Flowering phenology and density-dependent pollination success in Cephaelis elata (Rubiaceae)


Material Information

Flowering phenology and density-dependent pollination success in Cephaelis elata (Rubiaceae)
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vii, 87 leaves : ill. ; 28 cm.
Busby, William Huntoon, 1955-
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Subjects / Keywords:
Cephaelis   ( lcsh )
Rubiaceae   ( lcsh )
Pollination -- Costa Rica -- Monteverde   ( lcsh )
Fertilization of plants   ( lcsh )
bibliography   ( marcgt )
theses   ( marcgt )
non-fiction   ( marcgt )


Thesis (Ph. D.)--University of Florida, 1987.
Includes bibliographical references (leaves 77-86).
Statement of Responsibility:
by William Huntoon Busby.
General Note:
General Note:

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University of Florida
Rights Management:
All applicable rights reserved by the source institution and holding location.
Resource Identifier:
aleph - 000940990
notis - AEQ2524
oclc - 16664031
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Full Text








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.



ACKNOWLEDGEMENTS.................................................... ii

ABSTRACT.......................................................... vi

INTRODUCTION........................................................ 1

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

DISCUSSION.................................................................. 59

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
Conclusions.................................................... 74


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



William Huntoon Busby

May 1987

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.


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

nearly synonymous.

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

0 0.3-

o 0.2-

cc S 8 2
0.1 S 83


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
each site.

Study site



Area (m2)

Number of C. elata stems

Ratio of pin:thrum stems

Percent of nearest
neighbors of same morph


Meanb number of flowers/m2

3500 (900)a






a Subsample of study site sampled in 1983.

b Averaged by census date over entire season.

plants at








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


Number of
flowers with
Plants Flowers pollen tubes

Percent of
flowers with
pollen tubes




B. Pollinated flowers monitored for fruit set


Plants Flowers

Number of

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







150 -

75 -





Sparse 1982

Dense 1982


A M J J A S 0

Sparse 1983



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




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0 C0


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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).


Controlled Pollinations

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

are approximate.

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.

Pollen Carryover

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.

Pollen Receipt

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.

Pollen Dispersal

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.

Fruit Set

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.

o N

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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

corolla tube.

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.


Site Year

314 m2

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



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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

dense plot.

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. site
1982 -

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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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i ; 1983
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Figure 5--continued.


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.








1-4 20-26

Available flowers

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.

Site year

intercept slope

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


Pollen Carryover

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

4- 0)

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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

1 Pin

6 Pin

16-20 Thrum 17-20 Thrum

1 Thrum 6 Thrum

14-20 Pin

20 Pin

No. Trials

Total donor tubes
growing through
recipient styles
(X SD)

Mann Whitney U tests

No. recipient styles
with >1 donor tube
(X SD)

Mann Whitney U tests

Sequence no. of recipient
styles receiving median
donor tube (X SD)

Mann Whitney U tests

7.46.0 17.35.5

U = 1 p = .04

2.81.8 3.01.7

U = 7 p = .50

2.72.8 1.0+0.0

U = 4.5 p = .24

16.016.6 48.326.2

U = 1 p = .04



U = 4.5 p = .24

3. 62.6

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

averaged across
flowers is in

Mean SE N >1 tube

Mean SE N >1 tube

Sparse 1982
Period 1
Period 2

Sparse 1983
Period 1
Period 2
Period 3

Dense 1982
Period 1
Period 2
Period 3

Dense 1983
Period 1
Period 2
Period 3

2.4 1.7 47(116) 61.2
0.5 1.1 66(172) 23.3


1.7 66(272)
1.7 59(230)
1.6 61(138)

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.

Sparse site
Mean SD N

Dense site
Mean SD N

20.0 12.3 39

35.0 14.8 45


52.6 21.4

47.8 21.1

ANOVA results

Effect of site
Effect of morph
Site x morph interaction

F(1,118) =
F(1,118) =
F(1,118) =

26.9 18.2 29

32.7 21.6

33.7 18.2 43

43.3 21.4

ANOVA results

Effect of site
Effect of morph
Site x morph interaction






< .001
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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

isolated flowers.

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.



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
sample sizes).











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
rs n

Dense site 1982
r.s n

Dense site 1983
rs n

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

per flower.

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

15 plants.

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

male function.

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

(Figure 5).

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.

Jo Ewel
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.

Richard Kiltie
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.

Carmine Lanciani
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.

May 1987
Dean, Graduate School

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