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Detoxification and elimination of nicotine by nectar-feeding birds

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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.

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Acknowledgements

This research was funded by the University of Pretoria and the National Research Foundation (73671). We are grateful to Jan Cilliers Park and the Pretoria National Botanic Gardens for permission to mist-net sunbirds and white-eyes under permit from the Gauteng Directorate of Nature Conservation. All bird care procedure and experimental protocols followed the institutional regulations of the Animal Use and Care Committee of the University of Pretoria (reference number: EC022-09). We thank Dr. M. Stander of the Central Analytical Facility at Stellenbosch University for conducting the nicotine metabolite analyses, Prof. Z. Apostolides for assistance with analysis and Dr. F. Demares for advice on statistical procedure.

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  1. Department of Zoology and Entomology, University of Pretoria, Private Bag X20, Hatfield, 0028, South Africa

    S. Lerch-Henning, E. E. Du Rand & S. W. Nicolson

  2. Department of Biochemistry, University of Pretoria, Private Bag X20, Hatfield, 0028, South Africa

    E. E. Du Rand

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  1. S. Lerch-Henning
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  2. E. E. Du Rand
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Correspondence to E. E. Du Rand.

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Communicated by I. D. Hume.

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Lerch-Henning, S., Du Rand, E.E. & Nicolson, S.W. Detoxification and elimination of nicotine by nectar-feeding birds. J Comp Physiol B 187, 591–602 (2017). https://doi.org/10.1007/s00360-016-1055-4

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