Acta Oecologica 37 (2011) 521e530

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Acta Oecologica
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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, USA Adjunct Professor, University of Arizona, Tucson, AZ, USA c Department of Botany, MRC-166, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA
b

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 brie y review the evolutionary history of the mutualistic interaction between angiosperms 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 vertebrate 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 angiosperm family. 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 the distribution 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 of eshy fruits

* Corresponding author. 6211 N. Camino de Corozal, Tucson, AZ 85704, USA. Tel./fax: 1 520 797 5609. E-mail address: ted eming@dakotacom.net (T.H. Fleming). 1146-609X/$ e see front matter 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2011.01.016

Contemporary angiosperms produce a bewildering array of fruit types. Spujt (1994), for example, identi es 95 different kinds of fruit, most of which are non- eshy and are not consumed or

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Seed size variation (orders of magnitude)

dispersed by vertebrates. Here we are concerned mainly with those fruit types that are consumed by birds and mammals, the two groups of vertebrates that have been the most important seed dispersers throughout the Cenozoic. Van der Pijl (1982) classi ed these into four types based on the plant tissue providing the nutritional reward: (i) seeds with eshy sarcotestas (seed coats) as found in Arecaceae, Euphorbiaceae, Meliaceae, etc.; (ii) arilloid fruits as found in Annonaceae, Fabaceae, Myristicaceae, Sapindaceae, etc.; (iii) pulpa (fruits with a eshy endocarp protected by a hard pericarp) as found in Clusiaceae, Fabaceae, Rutaceae, Simaroubaceae, etc.; and (iv) pericarp fruit (drupes and berries) as found in many families. These fruit types have evolved independently and convergently many times throughout angiosperm phylogeny, indicating considerable evolutionary plasticity in the evolution of fruit types. This plasticity can be easily seen within families such as Melastomataceae, Rubiaceae, and Solanaceae, to name a few well-studied examples, in which eshy fruit have evolved from dry capsular fruit multiple times (Bremer and Eriksson, 1992; Clausing and Renner, 2001; Knapp, 2002). In this review we will focus on the phylogenetic distribution of the following fruit types: (i) berries and berry-like fruits (e.g., baccate fruits and syconia); (ii) drupes and syncarps; (iii) arillate fruits; (iv) dry fruits such as capsules, schizocarps, and nuts; and (v) mixed fruit types, including both dry and eshy fruits. We include noneshy fruits in this analysis because many families of advanced eudicots produce both eshy and non- eshy fruits. 2. Historical changes in angiosperm seed size and its implications for the fruit/frugivore mutualism Well-preserved fruits are relatively uncommon in the fossil record, especially in the Cretaceous when angiosperms were rst evolving. As a result, most botanists studying fruit evolution have relied on fossil seeds as surrogates for fruit size and type. This approach seems justi ed because there is a strong correlation between seed size and fruit size in contemporary angiosperms (e.g., Leishman et al., 2000; Wright et al., 2007). Assuming that this relationship was true in the past, palynologists have interpreted small fossil seeds (i.e., <100 mg) as being produced by small fruits and have inferred that they were abiotically dispersed. Large fossil seeds (i.e., >100 mg), in contrast, are usually interpreted as coming from large fruits that were biotically dispersed (Eriksson et al., 2000; Tiffney, 2004). Historical trends in seed (fruit) size are shown in Fig. 1. As reviewed by Eriksson (2008), most angiosperm seeds during the Cretaceous were small (median volume 1 mm3), but seed size and its interspeci c variation increased markedly in the early Cenozoic. Three non-exclusive hypotheses have been put forth to explain this pattern: (i) the fruit-frugivore coevolution hypothesis in which direct coevolution between vertebrate frugivores and seeds in the early Tertiary favored large seed size; (ii) the recruitment hypothesis in which changes in (tropical) vegetation from open habitats in the Cretaceous to closed forests early in the Tertiary favored the evolution of large seeds and biotic dispersal; and (iii) the life-form hypothesis in which small shrubby Cretaceous angiosperms evolved into larger plants early in the Tertiary; trees, in turn, evolved larger seeds that required vertebrates for their dispersal. As Eriksson (2008) indicates, there are likely to be elements of truth in each of these hypotheses. It is certainly true that (i) large plants tend to produce larger seeds and a greater range of seed sizes among species than small plants; (ii) on a per-capita basis, large seeds are more likely to produce seedlings that survive than small seeds in shady habitats because of their greater energy reserves; and (iii) large seeds are less mobile than small seeds, which would

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Fig. 1. Historical trends in median seed size (A) and range in seed size (in orders of magnitude) (B) in 25 paleo oras from the Early Cretaceous to the Pliocene. Source: Eriksson (2008).

favor the evolution of biotic dispersal via the production of eshy fruits (Leishman et al., 2000). But the primary driver behind the evolution of biotic dispersal is still not clear. Was it the evolution of closed forests under the warm, wet conditions of the early Tertiary? Or the evolution of larger plants per se? Or the evolution of fruiteating vertebrates? In the end, as Eriksson (2008) concluded, it is likely that large plant size, large seeds, and biotic dispersal evolved as coadapted traits in the context of the habitat mosaics present in the early Tertiary and that the presence of eshy-fruited plants in the Eocene set the stage for the radiation of modern groups of tropical frugivorous birds and mammals. 3. The phylogenetic distribution and biogeography of fruits and frugivores We will use phylogenies based on APG III (2009) as a template for our discussion of angiosperm evolution and the distribution of fruit types across this phylogeny. We interpret APG III as recognizing ve major categories of angiosperms: (i) basal angiosperms (8 orders, 28 families), (ii) monocots (12 orders, 83 families), (iii) basal eudicots (11 orders, 64 families), (iv) asterids (14 orders, 105 families), and (v) rosids (17 orders, 125 families). Three of these groups (monocots, asterids, and rosids) are monophyletic clades whereas the other two represent evolutionary grades rather than clades (Fig. 2). The distribution of families producing eshy fruits eaten by vertebrates differs among these lineages but not signi cantly (data not shown; X2 4.83, df 4, P 0.31). The highest proportions of eshy-fruited families occur in basal angiosperms (especially in the Magnoliales) and rosids (especially in the

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

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 with bird-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 family Cactaceae, in which numerous genera and species are batdispersed, is a notable exception.

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0.30

0.25 0.20 0.15

Birds

Primates

0.10 0.05
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BAng

Mon

BEud

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Ros

Fig. 3. Proportions of families within angiosperm lineages in which dispersal by birds, bats, and primates occurs. Source: Fleming and Kress (in prep.).

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 as bat- 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 batdispersed. 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 vertebrates. 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). Mixed families 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 few families 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 and is incompletely resolved currently 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, cracids 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 frugivores 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 Australasian 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 throughout much 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 Laurasiatheria and Euarchontoglires. Phylogenetically clustered evolution has occurred only in order Primates, in which most families are frugivorous.

Proportion of families

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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).

As in birds, the Neotropics has the greatest number of frugivorous mammal families (eight endemic families plus one family shared 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 of mammalian frugivores (except for humans). As in Neotropical manakins and cotingas, a parallel radiation of understory and

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1.0

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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.).

canopy frugivores has occurred in Neotropical phyllostomid bats. Understory frugivores include bats of the genera Carollia, Rhinophylla, Sturnira, and Glossophaga (classi ed in three separate subfamilies); canopy frugivores occur in subfamily Stenodermatinae, 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 relatively 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 de cient 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 of plant families and frugivores eshy-fruited

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 or core plant families as determined 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 and animal taxa that have formed strong mutualistic interactions. We can envision two possible answers to this question: (i) the chronologies of plants and their animal mutualists correspond closely to each other or (ii) the chronologies of animals lag behind that 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 divergence times of these plant and animal families based on data summarized in Hedges and Kumar (2009). We realize that molecular-based estimates of divergence times are still controversial (see a discussion of 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 estimated age of rst 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 Cactaceae, 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 Phyllostomidae (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 Paleognathae Galloanserae Neoaves Order Casuariiformes Galliformes Columbiformes Musophagiformes Caprimulgiformes Trogoniformes Coraciiformes Piciformes Family *Casuariidae (cassowaries) Cracidae (currasows, guans) *Columbidae (part) (fruit pigeons) Musophagidae (turacos) Steatornithidae (oilbirds) *Trogonidae (trogons) *Bucerotidae (hornbills) Lybiidae (African barbets) Megalaimidae (Asian barbets) Capitonidae (New World barbets) *Ramphastidae (toucans) Euylaimidae (broadbills) *Cotingidae (cotingas) *Pipridae (manakins) Ptilonorhynchidae (bower birds) *Paradisaeidae (birds of paradise) *Meliphagidae (honeyeaters) Turdidae (thrushes) Mimidae (mockingbirds) Sturnidae (starlings) *Dicaeidae ( owerpeckers) Pycnonotidae (bulbuls) *Emberizidae, Thraupinae (tanagers) Number of genera/species 1/3 11/50 12/126 6/23 1/1 6/39 13/49 6/36 2/26 2/14 5/38 9/14 33/96 13/48 8/18 16/40 44/174 24/165 12/34 26/115 2/44 22/118 50/202 Geographic distribution Australasia Neotropics Australasia (but a few frugivorous pigeons occur on other islands) Africa Neotropics Pantropical (but frugivorous only in Neotropics) Africa, SE Asia Africa Asia Neotropics Neotropics Africa, SE Asia Neotropics Neotropics Australia Australasia Australasia Cosmopolitan Neotropics, Nearctic Paleotropics SE Asia, Australasia Africa, SE Asia Neotropics

Proportion of families

Passeriformes

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

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 Fleming and 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 the K/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 in which 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 support the hypothesis that there has been close temporal congruence between the evolution of vertebrate frugivores and their major

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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 Marsupialia Afrotheria Laurasiatheria Order Diprotodontia Proboscidea Chiroptera Carnivora Perissodactyla Artiodactyla Primates Family Phalangeridae (brushtail possums) Elephantidae (elephants) *Pteropodidae (part) ( ying foxes) *Phyllostomidae (part) (American leaf-nosed bats) Viverridae (part) (palm civets) Procyonidae (raccoons) Tapiridae (tapirs) Tragulidae (chevrotains) *Lemuridae (large lemurs) *Cebidae (marmosets, capuchins) *Aotidae (night monkeys) *Pitheciidae (sakis, titi monkeys) *Atelidae (howlers, spider monkeys) *Cercopithecidae (part) (Old World monkeys) *Hylobatidae (siamangs, gibbons) *Hominidae (apes, humans) Echimyidae (spiny rats) Dasyproctidae (agoutis, pacas) Number of genera/species 6/27 2/3 36/160 20/70 6/8 6/14 1/4 3/8 5/19 6/56 1/8 4/40 5/24 9/57 4/14 4/7 21/90 2/13 Geographic distribution Australasia Africa, SE Asia Paleotropics Neotropics Paleotropics Neotropics, Nearctic Neotropics, SE Asia Africa, SE Asia Madagascar Neotropics Neotropics Neotropics Neotropics Africa, SE Asia SE Asia Africa, SE Asia Neotropics Neotropics

Euarchontoglires

Rodentia

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 X line, and it is of interest to know which planteanimal combinations these are. From oldest to youngest, these include: Myrtaceae/Casuariidae (68 Ma); Elaeocarpaceae/Casuariidae (66 Ma); Anacardiaceae/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 correlational 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 general picture that emerges from these data is that the evolution of families of vertebrate frugivores has lagged behind that

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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)

Fig. 8. Plot of the age of rst appearance of core 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 Carollia 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 less than 20 million years old (Baker et al., in press; Jaramillo and Callejas 2004; Simmons, 2005). Were Piper shrubs undiverse and uncommon members of the understory of Neotropical forests for tens of millions of years before Carollia bats evolved or did this genus radiate signi cantly 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 the Oligocene or Miocene (Gentry,1982), it is tempting to 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 vertebrate frugivores is likely to conform to a long-fuse model in which their major radiations have occurred long after their rst appearances 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 CharlesDominique 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, CharlesDominique (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). Nonspecialized, 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 speciesrich in the ora of French Guiana and elsewhere in the Neotropics (Fig. 9). The three most species-rich genera, for example, are core food genera for manakins (Miconia, Psychotria) and Carollia bats (Piper) (Fleming and Kress, in prep.). A question raised by these data is: What is the causeeeffect relationship between vertebrate
750 Bactris, Swartzia, Slonea, Hiratella, Eischweilera 120 Protium, Philodendron, Passiflora, Clidemia, Eugenia Ficus 80 60 40 20 0 Ocotea, Solanum Pouteria, Licania Inga Piper Psychotria, Miconia

feeding specialization and the proliferation of species within particular genera of eshy-fruited plants? As suggested by CharlesDominique (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 independently of 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 re ects the seed dispersal behavior of specialized frugivores. While many of these species are relatively small and sedentary, they nonetheless occasionally 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 topographically 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 result in plant speciation than either low or high levels of dispersability. Low levels of dispersability prevent the colonization of new habitats 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 choice for 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 successional plants in the Neotropics (Muscarella and Fleming, 2007), but their generally small sizes and low diversity limits the kinds and 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 dispersability provided by relatively sedentary birds and mammals have likely 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

Number of genera

100

10

15

20

25

30

35

40

45

50

55

60

65

Number of species/genus
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: CharlesDominique (1993).

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 from our forthcoming book (The Ornaments of Life, University of Chicago Press). We thank our editors (Christie Henry and John Thompson)

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T.H. Fleming, W. John Kress / Acta Oecologica 37 (2011) 521e530 Fleming, T.H., Breitwisch, R.L., Whitesides, G.W., 1987. Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecology and Systematics 18, 91e109. Gentry, A.H., 1982. Neotropical oristic diversity: phytogeographical connections between central and South America, Pleistocene climatic uctuations, or an accident of the Andean orogeny? Annals of the Missouri Botanical Garden 69, 557e593. Guimaraes, P.R., Galetti, M., Jordano, P., 2008. Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. Plos One 3. Hedges, S.B., Kumar, S. (Eds.), 2009. The Timetree of Life. Oxford University Press, Oxford, UK. Herre, E.A., Jander, K.C., Machado, C.A., 2008. Evolutionary ecology of gs and their associates: recent progress and outstanding puzzles. Annual Review of Ecology Evolution and Systematics 39, 439e458. Heywood, V.H., Brummitt, R.K., Culham, A., Seberg, O., 2007. Flowering Plant Families of the World. Fire y Books, Ontario, Canada. Hodgkison, R., Balding, S.T., Zubaid, A., Kunz, T.H., 2004. Habitat structure, wing morphology, and the vertical strati cation of Malaysian fruit bats (Megachiroptera: Pteropodidae). Journal of Tropical Ecology 20, 667e673. Jaramillo, M.A., Callejas, R., 2004. Current perspectives on the classi cation and phylogenetics of the genus Piper L. In: Dyer, L.A., Palmer, A.D.N. (Eds.), Piper: A Model Genus for Studies of Phytochemistry, Ecology, and Evolution. Kluwer Academic/Plenum Publishers, New York, New York, pp. 179e198. Knapp, S., 2002. Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. Journal of Experimental Botany 53, 2001e2022. Leishman, M.R., Wright, I.J., Moles, A.T., Westoby, M., 2000. The evolutionary ecology of seed size. In: Fenner, M. (Ed.), Seeds, the Ecology of Regeneration in Plant Communities. CABI Publishing, Wallingford, United Kingdom, pp. 31e57. Levin, D.A., 2006. Ancient dispersals, propagule pressure, and species selection in owering plants. Systematic Botany 31, 443e448. Lomscolo, S.B., Levey, D.J., Kimball, R.T., Bolker, B.M., Alborn, H.T., 2010. Dispersers shape fruit diversity in Ficus (Moraceae). Proceedings of the National Academy of Sciences of the United States of America 107, 14668e14672. Moyle, R.G., 2005. Phylogeny and biogeographical history of Trogoniformes, a pantropical bird order. Biological Journal of the Linnean Society 84, 725e738. Muscarella, R., Fleming, T.H., 2007. The role of frugivorous bats in tropical forest succession. Biological Reviews 82, 573e590. Nyffeler, R., 2002. Phylogenetic relationships in the cactus family (Cactaceae) based on evidence from trnK/matK and trnL-trnF sequences. American Journal of Botany 89, 312e326. Olesen, J.M., Valido, A., 2003. Lizards as pollinators and seed dispersers: an island phenomenon. Trends in Ecology & Evolution 18, 177e181. Pereira, S.L., Johnson, K.P., Clayton, D.H., Baker, A.J., 2007. Mitochondrial and nuclear DNA sequences support a cretaceous origin of columbiformes and a dispersaldriven radiation in the Paleogene. Systematic Biology 56, 656e672. van der Pijl, L., 1982. Principles of Dispersal in Higher Plants, third ed. SpringerVerlag, Berlin. Price, J.P., Wagner, W.L., 2004. Speciation in Hawaiian angiosperm lineages: cause, consequence, and mode. Evolution 58, 2185e2200. Ricklefs, R.E., Renner, S.S., 1994. Species richness within families of owering plants. Evolution 48, 1619e1636. Shanahan, M., So, S., Compton, S.G., Corlett, R., 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews 76, 529e572. Simmons, N.B., 2005. Order Chiroptera. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World, a Taxonomic and Geographic Reference. Johns Hopkins Press, Baltimore, Maryland, pp. 312e529. Spujt, R.W., 1994. A systematic treatment of fruit types. Memoirs of the New York Botanical Garden 70, 1e181. Sussman, R.W., 1991. Primate origins and the evolution of angiosperms. American Journal of Primatology 23, 209e223. Sytsma, K.J., Morawetz, J., Pires, J.C., Nepokroeff, M., Conti, E., Zjhra, M., Hall, J.C., Chase, M.W., 2002. Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcL, trnL-F, and ndhF sequences. American Journal of Botany 89, 1531e1546. Thomson, J.D., Wilson, P., 2008. Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. International Journal of Plant Sciences 169, 23e38. Tiffney, B.H., 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology, Evolution, and Systematics 35, 1e29. Wilson, D.E., Reeder, D.M. (Eds.), 2005. Mammal Species of the World: A Taxonomic and Geographic Reference, third ed. Johns Hopkins Press, Baltimore. Wright, I.J., Ackerly, D.D., Bongers, F., Harms, K.E., et al., 2007. Relationships among ecologically important dimensions of plant trait variation in seven neotropical forests. Annals of Botany 99, 1003e1015. Zerega, N.J.C., Clement, W.L., Datwyler, S.L., Weiblen, G.D., 2005. Biogeography and divergence times in the mulberry family (Moraceae). Molecular Phylogenetics and Evolution 37, 402e416.

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. References
APG III, 2009. An update of the angiosperm phylogeny group classi cation for the orders and families of owering plants: APG III. Botanical Journal of the Linnean Society 161, 105e121. Avise, J.C., 2009. Timetrees: beyond cladograms, phenograms, and phylograms. In: Hedges, S.B., Kumar, S. (Eds.), The Timetree of Life. Oxford University Press, Oxford, UK, pp. 19e25. Baker, R.J., Bininda-Emonds O.R.P., Mantilla-Meluk H., Porter C.A., Van den Bussche, R.A. in press. Molecular timescale of diversi cation of feeding strategy and morphology in New World leaf-nosed bats (Phyllostomidae): a phylogenetic perspective. Baker, R.J., Hoofer, S.R., Porter, C.A., Van den Bussche, R.A., 2003. Diversi cation among New World leaf-nosed bats: an evolutionary hypothesis and classi cation inferred from digenomic congruence of DNA sequences. Occasional Papers, Museum of Texas Tech University 230:1e32. Bolmgren, K., Eriksson, O., 2005. Fleshy fruits - origins, niche shifts, and diversi cation. Oikos 109, 255e272. Bolmgren, K., Eriksson, O., 2010. Seed mass and the evolution of eshy fruits in angiosperms. Oikos 119, 707e718. Bremer, B., Eriksson, O., 1992. Evolution of fruit characteristics and dispersal modes in the tropical family Rubiaceae. Biological Journal of the Linnean Society 47, 79e95. Butler, R.J., Barrett, P.M., Kenrick, P., Penn, M.G., 2009. Diversity patterns amongst herbivorous dinosaurs and plants during the cretaceous: implications for hypotheses of dinosaur/angiosperm co-evolution. Journal of Evolutionary Biology 22, 446e459. Charles-Dominique, P., 1993. Speciation and coevolution: an interpretation of frugivory phenomena. In: Fleming, T.H., Estrada, A. (Eds.), Frugivory and Seed Dispersal: Ecological and Evolutionary Aspects. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 75e84. Clausing, G., Renner, S.S., 2001. Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution. American Journal of Botany 88, 486e498. Correa, S.B., Winemiller, K.O., Lopez-Fernandez, H., Galetti, M., 2007. Evolutionary perspectives on seed consumption and dispersal by shes. Bioscience 57, 748e756. Cracraft, J., Barker, F.K., Cibois, A., 2003. Avian higher-level phylogenetics and the Howard and Moore checklist of birds. In: Dickinson, E.C. (Ed.), The Howard and Moore Complete Checklist of the Birds of the World. Princeton University Press, Princeton, NJ, pp. 16e21. Cracraft, J., Barker, F.K., Braun, M.J., Harshman, J., Dyke, G.J., et al., 2004. Phylogenetic relationships among modern birds (Neornithes). In: Cracraft, J., Donoghue, M.J. (Eds.), Assembling the Tree of Life. Oxford University Press, Oxford, pp. 468e489. Cronquist, A., 1988. The Evolution and Classi cation of Flowering Plants, second ed. The New York Botanical Garden, Bronx, NY. Dominy, N.J., Lucas, P.W., Osorio, D., Yamashita, N., 2001. The sensory ecology of primate food perception. Evolutionary Anthropology 10, 171e186. Edwards, E.J., Nyffeler, R., Donoghue, M.J., 2005. Basal cactus phylogeny: implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. American Journal of Botany 92, 1177e1188. Eriksson, O., 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences 169, 863e870. Eriksson, O., Friis, E.M., Lofgren, P., 2000. Seed size, fruit size, and dispersal systems in angiosperms from the early cretaceous to the late Tertiary. American Naturalist 156, 47e58. Fleming, T.H., 1988. The Short-tailed Fruit Bat, a Study in PlanteAnimal Interactions. University of Chicago Press, Chicago. Fleming, T.H., 1991a. Fruiting plant-frugivore mutualism: the evolutionary theater and the ecological play. In: Price, P.W., Lewinsohn, T.M., Fernandes, G.W., Benson, W.W. (Eds.), PlanteAnimal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. J. Wiley and Sons, New York, New York, pp. 119e144. Fleming, T.H., 1991b. The relationship between body size, diet, and habitat use in frugivorous bats, genus Carollia (Phyllostomidae). Journal of Mammalogy 72, 493e501. Fleming, T.H., 2004. Dispersal ecology of neotropical Piper shrubs and treelets. In: Dyer, L.A., Palmer, A.D.N. (Eds.), Piper: a Model Genus for Studies of Phytochemistry, Ecology, and Evolution. Kluwer Academic/Plenum Publishers, New York, NY, pp. 58e77. Fleming, T.H., Muchhala, N., 2008. Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems. Journal of Biogeography 35, 764e780.