Download Tesis Maestria en Ciencias de Marcos A. Caraballo Ortiz

MATING SYSTEM AND FECUNDITY OF
GOETZEA ELEGANS (SOLANACEAE),
AN ENDANGERED TREE OF PUERTO RICO
by
Marcos A. Caraballo Ortiz
A thesis submitted to the Department of Biology
FACULTY OF NATURAL SCIENCES
UNIVERSITY OF PUERTO RICO
RIO PIEDRAS CAMPUS
In partial fulfillment of the requirements for
the degree of
MASTER OF SCIENCE IN BIOLOGY
July 2007
Río Piedras, Puerto Rico
This thesis has been accepted by the faculty of the:
DEPARTMENT OF BIOLOGY
FACULTY OF NATURAL SCIENCES
UNIVERSITY OF PUERTO RICO
RIO PIEDRAS CAMPUS
In partial fulfillment of the requirements for the degree of
MASTER OF SCIENCE IN BIOLOGY
Thesis committee:
_________________________________________________Advisor
Eugenio Santiago Valentín, Ph.D.
_________________________________________________
Tugrul Giray, Ph.D.
_________________________________________________
James D. Ackerman, Ph.D.
_________________________________________________
Joseph M. Wunderle, Ph.D.
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A Sarilveth
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ACKNOWLEDGEMENTS
I would like to thanks Eugenio Santiago, James D. Ackerman, Tugrul Giray,
Joseph Wunderle, Tomás A. Carlo, Elvia Melendez-Ackerman, John Thomlinson, Sheila
Ward, Raymond Tremblay, Carla Restrepo, Alberto Sabat, Paul Yoshioka, Juliann E.
Aukema, Bert Rivera, Neftalí Rios, José Fumero and Carlos Trejo for revision and
valuable comments on writing, methodology, and statistical tests.
I am very grateful to the following persons for their advise and technical help in
data recompilation: Janet Soltero, Keren Umpierre, Vyrmar Mangual, Suzzette
Hernández, Laura Rivera, Ericka Napoleón, Cecilia Díaz, Johanna Colón, Fabiana Ortiz,
Cristina Calo, Beatriz Carrión, Marymir Miranda, Nirzka Martínez, Geysa Bone, Rosa
Linda González, Daihanés Torres, Vivian del Hoyo, Cynthia Viera, Beatriz Martínez,
Ana Maria Camacho, Rosimar (Ochi) Rivera, Juan D. Daza, Gail S. Ross, Efrén Vega,
Silvia Planas, Ivalú Cacho, José Fumero, Rodney Rodriguez, Ileana Galanes, Manuel
Mercado, Rafael Rivera, Juan Javier Llanos, Omara Ortiz, Noel Rivera, Wilfredo
Caraballo Castaing, Lydia Ortiz, Wilfredo Caraballo Ortiz, Miguel (Papo) Vives,
Wilfredo (Wilie) Hernández, and Sarilveth Flecha.
I am also very grateful to the following persons and/or institutions:
•
Conservation Trust of Puerto Rico, especially to Rafael Rivera, Juan
Rodriguez, Myrna Robles, Marangeli Vega, Maria de Lourdes Gonzales,
Orlando Díaz, Angel Quiñones, Marvin Gómez, Nephtalí Cortéz, Domingo
Cuba, Luis Velázquez, Debbie Boneta, Joel Mercado and Fernando Lloveras
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for providing the plants and continuous support for its maintenance, and for
providing assistance with study site satellite images, and seed germination and
propagation of Goetzea elegans.
•
Botanical Garden of University of Puerto Rico (especially to Fred Schaffner,
Rafael Davila, Charles Vecchini, and all the administrative, ornamental and
nursery staff) for permits to do research work at their sites.
•
International Institute of Tropical Forestry, especially Alberto Rodriguez, Iván
Vicens, Carlos Rodriguez, Olga Ramos, Michael Jiménez, Mariano Solorzano
and Ariel Lugo for providing support with GPS data recompilation and GIS
analysis.
•
John Thomlinson, Elvia Melendez-Ackerman and the Institute for Tropical
Ecosystem Studies for providing GPS equipment.
•
Staff members of Crest-Catec (especially to Zobeida Díaz, Joel Ruiz and Janet
Malavé) and Department of Biology of University of Puerto Rico (especially
to Diana Rosario, José (Cano) Rodriguez, Millie Viera, Yolanda Echevarría,
Ivan Olivo, Sonia Amaro and Aidamarie Pérez) for their support and
friendship.
•
The director of the Herbarium UPR Eugenio Santiago for academic guidance,
and for giving me many opportunities to develop my career.
•
To Tomás Carlo for his continuous encouragement and advice, to my father
Wilfredo Caraballo and my mother Lydia Ortiz for preparing the pellón bags
and for all their encouragement, support and love, to Wilfredo (Wilie)
Hernández and Miguel (Papo) Vives for providing housing and company
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during field work, for their teachings and for sharing with me their enthusiasm
and love for nature, and to my love Sarilveth Flecha for her constant support,
enthusiasm, caring for me and for being a constant source of inspiration.
I received financial support for travels and related expenses from CREST-CATEC
and the Biology Department of the University of Puerto Rico. I also acknowledge the
fundamental support of Elvira Cuevas for the realization of this work. This research was
funded by NSF-CREST (HRD-0206200) through the Center for Applied Tropical
Ecology and Conservation at the University of Puerto Rico.
Finally, I want to express my deepest gratitude to the forest for all its lessons
about plant taxonomy and life, to Coereba and Apis for helping me cultivate patience and
hope, and to the Goetzea trees for not disappointing me when I needed them the most.
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TABLE OF CONTENTS
Dedication………………………………………………………………………..………iii
Acknowledgements………………………………………………………………………iv
Table of contents…………………………………………………………………………vii
List of tables………………………………………………………………………………ix
List of figures……………………………………………………………………………...x
General introduction………………………………………………………………...…….1
Literature cited…………………………………………………………………………….4
Title page of Chapter I……………...……………………………………………………..7
Chapter I: Mating System and the Effectiveness of Native and Introduced Pollinators
of the Endangered Caribbean tree Goetzea elegans Wydler (Solanaceae)
-Abstract…………………………………………………………………………...8
-Introduction………………………………………….…………………………...9
-Methods………………………………………….……………………………...13
-Results…………………………………………….…………………………….17
-Discussion……………………………………….………………………………19
-Literature cited ………………………………….………………………………26
-Tables……………………………………………………………………………36
-Figures legends……………………………….…………………………………40
-Figures………………………………………….……………………………….41
Title page of Chapter II…………………………………………………………………..44
Chapter II: When number of flowers and distance to neighbors affects fecundity: the
case of the endangered tropical tree Goetzea elegans Wydler (Solanaceae)
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-Abstract………………………………………………………….………………45
-Introduction………….………………………………………………………….46
-Methods…………….…………………………………………………………...48
-Results….……………………………………………………………………….52
-Discussion………………………………………………………………………54
-Literature cited …………………………………………………………………59
-Table……………….……………………………………………………………64
-Figure legend……………………………………………………………………65
-Figure……………...…………………………………………………………….66
General conclusions……………………………………………………………………...67
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LIST OF TABLES
Chapter I: Mating System and the Effectiveness of Native and Introduced Pollinators
of the Endangered Caribbean tree Goetzea elegans Wydler (Solanaceae)
Table 1. Flower treatments used to determine the breeding system of G. elegans,
with remarks and purpose for each treatment……………………………………36
Table 2. Results of MANOVA for individual pollination treatments and their
interaction………………………………………..………………………………37
Table 3. Corolla-tube lengths of flowers visited and type of visit performed in the
flower by Coereba flaveola...……………………………………………………38
Chapter II: When number of flowers and distance to neighbors affects fecundity: the
case of the endangered tropical tree Goetzea elegans Wydler (Solanaceae)
Table 1. Standard Least Square multiple regression models between distance to
nearest neighbor and blooming intensity, and pollinator visits, fruit set, and seed
germination………………………………………………………………………64
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LIST OF FIGURES
Chapter I: Mating System and the Effectiveness of Native and Introduced Pollinators
of the Endangered Caribbean tree Goetzea elegans Wydler (Solanaceae)
Figure 1. Average frequency of fruit set among emasculated and nonemasculated pollination treatments in G. elegans flowers……………....………41
Figure 2. Average frequency of seed set per flower among emasculated and nonemasculated pollination treatments in G. elegans flowers……………….…...….42
Figure 3. Average frequency of seed germination per flower among emasculated
and non-emasculated pollination treatments in G. elegans flowers……..………43
Chapter II: When number of flowers and distance to neighbors affects fecundity: the
case of the endangered tropical tree Goetzea elegans Wydler (Solanaceae)
Figure 1. Relationship between blooming intensity and distance to nearest
neighbor, and pollinator visits, fruit set, and germination success........................66
x
General Introduction
Many plant species of tropical regions are self-incompatible (Bawa et al. 1985).
Thus, they depend on pollen interchange (i.e. outcrossing) for effective pollination.
Therefore, self-incompatible species require pollen from conspecific neighbors to achieve
fruit set. Self-incompatibility makes the spatial position of a flowering individual within a
population particularly relevant because factors such as flower timing, spatial isolation,
and/or neighborhoods could severely reduce pollination and fruit set (Feinsinger et al.
1991, Kunin 1993). This can be especially critical for rare and endangered species
(Demauro 1993, Kunin 1993, Byers 1995). Still, there are relatively few studies
conducted in the tropics that provide in-depth analyses of the effects of distances between
trees, seed set, seed viability, and pollinator visitation and behavior.
Pollinator behavior is an important determinant for successful reproduction
because low rates of visitation may result in decreased seed set (Jennersten 1988, Burd
1994) and reproductive isolation. Isolation of self incompatible plant species has been
shown to decrease seed set and recruitment (Wright 1943, 1946; Klinger et al. 1992,
Groom 2001). Isolation is accentuated by the generally sparse spatial distributions of
tropical trees (Wright 2002), the prevalence of self-incompatibility and dioecy (e.g., Yap
1980, Chan 1981, Bawa et al. 1985, Bawa 1992, Ward et al. 2005), and their dependence
on animals to perform pollination.
Plant-pollinator interactions can also be affected by perturbations including
deforestation and fragmentation (Whitmore & Sayer 1992, Heywood et al. 1994, Trejo &
Dirzo 2000, Severns 2003). These perturbations are especially relevant to tropical selfincompatible plants, as they could result in a population decline and possible isolation of
1
individuals. Plant-pollinator interactions can also be affected by recently introduced
species (Traveset & Richardson 2006), which can alter native pollinator populations
(Hansen et al. 2002, Dupont et al. 2004) and disrupt diverse aspects of the reproductive
biology of plants. Some introduced species are believed to affect the survival of many
species, especially in islands and archipelagos (Elton 1958, Carlquist 1965, Simberloff
1986, 1989, 1995; Crook & Fuller 1995, Bowen & Van Vuren 1997) where population
sizes are small and some species exhibit an inferior competitive ability (Cronk & Fuller
1995, Whittaker 1998), but this impact could be different among species.
The European honeybee Apis mellifera L. (Apidae) is an insect native to most of
Europe, Africa, and the Middle East (Winston 1987) that has been introduced in most
tropical areas to improve crop pollination and to produce honey (Hansen et. al 2002).
Some studies have found that the pollination service provided by A. mellifera is
beneficial for native plants (e.g., Paton 1993, Gross 2001), especially for dispersing
pollen in fragmented habitats (e.g. Dick 2001, Dick et al. 2003). However, in other cases,
their presence is a negative factor for native plant species fitness (e.g. Gross & Mackay
1998).
I selected the island endemic tropical tree Goetzea elegans Wydler (Solanaceae)
to test a series of hypothesis about the impact of introduced pollinators, spatial position
and tree fecundity. In the first chapter, I perform a series of experiments in the Botanical
Garden of the University of Puerto Rico using cultivated trees of G. elegans to test the
following hypotheses: 1. G. elegans, as other tropical trees, is a self-incompatible species;
2. G. elegans is effectively pollinated by the introduced A. mellifera and by the native
flower visitor Coereba flaveola Bryant (Coerebidae); 3. Apis mellifera is a less efficient
2
pollinator than C. flaveola, as some studies have found it a less efficient pollinator than
native pollinators (Westerkamp 1991, Freitas & Paxton 1998, Gross & Mackay 1998,
Hansen et al. 2002). In the second chapter, I report on field experiments in the largest
known population of G. elegans located in northwestern Puerto Rico to test the following
hypothesis about spatial pattern and reproduction: If G. elegans is a self-incompatible
species, then fecundity will decrease as distance to nearest flowering conspecific
increases.
3
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lowland rainforest trees. I. Sexual systems and incompatibility mechanisms.
American Journal of Botany 72: 331-345.
Bawa, K. S. 1992. Mating system, genetic differentiation and speciation in tropical rain
forest plants. Biotropica 24: 250-255.
Bowen, L., and D. van Vuren. 1997. Insular endemic plants lack defenses against
herbivores. Conservation Biology 11: 1249-1254.
Burd, M. 1994. Bateman’s principle and plant reproduction: the role of pollen limitation
in fruit and seed set. Botanical Review 60: 83-111.
Byers, D. L. 1995. Pollen quantity and quality as explanations for low seed set in small
populations exemplified by Eupatorium (Asteraceae). American Journal of
Botany 82: 1000-1006.
Carlquist, S. 1965. Island life: A Natural History of the Islands of the World. Natural
History Press, New York, USA.
Chan, H. T. 1981. Reproductive biology of some Malaysian dipterocarps. III. Breeding
systems. Malaysian Forester 44: 28-36.
Cronk, Q. C. B., and J. L. Fuller. 1995. Plant Invaders. Chapman and Hall, London, UK.
Demauro, M. M. 1993. Relationship of breeding system to rarity in the Lakeside Daisy
(Hymenoxys acaulis var. glabra). Conservation Biology 7: 542-550.
Dick, C. W. 2001. Genetic rescue of remnant tropical trees by an alien pollinator.
Proceedings of the Royal Society of London Series B 268: 2391-2396.
Dick, C. W., G. Etchelecu, and F. Austerlitz. 2003. Pollen dispersal of tropical trees
(Dizinia excelsa: Fabaceae) by native insects and African honeybees in pristine
and fragmented Amazonian rainforest. Molecular Ecology 12: 753-764.
Dupont, Y. L., D. M. Hansen, A. Valido, and J. M. Olesen. 2004. Impact of introduced
honeybees on native pollination interactions of the endemic Echium wildpretii
(Boraginaceae) on Tenerife, Canary Islands. Biological Conservation 118: 301311.
Elton, C. S. 1958. The ecology of invasions by animals and plants. Methuen, London,
U.K.
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Feinsinger, P., H. M. Tiebout III, and B. E. Young. 1991. Do Tropical Bird-Pollinated
Plants Exhibit Density-Dependent Interactions? Field Experiments. Ecology 72:
1953-1963.
Freitas, B. M., and R. J. Paxton. 1998. A comparison of two pollinators: the introduced
honeybee Apis mellifera and an indigenous bee Centris tarsata on cashew
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Groom, M. J. 2001. Consequences of subpopulation isolation for pollination, herbivory
and population growth in Clarkia concinna concinna (Onagraceae). Biological
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Gross, C. L., and D. Mackay. 1998. Honeybees reduce fitness in the pioneer shrub
Melastoma affine (Melastomataceae). Biological Conservation 86: 169-178.
Gross, C. L. 2001. The effect of introduced honeybees on native bee visitation and fruitset in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem. Biological
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Hansen, D. M., J. M. Olesen, and C. G. Jones. 2002. Trees, birds, and bees in Mauritius:
exploitative competition between introduced honey bees and endemic
nectarivorous birds? Journal of Biogeography 29: 721-734.
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Jennersten, O. 1988. Pollination in Dianthus deltoides (Carophyllaceae): effects of
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Klinger, T., P. E. Arriola, and N. C. Ellstrand. 1992. Crop-weed hybridization in radish
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Kunin W. E. 1993. Sex and the Single Mustard: Population Density and Pollinator
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6
Chapter I
Mating System and the Effectiveness of Native and Introduced Pollinators of the
Endangered Caribbean tree Goetzea elegans Wydler (Solanaceae)
7
Abstract
The effect of introduced species on native species and ecosystems is a major issue
in conservation biology. Although interactions between introduced and native species are
considered to be potentially detrimental for the native species, experimental data
confirming this are lacking. Understanding this and other aspects of reproductive biology
are fundamental for the conservation of endangered plant species. In this study, I
examined the mating system of the island-endemic endangered tree Goetzea elegans
(Solanaceae) and compared pollination effectiveness of its two floral visitors: the native
nectarivorous bird Coereba flaveola and the introduced honeybee Apis mellifera. I
experimentally manipulated flowers of G. elegans to test fruit and seed set, as well as
germination success after outcrossed, selfed and geitonogamy pollinations. Our results
indicate that G. elegans is a mainly self-incompatible species that requires crosspollination for successful fruit and seed set, and for high germination rates. This study
found that both, C. flaveola and A. mellifera exhibit similar pollination effectiveness for
fruit and seed set and for germination. Therefore this represents a case where the
introduced A. mellifera exhibit a beneficial effect for the pollination of an endangered
plant species.
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Introduction
The possible negative effects of introduced species and their impacts on
ecosystems are a major issue in conservation biology (e.g. Lugo 2005, Doody et al. 2006,
Gangoso et al. 2006, Keeler et al. 2006, Tierney & Cushman 2006, Towns et al. 2006).
Recently introduced species can disrupt animal-plant interactions, like plant-pollinator
mutualisms (Traveset & Richardson 2006), and thus, affect diverse aspects of the
reproductive biology of plants. The impacts of such disruptions could be more severe on
organisms found on islands than in the mainland for several reasons that include smaller
population sizes, limited dispersal, and inferior competitive ability (Cronk & Fuller 1995,
Whittaker 1998).
The Caribbean archipelago is considered a hotspot of global biodiversity (Myers
et al. 2000). Endemism in the flora of these islands -which is primarily at the generic and
specific levels- is very high, especially in the Greater Antilles (Santiago-Valentín &
Olmstead 2004). Only about 11% of the natural forests remain in the Caribbean (Myers et
al. 2000). However, little is known about the evolutionary relationships, the reproductive
biology, and the ecology of the species found in these remaining natural areas.
Puerto Rico is the fourth largest island in the Caribbean archipelago, and has
approximately 3200 plant species (including exotics), of which about 9% are endemics
(Liogier & Martorell 2000). In Puerto Rico and the U.S. Virgin Islands, about 50 endemic
plants are protected by the U.S. Endangered Species Act. Goetzea elegans Wydler is an
endemic tree from Puerto Rico that is considered endangered (U.S. Fish and Wildlife
Service 1987), and is a member of an ancient Caribbean-lineage of the Solanaceae family
(Santiago-Valentín & Olmstead 2003). As for most of the species designated as
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endangered, very little is known of its basic life history, such as breeding systems,
pollinators, dispersal agents, and demography (Santiago-Valentín 1995).
Populations of Goetzea elegans have been reduced by deforestation and land-use
changes (U.S. Fish and Wildlife Service 1987), and possibly, by impacts of introduced
species such as the honeybee Apis mellifera L. (Apidae). This common visitor to the
flowers of G. elegans is native to most of Europe, Africa, and the Middle East (Winston
1987), and has been intentionally introduced to most parts of the world to improve crop
pollination and to produce honey (Hansen et al. 2002).
The impacts of the introduction of A. mellifera on plant communities is a muchdebated issue (Paton 2000, Roubik 2000, Goulson 2003, Stanley et al. 2004, Moritz et al.
2005, Traveset & Richardson 2006), with cases showing the bees to be neutral or
beneficial for the pollination of native plants (e.g. Hernández-Prieto 1986, Vaughton
1992, Gross 2001, Dupont et al. 2004, Fumero-Cabán & Meléndez-Ackerman 2007),
especially for dispersing pollen in fragmented habitats (e.g. Dick 2001, Dick et al. 2003).
However, studies of the pollination of tropical plants indicate that the presence of this
species has negative consequences for the fitness of some native plants (e.g. Gross &
Mackay 1998, do Carmo et al. 2004). It is unknown whether A. mellifera represents a
negative or beneficial agent for G. elegans.
The other common visitor of G. elegans flowers is the native Coereba flaveola
portoricensis Bryant (Coerebidae), which is one of the most abundant birds in Puerto
Rico (Biaggi 1970). The species has been reported as a nectar robber for some plant
species (Kodric-Brown et al. 1984, Hernández-Prieto 1986, Fumero-Cabán & Meléndez-
10
Ackerman 2007). Although it is a very common flower visitor for many species, no data
exists to confirm legitimate pollination of G. elegans flowers by this bird.
The objectives of this study are to examine the mating system of G. elegans,
determine its pollinators, compare their effectiveness, and to assess the impact of the
introduced A. mellifera on the pollination system of this rare Caribbean tree. Specifically,
I test the following hypotheses: First, Goetzea elegans is mainly self-incompatible and
requires outcrossing to set seed. Some groups of tropical plants (Bawa et al. 1985, Bawa
1992), especially from oceanic islands (Barrett 1996, Carlquist 1965, 1974; Ehrendorfer
1979, Francisco-Ortega et al. 2000), have mechanisms that promote outcrossing.
Preliminary studies by Santiago-Valentín (1995) suggest this is the case for G. elegans,
but additional data are needed to confirm this hypothesis. Second, I hypothesized that G.
elegans is effectively pollinated by A. mellifera and C. flaveola. During Coereba flaveola
visits, its culmen seems to contact G. elegans reproductive structures, suggesting that it is
an effective pollinator. In addition, although A. mellifera presence has been reported as
negative for native plant reproduction (Paton 1993, Rojas 1994, Gross & Mackay 1998,
do Carmo et al. 2004), flower size and design in G. elegans indicate a possible pollen
transfer to the stigma during a visit. Successful pollination by A. mellifera depends on if
the bee contacts anthers and stigma, and the probability of this may be related to whether
the exploited resource is nectar or pollen (e.g. Paton & Turner 1985, Ramsey 1988a,
Vaughton 1992, Paton 1993, Vaughton 1996). Also, both animals are commonly seen
visiting the G. elegans flowers. Fruit set is frequently observed in these areas, indicating
possible high pollen transfer in the area. Last, I hypothesized that A. mellifera is a less
efficient pollinator than C. flaveola. Some studies have found that A. mellifera tends to be
11
a less efficient pollinator than native pollinators, including other bees and birds
(Westerkamp 1991, Freitas & Paxton 1998, Gross & Mackay 1998, Hansen et al. 2002).
12
Materials and Methods
Study site and study species- This study was conducted at the University of Puerto
Rico Botanical Garden in San Juan (18°23’38.17’’ N, 66°03’46.35’’ W; 19 m above sea
level), located within the subtropical moist forest zone (Ewel & Whitmore 1973).
Experiments were performed with cultivated individuals of G. elegans that had reached
maturity. To reduce the effect of genetic variation among individuals, all G. elegans
plants were grown from seeds from a single maternal plant. Although the species exhibits
a tree habit, reaching up to 10 meters or more (Little et al. 1974), young plants reach
maturity during the first 2-3 years of age. Accessibility to an adequate number of
individuals and flower samples, as well as the fact that the two putative pollinators are
common residents of the Botanical Garden, made the cultivated setting ideal for the
pollination experiments.
Goetzea elegans has complete flowers with no odor perceptible to humans. The
pale-yellow corolla is funnel-shaped, up to 2 cm long and 1.3 to 2 cm across. Six slender
stamens are borne near the base of the corolla and are exserted. The pistil has a slender
style with a bilobed stigma, and a hairy 2-celled ovary bearing few ovules. The fruits are
orange drupes covered by velvety and fine hairs, and a persistent calyx (Little et al.
1974). Fruit shapes are variable, and consistent within the individual plant. The seeds are
elliptic and 0.7 cm in size (Little et al. 1974). The tree produces flowers and fruit
throughout the year, but most frequently in February and in July (Santiago-Valentín
1995).
Mating system, pollinators, and pollination efficiency- Twenty cultivated adult
trees were studied to determine the mating system of G. elegans. They were planted in 30
13
L pots, reaching a mean height of 2.5 meters (S.E. ± 0.035) and all of them are positioned
within an area of about 100 m2. Each of the twenty trees was subjected to 13 pollination
treatments (Table 1). Each pollination treatment was replicated three times (i.e., in three
different flowers) on each tree (i.e., 39 flowers on each of the 20 trees: 780 flowers in
total). The thirteen flower treatments included: 1. exposed flowers, 2. bagged flowers (see
details of bagging technique below), 3. controlled visits of C. flaveola and, 4. A.
mellifera, 5. outcrossed hand pollinations, 6. geitonogamous hand pollinations, and 7.
selfed hand pollinations. To determine that tested flowers were not contaminated by their
own pollen, treatments one to six were repeated with emasculated flowers (representing
treatments eight to thirteen, respectively). The following describes details of each
treatment.
For the exposed treatments, flowers were left open continuously to all visitors
until abscission. In the bagged treatments, flowers were left covered to exclude all
possible pollinators. In the hand-pollinated treatments, flowers were bagged at all times
except while performing manual pollination and emasculation. For outcrossing
treatments, pollen was manually transferred between individuals. Geitonogamy was
tested by manual application of pollen between flowers of the same individual. To test
selfing, pollen was transferred from anthers to stigmas of the same flower.
Hand-pollinations were performed using a long-pointed fine brush. The brush was
rinsed thoroughly with water between each pollen transfer to avoid contamination.
Emasculations were performed one day prior to flower anthesis (and dehiscence of
anthers) by removing all anthers in the flower bud with forceps. For all treatments
involving bagged flowers, flower buds were covered one day prior to anthesis using a
14
“pellon” cloth bag. Pellon is a non-woven fabric used in the clothing industry that allows
light and air to pass through. It has previously been used to cover flowers (see Wyatt et
al. 1992a) with no apparent harm to them (e.g. Dent-Acosta 1987, Martinez 1993, Rojas
1994, Santiago-Valentín 1995, Acosta-Mercado 1996). Bagged flowers used to test
pollination of animal vectors (A. mellifera and C. flaveola) were exposed to allow only a
single visit per flower. For each treatment, fecundity was measured in three different
ways: as fruit set, as seed set, and as germination success.
Data Analysis: Comparing fruit set among pollination treatments- To test for
differences among fruit set among the thirteen pollination treatments I did the following.
For each pollination treatment at each experimental plant, I counted the fraction of
flowers that set fruit. Fruit set per plant was quantified by counting the fraction of fruits
that were formed from each experimental flower (N = 3 per treatment per replicate plant).
Thus if none of the three experimental flowers of a tree produced fruits, the input was 0;
if only one flower out of three produced fruit the input was 0.33, for two fruits the input
was 0.66, and for three fruits the input was 1.00. Individual plants (N = 20) were treated
as complete “blocks” where all treatments were represented and equally replicated. Then,
I performed a pairwise Wilcoxon Signed Rank test with a Bonferroni correction.
Data Analysis: Comparing seed number and viability among pollination
treatments- Seed set and seed germination was assessed first with a Multivariate Analysis
of Variance (MANOVA) because I measured multiple and correlated response variables
on the same set of experimental factors. Following significance of this analysis (and as
recommended by Scheiner 1993), I conducted post-hoc univariate tests of each response
variable separately using non-parametric ANOVA and General Linear Models, from
15
JMPIN software (version 4.0.2; SAS Institute 2000). For the MANOVA, two response
variables were entered: seed number per flower, and percentage of seed germination per
flower. Factors used were pollination treatment, individual plant, and the interaction
between pollination treatment and individual plant. After a detection of significant
differences in MANOVA, I performed univariate tests, including a Kruskal-Wallis nonparametric ANOVA, to test for differences in seed germination rates. Next I conducted
pairwise Wilcoxon Signed Rank tests with a Bonferroni correction to find which
treatments were significantly different from each other. To test for treatment effects on
seed number and viability, I used the General Linear Model (GLM) platform of JMPIN
(version 4.0.2; SAS Institute 2000) because these variables were continuous. As in
MANOVA, I used the pollination treatments, the individual plant, and the interaction
between pollination treatment and individual plant as independent variables.
16
Results
Mating system, pollinators, and pollination efficiency- Fruit set varied
significantly between pollination treatments (Figure 1). The highest yield (70%) was
obtained in hand-outcrossed flowers followed by exposed flowers (about 50%; Figure 1).
The lowest rates of fruit set were from the selfed, geitonogamy and bagged pollination
treatments (7%, 8% and 3% respectively; Figure 1). Flower visitation by both C. flaveola
and A. mellifera resulted in fruit set and there was no significant difference (P > 0.05)
between the amount of fruits produced by these animals (21% and 28% respectively;
Figure 1).
Seed set obtained from the pollination treatments followed the same general
pattern documented for fruit set (Figure 2). That is, flowers that were outcrossed had
significantly more seeds than all the other treatments, and the selfed, geitonogamy and
bagged pollination treatments had the fewest seeds. However, unlike fruit set, selfed,
geitonogamy and bagged treatments had similar numbers of seeds as C. flaveola and A.
mellifera pollination treatments (P values > 0.05). Again, seed set of flowers pollinated
by C. flaveola and A. mellifera were not significantly different.
Seed germination tests generally behaved similarly to fruit and seed set. Once
again, the outcrossed treatment had the highest percent germination and was not
statistically different (P > 0.05) from the exposed pollination treatment. Selfed,
geitonogamy and bagged treatments obtained the lowest germination percentages, and
were not statistically different from C. flaveola and A. mellifera treatments. Finally, seed
germination for C. flaveola and the A. mellifera visits were also not significantly
different.
17
Although two of the response variables (i.e. seed set and germination) were
positively correlated with each other, the MANOVA test detected significant differences
among pollination treatments, individuals, and the interaction between both (Table 2).
The pollination treatment explained most of the variance (81.3%), with 13.1% resulting
from individuals, and only 5.6% explained by the interaction between pollination
treatments and individuals. The regression model (r2) explained 57% of the variation.
Floral emasculations- None of the pollination treatments involving flower
emasculation were significantly different from their non-emasculated counterparts in
terms of fruit set, seed set, and seed germination (see Figures 1, 2 and 3).
18
Discussion
I found that G. elegans is mainly self-incompatible and requires cross-pollination
for successful fruit set. I also found that the two most common flower visitors (C.
flaveola and A. mellifera) were pollinators of G. elegans flowers with similar pollination
efficiency.
Mating system- The predominance of outcrossing in Goetzea elegans is consistent
with numerous studies that have found a prevalence of self-incompatibility (of varying
degrees) in the tropics (Bawa 1992, Ward et al. 2005) from Central America (e.g. Bawa
et al. 1985, Murawski & Hamrick 1991, Pérez-Nasser et al. 1993, Hall et al. 1994,
Boshier et al. 1995, Gibson & Wheelwright 1996, James et al. 1998, Ghazoul & McLeish
2001), South America (e.g. Doligez & Joly 1997, Jaimes & Ramírez 1999, Lacerda et al.
2001, Dick et al. 2003), and tropical Asia (Thomas & LaFrankie 1993, Murawski et al.
1994, Finkeldey et al. 1999, Kenta et al. 2002). In addition, outcrossing -resulting from
either dioecy or self incompatibility- has been reported among Caribbean plants,
including both non-woody (e.g. Negrón 1987, Aragón & Ackerman 2004, Sánchez
Cuervo 2006, Tremblay et al. 2006) and woody species (Hernández-Prieto 1986, Rojas
1994, O'Reilly 1995, González-Rodriguez 1998, Rathcke 2001, Morales Martinez &
Saralegui Boza 2002, Dunphy et al. 2004).
The maintenance of outcrossing, and its self-incompatibility mechanism in
hermaphrodite plant species has been explained as a mechanism that probably evolved to
avoid the negative effects of inbreeding (Charlesworth & Charlesworth 1979). Moreover,
outcrossing plants generally increase allele recombination and thus, genetic variability of
populations (Hamrick et al. 1979, Loveless & Hamrick 1984, Hamrick & Godt 1989,
19
Wyatt et al. 1992). Gene recombination is very important for plants that are found in
small populations (e.g., islands) because, due to founder effects, there is lower genetic
diversity expected in early stages after colonization (Pfosser et al. 2005). Therefore, G.
elegans may increase its capacity for gene flow and promote genetic diversity through
outcrossing. In this study, all experimental G. elegans trees were siblings, and it is
possible that the importance of outcrossing in wild populations was underestimated. In a
previous study, Santiago-Valentín (1995) found similar levels of outcrossing and selfing
among G. elegans trees from different genetic backgrounds. Nevertheless, the scattered
distribution of the extant G. elegans, and the considerable geographic distance among
populations could prevent optimal outcrossing, and possibly compromise the genetic
diversity of populations. Future studies should study the impact of isolation on the
genetic diversity and fecundity of G. elegans.
Goetzea elegans is not completely self-incompatible because some fruits with
viable seeds were produced in the pollination treatments with selfed pollen (Figures 1, 2
and 3). Although outcrossing assures genetic variability of populations, a degree of selfcompatibility ensures reproduction in isolation when outcrossing is not successful or
possible. This could be relevant in island plants, where a self-incompatibility mechanism
may be a disadvantage to founding a new population, if the colonizer is a single
individual (Baker 1955).
Fruit set, seed set, and seed germination of non-emasculated bagged flowers were
similar to selfed hand-pollinations (Figures 1, 2 and 3), demonstrating that G. elegans
flowers have the capacity of being pollinated in the absence of animal vectors (i.e.
automatic self-pollination). Autogamy was facilitated by the proximity of the anthers to
20
the stigma due to the similar length of the reproductive whorls in the majority of the
examined flowers. I observed, however, that a small number of trees presented either
reverse or approach herkogamy. The disparity in length of the stamens and the style in
these trees prevented them from performing autogamy, and could be interpreted as an
additional mechanism to promote outcrossing (e.g. Ennos 1981, Thomson & Stratton
1985, Barrett & Shore 1987, Ritland & Ritland 1989, Barrett & Husband 1990, Murcia
1990, Motten & Antonovics 1992, Belaoussoff & Shore 1995). Finally, no fruits were
obtained in the emasculated bagged flowers, demonstrating that G. elegans does not
produce fruits by apomixis, and therefore, requires pollen deposition for reproduction.
Effectiveness of Native and Introduced Pollinators- The pollination role of C.
flaveola in G. elegans contrasts with their robbing behavior reported in a number of
studies on flower visitation by birds in Caribbean plant species (e.g. Snow & Snow 1971,
Kodric-Brown et al. 1984, Hernández-Prieto 1986, Askins et al. 1987, Neill 1987,
Greenlaw 1990, Ricart 1992, Fumero-Cabán & Meléndez-Ackerman 2007). These
differences could be due to size dissimilarities between culmen and floral structures. For
instance, the short size of the corolla tube in G. elegans (11.11 ± 1.6 mm in length, and
10.20 ± 1.6 mm in width [mean ± S.D.]; Santiago-Valentín 1995) makes it easy for C.
flaveola (culmen length = 13.2 ± 0.7 mm; Santiago-Valentín 1995) to access nectar. In
addition, the exerted stamens promote pollen deposition on the bird’s forehead and
consequently, pollen transport. In contrast, robbing by C. flaveola has been reported in
flower species with longer corolla tubes (exceeding 19 mm in length; Table 3) where
legitimate access to the flower nectaries by short-culmen birds is prevented by the
disparity between bill and corolla length. In addition, species with very narrow corolla
21
tubes complicate even more the effectiveness of nectar acquisition, reducing the
possibilities of legitimate visitation. Although most studies indicate that C. flaveola is a
nectar robber (e.g. Kodric-Brown et al. 1984, Hernández-Prieto 1986, Askins et al. 1987,
Fumero-Cabán & Meléndez-Ackerman 2007), a few have found the species to be a
legitimate flower visitor (Feinsinger et al. 1979, Steiner 1979, Ricart 1992, Sazima et al.
1993, Sazima & Sazima 1999, Rathcke 2000). Three of these studies demonstrated its
role as a pollinator (Feinsinger et al. 1979, Sazima & Sazima 1999, Rathcke 2000). Ricart
(1992) determined that robbing or legitimate visitation behavior by C. flaveola was
dependent on corolla length.
The pollination of G. elegans by A. mellifera agrees with studies documenting
their beneficial role as pollinators of native plant species (Paton & Turner 1985,
Hernández-Prieto 1986, Vaughton 1992, Paton 1997, Dick 2001, Gross 2001, Dick et al.
2003, Fumero-Cabán & Meléndez-Ackerman 2007). However, in some studies A.
mellifera proved to be detrimental to the pollination of native plants (Paton 1993, Rojas
1994, Gross & Mackay 1998, do Carmo et al. 2004). Our results support the idea that
flower size and design, and behavior of A. mellifera influence pollination, as was found
previously (e.g. Paton & Turner 1985, Ramsey 1988a, Vaughton 1992, Paton 1993,
Vaughton 1996). When an A. mellifera visited flowers to collect pollen, it landed and
crawled throughout the anthers and usually contacted the nearby stigma. However, when
an A. mellifera foraged for nectar, it landed on the inner surface of the corolla lobes from
which it inserted its proboscis into the nectaries (located at the base of the ovary), this
occasionally did not result in pollination.
The pollination efficiency of both A. mellifera and C. flaveola was not statistically
22
different for fruit set, seed set and seed germination (Figures 1, 2 and 3 respectively).
This finding differs from previous studies where A. mellifera has been found to be a less
efficient pollinator than native nectarivorous birds (Ramsey 1988a, Paton 1993,
Vaughton 1996, Hansen et al. 2002, Celebrezze & Paton 2004). The lack of significant
difference in this study might be due to characteristics of the experimental site. The study
site included many trees in a small area (< 100 m2), and both vectors can easily perform
cross-pollination through the group. However, in the wild, distance between neighboring
trees may vary from a couple to several hundred meters and these vectors might behave
differently. Under wild conditions, A. mellifera has been found to promote geitonogamy
by restricting its foraging trips to densely flowering plants or to nearest neighbors (Paton
1993, Celebrezze & Paton 2004). On the other hand, C. flaveola behave like other
nectarivorous birds (Wunderle 1981), which have high-energy demands and move
frequently between plants while foraging (Paton 1986, Paton 1993, Vaughton 1996),
thereby promoting gene flow by outcrossing (Ramsey 1988b).
Single visits of both C. flaveola and A. mellifera produced less fruit set (Figure 1),
seed set (Figure 2) and seed germination (Figure 3) than exposed flowers. This suggests
that repeated visits to the flowers of G. elegans, which remained open an average of 3.4
days (S.D. ± 0.82; Santiago-Valentín 1995), are necessary to increase the probability of
pollen deposition. However, the outcrossing treatment achieved higher quantities of
fruits, seeds and higher germination rates than the exposed flowers, probably because this
artificial pollen deposition prevented geitonogamy or deposition of foreign pollen from
other plant species that can contaminate or obstruct the stigma. In contrast to fruit set,
seed set, and seed germination from single-visited flowers by C. flaveola and A.
23
mellifera, results from hand-selfed pollination treatments were not significantly different
(Figures 2 and 3). This could indicate that a significant proportion of pollen deposition
might be the result of geitonogamy. Some studies (e.g. Hessing 1988) have found that
geitonogamy is promoted when a single plant offers many flowers at the same time.
Cultivated G. elegans trees used in this study usually exhibited several dozens of flowers
at once, which increases the probability of geitonogamous pollination. I anticipate this
behavior to be present in larger wild trees, where thousands of flowers are presented to
visitors at once.
Floral emasculations- Flower emasculation did not produce any significant
difference for fruit set, seed set nor seed germination (Figures 1, 2 and 3), probably
because pollen present in mature anthers is not interfering (i.e. blocking or clogging) with
pollen deposition on the stigma by animal visitation or hand pollination of the flower.
Alternatively, pollen vigor can be an important factor. For example, selfed pollen has
been found to germinate later, to grow slower, and die earlier than outcrossed pollen and
thus, it cannot compete effectively for flower pollination (Cruzan 1989, Aizen et al.
1990, Harriss & Whelan 1993, Snow & Spira 1993). Also, some studies have found that
seed number per fruit was mainly affected by the quality and quantity of pollen received
(Bertin 1990, Colling et al. 2004). Pollen used to perform hand-pollinations was of
similar quality for both non-emasculated and emasculated flowers and thus, a factor that
could explain the similarity of their outcomes. However, some studies have found that
large amounts of self-pollen may congest the stigma surface, reducing subsequent
germination of compatible pollen and negatively affecting seed set (Galen et al. 1989,
Waser & Price 1991), but in this study I did not detect such effects.
24
Implications for conservation of Goetzea elegans- In this study, I report a case
where the introduced honeybee A. mellifera is a pollinator of an island-endangered tree.
This insect species proved to be as efficient as the native bird C. flaveola in pollinating G.
elegans. Current human threats to G. elegans survival are habitat destruction or
modification, including clearing for agriculture, selective logging for fence posts, and
limestone quarrying. These activities have resulted in the isolation of individual trees,
decreasing the possibilities for outcrossing. Although nearly all G. elegans populations
are restricted to small canyons or ravines, which also shelter important populations of
some other rare and endangered plants and animals, none of these areas have legal
designation for protection. Propagation efforts and establishment of ex situ populations
has been initiated in protected areas (Rafael Rivera [Conservation Trust of Puerto Rico],
pers. comm.). Establishment of these populations must consider distance between planted
individuals, as this will assure proper pollen transfer and fruit set. Although this study
demonstrates the positive influence of A. mellifera on G. elegans, there is another exotic
species that negatively disrupts the reproduction of this tree species: Rattus norvegicus
Berkenhout. During the course of this study, I found evidence of seed predation by this
rodent in both wild and cultivated trees. Further studies should investigate the extent of
this impact on seedling recruitment of G. elegans.
25
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35
Tables
Table 1. Flower treatments used to determine the breeding system of Goetzea elegans,
with remarks and purpose for each treatment.
Flower Treatments
Non-emasculated
exposed flowers
Emasculated exposed
flowers
Remarks
Flower exposed to all visitors
Purpose
Test for natural pollination
Flower exposed to all visitors
Test for natural pollination
excluding selfing possibility
Non-emasculated bagged
flowers
Flower restricted to all visitors
Test for automatic self-pollination
(autogamy) in the plant
Emasculated bagged
flowers
Flower restricted to all visitors
Test for apomixis in the plant
Non-emasculated
outcrossed flowers
Emasculated outcrossed
flowers
Hand-pollinated flower using pollen
from different individuals
Hand-pollinated flower using pollen
from different individuals
Test outcrossing pollination
Non-emasculated
geitonogamied flowers
Hand-pollinated flower using pollen
from another flower of the same
individual
Test self-compatibility degree in
the plant
Emasculated
geitonogamied flowers
Hand-pollinated flower using pollen
from another flower of the same
individual
Hand-pollinated flower with its own
pollen
Flower visited once by Coereba
flaveola
Test self-compatibility degree in
the plant excluding selfing
possibility
Test self-compatibility degree in
the plant
Test pollination efficiency by a
bird vector
Flower visited once by Coereba
flaveola
Test pollination efficiency by a
bird vector excluding selfing
possibility
Non-emasculated selfed
flowers
Non-emasculated
Coereba flaveola
controlled visits
Emasculated Coereba
flaveola controlled visits
Non-emasculated Apis
Flower visited once by Apis mellifera
mellifera controlled visits
Emasculated Apis
Flower visited once by Apis mellifera
mellifera controlled visits
36
Test outcrossing pollination
excluding selfing possibility
Test pollination efficiency by a
insect vector
Test pollination efficiency by a
insect vector excluding selfing
possibility
Table 2. Results of MANOVA for individual pollination treatments and their interaction.
________ _df__________
Source
Pillai’s trace Approx. F
Whole model
0.937
1.77
Individual
0.209
3.19
Treatments
0.376
10.04
Individual x Treatment
0.704
1.24
37
Numerator
518
38
24
456
Denominator
P__
1040
<0.001
1040
<0.001
1040
<0.001
1040
0.003
Table 3. Corolla-tube lengths of flowers visited by C. flaveola and type of visit
performed in the flower. Visits reported by: 1. Feinsinger et al. 1979, 2. Kodric-Brown et
al. 1984, 3. Hernández-Prieto 1986, 4. Askins et al. 1987, 5. Greenlaw 1990, 6. Ricart
1992, 7. Santiago-Valentín 1995, 8. González-Rodríguez 1998, 9. Sazima and Sazima
1999, 10. Rathcke 2000, and 11. Fumero-Cabán & Meléndez-Ackerman 2007. If report
not specifies corolla-tube length, it was obtained from: García & Kolterman 1992 (*),
Liogier 1995 (), Liogier 1997 (), Acevedo-Rodriguez 2005 (), Acevedo-Rodriguez &
Strong 2005 (), or direct measurements of specimens from UPR and UPRRP herbariums

( ).
Corolla tube
length (mm)
Type of visit by
Coereba flaveola
Plant Species
Family
mean ± SD
Coccoloba sintenisii Urban6
Polygonaceae
4-5
Legitimate
Calliandra locoensis Garcia & Kolterman8
Mimosoideae
3-4.5*
Legitimate
Renealmia antillarum (Gagnep.) Moscoso6
Zingiberaceae
6-12
Legitimate
Erythrina poepigiana (Walp.) O.F. Cook1
Faboideae
6-14
Legitimate
Lantana camara L.6
Verbenaceae
7-10
Legitimate
Palicourea crocea (Sw.) Roem. & Schultes6
Rubiaceae
8-12
Legitimate


Legitimate/
4, 5
, 4
Boraginaceae
10-32
Robber
Engler & Prantl6
Gesneriaceae
11-19
Legitimate
Goetzea elegans Wydler7
Solanaceae
11.11 ± 1.6
Legitimate
Aechmea distichantha Lem.9
Bromeliaceae
12.4 ± 1.7
Legitimate
Aechmea bromeliifolia (Rudge) Baker9
Bromeliaceae
15.1 ± 0.9
Legitimate
Pavonia bahamensis Hitchc.10
Malvaceae
18.1 ± 1.7
Legitimate
Klotzsch9
Bromeliaceae
18.8 ± 1.7
Legitimate
Tecoma stans (L.) Juss. ex HBK.5
Bignoniaceae
27-35
Robber
Cordia rickseckeri Millsp.2
Boraginaceae
29.6 ± 1.7
Robber
Cordia sebestena L.
Gesneria pedunculosa (A.P. DC.) Fritsch in
Acanthostachys strobilacea (Schult. f.)
38

Ipomoea arenaria (Choisy) Steud., non
Roem. & Schult.2
Convolvulaceae
31.9 ± 2.5
Robber
Tabebuia rigida Urban3
Bignoniaceae
33.8 ± 7.3
Robber
Ipomoea repanda Jacq.2, 6
Convolvulaceae
34.4 ± 2.4
Robber
Tabebuia schumanniana Urban2
Bignoniaceae
34.8 ± 4.0
Robber
Tabebuia haemantha (Bert.) DC.2, 6
Bignoniaceae
36.0 ± 2.7
Robber
Pitcairnia angustifolia Aiton.11
Bromeliaceae
38.2 ± 2.22
Robber
Neorudolphia volubilis (Willd.) Britton6
Faboideae
40-55
Robber
39
Figure Legends
Figure 1. Average frequency of fruit set among emasculated and non-emasculated
pollination treatments in G. elegans flowers. Different letters indicate statistical
differences among treatments ( = 0.05).
Figure 2. Average frequency of seed set per flower among emasculated and nonemasculated pollination treatments in G. elegans flowers. Different letters indicate
statistical differences among treatments ( = 0.05).
Figure 3. Average frequency of seed germination per flower among emasculated and
non-emasculated pollination treatments in G. elegans flowers. Different letters indicate
statistical differences among treatments ( = 0.05).
40
G
Pollination Treatment
41
to
ed
y
D
gg
m
25
Ba
ga
d
d
l fe
se
os
Se
cr
no
ut
d
B
ei
O
se
A
po
50
Ex
a
ra
ol
lif
e
ve
el
la
m
.f
A.
C
Average Percent of Fruit Set (± S.E.)
100
Emasculated
Non-Emasculated
75
C
BC
B
AB
AB
A
AD
D
D
0
D
G
42
Pollination Treatment
0.5
A
ed
y
C
gg
m
3
Ba
ga
d
d
lfe
se
2
Se
cr
os
d
B
no
ut
se
2.5
ei
to
O
a
ra
ol
el
lif
e
ve
A A
Ex
po
m
la
1
A.
C
.f
Average Seeds per Flower (± S.E.)
3.5
Emasculated
Non-Emasculated
BC
B
1.5
A
A
A
A
A
A
0
G
43
Pollination Treatment
ei
to
y
ed
m
gg
ga
A
Ba
no
d
d
lfe
se
B
Se
cr
os
d
AB
ut
se
A
O
a
ra
ol
el
lif
e
ve
A
Ex
po
m
la
25
A.
C
.f
Average Percent of
Seed Germination (± S.E.)
100
Emasculated
Non-Emasculated
75
B
50
B
B
A
A A
A
0
A
Chapter II
When number of flowers and distance to neighbors affects fecundity: the case of the
endangered tropical tree Goetzea elegans Wydler (Solanaceae)
44
Abstract
Many tropical tree species are dioecious, self-incompatible, and have sparse spatial
distributions. Each of these characteristics or any combination of them can easily lead to
the reproductive isolation of plants and to reproductive failure. Here I examined the
impact of reproductive isolation in Goetzea elegans (Solanaceae), a primarily selfincompatible tropical tree endemic to Puerto Rico. I tested for the effects of distance to
conspecifics and plant traits such as size, number of flowers (e.g., blooming intensity),
and flower neighborhoods on fecundity. Blooming intensity and distance to nearest
neighbor were the most important factors explaining pollinator visits, fruit set, and seed
germination. Blooming intensity increased visitation by pollinators, resulting also in
increased fruit set and germination success. In contrast, greater nearest neighbor distances
had a negative effect on pollinator visitation, fruit set and germination success. Results
indicate that isolation is detrimental to this mainly self-incompatible species, because
promotes reduction of pollinator visits and subsequent decrease in fruit set and seed
germination. However, blooming intensity increased pollinator visits and fecundity, and
could compensate for the negative effects of isolation.
45
Introduction
Many of the most fundamental relationships between plants and their animal
consumers (e.g., herbivores, pathogens, seed dispersers, and pollinators) are mediated by
space, especially by density and distance to intra and interspecific neighbors (Janzen
1970, Connell 1971, Johnson et al. 2003, Carlo 2005). However, the explicit role of
spatial patterns in these biological processes (i.e., spatial ecology) has not been well
studied.
Spatial patterns within plant populations could influence reproductive efficiency,
especially for self-incompatible plants that are pollinated by animals. Here, success in
pollen transfer among individuals could be severely compromised by long distances,
resulting in lower fecundity (Domínguez 1990). Thus, pollinator behavior could
determine reproductive success because low rates of visitation may result in decreased
seed set (Jennersten 1988, Burd 1994). Low seed set could also result from small
population sizes (Burd 1994), inbreeding depression in recently established populations,
or inbreeding depression from increased selfing rates (Ellstrand & Elam 1993). Seed set
is also affected by other factors such as plant height (Klinkhamer & de Jong 1990, Kearns
& Inouye 1993, Ohara & Higashi 1994, Conner & Rush 1996), asynchronous flowering
between individuals (which reduces inbreeding) (Linhart 1973, Stephenson 1982, Bawa
1983, Frankie & Haber 1983, Schmitt 1983), and the position of the flower in the plant
(Shaw & Allard 1982). Furthermore, presence of interspecific neighbors that share
pollinators might affect seed set via competition or facilitation.
Isolation of plant species can be detrimental to plant fecundity because it
decreases seed set and affects recruitment (Wright 1943, 1946; Klinger et al. 1992,
46
Groom 2001). This negative impact on reproduction is particularly evident in selfincompatible plants (see Wright 1943, 1946; Klinger et al. 1992, Aizen & Feinsinger
1994, Groom 2001). The degree of isolation is shaped by factors affecting pollinator
activity (Linhart 1973, Haddad & Tewksbury 2005), such as the spatial structure and size
of a plant population (Bosch & Waser 1999, Mustajarvi et al. 2001), and landscape
connectivity (Haddad & Tewksbury 2005). Isolation and its implications for fecundity is
of special interest for tropical trees because of the sparse spatial distribution of many
species (Wright 2002), the prevalence of self-incompatibility and dioecy (e.g. Yap 1980,
Chan 1981, Bawa et al. 1985, Bawa 1992, Ward et al. 2005), and their dependence on
animals to perform pollination.
Animal-plant interactions can be affected by perturbations including deforestation
and fragmentation (Whitmore & Sayer 1992, Heywood et al. 1994, Trejo & Dirzo 2000,
Severns 2003). Forest cutting results in reduced tree population size or trees isolated from
other conspecifics. These scenarios lead to limited gene flow and low reproductive
success (Templeton et al. 1990, Young et al. 1993, McCauley 1995, Nason & Hamrick
1997, Aizen et al. 2002), because population density is often positively correlated with
plant fecundity (Sih & Baltus 1987, Waser & Price 1991, Agren 1996, Kunin 1997,
Bosch & Waser 1999). Therefore, tropical self-incompatible plants can be sensitive to
environmental transformation and fragmentation, as those could result in a population
decline and possible reproductive isolation. The objective of this study is to examine the
effect of spatial distribution on the fecundity and pollinator visitation of the selfincompatible tropical tree Goetzea elegans. Specifically, I examined how fecundity is
affected by distance to conspecifics and by flower abundance.
47
Materials and Methods
Study species - Goetzea elegans Wydler (Solanaceae) is an endangered tree (U.S.
Fish and Wildlife Service 1987) endemic to Puerto Rico, and a member of an ancient
Caribbean-lineage in the Solanaceae (Santiago-Valentín & Olmstead 2003). Previous
studies have been conducted on its reproductive and population ecology (SantiagoValentín 1995), and its pollination biology (see chapter I), showing that the species is
mainly self-incompatible and requires animal vectors for successful pollination.
Goetzea elegans pollinators include one native bird and one introduced insect.
The native bird is the Bananaquit Coereba flaveola Bryant (Coerebidae), a nectarivorous
and very common species in Puerto Rico and across the Caribbean. This bird has been
described as a common nectar robber in flowers (e.g. Kodric-Brown et al. 1984).
However, in G. elegans it only performs legitimate visits (see chapter I).
The other flower pollinator of G. elegans is the common Honeybee Apis mellifera
L. (Apidae). This introduced bee is commonly found throughout the island in managed
and wild colonies visiting wild flowers. In spite of this, there are very few studies dealing
with the impact of this naturalized pollinator over reproduction of native plants (e.g.
Fumero-Cabán and Meléndez-Ackerman 2007).
Study area - This study was conducted on the largest known natural population of
G. elegans located at Quebrada Bellaca (18°28’30” N, 66°54’14” W), in the municipality
of Quebradillas, in the karst region of Northwestern Puerto Rico (Lugo et al. 2001).
Quebrada Bellaca is a wooded seasonally dry ravine, with some segments forming small
canyons that drain north into the Atlantic Ocean. Elevations along the Quebrada range
48
from 20 to 100 m above sea level. The area is classified as Subtropical Moist life zone
sensu Holdridge (Ewel & Whitmore 1973).
Tree characterizations - All G. elegans individuals in the study site were mapped
using a Trimble® Global Positioning System (GPS) with an accuracy of 2 meters.
Distances between trees were calculated using the Hawth’s tool (version 3.26; Beyer
2004) in ARCGIS 9 (ARCMAP version 9.1; ESRI, Redlands, California), and a digital
map of all G. elegans in the site was generated. Descriptive features recorded for
individual trees included height, diameter at breast height (DBH), and crown area. Crown
area was quantified by measuring the width and the length of the crown shade, and by
applying a circle area formula (a =  r2).
Pollinator visitations - I recorded G. elegans pollinator visits using systematic
focal observation of 25 randomly selected trees. I observed each focal tree for four-hour
periods: two hours in the morning from 0800-1000 am, and two hours in the afternoon
from 1500-1700 pm on the same day, for a total of 100 hours of observation. I selected
these periods to capture peaks of foraging activity for both C. flaveola and A. mellifera in
the study site (pers. obs.). I randomly selected a branch on the top of each focal tree and
there I recorded the total number of flowers, the number of flowers visited by each
pollinator, and the number of flowers of conspecifics and of other species present in a 20meter radius from the focal tree.
I applied a multiple regression model to assess the effects of G. elegans flower
crop size and neighborhood variables (i.e., flowers in the neighborhood) on the frequency
of pollinator visits. In the model, the response variable was the number of pollinator visits
(i.e., C. flaveola, A. mellifera, pooled species) and the explanatory variables were number
49
of flowers, height, DBH, crown area, distance to nearest neighbor, and number of
flowering conspecifics and interspecifics in the neighborhood of each sampled tree. I
input all these variables in the model (Standard Least Square) selected with a stepwise
backward procedure with probability to remove a variable set to 0.10 using JMPIN
software (version 4.0.2; SAS Institute 2000).
Fecundity measures - I measured fecundity for each individual tree by quantifying
fruit set and seed germination. All individuals of G. elegans in the population were
monitored during the peak flowering season from January to May 2005. Every week, I
collected all aborted ovaries (enclosed within the calyx), corollas, fruits and seeds from
underneath each tree and counted them. Fallen flowers and fruits were confidently
assigned to the tree above them, as they are sheltered from winds by the high rock walls
(of up to 50 meters) that form the ravine. I measured fruit set by collecting all fruits under
a tree each week, from which up to 32 fruits per tree were randomly selected to test seed
germination. The remaining fruits were removed from beneath the parental tree and
dispersed to the surrounding forest in places where other G. elegans trees were not
present. Seed germination tests were carried out at the Conservation Trust of Puerto Rico
nurseries (located within the UPR Botanical Garden grounds in Río Piedras) in a humid
peat moss bed with low sunlight conditions. Fruits collected in a particular week were
considered to have been produced from flowers that opened 45 days earlier, as this is the
approximate mean time for a G. elegans fruit to mature after pollination (SantiagoValentín 1995).
Blooming intensity was defined as the pooled sum of both aborted ovaries and
fruits found under each tree in April. Percent of fruit set was calculated for each
50
individual by dividing the number of fruits by the blooming intensity and then
multiplying by 100. I used least square multiple regression models to test the effects of
height, DBH, crown area, distance to nearest neighbor, and blooming intensity on two
response variables: fruit set and seed germination. I included all variables and interaction
terms in a procedure that combined backward, and forward stepping to select the best
model using JMPIN software (version 4.0.2; SAS Institute 2000), with probability of
stepping predictor variables set to 0.1.
51
Results
Pollinator visitations - I recorded 7654 pollinator visits to flowers of Goetzea
elegans by two animal species. The most frequent visitor was the Bananaquit (Coereba
flaveola, Coerebidae), providing 94.7% of the flower visits. The remaining 5.3% of the
visits were provided by the Honeybee (Apis mellifera, Apidae). Both animals are known
to pollinate with similar efficiency (see Chapter 1). More than half (i.e., 57%) of all
pollination visits were performed by C. flaveola during afternoon hours. This is in
contrast with visitation by A. mellifera, which was observed mostly during morning hours
(77.3 % of all reported A. mellifera visits).
Of the potential explanatory variables tested (i.e., nearest conspecific neighbor,
blooming intensity, height, crown area, and DBH) only blooming intensity and distance
to nearest neighbor were important predictors of pollinator visits (Figure 1 panels A & B,
respectively). I also tested other variables such as presence of flowering conspecific and
interspecific neighbors, but they were not important in explaining pollinator visits. In the
model, blooming intensity was the most important factor explaining 95% of the variance
in visitation, while distance to nearest neighbor explained only 5% of the variation.
Fecundity measures - As in the case of pollinator visits, the important explanatory
variables predicting fruit set and percentage seed germination were the distance to nearest
flowering neighbor and blooming intensity (Figures 1, panels C through F). Distance to
nearest neighbor was inversely related to fruit set and percentage seed germination
(Figure 1 panels D & F). Fruit set decreased significantly when distance to nearest
neighbor increased (Table 1, Figure 1 panel D). When distance to nearest conspecific
neighbor was greater than 45 meters, fruit set dropped to below 50%. Distance to nearest
52
neighbor was the most important factor in the model explaining 73% of the variance in
fruit set. This was followed by blooming intensity, which was positively correlated with
fruit set, but explained only 27% of the variance. In a parallel pattern, seed germination
decreased (i.e., below 85%) when distance to nearest neighbor was greater than 40
meters. The highest germination values were observed on nearest neighbors that were
within 20 meters. In fact, the only plants in the sample that achieved germination rates of
100% were individuals with blooming neighbors within a distance of 4.5 meters. On the
other hand, blooming intensity was positively related to seed germination (Figure 1 panel
E), and explained more of the variance (i.e. 57%) in germination success than distance to
nearest neighbor (43%).
53
Discussion
In this study I found that distances to nearest reproductive neighbors and
blooming intensity are factors determining pollinator visits, fruit set, and seed
germination in Goetzea elegans. The negative correlation between pollinator visitation
and distance among trees is in agreement with previous studies, in which pollinators are
more attracted to groups than to isolated plants (Figure 1 panel B; e.g. Klinkhamer et al.
1989). Groups of flowering trees can offer a continuous nectar source because of the
large quantity of available flowers, contrasting with isolated trees, where flowers can be
limited and nectar supply quickly exhausted (Pyke 1984, Sih & Baltus 1987). In addition,
and as in other plants (e.g. Steffan-Dewenter & Tscharntke 1999), the negative effects of
isolation on reproduction in G. elegans are exacerbated by the presence of a selfincompatible mechanism (Chapter 1). Furthermore, outcrossed pollen boosts seed
viability in G. elegans (Chapter 1), suggesting that low germination rates in isolated trees
may reflect high levels of geitonogamy and reduced outcrossing (Figure 1 panel B).
The positive correlation between high blooming intensity and pollination is
indicative of the dependence of effective visual cues for attracting pollinators, which
perform outcrossing successfully. This is congruent with previous studies that have
demonstrated that visitation is tightly correlated with the number of flowers on a plant
(Thomson 1981, Sih & Baltus 1987, Klinkhamer et al. 1989, Klinkhamer & de Jong
1990, Feinsinger et al. 1991). Although this study does not demonstrate categorically a
“magnet” effect from nearby flowering conspecifics, it is possible that this is occurring in
trees with few flowers that are close to trees with many. Competition from flowering
trees of other species did not compromise reproductive success of G. elegans. In fact, G.
54
elegans appears to have been the preferred resource since the main visitor of flowers in
this site (C. flaveola) was observed visiting mostly the flowers of G. elegans, and less
frequently those of other neighboring species (pers. obs.). However, additional
observations are needed to confirm this contention. In contrast, visits of A. mellifera to G.
elegans flowers were low. This could be due to low density of A. mellifera in the area or
maybe because A. mellifera prefers to visit flowers from other massive flowering species
present in the area. These massive flowering species include Andira inermis (W. Wright)
Kunth ex DC., Mangifera indica L., Persea americana Miller, Roystonea borinquena O.
F. Cook, Spondias mombin L., and Terminalia catappa L.. These species are frequently
visited by A. mellifera throughout tropical America (Ordetx Ros 1952). During this study,
I noticed a leaf shedding patterns that might also influence the attractiveness of this
species. At our site, old G. elegans leaves senesce sparsely throughout the bright green
foliage. These old leaves turn into a deep bright yellow color that is similar to that of the
corollas. These “color spots” might function as bracts to assist flowers to attract
pollinators. Future studies should test this hypothesis.
Blooming intensity also influenced fruit set, but to a lesser extent than distance to
nearest neighbor. I found that percentage fruit set increased with blooming intensity.
This may have occurred because the probability that an individual tree received pollen
from neighboring trees increased when the tree produced many flowers. Some studies
have found that abundance of floral rewards increases pollinator visitation (Willson &
Price 1977, Sih & Baltus 1987, Klinkhamer et al. 1989; Figure 1 panel A). Some studies
have found that the probability of geitonogamy in a plant increases when the tree opens
many flowers at the same time (e.g. Hessing 1988). However, I did not detect a negative
55
impact due to geitonogamy, even though both pollinators (i.e., A. mellifera and C.
flaveola) often visit many flowers in the same tree.
The positive correlation between seed germination and high blooming intensity is
also indicative of the role of adequate floral display for successful reproduction. On the
other hand, trees with few flowers (< 50) obtained 100 % seed germination success. This
is remarkable because they were proportionally more efficient than trees with many
flowers. This high efficiency is, however, linked to the short distances between trees
(here, within 4.5 m; Figure 1 panel F). This may indicate that pollinators are attracted to
and forage among groups of sparsely-flowered trees as if they were a single manyflowered tree, with the advantage that they perform pollen outcrossing throughout the
group. However, in an alternative scenario in which a single sparsely-flowered tree is
isolated, its fecundity could be compromised due to a reduction in pollinator visits
(because of both few flowers [Figure 1 panel A] and isolation [Figure 1 panel B]), and
subsequent failure of outcross pollen to arrive. Therefore, isolated sparsely-flowered trees
are expected to be mainly pollinated by geitonogamous pollen, resulting in a decrease in
fruit set, seed set, and seed germination (Chapter I). The high germination rates recorded
for the many-flowered individuals (Figure 1 panel E) are consistent with previous results
of seed germination obtained after floral manipulations with outcross pollen in G. elegans
(chapter I).
Implications for conservation- To effectively conserve rare plant species, efforts
must not only consider protecting extensive land tracts (Zuidema et al. 1996), but also
pay special attention to the small-scale spatial patterning that is closely connected to their
reproductive biology. Reintroductions for the recovery of Goetzea elegans must target the
56
establishment of new populations on protected lands following reproductively functional
spatial patterns of planting. Based on the present study, trees could maintain up to 100%
germination (in the case of few-flowered trees) if they were separated by 4.5 m or less.
Conversely, germination dropped to less than 50% when trees were more than 41 m
apart.
Many tropical species, such as Goetzea elegans, have suffered extirpation of
populations, severe loss of individuals in a population, and habitat fragmentation that
have contributed enormously to the current scarcity of the species (U.S. Fish and Wildlife
Service 1987). Most of the populations of G. elegans are confined to ravines or small
canyons, areas that were less affected by deforestation and agriculture as they were
considered by humans to be of “marginal” importance. Today the largest population of
the species occurs at our study site, as well as populations of several other rare species
(e.g., Anechites nerium (Aublet) Urban, Erythrina eggersii Krukoff & Moldenke,
Forchhammeria brevipes Urban, Mappia racemosa Jacquin, Ottoschulzia rhodoxylon
(Urban) Urban, Pisonia woodburyana Proctor, nom. ined., Polygala cowellii (Britton) S.
F. Blake and Psychilis kraenzlini (Bello) Sauleda) exist primarily in these ravines.
Preserving these relict populations is fundamental in addition to any ex situ conservation.
However, those populations will be a long-term valuable tool as long as populations are
functional in every step of the life cycle.
The population of G. elegans at Quebrada Bellaca appears to be healthy since the
pollinator is thriving, most of the trees that were reproductively active produced fruits to
some extent (evidence of outcrossing), and comprises individuals of all growth stages
(i.e., evidence of recruitment). However, this population faces severe dispersal limitation,
57
as nearly all of the individuals are found inside of the ravine. Although some remnant
trees that have been found in wooded hills or in pastures indicate that the habitat of the
species included moist lowland forests, I did not find any evidence of recruitment outside
the ravine. The surrounding grasslands are unsuitable for recruitment (Santiago-Valentín
1995).
I hypothesize that, because fruits float in water, the current dispersal agent of the
species is the intermittent water flow that moves through the ravine after heavy rain
events. Since all the recruitment takes place at the bottom of this intermittent drainage
system, high mortality of seedlings and saplings is anticipated. Therefore, effective
pollination and high fruit yield might be hindered by high mortality rates at early stages. I
do not eliminate the possibility that the species used to be dispersed by animals that no
longer exist on the island. In either case, for the species’ survival, humans will need to
take an active role as seed dispersers for G. elegans, a role that needs to be done using
schemes that reduce the reproductive isolation of the individuals by creating floral
neighborhoods.
58
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63
Table
Table 1. Results of the Standard Least Square multiple regression models testing the
effects of distance to nearest neighbor and blooming intensity (i.e., the number of flowers
in a plant) of G. elegans over pollinator visits, fruit set, and seed germination.
Variable
Pollinator Visits
Estimate (F ratio)
Fruit Set
Estimate (F ratio)
Germination Success
Estimate (F ratio)
Blooming
2.14 (F2,22 = 89.7)*
0.07 (F2,102 = 23.3)**
0.11 (F2,102 = 21.8)*
-0.67 (F2,22 = 89.7)***
-0.20 (F2,102 = 23.3)*
-0.18 (F2,102 = 21.8)*
0.89
0.31
0.30
Intensity
Distance to
Nearest Neighbor
Model r2
Note: All least square models were selected using a backward stepwise procedure (all
variables and interactions inputted, see methods section for details) with probability to
remove a variable set to 0.1. See Figure 1 for plots of relationships.
* = P < 0.0001, ** = P = 0.0003, *** = P = 0.0082
64
Figure Legend
Figure 1. Blooming intensity (i.e., the number of flowers in a plant) increased pollinator
visits (panel A), fruit set (panel C), and germination success (panel E). In contrast, greater
distance to nearest conspecific neighbor had an inverse relationship over pollinator
visitation (panel B), fruit set (panel D) and germination success (panel F). Horizontal
dashed line indicate fit mean, and diagonal dashed lines indicate 95% confidence interval.
65
B
12
Leverage Residuals
14
Total of Pollinator Visits
Total of Pollinator Visits
14
10
8
6
4
2
0
12
Leverage Residuals
A
2
3
4
5
6
8
6
4
2
-2
1
10
0
7
0
Blooming Intensity
Fruit Set
1.0
0.5
0.0
-0.5
2
3
4
5
6
7
8
Arcsin (Sqrt (Fruit Set)) Leverage Residuals
Fruit Set
Arcsin (Sqrt (Fruit Set)) Leverage Residuals
D
1
0.5
0.0
9
0
Germination Success
0.5
0.0
4
5
6
7
8
9
Blooming Intensity
Arcsin (Sqrt (Germ. Succ.)) Leverage Residuals
Arcsin (Sqrt (Germ. Succ.)) Leverage Residuals
Germination Success
1.0
3
2
3
4
5
log ((Distance to Nearest Neighbor) + 1)
Leverage, P<.0001
1.5
2
1
Distance to Nearest Neighbor
F
1
5
1.0
log ((Blooming Intensity) + 1)
Leverage, P=0.0003
0
4
1.5
Blooming Intensity
E
3
log ((Distance to Nearest Neighbor) + 1)
Leverage, P=0.0082
1.5
0
2
Distance to Nearest Neighbor
log ((Blooming Intensity) + 1)
Leverage, P<.0001
C
1
2.0
1.5
1.0
0.5
0.0
-0.5
0
1
2
3
4
5
Distance to Nearest Neighbor
log ((Blooming Intensity) + 1)
Leverage, P<.0001
log ((Distance to Nearest Neighbor) + 1)
Leverage, P<.0001
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General Conclusions
•
Goetzea elegans, as many other tropical trees, exhibits the best fruit and seed set,
as well as germination from outcrossing, although it is capable of some degree of
selfing.
•
The native nectarivorous Bananaquit Coereba flaveola, and the introduced
Honeybee Apis mellifera are pollinators of G. elegans, both pollinating with
similar efficiency.
•
Goetzea elegans flowers require multiple floral visits from its pollinators for a
good yield of fruits and seeds per fruit, and for a high germination rate.
•
I did not found statistical differences between emasculated and non-emasculated
pollination treatments.
•
Goetzea elegans does not produce fruits by apomixis, and therefore, requires
pollen deposition for reproduction.
•
I found that while G. elegans flower production increases in a tree, also increases
frequency of pollinator visits, fruit set and germination success.
•
In contrast, while distance to nearest reproductive neighbor increases, pollinator
visitation, fruit set and germination success decreases.
•
In conclusion, isolation is detrimental to this mainly self-incompatible species, as
it promotes reduction of pollinator visits and subsequent decrease in fruit set and
seed germination.
•
However, a high number of flowers can increase pollinator visits and fecundity,
and could compensate for the negative effects of isolation.
67