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Review
. 2009 Nov;104(6):1017-43.
doi: 10.1093/aob/mcp197. Epub 2009 Sep 29.

The evolution of bat pollination: a phylogenetic perspective

Affiliations
Review

The evolution of bat pollination: a phylogenetic perspective

Theodore H Fleming et al. Ann Bot. 2009 Nov.

Abstract

Background: Most tropical and subtropical plants are biotically pollinated, and insects are the major pollinators. A small but ecologically and economically important group of plants classified in 28 orders, 67 families and about 528 species of angiosperms are pollinated by nectar-feeding bats. From a phylogenetic perspective this is a derived pollination mode involving a relatively large and energetically expensive pollinator. Here its ecological and evolutionary consequences are explored.

Scope and conclusions: This review summarizes adaptations in bats and plants that facilitate this interaction and discusses the evolution of bat pollination from a plant phylogenetic perspective. Two families of bats contain specialized flower visitors, one in the Old World and one in the New World. Adaptation to pollination by bats has evolved independently many times from a variety of ancestral conditions, including insect-, bird- and non-volant mammal-pollination. Bat pollination predominates in very few families but is relatively common in certain angiosperm subfamilies and tribes. We propose that flower-visiting bats provide two important benefits to plants: they deposit large amounts of pollen and a variety of pollen genotypes on plant stigmas and, compared with many other pollinators, they are long-distance pollen dispersers. Bat pollination tends to occur in plants that occur in low densities and in lineages producing large flowers. In highly fragmented tropical habitats, nectar bats play an important role in maintaining the genetic continuity of plant populations and thus have considerable conservation value.

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Figures

Fig. 1.
Fig. 1.
Portraits of flower-visiting bats. Approximate body masses are in parentheses. (A) Glossophaga soricina (10 g), a basal glossophagine; (B) Choeronycteris mexicana (16 g), a derived glossophagine; (C) Artibeus jamaicensis (45 g) and (D) Phyllostomus elongatus (60 g), two opportunistic flower-visiting phyllostomids; (E) Syconycteris australis (20 g) and (F) Eonycteris spelaea (70 g), two specialized nectarivorous pteropodids; (G) Pteropus poliocephalus (750 g) and (H) Epomophorus gambianus (100 g), two opportunistic flower-visiting pteropodids. Photo credits: Merlin D. Tuttle, Bat Conservation International.
Fig. 2.
Fig. 2.
Nectar-feeding bats visiting flowers. (A) Glossophaga soricina at flowers of Mabea occidentalis (Euphorbiaceae); (B) Artibeus jamaicensis on a flower of Ochroma pyramidale (Bombacaceae s.s.); (C) Eonycteris spelaea on flowers of Durio zibethinus (Bombacaceae s.s.); (D) Pteropus conspicillatus at flowers of Castanospermum australe (Fabaceae). Photo credits: Merlin D. Tuttle, Bat Conservation International.
Fig. 3.
Fig. 3.
Bat-pollinated flowers, corolla or perianth length (when known), and their pollinators. (A) Agave palmeri (Asparagales: Agavaceae), corolla tube 45–60 mm, glossophagine bats; (B) Musa acuminata (Zingiberales: Musaceae), perianth 70 mm, opportunistic and specialized pteropodid bats; (C) Heliconia solomonensis (Zingiberales: Heliconiaceae), perianth 45–75 mm, specialized pteropodid bats; (D) Canna liliiflora (Zingiberales: Cannaceae), glossophagine bats; (E) Vriesia sp. (Poales: Bromeliaceae), glossophagine bats; (F) Psittacanthus acinarius (Santalales: Loranthaceae), corolla 50–75 mm, glossophagine bats; (G) Calyptrogyne ghiesbreghtiana (Arecales: Arecaceae), rachilla 220 mm, opportunistic phyllostomid bats; (H) Phenakospermum guyannense (Zingiberales: Strelitziaceae), perianth up to 280 mm, opportunistic phyllostomid bats. Photo credits: T. Fleming (A), W. J. Kress (B–E, G, H), C. Geiselman (F).
Fig. 4.
Fig. 4.
Bat-pollinated flowers, their corolla or perianth length (when known), and their pollinators. (A) Carnegiea gigantea (Caryophyllales: Cactaceae), corolla 112 mm, opportunistic and specialized phyllostomid bats; (B) Markhamia stipulata (Lamiales: Bignoniaceae), specialized pteropodid bats; (C) Burmeistera ceratocarpa (Asterales: Campanulaceae), corolla 13·2 mm, glossophagine bats; (D) Chelonanthus alatus (Gentianales: Gentianaceae), corolla 30–45 mm, glossophagine bats; (E) Lecythis poiteaui (Ericales: Lecythidaceae), androecium 50 mm, glossophagine bats; (F) Hymenaea courbaril (Fabales: Fabaceae), flower diameter 25 mm, opportunistic and specialized phyllostomid bats; (G) Ceiba pentandra (Malvales: Malvaceae), flower diameter 25–35 mm, opportunistic and specialized phyllostomids and pteropodids; (H) Caryocar glabrum (Malpighiales: Caryocaraceae), flower diameter 40 mm, opportunistic and specialized phyllostomid bats. Photo credits: T. Fleming (A, B), C. Geiselman (D), S. Mori (E–H), N. Muchhala (C).
Fig. 5.
Fig. 5.
Cladogram showing the evolutionary relationships of orders of angiosperms and the distribution of families containing bat-pollinated taxa among them. Five types of bat pollination are highlighted: pollination only by New World phyllostomids, pollination only by Old World pteropodids, pollination by both bat families, and single species pollinated either by New World or Old World bats. Cladogram based on Soltis et al. (2005).

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