Bumble-bee learning selects for both early and long flowering in food-deceptive plants

Internicola, Antonina I.; Harder, Lawrence D.

doi:10.1098/rspb.2011.1849

Cited by 34 publications

(33 citation statements)

References 33 publications

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“…Although some deceptive orchids mimic female insects or rewarding plant species, the majority are categorized as generalized food-deceptive species, and their deception relies on the innate preference of insects for flower-like objects (reviewed by Renner 2006). However, food deceptive species are often strongly pollinator limited (Neiland and Wilcock 1998;Tremblay et al 2005), as their pollinators often have a strong capacity for associative learning that allows them to avoid repeated visits to non-rewarding flowers (Biernaskie et al 2009), and it is therefore thought that pollinator limitation can promote the selection of floral traits that enhance pollinator attraction and pollination efficiency (Ashman et al 2004;Internicola and Harder 2012;Sletvold and Ågren 2011;.…”

Section: Introductionmentioning

confidence: 99%

Pollination system and the effect of inflorescence size on fruit set in the deceptive orchid Cephalanthera falcata

et al. 2015

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Larger inflorescences in reward-producing plants can benefit plants by increasing both pollinator attraction and the duration of visits by individual pollinators. However, ultimately, inflorescence size is determined by the balance between the benefits of large inflorescences and the increased cost of geitonogamy. At present, little is known about the relationship between inflorescence size and fecundity in deceptive plants. Given that pollinators are likely to leave inflorescences lacking rewards quickly, it seems unlikely that longer pollinator visits and the risk of geitonogamy would be strong selective pressures in these species, which indicates that pollinator attraction might be the most important factor influencing their inflorescence size. Here we examined the pollination ecology of the deceptive orchid Cephalanthera falcata in order to clarify the effects of inflorescence size on the fruit set of this non-rewarding species. Field observations of the floral visitors showed that C. falcata is pollinated by the andrenid bee Andrena aburana, whilst pollination experiments demonstrated that this orchid species is neither autogamous nor apogamous, but is strongly pollinator dependent. Three consecutive years of field observations revealed that fruit set was positively correlated with the number of flowers per inflorescence. These results provide strong evidence that the nectarless orchid C. falcata benefits from producing larger inflorescences that attract a greater number of innate pollinators. Large inflorescences may have a greater positive effect on fruit set in deceptive plants because a growing number of studies suggest that fruit set in reward-producing plants is usually unaffected by display size.

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Section: Introductionmentioning

confidence: 99%

Pollination system and the effect of inflorescence size on fruit set in the deceptive orchid Cephalanthera falcata

et al. 2015

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“…In addition, pollinators that approached N− plants were much less likely to probe flowers compared to N+ plants, and they visited fewer flowers per plant. The first response suggests avoidance learning (Jersáková and Kindlmann , Internicola and Harder ), whereas the second likely reflects reaction to poor foraging returns and the absence of reinforcement (Internicola et al. , , Internicola and Harder ).…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, deceitful plants signal, but do not reward, thereby exploiting pollinators’ innate or learned associations. Because deceitful species do not reinforce learned associations, they provoke avoidance learning (Internicola and Harder ), at least in the short term, and so are susceptible to reduced pollination success (Johnson and Bond , Harder ). Nevertheless, one‐third of orchid species provide no reward to pollinators (Dressler ), suggesting that the benefits of increased attractiveness must be outweighed by other advantages of rewardlessness under some circumstances.…”

Section: Introductionmentioning

confidence: 99%

The mating consequences of rewarding vs. deceptive pollination systems: Is there a quantity–quality trade‐off?

Hobbhahn

Johnson

Harder

2016

Ecological Monographs

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Plant mating commonly involves quality–quantity trade‐offs. Such a trade‐off features explicitly in the cross‐promotion hypothesis for the evolution of pollination by deceit. According to this hypothesis, rewardlessness enhances mating quality by altering pollinator behavior in ways that reduce self‐pollination and increase outcrossing, thus compensating for the reduced pollen dispersal and seed production resulting from lack of reinforcement of pollinator visitation behavior. The high prevalence of rewardlessness in orchids suggests that deceit pollination conveys benefits that outweigh the fecundity advantages of reward production. We test the cross‐promotion hypothesis in Disa, an African orchid genus in which nectar rewards have evolved repeatedly from rewardless ancestors. To address this hypothesis directly, we quantified pollinator behavior and the associated dispersal of stained pollen for four nectar‐producing (N+) and 10 nectarless (N−) species. We also assessed more extensive, if less direct, evidence from a survey of lifetime pollination outcomes for 15 N+ and 32 N− species. Pollinators visited N+ species more frequently and visited 1.5 times more flowers per inflorescence than in N− species. In contrast, pollinators skipped more conspecific plants between visits to donor and recipient plants when visiting N− species than when visiting N+ species. Over floral lifetimes, both N− and N+ species exhibited similar overall pollen‐transfer efficiency (8.2%) and did not differ in the overall fractions of pollen involved in self‐pollination (26% of all pollen deposited), geitonogamy (82% of all self‐pollination), or export to other conspecific plants (74%). N+ species set more fruit per flower (68.8% vs. 48.8%), but equivalent fractions of ovules per fruit were fertilized and subsequently developed into seeds in N− and N+ species. These findings provide only limited evidence that deceit pollination enhances mating quality (nectar production causes more local mating in N+ species than in N− species). Contrary to the hypothesis, deceit does not generally affect pollinator‐mediated self‐pollination. The repeated evolution of nectar production from rewardless ancestors in Disa likely occurred under severe visit limitation, favoring nectar‐producing mutants with higher reproductive output. Given that we did not find any mating quality advantage for rewardlessness in Disa, its persistence in some lineages remains an evolutionary enigma.

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“…It is generally known that the natural fruit set of plants is often limited by pollen, especially in deceptive plants (Tremblay et al ., ; Aizen & Harder, ; Wagenius & Lyon, ). This can be caused by the lack of reward, which discourages pollinators from visiting flowers (Ferdy et al ., ; Sun, Alexandersson & Ge, ; Internicola & Harder, ). In addition to the effect of pollen limitation (PL), fruiting failure (FF) may be a result of other causes, such as limited resources (Mattila & Kuitunen, ), habitat characteristics (Johnson & Bond, ; Nishikawa, ) and stochastic events (Dirzo & Domínguez, ) that limit natural fruit set (Ackerman & Montalvo, ).…”

Section: Introductionmentioning

confidence: 99%

Pollen limitation and fruiting failure related to canopy closure inCalypso bulbosa(Orchidaceae), a northern food-deceptive orchid with a single flower

et al. 2013

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Natural fruit set is constrained by pollen limitation and fruiting failure, and pollen limitation is expected to be especially severe in deceptive orchids. We performed hand cross‐pollinations in ten populations of a food‐deceptive orchid, Calypso bulbosa, under sparse and dense canopies in three non‐consecutive years. We explored the relationships between natural fruit set, pollen limitation and fruiting failure. Mean natural fruit set over the years was 60%, which is exceptionally high for a deceptive orchid. On average, hand cross‐pollination increased fruit set by 23%. Among open‐pollinated plants that did not set a fruit, 55.5% were estimated to be pollen limited and 44.5% to be limited by fruiting failure, i.e. inability to set a fruit after pollination. In species with high natural fruit set, hand cross‐pollination experiments may not always detect statistically significant pollen limitation. In our case, pollen limitation tended to become significant when the natural fruit set dropped below 60%. Canopy cover had a significant effect on fruiting failure, which was more severe under a dense canopy. Although our results demonstrate pollen limitation in many cases, they also highlight the fact that food deception can be a very effective pollination strategy. © 2013 The Linnean Society of London,

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Bumble-bee learning selects for both early and long flowering in food-deceptive plants

Cited by 34 publications

References 33 publications

Pollination system and the effect of inflorescence size on fruit set in the deceptive orchid Cephalanthera falcata

Pollination system and the effect of inflorescence size on fruit set in the deceptive orchid Cephalanthera falcata

The mating consequences of rewarding vs. deceptive pollination systems: Is there a quantity–quality trade‐off?

Pollen limitation and fruiting failure related to canopy closure inCalypso bulbosa(Orchidaceae), a northern food-deceptive orchid with a single flower

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