Abstract
Specific fatty acids (FA) such as unsaturated (UFA) and saturated (SFA) fatty acids contained in foods are key factors in the nutritional ecology of birds. By means of a field and experimental approach, we evaluated the effect of diet on the activity of three esterases involved in FA hydrolysis; carboxylesterase (CE: 4-NPA-CE and a-NA-CE) and butyrylcholinesterase, in two South American passerines: the omnivorous rufous-collared sparrow (Zonotrichia capensis) and the granivorous common diuca-finch (Diuca diuca). The activity of the three esterases was measured in the intestines of freshly caught individuals over two distinct seasons and also after a chronic intake of a UFA-rich or SFA-rich diet in the laboratory. In turn, we assessed the feeding responses of the birds choosing amongst diets contrasting in the kind of specific FA (UFA- vs. SFA-treated diets). During summer, field CE activities (4-NPA-CE and a-NA-CE) in the small intestine were higher in the rufous-collared sparrow (25.3 ± 3.3 and 81.4 ± 10.8 µmol min−1 g tissue−1, respectively) than in the common diuca-finch (10.0 ± 3.0 and 33.9 ± 13.1 µmol min−1 g tissue−1, respectively). Two hour feeding trial test indicated that both species exhibited a clear preference for UFA-treated diets. On average, the rufous-collared sparrow consumed 0.46 g 2 h−1 of UFA-rich diets and 0.12 g 2 h−1 of SFA-rich diets. In turn, the consumption pattern of the common diuca-finch averaged 0.73 and 0.16 g 2 h−1 for UFA-rich and SFA-rich diets, respectively. After a month of dietary acclimation to UFA-rich and SFA-rich diets, both species maintained body mass irrespective of the dietary regime. Additionally, the intestinal 4-NPA-CE activity exhibited by birds fed on a UFA-rich or SFA-rich diet was higher in the rufous-collared sparrow (39.0 ± 5.3 and 44.2 ± 7.3 µmol min−1 g tissue−1, respectively) than in the common diuca-finch (13.3 ± 1.9 and 11.2 ± 1.4 µmol min−1 g tissue−1, respectively). Finally, the intestinal a-NA-CE activity exhibited by the rufous-collared sparrow was about two times higher when consuming an UFA-rich diet. Our results suggest that the rufus-collared sparrow exhibits a greater capacity for intestinal FA hydrolysis, which would allow it to better deal with fats from different sources.
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References
Alan RR, McWilliams SR (2013) Oxidative stress, circulating antioxidants, and dietary preferences in songbirds. Comp Biochem Physiol B 164:185–193
Bairlein F (1991) Nutritional adaptations to fat deposition in the long-distance migratory garden warbler (Sylvia borin). Acta Congr Intern Ornithol 20:2149–2158
Bairlein F (2002) How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89:1–10
Bell GP (1990) Birds and mammals on an insect diet: a primer on diet composition analysis in relation to ecological energetics. Stud Avian Biol 13:416–422
Bewley J, Black D (1982) Physiology and biochemistry of seeds. Springer, Berlin
Bozinovic F, Méndez MA (1997) Role of dietary fatty acids on energetics and torpor in the Chilean mouse-opossum Thylamys elegans. Comp Biochem Physiol A 116:101–104
Bradford M (1976) A rapid and sensitive assay of protein utilizing the principle of dye binding. Anal Biochem 772:248–264
Brzęk P, Kohl K, Caviedes-Vidal E, Karasov WH (2009) Developmental adjustments of house sparrow (Passer domesticus) nestlings to diet composition. J Exp Biol 212:1284–1293
Brzęk P, Lessner KN, Caviedes-Vidal E, Karasov WH (2010) Low plasticity in digestive physiology constrains feeding ecology in diet specialist, zebra finch (Taeniopygia guttata). J Exp Biol 213:798–807
Bush FM, Price JR, Townsend JI (1973) Avian hepatic esterases, pesticides and diet. Comp Biochem Physiol 44:1137–1151
Caviedes-Vidal E, Afik D, Martínez del Rio C, Karasov WH (2000) Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis. Comp Biochem Physiol A 125:11–24
Caviedes-Vidal E, McWhorter TJ, Lavin SR, Chediack JG, Tracy CR, Karasov WH (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci USA 104:19132–19137
Chanda SM, Mortensen SR, Moser VC, Padilla S (1997) Tissue-specific effects of chlorpyrifos on carboxylesterase and cholinesterase activity in adult rats: an in vitro and in vivo Comparison. Fund Appl Toxicol 38:148–157
Cueto VR, Marone L, Lopez de Casenave J (2006) Seed preferences in sparrow species of the Monte desert: implications for seed–granivore interactions. Auk 123:358–367
Denbow DM (2000) Gastrointestinal anatomy and physiology. In: Whittow GC (ed) Sturkie’s avian physiology. Academic Press, New York, pp 299–325
di Castri F, Hajek ER (1976) Bioclimatología de Chile. Editorial Universidad Católica de Chile, Santiago
Diamond JM (1993) Logic of life: the challenge of integrative physiology. In: Noble D, Boyd CAR (eds) Evolutionary physiology, pp 89–111
Díaz M (1996) Food choice by seed-eating birds in relation to seed chemistry. Comp Biochem Physiol A 113:239–246
Eyer P, Worek F, Kiderlen D, Sinko G, Stuglin A, Simeon-Rudolf V, Reiner E (2003) Molar absorption coefficients for the reduced Ellamn reagent: reassessment. Anal Biochem 312:224–227
Finke MD (2002) Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biol 21:269–285
Gl Ellman, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Griminger P (1986) Lipid metabolism. In: Sturkie P (ed) Avian physiology. Springer, New York, pp 345–358
Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am J Physiol 282:1405–1413
Hargreaves M, Kiens B, Richter EA (1991) Effect of increased plasma free fatty acid concentrations on muscle metabolism in exercising men. J Appl Physiol 70:194–197
Karasov WH, Martínez del Rio C (2007) Ecological physiology: how animals process energy, nutrients and toxins. Princeton University Press, New Jersey
Khalilieh A, McCue MD, Pinshow B (2012) Physiological responses to food deprivation in the house sparrow, a species not adapted to prolonged fasting. Am J Physiol 303:551–561
Klasing KC (1998) Comparative avian nutrition. CAB International, Wallingford
Kohl K, Brzek P, Caviedes-Vidal E, Karasov WH (2011) Pancreatic and intestinal carbohydrases are matched to dietary starch level in wild passerines birds. Physiol Biochem Zool 84:195–203
Lepczyk CA, Murray KG, Winnett-Murray K, Bartell P, Geyer E, Work T (2000) Seasonal fruit preference for lipids and sugars by American robins. Auk 117:709–717
Linder R (2000) Adaptive evolution of seed oils in plants: accounting for the biogeographic distribution of saturated and unsaturated fatty acids in seed oils. Am Nat 156:442–458
Lopez-Calleja MV (1995) Dieta de Zonotrichia capensis (Emberizidae) and Diuca diuca (Fringillidae): efecto de la variación estacional de los recursos tróficos y la riqueza de aves granívoras de Chile central. Rev Chil His Nat 68:321–331
Lorenz K, Hwang YS (1986) Lipids in proso millet (Panicum miliaceum) flours and brans. Cereal Chem 63:387–390
Maldonado K, van Dongen WFD, Vásquez RA, Sabat P (2012) Geographic variation in the association between exploratory behavior and physiology in rufous-collared sparrows. Physiol Biochem Zool 160:117–124
Marone L, Lopez de Casenave J, Milesi FA, Cueto VR (2008) Can seed-eating birds exert top-down effects on the vegetation of the Monte desert? Oikos 117:611–619
Martínez del Rio C (1990) Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiol Zool 63:987–1011
McClelland GB (2004) Fat to the fire: the regulation of lipid oxidation with exercise and environmental stress. Comp Biochem Physiol B 139:443–460
McCue MD, Amitai O, Khozin-Goldberg I, McWilliams SR, Pinshow B (2009) Effect of dietary fatty acid composition on fatty acid profiles of polar and neutral lipid tissue fractions in zebra finches, Taeniopygia guttata. Comp Biochem Physiol A 154:165–172
McCue MD, McWilliams SR, Pinshow B (2011) Ontogeny and nutritional status influence oxidative kinetics of exogenous nutrients and whole-animal bioenergetics in zebra finches, Taeniopygia guttata. Physiol Biochem Zool 84:32–42
McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940
McWilliams SR, Kearney S, Karasov WH (2002) Dietary preferences of warblers for specific fatty acids in relation to nutritional requirements and digestive capabilities. J Avian Biol 33:167–174
McWilliams SR, Guglielmo CG, Pierce BJ, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a physiological ecology perspective. J Avian Biol 35:377–393
Pierce BJ, McWilliams SR, O’Connor TP, Place AR, Guglielmo CG (2004) Diet preferences for specific fatty acids and their effect on composition of fat reserves in migratory red-eyed vireos (Vireo olivaceous). Comp Biochem Physiol A 138:503–514
Ramirez-Otarola N, Narváez C, Sabat P (2011) Membrane-bound intestinal enzymes of passerine birds: dietary and phylogenetic correlates. J Comp Physiol B. doi:10.1007/s00360-011-0557-3
Ríos JM, Mangione AM (2010) Respuesta disuasiva del granívoro Zonotrichia capensis (Passeriformes: Emberizidae) frente a fenoles comunes en las semillas. Ecol Aust 20:215–221
Ríos JM, Mangione AM, Marone L (2012a) Effects of nutritional and anti-nutritional properties of seeds on the feeding ecology of seed-eating birds of the Monte desert, Argentina. Condor 114:44–55
Ríos JM, Mangione AM, Marone L (2012b) Tolerance to dietary phenolics and diet breadth in three seed-eating birds: implications for graminivory. J Exp Zool A 317:425–433
Sabat P, Novoa FF, Bozinovic F, Martínez del Rio C (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiol Zool 71:226–236
Sabat P, Ramirez-Otarola N, Bozinovic F, Martínez del Rio C (2013) The isotopic composition and insect content of diet predict tissue isotopic values in a South American passerine assemblage. J Comp Physiol B 183:419–430
Schaefer HM, Schmidt V, Bairlein F (2003) Discrimination abilities for nutrients: which difference matters for choosy birds and why? Anim Behav 65:531–541
Stiles EW (1993) The influence of pulp lipids on fruit preference by birds. Vegetatio 108:227–235
Thompson HM (1999) Esterases as markers of exposure to organophosphates and carbamates. Ecotoxicol 8:369–384
Valera F, Wagner RH, Romero M, Gutiérrez JE, Rey P (2005) Dietary specialization on high protein seeds by adult and nestling serins. Condor 107:29–40
Van Lith H, Meijer GW, van der Wouw MJA, Den Bieman M, Van Tintelen G, Van Zutphen LFM, Beynen AC (1992) Influence of amount of dietary fat and protein on esterase-1 (ES-1) activities of plasma and small intestine in rats. Br J Nutr 67:379–390
Wheelock C, Eder K, Werner I et al (2005) Individual variability in esterase activity and CYP1A levels in Chinook salmon (Oncorhynchus tshawytscha) exposed to esfenvalerate and chlorpyrifos. Aquat Toxicol 74:172–192
Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle River
Zurovchak JG (1997) Nutritional role of high-lipid fruits in the diet of migrant thrushes. Ph.D. Dissertation, Rutgers University
Acknowledgments
This work is from the postdoctoral project financed by Fondo Nacional de Desarrollo Científico y Tecnológico (Chile Proyecto No. 3130429 to JM Ríos and No. 1120276 to PS). Birds were captured with permits from SAG, Chile (No. 3935/2013). All protocols were approved by the Institutional Animal Care Committee of the Universidad de Chile, where the experiments were performed. We thank Andrés Sazo and Grabiela Píriz for their help in the field and laboratory. JMR gives special thanks to Jorgelina Altamirano and Nestor Ciocco.
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Communicated by I.D. Hume.
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Ríos, J.M., Barceló, G.F., Narváez, C. et al. Feeding and digestive responses to fatty acid intake in two South American passerines with different food habits. J Comp Physiol B 184, 729–739 (2014). https://doi.org/10.1007/s00360-014-0832-1
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DOI: https://doi.org/10.1007/s00360-014-0832-1