Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
A four-week white bread diet does not alter plasma glucose concentrations, metabolic or vascular physiology in mourning doves, Zenaida macroura
Graphical abstract
Introduction
Plasma glucose concentrations are 1.5–2 times higher in birds than in mammals of similar body mass (Braun and Sweazea, 2008). The evolutionary and physiological reasons for this difference are unknown and may include lower plasma insulin in birds than mammals (Hazelwood, 1973), insensitivity to the glucose lowering effects of insulin in birds (Dupont et al., 2004; Sweazea and Braun, 2005; Sweazea et al., 2006), and a higher sensitivity of birds than mammals to the effects of glucagon (Hazelwood, 1973). In fact, only supraphysiological doses of insulin have been shown to moderately lower blood glucose (Chen et al., 1945; Chida et al., 2000; Tokushima et al., 2005). Avian physiology also differs from that of mammals in that lipogenesis in birds predominantly occurs in the liver instead of adipose (Leveille et al., 1968) and absorbed dietary fat enters directly into the bloodstream in the form of portomicrons, instead of circulating through the lymphatic system as seen in mammals (Bensadoun and Rothfeld, 1972). Aside from their unique physiology, birds may serve as a natural model of hyperglycemia without the complications that mammals normally develop, and thus can aide in diabetes research (Szwergold and Miller, 2014).
In rodents, a diet rich in refined carbohydrates can cause adipose tissue inflammation and metabolic derangement (de Oliveira et al., 2013). This diet increases hepatic fat, triglycerides, and total cholesterol (de Oliveira and Menezes-Garcia, 2015), as well as visceral fat and plasma triglycerides (Spadaro et al., 2015), total serum cholesterol, and blood pressure while decreasing insulin sensitivity (Yamada et al., 2016; Fournier et al., 1986). Whether birds, which are naturally hyperglycemic, develop similar pathologies in response to an exclusive refined carbohydrate diet has not been determined. We investigated this question by measuring the effects of a diet consisting of highly refined carbohydrates (commercial white bread) fed to mourning doves. Mourning doves are mostly granivorous (Dillon, 1961) and their natural diet, therefore, consists primarily of complex carbohydrates. However, the processing of whole wheat seeds into white bread makes the stored starch more readily accessible to digestive enzymes and raises the glycemic load (GL) for humans per gram of food from 0.6 to 2.36 GL, thus increasing the rate at which the food is digested and absorbed after eating (Atkinson et al., 2008). Further, as birds predominately absorb monosaccharides via paracellular processes (Caviedes-Vidal et al., 2007), the added simple sugars to bread plus the readily available starch make a bread diet a strong choice to examine physiological responses to a high glycemic diet in birds.
In mammals, chronic hyperglycemia is associated with increased production of reactive oxygen species (ROS; Inoguchi et al., 2000). ROS can contribute to vascular damage such as impaired endothelium-dependent vasodilation, which can promote hypertension (Taniyama and Griendling, 2003). By contrast, mourning doves, although having high plasma glucose, have ROS concentrations that are similar to those of healthy rats (Smith et al., 2011). Studies of cranial tibial arteries from mourning doves found that ex vivo exposure to high glucose concentrations impairs endothelium-mediated vasodilation via an oxidative stress-dependent mechanism (Jarrett et al., 2016). The mechanism that protects intact birds from elevated plasma glucose-associated oxidative damage remains speculative.
Granivorous urban birds often consume human foods typical of a western diet that are obtained from waste or recreational feeding, and bread is reportedly the most common food given to birds by bird feeders (Galbraith et al., 2014). Although wheat seed is a choice food for mourning doves (Hayslette and Mirarchi, 2001), it is unknown how a fully refined wheat/bread diet would affect the metabolic and vascular physiology of these birds. We hypothesized that feeding adult mourning doves a refined carbohydrate diet for four weeks would 1) raise plasma glucose concentrations and alter metabolic pathways related to energy metabolism, and 2) impair vascular function when compared to birds fed nutritionally balanced bird seeds (seed diet). Determining how mourning doves respond to a highly refined carbohydrate diet may help us better understand their unique physiology and identify how granivorous birds in general protect themselves from diet-induced hyperglycemia and resultant diabetes-like pathologies as seen in mammals.
Section snippets
Animals and diet
Mourning doves commonly reside in the study area (Arizona State University [ASU] Tempe Campus; 33° 25′11.5”N - 111° 55′ 55.6”W; altitude: 365 m asl) and have been used for related studies (Jarrett et al., 2016, Jarrett et al., 2013; Smith et al., 2011; Sweazea et al., 2006). Adult male mourning doves (Zenaida macroura; 110–130 g body mass) were trapped as previously described (Jarrett et al., 2016; Jarrett et al., 2013; Smith et al., 2011), using a walk-in funnel trap baited with wild bird
Results
In total, 123 plasma metabolites as well as 92 liver and pectoral muscle metabolites were reliably detected in more than 80% of all samples (Supplemental file). In total, 15 metabolites were notably altered (ROAUC>0.90) although t-test significance was lost for all metabolites after adjusting for multiple hypothesis testing (q-value>0.05; Table 2). Table 2 contains significance information, area under receiver operating characteristic (AUROC) results, as well as fold change (FC) magnitude
Discussion
We used mourning doves as an experimental model to determine the metabolic and physiological effects of consuming a refined carbohydrate diet compared to their natural complex carbohydrate diet. Contrary to our hypothesis, which was based on mammalian response to a refined carbohydrate diet, WB consumption did not alter plasma glucose concentrations in doves, and PCA score plots suggest minimal differences in plasma, liver, and pectoralis muscle metabolites between groups. However, consumption
Acknowledgments
The authors would like to acknowledge Xinchen Wang from the Arizona State University Metabolomic Laboratory for their assistance with the multivariant analyses. We also thank Monique Bertin for her technical assistance with tissue and plasma assays.
Author contributions
KLS, PD and HG were senior authors on the study. AJB, WC, and KLS carried out the plasma and tissue biochemical assays and data analyses. KLS carried out the vasodilation measurements and analyses. AJB, KLS, PD, and HG conceived and planned, while XS, PJ, and HG carried out, the plasma and tissue metabolomics data collection and analyses. AJB, KLS, and PD contributed to the interpretation of the results. AJB took the lead in writing the manuscript and all authors provided critical feedback.
Funding
ASU School of Life Sciences/Office of Knowledge Enterprise Development - Research Investment Initiative (KLS, PD), a summer research fellowship from the American Physiological Society (WC), and an ASU Center of Evolution and Medicine Graduate Fellow Award (AJB).
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper
References (50)
- et al.
UHPLC–HRMS-based tissue untargeted metabolomics study of naringin and hesperidin after dietary supplementation in chickens
Food Chem.
(2018) - et al.
Glucose regulation in birds
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
(2008) - et al.
Deregulated Myc requires MondoA/mlx for metabolic reprogramming and tumorigenesis
Cancer Cell
(2015) - et al.
Carbohydrate metabolism in temporal and persistent hypoglycemic chickens induced by insulin infusion
Comp. Biochem. Physiol.
(2000) - et al.
Evaluation of dried bakery products for use in broiler diets
Poult. Sci.
(1965) - et al.
Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle
Domest. Anim. Endocrinol.
(2004) - et al.
Risks and drivers of wild bird feeding in urban areas of New Zealand
Biol. Conserv.
(2014) - et al.
High glucose impairs acetylcholine-mediated vasodilation in isolated arteries from mourning doves (Z. macroura). Comp. Biochem. Physiol. -part a Mol
Integr. Physiol.
(2016) - et al.
Breast cancer detection using targeted plasma metabolomics
J. Chromatogr. B Anal. Technol. Biomed. Life Sci.
(2019) - et al.
Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential
Mech. Ageing Dev.
(1993)
Transcriptome and DNA Methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal Cancer
Cell Rep.
A homologous radioimmunoassay for chicken insulin
Poult. Sci.
Metabolomic analysis of white and yellow seminal plasma in turkeys (Meleagris gallopavo)
Poult. Sci.
Naturally high plasma glucose levels in mourning doves (Zenaida macroura) do not lead to high levels of reactive oxygen species in the vasculature
Zoology
Inhibition of lipolysis does not affect insulin sensitivity to glucose uptake in the mourning dove
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
Glucose uptake in vivo in skeletal muscles of insulin-injected chicks
Comp. Biochem. Physiol.
Immunologic and metabolic effects of high-refined carbohydrate-containing diet in food allergic mice
Nutrition
Haematological traits and serum chemistry of broiler chicken fed bread waste based diets
J. Anim. Heal. Prod.
International tables of glycemic index and glycemic load values: 2008
Diabetes Care
The form of absorption of lipids in the chicken, Gallus domesticus
Proc. Soc. Exp. Biol. Med.
Candidate serum metabolite biomarkers for differentiating gastroesophageal reflux disease, Barrett’s esophagus, and high-grade dysplasia/esophageal adenocarcinoma
Metabolomics
The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts
Proc. Natl. Acad. Sci. U. S. A.
Susceptibility of birds to insulin as compared with mammals
J. Pharmacol. Exp. Ther.
The moisture content of white bread
Int. J. Food Sci. Nutr.
Mourning dove foods in Texas during September and October
J. Wildl. Manag.
Cited by (10)
Past and future: Urbanization and the avian endocrine system
2023, General and Comparative EndocrinologyCitation Excerpt :The result of a study on captive white ibis (Endocimus albus) nestlings receiving an anthropogenic diet (addition of white bread and reduction in seafood content) suggested that this diet decreases the birds' ability to fight pathogens (Cummings et al., 2019). Finally, captive mourning doves (Zanaida macroura) from a wild population that were fed white bread for four weeks had elevated hepatic glycogen but did not differ from control doves with regard to their plasma glucose and other indicators of metabolic physiology (Basile et al., 2020). These studies vividly illustrate the potential for anthropogenic food to disrupt physiological homeostasis, but also highlight how underexplored this topic is despite its relevance to our understanding of the consequences of urbanization to avian populations.
Effect of macronutrient and micronutrient manipulation on avian blood glucose concentration: A systematic review
2022, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyCitation Excerpt :Chronically, avian diets can impact blood glucose concentrations in various ways, though avian studies have produced varying results for all macronutrients. For example, a high refined carbohydrate diet (i.e., white bread) fed to adult mourning doves produced no change in blood glucose after four weeks (Basile et al., 2020), yet a one-day long study in turkey poults demonstrated an increase in blood glucose with a high carbohydrate diet (Donaldson and Christiansen, 1991). Similarly, blood glucose was lowered when dietary saturated fat was increased in broiler chicks after 31 days (Monfaredi et al., 2011); however, another study of broiler chicks showed an increase in blood glucose resulting from consumption of a high saturated fat diet after six weeks (Peebles et al., 1997).
Utilizing comparative models in biomedical research
2021, Comparative Biochemistry and Physiology Part - B: Biochemistry and Molecular BiologyCitation Excerpt :Though these changes are also seen in humans with fatty liver disease, birds are able to reverse the changes without incurring necrosis or cirrhosis (Wei et al., 2021). Recent work in birds illustrates that neither a refined carbohydrate diet nor a high fat diet has significant effects on plasma glucose, metabolic or vascular physiology (Basile et al., 2020, 2021). Cardiac disease and cardiac arrhythmias are a leading cause of mortality in developing countries, and the majority of research in this area relies heavily on rodent models.
Utilizing comparative models in biomedical research
2021, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyA four-week high fat diet does not alter plasma glucose or metabolic physiology in wild-caught mourning doves (Zenaida macroura)
2021, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyCitation Excerpt :All experimental procedures were approved by the ASU Institutional Animal Care and Use Committee and were conducted under appropriate state and federal permits. Metabolomics analyses were performed at the Arizona Metabolomics Laboratory as previously described (Basile et al., 2020). Briefly, plasma, liver, pectoralis muscle, and kidney samples (HF = 7; CON = 7 for each; batches were combined for analyses) were thawed overnight at 4 °C.