Evidence for Batesian mimicry in a butterfly-pollinated orchid

doi:10.1006/bijl.1994.1062

Biological Journal of the Linnean Society

Volume 53, Issue 1, September 1994, Pages 91-104

https://doi.org/10.1006/bijl.1994.1062 Get rights and content

Abstract

Observations in the Cape Province, South Africa, showed that Disa ferruginea (Orchidaceae) is dependent on a single butterfly species—Meneris tulbaghia (Nymphalidae: Satyrinae)—for pollination. The flowers of D. ferruginea contain no food reward and, instead, appear to secure pollinator visits by imitating flowers which are nectar sources for the butterfly. A red-flowered form of D. ferruginea appears to mimic the red nectar-producing flowers of Tritoniopsis triticea (Iridaceae) in the south-western Cape, while an orange-flowered form of D. ferruginea appears to mimic the orange nectar-producing flowers of Kniphofia uvaria (Asphodelaceae) in the Langeberg Mountains. Reflectance spectra of the orchid's flowers closely match those of its putative models. Analysis of foraging movements of the butterfly in a mixed stand of D. ferruginea and T. triticea indicated that it does not discriminate between the nectarless orchid and the nectar-producing model. Populations of D. ferruginea which are sympatric with T. triticea have relatively high levels of pollination and fruit production, compared with populations where the orchid grows alone. Although other studies have reported relatively low fecundity in deceptive orchids, pollination and fruiting success in D. ferruginea compares favourably with a nectar-producing congener, Disa uniflora, which is also pollinated solely by M. tulbaghia.

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Cited by (108)

Colour similarity to flowering neighbours promotes pollinator visits, pollen receipt and maternal fitness
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Citation Excerpt :
Fitness increases may be driven by greater pollinator visitation and seed set when similar neighbours help attract or maintain local pollinators (Moeller, 2004; Coetzee et al., 2021). Overlap in floral colour strongly impacts pollinator foraging when visitors are colour constant (Hill et al., 1997; Jones and Reithel, 2001), which increases pollinator movements between similar co-flowering species (Chittka et al., 1997; de Jager et al., 2016; de Jager et al., 2011; Johnson, 1994; Johnson et al., 2003). Consequently, flower colour similarity may result in pollinators perceiving different species to be the same, as suggested by indiscriminate pollinator movement between plant species during foraging (Chittka et al., 1997; Schemske, 1981).
While co-flowering plants often compete for pollination through pollinator visits and pollen transfer, recent studies reveal potential for the facilitation of pollination. Pollination may be promoted when similarities in the floral traits of co-flowering species enhance pollinator visitation and seed set. Floral similarity, however, could also lead to heterospecific pollen transfer, creating a fitness trade-off that is seldom explored empirically.
Here we construct experimental communities of Oxalis to investigate the trade-off between enhanced visitation and heterospecific pollen receipt, which can impact seed set at varying relative plant abundance. Our experimental communities comprise O. purpurea that is matched or mismatched to congeners in flower colour at low and high relative plant abundance. We investigate the consequences of colour overlap for pollinator visitation and the receipt of conspecific, heterospecific, and mixed pollen loads, and assess seed set in natural plots.
Flower colour similarity increases visitation by shared pollinators at both low and high relative abundance when O. purpurea occurs in matched flower colour communities. The receipt of pollen analogues from conspecifics is also greater at both abundances when neighbours are matched in floral colour. Although conspecific pollen in matched communities is mostly delivered in mixed pollen loads, hand pollinations confirm the receipt of mixed pollen carries no fitness costs for seed production. Consequently, plants in natural populations plots of O. purpurea experiences increase maternal fitness when growing in matching flower colour communities.
We demonstrate a positive net effect of flower colour similarity, relative to flower colour dissimilarity, that can facilitate plant reproduction. Through field experiments we systematically test previously observed patterns of clustered flower colour assembly in Oxalis communities to provide a comprehensive assessment of facilitative co-flowering interactions.
Butterfly pollination of Bonatea cassidea (Orchidaceae): Solving a puzzle from the Darwin era
2019, South African Journal of Botany
Citation Excerpt :
Since Lepidoptera have most of their bodies covered with scales, only a few body parts are considered sufficiently suitable (i.e. smooth) to carry orchid pollinaria (Johnson and Edwards, 2000). Therefore, in butterfly-pollinated species, pollinaria are usually attached to areas free of scales, such as the legs (Ridley, 1896; Johnson and Bond, 1994; Zhang et al., 2010), eyes (Robertson and Wyatt, 1990; Pedron et al., 2012), and proboscis of the insect (Johnson, 1994; Pansarin and Amaral, 2008; Zhang et al., 2010; Aguiar et al., 2012). The terrestrial orchid genus Bonatea Willd. (
Although moths and butterflies are closely related, they tend to respond to different floral cues for foraging and thus select for different suites of floral traits. Shifts between moth and butterfly pollination in the same plant clade provide an opportunity to assess the traits that are required to impart a shift between these pollination systems. The orchid genus Bonatea consists mostly of night-scented moth-pollinated taxa, but here we document a butterfly pollination system in Bonatea cassidea, a century after Mansel Weale's initial observations of butterflies carrying pollinaria of this taxon in South Africa were communicated to the Linnean Society by Charles Darwin. We recorded visits by a number of species of butterflies from the family Hesperiidae and Pieridae, but contrary to Weale, we found that the majority of pollinaria were firmly affixed between the palpi and not on the sternum. Removal of pollinaria from flowers during the day, but not at night, suggested that moths do not contribute to pollination, despite the white flower colouration. Floral traits found in B. cassidea but not its moth-pollinated congeners include diurnal anthesis, scent emission which is weak in the day and virtually absent at night, and the production of small amounts of relatively dilute sucrose-rich nectar in short spurs. These features are consistent with those expected for butterfly-pollinated plants in general. This study represents the first detailed report of butterfly-pollination in Bonatea and one of very few cases of orchid pollination by pierid butterflies.
Mimicry and Deception in Pollination
2017, Advances in Botanical Research
Citation Excerpt :
This also holds for deceptive flowers displaying a complex colour pattern referring to multiple-model species (Ma et al., 2015). A particular aspect of flower mimicry is the frequency of model species in relation to the frequency of mimic species (Anderson & Johnson, 2006; Bierzychudek, 1981; Dafni & Ivri, 1981; Johnson, 1994, 2000). Many food-deceptive plants show discrete or continuous floral polymorphism within their populations.
Mimicry and deception in pollination represent extended plant–pollinator communication systems including two senders of mistakable signals. Flower mimicry is a highly diverse phenomenon including Batesian mimicry, in which a nonrewarding flower mimics a rewarding one, and signal standardization, also known as Mullerian mimicry, in which two unrelated rewarding flowers display similar signals. In these floral mimicry systems, even experienced flower visitors are deceived. Some flowering plants exploit the pollinators' innate preferences of finding rewarding flowers or floral rewards: In some cases the flowers fit the innate search image of flower visitors so close that no real model exists. In other cases, only the floral reward is mimicked. Particularly, pollen and stamen mimicry systems are very common, in which flowers mimic visual and tactile signals of pollen and stamens, and by means of this fake stamens and pollen deceive or misdirect pollen-eating and pollen-collecting flower visitors that innately respond to these signals. In another type of floral mimicry, animal-pollinated flowers attract flower visitors by mimicking features related to aspects other than flower visitation of their pollinators, e.g., sexually deceptive flowers deceiving mate-seeking male insects, and brood-substrate mimicking flowers deceiving females searching for egg-laying substrates. These deceptive flowers attract specific pollinators by means of sensory exploitation of a well-developed innate behavioural response for distinct volatiles and other cues that have evolved in the context of mating or egg-laying behaviour. Floral mimicry is always beneficial for the mimic, but may impose costs for the deceived pollinators. Then the deceived pollinators likely evolve mechanisms not being deceived and the flowering plants to continue deception, and deception becomes trickier over evolutionary times.
Mimicry in plants
2016, Current Biology
Floral features, pollination biology, and breeding system of Comparettia coccinea (Orchidaceae: Oncidiinae)
2015, Flora: Morphology, Distribution, Functional Ecology of Plants
Citation Excerpt :
Psychophilous orchids offer the butterflies either nectar or are pollinated by food deception (e.g., van der Pijl and Dodson, 1966; Pansarin and Amaral, 2008b; Fuhro et al., 2010; Pansarin and Ferreira, 2015). Butterfly pollination occurs in many unrelated genera within the huge subfamily Orchidoideae (van der Pijl and Dodson, 1966; Robertson and Wyatt, 1990; Johnson, 1994; van der Cingel, 1995; Pedron et al., 2012; Pansarin and Ferreira, 2015). In Epidendroideae, this pollination syndrome was also reported in several unrelated groups, such as Oeceoclades (Aguiar et al., 2012) and some sections of the speciose genus Epidendrum (e.g., Pansarin, 2003; Pansarin and Amaral, 2008b; Fuhro et al., 2010).
In Orchidaceae, nectar offering has been reported in many unrelated groups, including Oncidiinae. Among members of Oncidiinae, pollination by hummingbirds has been recorded for Comparettia in Central America, but nothing is known for the Brazilian species. The phenology, floral morpho-anatomy, production of floral rewards, pollinators, pollination mechanisms, and breeding system of Comparettia coccinea were investigated in a nature reserve in southeastern Brazil. The reddish flowers of C. coccinea produce nectar (volume 0.5–5 μL, sugar concentration 17–28%) by two cylindrical glands located at the end of the labellum horns that can be accessed via two nectary entrances. The studied species is exclusively visited and pollinated by Nymphalidae butterflies and flower features, such as color, symmetry and morphology, support the occurrence of psychophily in C. coccinea. Pollinaria are attached to the butterfly eyes during the collection of nectar from the spur. When a butterfly visits the right nectar entrance, pollinaria are deposited on its left eye and vice versa. The species is self-compatible and depends on a biotic pollen vector to set fruits. This is the first record of effective pollination by butterflies in Oncidiinae .
Conservation status and management insights from tracking a cryptic and Critically Endangered species of Orchidaceae
2017, ORYX

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Regular ArticleEvidence for Batesian mimicry in a butterfly-pollinated orchid

Abstract

Regular Article
Evidence for Batesian mimicry in a butterfly-pollinated orchid