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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2013, Vol. 8 Issue (2) : 134-159    https://doi.org/10.1007/s11515-012-1206-2
REVIEW
Avian metabolism: its control and evolution
Colin G. SCANES1(), Eldon BRAUN2
1. Department of Biological Science, University of Wisconsin, Milwaukee, WI 53211, USA; 2. Department of Physiology, University of Arizona, Arizona Health Sciences Center, Tucson, AZ 85724, USA
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Abstract

This review discussed metabolism in poultry and wild birds with an emphasis on what remains to be elucidated. Circulating concentrations of glucose are much greater in both poultry and wild birds than in mammals which in turn are higher than in reptiles. The basis for this difference is unknown but does not appear to be related to the requirements of flight. Furthermore, birds exhibit a refractoriness to potential adverse effects of very high circulating concentrations of glucose. Again the basis of this is unclear. There is substantial information on the control of metabolism in poultry, although which hormones are exerting physiologic roles remains to be clarified. There is a tacit but unverified assumption that the control mechanisms are the same in wild birds and in poultry. Despite, significant research focus on metabolism in poultry and to a less extent wild birds, there is a dearth of studies determining metabolism in a quantitative manner.

Keywords metabolism      bird      circulating glucose      glucagon      insulin     
Corresponding Author(s): SCANES Colin G.,Email:scanes@uwm.edu   
Issue Date: 01 April 2013
 Cite this article:   
Colin G. SCANES,Eldon BRAUN. Avian metabolism: its control and evolution[J]. Front Biol, 2013, 8(2): 134-159.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-1206-2
https://academic.hep.com.cn/fib/EN/Y2013/V8/I2/134
FedFastedReferences
Class Mammalia
Human1311~802Edwards et al., 2001
Horse11584Christensen et al., 1997; Nadal et al., 1997
Rat13788Simon et al., 2011
Class: Aves (Birds)
Chicken241215Simon et al., 2011
Ducks178175Applegate et al., 1999; Farhat and Chavez, 2001
Hummingbird756306Beuchat and Chong, 1998
King penguin180Bernard et al., 2003
Ostrich218Verstappen et al., 2002
Class Reptilia
Turtle Melanochelys trijuga70-114Chandavar and Naik, 2008
Mediterranean Pond Turtles(Mauremys leprosa)74Hidalgo-Vila et al., 2007
Loggerhead sea turtle(Caretta caretta)18Lutz and Dunbar-Cooper, 1987
Morelet's crocodiles(Crocodylus moreletii)7.0Padilla et al., 2011
Alligators(Alligator mississippiensis)134(43-264)139(83-218)Lance et al., 1993
Snake(Psammophis Sibilans)127117Algauhari, 1967
Boa constrictor17-26Silva et al., 2011
Tab.1  Comparisons of circulating concentrations of glucose (mg/dL) in mammals, birds and reptiles in selected examples
Fig.1  Mean plasma glucose concentrations in 55 species of reptiles, in birds (97 species of wild birds) and in 162 species of mammals. The striking feature is the very high plasma level of plasma glucose in birds compared to the levels in either reptiles or mammals.
TreatmentGlucosemg/dLInsulinng/mLGlucagonpg/mLReferences
FastingChristensen et al., 2012a
Fed2431.54152Christensen et al., 2012a
Fasted 6 hours2190.85451Christensen et al., 2012a
Fed control2431.51142Christensen et al., 2012a
Fasted 24 hours1940.73406Christensen et al., 2012a
Blocking insulin
Fed+ 1 hour264-120Dupont et al., 2008
Fed+ anti-insulin+ 1 hour434-390Dupont et al., 2008
Fed+ 5 hour232-50Dupont et al., 2008
Fed+ anti-insulin+ 5 hour747-1080Dupont et al., 2008
Glucose loading1
Basal1940.37Zhao et al., 2009b
Glucose load (+ 30 minutes)2841.16Zhao et al., 2009b
Glucose load+ arginine (+ 30 minutes)2641.54Zhao et al., 2009b
Corticosterone plus glucose load (+ 30 minutes)2612.67Zhao et al., 2009b
Corticosterone (+ 2 hours)2381.20Zhao et al., 2009b
Tab.2  Examples of hormonal and metabolic perturbations on the circulating concentrations of glucose, insulin and glucagon in chickens
StimulusChickensDucksReferences
Fasting+++Christensen et al., 2012a
Low glucose++++++Honey et al., 1980; Laurent and Miahle, 1978
High glucoseHoney et al., 1980; Laurent and Miahle, 1978
Arginine++Honey et al., 1980; Laurent and Miahle,1978
InsulinHoney and Weir, 1979; Dupont et al., 2008
Somatostatin++Stroesser et al., 1980
Tab.3  Control of Secretion of glucagon in domestic birds
StimulusChickensDucksReferences
Fasting-Christensen et al., 2012a
High glucose++++King and Hazelwood 1976; Laurent and Miahle, 1978
Arginine++Honey et al., 1980; Laurent and Miahle, 1978
Glucagon+King and Hazelwood 1976
Somatostatin-Stroesser et al., 1980
Epinephrine-Langslow et al., 1970
Growth hormonea-Foltzer and Miahle, 1976.
Fatty acids--Laurent and Miahle, 1978
Glucocorticoids++Zhao et al., 2009b; Song et al., 2011
Tab.4  Control of insulin secretion in domestic birds
FedFastedDeltaCalculated from references
Whole body glucose utilization833521~322Belo et al., 1976
Hepatic net glycogen synthesis62.5b0~62.5De Beer et al., 2007
Hepatic net glycogenolysis0502+50De Beer et al., 2007
Muscle net glycogenolysisc0110+110Savenije et al., 2002
Glucose oxidationNANA
GluconeogenesisNANA but calculated as 370
Energy needs for protein synthesisNANA
Hepatic triglyceride net formation920~92Ekmay et al., 2010
83De Beer et al., 2007
Hepatic triglyceride net loss0117+117Ekmay et al., 2010
0250+250De Beer et al., 2007
Lipogenesis- Fatty acid synthesis from glucosed444.14.5~39.6Yeh and Leveille, 1970
Fatty acid oxidationNANA
GluconeogenesisNANA
LipolysisNANA
Adipose triglyceride formationNANA
Tab.5  Quantitative estimates of metabolic flows in adult chicks (mg/hour/kg)
Time (hours)Crop ingesta wet weightCrop lactate mMCrop lactate (mM)Crop lactate (mg)
+122.2±2.4xy13.4±4.47x0.3026.7
+325.6±4.7x38.0±9.6x0.9788
+522.4±3.9xy93.3±17.4y2.11190
+713.2±2.3xy87.6±15.7y1.16104
+910.2±1.8y98.4±11.4y1.0090
Tab.6  Changes in the crop contents of ingesta and lactate during the period of night when young turkey poults are not feeding (data from or calculated from Johannsen et al., 2005)
RegionDay/nightTime (hours)Young broiler chickens (32 day old)Laying hens
Crop
Photophase±72.0±1.9 ab4.5±2.8b
Photophase±11—122.5±1.6 ab15.5±7.7b
Scotophase±0—128.4±6.9c44.7±5.0c
Scotophase±511.6±3.5b20.0±4.8b
Scotophase±90.2±0.1a1.6±0.8a
Proventriculus+ gizzard
Photophase±715.1±2.0b22.0±2.8b
Photophase±11-1210.3±1.0ab26.2±3.0bc
Scotophase±0-122.2±3.0c30.4±2.8c
Scotophase±511.0±1.9ab23.0±1.6b
Scotophase±97.4±1.5a15.5±1.6a
ReferencesBuyse et al., 1993Scanes et al., 1987
Tab.7  Changes in the wet ingesta (grams) in the gastro-intestinal tract crop during a day night cycle (14L: 10D)
SpeciesChange in basal metabolic rateReferences
House sparrows (Passer domesticus)+ 29%Martin et al., 2003
Great tits (Parus major)+ 9%Ots et al., 2001
Blue tits (Parus caeruleus)+ 8-13% n.s.Swensson et al., 1998
Japanese quail (Coturnix coturnix)~7%Boughton et al., 2007
Tab.8  Effect of an immune challenge (adaptive) on basal metabolic rate in birds
SpeciesChallengeMortality/morbidityHigh growth% (n=)Low growth % (n=)References
Chicken?Marek’s Disease virusMortality25.5 (302)a7.6 (302)bHan and Smyth, 1972, 1973
Chicken?Marek’s Disease virusParalysis31.2 (160) a5.2 (173) bHan and Smyth 1972
Turkeys??Pasteurella multocida or Newcastle disease virusMortality49.3 (207) a25.4 (54) bNestor et al., 1996a,b; 1999a,b
Tab.9  Effect of selection for growth on ability growing poultry to withstand challenge by infectious organisms
Bursa weight in (g% of body weight)Thymus weight in (g% of body weight)Spleen weight in (g % of body weight)Anti-body responseb (after second challengec)References
ChickenRandom breda0.890.490.331.01Cheema et al., 2003
Male(0.40)(0.22)(0.15)(4.7)
Fast growing2.00*1.69*1.00*0.56Cheema et al., 2003
Commercial breed(0.26*)(0.22)(0.13)(3.9)
ChickenRandom breda1.030.970.330.86Cheema et al., 2003
Female(0.50)(0.47)(0.26)(4.2)
Fast growing Commercial breed2.02*(0.27*)2.24*(0.30*)0.82*(0.11*)0.42(4.3)Cheema et al., 2003
TurkeyRandom breda0.72N.A.N.A.6.9Cheema et al., 2007
Male(0.34)(5.6)
Fast growing2.58*N.A.N.A.6.5Cheema et al., 2007
Commercial breed(0.66*)(5.3)
TurkeyRandom breda0.61(0.36)N.A.N.A.6.6(4.9)Cheema et al., 2007
Female
Fast growing2.47*N.A.N.A.7.2Cheema et al., 2007
Commercial breed(0.65*)(4.6)
TurkeyRandom breda27.4N.A.26.61.6Li et al., 2001
Mixed(1.14)(1.11)
Growth selected line47.0*N.A.63.5*1.5Li et al., 2001
(0.94*)(1.27*)
Tab.10  Comparison of immune parameters in poultry selected for fast growth with either random bred controls or with lines selected for low growth
OrdernPlasma glucose concentration
Squamata (Sauria)17121
Squamata (Ophidia)2659
Testudines1064
Crocodilia287
Grand totals5580
Tab.11  Plasma Glucose Concentrations (mg/dL) of Reptiles
Fig.2  Comparison of the mean glucose concentrations in mammals, birds and reptiles with their evolutionary relationships and estimated separation dates of common ancestors. Bold lines indicate identical structures for insulin. Phylogeny and separation dates are based on Shen et al., 2011. Similar phylogenies are reported by Hedges and Poling () and Sanders and Lee ()
Fig.3  Structure of insulin in birds
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