Although the function of nectar is to attract and reward pollinators, secondary metabolites (SM) produced by plants as anti-herbivore defences are frequently present in floral nectars.Greater understanding is needed of the effects of SM in nectar on the foraging behavior and performance of pollinators, and on plant-pollinator interactions. We investigated how nectarfeeding birds, both specialist (white-bellied sunbirds Cinnyris talatala) and generalist (darkcapped bulbuls Pycnonotus tricolor and Cape white-eyes Zosterops virens), respond to artificial nectar containing the alkaloid nicotine, present in nectar of Nicotiana species.Preference tests were carried out with a range of nicotine concentrations (0.1-300 µM) in two sucrose concentrations (0.25 and 1 M). In addition, we measured short-term feeding patterns in white-bellied sunbirds that were offered nicotine (0-50 µM) in 0.63 M sucrose. Both nicotine and sugar concentrations influenced the response of bird pollinators to nicotine. The birds showed dose-dependent responses to nicotine; and their tolerance of high nicotine concentrations was reduced on the dilute 0.25 M sucrose diet, on which they increased consumption to maintain energy intake. White-bellied sunbirds decreased both feeding frequency and feeding duration as the nicotine concentration in artificial nectar increased. Of the three species, bulbuls showed the highest tolerance for nicotine, and sugar type (sucrose or hexose) had no effect. The indifference of bulbuls to nicotine may be related to their primarily frugivorous diet. Additional testing of other avian nectarivores and different SM is required to further elucidate whether generalist bird pollinators, which utilise dilute nectars in which SM have stronger deterrent effects, are more tolerant of 'toxic' nectar. 2 The occurrence of secondary metabolites (SM) in nectar has been reported in at least 21 angiosperm families (Adler 2000). Little is known about the significance of these nectar components in plant-pollinator relationships, or about the possible trade-offs between defence and attraction (Strauss 1997, Irwin et al. 2004, Kessler and Halitschke 2009 Alternatively, SM could help to protect nectar from degradation due to microorganisms such as yeasts (Irwin et al. 2004, Herrera et al. 2008; and there is some evidence that SM in nectar could have indirect benefits by reducing the pathogen loads of pollinators (Manson et al. 2010).Not to be excluded is the possibility that SM are present in nectar as a pleiotropic consequence of plant defence chemistry. This nonadaptive hypothesis leads to the prediction, partially supported by recent studies of Nicotiana and Asclepias, that defensive chemistry of nectar, flowers and leaves will be similar , Manson et al. 2012).Pollinators are generally repelled by artificial nectar containing compounds from the major SM classes of alkaloids and phenolics. High concentrations of various SM have been found to reduce food consumption of honeybees Apis mellifera (Detzel and Wink 1993, Hagler and Buchm...
Secondary compounds in nectar may play a decisive role in determining the spectrum of floral visitors on plants. Flowers of the African coral tree Erythrina caffra are visited mainly by generalist passerine nectarivores, such as weavers and bulbuls. As the nectar of this species tastes very bitter to humans, it was hypothesized that secondary compounds may repel sunbirds and honeybees which are common in the same habitats yet seldom consume the nectar. We conducted choice tests using fresh nectar and both sucrose and hexose (glucose/fructose) solutions of the same concentration as the nectar. White-bellied Sunbirds (Cinnyris talatala) were repelled by nectar of both E. caffra and a related species Erythrina lysistemon, but Dark-capped Bulbuls (Pycnonotus tricolor) did not discriminate between the Erythrina nectar and control sugar solution in terms of amounts consumed. Honeybees (Apis mellifera scutellata) probed exposed droplets of E. caffra nectar and a control sugar solution at the same rate, suggesting that there is no volatile deterrent, but they immediately withdrew their proboscis far more often from the droplets of Erythrina nectar than they did from the sugar solution, suggesting that they find Ery-thrina nectar distasteful. These results contribute to a growing awareness that non-sugar components of nectar can play important functional roles in plant pollination systems.
The paradox of secondary metabolites, toxic defence compounds produced by plants, in nectar and fruits is well known. Deterrence of feeding by nectarivorous and frugivorous birds is better understood than the effect of these chemicals on the digestive performance of birds. Digestive parameters such as transit time and sugar assimilation are important in assessing nutrient utilization and deterrence may be related to post-ingestive effects involving these parameters. Nectar and many fruits contain mainly sugars and water, and avian consumers compensate for low sugar content in their diet by increasing food intake: this may also increase their intake of secondary metabolites. We investigated how the alkaloid nicotine, naturally present in nectar of Nicotiana species, influences compensatory feeding and digestive performance of nectar-feeding birds. High nicotine concentration negatively affected compensatory feeding and apparent assimilation efficiency of white-bellied sunbirds Cinnyris talatala and Cape white-eyes Zosterops virens; but nicotine slowed gut transit time only in the latter species. In contrast, food intake and digestive performance of dark-capped bulbuls Pycnonotus tricolor was unaffected by nicotine up to a concentration of 50 µM.Bulbuls are primarily frugivorous, hence they are more exposed to secondary metabolites than sunbirds and possibly white-eyes. Because their diet is richer in toxins, frugivorous birds may have evolved more efficient detoxification strategies than those of specialist nectar-feeding birds.
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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