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Non-Flying Mammals as Pollinating Agents in the Amazonian Forest

1981; Wiley; Volume: 13; Issue: 2 Linguagem: Inglês

10.2307/2388065

1744-7429

Charles H. Janson, John Terborgh, Louise H. Emmons,

Plant Diversity and Evolution

Three species of flowers are used intensively by as many as seven species of diurnal and six species of nocturnal, non-flying mammals during the dry season in southeastern Peru. The possibility of a significant pollination role for these mammals is suggested by lack of severe damage to the flowers, heavy uptake of pollen on facial fur, and traplining behavior by several species. The heavy construction of these three flower species and the coincidence of their availability with a period of fruit scarcity suggest that they may be evolutionarily adapted to use by non-flying, omnivorous mammals. FLOWER POLLINATION BY NON-FLYING MAMMALS (therophily) has received recent attention after being largely neglected since the pioneering work of Porsch (1934, 1935, 1936). Use of nectar by non-flying mammals is well known (Petter 1962, Coe and Isaac 1965, Faegri and Van der Pijl 1971, Johnson and Briggs 1975, Sussman and Tattersall 1976, Lack 1977, Carpenter 1978), but few cases are sufficiently well documented to warrant the supposition of coevolved plant-pollinator relationships (Rourke and Wiens 1977, Sussman and Raven 1978). In addition to frequent use of a species of flower by a supposed pollinator, other evidence is necessary: lack of damage to the reproductive capacity of the flower during use, uptake and transferral of pollen by the animal, movement between individual plants, specific access to the flower by the pollinator, and structural modification of the flower for use by the pollinator. We shall present evidence concerning these points for several species of flowers used as nectar sources by a number of mammals at Cocha Cashu Biological Station, Manu National Park, Madre de Dios, Peru (ca 11?22'S, 71'22'W). The observations were made during a year-long study of primate foraging ecology in 1976-77, and in July and August of 1978. Many trees and vines flower conspicuously in southeastern Peru during the dry season (June-August), including several that are regularly visited by a wide variety of non-flying mammals: Erythrina 2 spp. (Leguminosae), Ceiba pentandra (L.) Gaertn. (Bombacaceae), Quararibea cordata (Humb. & Bonpl) Vischer (Bombacaceae), Ochronza pyrarnidale (Cav.) Urban (Bormbacaceae), and Combreturn fruticosurn (Loefl.) Stuntz (Combetraceae). Our observations suggest that non-flying mammals are significant pollinators of all but the Erythrina species, notwithstanding that among them are ones considered to be bat pollinated (Ceiba pentandra: Baker and Harris 1969; Ochroma pyrazmidale: Faegri and Van der Pijl 1971) or bird pollinated (Co;nbretunm: Sussman and Raven 1978 for Combretzun phaneropetalunm (C. fruticosum) ). Comibretum fruticosunz is a robust canopy liane that is especially common in seasonally inundated forest and along river margins where flood-induced disturbances provide numerous gaps that are invaded by its seedlings. The flowers progress through a sequence of color changes as they mature, being a yellow-green before opening, then turning to yellow, orange, and finally deep red. The dense terminal spikes are 10-20 cm long and carry an average of 90-100 flowers. Groups of 3-5 spikes are arrayed in horizontal sprays. The shallow 0.8 cm floral cups are held stiffly upright in multiple rows on short pedicels. Copious quantities of bright pink to orange pollen are released from 3 cm exserted stamens during anthesis in late June and July. DIURNAL VISITATION.-The flowers of C. fruticosum were visited diurnally by at least seven species of primates, including the tiny (100 g) pigmy marmoREPRODUCTIVE BOTANY 1-6 1981 1 lThe editor owes these authors an apology, for the note by Prance describing the probable pollination of Combretumn by monkeys (1980, Vol. 12(3) :239) was received after this paper. The earlier publication date was due to its notesize. Sorry! This content downloaded from 207.46.13.57 on Fri, 09 Sep 2016 04:23:01 UTC All use subject to http://about.jstor.org/terms set (Cebuella pygmaea) and the large (7 kg) spider monkey (Ateles paniscus), in addition to the five species listed in table 1. Primates tended to feed systematically, visibly lapping the nectar from one cup after another as they worked their way down the length of a spike. Typical feeding bouts per vine varied from a few minutes (Saimiri) to nearly half an hour (Saguinus imperator). After feeding, the muzzles of the animals would be conspicuously tinted pink by adherent pollen. Primate visitation resulted in moderate to heavy losses of the distal portions of the flowers, leaving the inferior ovaries attached to their pedicels. Abundant seed set by many plants that had been used by primates suggests that flower loss occurred mainly during the terminal phase of anthesis after pollination had been effected. Combretum fruticosum is the flower most avidly used by primates, accounting for as much as 71 percent of the feeding time of the tamarin Saguinus fuscicollis during a 10-day sample period in July 1977 (table 1). The home ranges of the primate species listed in the table are large enough (20-100 ha) to contain numbers of Combretum vines, several of which may be visited in rapid succession. A typical day's excursion by Cebus apella is illustrated in figure 1. Smaller monkeys tended to use fewer vines per day than larger ones, but may have used the ones they visited more intensively. Combretum also attracted at least 14 species of birds including small parrots, hummingbirds, jays, oropendolas, caciques, and tanagers. Birds often fed concurrently with monkeys in the vines, although their visits tended to be shorter ( 5 _ (07/22-08/07/77) 0.16 2.9 11 0.35 3.4 5 aFeeding time refers only to the use of vegetable resources. It is the sum of the times spent feeding for all the members of a monkey troop in a given sample. 2 Janson, Terborgh, and Emmons -e F C