Reward regulation in plant–frugivore networks requires only weak cues

Abstract

Theory assumes that fair trade among mutualists requires highly reliable communication. In plant–animal mutualisms the reliability of cues that indicate reward quality is often low. Therefore, it is controversial whether communication allows animal mutualists to regulate their reward intake. Here we show that even loose relationships between fruit brightness and nutritional rewards (r2 = 0.11–0.35) allow birds to regulate their nutrient intake across distinct European plant–frugivore networks. Resident, over-wintering generalist frugivores that interact with diverse plant species select bright, lipid-rich fruits, whereas migratory birds select dark, sugar- and antioxidant-rich fruits. Both nutritional strategies are consistent with previous physiological experiments suggesting that over-wintering generalists aim to maximize their energy intake, whereas migrants aim to enhance the build-up of body fat, their immune response and oxidative status during migration. Our results suggest that animal mutualists require only weak cues to regulate their reward intake according to specific nutritional strategies.

A physiological perspective on the ecology and evolution of partial migration

“…The intake of certain fruit components such as anthocyanins, in particular, likely reduces oxidative stress and additionally stimulates immune responses (Catoni et al 2008;Cooper-Mullin and McWilliams 2016). When resident and migratory species were compared, migratory species indeed selected sugar-and antioxidant-rich fruits (Albrecht et al 2018), which enhance the build-up of body fat as fuel for migration and are beneficial for oxidative status and immune function (Catoni et al 2008;Cooper-Mullin and McWilliams 2016). In contrast, generalist frugivorous residents favoured lipid-rich fruits, which helped to maximize their energy intake (Albrecht et al 2018).…”

“…When resident and migratory species were compared, migratory species indeed selected sugar-and antioxidant-rich fruits (Albrecht et al 2018), which enhance the build-up of body fat as fuel for migration and are beneficial for oxidative status and immune function (Catoni et al 2008;Cooper-Mullin and McWilliams 2016). In contrast, generalist frugivorous residents favoured lipid-rich fruits, which helped to maximize their energy intake (Albrecht et al 2018). Hence, in a partially migratory population, one might expect migratory individuals to eat more sugar-and antioxidant-rich fruits just before migration starts than their resident conspecifics.…”

Signal and reward in wild fleshy fruits: Does fruit scent predict nutrient content?

“…Whether visual and olfactory signals go beyond the signaling ripeness/presence and provide information on nutrient content is still debated (Albrecht, Hagge, Schabo, Schaefer, & Farwig, ). Studies of fruit color have predominated research on this debate.…”

“…In Mediterranean habitats, fruit color correlates with lipid content (Schaefer et al, ), and in northern Europe, fruit brightness predicts lipid, sugar, and anthocyanin content (Albrecht et al, ). Interestingly, the relationship between lipid content and brightness is inverted in the latter two studies (Albrecht et al, ; Schaefer et al, ), suggesting that color signals may be location dependent and do not reflect an inherent biochemical connection between signal and reward. The absence of biochemical associations between signal and reward renders the evolution of honest signals less likely and would require either repeated interactions that allow frugivores to punish dishonest mutualists or a costliness of signals (Schaefer & Ruxton, ).…”

“…Chromatic and achromatic (brightness) properties of fruits are also sometimes correlated with nutritional content (Cazetta, Galetti, Rezende, & Schaefer, 2012;Valido, Schaefer, & Jordano, 2011). In Mediterranean habitats, fruit color correlates with lipid content (Schaefer et al, 2014), and in northern Europe, fruit brightness predicts lipid, sugar, and anthocyanin content (Albrecht et al, 2018). Interestingly, the relationship between lipid content and brightness is inverted in the latter two studies (Albrecht et al, 2018;Schaefer et al, 2014), suggesting that color signals may be location dependent and do not reflect an inherent biochemical connection between signal and reward.…”