Partitioning of pollinators during flowering in an African Acacia community

Ecology, Dec, 1998 by Graham N. Stone, Pat Willmer, J. Alexandra Rowe

INTRODUCTION

Flowering plants may compete for pollination in at least two ways; for pollen quantity, and for pollen quality (Rathcke 1983, 1988). In cases where the quantity of pollen exchanged is a limiting factor for seed set, plants may compete for pollinator visits (Mosquin 1971, Bierzychudek 1981, Horvitz and Schemske 1988). In other cases, the purity of the pollen pollinators carry, rather than the number of visits they make, is the controlling factor. If pollinators visit a mixture of flowering species over a short period, some proportion of the pollen they deposit on stigmas may be heterospecific. Heterospecific pollen transfer has the potential to reduce reproductive success in two ways: male-function may be reduced through deposition on heterospecific stigmas, while female function may be reduced through physical blocking of limited stigmatic surface with heterospecific pollen (Waser 1978a, b, 1983, Waser and Fugate 1986, Fishbein and Venable 1996). Evidence to date suggests that avoidance of heterospecific pollen transfer is more important than competition for pollinator visits in natural systems (Waser 1983, Rathcke 1983, 1988) and minimization of the costs associated with either mechanism of competition is thought to be an important force structuring plant communities (Pleasants 1983, Rathcke 1983, 1988, Waser 1983, Armbruster and Herzig 1984, Rathcke and Lacey 1985, Feinsinger 1987).

An expected evolutionary consequence of competition is divergence along some resource axis (resource partitioning) to reduce the negative interaction between coexisting species (Brown and Wilson 1956, Pianka 1973, Schoener 1983). Four resource axes have received attention. First, plants may differ in the pollinators they recruit (axis 1), and so have independent vectors of pollen transfer (Heinrich 1976, Inouye 1978, Pleasants 1983, Armbruster and Herzig 1984, Rathcke 1988). However, pollinator guilds of plant species often overlap and many studies have examined mechanisms that partition the activity of shared flower visitors (Waser 1978a, b, Feinsinger 1983, Kephart 1983, Schemske 1983, Armbruster 1985, Campbell and Motten 1985, Waser and Fugate 1986, Rathcke 1988). Plants in the same pollinator guild may utilize effectively independent populations of the same pollinator species (and thus avoid competition) through separation in space (axis 2) (Pleasants 1980, Rathcke 1988) or in seasonal time (axis 3) (Levin and Anderson 1970, Mosquin 1971, Heithaus 1974, Poole and Rathcke 1979, Pleasants 1980, 1983, Kephart 1983, Rathcke 1983, Ashton et al. 1988). Relatively few studies have directly examined the effects of such putative mechanisms on the activity of shared pollinators (Waser 1978a, b, Pleasants 1980, Waser 1983, Campbell 1985, Armbruster and McGuire 1991, McGuire and Armbruster 1991, McGuire 1993).

An increasing number of studies, however, show that sympatric species may share pollinators and have overlapping flowering seasons. Such clustering may result through limited divergence of contemporary species from ancestral patterns of flowering (Kochmer and Handel 1986, Wright and Calderon 1995) or-from constraints on flowering imposed by seasonal patterns in the availability of resources such as water or thermo-period (Janzen 1967, Hocking 1968, Reich and Borchert 1984, Rathcke 1984, 1988, Johnson 1992). A fourth resource axis allowing such co-flowering species to share pollinator individuals is the utilization of discretely different parts of the pollinator's body for pollen transport (axis 4) (Dressier 1968, Armbruster et al. 1994). A further possibility is the evolution of floral traits, such as increased floral longevity, that confer tolerance of competition (Levin 1978, Molten 1986, Rathcke 1988, Ashman and Schoen 1994).

An alternative is for plant species to diverge along an additional resource axis: daily time (axis 5). Divergence among co-flowering species in their timing of pollen release (dehiscence) through the day could reduce competition in two ways (Levin and Anderson 1970, Ollerton and Lack 1992). First, daily partitioning of resource availability could result in temporal partitioning of pollinator behavior, so that co-flowering plants avoid competition for pollinator visits. Second, because many pollinators remove pollen from their bodies at regular intervals (Gilbert 1981, Roubik 1989), temporal partitioning of their activity will result in pollinators carrying predominantly one type of pollen at any one time, so reducing interspecific pollen transfer. Both mechanisms allow sympatric co-flowering plants to share both flowering seasons and pollinators.

Few studies have examined in detail the daily activity patterns of shared pollinators at the flowers of potentially competing plants (but see Armbruster and Herzig 1984, Armbruster 1985, Stone et al. 1996), despite the fact that these patterns may have important consequences for the inference of competition in plants whose flowering seasons overlap. Two plants with identical flowering seasons and pollinators may indeed compete if pollinators visit them indiscriminately during the day, but competition may be substantially reduced if the pollinators' daily activity patterns at the two plants are entirely separated. The importance of daily structuring in competition for pollination is unclear. Although shared pollinators are known to visit particular plant species at different times of day (Frankie et al. 1983, Stone 1994), most analyses of flowering phenology have addressed seasonal phenology and lack the necessary resolution to examine daily patterns.