Are there fitness advantages in being a rewardless orchid? Reward supplementation experiments with Barlia robertiana

Abstract

The Orchidaceae characteristically contain a very large number of species that attract pollinators but do not offer them any form of reward in return for visitation. Such a strategy is highly unusual in the plant kingdom. We conducted experiments in order to manipulate the reward strategy of the rewardless bumble-bee-pollinated orchid Barlia robertiana by adding sucrose solution to inflorescences. We found that supplementation decreased the probability of a pollinator removing pollinia by approximately ten times. Despite pollinators visiting many more flowers per inflorescence on supplemented plants, eight times fewer pollinia were removed from supplemented inflorescences during each visit. Pollinia deposition patterns were not significantly affected by supplementation and no geitonogamous deposition was recorded. In populations where inflorescences were supplemented for 20 days, pollinia removal was reduced by over half for supplemented inflorescences, whereas fruit set was unmodified by supplementation. We conclude that rewardlessness would increase total seed paternity, but not change either total seed maternity or the probability that offspring were outcrossed in this species. To the authors' knowledge this is the first time that there has been an unequivocal experimental demonstration of an evolutionary advantage for rewardlessness in the Orchidaceae.

Pollinator limitation and inbreeding depression in orchid species with and without nectar rewards

“…The evidence that this pollinator behaviour causes differences in geitonogamy rates is mixed, with some studies supporting (Johnson & Nilsson, 1999;Johnson et al, 2004) and some disputing (Smithson & Gigord, 2001;Smithson, 2002) this hypothesis. Since alternative mechanisms, such as slow post-removal pollinarium bending, can partially or completely prevent geitonogamous selfing in the Orchidaceae (Smithson & Gigord, 2001;Johnson et al, 2004), lack of nectar may be an inefficient evolutionary route for reduction in geitonogamy. The efficacy by which purging can remove deleterious mutations from an inbred population is expected to depend on these alleles being recessive, independent and of major effect (Lande & Schemske, 1985;Charlesworth & Charlesworth, 1987;Ballou, 1997;Byers & Waller, 1999;Crnokrak & Barrett, 2002).…”

“…There is good experimental evidence, including studies on B. robertiana and A. morio, that pollinators visit far fewer flowers on inflorescences without nectar ( Johnson & Nilsson, 1999;Smithson & Gigord, 2001;Smithson, 2002;Johnson et al, 2004), so that this hypothesis is unlikely. The evidence that this pollinator behaviour causes differences in geitonogamy rates is mixed, with some studies supporting (Johnson & Nilsson, 1999;Johnson et al, 2004) and some disputing (Smithson & Gigord, 2001;Smithson, 2002) this hypothesis. Since alternative mechanisms, such as slow post-removal pollinarium bending, can partially or completely prevent geitonogamous selfing in the Orchidaceae (Smithson & Gigord, 2001;Johnson et al, 2004), lack of nectar may be an inefficient evolutionary route for reduction in geitonogamy.…”

“…Barlia robertiana is locally frequent on sandy soils in southern Europe, bumblebee-pollinated (Smithson & Gigord, 2001), and early flowering (DecemberApril). A. morio is locally abundant in European meadows, bumblebee-pollinated ( Johnson & Nilsson, 1999;Smithson, 2002) and flowers April-May.…”

“…Thus, nectarless plants could accrue an overall fitness advantage if the fitness benefits of outcrossing exceed losses through lowered per flower visitation. There is experimental evidence that pollinators visit fewer flowers per inflorescence on nectarless plants, although the evidence that this causes reduced geitonogamy is contradictory ( Johnson & Nilsson, 1999;Smithson & Gigord, 2001;Smithson, 2002;Johnson et al ., 2004). For reduced selfing to be important in the evolution of lack of nectar, significant genetic load through inbreeding depression is expected.…”

How plant?animal interactions signal new insights in communication

“…The second strategy benefits from a behaviour called 'colour generalization', in which pollinators prefer novel colours that are most similar to those that they have learned to associate with rewards [11]. The evolutionary advantages of this strategy are lower production costs and a higher probability of outcrossing, because pollinators as less likely to visit several unrewarding flowers from the same plant [41,44]. Comparing the phylogenies of rewardless flowers across different taxa will help us to understand the occurrence of floral mimicry and the evolution of mimicry systems in general.…”