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The Ornaments of Life
Coevolution and Conservation in the Tropics
By Theodore H. Fleming, W. John Kress THE UNIVERSITY OF CHICAGO PRESS
Copyright © 2013 The University of Chicago
All rights reserved.
ISBN: 978-0-226-25340-4
CHAPTER 1
The Scope of This Book
Tropical forests and their marine counterparts, coral reefs, are the most species-rich and colorful ecosystems on earth. Much of this color comes from their animal inhabitants. In coral reefs, the corals themselves as well as anemones, gorgonians, sea fans, sponges, and giant clams, among the invertebrates, and wrasses, damselfish, angelfish, and butterfly fish, among the vertebrates, are major contributors to the color palette. In tropical forests, nectar-feeding birds—hummingbirds, sunbirds, and lorikeets—and their fruit-eating counterparts—tanagers, trogons, manakins, toucans, hornbills, and birds of paradise—are among the most colorful and conspicuous vertebrates (plates 1–5). Less colorful but nonetheless still notable because of their size, conspicuousness, and/or abundance are their mammalian ecological counterparts—phyllostomid and pteropodid bats and primates (plates 6–7). Supplying all of these animals with food is a cornucopia of colorful flowers and fruits produced by understory herbs (e.g., Heliconia, Musa), shrubs (e.g., Melastomataceae, Rubiaceae), vines (e.g., Bignoniaceae), epiphytes (e.g., Bromeliaceae, Gesneriaceae, Loranthaceae), and subcanopy, canopy, and emergent trees (e.g., Bignoniaceae, Fabaceae, Lauraceae, Malvaceae [Bombacoideae], Myristicaceae, Myrtaceae) (plates 8–13).
In emphasizing the beauty of tropical nature, the prominent twentieth-century evolutionary biologist Theodosius Dobzhansky wrote:
Becoming acquainted with tropical nature is, before all else, a great esthetic experience. Plants and animals of temperate lands seem to us somehow easy to live with, and this is not because many of them are long familiar. Their style is for the most part subdued, delicate, often almost inhibited. Many of them are subtly beautiful; others are plain; few are flamboyant. In contrast, tropical life seems to have flung all restraints to the winds. It is exuberant, luxurious, flashy, often even gaudy, full of daring and abandon, but first and foremost enormously tense and powerful. (Dobzhansky 1950, 209)
While lowland tropical rain forests usually harbor the greatest diversity of plant-visiting vertebrates on earth, some of this diversity and its outstanding beauty spill over into other tropical and subtropical habitats along gradients of rainfall and elevation. Thus, lowland tropical and subtropical dry forests as well as montane forests harbor many colorful plant-visiting vertebrates. The same is true of tropical islands. Although their diversity is usually lower than that of mainland communities, tropical islands nonetheless harbor a substantial number of plant-visiting birds and mammals. Finally, some of these animals migrate to temperate latitudes to breed. Tropical forests routinely export some of their colorful vertebrate mutualists (e.g., hummingbirds, tanagers, and parulid warblers in the New World) to far-flung places on a seasonal basis, thereby temporarily increasing the color palette of temperate habitats.
Why have tropical and subtropical plants evolved pollination and frugivory mutualisms with a wide array of colorful nectar-and fruit-eating birds and mammals? What are the ecological and evolutionary "rules" that govern these interactions and how important has earth history been in formulating these rules? How many variations on the themes of nectarivory and frugivory have evolved in tropical birds and mammals? We seek to answer these questions in this book, which is divided into three major sections. The first section (chaps. 2–4) examines regional and local species diversity patterns as well as patterns of resource availability and the functional (ecological) relationships between plant-visiting birds and mammals and their food plants. These chapters seek to determine (1) how communities of these mutualists are structured in space, (2) the nature of the resource base supporting plant-visiting vertebrates, (3) the extent to which fruit and seed set and seedling recruitment of tropical plants depend on the feeding and foraging behavior of nectarivorous and frugivorous birds and mammals, and (4) the population genetic consequences of this feeding behavior for their food plants. One possible genetic consequence is reproductive isolation and speciation, and the question arises, what impact, if any, have plant-visiting vertebrates had on speciation rates of their food plants? And, conversely, what effect have their food plants had on speciation rates of vertebrate nectar and fruit eaters? We address these questions in chapter 5 of the second section. In addition, we review the phylogeny and biogeography of the major families of animals and plants involved in these two mutualisms (chap. 6) as background for a detailed examination of the large array of morphological, physiological, and behavioral adaptations that have arisen during the evolution of these mutualisms (chaps. 7 and 8). Finally, in the third section we will synthesize the ecological and evolutionary consequences of these mutualisms (chap. 9) before discussing their conservation implications (chap. 10). How vulnerable are tropical vertebrate pollinators and frugivores to natural and human disturbances, and how can the loss of these species via extinction be minimized? In the rest of this introductory chapter, we briefly review the major players in this story and outline the basic ecological and evolutionary features of pollination and frugivory mutualisms.
A Brief Taxonomic Overview of Vertebrate Pollinator and Frugivore Mutualisms
Although fish and reptiles (e.g., tortoises and lizards) eat fruit and disperse seeds in certain contemporary habitats (e.g., fish in the Amazon Basin and lizards on islands; Anderson et al. 2009; Correa et al. 2007; Goulding 1980; Olesen and Valido 2003;) and reptiles probably were important seed dispersers in the Cretaceous (Ridley 1930; van der Pijl 1982; Wing and Tiffney 1987), we will focus on mutualistic interactions between higher vertebrates (birds and mammals) and their food plants in this book. We do this for the simple reason that birds and mammals account for the vast majority of vertebrate pollination and frugivory mutualisms today and undoubtedly have done so throughout the Cenozoic Era (Proctor et al. 1996; Tiffney 2004; van der Pijl 1982; Wing and Tiffney 1987).
Major groups of contemporary nectar-and fruit-eating birds and mammals are listed in table 1.1. Nectar-feeding birds and mammals currently exhibit relatively low taxonomic diversity. Nectarivorous birds occur in three orders and 11 families containing about 870 species. Seven of these families, totaling about 840 species, can be considered to be specialized nectarivores (i.e., species that are morphologically adapted for probing into flowers for nectar; Stiles 1981). Specialized nectar-feeding mammals occur in only two orders and three families containing about 49 species. A number of arboreal mammals, including lemurs, callitrichid and cebid monkeys, and procyonids, as well as many fruit-eating phyllostomid and pteropodid bats are occasional nectar feeders, but the number of morphologically specialized mammalian nectarivores is small. Overall, there are about 17 times more species of nectarivorous birds than nectarivorous mammals.
Fruit-eating birds and mammals are much more diverse taxonomically than nectarivores (table 1.1). Fruit-eating birds are widely distributed throughout avian phylogeny and are found in 10 orders and at least 23 families containing nearly 1,800 species. At least 18 of these families, with about 1,400 species, contain specialized frugivores (i.e., species whose diet contains a high percentage of fruit; Corlett 1998; Snow 1981). In mammals, frugivores are found in 10 orders and at least 24 families, containing about 600 species. Members of 12 families, with about 480 species, contain specialized frugivores. In contrast to the high ratio of species of nectarivorous birds to mammals (17:1), this ratio for species of frugivores is about 3:1.
As a final taxonomic point, neither feeding mode (nectarivory or frugivory) is especially common in birds and mammals. Of the 127 families of terrestrial birds listed by Gill (1990), only 11 (8.7%) and 23 (18.1%) contain nectar-or fruit-eating species, respectively. Insectivory is by far the most common feeding mode in birds (140 of 168 families [83.3%]). Similarly, of 119 families of terrestrial mammals listed by Vaughan et al. (2000), only three (2.5%) and 26 (21.8%) contain nectar-or fruit-eating species, respectively. Herbivory and granivory are the most common feeding modes in mammals (Eisenberg 1981; Vaughan et al. 2000).
We will discuss in detail other information contained in table 1.1 in subsequent chapters, but we wish to point out here the differences in body sizes associated with nectarivory and frugivory in birds and mammals. In both groups, nectarivores are much smaller than frugivores (table 1.2). Median body masses in families of nectarivores are 22–30 g, and the size ranges of nectar-feeding birds and mammals overlap broadly with each other. In contrast, median body masses in families of frugivores are 127–7,000 g, with mammalian frugivores exhibiting a vastly larger range of sizes than their avian counterparts because of the greater overall size range of terrestrial mammals (shrews to elephants; cf. hummingbirds to ostriches). In both groups, the size range of frugivores spans virtually the entire size range of all terrestrial species. As we will see, body size has profound consequences for the evolution of pollination and frugivory mutualisms.
Major families of flowering plants that provide nectar and/or fruit for their avian and mammalian mutualists are shown in table 1.3. Here and throughout this book we will use APG III (2009) as our basis for plant classification. This table focuses on many (but certainly not all) of the plant families that interact with birds, bats, and primates, three of the major groups of higher vertebrate nectarivores and frugivores. Plants producing bird-or bat-pollinated flowers occur in at least 30 orders (28 of which contain bird flowers and 16 contain bat flowers) and 62 families (54 with bird flowers and 28 with bat flowers). Plants producing fruits eaten by birds, bats, and primates occur in at least 40 orders (40 with bird fruits, 14 with bat fruits, and 20 with primate fruits) and 86 families (82 with bird fruits, 25 with bat fruits, and 35 with primate fruits). Thirty-four of the 112 families (30%) listed in table 1.3 contain taxa that are involved in both vertebrate pollination and frugivory. As in the case of their animal mutualists, more families of angiosperms are involved in vertebrate frugivory than in nectarivory by a factor of about 1.4. Overall, about 40% of the nonaquatic families listed in APG III contain species that produce vertebrate-pollinated flowers or vertebrate-dispersed fruits.
Brief sketches of the important biological features of the major families of animals and plants discussed in this book can be found in appendixes 1 and 2. A cornucopia of images of these animals and their food plants can be found in plates 1–13.
Basic Features of Pollination and Seed Dispersal Mutualisms
GENERAL CONSIDERATIONS
The two mutualisms examined in this book—pollination and seed dispersal—involve the transport of plant propagules, either pollen or seeds, from their point of origin to a point of deposition, usually someplace else in the environment. While acquiring these propagules, most often passively rather than actively, animals obtain a nutritional reward in the form of nectar, pollen, or fruit pulp. When effective mutualistic interactions occur between plants and their pollinators, animal vectors deposit pollen on conspecific stigmas, fertilization of ovules ensues, and fruits containing mature seeds are produced. When effective mutualistic interactions occur between plants and their seed dispersers, frugivores deposit intact seeds in places where they will eventually germinate. Effective pollination mutualisms result in the production of a new cohort of seeds, some of which will survive to become members of the next plant generation whenever effective dispersal takes place. Both of these mutualisms can be short-circuited by a variety of invertebrate and vertebrate "cheaters," species that obtain nutritional rewards without providing an effective "pay-off" or service to plants (Bronstein 2001; Ferriere et al. 2002). Thus, many animals, including legitimate pollinators, remove nectar from flowers without effectively pollinating them, and many frugivores destroy seeds in their mouths, in their guts, or by depositing them in inappropriate places, thereby preventing effective dispersal.
General features of these two mutualisms and how they interact ecologically are summarized in figure 1.1, which is adapted from Wang and Smith (2002). The two mutualisms can be viewed as two interlocking cycles. Starting with a population of adult plants, the pollination cycle begins with flower production and ends with fruit production, events that are basically under the control of plants. Pollen acquisition and deposition, in contrast, are often, but not always, under the control of animal pollinators. Once animals have shed their pollen, they have left this mutualism. The seed dispersal cycle begins with a crop of ripe fruit and mature seeds, which frugivores harvest, either as single units (fruits) or in groups (multiple fruits) depending on the size and behavior of each species. Once seeds are spit out, dropped, or defecated, frugivores have left this mutualism. Compared with the pollination cycle, plants have much less control over the different stages of the dispersal cycle. Germination, seedling recruitment, and seedling/sapling survival and growth, for example, often depend on a variety of extrinsic abiotic and biotic factors beyond the direct control of plants (although plants can have indirect control through the physiological and chemical characteristics of their seeds; Vasquez-Yanes and Orozco-Segovia 1993). Extrinsic abiotic factors include the availability of light and soil moisture and nutrients. Extrinsic biotic factors include the availability of soil mycorrhizae (another mutualism) and the impact of competitors, predators (including herbivores), secondary seed dispersers, pathogens, and "death from above" (i.e., death from falling branches and trees; e.g., Clark and Clark 1991). Because many more external processes (factors) are involved in successful plant recruitment from seed dispersal than in successful pollination, plant-pollinator mutualisms tend to be much more specialized and are subject to potentially stronger plant-animal coevolution, than plant-frugivore mutualisms (Feinsinger 1983; Howe and Westley 1988; Janzen 1983a; Wheelwright and Orians 1982).
With these generalizations in mind, we can now look at the two mutualisms in a bit more detail. Evolutionary aspects of these mutualisms will be thoroughly reviewed in chapters 7 and 8.
THE POLLINATION MUTUALISM
Dispersal propagules in this mutualism are tiny pollen grains, which range in size from about 5 µM to over 200 in length or diameter with most kinds averaging 30–40 µM in length (Proctor et al. 1996). The mass of most individual pollen grains is negligible, although their collective mass can be substantial. For example, male flowers of the bat-pollinated cactus Pachycereus pringlei produce about 470 mg (nearly 0.5 g) of pollen, with each mg containing about 3,540 pollen grains; individual pollen grains weigh about 2.8 × 10-4 mg (Fleming et al. 1994). Given their small size, pollen grains can be effectively dispersed by a wide variety of agents, ranging from the wind and tiny fig wasps (Agaonidae) to large birds and mammals. Pollen grain size does not seriously constrain the kinds of agents plants use to disperse their pollen.
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Excerpted from The Ornaments of Life by Theodore H. Fleming, W. John Kress. Copyright © 2013 The University of Chicago. Excerpted by permission of THE UNIVERSITY OF CHICAGO PRESS.
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