Title: Avian seed dispersal of neotropical gap-dependent plants
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Permanent Link: http://ufdc.ufl.edu/UF00102852/00001
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Title: Avian seed dispersal of neotropical gap-dependent plants
Physical Description: Book
Language: English
Creator: Murray, Kelvin Gregory, 1954-
Copyright Date: 1986
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Bibliographic ID: UF00102852
Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
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Resource Identifier: ltuf - AEN9830
oclc - 16141354

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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


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,


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.



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

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



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

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.


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.


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.


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


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"


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


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


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


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.


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


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.





4Q 0






C |



0 2




fa 4-

(a a)

4 U

u 0

a) a)


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

r CV)

-1 00


'> -- "

-- -- LL co
ez z -
0 0U


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


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









diameter (mm)

















2 25


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%


Bird Plant
speciesa species

















89 (100)

75 (100)

100 (3)

100 (3)

0 (2)





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

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

c Of those that germinated

dInsufficient number of seeds available for experiment


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).



after 60 days

Phytolacca rivinoides

Witheringia solanacea

Witheringia coccoloboides

after 410 days

Phytolacca rivinoides

Witheringia solanacea

Witheringia coccoloboides






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.


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),

Phytolacca rivinoides

40- *


0 80-
r- Witheringia solanacea

Z 60-


Z 20


80- Witheringia coccolobo




0 100 200 3



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








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


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.


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.



30 -



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

0- --

Witheringia coccoloboides


25 30

* 0

60 IL

Phytolacca rivinoides
(.25< p<.5)









-* .. *

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

TIME BURIED (months)


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


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,
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



o o
0 0

0 0

Co 0

00 0)
o u

o o

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


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












, I





(io101 10 %)
,83118 3dIVS, NI V38V ONV1





o UO

(eJeoeqI4/) A118N3G .3118 3dVS,

7Vo101 10 %)

8311S 3jVS8,


In o In

(ej eoeq/l#)

A11SN3G .311S

0 0
O c



,-4 4-4

0 0



ca 3.

(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


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



Phainoptila melanoxantha

Witheringia solanacea

Witheringia coccoloboides






40 -


O -







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

Figure 8 -- continued

Phytolacca rivinoides

Witheringia solanacea

I I i

40 50 60 70 80 90


Figure 8 -- continued

Semnornis frantzii

40 -






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.


) C
1) 0 )


1) 4

04 4
* 0 a

0-4 0

0 CH:

SO > -H
p C >

10-H 0


0 3 a)

-4J~ 0
u> O

a4 a

g0 -4 4
z e

E O4

(D 0

UO o 0)
->j 0

0 0 .0)

(U o U M
C / Um

OD O 00
mn cN n rt-

0co 0 -




>1 -r

(mo Ln 0

(y1 0 'a

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^' c' oo tt-
M- 0 -'

4J 4J 4J 4-J
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C) 0

-H (I
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a0 c
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0 0
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- 3
Ul r

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


.2 -


""fim ~fL .. p

. C.

. r.

2- Phainoptila melanoxantha



Semnornis frantzii








0 100 200 300 400



.... -

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

- -C



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


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













s x


-1 u

2H (0
,.i a


0 "




-o 6 6 6

0 o 0 o0 0o
6 d o o
dOuO .Lny.-

A-18V3A -O NOIJ.0OdOUd




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.





(a -H

7 0

> rl

r -







> 4

o 44




3 a f
*^ *r *-

fa O

0 0 0 0

(ou) indinO 3AuionfOcdd3



cri ~

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).







5 10 20


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


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

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).

M.m., P.m.

1 s.f.


M.m., P.m.



0* .


M.m., P.m.



fitness with increasing dormancy capability is not monotonically

increasing and linear, as suggested by Fig. 13, but is in fact


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


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.






















i i I

I 1




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


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


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


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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