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Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: Absence of premating barriers?

The Royal Society
Proceedings of the Royal Society B
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Abstract

Pollinator specificity has traditionally been considered the main reproductive isolation mechanism in orchids. Among Mediterranean orchids, however, many species attract and deceive pollinators by mimicking nectar-rewarding plants. To test the extent to which deceptive orchid species share pollinators, we collected and identified hemipollinaria-carrying insects, and used ribosomal sequences to identify the orchid species from which hemipollinaria were removed. We found that social and solitary bees, and also flies, carried hemipollinaria belonging to nine orchid species with different degrees of specialization. In particular, Anacamptis morio, Dactylorhiza romana and Orchis mascula used a large set of pollinator species, whereas others such as Orchis quadripunctata seemed to be pollinated by one pollinator species only. Out of the insects with hemipollinaria, 19% were found to carry hemipollinaria from more than one orchid species, indicating that sympatric food-deceptive orchids can share pollinators. This sharing was apparent even among orchid sister-species, thus revealing an effective overlap in pollinator sets among closely related species. These results suggest varying degrees of pollinator specificity in these orchids, and indicate that pollinator specificity cannot always act as the main isolation mechanism in food-deceptive temperate orchids.
... A measure of the effectiveness of pollen transfer is pollination efficiency (PE) that is typically measured as the ratio of pollinated flowers on flowers with pollinia removed 30,31 . During transfer by pollinators, pollen losses in orchids are expected to be high when mediated by generalist pollinators and by a range of pollinator types 27,32 . For these reasons, pollinator efficiency in orchids might be hampered by exotic and generalist honeybees that manage to collect the pollinia but are not morphologically configurated to successfully deposit the pollinia and guarantee reproduction of the plant. ...
... An important caveat is that, thus far, we have only documented the impact of introduced honeybees on pollinia removal and deposition. However, the generalist foraging behaviour of Apis mellifera 15 may have further implications, including the breakdown of pre-pollination reproductive barriers among coexisting orchid species 15,32,91 . Such hybridization can have evolutionary biological implications for the plant life cycle, the persistence of future generations, diversification, and speciation in Orchidaceae. ...
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Biological invasions threaten global biodiversity, altering landscapes, ecosystems, and mutualistic relationships like pollination. Orchids are one of the most threatened plant families, yet the impact of invasive bees on their reproduction remains poorly understood. We conduct a global literature survey on the incidence of invasive honeybees (Apis mellifera) on orchid pollination, followed by a study case on Australian orchids. Our literature survey shows that Apis mellifera is the primary alien bee visiting orchids worldwide. However, in most cases, introduced honeybees do not deposit orchid pollen. We also test the extent to which introduced honeybees affect orchid pollination using Diuris brumalis and D. magnifica. Diuris brumalis shows higher fruit set and pollination in habitats with both native and invasive bees compared to habitats with only introduced bees. Male and female reproductive success in D. magnifica increases with native bee abundance, while conversely pollinator efficiency decreases with honeybee abundance and rises with habitat size. Our results suggest that introduced honeybees are likely involved in pollen removal but do not effectively deposit orchid pollen, acting as pollen wasters. However, Apis mellifera may still contribute to pollination of Diuris where native bees no longer exist. Given the global occurrence of introduced honeybees, we warn that certain orchids may suffer from pollen depletion by these invaders, especially in altered habitats with compromised pollination communities.
... The mating system and gene flow within and among populations in Orchidaceae can generate common genetic diversity patterns and FSGSs [12]. Pollinator-mediated gene flow among populations, e.g., was higher in deceptive than in rewarding orchids [12,13]. The deceived pollinators generally visit only a limited number of flowers among plants within populations, facilitating cross-pollination and decreasing the chances of inbreeding [14][15][16][17][18][19]. ...
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Background: The patterns of inbreeding coefficients (FIS) and fine spatial genetic structure (FSGS) were evaluated regarding the mating system and inbreeding depression of food-deceptive orchids, Dactylorhiza majalis, Dactylorhiza incarnata var. incarnata, and Dactylorhiza fuchsii, from NE Poland. Methods: We used 455 individuals, representing nine populations of three taxa and AFLPs, to estimate percent polymorphic loci and Nei’s gene diversity, which are calculated using the Bayesian method; FIS; FST; FSGS with the pairwise kinship coefficient (Fij); and AMOVA in populations. Results: We detected a relatively high proportion of polymorphic fragments (40.4–68.4%) and Nei’s gene diversity indices (0.140–0.234). The overall FIS was relatively low to moderate (0.071–0.312). The average Fij for the populations of three Dactylorhiza showed significantly positive values, which were observed between plants at distances of 1–10 m (20 m). FST was significant in each Dactylorhiza taxon, ranging from the lowest values in D. fuchsii and D. majalis (0.080–0.086, p < 0.05) to a higher value (0.163, p < 0.05) in D. incarnata var. incarnata. Molecular variance was the highest within populations (76.5–86.6%; p < 0.001). Conclusions: We observed concordant genetic diversity patterns in three food-deceptive, allogamous, pollinator-dependent, and self-compatible Dactylorhiza. FIS is often substantially higher than Fij with respect to the first class of FSGSs, suggesting that selfing (meaning of geitonogamy) is at least responsible for homozygosity. A strong FSGS may have evolutionary consequences in Dactylorhiza, and combined with low inbreeding depression, it may impact the establishment of inbred lines of D. majalis and D. incarnata var. incarnata.
... A measure of the effectiveness of pollen transfer is pollination e ciency (PE) that is typically measured as the ratio of pollinated owers on owers with pollinia removed (Johnson et al. 2004;Tremblay et al. 2005). During transfer by pollinators, pollen losses in orchids are expected to be high when mediated by generalist pollinators and pollinator types overlap (Cozzolino et al. 2005;Scopece et al. 2010). For these reasons, pollinator e ciency in orchids might be hampered by exotic and generalist honeybees that manage to collect the pollinia but are not morphologically con gurated to successfully deposit the pollinia and guarantee reproduction of the plant. ...
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Biological invasion is one of the leading threats to global biodiversity. Invasive species can change the structure and dynamics of landscapes, communities, and ecosystems, and even alter mutualistic relationships across species such as pollination. Orchids are one of the most threatened plant families globally and known to have established specialised pollination mechanism to reproduce, yet the impact of invasive bees on orchid reproduction has not been comprehensively assessed. We conduct a literature survey to document global patterns of the impact of invasive honeybees on orchids’ pollination. We then present a study case from Australian orchids, testing the extent to which introduced honeybees can successfully pollinate orchids across different degrees of habitat alteration, using Diuris brumalis and D. magnifica (Orchidaceae). Globally, Apis mellifera is the principal alien bee potentially involved in orchid pollination. We show that pollinator efficiency and fruit set in D. brumalis is higher in wild habitats in which both native bees and invasive honeybees are present, relative to altered habitat with introduced honeybees only. Pollen removal and fruit set of D. magnifica rise with native bees’ abundance whilst pollinator efficiency decreases with honeybee abundance and increases with habitat size. Complementarily to our findings, our literature survey suggests that the presence of introduced honeybees adversely impacts orchid pollination, likely via inefficient pollen transfer. Given the worldwide occurrence of introduced honeybees, we warn that some orchids may be negatively impacted by these alien pollinators, especially in altered and highly fragmented habitats where natural pollination networks are compromised.
... Intense fires, floods, or severe environmental fluctuations are among the natural catastrophes threatening rare orchid species (Wraith et al. 2020;Phillips et al. 2020). Small and spatially isolated fragments of natural habitat destabilize populations and impede pollen and seed exchange (Kropf and Renner 2008;Cozzolino et al. 2005). Genetic diversity can be lost in fragmented populations, leading to decreasing the attraction of a diverse range of pollinators. ...
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Orchids are valuable plants in the global floricultural market due to their unique flower structure, attractive flower colors, and long flower life. The most critical technique for obtaining ornamental cultivars of orchids is hybrid breeding. This technique is routine work but usually laborious and time consuming mainly due to the long generation time of orchids. The increasing demand for orchids in the floricultural trade might push breeders to produce more varieties with novel characteristics to ensure their competitiveness. Theoretically, the target traits could be focused on flower characteristics including their colors and morphology, and the ability of disease resistance to viruses or other pathogens. In orchid production, numerous intraspecific, intragenic, and intergenic hybrids have been produced and applied through the most commonly used traditional breeding. Using a range of advanced approaches, such as genetic engineering with the aid of multi-omics technologies and genome editing, orchid breeders might have more opportunities and higher efficiency to achieve their breeding goals in the future. This chapter summarized the past and current approaches and their findings in the field of orchid breeding and discussed their possible applications in the horticultural industry.
... Intense fires, floods, or severe environmental fluctuations are among the natural catastrophes threatening rare orchid species (Wraith et al. 2020;Phillips et al. 2020). Small and spatially isolated fragments of natural habitat destabilize populations and impede pollen and seed exchange (Kropf and Renner 2008;Cozzolino et al. 2005). Genetic diversity can be lost in fragmented populations, leading to decreasing the attraction of a diverse range of pollinators. ...
Chapter
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