Nonflying Mammal Pollination of Southern African Proteas: A Non-Coevolved System

Abstract

Traits characterizing those proteas adapted for pollination by nonflying mammals include: bowlshaped heads bearing fleshy bracts, these borne on short, flexible peduncles, often at or near ground level (geoflorous) and hidden beneath dense overlying foliage (cryptic), and producing copious nectar (ca. 1.8 ml/head, standing crop); individual florets with wiry, yet flexible styles and a nectar-stigma distance of 10 mm; a distinctive yeastlike odor; nocturnal anthesis; sucrose-rich nectar with a high total carbohydrate content (ca. 36%) and a relatively low proportion of amino acids. Evidence of small-mammal visitation to protea flowering heads includes: the presence of pollen on the rostra (carried in a position to effect pollination when foraging for nectar); the transport of fluorescing powders to flowering heads both within and between plants; the accumulation of small-mammal feces in flowering heads, and the destruction of exclosure bags containing nectar-rich heads. The period of greatest small-mammal activity (1800 hr.) coincides with maximum flower opening. T maze experiments showed that small mammals, when given a choice between typically bird-pollinated proteas and those having characteristics of flowers pollinated by nonflying mammals, always foraged on the latter. That small mammals can effect pollination is indicated by their foraging behavior on flowering heads while in captivity, the morphological fit between individual florets and the rostra of small mammals, and by selective exclosure experiments that reduced seed set (50% and 95%) when small mammals were excluded and visitation was limited to insects (mostly honey bees). The ne~ctar produced 'The study was supported in part by NSF grant (DEB 78-11624). We thank B. Albee, L. Arnow, H. G. and I. Baker, P. Cox, V. Grant, S. D. Hopper, P. H. Raven, and V. Turner for helpful comments on the manuscript. People too numerous to mention individually assisted the research, in particular the staffs of the Karoo Botanic Garden, and Kirstenbosch Botanic Garden and its director Prof. Brian Rycroft. The curator of the Karoo Garden, Mr. Bruce Bayer, provided generous logistical and field assistance and engaged in stimulating discussions of the problem from its inception. Peter and Connie Smits offered unsurpassed hospitality and Peter's keen photographic sense was invaluable. Drs. Nick and Marie Strickland, Dr. Derek Mitchell, and Dr. J. U. M. Jarvis, all of Cape Town University, as well as Dr. Fred Kruger, South African Forestry Research Institute, Pretoria, assisted in various capacities. The late Fred du Plesis and his wife, Thelma, provided access to the unparalleled study sites on Jonaskop. Dr. Walter Veith, Stellenbosch University, obtained the metabolic rates of Aethomys and the caloric value of P. humiflora nectar; we are also indebted to Stellenbosch University for the use of their scanning electron microscope facility. Prof. H. G. and I. Baker, University of California, Berkeley, determined the carbohydrate and amino acid compositions of protea nectar, showed a continuing interest in the problem and offered various helpful suggestions. Finally, but not least importantly, we are indebted to field assistance from Tori Burns, Heidi Fain, and Jenny Turner, who survived the southeasters! 2 Department of Biology, University of Utah, Salt Lake City, Utah 84112. 3 Kirstenbosch Botanic Garden, Claremont, South Africa 7735. 4 Present address: Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104. 5 Department of Biochemistry, University of the Western Cape, Bellville, South Africa 7530. ANN. MISSOURI BOT. GARD. 70: 1-31. 1983. This content downloaded from 157.55.39.153 on Mon, 19 Sep 2016 04:55:36 UTC All use subject to http://about.jstor.org/terms 2 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VOL. 70 by these proteas meets the energy requirements of the small-mammal community for only several days annually, thus coevolution is impossible. Proteas adapted for pollination by nonflying mammals have evolved unilaterally, probably from bird-pollinated prototypes, possibly in response to progressive decrease in population size. Recent discoveries in the Neotropics of flowers with some similar characteristics and also pollinated by nonflying mammals support the existence of a worldwide class of flowers adapted for such pollinators. The pollination of flowers by nonflying mammals was first mentioned by Kerner (1895, v. 2, p. 230) and was discussed nearly 50 years ago by Porsch (1934, 1935, 1936a, 1936b). The subject was not given further attention, however, until Morcombe (1968) suggested pollinatory relationships between various proteaceous flowers and nonflying mammals in the southwestern Australian flora. Rourke and Wiens (1977) reviewed the problem and noted that various floral features convergent in Australian and South African Proteaceae suggested adaptations for pollination by nonflying mammals. The following year Wiens and Rourke (1978) offered substantive evidence for pollination by nonflying mammals (mostly rodents) in two species of South African proteas. Two previous studies of presumably bat-pollinated African plants, viz., the baobab (Bombacaceae) (Coe & Isaac, 1965) and Maranthes (Chrysobalanaceae) (Lack, 1977) demonstrated visitation and nectar feeding by bush babies (Galago crassicaudatus Geoffroy) and genets (Genetta tigrina Schreber), respectively. Recent interest in the subject has resulted in a number of publications: Sussman and Raven (1978) reviewed the problem and reported pollination by arboreal Madagascan mouselike lemurs; Sleumer (1955) and Carpenter (1978a) reported evidence for the pollination of eastern Australian banksias by sugar gliders (Petaurus breviceps Waterhouse) and the indigenous placental bushrat (Rattus fuscipes Waterhouse), respectively. Holm (1978) and Ford, Paton, and Forde (1979) commented on the problem and Armstrong (1979) reviewed the subject for Australia generally. Wiens, Renfree, and Wooller (1979) and Hopper (1980) studied the pollination of Banksia and other flowers by the southwestern Australian marsupial honey possum (Tarsipes rostratus = T. spenserae Gray). In the New World, Prance (1980) observed probable pollination by cebus monkeys; and Janson, Terborgh, and Emmons (1981) reported extensive visitation and apparent pollination in Bombacaceae and Combretaceae in the Amazon by monkeys [including the small (100 g) pigmy marmoset], opossums, and procyonids. Lumer (1980) observed pollination of Blakea (Melastomataceae) by rodents in Costa Rica, and Steiner (1981) discovered probable pollination by opossums in Mabea (Euphorbiaceae) in Panama. The suggestion of rodent pollination in Hawaiian Freycinetia (Degener, 1945) is apparently in error (Cox,