Chemical signal is in the blend: bases of plant-pollinator encounter in a highly specialized interaction

Proffit, Magali; Lapeyre, Benoît; Buatois, Bruno; Deng, Xiaoxia; Arnal, Pierre; Gouzerh, Flora; Carrasco, Davíd; Hossaert‐McKey, Martine

doi:10.1038/s41598-020-66655-w

Cited by 50 publications

(60 citation statements)

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“…Blastophaga psenes is involved in a highly specific mutualism with the Mediterranean fig species Ficus carica (Moraceae), being intimately associated with this plant for its reproduction and being its exclusive pollinator. Ficus carica occurs naturally in the Mediterranean region and presents an unusual phenology with male trees flowering twice a year (i.e., in late April—early May and in late July), but female trees flowering only once a year (i.e., in early July) (see [ 46 , 52 ] for more details about the life cycle. Blastophaga psenes uses a blend of 4 VOCs [S-linalool, Z-linalool oxide (furanoid), E-linalool oxide (furanoid) and benzyl alcohol] in the proportion of 76.34%, 0.38%, 0.38%, and 22.90%, respectively, to locate receptive figs of its host and any small change in this blend proportion alters pollinator attraction [ 46 ].…”

Section: Methodsmentioning

confidence: 99%

“…Ficus carica occurs naturally in the Mediterranean region and presents an unusual phenology with male trees flowering twice a year (i.e., in late April—early May and in late July), but female trees flowering only once a year (i.e., in early July) (see [ 46 , 52 ] for more details about the life cycle. Blastophaga psenes uses a blend of 4 VOCs [S-linalool, Z-linalool oxide (furanoid), E-linalool oxide (furanoid) and benzyl alcohol] in the proportion of 76.34%, 0.38%, 0.38%, and 22.90%, respectively, to locate receptive figs of its host and any small change in this blend proportion alters pollinator attraction [ 46 ]. All these biological properties of this fig-fig wasp association make it particularly well suited for understanding how specific plant-insect communication may be affected by atmospheric pollution.…”

Section: Methodsmentioning

confidence: 99%

“…In order to evaluate if O 3 exposure could affect the sensitivity to a given VOC, EAGs were conducted with different doses of synthetic VOCs (1, 10, 100, and 1000 µg). Previous studies reported that the overall intensity of floral scent produced by one inflorescence (or flower) is approximately 0.1 µg.min −1 for F. carica [ 46 ]. Similar intensities to this measured for F. carica have been found in two plants species pollinated by B. terrestris [ 67 , 68 ].…”

Section: Methodsmentioning

confidence: 99%

“…Similar intensities to this measured for F. carica have been found in two plants species pollinated by B. terrestris [ 67 , 68 ]. Based on the results of previous studies, we selected synthetic versions of VOCs that are detected by the antenna of our insect species and mediate the attraction toward their host-plants: the monoterpenes linalool (in racemic mixture [S and R forms, 50:50]) and linalool oxides (Z and E forms furanoid, 50:50) and the benzenoid benzyl alcohol in the specialist fig wasp [ 46 ], and the monoterpene R-linalool, the benzenoid benzaldehyde, and the alkyl aldehyde nonanal in the generalist bumblebee [ 69 , 70 ] (see Table S2 for providers and purity of the different compounds). Linalool mixture was used in our study of fig wasps because S-linalool alone is not available commercially.…”

Section: Methodsmentioning

confidence: 99%

“…Within the complex mixtures of VOCs emitted by plants, insects only use some of them, in particular proportions, as a signal to find their resource [ 31 , 45 , 46 ]. Any change in the detection of the different VOCs in a floral scent by insects can lead to the breakdown of the host recognition process and may, thus, impede pollinator foraging.…”

Section: Introductionmentioning

confidence: 99%

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Ozone Pollution Alters Olfaction and Behavior of Pollinators

et al. 2021

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Concentration of air pollutants, particularly ozone (O3), has dramatically increased since pre-industrial times in the troposphere. Due to the strong oxidative potential of O3, negative effects on both emission and lifetime in the atmosphere of plant volatile organic compounds (VOCs) have already been highlighted. VOCs alteration by O3 may potentially affect the attraction of pollinators that rely on these chemical signals. Surprisingly, direct effects of O3 on the olfaction and the behavioral response of pollinators have not been investigated so far. We developed a comprehensive experiment under controlled conditions to assess O3 physiological and behavioral effects on two pollinator species, differing in their ecological traits. Using several realistic concentrations of O3 and various exposure times, we investigated the odor antennal detection and the attraction to VOCs present in the floral scents of their associated plants. Our results showed, in both species, a clear effect of exposure to high O3 concentrations on the ability to detect and react to the floral VOCs. These effects depend on the VOC tested and its concentration, and the O3 exposure (concentration and duration) on the pollinator species. Pollination systems may, therefore, be impaired in different ways by increased levels of O3, the effects of which will likely depend on whether the exposure is chronic or, as in this study, punctual, likely causing some pollination systems to be more vulnerable than others. While several studies have already shown the negative impact of O3 on VOCs emission and lifetime in the atmosphere, this study reveals, for the first time, that this impact alters the pollinator detection and behavior. These findings highlight the urgent need to consider air pollution when evaluating threats to pollinators.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ozone Pollution Alters Olfaction and Behavior of Pollinators

et al. 2021

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The genetic structuring in pollinating wasps of Ficus hispida in continental Asia

Deng,

Liao,

Wong

et al. 2023

Ecology and Evolution

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The interaction between figs and fig wasps provides a striking example of obligate brood site pollination mutualism. Monoecious figs, constituting independent radiations in each tropical biome, are present in significant proportions worldwide, but in continental Asia, dioecious figs have diverged into various niches, making the region's assemblage remarkably diverse. However, the reproductive success of figs and fig wasps largely depends on the fig wasp dispersal process. Monoecious fig pollinators in continental Asian tropical rain forests exhibit high gene flow of the plant, while many dioecious fig pollinators have a more restricted gene flow. However, there are limited studies on the genetic structure of dioecious Ficus pollinators that pollinate figs with intermediate gene flow. Here, we used molecular methods to investigate the genetic structure of pollinating wasps of the widely distributed dioecious Ficus hispida in China and Southeast Asia. Sequence data from two gene regions were used: the mitochondrial protein‐coding gene cytochrome c oxidase subunit I (COI) and the nuclear 28S genes. Both molecular and morphological results support two fig wasp species at our sampling sites. Our findings suggest that for widely sympatric Ficus species in continental Asia, monoecious figs presenting long gene glow have the fewest fig wasp species, followed by dioecious figs presenting intermediate gene flow, and dioecious figs presenting local gene flow have the most fig wasp species.

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