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Avian seed dispersal of neotropical gap-dependent plants

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Title:
Avian seed dispersal of neotropical gap-dependent plants
Creator:
Murray, Kelvin Gregory, 1954-
Copyright Date:
1986
Language:
English

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Subjects / Keywords:
Birds ( jstor )
Dormancy ( jstor )
Ecology ( jstor )
Forests ( jstor )
Fruiting ( jstor )
Fruits ( jstor )
Germination ( jstor )
Seed dispersal ( jstor )
Seeds ( jstor )
Species ( jstor )

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University of Florida
Holding Location:
University of Florida
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All applicable rights reserved by the source institution and holding location.
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AEN9830 ( ltuf )
16141354 ( oclc )
0030223041 ( ALEPH )

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AVIAN SEED DISPERSAL OF NEOTROPICAL GAP-DEPENDENT PLANTS


By

KELVIN GREGORY MURRAY



























A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN
PARTIAL FULFILLMENT OF THE REQUIREMENTS
FOR THE DEGREE OF DOCTOR OF PHILOSOPHY



UNIVERSITY OF FLORIDA


1986


















ACKNOWLEDGMENTS

I am greatly indebted to many individuals for support and

assistance in completing this project. Kathy Winnett-Murray was

intimately involved in every phase of the project, providing assistance

in the field work as well as valuable advice on planning, data analysis,

and writing. That she was able to do all that, complete her own

dissertation work, and still be a wonderful wife in the face of both our

frustrations over the difficulties of field research, is truly amazing.

Peter Feinsinger likewise provided advice, assistance, and humane

editorial criticism from the earliest planning stages of the work.

Without several of his well-timed pep-talks, the study would surely have

suffered greatly and might never have been completed at all. I cannot

overestimate his positive influence on this work, or on my graduate

career in general. For this and for his friendship, I will always be

grateful.

I benefitted greatly from discussions with the other members of my

supervisory committee, H. Jane Brockmann, Thomas Emmel, Walter Judd, and

Francis Putz, who also provided valuable editorial advice on earlier

drafts of the dissertation. Discussions with Nicholas Brokaw, Carmine

Lanciani, Robert Lawton, Douglas Levey, Timothy O'Brien, Carlos Martinez

del Rio, and Harry Tiebout III were also very helpful.

My colleagues at the University of Florida, and especially the other

biologists who resided concurrently at Monteverde, were also invaluable.

Willow Zuchowski-Pounds, Bill Busby, Rita Schuster, and Sarah Sargent










provided assistance with field work. Jennifer Shopland kindly shared

mist-netting and feeding observation data on frugivores. Advice on

field techniques and data analysis were provided by these individuals as

well as by Jim Beach, Martha Crump, Eric Dinerstein, Sharon Kinsman, Yan

Linhart, David McDonald, Alan Pounds, Francis Putz, and Nat Wheelwright.

I am especially grateful to all of these Monteverde biologists, and to

members of the Monteverde community in general, for making my 27-month

tenure there one of the most enjoyable periods of my life.

Wolf Guindon, Gary Hartshorn, Joseph Tosi, Jr., Manuel Ramirez, and

Giovanni Bello kindly facilitated my use of the Monteverde Cloud Forest

Reserve. Logistical support in Costa Rica was provided by personnel of

the Organization for Tropical Studies, especially Roxanna Diaz.

Financial assistance was provided by the Jessie Smith Noyes Foundation

(administered by the Organization for Tropical Studies), the University

of Florida Department of Zoology, a Sigma Xi grant-in-aid, and NSF

grants DEB 80-11008 and 80-11023 to Peter Feinsinger and Yan Linhart,

respectively.

Finally, I thank my family. My parents, Max W. Murray and Lorene

M. Murray, and my sister, Gayle Fitchner, provided understanding and

unwaivering encouragement throughout my educational career. My wife,

Kathy, and my son, Dylan Winnett Murray, have taught me what is truly

important, and help me to keep the various aspects of my life in their

proper perspective.



















TABLE OF CONTENTS

Page


ACKNOWLEDGMENTS...... ............................................. ii

ABSTRACT........................... ................................ V

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

STUDY AREA ........................................................ 5

METHODS........ ................. .................................. 7

Crop Size, Fruiting Phenology, and Fruit Removal Rates.......... 7
Seed Germination Experiments.................................... 8
Seed Dormancy Experiments...................................... 10
Gap Dynamics of the Monteverde Cloud Forest..................... 11
Mist Netting and Analysis of Fecal Specimens................... 12
Fruit Handling, Seed Treatment, and Seed Passage Rates.......... 13
Movement Patterns of Frugivores................................. 14

RESULTS....... .................. .................................. 16

Natural History of the Plants.................................. 16
Fruit Consumers...... .......... ................................ 17
Fruit Handling and Seed Treatment in the Gut.................... 23
Spatial and Temporal Distribution of Suitable
Colonization Sites........................................... 27
Seed Shadows Produced by Birds............ .. .................. 41
Mediation of Plant Reproductive Success by Birds............... 59

DISCUSSION........................................................ 80

Effects of Fruit Handling and Gut Treatment.................... 80
Effects of Dispersal.............................................. 83
Limitations of the Model........................................ 92
Seasonal Constraints on Reproductive Success................... 94
Conclusions..... ................. .............................. 97

APPENDIX ESTIMATION OF "SEED SHADOWS" FROM DATA ON SEED
PASSAGE RATES AND BIRD MOVEMENT PATTERNS:
A HYPOTHETICAL EXAMPLE ............................... 100

LITERATURE CITED......................................................... 109

BIOGRAPHICAL SKETCH............................................... 119


















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


AVIAN SEED DISPERSAL OF NEOTROPICAL GAP-DEPENDENT PLANTS

By

Kelvin Gregory Murray

December 1986

Chairman: Peter Feinsinger
Major Department: Zoology

In cloud forest at Monteverde, Costa Rica, I investigated

reproductive consequences of avian seed dispersal for three species of

gap-dependent plants: Phytolacca rivinoides (Phytolaccaceae),

Witheringia solanacea, and W. coccoloboides (Solanaceae). Of six bird

species that consumed fruits of these plants, only three (Myadestes

melanops (Muscicapidae), Phainoptila melanoxantha (Ptilogonidae), and

Semnornis frantzii (Capitonidae) dispersed seeds in viable condition. I

estimated quality of dispersal service provided by these species by

comparing the seed shadows they produced with spatial and temporal

distributions of establishment sites for the plants.

I estimated seed shadows from data on gut passage rates of seeds

and on movement patterns of radio-tracked birds. Seed shadows produced

by all three effective dispersers were extensive, with few seeds

deposited near the parent plant, and some moved > 500 m.

Seeds of the species examined germinate in forest gaps formed by

treefalls or landslides. Germination success varies with gap size and










age, but the relationship is different for each species; both

Witheringia species germinate well in gaps as small as 15 m2 or as old

2
as 6 months, whereas P. rivinoides germinates well only in gaps > 70 m

or < 4 months. Consequently, establishment sites for all three plants

are both rare and ephemeral, but to differing degrees.

Seeds that are not dispersed to suitable habitat patches can remain

dormant in the soil until a gap is formed overhead.

To determine consequences of dispersal and dormancy for plant

reproductive success, I developed a simulation model that uses data on

seed shadows, germination requirements, seed dormancy, and forest

dynamic processes to estimate reproductive output (total offspring

produced during an individual's lifetime) and relative "fitness" (an

estimator that discounts the contribution of offspring produced after a

long period of dormancy). Results show that (1) dispersal by any of the

three effective dispersers increases reproductive output 16-36 times,

even without seed dormancy. (2) dormancy capabilities up to two years

greatly enhance both reproductive output and "fitness", but greater

capabilities increase only reproductive output. (3) Without dispersal,

dormancy has little effect on either reproductive output or fitness.

Thus, both dispersal and dormancy ("dispersal" in time) are essential to

these gap-dependent plants.


















INTRODUCTION

Recent interest in the ecology and evolution of plant-frugivore

mutualisms focuses largely on the reproductive consequences, to plants,

of fruit consumption by different animals (e.g., Snow 1965, 1971; McKey

1975; Howe and Estabrook 1977; Howe and De Steven 1979; Howe and Vande

Kerchove 1979, 1980, 1981; Thompson and Willson 1979; Howe 1980; Stiles

1980, 1982; Herrera 1981, 1984; Sorensen 1981, 1983; Thompson 1981;

Stapanian 1982; Skeate 1985). Most studies deal with fruit removal or

qualitative aspects of dispersal only: they distinguish between regular

and occasional visitors to fruiting plants (e.g., Leck 1972, Howe and

Primack 1975, McDiarmid et al. 1977, Howe 1977, 1980, Howe and De Steven

1979, Howe and Vande Kerchove 1979, Hilty 1980, Greenberg 1981), between

animals that pass seeds in viable condition and those that destroy seeds

(e.g., Howe 1980), or between animals that disperse seeds away from the

parent plant and those that drop seeds directly beneath it (e.g., Howe

1977, 1980, 1982, Howe and Vande Kerchove 1979, 1981). However, few

studies directly address the contributions to plant reproductive success

resulting from the spatial distributions of seeds, or "seed shadows,"

produced by dispersers.

This study deals with the reproductive consequences of avian seed

dispersal in three gap-dependent plant species of neotropical cloud

forest. Using data on the dynamics of gap formation and the seed

germination requirements of plants, I first identify the spatial and

temporal distributions of suitable habitat patches ("gaps" formed by











treefalls or landslides) within the forest. Second, I compare the

distribution of suitable patches with the "seed shadows" produced by

different frugivorous birds. Finally, I evaluate the impacts of

fruiting phenology, plant longevity, seed dormancy, and other plant life

history traits on plant reproductive success and on the ecology and

evolution of plant-disperser interactions.

In spite of the recent explosion of research on plant-frugivore

interactions (reviewed by Howe and Smallwood 1982, Janzen 1983a; see

also Estrada and Fleming 1986), knowledge of their ecology and evolution

lags behind that of plant-pollinator interactions (reviewed by

Feinsinger 1983, Jones and Little 1983, and Real 1983). This

discrepancy occurs because the reproductive consequences of pollen

dispersal by animals are more easily quantified than the consequences of

seed dispersal (Wheelwright and Orians 1982). In plant-pollinator

systems, both the origin of, and "target" for, pollen grains are

specific and easily recognized by dispersers and ecologists alike.

Furthermore, pollinators are rewarded for delivering pollen grains to

the target--the stigma of a conspecific flower. Thus, we can determine

the relative advantages of pollen dispersal by different animals by

determining which ones are most likely to deposit pollen grains on the

stigma of a conspecific flower. In contrast, the only target for

dispersed seeds is generally a patch of soil with a combination of

physical, chemical, and biotic characteristics that make it a suitable

site for germination and growth (i.e., a "safe site," sensu Harper

1977). Furthermore, no reward is offered to vectors that deposit seeds

in such sites. For most plants, we lack detailed knowledge of the

characteristics of suitable target sites for seeds, let alone their










spatial and temporal distributions. As a result, we know little about

the reproductive advantages of dispersal for most plants, and even less

about the consequences of dispersal by particular animals.

To understand plant-frugivore relationships and the phenotypic

traits associated with them, we must identify the spatial and temporal

distributions of seed "targets" and evaluate the likelihood of dispersal

to those sites by different animals. Howe and Smallwood (1982) proposed

three alternative functions of seed dispersal. First, dispersal may

result in decreased density- or distance-dependent mortality on seeds or

seedlings near the parent plant (e.g., Howe and Primack 1975, Janzen et

al. 1976, Platt 1976, Salmonson 1978, Clark and Clark 1981, Augspurger

1983a,b, 1984a,b, Howe et al. 1985). Second, dispersal by certain means

(e.g., by ants that carry seeds to rotting logs) may result in non-

random seed movement to particular sites where the probability of

survival is especially high (Docters van Leeuwen 1954, Handel 1978,

Culver and Beattie 1980, Thompson 1980, Davidson and Morton 1981a,b).

Third, widespread dispersal may allow colonization of ephemeral,

spatially unpredictable patches of disturbed habitat (cf., Augspurger

1983a,b, 1984a,b, Platt 1975, 1976).

Although the three functions proposed by Howe and Estabrook are not

mutually exclusive, the third may be most important for many plants. In

most tropical and temperate forests, recruitment of many plant species

occurs only in patches created by canopy disturbances such as treefalls

and landslides (Richards 1952, Schultz 1960, Whitmore 1975, Hartshorn

1978, Brokaw 1980, Denslow 1980). Such gap-dependent or "pioneer"

species typically germinate in forest gaps soon after formation, grow

rapidly to reproductive size, and produce large numbers of seeds. They











often die out as the gap is closed by lateral growth of trees on the

gap's border and by vertical growth of other plants within the gap. In

most gap-dependent species, germination is stimulated by the increased

red/far red ratio of incident light (e.g., Vazquez-Yanes 1977, 1980,

Vazquez-Yanes and Smith 1982, Vazquez-Yanes and Orozco-Segovia 1984) or

increasing soil temperature fluctuations (Aubreville and Leroy 1970,

Vazquez-Yanes 1976, Vazquez-Yanes and Orozco-Segovia 1982, 1984) that

characterize recent gaps (Schultz 1960). Such plants are ideal for

studies on seed dispersal. The spatial and temporal distributions of

suitable habitat patches can be determined by first establishing the

range of gaps in which germination and establishment occur, and then

measuring the distribution of those gaps over the landscape.

















STUDY AREA

From June 1981 through July 1983, I studied the interactions

between frugivorous birds and Phytolacca rivinoides Kunth & Bouche

(Phytolaccaceae), Witheringia solanacea L' Her, and W. coccoloboides

(Damm.) Hunz. (Solanaceae) in the Monteverde Cloud Forest Reserve, Costa

Rica (10018'N, 8448'W). Lawton and Dryer (1980) provide a thorough

description of the geography, climate, and forest types of the Reserve.

The Monteverde area lies on a gently sloping plateau, on the Pacific

slope of the continental divide in the Cordillera de Tilaran. Local

weather patterns and vegetation of the area are strongly influenced by

the northeast trade winds. Blowing mist is a nearly constant source of

water for plants near the continental divide, even during much of the

dry season (January to early May). Forest types in the area range from

Lower Montane Rain Forest (Holdridge life zone classification system,

Holdridge 1967) near the continental divide, through Lower Montane Wet

Forest to Lower Montane Moist Forest and Premontane Wet Forest zones

along the lower edge of the plateau.

Sites used in this study were all located between 1450 and 1650 m

elevation, within either Lower Montane Rain Forest (oak ridge forest,

windward cloud forest, and swamp forest, sensu Lawton and Dryer 1980),

or within the Lower Montane Wet Forest Rain Forest transition zone

(leeward cloud forest, sensu Lawton and Dryer (1980)). Dominant

overstory vegetation within the study area includes many species of

Lauraceae, Moraceae, and Araliaceae, in addition to Meliosma sp.,











Sloanea megaphylla, Guarea spp., Hieronyma poasana, Ardisia palmana, and

Clusia alata. The understory is dominated by Rubiaceae, Solanaceae,

Acanthaceae, Gesneriaceae, Piperaceae, and Palmae. Many species occur

most commonly in light gaps formed by falling branches or trees,

including the "pioneer" trees Cecropia polyphlebia, Urera elata, Trema

micrantha, Sapium pachystachys, Heliocarpus popayensis, Clibadium

leiocarpum, and several species of Miconia and Conostegia. Several

shrubs and large herbs also occur commonly in gaps, e.g., Solanum

acerosum, S. hispidum, Witheringia spp., Phytolacca rivinoides,

Heliconia tortuosa, Bocconia frutescens, and Eupatorium sexangulare.

Seedlings of Phytolacca rivinoides, Witheringia solanacea, and W.

coccoloboides are very common in recent treefalls, especially on soils

disturbed by uprooted trees. Within one month of formation, these "pits

and mounds" (sensu Putz 1983) are generally covered by hundreds of

seedlings of these and other species, especially Cecropia polyphlebia

and Bocconia frutescens. A typical treefall examined approximately one

month after formation contained 79 seedlings of P. rivinoides on the

"mound" area alone (Murray, unpubl. data). Of the many gap-dependent

species at Monteverde, I concentrated on P. rivinoides, W. solanacea,

and W. coccoloboides because they have similar fruits (small, multiple-

seeded berries) and growth forms, but slightly different life history

traits. By doing so, I hoped to evaluate the consequences of dispersal

by similar assemblages of frugivores to plants with different

reproductive schedules, longevities, and germination requirements.


















METHODS

Crop Size, Fruiting Phenology, and Fruit Removal Rates

I collected data on fruit crop sizes and fruiting phenology using

monthly censuses of 8, 36, and 33 individuals of P. rivinoides, W.

solanacea, and W. coccoloboides, respectively. Plants occurred in

several different building-phase (sensu Whitmore 1975) treefall plots

and in larger, man-made clearings within the reserve. During each

census, I counted all flowers, green fruits, and ripe fruits on each

plant.

Since most flowering and fruit development in both Witheringia

species occurs well before ripening begins, I defined the total fruit

crop in those species as the largest number of green fruits counted on

that plant during any census in that fruiting episode. In Phytolacca, I

estimated total fruit crop as the product of the number of

infructescences formed and the average number of fruits per

infructescence. I computed population-level fruiting phenology of each

species (i.e., that of the "average" individual) by first determining

the proportion of each individual's fruit crop that ripened each month

(number of ripe fruits censused in each month divided by the sum of all

ripe fruits censused on that plant over the fruiting season), and then

averaging this proportion over all individuals censused. Thus,

individuals with large fruit crops and those with small fruit crops were

weighted equally in determining the fruiting phenology of the "average"

individual.











To determine rates of fruit removal from individual plants, I

counted the number of ripe fruits on marked branches (Witheringia) or

infructescences (Phytolacca) on each census plant on one day, and then

counted those remaining 24-72 hours later. For purposes of the analyses

reported here, each observation consisted of two such censuses on one

plant. During the first count, I removed any damaged or desiccated

fruits that might abscise spontaneously before the next census. In most

cases (77% of all observations), I counted all ripe fruits on the plant.

On very large plants or those with inaccessible fruits (23% of all

observations), I marked and counted only a subsample of branches or

infructescences. Plants were checked in this way for 2-4 consecutive

days each month. Eighty-six percent of the observations were from

plants re-censused after 24 hours. In those checked after 2 or 3 days,

I divided the number of fruits removed by the number of days between

censuses. All removal data are thus reported on a per day basis. I

could not obtain information on removal rates by direct observation;

the birds responsible for removing most fruits from these plants are

extremely wary, and generally avoid feeding in the understory anywhere

near an observer.




Seed Germination Experiments

I conducted experiments to determine germination success of P.

rivinoides, Witheringia solanacea, and W. coccoloboides in closed-canopy

forest and in treefall gaps of various sizes and ages. Seeds used in

all experiments were collected from several plants, mixed, and assigned

to different treatments at random. Since many comparisons had to be

made at different times of year, strict controls were not possible for











all experiments. In such cases, I attempted to eliminate most of the

obvious biases introduced by seasonal weather conditions. For example,

during the driest months (March and April) when germinating seeds

desiccate easily, I watered all seeds 1-2 times per week. Although this

practice may result in an overestimate of seed and seedling survival in

gaps during very dry periods, it provides unbiased data for answering

the more immediate question of the relationships between germination

success and gap size and age.

To compare germination success in closed-canopy forest with that in

large gaps, I planted 100 seeds of each species in cups of sterile soil

in a large (ca. 2440 m2) man-made gap and 100 others (in like fashion)

in adjacent forest. Gap seeds received full sunlight for most of the

day, whereas canopy cover over forest seeds was greater than 98%, as

determined by a canopy densiometer. Both groups of seeds were covered

with a screened (ca. 1 mm mesh) enclosure to exclude herbivores and seed

predators. Setups were checked for germination and seedling survival at

1-14 day intervals for 14 months.

I measured the effects of smaller gaps on germination success by

planting 50 seeds of each species in small cans of soil (10 seeds/can)

near the centers of six recent treefall gaps of different sizes. Where

necessary, I placed cans above any ground-layer vegetation so that

shading was due solely to the crowns of trees bordering the gap. By

thus eliminating shade from rapidly growing plants within gaps, effects

of gap age (see below) on germination success were controlled. These

setups were checked at weekly intervals for 2-3 months. I determined

gap size using the formula for the area of an ellipse











(A = 7f-L W / 4, where L and W represent the lengths of the major and

minor axes of the ellipse), since most gaps were roughly elliptical.

Because light quality and intensity within a gap decrease over time

as a result of shading from rapidly growing vegetation within it, I also

determined the effects of gap age on germination success. Experiments

were conducted in four gaps as they aged naturally. Three of the gaps

were formed during a severe windstorm on 13-14 November 1982, the fourth

during a storm on 11 January 1983. I planted fifty seeds of each

species, in 5 groups of 10 seeds each, in small metal cans along

transects running through the centers of the gaps. Setups were checked

at weekly intervals for 1.5-2.5 months. The first run of this

experiment was started 2-4 weeks after gap formation, and was repeated

in each gap with 50 new seeds at 3-4 month intervals for one year.



Seed Dormancy Experiments

To estimate how long seeds of P. rivinoides, W. solanacea, and W.

coccoloboides can remain dormant in the soil, I determined the viability

of cohorts of seeds buried for different periods of time. In December

1981 I collected approximately 850 seeds from 5 to 20 individuals per

species. After combining seeds taken from all individuals of a

particular species, seeds were randomly assigned to treatments (burial

for different periods of time) and then packed in small bags of mosquito

netting or in microcentrifuge vials with mesh coverings. All seeds were

then buried approximately 15 cm deep at a forest site with approximately

98% canopy cover.

At one to two month intervals over the next 17 months, I recovered

50 seeds of each species from the burial site and planted them in











plastic cups of forest soil in the center of a large, man-made clearing

40 m away. Seeds were checked at least once every two days for

germination. During the dry season, seeds were watered at least every

other day.

In March 1984, I recovered an additional 50-75 seeds of each

species from the burial site and planted them in plastic cups of potting

soil in a greenhouse on the University of Florida campus. These seeds,

like those germinated in the field, were checked at least every two days

until all seeds had germinated, or until no further germination had

occurred for four weeks.




Gap Dynamics of the Monteverde Cloud Forest

From May to July 1983 I set up five permanent 500 m line transects

through representative areas of the Lower Montane Wet Forest and Rain

Forest zones in the reserve. For each "expanded" gap (the area bounded

by lines connecting the trunks of trees bordering the canopy gap; see

Runkle 1982) encountered along a transect, I measured the transect

interval within the canopy gap (defined as the land area directly

beneath the canopy opening), length and orientation of the major and

minor axes of the canopy gap, and height of the surrounding canopy. I

sampled even the very small gaps (down to 1.6 m2) formed by single

branches, because data from germination experiments suggested that even

gaps of that size affected germination success in P. rivinoides, W.

solanacea and W. coccoloboides. I also subjectively estimated gap age

in years. This was easily done for gaps formed in the previous year,

because most still contained intact twigs and leaves of the fallen tree,

as well as many epiphytes. The proportion of land area occupied by gaps











less than one year old was computed as the length of transect under

those canopy gaps divided by the total transect length. Gap area was

determined using methods described above. I censused the transects

again in March 1984 to collect data on gaps formed since the previous

July.




Mist Netting and Analysis of Fecal Specimens

From June 1981 through July 1983, I regularly mist-netted birds in

14 study plots: six in treefall gaps from 1.5 to 3.5 years old, four in

large, man-made clearings (hereafter termed "cutover" plots), and four

in mature forest with intact canopy. Plots were chosen primarily for

another study, and are described in detail in Feinsinger et al. (in

review). From June 1981 through July 1982, I netted for the first six

hours of daylight (ca. 0515-1115) in two plots of each of the three

habitat types each month. Plots used each month were alternated so that

sampling effort was approximately equal in all forest and cutover plots,

and most treefall plots, over the first 12-month period. From September

1982 through July 1983, I netted at least one day (i.e., for the first 6

hours of daylight) per month in each of three plots, one in each habitat

type. For this 11-month period, the same three plots were sampled each

month. Additional netting in these and other plots was conducted on an

irregular basis. I also netted in one of these plots from 4 to 20 March

1984.

All birds captured were weighed, measured, and checked for breeding

condition and molt. Frugivores were marked with unique color

combinations using plastic leg bands and then retained from 5 to 45

minutes in small holding cages (ca. 20x20x30 cm) to obtain fecal











specimens. I also collected samples from many, but not all,

insectivorous species. Fecal specimens were stored in 70% ethanol. In

the laboratory, I counted and identified all seeds in each sample using

a reference collection made over the two-year study. I also visually

estimated the percent arthropod composition of each sample to the

nearest 10%.




Fruit Handling, Gut Treatment, and Seed Passage Rates

To determine the consequences to P. rivinoides, W. solanacea, and

W. coccoloboides of fruit consumption by different bird species, I

conducted feeding experiments with captive individuals of six bird

species observed to eat their fruits. Birds were captured in mist nets

and maintained in a small (ixlxlm) cage during the experiments. Between

trials, fruits other than the experimental species, as well as water,

were provided ad libitum. In all but two cases, trials were completed

and the bird was released on the same day. After introducing the

experimental fruits into the cage, I noted whether or not birds consumed

the fruits, how fruits were ingested (e.g., swallowed whole vs. eaten

piecemeal), whether the ingested seeds were voided intact, and whether

they were defecated or regurgitated. Recovered seeds, or a subset if

many trials were run, were then planted in plastic cups of soil under a

screened enclosure in a large clearing. I checked seeds at least once

every two days for germination, and watered them when necessary.

To determine gut passage rates, I conducted feeding trials in a

similar fashion. Approximately 7-15 fruits of either P. rivinoides, W.

solanacea, or W. coccoloboides were introduced on the cage floor, and

all other fruits were removed from the cage. I observed subsequent


I











events through a small hole cut in one opaque side of the cage. Birds

usually descended from perches to feed within a few minutes after the

test fruits were introduced. All uneaten fruits were removed 5 min.

after the first fruit was consumed. The midpoint of the interval during

which fruits were eaten was considered as the time of ingestion for all

fruits in a particular trial.

Each time a bird defecated, I recorded the time and the location of

the fecal mass on the floor of the cage. After 3-5 fecal masses had

accumulated, I removed the paper from the bottom of the cage and

replaced it. At the end of the feeding trial, all fecal masses were

recovered; seeds were later identified and counted. Successive feeding

trials were done approximately 30 min apart; i.e., the next trial (with

a different fruit species) began 30 min after the beginning of the

previous trial. In this way, I could usually complete 1-2 feeding

trials on each bird with each of the three fruit species before

releasing it on the afternoon of the same day it was caught.

After counting seeds in the fecal masses, I grouped the data into

5-min classes, recording the proportion of all seeds voided in each 5

min time segment following ingestion.



Movement Patterns of Frugivores

To determine the movement rates and patterns of birds taking P.

rivinoides, W. solanacea, and W. coccoloboides fruits in the field, I

fitted mist-netted birds with small (ca. 3.5g) radio transmitters and

followed their movements for 3-8 days. Transmitters used were homemade

units similar to those available from a number of commercial telemetry











suppliers. I used an LA-12DS receiver (AVM Instrument Company, Dublin,

CA) and a homemade 5-element yagi antenna.

Transmitters were attached to the skin and feathers on a bird's

back (just anterior to the synsacrum) with Super Gluem. Birds fitted

with transmitters were held in the field in a small cage for

approximately 30 min to ensure that they were healthy when released.

By using a carefully mapped network of trails, I could often remain

within sight of radiotagged birds for long periods of time. Each time

the bird moved to a new location, I simply recorded the time and the

bird's location on a map of the study area. When I was out of visual

contact with the bird, I determined its location by triangulation. I

took compass bearings on the direction of the strongest signal from two

points, separated by at least 50 m, on the mapped trail system. After

taking the second bearing, I rechecked the first to ensure that the bird

had not moved. I took new bearings as soon as the signal received

indicated (by a change in signal strength or direction) that the bird

had moved. In the absence of any such indication, I took two new

bearings every 3-5 minutes to check the bird's location.

















RESULTS

Natural History of the Plants

Phytolacca rivinoides is a large herb ranging from Mexico to

Bolivia (including the Antilles, Raeder 1961) at elevations from sea

level to 3000 m (Standley 1937). Usually among the first colonists of

treefalls and landslide edges, individuals commonly spread to cover

approximately 25 m2 within 1-2 years of seedling establishment. Plants

begin to ripen fruits at about one year of age, but most die (presumably

as a result of shading and/or root competition) within 2.5 years of

establishment. Of the eight individuals I monitored closely, the median

age at death was 24 months (range 21 to 31 months). During the single,

extended fruiting season, individuals produce 1,500-30,000 (median =

4700) fruits borne on axillary racemes containing ca. 30-100 fruits

each. The fruits are purple-black, about 7.5 mm in diameter, and

contain 5-12 (x=9.4, n=20) seeds in a watery pulp.

Witheringia solanacea and W. coccoloboides are both shrubs

attaining heights of about 1.5-2.5 m. Witheringia solanacea ranges from

Mexico to Brazil, including the Antilles (D'Arcy 1973), occurring from

sea level to 2000 m (Standley 1937). Witheringia coccoloboides is

typical of cloud forests from Costa Rica to Colombia at elevations from

300 to 2500 m (D'Arcy 1973). Both species grow much more slowly than

does P. rivinoides; although seedlings are common in young gaps, they do

not attain reproductive size for about 3-5 years, and they usually live

for 8 or more years before being shaded out by the reestablishing











canopy. Fruits of both Witheringia species are red, ca. 10-12 mm in

diameter, and are borne in axillary fascicles. Fruit crop size and seed

number are highly variable in both species. Total seasonal fruit crops

in W. solanacea ranged from 5 to 1084 (median=154, n=121), and seed

number per fruit ranged from 6 to 39 (x=22.8, n=44). Seasonal fruit

crops in W. coccoloboides ranged from 5 to 1150 (median=120, n=84), and

seed number ranged from 46 to 73 (x=59.1, n=17).

Fruits of all three species show typical adaptations for bird

dispersal (van der Pijl 1972). Removal by animals other than birds is

probably rare. Although rodents are known to eat fruits of some

understory plants, including P. rivinoides (Denslow and Moermond 1982),

I found no evidence of removal by rodents at Monteverde. Early morning

counts of fruits marked on the previous afternoon showed no evidence of

nocturnal removal, and no fruits were removed from two plants each of W.

solanacea and W. coccoloboides from which birds, but not rodents, were

excluded by screened enclosures left open at the bottom (Murray, unpubl.

data). In addition, an intensive concurrent study of frugivorous bats

revealed no evidence of these fruits in bat fecal specimens (E.

Dinerstein, pers. comm.).



Fruit Consumers

The disperser assemblages for P. rivinoides, W. solanacea and W.

coccoloboides at Monteverde are surprisingly limited. Data from ca. 200

fecal samples collected from mist-netted frugivores, as well as

extensive observations by several investigators (Wheelwright et al.

1984), suggest that only ten bird species commonly consume fruits of any

of these plants in the Monteverde vicinity. The limited size of the











disperser assemblage comes about because few species of frugivorous

birds commonly descend to the forest understory or into treefall gaps;

similar fruits of canopy trees and epiphytes are often taken by a much

larger number of bird species (Wheelwright et al. 1984). The three

major dispersers for all three plant species in cloud forest above 1500

m are Black-faced Solitaires (Myadestes melanops, Muscicapidae), Black

and Yellow Silky Flycatchers (Phainoptila melanoxantha, Ptilogonatidae),

and Prong-billed Barbets (Semnornis frantzii, Capitonidae). Of the 360

seeds of these three plant species recovered in fecal specimens from 196

frugivores, all were from these three bird species. Furthermore, these

data also suggest that Myadestes is responsible for far more dispersal

of these plants than are either Semnornis or Phainoptila: 84% of

recovered seeds were from Myadestes alone.

Although P. rivinoides, W. solanacea, and W. coccoloboides are

highly dependent upon a very few bird species for dispersal services,

none of the birds is similarly dependent upon any of the three plant

species. The known diets of Myadestes, Phainoptila, and Semnornis

include fruits of 51, 14, and 30 species, respectively (Wheelwright et

al. 1984; K. G. Murray, unpubl. data). In fact, fruits of the three

plants are of relatively minor importance in the diets of these birds.

Of the 154 fecal specimens collected from these three species, only 35%

contained seeds of P. rivinoides, W. solanacea, or W. coccoloboides.

The ecological relationships between these three plants and their

dispersers are thus highly asymmetrical.

Seven other bird species removed fruits from at least one of the

plant species. The tanagers Chlorospingus opthalmicus and Tangara dowii

and the finch Pselliophorus tibialis occasionally removed fruits, but











failed to ingest most seeds (see below). Of the remaining four species

recorded feeding on P. rivinoides, W. solanacea and W. coccoloboides,

only one was a frequent visitor to any of these plants: at elevations

below approximately 1420 m, seeds of W. solanacea were commonly found

under display perches of Long-tailed Manakins (Chiroxiphia linearis,

Wheelwright et al 1984).

Data from mist net captures (Table 1) also suggest the unequal

importance of these ten bird species as dispersers for P. rivinoides, W.

solanacea, and W. coccoloboides. Of the three primary dispersers, M.

melanops was the most frequently captured in all three habitats. In

fact, M. melanops may be the most important disperser for all understory

plants with bird-disseminated seeds within the Monteverde Cloud Forest

Reserve.

Capture rates for Myadestes were highly variable over time, however

(Fig. 1). While usually very common in the reserve from February

through August, they were all but absent from late October through early

January. The seasonal decline in capture rate was due to emigration of

both adults and young following the breeding season. Visual and

auditory censuses confirmed this seasonal pattern of abundance (K. G.

Murray, unpubl. data). Where Solitaires go when they leave the

Monteverde area remains somewhat a mystery, but D. J. Levey (personal

communication) has caught several individuals during this season at

Finca La Selva, at ca. 50 m elevation in the Atlantic lowlands.

Although some other species of frugivorous birds at Monteverde are also

altitudinal migrants (e.g., Three-wattled Bellbirds, Procnias

tricarunculata, and Resplendant Quetzals, Pharomachrus moccino;

Wheelwright 1983, and K. G. Murray, personal observation), I have no





























Table 1. Capture data for bird species feeding at least occasionally
on fruits of P. rivinoides, W. solanacea, and W.
coccoloboides at Monteverde. Total numbers of mist net hours
in forest, treefall, and "cutover" (see text) plots were 1158,
1164, and 1449, respectively.



Species forest treefalls "cutovers"a
Myadestes melanops 66 30 33

Phainoptila melanoxantha 1 0 4

Semnornis frantzii 0 0 3

Chlorospingus opthalmicus 10 9 5

Tangara dowii 0 0 1

Pselliophorus tibialis 1 0 2


a Capture data from these unusually large (1155-2442 m2) man-made
clearings are not included with those from natural treefalls.
Plant and bird assemblages in the large clearings were more
typical of early second growth habitats than those of natural
forest or treefall gaps.


I















>1


0
4-O














4-4
0










04
4Q 0
















0
C4-


o























44
0
S4

0
O








-4-
0











(d4
C |































a)
aa
Qi






































00
0
EU


















0 2
4




















oa)


















0-)
0-



S-4


aa-)
fa 4-


(a a)






4 U

u 0
Q4

a) a)
a)





4-1


0lt)
'o a)
(0 4-
>,l ro
s lua





















r CV)

-1 00
SLL0
-1




IiC








0
'> -- "















-- -- LL co
o
SLLC)
ez z -
0 0U





-/C)





0 0 0 0 0
d d o o
6 6 0 0nH-

unOH-i3N u3d Q3ufnidVO S0JSGpeiJV











evidence that any other disperser of P. rivinoides, W. solanacea, and W.

coccoloboides undertakes such annual movements.




Fruit Handling and Seed Treatment in the Gut

Consumers of P. rivinoides, W. solanacea, and W. coccoloboides at

Monteverde handled fruits by one of two methods. Myadestes,

Phainoptila, and Semnornis invariably swallowed fruits whole, with

little or no manipulation in the bill. In contrast, the tanagers

Chlorospingus opthalmicus and Tangara dowii, and the finch Pselliophorus

tibialis, mashed fruits extensively in the bill before swallowing. This

behavior resulted in the fruit skin and many of the seeds being dropped

before the pulp was ingested. Field observations of these and other

tanager and finch species suggest that most handle fruits in this

manner. As a result, these birds ingest and disperse few, if any, of

the seeds they remove from most plants.

The probability of seed ingestion in tanagers and finches seems to

depend at least in part on seed size. In Pselliophorus, Chlorospingus,

and Tangara, most seeds were discarded along with the fruit skin during

handling (Table 2). Nevertheless, some W. solanacea seeds (ca. 1.5 mm

diameter) were ingested by all three species, especially by

Pselliophorus. In contrast, none of the birds ingested any of the

larger seeds of W. coccoloboides (ca. 2.4 mm diameter); all were

discarded with the fruit skin. For seeds of a given size, the

probability of ingestion increases with bird size. P. tibialis (ca.

30.5 g; gape 10.3 mm) ingested 71% of the W. solanacea seeds offered,

whereas C. opthalmicus (ca. 20.0 g; gape 9.1 mm) and T. dowii (ca. 20.0

g; gape 8.5 mm) ingested only 10.7% and 15.8%, respectively.










Apparently, larger seeds are more easily separated from the fruit pulp

during manipulation in the mandibles, especially by birds with smaller

bills. Data on the seed loads recovered from mist-netted tanagers at

Monteverde support this suggestion: feces of these birds generally

contained only the minute (ca. 0.2-.06 mm diameter) seeds from species

of Ericaceae, Melastomataceae, and Gesneriaceae (K. G. Murray, unpubl.

data). Small tanagers such as Chlorospingus and Tangara may act as

dispersers only for plants with such minute seeds.

The effect of gut passage on seeds also varies among bird species.

Data from feeding trials suggest that although many seeds of W.

solanacea may be ingested by Pselliophorus, very few survive passage

through the gut (Table 2). Instead, most seeds were apparently ground

up in the gut; feces of the individual used in this experiment contained

large numbers of recognizable W. solanacea seed fragments. Only two W.

solanacea seeds emerged intact, and these were inviable (Table 3). The

absence of seed fragments in feces of the same bird after feeding on W.

coccoloboides fruits again strongly suggests that seeds of this species

are not ingested by Pselliophorus. Data for Chlorospingus and Tangara

suggest that the few W. solanacea seeds that are ingested pass through

the gut intact (Table 2); no evidence of destruction in the gut (such as

seed fragments in the feces) was found, and the few seeds recovered from

feces were fully viable (Table 3).

Seeds eaten by Myadestes, Phainoptila, and Semnornis were always

voided intact. Although I found no evidence of either increased or

decreased germination success (defined simply as the percent of seeds

that germinated following gut passage) as a result or gut passage in any

of these birds, the rate at which seeds of all three plant species










25

















Table 2. Fruit handling techniques and gut treatment effects on seeds
eaten by captive individuals of six frugivore species.


Bird
speciesa
M.m.




P.m.




S.f.




C.o.



T.d.

P.t.


M.m.
S.f.=
T.d.=


Plant
species
P.r.
W.s.
W.c.


seed
diameter (mm)
2.0
1.5
2.4


fruits
eaten
53
69
36


P.r.
W.s.
W.c.

P.r.
W.s.
W.c.

W.s.
W.c.

W.s.

W.s.
W.c.


seeds
dropped
0
0
0

0
0
0

0
0
0

16
36


seeds
ingested
411
1366
1206

168
447
524

413
145
477


voided
intact
411
1366
1206

168
447
524

413
145
477


2 25


38
111


Myadestes melanops, P.m.= Phainoptila melanoxantha,
Semnornis frantzii, C.o.= Chlorospingus opthalmicus,
Tangara dowii, P.t.= Pselliophorus tibialis


P.r.= Phytolacca rivinoides, W.s.= Witheringia solanacea,
W.c.= Witheringia coccoloboides


c Of seeds ingested


--


--


























Table 3. Effects of gut passage on germination success and germination
rate. Data on untreated controls taken from Table 4.


percent germination (n)


days to 95%


germination


Bird Plant
speciesa species


M.m.


P.m.




S.f.




C.o.

T.d.

P.t.


P.r.
W.s.
W.c.

P.r.
W.s.
W.c.

P.r.
W.s.
W.c.

W.s.

W.s.

W.s.


treated


(100)
(100)
d


untreated


89
86
86


89 (100)
d
d

75 (100)
d
d

100 (3)

100 (3)

0 (2)


(100)
(100)
(100)

(100)
(100)
(100)


treated


22
45
31


89 (100)
86 (100)
86 (100)

86 (100)

86 (100)

86 (100)


a M.m.= Myadestes melanops, P.m.= Phainoptila melanoxantha,
S.f.= Semnornis frantzii, C.o.= Chlorospingus opthalmicus,
T.d.= Tangara dowii, P.t.= Pselliophorus tibialis

b
P.r.= Phytolacca rivinoides, W.s.= Witheringia solanacea,
W.c.= Witheringia coccoloboides

c Of those that germinated

dInsufficient number of seeds available for experiment


untreated











germinated was often enhanced by gut passage (Table 3). Thus, although

treatment in a bird gut is not required for germination in any of these

plants, seedlings from treated seeds may gain a competitive advantage

through rapid germination in a newly created patch of suitable habitat.




Spatial and Temporal Distribution of Suitable Colonization Sites

Germination Requirements

Gap vs. understory comparisons. Results of forest vs. gap

germination experiments (Table 4) show that after 60 days, all three

species had significantly higher germination success under gap

conditions than under closed canopy. Many Witheringia seeds did

eventually germinate in the forest after more than a year. These seeds,

however, were protected from litter fall by the screened enclosure.

Ordinarily, seeds on the forest floor would be covered by leaf litter

and incorporated into the soil seed bank in a dormant state long before

they germinated.

Germination success vs. gap size. Germination success increased

with increasing gap size in all three species (Fig. 2). In fact, slopes

of the regressions (on transformed variables; see Fig. 2 legend) of

germination success on gap area do not differ significantly among the

three species (Fs=1.550 with df=2,15, 0.1 < P < 0.25). Furthermore,

analysis of covariance shows that the regression lines for the two

Witheringia species are indistinguishable (Fs=0.07 with 1,17 df,

P > .75), but that the adjusted mean germination success in P.

rivinoides is less than that for the other two species (Fs=12.82 with

1,17 df, P < .005). Equations for the adjusted (by analysis of covariance)

regressions are y = 6.84x + 12.88 for both W. solanacea and W.

































Table 4. Percent germination success in forest and large gap habitats.
Sample size for all experiments was 100. Differences between
gap and forest values were tested with a test for equality of
two percentages (Sokal and Rohlf 1969: 608).


gap


forest


after 60 days


Phytolacca rivinoides

Witheringia solanacea

Witheringia coccoloboides


after 410 days


Phytolacca rivinoides

Witheringia solanacea

Witheringia coccoloboides


<.001

<.001

<.001


<.001

<.001


87 >.5











coccoloboides, and y = 6.84x + 1.14 for P. rivinoides, where y is the

arcsin transform of the proportion of seeds germinating and x = In(gap

area + 1). Thus, germination success increases with gap size at the

same rate in all three species, but for a given gap size, germination

success in P. rivinoides is always less than for either species of

Witheringia. Consequently, P. rivinoides requires larger gaps than

either species of Witheringia for germination. Such differences in the

relationship between gap size and germination success translate directly

into differences among species in the distribution of suitable

germination sites over the landscape.

Germination success vs. gap age. Seeds of P. rivinoides, W.

solanacea and W. coccoloboides also differ in the relationship between

germination success and gap age (Fig. 3). Because the gaps used were of

different sizes, data plotted in Figure 3 were adjusted to control for

the effects of gap size, according to the relationships in Figure 2. To

facilitate comparison among species, data were also scaled such that the

highest germination success attained in each species was set at 100%.

Germination success decreased with increasing gap age in all three

species, presumably as a result of decreasing light intensity (or

quality) as the understory vegetation within the gap grew and shaded

more of the soil surface. The initial increase in germination success

of P. rivinoides may have resulted from increased light intensity or

quality in the first few months after gap formation, as the leaves and

epiphytes on fallen trees and branches decayed and fell to the ground.

Such an increase in light intensity or quality would be expected to have

the greatest effect on an extremely shade-intolerant species such as P.

rivinoides.





































Figure 2. Germination success vs. gap area. Results from germination
experiments in 6 recent gaps and 1 forest understory site (gap area=0).
Curves shown are de-transformed linear regressions of the proportion of
seeds germinating (arcsin transformed) on In(gap area + 1). Equations,
F-values, and significance levels for P. rivinoides, W. solanacea and W.
coccoloboides are y = 6.99x + 0.54 (F=71.8, p < .001), y = 5.15x + 20.08
(F=10.11, p < .05), and y = 8.36x + 6.35 (F=40.35, p < .002),
respectively.









60-
Phytolacca rivinoides


40- *
40


20-




z
0 80-
r- Witheringia solanacea

Z 60-


S40-


Z 20

w


80- Witheringia coccolobo


60-


40-
40

20



0 100 200 3
GAP AREA (m2)


ides


00







































Figure 3. Germination success vs. gap age. Results from germination
experiments in 4 gaps as they aged naturally (see text). Missing data
for W. solanacea at 3.5 months and for W. coccoloboides at 1.5 and 3.5
months are due to a lack of sufficient seeds for those experiments.
Different symbols indicate values for each of the 4 gaps. Lines connect
mean germination success values at each gap age.












Phytolacca rivinoides


Witheringia solanacea


*


Witheringia coccoloboides




3-


100


100

80

60

40

20


0 2 4 6 8 10 12
GAP AGE (months)


100-

80- *











Following the initial increase in P. rivinoides, germination

success decreased with increasing gap age much more rapidly than in

either species of Witheringia. In fact, germination success in P.

rivinoides was negligible by 7 months after gap formation, whereas some

W. coccoloboides seeds germinated in gaps as old as 12 months.

Germination success decreased least rapidly with increasing gap age in

W. solanacea, although it reached zero by 10 months (Fig. 3). Thus, a

given gap remains open for colonization by W. coccoloboides and W.

solanacea for some time after it is no longer suitable for P.

rivinoides.

Seed dormancy. In all three plant species, seeds buried for up to

27 months showed no significant decrease in viability (Figure 4). Mean

germination success for all seeds was similar in all three species;

values for P. rivinoides, W. solanacea, and W. coccoloboides were 65%,

50%, and 55%, respectively. In a similar experiment (K.G. Murray,

unpubl. data), I collected 100-200 seeds of each species at

approximately two-month intervals for the same 27-month period and

buried these seeds together in a similar forested site. These seeds

were recovered in March 1984 and planted in the greenhouse. The results

of this experiment were similar to those obtained in the previously

described one: no decrease in seed viability was demonstrated in the

first 27 months of burial.




Spatial Distribution of "Safe Sites"

New canopy gaps covered approximately 1.5% of the total land area

sampled by forest transects each year. Percentages of the five forest

transects under new canopy gaps (less than 1 year old) were 0.2, 3.1,









































Figure 4. Results of seed dormancy experiments with P. rivinoides, W.
solanacea, and W. coccoloboides, and results of regression analyses on
germination success vs. seed burial period.













90-





60-





30 -





0-


I I I







Witheringia solanacea
0 y-0.92x+55.8 (.05

0- --


Witheringia coccoloboides
(.5

*


25 30


* 0


60 IL


Phytolacca rivinoides
(.25< p<.5)


90-


30-





0-


90-


60-





30





0-


*


-* .. *


. I 1 I r 1 ' I '1 1
5 10 15 20

TIME BURIED (months)


I











3.1, 1.5, and 0.5, respectively, for the 1983 census, and 0.7, 2.1, 1.3,

1.3, and 1.1 for the 1984 census. Most gaps were formed during severe

windstorms, which occur primarily from November through January at

Monteverde.

The size distribution of canopy openings associated with the 90

"expanded" (sensu Runkle 1982) gaps sampled is shown in Figure 5. It is

typical of such distributions in that very small gaps are exceedingly

common, whereas very large gaps are exceedingly rare. Most gaps smaller

than 10 m2 were formed by one or more branches falling from the canopy,
2
although entire trees occasionally formed gaps as small as 5 m2

The gap size distribution shown in Figure 5 slightly overrepresents

large gaps, since the probability that a gap will be sampled by a line

transect is directly proportional to its size. To construct an unbiased

gap-size distribution, I weighted the number of gaps in each size class

by first dividing that number by the diameter of a circular gap equal in

area to the median-sized gap in that class. I then determined the

proportion of all weighted values occurring in each size class. The

resulting adjusted gap-size distribution is very similar to the

unweighted one in Figure 5, and is not shown here. However, all

estimates of the density of gaps in each size class, and the proportion

of land area they occupy (see below), are based upon the unbiased gap-

size distribution.

Assuming that the canopy disturbance rate of 1.5% per year and the

adjusted gap-size distribution are representative for the Monteverde

cloud forest over the long term, I determined the density of gaps of

various sizes over the landscape and the amount of land area they

occupy. I first divided the range of observed gap sizes into the







38








0
-0



a)
04
o o
0 0


0 0





Co 0


N
CC,
00 0)
o u

o o
00





000 0 -




S3 0
0 Q 00



O < -









SdVE)D dO 83aeNfN
000-00- "O** ** **











following 16 size categories: < 4.9, 5-9.9, 10-14.9, 15-19.9, 20-24.9,

25-29.9, 30-39.9, 40-49.9, 50-59.9, 60-79.9, 80-99.9, 100-149.9, 150-

199.9, 200-299.9, 300-399.9, and > 400 m To determine the density and

coverage (proportion of land area) of gaps in each category that are

formed each year, I used a modification of the methods of Lucas and

Seber (1977) for line transect data. Because the gaps censused in this

study were actually formed over a period of several years, I weighted

the coverage estimates such that the total area in gaps (over all size

categories) equals 1.5% of total land area. Density estimates were

weighted in a similar manner, so that all final values are expressed on

a per-year basis.

I used this analysis to approximate the availability of suitable

germination sites over the landscape. For purposes of illustration, let

us arbitrarily define a "safe site" with respect to gap size as any gap

in which germination success is at least 25%. My use of the term "safe

site" here is not exactly equivalent to that of Harper (1977), since one

gap could provide many germination sites, and each of these would be

termed a "safe site" by Harper's definition. Figure 6 shows the density

of safe sites and the proportion of land area they occupy as a function

of minimum safe site area, using the gap density and coverage estimates

derived above. Both density and land area covered decrease rapidly with

increasing minimum safe site area. For a plant that requires a gap of

at least 100 m2 (e.g., a circular gap of 11.3 m diameter) as a safe

site, for example, there is approximately 1.0 safe site per hectare, and

0.62% of the total land area is available for colonization. For a plant

whose seeds can germinate in a much smaller gap, however, say 10 m

(e.g., a circular gap of 3.6 m diameter), suitable patches for







40


colonization are much more common: 6.0 "safe sites" per hectare,

representing 1.32% of the total land area.

Similar analyses demonstrate that suitable germination sites are

indeed distributed differently for the species in this study. Minimum

gap sizes in which germination success is at least 25% (based on the

regression lines in Figure 1) are 66.7, 5.9, and 15.9 m2 for P.

rivinoides, W. solanacea, and W. coccoloboides, respectively. Thus,

from Fig. 6, we can estimate approximately 1.6, 8.8, and 4.3 suitable

patches per hectare, representing 0.8, 1.4, 1.2% of the total land area.

The foregoing discussion treated the availability of suitable

patches only on the basis of gap size and its effect on germination

success; i.e., it assumes that all gaps formed in a particular year are

equally suitable for colonization at any time. Since germination

success varies among the species with respect to gap age as well as to

gap size, however, the availability of suitable colonization sites

varies among species temporally as well as spatially. If we again

arbitrarily define the length of time a gap remains open for

colonization as the length of time during which germination success

remains at least 25%, then for P. rivinoides, W. solanacea, and W.

coccoloboides gaps remain open for colonization for approximately 4.5,

8.0, and 5.5 months, respectively. Figure 7 shows the density of safe

sites and the proportion of land area they contain as a function of time

of year, for plants that can colonize gaps up to 4, 6, and 8 months old.

The figure was generated by multiplying both the canopy disturbance rate

of 1.5% / year or the overall gap density of 17.5 gaps / hectare / year

by the estimated proportion of gaps occurring in each month. The result

(the line labelled "0 months") is the density of gaps formed that month,











or the proportion of land area they occupy. Other lines in the figure

were generated by including, for each month, the density of new gaps or

the proportion of land area disturbed in the 4, 6, or 8 previous months.

For species capable of invading only very young gaps, suitable

colonization sites are available for only a short period of time each

year (Fig. 7). For species capable of colonizing older gaps, however,

the availability of suitable colonization sites remains high for a much

longer period of time. For example, suitable colonization sites for W.

solanacea are relatively common for 9 months of the year, while those

for P. rivinoides are common for only 5 months.

Although these analyses are useful for gaining a qualitative

impression of the relationship between germination requirements and the

availability of suitable habitat patches over the landscape, data

presented in Figures 6 and 7 clearly show that applying the concept of

"safe site" to treefall gaps oversimplifies the relationship between

germination requirements and availability of suitable patches over the

landscape. The effects of gap size and age on germination are not

threshold effects, in which germination success in gaps below a certain

size or above a certain age is zero and that in younger or larger gaps

is 100%. Instead, germination success is a continuous function of both

gap size and age, and each gap size has an associated germination

probability for each plant species.



Seed Shadows Produced by Birds

Seed Passage Rates

Most birds fed on fruits placed in the experimental cage soon after

the fruits were introduced. In most cases, birds ate 4-10 fruits























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(depending upon fruit and bird species) and then perched for

approximately 10-15 minutes. During this time, birds generally closed

their eyes, puffed out their feathers, and remained nearly motionless.

Similar behavior was often observed in actively foraging birds in the

field: after taking a number of fruits from a plant (and presumably

filling the gut), birds often flew to a perch in a neighboring tree or

shrub and remained there for 10 or more minutes. This period of

inactivity almost always continued until the first defecation of

material from the previous foraging bout. Birds became progressively

more active after each successive defecation, as fruits were processed

through the gut.

Data on gut passage times for seeds of P. rivinoides, W. solanacea,

and W. coccoloboides are shown in Figure 8. Although variation in gut

passage time is considerable at all levels (i.e., among seeds of a

particular plant species ingested at the same time, among plant species

in a given bird species, and among bird species), it is useful to ask

whether gut passage rates vary among plant species and bird species in a

systematic way. To determine whether seeds of some plant species are

processed more quickly than others, I compared median passage times for

the three plant species in the three bird species. In all three bird

species for which I have detailed data, median passage times were

longest for seeds of P. rivinoides, intermediate for W. coccoloboides,

and shortest for W. solanacea (Table 5). All else being equal, P.

rivinoides seeds should thus travel farther than those of either species

of Witheringia. The reasons for these consistent differences are as yet

unclear; fruits of all three species are similar in size, have fruit

skins of similar thickness and toughness, and contain seeds that seem to





















Myadestes melanops


. Witheringia solanacea


0 10 26


Witheringia coccoloboides






Phytolacca rivinoides



'.-M r ,


30 40 50 60 70 80 90


MINUTES AFTER INGESTION





Figure 8. Seed passage rates for the three plant species in Myadestes
melanops, Phainoptila melanoxantha, and Semnornis frantzii. Arrows
indicate median passage times.


40

20















Phainoptila melanoxantha


Witheringia solanacea


Witheringia coccoloboides


80-

60

40

20

0-

40 -

20

O -

100-

80-

60-

40-

20-

O
0


iI I i
10 20 30 40 50 60 70 80 90
MINUTES AFTER INGESTION


Figure 8 -- continued


Phytolacca rivinoides






























Witheringia solanacea


I I i


40 50 60 70 80 90


MINUTES AFTER INGESTION


Figure 8 -- continued


Semnornis frantzii


40 -


20-


0-


S+


I


I





























Table 5. Summary of differences among median seed retention times, (A)
among bird species within plant species, and (B) among plant
species within bird species. Based on multisample median tests
(Zar 1984:179-180) and subdivisions of the multisample
contingency tables (Zar 1984: 69-70).


plant species comparisons

Phytolacca rivinoides Sf > Mm = Pm
Witheringia solanacea Sf = Mm > Pm
Witheringia coccoloboides Sf = Mm > Pm





bird species comparisons
** **
Phainoptila melanoxantha Pr > We > Ws
** **
Myadestes melanops Pr > We > Ws
Semnornis frantzii Pr > Wc > Ws


p < .05
p < .005











be about equally easily extracted from the pulp. In fact, P. rivinoides

fruits are slightly smaller than those of either Witheringia species and

have a more watery, amorphous pulp. It would seem that seeds would be

most easily separated from this pulp, yet retention times were

consistently longer in P. rivinoides than in the two Witheringia

species. Fruits of W. solanacea and W. coccoloboides may contain a

compound with laxative properties, or perhaps P. rivinoides contains a

compound having the opposite effect.

Median passage times vary systematically among bird species as

well. For seeds of all three plant species, passage times are longer in

Semnornis than in Phainoptila (Table 5). Median passage times in

Myadestes were generally intermediate between those in Semnornis and

Phainoptila, but were statistically indistinguishable from those of one

or the other bird species for seeds of each plant.

Several features of the seed retention distributions in Figure 8

are important to the relationship between gut passage times and the

spatial patterns of seeds produced by an actively foraging bird. First,

seeds ingested at one point in time do not emerge from the gut together;

in these experiments, the last seeds emerged more than 75 minutes after

the first-emerging seeds ingested at the same time. Second, the

distributions of retention times are not symmetrical, but instead are

skewed to the right. As a result, neither the length of time for the

appearance of the first-voided seeds, pulp, or marker stain (e.g.,

Herrera 1984, Holthuijzen and Adkisson 1984, Sorensen 1984) nor the

mean seed retention time (e.g., Walsberg 1975) is likely to provide

complete information for inferring seed dispersal patterns. Third,

although retention times are variable in all cases, the variation is










greater in some bird species than in others. For example, coefficients

of variation for P. rivinoides passage times in Myadestes, Semnornis,

and Phainoptila were 44.5, 35.9, and 9.2, respectively. Clearly, any

inferences about the seed shadows produced by animals must be based on a

consideration of the entire frequency distribution of retention times,

rather than on a descriptive statistic (e.g., mean, median, mode, etc.)

derived from it.




Movement Patterns of Frugivorous Birds

A total of 195.7 hours of data on movement patterns was collected

from 8 birds of three species. Totals for Myadestes melanops,

Phainoptila melanoxantha, and Semnornis frantzii, respectively, were 4

individuals for 96.2 total hours, 3 individuals for 90.3 hours, and 1

individual for 9.3 hours. I also attached transmitters to eight other

individual Myadestes, one Phainoptila, and one Semnornis, but I was

unable to collect enough data on these birds to include here.

Transmitters fell off two of these birds less than one day after the

birds' release. In five other cases, the tagged individual moved out of

the area before I could begin tracking it. These five individuals were

non-territorial birds that foraged over very large areas of the forest.

The few hours of data collected from two of these birds indicate that

they did not move more rapidly through the forest than those on well-

defined home ranges; rather, their movements were simply more linear

than those of other individuals of the same species, which turned more

often. Seeds dispersed by a particular widely foraging bird are thus

unlikely to travel much farther from their source than those dispersed

by birds with more restricted home ranges.











Birds fitted with transmitters generally showed no adverse effects

of carrying the 3.5 g package. Within 2 hours of release, most

individuals had begun foraging actively and chasing territory intruders.

Data from two individuals that did not adjust quickly to carrying the

transmitter were not used in the analysis.

Foraging behavior of the primarily frugivorous Myadestes,

Phainoptila, and Semnornis resulted in very different movement patterns

than those of primarily insectivorous birds. Whereas most insectivores

seem to move through the forest almost continuously while feeding, the

frugivores studied here punctuated brief episodes of rapid movement with

relatively long stationary periods. Radio tracking data indicate that

birds generally spent 7 to 12 minutes in one location (Table 6),

presumably consuming and processing fruits, and then moved rapidly to

another location without feeding along the way. Not surprisingly, this

pattern corresponds well with the patchy distribution of fruiting

plants. In addition, the mean times between successive movements in

Table 6 correspond closely with behavior I noted during feeding

experiments with captive birds: after eating a number of fruits, most

birds perched nearly motionless for approximately 10 minutes before

moving about the cage in search of more fruit. The fact that data from

remotely monitored birds correspond well with the behavior of closely

observed individuals again suggests that the transmitters did not

interfere with normal foraging activity.

Movement patterns of radio-tracked birds did not suggest any

tendency for gap-to-gap movement. Rather, birds seemed to travel

rapidly between well-defined fruit sources, regardless of where they

occurred. Locations to which birds returned frequently were always











found to be large fruiting plants such as trees, rather than gaps.

Furthermore, data from mist-net captures and analysis of fecal specimens

suggest no tendency for preferential foraging in gaps. First, none of

the frugivore species was captured more frequently in gaps than in

forest (Table 1). Indeed, one species (Myadestes melanops) was captured

significantly more often in forest (X2 = 12.942, p < .001; expected

values corrected for differences in sampling effort). Second, over 82%

of the fecal specimens from mist-netted Myadestes, Phainoptila, and

Semnornis contained seeds of canopy or subcanopy trees and epiphytes,

suggesting that these birds concentrate much of their foraging outside

gaps. Thus, although these three bird species are the primary

dispersers of the gap-dependent P. rivinoides, W. solanacea, and W.

coccoloboides, there is no reason to suspect that they commonly

transport seeds of any of these plants directly to other gaps in a non-

random fashion.

Mean distances and time intervals between successive bird movements

varied more among individuals of a given species than among species

(Table 6). This variation may reflect different densities of fruit

sources within different birds' feeding ranges or between different

seasons. Without collecting data from numerous individuals of each

species throughout the year, it is impossible to identify sources of

variation in movement patterns more precisely. Because variation among

individuals within species was so high, data from each individual were

weighted equally for purposes of estimating seed shadows. Individuals

from which I was able to collect more extensive data are thus not

overrepresented in the analysis.



















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Table 6 -- continued

C. Movement distances


source df SS MS F
among species 1 7080 7080 0.029 (ns)
within species 5 1236278 247256 60.101 (p < .001)
error 991 4076727 4114

total 997 5320085 5336











Estimation of Seed Shadows

I estimated seed dispersal distances from data on bird movement

patterns and seed passage times as follows. Each time a bird moved to a

new location, I recorded the time and that location on a map of the

study area. These data allow relatively precise measurement of the

distances between all mapped locations and the time spent at each. By

knowing the bird's distance from each location during each subsequent

minute, and by combining these data from many such "initial" locations,

I constructed a probability matrix of distance versus time. Thus, I

computed the probability that a given bird will be at a distance of d

meters from an initial location at time t. Multiplying this matrix by

the probability distributions of seed passage times resulted in

probability distributions of seed movement distances for all three plant

species. This method assumes that an individual's behavior after

leaving each initial location is not different from that after leaving a

fruiting P. rivinoides, W. solanacea, or W. coccoloboides. Data from

initial locations at which the bird spent more than 30 min were not used

in the analysis, because they indicate non-foraging periods or long

visits to plants with very large fruit crops, such as trees. The

appendix demonstrates the use of this method to estimate seed shadows.

The estimated seed shadows produced by the three bird species are

shown in Figure 9. Those for Myadestes melanops and Phainoptila

melanoxantha are very similar: only 20-36% of seeds are deposited within

30 m of the parent plant, and some seeds may be moved up to 370 m by

Myadestes and 510 m by Phainoptila. Estimated seed shadows for

Semnornis frantzii are similar to those of the other two species in that

the probability of seed deposition within 30 m of the parent is low (12-







































Figure 9. Estimated seed shadows produced by Myadestes, Phainoptila,
and Semnornis around individuals of Witheringia solanacea (W.s.), W.
coccoloboides (W.c.), and Phytolacca rivinoides (P.r.). Dots indicate
probability of deposition less than 0.005.












Myadestes melanops


W.s.


.2 -




.2-


""fim ~fL .. p


. C.


. r.


2- Phainoptila melanoxantha
W.s.


Y.c.


P.r.


Semnornis frantzii


W.s.


W.c.


P.r.


500


FROM ORIGIN


.2-




.2-


0 100 200 300 400


T


I I T I


.... -


. . . i . . ; . .. m I m


-C


DISTANCE


(meters)










25%), but the estimated maximum dispersal distance is only 220 m. This

estimate is based on movement data from only one individual, however,

and with a larger sample size the estimated extreme dispersal distances

might approach those of the other two species more closely.




Mediation of Plant Reproductive Success by Birds

A Model of Plant Reproductive Success

Because germination success is a continuous function of both gap

size and gap age, suitable colonization sites are not discrete,

recognizable units, even for the gap dependent-plants studied here. As

a result, evaluating the effect of different seed shadows, temporal

fruiting patterns, and seed dormancy characteristics on plant

reproductive success is complex. For example, we cannot simply

determine the probability with which seeds fall into gaps of a

particular size or age, and assume that they will have encountered safe

sites. In order to compare the reproductive consequences of different

seed shadows, phenological patterns, and dormancy capabilities then, I

designed a computer simulation model that estimates the potential

maximum lifetime reproductive success of individual plants. Parameters

of the model include the phenology of fruiting and gap formation, the

seed shadows produced by animals, the relationships of germination

success to gap size and age, and the density of, and area occupied by,

gaps in various size categories.

Based on either an empirically derived or hypothetical seed shadow,

the model first computes the density of seeds in each of a series of

concentric distance intervals away from the parent plant. Densities are

incremented monthly according to the observed fruiting phenology and










seed dormancy capabilities of each species. Using data on observed

gap-size distributions and rates of canopy disturbance, the model then

determines for each distance interval the amount of land area occupied

by gaps in each of 16 gap size categories. Gaps are "formed" according

to the estimated phenology at Monteverde. The number of seeds

potentially germinating in each distance interval equals the density of

seeds in that interval (at that time) times the area in gaps that size,

summed over all 16 gap size categories. Within this operation, a

similar one based upon the relationship between gap age and germination

success takes place. Because a relatively small number of seeds can

survive to reproduce in any one gap, another function limits the total

number of offspring in gaps of various sizes to the maximum number

observed in gaps of that size in the field. For P. rivinoides, this

number varied from zero in gaps smaller than 10 m2 to four in the

largest gaps. For both W. solanacea and W. coccoloboides, the maximum

number varied from one to five.

The model can be stated mathematically as




nm 51 16 12

RO T ( SNi,m GS PS GAkm PAk)

m=1 i= j=1 k=l




or (GNi,j MXj GF m) whichever is smaller, (1)




where RO is potential lifetime reproductive output, SNi,m is the number

of seeds in distance interval i during month m, GS is the proportion of

land area in gaps of size category j, PSj is the probability of


I










germination in gaps of size category j, GAk,m is the proportion of gaps

of age k (in months) during month m, PAk is the probability of

germination in gaps of age k, GNij is the number of gaps of size

category j in distance interval i, MXj is the maximum number of seeds

that can survive to maturity in gaps of size category j, and GFm is the

proportion of gaps (out of those formed in one year) occurring during

month m. Here I distinguish "reproductive output", which I define as

the total number of offspring produced during an individual's lifetime,

from relative fitness, which depends upon the age-specific schedule of

reproduction (see below). Note that the model estimates potential

lifetime reproductive output only; although it limits the number of

germinated seeds that survive in any one gap (simulating competition

with siblings), it does not include any other sources of mortality,

e.g., predators, pathogens, or accidents such as treefalls. RO as used

here is thus not exactly equivalent to the net reproductive rate, Ro.

Although a Monte Carlo simulation using a stochastic model might yield

more realistic results, the deterministic model is more suitable for the

present purpose, due to its relative simplicity and to the fact that

with a large number of runs, results from a stochastic model should

converge on those from the deterministic one.




Dispersal Effects on Reproductive Output (RO), Assuming No Seed Dormancy

To evaluate the reproductive consequences of dispersal by

Myadestes, Phainoptila, and Semnornis, I first ran the model described

above four times for each plant species; once with each of the seed

shadows in Figure 9, ana a fourth time using a seed shadow in which all

seeds are deposited within 10 m of the parent plant. This last run thus










approximates the case of no dispersal, or the fate of most seeds removed

by tanagers and finches. Other parameters of the model were the same

for each run on a particular species, and were taken from data collected

at Monteverde. The relationships between germination success and gap

size are the adjusted regressions given previously. Relationships

between gap age and germination success were interpolated from the lines

connecting observed mean values in Figure 2. The availability of gaps

of different sizes was estimated directly from data on the canopy

disturbance rate and adjusted gap size distribution. Fruiting and gap

formation phenologies were those shown in Figures 10 and 11. Yearly

seed crops, estimated by multiplying the mean number of seeds per fruit

by the median yearly fruit crop sizes for each species, were 8,345,

13,061, and 44,180 for W. solanacea, W. coccoloboides, and P.

rivinoides, respectively. Because both Witheringia species produce two

fruit crops per year, crop sizes used here were yearly medians, rather

than the seasonal medians reported above. The number of reproductive

seasons was assumed to be that estimated for plants at Monteverde: one

in P. rivinoides, and five in W. solanacea and W. coccoloboides.

Estimates of total lifetime reproductive output (assuming no seed

dormancy) using the four seed shadows are shown in Figure 12. For each

plant species, the advantage of dispersal by any of the three legitimate

dispersers is obvious. Within 10 m of the parent plant, very few

suitable germination sites are available, and density-dependent

mortality among seedlings within them is high. Seed shadows produced by

Semnornis, Phainoptila, and Myadestes result in much higher estimates of

reproductive output, because seeds are distributed over a greater number

of suitable patches. However, these estimates are for seeds that are















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A S O N O J


M A M J J


MONTH











Figure 11. Estimated phenology of gap formation at Monteverde. Values
given are the proportions of all gaps formed in a particular year that
occur each month.


0.3



0.2



0.1


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dispersed to sites currently suitable for germination, and thus

germinate in the same month they are dispersed. These estimates do not

include later reproduction from dormant seeds that germinate after a new

canopy gap occurs overhead. Yet seeds of P. rivinoides, W. solanacea,

and W. coccoloboides exhibit "enforced" seed dormancy (sensu Harper

1977), and are capable of remaining dormant in the soil for at least 2.5

years with no detectable decrease in viability, and probably for much

longer (Fig. 4).




Reproductive Consequences of Seed Dormancy

Effects on reproductive output (RO). Because plant reproductive

success should be enhanced by enforced seed dormancy, I repeated the

four model runs for each species, this time allowing any ungerminated

seeds to remain dormant for maximum periods of 2, 5, 10, 20, and 40

years. Not surprisingly, potential reproductive output increases

dramatically with increased dormancy capabilities of seeds (Fig. 13).

For example, plants whose seeds are capable of remaining dormant for

just two years can potentially produce 11 to 31 times as many offspring

as plants whose seeds die if they are not dispersed directly to sites

immediately suitable for germination. If seeds can remain dormant for

up to 40 years, up to 611 times as many offspring may be produced. Even

more interesting, however, is the fact that the relative differences in

estimated reproductive output using different seed shadows are greatly

magnified when we also consider reproduction from dormant seeds. Thus

for P. rivinoides, dispersal by Myadestes results in only a 4% increase

in RO over dispersal by Semnornis, considering only those seeds

encountering currently suitable sites when dispersed (Fig. 12).







































Figure 13. Estimated lifetime reproductive ouptut (RO) vs. seed
dormancy capability, for plants receiving all dispersal service from
Semnornis (S.f.), Phainoptila (P.m.), Myadestes (M.m.), or having all
seeds deposited within 10 m of the parent (none).














WITHERINGIA SOLANACEA


none


WITHERINGIA COCCOLOBOIDES


none


PHYTOLACCA RIVINOIDES


none

5 10 20

MAXIMUM SEED DORMANCY CAPABILITY (years)










However, if we also consider seeds that can remain dormant in the soil

for up to two years until a gap is formed overhead, dispersal by

Myadestes confers a 54% increase over dispersal by Semnornis (Fig. 13).

Furthermore, if seeds can remain dormant for even longer periods, these

differences become even larger.

Effects on relative fitness. Although Figure 13 clearly shows that

the total number of potential offspring is greatly increased by seed

dormancy, it gives a misleading impression of the influence of seed

dormancy on relative fitness. The estimator of reproductive output

computed by equation 1 is most useful for plants without overlapping

generations or age-structured populations, e.g., monocarpic plants

without seed dormancy. In such plants, RO will be an unbiased estimator

of relative "fitness", and comparisons among treatments (e.g., different

seed shadows) yield unbiased information about the fitness consequences

of the different treatments. If fecundity and/or survival are age

dependent, however, the total number of offspring produced by an

individual is not an unbiased estimator of relative fitness, because

seeds produced later in life, or those that germinate after a long

period of dormancy, contribute less to the population gene pool than

those germinating earlier. Fecundity, at least, is age-dependent in all

three species considered here. Both W. solanacea and W. coccoloboides

typically produce seeds for five or more years. More importantly, all

three species demonstrate the capacity for enforced seed dormancy, which

has the effect of greatly increasing the parent plant's reproductive

lifespan. Therefore, I computed a less biased estimator of relative

fitness by solving for r the equation










YP+YD

1 = e-rxlx x' 2)
= ix. mx (2)
x=0




where lx is the probability of seed survival in the soil for x years,

and mx is the number of seeds germinating in year x. This equation is

commonly used to compute the exact value of the intrinsic rate of

natural increase of a population. Here, r is not the intrinsic rate of

natural increase, but an estimator of relative fitness that discounts

the contribution of offspring produced later in the parent's life

relative to that of those produced earlier. The parent plant germinates

in year 0, and x can take on values from 0 to YP + YD, where YP is the

last year of seed production and YD is the maximum number of years that

seeds can remain dormant. Survival of ungerminated seeds (1x) was

assumed to equal 1.0 for all years up to the maximum dormancy period,

followed by complete mortality. Values of mx were the yearly estimates

of seeds germinating generated by the model, which summed to the value

for RO given in Fig. 13. The age at first reproduction and number of

years of seed production were those estimated for plants at Monteverde.

In P. rivinoides, all seed production occurs in year 1 (plants between 1

and 2 years of age). In the two Witheringia species, seed production

was assumed to begin at age 3 and continue for 5 years.

Estimates of relative fitness based on equation 2 are shown in

Figure 14. The figure shows that seed dormancy indeed greatly enhances

plant fitness, but that most of this enhancement is due to short-term,

rather than long-term dormancy. Dormancy capability of more than two

years does little to increase the value of r. Thus, the increase in







































Figure 14. Estimated relative "fitness" (r; see text) vs. seed dormancy
capability ,for plants receiving all dispersal service from Semnornis
(S.f.), Phainoptila (P.m.), Myadestes (M.m.), or having all seeds
deposited within 10 m of the parent (none).












2- WITHERINGIA SOLANACEA
M.m., P.m.

1 s.f.
1-
none

0,




2- WITHERINGIA COCCOLOBOIDES
M.m., P.m.

S.f.

none

0* .


PHYTOLACCA RIVINOIDES


M.m., P.m.


none


MAXIMUM SEED DORMANCY CAPABILITY (years)











fitness with increasing dormancy capability is not monotonically

increasing and linear, as suggested by Fig. 13, but is in fact

asymptotic.




Reproductive Consequences of Fruiting Phenology

Fruit ripening in all three plant species is concentrated in the

wet season, although some fruits may be found at any time of the year

(Fig. 10). In P. rivinoides, a single well-defined peak occurs early in

the wet season, with 91% of all fruits ripening from April through June.

In both W. solanacea and W. coccoloboides, two distinct ripening peaks

occur in the wet season: one early (May-June), and one late (November-

January). These distinct peaks were not due to individual plants within

each population ripening at different times; nearly all individuals of

each species produced two separate fruit crops each year, although these

were not usually of the same size.

Fruiting in W. solanacea was somewhat less seasonal than in W.

coccoloboides. Although peak ripening periods in both species

coincided, the May-June and November-January peaks accounted for a

greater proportion of the total fruit crop in W. coccoloboides than in

W. solanacea. More importantly, the major ripening peak in W.

coccoloboides was in the early wet season, while that in W. solanacea

was in the late wet season.

Because the major disperser for all three plant species, Myadestes

melanops, is essentially absent from the Monteverde area from late

October through December (Fig. 1), we might expect fruit removal rates

to be depressed during the late wet season fruiting peak. To test the

hypothesis that daily fruit removal rates are correlated with seasonal










patterns of Myadestes abundance, I examined the relationship between

Myadestes capture rate and daily fruit removal rate from May 1982

through April 1983. Daily fruit removal rate was computed as the

proportion of marked ripe fruits on all plants that were removed.

Because daily fruit removal rate is negatively correlated with the size

of the fruit crop (Murray, in press), I computed partial correlations of

removal rate with the monthly Myadestes capture rate, holding crop size

constant.

In all three plant species, a significant partial correlation

existed between Myadestes capture rate and daily fruit removal rate.

Coefficients for P. rivinoides, W. solanacea, and W. coccoloboides were

0.74 (P < .02), 0.66 (P < .05), and 0.69 (P < .05), respectively. Thus,

individual plants that ripen fruits during the season when Myadestes is

absent should have, on average, lower reproductive success than those

ripening fruits at other times.

Because the availability of suitable germination sites varies over

the year (Fig. 7), plant reproductive success may be affected by

seasonal fruiting patterns for reasons other than variation in fruit

removal rate. To estimate the relative importance of this selective

pressure on fruiting phenology, I compared the potential lifetime

reproductive output of individuals that peak ripening in February,

April, June, August, October, and December. For each plant species, I

ran the simulation model described above six times, each time shifting

the fruiting phenology curve temporally with respect to the estimated

phenology of gap formation. For all runs, I used the estimated seed

shadow produced by Myadestes, and allowed ungerminated seeds to remain










dormant for two years. All other model parameters were the same for all

runs on each species, as outlined above.

Somewhat surprisingly, estimates of reproductive output were very

similar for plants that fruit at different times of year (Fig. 15): the

highest estimates for each species are only 1% to 13% higher than the

lowest estimates. Two factors account for this result. First, because

treefall gaps sometimes remain open for germination for up to a year

after formation, the temporal availability of suitable habitat patches

is actually somewhat more constant than the highly seasonal nature of

gap formation would suggest (e.g., Fig. 7). Second, and more

importantly, enforced seed dormancy greatly reduces temporal variation

in the number of seeds available for colonization of newly formed gaps.

Even though fruit ripening is highly seasonal, the effective pool of

seeds from a given parent remains much more constant over time. Had the

estimates in Figure 15 been determined for plants with no seed dormancy

capability, variation in reproductive output of plants that peak

fruiting at different times would have been much greater.







































Figure 15. Estimated lifetime reproductive output (RO) of plants that
peak fruit ripening at different times of year (see text). All
estimates assume a maximum seed dormancy capability of two years, and
all dispersal service from Myadestes melanops.






PHYTOLACCA RIVINOIDES


Hi


H


H


H


WITHERINGIA SOLANACEA


800-

600-

400-

200-



1000-

800

600

400-
200


COCCOLOBOIDES


MONTH OF PEAK


V7


200-


WITHERINGIA
m77


J F M A M J J A S O N D


FRUITING


i i I


I 1


11


I I

















DISCUSSION

Data presented here demonstrate that determining the consequences

of seed dispersal ("dispersal quality", sensu McKey 1975) by different

bird species is exceedingly difficult. Animal dispersers may influence

plant reproductive success in three ways. First, animals may differ in

the likelihood with which they ingest seeds of the fruits they remove

from plants ("fruit handling"). Second, animals may differ in the

chemical or mechanical effects exerted on seeds that are ingested ("seed

treatment in the gut"). Third, animals can affect plant reproductive

success through the seed shadows they produce, via colonization of

patchily distributed microhabitats or escape from high density-dependent

mortality near the parent plant.




Effects of Fruit Handling and Gut Treatment

Avian consumers of P. rivinoides, W. solanacea, and W.

coccoloboides fruits differ in the "quality" of dispersal service they

provide in all three of the above ways. Whereas Myadestes melanops,

Phainoptila melanoxantha, and Semnornis frantzii invariably ingested

fruits of these plants whole and ingested all of the seeds, the two

tanagers (Chlorospingus opthalmicus and Tangara dowii) and the finch

(Pselliophorus tibialis) discarded many or most seeds before swallowing

the fruit pulp. Similar fruit-handling behavior in tanagers and finches

has also been noted by several other investigators (Snow and Snow 1971,

Moermond 1983, Moermond and Denslow 1985, Levey 1986). As with the










species considered here, Levey (1986) also found that the probability of

seed ingestion by tanagers and finches was inversely correlated with

seed size within bird species, and positively correlated with seed size

among bird species. Clearly, such differences in the ways that

different birds handle fruits may result in different reproductive

consequences to plants. In general, tanagers and finches are less

likely to ingest seeds of any size than are birds that swallow fruits

whole. Instead, most seeds will be dropped directly beneath the parent

plant where they may be subject to high density-dependent mortality

(e.g, Wilson and Janzen 1972, Howe and Primack 1975, Janzen et al. 1976,

Platt 1976, Salmonson 1978, Clark and Clark 1981, Lemen 1981, Augspurger

1983a,b, 1984a,b, Howe et al. 1985). In addition, the lack of gut

treatment may retard germination in such seeds (see below). Thus, not

only does fruit size limit the number of potential consumer species for

a given plant (e.g., Diamond 1973, Snow 1973, Moermond and Denslow 1985,

Wheelwright 1985a), seed size may also impose constraints on the quality

of dispersal service rendered by those animals that actually consume

fruits.

Reproductive consequences of fruit removal by different birds may

also vary due to different treatment effects of gut passage. Among the

bird species considered here, all except the finch P. tibialis passed

all ingested seeds intact (Table 2). Furthermore, germination success of

these seeds (Table 3) did not differ from that of seeds carefully

removed from fruits by hand (test for equality of percentages, Sokal and

Rohlf 1969: 608; P>0.3 for all comparisons). In contrast, the one P.

tibialis tested destroyed 98% of the W. solanacea seeds it ingested, and

the remaining 2% that emerged intact were inviable. The implications of










these differences in gut treatment effects for plant reproductive

success are obvious: seeds ingested by P. tibialis are likely to be

destroyed, hence these finches (but not all finches; e.g., see Jenkins

1969, Levey 1986), like most parrots (e.g., Forshaw 1978, Janzen 1981)

and many doves (Snow 1971, Moermond and Denslow 1985), act primarily as

seed predators.

Although gut treatment in some animals may have negative effects on

germination, the opposite is often true. Germination success of many

plant species is enhanced by gut treatment (Krefting and Rowe 1949, Rick

and Bowman 1961, Olson and Blum 1968, Hladik and Hladik 1969, Nobel

1975, McDiarmid et al. 1977, Applegate et al. 1979, Lieberman et al.

1979, Fleming and Heithaus 1981, Glyphis et al. 1981), and is even

absolutely required by some (e.g., Calvaria major; Temple 1977). In

addition, gut passage may affect germination in ways more subtle than

merely altering the proportion of seeds that eventually germinate. Data

on germination rates of seeds with and without gut treatment (Table 3)

indicate that in all cases except one (W. solanacea passed by

Phainoptila), seeds processed through bird guts germinated more rapidly

than those receiving no gut treatment. Similar results were obtained by

Hladik and Hladik (1969) for seeds of some, but not all, plant species

passed by monkeys. This response may be due to mild chemical and

mechanical abrasion of the seed coat, facilitating perception of

germination cues (e.g., light) and/or water imbibition. Whatever the

mechanism, rapidly germinating seeds may enjoy a competitive advantage

over those that take longer, especially among seedlings of rapidly

growing pioneer species. Patches of soil disturbed by uprooting trees

commonly contain more than 100 seedlings of P. rivinoides alone within










one month, yet only one to three of these will survive to maturity (K.

G. Murray, personal observation). In the face of such competition, even

subtle treatment effects on germination rate may have important fitness

consequences. While the data on germination rates shown in Table 3 are

for seeds treated by a single individual of each bird species, and

therefore do not allow statistical comparisons between bird species, the

data suggest that gut treatment by some species (e.g., Semnornis) may

result in more rapid germination than that resulting from treatment by

other species.



Effects of Dispersal

Seed Shadows

Variation among the "seed shadows" produced by different birds can

also produce differences in the quality of dispersal service rendered.

The seed shadow estimates presented in Fig. 9 are, to my knowledge, the

first such estimates for free-ranging birds in a natural habitat.

Although estimates of the "seed rain" produced over the landscape by

frugivorous animals are available from seed trapping studies and

assessments of soil seed banks (e.g., Burtt 1929, Smythe 1970, Guevarra

and Gomez-Pompa 1972, Foster 1973, Smith 1975, Vazquez-Yanes et al.

1975, Brunner et al. 1976, Lieberman et al. 1979, Thompson 1980, Bullock

1978, Janzen 1978), neither the sources of seeds sampled nor the

identity of their dispersers is generally known. Thus, measures of the

seed rain within a forest tell us nothing about the seed shadows

produced by particular disperser species around individual plants. In

contrast, the methods used in this study do allow estimation or

individual plant seed shadows, albeit indirectly. Furthermore, the










techniques are applicable to a wide variety of dispersal agents and

habitats, and yield much additional information on temporal patterns of

foraging, home range size, and digestive physiology of particular

disperser species.

The estimated seed shadows in Figure 9 are remarkable in several

respects. First, they are not, as is sometimes suggested (e.g., Harper

1977, Levin 1979, Fleming and Heithaus 1981), highly leptokurtic, with

the great majority of seeds being deposited within a few meters of the

parent plant. Instead, a large proportion of seeds may be moved for

considerable distances. Median dispersal distances vary from 35 to 60

meters among the 9 bird species/plant species combinations, and maximum

dispersal distances exceed 500 meters. Second, the range of estimated

dispersal distances presented here exceeds that suggested for most other

bird-dispersed plants. Longer dispersal distances have been suggested

for seeds cached by Clark's Nutcrackers (Vander Wall and Balda 1977) and

for some species dispersed by bats (e.g., Janzen et al. 1976, Fleming

1981), however. Dispersal distances of 70 m, 25 m, and "up to several

hundreds of meters" were suggested for seeds of Casearea nitida (Howe

and Primack 1975), Prunus mahaleb (Herrera and Jordano 1981), and Virola

surinamensis (Howe and Vande Kerchove 1981), respectively. These

authors' estimates, however, were based on relatively few visual

observations of birds leaving fruiting trees. Because only short bird

movements could be observed, their data may be biased in favor of short

distances. This bias notwithstanding, it is unlikely that the large (5

to 20 mm) seeds of the trees studied by Howe and Primack (1975), Herrera

and Jordano (1981), and Howe and Vande Kerchove (1981) are dispersed as

far as the much smaller (ca. 1-3 mm) seeds of P. rivinoides, W.










solanacea, and W. coccoloboides. Large seeds are voided more rapidly by

birds (often by regurgitation; Levey 1986, and personal observation),

and the large fruit crops produced by trees encourage more sedentary

behavior by frugivores (Pratt and Stiles, 1983). Thus, small seeds are

probably dispersed farther, on the average, than large ones, especially

when produced by plants with small fruit crops that do not encourage

long or frequently repeated visits by individual frugivores.

Do the data suggest any tendency for non-random or "directed

dispersal" (sensu Howe and Smallwood 1982) of seeds to gaps? Direct

dispersal to gaps has been suggested by the common observations (e.g.,

Blake and Hoppes 1986, D. Levey, personal communication) that (1) herb-

and shrub-layer fruit resources are often more concentrated within gaps

than in surrounding forest understory, and that (2) mist net captures of

frugivorous birds often reflect this concentration. At Monteverde,

however, none of the bird species for which I have adequate data was

captured most frequently in gaps (Table 1). In fact, the major

understory frugivore at Monteverde, Myadestes melanops, was captured

significantly less often in gaps than in forest understory.

Furthermore, data from individual birds fitted with transmitters suggest

no tendency for non-random gap-to-gap movement.

The lack of any preference for gaps in Myadestes, Phainoptila, and

Semnornis reflects the fact that their fruit resources are not highly

concentrated there. Individuals of these species forage from the lowest

levels of the forest understory to subcanopy and even canopy levels (K.

G. Murray, personal observation). In fact, most of the fecal specimens

from captured individuals contained seeds of canopy and subcanopy trees

and epiphytes. Although fruit resources within a few meters of the










ground may be more concentrated in gaps at Monteverde as in other

forests (Blake and Hoppes 1986, D. Levey, personal communication),

fruits used by Myadestes, Phainoptila, and Semnornis are not

concentrated in gaps if the entire vertical foraging ranges of birds are

considered.




Distribution of "Safe Sites"

Although dispersal may result in decreased density-dependent

mortality of seeds and seedlings near the parent plant, the advantage of

dispersal for gap-dependent plants more likely results from two other

factors: (1) an increased probability of encountering spatially and

temporally unpredictable habitat patches (i.e., treefall gaps), and (2)

reduced density-dependent mortality within those patches.

Tropical forests are often characterized as mosaics of mature-phase

and gap-phase patches that differ in size, intensity of disturbance, and

time elapsed since last disturbance (Richards 1952, Richards and

Williamson 1975, Whitmore 1975, 1978, 1982, Oldeman 1978, Hartshorn

1978, 1980, Hladik 1982, Brokaw 1985). The Monteverde cloud forest also

represents such a disturbance mosaic. Approximately 1.5% of the total

land area at Monteverde is subjected to canopy disturbances each year,

and the average density of new gaps (including even those as small as

1.6 m2) over the landscape is approximately 17.5 per hectare per year.

The 1.5% per year canopy disturbance rate reported here is similar to

that reported for "elfin" forest along the continental divide at

Monteverde (1.1%; Lawton and Putz, unpublished ms), as well as for other

tropical forests (Leigh 1975, Hartshorn 1978, Brokaw 1982a, Foster and

Brokaw 1982, Uhl 1982), and many temperate ones (Heinselman 1973, Abrell










and Jackson 1977, Runkle 1982, Zackrisson 1977, Naka 1982, Platt et al.

unpublished ms). Furthermore, the gap size distribution at Monteverde

(Fig. 5) is similar to that determined for several other tropical and

temperate forests (Runkle 1979, Brokaw 1982b, Lawton and Putz,

unpublished ms). For seeds of gap-dependent plants, then, suitable

patches for colonization are similarly rare in most forests.

Detailed analyses of the germination requirements of P. rivinoides,

Witheringia solanacea, and W. coccoloboides show that the landscape is

even more complex than just a mosaic of "safe sites" (sensu Harper 1977)

surrounded by unsuitable habitat. For each gap in the forest, there is

an associated probability of germination for seeds of gap-dependent

plants, which depends upon its size and age (e.g., Figs. 2 and 3).

Furthermore, the suitability of a given gap differs among the three

species studied here, and probably for other species as well. For

plants such as these, it is more useful to think of the forest not as

discrete patches of suitable habitat embedded in a matrix of hostile

environment, but rather as a mosaic of patches of different sizes and

ages, each of which has an associated suitability for seeds of

particular gap-dependent plants. At any point in time, the great

majority of land area (>98.5% for these three species) consists of

patches in which the probability of germination and establishment is

negligible, and the remainder of the land area is occupied by patches of

varying, but higher suitability.




Reproductive Consequences of Dispersal and Dormancy

Because the germination requirements of gap-dependent plants are

complex, determining the reproductive consequences of seed shadows











produced by birds is exceedingly difficult. Results presented here

clearly demonstrate that seed dispersal increases both reproductive

output and relative "fitness" of gap-dependent plants. However, the

underlying cause of these increases has less to do with the number of

seeds encountering suitable gaps than with the number of individual gaps

they encounter. Assuming that gaps are formed randomly in space, any

location has an equal probability of being within a gap. Consequently,

the probability that a given seed will encounter a gap does not depend

upon the distance it is dispersed. A major advantage of dispersal for

gap-dependent plants is that it serves to spread seeds over a greater

number of gaps, so that each germinating seed is faced with fewer

potential competitors (i.e., siblings). Thus, even though seeds of

these plants can germinate only in ephemeral habitat patches that occur

unpredictably in space, one of the primary advantages of seed dispersal

lies in avoiding density-dependent mortality within patches near the

parent plant. This does not mean that avoidance of density-dependent

mortality is the only advantage of dispersal in these plants, however.

On average, widely dispersed seeds will encounter suitable germination

sites after shorter periods of dormancy, and thus contribute more to the

population gene pool, than those deposited closer to the parent plant.

As a result, more extensive dispersal increases relative "fitness" (but

not reproductive output) for reasons unrelated to density-dependent

mortality. Results presented for these gap-dependent plants therefore

support both the "escape" and "colonization" hypotheses proposed by Howe

and Estabrook (1977).

The ability of seeds to remain dormant in the soil for long periods

does not preclude the necessity for effective seed dispersal. Because










undispersed dormant seeds could survive until the next canopy

disturbance occurs on a particular site, it might be argued that

dispersal is unimportant if seeds remain viable sufficiently long, and

if mortality in the soil is low. Nevertheless, more effective dispersal

mechanisms will always be favored; plants that disperse seeds always

have higher reproductive success than those without dispersal,

regardless of dormancy capability (Figs. 13 and 14).

Three factors account for this result. First, because the

probability of germination in the gap of origin is negligible by the

time a parent plant produces seeds (Fig. 3), the next germination

opportunity for seeds deposited there will occur when the next

disturbance occurs on that site. The 1.5% per year canopy disturbance

rate at Monteverde suggests a "turnover rate" (i.e., the "mean time

between successive creations of gap area at any one point in the

forest"; Brokaw 1985) of 67 years. Thus, undispersed seeds of a gap-

dependent plant should encounter new treefall gaps only once every 67

years, on the average. By dispersing its seeds, a plant greatly

increases the number of suitable patches encountered by its seeds at any

point in time (cf. Green 1983, Geritz et al. 1984). Second, because

seeds germinating after a long period of dormancy contribute less to the

population gene pool than those that germinate soon after dispersal,

plant "fitness" is always increased by mechanisms (e.g., dispersal) that

promote earlier encounter of suitable patches. Third, intense density-

dependent mortality (due to intraspecific competition and/or predation)

among seeds deposited very near the parent should always favor more

effective dispersal, regardless of when seeds germinate. Thus, although

enforced seed dormancy greatly increases reproductive success of gap-










dependent plants, it can in no way be thought of as a "substitute" for

effective dispersal.

Although none of the birds considered here is likely to transport

seeds directly to gaps, the quality of dispersal service provided by

different bird species to gap-dependent plants may vary considerably, as

a function of the seed shadows they produce. The degree to which

different seed shadows are selectively advantageous depends upon how we

estimate relative plant fitness. On the one hand, the model described

by equation 1 predicts that the number of seeds potentially germinating

during the month dispersed (RO, assuming no seed dormancy) is quite

similar following dispersal by Semnornis, Phainoptila, or Myadestes

(Fig. 12). When reproduction from dormant seeds is also considered,

however, differences between effects of dispersal by different birds on

lifetime reproductive output are greatly accentuated (e.g., Figure 13).

In fact, Fig. 13 shows that the number of offspring produced is a

monotonically increasing linear function of dormancy, at least over most

of the range of dormancy capability. This result suggests that (1) a

given increment in the capacity for seed dormancy always has the same

selective advantage, and (2) differences in the selective advantages of

different seed shadows are greatly magnified by increasing seed dormancy

capability. If seeds can remain dormant for just two years, for

example, the increment to lifetime reproductive output resulting from

dispersal by Semnornis is only 65-85% as great as that resulting from

dispersal by Myadestes or Phainoptila, and these differences are further

accentuated if seeds can remain dormant for even longer periods of time.

Thus, even small increases in mean or extreme dispersal distances might










result in substantial differences in lifetime reproductive success for

plants that exhibit enforced seed dormancy.

In contrast, if we use r (equation 2) as an estimator of fitness,

the effect of dormancy is less pronounced. Because seeds germinating

after a long period of dormancy contribute less to plant fitness than

those germinating sooner, r is greatly increased by the ability of seeds

to remain dormant for a few years, but is increased only slightly by

further increases in dormancy capability (Fig. 14). This result

suggests that (1) seed dormancy beyond a few years may have no selective

value, (2) differences among the fitness increments associated with

different seed shadows are not as great as is suggested by comparison of

the total numbers of offspring produced, and (3) these differences do

not increase appreciably with increasing dormancy capability.

As used here, however, equation 2 also has important sources of

bias. For example, the value of r is especially sensitive to the

magnitudes of values for 1x and mx. When values of mx are large,

estimates of r reach an asymptote quickly as x increases. When values

of mx are lower, but still retain the same proportional relationships to

one another, values for r do not reach an asymptote until much higher

values of x. This property of equation 2 is very important for its use

as a fitness estimator here. Because the simulation model used to

generate mx values does not consider most sources of pre- or post-

germination mortality, the mx values estimated are artificially high.

If we choose more realistic values for mx while retaining the same

proportional relationships between them (e.g., by multiplying each value

by 0.001), r increases appreciably over much more of the range of values

of x. In addition, differences among the increments in r associated











with different seed shadows are larger, and become even larger as

dormancy capability increases.

Because solutions for r in equation 2 are highly sensitive to the

magnitude of values of mx, and because I lack information on exact

values, Figure 14 conservatively estimates the influence of both seed

dormancy and different seed shadows on plant fitness. On the other

hand, estimates of lifetime reproductive output derived from equation 1

(Fig. 13) present an inflated estimate of the influence of these factors

on plant fitness. Thus, neither approach yields an unbiased estimator

of fitness, and the real effects of dispersal and dormancy on plant

fitness lie somewhere between the extremes presented here. Thus, (1)

seed dormancy does increase plant fitness (to an unknown degree) over a

wide range of dormancy capabilities, but especially over the short term.

(2) Because seeds germinating soon after dispersal contribute more to

plant fitness than those germinating later, dispersal by bird species

whose seed shadows result in a greater probability of deposition in

currently (or imminently) suitable sites confers a large fitness

advantage on the parent. (3) Increasing dormancy capability magnifies

(also to an unknown degree) differences between the fitness increments

associated with different seed shadows, such that relatively minor

differences between seed shadows may result in important differences in

the increments to plant fitness associated with each.



Limitations of the Model

Results of the model runs for reproductive success presented in

Figs. 12-15 should be interpreted with some caution. All values of

reproductive success computed by the model are maximum possible values,










for several reasons. First, my measures of the proportion of land area

in gaps of different sizes probably overestimate the proportion of land

area actually available for colonization. I measured germination

success with respect to gap size at the approximate center of each gap,

above any herb-layer vegetation that might obstruct sunlight. All other

locations within gaps are subject to a greater degree of shading, both

from trees bordering the gap and from existing vegetation within it. In

addition, I conducted my experiments on exposed mineral soil, without an

intact humus and leaf litter layer that may inhibit germination and

seedling establishment of some plants (Putz 1983). Most of the soil

surface in treefall gaps is covered by an intact litter layer; exposed

mineral soil generally occurs only on the "mound" and "pit" created by

uprooted trees. Second, the model assumes no mortality of dormant seeds

other than that set by physiological limits on the maximum amount of

time seeds can remain dormant but viable. In reality, many dormant

seeds may be removed from the soil by predators and pathogens. Third,

the model assumes that all dormant seeds are equally likely to germinate

in response to a given canopy disturbance. However, seeds present in

the soil for longer periods may be moved into successively lower soil

horizons (by the actions of soil organisms such as earthworms), so that

individual seeds become less and less likely to germinate in response to

a given disturbance with increasing time in the seed bank. Fourth, the

model assumes homogeneous dispersion of seeds within each distance

interval, which minimizes seedling mortality due to interspecific

competition. Actual seed shadows produced by birds are undoubtedly more

heterogeneous, and mortality among seedlings in clumps should result in

lower reproductive success than indicated by the model presented here.











Undoubtedly, most of the model's assumptions are often violated in

nature, so that actual reproductive output and relative fitness are much

lower than the estimates presented here. Nevertheless, the estimates

are useful for comparing the consequences of different seed shadows,

germination requirements, seed dormancy capabilities, and fruiting

phenologies for potential reproductive success of individual plants.




Seasonal Constraints on Reproductive Success

In the sections above, I have discussed how plant reproductive

success is influenced by interacting characteristics of the dispersal

service rendered by birds, the landscape-level disturbance regime, and

the physiological and life historical attributes of the plants

themselves. Another plant characteristic that may influence

reproductive success is the timing of seed dispersal in relation to

seasonal patterns of patch formation and disperser abundance. Results

presented in Fig. 15 suggest that even short-term seed dormancy

effectively uncouples dispersal and germination; estimated reproductive

output varies only slightly among plants that ripen fruits at widely

different times of year. Thus, plant reproductive success should not

suffer appreciably if fruit ripening does not coincide closely with peak

periods of gap formation, even though gap formation is highly seasonal,

and although gaps remain open for colonization for only short periods of

time.

On the other hand, fruit removal rates, hence possibly plant

reproductive success, do vary seasonally as a positive function of the

abundance of Myadestes melanops, the primary dispersal agent. That many

species of tropical frugivores undertake seasonal migrations is well




Full Text

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AVIAN SEED DISPERSAL OF NEOTROPICAL GAP-DEPENDENT PLANTS By KELVIN GREGORY MURRAY A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UN I VERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 1986

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ACKNOWLEDGMENTS I am greatly indebted to many individuals for support and assistance in completing this project Kathy Winnett-Murray was intimately involved in every phase of the project providing assistance in th e field work as we ll as valuable adv ice on planning, data analysis and writing That she was able to do all that, complete her own dissertat i on wo rk and still be a wonderful wife in the face of both our frustrations over the difficulties of field research, is truly amazing. Peter F einsinger likewise provided adv i ce, assistance and humane editorial criticism from the earl iest planning stages of the work Without several of his well-timed pep -t alks, the study would surely ha ve suffered greatly and might never have been completed at all. I cannot overestimate his positive influence on this work or on my graduate career in general For this and for his friendship I will always be grateful I benefitted greatly from discussions with the other members of my supervisory committee H Jane Brockmann, Thomas Emmel, Walter Judd, and Francis Putz, who also pr ov ided valuable editorial advice on earlier drafts of the d iss ertation Discussi o ns with Nicholas Brokaw Carmine Lanciani, Robert Lawton, Douglas Lev ey Timothy O'Brien, Carlos Martinez del Rio and Harry Tiebout III were also very helpful My collegues at the University of Florida and especially the other biologists who resided concurrently at Monteverde, were also invaluable. Willow Zuchowski-Pounds, Bill Busby, Rita Schuster and Sarah Sargent ii

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provided assistance with field work Jennifer Shopland kindly shared mist-netting and feeding observation data on frugivores. Advice on field techniques and data analysis were provided by these indi v iduals as well as by Jim Beach Martha Crump, Eric Dinerstein Sharon Kinsman, Yan Linhart, David McDonald, Alan Pounds Francis Putz, and Nat Wheelwright. I am especially grateful to all of these Monteverde biologists, and to members of the Monteverde community in general for making my 27 month tenure there one of the most enjoyable periods of my life. Wolf Guindon, Gary Hartshorn Joseph Tosi, Jr Manuel Ramirez, and Giovanni Bello kindly facilitated my use of the Monteverde Cloud Forest Reserve. Logistical support in Costa Rica was provived by personnel of the Organization for Tropical Studies, especially Roxanna Diaz. Financial assistance was provided by the Jessie Smith Noyes Foundation (administered by the Organization for Tropical Studies) the University of Florida Department of Zoology, a Sigma Xi grant-in-aid and NSF grants DEB 80-11008 and 80 11023 to Peter Feinsinger and Yan Linhart respecti vely Finally, I thank my family. My parents, Max W. Murray and L orene M. Murra y and my sister, Gayle Fitchner, provided understanding and unwaivering encouragement throughout my educational career. My wife Kathy, and my son, Dylan Winnett Murray, have taught me what is truly important, and help me to keep the various aspects of my life in their proper perspective. iii

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TABLE O F CONTENTS ACKNOWLEDGMENTS. . . . . . . . . . . . . . . . . . . . . . . . . . ii ABSTRACT ..... .. .... .. .... ... ...................... .............. v INTRODUCTI ON ........... .. ........................................ 1 STUDY AREA. . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 METHODS ..................... ............................... ...... 7 Crop Size Fruiting Phenology, and F ru i t Removal Rates .. ...... 7 Seed Germination Experiments .. ... ... .......... .. .. .... .... .. 8 Seed D ormancy Experiments .... ......... ...... .. ............... 10 Gap Dynamics of the Monteverde Cloud Forest .................... 11 Mist Netting and Analysis of Fecal Specimens ................... 12 Fruit Handling, Seed Treatment, and Seed Passage Rates ......... 13 Movement Patterns of F rugivores ......... .... ................... 14 RESULTS ........................................................... 16 Natural History of the Plants .................................. 16 F ruit Consumers . . . . . . . . . . . . . . . . . . . . . . . . 1 7 F ruit Handling and Seed Treatment in the Gut ... .............. 23 Spatial and Temporal Distribution of Suitable Colonization Sites .. .. .... ... ... .... . .. .... .... .. .. ..... 27 Seed Shadows Pr od u ced by Birds ... . ... ..... .......... .. ...... 41 Mediation of Plant Reproductive Success by Birds .... ......... 59 DISCUSS I ON . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80 Ef fects of F ruit Handling and Gut T reatment .................... 80 Effects of Dispersal ........................................... 83 Limitations of the Mode 1. . . . . . . . . . . . . . . . . . . . 92 Seasonal Constraints on Reproductive Success ................... 94 Cone lusions .. .............. ... .. .... ... .. .... ... .... .. ..... 97 APPENDIX ESTIMATION O F SEED SHADOWS FROM DATA ON SEED PASSAGE RATES AND BIRD MOVEMENT PATTERNS: A HYPOTHETICAL EXAMP LE.... . . . . . . . . . . . . . . 100 LITERATURE CITE D. . . . . . . . . . . . . . . . . . . . . . . . . 109 BIOGRAPHICAL SKETC H ... ...... .. . ..... .... . ........ .... .. ....... 119 iv

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Abstract of Dissertati on Prese n t ed to the Graduate Sc ho ol of the Uni ve rsity of Fl or ida in Partial Fu lfillment of the Requirements for the Degree of Doct o r o f Phil osophy AVIAN SEED DISPERSAL OF NE O TR O PICAL GAP-DEPENDENT PLANTS B y Kel v in Gregory Murra y Cha i rman: Peter Feinsinger Major Department: Zoology December 1986 In cloud forest at Monteverde, C o sta Rica, I investigated reproducti ve consequences o f avian seed dispersal for three species of gap-dependent pla nts: Phytolacca rivinoides ( P hy t olaccace a e ) Witheringia solanacea, and w. coccolo boides (Solanacea e ) Of six bird species that co nsumed fruits o f thes e plants, only three ( M y ades tes melanops ( Muscicapidae), Phainoptila m ela noxantha ( Ptil ogo ni dae ) and Semnornis frantzii (Capitonidae) dispersed seeds in v iabl e condi ti on I estimated quality o f dispersal service provided by these species by comparing the seed shadows they produced w ith spatial and t e m pora l distributions o f es tablishment sites for the plants. I estimated seed shadows from da ta on gut passage r a tes of seeds a nd o n movement patterns of radio-tracked birds. Seed s hadow s p r oduced by all three effect i v e dispersers were extens i ve with fe w seeds deposit e d near the parent plant, and s o m e mo ved > 500 m Seeds of th e spec i es exam i ned germina t e in fores t gaps formed by treefa l ls o r l ands l i d es Ger m i na ti o n su cce ss va ri e s w it h gap size and V

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age, but the relationship is different for each species; both Witheringia species germinate well in gaps as small as 15 m 2 o r as old as 6 months whereas P. rivinoides germinates well only in gaps > 70 m 2 or < 4 months Cons equently establishment sites for all three plants are both rare and ephemeral, but to differing degrees. Seeds that are not dispersed to suitable habitat patches can remain dormant in the soil until a gap is formed overhead. To determine consequences of dispersal and dormancy for plant reproductive success, I developed a simulation model that uses data on seed shadows, germination requirements, seed dormancy, and forest dynamic processes to estimate repr oduc tive output (total offspring produced during an individual's lifetime) and relative "fitness" ( an estimator that discounts the contribution of offspri n g produced after a long period of dormancy). Results s how that ( 1) dispersal by any of the three effective dispersers increases reproductive output 16 36 times, even without seed dormancy (2) dormancy capabilities up to t wo years g reatl y enhance both reproductive output and "fitness", but greater capab ilities increase only reproductive output (3) Without dispersal, dormancy has little effect on either reproducti ve output or fi tness. Thus, both dispersal and dormancy ( "di spersal in time) are essential to these gap-dependent plants. vi

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INTRODUCTION Recent interest in the ecology and evolution o f plant-frugivore mutualisms focuses largely on the reproductive consequences, to plants, of fruit consumption by different animals (e.g., Snow 1965 1971; McKey 1975; Howe and Estabrook 1977; Howe and De Steven 1979 ; Howe and Vande Kerchove 1979 1980, 1981; Thompson and Willson 1979; Howe 1980 ; Stiles 1980 1982; Herrera 1981, 1984; Sorensen 1981, 1983; Thompson 1981 ; Stapanian 1982; Skeate 1985). Most studies deal with fruit removal or qualitative aspects of dispersal only: they distinguish between regular and occasional visitors to fruiting plants ( e.g., Leck 1972, Howe and Primack 1975, McDiarmid et al. 1977, Howe 1977, 1980, Howe and De Steven 1979, Howe and Vande Kerchove 1979, Hilty 1980, Greenberg 1981), between animals that pass seeds in viable condition and those that destroy seeds ( e.g., Howe 1980), or between animals that disperse seeds away from the parent plant and those that drop seeds directly beneath it ( e.g., Howe 1977, 1 980 1982, Howe and Vande Kerchove 1979, 1981). However, few studies directly address the contributions to plant reproductive success resulting from the spatial distributions of seeds, or "seed shadows," produced by dispersers. This study deals with the reproductive consequences of avian seed dispersal in three gap-dependent plant species o f neotropical cloud forest. Using data on the dynamics of gap formation and the seed germination requirements of plants, I first identify the spatial and temporal distributions of suitable habitat patches ("gaps" formed by

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2 treefalls or landslides) within the forest Second I compare the distribution of suitable patches with the "seed shadows" produced by different frugivorous birds. Finally, I e v aluate the impacts of fruiting phenology, plant longevity, seed dormanc y and o ther plant life history traits on plant reproductive success and on the ecology and evolution of plant-disperser interactions. In spite of the recent explosion of research on plant-frugivore interactions (reviewed by Howe and Smallwood 1982, Janzen 1983a; see also Estrada and Fleming 1986), knowledge of their ecology and evolution lags behind that of plant-pollinator interactions ( reviewed by Feinsinger 1 983 Jones and Little 1983, and Real 1983). This discrepancy o ccurs because the reproductive consequences of pollen dispersal by animals are more easily quantified than the consequences of seed dispersal (Wheelwright and Orians 1982) In plant-pollinator systems, both the origin of, and "target" for, pollen grains are specific and easily recognized by dispersers and ecologists alike. Furtherm or e, pollinators are rewarded for delivering pollen grains to the target--the stigma of a conspecific flower. Thus, we can determine the relative advantages of pollen dispersal by different animals by determining which ones are most likely to deposit pollen grains on the stigma of a conspecific flower. In contrast, the only target for dispersed seeds is generally a patch of soil with a combination of physical, chemical, and biotic characteristics that make it a suitable site for germination and growth ( i.e., a "safe site," sensu Harper 19 77 ) Further mo re, no reward is offered to vec t o rs that deposit seeds in such sites. For most plants, we lack detailed knowledge of the characteristics of suitable target sites for seeds, let alone their

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3 spatial and temporal distributions. As a result, we know little about the reproductive advantages of dispersal for most plants, and even less about the consequences of dispersal by particular animals. To understand plant-frugivore relationships and the phenotypic traits associated with them, we must identify the spatial and temporal distributions of seed "targets" and evaluate the likelihood of dispersal to those sites by different animals. Howe and Smallwood (1982) proposed three alternative functions of seed dispersal. First, dispersal may result in decreased densityor distance-dependent mortality on seeds or seedlings near the parent plant (e .g., Howe and Primack 1975, Janzen et al. 1976, Platt 1976 Salmonson 1978, Clark and Clark 1981, Augspurger 1 9 83a,b, 198 4a,b Howe et al. 1 98 5). Second, dispersal by certain means (e.g ., by ants that carry seeds to rotting logs) may result in non rando m seed movement to particular sites where the probability of survival is espec iall y high ( Docters van Leeuwen 1954, Handel 1978, Culver and Beattie 1980, Thompson 1980, Davidson and Morton 1981a,b ) Third, widespread dispersal may allow colonization o f ephemeral, spatial ly unpredictable patches o f disturbed habitat ( cf., Augspurger 1983a b 1984a,b Platt 1975, 1976) Although the three functions proposed by Howe and Estabrook are not mutually exclusive, the third may be most important for many plants. In most tropical and temperate forests, recruitment of many plant species occurs only in patches created by canopy disturbances such as treefalls and landslides (Richards 1952, Schultz 1960, Whitmore 1975, Hartshorn 19 7 8, Brokaw 19 8 0, Denslow 1980) Such gap-dependent or "pioneer" species typically germinate in forest gaps soon after formation, grow rapidl y to reproductive size, and produce large numbers of seeds. They

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4 often die out as the gap is closed by lateral growth of trees on the gap's border and by vertical growth of other plants within the gap. In most gap-dependent species, germination is stimulated by the increased red / far red ratio of incident light (e.g., Vazquez-Yanes 1977, 1980, Vazquez-Yanes and Smith 1982, Vazquez-Yanes and Orozco-Segovia 1984) or increasing soil temperature fluctuations (Aubreville and Leroy 1970, Vazquez-Yanes 1976, Vazquez-Yanes and Orozco-Segovia 1982, 1984) that characterize recent gaps (Schultz 1960). Such plants are ideal for studies on seed dispersal. The spatial and temporal distributions of suitable habitat patches can be determined by first establishing the range of gaps in which germination and establishment occur, and then measuring the distribution of those gaps over the landscape.

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STUDY AREA From June 1981 through July 1983, I studied the interactions between frugivorous birds and Phytolacca rivinoides Kunth & Bouche (Phytolaccaceae), Witheringia solanacea L' Her, and w. coccoloboides (Damm.) Hunz. (Solanaceae) in the Monteverde Cloud Forest Reserve, Costa Rica (10'N, 84'W). Lawton and Dryer (1980) provide a thorough description of the geography, climate, and forest types of the Reserve. The Monteverde area lies on a gently sloping plateau, on the Pacific slope of the continental divide in the Cordillera de Tilaran. Local weather patterns and vegetation of the area are strongly influenced by the northeast trade winds. Blowing mist is a nearly constant source of water for plants near the continental divide, even during much of the dry season (January to early May). Forest types in the area range from Lower Montane Rain Forest (Holdridge life zone classification system, Holdridge 1967) near the continental divide, through Lower Montane Wet Forest to Lower Montane Moist Forest and Premontane Wet Forest zones along the lower edge of the plateau. Sites used in this study were all located between 1450 and 1650 m elevation, within either Lower Montane Rain Forest (oak ridge forest, windward cloud forest, and swamp forest, sensu Lawton and Dryer 1980), or within the Lower Montane Wet Forest Rain Forest transition zone (leeward cloud forest, sensu Lawton and Dryer (1980) ). Dominant overstory vegetation within the study area includes many species of Lauraceae, Moraceae, and Aral iaceae, in addition to Meliosma sp., 5

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6 Sloanea megaphylla, Guarea spp., Hieronyma poasana, Ardisia palmana, and Clusia alata. The understory is dominated by Rubiaceae, Solanaceae, Acanthaceae, Gesneriaceae, Piperaceae, and Palmae. Many species occur most commonly in light gaps formed by falling branches or trees, including the "pioneer" trees Cecropia polyphlebia, Urera elata, Trema micrantha, Sapium pachystachys, Heliocarpus popayensis, Clibadium leiocarpum, and several species of Miconia and Conostegia. Several shrubs and large herbs also occur commonly in gaps, e.g., Solanum acerosum, hispidum, Witheringia spp., Phytolacca rivinoides, Heliconia tortuosa, Bocconia frutescens, and Eupatorium sexangulare. Seedlings of Phytolacca rivinoides, Witheringia solanacea, and W. coccoloboides are very common in recent treefalls, especially on soils disturbed by uprooted trees Within one month of formation, these "pits and mounds" (sensu Putz 1983) are generally covered by hundreds of seedlings of these and other species, especially Cecropia polyphlebia and Bocconia frutescens. A typical treefall examined approximately one month after formation contained 79 seedlings of.!:.:_ rivinoides on the "mound" area alone (Murray, unpubl. data). Of the many gap-dependent species at Monteverde, I concentrated on P. rivinoides, w. solanacea, and W. coccoloboides because they have similar fruits (small, multiple seeded berries) and growth forms, but slightly different life history traits. By doing so, I hoped to evaluate the consequences of dispersal by similar assemblages of frugivores to plants with different reproductive schedules, longevities, and germination requirements

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METHODS Crop Size, Fruiting Phenology, and Fruit Removal Rates I collected data on fruit crop sizes and fruiting phenology using monthly censuses of 8, 36, and 33 individuals of P. rivinoides, W. solanacea, and W. coccoloboides, respectively Plants occurred in several different building-phase (sensu Whitmore 1975) treefall plots and in larger, man-made clearings within the reserve. During each census, I counted all flowers, green fruits and ripe fruits on each plant Since most flowering and fruit development in both Witheringia species occurs well before ripening begins, I defined the total fruit crop in those species as the largest number of green fruits counted on that plant during any census in that fruiting episode. In Phytolacca, I estimated total fruit crop as the product of the number of infructescences formed and the a verage number of fruits per infructescence. I computed population-level fruiting phenology of each species (i e ., that of the "average" individual) by first determining the proportion o f each individual's fruit crop that ripened each month (number of ripe fruits censused in each month divided by the sum of all ripe fruits censused on that plant over the fruiting season), and then a ve raging this proportion over all individuals censused. Thus, individuals with large fruit crops and those with small fruit crops were weighted equally in determining the fruiting phenology of the "average" individual. 7

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8 To determine rates of fruit removal from individual plants, I counted the number of ripe fruits on marked branches (Witheringia) or infructescences (Phytolacca) on each census plant on one day, and then counted those remaining 24-72 hours later. For p urposes of the analyses reported here, each observation consisted of t wo such censuses on one plant. During the first count, I remo ved any damaged or desiccated fruits that might abscise spontaneously before the next census. In most cases (77% of all observations), I counted all ripe fruits on the plant. On very large plants or those with inaccessible fruits (23% of all observations), I marked and counted only a subsample of branches or infructescences. Plants were checked in this way for 2-4 consecutive days each m onth Eighty-six percent of the observations were from plants re-censused after 24 hours. In those checked after 2 or 3 days, I divided the number of fruits removed by the number of days between censuses. All removal data are thus reported on a per day basis. I could not obtain information on removal rates by direct observation; the birds responsible for removing most fruits from these plants are extremely wa r y and generally avoid feeding in the understory anywheYe near an o bserv er Seed Germination Experiments I conducted experiments to determine germination success of P. rivinoides, Witheringia solanacea, and W. co cc olo boides in closed-canopy forest and in treefall gaps of va rious sizes and ages. Seeds used in all experiments were collected from se veral plants, mixed, and assigned to different treatments at random. Since many comparisons had to be made at different times of year, strict controls were not possible for

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9 all experiments. In such cases, I attempted to eliminate most of the obvious biases introduced by seasonal weather conditions For example, during the driest months (March and April) when germinating seeds desiccate easily, I watered all seeds 1-2 times per week. Although this practice may result in an overestimate of seed and seedling survival in gaps during very dry periods, it provides unbiased data for answering the more immediate question of the relationships between germination success and gap size and age To compare germination success in closed-canopy forest with that in large gaps, I planted 100 seeds of each species in cups of sterile soil in a large (ca. 2440 m 2 ) man-made gap and 100 others (in like fashion) in adjacent forest. Gap seeds received full sunlight for most of the day, whereas canopy cover over forest seeds was greater than 98%, as determined by a canopy densiometer. Both groups of seeds were covered with a screened (ca. 1 mm mesh) enclosure to exclude herbivores and seed predators. Setups were checked for germination and seedling survival at 1-14 day intervals for 14 months. I measured the effects of smaller gaps on germination success by planting 50 seeds of each species in small cans of soil (10 seeds / can) near the centers of six recent treefall gaps of different sizes. Where necessary, I placed cans above any ground-layer vegetation so that shading was due solely to the crowns of trees bordering the gap. By thus eliminating shade from rapidly growing plants within gaps, effects of gap age (see below) on germination success were controlled These setups were checked at weekly intervals for 2-3 months. gap size using the formula for the area of an ellipse I determined

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10 (A = 71 L W / 4, where L and W represent the lengths of the major and minor axes of the ellipse), since most gaps were roughly elliptical Because light quality and intensity within a gap decrease over time as a result of shading from rapidly growing vegetation within it, I also determined the effects of gap age on germination success. Experiments were conducted in four gaps as they aged naturally Three of the gaps were formed during a severe windstorm on 13-14 November 1982, the fourth during a storm on 11 January 1983. I planted fifty seeds of each species, in 5 groups of 10 seeds each, in small metal cans along transects running through the centers of the gaps Setups were checked at weekly intervals for 1.5-2.5 months. The first run of this experiment was started 2-4 weeks after gap formation, and was repeated in each gap with 50 new seeds at 3-4 month intervals for one year. Seed Dormancy Experiments To estimate how long seeds of:__ rivinoides, w. solanacea, and w. coccoloboides can remain dormant in the soil, I determined the viabilit y of cohorts of seeds buried for different periods of time. In December 1981 I collected approximately 850 seeds from 5 to 20 individuals per species. After combining seeds taken from all individuals of a particular species, seeds were randomly assigned to treatments (burial for different periods of time) and then packed in small bags of mosquito netting or in microcentrifuge vials with mesh coverings. All seeds were then buried approximately 15 cm deep at a forest site with approximately 98% canopy cov e r. At one to two month intervals over the next 17 months, I recovered 50 seeds of each species from the burial site and planted them in

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11 plastic cups of forest soil in the center of a large, man -made clearing 40 m away Seeds were checked at least once every two days for germination. During the dry season, seeds were watered at least every other day In March 1984, I recovered an additional 50-75 seeds of each species from the burial site and planted them in plastic cups of potting soil in a greenhouse on the University of Florida campus. These seeds, like those germinated in the field, were checked at least every two days until all seeds had germinated, or until no further germination had occurred for four weeks. Gap Dynamics of the Monteverde Cloud Forest From May to July 1983 I set up five permanent 500 m line transects through representative areas of the Lower Montane Wet Forest and Rain Forest zones in the reserve. For each "e xpanded" gap (the area bounded by lines connecting the trunks of trees bordering the canopy gap; see Runkle 1982 ) encountered along a transect, I measured the transect interval within the canopy gap (defined as the land area directly beneath the canopy opening), length and orientation of the major and minor axes of the canopy gap, and height of the surrounding canopy. I sampled even the very small gaps (down to 1.6 m 2 ) formed by single branches, because data from germination experiments suggested that even gaps of that size affected germination success in.!:.:_ rivinoides, w. solanacea and w. coccoloboides. I also subjectively estimated gap age in years This was easily done for gaps formed in the previous year, because most still contained intact twigs and leaves of the fallen tree, as well as many epiphytes. The proportion of land area occupied by gaps

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12 less than one year old was computed as the length of transect under those canopy gaps divided by the total transect length. Gap area was determined using methods described above. I censused the transects again in March 1984 to collect data on gaps formed since the pre v ious Jul y Mist Netting and Analysis of Fecal Specimens From June 1981 through July 1983, I regularly mist-netted birds in 14 study plots: six in tree fall gaps from 1 .5 to 3.5 y ears old, four in large, man-made clearings (hereafter termed "cut ove r" plots), and four in mature forest with intact canopy. Plots were chosen primarily for an o ther stud y and are described in detail in Feinsin g er et al. ( in re v iew ) From June 1981 through Jul y 1982, I netted for the first six hours of daylight (ca. 0515-1115) in two plots of each of the three habitat types each month. Plots used each month were alternated so that sampling effort was approximately equal in all forest and cutover plots, and m os t treefall plots, over the first 12 m onth period. From September 1982 th r ough Ju ly 1983, I netted at least on e day ( i. e ., for the first 6 hours of daylight) per month in each o f thr ee plots, one in each habitat type. For this 11 -month period, the same three plots were sampled each month. Additional netting in these and other plots was conducted on an irregular basis. I also netted in one of these plots from 4 to 2 0 March 1984. All birds captured were weighed, measured, and checked for breeding condition a nd molt Frugi vo r es we r e marked with un i que color combinations using plastic leg bands and then retained from 5 to 45 minutes in small holding cages (ca. 20x20x30 cm) to obtain fecal

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13 specimens. I also collected samples from many, but not all, insectivorous species. Fecal specimens were stored in 70% ethanol. In the laboratory, I counted and identified all seeds in each sample using a reference collection made over the two-year study. I also vi sually estimated the percent arthropod composition of each sample to the nearest 10 % Fruit Handling, Gut Treatment, and Seed Passage Rates To determine the consequences to P. rivinoides, W. solanacea, and W. coccoloboides of fruit consumption by different bird species, I conducted feeding experiments with captive individuals of six bird species observed to eat their fruits. Birds were captured in mist nets and maintained in a small (lxlxlm) cage during the experiments Between trials, fruits other than the experimental species, as well as water, were provided ad libitum. In all but two cases, trials were completed and the bird was released on the same day. After introducing the experimental fruits into the cage, I noted whether or not birds consumed the fruits, how fruits were ingested (e .g., swallowed whole vs. eaten piecemeal), whether the ingested seeds were voided intact, and whether they were defecated or regurgitated Recovered seeds, or a subset if many trials were run, were then planted in plastic cups of soil under a screened enclosure in a large clearing. I checked seeds at least once every two days for germination, and watered them when necessary. To determine gut passage rates, I conducted feeding trials in a similar fashion. Approximately 7-15 fruits of either P. rivinoides, W. solanacea or w. coccoloboides were introduced on the cage floor, and all other fruits were removed from the cage I observed subsequent

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14 events through a small hole cut in one opaque side of the cage. Birds usually descended from perches to feed within a few minutes after the test fruits were introduced. All uneaten fruits were removed 5 min. after the first fruit was consumed The midpoint of the interval during which fruits were eaten was considered as the time of ingestion for all fruits in a particular trial. Each time a bird defecated, I recorded the time and the location of the fecal mass on the floor of the cage. After 3-5 fecal masses had accumulated, I removed the paper from the bottom of the cage and replaced it. At the end of the feeding trial, all fecal masses w ere recovered; seeds were later identified and counted Successive feeding trials were done approximately 30 min apart; i.e., the next trial ( with a different fruit species) began 30 min after the beginning of the previous trial. In this way, I could usually complete 1-2 feeding trials on each bird with each of the three fruit species before releasing it on the afternoon of the same day it was caught After counting seeds in the fecal masses, I grouped the data int o 5-min classes, recording the proportion of all seeds vo ided in each 5 min time segment following ingestion. Movement Patterns of Frugivores To determine the movement rates and patterns of birds taking~ rivinoides, W. solanacea, and W. coccoloboides fruits in the field, I fitted mist-netted birds with small (ca. 3.Sg) radio transmitters and f ollowed their movements for 3 -8 days. Transmitters used were homemade units similar to those available from a number of commercial telemetry

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15 suppliers. I used an LA-120S receiver (AVM Instrument Company, Dublin, CA) and a homemade 5-element yagi antenna. Transmitters were attached to the skin and feathers on a bird's back (j ust anterior to the synsacrum) with Super Gluetm_ Birds fitted with transmitters were held in the field in a small cage for approximately 30 min t o ensure that they were healthy when released. By using a carefully mapped network of trails, I could often remain within sight of radiotagged birds for long periods of time. Each time the bird moved to a new location, I simply recorded the time and the bird's location on a map of the study area. When I was out of visual contact with the bird, I determined its location by triangulation. I took compass bearings on the direction of the strongest signal from two points, separated by at least 50 m, on the mapped trail system. After taking the second bearing, I rechecked the first to ensure that the bird had not moved. I took new bearings as soon as the signal received indicated ( by a change in signal strength or direction) that the bird had moved. In the absence of any such indication, I took two new bearings e v ery 3 5 minutes to check the bird's location.

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RESULTS Natural History of the Plants Phytolacca rivinoides is a large herb ranging from Mexico to Bolivia (including the Antilles, Raeder 1961) at elevations from sea level to 3000 m (Standley 193 7). Usually among the first colonists of treefalls and landslide edges, individuals commonly spread to cover approximately 25 m 2 within 1-2 years of seedling establishment. Plants begin to ripen fruits at about one year of age, but most die (presumably as a result of shading and/or root competition) within 2 5 years of establishment. Of the eight individuals I monitored closely, the median age at death was 24 months (range 21 to 31 months). During the single, extended fruiting season, individuals produce 1, 500-30,000 (median = 4700) fruits borne on axillary racemes containing ca. 30-100 fruits each. The fruits are purple-black, about 7.5 mm in diameter, and contain 5-12 (x = 9 4 n=20) seeds in a wate ry pulp. Witheringia solanacea and W. coccoloboides are both shrubs attaining heights of about 1.5-2.5 m. Witheringia solanacea ranges from Mexico to Brazil, including the Antilles ( D'Arcy 1973), occurring from sea level to 2000 m ( Standley 1937). Witheringia coccoloboides is typical o f cloud forests from Costa Rica to Colombia at elevations from 300 to 2500 m (D'Arcy 1973). Both species grow much more slowly than does.!'...:... rivinoides; although seedlings are co mm on in young gaps the y do not attain reproductive size for about 3-5 years, and they usually live for 8 or more y ears before being shaded out by the reestablishing 16

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17 canopy. Fruits of both Witheringia species are red, ca 10-12 mm in diameter, and are borne in axillary fascicles. Fruit crop size and seed number are highly variable in both species. Total seasonal fruit crops in'!!.:.__ solanacea ranged from 5 to 1084 (median=l54 n=121), and seed number per fruit ranged from 6 to 39 (x = 22.8, n=44). Seasonal fruit crops in'!!.:.__ coccoloboides ranged from 5 to 1150 (median =1 20, n=84), and seed number ranged from 46 to 73 (x=59 .1, n=l 7). Fruits of all three species show typical adaptations for bird dispersal (van der Pij l 1972). Removal by animals other than birds is probably rare. Although rodents are known to eat fruits of some understory plants, including rivinoides (Denslow and Moermond 1982), I found no evidence of removal by rodents at Monteverde. Early morning counts of fruits marked on the previous afternoon showed no evidence of nocturnal removal, and no fruits were removed from two plants each of'!!.:.__ solanacea and w. coccoloboides from which birds, but not rodents, were excluded by screened enclosures left open at the bottom (Murray, unpubl. data). In addition, an intensive concurrent study of frugivorous bats revealed no evidence of these fruits in bat fecal specimens (E. Dinerstein, pers. comm.). Fruit Consumers The disperser assemblages for~ rivinoides, w. solanacea and w. coccoloboides at Monteverde are surprisingly limited. Data from ca. 200 fecal samples collected from mist-netted frugivores, as well as extensive observations by several investigators (Wheelwright et al. 1984), suggest that only ten bird species commonly consume fruits of any of these plants in the Mont everde vicinity The limited size of the

PAGE 24

18 disperser assemblage comes about because few species of frugivorous birds commonly descend to the forest understory or into treefall gaps; similar fruits of canopy trees and epiphytes are often taken by a much larger number of bird species (Wheelwright et al. 1984) The three major dispersers for all three plant species in cloud forest above 1500 mare Black-faced Solitaires (Myadestes melanops, Muscicapidae), Black and Yellow Silky Flycatchers (Phainoptila melanoxantha, Ptilogonatidae), and Prong-billed Barbets (Semnornis frantzii, Capitonidae). Of the 360 seeds of these three plant species recovered in fecal specimens from 196 frugivores, all were from these three bird species. Furthermore, these data also suggest that Myadestes is responsible for far more dispersal of these plants than are either Semnornis or Phainoptila: 84 % of recovered seeds were from Myadestes alone. Although!::_ rivinoides, W. solanacea, and W. coccoloboides are highly dependent upon a very few bird species for dispersal services, none of the birds is similarly dependent upon any of the three plant species. The known diets of Myadestes, Phainoptila, and Semnornis include fruits of 51, 14, and 30 species, respectively (Wheelwright et al. 1984; K. G. Murray, unpubl. data). In fact, fruits of the three plants are of relatively minor importance in the diets of these birds. Of the 154 fecal specimens collected from these three species, only 35% contained seeds of P. rivinoides, w. solanacea, or w. coccoloboides. The ecological relationships between these three plants and their dispersers are thus highly asymmetrical. Seven other bird species removed fruits from at least one of the plant species. The tanagers Chlorospingus opthalrnicus and Tangara dowii and the finch Pselliophorus tibialis occasionally removed fruits, but

PAGE 25

19 failed to ingest most seeds (see below). Of the remaining four species recorded feeding on P. rivinoides, W. solanacea and W. cocco lob oides only one was a frequent visitor to any of these plants: at elevations below approximately 1420 m, seeds of'!!..:_ solanacea were commonly found under display perches of Long-tailed Manakins (Chiroxiphia linearis, Wheelwright et a l 1984). Data from mist net captures (Table 1) also suggest the unequal importance of these ten bird species as dispersers for P. rivinoides, w. solanacea, and w. coccoloboides. Of the three primary dispersers, M. melanops was the most frequently captured in all three habitats. In fact, M. melanops may be the most important disperser for all understory plants with bird-disseminated seeds within the Monteverde Cloud Forest Reserve. Capture rates for Myadestes were highly variable over time, however (Fig. 1 ). While usually very common in the reserve from Februar y through August, they were all but absent from late October through early January. The seasonal decline in capture rate was due to emigration of both adults and young following the breeding season. Visual and auditory censuses confirmed this seasonal pattern of abundance (K. G. Murray, unpubl. data). Where Solitaires go when they leave the Monteverde area remains somewhat a mystery, but o. J. Levey (personal communication) has caught several individuals during this season at Finca La Selva, at ca. 50 m elevation in the Atlantic lowlands. Although some other species of frugivorous birds at Monteverde are also al ti tud inal migrants (e.g ., Three-wattled Bellbirds, Procnias tricarunculata, and Resplendant Quetzals, Pharomachrus moccino; Wheelwright 1983, and K. G. Murray, personal observation) I have no

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20 Table 1. Capture data for bird species feeding at least occas i onally on fr u it s of P. rivinoides, W. solanacea and w. coccolo b oides at Monteverde Total numbers of mist net hours in forest treefall, and cutover ( see text) plots were 115 8 1164 and 144 9 respecti v el y Species forest treefa ll s cutov ers .,a Myadestes melanops 66 30 33 P hainoptila melanoxantha 1 0 4 Semnornis frantzii 0 0 3 C hlorospingus opthalm i cu s 10 9 5 Tangara dowii 0 0 Psel liop h or us t ibialis 1 0 2 a Capture data from these unus u all y large (1155 2442 m 2 ) m an-made clearings are not included with those from natural treefalls P lant and bird asse m blages in t he large c l earings were m ore t ypical of early secon d growth habitats than those of natural fores t or treefall gaps

PAGE 27

Figure 1. Myadestes capture rates and breeding activity from July 1981 to June 1983 Bars at bottom of figure indicate the presence of breeding adults (i.e., with brood patches) and young of the year on study plots. 1

PAGE 28

a: ::J 0 J: 0 1 I t0.08 w z a: W 0 06 Cl. 0 w 0: ::J t(l_
PAGE 29

23 evidence that any other disperser of P. rivinoides, W. solanacea, and W. coccoloboides undertakes such annual movements. Fruit Handling and Seed Treatment in the Gut Consumers of P. rivinoides, w. solanacea, and w. coccoloboides at Monteverde handled fruits by one of two methods. Myadestes, Phainoptila, and Semnornis invariably swallowed fruits whole, with little or no manipulation in the bill. In contrast, the tanagers Chlorospingus opthalmicus and Tangara dowii, and the finch Pselliophorus tibialis, mashed fruits extensively in the bill before swallowing. This behavior resulted in the fruit skin and many of the seeds being dropped before the pulp was ingested. Field observations of these and other tanager and finch species suggest that most handle fruits in this manner. As a result, these birds ingest and disperse few, if any, of the seeds they remove from most plants. The probability of seed ingestion in tanagers and finches seems to depend at least in part on seed size. In Pselliophorus, Chlorospingus, and Tangara, most seeds were discarded along with the fruit skin during handling ( Table 2) Nevertheless, some w. solanacea seeds (ca. 1.5 mm diameter) were ingested by all three species, especially by Pse lliophorus. In contrast, none of the birds ingested any of the larger seeds of W. coccoloboides (ca. 2.4 mm diameter); all were discarded with the fruit skin. For seeds of a given size, the probability of ingestion increases with bird size. P. tibialis (ca 3 0.5 g; gape 10 3 mm) ingested 71 % of the w. solanacea seeds offered, whereas opthalmicus (ca. 20 .0 g; gape 9.1 mm) and T. dow ii (ca 20.0 g; gape 8.5 mm) ingested only 10.7% and 15.8%, respectively.

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24 Apparently, larger seeds are more easily separated from the fruit pulp du ring manipulation in the mandibles, especially by bird s w ith smaller bills. Data on the seed loads recovered from mist-netted tanagers at Monteverde support this suggestion: feces of these birds generally contained only the minute (ca 0.2-.06 mm diameter ) seeds from species of Ericaceae, Melastomataceae, and Gesneriaceae ( K. G. Murray, unpubl. data). Small tanagers such as Chlorospingus and Tangara may act as dispersers only for plants with such minute seeds. The effect of gut passage on seeds also varies among bird species. Data from feeding trials suggest that although many seeds of w. solanacea may be ingested by Pselliophorus, very few survive passage through the gut (Table 2) Instead, most seeds were apparently ground up in the gut; feces of the individual used in this experiment contained large numbers of recognizable~ solanacea seed fragments. Only two~ solanacea seeds emerged intact, and these were in viable ( Table 3) The absence of seed fragments in feces of the same bird after feeding on W coccoloboides fruits again strongly suggests that seeds of this species are not ingested by Pselliophorus. Data for Chlorospingus and Tangara suggest that the few W. solanacea seeds that are ingested pass through the gut intact (Tab le 2); no evidence of destruction in the gut (such as seed fragments in the feces) was found, and the few seeds recovered fr om feces were fully viable ( Table 3). Seeds eaten by Myadestes, Phainoptila, and Semnornis were always voided intact. Although I found no evidence of e it her increased or decreased g ermination success ( defined si m pl y as the percent of seeds t h at ge rmi n a ted follo win g g ut pa ss ac;e ) as a resul t of gu t pa ssa ge i r: any of these birds the rate at which seeds of all t h ree p l ant s p eci e s

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25 Table 2 Fruit handling techniques and gut treatment effects on seeds eaten by captive individuals of six frugivore species Bird Plant seed frui t s seeds seeds voided a species b species diameter(mm) eaten dropped ingested intactc M m P.r 2 0 53 0 411 411 w s. 1.5 69 0 1366 1366 w c. 2.4 36 0 1206 1206 P.m P r. 17 0 168 168 w s. 19 0 447 447 w.c. 18 0 524 524 s. f. P. r. 36 0 413 413 w.s 7 0 145 145 w.c. 8 0 477 477 c.o. W.s. 3 16 3 3 w.c 4 36 0 T.d W.s 2 25 3 3 P. t. w s. 9 38 95 2 w.c. 4 111 0 a M.m.= Myadestes mela n oes, P m.= P h ainoptila melanoxantha, S.f.= Semnornis frantzii, c.o = Chlorospingus optha l micus, T.d.= Tang:ara dowii, P.t.= P selliophorus tibialis b P.r.= Phytolacca rivinoides, w.s. = Witheringia solanacea w.c = Witheringia coccoloboides C Of seeds ingested

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26 Table 3. Effects of gut passage on germination success and germination rate. Data on untreated controls taken from Table 4 pe r cent germination (n) days to 95% germinationc Bird Plant a spec i es speciesb treated untreated t r eated untreated M m. P. r. 78 ( 100) 89 ( 100) 22 49 w.s. 73 ( 100) 86 ( 100) 45 56 w. c d 86 (100) 3 1 56 P m. P r. 89 (100) 89 ( 10 0) 37 49 w.s. d 86 ( 100) 73 5 6 w c. d 86 ( 100) 54 56 S.f. P r 75 ( 100) 89 (100) 26 4 9 w s. d 86 ( 100) 19 56 w.c d 86 ( 100) 19 56 C o w.s. 100 (3) 86 ( 100) d d T d. w.s 100 (3) 86 (100) d d P. t. w.s. 0 (2) 86 ( 100) d d a M. m. = Myadestes melanops P .m. = P ha i noptila melanoxantha S.f. = Semnornis frantzi i, c.o .= Ch l orospingus opthalrnic u s, T .d = T angara dowii P t. = Pselliophorus tibialis b P r = Phytolacca rivinoides w.s.= Witheringia solanacea, W.c .= Witheringia cocco l oboides c Of those that germinated d Insuffic i ent number o f seeds available for e xpe riment

PAGE 33

27 germinated was often enhanced by gu t passage ( Table 3). Thus, although treatment in a bird gut is not required for germination in any of t hese plants, seedlings from treated seeds may gain a competitive advantage through rapid germination in a newly created patch of suitable habitat Spatial and Temporal Distribution of Suitable Colonization Sites Germination Requirements Gap vs. understory comparisons Results of forest vs gap germination experiments (Table 4) show that after 60 days, all three species had significantly higher germination success under gap conditions than under closed canopy. Many Witheringia seeds did eventually germinate in the forest after more than a year. These seeds, however were protected from litter fall by the screened enclosure. Ordinarily, seeds on the forest floor would be covered by leaf litter and incorporated into the soil seed bank in a dormant state long before they germinated. Germination success vs gap size Germination success increased with increasing gap size in all three species ( Fig 2) In fact, slopes of the regressions (on transformed variables; see Fig. 2 legend) of germination success on gap area do not differ significantly among the three species (Fs=l.550 with df=2 15, 0.1 < P < 0 25). Furthermore, analysis of covariance shows that the regression lines for the two Witheringia species are indistinguishable ( Fs=0.07 with 1,17 df, P > 75), but that the adjusted mean germinat i on success in~ rivinoides is less than that for the other two species ( Fs= 12 82 w ith 1,17 df, P < .005). Equations for the adjusted (by analysis of covariance ) regressions are y = 6.84x + 12.88 for both W. solanacea and W.

PAGE 34

28 Table 4. Percent germination success in forest and large gap habitats Sample size for all experiments was 100. D ifferences between gap and forest values were tested with a test for equality of two percentages ( Sokal and Rohlf 1969: 608 ) gap forest p afte r 60 days P hytolacca riv i noides 89 0 < 001 Witheringia solanacea 86 14 <-001 Witheringia coccoloboides 86 2 <.001 after 410 days Phytolacca rivinoides 89 0 < .001 Witheringia solanacea 86 61 < 001 Witheringia coccoloboides 86 87 > .5

PAGE 35

29 coccoloboides, and y = 6.84x + 1.14 for P rivinoides, where y is the arcsin transform of the proportion of seeds germinating and x = ln(gap area + 1). Thus, germination success increases with gap size at the same rate in all three species, but for a given gap size, germination success in P. rivinoides is always less than for either species of Witheringia Consequently, rivinoides requires larger gaps than either species of Witheringia for germination. Such differences in the relationship between gap size and germination success translate directly into differences among species in the distribution of suitable germination sites over the landscape. Germination success v s. gap age. Seeds of P. rivinoides, w. solanacea and w. coccoloboides also differ in t h e relationship between germination success and gap age (Fig 3) Because the gaps used were of different sizes, data plotted in Figure 3 were adjusted to control for the effects of gap size, according to the relationships in Figure 2. To facilitate comparison among species, data were also scaled such that the highest germination success attained in each species w as set at 100% Germination success decreased with increasing gap age in all three species, presumably as a result of decreasing light intensity (or quality) as the understory vegetation within the gap grew and shaded more of the soil surface. The initial increase in germination success of P. rivinoides may have resulted from increased light intensity or quality in the first few months after gap formation, as the leaves and epiphytes on fallen trees and branches decayed and fell to the ground. Such an increase in light intensit y or quality wo uld be e x pected t o have the greatest effect on an extremely shade-intolerant species such as P. rivinoides.

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Figure 2. Germination success vs. gap area. Results from germination experiments in 6 recent gaps and 1 forest underst ory site ( gap area=0). Curves shown are de-transformed linear regressions of the proportion of seeds germinating (arcsin transformed) on ln ( gap area+ 1). Equations, Fval ues, and significance levels for~ rivinoides, '!i.:_ solanacea and '!i.:_ coccoloboides are y = 6.99x + 0.54 (F=71.8, p < .001), y = S.lSx + 20.08 (F=l0.11, p < .05), and y = 8.36x + 6.35 (F=40.35, p < .002), respectively.

PAGE 37

31 60 Phytolacca rivinoides 40 20 z 0 80 IWitheringia solanacea <( z 60 a: w 40 C, Iz w (.) a: w a. 80 Witheringia coccoloboides 60 40 20 0 100 200 300 400 GAP AREA (m 2 )

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Figure 3. Germination success vs. gap age. Results from germination experiments in 4 gaps as they aged naturally (see text). Missing data for w. solanacea at 3.5 months and for W. coccoloboides at 1.5 and 3.5 months are due to a lack of sufficient seeds for those experiments. Different symbols indicate values for each of the 4 gaps. Lines connect mean germination success values at each gap age.

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33 1 00 80 Phytolacca rivinoides 60 40 20 o z 0 I100 {:,. <( z 80 Witheringia solanacea a: 60 0 w C, 40 Iz 20 w c., a: w a.. 100 {:,. 80 Witheringia coccoloboides 60 0 40 20 0 2 4 6 8 1 0 1 2 GAP AGE (months)

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34 Following the initial increase in~ rivinoides, germination success decreased with increasing gap age much more rapidly than in either species of Witheringia. In fact, germination success in~ rivinoides was negligible by 7 months after gap formation, whereas some '!!..:.._ coccoloboides seeds germinated in gaps as old as 12 months. Germination success decreased least rapidly with increasing gap age in W solanacea although it reached zero by 10 months (Fig 3) Thus, a given gap remains open for colonization by'!!..:.._ coccoloboides and w. solanacea for some time after it is no longer suitable for P rivinoides. Seed dormancy. In all three plant species seeds buried for up to 27 months showed no significant decrease in viability ( Figure 4). Mean germination success for all seeds was similar in all three species; values for P rivinoides W. solanacea and W. coccoloboides were 65%, 50%, and 55% respectively. In a similar experiment (K.G. Murray, unpubl. data), I collected 100-200 seeds of each species at approximately two month intervals for the same 27-month period and buried these seeds together in a similar forested site. These seeds were recovered in March 1984 and planted in the greenhouse The results of this experiment were similar to those obtained in the previously described one: no decrease in seed viability was demonstrated in the first 27 months of burial. Spatial Distribution of "Safe Sites" New canopy gaps covered approximately 1.5 % of the total land area sampled by forest transects each year. Percentages of the five forest transects under new canopy gaps (less than 1 year old) were 0.2, 3 1,

PAGE 41

Figure 4. Results o f seed dormanc y experiments with P. rivinoides, W. solanacea, and W. coccoloboides, and results of regression analyses on germination success vs. seed burial period.

PAGE 42

C: 0 as C: E ... Q) O> a. C: (I) (.) ... as 36 90 60 Phytolacca rivinoides 30 ( 25< P< 5) 0 ------..----........ ----...----~--------90 60 ... 30 Witheringia so/anacea y=-0.92x+55 8 (.05
PAGE 43

37 3.1, 1.5, and 0.5, respectively, for the 1983 census, and 0.7, 2.1, 1.3, 1.3, and 1.1 for the 1984 census. Most gaps were formed during severe windstorms, which occur primarily from November through January at Monteverde. The size distribution of canopy openings associated with the 90 expanded" ( sensu Runkle 1982) gaps sampled is shown in Figure 5. It is typical of such distributions in that very small gaps are exceedingly common, whereas very large gaps are exceedingly rare. Most gaps smaller than 10 m 2 were formed by one or more branches falling from the canopy, although entire trees occasionally formed gaps as small as 5 m 2 The gap size distribution shown in Figure 5 slightly overrepresents large gaps, since the probability that a gap will be sampled by a line transect is directly proportional to its size. To construct an unbiased gap-size distribution I weighted the number of gaps in each size class by first dividing that number by the diameter of a circular gap equal in area to the median-sized gap in that class. I then determined the proportion of all weighted v alues occurring in each size class. The resulting adjusted gap-size distributi o n is very similar to the unweighted one in Figure 5, and is not shown here. However, all estimates of the density of gaps in each size class, and the proportion of land area they occupy (see below), are based upon the unbiased gapsize distribution. Assuming that the canopy disturbance rate of 1.5 % per year and the adjusted gap-size distribution are representative for the Monteverde cloud forest o v er the long term, I determined the density of gaps of various sizes over the landscape and the amount of land area they occupy. I first divided the range of observed gap sizes into the

PAGE 44

30 25 en a. <( 20 C, u.. 0 15 a: w m 10 i 11 :J z 5 01''''1''''1""''' r '' I' ,,, 'I '' '' 1 0 100 200 300 400 500 GAP SIZE (m 2 ) Fig u re 5 Size di str i b u t i o n o f 90 ca nopy gap s form e d over a 2 -y ear period from ca M arch 19 82 M arc h 1 984 ----w CD

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39 following 16 size categories: < 4 9 5 9.9, 10-14.9, 15-19 9, 20-24 9, 25-29.9, 30-39.9, 40-49.9, 50-59.9, 60-79 9, 80-99.9, 100-149 9, 150199 9, 200-299 9, 300-399.9, and > 400 2 m To determine the density and coverage (proportion of land area) of gaps in each category that are formed each year, I used a modification of the methods of Lucas and Seber (1977) for line transect data. Because the gaps censused in this study were actually formed over a period of several years, I weighted the coverage estimates such that the total area in gaps (over all size categories) equals 1.5% of total land area Density estimates were weighted in a similar manner, so that all final values are expressed on a per-year basis I used this analysis to approximate the availability of suitable germination sites over the landscape. For purposes of illustration, let us arbitrarily define a safe site with respect to gap size as any gap in which germination success is at least 25%. My use of the term "safe site" here is not exactly equivalent to that of Harper (1977), since one gap could provide many germination sites, and each of these would be termed a "safe site" by Harper's definition. Figure 6 shows the density of safe sites and the proportion of land area they occupy as a function of minimum safe site area, using the gap density and coverage estimates derived above. Both density and land area covered decrease rapidly with increasing minimum safe site area. For a plant that requires a gap of at least 100 m 2 (e.g., a circular gap of 11.3 m diameter) as a safe site, for example, there is approximately 1 0 safe site per hectare, and 0.62 % of the total land area is available for colonization For a plant whose seeds can germinate in a much smaller gap, however, say 10 m 2 (e.g., a circular gap of 3.6 m diameter), suitable patches for

PAGE 46

40 colonization are much more common: 6.0 "safe sites" per hectare, representing 1.3 2% of the total land area. Similar analyses demonstrate that suitable germination sites are indeed distributed differently for the species in this study. Minimum gap sizes in which germination success is at least 25% (b ased on the regression lines in Figure 1) are 66.7, 5.9, and 15.9 m 2 for P. rivinoides, W. solanacea, and W. coccoloboides, respectively. Thus, from Fig. 6, we can estimate approximately 1.6, 8.8, and 4.3 suitable patches per hectare, representing 0.8, 1.4, 1.2% of the total land area. The foregoing discussion treated the availability of suitable patches only on the basis of gap size and its effect on germination success; i.e., it assumes that all gaps formed in a particular year are equally suitable for colonization at any time. Since germination success varies among the species with respect to gap age as well as to gap size, however, the availability of suitable colonization sites varies among species temporally as well as spatially. If we again arbitrarily define the length of time a gap remains open for colonizati o n as the length of time during which germination success remains at least 25 % then for P. rivinoides, W. solanacea, and w. coccoloboides gaps remain open for colonization for approximately 4.5, 8.0, and 5.5 months, respectively. Figure 7 shows the density of safe sites and the proportion of land area they contain as a function of time of year, for plants that can colonize gaps up to 4, 6, and 8 months old. The figure was genera ted by multiplying both the canopy disturbance rate of 1.5 % / year o r the overall gap density of 17 5 gaps / hectare / year by the estimated proportion of gaps occurring in each month. The result (the line labelled "0 months") is the density of gaps formed that month, I I I I I I I I I I I

PAGE 47

41 or the proportion of land area they occupy. Other lines in the figure were generated by including, for each month, the density of new gaps or the proportion of land area disturbed in the 4, 6, or 8 previous months. For species capable of invading only very young gaps, suitable colonization sites are available for only a short period of time each year (Fig 7). For species capable of colonizing older gaps, however, the availability of suitable colonization sites remains high for a much longer period of time. For example, suitable colonization sites for W. solanacea are relatively common for 9 months of the year, while those for P. rivinoides are common for only 5 months. Although these analyses are useful for gaining a qualitative impression of the relationship between germination requirements and the availability of suitable habitat patches over the landscape, data presented in Figures 6 and 7 clearly show that applying the concept of "safe site" to treefall gaps oversimplifies the relationship between germination requirements and availability of suitable patches over the landscape. The effects of gap size and age on germination are not threshold effects, in which germination success in gaps below a certain size or above a certain age is zero and that in younger or larger gaps is 100%. Instead, germination success is a continuous function of both gap size and age, and each gap size has an associated germination probability for each plant species. Seed Shadows Produced by Birds Seed Passage Rates Most birds fed on fruits placed in the experimental cage soon after the fruits were introduced. In most cases, birds ate 4-10 fruits

PAGE 48

Figure 6 Density and areal coverage of "safe sites" (see text) vs. minimum safe site area.

PAGE 49

43 (7'1' 101 .:10 %) uS3.11S 3.:1'1'S" NI v'3~V 0NVl LO 0 LO . 0 "'"" "'"" 0 0 I d I I C\I <( 0 E IJ.J 0 C: C".) w <( I != >0 I (/} t-z w Cl)< 9 z ..J LL w <( o'#I (/} I! :;: I 0 LL 0 I C\I 0 0/ <( w I a: <( I ::::> I 0 0 O/ "'""z t5 (f / .,,,o /0 (Y' 0 LO 0 "'"" "'"" (8JBl084/-#) A.11SN30 11 3llS 3.:IVS,,

PAGE 50

I(/) z,... w t o ca I;; 0 w (1) I.c "" (/) w u. < (/) '-' 20 10 0 I :::::-> ;::::::, ;::;..,o:::::; I I I I I I I I I I ,, I I I I I I J M M J S N J M M J s N MONTH ,... Z 1111 ...J 1.5 (/) < c( w 1w t: O 0 a: (/) II. c( w u. o u. 0 z c( 0 5 c( (I) ...J '-' Figure 7. D e nsity and areal coverag e of sa fe sites as a f un c ti o n of time of year. Lin es lab e ll e d O 4 6 and 8 mo nth s show th e density a n d cove rage of gaps O, < 4 < 6 and < 8 months old ------------.i:,. .i:,.

PAGE 51

45 (depending upon fruit and bird species) and then perched for approximately 10-15 minutes. During this time, birds generally closed their eyes, puffed out their feathers, and remained nearly motionless. Similar behavior was often observed in actively foraging birds in the field: after taking a number of fruits from a plant (and presumably filling the gut) birds often flew to a perch in a neighboring tree or shrub and remained there for 10 or more minutes. This period of inactivity almost always continued until the first defecation of material from the previous foraging bout. Birds became progressively more active after each successive defecation, as fruits were processed through the gut. Data on gut passage times for seeds of P. rivinoides, W. solanacea, and w. coccoloboides are shown in Figure 8. Although variation in gut passage time is considerable at all levels (i.e., among seeds of a particular plant species ingested at the same time, among plant species in a given bird species, and among bird species), it is useful to ask whether gut passage rates vary among plant species and bird species in a systematic way. To determine whether seeds of some plant species are processed more quickly than others, I compared median passage times for the three plant species in the three bird species. In all three bird species for which I have detailed data, median passage times were longest for seeds of P. rivinoides, intermediate for w. coccoloboides, and shortest for w. solanacea (Table 5) All else being equal, P. rivinoides seeds should thus travel farther than those of either species of Witheringia The reasons for these consistent differences are as yet unclear; fruits of all three species are similar in size, have fruit skins of similar thickness and toughness, and contain seeds that seem to I I I I I I I I I I I I

PAGE 52

c:, z c:, C: w w (/') 0 w w (/') 20 40 20 46 Myadestes melanops Witheringia solanacea Witheringia coccoloboides Phytolacca rivinoides 0 ~~t----,,1--+~--f........ -+-..C::~--4---.------. 0 10 30 40 50 60 70 80 90 MINUTES AFTER INGESTION Fi gure 8 Seed passage rates for the three plant species in Myadestes rnelanops Phainoptila rnela n oxantha and Semnornis frantzii. Arro w s indicate med i an passage times

PAGE 53

..J 80 60 40 47 Phainoptila melanoxantha Witheringia solanacea < 20 0 0-+......... -+-t_,_+--=~~e---.----,.----,----,--~ LI.. 0
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40 ...J c( 20 0 u.. 0 #, 40 C, z C, a: w w C/J 20 40 Cl 20 w w C/J 48 Semnornis frantzii Witheringia solanacea Witheringia coccoloboides Phytolacca rivinoides 0 10 20 50 60 70 80 90 MINUTES AFTER INGESTION F igure 8 -continued

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49 Table 5. Summary of differences among median seed retention times, (A) among bird species within plant species, and (B) among plant species within bird species. Based on multisample median tests (Zar 1984:179-180) and subdivisions of the multisample contingency tables (Zar 1984: 69-70 ) A. plant species Phytolacca rivinoides Witheringia solanacea Witheringia coccoloboides B. bird species ** Phainoptila melanoxantha Myadestes melanops Semnornis frantzii p < 05 p < 005 Sf Sf Sf Pr Pr Pr comparisons ** > Mm = Pm ** Mm > Pm ** = Mm > Pm comparisons ** ** > We > Ws ** ** > We > Ws ** > We > Ws

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50 be about equally easily extracted from the pulp. In fact, P. rivinoides fruits are slightly smaller than those of either Witheringia species and have a more watery, amorphous pulp. It would seem that seeds would be most easily separated from this pulp yet retention times were consistently longer in P. rivinoides than in the two Witheringia species. Fruits of w. solanacea and~ coccoloboides may contain a compound with laxative properties, or perhaps P. rivinoides contains a compound having the opposite effect. Median passage times vary systematically among bird species as well For seeds of all three plant species, passage times are longer in Semnornis than in Phainoptila (Table 5). Median passage times in Myadestes were generally intermediate between those in Semnornis and Phainoptila, but were statistically indistinguishable from those of one or the other bird species for seeds of each plant. Several features of the seed retention distributions in Figure 8 are important to the relationship between gut passage times and the spatial patterns of seeds produced by an actively foraging bird. First, seeds ingested at one point in time do not emerge from the gut together; in these experiments, the last seeds emerged more than 75 minutes after the first-emerging seeds ingested at the same time. Second, the distributions of retention times are not symmetrical, but instead are skewed to the right. As a result, neither the length of time for the appearance of the first-voided seeds, pulp, or marker stain (e.g., Herrera 1984, Holthuijzen and Adkisson 1984, Sorensen 1984) nor the mean seed retention time (e.g. Walsberg 1975) is likely to provide complete information for inferring seed dispersal patterns. Third, although retention times are variable in all cases, the variation is

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51 greater in some bird spec i es than in others F o r example coefficients of va riati on for~ rivinoides passage times in Myadestes Semn o rnis, and Phainopti la were 44 5 35 9 and 9 2 respecti vely Clearly any inferences about the seed shadows produced by animals must be based on a cons iderati o n of the entire frequen cy dis tributi on of rete nt i o n ti m e s rather t han on a descriptive statistic ( e g ., mean, median mode etc ) der i ved from it Movement Patterns of Frugivorous Birds A t o tal of 195 .7 hours of data on movement patterns was collec t ed from 8 birds of three species. Tota\s for M y adestes m el anops, Phainoptila melanoxanthq, and Semnornis frantzii, respe c ti ve ly, w ere 4 individuals f or 96 .2 total hours, 3 individuals f o r 90.3 h o urs, and 1 individual f or 9 .3 hours. I also attached transmitte r s t o eight o t her individual Myadestes, o ne P hainop ti la and one Semnornis, but I was unable to collect enough data o n these birds to include here Transmitters fell o ff t wo of these birds le ss than one day after th e birds re lease In five other cases, the tagged indi v idua l moved out of the area before I could begin tracking it. These five individuals were non-territorial birds that foraged ov er ve ry large areas of the forest. The few hours of data collected from t wo o f these birds indicate that they did not move more r ap idl y through the forest t han those on well def ined home ranges; rather, th eir moveme nts were simpl y more l inear than those of other individuals of the same species which turned more of ten. Seeds d ispersed by a particular wid el y foraging bird are thus unl ike y t o tr avel much farther fr om their source t han t hos e j1spersed by birds w it h mo re rest ri cted home ranges

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52 Birds fitted with transmitters generally showed no adverse effects of carrying the 3.5 g package. Within 2 hours of release, most individuals had begun foraging actively and chasing territory intruders. Data from two individuals that did not adjust quickly to carrying the transmitter were not used in the analysis. Foraging behavior of the primarily frugivorous Myadestes, Phainoptila, and Semnornis resulted in very different movement patterns than those of primarily insectivorous birds. Whereas most insectivores seem to move through the forest almost continuously while feeding, the frugivores studied here punctuated brief episodes of rapid movement with relatively long stationary periods. Radio tracking data indicate that birds generall y spent 7 to 12 minutes in one location (Table 6), presumably consuming and processing fruits, and then moved rapidly to another location without feeding along the way. Not surprisingly, this pattern corresponds well with the patchy distribution of fruiting plants. In addition, the mean times between successive movements in Table 6 correspond closely with behavior I noted during feeding experiments with captive birds: after eating a number of fruits, most birds perched nearly motionless for approximately 10 minutes before moving about the cage in search of more fruit. The fact that data from remotely monitored birds correspond well with the behavior of closely observed individuals again suggests that the transmitters did not interfere with normal foraging activity. Movement patterns of radio-tracked birds did not suggest any tendency for gap-to-gap movement. Rather, birds seemed to travel rapidly between well-defined fruit sources, regardless of where they occurred. Locations to which birds returned frequently were always

PAGE 59

53 found to be large fruiting plants such as trees, rather than gaps. Furthermore, data from mist-net captures and analysis of fecal specimens suggest no tendency for preferrential foraging in gaps. First, none of the frugivore species was captured more frequently in gaps than in forest ( Table 1 ) Indeed, one species (Myadestes melanops) was captured significantly more often in forest (x 2 = 12.942, p < .001; expected values corrected for differences in sampling effort). Second, over 82% of the fecal specimens from mist-netted Myadestes, Phainoptila, and Semnornis contained seeds of canopy or subcanopy trees and epiphytes, suggesting that these birds concentrate much of their foraging outside gaps Thus, although these three bird species are the primary dispersers of the gap-dependent !'..:_ rivinoides, w. solanacea, and w. coccoloboides, there is no reason to suspect that they commonly transport seeds of any of these plants directly to other gaps in a non random fashion. Mean distances and time intervals between successive bird movements varied more among individuals of a given species than among species ( Table 6). This variation may reflect different densities of fruit sources within different birds' feeding ranges or between different seasons. Without collecting data from numerous individuals of each species throughout the year, it is impossible to identify sources of variation in movement patterns more precisely. Because variation among individuals within species was so high, data from each individual were weighted equally for purposes of estimating seed shadows. Individuals from wh ich I was able to collect more extensive data are thus not overrepresented in the analysis.

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Table 6. Movement data from individual frugivores fitted with radio transmitters. A) Descriptive statistics on number of foraging movements mean time interval between successive movements, A. B and mean distance per movement. Standard deviations in parentheses. B) Results of nested ANO V A on time intervals between movements in Myadestes melanops and Phainoptila melanoxantha. C) Results of nested ANOVA on mean distances moved by individual Myadestes and Phainoptila. Because movement data were co llected from only one Semnornis frantzii those data co uld not b e included in the ANOVAs D escriptive statistics recorded time interval (min) movement bird species individual movements between movements distance (meters) Myadestes melanops KN/rt 2 58 9. 1 (4 94) 106.9 (90. 67) KB/lt 21 7 2 (4. 58) 59.7 (64 29) BO /rt 1 58 1 0. 3 (6. 90) 51. 8 ( 37. 18) OG/lt 178 7.7 (7. 47) 16. 4 ( 17. 16) Phainoptila melanoxantha YY /r t 1 14 12. 0 (9. 54) 3 9. 1 ( 33 54) 00/rt 189 11. 5 (7. 05) 100 3 (85.01) OY/rt 80 8.7 ( 10. 98) 44 4 (40. 03) Semnornis frantzii YW/rt 45 9.8 (8. 78) 38 8 ( 26 28 ) Time intervals between successive movements sourc e df ss MS F among species 1 1064.8 10 6 4.8 4.48 (ns) within species 5 1189.5 237 9 4.43 (p < 001) error 991 53185.8 53.7 total 997 55440.1 55.6 V1 .i,.

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55 Table 6 -continued c. Movement distances source df ss MS F among species 1 7080 7080 0.029 ( ns) w ithin species 5 1236278 2472 5 6 60 101 ( p < 001) error 991 4076727 4114 total 997 5320085 5 336

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56 Estimation of Seed Shadows I estimated seed dispersal distances from data on bird movement patterns and seed passage times as follows. Each time a bird moved to a new location, I recorded the time and that location on a map of the study area. These data allow relatively precise measurement of the distances between all mapped locations and the time spent at each. By knowing the bird's distance from each location during eac h subsequent minute, and by combining these data f ram many such "initial" locations, I constructed a probability matrix of distance ver sus time. Thus, I computed the probability that a given bird will be at a distance of d meters from an initial location at time t. Multipl ying this matrix by the probabilit y distributions of seed passage times resulted in probability distributions of seed movement distances for all three plant species. This method assumes that an individual's behavior after leaving each initial location is not different from that after leaving a fruiting~ rivinoides, w. solanacea, or w. coccoloboides. Data from initial locati on s at which the bird spent more than 30 min were not used in the analysis, because they indicate non-foraging periods or long visits to plants with very large fruit crops, such as trees. The appendix demonstrates the use of this method to estimate seed shadows. The estimated seed shadows produced by the three bird species are shown in Figure 9. Those for Myadestes melanops and Phainoptila melanoxantha are very similar: only 20 36% of seeds are deposited wi thin 30 m of the parent plant, and some seeds may be moved up to 370 m by M y adestes and 510 m by Phainoptila. Estimated seed shadows for Semnornis frantzii are similar to those of the other two species in that the probability of seed deposition within 30 m of the parent is low (12

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Figure 9. Estimated seed shadows produced by Myadestes, Phainoptila, and Semnornis around individuals of Witheringia solanacea (W.s .), W. coccoloboides (W.c ), and Phytolacca rivinoides (P .r. ). Dots indicate probability of deposition less than 0.005.

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-------------z 0 ICl) 0 a.. w 0 5 8 2 ~Myadestes melanops W.s. F" 'I I I I I ..... W.c. p 07 I 2 ~Phainoptila melanoxantha W.s. = . -r .. P.r. = = .,.-, 2 ~Semnornis frantzii W.s. .n_ I 2~ W.c. n . 2~ P.r . c::Cb 0 100 200 3 00 c::, . 4 00 DISTANCE FROM ORIGIN (meters) 500

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59 25%) but the estimated maximum dispersal distance is only 220 m. This estimate is based on movement data from only o ne indi v idual, however and with a larger sample size the estimated extreme d ispersal distances might approach those of the other two species more clo sel y Mediation of Plant Reproductive Success by Birds A Model of P lant Reproductive Success Because germination success is a cont inu ous function of both gap size and gap age suitable colonization sites are not discrete recognizable units, even for the gap dependent-plants studied here As a result, evaluating the effect of different s eed shadows, temporal fruiting patterns, and seed dormancy cha racteri st i cs on plant reproductive success is complex. F or example we cannot simply determine the probability w ith wh i ch seeds fall into gaps of a part i cular size or age, and a sssume that they will have encountered safe sites. I n order to compare the reproductive consequences of different seed shadows, phenological patterns, and dormancy capabilities then, I designed a compute r s imulati on model that estimates the potential maximum lifetime reproductive success of indi vidual plants Parameters of the model include the phenology of fruiting and gap formation, the seed shadows produced by an imals, the relationships of germination success to gap size and age, and the density of and a rea occupied by gaps in various size categories Based o n either an empirically deri v ed or hypothetical seed shado w the mode l first computes the density of seeds in ea ch o f a series of concentr i c dis t ance interv al s away fr om t he parent ? l ant Densit i es are incremente d monthly a cc ording t o the o bser v ed f ruit ing phenology and

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60 seed dormancy cap abilities of each species. Us i ng data on ob served gap -size d i s tri but i o ns a n d rates of canopy disturbance the model then dete rmines for each distance interval the amo unt o f la nd area occup i ed b y gaps in each of 16 gap size categories. Ga p s a re "f ormed acco rdin g to the estimated phenology at Monteverde. The number of seeds potentially germinating in each distance interva l equals t he dens it y of seeds in that inter v al ( at that time ) ti mes the area in g aps that size, summed over all 16 gap size categories. Within this opera ti on a similar one based upon the relationship between gap age and germination success takes place. Because a relatively small number o f seeds can survive to reproduce in an y one gap another function limits the t o tal number of offspring in gaps of various sizes t o the maximum nu mb er observed in gaps of t h at size in the field. For P. rivinoides this number va ried from zero in gap s smaller than 10 m 2 to four in the largest gaps F o r both w. solanacea and w. coccoloboides, the maximum number varied from one to fi v e. The model can be stated mathematically as ( 1 ) wh er e RO is poten ti al l if e tim e re p r oductive ou t put SN is the nu mber l, m o f seeds in distance interva l i during man h m GSJ 1s tr 1 e r opo rti un o f land area i n gaps of size ca tegory j, P Sj is the probability of

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61 germination in gaps of size category j, GAk is t he p r oport i o n of g aps ,m o f age k ( in months) during month m, PAk is the p r ob abilit y o f ge rminati o n in gaps of age k, GN is th e number of gaps of size l_ I] category j in distance inter va l i, MXj is the maximum number of seeds t h at can survive to maturity in gaps o f size category j, and GFm is the proportion of gaps (o ut of those formed in o ne yea r ) occ urring during month m. Here I distinguish reproductive ou tput", wh ich I def ine as the total number of offspring produced during an individual s lifetime, from relative fitness, which depends up o n the age-specific schedu le of reproduction ( see below) Note that the model estimates potential lifetime reproductive output only; although it limits the number of germinated seeds that survive in any one gap ( si m ulating competition with siblings), it does not include any other sources of mortality, e.g., predators, pathogens, or accidents su ch as treefalls. RO as used here is thus not exactly equivalent to the net reproductive rate, R 0 Although a Monte Carlo simulation using a stochastic model might y iel d more realistic results, the deterministic model is more suitable for the present purpose due to its relative simplicity and to the fact that with a large number of runs, results from a stochastic model should converge on those from the deterministic o ne. Dis p ersal Effe cts o n Reproducti ve Output ( RO ) Assuming No Seed Dormanc y To evaluate the reproductive consequences of disp ersal by Myadestes, Phain optila and Semnornis I first r an the model desc ri bed above fo u r times for each plant spe c i es ; o nce w it h each of the seed shadows in F iqure 9 an d a four th ti me using a seed shacio1, in v1h i ch all seeds are depos it ed w ithin 10 m o f the parent plant This last r un t hu s

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62 approximates the case of no dispersal, or the fate of most seeds re moved by tanagers and finches Other parameters of the model were the sam e f o r each run o n a particular species, and were taken from data collected at Monteverde. The relationships between ge r minat i o n suc c ess and gap size are the adjusted regressions given previously. Relationships between gap age and germination success were interpolated from t h e lines connecting ob served mean values in Figure 2 The availability of gaps of different sizes was estimated directly from data on the canopy disturbance rate and adjusted gap size distribution Fruiting and gap formation phenologies were those shown in Figures 10 and 11 Yearly seed crops, estimated by multiplying the mean number of seeds per fruit by the median yea rly fruit crop sizes for each species, were 8 ,345, 13,061, and 44,180 for w. solanacea, w. coccoloboides, and P. rivinoides, respectively Because both Witheringia species produce t wo fruit crops per yea r, crop sizes used here were yearly medians, rather than the seasonal medians reported above. The number of reproductive seasons was assumed to be that estimated for plants at Monteverde: one in P. rivinoides, and five in W. solanacea and w. coccoloboides. Estimates of total lifetime reproducti v e output (a ssuming no seed dormancy) using the four seed shadows are shown in Figure 12. For each plant species, the advantage of dispersal by any of the three legitimate dispersers is obvious Within 10 m of the parent plan t, very fe w suitable germination sites are available and density-dependent m o rtality amon g seedlings w ithin them is high. Seed shadows produced by Semnornis Ph ainoptila and M ya deste s result i n much highe r estima t es of re productive ou tput because seeds are distributed over a g r ea ter number of suit able pa t ches H ow e ve r, t hese estimates are for seeds that are

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Figure 10. Fruiting phenology of~ rivinoides, solanacea, and W. coccoloboides at Monteverde. given are for the "average" individual of each species (see text). Values

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0.5 0.. 0 4 0 0: 0 0 3 l:::> 0: 0 2 u. ...J 0:
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65 u. 0.3 0 Cl w z 0 C: 0 2 I0 C: LL 0 Cl) 0.1 a. a. 0 < n a: C, a. A s 0 N 0 J F M A M J J MONTH F ig u re 11 Estima t ed phenology of gap forma t ion a t Mon t everd e. Val u es g i ven are the proport i ons of all gaps formed in a particular year that occur each month.

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Figure 12. Estimated lifetime reproductive output (RO; assuming no seed dormancy) of plants re c eiving all dispersal service from Semnornis (S.f .) Phainoptila (P.m.), Myadestes (M.m), or having all seeds deposited within 10 m of the parent (0).

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0 CX) 0 cc 6 7 I I 0 C\I Cl) e (1) :e "0 -0 .Q e 0 Q. 0 ...: (.) (.) 0 (.) 0 :ii:: e :e (1) (,) e C: ...: 0 Cl) :ii:: 0 e :e Cl) (1) e "0 -0 C: -...: :::. -... Q.. 0 0

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68 dispersed t o sites currently suitable f o r ge r m inati on a nd thus ge rmi nate in t he same m o nth the y a r e d is pe r sed These e sti ma t es do not in c lude la ter repr oduc tion fr om dormant seeds that g ermina te aft e r a new canopy gap occurs overhead. Yet seeds of P. ri v i noides w solanacea, and w. coccoloboides exhibit "enforced" seed dormancy ( sensu Harper 1977) and are capable of remaining dormant in the s o il for at l eas t 2 5 y ears with no detectable decrease in v iabi l it y and probably for much longer ( Fig. 4) Reproductive Consequences of Seed Dor mancy Effects on reproductive output (RO). Because plant reproductive success should be enhanced by enforced seed dormancy, I repeated the four model runs for each species, this time allo w ing an y ungerminated seeds to remain dormant for maximum periods of 2, 5 1 0 20 and 40 ye ars. Not surprisingly, pote ntial repr o ducti v e output in c reas es dramatically with increased dormancy capab i lities of seeds ( Fi g 13} F or example, plants whose seeds are capable of remaining dormant f o r just t wo years can potentially produce 11 to 31 times as many offspring as plants whose seeds die if they are not dispersed directly to sites immediately suitable for germination. If seeds can remain dormant f or up to 40 years, up to 611 times as many offspring may be pro du ced Even mo re interesting, however is the fact that t h e relati v e d i fferences in estimated repr od u c tive output usin g different se ed shadows a re g reat ly magnified wh en we also consider repr o du ct ion fr om dorman t seeds. Th us fo r P. ri v i no i des, dispersal by Myadest e s r e su l ts in only a 4% in c r ease i n RO ov er dis pe r s a l b y S em nornis c ons i d e ri ng o n l y th e s e se e d s encoun t er i ng cu rr en t ly suitab le sites when dispersed ( Fi g 12 )

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Figure 13. Estimated lifetime reproductive ouptut (RO) vs. seed dormancy capability, for plants receiving all dispersal service from Semnornis (S.f.), Phainoptila (P. m.), Myadestes (M.m.), or having all seeds deposited within 10 m of the parent (none).

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--------------70 10 8 WITHERING/A SOLANACEA 6 4 2 0 none 0 0 0 12 )( 0 10 WITHERING/A COCCOLOBOIDES a: I:::, a. I8 :::, 0 w > 6 j:: (.) :::, C 0 a: 4 a. w a: 2 non 0 6 PHYTOLACCA RIVINOIDES 4 2 non o~r:::.;.----...... -----...... -------------, 0 2 5 10 20 40 MAXIMUM SEED DORMANCY CAPABILITY (years)

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71 However, if we also c o nsider seeds that can remai n d o rmant in the so i l fo r up t o t wo ye ars until a g ap i s fo r m ed ove r h e ad d i spe rsa l by Myadestes confers a 54 % increase o ver dispersal by Semn o r n is ( Fi g 1 3 ) Furthermore, if seeds can remain dormant f o r eve n l o n g er peri o ds, t h ese differences become even larger. Effects on relative fitness. Although Fi gure 13 clearly sh o ws that the total number of potential offspring is greatl y increased b y seed dormancy it gives a misleading impression of the influence of seed dormancy on relative fitness The estimator of reproducti v e output computed by equation 1 is most useful for plants without overlapping generations or age-structured populations, e.g., monocarpic plants without seed dormancy In such plants, RO will be an unbiased estimat o r of relative "fitness", and compa ris ons among treatments ( e g ., differ e nt seed shadows) yield unbiased information about the fitness consequences of the different treatments. If fe c undity and / or survival are age dependent, however, the total number of offspring produced by an individual is not an unbiased estimator of relative fitness, because seeds produced later in life, or those that germinate after a l o ng period of dormancy, contribute l ess to the population gene pool than those germinating earlier. Fecundity, at leas t, is age-dependent in all three species considered here. Both W. solanacea and W. cocco lo boides t y pical ly produce seeds for five o r m o re y ears More import a ntly, a l l three species dem o nstrate th e capacity f o r enf o rced seed d o r m an cy wh ic h h as t h e e ffe c t o f greatl y increasin g t h e p arent pl ant's repr od u c ti ve l i fe s p an. Ther efo re, I c o m p uted a l e ss b ia se d e s t i ma t or o f rela ti ve fitness b y s ol v i ng f o r r the equati o n

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72 YP+YD 1 = L (2) x=O where lx is the probability of seed survival in the soil for x years, and mx is the number of seeds germinating in year x. This equation is commonly used to compute the exact value of the intrinsic rate of natural increase of a population. Here, r is not the intrinsic rate of natural increase, but an estimator of relative fitness that discounts the contribution of offspring produced later in the parent's life relative to that of those produced earlier. The parent plant germinates in year O, and x can take on values from Oto YP + YD, where YP is the last year of seed production and YD is the maximum number of years that seeds can remain dormant. Survival of ungerminated seeds (lx) was assumed to equal 1.0 for all years up to the maximum dormancy period, followed by complete mortality. Values of mx were the yearly estimates of seeds germinating generated by the model, which summed to the value for RO given in Fig. 13. The age at first reproduction and number of years of seed production were those estimated for plants at Monteverde. In P. rivinoides, all seed production occurs in year 1 (plants between 1 and 2 years of age). In the two Witheringia species, seed production was assumed to begin at age 3 and continue for 5 years Estimates of relative fitness based on equation 2 are shown in Figure 14. The figure shows that seed dormancy indeed greatly enhances plant fitness, but that most of this enhancement is due to short-term, rather than long-term dormancy. Dormancy capability of more than two years does little to increase the value of r. Thus, the increase in

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Figure 14. Estimated relative "fitness" (r; see text) vs. seed dormancy capability ,for plants receiving all dispersal service from Semnornis (S.f.), Phainoptila (P.m.), Myadestes (M.m.), or having all seeds deposited within 10 m of the parent (none).

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74 2 WITHERING/A SOLANA CEA M.m., P.m. S.f. none 0-+---r---r---...----------.----------------. 2 WITHERING/A COCCOLOBOIDES M.m., P.m. S f. 1 none en 0 en w z ILL w 5 PHYTOLACCA RIV/NO/DES > M m., P.m. I< 4 ..J S.f. w cc 3 2 none 0 -1 -2 ....... ----------------.----------------. 0 2 5 10 20 40 MAXIMUM SEED DORMANCY CAPABILITY (years)

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75 fitness with increasing dormancy capability is not monotonically increasing and linear, as suggested by Fig. 13, but is in fact asymptotic. Reproductive Consequences of Fruiting Phenology Fruit ripening in all three plant species is concentrated in the wet season, although some fruits may be found at any time of the year (Fig. 10). In.!::._ rivinoides, a single well-defined peak occurs early in the wet season, with 91% of all fruits ripening from April through June. In both w. solanacea and W. coccoloboides, two distinct ripening peaks occur in the wet season: one early (May-June), and one late (November Januar y) These distinct peaks were not due to individual plants within each population ripening at different times; nearly all individuals of each species produced two separate fruit crops each year, although these were not usually of the same size. Fruiting in w. solanacea was somewhat less seasonal than in W. coccoloboides. Although peak ripening periods in both species coincided, the May-June and November-January peaks accounted for a greater proportion of the total fruit crop in w. coccoloboides than in w. solanacea. More importantly, the major ripening peak in W. coccoloboides was in the early wet season, while that in w. solanacea was in the late wet season. Because the major disperser for all three plant species, Myadestes melanops, is essentially absent from the Monteverde area from late October through December (Fig. 1), we might expect fruit removal rates to be depressed during the late wet season fruiting peak. To test the hypothesis that daily fruit removal rates are correlated with seasonal

PAGE 82

76 patterns of Myadestes abundance, I examined the relationship between Myadestes capture rate and daily fruit removal rate from May 1982 through April 1983. Daily fruit removal rate was computed as the proportion of marked ripe fruits on all plants that were removed. Because daily fruit removal rate is negatively correlated with the size of the fruit crop (Murray, in press), I computed partial correlations of removal rate with the monthly Myadestes capture rate, holding crop size constant. In all three plant species, a significant partial correlation existed between Myadestes capture rate and daily fruit removal rate. Coefficients for P. rivinoides, W. solanacea, and w. coccoloboides were 0.74 ( P < .02 ) 0 66 ( P < .05), and 0.69 (P < .05 ) respectively. T hus individual plants that ripen fruits during the season when Myadestes is absent should have, on average, lower reproductive success than those ripening fruits at other times. Because the availability of suitable germination sites varies over the year ( Fig. 7), plant reproducti ve success may be affected by seasonal fruiting patterns for reasons other than variation in fruit removal rate. To estimate the relative importance of this selecti ve pressure on fruiting phenology, I compared the potential lifetime reproductive output of individuals that peak ripening in February, April, June, August, October, and December. For each plant species, I ran the simulation model described above six times, each time shifting the fruiting phenology curve temporally with respect to the estimated phenology of gap formation. For all runs, I used the estimated seed shadow produced by Myadestes, and allowed ungerminated seeds to remain

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77 dormant for two years. All other model parameters were the same for all runs on each species, as outlined above. Somewhat surprisingly, estimates of reproductive output were very similar for plants that fruit at different times of year (Fig. 15): the highest estimates for each species are only 1% to 13% higher than the lowest estimates. Two factors account for this result First, because treefall gaps sometimes remain open for germination for up to a year after formation, the temporal availability of suitable habitat patches is actually somewhat more constant than the highly seasonal nature of gap formation would suggest (e.g Fig. 7). Second, and more importantly, enforced seed dormancy greatly reduces temporal variation in the number of seeds available for colonization of newly formed gaps. Even though fruit ripening is highly seasonal, the effective pool of seeds from a given parent remains much more constant over time. Had the estimates in Figure 15 been determined for plants with no seed dormancy capability, variation in reproductive output of plants that peak fruiting at different times would have been much greater.

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Figure 15. Estimated lifetime reproductive output (RO) of plants that peak fruit ripening at different times of year (see text). All estimates assume a maximum seed dormancy capability of two years, and all dispersal service from Myadestes melanops.

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0 a: '""' ::, a.. ::, 0 UJ > 1(.) :::, Cl 200 800 600 400 200 7 9 PHYTOLA CCA RIV/NO/DES WITHERING/A SOLANACEA . . 0 1 ooo WITHERING/A COCCOLOBOIDES a: ----a. UJ 800 a: 600. 400 200 J F M A M J J A S O N D MONTH OF PEAK FRUITING

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DISCUSSION Data presented here demonstrate that determining the consequences of seed dispersal ("dispersal quality", sensu Mc Key 1975) by different bird species is exceedingly difficult. Animal dispersers may influence plant reproductive success in three ways. First, animals may differ in the likelihood with which they ingest seeds of the fruits they remove from plants ("fruit handling"). Second, animals may differ in the chemical or mechanical effects exerted on seeds that are ingested ("seed treatment in the gut"). Third, animals can affect plant reproductive success through the seed shadows they produce, via colonization of patchily distributed microhabitats or escape from high density-dependent mortality near the parent plant. Effects of Fruit Handling and Gut Treatment Avian consumers of P. rivinoides, w. solanacea, and W. coccoloboides fruits differ in the "quality" of dispersal service they provide in all three of the above ways. Whereas Myadestes melanops, Phainoptila melanoxantha, and Semnornis frantzii invariably ingested fruits of these plants whole and ingested all of the seeds, the two tanagers (Chlorospingus opthalmicus and Tangara dowii) and the finch (Pselliophorus tibialis) discarded many or most seeds before swallowing the fruit pulp. Similar fruit-handling behavior in tanagers and finches has also been noted by several other investigators (Snow and Snow 1971, Moermond 1983, Moermond and Denslow 1985, Levey 1986). As with the 80

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81 species considered here, Levey (1986) also found that the probability of seed ingestion by tanagers and finches was inversely correlated with seed size within bird species, and positively correlated with seed size among bird species. Clearly, such differences in the ways that different birds handle fruits may result in different reproductive consequences to plants In general, tanagers and finches are less likely to ingest seeds of any size than are birds that swallow fruits whole I nstead, most seeds wil l be dropped directly beneath the parent plant where they may be subject to high density-dependent mortality (e.g, Wilson and Janzen 1972, Howe and Primack 1975, Janzen et al. 1976, Platt 1976, Salmonson 1978, Clark and Clark 1981, Lemen 1981, Augspurger 1983a,b, 1984a,b, Howe et al. 1985). In addition, the lack of gut treatment may retard germination in such seeds (see below). Thus, not only does fruit size limit the number of potential consumer species for a given plant (e.g., Diamond 1973, Snow 1973, Moermond and Denslow 1985, Wheelwright 1985a), seed size may also impose constraints on the quality of d i spersal ser v ice rendered by those animals that actually consume fruits. Reproductive consequences of fruit removal by different birds may also vary due to different treatment effects of gut passage. Among the bird species considered here, all except the finch~ tibialis passed all ingested seeds intact (Table 2). Furthermore germination success of these seeds (Table 3) did not differ from that of seeds carefully removed from fruits by hand (test for equality of percentages, Sokal and Rohlf 1969 : 608 ; P > 0 .3 for all comparisons). In contrast, the one P. tibialis tested destroyed 98% of thew. solanacea seeds it ingested, and the remaining 2 % that emerged intact were inviable. The implications of

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82 these differences in gut treatment effects for plant reproductive success are obvious: seeds ingested by E.:_ tibialis are likely to be destroyed hence these finches (but not all finches; e.g. see Jenkins 1969, Levey 1986) like most parrots (e g., Forshaw 1978, Janzen 1981) and many doves (Snow 1971, Moermond and Denslow 1985), act primarily as seed predators. Although gut treatment in some animals may have negative effects on germination, the opposite is often true Germination success of many plant species is enhanced by gut treatment (Krefting and Rowe 1949, Rick and Bowman 1961, Olson and Blum 1968, Hlad i k and Hladik 1969, Nobel 1975, McDiarmid et al. 1977, Applegate et al. 1979, Lieberman et al. 1979, Fleming and Heithaus 1981, Glyphis et al 1981), and is even absolutely required by some (e.g Calvaria major; Temple 1977). In addition, gut passage may affect germination in ways more subtle than merely altering the proportion of seeds that eventually germinate Data on germination rates of seeds with and without gut treatment (Table 3) indicate that in all cases except one (~ solanacea passed by Phainoptila), seeds processed through bird guts germinated more rapidly than those receiving no gut treatment. Similar results were obtained by Hladik and Hladik (1969) for seeds of some, but not all, plant species passed by monkeys. This response may be due to mild chemical and mechanical abrasion of the seed coat, facilitating perception of germination cues (e.g., light) and/or water imbibition. Whatever the mechanism, rapidly germinating seeds may enjoy a competitive advantage over those that take longer, especially among seedlings of rapidly growing pioneer species. Patches of soil disturbed by uprooting trees commonly contain more than 100 seedlings of P rivinoides alone within

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83 one m o nth, yet only o ne t o three of these will s ur v i ve t o m aturity ( K G. Murra y personal o bser va ti o n ) In the face of such compet iti on even subtle tr e atm en t effe c ts o n germination rate may have important fitness consequences. While the data on germinati o n rates shown in Tab le 3 are for seeds treated by a single indi vidua l o f each bird species, and therefore do not allow statistical co mparis o ns between bird species, the data suggest that gut treatment by some species (e g ., Semnornis) may result in more rapid germination than that resulting from treatment by other species. Effects of Dispersal Seed Shadows Variation among the "seed shadows" produced by different birds can a ls o produce differences in the quality of dispersal ser v ice rendered. The seed shadow estimates presented in Fi g. 9 are, to my knowledge, t he first such estimates for free-ranging birds in a natural h abitat. Although estimates of the "seed rain" produced over the landscape by frugivorous animals are available from seed trapping studies and assesments of soil seed banks (e g., Burtt 1929, Smythe 1970, Gue v arra and Gomez-Pompa 1972, Foster 1 973 Smith 1975 Vazquez-Yanes et al. 1975 Brunner et al. 1976, Li ebe rman et al. 1979 Th omp son 1980 Bullock 1978 Janzen 1978) neither the sources of seeds sampl ed n or the identit y o f th e ir dispersers is genera lly known Thus, measures of t he seed rain within a forest tell us n o thi ng a b o ut the s eed shadows p r oduced by pa rticular disperser specie s around individual plants In cont rast the method s used in this scudy do allow esci ma ti on o r ind i v i dua l plant seed shadows albeit indirectly F urthermore t he

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--------------------------84 techniques are applicable to a wide variety of dispersal agents and habitats, and yield much additional information on temporal patterns of foraging, home range size, and digestive phys i ology of particular disperser species. The estimated seed shadows in Figure 9 are remarkable in several respects. First, they are not, as is sometimes suggested (e.g., Harper 1977, Levin 1979, Fleming and Heithaus 1981), highly leptokurtic, with the great majority of seeds being deposited within a few meters of the parent plant. Instead, a large proportion of seeds may be moved for considerable distances Median dispersal distances vary from 35 to 60 meters among the 9 bird species/plant species combinations, and maximum dispersal distances exceed 500 meters. Second, the range of estimated dispersal distances presented here exceeds that suggested for most other bird-dispersed plants. Longer dispersal distances have been suggested for seeds cached by Clark's Nutcrackers (Vander Wall and Balda 1977) and for some species dispersed by bats (e.g., Janzen et al. 1976, Fleming 1 9 81), however. Dispersal distances of 70 m, 2 5 m, and "up to several hundreds of meters" were suggested for seeds of Casearea nitida (Howe and Primack 1975), Prunus mahaleb (Herrera and Jordana 1 9 81), and Virola surinamensis (Howe and Vande Kerchove 1981), respectively. These authors' estimates, however, were based on relatively few visual observations of birds leaving fruiting trees. Because only short bird movements could be observed, their data may be biased in favor of short distances This bias notwithstanding, it is unlikely that the large (5 to 20 mm) seeds of the trees studied by Howe and Primack ( 1975), Herrera and Jordano (1981), and Howe and Vande Kerchove (1981) are dispersed as far as the much smaller (ca. 1-3 mm) seeds of P. rivinoides, w.

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8 5 solanacea, and W coccoloboides. Large seeds are vo i ded more rapidly by birds (o ften by regurgitati o n; Leve y 1986 and pe r sonal o bservation), and the l a rg e fruit crops produced by trees encourage more sedentary behavior by frugivores (Pratt and Stiles 1983 ) Thus small seeds are probably dispersed farther, on the average, than large o nes, especial ly when produced by plants with small fruit crops that do not encourage long or frequently repeated visits by indi vidual fru g i vo res. Do the data suggest any tendency for non-rand om o r d ir ec ted dispersal" ( sensu Howe and Smallwood 1982) of seeds t o gaps? Direct dispersal to gaps has been suggested by the common observations (e.g ., Bl ake and Hoppes 1986, D. Leve y personal communication) that (1) herb and shrub-layer fruit resources are often more concentrated within g aps than in surrounding forest understor y and that (2) mist net captur e s of frugivorous birds often reflect this concen trati on. At Monteverde, h ow ever, none of the bird species for which I have adequate data was captured most freq uent ly in gaps ( Table 1 ) In fact, the maj or understory frugivore at Monteverde, Myadestes melanops, was captured significantly less often in gaps than in forest understory. Furthermore, data from individual birds fitted with transmitters suggest no tendency for non-random gap-to-gap movement. The lack of any preference for gaps in Myadestes, P h ain op tila, and Semnornis reflects the fact that their fruit res o ur c es a re n ot h i ghly co nce n trated there. Individuals of t he se species f o ra ge from the l owest levels of the forest under s t ory to sub canop y and even ca no py le v e l s ( K. G. Murray personal obs er vat i on) In fact mo st o f t h e fec al s p eci m ens f r om c a p t u r ed i n di v idua l s co ntai n e d s ee ds of canopy and subcano~y trees and epiphytes Alth o ugh fr ui t reso u rces w ithin a f e w mete rs of t h e

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86 ground may be more concentrated in gaps at Monteverde as in other forests (Blake and Hoppes 1986, D. Levey, personal communication), fruits used b y Myadestes, Phainoptila, and Semnornis are not concentrated in gaps if the entire vertical f o raging ranges of birds are considered Distribution of "Safe Sites" Although dispersal may result in decreased density-dependent mortalit y of seeds and seedlings near the parent plant, the advantage of dispersal for gap -d ependent plants more likely results from two other factors: (1) an increased probabilit y of encountering spatially and temporall y un p redictable habitat patches ( i.e., treefall gaps), and (2) reduced density-dependent mortality within those patches. Tropical forests are often characterized as mosaics of mature-phase and gap-phase patches that differ in size, intensity of disturbance, and time elapsed since last disturbance ( Richards 1952, Richards and Williamson 1975 Whitmore 1975 1 978 1982, Oldeman 1978, Harts horn 1978, 1980 Hladi k 1 982, Brokaw 1985). The Mont ev erde cloud forest also represents such a disturbance mosaic Approximately 1.5% of the total land area at Monteverde is subjected to canopy disturbances each year, and the average density of new gaps (including even those as small as 1. 6 m 2 ) over the landscape is appro x imatel y 1 7 .5 per hectare per year. The 1.5 % per year canopy disturbance rate reported here is similar t o that rep o rted for "elfin" forest al o ng the continental divide at Monte verde (1.1 % ; La w t on and Putz, unpublished ms), as w e ll as for other tropical forests (Leigh 1975, Hartshorn 1 978 Brokaw 1982a, Foster and Br okaw 1982, Uhl 1982) and many temperate o nes (H einselman 1973 Abrell

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87 and Jackson 1977, Runkle 1982, Zackrisson 1977, Naka 1982, Platt et al. unpublished ms). Furthermore, the gap size distribution at Monteverde (Fig. 5) is similar to that determined for several other tropical and temperate forests (Runkle 1 9 79, Brokaw 1982b, Lawton and Putz, unpublished ms). For seeds of gap dependent plants, then, suitable patches for colonization are similarly rare in most forests. Detailed analyses of the germination requirements of P. rivinoides, Witheringia solanacea, and W. coccoloboides show that the landscape is even more complex than just a mosaic of "safe sites" (sensu Harper 1977) surrounded by unsuitable habitat. For each gap in the forest, there is an associated probability of germination for seeds of gap-dependent p 1 an ts w h i c h depends u po n i ts s i z e and age ( e g. Figs 2 and 3 ) Furthermore, the suitability of a given gap differs among the three species studied here, and probably for other species as well. For plants such as these, it is more useful to think of the forest not as discrete patches of suitable habitat embedded in a matrix of hostile en v ir o nment, but rather as a mosaic of patches of different sizes and ages, each of which has an associated suitability for seeds of particular gap-dependent plants. At any point in time, the great majority of land area (~98.5% for these three species) consists of patches in which the probability of germination and establishment is negligible, and the remainder of the land area is occupied by patches of varying, but higher suitability. Reproducti v e C o nsequences o f Dispersal and Dormancy Because the germination requirements of gap-dependent plants are complex, determining the reproductive consequences of seed shadows

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88 produced by birds is exceedingly difficult. Results presented here clearly demonstrate that seed dispersal increases both reproductive output and relative "fitness of gap-dependent plants. However, the underlying cause of these increases has less to do with the number of seeds encountering suitable gaps than with the number of individual gaps they encounter Assuming that gaps are formed randomly in space, any location has an equal probability of being within a gap. Consequently, the probability that a given seed will encounter a gap does not depend upon the distance it is dispersed A major advantage of dispersal for gap-dependent plants is that it serves to spread seeds over a greater number of gaps, so that each germinating seed is faced with fewer potential competitors (i.e., siblings). Thus, even though seeds of these plants can germinate only in ephemeral habitat patches that occur unpredictably in space, one of the primary advantages of seed dispersal lies in avoiding density-dependent mortality within patches near the parent plant. This does not mean that avoidance of density-dependent mortality is the o nly advantage of dispersal in these plants, however. On a v erage, widely dispersed seeds will encounter suitable germination sites after shorter periods of dormancy, and thus contribute more to the population gene pool, than those deposited closer to the parent plant. As a result, more extensive dispersal increa s es relative "fitness" (but not reproductive output) for reasons unrelated to density-dependent mortality. Results presented for these gap-dependent plants therefore support both the "escape" and "colonization" hypotheses proposed by Howe and Estabr oo k (197 7). The ability of seeds to remain dormant in the soil for long periods does not preclude the necessity for effective seed dispersal. Because

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--------------89 undispersed dormant seeds could sur v i ve unti l t h e ne xt ca n o py disturban c e o ccurs o n a p arti c ul a r s it e it m i g ht be a r gu ed t ha t dispersal is unimportant if seeds remain v iab le suffi c i e nt ly lo ng, a nd if mortality in the soil is low Ne v erthe l ess, m o re eff e cti v e dis p ersa l mechanisms will always be favored; plants that disperse seeds al w ays have higher reproductive success than those w ithout dispersal, regardless of dormancy capability (Figs 13 and 14) Three factors account for this result. First, because the probability of germination in the gap of origin is negligible by the time a parent plant produces seeds ( Fig. 3 ) the next germination opportunity for seeds deposited there will occur when the next disturbance occurs on that site. The 1.5 % per year canopy disturbance rate at Monteverde suggests a "turnover rate" ( i.e., the "mean time between successive creations of gap area at any one point in the forest" ; Brokaw 1985) of 6 7 years. Thus, undispersed seeds of a gapdependent plant should encounter new treefall g aps only once e v er y 6 7 y ears, on the average. By dispersing its seeds, a plant greatl y increases the number of suitable patches encountered by its seeds at an y point in time (cf. Green 1983, Geritz et al. 1984). Second, because seeds germinating after a long period of dormancy con t ribute less to the population gene pool than those that germinate soon after dispersal, plant "fitness" is always increased by me c hanisms ( e g ., dispersal ) that p r o m o te earlier encounter of suitabl e pat c h e s. Thir d int e ns e d ensit y dependent m o rta l it y ( due t o intraspecifi c compe titi o n an d / o r p r e d a ti on ) amo n g seeds depo sited v ery near t h e p ar e nt s hould always f a vor mo r e effect i ve d i spersal regardless o f when seeds g er~in a ce Thus a l ho u yh enfo r ced s ee d d o r m a ncy g r ea tl y in c r eases rep r oduc ti ve s u cce s s o f g ap

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9 0 dependent plants it can in no way be thought of as a subst itute" for effective dispersal. Although none of the birds considered here is likel y to transport seeds directly to gaps, the quality of dispersal service pr ov ided by different bird species to gap-dependent plants may v ary considerably as a function of the seed shadows they produce The degree to which different seed shadows are selectively advantageous depends upon how we estimate relative plant fitness. On the one hand, the model described by equation 1 predicts that the number of seeds potentially germinating during the month dispersed (RO assuming no seed dormancy ) is quite similar following dispersal by Semnornis, Phainoptila, or Myadestes ( Fi g 12). When reproduction from dormant seeds is also considered, however, differences between effects of dispersal by different birds on lifetime reproductive output are greatly accentuated ( e g ., Figure 13) In fact, Fig. 13 shows that the number of offspring produced is a monotonically increasing linear function of dormancy, at least ove r most of the range of dormancy capability. This result suggests that ( 1) a given increment in the capacity for seed dormancy always has the same selective advantage, and (2) differences in the selective advantages of different seed shadows are greatly magnified by increasing seed dormancy capability If seeds can remain dormant for just two yea rs, for example, the increment to lifetime reproductive o utput resulting from dispersal by Semnornis is only 65-85% as great as that resulting from dispersal by Myadestes or Phainopti la and these differences are further acc entuated if seeds ca n remain dormant for even longe r pe ri ods o f ti me Thus even small increa ses in mean or extreme d is ~ersa d i scances mighc

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91 result in substantial differences in lifetime reproductive success for plants that exhibit enforced seed dormancy. In contrast, if we user (equation 2) as an estimator of fitness, the effect of dormanc y is less pronounced. Because seeds germinating after a long period of dormancy contribute less to plant fitness than those germinating sooner, r is greatly increased by the ability of seeds to remain dormant for a few years, but is increased only slightly by further increases in dormancy capability (Fig. 14). This result suggests that (1) seed dormancy beyond a few years may have no selective value, (2) differences among the fitness increments associated with different seed shadows are not as great as is suggested by comparison of the total numbers of offspring produced and (3) these differences do not increase appreciably with increasing dormancy capability As used here, however, equation 2 also has important sources of bias. For example, the value of r is especially sensitive to the magnitudes of values for lx and mx. When values of mx are large, estimates of r reach an asymptote quickly as x increases. When values of mx are lower, but still retain the same proportional relationships to one another, v alues for r do not reach an asymptote until much higher values of x. This property of equation 2 is very important for its use as a fitness estimator here. Because the simulation model used to generate mx values does not consider most sources of preor post germination mortality, the mx values estimated are artificially high. If we choose more realistic values for mx while retaining the same proportional relati on ships between them (e.g., by multiplying each v alue by 0.001), r increases appreciably over much more of the range of values of x. In addition, differences among the increments in r associated

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92 with different seed shadows are larger, and become even larger as dormancy capability increases. Because solutions for r in equation 2 are highly sensitive to the magnitude of values of mx' and because I lack information on exact values, Figure 14 conservatively estimates the influence of both seed dormancy and different seed shadows on plant fitness. On the other hand, estimates of lifetime reproductive output derived from equation 1 (Fig. 13) present an inflated estimate of the influence of these factors on plant fitness. Thus, neither approach yields an unbiased estimator of fitness and the real effects of dispersal and dormancy on plant fitness lie somewhere between the extremes presented here. Thus, (1) seed dormancy does increase plant fitness ( to an unknown degree) over a wide range of dormancy capabilities, but especially over the short term. (2) Because seeds germinating soon after dispersal contribute more to plant fitness than those germinating later, dispersal by bird species whose seed shadows result in a greater probability of deposition in currently (or imminently) suitable sites confers a large fitness advantage on the parent. (3) Increasing dormancy capability magnifies (also to an unknown degree) differences between the fitness increments associated with different seed shadows, such that relatively minor differences between seed shadows may result in important differences in the increments to plant fitness associated with each. Limitations of the Model Results of the model runs for reproductive success presented in Figs 12-15 should be interpreted with some caution. All values of reproductive success computed by the model are maximum possible values,

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93 for several reasons. First, my measures of the proportion of land area in gaps of different sizes probably overestimate the proportion of land area actually available for colonization. I measured germination success with respect to gap size at the approximate center of each gap, above any herb layer vegetation that might obstruct sunlight. All other locations within gaps are subject to a greater degree of shading, both from trees bordering the gap and from existing vegetation within it. In addition, I conducted my experiments on exposed mineral soil, without an intact humus and leaf litter layer that may inhibit germination and seedling establishment of some plants (Putz 1983). Most of the soil surface in treefall gaps is covered by an intact litter layer; exposed mineral soil generally occurs only on the "mound" and "pit" created by uprooted trees. Second, the model assumes no mortality of dormant seeds other than that set by physiological limits on the maximum amount of time seeds can remain dormant but viable. In reality, many dormant seeds may be removed from the soil by predators and pathogens. Third, the model assumes that all dormant seeds are equally likely to germinate in response to a given canopy disturbance. However, seeds present in the soil for longer periods may be moved into successively lower soil horizons (by the actions of soil organisms such as earthworms), so that individual seeds become less and less likely to germinate in response to a given disturbance with increasing time in the seed bank. Fourth, the model assumes homogeneous dispersion of seeds within each distance interval, which minimizes seedling mortality due to interspecific competition. Actual seed shadows produced by birds are undoubtedly more heterogeneous, and mortality among seedlings in clumps should result in lower reproductive success than indicated by the model presented here.

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94 Undoubtedly, most of the model's assumptions are often violated in nature, so that actual reproductive output and relative fitness are much lower than the estimates presented here. Nevertheless, the estimates are useful for comparing the consequences of different seed shadows, germination requirements, seed dormancy capabilities, and fruiting phenologies for potential reproductive success of individual plants. Seasonal Constraints on Reproductive Success In the sections above, I have discussed how plant reproductive success is influenced by interacting characteristics of the dispersal service rendered by birds, the landscape-level disturbance regime, and the physiological and life historical attributes of the plants themselves. Another plant characteristic that may influence reproductive success is the timing of seed dispersal in relation to seasonal patterns of patch formation and disperser abundance. Results presented in Fig 15 suggest that even short-term seed dormancy effectively uncouples dispersal and germination; estimated reproductive output varies only slightly among plants that ripen fruits at widely different times of year Thus, plant reproductive success should not suffer appreciably if fruit ripening does not coincide closely with peak periods of gap formation even though gap formation is highly seasonal, and although gaps remain open for colonization for only short periods of time. On the other hand, fruit removal rates, hence possibly plant reproductive success, do vary seasonally as a positive function of the abundance of Myadestes melanops, the primary dispersal agent. That many species of tropical frugivores undertake seasonal migrations is well

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95 known (e.g., Fogden 1972; Crome 1975a,b; Karr et al. 1982, Wheelwright 1983), and these are generally correlated with depressed fruit resource levels in some seasons. For plant species that are highly dependent upon such seasonal migrants for dispersal, seasonal variation in disperser abundance may be an important constraint on seasonal fruiting patterns. The relationship between Myadestes abundance and fruit removal rates at Monteverde may explain, in part, the observed seasonality of fruit ripening in P. rivinoides, w. solanacea and w. coccoloboides. The positive relationship between Myadestes abundance and fruit removal rates reported above is not a strong one however; removal rates are only slightly depressed during the months when Myadestes is entirely absent from the Monteverde area. The highly seasonal fruiting patterns in these plants thus beg an additional adaptive explanation. Such patterns might also result from (1) phylogenetic constraints on phenological plasticity, (2) seasonal constraints on seed or seedling survival, or (3) competition with other plant species for dispersal ( e.g., Wheelwright 1 98 5b). First, fruiting phenolog y in these plants may not be a very plastic character. All three species are both altitudinally and geographically widespread throughout Central America, and even northern South America. Populations in different locations face different selection pressures on fruiting phenology, because seasonal patterns of both gap formation and frugivore a va iliabilit y vary among sites. The phenological patterns observed at Monteverde may actually have evolved in other populations, under different selecti o n pressures.

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96 Second, strong seasonal variation in seedling survival might impose more significant constraints on fruiting phenology than seasonal variation in fruit removal or seed germination Garwood (1983) studied temporal patterns of seed germination in a seasonal rainforest on Barro Colorado Island, Panama. She found that germination in most gap dependent tree species occurred early in the wet season, and that older seedlings were better able to survive through the first dry season than younger seedlings. She concluded that seedlings of gap-dependent species that emerge during the early wet season would have higher survival through their first dry season, especially at sites where the density of competing seedlings is high. The same may be true at Monteverde. Although forest soil at Monteverde does not dry out during the "dry season", the surface layer of soil in large gaps does, and seedlings in gaps commonly die from water stress during the height of the dry season (Murray, unpubl. data). Seeds that germinate during the early dry season may die before the rains begin. Thus, even though the early dry seas on (January March) is quite favorable with respect to the availability of suitable colonization sites (Fig. 7) and Myadestes abundance (Fig. 1), it may actually be the worst season to ripen fruits. The timing of fruit ripening may be of little consequence for survival of most seeds, which germinate only after some period of dormancy. For those dispersed by chance to currently suitable sites (where they germinate immediately), however, dispersal during the early wet season (beginning in midto late May) may result in much higher survival.

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97 Conclusions The wide variation in dispersal quality provided by different birds at Monteverde suggests the potential for close coevolution between the three plant species and those dispersers providing high quality dispersal service. That potential appears even stronger when we also consider another important aspect of the plant-frugivore interaction, that of dispersal quantity. At Monteverde, Myadestes is by far the predominant understory frugivore: over 50% of all understory frugivores captured during an intensive (ca. 4100 total mist-net hours) study were of this species (Murray unpubl. data). Phainoptila and Semnornis comprised only 2.0% and 1.2% of the total, respectively. Furthermore, of all P. rivinoides, W. solanacea, and w. coccoloboides seeds recovered in fecal samples from mist-netted birds, the majority were from Myadestes Thus, although Phainoptila and Myadestes may provide similar dispersal quality for some plants (e.g. P rivinoides), Myadestes probably disperses a far greater quantity of seeds, and therefore is probably responsible for a greater proportion of successful reproduction in all three plant species at Monteverde. Does the fact that only three bird species are responsible for most dispersal of P. rivinoides, W. solanacea and w coccoloboides seeds at Monteverde indicate a specialized dispersal system? Furthermore, does the overwhelming importance of Myadestes indicate the potential for a tight coevolutionary relationship? The answer to both of these questions is probably no. All three plant species are geographically and altitudinally widespread in Central and South America (Standley 1937, Raeder 1961, D'Arcy 1973). In contrast, Myadestes melanops, Phainoptila melanoxantha, and Semnornis frantzii are limited to Costa

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98 Rica and western P anama and are generally restricted t o middle and high elevations ( Rid gely 1976) These plants like many o t hers ( e.g ., s ee H ow e and Primack 1975 Howe 1977), are thus confronted by diffe rent disperser assemblages in different parts of their ran g es. In fact, disperser assemblages may change markedly over ve ry s ho rt distan ces For example, although Myadestes is the major disperser of W solanacea at elevations above 1500 m, at lower ele va tions o n the Pa c ifi c slope o f the Cordillera de Tilaran, the major dispersers may be Long t a iled Manakins (Chiroxiphia linearis, Wheelwright et al. 1984) Durin g the breeding season, male manakins spend most of their time ( and deposit most seeds) at their display perches. Dispersal by male manakins may thus have very different conseq uen ces for individual W solanacea fr om dispersal by Myadestes just a few kilometers away. And although adaptation for dispersal by particular bird species is conceivable w ithin single plant populations, gene flow between closely adJacent plant populations may swamp any such local adaptation. Furthermore, the relationships between~ rivinoides w solanacea, w coccolobo i des and their major dispersal agents at Monte ve rde are exceedingly asymmetrical. Although virtually all dispersal o f these plants in the Monteverde Cloud Forest Preserve is performed by Myadestes, Phainoptila, and Semnornis, fruits of the three plant sp ecies comp rise only a small proportion of the diets of the t h ree bird species. Thus it is un l ikely that any specializati o n of these birds for feeding on fruits o f P. ri v inoides, w. so lana cea, and W co c colo boides woul d be selectively advantageous. Such diffuse ( sensu Janz en 1980) a nd asymmetrical ecolog i cal relationships between plan ts and their anim al

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99 seed dispersers l i kely preclude tight coevolution between them ( see also Wheelwright and Orians 1982, Janzen 1 983 b Ho w e 1984)

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APPENDIX ESTIMATION OF "SEED SHADOWS" FROM DATA ON SEED PASSAGE RATES AND BIRD MOVEMENT PATTERNS: A HYPOTHETICAL EXAMPLE The distribution of seed dispersal distances away from a particular plant was estimated from data on seed retention times and bird movement patterns. The data in Figure A-1 allow relatively precise measurement of the distances between all mapped locations, each of which is treated as a potential source plant, and the time spent at each. Figure A-2 shows, for each location, the bird's distance away from that location for each minute following the midpoint of the time interval spent there. Such data from many initial locations (source plants) are then combined to produce a probability matrix of distance versus time. The elements of this matrix (shown graphically in Figure A-3) represent the probabilities that the bird will be at a particular distance from the source plant at a particular time after the midpoint of the interval spent there. Multiplying this matrix by the probability distribution of seed passage times (Fig. A-4), and then summing the results for each distance interval over all 12 time intervals, yields a probability distribution of seed movement distances, or the probable "seed shadow" produced by one individual around one plant (Fig. A-5). Data from many individuals are combined (weighting the seed shadow computed for each individual equally) to estimate the overall seed shadow produced by particular frugivore species around individual plants. 100

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Figure A-1. Foraging movements of a single frugivorous bird for a period of four hours. Times of arrival are shown for each location. See text for methods.

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.. N 0 0 ., 0 0 0 "' 0 0 0 ., 0 102 .. 0 0 ., 0 m 0 0 "' ., 0 0 "' m 0 0 0 ... 0 "' ., 0 ., ... 0 0 "' "' 0 "' "' "' 0 .. "' 0

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TIME MINUTES SINCE MIDPOINT START MIDPOINT tl 5 10 15 20 25 30 35 40 45 50 55 60 0530 0535 0 I 2 1 I 25 I 48 l 82 I 73 0540 0545 0 I 22 I 28 I 62 I 53 I 39 0550 0557 0 I 34 I 64 I 69 l 61 l 75 0605 0610 0 I 33 I 40 I 49 I 63 l 64 0615 0620 0 I 47 I 7 4 I 85 I 90 I 118 0625 0632 0 I 37 I 44 I 51 1 105 I 88 0640 0642 0 1 14 I 16 I 75 I 85 I 92 0645 0652 0 I 10 I 82 I 99 1 105 l 13o ho3 0700 0 7 07 0 I 7 3 I 95 I 99 11 29 I 101 I 1 38 0715 0717 0 1 72 I s7 1 111 I 88 l 81 I 14 0720 0730 0 I 2 3 I 40 I 18 I 58 I 68 I 78 0740 0742 o I 57 I 41 I 41 I 50 l 59 I 71 0745 0747 0 1 28 I 73 1 10 6 I 1 16 I 127 I 1 24 0750 0755 0 I 7 2 I 85 I 95 I 104 I 97 0800 0807 0 I 68 I 73 I 89 l 109 l 105 0815 0817 0 1 10 I 22 I 47 l 59 I 59 0820 0827 0 I 16 I 49 l 66 l 57 Figure A2 Bird distance from seed source plant vs. time For each sequence of foraging movements beginning with a visit to a fruiting plant, nu m bers given indi ca te the bird s distance (in met e rs) from that plant during the following hour. Each sequence begins (time 0) at the midpoint of the time interval spent in the source plant ...... 0 w

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Figure A-3. Probability distributions of bird movement vs. distance and time. For each successive 5 minute time interval following the midpoint of the interval spent at the source plant (see Fig. A-2), the figure shows the probability that a bird will be in each of 14 distance intervals (10 m each) away from the source plant.

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ID ... I 0 ... 0 CII I ID I... z ID 0 CII I Cl. 0 CII 0 :E 0 (') I ID w CII (.J z ID (') I en 0 (') en w 0 ... II ID :::::, (') z ID :E "' I 0 "' 0 ID I ID ... ID ID I 0 ID 0 C0 I ID ID 10 5 0 20 <40 60 80 100 120 1<40 DISTANCE FROM ORIGIN >1...J CD < CD 0 a: Cl.

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a3 0 60 0 C, z C, a: w w 40 20 106 (J) C w w (J) 0+--....---1---1--~-~--+--4----+---+--+--+---, 0 10 20 30 40 50 60 MINUTES AFTER INGESTION Figure A-4. Retention time distribution for seeds of the source pla nt species in a partic ular bird species' gut See text for met h ods

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Figure A-5. Probability distribution of dispersal distances, or the probable "seed shadow" produced as a result of the 17 foraging movement sequences in Figure A-2 For each 5 minute time interval, the probability of seed emergence (Fig. A-4) is multiplied by the probability distributions of bird movement in Fig. A-3 For each distance interval, these products are then summed over all time intervals to yield the seed shadow

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.2 z 0 I(f) 0 a.. w 0 u. 0 1 >I_J m <( m 0 a: a.. 0 0 20 40 60 80 100 120 DIST ANGE FROM ORIGIN (meters) I I 140 ..... 0 CD

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LITERATURE CITED Abrell, D. B., and M. T. Jackson. 1977. A decade of change in an oldgrowth beech-maple forest in Indiana. American Midland Naturalist 98: 22-32. Applegate, R. D., L. L. Rogers, D. A. Casteel, and J. M. Novak. 1979. Germination of cow parsnip seeds from grizzly bear feces. Journal of Ma mm a logy 60: 655. Aubreville, A., and J. F. Leroy. 1970. Contribution a L'etude biologique d'une Araliaceae d'America tropicale: Didymopanax morotoni. Adansonia 10 : 383 -407. Augspurger, C. K. 1983a. Offspring recruitment around tropical trees: changes in cohort distance with time. Oikos 40: 189-196. 1983b. Seed dispersal by the tropical tree, Platypodium elegans, and the escape of its seedlings from fungal pathogens. Journal of Ecology 71 :759-771. 1984a. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61: 211-217. 1984b Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65 : 17051712 Blake, J. G., and w. G. Hoppes. 1986. Influence of resource abundance on use of tree-fall gaps by birds in an isolated woodlot. Auk 103 : 328-340. Brokaw, N. V. L. 1980. Gap phase regeneration in a neotropical forest. Dissertation. Univ. of Chicago, Chicago, Illinois, USA. 1982a. Treefalls: frequency, timing, and consequences. Pages 101-108 in E.G. Leigh, A. s. Rand, and D. M. Windsor, editors. The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institution Press, Washington, D. c., USA. 1982b The definition of treefall gap and its effect on measures of forest dynamics. Bi otropica 14 : 158 160. 1985. Treefalls, regrowth, and community structure in tropical forests. Pages 53-69 in S.T.A. Pickett and P.S. White, editors. Natural disturbance: the patch dynamics perspective. Academic Press, New York, New York, USA. 109

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110 Brunner, H., R. V. Harris, and R. L. Amor. 1976. dispersal of seeds of blackberry (Rubus procerus foxes and emus. Weed Research 16: 171-173. A note on the P. J. Muel 1.) by Bullock, s. H. 1978. Plant abundance and distribution in relation to types of seed dispersal in chaparral. Madrano 25 : 104-105. Burtt, B. D. 1929 A record of fruits and seeds dispersed by mammals and birds from the Singida district of Tanganyika territory. Journal of Ecology 17: 351-355 Clark, D. A., and D. B. Clark. 1981. Effects of seed dispersal by animals on the regeneration of Bursera graveolens (Burseraceae) on Santa Fe Island, Gal&pagos. Oecologia 49: 73-75 Crome, F. H. J. 1975a. northern Queensland. The ecology of fruit pigeons in tropical Australian Wildlife Research 2: 155-185. Crome, F. H. J. 1975b. Breeding, feeding, and status of the Torres Strait Pigeon on Low Isles, northeastern Queensland. Emu 75: 198-198. Culver, D. C., and A. J. Beattie. 1980. The fate of Viola seeds dispersed by ants. American Journal of Botany 67 : 710-714. D'Arcy, w. G. 1973. Solanaceae. Pages 573-780 in R. E. Woodson, Jr. and R. w. Schery, editors. Flora of Panama. Annals of the Missouri Botanical Garden, volume 60. Davidson, D. w., and s. R. in ant-dispersed plants. Morton. 1981a. Competition for dispersal Science 213 : 1259 1261. 1981b. Myrmecochory in some plants (F. Chenopodiaceae) of the Australian arid zone Oecologia 50: 357-366. Denslow, J. s. 1980 Gap partitioning among tropical rainforest trees. Biotropica 1 2 ( supplement on tropical succession): 47-55. and T. C. Moermond. 1982. The effect of accessibility on rates ---of fruit removal from tropical shrubs: an experimental study. Oecologia 54: 170-176. Diamond, J. M. 1973. Distributional ecology of New Guinea birds. Science 179: 759-769. Docters van Leeuwen, w. M. 1954. On the biology of some Loranthaceae and the role birds play in their life-history. Beaufortia 4: 105-208. Estrada, A., dispersal. and T. H. Fleming, editors. 1986. Frugivores and seed w. Junk, Dordrecht, The Netherlands. Feinsinger, P. 1983 Coevolution and pollination. Pages 282 310 in D. J. Futuyma and M. Slatkin, editors Coevolution. Sinauer Associates, Sunderland, Massachusetts, USA.

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111 J. H Beach, Y. B. Linhart W. H. Busby, and K. Greg Murray. -Disturbance, pollinator predictability, and pollination success among Costa Rican cloud forest plants. Ecology, in review Fleming T. H. 1981. Fecundity, fruiting pattern, and seed dispersal in Piper amalago (Piperaceae), a bat-dispersed tropical shrub. Oecologia 51: 42-46 __ _ and E. R. Hei thaus 1981 Frugivorous bats seed shadows, and the structure of tropical forests. Biotropica 13 (Supplement on reproductive botany): 45-53. Fogden, M P. L. 1972. The seasonality and population dynamics of equatorial forest birds in Sarawak. Ibis 114: 307-343. Forshaw, J. M. 1978. Parrots of the world. David and Charles, London, England. Foster, R 1973. Seasonality of fruit production and seed fall in a tropical forest ecosystem. Dissertation. Duke University, Durham, North Carolina, USA. __ _ and N V. L. Brokaw. 1982. Structure and history of the vegetation of Barro Colorado Island. Pages 67-81 in E. G. Leigh, A. s. Rand, and D. M. Windsor, editors The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian I nstitution Press, Washington, D c., USA. Garwood, N 1983. Seed germination in a seasonal tropical forest in Panama: a community study Ecological Monographs 53 : 159-181. Geritz, s A. H., T J. de Jong, and P. efficacy of dispersal in relation to production. Oecologia 62: 219-221. G. L. Klinkhamer. 1984. safe site area and seed The Glyphis, J P s J Milton, and w. R. Siegfried. 1981. Dispersal of Acacia cyclops by birds. Oecologia 48: 138-141. Green, D S. 1983 The efficacy of dispersal in relation to safe site density. Oecologia 56: 356-358. Greenberg, R. 1981. Frugivory in some migrant tropical forest wood warblers. Biotropica 13: 215 22 3. Guevara, s., and A. Gomez-Pompa 1972. tropical region of Veracruz, Mexico. 53:312-335. Seeds from surface soils in a Journal of the Arnold Arboretum Handel, S. N. 1978 The competitive relationship of three woodland sedges and its bearing on the evolution of ant dispersal of Carex pedunculata. Evolution 32: 151-163. Harper, J L 1977. Population biology of plants. Academic Press, London, England.

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-------------------112 Hartshorn, G. s. 1978. Tree falls and tropical forest dynamics. Pages 617-638 in P. B. Tomlinson and M. H. Zimmerman, editors. Tropical trees as living systems. Cambridge Univ. Press, London, England. 1980. Neotropical forest dynamics. Biotropica 12 (supplement on tropical succession): 23-30. Heinselman, M. L. 1973. Fire in the virgin forests of the Boundary Waters Canoe Area, Minnesota. Quaternary Research 3: 329-382. Herrera, c. M. 1981. Fruit variation and competition for dispersers in natural populations of Smilax aspera. Oikos 36: 51-58. 1984. Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 6 5: 609-61 7. and P. Jordana. 1981. Prunus mahaleb and birds: the high---efficiency seed dispersal system of a temperate fruiting tree. Ecological Monographs 51: 203-218. Hilty, S. L. 1980 Relative abundance of north temperate zone breeding migrants in western Colombia and their impact at fruiting trees. Pages 265 271 in A Keast and E.S. Morton, editors. Migrant birds in the neotropics. Smithsonian Institution Press, Washington o.c., USA. Hladik, A. 1982. Dynamique d'une foret equatoriale africaine: mesures en temps reel et comparison du potential de croissance des differentes especies. Acta Oecologica Oecologia Generalis 3: 373-392. ____ and c. M. Hladik. 1969. Rapports trophiques entre vegetation et primates dans la foret de Barro Colorado (Panama) Terre et la Vie 116 : 25-117. Holdridge, L. 1967 Life zone ecology. Tropical Science Center, San Jose, Costa Rica. Holthuijzen, A. M.A., and c. s. Adkisson. 1984. Passage rate, energetics, and utilization efficiency of the cedar waxwing. Wilson Bulletin 96 : 680 -6 84. Howe, H. F. 1977. Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58: 539-550. 1980. Monkey dispersal and waste of a neotropical fruit. Ecology 61: 944-959. 1982 Fruit production and animal activity at two tropical trees. Pages 189-200 in E. Leigh, Jr., A. s. Rand, and D. Windsor, editors. The ecology of a tropical rainforest. Smithsonian Institution Press, Washington o.c., USA. 1984. Constraints on the evolution of mutualisms. American Naturalist 123: 764-777.

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11 3 ____ and D. De Steven. 1979. Fruit production, migrant bird visitation and seed dispersal of Guarea glabra in Panama. Oecologia 39: 185-196. ____ and G. F. Estabrook. 1977. On intraspecific competition for avian dispersers in tropical trees. American Naturalist 111 : 817-832. ____ and R. B. Primack. 1975. Differential seed dispersal by birds of the tree Casearia nitida ( Flacourtiaceae ). Biotropica 7 : 278 283 ____ E. W. Schupp, and L. c. Westley. seed dispersal for a neotropical tree 66: 781-791. 1985. Early consequences of (Virola surinamensis). Ecology ___ and J. Smallwood. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13: 201-228. and G. A. Vande Kerchove. ---of a tropical tree. Ecology 60: and G. A. Vande Ke re hove. ---birds. Science 210: 925-927. 1979. Fecundity and seed dispersal 180-189. 1980. Nutmeg dispersal by tropical ____ and G. A. Vande Kerchove. 1981. Removal of wild nutmeg (Virola surinamensis) crops by birds. Ecology 62: 1093-1106. Janzen, D. H. 1978. The size of a local peak in a seed shadow. Biotropica 10: 78. 1980. When is it coevolution? Evolution 34: 611-612 1981. Ficus oval is seed predation by an orange-chinned parakeet (Brotogeris jugularis) in Costa Rica. Auk 98: 841-844 1983a. Dispersal of seeds by vertebrate guts Pages 232-262 in D. J. Fu tuyma and M. Slatkin, editors. Coevolu tion. Sinauer Associates, Sunderland, Massachusetts, USA. 1983b. Seed and pollen dispersal by animals: convergence in the ecology of contamination and sloppy harvest. Biological Journal of the Linnaean Society 20: 103-113. ____ G. A. Miller, J. Hackforth-Jones, c. M. Pond, D. Hooper, and D. P. Janos. 1976. Two Costa Rican bat generated seed shadows of Andira inermis (Leguminosae) Ecology 56: 1068-1075. Jenkins, R. 1969. Ecology of three species of s al ta tors in Costa Rica with special reference to their frugivorous diet. Dissertation. Harvard University, Cambridge, Massachusetts, USA. Jones, C. E., and R. J. Little. 1983. Handbook of experimental pollination biology. Van Nostrand, New York, New York, USA.

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114 Karr, J. R., D. w. Schemske, and N. Brokaw. 1982. Temporal variation in the undergrowth bird community of a tropical forest. Pages 441-453 in E.G. Leigh, Jr., A. s. Rand, and D. Windsor, editors. The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Ins ti tut ion Press, Washington, D.C., USA. Krefting, L. w., and E. L. Roe. mammals in seed germination. Lawton, R., and V. Dryer. 1980. forest reserve. Brenesia 18: 1949. The role of some birds and Ecological Monographs 19: 269-286. The vegetation of the Monteverde cloud 101-116. Lawton, R. o., Costa Rica. and F. E. Putz. Elfin forest dynamics in Monteverde, Unpublished manuscript. Leck, C. F. 1972. The impact of some North American migrants at fruiting trees in Panama. Auk 89: 842-850. Leigh, E. G., Jr. 1975. Structure and climate in tropical rain forest. Annual Review of Ecology and Systematics 6: 67-86. Lemen, c. 1981. Elm trees and elf leaf beetles: patterns of herbivory. Oikos 36: 65-67. Levey, D. J., 1986. Methods of seed processing by birds and seed deposition patterns. In A. Estrada and T. H. Fleming, editors. Frugivory and seed dispersal. W. Junk, Dordrecht, The Netherlands. Levin, D. A. 1979 The nature of plant species. Science 204: 381-384. Lieberman, D., J. B. Hall, M. D. Swaine, and M. Lieberman. 1979. Seed dispersal by baboons in the Shai Hills, Ghana. Ecology 60: 65-75. Lucas, H. A., and G. A. F. Seber. 1977. Estimating coverage and particle density using the line intercept method. Biometrika 64: 61 8 622. McDiarmid, R. w., R. E. Ricklefs, and M. s. Foster. 1977. Dispersal of Stemmadenia donnell-smithii (Apocynaceae) by birds. Biotropica 9: 925. McKey, D. 1975. The ecology of coevolved seed dispersal systems. Pages 159 -1 91 in L. E. Gilbert and P. H. Raven, editors. Coevolution of animals and plants University of Texas Press, Austin, Texas, USA. Moermond, T. c. 1983 Suction-drinking in tanagers Thraupidae and its relation to frugivory. Ibis 125: 545-549. ____ and J. s. Denslow. 1985. Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithological Monographs 36: 865-897. Murray, K. G. In press. Selection for optimal fruit crop size in bird dispersed plants. American Naturalist.

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115 Naka, K. 1982. Community dynamics of evergreen br oadleaf forests in southwestern Japan. I. Wind damaged trees and ca nop y gaps in an evergreen oak forest. The Botanical Magazine, Tokyo 9 5: 385-399. Nobel, J. C. 1975 The effects of emus (Dromaius novae-hollandiae Latham) on the distribution of the nitre bush ( Nitraria billardieri DC.). Journal of Ecology 6 3: 979-984 Oldeman, R. A. A. 1978. Architecture and energy exchange of dicotyledonous trees in the forest. Pages 535-560 in P. B. Tomlinson and M. H. Zimmermann, editors. Tropical trees as living systems. Cambridge Univ. Press, London, England. Olson, S. L., and K. E. Blum. 1968. Avian dispersal of plants in Panama. Ecology 49: 565-566. Platt, w. J. 1975. The colonization and formation of equilibrium plant species associations on badger disturbances in a tall-grass prairie. Ecological Monographs 45: 285-305. 1976. The natural history of a fugitive prairie plant (Mirabilis hirsuta ( Pursh)MacM.). Oecologia 22: 399 409 ____ s. L. Rathbun, M. M. Platt, and D. w. Hirsh. Compostion and dynamics of a mixed-species forest dominated by Southern Magnolia (Magnolia grandiflora) and American Beech (Fagus grandiflora). Unpublished manuscript. Pratt, T. K., and E. w. Stiles. 1983. How long fruit-eating birds stay in the plants where they feed: implications for seed dispersal. American Naturalist 122: 797-805. Putz, F. E. 1983 Treefall pits and mounds, buried seeds, and the importance of soil disturbance to pioneer trees on Barro Colorado Island, Panama. Ecology 64: 1069 1074. Raeder, K. 1961. Phytolaccaceae. Pages 66-79 In R. E. Woodson, Jr. and R. W. Schery, editors. Flora of Panama. Annals of the Missouri Botanical Garden, volume 48. Real, L. 1983. Pollination biology. Academic Press, Orlando, Florida, USA. Richards, P. w. 1952. The tropical rain forest. Cambridge Univ. Press, London, England. ____ and G. B. Williamson. 1975. Treefalls and patterns of understory species in a wet lowland tropical forest. Ecology 56: 1226-1229. Rick, c. M., and R. I. Bowman. 1961. Galapagos tomatoes and tortoises. Evolution 15: 407 447.

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116 Ridgely, R. S. 1976 A guide to the birds of Panama. Princeton Univ. Press, Princeton, New Jersey, USA. Runkle, J. R. 1979. Gap phase dynamics in climax mesic forests. Dissertation. Cornell University, Ithaca, New York, USA. 1982 Patterns of disturbance in some old-growth mesic forests of eastern North America. Ecology 63: 1533-1546. Salmonson, M. G. juniper seeds. 1978. Adaptations for animal dispersal of one -seeded Oecologia 32: 333-339. Schultz, J. P. 1960. Ecological studies on rain forest in Northern Surinam. N. V. Noord-Hollandsche VitGevers Maatshappij, Amsterdam, The Netherlands. Skeate, S. T. 1985. Mutualistic interactions between birds and fruits in a northern Florida hammock community. Dissertation. Univ. of Florida, Gainesville, Florida, USA. Smith, A. J. 1975. Invasion and ecesis of bird-disseminated woody plants in a temperate forest sere. Ecology 56: 19-34. Smythe, N. 1970. Relationships between fruiting seasons and seed dispersal methods in a neotropical forest. American Naturalist 104: 25-36. Snow, B. K., and D. W. Snow. honeycreepers in Trinidad. 1971. The feeding ecology of tanagers and Auk 88: 291-322. Snow, D. w. 1965 A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos. 15: 274-281. 1971. 194-202. Evolutionary aspects of fruit-eating by birds Ibis 113: 1973. Distribution, ecology and evolution of the bellbirds (Procnias, Cotingidae). Bulletin of the British Museum of Natural History (Zoology) 25: 369-391. Sokal, R.R., and F. J. Rohlf. 1969. Biometry. W. H. Freeman, San Francisco, California, USA. Sorensen, A. E. 1981. temperate woodland Interactions between birds and fruit in a Oecologia 50: 242-249. 1983. Taste aversion and frugivore preference. 117 120 Oecologia 56: 1984. Nutrition, energy and passage time: experiments with fruit preference in European blackbirds (Turdus merula). Journal of Animal Ecology 53: 545-557.

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11 7 Standley, P. c. 1937. Flora of Costa Rica. Publications of the Field Museum of Natural History(Chicago, Illinois, USA), Botanical series, volume 18. Stapanian, M. A. 1982. A model for fruiting display: seed dispersal by birds for mulberry trees. Ecology 63: 1432-1443. Stiles, E. W. 1980. Patterns of fruit presentation and seed dispersal in bird-disseminated woody plants in the eastern deciduous forest. American Naturalist 116: 670-688. 1982. Fruit flags: two hypotheses. American Naturalist 120: 500-509. Temple, s. A. 1975. Plant-animal mutualism: coevolution with dodo leads to near extinction of plant. Science 197: 885-886 Thompson, J. N. forest herbs. 1980 Treefalls and colonization patterns of temperate American Midland Naturalist 104: 176-184 1981. Elaisomes and fleshy fruits: phenology and selection pressures for ant-dispersed seeds. American Naturalist 117: 104-108. and M. F. Willson. 1979. Evolution of temperate fruit /bi rd ---interactions: phenological strategies. Evolution 33: 973-982. Uhl, C. 1982. Tree dynamics in a species rich tierra firme forest in Amazonia, Venezuela. Acta Cientifica Venezolana 33: 72-77. van der Pijl, L. 1972. Principles of dispersal in higher plants. Second edition. Springer-Verlag, Berlin. Van der Wall, s. B., and R. P. Balda. 1977. Coadaptations of the Clark's nutcracker and the pinon pine for efficient seed harvest and dispersal. Ecological Monographs 47: 89 -11 1 Vazquez-Yanes, C. 1976. Estudios sabre ecofisiologia de la germinacion en una zona calido-humeda de Mexico. Pages 279-387 in A. Gomez-Pompa, C. Vazquez-Yanes, S. Del Arno, and A. Butanda, editors. Regeneracion de selvas. Editorial Continental, Mexico. 1977. Germination of a pioneer tree (Trerna guineensis Ficahlo), from equatorial Africa. Turrialba 23(3): 301-302 1980. Light quality and seed germination in Cecropia obtusifolia and Piper auritum from tropical rain forest in Mexico. Phyton 38: 33-35. ____ and A. Orozco-Segovia. 1982. rain forest tree (Heliocarpus donnell diurnal fluctuations of temperature. 298. Seed germination of a tropical smithii) in response to Physiologia Plantarum 56: 295

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118 ____ and A. Orozco-Segovia. 1984. Ecophysiology of seed germination in the tropical humid forests of the world: a review. Pages 37-50 in E. Medina, H. A. Mooney, and C. Vazquez-Yanes, editors. Physiological ecology of plants in the wet tropics. w. Junk, Dordrecht, The Netherlands. ____ Orozco-Segovia, G. Francois, and L Trejo. 1975. Observations on seed dispersal by bats in a tropical humid region in Veracruz, Mexico. Biotropica 7: 73-76. ____ and H. Smith. 1982. Phytochrome control of seed germination in the tropical rain forest pioneer trees Cecropia obtusifolia and Piper auritum and its ecological significance. New Phytologist 92: 477-485. Walsberg, G. E. 1975. Digestive adaptations of Phainopepla nitens associated with the eating of mistletoe berries. Condor 77: 169-174. Wheelwright, Quetzals. N. T. 1983. Fruits and the ecology of Resplendant Auk 100: 286-301. 1985a. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66: 808-818 1985b. Competition for dispersers, and the timing of flowering and fruiting in a guild of tropical trees. Oikos 44: 465-477. ____ W. A. Haber, K. G. Murray, and c. Guindon. 1984. Tropical fruit-eating birds and their food plants: a survey of a Costa Rican lower montane forest. Biotropica 16: 173-192. ____ and G. H. Orians. 1982. Seed dispersal by animals: contrasts with pollen dispersal, problems of terminology, and constraints on coevolution American Naturalist 119: 402-413. Whitmore, T. C. 1975. Tropical rain forests of the far east. Clarendon Press, Oxford, England. 1978. Gaps in the forest canopy. Pages 639 655 in P. B. Tomlinson and M. H. Zimmermann, editors. Tropical trees as living systems. Cambridge Univ. Press, London, England. 1982. On pattern and process in forests. Pages 45-57 in E. J. Newman, editor. The plant community as a working mechanism. Blackwell, Oxford, England. Wilson, D. E., and D. H. Janzen. 1972. Predation on Scheelea palm seeds by bruchid beetles: seed density and distance from the parent palm. Ecology 53: 954 959 Zackrisson, o. boreal forest. 1977 Influence of forest fires on the North Swedish Oikos 29: 22-32 Zar, J. H. 1984. Biostatistical analysis. Second edition. PrenticeHall, Englewood Cliffs, New Jersey, USA.

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BIOGRAPHICAL SKETCH Kelvin Gregory Murray was born to Max w. and Lorene M. Murray on August 8, 1954. Those who gleefully poke fun at his Southern California manner, dress, and habits of personal hygiene will be distressed to learn that he is actually a native of Chicago, Illinois. Despite brief forays into eastern religions, motorcycle racing, and particle physics, Greg knew that he wanted to be a biologist at least by the 8th grade, a fact much-lamented by the science faculties at his junior high and high schools. Following graduation from high school, Greg studied biology at California State University, Northridge. There, he received his B.S. in 1977, with an emphasis on marine invertebrate ecology. For the next two years, he studied seabird and deermouse ecology on the Southern California Channel Islands and on the Pribilof Islands, in the Bering Sea. He received the M S degree in 1980 for his studies of deermouse predation on Xantus' Murrelet eggs. In 1979 Greg married his childhood sweetheart, Kathy Winnett, whom he had met three years previously in a class on population and community ecology. Later that year they made their way to Gainesville, to further their graduate careers at the University of Florida. Following two years of course work on campus they moved to Costa Rica for 27 months of intense fieldwork. Upon their return, they initiated a biological project involving a lifetime of intense homework. Their son, Dylan, was born on June 6, 1984. 119

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120 Greg's interests are diverse. In addition to his professional pursuits, he dabbles in electronics, photography, physical fitness, and LEGOtm building blocks. He enjoys almost all types of music and theater, and he is an avid devotee of the Firesign Theater. He is not now, nor has he ever been, a strict adaptationist.

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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. Peter 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. H. Jane Brockmann 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. Thomas c. Emmel 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. Walter Judd Associate 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. rancis E. sistant Professo f Botany

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This dissertation was submitted to the Graduate Facult y of the Department of Zoology in the College of Libera l Arts and Sciences and to the Graduate School and was accepted as partial fulfillment of the requirements for the degree of D oc t or of Philoso phy. December 1986 Dean, Graduate School

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UNIVERSITY OF FL ORIDA II I II IIIIII Ill Ill lllll lllll II IIIIII IIII II l\111111111111111111111 3 1262 08553 4211