Energetic costs and implications of the intake of plant secondary metabolites on digestive and renal morphology in two austral passerines

Abstract

Seed-eating birds have a diet of high nutritional value; however, they must cope with plant secondary metabolites (PSM). We postulated that the detoxification capacity of birds is associated with a metabolic cost, given that the organs responsible for detoxification significantly contribute to energetic metabolism. We used an experimental approach to assess the effects of phenol-enriched diets on two passerines with different feeding habits: the omnivorous rufous-collared sparrow (Zonotrichia capensis) and the granivorous common diuca-finch (Diuca diuca). The birds were fed with one of three diets: control diet, supplemented with tannic acid, or supplemented with Opuntia ficus-indica phenolic extract (a common food of the sparrow but not the finch). After 5 weeks of exposure to the diets, we measured basal metabolic rates (BMR), energy intake, glucuronic acid output and digestive and kidney structure. In both species, detoxification capacity expressed as glucuronic acid output was higher in individuals consuming phenol-enriched diets compared to the control diet. However, whereas sparrows increase energy intake and intestinal mass when feeding on phenol-enriched diets, finches had lower intestinal mass and energy intake remains stable. Furthermore, sparrows had higher BMR on phenol-enriched diets compared to the control group, whereas in the finches BMR remains unchanged. Interspecific differences in response to phenols intake may be determined by the dietary habits of these species. While both species can feed on moderate phenolic diets for 5 weeks, energy costs may differ due to different responses in food intake and organ structure to counteract the effects of PSM intake.

Detoxification and elimination of nicotine by nectar-feeding birds

“…In these studies, the water balance of specialist herbivores was less affected by plant defence chemicals than that of generalist herbivores (Dearing et al 2001;Dearing et al 2002). This is confirmed by a recent study of seedeating birds in which increased water intake on a diet supplemented with phenols was recorded in common diuca-finches D. diuca but not in rufous-collared sparrows Zonotrichia capensis which are more accustomed to consuming toxins (Barceló et al 2016).…”

“…Glucuronic acid is a derivative of endogenous glucose, and therefore expensive to excrete: its presence in urine is an indication that detoxification may impact animals energetically (Mangione et al 2004;Sorensen et al 2005). The glucuronidation pathway is a major route of phenolic detoxification in birds (Jakubas et al 1993;Guglielmo et al 1996;Barceló et al 2016). Glucuronic acid output is considered a biomarker of the capacity to detoxify phenolics (Ríos et al 2012;Barceló et al 2016) and may have high energetic costs (Guglielmo et al 1996;Barceló et al 2016) in birds.…”

“…The action of detoxification enzymes, the synthesis of conjugation substrates and the active elimination of the by-products by the kidneys all require energy (Karasov and Martínez del Rio 2007;Au et al 2013). Increased energy expenditure associated with detoxification processes has been observed in birds challenged with secondary metabolites in their diet (Guglielmo et al 1996; Barceló et al 2016). This suggests that there may be a tradeoff between the energy birds gain by passively absorbing water-soluble nutrients such as glucose through the paracellular route and the increased metabolic demand to elminate the water-soluble nectar toxins that are absorbed concurrently.…”

Individual diet specialisation in sparrows is driven by phenotypic plasticity in traits related to trade‐offs in animal performance

“…; Kohl & Dearing ; Barceló et al . ). Thus, nutritional differences in the energy and macromolecular content among diet items may impact digestive performance, which could affect energy budgets when animal are faced with the prospect of switching diets.…”

“…Consumption of a wide range of resources that differ in quality result in physiological trade-offs associated with resource digestion; e.g. different diets require different digestive conditions, enzymes, or detoxification mechanisms for efficient assimilation (Afik & Karasov 1995;Karasov et al 2011;Kohl & Dearing 2011;Barcel o et al 2016). Thus, nutritional differences in the energy and macromolecular content among diet items may impact digestive performance, which could affect energy budgets when animal are faced with the prospect of switching diets.…”