A Brief History of Futs and Frugivores

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Original article

A brief history of fruits and frugivores

Theodore H. Fleming a,b,*, W. John Kress c

a Emeritus Professor, University of Miami, Tucson, AZ, USAbAdjunct Professor, University of Arizona, Tucson, AZ, USAc Department of Botany, MRC-166, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA

a r t i c l e i n f o

Article history:

Received 30 August 2010

Accepted 20 January 2011

Available online 26 February 2011

Keywords:

Coevolution

Fruits

Frugivores

Phylogenies

a b s t r a c t

In this paper we briey review the evolutionary history of the mutualistic interaction between angio-

sperms that produce eshy fruits and their major consumers: frugivorous birds and mammals. Fleshy

fruits eaten by these vertebrates are widely distributed throughout angiosperm phylogeny. Similarly,

a frugivorous diet has evolved independently many times in birds and mammals. Bird dispersal is more

common than mammal-dispersal in all lineages of angiosperms, and we suggest that the evolution of

bird fruits may have facilitated the evolution of frugivory in primates. The diets of fruit-eating bats

overlap less with those of other kinds of frugivorous vertebrates. With a few exceptions, most families

producing vertebrate-dispersed fruit appeared substantially earlier in earth history than families of their

vertebrate consumers. It is likely that major radiations of these plants and animals have occurred in the

past 30 Ma, in part driven by geological changes and also by the foraging behavior of frugivores in

topographically complex landscapes. Overall, this mutualistic interaction has had many evolutionary and

ecological consequences for tropical plants and animals for most of the Cenozoic Era. Loss of frugivores

and their dispersal services will have a strong negative impact on the ecological and evolutionary

dynamics of tropical and subtropical communities.

2011 Elsevier Masson SAS. All rights reserved.

Nearly two decades ago, Fleming (1991a) published a review of

the historical ecology and evolution of the mutualistic interaction

between eshy fruits produced by angiosperms and their verte-

brate mutualists. Major points that emerged from that review

include: (i) magnoliids and rosids have the highest percentage of

families producing eshy fruits among Cronquists (1988) six

angiosperm subclasses; (ii), eshy fruits are most common in

families of woody plants; families that are primarily herbaceous

produce capsular or other kinds of dry fruits; and (iii) the most

popular fruit families for vertebrates tend to be more species-rich,

pantropical, and geologically older than the average angiospermfamily. Although an attempt was made to place this evolution into

a phylogenetic context, at least for plants, this effort was crude

because DNA-based molecular phylogenies of the angiosperms and

their mutualists were then in their infancy. Nearly twenty years

later, our knowledge of the phylogenetic histories of plants and

animals is much better-developed, and it is now possible to

examine the evolutionary history of fruits and frugivores in much

greater detail. We will attempt such a synthesis in this paper. We

note that this review is basically an abstract of a much more

comprehensive look at this mutualism (as well as the mutualism

between owers and their vertebrate pollinators) that will appear

in our forthcoming book, The Ornaments of Life (Fleming and Kress,

University of Chicago Press, in prep.). As in Ornaments, our focus

here will be on interactions between frugivorous birds and

mammals because they are the major vertebrate seed dispersers in

most terrestrial habitats. Fish and lizards (as well as a few other

reptiles) do consume fruits and disperse seeds in certain habitats

(reviewed in Correa et al., 2007; Olesen and Valido, 2003), but we

will not consider them here.

We have three major objectives in this paper: (i) to examine thedistribution of dispersal syndromes involving birds, bats, and

primates across angiosperm phylogeny; how much concordance is

there in this distribution?; (ii) to map the occurrence of frugivory

onto avian and mammalian phylogenies to look for phylogenetic

clustering; and (iii) to examine the degree of temporal congruence

between the evolution of frugivores and their major food plants;

how much co-radiation has occurred as a result of this interaction?

1. Basic types ofeshy fruits

Contemporary angiosperms produce a bewildering array of fruit

types. Spujt (1994), for example, identies 95 different kinds of

fruit, most of which are non-eshy and are not consumed or

* Corresponding author. 6211 N. Camino de Corozal, Tucson, AZ 85704, USA.

Tel./fax: 1 520 797 5609.

E-mail address: [email protected] (T.H. Fleming).

Contents lists available at ScienceDirect

Acta Oecologica

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m/ l o c a t e / a c t o e c

1146-609X/$ e see front matter 2011 Elsevier Masson SAS. All rights reserved.

doi:10.1016/j.actao.2011.01.016

Acta Oecologica 37 (2011) 521e530


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Sapindales and Rosales); these proportions are 0.29 and 0.26,

respectively. When we break our data down into families by major

primary disperser (i.e., birds, bats, and primates), families withbird-dispersed fruits are more common than those with species

dispersed by bats or primates in each of the ve lineages (Fig. 3).

The bird curve sets the pattern for vertebrate dispersal, and the

primate curve mirrors the bird curve. Bat dispersal is especially

uncommon in families of basal eudicots. The basal eudicot familyCactaceae, in which numerous genera and species are bat-

dispersed, is a notable exception.

Fig. 2. The phylogeny of angiosperms by order. Source: APG III (2009).

T.H. Fleming, W. John Kress / Acta Oecologica 37 (2011) 521e530 523


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As described in detail in Fleming and Kress (in prep.), birds

appear to be the main evolutionary attractors (de Thomson and

Wilson, 2008) as dispersers of angiosperm fruit. We estimate that

bird-dispersed fruits occur in at least twice as many families asbat- or primate-dispersed fruits (Fig. 3). We can use the phylogeny

of rosids, a clade of advanced eudicots, to illustrate this and other

points about the use of different kinds of vertebrates as seed

dispersers by angiosperms (Fig. 4). In this clade, 12 families

contain fruits that are exclusively bird-dispersed compared with

none and one family with fruits that are exclusively bat- or

primate-dispersed, respectively; 10 families are both bird- and

primate-dispersed; and only two families are both bird- and bat-

dispersed. Finally, 10 families contain fruits that are dispersed by

all three groups of vertebrates. In this clade, phylogenetically

clustered families involving vertebrate dispersal occur in the

Sapindales and Rosales (Fig. 4). In sum, bird dispersal either alone

or in combination with the other two groups of major primary

dispersers occurs in most of the vertebrate-dispersed families of

rosids. Fruits dispersed by birds and primates occur in more

families than those dispersed by other combinations of verte-

brates. This suggests that the presence of bird fruits may have

facilitated the evolution of frugivory in primates. A detailed

species-level phylogeny onto which mode of vertebrate dispersal

is mapped is needed for particular families, however, to rigorously

test this hypothesis, which predicts that bird dispersal is usually

basal to primate dispersal within families. A start in this direction

is Lomscolo et al. (2010) analysis of the phylogenetic distribution

of fruits dispersed by birds and bats (or both) in species of Ficus in

New Guinea.

Another important evolutionary trend in angiosperms is that

the proportion of families producing both eshy and non-eshy

(e.g., dry capsules, follicles) fruits (i.e., mixed fruit-type families)

varies among these lineages, as summarized by Heywood et al.(2007). Basal eudicots, asterids, and rosids contain much higher

proportions of mixed fruit families than basal angiosperms, in

which mixed families are absent, or monocots (Fig. 5). Mixedfamilies contain substantially more species and exhibit a greater

diversity of growth forms and dispersal strategies than non-mixed

families (Fleming, 1991a; Ricklefs and Renner, 1994). In mixed

families, species producing non-eshy fruits with abiotically

dispersed seeds tend to be herbs or vines growing in open and/or

frequently disturbed habitats. In these families, biotically dispersed

eshy fruits are usually produced by woody plants (trees and

shrubs) in closed, less frequently disturbed habitats (Bolmgren and

Erikksson, 2005, 2010).

In contrast to vertebrate pollination, which often requires the

evolution of specialized morphology and occurs in relatively fewfamilies of birds and mammals (Fleming and Muchhala, 2008),

frugivory is widespread throughout the phylogenies of birds and

mammals. The phylogenetic structure of birds is rather complex

andis incompletely resolvedcurrently but can be broken down into

three major clades or radiations: (i) Paleognathae (tinamous,

cassowaries, and other ightless birds; six orders, six families); (ii)

Galloanserae (chickens and their relatives, ducks and geese; two

orders, nine families); and (iii) Neoaves (all other birds; 23 orders,about 181 families) (Cracraft et al., 2003). Passeriformes, which

includes about 97 families and nearly two-thirds of all species of

modern birds, can be divided into suboscine and oscine (true

songbird) clades. Frugivory is found in each of the major clades,

including cassowaries and tinamous among the paleognaths, cra-

cids among the Galloanserae, and many orders and families among

the Neoaves (Table 1). Frugivory has evolved independently in most

of these families but two phylogenetic clusters of frugivores are

notable: (i) the piprid/cotingid/tyrannid (PCT) clade of Neotropical

suboscine passerines and (ii) the sturnid/mimid clade of Old World/

New World sister families (Fig. 6). The PCT clade is particularly

interesting because it represents a parallel radiation of understory

(manakins and certain tyrannids) and canopy (cotingids) feeders. A

similar radiation of closely related understory and canopy frugi-vores has not occurred in the Paleotropics. Most Old World avian

frugivores are canopy feeders.

In terms of biogeography, only one family of largely frugivorous

birds (Turdidae) has a cosmopolitan distribution (Table 1). Two

other avian families containing numerous frugivorous species

(Columbidae, Trogonidae) have broad tropical distributions but are

strongly frugivorous in only part of their ranges (fruit pigeons and

doves in Australasia and quetzals and trogons in the Neotropics).

Overall, the Neotropics has the greatest number of families and

species of frugivores (10 families; one cosmopolitan and nine

endemic families; the frugivorous trogons are counted as endemic

here). Africa/Madagascar has a total of seven families (one

cosmopolitan, two endemic, and four families shared with Asia);

Asia has eight families (one cosmopolitan, two endemic, and ve

shared families); and Australasia also has eight families (one

cosmopolitan, ve endemic [including fruit pigeons], and two

families shared with Asia). Passerines dominate the frugivore

faunas in terms of number of families and species throughout the

tropics. Of the two broadly distributed non-passerine families in

which extensive frugivory occurs in only part of their ranges,

neotropical trogons feed heavily on fruits of Lauraceae whereas

paleotropical trogons, which are apparently derived from

neotropical ancestors (Moyle, 2005), are largely insectivorous.

A similar hemispheric difference in the importance of frugivory

occurs in the non-passerine Columbidae (pigeons). The Austral-

asian fruit pigeons are an advanced clade of 12 genera and about

126 species (Pereira et al., 2007) that feed heavily on fruits of

Lauraceae, Moraceae (gs), and Myristicaceae.

As in birds, families of frugivores are distributed throughoutmuch of mammalian phylogeny. The structure of this phylogeny

includes six major clades: (i) Monotremata (platypus and echidna;

one order, two families); (ii) Marsupialia (marsupials; seven orders,

21 families); (iii) Xenarthra (armadillos and anteaters; two orders,

ve families); (iv) Afrotheria (African placentals; six orders, eight

families); and (v) Boreotheria, which includes two subclades e

Laurasiatheria (northern shrews, bats, carnivores, ungulates, etc.;

eight orders, 63 families) and Euarchontoglires (tree shrews,

primates, rodents, lagomorphs; ve orders, 54 families) (Wilson

and Reeder, 2005). The major families of mammalian frugivores

are listed in Table 2. Frugivory has evolved independently

numerous times among mammals. It is absent in extant members

of Monotremata and Xenarthra and is especially common in Laur-

asiatheria and Euarchontoglires. Phylogenetically clustered evolu-tion has occurred only in order Primates, in whichmost families are

frugivorous.

0.05

0.10

0.15

0.20

0.25

0.30

Proportion

offamilies

Birds

Bats

Primates

BAng Mon BEud Ast Ros

Fig. 3. Proportions of families within angiosperm lineages in which dispersal by birds,

bats, and primates occurs. Source: Fleming and Kress (in prep.).

T.H. Fleming, W. John Kress / Acta Oecologica 37 (2011) 521e530524


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As in birds, the Neotropics has the greatest number of frugivo-

rous mammal families (eight endemic families plus one familyshared with SE Asia) followed by Asia (one endemic family and

seven shared families) and Africa (one endemic family [other

families of lemurs could arguably be added here] and seven shared

families). Unlike birds, there are no pantropical families ofmammalian frugivores (except for humans). As in Neotropical

manakins and cotingas, a parallel radiation of understory and

Fig. 4. The phylogeny of rosid families coded by the presence of different kinds of vertebrate seed dispersers. Source: Fleming and Kress (in prep.) based on APG III (2009).



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canopy frugivores has occurred in Neotropical phyllostomid bats.

Understory frugivores include bats of the genera Carollia, Rhino-phylla, Sturnira, and Glossophaga (classied in three separate

subfamilies); canopy frugivores occur in subfamily Sten-

odermatinae, the most advanced clade of phyllostomids (Baker

et al., 2003). A similar marked separation into understory- and

canopy feeders has not occurred in pteropodid bats, most of which

are canopy feeders (Hodgkison et al., 2004). Because of their rela-

tively large size, most primates are also canopy feeders. A few

smaller species (e.g., marmosets) feed in the subcanopy, and a few

very large Paleotropical cercopithecines and apes are terrestrial.

Compared with the Paleotropics, the Neotropics are decient in

terrestrial frugivorous mammals, although a few clades persisted

until the Pleistocene (Fleming et al., 1987; Guimaraes et al., 2008).

4. Chronology of the evolution ofeshy-fruited

plant families and frugivores

Here we address the question, how congruent are the geological

ages of the major plant families that provide food for frugivorous

birds and mammals and their vertebrate mutualists? That is, how

closely did the appearance of vertebrate frugivores match the

appearance of their major food families? To address this question,

we focused on a subset of well-studied families of avian and

mammalian frugivores (i.e., those marked with an * in Tables 1

and 2) and their most important orcore

plant families as deter-

mined by Fleming and Kress (in prep.). Our reasoning here is that if

temporal congruence is going to occur, it will most likely occur

between plant andanimal taxa that have formed strong mutualistic

interactions. We can envision two possible answers to this ques-

tion: (i) the chronologies of plants and their animal mutualists

correspond closely to each other or (ii) the chronologies of animals

lag behindthat of their families of food plants. In scenario (i), plants

and their mutualists have interacted via generalized coevolution

for most of their histories; in scenario (ii), mutualists did not begin

to interact with their food plants until well after their rst

appearance.

We used DNA-based estimates of the phylogenies and diver-

gence times of these plant and animal families based on data

summarized in Hedges and Kumar (2009). We realize that molec-ular-based estimates of divergence times are still controversial (see

a discussionof this issue in Avise (2009)) because they often predict

earlier divergence times than is revealed by the fossil record.

Furthermore, these estimates are for particular nodes on (hopefully,

well-resolved) phylogenetic trees and hence represent the esti-

mated age ofrst appearance of our families of concern. They do

not indicate the ages of crown groups, i.e., the ages of extant

members of these families. In many cases, tens of millions of years

have elapsed between the appearance of stem and crown members

of particular families. For example, the New World family Cacta-

ceae, whose advanced subfamily Cactoideae contains many species

that are vertebrate-pollinated and dispersed, is sometimes thought

to be Cretaceous in age, but recent studies suggest that its modern

radiation dates from the Oligocene (about 30 Ma) when the

northern Andes were undergoing uplift (Edwards et al., 2005;

Nyffeler, 2002). Similarly, it is likely that the stem group of Phyl-

lostomidae (American leaf-nosed bats) evolved about 35 Ma, but

the crown group of stenodermatines, which are major consumers

Table 1

Major families of frugivorous birds, based on Cracraft et al. (2003). Families marked with an asterisk (*) were included in the chronological analysis (see Chronology

of.......).

Clade Order Family Number of

genera/species

Geographic distribution

Pal eogna th ae C asua ri iformes *Casuariidae (cassowaries) 1/3 Australasia

Galloanserae Galliformes Cracidae (currasows, guans) 11/50 Neotropics

Neoaves Columbiformes *Co lumbidae ( part ) ( fruit pig eons) 12/126 Aust ralasia ( but a few f rugivoro us

pigeons occur on other islands)

Musophagiformes Musophagidae (turacos) 6/23 Africa

Caprimulgiformes Steatornithidae (oilbirds) 1/1 NeotropicsTrogoniformes *Trogonidae (trogons) 6/39 Pantropical (but frugivorous

only in Neotropics)

Coraciiformes *Bucerotidae (hornbills) 13/49 Africa, SE Asia

Piciformes Lybiidae (African barbets) 6/36 Africa

Megalaimidae (Asian barbets) 2/26 Asia

Capitonidae (New World barbets) 2/14 Neotropics

*Ramphastidae (toucans) 5/38 Neotropics

Passeriformes Euylaimidae (broadbills) 9/14 Africa, SE Asia

*Cotingidae (cotingas) 33/96 Neotropics

*Pipridae (manakins) 13/48 Neotropics

Ptilonorhynchidae (bower birds) 8/18 Australia

*Paradisaeidae (birds of paradise) 16/40 Australasia

*Meliphagidae (honeyeaters) 44/174 Australasia

Turdidae (thrushes) 24/165 Cosmopolitan

Mimidae (mockingbirds) 12/34 Neotropics, Nearctic

Sturnidae (starlings) 26/115 Paleotropics

*Dicaeidae (owerpeckers) 2/44 SE Asia, Australasia

Pycnonotidae (bulbuls) 22/118 Africa, SE Asia

*Emberizidae, Thraupinae (tanagers) 50/202 Neotropics

Proportionoffa

milies

0.2

0.4

0.6

0.8

1.0

Mixed

Fleshy

7 16 10 25 44

BAng Mon BEud Ast Ros

Fig. 5. Proportions of families producing either eshy fruits or a combination of dry

and eshy fruits by angiosperm lineage. Source: Fleming and Kress (in prep.).



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of small canopy fruits such as Ficus, likely evolved only about 12 Ma

(Baker et al. in press). It is widely believed that many modern

groups of frugivores evolved in the Oligocene/Miocene (i.e.,

between 34 Ma and about 10 Ma) regardless of the ages of their

stem groups. Despite these problems, these estimates are the best

currently available and should be adequate for broadly addressing

our question.

To address this question, we plotted the cumulative rst

appearances of 78 families of eshy-fruited angiosperms and 56

families of avian and mammalian frugivores through time in Fig. 7.

These data come from Tables 1.3 and 1.1, respectively, in Flemingand Kress (in prep.). The plant accumulation curve reaches 50%

saturation at about 78 Ma, well before the K/T boundary, whereas

the frugivore accumulation curve reaches 50% saturation over 30

Ma later, well after theK/T boundary. This suggests that scenario (ii)

rather than scenario (i) is likely to be correct. Support for this

conclusion comes from data in Fig. 8 inwhich we plotted the ages of

22 families of birds and mammals (Tables 1 and 2) against the ages

of 23 of their core families of food plants. Plant families were

plotted multiple times when they were core families for multiple

animal families. If scenario (i) is correct, then all points should fall

on or close to the Y X line; if scenario (ii) is correct, then most

points should fall below the Y X line. Clearly, most of the points

fall below the line and often far below it. These data do not supportthe hypothesis that there has been close temporal congruence

between the evolution of vertebrate frugivores and their major

Fig. 6. The phylogeny of passeridan (advanced) passerines showing major and minor families in which frugivory occurs. Source: Cracraft et al. (2004).



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food plants. Many families of plants providing eshy fruits for birds

and mammals evolved long before their current vertebrate

dispersers. For example, substantial radiations in a number of

frugivores (e.g., various haplorhine primates, tanagers, birds of

paradise, and certain phyllostomid bats) have occurred within the

last 15 Ma, long after the appearance of their core fruit families.

Among other things, this raises the question, who were the

dispersers of stem members of these and other plant families? The

usual explanation is that herbivorous dinosaurs were seed

dispersers of early angiosperms, but an analysis by Butler et al.

(2009) suggests that these animals did not co-radiate with

angiosperms.

A handful of points in Fig. 8 do lie on or very close to the Y Xline, and it is of interest to know which planteanimal combinations

these are. From oldest to youngest, these include: Myrtaceae/Cas-

uariidae (68 Ma); Elaeocarpaceae/Casuariidae (66 Ma); Ana-

cardiaceae/Pteropodidae (56 Ma); Loranthaceae/Meliphagidae (53

Ma); Burseraceae/Cotingidae (51 Ma); Meliaceae/Bucerotidae (40

Ma); and Cactaceae/Phyllostomidae (30 Ma). Despite the temporal

congruence in the rst appearance of these groups, it remains to be

seen whether this represents true causal co-radiation or merely

temporal correlation. We suspect that this congruence is correla-

tional rather than causal in most cases.

Figs (Ficus, Moraceae) is an interesting case because nearly all

contemporary frugivores eat gs, at least occasionally (Shanahan

et al., 2001). Some groups (e.g., birds such as barbets, hornbills,

toucans, and birds of paradise and mammals such as many

primates and phyllostomid and pteropodid bats) have probably

relied heavily on them as core food items for all or most of their

history. According to Herre et al. (2008), the g-g wasp mutualism

dates from 70 to 90 Ma, much earlier than the molecular estimates

of 55e40 Ma for Ficus by Sytsma et al. (2002) and Zerega et al.

(2005) or 36 Ma in Hedges and Kumar (2009). If this is true, then

these fruit predate the evolution of many groups of modern

frugivorous vertebrates and could have provided the impetus for

their evolution (e.g., in primates; Dominy et al., 2001; Sussman,1991). Fig. 7 shows the family appearance curve for 12 families of

vertebrates that rely heavily on gs for food. If anything, these

families are younger, not older, on average, than other families of

frugivores. Clearly, the origins of these families and their primary

food source were not coeval.

Assuming that the chronologies shown in Fig. 7 are not wildly

incorrect,the generalpicture thatemerges from these datais thatthe

evolution of families of vertebrate frugivores has lagged behind that

Table 2

The major families of mammalian frugivores, based on Wilson and Reeder (2005). Families marked with an asterisk (*) were included in the chronological analysis (see

Chronology of..).

Clade Order Family Number of

genera/species

Geographic distribution

Marsupialia Diprotodontia Phalangeridae (brushtail possums) 6/27 Australasia

Afrotheria Proboscidea Elephantidae (elephants) 2/3 Africa, SE Asia

Laurasiatheria Chiroptera *Pteropodidae (part) (ying foxes) 36/160 Paleotropics

*P hyllo stomidae (part) ( American leaf-nosed bat s) 20/70 Neot ropics

Carnivora Viverridae (part) (palm civets) 6/8 Paleotropics

Procyonidae (raccoons) 6/14 Neotropics, Nearctic

Perissodactyla Tapiridae (tapirs) 1/4 Neotropics, SE Asia

Artiodactyla Tragulidae (chevrotains) 3/8 Africa, SE Asia

E uarchontog lires P rimat es *Lemuridae (large lemurs) 5/19 Madagascar

*Cebidae (marmosets, capuchins) 6/56 Neotropics

*Aotidae (night monkeys) 1/8 Neotropics

*Pitheciidae (sakis, titi monkeys) 4/40 Neotropics

*Atelidae (howlers, spider monkeys) 5/24 Neotropics

*Cercopithecidae (part) (Old World monkeys) 9/57 Africa, SE Asia

*Hylobatidae (siamangs, gibbons) 4/14 SE Asia

*Hominidae (apes, humans) 4/7 Africa, SE Asia

Rodentia Echimyidae (spiny rats) 21/90 Neotropics

Dasyproctidae (agoutis, pacas) 2/13 Neotropics

Years before present (Ma)

0 20 40 60 80 100 120 140

Cumulativepercentage

0

20

40

60

80

100

Fruits

Frugivores

K/T

Fig-eaters

Fig. 7. The chronology of rst appearances of major angiosperm families providing

eshy fruits for vertebrates, families of frugivorous birds and mammals, and families

that specialize in consuming gs. Source: Fleming and Kress (in prep.).

Age of fruit families (Ma)

0 20 40 60 80 100 120

Ageoffrugivorefamilies

(Ma)

0

20

40

60

80

100

Y=X

Fig. 8. Plot of the age ofrst appearance ofcore angiosperm families providing eshy

fruits for major families of frugivorous birds and mammals vs. the rst appearances of

families of those birds and mammals. Source: Fleming and Kress (in prep.).



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of their major food families, sometimes by a considerable amount of

time. For example, Neotropical phyllostomid bats of the genus Car-

ollia are strongly associated with Piper fruits (Fleming, 2004).

According to current estimates, Piperaceae (with about 1100

Neotropical species and far fewer in the Paleotropics) is nearly 100

million years old whereas Carollia (with about nine species) is lessthan 20 million years old(Baker et al., in press; Jaramillo and Callejas

2004; Simmons, 2005). Were Pipershrubsundiverseand uncommon

members of the understory of Neotropical forests for tens of millions

of years before Carollia bats evolved or did this genus radiate

signicantly in the New World well before the rst appearance of

phyllostomid bats? Since New World Pipers are geographically

associated with Andean orogeny and thus likely began their modern

radiation in theOligoceneor Miocene (Gentry,1982), itis temptingto

conclude that the radiation of this speciose genus probably was

coeval with the appearance of Carollia bats. We suspect that this

scenario will also hold for a variety of other old groups of plants and

their much younger vertebrate frugivores. If this is true, it suggests

that the evolution of many plant families providing fruits for verte-

brate frugivores is likely to conform to a

long-fuse

model in whichtheir major radiations have occurred long after their rst appear-

ances and in conjunction with radiations of their major pollinator or

seed dispersal mutualists. Tests of this hypothesis are sorely needed.

In closing, we would like to turn to a gure that Pierre Charles-

Dominique published in the second symposium/workshop on

frugivores and seed dispersal (Charles-Dominique, 1993: Fig. 1; our

Fig. 9). Data in this gure has important implications for the effect

of vertebrate seed dispersers on speciation in their food plants and,

ultimately, on the adaptive radiation of fruits and frugivores. These

data come from studies of fruitefrugivore interactions in primary

rainforest in central French Guiana. Based on these studies, Charles-

Dominique (1993) placed avian and mammalian frugivores into

two general classes: specialized frugivores that consume

a restricted range of fruit types and generalized frugivores that eat

many different fruit types. Examples of specialized frugivores

include birds such as manakins, cock-of-the-rock, and trogons as

well as phyllostomid bats (e.g., Artibeus and Carollia). Non-

specialized, or generalized, frugivores include mammals, such as

opossums, kinkajous, and some primates. Many of the genera of

fruit eaten by specialized frugivores are among the most species-

rich in the ora of French Guiana and elsewhere in the Neotropics

(Fig. 9). The three most species-rich genera, for example, are corefood genera for manakins (Miconia, Psychotria) and Carollia bats

(Piper) (Fleming andKress, in prep.). A question raisedby these data

is: What is the causeeeffect relationship between vertebrate

feeding specialization and the proliferation of species within

particular genera ofeshy-fruited plants? As suggested by Charles-

Dominique (1993), has the close association between particular

plant types (genera) and groups of frugivores promoted parallel

evolution between them and particularly rapid speciation? Or,

alternatively, has speciation in these plants occurred independentlyof the effects of specialized frugivores with frugivores responding

opportunistically to particularly species-rich groups of plants?

Like Charles-Dominique (1993), we suspect that this association

is based on a causeeeffect relationship and that it reects the seed

dispersal behavior of specialized frugivores. While many of these

species are relatively small and sedentary, they nonetheless occa-

sionally move among habitats while foraging and thus move seeds

from one habitat to another (e.g., Carollia bats; Fleming, 1988,

1991b). Given occasional long-distance seed dispersal in a topo-

graphically heterogeneous environment (e.g., in emerging montane

regions [e.g., the Andes] or in regions fragmented by large rivers),

genetic isolation and speciation are likely to occur occasionally in

plants (Levin 2006; Price and Wagner, 2004). The key idea here is

that

intermediate levels

of dispersability are more likely to resultin plant speciation than either low or high levels of dispersability.

Low levels of dispersability prevent the colonization of new habi-

tats with new selection regimes. High levels of dispersability result

in high levels of gene ow among habitats that prevent the

reproductive and genetic isolation needed for speciation to occur.

5. Conclusions

Fruit-eating birds and mammals have likely had a mutualistic

relationship as seed dispersers with owering plants for at least 90

Ma. This mutualism is widely distributed across angiosperms and is

well-represented in families of basal angiosperms as well as

advanced eudicots. Birds have clearly been the disperser of choicefor many angiosperms, probably because of their species diversity,

abundance, and range of sizes, and frugivory is widely distributed

throughout avian phylogeny. Among mammals, the evolution of

Order Primates is closely associated with a frugivorous diet, and

primate dispersal often co-occurs in plant families exhibiting bird

dispersal, suggesting that the evolution of bird fruits may have

facilitated the evolution of frugivory in primates. Bats are also

important seed dispersers, especially of small-seeded, early succes-

sional plants in the Neotropics (Muscarella and Fleming, 2007), but

their generallysmallsizes andlow diversity limits thekindsand sizes

of fruit they can eat and effectively disperse. With a few exceptions,

families of frugivorous birds and mammals evolved long after the

rst appearances of their major food families. Major radiations in

both eshy-fruited plants and frugivorous birds and mammals have

likely taken place in the last 30 Ma. Intermediate levels of dispers-

ability provided by relatively sedentary birds and mammals havelikely increased rates of speciation in their food plants. As discussed

in detail by Fleming and Kress (in prep.), the mutualism between

eshy-fruited plants and frugivorous vertebrates has had many

important evolutionary and ecological consequences. Without these

frugivores, the ecological and evolutionary dynamics of tropical and

subtropical forests and other habitats would be very different.

Preservation of these interactions and the habitats in which they

occur in tropical biomes is therefore imperative.

Acknowledgements

Fleming thanks Dr. Pierre Michel-Forget for inviting him to

participate in the Fifth Symposium/workshop on Frugivores and

Seed Dispersal. Most of the material in this review was taken fromour forthcoming book (The Ornaments of Life, University of Chicago

Press). We thank our editors (Christie Henry and John Thompson)

Number of species/genus

0 5 10 15 20 25 30 35 40 45 50 55 60 65

Numberofgenera

0

20

40

60

80

100

120

750

Bactris, Swartzia, Slonea,

Hiratella, Eischweilera

Protium, Philodendron, Passiflora,

Clidemia, Eugenia

Ficus

Ocotea, Solanum

Pouteria, Licania

Inga

Piper

Psychotria,

Miconia

Fig. 9. Number of angiosperm genera in the ora of French Guyana containing x

number of species, where x ranges from 1 to 60 species per genus. Source: Charles-

Dominique (1993).



10/10

for permission to use material from that book in this review. We

thank R. Corlett, P. Michel-Forget, and an anonymous reviewer for

comments that helped sharpen this paper. Ida Lopez prepared the

cladograms.

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A Brief History of Futs and Frugivores