Horizontal orientation facilitates pollen transfer and rain damage avoidance in actinomorphic flowers of Platycodon grandiflorus

Abstract

In zoophilous plants, floral orientation evolved under both biotic and abiotic pressure to enhance pollination success. However, the adaptive significance of horizontal orientation in radially symmetrical (actinomorphic) flowers remains largely unknown, although that of bilaterally symmetrical flowers has been well studied.• We experimentally altered floral angle in a population of insect-pollinated Platycodon grandiflorus flowers to examine the effects of floral orientation on pollinator behaviour, pollination success and pollen rain damage avoidance. To further investigate the potential pollen damage by rain, we obtained past precipitation records for the study area during the flowering season, and experimentally tested P. grandiflorus pollen damage by water.• Horizontally oriented flowers received more pollinator visits and had pollen grains on the stigma in male and/or female phases than downward-and/or upward-oriented flowers and avoided pollen damage by rainfall better than upward-oriented flowers. A pollen germination experiment showed that approximately 30% of pollen grains burst in distilled water, indicating that pollen damage by rainfall may be significant in P. grandiflorus.• Our field experiments revealed that upward-oriented flowers cannot avoid pollen damage by rainfall during the flowering period, and that both upward-and downward-oriented flowers experience pollinator limitation in female success. Therefore, horizontal flower orientation appears to be adaptive in this insect-pollinated actinomorphic species that blooms during the rainy season.

Floral orientation affects outcross‐pollen deposition in buzz‐pollinated flowers with bilateral symmetry

“…Nevertheless, orientation may still be important in other radially symmetric flowers or for reasons unrelated to pollinator visitation. For example, in nectar‐producing Platycodon grandiflorus (Campanulaceae), experimentally switching floral orientation from horizontal to upward increases rain damage to anthers, and switching to downward orientation reduces pollen receipt compared to the natural, mostly horizontal orientation in this species (Nakata et al, 2022 ).…”

“…Floral orientation, the position of the corolla's main axis relative to the horizontal, plays an important role in plant reproductive success and in mediating plant–pollinator interactions (Stebbins, 1974 ; Fenster et al, 2009 ; Armbruster and Muchhala, 2020 ). A pendant orientation might protect pollen grains and nectar from rainfall (Huang et al, 2002 ; Aizen, 2003 ; Wang et al, 2010 ; Lin and Forrest, 2017 ; Nakata et al, 2022 ), heat (Haverkamp et al, 2019 ), or favor certain types of floral visitors (Ushimaru et al, 2009 ; Makino and Thomson, 2012 ; Campbell et al, 2016 ; Haverkamp et al, 2019 ). Meanwhile, a horizontal or vertical orientation might make flowers more attractive to pollinators or easier to access (Haverkamp et al, 2019 ; Nakata et al, 2022 ).…”

“…A pendant orientation might protect pollen grains and nectar from rainfall (Huang et al, 2002 ; Aizen, 2003 ; Wang et al, 2010 ; Lin and Forrest, 2017 ; Nakata et al, 2022 ), heat (Haverkamp et al, 2019 ), or favor certain types of floral visitors (Ushimaru et al, 2009 ; Makino and Thomson, 2012 ; Campbell et al, 2016 ; Haverkamp et al, 2019 ). Meanwhile, a horizontal or vertical orientation might make flowers more attractive to pollinators or easier to access (Haverkamp et al, 2019 ; Nakata et al, 2022 ). Crucially, a horizontal orientation in bilaterally symmetrical flowers is understood to promote precise pollinator positioning and improve pollen transfer, relative to pendant flowers (Giurfa et al, 1999 ; Fenster et al, 2009 ; Armbruster and Muchhala, 2020 ; Stewart et al, 2022 ).…”

“…In radially symmetrical flowers, pollen placement is thought to be less precise, pollinator positioning less crucial, and floral orientation under fewer selective constraints (Naghiloo et al, 2020 ; Stewart et al, 2022 ). In some taxa, radial symmetry is associated with a vertical orientation (Stewart et al, 2022 ), but they can also benefit from the increased attractiveness of a horizontal orientation (Nakata et al, 2022 ). In contrast, bilateral flowers are consistently associated with horizontal orientations across angiosperms (Giurfa et al, 1999 ; Ushimaru et al, 2009 ; Naghiloo et al, 2020 ; Stewart et al, 2022 ).…”

“…Although some bees (including bumblebees, Bombus spp.) tend to prefer vertical or horizontal to pendant flowers (Makino and Thomson, 2012 ; Nakata et al, 2022 ), even when flowers are naturally pendant (Prokop et al, 2020 ), bees will readily visit all orientations and can handle pendant flowers more effectively than other insects can (Wang et al, 2014 ; Haverkamp et al, 2019 ; Prokop et al, 2020 ). A pendant orientation in buzz‐pollinated flowers may therefore serve to exclude unwanted or illegitimate visitors, although this possibility has not been thoroughly investigated.…”