The Size of it: Scant Evidence That Flower Size Variation Affects Deception in Intersexual Floral Mimicry

Avery L Russell,Stephanie R Sanders,Liam A Wilson,Daniel R Papaj

doi:10.3389/fevo.2021.724712

Avery L Russell, Stephanie R Sanders + Show 2 more

Open Access

https://doi.org/10.3389/fevo.2021.724712

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Abstract

Mutualisms involve cooperation, but also frequently involve conflict. Plant-pollinator mutualisms are no exception. To facilitate animal pollination, flowering plants often offer pollen (their male gametes) as a food reward. Since plants benefit by maximizing pollen export to conspecific flowers, we might expect plants to cheat on pollen rewards. In intersexual floral mimicry, rewarding pollen-bearing male flowers (models) are mimicked by rewardless female flowers (mimics) on the same plant. Pollinators should therefore learn to avoid the unrewarding mimics. Plants might impede such learning by producing phenotypically variable flowers that cause bees to generalize among models and mimics during learning. In this laboratory study, we used partially artificial flowers (artificial petals, live reproductive parts) modeled after Begonia odorata to test whether variation in the size of rewarding male flowers (models) and unrewarding female flowers (mimics) affected how quickly bees learned both to recognize models and to reject mimics. Live unrewarding female flowers have 33% longer petals and have 31% greater surface area than live rewarding male flowers, which bees should easily discriminate. Yet while bees rapidly learned to reduce foraging effort on mimics, learning was not significantly affected by the degree to which flower size varied. Additionally, we found scant evidence that this was a result of bees altering response speed to maintain decision accuracy. Our study failed to provide evidence that flower size variation in intersexual floral mimicry systems exploits pollinator cognition, though we cannot rule out that other floral traits that are variable may be important. Furthermore, we propose that contrary to expectation, phenotypic variability in a Batesian mimicry system may not necessarily have significant effects on whether receivers effectively learn to discriminate models and mimics.

Highlights

Conflicts of interest are common in plant-pollinator mutualisms (Bronstein, 2001; Thompson et al, 2013; van der Kooi et al, 2021)
Flower-naïve bees strongly and significantly preferred mimics over models, with 70.3% of first landings being on mimics
Initially flower-naïve bees rapidly learned to discriminate between mimic and model flowers (Figure 5). Bees in both the control and corolla variation treatment that reached the learning criterion made proportionally more correct decisions across consecutive visits (Figure 5A; GLMM: χ21 = 12.71, P < 0.0004). These bees did not show any differences in learning between control and corolla variation treatments (Figure 5A; GLMM: treatment effect: χ21 = 1.47, P = 0.226; treatment × experience effect: χ21 = 0.43, P = 0.512) and both sets of bees required a similar number of flower visits to reach the learning criterion (t-test: t19.94 = 0.942, P = 0.357: mean no. visits ± SE: variation: 25 ± 3.4; control: 21 ± 2.3; N = 26 bees)

Summary

Introduction

Conflicts of interest are common in plant-pollinator mutualisms (Bronstein, 2001; Thompson et al, 2013; van der Kooi et al, 2021). The pollinator might reduce time spent foraging by bypassing the floral sex organs to extract floral rewards (“robbing”) (Maloof and Inouye, 2000; Barker et al, 2018). Such reciprocal exploitation between plant and pollinator is common and frequently involves plants deceiving pollinators into pollinating flowers that lack rewards. How constraints on pollinator learning are exploited in Batesian floral mimicry systems is still poorly understood (Dukas, 1987; Gigord et al, 2001; Schiestl and Johnson, 2013; Johnson and Schiestl, 2016; Goodrich and Jurgens, 2017; but see Kunze and Gumbert, 2000; de Jager and Ellis, 2014; Russell et al, 2020)

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