FLOWERING PHENOLOGY AND DENSITY-DEPENDENT POLLINATION SUCCESS
IN CEPHAELIS ELATA (RUBIACEAE)
WILLIAM HUNTOON BUSBY
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN
PARTIAL FULFILLMENT OF THE REQUIREMENTS
FOR THE DEGREE OF DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
I would like to express my thanks to many individuals for helping
to make this study possible. Peter Feinsinger, my major professor,
provided thoughtful guidance through all phases of this work. His
insight and encouragement have been truly appreciated. I am indebted to
the other members of my committee, John Ewel, Richard Kiltie, and
Carmine Lanciani, for valuable suggestions and editorial comments. I
also thank Jack Putz for helpful discussions and for attending my
To the biologists with whom I overlapped at Monteverde I am
especially indebted. My associates from the University of Florida, Greg
Murray, Kathy Winnett-Murray, and Willow Zuchowski-Pounds, provided
helpful suggestions, comradeship, and assistance in the field.
Discussions with Jim Beach were critical to the conception of the study.
I thank Jim Wolfe, Frank Joyce, Sarah Sargent, and Anna Fortenbaugh for
help with the field work. Valuable advice was provided by Yan Linhart,
Sharon Kinsman, Martha Crump, Alan Pounds, Carlos Guindon, Bill Haber,
Eric Dinerstein, Nat Wheelwright, and Rita Shuster.
Personnel of the Tropical Science Center, especially Wolf Guindon
at Monteverde and Joseph Tosi in San Jose, facilitated my use of the
Monteverde Cloud Forest Reserve. Timely logistical support was provided
by personnel of the Organization for Tropical Studies in Costa Rica,
especially Roxana Diaz. Statistical advice was provided by John Saw and
John Cornell at the University of Florida. The study was supported by
the Jessie Smith Noyes Foundation (grant administered by the
Organization for Tropical Studies), the University of Florida Department
of Zoology, and NSF grants DEB 80-11008 to Peter Feinsinger and DEB 80-
11023 to Yan Linhart.
Finally, I extend my warmest thanks to my wife, Anna, for her
support and encouragement during my graduate studies.
TABLE OF CONTENTS
STUDY SITE AND PLANT NATURAL HISTORY................................ 5
METHODS................................. ............................. 17
Controlled Pollinations........................................ 17
Plant and Flower Censuses.......... .................... ........ 18
Observations of Pollinators................................... 19
Analysis of the Visit Data...................... ......... .. 20
Flower Removal Experiment...................................... .. 22
Pollen Carryover............................................... 22
Pollen Receipt................................................. 23
Analysis of Pollen Receipt Data ................................ 24
Pollen Dispersal.............. ....... .... ......... ........... 26
Fruit Set............................. .............. ......... 29
RESULTS......... o................. ....... ..................... ..... 30
Pollinator Identity and Foraging Behavior...................... 30
Effects of Flower Density on Visitation........................ 32
Pollen Carryover................................................. 41
Variation in Pollen Receipt and Fruit Set.................... 41
Effects of Flower Density on Pollen Receipt................... 46
Dispersal of Powdered Dye...................................... 51
Effects of Floral Display Size on Pollinator Behavior and
Pollination Success ............................. ......... 59
Flower Density and Visitation.................................. 64
Effects of Neighbors on Pollination Success.................... 66
Territoriality and Pollination Success......................... 68
Genetic Implications of Plant Density.......................... 69
Implications of Pollination for Reproductive Success........... 70
Floral Display Size and Sexual Function....................... 73
LITERATURE CITED........................................ ............ 77
BIOGRAPHICAL SKETCH................................................. 87
Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
FLOWERING PHENOLOGY AND DENSITY-DEPENDENT POLLLINATION SUCCESS
IN CEPHAELIS ELATA (RUBIACEAE)
William Huntoon Busby
Chairman: Peter Feinsinger
Major Department: Zoology
In cloud forest near Monteverde, Costa Rica, the self-incompatible,
distylous treelet, Cephaelis elata (Rubiaceae), is pollinated by the
hummingbird, Lampornis calolaema. I investigated the importance of two
potentially conflicting relationships affecting pollination service to
C. elata flowers: (1) positive density-dependence in pollinator
visitation, and (2) negative influences of large floral displays and
pollinator territoriality on pollen transfer between plants of different
floral morphs. I measured effects of floral display size, flower
density, and nearest-mate distance on pollen receipt (numbers of stylar
pollen tubes) and pollen donation (measured with powdered dye) at two
sites during two 7-mo flowering seasons.
Lampornis calolaema males defended feeding territories composed of
rich patches of flowers of C. elata and other short-corolla species;
females foraged mainly at dispersed flowers. Due to the small size of
most C. elata floral displays (median = 3 flowers/plant), individual
territories usually contained many plants. Consequently, compatible
pollen transfer within territories was high, and pollination success of
C. elata flowers within territories was often greater than pollination
success outside territories.
At each site, the density and dispersion of flowers influenced
pollination service to flowers. There was, however, considerable
seasonal variation in the strength and, in some cases, even the
direction of the relationships examined. (1) Hummingbird visit rates to
flowers were often highest during seasonal flowering peaks and at plants
with many flowers. (2) Pollen receipt, and occasionally pollen donation,
were greatest during flowering peaks. (3) The amount of pollen received
by flowers was negatively correlated with the distance to the nearest
compatible plant. (4) Presumably due to the spatial segregation of
morphs and limited pollen carryover (measured in the lab with captive L.
calolaema), flowers in dense patches frequently received fewer
compatible pollen grains than isolated flowers. These results suggest
pollination service may be highest at plants that do not produce large
numbers of flowers per day, that spread out flowering over time, yet
still flower in phase with the population.
In hermaphroditic plants, sexual reproduction can occur through
seeds sired as a result of pollen dispersed from male structures of the
flower, or through seeds set after pollen receipt by female structures.
Within a population, variation in the timing and intensity of flower
production by plants can affect both pollen donation and pollen receipt.
Considerable recent attention has focused on the evolution of floral
display size (Willson and Rathcke 1974, Schaffer and Schaffer 1979,
Stephenson 1979, Willson et al. 1979, Wyatt 1980, Augspurger 1980, 1981,
Schemske 1980a_,b, Geber 1985). Most of these studies have examined the
relationship between the number of flowers displayed by inflorescences
or plants and measures of the maternal component of reproductive
success. Although flowering characteristics may reflect differing
selection on male and female function (Janzen 1977, Charnov 1979,
Willson 1979, Stephenson and Bertin 1983, Willson and Burley 1983,
Sutherland and Delph 1984, Sutherland 1986), few studies have examined
the relationship between floral display size and pollen donation
(Schemske 1980a, Bell 1985). The density and spatial dispersion of
flowers on neighboring conspecifics may also influence pollen receipt
(Richards and Ibrahim 1978, Feinsinger et al. 1986) and pollen dispersal
(Levin and Kerster 1969a_,b, 1974, Beattie 1978, Handel 1983).
Furthermore, because conspecific and heterospecific flower density,
pollinator availability, and other environmental factors change
seasonally, the effectiveness of a given plant's floral display in
donating and receiving pollen should vary over time. This topic has
received little attention (although see Schemske 1977, Willson and Price
1977, Woodell et al. 1977). In this study, I examine the effects of the
number of flowers displayed by a plant, conspecific flower density and
dispersion, and seasonal variation in all three, on male and female
components of pollination service.
In zoophilous plants, the effect of the spatial distribution of
flowers on pollination is mediated by the foraging movements of flower-
visiting animals. The density-dependent foraging behavior exhibited by
many pollinators (Levin and Kerster 1974, Heinrich 1979, Linhart and
Feinsinger 1980, Schmitt 1980, Waddington 1980, Real 1981, Zimmerman
1981, Waser 1983a) has several consequences for pollen flow. (1) Visit
rates to flowers or inflorescences are often highest in areas of high
flower concentration (Willson and Price 1977, Silander 1978, Thomson
1981, Roubik 1982). (2) At many-flowered plants, pollinators may visit
large numbers of flowers per plant during each foraging sequence
(Frankie et al. 1976, Feinsinger 1978, Pyke 1978, Schemske 1980b). As a
result, intraplant pollen flow may increase in relation to interplant
pollen flow. For self-incompatible plants, at least, this trend may
lead to lower pollination rates at large plants (Kalin de Arroyo 1976,
Wyatt 1980). (3) As flower density increases, pollinator flight
distances will, on average, decrease (Levin and Kerster 1969a,b, 1974,
Beattie 1976, 1978, Zimmerman 1981), and this may result in localized
pollen flow (see Handel 1983). The relationship between the movements
of pollinators and that of pollen depends on pollen carryover, the
pattern of pollen deposition rom a pollen source on sequentially
visited stigmas. Because pollen carryover is often substantial (Thomson
and Plowright 1980, Price and Waser 1982, Geber 1985, Thomson et al.
1986), pollen dispersal distances will often exceed pollinator flight
distances between flowers (Handel 1983).
In general, pollinator visitation to flowers and pollination
service are expected to be positive functions of flower density (Thomson
1981, 1983, Rathcke 1983, Feinsinger et al. 1986). Yet, due to such
factors as competition among plant species for pollination service
(reviewed by Waser 1983a), sedentary behavior by pollinators at large
plants (Frankie et al. 1976, Kalin de Arroyo 1976, Feinsinger 1978,
Schemske 1980b), or pollinator satiation due to abundant floral
resources (Carpenter 1976, Rathcke 1983), flower visitation and
pollination service may sometimes be unrelated, or negatively related,
to flower density, particularly during flowering peaks.
I addressed the following major questions:
(1)(a) Does the frequency of pollinator visits to flowers increase
with the number of flowers on a plant and with the surrounding density
of flowers? (b) How does the number of flowers visited per plant change
with floral display size?
(2) What is the extent of pollen carryover, and how does it
affect pollen transfer among plants?
(3) What is the effect of the number of flowers displayed by a
plant on pollen donation and pollen receipt?
(4) How is pollen donation and pollen receipt affected by the
density of flowers on neighboring plants?
The study species, Cephaelis elata Sw. (Rubiaceae), is a distylous
treelet with an extended flowering season. This species was chosen for
several reasons. First, being self-incompatible, C. elata is completely
dependent on pollinators that transfer pollen between plants for sexual
reproduction. Evaluation of pollination success is not complicated by
geitonogamy and the relative fitness of inbred progeny. Additionally,
the pollination system is straightforward. At Monteverde, Costa Rica,
the plant is pollinated almost entirely by a single resident hummingbird
species. Thus, compared to plants in fluctuating environments or those
pollinated by several pollinator taxa, plants face a predictable
environment for pollination. This suggests that, at least relative to
many other plant species, pollination service to flowers may be a
predictable consequence of the spatial arrangement of flowers on plants
in a population.
STUDY SITE AND PLANT NATURAL HISTORY
All studies took place in the Monteverde Cloud Forest Reserve,
Costa Rica (10018' N, 84048' W) from August 1981 through September 1983.
The Reserve consists mainly of Lower Montane Rain Forest (Holdridge
1967) along the continental divide in the Cordillera de Tilaran. Due to
the broken topography and the influence of weather patterns from both
the Atlantic and Pacific, local climates and vegetation in the
Monteverde area exhibit great spatial variation (Lawton and Dryer 1980).
Mean annual rainfall exceeds 2.5 m. Precipitation declines during the
dry season from January through May, but along the continental divide
blowing clouds and mist from the northeast trade winds maintain almost
continuously wet conditions.
I selected two study locations approximately one km apart in
windward cloud forest (sensu Lawton and Dryer 1980) at an elevation of
1540 m. The "dense" site was located 300 m east of the Pantanoso trail
adjacent to swamp forest (sensu Lawton and Dryer 1980). The "sparse"
site was off a cattle trail approximately 100 m west of the continental
divide. The forests at these sites are characterized by epiphyte-laden
trees 10 to 20 m in height. Small gaps in the canopy are frequent, and
there is a dense understory of shrubs and large herbs. Especially well-
represented are the Acanthaceae, Gesneriaceae, Musaceae, Palmae and
Rubiaceae. Gap frequency and understory development were greater in the
dense plot than in the sparse plot.
Cephaelis elata is an evergreen treelet of moist to wet forests,
ranging from Mexico to Colombia and the West Indies at elevations of
1550 m or less (Standley 1938). The plant is typically 2 to 3 m tall,
but it occasionally reaches 8 m (Woodson and Shery 1980). At
Monteverde, C. elata is common and widespread. Population densities are
generally high: most plants have over 10 conspecifics within 10 m
(Figure 1). The density of C. elata stems at the two study sites
differed strikingly (Table 1). At the dense site, stem densities were
an order of magnitude greater than at the the sparse site. The ratio of
long-style to short-style stems also varied between sites, but in
neither case were the ratios significantly different from one (sparse
site: X2 = 1.0, p > .05, dense site: X2 = 1.5, p > .05). Adjoining
stems tend to be of the same floral morph. This spatial segregation of
morphs was significant in the dense plot (X2 = 39.3, p < .001, N = 177,
2 X 2 contingency table), but in the sparse plot, where the sample size
was low, it was not (X2 = 0.7, p > .05, N = 35). Additionally, judging
by similarities in morphological features and flowering phenology,
adjacent stems of the same morph are often clonal. The mechanism of
clonal spread appears to be through rooting of stems broken off by
falling canopy debris, not through subsoil propagation. In this study,
I defined a plant as all stems of the same morph within 1.5 m (the
average canopy radius of C. elata) of one another measured at the stem
base. With this definition, plants and genetic individuals should be
Flowers are borne in compact red-bracted heads (Figure 2), open
shortly before or after dawn, and last a single day. The white tubular
0.4- u o
cc S 8 2
0.1 S 83
CONSPECI FIC NEIGHBORS/314 m2
Figure 1. Estimated numbers of flowering conspecifics within 10 m of
C. elata plants. Frequencies were calculated from 585 plants censused
in 50 randomly selected locations in the Monteverde Cloud Forest
Reserve. The mean density of C. elata plants (adjusted to plants/314
m2) in the sparse (S) and dense (D) study plots in 1982 and 1983 are
indicated above appropriate columns.
Table 1. Characteristics of the study sites and of C. elata
Number of C. elata stems
Ratio of pin:thrum stems
Percent of nearest
neighbors of same morph
Meanb number of flowers/m2
a Subsample of study site sampled in 1983.
b Averaged by census date over entire season.
Figure 2. Inflorescence of Cephaelis elata with two 1-d flowers
(drawn by W. Z. Pounds).
corollas have a mean length of 18.2 mm (pin: X = 18.0, SD = 1.6, N = 43;
thrum: X = 18.4, SD = 1.7, N = 27) and an inside diameter of 3 to 4 mm
at the apex. Except for reciprocal location of sexual parts within the
corolla, the long-style (pin) and short-style (thrum) flowers have
similar morphologies. In short-style flowers the stigma is located an
average of 8.2 (SD = 1.5, N = 20) mm from the nectary and the anthers an
average of 13.3 mm (SD = 1.6, N = 29). The mean distance from the
nectary to the stigma and to the anthers in long-style flowers is 17.2
mm (SD = 1.9, N = 19) and 8.8 mm (SD = 1.1, N = 20), respectively. The
ovary contains two ovules. Each flower is simultaneously
hermaphroditic; at the time of flower-opening the stigma is receptive
and the anthers have dehisced.
Results of controlled pollinations confirm that Monteverde
populations of C. elata are completely self- and intramorph-incompatible
(Table 2; see also Bawa and Beach 1983). The only compatible or
"legitimate" pollen flow is between floral morphs. Only intermorph
crosses produced pollen tubes that grew to the base of the style and
resulted in fruit production. The few exceptions were styles with
single pollen tubes, and these may have resulted from accidental
contamination with intermorph pollen. Thrum grains occasionally
germinated on thrum stigmas, but pollen tubes did not penetrate into the
style. Pin grains on pin stigmas often produced tubes that grew into
the style, a few of which penetrated 3/4 the length of the style.
Fruits mature after 4 to 6 months, becoming blue-black berries
about 2 cm in length. A variety of bird species, including Myadestes
melanops, Chlorospingus opthalmicus, and Turdus plebejus, consume the
Table 2. Results of hand pollinations of C. elata flowers.
A. Pollinated flowers monitored for presence of pollen tubes
Short X Self
Short X Short
Short X Long
Plants Flowers pollen tubes
B. Pollinated flowers monitored for fruit set
Long X Self 4 34 0 0.0
Long X Long 3 23 0 0.0
Long X Short 5 51 26 51.0
fruits and disperse the seeds (Wheelwright et al. 1984; Busby, personal
In Costa Rica, C. elata has an extended flowering season with a
peak in the early wet season (Stiles 1978). Plants in a population
flower synchronously (Opler et al. 1980). At Monteverde, a few plants
with flowers can be found almost year around, but most flowering occurs
between March and September (Figure 3). Plants initiate inflorescences
synchronously during one to four episodes each year. Each inflorescence
produces an average of 21.2 (SD = 8.6, N = 156) flowers over a 30- to
60-d period. As a result, most plants display 1 to 10 flowers each day
for 3 to 8 mo per year (Figure 4). Small plants often fail to flower on
a given day, while large plants may produce > 30 flowers a day.
Flowers of C. elata at Monteverde are utilized by at least 4
species of hummingbirds and a number of insect species, mainly
lepidopterans. The great majority of all flower visits are by a single
species, the purple-throated mountain-gem, Lampornis calolaema.
Lampornis calolaema is the most abundant short-billed hummingbird in the
Reserve where it visits numerous species of flowers in the canopy and
understory (Feinsinger et al. 1986, Feinsinger et al. in press, Murray
et al. in press). Sexes are dimorphic. The brightly colored 5.5 g
males (Feinsinger, personal communication) are highly aggressive and
frequently defend feeding territories. Females have similar bill
morphologies (23 mm total culmen), but are smaller (4.5 g) and less
aggressive. Females forage mainly at dispersed flowers. A number of
other plant species share pollinators with C. elata at Monteverde. In
the Reserve, approximately 30 herbs, shrubs, vines and epiphytes in both
I II II l
A M J J A S 0
F M A M J J A S
Figure 3. Flowering phenology of C. elata at the sparse and dense
study sites in 1982 and 1983. Shaded areas indicate time periods
used in analysis of pollen receipt.
0. n .1 I-1- Q-. n .
I I I f
I I I
I V U 0 -1 d
- 0 I-
0 4-j 0
- Cn Cn I- I- m m m I-
H d b 0 W
the canopy and the understory produce flowers and are pollinated by
short-billed hummingbirds (Feinsinger et al. 1986, Linhart et al. in
press). Cephaelis elata is probably the most important nectar resource
in the understory for these short-billed hummingbirds, but Besleria
triflora (Oerst.) Hanst., Palicourea lasiorrachis Benth. ex Oerst., and
Hansteinia blepharorachis (Leonard) Durkee are also common species. A
number of species of epiphytic Ericaceae also provide seasonally
abundant nectar resources for hummingbirds, but usually flower at
different times of year from C. elata (Busby, personal observation).
Hand pollinations were performed to confirm self-incompatibility in
C. elata in September 1981 and in August 1983. In 1981, inflorescences
with buds were enclosed with Kraft Pollen Tector bags on the day prior
to flower opening. Three hand pollination treatments were applied to
flowers of each style morph, using 1) pollen from the same flower or
from another flower on the same stem, 2) pollen from a different stem of
the same morph, or 3) pollen from one or more plants of the other morph.
All flowers were pollinated between dawn and 1100 and then were
rebagged for at least 5 hours. Later the same day I collected the
styles and preserved them in FAA (9:1:1 ethanol:acetic acid:formalin).
In 1983, the same procedure was used with flowers on cut inflorescences
in the lab. The inflorescences were placed in water-filled glass
bottles and covered with plastic bags to minimize desiccation. Flowers
are initiated normally for at least three days in this manner. I
allowed at least 10 hours for pollen tubes to grow before preserving the
styles. The styles were later examined using aniline blue staining and
epifluorescence microscopy (Martin 1959). The number of pollen tubes at
the base of each style was counted.
Pin pollen grains applied to pin stigmas frequently produced pollen
tubes that grew well into the style before gradually losing fluorescence
(Bawa and Beach 1983; this study). To determine whether these pollen
tubes actually stopped growing or simply became too faint to detect in
the lower part of the style, I conducted additional controlled
pollinations on pin plants in 1983 and monitored fruit set. Because I
could not permanently mark individual flowers, all flowers on each of 16
inflorescences on 5 plants received one of the three (self, intramorph,
and cross) treatments. Approximately 1 mo after all inflorescences had
finished flowering, I collected all inflorescences that had not aborted
and counted the number of developing fruits.
Plant and Flower Censuses
At each site, all stems of C. elata were marked with numbered metal
tags, and the morph of each stem was recorded at the time of flowering.
At approximately weekly intervals throughout the flowering season each
year, I censused the number of open flowers on all stems at each site.
To determine how the density of C. elata plants in the study plots
compared to that elsewhere at Monteverde, I censused numbers of stems
per unit area at 50 sites within two km of the study areas. At 50 m
intervals along selected trails, I followed a randomly determined
compass bearing for a randomly determined distance of 1 to 50 m. The
nearest C. elata plant within 20 m (if any) was located, and then the
number of conspecific stems within a 10 m radius of the plant was
determined. I assumed each plant within the 314 m2 area had the same
number of neighbors within 10 m as the central plant, and therefore
weighted each sample by the number of plants within it minus one. Fifty
such samples were taken. Because plants not located in the center of a
sample area may actually have had differing numbers of neighbors within
10 m than did the central plant, values for numbers of neighbors are
Observations of Pollinators
I conducted flower observations at selected plants throughout the
flowering seasons at both study sites. To enable individual
identification of hummingbirds, I mist-netted at each site 2 to 4 times
each season and color-tagged all hummingbirds (Stiles and Wolf 1973).
Observations began at dawn or at 3 h after dawn and lasted 3 h, except
for several observations in 1982 that were initiated at dawn and lasted
6 h. For all flowers on the observed plant I recorded visitor identity,
time of day, number of flowers probed and the occurrence of aggressive
behavior. At the distances from which I observed, 4 to 10 m, I could
discern insect visits to flowers without affecting hummingbird
visitation. Two plants were observed simultaneously if they had non-
overlapping canopies and were > 2 m apart. Each month, I conducted four
observations, two of each floral morph, in each study plot during the
1983 season. In 1982, the frequency of observations each month was
similar to that of 1983 but I did not attempt to equalize observations
of pin and thrum plants. Observations were made in conjunction with dye
experiments (see below). Consequently, two or more flowers on most
observation plants contained powdered dye on the anthers. Judging from
pollinator behavior at plants containing both dyed and dye-less flowers,
the application of dye to the anthers rarely affected pollinator
visitation. I discarded or repeated the few observations where dyed
flowers were avoided by pollinators. In these instances it appeared
that an excess of dye contaminated the nectary.
The effectiveness of insects and hummingbirds as pollinators was
tested with a 1-d exclusion experiment. On 29 June 1983, I allowed all
pollinators to visit a thrum plant in the sparse plot. I collected
styles from the plant at 1100, 1400 and 1700 h and preserved them in
FAA. The following day I remained near the plant and actively prevented
hummingbirds from approaching the plant from just prior to dawn to 1400
h. Insects were allowed to visit flowers on the plant without
interference. All insect visits were recorded, and styles were
collected in the same manner as the previous day. Later, styles were
examined for the presence of pollen tubes (Martin 1959).
Analysis of the Visit Data
The effect of flower density on visit rate was analyzed with
stepwise multiple regression. I defined the dependent variable, visit
rate, as the number of hummingbird probes per flower each hour. A visit
rate was calculated for each plant observed on a given day, then log-
transformed. Independent variables were (1) the number of flowers on
the observed plant, (2) local flower density (the number of C. elata
flowers within 10 m of the observed plant, excluding the observed
plant), (3) seasonal flower density (the number of C. elata flowers in
the study plot), and (4) heterospecific flower density (the number of
all short-corolla hummingbird-visited flowers, excluding those of C.
elata, in the understory of the study plot). The number of flowers on
the observed plant was recorded at the time of the observation. The
other three variables were derived from weekly flower censuses made on a
separate day, and thus were estimates. If a census occurred within 2 d
of the observation I used data from that census. Otherwise, I averaged
values from the censuses immediately before and after the observation.
I first examined the independent variables for multicollinearity.
I removed heterospecific flower density from consideration in the dense
plot in both years due to high negative collinearity with seasonal
flower density. The stepwise selection option of Proc Stepwise (SAS
Institute Inc. 1982) was used with a cutoff value of alpha = .10 for
entry of a variable into the model as well as for retention in the model
at each step. With stepwise regression procedures, alpha levels used to
select variables cannot be used as levels of significance because the
partial F-value used at each step is the maximum of several correlated
partial F-values (Sokal and Rohlf 1981). For this reason, the
significance levels associated with each selected independent variable
In the initial stepwise regression models both first-order and
second-order (squared) terms were considered for entry into the model.
Second-order terms were used to examine possible nonlinear relationships
between visit rate and measures of flower density. A second-order term
was entered only if it explained a significant amount of the residual
variance of the model in the presence of the corresponding first-order
term. Because the slope of the relationship between measures of flower
density and visitation may decrease as flower density increases (Thomson
1982, 1983, Rathcke 1983), I also evaluated log-transformed independent
variables for entry into regression models. In cases where the second-
order term of a variable failed to meet model entry criteria, I used
both standard (Proc Reg, SAS Institute Inc. 1982) and stepwise multiple
regression procedures to choose between the raw (first-order) and log-
transformed versions of each independent variable, retaining whichever
one had a higher partial F-value in the presence of the other
independent variables (i.e., SAS type III sums of squares).
Flower Removal Experiment
I conducted flower removal experiments to determine the effect of
the number of flowers on a plant on pollinator visit rates to flowers.
Using 19 x 16 mm mesh plastic netting, I bagged all but a few
inflorescences on a large pin plant in the sparse plot. The plant was
observed for pollinator visits for 3 or 6 h in the morning on four
occasions: 1) the day prior to the manipulation, 2) twice on separate
days 2 to 5 d after bagging the plant, and 3) once 2 d after removal of
the netting. The experiment was conducted in August 1982 and repeated
on the same plant in July and in August of 1983.
I measured pollen carryover in 1983 with caged hummingbirds offered
flowers on cut inflorescences. Lampornis calolaema were mist-netted in
the field and caged in an outdoor enclosure, 4 x 4 x 3 m, made of nylon
mesh. The birds, one male and one female, were maintained on a 20%
sucrose solution presented in an artificial feeder, and were kept for up
to a week before release. One half hour prior to an experiment, I
removed the feeder. Using virgin flowers on inflorescences in water-
filled jars, I offered the bird one or more donor flowers followed
immediately by 14 to 20 recipient flowers of the other morph. I
recorded the visit sequence to recipient flowers before removing them
from the cage. I conducted one to three trials per day and cleaned the
bird's bill between runs. A separate series of experiments was made
using 1) a single donor flower and 2) six donor flowers in succession.
The numbers of pin-to-thrum and thrum-to-pin trials were equalized.
Because pin and thrum pollen grains could not reliably be
distinguished, I counted the number of pollen tubes in the styles of
recipient flowers (Martin 1959). Styles were picked from inflorescences
12 to 24 h after each experiment and preserved in FAA. Only compatible
pollen grains produce pollen tubes that penetrate to the style base
(Bawa and Beach 1983; this study); thus, counts of stylar pollen tubes
provide a conservative estimate of the number of viable pollen grains
deposited on each stigma. Rarely did more than 20 pollen tubes
penetrate to the style base regardless of the number of compatible
grains on the stigma.
I quantified pollination levels by counting numbers of pollen tubes
at the base of floral styles. Plants in both plots were sampled between
1500 h and 1700 h, following flower censuses. The entire style was
removed with forceps and pickled in a vial containing FAA. I collected
all intact styles from plants with < 6 flowers and a subsample of styles
(usually 5) from plants with > 5 flowers. In the sparse plot, I sampled
all plants on each census throughout the flowering season. Due to the
large number of plants in the dense plot, I collected styles from a
subsample (usually 15 to 30) of plants each census. In the lab, using
aniline blue staining and epifluorescence microscopy (Martin 1959), I
counted the number of pollen tubes at the base of each style.
Because styles were collected several hours before the end of
flower life, some styles may have contained actively growing pollen
tubes that had not reached the style base. Thus, actual pollination
levels may be somewhat higher than those reported here. Additionally,
because the time required for pollen tubes to grow to the base of the
longer pin styles (ca. 5 h) was greater than that required in thrum
styles (ca. 3.5 h), I was effectively collecting pin styles 1.5 h
earlier in the day than thrums. This bias prevents an objective
comparison of pollination levels between morphs.
Analysis of Pollen Receipt Data
Weighted stepwise multiple regression was used to analyze the
relationship between pollination and measures of flower density and
dispersion. I used five independent variables, three of which were
previously defined: (1) the number of flowers on the central plant (i.e,
a plant from which styles were collected), (2) local flower density, and
(3) seasonal flower density. Heterospecific flower density, used in
visit analyses, was eliminated because of frequent high negative
collinearity with seasonal conspecific density. I used the number of C.
elata flowers within either 5 m or 10 m of the central plant (exclusive
of the central plant) as the measure of local flower density: a 10 m
radius was used in the sparse plot, a 5 m radius in the dense plot in
1983, and both a 5 m and a 10 m radius in the dense plot in 1982. These
two measures of local density tended, of course, to be highly collinear;
where both were evaluated for entry into the model only the more
significant of the two was retained. (4) Another variable was the
distance to the nearest mate: the number of meters from the central
plant to the closest plant of the other morph with one or more open
flowers. (5) Lastly, a categorical, or "dummy" variable was included to
represent the two morphs (0 = thrum, 1 = pin).
The dependent variable was the mean number of pollen tubes at the
base of the style averaged across all styles collected from a plant.
Pollen tube counts from individual flowers were not used as the
experimental unit since flowers on the same plant are not independent.
Because the sample size generated from each census was small, at
each site I pooled censuses into 2 or 3 periods for each flowering
season (Figure 3). Criteria for determining break points for the
different periods were 1) maximizing the ranges of the independent
variables, and 2) equalizing sample sizes among periods. Prior to
regression analyses by period, I checked for significant variation among
plants in pollination levels by date and style morph with one-way ANOVA.
I used raw pollen tube counts from styles of all flowers on each plant.
Generally, among plant variation was highly significant.
From this point on, the stepwise multiple regression procedures
were as described for the visit data with the following differences:
(1) observations were weighted by the number of styles on the plant
examined up to a maximum weighting of five; (2) a selection level of
alpha = .05 was used for entry and retention of variables in the model;
and 3) first order interaction terms were included as variables in the
stepwise process. An interaction term was retained in the model only if
it was significant in the presence of both component variables.
To determine whether my definition of a plant influenced results
from the analyses, I redefined the dependent variable and repeated
regressions for the sparse plot. Instead of using the multi-stem
definition of a plant (see above), I used pollen tube values for
individual C. elata stem.
Powdered ultraviolet-fluorescent dyes (Helecon and U.S. Radiant)
were used as pollen analogues. The relationship of the dispersal of dye
to that of pollen is not well understood; it probably varies among plant
species and pollinating agents. Price and Waser (1982) found a close
relationship between dispersal of dye and pollen in the hummingbird-
pollinated Ipomopsis aggregata. In contrast, Thomson et. al. (1986)
showed that dye particles were dispersed farther and in greater
quantities than pollen of bee-pollinated Erythronium. Because the
relationship between dye and pollen dispersal is unknown for C. elata, I
utilized dyes only for comparative purposes. Two types of experiments
were conducted. I measured pollen dispersal per flower by placing dye
on two flowers of a plant. To quantify pollen dispersal per plant I
placed dye on all open flowers of a plant. Dye experiments were
conducted on four plants per month, two of each morph, in each study
plot during the 1983 season. In 1982 the frequency of experiments each
month was similar to that of 1983, but the numbers of pin and thrum
donor plants were not deliberately equalized.
At dawn, I applied the powdered dyes to the anthers of the newly
opened flowers at dawn with a toothpick. Experiments using pin and
thrum flowers as dye-donors were alternated. Because I was unable (1)
to place precise amounts of dye on anther surfaces, and (2) to duplicate
effects of possible differences in pollen size and pollen surface
features between pin and thrum flowers, I did not make intermorphic
comparisons of dye dispersal.
I used two dyes (Helecon green and yellow) that appeared pastel in
visible light and one day-glow dye (U.S. Radiant orange-red). In 1982,
I used two colors of dye each day, one color per plant. The following
year three colors were utilized: one color for two flowers on the first
plant, the second color for two flowers on a second plant and the third
color for all remaining flowers on one of the two plants. All flowers
on each plant were then observed for pollinator visits. Hummingbird
behavior was not affected by the color of the dye within flowers. Later
that day (1300 to 1500 h), I collected flowers from plants surrounding
the donor plant, and pinned them in an insect box for transport to the
lab. Only compatible flowers, i.e., those of the other morph from the
donor flower, were analyzed for dye receipt. Except in the dense plot
in 1982, virtually all compatible flowers were collected on all plants
within predefined areas. Using a ladder, I was able to reach all but a
few flowers on the tallest plants. At plants containing more than 10
open flowers, I attempted to pick at least half of the flowers. I used
the fraction of sampled dye-receiving flowers to estimate the total
number of dye-receiving flowers on the plant. In the sparse plot in
1982, all flowers were collected within the study plot for an effective
radius of 50 to 100 m around the donor plant. The following year I
expanded collections to all compatible flowers within 100 m, whether
within or outside the study plot. In the dense plot in 1982, I
collected 1 to 3 flowers from approximately half of the plants within 35
m of the dye source. In 1983, I sampled all flowers on all plants
within 25 m or the first 15 nearest neighbors, whichever came first.
In the lab I used a black light with a 10X to 40X dissecting
microscope to record the presence and color of any dye on the stigma.
Because the size of individual dye particles ranged over several orders
of magnitude, rather than count particles I recorded the amount of dye
on stigmas using four relative classes. Using maps of the study areas,
I calculated the distance from each compatible plant to the dye source.
Three variables describe dye dispersal: (1) The number of flowers
receiving dye was based on all compatible flowers examined that
contained dye on the stigma, plus estimates from plants on which I
sampled < 100% of the flowers; (2) the dispersal distance and (3) the
"plant sequence" are indices of the distance of dye dispersal in meters
and in nearest neighbor units, respectively. I first ranked all
recipient flowers with dye on the stigma in order of distance from the
dye source, then determined the 90th percentile flower from the donor
plant. Dispersal distance is the linear distance from the dye source to
the plant containing the 90th percentile dye-receiving flower. To
calculate plant sequence, all plants for which I had collected flowers
that day (i.e., all flowering individuals of the other morph from that
of the donor plant) were ranked in order of distance from the donor
plant. Plant sequence is the rank of the plant containing the 90th
percentile dye-receiving flower. Dispersal distance and plant sequence
are roughly analogous to neighborhood size, Ne, and neighborhood area,
Na (Wright 1969, Levin and Kerster 1971). Neighborhood size and plant
sequence both provide an index of the number of interbreeding plants, Na
and the dispersal distance an index to the spatial scale of pollen
dispersal. Because neighborhood size and area are based on the
variation in dispersal distances, however, their values are especially
sensitive to the maximum distances recorded. In this study, I gathered
nearly complete data on dispersal events within prescribed areas, but I
did not attempt to determine maximum dispersal distances of pollen.
Thus, neighborhood size and area could not be quantified.
Each year, in both plots, I measured percent fruit set on
infructescences from pin and thrum plants. Late in the flowering
season, I collected a random sample of heads that had flowered during
the early to middle portions of the season. Only infructescences that
had completed flowering and had not yet matured fruit were collected.
Because the ovary remains in the head after corolla abscission, the
number of flowers produced by each head could be determined. By
dissecting infructescences, I determined the number of developed,
undeveloped, and damaged fruits.
Pollinator Identity and Foraging Behavior
The great majority of hummingbird visits to C. elata flowers were
made by Lampornis calolaema (Table 3). Other species of hummingbirds
made regular visits to flowers only at times when visit rates by L.
calolaema were extremely low.
In the dense plot, L. calolaema males established large
territories (about 600 to 2000 m2) early in the flowering season and
defended them throughout each day against other hummingbirds and against
lepidopterans. Territories in this plot contained approximately 20 to
40 C. elata plants; elsewhere L. calolaema males were occasionally
observed defending territories primarily composed of other flowering
species, with few C. elata. At the dense site, territory boundaries
were well defined. Repeated sightings of individually tagged males
indicate that territories were often stable over periods of at least 6
to 8 wk. Territorial behavior included vocalizations and active defense
against other flower-visitors. The fact that territory-holders
generally moved frequently among perches within their territories
suggests they were not able to survey the entire territory from one
location. At this site, I estimated that the proportion of all
hummingbird visits to flowers made by the territory-holder was over 73%
in 1982 and about 84% in 1983. Intruders consisted primarily of L.
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calolaema females, unmarked males, and marked males from nearby
At the sparse site, both male and female L. calolaema were frequent
flower visitors, with relative abundance of each shifting with the
abundance of flowers. Flowers on small, isolated plants were visited
mostly by females. Individual females often returned to observed plants
at regular intervals, but did not appear to follow consistent foraging
circuits. Females, therefore, acted as "generalists" (sensu Feinsinger
1976) but did not trapline in the strict sense (Janzen 1971). Foraging
areas were typically utilized by a single bird. It was not uncommon,
however, for two individuals of either sex to repeatedly return to a
plant during an observation. At this site, males were present mainly
during periods of high flower availability. Males usually chased other
flower-visitors whenever encountered, but presumably due to the spatial
dispersal of flowers, rarely defended clearly defined territories. The
few well-established territories at the sparse site usually coincided
with heavy flowering by other short flowered species adapted for
hummingbird pollination, such as Besleria triflora or Palicourea
lasiorrachis in the understory and various Ericaceae in the canopy.
Territories incorporating flowers in both the understory and canopy,
while uncommon, were observed in both study plots.
The most common insect visitors to C. elata flowers were
lepidopterans (Table 3). Visits by butterflies were heaviest during
dry, sunny weather. Butterflies began visiting flowers by mid-morning
and were active throughout the afternoon. Heliconius clysonymus was the
most regular insect visitor to C. elata flowers. Individuals of this
species often returned to the same flowers of a plant at frequent
intervals throughout the day. Moths were observed visiting flowers at
dawn prior to foraging activity by other pollinators.
Flowers suffered few depredations by nectar thieves or robbers. The
basal 5 to 10 mm of the flower is embedded within the rigid bracts of
the inflorescence, making the nectary inaccessible except through the
In the pollinator exclusion experiment, flowers were not pollinated
unless visited by hummingbirds. On the control day (open pollination),
six of eight flowers were pollinated; of these, each contained an
average of 10.8 (SD = 9.4) pollen tubes. The following day, in the
absence of hummingbirds, lepidopterans visited each of the five flowers
an average of five times between dawn and 1400 h. None of these styles
contained pollen tubes. The presence of heterospecific pollen on four of
the five stigmas confirmed, however, that some insect visitors did
contact the reproductive parts of the flower.
Effects of Flower Density on Visitation
At each site, the number of flowers on and surrounding observed
plants varied greatly (Table 4). Factors characterizing flower density
explained 32 to 68% of the seasonal variation in visit rates by
hummingbirds (Table 5). Correlations between measures of conspecific
flower density and visitation were generally stronger in 1983 than in
1982. As expected, flower visitation was generally positively density-
dependent. In all four comparisons, visit rates significantly increased
with seasonal flower density. The significant squared term indicates
Table 4. Ranges of the independent variables
regression analysis of flower visitation.
used in multiple
Sparse 1982 22 1-60 0-60 15-122 2-210
Sparse 1983 28 1-26 0-34 6-142 4-253
Dense 1982 44 1-16 4-55 79-638 0-311
Dense 1983 43 1-29 0-35a 5-280 7-130
a A 5 m radius (flowers/78 m2) was used to
at the dense site in 1983.
compute local flower density
o t- o
C0o* 0 C\ 00 *
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that the slope of the relationship between seasonal flower density and
visitation was not linear; positive hummingbird responses to increases
in flower density were weaker at peak flowering than during either tail
of the flowering season. The number of flowers within 10 m of observed
plants was not strongly correlated with floral visit rates, although at
the dense site, territorial birds did visit flowers in dense patches
significantly less frequently in 1983. Flowers on plants with more
flowers received more frequent visits in 1983 but not in 1982. The
number of heterospecific flowers in the understory was positively
correlated with visit rate both years. Due to high negative
collinearity with the seasonal density of C. elata flowers, the density
of heterospecific flowers was not included in regression analyses in the
While multiple regression analysis shows a positive effect of
seasonal flower density on visit frequency in all four cases (Table 5),
seasonal variation in this relationship was great (Figure 5). In 1983,
mean monthly visit rates in both plots rose and fell in accordance with
flower density throughout the season. In 1982, the relationship between
seasonal flower density and visitation was weak or nonexistent during
the first two thirds of the season. Only late in the season was a
positive relationship evident. Visit rates were high during the first
part of the season, then dropped off abruptly at peak flowering. The
cause for the sudden decline remains uncertain, but may be related to a
flowering pulse in the canopy. Satyria warscewiczeii and Gonocalyx
pterocarpus, two common hummingbird-pollinated epiphytes, bloomed
abundantly in July and August 1982 (Busby, personal observation). In
100 4 o. o e n 1 .0
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S -o 1982 I-
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A M J J A S O
Figure 5. Seasonal fluctuations in total number of C. elata flowers
( ), mean monthly visit rates to flowers by hummingbirds (- -),
and pollen receipt (numbers of pollen tubes at the base of the style)
(....) at each site in 1982 and 1983.
10 0 4 "o 1 .0
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F M A M J J A S
mid-July a tagged L. calolaema male abandoned a long-held territory in
the understory and was sighted in the canopy attempting to defend a
profusely-flowering S. warscewiczeii plant against a host of other
hummingbirds. This is evidence that flowering in the canopy drew
pollinators away from C. elata flowers, and stands in contrast to the
positive effects of understory heterospecifics on visit rates to C.
elata flowers in the sparse plot (Table 5).
Results of the flower removal experiment are consistent with
observations of unmanipulated plants: individual flowers on plants with
large floral displays received more visits than those in small displays
(Figure 6). In all three replicates, visit rates to flowers
consistently dropped when the number of flowers on the plant was
artificially reduced, then recovered after removal of netting from the
The relationship between the number of flowers on a plant and the
number of flowers probed during each visit by hummingbirds was analyzed
with least squares regressions (Table 6). Regression coefficients
(slopes) were large, indicating that hummingbirds probed a high
proportion of the flowers during typical bouts at plants of all sizes.
Birds probed, on average, at least half of the flowers on plants with 10
or fewer flowers and at least one third of the available flowers on
plants with > 10 flowers. The results were similar across plots and
years, and in all four cases linear models accounted for more of the
variance in the number of flowers visited per plant than did logarithmic
or exponential models.
Figure 6. Mean visit rates by hummingbirds to flowers on a C. elata
plant before, during, and after bagging the majority of flowers with
plastic netting. Vertical lines indicate 1 standard deviation;
numbers above each mean indicate sample size.
Table 6. Results of linear regression analysis on the number of
flowers visited per foraging bout by hummingbirds as a function of the
number of flowers on the plant.
Sparse 1982 1.44 0.57 0.76 343.2(1,110) <<.001
Sparse 1983 0.71 0.48 0.40 151.1(1,166) <<.001
Dense 1982 1.49 0.45 0.45 134.2(1,230) <<.001
Dense 1983 1.63 0.36 0.41 161.1(1,232) <<.001
Results from the pollen carryover experiments for both floral
morphs are shown in Figure 7. Pollen from thrum flowers was transferred
by hummingbirds to many of the first 20 recipient stigmas. In contrast,
pin pollen was dispersed to few thrum flowers; nearly all successful
pollen donation by pins was to the first five thrum flowers. Summary
values derived from the carryover data quantify these differences (Table
7). In both single and six donor flower trials, thrum pollen was
carried to more recipient flowers than was pin pollen. Furthermore, the
average amount of pollen transferred from thrum to pin flowers was over
twice that transferred from pin to thrum flowers.
In both morphs, the number of donor flowers visited by the
pollinator also influenced the pattern of pollen carryover (Figure 7 and
Table 7). The major effect of increasing the number of donors from one
to six was to increase the amount of pollen donated. The total number
of pollen tubes in recipient styles was an average of 2 to 3 times
greater in trials where hummingbirds visited six donor flowers rather
than one donor. It is less clear if the number of donors affects (1)
the number of flowers receiving pollen or (2) the median distance of
pollen dispersal. The trends are weak and non-significant.
Variation in Pollen Receipt and Fruit Set
Several sources of variation in pollen receipt by naturally
pollinated flowers are shown in Table 8. (1) Variation in the mean
number of pollen tubes per style among plants was high. (2) Pollen tube
co u a
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Table 7. Effect of numbers of donor flowers on pollen transfer
between floral morphs. Data are from pollen carryover experiments.
No. Donor Flowers
No. Recipient Flowers
16-20 Thrum 17-20 Thrum
1 Thrum 6 Thrum
Total donor tubes
Mann Whitney U tests
No. recipient styles
with >1 donor tube
Mann Whitney U tests
Sequence no. of recipient
styles receiving median
donor tube (X SD)
Mann Whitney U tests
U = 1 p = .04
U = 7 p = .50
U = 4.5 p = .24
U = 1 p = .04
U = 4.5 p = .24
U = 3.5 p = .30
Table 8. Numbers of pollen tubes at the base the style
flowers on plants. N = number of plants. The number of
flowers is in
Mean SE N >1 tube
Mean SE N >1 tube
2.4 1.7 47(116) 61.2
0.5 1.1 66(172) 23.3
5.5 1.7 101(258)
1.9 1.6 84(322)
1.4 1.7 85(236)
4.8 1.4 64(277)
8.0 1.4 83(334)
1.1 1.1 74(206)
0.6 1.1 28(161 ) 16.1
0.2 0.4 40(330) 5.2
1.3 1.1 40(136)
3.7 1.9 42(181)
0.6 1.4 41(162)
4.8 1.7 114(325)
1.1 1.5 114(404)
0.4 0.9 89(227)
1.9 1.8 65(340)
4.0 1.6 69(390)
1.1 1.6 47(144)
counts at the base of thrum styles consistently exceeded those at the
base of pin styles. This difference is at least partly attributable to
the sampling method. (3) Pollination levels varied seasonally. During
some periods, most styles contained 10 to 20 pollen tubes, well over the
absolute minimum of two needed to fertilize both ovules. At other
times, most flowers received no compatible pollen. Pollination levels
early in each flowering season were consistently higher than late in the
season. In 1983, but not in 1982, flowers produced during mid-season
contained more pollen tubes than those in either tail of the season.
The mean percentage of flowers producing fruits varied from 20 to
53% (Table 9). During both years, inflorescences at the dense site set
a significantly higher percentage of fruits than at the sparse site.
Because of a significant site x morph interaction in 1982, the effect of
site on fruit set was examined separately for pins (t = 7.7, p < .001)
and for thrums (t = 2.2, p < .05). Differences between morphs in fruit
set were complex. In 1983, fruit set of thrum inflorescences was higher
than that of pins. In 1982, fruit set of pins was higher at the dense
site, while thrums set more fruit at the sparse site.
Effects of Flower Density on Pollen Receipt
Using stepwise multiple regression, variation in the density and
dispersion of C. elata flowers at each site (Table 10) accounted for 12
to 41% of the variation in pollen receipt (Table 11). No single
independent variable explained large amounts of the variation in stylar
pollen tube counts, yet each variable was significantly correlated with
pollination levels in the majority of trials.
Table 9. Fruit set of inflorescences. Analysis of variance performed
on arc-sine transformed data.
Mean SD N
Mean SD N
20.0 12.3 39
35.0 14.8 45
Effect of site
Effect of morph
Site x morph interaction
26.9 18.2 29
33.7 18.2 43
Effect of site
Effect of morph
Site x morph interaction
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As expected, the distance from the focal plant to the nearest
compatible plant in flower was negatively correlated with pollen receipt
(6 of 9 trials, Table 11). In other words, flowers with compatible
pollen source nearby received more pollen. The effect of nearest-mate
distance was important at the dense site, where potential mates were
typically within a few meters, and at the sparse site, where pollen
sources were often 30 m or more distant. Of the three measures of
density, seasonal flower density was most consistently (7 of 10 trials)
and, in general, most strongly correlated with the number of stylar
pollen tubes. Local flower density and the central plant's display size
each had effects on pollination in 6 of 11 trials, but the direction of
the relationship varied; the amount of pollen received by flowers in
dense patches was often lower but sometimes higher than that received by
Does treating all same-morph stems within 1.5 meters as one plant
bias the results? To answer this question I re-analyzed the data using
mean pollen tube counts of styles from individual stems in the sparse
plot (Table 12). Results from these analyses were qualitatively and
quantitatively similar to those for multi-stem plants.
Dispersal of Powdered Dyes
All measures of the dispersal of powdered dye from donor flowers
are characterized by high variation (Table 13). Little of this
variation, however, is explained by the number of flowers on a plant or
by seasonal changes in flower density (Table 14). No correlations
between the measures of dye dispersal and the number of flowers on the
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donor plant were significant, and given the mixture of positive and
negative coefficients, no trends are apparent. As the density of
surrounding compatible flowers increases over time, one might expect
that pollen from a given source would 1) be dispersed to more target
flowers, 2) be carried to more consecutive neighbors, and 3) assuming
density-dependent foraging movements by pollinators, be transferred
shorter distances. Correlations of seasonal flower density with the
number of flowers receiving dye and with plant sequence are, in general,
positive, but rarely significantly so. Dispersal distance was not
clearly related to flower density in any of the four comparisons.
In contrast, all three expected relationships are confirmed in
comparing mean values of dye dispersal variables among sites (Table 13).
Dye was dispersed to approximately twice as many flowers and plants at
the dense site as at the sparse site, while dispersal distances were 2
to 3 times greater at the sparse site. That differences between sites
in dye movement are greater than seasonal differences at a single site
is not surprising: the ten-fold difference in flower and plant density
between the sparse and dense site is substantially larger than the
range of densities over which I measured dye dispersal at each site.
Inter-site differences must be interpreted with caution due to variation
in sampling regimens. Despite differences among sites in the area and
number of plants sampled, frequency distributions of dye receipt (Figure
8) indicate that, at least in 1983, the area I sampled for recipient
flowers was sufficiently large to capture the majority of flowers that
received dye. The proportion of flowers and plants receiving dye at the
most distant sampling intervals was generally very low.
fl PLANTS O FLOWERS
S <' / .
, 0 0 j .0 0 .
T > ,c 3 -c -
Figure 8. Proportion of compatible flowers and plants receiving
powdered dye on the stigma from two donor flowers (see Table 13 for
The number of pollinator visits received by donor flowers had a
strong effect on the dispersal of fluorescent dye (Table 14). In all
four comparisons, dye reached significantly more compatible stigmas
where visit rate was higher. Correlations of seasonal flower density
with dispersal distance and plant sequence were also consistently
positive, but usually not significantly so.
Lastly, dye dispersal per plant varied markedly with floral display
size (Table 15). When dye was placed on the anthers of all the flowers
of a plant, dye from plants with more flowers was transferred to more
stigmas on plants spread over a wider area. This relationship was
pronounced at the dense site each year but absent at the sparse site in
Table 15. Spearman rank correlation coefficients floral display size
(number of donor flowers/plant) and measures of dye dispersal. Dye
placed on the anthers of all open flowers of each experimental plant.
Sparse site 1982
Dense site 1982
Dense site 1983
Number of flowers
receiving dye +.04 22 +.63*** 17 +.70*** 18
Plant sequence -.01 22 +.48* 16 +.55* 18
distance(m) .00 22 +.34 16 +.48* 18
* p < .05, ** p < .01, *** p < .001
Effect of Floral Display Size on Pollinator Behavior
and Pollination Success
Two aspects of hummingbird behavior varied with the number of
flowers on C. elata plants: visit rates to individual flowers and the
numbers of flowers probed per plant during each hummingbird visit.
Other studies have shown that visit frequencies to plants increase with
the size of the floral display (Willson and Rathcke 1974, Willson and
Bertin 1979, Wyatt 1980, Schemske 1980b). Visit rates to individual
flowers may also increase with the number of flowers on a plant
(Augspurger 1980, Geber 1985). In this study, hummingbird visit rates
to flowers increased significantly with floral display size in field
experiments (Figure 6), and in natural populations during one of the two
years (Table 5).
For plants with large floral displays, the benefits of providing
rich resources for pollinators has a potential disadvantage. The
tendency of pollinators to visit many flowers at large floral displays,
and to move less often between plants, may increase within-plant
(geitonogamous) pollen transfer and result in reduced rates of
outcrossing (Linhart 1973, Carpenter 1976, Feinsinger 1978, Augspurger
1980, Stephenson 1982). This reduction in visit quality with increasing
numbers of flowers on a plant may select for an upper limit on floral
display size, particularly for obligate outcrossers (Schemske 1980b,
Wyatt 1980). This argument may apply especially to hummingbird-
pollinated plants: hummingbirds generally forage in a density-dependent
manner, often probing many of the available flowers on a plant during
each foraging trip (Stiles 1975, Feinsinger 1978, Schemske 1980b). In
this study, at C. elata plants of all sizes, hummingbirds probed a large
proportion, usually > 50%, of the flowers each visit (Table 6).
The extent to which outcrossing is limited by long pollinator
foraging sequences at individual plants depends on pollen carryover. If
all pollen picked up at a flower is deposited on the next flower--i.e.,
a carryover of 1.0-only pollen from the last flower visited on a plant
could potentially cross-pollinate flowers on other plants. In carryover
experiments with hummingbirds, I found that the median pollen grain was
deposited on the first to sixth recipient flower, but that some pollen
reached as far as the 14th consecutive thrum stigma and at least as far
as the 20th pin stigma (Table 7). Such high variation in pollen
deposition has been found in most studies of pollen carryover (Thomson
and Plowright 1980, Waser and Price 1982, Lertzman and Gass 1983, Geber
1985). With the carryover values reported here, hummingbirds can
effectively transfer pollen to and from C. elata plants with large
floral displays despite long within-plant visit sequences. A bird
arriving at a plant carrying compatible pollen, for instance, would
typically deposit that pollen on 3 to 9 flowers during a foraging
sequence of 20 flowers (Table 7).
The amount of pollen dispersed per flower from the plant, however,
should be inversely related to the number of flowers probed per plant.
In the carryover experiments, as the number of flowers probed per plant
increased from one to six flowers, the average number of pollen tubes
attributed to each donor flower declined from 7.4 to 2.9 in pin flowers
and 16.0 to 8.1 in thrums (Table 7). As the number of flowers probed
per plant increases beyond six, average amounts of pollen donated and
received per flower each visit probably continue to decrease. In
summary, moderate pollen carryover in C. elata promotes outcrossing
despite multiple-flower visits by pollinators to plants with many
flowers, but visit effectiveness nonetheless drops markedly as
intraplant pollinator flights to flowers increase relative to interplant
Were differences in foraging behavior by hummingbirds at plants
with many and few flowers reflected in pollination? In the field, the
number of flowers on a plant had no effect on pollen donation per flower
(Table 14) and often had no effect on pollen receipt (5 of 11 trials,
Table 11). Occasionally, pollen receipt per flower was positively (2 of
11 trials) or negatively (4 of 11 trials) correlated with floral display
size. These results imply that factors influencing pollination success
are complex. Often, the advantage of large floral displays (pollinator
attraction) may simply cancel out the disadvantage (sedentary pollinator
behavior), resulting in no net effect of floral display size on
pollination. Alternatively, pollen carryover may mask slight
differences in pollinator behavior at many- and few-flowered plants.
For a plant, the effects of displaying a given number of flowers may
also shift seasonally. At times when pollinator visitation limits
pollination and seed set, plants will compete for pollinator attention
(Zimmerman 1980). Under these conditions, the greater attractiveness of
plants with large numbers of flowers to pollinators may result in a
positive correlation between floral display size and pollination success
of flowers. Alternatively, at peak flowering, sedentary behavior by
pollinators at large floral displays may result in low rates of pollen
flow among plants. If visit rates to flowers vary little with floral
display size, which was often the case where plant density was high,
pollen donation and receipt by flowers on few-flowered plants may be
higher due to low levels of geitonogamous pollen flow. In any event,
while pollination success of flowers often varies with the number of
flowers on in C. elata plants, no single floral display size
consistently receives better pollination service (Tables 11 and 14). In
studying these same relationships, Geber (1985) found that despite
subtle differences in visit patterns by bees to Mertensia plants of
differing sizes, flowers on all plants received similar amounts of
pollen from conspecifics and had similar reproductive outputs.
Reproductive performance in plants can be evaluated at the level of
the plant, the inflorescence, or individual flowers. This study
evaluates visitation and pollination per flower, and in doing so,
provides a measure of the efficiency of pollination service to plants.
The importance of the efficiency of resource utilization for
reproduction should depend on the degree to which a plant is resource-
limited. Located in forest understory, most C. elata plants appear to
be strongly limited by light. Flower production, for example, clearly
increases with the amount of available light, and plants growing in
dense shade sometimes fail to flower altogether (Busby, personal
observation; see also Schemske 1977, Motten et al. 1981, Campbell 1985).
Thus, the pollination success of individual flowers should be a
biologically important measure for C. elata plants. For those plants
located in treefall gaps or other high-light environments, however,
reproductive efficiency may be less important than total reproductive
output. Conditions in treefalls are generally favorable for plant
reproduction (Linhart et al., in press). Cephaelis elata plants in
forest gaps often flower profusely. High light availability is
generally temporary, however, because the canopy closes over and light
levels return to near pre-perturbation levels within a very few years
(R. Lawton, personal communication). For these plants, the importance
of maximizing short-term reproductive output may make pollination
success of the plant a more appropriate measure than pollination success
Regardless of how individual flowers fared on plants of differing
sizes, plants with many open flowers generally donated and received more
compatible pollen than plants with few open flowers. The dye
experiments showed that many-flowered plants dispersed their pollen not
only to more compatible flowers but also to more plants and, in some
cases, to greater distances (Table 15). It is not clear which of these
measures--flowers, plants, or location of plants--is most directly
related to male reproductive success (see Janzen 1977, Stephenson and
Bertin 1983). In any event, all three were positively correlated.
Pollen receipt per plant is simply the sum of the pollen received by
individual flowers. Thus, unless pollen receipt per flower decreases
sharply with increasing floral display size, plants with more flowers
will receive greater total amounts of compatible pollen. At times when
pollination is not limiting to fruit set, potential fruit set per plant
will simply be equal to the number of flowers produced by the plant.
Flower Density and Visitation
Optimal foraging theory predicts that pollinators should
concentrate foraging efforts in rich patches of flowers (see Heinrich
and Raven 1972, Pyke 1978, Heinrich 1979, Thomson 1981, Zimmerman 1981).
While the positive effects of floral display size on flower visitation
support the theory, effects of local flower density (the number of
conspecific flowers within 10 m of the central plant) on visitation did
not. Local flower density had little detectable effect on hummingbird
visit rates to flowers (Table 5). The absence of an effect of local
flower density is not surprising where plant density is high, pollinator
flights short, and pollinator foraging behavior complicated by
territoriality, as in the dense plot. However, in the sparse plot,
where pollinators often had to traverse long distances between plants,
theory predicts isolated plants should have received fewer visits than
those in clumps. The lack of such an effect may be due to confounding
effects of heterospecific flowers. Alternatively, hummingbird responses
may be more closely keyed to resource dispersion on a larger scale.
Thomson (1981) found that correlations between insect visitation and
flower density varied markedly with spatial scale.
Over the course of the blooming season, hummingbird visit rates to
flowers often tracked changes in seasonal flower density. In general,
mid-season visit rates exceeded those earlier and later in the season
(Figure 5). Increases in pollinator activity during seasonal peaks in
flowering have been shown for a number of plants (Zimmerman 1980,
Thomson 1982, Schmitt 1983a, Motten 1986), but exceptions are not
uncommon (Thomson 1982). In this study, the consistency of the
correlation between flower density and visitation across 7 mo of
flowering in 1983 demonstrated the extent to which floral resource
levels of a single species can produce consistent pollinator responses
in a complex community. On the other hand, the sudden decline in visit
rates at mid-season the preceding year indicates that seasonal trends in
pollinator visitation can be strongly influenced by other environmental
One such factor affecting visitation to C. elata flowers was the
availability of heterospecific flowers. At the sparse site, flowering
by other hummingbird-pollinated species in the understory was positively
correlated with seasonal changes in visit rates to C. elata flowers
(Table 5). Circumstantial evidence suggests flowering by canopy species
had just the opposite effect: hummingbirds abandoned territories in the
understory to forage at rich nectar sources in the canopy. Such
variable effects of heterospecifics on visitation are consistent with a
model proposed by Thomson (1982, 1983). He suggests that as spatial
intermingling of two species decreases, the effects on visitation switch
from mutualistic to competitive. If spatial proximity does underlie
these complex effects of pollinator-sharing species, their effect on
visitation to C. elata flowers should vary among plants depending upon
location. Consequently, only species that occupied different habitats
or forest strata should have a consistent competitive relationship with
C. elata in terms of visitation.
Effects of Neighbors on Pollination Success
For a self-incompatible plant the presence of flowering
conspecifics is necessary for sexual reproduction. It is surprising,
therefore, to find the density of surrounding conspecific flowers often
(5 of 11 trials, Table 11) had a significant negative effect on pollen
receipt by C. elata flowers. The explanation may lie in the
distribution of pin and thrum plants. Spatial aggregation of morphs
(Table 1) increases the chance that pollinator flights will be between
stems of the same morph. Consequently, intramorphic pollen transfer
should increase relative to legitimate pollen transfer, resulting in
lower pollination of flowers in such clumps. This may be the cause
underlying the negative correlations between local flower density and
pollen receipt. Similarly, Price and Barrett (1984) proposed that
legitimate pollination in tristylous Pontederia cordata is limited at
some sites by spatial segregation of floral morphs in combination with
density-dependent pollinator movements. Clumped distributions of
morphs have been reported for several other heterostylous species as
well (Levin and Kerster 1974, Wyatt and Hellwig 1979, Hicks et al. 1985,
Nichols 1985). Additional evidence that the local distribution of
morphs is important to pollination is provided by the effect of the
distance to the nearest mate. As expected, the distance to the nearest
compatible plant in flower was inversely related to pollen receipt by
flowers in most cases (6 of 9 trials, Table 11). Only at times where
pollination levels were extremely low or extremely high was mate
distance non-significant. Although it is generally expected that the
distance to mates should affect pollination and reproductive success
(Levin and Kerster 1974, Richards and Ibrahim 1978, Bawa 1983, Handel
1983), several studies have failed to detect an effect of the proximity
of neighbors on pollen receipt (Bell 1985) or fruit set (Willson and
Rathcke 1974; see also Keegan et al. 1979, Wyatt and Hellwig 1979).
Seasonal increases in flower density were often positively
correlated with pollen receipt (7 of 10 trials, Table 11), but less
often with pollen dispersal (1 of 4 trials, Table 14). Higher
pollination rates at mid-season may be a function of 1) the generally
high number of visits flowers received at such times, 2) the increased
effectiveness of pollinator visits with increasing flower density, or 3)
a combination of these two factors. I did not measure visit
effectiveness, but the correspondence between visit rates and
pollination levels over a wide range of values (Figure 5 and Table 14)
suggests that visitation is an important factor in determining both male
and female components of pollination success. The amount of variation
in pollen donation from flowers explained by visit rate ranged from 19
to 50% (Table 14). In two other neotropical, hummingbird-pollinated
plant species relationships between visitation and measures of female
reproductive success were not strong. Hummingbird visitation was only
weakly related to stigmatal pollen loads in Passiflora vitifolia (Snow
1982). Similarly, McDade and Davidar (1984) found the number of
hummingbird visits received by Pavonia dasypetala flowers was not a good
predictor of fruit set or seed set.
Territoriality and Pollination Success
Territorial hummingbirds restrict pollen flow by confining the bulk
of foraging movements within the boundaries of defended feeding areas
(Schlissing and Turpin 1971, Linhart 1973, Stiles 1975, Feinsinger
1978). A plant producing sufficient nectar to support a territorial
hummingbird may encounter few opportunities for outcrossing due to
sedentary pollinator behavior. This may set an effective upper limit on
floral display size for self-incompatible plants dependent on
hummingbirds for pollination (Stiles 1975, 1978, Feinsinger 1978,
Schemske 1980b). Evidence presented here supports this idea. The
floral displays of most plants were small. At peak flowering the
average plant produced only 5 to 10 flowers each day. The most
reproductively active plants I observed contained approximately 70
flowers. A floral display of this size produces an estimated 812
calories in nectar per day (based on 11.6 calories/flower-day; Busby,
personal observation). Energy budgets of other territorial hummingbirds
indicate that this is slightly less than the amount of nectar necessary
to support a L. calolaema male (Hainesworth and Wolf 1972, MacMillen and
Carpenter 1977, Ewald and Carpenter 1978). Assuming a territorial L.
calolaema male requires 1160 calories per day, the nectar from several
profusely-flowering plants or approximately 15 plants with average
floral display sizes would be needed to support one bird. In the field,
territories composed primarily of C. elata generally contained at least
How does the pollination service provided by territorialists
compare with that of non-territorial hummingbirds? At the dense site,
where L. calolaema males defended territories through most of the
flowering season, both maternal and paternal components of pollination
success were consistently higher that at the sparse site where
generalists pollinators predominated (Tables 8 and 13). I have no
evidence, however, that territoriality per se affected pollination
success either positively or negatively. In all likelihood, the cause
of higher pollination levels at the dense site was the greater
availability of mates associated with high flower density. Regardless,
this study demonstrates that territorial hummingbirds can provide highly
effective pollination service to obligately outbred plants.
Genetic Implications of Plant Density
Evidence suggests gene flow through both pollen and seeds is high.
Dispersal of powdered dyes indicates that pollen is commonly transported
15 to 50 m by pollinators (Table 13). Frugivorous birds may carry seeds
much further. Murray (1986) estimated bird-generated seed shadows of
three understory shrub species at Monteverde and found median dispersal
distances of 35 to 60 m. Some of the same bird species he studied also
consume C. elata fruits (Wheelwright et al. 1984, Busby personal
observation). The high mobility of pollen and seeds leads to the
prediction that neighborhood area in C. elata is large.
Differences between sites in dye movement indicate flower density
plays an important role in pollen flow. At the dense site, the average
distance of pollen transport was lower than at the sparse site, but
pollen was dispersed to more flowers on greater numbers of plants (Table
13). This increased interplant pollen exchange suggests the pollen
component of gene flow is greater at higher plant density despite
shorter pollinator flights. Beattie (1976, 1978) found a similar
relationship between plant spacing and pollen-mediated gene flow in
Viola, and concluded that plants in high density colonies contained
greater evolutionary flexibility (cf. Levin and Kerster 1969a).
In contrast to differences between sites, seasonal changes in
pollen flow at each site were surprisingly modest. Neither the distance
nor the amount of interplant pollen transfer was significantly related
to seasonal fluctuations in flower density. A confounding factor was
floral visit rate. Visitation, which was strongly tied to pollen
dispersal itself (Table 14), generally rose with flower density and may
have counteracted any effect of decreasing pollinator mobility on pollen
dispersal during flowering peaks. Richards and Ibrahim (1978) point out
that changes in visitation due to flower density bias calculations of
genetic neighborhoods. Thus, while flower density clearly influences
pollen flow, other factors that change seasonally in natural populations
may complicate the density-pollination relationship.
Implications of Pollination for Reproductive Success
Considerable debate exists over the importance of pollination
events for plant reproductive success (Stephenson 1981, Bawa and Beach
1981, Bierzychudek 1981, Willson and Burley 1983). Certainly, where
numbers of pollen grains reaching stigmas are insufficient for
fertilization of all ovules, pollination potentially limits seed set.
In C. elata, substantial numbers of styles contained fewer than the two
pollen tubes required for full seed set (Table 8). The proportion of
flowers receiving no compatible pollen varied among seasons from 14.4 to
76.7% for thrums and from 32.7 to 94.8% for pins. Because styles were
collected prior to the end of flower life, pollen tube numbers reflect
only pollination events of the first half of the day. The bulk of
pollination should occur during this time: anthers dehisce about dawn,
and both nectar secretion and pollinator visits are greater earlier than
later in the day. In any event, failure to receive any compatible
pollen limits potential reproductive success of many C. elata flowers to
That pollination events influenced fecundity is supported by the
fruit-set data (Table 9). During both years, pollen receipt and fruit
set at the sparse site were lower than at the dense site. This
indicates that pollination at the sparse site limited fruit set.
Pollination may also have limited fruit set at the dense site where the
proportion of flowers with stylar pollen tubes (Table 8) was not
substantially greater than the proportion of flowers setting fruit
(Table 9). Many factors other than pollination, however, are
potentially important in determining fruit-set (Primack 1978, Stephenson
1980, 1981, Udovic 1981, Udovic and Aker 1981, Wiens 1984, Sutherland
and Delph 1984).
While some flowers received no pollen, many others received pollen
loads greatly exceeding the number of ovules. Furthermore, because
pollen from a plant was often dispersed to many different neighbors
(Table 13), it is likely that the reverse is true: pollen arriving at
stigmas often came from different individuals. Growing evidence
suggests that where large numbers of pollen grains from different
sporophytes reach the stigma, resulting seed fitness may be enhanced
through pollen tube competition or maternal selection (Mulcahy and
Mulcahy 1975, Mulcahy 1979, Schaal 1980, Bertin 1982, Marshall and
Ellstrand 1985). Variation in pollen tube growth rates and the
frequency of pollen arrival at stigmas (Busby, personal observation)
indicate that competition among pollen grains for access to ovules may
occur in some C. elata flowers As a consequence, high pollen loads
may result in improved seed quality (Stephenson and Winsor 1986).
The relationship between paternal pollination success and
reproductive success as a male should depend on levels of pollen
receipt. When the number of pollen grains reaching stigmas is less than
the number of available ovules, every compatible pollen grain arriving
at a stigma stands a good chance of fertilizing an ovule, and paternal
reproductive success should be a linear function of the number of
successfully dispersed pollen grains. Where pollen loads on stigmas are
high, pollen grains will compete for access to ovules and factors such
as the timing of pollen arrival at the stigma, pollen tube growth rate
(Mulcahy et al. 1983), and genetic compatibility of the haploid genomes
(Stephenson 1981, Stephenson and Bertin 1983, Wiens 1984) come
increasingly into play. Few successfully dispersed grains will
fertilize ovules when pollen loads are high. Consequently, male fitness
per successfully-dispersed pollen grain should decrease, on average, as
stigmatal pollen loads increase. Because pollen donation per flower
tended to be highest exactly at times when pollen receipt was also high,
the implications for reproductive success of high pollen donation may be
limited. Extensive pollen dispersal by flowers under conditions of
heavy competition among males for ovules may enhance male fitness no
more than moderate pollen dispersal at times when competition is weak.
This being the case, male reproductive success may be just as high
during times of low to moderate pollinator visitation (when pollen
donation and receipt are lower) as at peak flowering (when pollen
donation and receipt are higher).
Floral Display Size and Sexual Function
There has been considerable interest in the role of intersexual
selection in the evolution of flowering characteristics of
hermaphroditic plants (Janzen 1977, Charnov 1979, Willson 1979,
Stephenson and Bertin 1983, Sutherland 1986). Among monoecious and
dioecious plants, flowering by males and females may differ in timing,
duration and intensity of flowering (Thomson and Barrett 1981, Bullock
and Bawa 1981, Lloyd and Webb 1977; see Stephenson and Bertin 1983).
Presumably due to the difficulties of quantifying pollen donation,
little is known about how variation in flowering characteristics in
bisexual plants affects both pollen donation and receipt. In this
study, I found little evidence that floral display size or the seasonal
timing of flower production affected pollen donation differently than
pollen receipt. Floral display size had no consistent effect on
maternal or paternal measures of pollination success of flowers (Tables
11 and 14). Pollen receipt was more often significantly related to the
seasonal changes in flower density than was pollen donation, but this
may be an artifact of the smaller sample sizes for pollen donation. The
frequency of pollinator visits to flowers strongly influenced pollen
donation (Table 14), yet the same appears true for pollen receipt
Is there evidence in C. elata of gender specialization in pin and
thrum flowers? In other heterostylous species, differences among morphs
have been observed in pollen loads on stigmas (Levin 1968, Ornduff 1970,
1975a,b, 1980, Ganders 1976, Barrett and Glover 1985), fruit set
(Ganders 1975, Philipp and Schou 1982, Wyatt 1983, Hicks et al. 1985),
and pollen donation (Nichols 1985). In this study, two different
indices of reproductive success have contrasting implications for the
relative gender of the two morphs. In pollen carryover experiments,
hummingbirds transferred larger amounts of pollen to more recipient
flowers from thrum donors than from pin donors (Figure 7 and Table 7).
This implies that thrums function more as males and pins function more
as females. However, thrum inflorescences had higher fruit set than pin
inflorescences in 1983, indicating thrums were more successful as
females than were pins. Unfortunately, the techniques used in this
study for measuring pollen receipt and donation by flowers in the field
were not designed to make intermorphic comparisons. Asymmetries among
floral morphs in gender may be an important feature of the pollination
system of C. elata, but additional studies are needed to address this
Patterns of flower presentation can influence plant reproductive
success through effects on pollinator foraging movements. Mass-
flowering is frequently an effective means of recruiting large numbers
of pollinators to plants (Gentry 1974, Augspurger 1980, Frankie and
Haber 1983), whereas extended flowering, the production of few flowers
per day over long periods of time, is thought to maximize outcrossing
(Janzen 1971, Frankie 1976, Bawa 1983). The problem of balancing
attraction of pollinators with maintaining high rates of interplant
pollen transfer appears to a central one for C. elata. In this study,
visit frequency, closely tied to both male and female components of
pollination success, was often highest during seasonal blooming peaks.
Flowers on plants with many flowers also often received more hummingbird
visits. Nevertheless, because of lower rates of legitimate pollen
transfer, pollen receipt by flowers within large pin or thrum clumps was
frequently lower than pollen receipt by isolated flowers. Thus,
benefits of flowering in synchrony with the population were partly
offset by negative effects of high local densities of unimorphic
flowers. These results suggest that pollination service may well be
highest at plants that do not present large numbers of flower per day,
spread out flowering over time, yet still flower in phase with the
The optimal size of floral display in terms of pollination success
may vary with the plant's resource state. Pollen donation and receipt
per flower were often highest at plants that contained few flowers.
This means that the small floral displays, typically produced by small
or resource-poor plants, frequently receive the best pollination service
per unit investment in flowers. Nevertheless, the pollination data
suggest that over the range of floral display sizes monitored, the total
number of embryos potentially sired or set is a monotonic increasing
function of the number of flowers produced. In other words, at a small
cost in the "efficiency" of pollination, profusely flowering plants gain
considerably in potential reproductive output. The drop in pollination
efficiency on plants with many flowers might be offset by prolonging the
flowering season and producing fewer flowers each day, as described
above. Still, differences in resource availability among plants are
likely to outweigh weak effects of floral display size on the
pollination success of flowers.
In any event, it is questionable how finely tuned floral displays
in C. elata can be. First, while the seasonal timing of flower
initiation may have a genetic basis, size of floral display may be very
plastic (cf. Primack 1980, Schmitt 1983b). It is also not clear what
consequences differential pollination success has for plant fitness.
Second, although this study documents frequent, and sometimes strong,
density-dependent effects on pollen donation and receipt by plants, few
of the independent variables I examined consistently affected
pollination success. Often, the strength and even direction of
relationships showed marked seasonal and annual variation. Any
evolutionary consequences of such variable influences would be as likely
to increase as to decrease the natural variation in the size and timing
of floral displays. Existing flowering phenologies, where flowering by
all plants is extended but the magnitude of flower production varies
greatly among plants with available resources, may be in part a
consequence of conflicting ecological events and selective pressures
over space and time.
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William Huntoon Busby was born in Santa Monica, California, on
February 2, 1955. Fleeing the growing congestion and smoggy skies of
the Los Angeles Basin early in his second year, he moved to northern
California. In subsequent years, summers were passed hiking the trails
of the Sierra Nevada; winters, learning New Math or running with the
Tamalpais High School cross country team.
In 1973, Bill entered Colorado College. Despite unpleasant
memories of mitochondria and DNA structure from high school, he found he
enjoyed biology and majored in that field. Bachelor of Arts in hand, he
spent two years studying peregrine falcons with the Colorado Division of
Wildlife, teaching environmental science to 6th graders in coastal
California, and painting houses.
In the fall of 1979, he began graduate studies at the University of
Florida. After an Organization for Tropical Studies course in 1980, he
became fascinated with tropical ecology. Two and a half years were
spent in the cloud forest near Monteverde, Costa Rica, where he studied
the pollination ecology of "hot lips" (Cephaelis elata). There he met
his future wife, Anna Fortenbaugh. They were married in Bayhead, New
Jersey, in 1986.
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Pet. Feinsinger, Chairman /
Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Professor of Botany
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Associate Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Professor of Zoology
This dissertation was submitted to the Graduate Faculty of the
Department of Zoology in the College of Liberal Arts and Sciences and to
the Graduate School and was accepted as partial fulfillment of the
requirements for the degree of Doctor of Philosophy.
Dean, Graduate School
UNIVERSITY OF FLORIDA
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