Cryptic petal coloration decreases floral apparency and herbivory in nocturnally closing daisies

Abstract

Floral apparency is shaped by both mutualistic and antagonistic interactions that can act in opposing ways. Pollinators are expected to select for more visually apparent flowers, but this likely trades off against the potentially severe fitness costs of damage to apparent flowers by floral herbivores. One way in which flowers that close during parts of the day might circumvent this trade‐off is by evolving less visible lower petal surfaces that are inconspicuous to herbivores when flowers are closed. Here, we used visual system modelling and herbivory experiments to test whether petal surfaces that are exposed when flowers are closed are cryptically coloured. We collected lower and upper petal surface spectra for 77 Asteraceae species from Namaqualand, South Africa. This included closing species that expose their lower petal surfaces for 5–6 daylight hours and non‐closing species that do not expose their lower surfaces. We used these contrasting groups to test the expectation of reduced conspicuousness of lower petal surfaces in closing, but not non‐closing species. By modelling reflectance spectra of petal surfaces against a green leaf background in various visual systems, we showed (a) that conspicuousness of upper petal surfaces to pollinators and various herbivores was strongly correlated, suggesting the potential for fitness trade‐offs between attracting mutualists and antagonists to open flowers, (b) that closing species' lower petal surfaces were less visible to herbivores against a leaf background than those of non‐closing species and (c) that closing species had larger differences between upper and lower petal surface coloration than non‐closing species. Behavioural experiments with tortoise herbivores demonstrated that flowers are easily detected when upper surfaces are exposed, but that tortoises were unable to distinguish lower petal surfaces against a leaf background, resulting in reduced flower herbivory. These results are consistent with selection by herbivores for cryptic coloration of lower petal surfaces, and divergence of coloration between lower and upper petal surfaces in species with closing flowers. Visual crypsis of flowers may be an effective anti‐herbivory strategy during times when pollinators are inactive, and provides an alternative to chemical defence, which often involves costs to pollination. A free Plain Language Summary can be found within the Supporting Information of this article.

Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions

“…For example, South African daisies reduce florivory by closing flowers and exposing the cryptic‐coloured undersides of petals when pollinators are inactive at low temperatures. In accordance with this relaxation of phenotypic trade‐offs , the upper surface of petals in flower‐closing species exhibits more conspicuous colour than in non‐closing ones (Kemp & Ellis, 2019 ). Temporal switches may also occur in morphological traits.…”

Mutualisms and (A)symmetry in Plant–Pollinator Interactions

“…Flowers that lose colour are less attractive to Review pollinators, but still enhance long-distance attraction of the inflorescence as a whole 66 , because the unpigmented, pale flowers generate a bright signal that will be visible from long distances 58 . Flower visibility can also be reduced temporarily by closing inflorescences after pollination, which reduces conspicuousness to antagonists 67 , due to changes in inflorescence display size/ shape and a less colourful lower side of the florets 68,69 . Scent emission is more plastic than colour, and diel patterns in scent emission frequently match anthesis and nectar availability, particularly for nocturnal pollinated flowers 70,71 .…”

Floral reorientation: the restoration of pollination accuracy after accidents

“…Flower and flowering‐shoot reorientation ought to represent natural extensions of such movement capabilities, yet this phenomenon has been remarkably little‐studied. There has been some work on the movement of individual floral parts, such as petal closure in response to cold or nightfall (Darwin, 1862, 1880; Bynum & Smith, 2001; Armbruster et al , 2006; Prokop & Fedor, 2016; Kemp & Ellis, 2019) or the movement of stamens to reduce intersexual interference (Sprengel, 1793; Martens, 1936; Ren, 2010; Ren & Tang, 2012; Armbruster et al , 2014a). However, the only studies on whole‐flower reorientation of which we are aware are descriptions of floral heliotropism in response to the sun's position (see review in van der Kooi et al , 2019) and recent work by Yon et al .…”