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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.

SUBMITTER: Albrecht J

PROVIDER: S-EPMC6240120 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Reward regulation in plant-frugivore networks requires only weak cues.

Albrecht Jörg J Hagge Jonas J Schabo Dana G DG Schaefer H Martin HM Farwig Nina N

Nature communications 20181116 1

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 (r<sup>2</sup> = 0.11-0.35) allow birds to regulate their nutrient intake across distinct European plant-frugivore ...[more]

PMID: 30446651

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Project description:There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.

Project description:The paraventricular nucleus of the thalamus (PVT) has been implicated in cue-induced motivated behaviors. Although reward-associated cues (conditioned stimuli, CSs) contain different types of information including predictive information of future reward delivery and incentive (motivational) value of the reward, it remains unknown whether PVT neurons represent predictive and incentive information of CSs. It is suggested that neural activity just after the onset of CSs (early activity) and that just before reward delivery (late activity) might more strongly represent predictive and incentive information, respectively. In this study, rats were trained to lick a tube, which was protruded close to their mouth just after a CS, to obtain a reward (sucrose or water) (cue-induced licking task). Auditory and visual CSs were used: each elemental cue (CS) predicted reward or non-reward outcome, while simultaneous presentation of the two elemental cues (configural cues) predicted the opposite reward outcome. We recorded PVT neurons in the cue-induced licking task, and report that half of the CS-responsive PVT neurons responded selectively to the CSs predicting reward outcome regardless of physical property of the cues (CS+-selective). In addition, the early activity of the CS+-selective neurons discriminated reward/non-reward association (predictive information) and was less sensitive to reward value and motivation reflected by lick latency (incentive information), while the late activity of the CS+-selective neurons was correlated with reward value and motivation rather than reward/non-reward association. Early and late population activity of the CS+-selective neurons also represented predictive and incentive information of the CSs, respectively. On the other hand, activity of more than half of the PVT neurons was correlated with individual licking during licking to acquire reward. Taken together, the results suggest that the PVT neurons engage in different neural processes involved in cue-induced motivated behaviors: CS encoding to determine reward availability and form motivation for reward-seeking behavior, and hedonic mouth movements during reward consumption.

Dataset Information

Reward regulation in plant-frugivore networks requires only weak cues.

Publications

Reward regulation in plant-frugivore networks requires only weak cues.

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