Detoxification and elimination of nicotine by nectar-feeding birds

Abstract

Many dilute nectars consumed by bird pollinators contain secondary metabolites, potentially toxic chemicals produced by plants as defences against herbivores. Consequently, nectar-feeding birds are challenged not only by frequent water excess, but also by the toxin content of their diet. High water turnover, however, could be advantageous to nectar consumers by enabling them to excrete secondary metabolites or their transformation products more easily. We investigated how the alkaloid nicotine, naturally present in nectar of Nicotiana species, influences osmoregulation in white-bellied sunbirds Cinnyris talatala and Cape white-eyes Zosterops virens. We also examined the metabolic fate of nicotine in these two species to shed more light on the post-ingestive mechanisms that allow nectar-feeding birds to tolerate nectar nicotine. A high concentration of nicotine (50 µM) decreased cloacal fluid output and increased its osmolality in both species, due to reduced food intake that led to dehydration. White-eyes excreted a higher proportion of the ingested nicotine-containing diet than sunbirds. However, sugar concentration did not affect nicotine detoxification and elimination. Both species metabolised nicotine, excreting very little unchanged nicotine. Cape white-eyes mainly metabolised nicotine through the cotinine metabolic pathway, with norcotinine being the most abundant metabolite in the excreta, while white-bellied sunbirds excreted mainly nornicotine. Both species also utilized phase II conjugation reactions to detoxify nicotine, with Cape white-eyes depending more on the mercapturic acid pathway to detoxify nicotine than white-bellied sunbirds. We found that sunbirds and white-eyes, despite having a similar nicotine tolerance, responded differently and used different nicotine-derived metabolites to excrete nicotine.

Multiscale variability in nutrients and secondary metabolites in a bat‐dispersed neotropical fruit

“…At the same time, some seed dispersers might select high-proteinaceous (Rojas et al, 2021) Piper fruit pulp, coping with a relatively higher concentration of total phenolics that serve to defend the fruit against pests, as predicted by the "nutrient-toxin titration hypothesis." Although the detoxification capacities of vertebrate frugivores have been little explored, a suite of detoxification enzymes (Foley & Moore, 2005;Lerch-Henning et al, 2017) and microbes (Kohl et al, 2018) might play a role in coping with high concentrations of fruit secondary metabolites. In contrast, for alkenylphenols, we found a significant negative association with proteins, supporting the "removal-rate hypothesis."…”

“…We found a significant positive association with proteins for phenolics, supporting the “nutrient‐toxin titration/relative risk hypotheses.” Nutritious fruits are likely at high risk of attack from pathogens, which could necessitate a higher concentration of defensive metabolites. At the same time, some seed dispersers might select high‐proteinaceous (Rojas et al, 2021 ) Piper fruit pulp, coping with a relatively higher concentration of total phenolics that serve to defend the fruit against pests, as predicted by the “nutrient‐toxin titration hypothesis.” Although the detoxification capacities of vertebrate frugivores have been little explored, a suite of detoxification enzymes (Foley & Moore, 2005 ; Lerch‐Henning et al, 2017 ) and microbes (Kohl et al, 2018 ) might play a role in coping with high concentrations of fruit secondary metabolites. In contrast, for alkenylphenols, we found a significant negative association with proteins, supporting the “removal‐rate hypothesis.” Once ripe, P. sancti‐felicis fruits ripen late in the afternoon and more than 91% are removed that same night by bats (Maynard et al, 2020 ).…”

The evolution of UDP-glycosyl/glucuronosyltransferase 1E (UGT1E) genes in bird lineages is linked to feeding habits but UGT2 genes is not

“…Specifically, EROD activity is higher in insectivores than in granivores, possibly because some insects use defensive compounds from plants [ 39 ]. Still other reports have suggested that conjugation enzymes are important in nectar-eating birds for metabolizing nicotine, a process that varies in mechanism across avian species [ 40 ]. Together, these studies indicate that increased granularity in feeding classifications may yield a clearer picture regarding how diet influences UGT evolution.…”