Pollen Carryover, Geitonogamy, And The Evolution Of Deceptive Pollination Systems In Orchids

S. D. JOHNSON [1,3]

L. A. NILSSON [2]

(1.) School of Botany and Zoology, University of Natal, Private Bag X01, Scottsville, Pietermaritzburg 3209, South Africa

(2.) Department of Systematic Botany, University of Uppsala, Villavagen 6, S-75236 Uppsala, Sweden

Abstract. Geitonogamy (transfer of pollen among flowers on the same plant) may lead to reduced outcrossing and interfere with sex function. Orchids with pollen packaged into pollinaria would be expected to be particularly vulnerable to the loss of cross-mating opportunities imposed by geitonogamy. We tested the hypothesis that the absence of floral rewards in many orchid species is a means of reducing geitonogamy. Experiments with the deceptive species Orchis mascula and Orchis morio showed that queen bumble bees probe more flowers and stay longer on plants when artificial nectar is added to the flowers. Overall, the data indicated that the evolution of nectar production in deceptive Orchis species would result in moderate to high levels of geitonogamy, as a consequence of the greater number of flowers probed and longer visit duration (60 s) by pollinators. However, the estimated levels of geitonogamy were less than expected, due both to a time delay before freshly withdrawn pollinaria bend into the correct position to strike a stigma and to extensive carryover of pollen. The time elapsed before a freshly withdrawn pollinarium is in the correct position to strike the stigma was found to vary 30-80 s, depending on the orchid species. Since pollinators usually spend [less than]30 s on an inflorescence, we estimate that natural populations of the study species are highly outcrossed. The fraction of the pollen load carried over from flower to flower was found to be 0.67 in O. mascula. Selection should favor longer delays in pollinaria bending and extensive pollen carryover in nectar-producing orchids. This is corroborated by the nectariferous orchid Platanthera chlorantha, which we found to have a pollinaria bending delay of 80 s and a high pollen carryover fraction (0.87). In general, selection for traits that prevent geitonogamy should occur only when pollinators are abundant. Since fruit set of orchids is usually pollinator limited, additional explanations may have to be sought to explain deception. The most pla usible complementary hypothesis is that resources in pollinator-limited orchids are invested in advertising display, rather than nectar production.

Key words: deception; floral traits; geitonogamy; nectar; Orchidaceae; Orchis mascula; Orchis morio; Platanthera chlorantha; pollen carryover; pollen limitation; pollination.

INTRODUCTION

Apparently, plants are able to attract pollinators, while at the same time encouraging them to leave quickly

de Jong et al. (1993)

Most angiosperm flowers produce rewards, e.g., nectar, pollen, oils, resins, or fragrances, which are sought by animal pollinators (Simpson and Neff 1983). Nectar is by far the most common reward in flowers. Larger volumes of nectar have been shown to increase the number of flowers probed by pollinators, as well as the duration of probes, which in turn lead to greater levels of pollen deposition and removal per plant (Thomson and Plowright 1980, Hodges 1981, 1995, Waddington 1981, Zimmerman 1983, Galen and Plowright 1985, Thomson 1986, Pyke et al. 1988, Harder 1990, Mitchell and Waser 1992, Mitchell 1993, Burd 1995).

The seemingly well-established idea that nectar confers fitness benefits is, however, confounded by the existence of thousands of animal-pollinated plant species that produce no rewards in their flowers. The majority of these plants belong to the Orchidaceae. There are an estimated 19 500 orchid species (Dressler 1993), of which more than one-third (8000 species) are deceptive, i.e., do not offer floral rewards to their pollinators (Little 1983, Dafni 1984, Ackerman 1986).

Nonrewarding orchids use a variety of ploys (e.g., sexual deception, brood-site mimicry, Batesian mimicry, and generalized food source deception) to attract pollinators (Little 1983, Dafni 1984, Ackerman 1986, Nilsson 1992, Johnson 1994). Here we are concerned only with the most common type of deception, which involves the exploitation of generalized food-seeking behavior in pollinators. Almost all food source deceptive orchids are pollinated by nectar-seeking insects (Dafni 1984, Ackerman 1986).

Although the pollination biology of many deceptive orchids has been investigated, there has been little progress in determining what selective pressures result in the loss of rewards and why the orchid family should be especially prone to deception (Ackerman 1986, Gill 1989). Shifts between rewarding and deceptive pollination systems have occurred many times in the evolution of the Orchidaceae (Dressler 1981). In the South African genus Disa, for example, there have been at least three evolutionary transitions between nectar-producing and nonrewarding flowers (Johnson et al. 1998).

Most attempts to explain deception have invoked trade-offs between seed production and the energetic costs of nectar (Boyden 1982, Ackerman 1986). According to these arguments, the resources used to produce rewards are costly and better allocated to fruit production and survivorship in some species (cf. South-wick 1984, Ackerman 1986, Ackerman and Montalvo 1990, Pyke 1991). The main problem with this hypothesis is that the lifetime fitness of many orchids is pollination limited, rather than resource limited (Calvo and Horvitz 1990, Calvo 1993).