Murphy 1986, Murphy and Lugo 1986b, 1990, Murphy et al. 1995, Lugo et al. 1996, Molina
Colon 1998, Dunphy et al. 2000, Genet et al. 2002a, Genet et al. 2002b, Quigley and Platt
2003, Ramjohn 2004). The forest was set aside for protection in 1917 and its boundaries
expanded in the 1930’s to include all the plots within this study. Forest structure before
Hurricane Georges had been shaped by multiple factors, including human activity (Molina
Colon 1998, Lugo et al. 2002). Surrounding Guanica Forest are a collection of dry-forest
fragments that vary in land use history, size, age, and dominant tree cover (Lugo et al. 1996,
Genet et al. 2002a, Ramjohn 2004). Most fragments exist in a matrix of agriculture or
pasture but some are surrounded by residential areas.

The ﬂora of Guanica Forest provides a good basis to study regional effects of
hurricane disturbance. Of the 18 species for which we had at least 10 trees in our plots, only
one (Pictetia am/eata (V ahl) Urban) is endemic to Puerto Rico, 17 are found elsewhere in the
Caribbean, 10 in Florida, 10 in Central America, and 5 in South America.

The eye of Hunicane Georges passed over Guanica Forest on September 21-22,

1998. Sustained winds blew at 176-184 km/ h and gusted up to 240 km/ h (Bennett and
Mojica 1998), making this a Category 3 hurricane. It took about 18 hr to cross over the
forest and maximum winds lasted about 4 hr. Georges was a relatively dry hurricane
(Bennett and Mojica 1998), depositing 151 mm of rainfall, about equal to the September
average (Murphy et al. 1995).

Between 1700 and 2004, the eyes of 37 hurricanes traversed some portion of PR, a
return interval of one hurricane every 8 yr (Quiﬁones 1992). Only 15 approached the dry
forest area (Figure 1), including the last two — Hortense in 1996 and Georges in 1998 — an

average return interval of 20 yr. Not all of the 15 hurricanes affected the forest equally.

98

Historical records report that seven of the 15 hurricanes were at least category 3 in the
Guanica area, therefore most likely to inﬂuence forest structure. Thus, strong hurricanes
have an average return interval of 43 yr. Hortense was a category 1 hurricane (Safﬁr-
Simpson Index) with less than 100 mm of rainfall in the Guanica area (Bennett 1996) and
resulted in very little damage to the forest (AE Lugo & M Canals Mora, pers. obs.). Prior to
Georges, the structure of Guanica Forest was probably last affected by Hurricane San Felipe

in 1928.

PLOTS AND TERMINOLOGY USED IN THIS STUDY.-——We compiled data for this study from a
variety of different plots established prior to September 1998 for other research projects.
Following the hurricane, we pooled all available data to provide a more comprehensive
explanation of hurricane effects than would have been possible otherwise. We measured
hurricane effects in 33 experimental plots in Guanica Forest (Figure 2). These plots were
located in semi-deciduous forest (Murphy and Lugo 1986b, Molina ColOn 1998) but differed
in size, time studied, and land-use history (Table 1). Twenty-eight of the plots were
established before the hurricane to study long-term forest growth, structure, and
regeneration (Lugo and Murphy 1986, Murphy and Lugo 1986b, Murphy et aL 1995, Molina
ColOn 1998). Following the hurricane, we established one plot in each of three old Swietem'a
mabagonijacq. plantations and two new plots on ridges after extensive ﬁeld surveys revealed
that ridges received the greatest damage. Total area sampled was 1.3 ha spread across an
area of 3162 ha in the eastern portion of Guanica Forest. However, much more of the
forest was inspected as we conducted ﬁeld surveys, leading us to conclude that our results

were representative of the forest as a whole.

99

We also sampled hurricane effects in 19 forest fragments within 31 km of Guanica
Forest (Figure 2) (Genet et al. 2002a, Genet et al. 2002b, Ramjohn 2004). Fragments ranged
in size from 001-756 ha and had species assemblages comparable to the native forest plots.
The fragments faced various directions and occurred over the same elevation range as
Guénica Forest. Hurricane effects were measured along 2-m wide transects, the lengths of
which varied by fragment size. Transects started on the north and south edges of fragments
and ran toward the center. Total area sampled in the 19 fragments was 0.68 ha.

Land-use history of Guanica Forest resulted in two types of forest: 1) those
dominated by native species, and 2) those that consisted primarily of naturalized species (i.e.,
Dilemma leucocep/Jala (Lam) deWitt and Pmrqpirja/zjflora (SW.) DC.). We refer to these types of
forest as “native forest” and “Leucaena forest” (Table 1). Leucaena forest plots had been
used for a baseball ﬁeld, agriculture, and housing sites until about 65 years ago (Molina
ColOn 1998). Native forest plots either had no signs of human disturbance or some selective
cutting prior to the 19305 for subsistence charcoal production (Murphy and Lugo 1986b,
Molina ColOn 1998). The native forest plots on the north side of Guanica Forest occurred
in the lee of hurricane winds, while those on the south side faced Georges’ strongest winds
(Bennett and Mojica 1998). Thus, we use “native-north” and “native-south” to highlight the
inﬂuence of aspect on hurricane effects.

Since many trees were multi-stemmed, we use “tree” to refer to single-trunked
individuals and entire clumps. When discussing individual trunks, regardless of whether
growing singly or clumped, we use “stem.” Thus, there will be more stems than trees at each

site. Effects were seldom uniform among stems in a clump.

100

STEM MEASUREMENTS FOR FOREST STRUCTURE—Within each plot, we tagged all stems 22.5
cm diameter at breast height (DBH). Species identiﬁcations were based on Little and
Wadsworth (1964) and Little et al. (1974). Stem height and DBH were measured on all trees
between June and September 1998. Height was measured to the nearest 0.25 m using a
telescoping pole. DBH was measured at 1.3 or 1.4 m depending on who established the
plot (Murphy & Lugo 1986, Molina ColOn 1998). In the fragments, we measured the height

and DBH of damaged (but living) and hurricane-killed stems only.

ASSESSMENT OF EFFECTS—We assessed effects on each tagged stem in the native-south
forest plots and in two of the three mahogany plots within 10 days of the storm.
Assessment of other plots and fragments was completed by February, 1999. Hurricane
impacts on stems were divided into six categories: uprooted, snapped, large branches
broken, leaning, defoliated only, and no visible effect. The ﬁrst four categories result in

severe structural damage to a stem and are collectively referred to as such. “Large branches
broken” indicates that 225% of the secondary or tertiary branches were snapped off. For
our purposes, secondary branches had diameters 2 50% of DBH and tertiary branches had a

diameters 25-50% of DBH. Branch loss was not evaluated for the native-north or Leucaena
plots, precluding their inclusion in some of our analyses. Leaning stems were bent to an
angle >30° from vertical at some point along the trunk, but lacked signs of uprooting or
breakage. We compared the direction of fall for snapped, uprooted and leaning stems to the
direction of the strongest winds based on meteorological reports (Bennett and Mojica 1998).
We estimated defoliation visually for each tree using six classes: 100% (no leaves at
all), 95% (one to a few leaves remaining), 75%, 50%, 25% and 0% (all leaves present). New

leaf growth prevented assessment of defoliation in plots sampled after late-November 1998

101

and in all fragments. Thus, analyses of defoliation patterns were restricted to the native-

south plots and two mahogany plots.

LI'I’I’ERFALL.—We collected litterfall in thirty 50 x 70 cm wire baskets haphazardly placed in
the 1.44 ha native-south forest plot. We emptied the baskets the day before the hurricane
and on September 26, 1998 — four days after the hurricane. We checked baskets again in
early October, but <1 g of new litterfall was present in any basket, suggesting that all litter
had fallen out of the canopy by Sept. 26. Thus, we considered the litterfall samples to have
been created during the 18 hours it took the hurricane to traverse the site.

We also collected standing litter on the forest ﬂoor 12 d after the hurricane in the
1.44-ha native-south plot. A 15 x 15 cm template was randomly located in the vicinity of the
litter baskets (N = 26). All material within this area was collected and sorted into four
categories: leaves, brown wood, green wood, and miscellaneous. We distinguished brown
wood from green wood based on ﬂexibility. By the twelfth day, green and brown leaves
could not be distinguished. Leaves included all leaf parts, and wood included stems,
branches and woody vines. The miscellaneous category included any material that did not ﬁt
into other categories, including reproductive parts and small fragments of leaves or wood.

Nutrient stocks in standing litter and litterfall are expressed here on a content basis
(kg/ ha). Tissues were dried at 65°C to a constant weight and ground in a Wiley mill (18
mesh) before analysis. Ground samples were digested with H202 and concentrated HNO3
(Luh Huang and Schulte 1985), and concentrations of P, K, Ca, and Mg were determined on
a Beckman Spectra Span V plasma emission spectrometer. Because forest ﬂoor samples
often harbor soil particles, we express all standing litter mass values on an ash-free basis.

Forest ﬂoor nutrients were analyzed using bulked samples (N = 6), except for green wood,

102

which was not present in all samples (N = 4). Forest ﬂoor N was determined using
duplicate samples in a CE Instruments NC2100 analyzer. Litterfall N was determined on

duplicate samples using a LECO CNS 2000 analyzer.

SHORT-TERM RESPONSE—We determined mortality for stems with DBH 22.5 cm. Stems
were considered dead if they had no leaves, no sprouts, and dried bark as of June 1999 (9
months post-hurricane) when the plots were resampled. Multi-stemmed trees were
considered dead only if all stems were dead. Mortality was not assigned to mode of damage
in the native—north or Leucaena forests. Mahogany plots were not revisited, so mortality was
not assessed there.

We recorded sprouting from roots and trunks below breast height to evaluate the
potential for hurricanes to generate multi-stemmed trees. We counted sprouts on each of
the living, tagged stems in the native-south and ridgetop plots in September or November
1998 to determine the number of sprouts existing before the hurricane. In June 1999, we
counted new sprouts and noted their point of origin on the stem. New sprouts were
distinguished from old sprouts by bark coloration and ligniﬁcation. Summary data are
presented here. Patterns of sprout survival after two years were reported elsewhere (Van

Bloem et al. 2003).

STATISTICAL ANALYSES—Plots were pooled by forest type. Categorical data (height, DBH,
damage type) were analyzed using x2 statistics. Categories were pooled when sample sizes
were too small to produce valid X25 — these instances are noted in the results. For analysis of

species effects, we only included species that had 225 individuals in our samples. We used a

103

null hypothesis of equal damage or mortality across all categories (locations, stands, or stem
size).
We used regression to compare snap heights to stem diameter, sprouting rates to

structural damage rates, and rate of structural damage to wood density (reported for species
we examined in Molina Colén 1998). For all tests, 0L: 0.05 and we veriﬁed normal

distribution of data sets with Kolmogorov-Smirnov tests.

RESULTS

FOREST-WIDE EFFECTS—In Guanica Forest as a whole, structural damage was present on
12.4% of stems (1004 stems / ha) as a result of Hurricane Georges. Both hurricane winds
and falling limbs or stems caused structural damage to stems. Details of stem damage are
below. The median rate of defoliation was 50%. Overall, 74.6% of stems were at least 25%
defoliated and 69% were at least 50% defoliated. New leaves began to appear within two
weeks for many species, particularly Como/012a divernﬁ/ia Jacq., Baun'm'a yucca/cum Jacq., Pirom'a

albida (Heirnerl) Britton, Guettarda kmgz'z' Urban, and Pictetz'a amleata.

EFFECTS BY FOREST TYPE—Severity of defoliation and stem damage varied by forest type
and topographic setting (Figure 3). Structural damage was greatest on ridgetops (20%).
Native-north forest, in the lee of the strongest winds, had the highest percentage of stems
without visible hurricane effects and the lowest amount of structural damage (Figure 3). The
basal area of stems suffering structural damage was 4.0 m2/ ha in native-south plots and 3.5
m2/ ha in ridgetops, 22% and 19%, respectively, of total live pre-hurricane basal area.
Ridgetops lost less basal area than native-south forests because the average stem diameter in

ridgetops was lower before the storm. The mode of structural damage varied by forest type

104

and topography (Figure 4). Ridgetops generally had higher rates of each mode of structural
damage than other forest stands, with the exception of snapping, which affected the greatest
number of stems in native-south forests. Although having low damage overall, Leucaena

forest had the highest proportion of snapped stems.

HURRICANE EFFECTS BY STEM SIZE—Throughout the dry forest region of Puerto Rico,
stems in all height and DBH classes sustained structural damage and the size classes with the
most stems (3 to 6 m in height and 2.50 to 4.99 cm in DBH, Murphy and Lugo 1986b) had
the greatest number of stems damaged. Proportionally, stem damage increased with stem
diameter in native-south forest (x2 = 26.60; 4 df; P < 0.0005; diameter classes >12.5 cm
pooled), but not in native-north or Leucaena forests (Figure 5a). Native-north forests had
the least damage of all forest types in all diameter classes. In plots where all modes of
damage were measured (i.e., native—south, ridgetops, and mahogany plantations), stems 27.5
cm DBH incurred proportionally more damage than smaller stems (Figure 5b), but damage
was not related to stem height (Figure 5b). Unlike other studies (Putz et al. 1983), no
relationship existed between damage and heightzdiameter ratios.

The type of damage was related to stem size (Figure 5b). Both taller and wider stems
were more likely to have broken branches while shorter, thinner stems more often leaned.
Snap height was not related to stem diameter (r2 = 0.03). Stems that were poorly rooted or
damaged at or near root level before the hurricane were nearly always snapped or uprooted
after the hurricane. Taller, wider stems were also more likely than short, narrow stems to be

defoliated (x2 for height = 70.432; 5 df; P < 0.0001; height classes 27 m pooled; X2 for DBH

= 31.475; 3 df; P = 0.0076; 2 10 cm DBH classes pooled). The strongest hurricane winds

105

came from the southeast (Bennett and Mojica 1998) resulting in northwesterly fall directions
of stems in Guanica Forest and fragments (Figure 6).

Surveys in fragments included only damaged stems along a transect, so proportional
damage could not be assessed among size classes. However, patterns of stem damage in
fragments and Guanica Forest were similar. Total density of damage was 703 stems/ ha in
fragments and 1004 stems / ha in Guanica Forest. The proportion of damaged stems in the

2.5 to 4.9 cm DBH class differed by only 8% between the fragments and Guanica Forest

(52-60%, respectively) and by 55% in all other size classes.

SPECIES EFFECTS—Rates of both defoliation and structural damage differed by tree species.
However, defoliation rates were not related to functional traits such as successional status or
leaf phenology (Table 2). Pioneers accounted for 80% of species with above-average stem
damage rates (Table 2). As in other studies of hurricane effects (Putz et al. 1983,
Zimmerman et al. 1994, Asner and Goldstein 1997), no relationship existed between wood

density and structural damage.

LI'I'I’ER AND NUTRIENTS—Total litterfall averaged 7.5 Mg/ ha during the 18 h period of
Hurricane Georges or 1.6 times the annual rate reported by Lugo and Murphy (1986).
Compared to non-hurricane years, the litterfall pulse was 499 times average daily September
litterfall and 17 times the average September monthly rate (Murphy et al. 1995). Leaf
litterfall totaled 55% of annual estimates for the semi-deciduous Guanica Forest,
corresponding to the median 50% defoliation estimate. Wood litterfall from Hurricane
Georges was >11 times than measured for the year 1981. In October 1998, leaves

comprised 46%, and wood 33%, of the total standing litter mass (Table 3). Post hurricane

106

wood litter stocks more than doubled those found in 1981, a non-hurricane year (Lugo and
Murphy 1986).

Nutrient content (kg/ ha) of standing litter and litterfall immediately after Hurricane
Georges exceeded that measured in 1981, primarily due to wood (Table 3). Hurricane leaf
litterfall deposited 100% of annual N and 170% P, despite equaling only 55% of annual leaf
litterfall. Wood litterfall contained 9.6 times the amount of N and 13.8 times the amount of
P deposited in a non-hurricane year (Table 3). Total N, P, and K stocks on the forest ﬂoor
after the hurricane were 71%—320% higher than in 1981 (I' able 3). The total standing stocks
of Ca (930 kg/ ha) and Mg (37.7 kg/ ha) after the hurricane were each 5 times greater than
hurricane litterfall inputs. Ca and Mg stocks in 1998 were 47% and 8% of stocks found in
the top 5 cm of soil in 1981 (forest ﬂoor Ca and Mg were not measured at that time, Lugo

and Murphy 1986).

SHORT-TERM RESPONSE—After nine months, mortality ranged from 1.3—2.2% for trees,

and 0.7—7.4% for stems (Table 4). Total tree and stem mortality averaged 1.7% and 2.0%,
respectively. There were no species effects, nor was mortality related to stem DBH or
height classes (T able 5). The dead stems in ridgetop and native-south plots included 40% of
the snapped stems, 21% of uprooted stems, 4.5% with large branches broken, 8.5% that
were at least 95% defoliated, and 1.5% of stems incurring less defoliation. No stems that
leaned or lacked visible effects died. Thus, the seventy of damage increased the odds of
mortality, but not all damaged stems died because many of them resprouted from stumps or
roots.

New sprouts appeared below breast height on 29—63% of stems across Guanica

Forest (Figure 7), far outnumbering the pre-hurricane sprouting rate of 3.5%. Stems on

107

ridgetops sprouted most. The proportion of stems sprouting correlated with the proportion
having structural damage (r = 0.94; P = 0.017), but even undamaged stems without signs of
defoliation sprouted at eight times the pre—hurricane rate (Van Bloem et al. 2003). In
addition to the sprouts measured, many stems also sprouted above breast height. These
higher sprouts would not contribute to increased stem density, basal area, or multi-stemmed
growth forms common to Guanica Forest, but would ﬁll in the small canopy gaps opened by

the hurricane.

DISCUSSION

The effects of Hurricane Georges suggest that hurricane disturbance can be an
important force in creating and maintaining the structure of West Indian dry forests. The
hurricane reduced the number of large-diameter stems in windward sites by snapping or
uprooting but without necessarily causing mortality of these trees due to subsequent
resprouting. Low mortality and abundant sprouting would, over time, lead to increased stem

density and multi-stemmed trees without changing species composition (Van Bloem 2004).

HURRICANE EFFECTS ON GUANICA FOREST IN CONTEXT OF PREVIOUS STUDIES.—
Hurricane effects have been studied in nine tropical and subtropical dry forests, including
this study, but comparing hurricane effects from different storms or forests is difﬁcult
because the combined effects of storm intensity and duration cannot be easily standardized.
However, Everham and Brokaw (1996) and Whigham at al (1999) reviewed the effects of
catastrophic winds on various temperate and tropical forests, providing a context into which

our results can be placed.

108

In general, mortality and damage were low in dry forests (Table 6). Guanica Forest
(12.4%) was near the middle of the range (7 -32%) in stem damage, but lost the most basal
area (21%). As suggested by Whigham et al. (1999), mortality and basal area loss were lower
in dry forests than in wet forests, as was structural damage, with the exception of the S.
Florida site (T able 6).

Guanica Forest incurred disproportionate damage to larger-diameter stems — a

general trend for dry forests hit by category 3 or stronger hurricanes. Hurricanes affected
larger diameter trees in Jamaica (Wunderle et al. 1992), St. John (Reilly 1991), and Sri Lanka
(Dittus 1985). In Guadalupe, stems of 7.5-15 cm DBH (compared to average stand DBH
of 7 cm) were most affected while those >15 cm were less affected. Everham and Brokaw
(1996) proposed a unimodal pattern of damage relative to stem diameter with the most
damage in intermediate-size stems. This was not the trend in dry forests but large-diameter
stems can be quite rare in these forests. For example, our samples included only 86 stems
larger than 15 cm DBH, and only 26 stems >20 cm. Therefore, dry forests may represent
only the increasing part of the curve.

In Guanica Forest, stem size inﬂuenced the mode of damage incurred (Figure 5b).
Tall, wide-diameter stems would be most exposed to hurricane winds, but potentially the
best anchored. Branch loss on these stems would reduce wind resistance before snapping or
uprooting occurred (V ogel 1994). Uprooting was absent in larger stems, suggesting that
their root systems were strong enough to withstand winds. Leaning stems were most
common in small size classes because thin, ﬂexible stems bent without breaking. Only the
distribution of snapped stems across diameter classes followed the unimodal pattern
predicted by Everham and Brokaw (1996). F all—direction patterns indicated that the

strongest hurricane winds created the most damage (Figure 6), a commonly observed pattern

109

(Boose et al. 1994). The greater variability of fall directions in the forest fragments reﬂects
their position in relation to the trajectory of the storm and the mitigating effects of
topography.

As in other forests, aspect and forest type inﬂuenced damage severity (Everham and
Brokaw 1996). Native-north forest incurred substantially less damage than native-south
stands. The low damage rates in mahogany plantations and Leucaena forests can be
attributed to a combination of factors. First, dominance by trees of a single species and age
leads to a continuous canopy resistant to wind. Second, the mahogany plantations were in
valleys and the Leucaena forests were on ﬂat land and therefore relatively sheltered. Neither
introduced forest type was found on ridges or south facing slopes and it was therefore

impossible to determine whether their lower damage rates were due to topography or forest

type.

RESISTANCE, RESILIENCE AND THE POTENTIAL EFFECTS OF NUTRIENTS—Guanica Forest
contained species that exhibited either resistance (displayed by low rates of damage) or
resilience (low mortality and high sprouting) to hurricane winds, which resulted in only
minor changes in species composition. Resistance was increased by the prevalence of multi-
stemmed trees because the likelihood of mortality was lower and wind-speed effects on any
one stem in a clump were reduced (V ogel 1994). Resistance may also be related to nutrient
supply (DeAngelis et al. 1989). Following a hurricane in Hawaii, trees in nutrient-limited
moist forests resisted damage, breaking less than those in fertilized plots. Conversely,
fertilized trees responded with higher post-hurricane growth rates and productivity (Herbert
et al. 1999). Similarly, Guanica Forest’s structural resistance may be related to water or

phosphorus limitation, both of which are in short supply (Lugo and Murphy 1986). Trees in

110

resource-limited environments tend to invest high amounts of carbon into physical structure
built for strength and longevity (Chapin 1980).

Unable to undergo retranslocation, hurricane leaf litter provided a nutrient pulse to
the forest ﬂoor equal to average annual inputs with two-thirds of the rainy season remaining.
Studies in wet forests have shown that pulses of dead wood resulted in short-term (< 5 yr)
immobilization of nutrients in microbial pools and decreased forest productivity
(Zimmerman et al. 1994, Scatena et al. 1996). However, dry forest soils rarely remain wet
throughout the entire rainy season and wet—dry cycles can release a signiﬁcant portion of
immobilized nutrients by plasmoptysis of microbes (Kieft et al. 1987, Lodge et al. 1994a,
Jammillo and Sanford 1995, Campo et al. 1998). Some portion of the hurricane nutrient
pulse may therefore have been available for plant uptake, aiding sprout development and

refoliation (Lugo and Murphy 1986, Comejo et al. 1994, Cuevas and Lugo 1998).

EFFECTS OF FRAGMENTATION .—Overall damage rates in forest fragments of the region
were similar to Guanica Forest. Throughout the dry forest zone, larger-diameter stems
incurred proportionally higher structural damage than smaller stems. Most fragments were
located on sites that are highly marginal for cultivation or grazing due to slope or thin, rocky
soils (Lugo et al. 1996). These sites, like ridgetops in Guanica Forest and slopes in Luquillo
Forest (Wadsworth and Englerth 1959, Basnet et al. 1992, Basnet et al. 1993, Scatena and
Lugo 1995), provided poor anchorage for trees and resulted in uprooting being the most

common type of structural damage in fragments.

SHORT—TERM RESPONSE—Whereas hurricane disturbance resulted in >20% stem

mortality in moist or wet tropical forests (Everham and Brokaw 1996), mortality was low in

111

Guanica and other dry forests (Table 6). Catastrophic stem mortality (CSM: mortality
resulting directly from a disturbance) was only 2% after 9 months for stems of 22.5 cm
DBH. Mortality was unrelated to stem size, but this was not surprising considering that
larger stems have root systems able to support a ﬂush of new sprouts. The 2% mortality
rate would lead to an average loss of 240 stems / ha and 0.4 m2/ ha basal area (Murphy and
Lugo 1986b). We estimated CSM because delayed mortality can continue for at least 4 yr
after a hurricane (Dittus 1985, Lugo and Scatena 1996) as heavily damaged or defoliated
stems may die as a result of subsequent stresses such as seasonal or more prolonged
droughts (Lugo and Waide 1993, Walker 1995). Although hurricane mortality in stems did
not show an association with size class, if delayed mortality caused by CSM is related to
structural damage or to degree of defoliation, then larger stems may eventually die in higher
proportions.

Over time, however, it is unlikely that CSM will impact as many total stems as
background stem mortality (BSM: mortality due to senescence or competition). BSM in
Guanica Forest has been calculated at 0.3% yr’1 (PG Murphy unpub data). Although CSM
from Hurricane Georges was nearly seven times greater than BSM, a hurricane as strong as
Georges would have to cross the forest once every ten years to kill the same the number of
stems, or twice as often as has historically occurred (Salivia 1972, Quiﬁones 1992, Miner-S015.
1996).

Whigham et al. (1999) predicted that sprouting would be an important response in
dry forests, particularly when mortath and damage rates were low. Furthermore, they
predicted that sprouting would be greater on damaged stems and that the sprouting response
would result in minimal changes in species composition of the forest. The prevalence of

sprouting following Hurricane Georges (Figure 7) largely followed these predictions except

112

that sprouting occurred regardless of mode or severity of structural damage, even on
undamaged stems (Van Bloem et al. 2003). Survival of sprouts would generate multi-
stemmed trees and result in the dense, clumped growth form of West Indian dry forest.
Although the cohort of new sprouts experienced some mortality, 88% survived two years
after the hurricane (Van Bloem et al. 2003) and, in some cases, sprout growth exceeded 2 m
in height. With a forest-wide sprouting rate of 33%, it would take only two hurricanes per
tree generation to achieve the current proportion of multi-stemmed trees (42%), assuming
sprouting effects were roughly additive, or a single hurricane in heavily impacted areas, such
as the ridgetops (Figure 7). Based on typical growth rates (Murphy et al 1995), and the size
of some stems in multi-stemmed trees, it appears that many stems could have arisen as a
response to a hurricane in 1928 (Figure 1). Although we recognize that alternative
explanations exist (cg. cutting and drought), our observations support hurricane disturbance
as a plausible explanation for the maintenance of high stem densities seen in Guanica Forest

and throughout dry forests of the West Indies.

Whigham et al. (1999) noted that “there are few examples where it has been shown
that the structure and dynamics of the forest are strongly inﬂuenced by periodic hurncane
events as much or more than by background canopy gaps.” Dry forests of the West Indies
may be an exception. As demonstrated in Guanica Forest, hurricanes disproportionately
damaged larger stems and promoted sprouting at or near the base of trees, even on
undamaged stems. Damage rates were primarily determined by stem diameter and
topographic exposure to wind. Damaged stems did not necessarily die. Sprouting
minimized mortality and changes in species composition, and increased the potential to add

new stems to the forest. Post-hurricane mortality rates were elevated over background

113

mortality, but would affect fewer stems over time. A collection of forest fragments incurred
the same rate and type of structural damage as Guanica Forest, suggesting that the spatial
extent of a forest stand did not inﬂuence hurricane effects. The effects of Hurricane
Georges on the structure of Guanica Forest were comparable to other cases of hurricane
disturbance in dry forests, but were less than those reported for most wet tropical forests.
Climate characteristics alone fail to explain dry forest structure in the West Indies and, as
hurricanes are common in the region (N eumann et al. 1993), we conclude that the unique

West Indian dry forest structure arises at least in part from recurring hurricane disturbance.

114

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Table 5-2. Hurricane effects on representative tree species in Guanica Forest. Defoliation
was assessed in native-south forests and mahogany plantations within two weeks for species
with 225 total trees. Median defoliation rate was 50%. Damage was assessed in all forest
types for species with 225 total stems. Average damage rate was 12.4%. Designation of
species as evergreen, deciduous, and pioneer from Little and Wadsworth (1964), Little et al.
(1974), and Molina Colon (1998).

 

 

 

Successional Percent 250%
Species status Total trees Vdefoliated Leaf habit
Defoliated trees
Guettarda kmgii 42 91 deciduous
Barrera Jimamba pioneer 65 86 deciduous
ngz'odendmnfemum 25 84 evergreen
Coccoloba diwmfo/ia 83 83 evergreen
Exortema caribaeum pioneer 9O 78 deciduous
Pictetia am/eata pioneer 97 75 deciduous
Anya)“ elemiﬁra 1 15 73 evergreen
Eugenia foetz'da 94 73 evergreen
Sudetem'a mabagam' 37 51 deciduous
Gjmnant/m ludda 257 43 evergreen
Damaged stems Total stems Percent damaged
Pilosocmm' mjcnz'z' pioneer 47 V 63.8
Egytbrwgr/um mtundzfo/z'um 35 37.1
Bursera .rz'mamba pioneer 1 13 30.1
Pixom'a albida pioneer 52 25.0
Eritbalixfmticom pioneer 37 21.6
Eugeniafoetida 1 84 12.5
Exoxtema caribaeum pioneer 130 12.3
Mgiodmdmnﬁmwm 39 10.2
Amyri: elem' cm 204 10.1
Bomrm'a mam/mm pioneer 54 9.3
Budda bumw 65 9.2
.S'ndetenia mabagam' 54 7.4
Tbota'nia poﬁoricemis 148 7.4
Gymnant/Je: lucida 452 7.1
mesopetalum rbacoma 30 6.7
Coma/aka diwruﬁ/z'a 320 6.3
C arm/01m microxtacbja 190 5. 8
Cuettarda kmgii 187 5.3
Pictetia am/eata 218 2.8
Pitbecel/obium unguiJ-mti pioneer 44 2.3
Tabebuia betemp/le/a 138 1.1
Eugenia xemp/pltica 55 0.0

116

Table 5-3. Biomass and nutrient content of litterfall and standing litter in the 1.44-ha native-
south forest plot. Mass values of standing litter are expressed as means (standard errors) and
are corrected for ash-free dry mass.

Component Dry mass N Ca P K Mg
g/m2 ------------ kg/ ha -----------
October 1998 Standing Litter 8‘

Leaves 845 (126) 160 370 3.8 39.5 19.6

Brown wood 573 (65) 69 195 1.4 18.8 5.0

Green wood 30 (16) 3 7 0.1 1.5 0.4

Misc.” 356 (38) 92 358 2.3 21.7 12.7

Total 1833 (148) 324 930 7.6 81.5 37.7

July 1981 Standing Litter 3' °

Leaves 1033 (56) 165 3.7 17.0

Wood 244 (1) d 24 0.5 2.3

Total 1277 (56) 189 4.2 19.3
September 1998 Litterfall

Leaves 238.7 43.8 44.4 1.2 17.5 4.5

Wood 509.5 40.3 140.7 1.1 21.0 3.1
1981-82 Annual Litterfallc

Leaves 433.7 44.3 0.7 35

Wood 45.6 4.2 0.08 1.0

a N=26. t’Miscellaneous category includes small leaf fragments, fruits, and ﬂowers. cJuly
1981 standing litter and 1981-82 leaf litter values from Lugo and Murphy 1986; N = 30,

missing nutrient values were not reported therein. dCalculated from data reported in Murphy
and Lugo (1986) and Lugo and Murphy (1986).

117

Table 5-4. Hurricane-related mortality of trees and stems 2.2.5 cm DBH in four types of
forest in Guanica Forest 9 mo after Hurricane Georges.

 

Site Mortality %a Total Trees Total Stems Area sampled
Trees a Stems a live and dead live and dead (m2)

Native-South 1.6 b 2.7 850 ‘ 1886 2490

N ative-North 2.2 1.6 836 1223 4000

Ridgetops 2.0 7.4 102 162 200

Leucaena 1.3 0.7 853 1 172 6000

Total 1.7 2.0 2641 4443 12690

aThere were no signiﬁcant differences in tree mortality among sites (x2 = 2.262; P = 0.45; 3
df). Stem mortality differed among sites (X2 = 36.664; P < 0.0005; 3 df).

b Tree mortality reported here is only for the two 1.0—ha sites in native-south stands
(sampled area was 1800 m2) because multi-stemmed trees in the 1.44-ha native-south site
were not assessed for mortality. Stem mortality includes all native south stands.

118

Table 5-5. Percent stem mortality by size class for height and DBH for all stems in native-
north, native-south, ridgetop, and Leucaena plots. Mortality was not assessed in mahogany
plantations.

Height (m) 33.9 44.9 5-5.9 6-6.9 7-7.9 8-8.9 29,0 Total
Total stems 447 865 843 738 364 196 213 3690“
% Mortality 2.7 2.5 3.2 2.0 1.4 1.0 1.9 2.0

DBH (cm) 2.5-4.9 5.0-7.4 7.5-9.9 10.0-12.4 12.5-14.9 215,0 Total

Total stems 2192 1482 464 153 64 86 4441a
°/o Mortality 2.4 1.8 1.3 1.3 1.6 1.2 2.0
aTotals for height and DBH are not equal because heights were not measured on all live

stems. Mortality was not associated with size class. For height: x2 = 6.165; P = 0.19; 01 =

0.05; 4 df; 7 to 9 m height classes pooled. For DBH: X2 = 4.021; P = 0.13; (X = 0.05; 2 df;
7.5 to 15 cm DBH classes pooled.

119

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120

Figure 5—1. Hurricane tracks with year of occurrence of the 15 storms most likely to have
affected Guanica Forest Hurricane Georges is the thickest line across the center. Bolded
years are hurricanes likely to have had the strongest effects on Guanica Forest. Solid lines
are known hurricane tracks. Dashed lines are best—estimate trajectories based on Salivia
(1972), Neuman at al. (1993), and Miner-Sole: (1996). Hortense was a low-level storm that,
according to local reports, had little impact on the forest. Luquillo Forest and Hurricane

Hugo included for reference.

 

 

Hugo 1989
1899, 1928 N 391
1867
i _ 1738, 1772
‘
w m “"1738,1876
<—
\ Q I \ ~ ‘
‘___ ___,, \ \ xgeonoeswss
1896 \ \
mans... 1780, 1816
NM“ 1901, 1926
~160 km

121

FIGURE 5-2. Locations of study plots in Guanica Forest and nearby fragments (inset) in
southwestern Puerto Rico. Forest types indicated by symbols in legend. Numbers next to

symbols denote multiple plots of a type in the area.

Southwestern Puerto Rico 66°50’W F = Fragments
I

N = Native North

0 S = Native South
18 N L = Leucaena
R = Ridgetops
M = Mahogany

 

      
 
 
  
   
   
 
   
  

    

- Cabo Rojo . Yauco F

 

v Paved road

Nonh

Guanica Forest (Eastern Portion)

  

Private
Land

1 km Caribbean Sea 66°50,

122

FIGURE 5-3. Hurricane effects on stems for different forest types within Guanica Forest,
Puerto Rico. Structural damage includes uprooting, snapping, breakage of large branches, or
leaning. “Undetermined” refers to stems that lacked structural damage but were sampled
after signiﬁcant refoliation had occurred. Most of the stems in this category probably had
been defoliated. Numbers below forest type labels indicate the total number of stems

sampled in each forest type. “All forests” is pooled data for the ﬁve forest types.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

7 Structural >259. Defoliated ; No Visible Undetermined
% Damage '~ Damage ﬂ
Mature native forest Introduced Pooled
1 00 forest types
75 F—
.S. i"
9 50-
o
n.
25-
o ,8 - 1- ,8 _I_
Native Native Ridgetops Mahogany Leucaena All Forests
North SOUth 162 Plantation Forest 2915
868 1886 126 867
Forest Type

123

FIGURE 5-4. Stern density of various modes of structural damage in different stands of

Puerto Rico dry forest. Sample included all stems 2 2.5 cm DBH. Numbers below forest

type labels indicate total stem density of each forest type. *Branch loss not estimated for

native—north or Leucaena sites, structural damage densities are therefore underestimated.

Stems per hectare

 

 

 

 

 

Mature native forest Introduced
1 800 forest types
1 500 . D Branch loss
1200_ DSnapped
ES Uprooted
9oo~ 83 Leaned
600‘
3001 , m . .
o m g , . ..... . m
Native Native Ridgetops Fragments Mahogany Leucaena
North South 8100 5790 Plantation Forest
21 70 9354 4200 1 445

Forest Type

124

 

FIGURE 5—5. (A) Proportion of structural damage incurred by stems within diameter
classes for three forest types in Guanica Forest. Broken branches not assessed in native-
north or Leucaena forests. (B) Stems incurring various modes of structural damage as a
proportion of all stems in each diameter or height class. Data included stems only from
native—south, mahogany, and ridgetop sites because broken branches were not assessed for

native-north or Leucaena forest.

 

A 40

 

 

 

 

 

 

 

 

 

 

Native m- Native North Leucaena
8 South 1,11,}
59 o , ”“17:
O C) 30 7 :‘ ”ii“
0 cu . M,
.g g “”11””
_ ‘i
E 3 ’“liu:
in 9 "'lm
g 3 20 - '1‘ .1" ‘
.. o {Iii-1. .Q.
3 g 1 film '1-
° 0’ _ '. ' .3,
E .c ’1 {will
o 3" _ ”it “ . '
0 g 10 '. mil .1 .“ii
g5 will!" .‘ I. if
iii: . . ‘ ”it. 5’“
{mil 'liir ‘ "I
0 ‘11. . 1 .“"l '1‘ 1, ’1 . z.
+ a) V; a) V: O; + a) <- 0) V: 02 +
E;- 51 'T C? N 8 S; 9." rr' °.> N 5* °-
v- Ln O_ l!) g E .- 112 o to g E 59
N in l\ o' - N in N 2- 93

m

 

 

Diameteﬁcﬁ)

I leaned Dsnapped uprooted I broken branches

30

 

 

20

Percent of stems in size class

0
tn V: a: <-
‘i 'T °.’ N
in q in ‘T
N I!) is 0.
2
Diameter (

 

15.00+

125

 

Height (m)

FIGURE 5-6. Stem-fall directions of snapped, uprooted, and leaning stems in Guanica
Forest and nearby forest fragments. Totals are pooled from both Guanica Forest and the
fragments. Strongest winds from Hurricane Georges came from the southeast. The radial
scale is number of stems. The direction of fall was measured for 259 fallen stems in total;

119 from Guanica Forest and 140 from fragments.

 

Total
— - Guanica Forest
- - - - Fragments

NW NE

N

 

60E

 

 

SW SE

Direction of
strongest wind

 

126

FIGURE 5-7. The relationship between sprouting and structural damage to stems in
Guanica Forest as a result of hurricane winds. Structural damage includes uprooting,
snapped stems, breakage of large branches, and leaning. Only living tagged stems were
surveyed for sprouting. Each point represents a site. All sites are located in mature native
south (S) or ridgetop (R) forests. Note that in all sites, the percentage of stems with new
sprouts exceeds the percentage of stems with structural damage reﬂecting sprouting on
defoliated and unaffected stems. Sprouting rates and structural damage rates are correlated

(r = 0.94; P = 0.017). Pre-hurricane sprouting rates were 3.5%.

S = Native South Forest R = Ridgetops

 

 

 

 

80
A
3*, 60 — R
in R
E _
.93
in 40 —
5’ S
C _
"-5: s 3
3
o 20 —
h
a.
m _.

0 I I ﬂ l

0 5 1o 15 20 25

Damaged stems (%)

127

CHAPTER SIX

Van Bloem, S. J., P. G. Murphy, and A. E. Lugo. 2003. Subtropical dry forest trees with no
apparent damage sprout following a hurricane. Tropical Eco/0g 44:137-145.

128

Tropical Ecology 44(2): 137-146, 2003 ISSN 0664-3295
0 International Society for Tropical Ecology

Subtropical dry forest trees with no apparent damage sprout
following a hurricane

SKIP J. VAN BLOEM", PETER G. MURPHY 1 & ARIEL E. LUGO2

'Department of Plant Biology, Michigan State University, East Lansing, MI 48824, U.S.A.;
”International Institute of Tropical Forestry, USDA Forest Service Ceiba 1201,
Jardin Botdnico Sur, Rio Piedms, PR 00.926, U.S.A.

Abstract: Hurricane Georges passed over mature dry forest near Guénica, Puerto Rico in ‘
September, 1998. The trees of the dense, short-statured Guanica Forest have a multi-stemmed
structure unique to the West Indies in the nee-tropics, a characteristic that has been diﬁicult to
explain. Following the hurricane, we measured sprout development below breast height on
1407 stems to assess how response to hurricane disturbance may inﬂuence dry forest structure-
Basal sprouting increased 814 fold after Hurricane Georges. Basal sprouting was found on.
almost 68% of damaged stems and, notably, on about 32% of undamaged stems. Basal
sprouting wasfound in all common species surveyed. The rate of defoliation was not related to
sprout production. Aﬁer two years, sprout mortality was only about 13%. We conclude that
continued growth of basal sprouts will contribute to high stem densities and multi-stemmed
growth forms commonly found in Guanica Forest and in the hurricane-prone West Indies.

Resumen: El huracan Georges pasd sobre el bosque maduro cerca de Guanica, Puerto
Rico, en septiembre de 1998. Los arboles del Bosque Guanica, que es dense y de bajagestatura,
poseen numerosos tallos, caracteristica que es {mica de las Indias Occidentales en el Neotrbpico
y que ha sido dificil de explicar. Después del‘ huracén', nosotros medimos el desarrollo de
rebrotes por debajo de la altura del pecho en 1407 tallos con el fin de evaluar de qué manera la
respuesta a1 disturbio del huracan puede inﬂuir sobre la estructura del basque seco. El rebrote
basal incrementé entre 8 y 14 veces después del huracan Georges. Se encontrd rebrote basal en
casi 68% de los tallos daﬂados y, de manera notable, en cerca de 32% de los tallos no daﬁados.
El rebrote basal fue observado en todas las especies comunes' examinadas. La tasa de
defoliacién no estuvo relacionada con la produccién de rebrotes. Al cabo de dos shoe, is
mortalidad de los rebrotes fue tan 8610 de alrededor de 13%. Concluimos que el crecimiento
continua de rebrotes basales contribuye a tener altas densidades de tallbs y formas de
crecimiento con multiples troncos, comunmente encontradas en el Bosque' Guénica y en general
en las Indias Occidentales, susceptibles a los huracanes.

Resumo: 0 furacéo Georges passou sobre uma floresta ,seca adults perto de Guanica,
Porto Rico em Setembro, 1998. As Arvores da ﬂoresta densa de Guanica, de baixo porte
tém uma estrutura de troncos multiplos, {mica nos neo-trépicos das Indias Ocidentais,
caracteristica esta que tem sido dificil de explicar. Depois do furacﬁo, foi medido o desen-
volvimento dos rebentos abaixo da altura do peito numa amostra de 1407 troncos para
avaliar a resposta as perturbacées e it forms como influéncia a estrutura da floresta seca.
A rebentacﬁo basal aumentou entre 8 — l4 vezes depois do furacﬁo George. Encontrou-se
rebentacﬁo basal em quase 68% dos troncos afectados e, normalmente, em cerca de 32%
dos troncos n50 afectados. A rebentacéo basal ocorreu em todas as espécies comuns

 

*Corresponding Author, Present Address: Department of Biology, PO. Box 6057, West Virginia University,
Morgan town, WV 26506, USA.

129

SPROUTING IN DRY FOREST AFTER HURRICANES

comuns amostradas. A taxa de Adesfoliacao nao estava relacionada com a producao de re-
,bentos. Apés dois anos, a mortalidade dos rebentos séatingiu cerca de 13%. Conclui-se que
o crescimento continuado dos rebentos ‘basais contribuiu para a elevada densidade de
troncos e' as formas de‘ crescimento de multiplos troncos encontrados na floresta de
Guanica e as zona das Indias Ocidentais propensa aos furacées.

Key words:

Forest structure, Guanica Forest, hurricane disturbance, Hurricane Georges, multiple

stems, multiple-stemmed, sprouting, subtropical dry forest.

Introduction

Among the environmental factors that inﬂu«
ence the structure of tropical and subtropical dry
forests are low annual rainfall and seasonal
drought. However,comparisons among dry forests
with similar climate regimes show that there are
major differences in stem density (Murphy &. Lugo
1986b, 1990). Generally, stem densities are higher
in coastal or Caribbean forests. High densities can
result from a multiple-stemmed growth habit of
trees which is prevalent in Guanica Forest, Puerto
Rico (at least 42% of trees) (Murphy & Lugo 1986b;
Ramjohn 2003) and North Andros Island, Bahmas
(Smith & Vankat 1992). Drought may be a factor
involved in generating multi-stemed trees, but
stem densities in Guanica Forest are at least twice
that found in continental dry forests (e.g.,
Chamela and Ecuador) (Josse & Balslev 1994; Lott
et al.‘ 1987). Considering the similar climates of
dry forests throughout the tropics, it seems that
the high stem' density found in Guanica Forest
must be inﬂuenced by some other factor. Multi-
stemmed trees have been documented as a re
sponse to cutting by humans, grazing or browsing
by animals, fire damage, or stem breakage by
storms (Gonzalez & Zak 1996; Kelly et al. 1988;
Molina Colén 1998; Murphy et al. 1995). Each of
these disturbance types would result in the loss of
terminal buds and wounding near the base of tree,
leading to internal changes in hormone balances
which could affect sprouting. Recent discussions of
sprouting response to disturbance suggest that
sprouting should occur on trees immediately below
the point where biomass has been lost (Bellingham
& Sparrow 2000; Bond & Midgley 2001). Thus, deo
foliated trees should sprout from leaf axils while
out trees should sprout from roots or stumps. Our
observations in Guanica Forest after Hurricane

Georges suggest that strong winds can elicit basal
sprout development without breaking stems - thus
providing a new eirplanation for the multi-
stemmed growth habit of Ca‘ribbeaif'For'ests. _

Wind stress results in different responses by
forests depending on the severity of the wind.
Trees in chrOnically wind-stressed ,environments
are often shorter with larger diameters than indi-
viduals of the same species in sheltered environ-
ments (Telewski 1995), develop buttresses (Ennos
1995), or produce reaction wood (reviewed in
'I‘imell 1986). Compared to;chronic low-level stress
from the trade winds, hurricanes impact a forest
with extreme, but relatively brief, wind stress.
However, the effects of a single acute wind event
can drastically change the developmental trajec-
tory of a forest (Brokaw &, Grear 1991; Foster &
Boose 1995; Steudler et al. 1991). Hurricane-force
winds can inﬂict plastic damage (i.e., irreversible,
as opposed to elastic, or reversible, damage) on
stems including defoliation, snapping, uprooting,
and branch loss (Foster & Boose 1995). In such
cases, trees frequently respond by sprouting, as
seen after Hurricane Joan in Nicaraguan wet for-
est (Vandermeer et al. 1990; Yih et al. 1991), after
Hurricane Hugo in dry forests of Guadeloupe (Im-
bert et al. 1998) and wet forests of Puerto Rico
(Walker 1991; Zimmerman et al. 1994) and after
Hurricane Gilbert in Yucatan dry forest (Whigham
et al. 1991) and Jamaican montane wet forest (Bel-
lingham et al. 1994). i

There is some evidence for sprouting in appar-
ently undamaged trees exposed to wind stress.
Sprouting has been noted below 2.5 m height on '
about 47% of “undamaged or lightly damaged"
stems following hurricanes in. Jamaica (Belling-
ham et al. 1994). In Puerto Rican rainforest about
57% of “undamaged” stems sprouted after Hurri-
cane Hugo in one study (Zimmerman et al. 1994),

130

VAN BLOEM. MURPHY & LUGO

but the location of sprouts on stems was not noted.
Sprouts developing within 40-50 cm of the ground
may lead to multi- stemmed trees if the sprouts
grow and survive. Walker (1991) reported 6% of
“upright” (not snapped or uprooted) stems in sub-
tropical wet forest sprouted below' 50cm on the
trunk. Imbert et al. (1998) and Vandermeer et al.
(1995) mention sprouting below 50 cm on trunks,
but neither specifically. state whether undamaged
stems sprouted at that height.

To date, no satisfactory explanation for the
high stem density of mature dry forest (>12,000
stems ha-l) nor the prevalence of multi-stemmed
trees (42%) in study plots, near‘Guénica, Puerto
Rico, has been preposed. Because of the govern-
mentally protected status of Guanica Forest, cut-
ting and grazing in the vicinity of our plots has
been light or absent in .the last 70 years and fire
has never been an inﬂuential factor. Where cutting
has taken place in Guanica Forest, sprouting is
common (Molina Colén 1998; Murphy et al.1995),
but sprouting is also common in areas which were

not subject to cutting. Dunphy et al. (2000) ana- '

lyzed multi-stemmed trees in Guanica Forest and
concluded that fora majority of species the growth

form was natural - not the result of cutting. The.

last few hurricanes that have passed over the for-
est have broken few stems (<13%) (Van Bloem et
al. 2001). Sprout development following Hurricane
Georges has provided new insight into tropical dry

forest structure. Following the hurricane, we ex- .

pected that: (1) sprouting frequency would be
higher on damaged stems, (2) sprouting would be
proportional to defoliation because sprouting re-
sponse might be related to biomass loss, and (3) a

majority of sprouts produced after Hurricane-

Georges would die after the first or second dry sea-

5011 due to thinning of new sprouts as they com- '

peted for resources. The objectives of this paper
are to evaluate these expectations; to report pat-
terns in post-hurricane sprouting, and to assess
the potential role of hurricanes in creating multi-
stemmed trees and shert~statured, dense forests.

Methods

Guanica Forest is comprised primarily of semi-
deciduous dry forest and is located along the
southwestern coast of Puerto Rico (17° 58' N, 65°
30' W). The forest was originally protected in 1917
and its boundaries expanded in the 1930’s to in-

clude all the plots within this study. Canopy
height is generally 5-7 m, and density of live stems
(>2.5 cm dbh) averages 12,000 per hectare (Mur-
phy & Lugo 1986b). About 42% of trees are multi-
ple-stemmed and they include 56% of all stems
(Murphy & Lugo 1986b). Annual rainfall averages
860 mm, 45% of which comes between September
and November, corresponding to the height of hur-
ricane season (Murphy & Lugo 19868). Mean an-
nual temperature is 25.1°C and the PET/precipita-
tion ratio averages 1.4 (Murphy & Lugo 1986a).
Previous investigations in the forest have deter-
mined that the multi-stemmed growth habit of the
trees cannot be solely explained by cutting,
although this is a likely explanation for a few
species (Dunphy et al. 2000).

Hurricane Georges crossed over the island of

’ Puerto Rico onSeptember 21-22, 1998. The south-

ern portion of the hurricane's eye passed over
Guanica Forest. This category 3 hurricane (Saﬁr-
Simpson Index).ha'd sustained winds of 176-184
km 11" with gusts up to 240 km h'l (Bennett & Mo-
ﬁes-1.998). Rainfall measured in the forest was 151
mm during the two days of Georges’ passage. Av-
erage September rainfall in Guanica forest is 155
mm (Murphy & Lugo 1986b). Hurricane- force
winds from Georges impacted Guanica forest for
about four hours.

In the last 300 years, hurricanes have passed
over the areas containing our research sites at an
average return rate of 25 years (Miner-Sela 1996;
Salivia 1972). The last hurricane that passed over
Guanica Forest and had a strength similar to Hur-
ricane Georges was San Felipe in 1928 (Salivia
1972).

- We studied sprouting response in five plots in
Guanica Forest ranging from 0.01_ to 1.44 ha in
size and located in various topographic settings
that represent a gradient of wind conditions de-
termined‘ by slope, aspect, and elevation. Low
elevation", topographically level plots had the least.

' wind exposure while plots at higher elevation (e.g.

175 200 m) with steeper, south- facing slopes had
the greatest exposure. All plots were comprised of
semi-deciduous forest (Ewel & Whitmore 1973)
and had trees permanently marked and censused
for previous studies. Our plots included over 40
species of trees, but have relatively high species
evenness (Murphy & Lugo 1986b), as is common in
many mature subtropical forests. All plots were on
the same type of soil, an alkaline clay mollisol over

131

SPROUTING IN DRY FOREST AFTER HURRICANES

a limestone base. Within these plots, we had 1407
' permanently tagged stems of at least 2.5 cm dbh
(measured at 1.4 m). ’ ' ' .

We determined the type and severity of dam-i
age to the 1407 tagged stems in our plots within
one week of Hurricane Georges. Snapped trunks,
uprooting, loss of large branches, and permanent
bending of trees beyond 45° from vertical were con-
sidered major structural damage. On stems with-
out major damage, defoliation was estimated visu-
ally on a percentage basis. Some trees appeared to
escape both major stem damage and defoliation
and were considered to have no visible damage.
The type and rates of damage and species eﬂ'ects
resulting from Hurricane Georges will be reported
elsewhere. ’

Following Hurricane Georges, we measured
sprout development on the tagged stems within
our plots six times over two years. We considered
any woody twig growing from a mature stem below
breast height at an angle < 45° from the trunk to
be a sprout (Dunphy 1996).- To quantify pre-
hurricane rates of sprouting, we inventoried all old
sprouts on 451 tagged stems along 6 transects to-
taling 680 m in our largest plot. Subsequently, we
were able to distinguish new sprouts by their dis-
tinctive bark colors as compared to old sprouts. On
all of the 1407 tagged stems, we counted all new
sprouts growing at breast height (1.4 m) or lower.
Technically, some of these sprouts would be con-
sidered branches rather than additional stems;
therefore, we noted whether new sprouts arose
from trunks or roots and where on the trunk new
sprouts emerged from tagged stems. In mature
trees, it can be diﬁcult to distinguish between
branches and stems when they attain diameters 2
2.5 cm, grow at angles < 45" from vertical and
emerge from trunks below 40 cm, so we attempted
to take this into account with our measurements.
The length of the longest sprout on each tagged
stem was measured to the nearest cm and its point
of origin noted (i.e., ground, or height on trunk).

Results

Pre-hurricane sprouts were present on 16 of
451 stems (3.5%). No new sprouts emerged on the
1407 tagged stems in Guanica Forest within eight
days of the hurricane. However, new sprouts were
present by mid-November, 1998 (8 weeks post-
hurricane), on both damaged and undamaged
stems, and by January, 1999 (15 weeks post-

hurricane), 481, total stems had new sprouts. In
June, 2000 (90 weeks post-hurricane), 493 stems
had post-hurricane sprouts (34.2%). The plots with
the greatest exposure to hurricane winds had the
greatest proportion of sprouting stems (Fig. 1). In
each plot, the proportion of sprouting stems was 2—
3 times the proportion of stems incurring major
structural damage. '

The proportion of stems sprouting after Hurri-
cane Georges was 8—14 times higher than before
the hurricane. The sprout rate (number of sprouts
per stem) was 3—13 times higher than pre-
hurricane rates (Table 1). While we expected stems
with major structural damage to sprout, we were
surprised at the increase in sprouting on defoliated
stems and stems without any visible damage. The
proportion of stems sprouting and sprout‘rates did
not differ with severity of defoliation (Fig.2).

New sprouts emerged from both roots and
trunks of trees, sometimes in both locations for a
single stem (Table 2). Over 73% of sprouting stems
had sprouts emerging below 40 cm on a stem.

Tree species in Guanica Forest had different
sprouting response patterns after the hurricane.

 

7.0 .
Ddamage

I sprouting

 

 

 

Fig. 1. Percent of stems in Guanica Forest incurring
structural damage and with new sprouts relative to
wind exposure. Sprouting data are from four months af-
ter Hurricane Georges. Structural ddmage includes

, snapping, permanent bending, uprooting, or loss of large

branches. Exposure is determined by elevation and
slope based on wind speeds and directions reported after
Hurricane Georges (Bennett 1998), all plots face south.
Exposure 1 is most protected at low elevation and a level
slope. Exposures 4 8r. 5 are at the highest elevations, 5
has the steepest slope. Both damage and sprouting are

7 greater at higher exposures (1" tests: p = 0.016, p <

0.00001 respectively).

132

'VAN BLOEM, MURPHY & LUGO

Table l. Sprouting in Guanica Forest, Puerto
Rico. Pre-hurricane sprouts were counted on 451
stems. Post-hurricane sprouts were counted on
1407 stems pooled from ﬁve plots. Only sprouts
developing below breast height (134 m) were
counted. A sprout was deﬁned as buy woody twig
with an orientation greater than 45° relative to the
ground. Post hurricane sprouts compared against
pre-hurricane sprouts using 2 or t tests as appro-
priate.

 

%of

 

 

Total Sprouts per
number stems sprouting
of with stem
stems sprouts (se)
Pro-Hurricane Sprouts 451 3.5 1.7 (0.3)
Post-Hurricane Sprouts
Major structural 205 48.3“" 21.3 (3.3)"
damage
Defoliated stems? 1153 31.8"” 10.1 (1.0)”
No visible stem 49 28.6“" 5.8 (1.6)‘.
damage
1 Stems with defoliation but without major structural
damage.

***p‘< 0.0002; "p < 0.0005; *p < 0.01

A96 sprouting stems 0 mean sprouts/stem

 

 

 

in

40 A

O.

6 30 ‘ ‘ a A

‘3; 20 '1-

3 10 I I I: I}
o . . - 2 -

o 25 50 75 100

Defoliation rats

Fig. 2. Trends in proportion of sprouting stems or
sprouting rate with defoliation severity in Guanica For-
est following Hurricane Georges. Bars are :l: 1 SE Pre-
hurricane sprouting shown in Table 1. Severity of defo-
liation is not related to sprouting response. 1’ tests: p =
0.60 for percent of stems sprouting; p = 0.92 for sprouts
per stem.

For species with at least 10 stems in our plots,
4-100% of stems sprouted (Table 3). For our six most
common species, each with at least 100 stems,
15-7 1% sprouted. Sprout rate ranged from 5—34
sprouts per stem for our 6 most common species.

Table 2. Percentage of post-hurricane sprouts
arising from trunks or roots. Sample size is num-
ber of stems sprouting.

 

All stems (n = 481) Percent
Only from roots 21.7
Only from trunk 61.1
From both trunk and roots 17.2
At or below 40 cm on trunk 73.4

Defoliated or no damage stems (n = 382)

Only'from roots 24.3
Only‘Eom trunk 58.6
From both trunk and roots 17.0
At or below 40 cm on trunk 75.1 ,

 

Some produced many short sprouts (e.g. Emstema
caribaeum) while others produced few long sprouts
(e.g. Coccoloba diversifolia). For species with at
least 20 stems in our plots, the median length of
the longest sprouts for each species showed was
positively correlated with the number of stems per
tree (p = 0.012, Fig. 3) and the percentage of
multistemmed trees of a species (p = 0.018).

By January 1999 there were 5898 new sprouts
on the 1407 stems in our plots. By June 2000
sprout mortality was 13.6%, leaving 5095 new
sprouts. Mortality for sprouts growing from trunks
was about 25%, but this was offset by a 20% in-
crease in root sprouts. Mortality of sprouts was
15.8% on stems with major structural damage and
12.4% on defoliated or undamaged stems. By June
2000, 65% of all post-hurricane sprouts were on
defoliated or undamaged stems. The longest sprout
on each stem averaged 44 cm in January 1999 and
doubled to 89 cm in June 2000. I

Discussion

Trees responded to Hurricane Georges by pro-
ducing a large flush of new sprouts, many at or
near the base of trees. After two years, survival of
sprouts has been surprisingly high. While we ex-
pect thinning of the sprout cohort to continue for
some time, the proportion of stems producing post-
hurricane sprouts suggests that hurricanes can
have a long-term impact on forest structure by ini-
tiating the production of new stems. We cannot de-
ﬁnitively relate the current structure of mature
forest to previous hurricanes because we cannot
completely quantify past human disturbance in

133

-—-‘-

SPROUTING IN DRY FOREST AFTER HURRICANES

Table 3.

Species effects in proportion of stems sprouting, sprout- rates and sprout lengtlofor species

with at least 10 individuals sampled. All sprouts are post-hurricane. Some individual trees were multi-
stemmed, but only one stem per tree was sampled for sprouts.

 

 

' Numbdr % Sprouts. per Median % Multi- Mean number
spec”! of stems sprouting sprouting longest sprout stemmed of stems per
# stem length (cm) trees tree
Gymnanthes lucida 305 19.9 7.3 24 29.0 1.5
Amyn's elemifem 140 10.7 17 .3 8 29.2 1.5
Eugenia foetida 113 70.8 12.8 30 24.4 - 1.4
Emstema cariboeum .. 107 34.6 33.9 8 8.3 1.2
Coccoloba diversifolia 104 67.3 7.7 92 52. 1 3.1
Pictetia aculeata 104 15.4 5.5 ’ 16 50.0 2.4
Bursesera simaruba A 98 4.1 5.5 24 4.4 1.0
Guettardo hrugii 57 22.8 3.0 17 66.7 3.4
Coccoloba microstochyo 37 54.1 4.4 81 76.6 . 6.1
Boumn'a succulenta 33 36.4 4.9 76 35.3 ‘ 1.5
Thouinia portoricensis 33 90.9 18.9 34 68.6 4.2
.ngiodendron ferreum 31 71.0 20.3 17 16. l 1.2
Pisom'a olbida 29 10.3 14.3 - 7 1 34.5 1.6
'Tabebouia heterophylla 28 39.3 9.0 61 92.9 5.5
Bucida bucerus ' 23- 30.4 8.9 37 38.1 2.3
En'throxylan rotundifolium 23 52.2 11.8 51 35.3 2.3
Leucaena leucocephala . 14 100.0 19.1 29 23.1 1.4
Crossopetalum rhacomo ' 12 75.0 9.2 13 53.8 2.5
Eugenia nrophytica 10 100.0 9.1 11 80.0 6.4

 

the forest, however, the forest after Hurricane
Georges is clearly primed to have more stems than
before the hurricane. As the sprout cohort thins,
we may see patterns begin to developbetween the
number of stems per tree and the percent of stems
sprouting or sprout rate. By 90 weeks post-
hurricane, the length of the longest sprout on each
tree was positively associated with the mean num-
ber of stems per tree and the percent of stems
sprouting within a species.

As expected, stems incurring major structural
damage had the highest sprouting rates, but
sprouting was also common 0n defoliated and ap-
parently undamaged stems. Sprouting on defoli-
ated stems was notable because allocation of re-
sources to production of new leaves would be less
costly than to leaves and woody tissues needed for
sprouts. Root biomass is nearly equal to shoot
biomass in Guanica Forest (Murphy & Lugo
1986b), so it appears that roots were able to pro-
vide enough resources for the production of new
leaves and sprouts simultaneously which we ob-

134

 

% multistemmed trees

 

 

l

1 20
Median length of longest sprout (cm)

 

 

G l l l

O 30 60 90 1 50

Fig. 3. The median length of the longest sprouts on
stems in 16 species of dry forest trees is related to the
number of stems of each tree. (p = 0.012) Median sprout
length is similarly related to the percent of multi-
stemmed trees (p = 0.018). The data are from species
with at least 20 trees in our plots. Each point represents
a tree species.

VAN BLOEM. MURPHY 8: LUGO

served on most stems after Hurricane Georges.
The severity of defoliation did not affect sprouting
rate, suggesting that defoliation itself was not the
mechanism that elicited sprouting. '

It is likely that sprout development following
the hurricane was inﬂuenced by altered hormone
balances in trees. High winds and vertical dis-
placement are known to increase ethylene produc-
tion (Brown & Leopold 1973; Leopold et al. 1972;
Nelson &_ Hillis 1978; Telewski 8: Jaﬁ'e 1986). Eth-
yle'ne production would be highest at the point of
greatest bending - below breast height near the
root collar (Vogel 1994; Wood 1995). Ethylene has
been shown to block auxin transport (e. g. Wood
1985). Because auxin suppresses lateral bud de-
velopment, blockage of auxin can release these
buds (Cli'ne 1991'; Kramer 8: Kozlowski 1979).
While we have no direct evidence of altered hor-
mone concentrations, following Hurricane Goerges,
this model.w0uld explain the prevalence of basal
sprouting, even on undamaged stems. A mecha-
nism to explain basal sprouting must be applicable
across species because basal sprouting occurred on
undamaged stems of all species in our plots. .Al-
tered hormone balances would be. a generalized re-
sponse to wind stress among all species. Variation
in the degree of sprouting response could be the
result of unique characteristics of each species in
hormone regulation as well as wood density, crown
geometry, etc.

Conditions necessary to maintain sprouting as
a disturbance recovery mechanism have recently
been reviewed by Bellin'gham -& Sparrow (2000).
They suggest a tradeoff in recovery strategies be-
tween sprouting and seeding. This seems to be the
case in Guanica Forest as seedling establishment
is generally very low (Molina Colon 1998), while
resprouting ability is widespread. Resprouting on
mature trees would be supported by well-
developed root systems and increasing leaf area to
maximize photosynthesis after a disturbance. Re-
sprouting would be a strategy for trees to maxi-
mize spatial coverage in order to access more re-
sources (sunlight, water or nutrients) and would,
therefore, be a case of reiteration (sensu Halle et
al. 1978). Bellingham- & Sparrow (2000) further
suggest that the proportion of biomass lost from a
tree following a disturbance will determine
whether a tree will resprout and where, resprout-
ing will occur on the tree. They suggest that basal
sprouting should only become prevalent when a

large proportion of aboveoground biomass is lost.

In this context the amount of sprouting on defoli-
ated stems andstems without any type of visible

6 damage was surprising. Our results suggest that

basal sprouting occurs even with the small bio-
mass loss associated with partial defoliation, in
contrast to‘ the Bellingham & Sparrow model. Our
results likely differ from their predictions because
resources following the hurricane (water and nu-
trients in fresh litter) were high, and thus the reli-
ance on storage organs to support sprouting would
be low. Also, our mechanism for eliciting sprout
development does not rely on biomass loss, but in-
stead on internal hormone balance altered by ex~
ogenous factors.

Conclusions

Hurricane Georges clearly stimulated the de-
velopment of sprouts above pre-hurricane levels.
The production of post-hurricane sprouts was
higher in stems with major structural damage
than defoliated stems, but not limited to damaged
stems nor related to defoliation severity. Sprouts
produced on defoliated stems or stems without
visible effects of the hurricane accounted for over.
half of all new sprouts. The amount of production
of basal sprouts varied by species, but the phe-
nomenon was not species-speciﬁc. After two dry
seasons, sprout mortality was low. Our results
suggest that hurricane disturbance. leaves sub.
trOpical dry forest with the potential to greatly in-
crease stem density and the proportion of multiple-
stemmedtrees. characteristics common to dry for-
ests in the hurricane-prone Caribbean region.

Acknowledgements

This research was conducted in collaboration
with the Puerto Rico Department of Natural‘ Re-
sources and the Environment and the University
of Puerto Rico. Funding was provided by USDA
Forest Service Agreement IITF-98-ca-006 and
travel funds from the Michigan State University
EEBB Program and Paul Taylor Fund. Thanks to:
M. Canals for excellent logistical support, C. Ti-
rado, J. Genet, S. Whitmire, C. Jen, K. Donaghue,
A. Talhelm, and A. La Voy for valuable ﬁeld assis-
tance, F. Telewski, K. Genet, 1. Ramjohn and F.
Ewers for useful comments on the manuscript, P.
Hinson and I. Hinson for safe haven during Hurri-

cane Georges.

135

SPROUTING IN DRY FOREST AFTER HURRICANES

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CHAPTER 7

OVERALL CONCLUSIONS

Forest growth and structure are inﬂuenced by a variety of factors, each of which
operates on varying spatial and temporal scales and with different intensities. Two factors
that shape the structure and function of dry forests in the West Indies are hurricanes and
nutrients. Hurricanes impact large swaths of forest, but the timing and intensity of hurricane
effects depend on storm strength and trajectory. Nutrients appear to affect some functional
traits in the forest, such as limitation of growth, and may be important during the rainy
seasons when water is abundant. As a result of this dissertation research, I conclude that
hurricane disturbance has a greater inﬂuence than variation in nutrients on forest structure.
Hurricane Georges arrested forest development, damaging large stems and causing basal area
losses that equaled decades of growth. Furthermore, the hurricane resulted in a widespread
sprouting response that could increase stem density and the proportion of multi—stemmed
trees as sprouts mature into stems. Even though strong associations between tree growth
and soil nutrient content were absent, trees still exhibited symptoms of nutrient stress, such
as high phosphorus use efﬁciency and the satisfaction of 65% of annual P budget by
retranslocation.

Within the broad interpretation reached above, a number of speciﬁc conclusions
regarding nutrient effects, hurricane effects, and long-term growth have been generated by

this research. These include:

138

NUTRIENT EFFECTS

1.

Pool sizes of most nutrients in Guanica Forest were large compared to other dry
forests. Guanica Forest had the highest amount of total N (0.5-1.8%), available Ca
(5-12 mg/ g), organic matter (17-49°/o), and pH (7 .7—8.0) reported for dry forest areas.
Only forests in the Yucatan had more total P (2.2 mg/ g) than Guanica (0.5-1.0

mg/ g) Despite large amounts of total P, only 1.3 to 2.9% was available. High
organic matter in the soil suggested that a large proportion of soil nutrients could be
immobilized in microbial pools to facilitate decomposition. (Chapter 2)

While studies in other forest life zones have indicated that soil nutrient patches tend
to be the same size or smaller than crown diameters of mature trees, this was not the
case in Guanica Forest. Based on spatial analyses, patch sizes of nutrients were
inferred to be 17-25 m, much larger than the 3-5 m crown diameters of mature trees
in Guanica Forest. Patches tended to be about the same size for different nutrients
as well as from site to site in the forest and appeared to be the result of
microtopography. (Chapter 3)

Among soil properties, spatial patterns of N and organic matter were the most
similar, reﬂecting strong correlations in their pool sizes. Total P was also strongly
correlated to N and OM pools at three of the four research sites. Spatial
autocorrelation was able to explain at least 70% of variability in soil properties for a
majority of nutrients. (Chapter 3)

Neither Ca nor pH was consistently related to pool sizes of TP or P“, despite the
potential for occlusion of P by Ca at the high pH found in the forest soils. The

control of P pools was therefore not simply a matter of soil chemistry, but probably

139

also strongly affected by biotic inﬂuences, such as cycling through plant and
microbial communities. (Chapter 3)

Microtopography interacted with nutrient pools. Small depressions or rocky areas
with crevices accumulated litter and had higher nutrient contents, even when these
areas were in exposed locations or had smaller trees growing in them. On the other
hand, mean elevation of sites was not related to nutrient pool sizes. (Chapter 3)

All common tree species appeared to be able to grow across the entire portion of
each nutrient gradient measured in Guanica Forest. The presence of some mature
individuals of each common species, even at the lowest end of a nutrient gradient,
suggested that all species were able to survive the most extreme nutrient conditions
in the forest. However, some species grew more frequently along portions of
nutrient gradients, suggesting either greater tolerance to low nutrient conditions or
competitive exclusion from high nutrient locations. (Chapter 4)

Nutrient limitation of growth affected only smaller stems and sprouts. Growth or
survival of sprouts and smaller trees responded to nutrient pool sizes, most
frequently to P, but often in relation to CM or N. There was no strong evidence for
nutrient limitation on the growth of mature trees based on nutrient pool size.
Smaller trees would be able to access a smaller volume of soil and thus be restricted
in nutrient uptake. Trees resprouting after hurricane disturbance would have lost a
signiﬁcant portion of internal nutrient pools to defoliation. Therefore, growth of
small and sprouting trees would have been more likely to respond to nutrient pool
size. (Chapter 4)

Nutrient limitation of tree growth appeared to result from the combined effects of N

and P. Co-limitation by both N and P was indicated by root in-growth experiments.

14o

Species—speciﬁc growth responses, either to pools of P or N, or N:P ratios, also

suggested that the forest responded to both nutrients. (Chapter 4)

HURRICANE EFFECTS

1.

Hurricane winds resulted in greater damage to larger stems than smaller stems.
However, wind damage overall was relatively low (12.4% of stems) even though
Georges was a strong hurricane and its eye crossed over Guanica Forest. (Chapter 5)
Topography, aspect, and forest type inﬂuenced the amount and type of damage a
forest stand incurred from high winds. Forests in exposed areas had greater damage
than those in valleys or on leeward slopes. Mahogany plantations and stands
dominated by the exotic species Leucaena leucocep/Ja/a incurred less damage than native
forests. (Chapter 5)

The majority of damage was caused by the strongest winds, which gusted up to 240
km/ hr and came from the southeast. A critical wind speed between 176 (Category 3
hurricane level) and 240 km/ hr was necessary to cause the majority of damage, based
on tree fall directions. Hurricane Hortense crossed over Guanica Forest in 1996, but
its winds of 130 km/ hr did very little damage. (Chapter 5)

Forest fragmentation had little effect on hurricane damage rates in a collection of
forest fragments in SW PR. Rates of damage and the effects of aspect and
topography in fragments were similar to Guanica Forest. (Chapter 5)

Compared to annual litterfall, hurricane litterfall was enriched in nutrients. Nutrient
return to the forest ﬂoor by leaf litterfall during the hurricane was equal to or greater
than annual nutrient return for N and P although leaf litterfall biomass was only 55%
that of annual rates. Wood litter was 11 times greater than annual rates as were its

contributions of N and P. (Chapter 5)

141

6. Stem mortality due to Hurricane Georges was only 2%, lower than damage rates and

mortality rates reported from other dry forests. Although 2% mortality was tenfold
greater than background rates in Guanica Forest, hurricanes do not occur frequently
enough to kill as many stems as are lost to other factors (senescence, thinning,
drought, etc.) over time. (Chapter 5)

Basal sprouting that occurred after Hurricane Georges minimized mortality and may
have a long—term inﬂuence on forest structure. Basal sprouting occurred on 34% of
stems, nearly three times the rate of stem damage. After two years, sprouts
continued to survive, suggesting that the incidence of multi—stemmed trees will
increase as a result of Hurricane Georges, maintaining wind-resistant physiognomy.
(Chapter 6)

Basal sprouting following the hurricane appeared to be the result of gravitational
displacement by high winds rather than structural damage to or defoliation of stems.
Sprouting was 10 times higher than pre-hurricane rates on undamaged and defoliated
stems, but the severity of defoliation was not related to sprout rates. It is suggested
that high winds may trigger an ethylene response at or near the base of a stem, where
ﬂexure would be greatest, altering hormone balances sufﬁciently to reduce inhibition

of basal sprouts. (Chapter 6)

LONG-TERM GROWTH PATTERNS

1.

Native forest stands in Guanica Forest appear to be mature, based on species
turnover, mortality and in-growth rates, and stable size distributions, densities, and
basal areas of stems. Stable soil properties over the 18-year period between sampling

events also indicated forest maturity. (Chapter 2)

142

2. The tree species assemblage changed little in the Main site over an 18—year period
and the changes that did occur are typical of a mature forest. Putative pioneer
species in the forest became less important over time. Individuals of three new tree
species entered the smallest diam&er class measured (2.5 cm), but only one of these
species had not been noted in the understory previously. (Chapter 2)

3. Without the effects of Hurricane Georges, the forest would appear to be aggrading,
with increasing stem density and in-growth exceeding mortality. Stem losses
resulting from the hurricane nearly equaled growth over the 18-year period.
Considering that hurricanes are a permanent part of the environment, the forest has

reached a dynamic equilibrium and can therefore be considered mature. (Chapter 2)

FUTURE RESEARCH

The ﬁndings of this research highlight additional avenues of inquiry which would
further our understanding of tropical dry forest structure and function. Potential topics
include:

1) anm' ggd fQquz-gp of long term research sites 19' Qua’gjga Egrgst. Long term
permanent plot studies with multiple sampling periods are rare in tropical dry forest (see
Chapter 2). Future measurements will provide more complete insight into background
mortality rates, in-growth patterns, species turnover, invasion of exotic species, and the
relationship between tree growth and annual precipitation.

2) WM. My research only focused on nutrient
pools, an important ﬁrst step in understanding nutrient dynamics. The role of microbes,
particularly mycorrhizae, in cycling nutrients needs to be addressed in more detail. Studies

should focus on timing of major ﬂuxes, amount of nutrients in ﬂux, the effects of high

143

amounts of organic matter in soil, and forms of nutrients (e.g., Ca-bound P or organic P)
accessed and released by various microbial populations.

3) W. Mainly due to logistical considerations, water limitation has never
been explicitly studied in Guanica Forest. Manipulative studies which control the quantity
and timing of water availability would be useful to understand how much tree growth is
determined by water supply and how much nutrient limitation is determined by transport (or
lack thereof) or nutrients through soil by water.

4) W. The sprout response following
Hurricane Georges was likely to have been generated by the hurricane altering hormone
balances in stems, as discussed in Chapter Six. This mechanism is the subject of a grant to
Skip Van Bloem recently funded by the US Department of Agriculture.

5) WWW. Once the hormone
mechanism for sprouting is identiﬁed, we should determine if this is a trait common to all
trees, or only species and populations growing in wind-stressed areas. The ﬂora of Guanica
Forest contains species found in Florida, Central America, and South America. Dry forests
in these areas exist along a hurricane gradient, and it should therefore be possible to

determine whether the sprouting is an adaptation or simply a physiological response.

144

APPENDICES

APPENDIX 1: FULL SITE DESCRIPTIONS

The Main site was located on the north side of Camino Couto (or Fuerte),
approximately 50 m past the K5H2 marker. The SW corner of the site was 81 m north of
the road. Elevation at the Main site ranged from 120—140 m (Figure 2). The site was dotted
with dogtooth limestone outcrops which averaged 25% of surface area. Previous
excavations have shown that the outcrops form a crust on the surface rather than being
extensions of bedrock (Murphy and Lugo 1986b). The northeastern portion of the site was
ﬂat with shallow litter layers and few outcrops. The northwestern, center, and southern
portions of the site were sloping and rocky with deep (>10 cm) litter layers. Where
outcropping was prevalent, soil was only found at the surface in crevices between rocks and
plants rooted in loosely consolidated humus layers. The western side of the site consisted of
a shallow draw which drained the northeast corner and most of the western half of the site.
Surface rocks were absent in the draw and the litter layer varied in thickness, presumably
accumulating in the bottom both from transport from the sides and direct deposition from
trees overhead. Along the eastern edge of the site, the ground sloped toward the east, so the
topography of the entire site was like a knob or protrusion sticking out of a south-facing
slope. The site had been used before 1930 for small-scale charcoal production, where pits of
3-5 m diameter were dug, ﬁlled with wood cut from nearby, lit on ﬁre, and covered with soil.
The pits have been reﬁlled and the soil surface was leveled. One pit was located in the draw
and at least three were located in the northeastern portion of the site. There was no
evidence of charcoal pits in sloped areas. In 1999, there were at least 37 tree species with

stem diameter 2 2.5 cm in the site (Table 1). Gymnantbc: lucida was most important, followed
by Cocoa/aha microitac/ya, Pictctia amleata, and Pixom'a albida. The most common exotic tree
species in the dry forest region of Puerto Rico are Leucaena leucocgbbala and Pmropiijuliﬂora.
Neither of these species were present in the Main site.

The 1-ha Lluberas site was located off Camino Lluberas. The NW corner of the plot
was about 30 m off the road, to the east, about 100 m south of the intersection of Lluberas
and Granados Trail. Most measurements were taken within a 30 x 30 m block in center of
the NW quadrant of the site, but twelve 5 x 5 m blocks were sampled in the remainder of
the site to verify that patterns found in the 30 x 30 m block were representative of the
whole. This same scheme was used at the Ventana site (described below). Elevation ranged
from 141-151 m (Figure 2). The northwestern portion of the site formed a very shallow
draw that ﬂowed out of the site to the west (Figure 2). This area had few outcrops. The
eastern two-thirds of the site had numerous outcrops and sloped generally southward.
There were no signs of human use since 1930. Trees from 33 species (minimum diameter
2.5 cm) were censused at the site (520 trees in 900 m2). The species assemblage was similar
to the Main site (I' able 2), with Gymnant/Je: lucida most important, followed by Cacao/017a
divemﬁlia, Pictetia am/eata, and Eugenia ﬁctida. Two trees of bucaena leucocepba/a were present.

The l-ha Ventana site was located in a shallow draw which eventually becomes a
gully about 100 m southeast of the site. The gully leads to Punto Ventana and crosses the
forest boundary about 300 m southeast of the site. The eastern edge of the plot was about
50 111 west from the old barb wire fence marking the eastern boundary of Guanica Forest.
The 30 x 30 m plot was in the SE quadrant. Elevation ranged from 20—36 m and the draw

145

rans N-S through the site, turning out the SE corner. The soil surface was rocky, resulting in
rooting in the lower layers of litter. Of all the sites, Ventana was the most open, having
about 65% of the stem density and 90% of the basal area found elsewhere. There were no
signs of human use since 1930, but before 1920 there had been extensive ranching to the
west of this plot and old two-tracks were faintly visible between the site and Camino
Lluberas. In the 16003 there was a Spanish settlement about 1.5 km west (M. Canals,
personal communication), so the site probably incurred human disturbance in the past,
perhaps more so than the other sites. Like Lluberas and Main, Gymnant/m lucida was the
most important tree species (Table 3). Affljli! e/emzfera, Coccoloba divemfo/ia, and Barrera
dmamba followed in importance. There were 32 tree species at the site (320 trees in 900 m2),
including three Leucaena leucocep/Ja/a trees.

146

Table A-1. Importance values for stems 22.5 cm at the Main site in Guanica Forest in 1999.
I.V. is the sum of relative frequency (RF), relative density (RD), and relative dominance
(RBA; basal area).

 

 

 

°/o of
Rank Species IV Total IV RF RD RBA

1 Gymnantbfi lucida - 48.45 . 16.15 8.38 25.38 14.68
2 Cocoa/aka mimrtacbja 23.38 7.79 7.26 8.57 7.55

3 Pictetia aadeata 23.38 7.79 5.59 1 1.19 6.60
4 Pirom'a albida 21.56 7.19 5.03 2.75 13.78

5 Tboaim'apoﬂoticemi: 17.76 5.92 5.03 8.95 3.78

6 Exortema caribeaam 15.88 5.29 7.26 3.77 4.84
7 Barrera .rimamba 10.83 3.61 5.03 1.02 4.78

8 Boarmia mam/mm 9.32 3.1 1 5.03 2.11 2.18
9 Como/05a divera'jb/ia 9.21 3.07 4.47 1.34 3.39
10 Tabebuia beterop/lela 8.82 2.94 3.91 2.37 2.54
11 H Jpelate tnfo/z'ata 8.29 2.76 2.23 1.79 4.26
12 Caettarda ell¢tica 7.53 2.51 2.23 3.58 1.72
13 Pilosocereu: mjenii 7.30 2.43 1.68 0.64 4.99
14 Eritbalirﬁuticora 7.26 2.42 2.79 2.75 1.72
15 Canine aglocarpa 7.20 2.40 2.79 2.37 2.04
1 6 Liptocma: quadricortatm 7.12 2.37 1 .12 2.17 3. 83
17 ngiodendmnfmam 7.10 2.37 3.91 0.83 2.35
18 jacqainia beﬁerii 6.76 2.25 3.35 1.28 2.13
19 Antir/Jea acutata 6.15 2.05 1.68 2.56 1.92
20 Gaettarda kmgz'z' 5.53 1.84 2.23 2.17 1.12
21 Anya} elemgfera 5.48 1.83 2.79 0.96 1.73
22 Cmmopetalum r/Jacoma 5.31 1.77 2.23 1.85 1.22
23 En't/Jmaglam mtandzfo/iam 4.62 1.54 2.23 0.90 1.49
24 Cacao/017a kmgiz' 3.88 1.29 1.12 1.85 0.91
25 Fonsh'era :egngata 3.76 1.25 1.12 1.85 0.79
26 Eugenia xemp/thica 3.70 1.23 1.68 0.96 1.07
27 Linodera boldn'dgii 2.43 0.81 0.56 1.02 0.85
28 Comodadia dodonaea 1.95 0.65 1.12 0.58 0.26
29 Ryaou'aguama 1.73 0.58 1.12 0.38 0.23
30 Plumm'a alba 1.64 0.55 1.12 0.32 0.21
31 Colabn'na arborm‘em 1.54 0.51 0.56 0.77 0.21
32 Zantboag/amﬂamm 1.01 0.34 0.56 0.26 0.19
33 Eugenia jbetida 0.93 0.31 0.56 0.26 0.12
34 Eugenia rbombea 0.89 0.30 0.56 0.26 0.07
35 T/m'nax moniiii 0.83 0.28 0.56 0.06 0.21
36 Rocbefom'a acant/Jop/Jora 0.75 0.25 0.56 0.06 0.13
37 Ramada andnata 0.71 0.24 0.56 0.06 0.09

147

Table A-2. Importance values for plant species having dbh 22.5 cm in nine 10 x 10 m

blocks in the Lluberas site in 1998. See Table A-1 for abbreviations.

 

 

°/o of
Rank Species I.V. total I.V. RF RD RBA

1 Gymnaatberladda 49.24 16.41 6.72 29.68 12.85
2 Cocoa/017a divem'jblia 28.38 9.46 6.72 10.96 10.70
3 Pictetz'a acaleata 25.87 8.62 6.72 6.62 12.54
4 Eugenia foetida 24.46 8.15 5.97 13.61 4.88

5 Barrera Jimaraba 21.91 7.30 5.97 3.59 12.35

6 Gaeﬂarda kmgii 17.42 5.81 6.72 6.81 3.90

7 Atrgiri: elemi era 15.66 5.22 6.72 5.48 3.46

8 Pixom'a a/bz'da 14.54 4.85 5.22 3.02 6.29
9 ngz'odmdmnfmvam 14.13 4.71 6.72 3.21 4.20
10 Tabeboaia betemp/y/la 13.55 4.52 4.48 1.89 7.18
11 Tboaz'm'apoﬁoricem‘i: 9.68 3.23 5.22 3.21 1.24
12 Boamria Jacca/eata 8.85 2.95 4.48 2.27 2.10
13 Cocmloba miawtacéya 8.30 2.77 2.99 0.95 4.37
14 Pit/Jecellobiam aagz'J-cati 6.68 2.23 3.73 1.51 1.44
15 Bame/z'a obovata 5.21 1.74 2.24 0.76 2.21
16 Laptomm: qaadn'coﬂata: 4.90 1.63 2.24 1.13 1.53
17 Pilomcma: mjem' 4.88 1.63 1.49 0.38 3.01
18 Badda bacera: 3.22 1.07 0.75 0.76 1.72
19 H Jpelate tnfo/ia 2.32 0.77 1.49 0.38 0.45
20 Exortmza caribaeam 2.24 0.75 1.49 0.57 0.18
21 Caaiacam madam 2.20 0.73 1.49 0.38 0.33
22 Cappan'r gnop/y/lop/Jora 2.02 0.67 1.49 0.38 0.15
23 Ixameaa leacoc¢bala 2.01 0.67 1.49 0.38 0.14
24 Eagem'a rbombea 1.76 0.59 0.75 0.38 0.64
25 Caaiacam oﬂia'rza/e 1.73 0.58 0.75 0.19 0.79
26 Uaocera boldn'dgii 1.57 0.52 0.75 0.19 0.63
27 Cabptrant/m $° 1.39 0.46 0.75 0.19 0.46
28 Canine >9I/ocarpa 1.00 0.33 0.75 0.19 0.07
29 Eugenia xemp/thz'ca 1.00 0.33 0.75 0.19 0.06
30 Eritbmaglon anolatam 0.99 0.33 0.75 0.19 0.06
31 Comocladia dodonaea 0.97 0.32 0.75 0.19 0.04
32 Cola/aim arbonm’m“ 0.97 0.32 0.75 0.19 0.03
33 Coma/aha kmgii 0.96 0.32 0.75 0.19 0.03

 

148

Table A-3. Importance values for plant species having dbh 22.5 cm in nine 10 x 10 m

blocks in the Ventana site in 1998. See Table A-1 for abbreviations.

 

ﬂ

 

°/o of total
Rank Species I.V. I.V. RF RD RBA

1 Gjmriantber/arida 35.84 11.95 7.897 722.50 ' 6.25
2 Amyn'r e/erm' era 34.51 11.50 7.09 18.44 8.99
3 Como/012a diverrzﬁ/ia 26.55 8.85 6.30 7.81 12.44
4 Barrera rimamaba 24.20 8.07 7.09 5.00 12.11
5 Tabeboaia betemply/la 19.35 6.45 5.51 5.63 8.21
6 Badda barerar 19.23 6.41 4.72 2.19 12.32
7 Pilorocerear mjem' 17.08 5.69 3.15 2.19 11.74

8 Pirom'a albida 16.45 5.48 5.51 2.50 8.44
9 Pirtetia ara/eata 15.52 5.17 7.09 6.25 2.18
10 Corro/oba mimrtar/yia 13.97 4.66 4.72 3.75 5.49
1 1 Exortema raribaeam 10.03 3.34 4.72 4.06 1.25
12 Tboaz'm'apoﬁoriremir 7.13 2.38 3.94 2.50 0.70
13 Gaettarda kragiz' 7.09 2.36 3.94 2.19 0.96
14 ngz'odendmafmam 5.82 1.94 3.15 2.19 0.48
15 Eytbmag'lon mtaadzfo/zam 5.1 1 1.70 2.36 1.25 1.49
16 Eageaia xemp/thira 4.42 1.47 2.36 1.25 0.81
17 Boamria raccalenta 4.08 1.36 2.36 0.94 0.78
18 Gaettarda ell¢tira 3.85 1.28 2.36 0.94 0.55
19 Unknown species 3.45 1.15 0.79 0.31 2.35
20 Comor/adz'a dodonaea 3.45 1.15 2.36 0.94 0.15
21 Boarrm'a virgata 3.43 1.14 2.36 0.94 0.13
22 Eugenia foetz'da 2.95 0.98 1.57 1.25 0.13
23 Como/aka kmgz'i 2.90 0.97 1.57 0.94 0.39
24 Daraena learocep/Ja/a 2.66 0.89 1.57 0.94 0.15
25 [arqainia beﬁen'i 2.36 0.79 0.79 0.94 0.63
26 Pitberellobiam angir—rati 1.61 0.54 0.79 0.31 0.51
27 Ximenia amm'raaa 1.25 0.42 0.79 0.31 0.15
28 Seran'nega acidotorz 1.19 0.40 0.79 0.31 0.09
29 Cam/la winterana 1.14 0.38 0.79 0.31 0.04
30 Cmrropeta/am rbaroma 1.13 0.38 0.79 0.31 0.03
31 Plamnia a/ba 1.13 0.38 0.79 0.31 0.03
32 Eritbroaglon arm/afar): 1.13 0.38 0.79 0.31 0.03

 

149

 

APPENDIX 2: PROPERTIES OF SOIL NUTRIENTS NOT DISCUSSED IN
CHAPTER THREE.

Chapter Three focused on a selection of nutrients that were considered the most relevant for
limiting tree growth in Guanica Forest. However, other nutrients were analyzed as well, as
reported here.

Table A-4. Means of elevation (m above sea level) and soil properties of four sites in
Guanica Forest. Means across sites were different unless indicated with the same letter.
Samples were analyzed as described in Chapter Three. Subscripts av and to refer to available
and total forms of elements. All concentrations are in mg/ g unless speciﬁed.

 

Main Lluberas Ventana Honda
mean SD mean SD mean SD mean SD
C (9.) 'T14.86a' 5.19 26.35 8.37 17.46 8.06 13.542. 1716

Kb (mg/g) 10.07a 1.90 6.87 1.63 8.60 0.97 10.03a 0.47
Kev (mg/g) 0.69a 0.22 0.70a 0.19 0.49 0.17 0.54a 0.15

% Km, 6.9 10.2 5.7 5.4

Caav (mg/g) 8.27 2.52 12.08 3.02 10.16 1.30 5.19 0.77
% Caav 4.6 13.8 19.2 2.0

Mg“, 3.5 1.2 4.6a 1.0 6.7 1.6 4.6a 1.2
Mg” 0.51a 0.29 0.95b 0.34 0.95b 0.35 0.46a 0.20
% Mg“ 14.6 20.7 14.2 10.0

AI 19.6 10.1 17.1 9.6 35.7 13.1 8.5 1.9
Fe 24.1 12.6 17.5 10.3 35.8 14.5 9.5 2.3
Mn 0.36 0.21 0.49 0.21 0.70 0.21 0.20 0.03
S 1.1 0.7 2.5 0.8 1.7 0.7 0.6 0.1
Nam, 0.12a 0.10 0.16 0.05 0.11a 0.05 0.04 0.03

150

 

 

Table A-5. Parameters for variogram models of soil C, available Ca, available K, and total K.
Spatial analyses were performed as described in Chapter Three.

 

Eﬂ'ective PSV

Site Max lag Model Range (m) r2 0/o
Carbon 7 i Y . V
Honda 27 spherical 27.34 0.97 99
Lluberas 32 spherical 21 .49 0.97 82
Ventana 32 spherical 20.82 0.94 100
Main 32 spherical 16.55 0.76 91
Main 150 spherical 125.70 0.87 81
Available Ca
Honda 27 spherical 20.20 0.92 89
Lluberas 32 spherical 6.35 0.66 86
Ventana 32 spherical 19.10 0.86 74
Main 32 spherical 23.39 0.93 90
Main 150 spherical 58.50 0.78 85
Available K
Honda 27 spherical 20.20 0.92 89
Lluberas 32 nugget only
Ventana 32 spherical 19.10 0.86 74
Main 32 spherical 17.33 0.93 89
Main 150 spherical 56.90 0.78 88
Total K
Honda 27 nugget only 0
Lluberas 32 spherical 26.67 0.96 100
Ventana 32 linear * 0.77
Main 32 exponential 12.24 0.82 88
Main 150 exponential 10.20 0.36 88

* eater than maximum la interval
gr g

151

 

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