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Crisci, J. V., M. M. Cigliano, J. J. Morrone, and S. Roigjunent. 1991. Historical biogeography of southern South America. Syst. Zool. 40:152 171. Crisci, J. V., L. Katinas, and O. Posadas. 2003. Historical biogeography: an introduction. Harvard University Press, Cambridge, Massachusetts. Darwin, C. 1872. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, sixth edition. John Murray, London. Ebach, M., and C. J. Humphries. 2003. Ontology of biogeography. J. Biogeogr. 30:959962. Ebach, M., C. J. Humphries, and D. M. Williams. 2003. Phylogenetic biogeography deconstructed. J. Biogeogr. 30:12851296. Heads, M., and R. Craw. 2004. The Alpine Fault biogeographic hypothesis revisited. Cladistics 20:184190. Heads, M., and B. Patrick. 2003. Biogeography. Pages 89100 in The natural history of southern New Zealand. (J. Darby, R.E. Fordyce, A. Mark, K. Probert, and C. Townsend, eds.). University of Otago Press, New Zealand. Humphries, C. J. 2000. Form, space and time: Which comes rst? J. Biogeogr. 27:1115. Humphries, C. J., and L. R. Parenti. 1999. Cladistic biogeography. 2nd edition. Oxford University Press, New York. Katinas. L., J. J. Morrone, and J. V. Crisci. 1999. Track analysis reveals the composite nature of the Andean biota. Aust. J. Bot. 47:111 130. McDowall, R. M. 2004. What biogeography is: A place for process. J. Biogeogr. 31:345351.

Morrone, J. J., and J. V. Crisci. 1995. Historical biogeography: Introduction to methods. Ann. Rev. Ecol. Syst. 26:373401. Page, R. D. M., and M. A. Charleston. 1998. Trees within trees: Phylogeny and historical associations. Trends Ecol. Evol. 13:356359. Ronquist, F. 1997. Dispersal-vicariance analysis: A new biogeographic approach to the quantication of historical biogeography. Syst. Biol. 46:195203. Ronquist, F. 1998. Phylogenetic approaches in coevolution and biogeography. Zool. Scr. 26:313322. Sanmartin, I., and F. Ronquist. 2004. Southern hemisphere biogeography inferred by event-based models: Plant versus animal patterns. Syst. Biol. 53:216243. Trewick, S. A. 2000. Molecular evidence for dispersal rather than vicariance as the origin of ightless insect species on the Chatham Islands, New Zealand. J. Biogeogr. 27:11891200. Wallace, A. R. 1876. The geographical distribution of animals. Hafner, New York. Wallis, G. P., and S. A. Trewick. 2001. Finding fault with vicariance: A critique of Heads (1998). Syst. Biol. 50:602609. Waters, J. M., D. Craw, J. H. Youngson, and G. P. Wallis. 2001. Genes meet geology: sh phylogeographic pattern reects ancient, rather than modern, drainage connections. Evolution 55:18441851. Waters, J. M., and G. P. Wallis. 2000. Across the southern Alps by river capture? Freshwater sh phylogeography in South Island, New Zealand. Mol. Ecol. 9:15771582. Jonathan M. Waters, Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand; E-mail: jonathan.waters@stonebow.otago.ac.nz
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Syst. Biol. 54(2):340344, 2005 Copyright c Society of Systematic Biologists ISSN: 1063-5157 print / 1076-836X online DOI: 10.1080/10635150590923209

Hallmarks of the New World

Bromeliaceae: Prole of an Adaptive Radiation.D. H. Benzing (with contributions from B. Bennet, G. Brown, M. Dimmitt, H. Luther, I. Ramirez, R. Terry, and W. Till). 2000. Cambridge University Press, Cambridge, U.K. xii + 690 pp. ISBN 0-521-43031-3. $160.00 (hardcover).

Bromeliads are characteristic and frequently dominant features of tropical and subtropical plant communities in the New World, ranging from the mist-shrouded tepuis of the Guayana Shield to the arid Atacama, from Amazonian rain forests and Andean cloud forests to North American cypress swamps, and from the sun-baked domes of the Brazilian Shield to the frigid puna. Many are epiphytes that live perched on twigs, branches, and boles, without access to reliable sources of moisture and nutrients in terrestrial soil, yet helping shape the ecology of the forests in which they dwell. Others are lithophytes that grow on bare sandstone or granite. How do bromeliads cope with such extreme environments? Why are they often dominant among epiphytes in Neotropical communities? What factors contribute to their remarkable diversity: ca. 2800 species, the fth largest family of monocots, after orchids, grasses, sedges, and aroids? What has been the historical pattern of their ecological radiation and geographic expansion? David Benzing addresses these and many other issues after having devoted a distinguished career to the biology of bromeliads and other epiphytes. He has made

fundamental contributions to understanding the role for water and nutrient uptake of trichomes (leaf hairs) in bromeliads, and analogous structures (root velamen) in orchids, executed clever experiments to quantify the demographics of epiphytic bromeliads and factors restricting them to particular tree species, studied photosynthetic adaptations of bromeliads to different light levels, explored the role of ants in epiphytes in the New World and New Guinea, and pioneered the use of nutrient-hoarding bromeliads as indicators of air quality in south Florida. Bromeliaceae has eight core chapters, dealing with vegetative and reproductive structures, carbon and water balance, mineral nutrition, reproduction, ecology, plantanimal interactions and evolutionary history. Much of the material presented relates to the traditional taxonomic treatment of three subfamilies (Pitcairnioideae, Tillandsioideae, Bromelioideae) based on seed/fruit structure (winged seeds, plumed seeds, or eshy fruits, respectively) and to Benzings classication of bromeliads into ve ecological types, based on earlier systems of Tietze (1906) and Pittendrigh (1948). Bromeliad specialists have long viewed these typesrst recognized in some form by the great ecologist and phytogeographer A. F. W. Schimper (1888)as a scala naturae, leading from the almost exclusively terrestrial pitcairnioids to the terrestrial and epiphytic bromelioids, and reaching

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the acme of physiological and ecological specialization in the almost exclusively epiphytic tillandsioids. Schimper argued that epiphytic bromeliads evolved from species growing in the understory of wet tropical forests, although Pittendrigh countered that epiphytes more likely evolved from species on exposed rocks, adapted to bright light and droughty conditions. Benzing reviews several features of vegetative structure that are crucial for the ecological success of bromeliads, especially as epiphytes. Primary among these are tanks and absorptive trichomes. For epiphytes or lithophytes lacking access to mineral soil, tanks provide a source of moisture and nutrients, with the latter arriving via fallen debris, prey, or commensals. Trichomes provide an answer to a key problem faced by all terrestrial plants: how do the live cells that absorb water and nutrients not become avenues through which moisture exits, leading to desiccation and death? In tillandsioids especially, trichomes serve as one-way valves, allowing moisture and nutrients into the plant but preventing moisture loss. When rainwater wets a leaf, the dead cells of each trichome cap ll and the solution is then absorbed directly by the live cells of the trichome stalk. As the leaf surface dries, the cap cells drain and a vapor lock is established, preventing further water loss from the live stalk cells. Such trichomes can largely replace roots by absorbing water and nutrients through the leaf bases of tank species, or through the infrequently wetted surfaces of the entire leaf in atmospheric species. The downside is that, in areas of very frequent rainfall, constantly wet trichomes can suffocate the plant by occluding the stomata. In the remarkable genus Brocchiniawhich recent molecular analyses place sister to all other bromeliads (Terry et al., 1997a; Horres et al., 2000; Crayn et al., 2004; Givnish et al., 2004, 2005)the absorptive trichomes are unique in remaining alive and retaining protoplasts in both cap and stalk cells. Brocchinia is restricted to extremely humid and nutrient-poor tepuis and sandplains of the Guayana Shield, and its trichomes remain alive and absorptive only on the leaf bases of impounding species. Bromeliads include some of the smallest and largest monocots, from Tillandsia that bloom when a few centimeter tall to giants like Puya raimondii that have the most massive inorescences in the world. Many bromeliads have spinose leaves. Benzing doesnt discuss why, but they almost certainly represent defenses against vertebrate herbivores, and are most common in terrestrial bromeliads on dry or exceedingly nutrient-poor sites, as expected on economic grounds. Rosettes can include hundreds of leaves, or be reduced to a single leaf and enlarged prophyll per rootless ramet in vigorously spreading Spanish moss (Tillandsia usneoides). Curiously, the leaves of some species are marked with dark leaf bases, highlighted with alternating dark and light green shutters and windows, or splashed with bright reds, oranges, or yellows on leaf tips or young foliage. The last almost surely helps attract hummingbirds, especially to bromeliads with inconspicuous owers or inorescence bracts. Benzing suggests that dark leaf bases help hide detritivores, which in turn could accelerate litter break-

down in tanks and benet the plant by speeding nutrient release. This is an attractive hypothesis that could easily be tested. Shutters and windows, especially when most pronounced near the leaf bases, may also help camouage tank inhabitants, but Benzings proposals for their function when they extend across entire leaf rosettes to deter leaf miners by mimicking their damage, increase photosynthetic efciency of multilayered rosettes, or concentrate CO2 in shuttersare not compelling. The signicance of visual banding in epiphytes thus remains an intriguing open question. Unmentioned are mottled leaves in a number of terrestrials (e.g., Cryptanthus), in which variegation may provide camouage from colorblind vertebrate herbivores (Givnish, 1990). Benzings proposal that dense trichome coverage and high reectivity may reduce photodamage is plausible for some highly reective atmospheric species, However, Pierce et al. (2001) show no effect of trichomes on photodamage in others, and little effect on reectivity, and instead show that scattered, non-absorptive trichomes (often on lower leaf surfaces, with stomata) may serve to create hydrophobic, self-cleaning surfaces, which may prevent rain or splashed water and debris from blocking CO2 uptake. Benzing repeatedly raises an argument rst made by Tomlinson (1969), that paedomorphosis is a key adaptation in bromeliads, and that owering at reduced size helps make them fast cyclers that are well-adapted for life on ephemeral epiphytic perches. Perhaps, but few data are presented on leaf and plant longevity, and bromeliads give every impression of being slow growers with long generations, based on the shortages of water and nutrients they often face, low leaf N contents, slow growth rates in many of the (few) species studied (Laube and Zotz, 2003), and slow rates of cpDNA evolution. Ibisch (1996) found that epiphytic Tillandsia adpressa takes 6 to 8 years to begin owering, about 10 years after twigs are rst formed, making even such epiphytic pioneers more similar to slow-growing forest herbs like Trillium than desert annuals. Neoteny may indeed reduce generation time relative to what it would be if owering were delayed until a larger rosette were attainedwhich delay might be incompatible with life in on well-lit twigsbut it may also be associated with a long absolute generation time, due to the lack of moisture and/or nutrients on such perches. Given that rapid cycling features frequently in Benzings argument for why bromeliads are exceptionally diverse (via an effect of generation time on speciation rate), that argument itself becomes questionable. Several fascinating features of bromeliad physiology and reproductive biology are reviewed. Two thirds of bromeliads have CAM (Crassulacean acid metabolism) photosynthesis (which allows CO2 xation at night, greatly reducing water loss but at the cost of reduced photosynthetic capacity); most of these are epiphytes and rock-dwellers. Many epiphytic taxa are restricted to hosts with rough barks that leak nutrients, and they may act as nutritional pirates that soak up nutrients to their hosts disadvantage. Most are pollinated by hummingbirds, but some by bees, butteries, and

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bats. Floral scents range from the ethereal to whiffs of coal gas and spoiled cabbage. Bromeliads are dominant on rock outcrops and the resting a strand communities of southern Brazil, and most especially in the Atacama desert, where several Tillandsia are often the only owering plants present between El Nino years. Among cloud-forest epiphytes, bromeliads are often beaten by orchids to the newest twigs; pioneer bromeliads can take 10 years to bloom; and ericads, ferns, and Peperomia often oust them soon after that. Carnivory has evolved at least twice, and the ant-fed habit many times. A few species emit pheromone-like chemicals to induce ants to haul away their seeds, and land-crabs go bonkers over Bromelia fruits, risking predation as they eagerly clatter over leaves and infructescences. One fruit-eating frog helps coca shrubs establish in the bromeliad rosettes where it seeks haven; a few other bizarre frogs with sclerotized heads hide in tubular Billbergia tanks on sunbaked granitic domes, reducing water loss from themselves and their hosts and possibly providing nutrients as well. Tough-leaved bromeliads may appear to suffer little herbivory, but several are devastated by primates, opposums, and arboreal rodents that tear epiphytes apart to get at prey. And bromeliads are bird magnets, attracting about a third of avian foraging time in some cloud forests. Concluding the core of the book, Benzing joins with Greg Brown and Randall Terry to discuss bromeliad evolution. They opine, without evidence, that the family became recognizable 40 to 65 Mya. The earliest, clearly assignable fossil is only 36 My old, but bromeliads do not occur in habitats favorable for fossilization. Givnish et al. (2004, 2005) provide the rst detailed time lines for bromeliad evolution, using Cretaceous fossils in other groups to calibrate an ndhF monocot phylogeny, including the most complete sampling to date of bromeliad genera. We estimate that bromeliads diverged from their closest relatives about 84 Mya, and that present-day genera began to diverge about 23 Mya with the split of Brocchinia from the ancestor of all the others. The divergence of Brocchinia species from each other began about 20 Mya, at about the same time that other bromeliad genera began to diverge. This casts new light on the remarkable adaptive radiation within Brocchinia; it may replicate the range of nutrient-capture strategies across all other bromeliads (except atmospherics, excluded by live trichomes) partly because it had the same large amount of evolutionary time to do so. Benzing, Brown, and Terry discuss some of the ecological factors that may have resulted in the evolution of large numbers of bromeliad species. Adaptive radiation, driven in part by the key innovations of absorptive trichomes and tanks, and by repeated acquisition of CAM photosynthesis, clearly led to part of this diversity, through the invasion of the epiphytic and lithophytic adaptive zones. The authors argue for broaderscale divergence in habitat as well among several important groups, noting that terrestrial Pitcairnia is often found in warm lowland areas near waterways (50 species in pluvial areas of Ecuador alone!); Nidularium and Cryptanthus in deep shade; tank-dependent tilland-

sioids mainly in cool, humid montane forests; and atmospheric tillandsioids at high and low elevations, probably mainly in more exposed epiphytic microsites. Clearly, highly humid montane areas are favorable for bromeliads; a mid-elevational bulge in the diversity of epiphytes of all kinds has long been recognized. The authors note the apparent dearth of bromeliads in Amazonia. Dense shade may exclude most terrestrial species, and high night temperatures may exclude many CAM epiphytes. Recent surveys (Kreft et al., 2004; Kuper et al., 2004) show a surprising number of lowland epiphytic bromeliad species, especially in the rainiest and least seasonal area of western Amazonia. Kreft and colleagues show a highly regular increase in lowland epiphyte diversity with rainfall and decrease with length of dry season, paralleling a similar pattern documented for trees and shrubs by Gentry (1982). Benzing, Brown, and Terry cite Ibisch et al. (1996) to claim that, after all, perhaps epiphytism doesnt promote high rates of speciation because individual epiphytic bromeliad species have wider ranges than terrestrial species. I believe this is the wrong inference to draw from these data. Epiphytism is clearly associated with increased dispersal ability, potentially opening up large stretches of the Andes to colonization and subsequent differentiation and speciation. Ibisch et al. (1996) demonstrate that epiphyte ranges become narrower at higher elevations, presumably because of the greater dissection of higher elevation habitats by intervening valleys. Evolution of epiphytism may thus accelerate speciation in bromeliads, by opening up a much wider latitudinal range and allowing speciation in highly dissected montane-forest habitats (Givnish et al., 2004, 2005). Widespread selng and limited seed dispersal are two additional factors that may promote genetic differentiation and speciation at small spatial scales, and in my opinion cry out for study. Benzing and colleagues rehearse just about every scenario for the origin of the family, and for relationships among the traditional subfamilies and ecological types, that has ever been advanced. This is a useful service for professionals with a deep interest in bromeliads, but Im not sure it makes for good reading. One problem is that traits are constantly discussed in precladistic fashion with reference to the traditional subfamilies, using a scala naturae slant. Among the scenarios proffered by the pre-cladistic writers, I would say that Medina (1990) came closest to having inferred the state of affairs revealed by the cladistic analyses of ndhF sequence variation (Terry et al., 1997a, 1997b) reviewed in the book, as well as the more denitive treatments that have subsequently appeared. Medina stated that ancestral bromeliads were probably most similar to mesic, heliophytic genera from the Venezuelan tepuis, such as Brocchinia and Navia. In Brocchinia, however, tanks arose in an entirely unexpected fashion, as gutter-like axils among the gigantic leaves of palm-like species in cloud-forest gaps (Givnish et al., 1997). Subsequent reductions produced smaller unitary tanks and led to epiphytism, carnivory, myrmecophily, and nitrogen xation, with all of

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theseand absorptive trichomesalmost surely adaptations to mineral poverty rather than moisture shortage. On page 522, Benzing and colleagues present an ndhF phylogeny for the Bromeliaceae, arguably the bestand perhaps only decisivedata then available with which to the questions regarding relationships within the family and patterns of physiological and ecological evolution that were so prominently raised at the books outset. The original work by Terry et al. (1997a) revolutionized our understanding of bromeliad systematics, which had foundered on widespread convergence in morphological characters and glacially slow rates of chloroplast molecular evolution. A companion paper, also reviewed, presented a more detailed picture of relationships within the subfamily Tillandsioideae. The books treatment extends these analyses signicantly by overlaying Benzings ecological types and gross habit related to water balance (mesic, semixeric, xeric) on the ndhF trees. They infer that, across the family as a whole, nontank species were ancestral and led directly to at least two origins of taxa having weakly developed tanks with some internal roots (e.g., Bromelia and Ananas in Bromelioideae) and three origins of bromeliads having well-developed tanks with absorptive trichomes on their leaf bases (including some Brocchinia, higher bromelioids, and ancestral tillandsioids). These spawned at least two origins of similar forms with CAM photosynthesis, and probably also led to the evolution of atmospheric taxa (like Spanish moss) with few or solely mechanical roots and trichomes over the entire plant surface. So the progression of ecological types, predicted by Benzing and his forebears on functional grounds, appears to have some support, although the taxon sampling is inadequate to assay the full range of variation in ecological types (especially among tillandsioids) and the analysis is misleading because it lumps extremely xerophytic CAM genera (e.g., Dyckia, Puya) with highly mesophytic genera (e.g., Brocchinia) among the nontank forms. If Brocchinia and outgroup Stegolepis were instead classied as a sixth type (mesophytic, C3 nontank species), the authors would have had to conclude that nontank or tank species with leafbase trichomes were ancestral to the family; that nontank species were ancestral to tillandsioids; and that tank species with leaf-base trichomes were ancestral to the remaining species. Tillandsioids were identied as the next divergent branch of bromeliads after Brocchinia, Puya was identied as sister to the bromelioids, and the remaining pitcairnioids samples sister to the Puya-bromelioid clade. Within tillandsioids, the authors inferred the direction of evolution as having been mainly from mesic to xeric conditions, although the ancestral state of the subfamily was unresolved. These analyses were a signicant step forward and complemented earlier analyses of phenotypic, ecological, and geographic evolution in Brocchinia by Givnish et al. (1997). The analyses of Benzing, Brown, and Terry, however, were hampered by extensive gaps in generic coverage, including most pitcairnioid genera. The most recent analyses (Givnish et al., 2004, 2005) conrm the basal position of Brocchinia, support recognition of eight

subfamilies, provide a time line for evolution (Puya species apparently diverged from each other just in the last million years), and imply an origin for bromeliads in humid, nutrient-poor habitats at low elevations in the Guayana Shield. This phylogeny points to repeated origins of epiphytism, CAM photosynthesis (see also Crayn et al., 2004), and the tank habit, repeated acquisition of hummingbird pollination at high elevations, at least two invasions of the Andes, recent long-distance dispersal of Pitcairnia to Africa, and convergence of several xeromorphic traits in Hechtia and a clade consisting of Abromeitiella, Deuterocohnia, Dyckia, and Encholirium. The new time line is crucial, because it connects the rapid burst in bromeliad diversication about 15 Mya with uplift of the northern Andes, the acquisition of CAM, the tank habit, epiphytism, and the invasion of drier habitats and montane habitats beyond the Guayana Shield. This bromeliad revolution can thus be tied to changes in the geography (and climates) of South America and related adaptations to drier conditions, and then led to a great expansion in range and invasion of the epiphytic adaptive zone. Our hope is that such analyses, and a multigene phylogeny now being pursued by an international consortium, will meet the grand challenge laid down by Benzing and provide a truly detailed, integrative prole of the bromeliad radiation. Benzings career-long study of bromeliads, his remarkable breadth of knowledge of research and the classic literature, and his abiding focus on big issues make this book a treasure trove of facts, experimental ndings, hypotheses, and possible areas for future research that all serious students of Bromeliaceae will want to buy and read. But the book is not perfect. Under no circumstance should you read the Introduction rst; it has to be one of the worst lead-ins to great material Ive ever seen, with continual reference to topics or terms undened and to tables and gures scattered deeper in the book. The prose is this section is also turgid. Both aws are unexpected, given Benzings usual gift with language and ability to convey complex topics to popular audiences. I found the separation of chapters on vegetative form and function (carbon metabolism, nutrient capture) inefcient, especially when interleaved with separate chapters on reproductive structure and function. Too frequently, evolutionary ideas were framed in a precladistic schema. Certain parts of the book (e.g., those on photosynthetic adaptations) hide truly critical facts in a welter of detail. Other portionsincluding some delightful concluding chapters by other authors on bromeliad ethnobotany (of great interest since Columbus introduced the pineapple as a hallmark of the New World), tillandsioid systematics (which itself is rapidly evolving), and bromeliad conservation (too many species have been endangered or extirpated in the wild by collectors)are wonderful. A new generation of highly productive, incisive researchers is already hard at work. Pierce et al. (2002) have solved the mystery of widespread CAM in epiphytic bromelioids in wet forests. Schmidt and Zotz (2001) have carefully quantied how the advantages of the tank and atmospheric habits vary with plant size. Laube and Zotz

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(2003) and Graham and Andrade (2004) have shown that water is more important than nutrients in determining growth by epiphytic bromeliads, and that the apparent adaptation of epiphytic bromeliads to different light levels may actually involve adaptations to different levels of drought stress instead. In many ways, Portrait of an Adaptive Radiation may ultimately be seen as the concluding and most decisive book of the Old Testament of bromeliad ecology and evolution, begun by Schimper, Tietze, Baker, Mez, Harms, Pittendrigh, Tomlinson, and Smith. Efforts now under way will likely open a New Testament, based on highly resolved molecular phylogenies; closer integrations of physiological, ecological, and ecosystem studies; rigorous quantication of tradeoffs associated with specic growth forms and means of nutrient capture; research on the spatial scales of genetic divergence and incipient mating barriers and limits to plasticity; and careful analyses of the roles of adaptive radiation vis-` -vis isolation by distance, coevolution, and a other factors generating bromeliad diversity. R EFERENCES
Crayn, D. M., K. Winter, and J. A. C. Smith. 2004. Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proc. Natl. Acad. Sci. U.S.A. 101:37033708. Gentry, A. H. 1982. Patterns of Neotropical plant species diversity. Evol. Biol. 15:184. Givnish, T. J. 1990. Leaf mottling: Relation to growth form and leaf phenology, and possible role as camouage. Funct. Ecol. 6:463474. Givnish, T. J., K. C. Millam, P. E. Berry, and K. J. Sytsma. 2005. Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data. In: Monocots: Comparative biology and evolution (2 volumes). (J. T. Columbus, E. A. Friar, C. W. Hamilton, J. M. Porter, L. M. Prince, and M. G. Simpson, eds.). Rancho Santa Ana Botanic Garden, Claremont, California, in press. Givnish, T. J., K. C. Millam, T. M. Evans, J. C. Hall, J. C. Pires, P. E. Berry, and K. J. Sytsma. 2004. Ancient vicariance or recent long-distance dispersal? Inferences about phylogeny and South American-African disjunctions in Rapateaceae and Bromeliaceae. Int. J. Plant Sci. 165:S35S54. Givnish, T. J., K. J. Sytsma, J. F. Smth, W. J. Hahn, D. H. Benzing, and E. M. Burkhardt. 1997. Molecular evolution and adaptive radiation in Brocchinia (Bromeliaceae: Pitcairnioideae) atop tepuis of the Guayana Shield. Pages 259311 in Molecular evolution and adaptive radiation (T. J. Givnish and K. J. Sytsma, eds.). Cambridge University Press, New York.

Graham, E. A., and J. L. Andrade. 2004. Drought tolerance associated with vertical stratication of two co-occuring epiphytic bromeliads in a tropical dry forest. Am. J. Bot. 91:699706. Horres, R., G. Zizka, G. Kahl, and K. Weising. 2000. Molecular phylogenetics of Bromeliaceae: Evidence from trnL(UAA) intron sequences of the chloroplast genome. Plant Biol. 2:306315. Ibisch, P. L. 1996. Neotropisiche Epiphytendiversit tdas Beispiel a Bolivien. Martina Galunder Verlag, Wiehl. Ibisch, P. L., A. Boegner, J. Nieder, and W. Barthlott. 1996. How diverse are Neotropical epiphytes? An analysis based on the Catalogue of owering plants and gymnosperms of Peru. Ecotropica 2:1328. Kreft, H., N. Koster, W. Kuper, J. Nieder, and W. Barthlott. 2004. Diversity and biogeography of vascular epiphytes in Western Amazonia, Yasuni, Ecuador. J. Biogeogr. 31:14631476. Kuper, W., H. Kreft, J. Nieder, N. Koster, and W. Barthlott. 2004. Largescale diversity patterns of vascular epiphytes in Neotropical montane rain forests. J. Biogeogr. 31:14771487. Laube, S., and G. Zotz. 2003. Which abiotic factors limit vegetative growth in a vascular epiphyte? Funct. Ecol. 17:598604. Medina, E. 1990. Eco-siologia y evolution de las Bromeliaceae. Bot. Acad. Nac. Cien. Cord. 59:72100. Pierce, S., K. Maxwell, H. Grifths, and K. Winter. 2001. Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. Am. J. Bot. 88:13711389. Pierce, S., K. Winter, and H. Grifths. 2002. The role of CAM in high rainfall cloud forests: An in situ comparison of photosynthetic pathways in Bromeliaceae. Plant Cell Environ. 25:11811189. Pittendrigh, C. S. 1948. The bromeliad-Anopheles-malaria complex in Trinidad. I. The bromeliad ora. Evolution 2:5889. Schimper, A. F. W. 1888. Die epiphytische vegetation Amerikas. Botanische Mitteilungen aus den Tropen, Band II. Gustav Fischer Verlag, Jena. Schmidt, G., and G. Zotz. 2001 . Ecophysiological consequences of differences in plant size: In situ carbon gain and water relations of the epiphytic bromeliad, Vriesea sanguinolenta. Plant Cell Environ. 24:101111. Terry, R. G., G. K. Brown, and R. G. Olmstead. 1997a. Examination of subfamilial phylogeny in Bromeliaceae using comparative sequencing of the plastid locus ndhF. Am. J. Bot. 84:664670. Terry, R. G., G. K. Brown, and R. G. Olmstead. 1997b. Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) using ndhF sequences. Syst. Bot. 22:333345. Tietze, M. 1906. Physiologische Bromeliaceen-Studien II. Die Entwicklung der wasseraufnehmenden Bromeliaceen-Trichome. Zeitschrift fur Naturissenschaften 78:150. Tomlinson, P. B. 1969. Anatomy of the monocotyledons: III. Commelinales-Zingiberales. Oxford University Press, London. Thomas J. Givnish, Department of Botany, University of Wisconsin, Madison, Wisconsin 53706, USA; E-mail: givnish@facstaff.wisc.edu

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