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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).
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Acta Oecologica
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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.).
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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).
T.H. Fleming, W. John Kress / Acta Oecologica 37 (2011) 521e530 525
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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).
T.H. Fleming, W. John Kress / Acta Oecologica 37 (2011) 521e530 529
7/31/2019 A Brief History of Futs and Frugivores
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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