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Mutualistic interactions between birds and fruits in a northern Florida hammock community

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Title:
Mutualistic interactions between birds and fruits in a northern Florida hammock community
Creator:
Skeate, Stewart T., 1952-
Publication Date:
Language:
English
Physical Description:
viii, 111 leaves : ill. ; 28 cm.

Subjects

Subjects / Keywords:
Birds ( jstor )
Ecology ( jstor )
Fruit crops ( jstor )
Fruiting ( jstor )
Fruits ( jstor )
Hammocks ( jstor )
Latitude ( jstor )
Lipids ( jstor )
Ripening ( jstor )
Species ( jstor )
Birds -- Florida ( lcsh )
Botany -- Ecology -- Florida ( lcsh )
Dissertations, Academic -- Zoology -- UF
Frugivores -- Florida ( lcsh )
Fruit -- Florida ( lcsh )
Seeds -- Dispersal -- Florida ( lcsh )
Zoology thesis Ph. D

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1985.
Bibliography:
Bibliography: leaves 103-110.
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Stewart T. Skeate.

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University of Florida
Holding Location:
University of Florida
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Copyright [name of dissertation author]. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
Resource Identifier:
000869462 ( ALEPH )
14388327 ( OCLC )
AEG6499 ( NOTIS )

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MUTUALISTIC INTERACTIONS
IN A NORTHERN FLORIDA


BETWEEN
HAMMOCK


BIRDS AND
COMMUNITY


FRUITS


STEWART


SKEATE


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


UNIVERSITY


OF FLORIDA


1985
















ACKNOWLEDGEMENTS



It is my pleasure to acknowledge the many friends and


colleagues who have aided me in this work.


The members of


dissertation committee,


John W.


Hardy


(chairman),


Peter


Feinsinger, Jack Kaufmann, and Walter Judd, provided helpful


research and editorial suggestions.

this study is the result of a discus

Feinsinger's community ecology class.


I should mention that


sion question from Peter

I was also very


fortunate to have the assistance


e of Edmund W.


Stiles,


Rutgers University,


in the nutrient analysis of my fruits.


I have also drawn heavily from Stiles' work on bird-fruit


dispersal systems of North America.


To Ted I extend my


sincerest


thanks.


I also thank Doug White,


Rutgers


University, for providing me with invaluable manuscripts.


A number of


post-doctoral


associates and graduate


students have helped me throughout my studies.


especially


would


like to thank Peter G. May, Nathaniel T.


Wheelwright, and E.E.


Spears for their help and suggestions.


I also acknowledge the Department of Zoology and the


Frank M.

support.


Chapman Memorial Fund for their generous


Thanks also


financial


go to the Florida Division of Natural











Felasco Hammock is truly a Florida jewel; I hope that this

study adds to the understanding of this unique community.

I would like to separately thank my wife, Lea, for her


field help and companionship.

the hammock with her. It wil


It was a joy for me to share


.1 be a time and place we will


always remember and cherish.


I must also thank my canine companion,


Virgil.


Through


the miles and mil


of walking, my wee westie was always


there beside me (except when he was off


Finally,


chasing armadillos).


I would like to thank everyone I've been


associated with at the Department of Zoology at UF for

making my six year stay in Florida a wonderful experience.













TABLE OF CONTENTS



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


LIST OF


LIST


OF FIGURES..... .................................vi


ABSTRACT..............................................vii

CHAPTERS


Temperate Bird-Fruit D
Nutritional Properties


ispe
of


rsal Systems...........3
Temperate Fruits.......5


SEASONAL PATTERNS OF FRUGIVORE
AVAILABILITY AND FRUIT RIPENING..................9


Study Site and Methods...........................9
Results and Discussion..........................14
Conclusions ..................................... 56


THREE SEASONAL PATTERNS OF BIRD-DISPERSED
FRUIT CHARACTERISTICS AND FRUIT REMOVAL.........57

Methods............. .............................57
Results and Discussion..........................59
Conclusions.....................................83


FOUR


SUMMARY


APPENDICES


METHODS


OF CALCULATING RIPENING SYNCHRONY.......92


FLOWERING AND FRUITING SCHEDULES OF BIRD-
DISPERSED PLANTS OF SAN FELASCO HAMMOCK.........94


III FRUIT TRAITS ANALYZED FOR BIRD-DISPERSED
PLANTS OF SAN FELASCO HAMMOCK.....................98

IV BIRD-DISPERSED PLANT SPECIES AND THE BIRDS THAT


TAB LES V


86


~NTRODUCTION........,...................














LIST OF TABLES


Table 2-1.


Fruit types of vascular plants found


in San Felasco Hammock State Preserve, Florida.........11


Table
Felas


2-2.


Avian frugi


vores


observed at San


Hammock during cenususes.......................15


Table


2-3.


Observed frugivory by major and


minor frugivores in


Felasco Hammock................17


Table


2-4.


Resident status of avian frugivores


at San Felasco Hammock.................................19


Table
rs,
spec


Spearman rank correlation


coe


fficients,


for the relationship between frugivo


ies


diversity and abundance and the number


of plant


species


in fruit...........


Table


Relationship of mammal-bird fruits


and bird-fruits to


seasonal fruiting patterns..........35


Table


2-7.


Relationship of


evergreenness to


seasonal fruiting patterns for bird-dispersed


plants of San Felasco Hammock..


Table


2-8.


Seasonal relationships of ripening


characters for bird-dispersed plants of San


Felasco Hammock............


Table


2-9.


Spearman rank


correlation coefficients,


rg for ripening characters.......


Table 3-1.


Relationship of


fruit traits to seasonal


fruiting patterns of bird-dispersed plants of
San Felasco Hammock....................................61


31


.39


.42


.43














LIST OF FIGURES


Figure 2-1.


Number of frugivorous bird


species


observed along census route from April 1982


through May


1984 in


San Felasco Hammock................21


Figure


2-2.


Number of frugivore individuals


observed along
through May 19


census route from April 1982


84 in


San Felasco Hammock................ 24


Figure


2-3.


Standard deviation of frugivore


numbers for birds observed along
from April 1982 through May 1984


census route


in San Felasco


Figure


2-4.


Number of bird-dispersed plant


spec


with ripe fruit in San Fela


SCO


Figure 3-1.


Fall fruiting species.


Pmock. ................30

Percent


of the initial total number of fruits removed
within a single week for Cornus foemina,
Callicarpa americana, and Aralia spinosa...............71


Figure


3-2.


Fall-winter fruiting species.


Percent


of the initial total number of fruits removed
within a single week for Viburnum rufidulum,
Viburnum obovatum, Symplocos tinctoria,
Ilex decidua, Smilax bona-nox, and Smilax
auriculata.............................................73


Figure


3-3.


Winter fruiting sp


ecies.


Percent


of the initial total number of fruits removed


within a single week for


Ilex


opaca


Prunus caroliniana.....................................78


HBIILP1OCk r











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



MUTUALISTIC INTERACTIONS BETWEEN BIRDS AND FRUITS
IN A NORTHERN FLORIDA HAMMOCK COMMUNITY


By


Stewart T. Skeate


August, 1985


Chairman:


John W. Hardy


Major Department:


Zoology


The ecological relationships between frugivorous birds

and bird-dispersed plants have been unexplored at lover


latitudes in North America.


interactions between


This paper examines


bird species and 45 species of bird-


dispersed plants in a northern Florida hardwood hammock


community from January


1982 to May


1984.


Seasonal


patterns


of frugivore availability, fruiting phenology, and fruit

characteristics were determined and compared.

Frugivore species diversity and abundance were highest

during the fall and winter months and lowest in the spring


and summer.


Increases


in frugivore numbers and diversity


were


attributed to the presence of migrant thrushes in the











abundance.


Spring and summer months showed the lowest


number of fruiting species and fall and winter the highest,

with a peak of 28 species in fruit in December.

Fruiting patterns of plant species fell into four


seasonal groups:


summer fruiting, fall fruiting, fall-winter


fruiting,


and winter fruiting.


Nine species showed summer


fruiting,


bearing ripe fruit between early spring and late


summer.


Summer fruits were


characterized by high water and


carbohydrate content,


large fruit mass, and low persistence.


The 12 fall fruiting species ripened fruit at the peak of


frugivore migration through northern Florida.


Fall fruiting


species were common or abundant in the community and


included


species with high lipid fruits.


The 20 fall-


winter fruiting species produced highly persistent fruits

that were available to migrant frugivores through fall and


winter.


These species were typically


evergreen and included


species with high lipid fruits.


The 4 winter fruiting


species matured fruit in December and depended on


overwintering birds for seed dispersal.


All


4 species


produced persistent,


lipid fruits.


The bird-fruit dispersal system of the lower temperate


latitude hammock community shows similarity


in fruiting


patterns and fruit characteristics to middle latitudes of


North America.


Mild winters,


the presence of evergreen















CHAPTER ONE
INTRODUCTION


The importance of birds


many plant speci


seed dispersal agents for


has long been recognized (Grinnell 1897,


Proctor

1949).


1897, Ridley

Nonetheless,


1930, McAtee 1947, Krefting and Roe

only within the last ten years have


researchers examined in depth the relationships between


frugivorous birds and bird-dispersed plants.


Early studies


of bird-fruit interactions typically involved species

records of birds that were observed visiting fruiting trees

(Petrides 1942, Sutton 1951, Land 1963, Willis 1966, Leck


1969,


Cruz 1974


and did not discuss possible mechanisms of


bird-fruit relationships.


Snow (1971) and McKey (1975)


first speculated on possible


coevo


lutionary trends between


fruit-eating birds and plants,


and presented a theoretical


framework of bird-fruit relationships for future workers to

investigate.

Bird-fruit interactions have also been of considerable


interest to botanists from evolutionary,


eco


logical, and


morphological standpoints.


Botanists agree that zoochorous


seed dispersal has an ancient evolutionary history, probably


n'r~i ainat*i nc in -t-rnni 1 anv4~ranmnn-t-a Flrt a vV n


1 aflY!


''












edible portion, an outer protection against


eating,


premature


an inner protection of the seed against digestion,


colors that signal maturity,


lack of odor, permanent


attachment, absence of hard rind, and seeds exposed or


dangling in hard fruits.


These adaptations are highly


variable among bird-dispersed plants.


This


surprising considering the widespread occurrence both

geographically and taxonomically of fruits adapted for bird


dispersal


(Snow


1981,


Wheelwright et al.


1984).


Recent field studies have examined various aspects of


bird-fruit coevolution,


including interactions between


individual plant species and their dispersers


1980,


Howe 1977,


1981, McDiarmid et al. 1977, Howe and DeSteven 1979,


Howe and Vande Kerckhove 1980,


1981, Herrera 1981b, Herrera


and Jordano 1981); nutrient quality of fruit (Foster


Stiles 1980, Sorensen 1981, Herrera 1981a,


1977,


1982b, Stapanian


1982,


White and Stiles unpub.


ms.);


importance of fruit


color and morphology to dispersal


Turcek 1963, Stil


1982,


Willson and Thompson 198

Denslow and Moermond 198


Morden-Moore and Willson 198


, Janson 1983, Willson and Melampy


1983


, Levey


, Moermond and Dens low 1984)


relationship of


seed dispersal


to succession (Smith 197


Thompson and


Willson 1978, Debussche et al. 1982, McDonnell and Stiles


,rvQ\


- a -


r _


LI-- 4..~. It nnh













of bird-dispersed plants (Snow


1962,


Thompson and Willson


1979, Herrera 1982b,


1984a,


Wheelwright,


in press).


These studies


have spawned a "second generation" of


review pap


ers


on the coevolution of seed dispersal systems


Stiles


1980,


Wheelwright and Orians 198


Howe and


Smallwood 198


Janzen 1983).


These papers have contributed


to the theoretical framework of bird-fruit research, but


have also questioned existing the


ories


on bird-fruit


coevolution (


see


Wheelwright and Orians 1982).


The field of


seed-dispersal biology


other related fields such


in its infan


cy and lags behind


as pollination biology.


Clearly


more detailed field studies are needed in both tropical and


temperate


areas.


Temperate Bird-Fruit Dispersal Systems


The study of coevolved relationships between bird-

dispersed plants and frugivorous birds in temperate regions

has received considerable attention since Snow (1971) first


discussed possible temperate


e fruiting patterns (Thompson and


Willson 1979,


Stiles


1980, Herrera 1981a,b


, 1982a,b,c,


1984a,b, Herrera and Jordano


1981


Jordano


1982,


Sorensen


1981, Stapanian 1982, Johnson et


1985).


relationship between the time of fruiting by bird-dispersed









4


patterns of frugivore presence may be the primary selecting

force influencing mid-latitude fruiting patterns in North


America.


They recognized three mid-latitude fruiting


patterns:


summer, fall, and winter fruiting,


in which the


respective fruiting patterns showed distinct adaptations to


differing levels of frugivore availability.


was the most common pattern,


Fall fruiting


coinciding with the peak of


avian frugivore migration.

To date, field studies of temperate bird-fruit

dispersal systems in North America have been made at middle


latitudes,


north of the usual wintering grounds of most


major avian frugivores (Sherburne 1972


, Thompson and Willson


1979, Baird 1980, Johnson et al.


1985).


The relationship


between frugivorous birds and bird-dispersed plants at


lower


temperate latitudes in North America has been unexplored.


Lower temperate latitudes differ from higher


latitudes in


their bird-dispersed flora and in seasonal diversity and


abundance of frugivorous birds.


This suggests that


differences in fruiting patterns may be evident between

middle and lower temperate latitudes in North America.


Thompson and Willson (1979) suggest that


both summer and


winter fruiting patterns should be more profitable at


lower


temperate latitudes due to the greater availability of












1984a,b).


The majority of bird-fruit studies have involved


dispersal strategies of individual plant species (e.g. Howe


1977,


1981, McDiarmid et al. 1977, Howe and Vande Kerchove


1980, 1981, Herrera and Jordano 1981, Jordano 1982).


dealing with single plant species may mis


Studies


s significant


factors in the evolution or ecology of bird-fruit systems,

factors that may be evident only through research at the


community


level


(Herrera 1984a).


In this study


I examine the bird-fruit system,


involving 45 species of bird-dispersed plants and


frugivorous bird species,

hammock forest community.


in a northern Florida hardwood

Four seasonal fruiting patterns


are analyzed in the context of their relationship to

frugivore availability, ripening synchrony, fruit abundance,


habitat, and evergreenness.


I also compare the bird-fruit


systems of middle and lower temperate latitudes of North

America in an attempt to derive a more complete picture of


bird-fruit interactions


in eastern North America.


Nutritional Properties of Temperate Fruits


The nutritional composition of fruits has been a major

focal point in the study of temperate zone bird-fruit


dispersal systems (Sherburne 1972, Stiles 1980,


Sorensen













content and that this

ripening patterns. H


is roughly related to seasonal


igh reward fruits are produced during


peak periods of frugivore availability, and the nutritional


properties of the fruits


are


correlated with the seasonally


changing demands of their major dispersers


Stiles


1980,


Herrera 1982a,


White and Stiles unpub.


ms.).


Bird-dispersed plants are therefore under some

selection pressure to produce fruits that are nutritionally


attractive to frugivorous birds.


By inducing birds to eat


their fruits and then to regurgitate or defeat


the seeds


intact


(see


Snow


1971),


plants obtain an effective method of


seed dispersal away from the parent plant.


This dispersal


may result in lower seed and seedling mortality (Janzen

1970, Hove and Primack 1975), reduced seedling competition


(Connell 1971, Harper


1977), increased gene flow (Levin and


Kerster


1974),


and dispersal


to new habitats


Smith 1975).


The nutritional reward offered by


a plant in its fruit may


also be related to the quality of


seed


dispersal by birds


(Snow


1971, McKey


, Howe and Estabrook 1977, Howe and


Vande Kerckhove 1980,


see


Wheelwright and Orians 1982).


The actual nutritional reward in a fruit


determined


by its dry mass content of carbohyd


rates,


proteins


lipids.


The latter two elements, howe


ver,


appear to be the












attractiveness of


a fruit.


Therefore,


in addition to the


chemical


(i.e.


nutritional) properties,


the structural


"design" features


(Herrera 1982a) of


a fruit may be


important to a fruit-eating bird and may affect rates of

fruit removal and digestive processing (White and Stiles,


unpub.


ms.).


Structural


fruit traits that may be important


to birds include pulp moisture (Herrera 1982a), seed size


and number (Sorensen 1984),


taste (Stiles


1980,


Sorensen


1983), fruit mass (Moermond and Denslow


1983),


fruit


diameter (Wheelwright 1985


, presence of secondary compounds


(Herrera 1982b), and fruit color (Turcek 1963, Morden-Moore

and Willson 1982, Willson and Thompson 1982, Willson and


Melampy


1983).


Therefore,


the attractiveness and


profitability of any fruit to a bird is directly related to


the combination of


chemical and structural components of the


fruit


(Herrera


1982a).


The design and chemistry of fruits, by themselves,

reveal relatively little about the evolution of bird-fruit


dispersal systems.


Only when this information is examined


in the context of other community parameters can


evolutionary patterns be discerned.


characteristic


Here, I report on fruit


of 43 species of bird-dispersed plants in a


northern Florida hammock forest community.


Fruit


characteristics analyzed are fruit mass. seed mass.


total










8


nutritional standpoint and have been analysed in other

studies (Stiles 1980, Sorensen 1981. Herrera 1982a, White


and Stiles unpub.


ms.).


I discuss the relationship of the


nutritional content of fruits to seasonal ripening,


fruit


removal rates, frugivore availability, and fruit


abundance.


I also compare these result


s with the fruiting


patterns described by Stiles (1980) and White and Stiles


(unpub.


ms.) for bird-dispersed plants of


eastern North


America.


These studies have developed a framework for the


study of bird-fruit dispersal systems for eastern North

America and allow comparisons of fruit characteristics


between middle and lower


latitudes.














CHAPTER TWO
SEASONAL PATTERNS OF FRUGIVORE
AVAILABILITY AND FRUIT RIPENING



Study Site and Methods


Study Site


San Felasco Hammock State Preserve (29045'N, 8230'W),


in Alachua Co., Florida,


covers 2306 hectares and includes


a variety of plant communities, including the largest

protected stand of climax mesic hammock in the state of


Florida (Dunn 1982).


This area is characterized by moderate


winters (15-20C average temperatures) and hot summers


(300C average temperature).


Rainfall is variable in its


seasonal distribution, although more than half the annual

rainfall (average 1370 mm) occurs between June and September

(Dohrenvend 1978).

This study focused on the mesic hammock community,

which consists of 129h hectares of rolling hills, plateaus,


and stream valleys within San Felasco Hammock.


mesic hammock refers to


The term


a mixed hardwood forest situated


within a region where the predominant vegetation


marsh, or pine forest (Harper 1905).


prairie,


Mesic hammock












community may be found in Laessle (1958),


Delcourt and Delcourt (1977),


Monk (1965),


while analysis of the plant


communities and flora of San Felasco Hammock may be found in


Ansley (1952) and Dunn (1982).


Dominant canopy trees within


this community include Quercus


laurifolia, Q.


virginiana,


glabra,


tomemtosa, Magnolia grandiflora, Persea


borbonia, and Liquidamber styraciflua.


The mixed deciduous-


evergreen nature of this community is especially evident


during the winter months,


when the forest becomes a mosai


of evergreen and leafless broad-leaved trees.


Plants with


bird-dispersed fruits make up approximately one-half of the


vascular flora of San Felasco's mesic han

They are especially evident among shrubs,


mock (Table 2-1).


understory trees,


vines.


The Frugivores


I censused avian frugivore abundance and species


diversity from January


community.

twice weekly


1982 to May


I walked three separate

, one-half hour after s


1984 in the mesic hammock

700 m line transects

sunrise, during which all


birds


seen


or heard for 40 m to


either


side of the transect


line were recorded.


I determined 40 m to be an effective


maximum distance for all


seasons


, particularly in the


a













TABLE 2-1.


Fruit types of vascular plants found in San


Felasco Hammock State Preserve, Alachua Co., Florida.

Life Form Fleshy Fruits (%) Dry Fruits (%) Total Spp

Canopy Trees 4 (25) 12 (75) 16
Understory Trees 10 (67) 5 (33) 15
Shrubs 13 (93) 1 (7) 14
Vines 10 (63) 6 (37) 16
Herbs 4 (21) 15 (79) 19

Total Species 41 (51) 39 (49) 80









12



the birds during the summer months permitted an accurate


census of their numbers.


I combined data from the three


transects to obtain a single daily count.


Mean values of


four daily transects over a two-week period were calculated,


resulting in two values per month for abundance and

diversity.


species


Fruit-eating birds


were


determined to be


by direct


observation during bird and fruit censusing.


Only birds


that swallowed entire fruits and that voided seeds intact


were classified


frugivores.


The term frugivore refers


only to birds that disperse


seeds


(Snow


1971, Morton 1973).


Birds that chewed fruits,


swallowing only the fruit pulp and


dropping the


seeds


below the parent


plant, were considered


"fruit-thieves"


parent


they did not disperse


plant (Howe and Estabrook 1977).


seeds away from the

I differentiated


major frugivores from minor frugivores by the quantity of


fruit eaten,


the number of plant


species


visited, and the


observed frequency of each species during weekly censuses.



The Plants


I collected phonological data on 4


bird-dispersed


plant


species


in a 332


area


of mesic hammock by


monitoring ten individual plants per


species


when possible.













dates


of first ripe fruit and disappearance of all fruit for


each individual.


I collected fruit ripening data for 27


species (24


,238


fruits and 250 plants) in 198


and for


species (12,390


fruits and 180 plants) in 1983-84.


Weekly counts of ripe


and unripe fruits were taken from tagged branches of ten


plants per species when possible.


I tagged approximately


equal numbers of fruits for each individual of a particular


species.


The number of ripe fruits was corrected for fruit


removed; I assumed that removed fruit were ripe.


fruit ripening


Prior to


, I made fruit crop counts for each individual


by direct count or extrapolation from fruit on a few

branches and the total number of branches on the tree.

I analyzed ripening data by four measures: 1) between-


plant ripening


the number of days for all marked


individuals to show 90% ripe fruit


2) population ripening


number of days for the total fruit crop to reach 90%


ripe fruit;


individual plant ripening


the mean number


days for the marked individual plants of each species to


reach 90% ripe fruit;


4) population synchrony index


determined from a composite measure of individual synchrony.

Individual synchrony measures the overlap of a given


individual's


ripening period


(90% ripe fruit


with those of












population.


This measure of


population ripening synchrony


is a modification of Augspurger's method


determination of


(1983) for


flowering synchrony.


I measured the abundance of the bird-dispersed plant


species


using a belt transect technique.


number of individual plants


I counted the


of each species within


belt


transects measuring 100 m X 10 m along a


through the study area.


km line transect


Only individuals judged to be


capable of fruit production were counted.


Fruiting species


were then categorized as abundant,


common,


uncommon,


rare


, based on their censused frequency,


fruit crop


size,


and observed percentage of individual


s fruiting within the


population of


each spec


ies.


In addition to fruiting records, I recorded flowering

dates for the 45 bird-dispersed species by observation of


plants within the study area.


The flowering to fruiting


duration was the time between the date of first flowering

and the appearance of bhe first ripe fruit for each species.



Results and Discussion


The Frugivores


The frugivorous birds I observed in San Felasco Hammock














TABLE


2-2.


Avian frugivores observed at San Felasco


Hammock during censuses.


Major frugivores are marked


by asterisk.


Picidae
Red-bellied Woodpecker (Melanerpes carolinus)*


Code
1


Northern Flicker (Colapt


auratus )*


Yellow-bellied Sapsucker (Sphyrapicus various *
Pileated Woodpecker (Drycocopus pileatus)
Tyrannidae
Acadian Flycatcher (Empidonax virescens)
Eastern Phoebe (Sayornis phoebe)
Sylviidae


Ruby-crowned Kinglet


(Regulus calendula)


Mimidae
Brown Thrasher (Toxostoma rufum)
Gray Catbird (Dumetella carolinensis)*
Turdidae
American Robin (Turdus migratorius)*
Veery (Catharus fuscescens)*


Wood Thrush


(Hylocichla mustelina)*


Hermit Thrush (Catharus guttatus)*
Swainson's Thrush (Catharus ustulatus)*
Gray-cheeked Thrush (Catharus minimus)*


Eastern Bluebird


(Sialia sialis)


Bombycillidae
Cedar Waxwing (Bombycilla cedrorum)*
Vireonidae
Red-eyed Vireo (Vireo olivaceous)
White-eyed Vireo (Vireo griseus)
Solitary Vireo (Vireo solitarius)
Yellow-throated Vireo (Vireo flavifrons)
Parulidae
Yellow-rumped Warbler (Dendroica coronata)*












by these birds and by their observed frequency during


the weekly cenuses


(see


Methods).


Thus the Eastern Bluebird


(Sialia sialis),


while showing a relatively high number of


fruit visits,


was not considered a major frugivore in the


community as it was observed only twice in the study area


during the two-year censusing period.


Major frugivores


accounted for 96.9% of the total observations of frugivory

(one observation=one feeding bout) and 97.4% of the total


visits (one visit=one fruit


eaten)


(Table


-3).


Fruit thieves, birds that ate only the pulp of the

fruit, dropping the seeds, included the Northern Cardinal


(Cardinalis cardinalis,


Summer Tanager (Piranga rubra),


Rose-breasted Grosbeak (Pheucticus


cardinalis).


American Robins (Turdus migratorius) showed the highest

number of fruit visitations among the major frugivores.

Wintering robins were responsible for 57.2% of the total


visits,


while Cedar Waxwings (Bombycilla cedrorum) accounted


19.8% of the total


visits (Table


These figures


are derived from the total number of visits over a two year


period and may not reflect the importance of any


single


frugivore at one time of the year.


(Catharus fuscescens),


Thus transient


while accounting for only


Veerys


7.6% of the


total


visits,


were the most important frugivores within the


hammock


community in the early fall orior to the arrival of













TABLE


2-3.


Observed frugivory by major and minor frugivores


in San Felas
feeding bout


Hammock, Florida.


one


visit=one


fruit


One observation=one


eaten.


No. of
Observations (%)


Bird


No. of


No. of


Visits (%) Spec


Major Frugivores


Northern Flicker


Red-bellied Woodpecker
Yellow-bellied Sapsucker
Gray Catbird
Cedar Waxving
Veery
Wood Thrush
Hermit Thrush
Swainson's Thrush
Gray-cheeked Thrush
American Robin
Yellow-rumped Warbler


30 (1.21)
30 (1.21)
22 (0.89)
19 (0.77)
42 (13.77)
22 (4.91)


1556 (
142 (


.64)
72)


306 (1.16)
240 (0.01)
268 (1.01)
180 (0.68)
5245 (19.79)
2023 (7.63)
317 (1.20)
207 (0.78)
825 (3.11)
158 (0.60)
15165 (57.22)
889 (3.35)


Total


2406 (96.85


(97.43)


Minor Frugivores


Pileated Woodpecker
Acadian Flycatcher
Eastern Phoebe
Ruby-crowned Kinglet
Brown Thrasher
Eastern Bluebird
White-eyed Vireo
Red-eyed Vireo
Solitary Vireo
Yellow-throated Vireo


8 (0.32)
1 (0.04)
3 (0.12)
13 (0.52)
7 (0.28)
19 (0.77)
4 (0.16)
15 (0.60)
6 (0.24)
2 (0.08)


120 (0.45)
10 (0.04)
4 (0.02)
81 (0.31)
73 (0.28)
260 (0.98)
37 (0.14)


16 (0.06)
7 (0.03)


Total


.14)


680 (








18


The number of frugivores in residence during each


season


shown in Table 2-4.


Only two major frugivores,


the Red-bellied Woodpecker (Melanerpes carolinus) and the


Wood Thrush (Hylocichla mustelina),


were present in San


Felasco Hammock during the summer.


rare summer resident.


The Wood Thrush is a


The number of major frugivore species


increased in the fall and winter;

and five were winter residents.


four were fall transients

Migrants played a dominant


role within the frugivore guild of thi


community.


Migrants


constituted 82% of the total number of frugivore species and


92% of the major frugivore species.

responsible for 98.2% of the total


plants, involving 30 plant species.


Migrants were

visits to fruiting


Furthermore,


Eastern Bluebird (Sialia sialis) and Northern Flicker


Colaptes auratus),


while year-round residents in northern


Florida,


appeared in the hammock community only during the


fall and winter and were classified


"immigrants."


Frugivore Diversity and Abundance


Frugivore and major frugivore species diversity,


remained low throughout the summer months,


which


increased in late


September,


reach


thing a peak in mid-October in both


years


(Fig.


2-1).


This increase was due primarily to the
















TABLE 2-4. Resident status of avian frugivores at San
Felasco Hammock, Florida.


Year-round Summer Winter Fall
Residents Residents Residents Transients Total


All
Frugivores 4 4 10 4 22

Maj or
Frugivores 1 1 6 4 12




































Co
ow
r4cd


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-a





















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or-


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remained in San


Felasco


Hammock through October and departed at


the end of the month.


At this time,


wintering Robins,


Hermit


Thrushes,


Yellow-bellied Sapsuckers (Sphyrapicus various ,


flickers,


and Yellow-rumped Warblers (Dendroica coronata)


arrived in the area.


Frugivore


species


diversity remained


high throughout the winter,


early April,


decreasing from late March to


when the wintering frugivores left the hammock.


Avian migration through San Felasco Hammock during the


spring months was much


less


pronounced than fall migration,


and frugivore diversity increased only slightly in the

spring.

Frugivore abundance showed a pattern similar to that

of frugivore species diversity: the number of frugivore


individuals remained low during the summer months,


in September


increased


, and reached a first peak in mid-October of


both


years


Fig.


2-2).


A second peak was evident in both


years, in mid-November in 1982 and mid-December in 1983.

The first pulse of frugivore migration was due primarily to


the arrival of migrant thrushes,


while the second was due to


the arrival of wintering robins, Cedar Waxwings, Hermit


Thrushes


, and Yellow-rumped Warblers.


In 1982, robins


arrived in large numbers in early November,


large


while in 1983,


flocks of robins were not observed until mid-


December.


Cedar Waxwings


were


erratic


in their


occurrence





































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Fig.


2-3.


Standard deviation


values


increased in early


fall,


reaching their


greatest


values in the late fall and


early winter,


values.


while the summer months showed the lowest


The high standard deviations evident in the late


fall and winter months reflect the unpredictable nature of


wintering frugivores


within


as a res


ource for fruiting plants


the hammock community (Stapanian


1982).


There was no


significant difference in major frugivore


species


diversity


Wilcoxon's Matched Pairs Signed-Ranks


Test,


P>0.05) or frugivore


species


diversity (Wilcoxon's


Matched Pairs Signed-Ranks Test,


P>O.05) between


1982-3


3-4.


There was also no significant difference in major


frugivore abundance (Wilcoxon's Matched Pairs Signed-Ranks


Test,


P>0.05) or frugivore abundance (Wilcoxon's


Matched


Pairs Signed-Ranks


Test,


P>0.05) between the two


years.


However,


there


was


a significant difference in major


frugivore and frugivore abundance from September through


March for the two


years


(Wilcoxon'


s Matched Pairs Signed-


Ranks Test,


P

due to the higher number of frugivo


observed in the fall and winter of


1982-83


compared to 1


983-


(see


suggest


that the


lower numbers


wintering frugi


vores


in 1983-84


were


due to the small fruit


crop of Cornus florida in


1983


(see


below),


which attracted


fewer


robins to the study


site.


1982-83


the mean flock


res





























































Irr-


wow
~OH
W~r4


O~G)
























































































-


0)


cy











to available fruit crops (Speirs 1946,


Thompson and Willson


1979).



The Plants


The number of plant sp


ecies


with ripe fruits from April


1982 through March 1984 is shown in Fig. 2-4.


The lowest


number of species with ripe fruit occurred during the spring


and summer.


The number of species in fruit began to


increase in late August and continued to increase through


the fall, reaching a peak of


December.


8 species in fruit in


The number of fruiting species remained high


throughout January,


and began to decrease


in February.


There was no significant difference in the number of


species


in fruit per census period between 19


82-3


and 1983-4


(Wilcoxon's


Signed-Ranks


Test,


P>O.05).


There


was


significant correlation between the number of fruiting

species per census and major frugivore species diversity,


frugivore species diversity, major frugivore abundan


frugivore abundance (Table


There was a significant


difference in the flowering to fruiting interval between

summer fruiting and fall and winter fruiting species (Mann


Whitney U-Test;


Z=2.71,


P

cause


seasonal


fruiting


patterns are independent of seasonal flowering patterns,


iii t~irnt~s timinn nf fri4 +4 na c nnva, ~ n~aan








































V
C4
Sri
L4
0
'CO
rl%-4




*r4$..
00


to
0~
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H



00
wc


Cd
to.
~ ..h4






'U
r4.4OZ
00



,oWO
'C



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o Ca~
In-4H
c'J
-J

















2
q~*.

0)


0)


CJ














TABLE


2-5.


for the rela


Spearman rank correlation coefficients, r ,
tionship between frugivore species diversity


and abundance and the numb


of plant


species


in fruit per


two-week census period in San Felasco Hammock.


1982-83


1983-84


of Species
in Fruit


of Species
in Fruit


Major Frugivore
Species Diversity


0.846**


0.784**


Frugivore


Species


Diversity


0.838**


0.841**


Major Frugivore
Abundance


Frugivore
Abundance


0.855**


0.879**


0.787**


0.673**


** P<0.01.













were


78.4 d (N=9) for summer fruiting


species


and 142.1 d


(N=36) for fall and winter fruiting species.


The majority of shrub and vine


species


produced ripe


fruits annually,


whereas a number of tree species only


fruited heavily in alternate years or every three years.


latter fruiting behavior was evident in Cornus florida,


Persea borbonia, and Nyssa sylvatica.


Cornus florida had


large fruit crops in 1982 but small crops in 1983,


when


isolated branches of individual trees produced flowers and


fruits.


Persea borbonia had large fruit crops in 1981, but


very small fruit crops in 19

individuals produced fruit.


and 1983, when only a few


Most Nyssa sylvatica


individuals produced ripe fruits in 1981 and again in 1983,


but only a few individuals bore fruit in 1982.


The small


fruit crop of Cornus florida in 1983 appeared to be a major


factor in the lower number of frugivores


seen


in the fall of


1983 compared to 1982,


when Cornus florida was a major


source of fruit for a number of frugivore species.


Persea


borbonia may also affect frugivore abundance due to its


potentially


large fruit crops and lipid rich fruits.


that showed high annual varis

included Symplocos tinctoria,


Ltion in fruit crop


Ilex


Shrubs


size


decidua, and Crataegus


viridis.


'S J -


O








33


important factor in the proximate timing of fruiting (see


Appendix II).


Symplocos tinctoria showed the greatest


annual variation in ripening times,


as this species ripened


fruit in late July of 1982, but not until early October in

1983.



Fruiting Patterns


I have classified the 45 species of bird-dispersed

plants in the hammock community into four seasonal fruiting

patterns based on observed seasonal fruiting phenologies


(see Appendix II).


These include summer fruiting, fall


fruiting, fall-winter fruiting, and winter fruiting.



Summer Fruiting


Nine species produced ripe fruit from early spring to


late summer, before the arrival of fall migrants.


subgroups were evident; Vaccinium mrysinites, Smilax

smallii, Rubus cuneifolius, and Morus rubra had ripe fruit

in the spring and early summer, while Chionanthus

virginiana, Prunus angustifolia, P. serotina, Vitis

aestivalis, and V. rotundifolia had ripe fruit in the late


summer.


The average fruiting duration for summer fruiting


species was 64.9 d.












(Stiles


1980).


There is a decrease in the number of


"mammal-bird" fruits from summer to fall


to winter (Table


The predominance of mammal-bird fruits during the


summer suggests that birds are unreliable seed dispersers at

this time, and mammal-bird fruits may have evolved to


increase the dispersal coterie of these plants.


unreliable nature of birds


summer is most likely due to t]


diversity at


dispersal agents during the

heir low abundance and


this time and to their preference for abundant,


protein-rich insects as a food source


e (Morton 1973).


Summer fruiting species consisted primarily of uncommon

and rare fruiting species, with only two, Rubus cuneifolius

and Vitis rotundifolia considered common in the study area.


In contrast,


of the 36 fall and winter fruiting species


were either abundant or common in the study area (see

Appendix II).

Summer fruiting species typically occurred along second


growth forest edge and in gaps within the forest.


Only two


summer species, Smilax smallii and Chionanthus virginiana,


were found within the closed forest,


whereas 28 of the


fall and winter fruiting


species


were forest inhabitants.


Few frugivores visited second growth habitats in the hammock


during the summer.


The two major frugivores present during


ths ~iimmsr ths Pnd~hnl 1innWnnefn nn T'ru ir


t~F~p


1















TABLE


2-6.


Relationship of mammal-bird fruits and


bird-fruits to seasonal fruiting patterns in San Felasco
Hammock, Florida.


No. of Species


Fruiting Pattern


Mammal-Bird Fruits (%)


Bird Fruits (%)


Summer Fruiting


7 (77.8


Fall Fruiting

Fall-Winter Fruiting

Winter Fruiting


I (8.3)

1 (5.0)


11 (91.7)

19 (95.0)


0 (0.0)


4 (100.0)


Total 9 36









36


erythrophthalmus), which may be considered fruit-thieves or


seed predators.


However,


I have observed cardinals


on these fruits and dropping the seeds intact,


while feeding only on the pulp.


If a cardinal moves the


seed away from the parent plant, even a short distance,


effective dispersal may result.


Also,


Thompson and Willson


(1979) have found that while cardinals crush the large seeds


of Lindera benzoin,


the small seeds of Sambucus canadensis


are


passed


unharmed.


Finally,


the tendency of plants inhabiting disturbed


habitats to fruit early may result from the importance of

rapid reproduction and dispersal due to the colonizing


nature of these plants.

reaching maturity, rega


Such plants may reproduce upon


.rdless of the time of year (Janzen


1967).


Forest plants may not be under such


constraints and


may delay fruiting until the fall or winter.



Fall Fruiting


The 12 fall fruiting specie


s (see Appendix II) yielded


ripe fruits during September and October, at the peak of

fall bird migration through northern Florida. The average


duration of fall fruiting


species


was


74.1 d.


Fruit


disappearance typically occurred by January.


"chewing"









37


important than the second in the evolution of fruiting


phenologies,


due its greater predictability and higher


species


diversity.


Certain fall fruiting


species,


such


Amelopsis arborea, Aralia spinosa, Cornus foemina, Magnolia

grandiflora, Parthenocissus quinquefolia, and Phytolacca

americana have their fruit dispersed almost exclusively by


the first pulse,


their fruit crops are exhausted by the


time the second wave arrives.


Other fall fruiting species,


including Cornus florida, Crataegus marshall,


Crataegus


uniflora, Callicarpa americana, and Arisaema dracontium,


still ha


fruit available for the second pulse.


Fall fruiting species are predominately "bird" fruits


(Table


), although Crataegus uniflora and Crataegus


viridis, a fall-winter fruiter,


appear to be adapted for


dispersal


primarily by mammals.


These fruits exhibited poor


persistence,


often falling to the ground while still green.


The ripe fruits are probably


located by smell by ground


foraging mammals.



Fall-Winter Fruiting


The fall-winter fruiting pattern was the most prevalent


fruiting pattern in the hammock,


occurring in twenty


species.


These


species


produced ripe fruits during the fall













This fruiting pattern


synchronized with the first


and second pulse of migrant frugivores.


The highly


persistent nature of these fruits may be an adaptation to

the unpredictable nature of wintering frugivores in time and


space (Stapanian 1982). Persist

fruit quality and removal rates,


ence may also be related to


low quality fall-winter


fruit


s show


low removal rates (see Chapter


iii ).


Many of


these species have ripe fruit in the fall, but do not have

their fruits removed until January or February.

Fall-winter fruiting species consist of a higher


proportion of evergreen sp


fruiting spec


ecies


(Table 2-7).


than summer or fall


The fruits of most evergreen


species persist or ripen after the deciduous trees in the


community have lost their


leaves in late November.


The possession of persistent fruits or delayed fruit


ripening in evergreen


basis,


species may have a physiological


in that the evergreen condition allows for


maintenance of


persistent fruits or continued photosynthate


buildup for maturing fruits.


The abundant fall-winter fruit


production in the scrublands of southern Spain has been


attributed in part to the predominance of evergreen


species


within this community (Herrera


1982a,


1984a).


Evergreen


species


with persistent fruits are also


I............ *r a a


r r r r r















TABLE 2-7.


Relationship of evergreenness to seasonal


fruiting patterns for bird-dispersed plants of San
Felasco Hammock, Florida.


No. of Species


Fruiting Pattern


Dec iduous


Evergreen


Summer; Fall Fruiting

Fall-Winter; Winter Fruiting


Total 25 20


Note


- For


contingency: X2=12.3, P<0.005












leaves of these species may act


(Stiles 1982), and a

to trees with leaves


foliar fruit flags


vian dispersal agents may be attracted


possible sources of fruit.


Winter Fruiting


The winter fruiting pattern was shown by four evergreen


species


(see Appendix II).


In these species,


fruit ripening


did not occur until December, at which time the majority of


wintering frugivores had arrived in Florida.


The average


fruiting duration of winter fruiting species was 87.8 d.

These fruits showed high persistence and low spoilage.

Important winter fruiting species included Prunus


caroliniana and Phoradendron serotinum.


Prunus caroliniana,


a common tree along forest edges,


provided an abundant food


supply for wintering robins and woodpeckers, whereas


Phoradendron serotinum constituted 70.5% of the total


visits


to fruiting plants by wintering waxwings.


There was a close


relationship between fruit ripening in Phoradendron


serotinum and the arrival


of waxwings at San Felasco


Hammock.


In 1982 and 1983,


Phoradendron serotinum fruits


ripened in mid-December,


observed in


at which time waxwings were first


the area.


Winter fruiting specie


s have


large ripe fruit crops at








41


provide wintering frugivores with low quality (see Chapter


III) but abundant,


supply


concentrated fruits at a time when fruit


is diminishing and frugivore metabolic needs are


increasing due to colder temperatures.


Delayed fruiting in


winter fruiting species may also be an adaptation for the


avoidance


of competition for dispersal agents in the fall,


when up to


spec


have ripe fruit.


Ripening Synchrony


There were no significant differences among the four

seasonal fruiting patterns in between-plant ripening,


population ripening,


population synchrony (Table


individual plant ripening, and


There was also no


significant difference in these characteristics between the


two years


(Mann-Whitney U-test,


P>0.05).


Between-plant


ripening, population ripening, and individual plant ripening


showed a significant positive correlation,

of population synchrony, Z, showed a signi

correlation to between plant ripening, pop


while the index


ficant negative

)ulation ripening,


and individual


plant ripening (Table


-9).


Therefore, low


values (low population synchrony) were associated with long

asynchronous ripening periods (high between-plant ripening,

population ripening, and individual plant ripening values).

































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TABLE


2-9.


Spearman rank correlation coefficients, r
so


for ripening characters


Correlation coefficients were


calculated from 1983-84 data from Table


2-8.


100/90% 90% x90% Z


100/90% 1.0000 -

90% 0.9705* 1.0000 -

x/90% 0.8662* 0.8524* 1.0000 -

Z -0.6994* -0.6936* -0.5006* 1.0000


* P











individual


ripening rates were 19.5 d (1982-83) and 14.8 d


(1983-84); and average population synchrony values were


Z --'S.


82-8


and


Z=0.62


(1983-84).


Individual species often differed greatly in the above


characteristics.


Between plant ripening rates ranged from 7


d (Smilax bona-nox) to


115 d


Symplocos tinctoria).


Individual ripening rates


varied from 7


d (Smilax bona-nox)


39.3


d (Symplocos tinctoria).


Population synchrony ranged


from


Z=0.32


(Symplocos tinctoria


Z=1.0


(Smilax bona-


nox).

The seasonal relationship of ripening synchrony

suggested by Thompson and Willson (1979), in which summer

fruiting species exhibit asynchronous between-plant ripening

and fall fruiting species show synchronous between-plant


ripening,

species.


was not evident for the northern Florida fruiting

Herrera (1984a) also has found no obvious


relationship between seasonality and ripening patterns in

the bird-dispersed plants of the scrubland community in


southern Spain. The extended availability of migrant

fruigivores at lower latitudes (September-November) may have


resulted in less selection pressure for synchronous fall


ripening


compared to more northern latitudes in North


America.


This


would be especially true for those


species











tendency for synchronized ripening.


Also, pronounced annual


variation in ripening rates for a number of species suggests

that proximate factors related to the physiology of fruit

ripening may play an important role in the length of the


ripening


periods.


Middle and Lower Temperate Comparisons


The phenological patterns of northern Florida bird-


dispersed plant


s and seasonal patterns of frugivore


availability show a logical relationship with tho


patterns described by Thompson and Willson (1979) in


Illinois.


Frugivore diversity and abundance were highest in


September in Illinois,

occurred in October.


while in Florida, highest values

The month-long difference would


reflect the movement of migrant frugivores from middle to


lower


latitudes.


The two


eptember peaks in frugivore


diversity and abundance in Illinois correspond to the two

peaks evident in northern Florida in October and November.

The first peak in both areas consisted primarily of thrush

species, while the second pulse consisted of robins, Hermit


Thrushes, and Yellow-rumped Warbler


The number of


species


in fruit in Illinois begins to


increase in August, reaching peaks in late August and











both areas correspond to periods of high frugivore


availability.


from upper to middle


likely that, as migrant frugivores pass

to lover latitudes in North America,


they encounter peaks of fruit production at each latitude.


As predicted by Thompson and Willson


1979),


the winter


fruiting strategy at lower temperate latitudes in North

America is more pronounced than at middle or upper


latitudes.


Twenty-four species of plants have ripe fruit


during the winter months in the hammock community,


compared


to only four speci


in Illinois.


High frugivore


availability, mild winters, and the presence of evergreen

species have made winter fruiting possible and profitable in


northern Florida.


Low frugivore abundance,


cold winters,


and the dominance of


deciduous species restrict winter


fruiting to only a few species at northern latitudes.

The second prediction of Thompson and Willson (1979),

that summer fruiting should be more profitable at lower


temperate latitudes, is not supported by this study.


absence of major frugivores, abundance of insects, and

potential problems with microbial spoilage apparently have

restricted summer fruiting to a relatively few species,


which may depend more on mammals for dispersal


than on


birds.


I suggest


that the summer fruiting strategy should


be more profitable at more northern latitudes,


where








47


accounts of adult thrushes feeding fruits to their young do


exist


(see


Bent


1949).


Lower Temperate Latitude Dispersal Systems


Possibly the most thorough single community analysis of


bird-fruit coevolution to dat


e has been made in the


scrublands of southern Spain (Herrera 1981a,b,


1982a,b,c,


1984a,b, Herrera and Jordano 1981, Jordano 1982, Jordano and


Herrera 1981).


imilarities between Florida and southern


Spain in seasonal frugivore availability make a comparison

of the bird-fruit system in these two areas worthwhile.

Southern Spain is a major flyway in the fall for transient


avian frugivor


migrating south to wintering grounds in


Africa, while during the winter it is home to a number of


overwintering frugivores (Herrera 1982a,

an analgous situation to that in Florida,


1984s4.


As this is


it is logical


that


similar phenological strategies related to dispersal should

be evident for the bird-dispersed plants in these two

regions.

Fruit-eating by birds in the scrubland community of

southern Spain appears to be limited to passerine species


(Herrera 1984a,b),


whereas in the Florida hammock community


four woodpecker species are significant consumers of fruit.












the passerine species in the hammock community.


Fruit


predators are also more prevalent in the scrublands,

69% of the fruit-eating birds are considered fruit


predators,


where


while only three species of fruit predator were


observed in the hammock community.


does the hammock community,


the scrublands has a


subset of major frugivores, consisting primarily of fall


migrants and overwintering species,


that is responsible for


most of the frugivory within the community (Herrera 1984a).

The major frugivores in the Spanish scrublands tend to be


smaller,


12-18g body mass (Herrera 1984a,b) than those in


Florida (40-100g body mass


and other North American forests


(Sherburne 1972; Stiles 1980; Rybczynski and Riker


1981).


Herrera (1984a) has attributed the absence of large

frugivores in this community to possible difficulties in

foraging for fruit in the dense scrub and to the prevalence

of fruiting displays involving thin stems and erect

infructesences.

The Spanish scrubland community shows a proportion of


bird-dispersed plant species,


49-66% (Herrera 1984a)


similar to that in the hammock community (approximately


0%).


The presence of


resident,


transient


overwintering frugivores in southern Spain and Florida has

resulted in the availability of fruit during every month of













attributed the prevalence of fall-winter fruiting in the

Spanish scrublands to the high degree of evergreenness and

mild winters that are characteristic of this community.

This is a similar situation to that in the hammock


community,


where mild winters have allowed the establishment


of such subtropical evergreen species


grandiflora,


Magnolia


Persea borbonia, Symplocos tinctoria, Osmanthus


americanus, and Prunus caroliniana.

Herrera (1984a) maintains that the scrubland bird-plant

dispersal system during fall and winter is driven by

relatively few pairs of strong reciprocal primary plant-bird


interactions (e.g.


Pistacia lentiscus-Sylvia atricapilla;


Viburnum tinus-Erithacus rubecula).


These highly nutritious


primary plants indirectly favor seed dispersal of low-reward

or rare coexisting plants due to the varied diets exhibited


by the primary frugivores.


Thus the plant species interact


via diet-sharing and form an interdependent dispersal guild

(Herrera 1984a).

There is also good evidence for the presence of primary

plant-bird interactions in the northern Florida hammock


community.


In the early fall,


when the Veery is the primary


visitor to these plants, Parthenocissus quinquefolia and

Aralia spinosa are the most frequently visited plants in the


n ~'n*' ~ O .b.In a- n ,. ni -n *. a I- 4.4


C ~t


rn












Parthenocissus and Aralia fruit crops are exhausted,


there


is a close relationship between Veerys and Cornus florida,


another high lipid fruit.


In November, after Veerys leave


the area, robins become the primary dispersal agent in the


hammock community.


During late fall and winter, robins


sequentially become the primary dispersal agent for a


of fruiting plants,


series


including Cornus florida, Persea


borbonia, and Prunus caroliniana.


At these times,


while the


majority of visits by robins are to these primary plants,

they also visit 15 other fruiting plant species.

A similar situation exists for the Cedar Waxwing and


the mistletoe,


Phoradendron serotinum.


The presence of


mistletoe fruits,


the waxwing


s principal food within this


community,


attracts the highly frugivorous waxwing to the


hammock community,

It does appear


where it feeds on

, therefore, that


fruiting species.


the bird-dispersed


plants of the hammock community form a dispersal guild,

dependent on a relatively few species of lipid-rich or


abundant fruiting species. Th

dependent on a few species of


Veerys and robins).


Lis dispersal guild is in turn

abundant frugivores (e.g.


The temporal sequence of primary plants


ensures frugivore abundance throughout the fall and winter


months and sugg


ests


possible temporal partitioning in


fruiting among the primary plant


species.


The importance of












significantly


lower than in 1982,


when Cornus florida showed


a large fruit crop.

Despite the similarities in fruiting patterns between


the hammock and scrubland communities,


physiognomic differences


communities.


climatic and


limit comparisons between these two


The Spanish scrublands receive approximately


one-half the annual rainfall of the hammock community and


have a drier summer.


Also,


the scrublands have a


continuous distribution of fruit-producing low shrubs


(Herrera 1984a),


while


the hammock community has a patchy


distribution of fruiting tr


ees,


shrubs,


vines.


Community analysis of bird-fruit interactions in the

southern California chaparral community of North America

should show patterns more similar to those found in the


Spanish scrublands, due to the similarity in the climate and

vegetation of the two areas.


Historical Considerations


It is


likely that mesic hardwood communities were


present in northern Florida throughout the Pleistocene,


when this area acted


as a possible glacial refuge for


northern deciduous trees (Delcourt and Delcourt


1981).


Glaciation over the past 80,000 years appears to have had a











glacial periods compared to the boreal


vegetation of the


middle and upper temperate latitudes (Delcourt and Delcourt

1981).

The Quaternary glaciations also have had a major

influence on avian migration patterns and are responsible


for the current geography


of avian migrations (Dorst


1962).


likely that northern Florida, with its mild climate


and mesic hardwood forests, served as a refugium for many


North American bird sp


ecies


during the glaciations.


The


Atlantic coast


flyway migration route (Lincoln 1939


channels avian migrants from most of


eastern North America


through northern Florida on their way to wintering grounds


in Central America,


South America,


and the West Indies.


predictable pulse of fall migrants,


northern Florida,


the mild winters of


and the established southern mesic


hardwood forest community have provided the raw materials

necessary for the evolution of mutualistic interactions

between fruiting plants and fruit-eating birds in the

southern mixed-hardwood community.

No discussion on the evolution of eastern North

America forest community structure would be complete without


mention of the extinct Passenger Pigeon,


Ectopistes


migratorius.


It was once extremely abundant in deciduous


forests from the great plains to the Atlanti


coast of New









53


chestnuts, but they were also known to feed upon a variety


of fruits,


including Prunus spp., Ilex spp., Nyssa


syiv atica,


Cornus florida, Morus spp., Rhus spp.,


Mitchella


repens, Phytolacca americana,

and Aralia spinosa (Schorger


Myrica cerifera,


1955).


Vitis spp.,


It is likely that


Passenger Pigeons were effective dispersal agents for the


majority of these fruits,


Nonetheless,


voiding the seeds intact.


we do not know the relative importance of fruit


compared


to mast


in the Passenger Pigeon's diet.


The southernmost limit of the Passenger Pigeon's


wintering range in Florida has been listed

where it was reported to be abundant in the


century (Howell 1932).


Alachua Co.,


eighteenth


The primary ecological role of the


Passenger Pigeon was probably that of a seed predator of mast-


producing species.


However, due to the inclusion of fruit


within its diet and its large numbers, it is possible that

the Passenger Pigeon played a significant role in the

evolution of the bird-fruit dispersal system in eastern


North America.


Thus,


its presence in northern Florida


during the winter may have in part


selected for the


predominance of fall-winter fruiting in this area.


Numbers of the American Robin,

frugivore in northern Florida today,


the primary wintering

seem to have increased


due to the clearing of forests in is breeding grounds












Florida.


This would be especially true in the selection for


fall-winter fruiting,


as the primary wintering ground for


robins i


Florida, wh


ere


flocks of up to 50,000 have been


recorded


(Speirs


Phytogeographic Considerations


The bird-disper


sed flora of San Felasco Hammock shows


strong taxonomic affinities with the mid-latitude flora of


eastern North America.


Of 22 plant families represented in


San Felasco Hammock,


only


Palmae and Symplocaceae, are


confined to the southeastern United States


in their U.S.


distribution.


At the generic level,


of 3


1 genera


represented in San Felasco Hammock, only 8, Amelopsis,


Callicarpa, Chionanthus, Osmanthus,


Persea, Phoradendron,


Sabal,


and Symplocos, are restricted primarily to the


southeast.


At the species


level, however,


of the 45


species present at San Felasco Hammock (64.h%) are limited


to the southeast.


Twenty-four of these species bear ripe


fruit in the fall or winter.


level


Therefore, at the species


, the bird-dispersed flora of lower latitudes


distinct from the flora of mid-latitudes of eastern North


America.


Yet many of the


species confined to the southeast


have congeners at more northern latitudes that show similar









55


-erotinum, Persea borbonia, Magnolia grandiflora, and

Symplocos tinctoria, show strong tropical affiliations.

This contrasts with the bird-dispersed flora of southern


Florida

of the


where tropical elements comprise approximately 87%


9


bird-dispersed plant species (Tomlinson 1980).


Certain taxa show wide variation in fruit types and


phenology,


while others are quite uniform.


Prunus


angustifolia, P. serotina, and P. caroliniana,


while all


flowering in early spring,

fruiting phenology. Prun


show pronounced differences in


us angustifolia and P. serotina


bear ripe fruit in the summer,


while P. caroliniana ripens


fruit in December.


Also,


while P. angustifolia produces a


sweet mammal-bird fruit that shows


low persistence, P.


caroliniana produces a bitter bird-dispersed fruit that is


highly persistent.


Evergreenness is a good indicator of


phenological


patterns:


the deciduous species, P.


angustifolia and P. serotina, are summer fruiters,


while the


evergreen, P. caroliniana,


is a winter fruiter.


This


latter


situation also exists for two


species


within the Oleaceae,


Chionanthus virginianus and Osmanthus americanus.


deciduous


evergreen


virginianus shows summer fruiting,


americanus is


while the


a winter fruiter.


Within certain genera such


as Smilax and


Ilex,


however,


different species tend to exhibit similar fruiting patterns,









56


taxonomic constraints or the result of similar selective


pressures acting on each sp


ecies.


The relationship between


systematics and ecological adaptation


indirect,


is complex and may be


and the effects of evolutionary canalization must


be considered in analyzing the biological interactions of


each taxon


(Stebbins


19 Th4).


Conclusions


The strong similarity in the bird-dispersed floras of

lower and mid-temperate latitudes in eastern North America

has probably played an important role in the evolution of


the bird-fruit seed dispersal system that we


see


today.


Wide-ranging spe


cies,


such as Parthenocissus quinquefolia


and Cornus florida, supply migrating frugivores with a


continuous,


familiar food supply in time and space along the


Atlantic flyway,


while congeners in the south show


fruiting


displays to migrating frugivores similar to those of their


relatives in the north.


Thus throughout eastern North


America there is a continuity in both the floral and

frugivorous components of the bird-fruit dispersal system.

Add to this the highly predictable nature of the annual fall


migration of avian frugivores from upper to lower


latitudes,


and it


not surprising that we


see


phenological patterns of


-
















CHAPTER THREE
SEASONAL PATTERNS OF BIRD-DISPERSED


FRUIT CHARACTERISTIC


AND FRUIT REMOVAL


Methods


Fruit Samples


I collected ripe fruits from


bird-dispersed plant


species


in San Felasco Hammock.


Fruit mass,


seed (or


pyrene) mass, pulp yield, and water content were determined


from an aggregate sample of


3474 undamaged fruits (mean


91.4).


Fruits were counted,


weighed, and separated into


pulp and seed components by dissection with forceps and by


hand.


Pulp and cleaned


seeds


were weighed, and the pulp was


oven-dried to constant mass at 60oC.


All


masses


were


measured to the nearest 0.1mg on


a Mettler AK 160


scale.


defined pulp moisture

separated pulp. Tota


from the mass of wet pulp


as percent mass lost on drying


1 dry pulp per fruit was determined


fruit mass minus the mass of


clean seeds) and its moisture content.


I determined


individual


seed


mass from wet


seed


load per fruit and mean


number of


seeds


per fruit for each sampl


-- 1 -


F. -


r 1 I I n in r' I C *~ a a p a F. -J


r- f jJ












petroleum ether in Micro-Soxhlet apparatus.


Protein content


was estimated as


6.25


times nitrogen found by micro-Kheldahl


extraction (Association of Official Agricultural Chemists


1965),


and soluble


carbohydrate content was determined by


the anthrone method (Yemm and Willis 1954;


Results for each chemical test a

from analysis of two subsamples.


Allen 1974).


re mean percent of dry mass

In addition to the 38


species of fruits collected from San Felasco Hammock,


included in my results analysis of


I have


species (Morus rubra,


Rubus cuneifolius, Prunus serotina, Ilex glabra, and


Toxicodendron radicans) from sample


collected in New Jersey


and analysed by White and Stiles.


San Felasco Hammock,


These species occur in


but I was unable to collect sufficient


numbers of fruits for analysis due to their scarcity or


inaccessibility.


The nutritional composition of species of


Morus, Rubus, Prunus, and Ilex have been shown to be


consistently similar (see Stiles 1980,


White and Stiles


unpub.


ms.).


I have therefore included figures


from the New


Jersey samples in my seasonal analyses.


I have omitted


Toxicodendrom radicans from my statistical comparisons as


consistent nutritional


genus


0 nnrn *1r


patterns are not evident for this


compared to the other genera.


Ila


II G









59


and 13,902 fruits in 1982-83, and for 8 species, involving


74 individuals and 6,334 fruits, in 1983-84.


of fruits on


Weekly counts


tagged branches of marked plants were made.


also tagged additional branches of marked plants each week


to replace removed fruits.


This was done in an attempt to


maintain a constant number of marked fruit


s for each


individual for each week. I defined removal rate


percentage of the total marked population of fruit removed

within a seven-day period.

I obtained additional information on fruit removal by


direct observations of fruit-eating birds. I

of fruit-eating while walking a 2100m transect


made records


mornings


each week during bird censuses (


see


Chapter II


and during


fruit censusing from January 1982 to April 1984.



Results and Discussion


Fruiting Patterns


The 43 species of bird-dispersed plants of San Felasco

Hammock fall into four fruiting patterns: summer fruiting,

fall fruiting, fall-winter fruiting, and winter fruiting


(see


Chapter II).


These fruiting patterns


are


based only


on seasonality of fruiting, a single fruiting pattern may









60


preference, and fruit abundance are related to fruiting

seasonality.



Summer Fruiting


Summer fruits (9 species) of the hammock community are


characterized by a large fruit mass,


low seed load,


high


water content, low


lipid and protein content, and high


carbohydrate content (Table 3-1).


speci


disperse


Summer fruits include


that depend on both mammals and birds for seed

1. These "mammal-bird" fruits are characterized by


low persistence (fall


to the ground upon ripening), high


sugar content, and a sweet taste (Stiles 1980).


Morus


rubra,


Rubus spp.,


Vitis spp.,


Vacciniun spp.,


and Prunus


spp.


(but not P.


caroliniana) are eaten on a regular basis


by a number of mammals,


including raccoon


and skunks


(Martin et.


1951).


The production of fruits that are


attractive to mammals may be advantageous due to the low

availability of avian frugivores during the summer months.

Fruit use by breeding birds is probably also reduced due to

the abundance of insects at this time and the importance of


insects


a high-protein food for breeding birds (Morton


1973).


Stiles (1980


has suggested that a dichotomy in seed


























*
**


tr.Cu


*
*
at

"0

-a-


0\

04

CM

\0
CM
at

-a-
Cr


U'
CM



H


U"'0 -%

C\\D
a~rflC'J
H~H
(no ~
.

,nCflC~J


02
0)cn'd
~02d
~cdO
SI-ti


.0-












through the guts of small mammals undamaged,


large-seeded species may produce seeds


discourage seed predation by small mammals.


while the


large


Hammock mammal-


bird fruits separate into small-seeded species (mean seed


mass


1.53


+0.80mg,


n=3) and


large-seeded species


(mean seed


mass


= 241.70+116.79mg,


11=3.


The small-seeded species also


show very


low seed loads (mean seed load


= 8.2%).


Two summer fruiting species, Prunus angustifolia and

Vitis rotundifolia, produce large fruits (> 2000mg) that are

clearly too large to be swallowed by any resident bird.

Mammal-dispersed fruits have been characterized by a large


size


and an orange or yellow color (Janson 1983,


Stiles unpub. ms.).


Prunus anugustifolia and


White and


Vitis


rotundifolia, however,

"chewed" by cardinals.


produce purple fruits that are

If the cardinal flies away with the


fruit, even without swallowing the seeds, it may still


deliver short distance dispersal.


Nonetheless, it appears


that mammals may be the primary dispersal agents for these


large


fruits.


The presence of a red preripe fruit color is also


characteristic of


summer mammal-bird fruit


The bi-color


display of unripe red and ripe blue-black fruit may increase

the conspicuousness of the fruiting display (Thompson and

Willson 1979, Stiles 1980. 1982. Stananian 1982. White and












only


of the 11 fall fruiting


species


and


of the 19 fall


winter fruiting species.



Fall Fruiting


The 11 fall fruiting species in the hammock community


include


ecies


, Cornus foemina,


Cornus florida, Euonymus


americanus, Parthenocissus quinquefolia, and Magnolia


grandiflora, with high lipid content (>


Appendix III).


10% dry mass,


High lipid content has typically been


correlated with high fruit quality


lipids yield about


twice the energy content


carbohydrates (Stiles


1980,


Herrera 1982a).


As a group, fall fruiting species show the


highest mean percentage in lipid content compared to the


other fruiting patterns (Table


3-1).


These high-lipid


fruits become available in the early fall,


when local


frugivore diversity and abundance are at a peak due to the


presence of migrant frugivores.


Herrera


1982a,


1984a


also found a strong correlation between the timing of

production of lipid-rich fruits by bird-dispersed plants in

the fall and frugivore abundance in the scrublands of


southern


Spain.


High quality fruits,


because of their high lipid


content, may also attract insects and microbes.


This may









64


five fall high-lipid fruits showed some fruit damage

resulting from invertebrate and microbe attack.


According to White and Stiles


(unpub.


ms.), production


of lipid-rich fruits in eastern North America may be limited


by season and plant growth form.


These fruits tend to be


produced in the fall when flocks of vagile,


hyperphagic


migrant frugivores are available for rapid fruit removal,

and appear also to be limited to woody shrubs and trees,


which can produce moderate to large fruit crops.


The small


fruit crops of herbs may limit repeat visits by birds and

thus decrease selection for high-lipid fruits (Stiles and


Devito,


unpub.


ms.).


Based on the analysis of 77


species of


mid-latitude bird-dispersed fruits from eastern North


America,


White and Stiles (unpub. ms.) have found that


fruits with lipid contents greater than 10% are limited to


fall fruiting woody plants.


the lower


A similar situation occur


latitude hammock community.


s for


No summer fruiting


species produces a high-lipid fruit,


while


of the 11 fall


fruiting species show fruits rich in lipids.


High lipid


fruits are also found among fall-winter fruiting species


(see


below).


High lipid fruits in the hammock community are


limited to woody plants,


lipid fruits


no herbaceous plants produced high


(see below).


Stiles (1980) has nronosed two dispersal strateales for












to decay,


thus permitting slower removal rates.


Based on


Stiles


' dichotomy, Callicarpa americana, Crataegus uniflora,


Aralia spinosa, Arisaema dracontium, Phytolacca americana,

and Amelopsis arborea would be considered low quality fruits


in the hammock community.


dracontium and Crataegus uniflora,


With the exception of Arisaema


these species produce low


lipid fruits


< 3.0% dry mass) with small seed masses (mean


= 9.2mg) and low seed loads (mean


= 16.6%).


Crataegus uniflora fruits show characteristics of


mammal-bird fruits (low persistence, sweet taste,


large


fruit mass) and appear to be adapted primarily for mammal


dispersal.


The herb Arisaema dracontium produces low-reward


fruits

lipid


for birds due to their high seed load (40.4%),


content (2.1%),


and low yield in dry matter per fruit


(31.3mg).


Stiles and Devito


(unpub. ms.)


have


suggested


that


certain low quality,


rare herbs may rely on generalized


mimicry of high-quality fruits for seed dispersal.


Arisaema


dracontium fruits resemble fallen Cornus florida fruits (a

high-lipid fruit) and may be taken accidentally by ground


foraging thrushes and


robins.


Fall-Winter Fruiting


Fall-winter fruiting


species


species)


produce












show the


lowest mean fruit mass (251.8mg) and lowest mean


water content (55.4%) of the four seasonal


(Table 3-1).


fruiting patterns


The low water content of these fruits may be


an adaptation for persistence (Stapanian 1982,


White and


Stiles


unpub.


ms.).


Contrastingly,


summer fruits show a


high mean water content


(82.7%) and are


poorly persistent.


Fall-winter fruiting species include


species, Persea


borbonia, Symplocos tinctoria, Myrica cerifera, Rhus


coppalina and Toxicodendron radicans,


that show high lipid


content.


White and Stiles


(unpub.


ms.)


have recognized


three distinct fruit types for


lipid-rich fruits:


1) waxy-


pulped fruits,


genus Rhus,


2) dry (<


) moist (


0% water),


> 40% water),


oily fruits of the


fleshy fruits of the


high-quality fruiting pattern.


Toxicodendron radicans and


Myrica cerifera would be considered waxy-pulped fruit


will be discussed below.


Rhus coppalina (12.0% lipid) would


be considered a dry, oily


, lipid-rich fruit.


The fruits of


Rhus,


although fed on by


six bird species (Appendix IV), were


taken infrequently.


Over a two-year period,


I observed only


12 visits to this species,

Sumacs (Rhus spp.) general


in which 190 fruits were removed.


ly are considered to be


unattractive to birds and


are


used primarily as an emergency


food


source


(White and Stiles,


unpub.


ms.).


Persea borbonia and SymDlocos tinctoria would he











duration for these


of North America.


species


Symp


unusual for


ocos


lipid-rich fruits


had a highly asynchronous


fruit ripening pattern (Chapter


II), resulting in a small


standing crop of ripe fruits at any one time. This resulted

in high removal rates of ripe fruits (see below), thus


limiting the number of ripe fruits available for insects and


microbes.


The fruits of Symplocos also turned from purple


and moist to brown and dry.


Persea borbonia fruits showed


little evidence of extensive damage from insects or


microbes.


This species may possess effective toxins that


discourage insect and microbe attack.



Winter Fruits


The 4 winter fruiting species produced ripe fruits in


January when the majority of fall-fruiting


depleted fruit crops.


species showed


The fruits of Prunus caroliniana,


Osmanthus americanus, and Ilex opaca showed a nutrient

content similar to that of fall-winter low-quality fruits


(lipid content


< 2.5%),


while Phoradendron serotinum


exhibited a distinct fruit type and dispersal syndrome from

the other fall-winter and winter fruiting species (see


below).


Prunus caroliniana, Osmanthus americana, and Ilex


opaca produced large fruits


(mean fruit mass


= 55


2.4mg),









68


Specialized Dispersal Systems


Several specialized dispersal systems, involving single


plant sp


ecies


that are dependent upon a small set of


dispersal agents,


occur in the hammock community.


Such


associations are rare in bird-fruit dispersal systems

(Wheelwright and Orians 1982) and typically involve fruits

with distinct fruit structure or chemistry (White and


Stiles unpub.


ms.).


Toxicodendron radicans and Myrica


cerifera produce waxy-pulped fruits unlike the fleshy-pulped


fruits exhibited by most species


in the hammock.


These species produce high lipid fruits,


which may be a


necessity for plants that have a small dispersal coterie


(McKey


1975.


Removal of Toxicodendron fruits in the


hammock is limited to woodpeckers and Yellow-rumped Warblers


(Dendroica coronata)


(Appendix IV).


Based on gut content


records of fruit-eating birds in North America,


White and


Stiles (unpub. ms.) have found woodpeckers and warblers to


use


waxy-pulped fruits


significantly more frequently than


other fruit-eating birds.


Greenberg (1984


also found a


close relationship between warblers and the waxy fruits of


Lindakeria laurina in Panama.


Removal of Myrica cerifera


fruits in the hammock


Warblers.


limited primarily to Yellow-rumped


These warblers accounted for 91% of the total












cedrorum).


Cedar Waxwings accounted for 80.7% of the total


visits to Phoradendron; mistletoe constituted 70.5% of the


total


visits to fruiting plants by waxwings.


Mistletoe


fruits show a distinct fruit structure typical of many


mistletoe


species


(Gill and Hawksworth 1961), while vaxwings


probably show similar morphological fruit-eating adaptations


to those of other mistletoe birds (Wetmore 1914,


1975).


Walsberg


Phoradendron berries also have a high protein


content (11.5%),


waxwing' s


which may contribute to its prevalence in


diet.


Fruit Removal


The high lipid fruiting species, Cornus foemina and

Symplocos tinctoria, had consistently high fruit removal


rates.


Removal rat


for Cornus foemina,


a fall fruiting


species


, increased in early September upon the arrival of


migrant frugivores (Fig.


3-1).


Fruit removal remained high


throughout September until its fruit crops were exhausted in


late September.


Symplocos tinctoria,


a fall-winter fruiting


species,


had high weekly removal rates from August through


January


(Fig.


This


species


exhibited


highly


asynchronous ripening pattern (Chapter


II ).


This resulted


in a relatively small standing crop of ripe fruit


s that was




































Fig.


3-1.


Fall fruiting species.


Percent of the


initial total number of fruits removed within a single
week for Cornus foemina, Callicarpa americana, and


Aralia spinosa.


Solid line represents 1982 season,


dashed line 1983 season.















/


Cornus foemina


aein


aca

Calilcarpa americana


O0 -Q-


































Fig.


3-2.


Fall-winter fruiting


species.


Percent of


the initial total number of fruits removed within a


single week for Viburnum rufidulum,


Viburnum obovatum,


Symplocos tinctoria, Ilex decidua, Smilax bona-nox, and
Smilax auriculata. Solid line represents 1982-83
season, dashed line 1983-84 season.












100 -


80


60-



40


20 -


0-


100-


80-


60-



40-


20 -


0-


100-


80-


60-






20-


Vib urunum rufidulum


Viburnum obo vatum


It
I'
6''


- aI a


I


















Ilex decidua


Smilax bona-nox


Smilax auriculata


rI









75


plant was visited regularly by small flocks of migrant

thrushes (Appendix IV) and was considered a primary plant


species for the local frugiv

display, abundant fruit crop

seed load of its fruits (14.


The showy fruiting


, clumped distribution, and low

9%), may account for the


attractiveness of this species to fruit-eating birds. High

removal rates appear to be advantageous for Aralia as its


fruits are highly susceptible to drying out and rotting.

Callicarpa americana, another fall, low lipid fruiting

species, showed a fruit removal pattern similar to Aralia's.

Removal rates for Callicarpa were high in September and


October until its


fruit crops were exhausted


(Fig. 3-1).


This species,


which was visited regularly by migrant


thrushes (Appendix IV),


has a stunning fruiting display


and was highly visible in the hammock.


The popularity of


Callicarpa may also be attributed to its individual

abundance, large fruit crops, and the low seed load of its

fruits (11.1%).

Fall-winter low lipid fruits typically showed low

removal rates throughout the fall until January or February,


when removal rates increased.


These increases occurred


after the fruit crops of the fall and fall-winter high lipid


fruiting species were all removed.


This pattern is shown by


TinY iri11 mlyhn nn S in nirrimt.Vhi m


V i hii rnlr rn












result of the inclusion of a specific fruit in the diet of


robins,


the most abundant wintering frugivore in the


community.


Once a fruit was


included in the robin's diet,


its fruit crop was regularly visited until it was exhausted.


The winter fruiting Prunus caroliniana showed a


fruit


removal pattern similar to those of fall-winter


fruits.


low quality


Removal rates of Prunus were moderate until it


became the primary fruit for robins.


At this time,


removal rates for this species increased sharply until its


fruit


crop was completely removed (Fig.


3-3).


attractiveness of Prunus caroliniana to robins may be due to


several factors.


Its fruits, while having a low lipid


content and high seed mass, h

of fruits of its congener, P.


ave three times the dry pulp mass

serotina, a summer fruiting


species.


Also, the large seed of Prunus caroliniana is


regurgitated, which may negate the disadvantages of a high


seed


load


(Sorensen


1984).


Seasonal Patterns of Fruit Removal


Based on weekly observations of fruit-eating birds from


1982-84 and fruit removal rates of marked individuals, th

fruit removal picture in the hammock community appears as


follows.


In the early fall,


when frugivore availability
































Fig. 3-3. Winter fruiting species. Percent of the
initial total of fruits removed within a single week
for Ilex oaca and Prunus caroliniana. Solid line
represents 192-83 season, dashed line 1983-84 season.














IC3 -




80-




60-




40-




20-




0 -


Ilex opaca


I I


100 -


80-


60-




40-




20-




0


Prunus caroliniana















0 /


*


*


I


i I I --












source.


Fall high lipid fruiting species often had small


fruit crops (e.g. Symplocos tinctoria,


Magnolia grandiflora)


or may be more difficult to


locate (e.g.


Parthenocissus


quinquefolia) than many


lipid species.


Thus,


while


lipid-rich fruits may offer a higher


birds,


caloric reward to


the search time for these fruits may be higher than


for some low-quality species.


Therefore it may be


practical, energetically, for a transient frugivore to visit


abundant


low lipid fruits (e.g. Aralia,


Callicarpa) when


lipid-rich fruits are not readily visible


Cornus florida, with its lipid-rich fruit, is the


primary fruiting plant in the mid-fall,


when it


visited


by small flocks of migrant thrushes and later, robins


(Appendix IV). In late fall,


when the fruit crop of Cornus


florida is completely removed, Persea borbonia, another high

lipid species, becomes the primary fruit for wintering


frugivores.


The size of the fruit crop of Cornus florida


and Persea borbonia varies greatly in different years and


size


of their crops appears to influence frugivore


numbers


in the


hammock.


Nonetheless,


while Cornus florida and Persea borbonia


were primary food plants for


local frugivores during late


fall and early winter, other fruiting species were also


visited daily.


On one day in mid-November.


I observed









80


appears to be a common practice among many frugivorous birds


(Snow


1977, Wheelwright 1983, Herrera 1984a) and may be


related to dietary requirements or "optimal foraging".

varied feeding behavior of frugivorous birds may be


essential to low-reward or rare species that by themsel


would be unable to attract dispersers.


ves


Therefore, at the


community


level,


there is an interdependence, in relation to


dispersal,


in which low-reward species may benefit from


coexisting with primary plant


In late January


species (Herrera 1984a).


, when the fruit crop of Persea borbonia


is gone, the hammock frugivores shift to persistent, low

lipid fruits such as Prunus caroliniana, Osmanthus


americanus, Celtis laevigata, Ilex spp., and Vaccinium


arboreum.


The last fruits to be taken include low


lipid


Smilax spp., Mitchella repens, and Viburnum obovatum.


this time wintering frugivores are beginning to lay down fat

deposits for the northward migration to their breeding

grounds.

I found no absolute relationship between high and low-


quality fruits and fruit removal rates.


The majority of


high-quality fruits did show higher fruit removal rates than


most low-quality


spec


species, however, certain low-quality


(e.g. Callicarpa americanus, Aralia spinosa)


. n a a --












factors,


including crop


size,


fruiting display, seed load,


and plant distribution, may be equally


important


lipid


content in relation to removal


success.


This


suggests


that


the dichotomy gf high and low-quality fruits,


based on


lipid content


McKey


1975


, Hove and Estabrook 1977), may not


always be correlated with fruit removal


success.


Eastern North American Comparisons


The bird-dispersed flora of San Felasco Hammock shows a

close taxonomic affinity to the mid-latitude flora of


eastern North America.


This


especially evident at the


generic level:


of the 31 genera present in the


hammock are found at mid-latitudes.


Stiles (unpub.


77 spec


White and


ms.) have analyzed the nutritional content of


of mid-latitude bird-dispersed plants of eastern


North America.


At the generic level,


22 Florida


species


13 genera showed similar nutritional composition to


congeners from New Jersey.


Of 7


species


common to San


Felasco Hammock and New Jersey,


had marked nutritional


differences.


Parthenocissus quinquefolia fruits


collected


in New


Jersey


were found to have a lower lipid content than


fruits


from Florida


(16.


vrs.


9%).


Stapanian (1


also found higher lipid values for Parthenocissus fruits in











content


for the congener,


atropurpureus


(31.2%) has also


been recorded (Johnson et. al.


1985).


Finally,


Nyssa


sylvatica,


a high-quality fruit as determined by White and


Stiles,


showed a much lower


lipid content in Florida than in


New Jersey


1.4% vrs. 14.8%).


The bird-dispersed flora of San Felasco hammock has a


high proportion of lipid-rich fruits


more northern latitudes.


compared to floras of


s is due in part to the


inclusion of such tropical-affiliated species as Magnolia


grandiflora, Persea borbonia,


and Symplocos tinctoria.


These species occur in families that have characteristically


high lipid fruits


(e.g.


Lauraceae)


The mild Florida


winters have permitted the establishment of these

subtropical species and have also resulted in large


populations of wintering frugivores.


Furthermore, a number


of these species show extended fall-winter fruiting,


wintering frugivores for seed dispersal.


latitudes,


using


At more northern


small populations of wintering birds should


select against the


evolution of lipid-rich fall-winter


fruits.


Thus,


high lipid fruits are limited to fall


fruiting species at middle and upper temperate latitudes


Thompson and Willson 1979


, White and Stiles unpub. ms.).


The remaining high lipid fruits from the hammock


community belong to


species


from temperate


families (e.g.












example,


the Vitaceae shows both high and low lipid fruiting


species in the hammock.


The fall fruiting Parthenocissus


quinquefolia has a high lipid fruit,


while the summer


fruiting Vitis rotundifolia and V. aestivalis have low lipid


fruits.


The variability in fruit quality in temperate


families suggests an independent evolution of lipid-rich


fruits


for these families


(White and Stiles,


unpub.


ms.).


Conclusions


The 43


species of bird-dispersed plants in the hammock


community represent a heterogeneous mixture of fruit types,

which exhibit a wide range in nutrient composition.


Nonetheless,


clear nutritional patterns related to dispersal


strategies and seasonality are evident.


into categories is thus possible


Grouping species


Summer fruiting species


form a distinct set, in which fruit morphology and nutrient


composition show characteristics


(e.g.


sweet


taste,


persistence) that may favor mixed mammal-bird seed


dispersal.


This strategy appears to be an adaptation to the


low abundance of frugivores during the summer months and to


the preference of breeding birds for insects

primary food supply.


their


Fall fruiting sp


ecies


fall into two category


, high












fruits,


while designated


low-quality, may offer migrants


an abundance of fruits with low seed loads.


fruiting species show variable removal rates,


lipid


with some


species showing low removal rates, while others exhibit

removal rates comparable to high lipid species.


Fall-winter fruiting


species also consist of high and


low lipid species, in which the high lipid species typically

have their fruit crops removed before the low lipid species.


lipid fruits persist until late winter


- early spring,


when they are taken sequentially by flocks of robins.

Winter fruiting species have fruits with low lipid

content and exhibit fruit removal patterns similar to low


lipid fall-winter fruiting


species.


The delayed ripening


pattern of these species may be an adaptation for the

avoidance of competition for dispersal agents from high

lipid species.

Within the hammock community are a series of primary


fruiting plants.


These plants receive the majority of


visits from local frugivores and may be instrumental in

attracting flocks of migrant frugivores into the community.


Less


preferred fruiting species may thus


benefit from


coexistence with these primary plant species.


species


Primary plant


included both high and low lipid species.


Characteristics of primary plants that may account for their












The nutritional


patterns of bird-dispersed fruits in


northern Florida show strong similarities to those patterns


described by Stiles


1980) and White and Stiles


(unpub. ms.)


for mid-latitude bird-dispersed plants of


eastern North


America.


These similarities


s are


the result of the close


taxonomic relationship in the bird-dispersed floras of the


two regions and to similar


selection pressures related to


the seasonal availability of frugivores.


The major


difference in the bird-fruit system between middle and lower

temperate latitudes in eastern North America is the

prevalence of the fall-winter fruiting pattern at lower


latitudes compared to middle latitudes.


Mild southern


winters have permitted the establishment of high lipid,

bird-dispersed species of tropical affinity and large


populations of wintering frugivores at lower


latitudes,


which have selected for fall-winter fruiting for many


species.


The presence of these subtropical species has


resulted in a greater proportion of high lipid fruits in the


bird-dispersed flora at lower


and upper


latitudes compared to middle


latitudes in eastern North America.















CHAPTER FOUR
SUMMARY


The bird-fruit dispersal system of San Felasco Hammock


involves


22 species of frugivorous birds and 45 species of


bird-dispersed plants.


The frugivorous birds include


members from eight families and range in size from


approximately


to 400g.


Twelve of the twenty-two bird


species are considered major frugivores as they were


involved in the majority of fruit visitations.

dispersed flora consists of plants representing


The bird-


families.


These plants show high variability in fruit type and

composition.

The fruiting phenology of the bird-dispersed plants of

San Felasco Hammock show similarities to both tropical and

middle latitude temperate bird-dispersed plant fruiting


systems.

of the yea


The hammock community shows ripe fruit every month


typical of many tropical communities


(Daubenmire 1972,

Liebermann 1982,


Frankie et. al.

Wheelwright, in


1974,


press).


Putz 1979,

Bird-dispersed


plants of middle temperate latitudes tend to fruit only


during the summer and fall,


few specie


s bearing ripe fruit


during the winter months (Thompson and Willson 1979). The


r,









87


situation to that observed at middle temperate latitudes in

North America (Thompson and Willson 1979, Stiles 1980, White


Stiles unpub.


ms.).


Most bird-dispersed plants in the hammock


bear ripe fruit in the fall,


when the community is invaded


by a high diversity of migrant frugivores.


Frugivore


diversity and abundance remain high throughout the fall and


winter months as does the number of fruiting species.


number of fruiting species decreases in the spring and


remains low throughout the summer months.


Frugivore


diversity and abundance is also low at this time.

The 44 species of bird-dispersed plants fall into four


distinct seasonal fruiting patterns:


fruiting,


summer fruiting,


fall-winter fruiting, and winter fruiting.


fall

Most


summer fruiting species have fruit characterized by high


water content,

sweet taste, a


large fruit mass,


Lnd low persistence.


high carbohydrate content,

These species produce


"mammal-bird fruits that may depend on mammals and birds


for dispersal.


Summer fruiting species typically are rare


or uncommon in the community and occur in disturbed

habitats.


Fall fruiting species produce ripe fruit


s during the


peak of fall migration of frugivorous birds through northern


Florida.


Fall fruiting species include five species that












with low


seed loads.


Fall fruiting species usually occur in


the closed forest and are common or abundant in the

community.

The fall-winter fruiting pattern is the most prevalent


fruiting pattern in the hammock, being


shown by 20 species.


Fall-winter fruiting species produce highly persistent fruit

that become ripe in the fall, persisting into January and


February.


This fruiting pattern is thus synchronized with


the first wave of transient frugivores and also the second


wave of overwintering frugivores.


Fall-winter fruiting


species are typically evergreen, and their fruits have the

lowest mean fruit mass and water content of the four


fruiting patterns.


Six fall-winter fruiting species have


high lipid fruits, including two with waxy-pulped fruit, one


with dry fruits, and three with moist fleshy fruits.


remaining fall-winter fruits produce low lipid fruits.


The winter fruiting pattern


shown by 4 evergreen


species, in which fruit maturation does not occur until


December.


These species use only overwintering frugivores


for seed dispersal.


Winter fruiting species exhibit low


lipid fruits, although Phoradendron serotinum produces a


relatively high protein fruit and


a unique dispersal


syndrome compared to the other winter specie


T1 h ta h-i vrl-fT'll-i-k ^i r1 rnf t n hcwi ^ lr








89


instrumental in attracting frugvorous birds into the


community.


These primary plants may also indirectly favor


seed dispersal of non-primary plants due to the varied diets


exhibited by fruit-eating birds.


The primary plants in this


community consist primarily of high lipid fruiting species


(e.g. Parthenocissus quinquefolia,


Cornus


florida,


Persea


borbonia),


but also include several low


species (e.g. Aralia spinosa,


lipid fruiting


Callicarpa americana).


These


lipid species produce large fruit crops and high


carbohydrate fruit


with small seeds and low seed loads.


Primary plants show high removal rates,


whereas fall-winter


low quality fruiting species exhibit low removal rates until

January or February when the fruit crops of Cornus florida


and Persea borbonia are exhausted.


At this time,


the fruits


of these highly persistent species are taken regularly until

their fruit crops are gone.

Primary frugivore bird species in the hammock include

migrant thrushes in the early fall and robins in the late


fall and winter.


Transient


Veerys are the primary dispersal


agent in the early fall when they form small flocks and


visit a variety of fruiting species.


When Veerys leave the


hammock in the late fall,


robins,


due to their


large numbers


and highly frugivorous diet become the primary dispersal


agent in the community.


Robins become the primary


disperser








90


responsible for the bulk of the fruit removal of the fall-


winter


low quality fruiting species in January and February.


Several specialized dispersal systems, involving single

plant species that are dependent upon a single or few

dispersal agents, are evident in the hammock community.

These include a close relationship between the mistletoe,


Phoradendron serotinum and the Cedar Waxwing,


Toxicodendron


radicans and woodpeckers and Yellow-rumped Warblers, and


Myrica cerifera and the Yellow-rumped Warbler.


These plant


species produce fruits with a distinct fruit structure or

chemistry related to their dispersal syndromes.

The bird-dispersed plants of the lower temperate

latitude hammock community show similar phenological

patterns and fruit characteristics to middle latitude


temperate bird-dispersed plants of North America.


Fall


fruiting is the most prevalent fruiting pattern shown at


middle latitudes of North America,


where the timing of


fruiting is closely correlated with the availability of


migrant frugivores (Thompson and Willson 1979).


latitudes

however,


At lower


the fall fruiting pattern is also common


the fall-winter fruiting pattern is shown by th


largest number of


species.


Thus while


species


of bird-


dispersed plants have ripe fruit during the winter months in


the hammock community,


only 4 species in Illinois have fruit








91


fruiting possible and profitable in northern Florida

compared to the middle latitudes of North America.

Similar selection pressures related to frugivore

availability and close taxonomic affinities have resulted in

close similarities in the fruit characteristics of the bird-

dispersed flora between lower and middle temperate latitudes


of eastern North America.


Nonetheless, the bird-dispersed


flora of the hammock community shows a higher proportion of


lipid-rich fruits than at more northern latitudes.


This


is due in part to the inclusion within its flora of such


lipid-rich tropical-affiliated species


as Magnolia


grandiflora, Persea borbonia, and Symplocos tinctoria.

The bird-dispersed flora of the hammock community also

shows fruiting patterns and fruit characteristics similar to

the lower temperate latitude scrubland community of southern


Spain (Herrera 1981, 1982a, 1984a).


Both communities show a


predominance of fall-winter fruiting species, in which


lipid-rich fruits are produced in the fall.


This pattern


can be attributed to similar patterns of frugivore

availability, in which the presence of overwintering

frugivores in both communities has selected for fall-winter

fruiting and also to the high degree of evergreenness

characteristic of both communities.











APPENDIX


METHODS OF CALCULATING RIPENING


SYNCHRONY (MODIFIED FROM AUGSPURGER 1983)


A. Synchrony of a given individual with its


conspecifics
individual i


1


where,


: Xi, the index of synchrony for
. is defined as:


1


ej~l


ej = number of days both individuals
i and J are ripening 90% of fruit crop,
jl; fi = number of days individual
i is ripening 90% of fruit crop;
n = number of individuals in population.


When


1.0,


perfect


synchrony


occurs, i.e.,


ripening period of individual i overlaps with
ripening period of each other individual, j#i
in the population.


When


= 0.0, no synchrony


occurs,


*, no


overlap occurs in the ripening period of individual
i and any other individual, jV1 in the population.

Synchrony of the population:


the ind


of population synchrony,


defined


where Xi is synchrony of individual i with its
conspecifics from part A. (above).


as:




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