Haematological and blood chemistry variables are widely used in ecophysiological research as physiological indices of body condition in various vertebrate taxa. In this study, we analysed relationships between blood glucose and blood haemoglobin concentrations of adult birds in wild populations of Blue Tits (Cyanistes caeruleus) and Great Tits (Parus major) during the breeding season in central Poland. We found that blood glucose and blood haemoglobin concentrations are negatively correlated. We also show that individual Blue Tits have higher mean haemoglobin levels adjusted for the common value of glucose concentration than individual Great Tits and that females of both species have higher mean haemoglobin concentrations than males. Our results suggest that haematological as well as biochemical variables may be used in tune as complementary indices of body condition in wild bird populations.
Alonso-AlvarezC., and FerrerM. (2001) A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol. Biochem. Zool., 74, 703–713.
2.
ApplebyR.C. (1984) Diabetes mellitus in a budgerigar (Melopsitaccus undulatus). Vet. Rec., 115, 652–653.
3.
ArtachoP., Soto-GamboaM., VerduggoC., and NespoloR. (2007) Using haematological parameters to infer the health and nutritional status of an endangered Black-necked Swan population. Comp. Biochem. Physiol. A, 147, 1060–1066.
4.
BańburaJ., BańburaM., KalińskiA., SkwarskaJ., SłtomczyriskiR., WawrzyniakJ., and ZielińskiP. (2007) Habitat and year-to-year variation in haemoglobine concentration in nestling Blue Tits Cyanistes caeruleus. Comp. Biochem. Physiol. A, 148, 572–577.
5.
BeuchatC.A., and ChongC. (1998) Hyperglycemia in hummingbirds and its consequences for hemoglobin glycation. Comp. Biochem. Physiol. A, 120, 409–416.
6.
BraunE.J., and SweazeaK. (2008) Glucose regulation in birds. Comp. Biochem. Physiol. B, 151, 1–9.
7.
CohenA., KlasingK., and RicklefsR. (2007) Measuring circulating antioxidants in wild birds. Comp. Biochem. Physiol. B, 147, 110–121.
8.
CuervoJ.J., MøllerA.P., and De LopeF. (2007) Haematocrit is weakly related to condition in nestling Barn Swallows Hirundo rustica. Ibis, 149, 128–134.
9.
DaveyC., LillA., and BaldwinJ. (2000) Variation during breeding in parameters that influence blood oxygen carrying capacity in shearwaters. Aust. J. Zool., 48, 347–356.
10.
EllisR., McWhorterT.J., and MaronM. (2012) Integrating landscape ecology and conservation physiology. Landsc. Ecol., 27, 1–12.
11.
GanczA.Y., WellehanJ.F.X., BoutetteJ., MalkaS., LeeS.E., SmithD.A., and TaylorM. (2007) Diabetes mellitus concurrent with hepatic haemosiderosis in two macaws (Ara severa, Ara militaris). Avian Pathol., 36, 331–336.
12.
GayathriK.L., ShenoyK.B., and HegdeS.N. (2004) Blood profile of pigeons (Columba livia) during growth and breeding. Comp. Biochem. Physiol. A, 138, 187–192.
13.
GlądalskiM., SkwarskaJ., KalińskiA., BańburaM., MarkowskiM., WawrzyniakJ., ZielińskiP., and BańburaJ. (2015) Patterns of year-to-year variation in haemoglobin and glucose concentrations in the blood of nestling Pied Flycatchers, Ficedula hypoleuca. J. Ornithol., 156, 811–817.
14.
GrunstM.L., RotenberryJ.T., and GrunstA.S. (2014) Variation in adrenocortical stress physiology and condition metrics within a heterogeneous urban environment in the song sparrow Melospiza melodia. J. Avian Biol., 45, 1–10.
15.
HeckR.H., ThomasS.L., and TabataL.N. (2010) Multilevel and longitudinal modeling with IBM SPSS.Routledge, New York.
16.
JenniL., and Jenni-EiermannS. (1994) Plasma metabolite levels predict individual body-mass changes in a small long-distance migrant, the Garden Warbler. Auk, 111, 886–897.
17.
JenniL., and Jenni-EiermannS. (1998) Fuel supply and metabolic constraints in migrating birds. J. Avian Biol., 29, 521–528.
18.
JenniL., and WinklerR. (1994) Moult and ageing of European passerines.Academic Press, London.
19.
JohnstoneC.P., ReinaR.D., and LillA. (2012) Interpreting indices of physiological stress in free-living vertebrates. J. Comp. Physiol. B, 182, 861–879.
20.
KalińskiA., BańburaM., SkwarskaJ., WawrzyniakJ., ZielińskiP., GlądalskiM., MarkowskiM., and BańburaJ. (2012) Parallel variation in haemoglobin concentration in nestling-rearing Blue Tits Cyanistes caeruleus and Great Tits Parus major. Acta Ornithol., 47, 129–136.
21.
KalińskiA., BańburaM., GlądalskiM., MarkowskiM., SkwarskaJ., WawrzyniakJ., ZielińskiP., CyżewskaI., and BańburaJ. (2014) Landscape patterns of variation in blood glucose concentration of nestling blue tits (Cyanistes caeruleus). Landscape Ecol., 29, 1521–1530.
22.
KalińskiA., BańburaM., GlądalskiM., MarkowskiM., SkwarskaJ., WawrzyniakJ., ZielińskiP., CyżewskaI., and BańburaJ. (2015a) Long-term variation in haemoglobin concentration in nestling great tits Parus major. Comp. Biochem. Physiol. A., 185, 9–15.
23.
KalińskiA., BańburaM., GlądalskiM., MarkowskiM., SkwarskaJ., WawrzyniakJ., ZielińskiP., CyżewskaI., and BańburaJ. (2015b) Long-term variation in blood glucose concentration in nestling Great Tits (Parus major). Avian Biol. Res., 8, 129–137.
24.
KalińskiA., WawrzyniakJ., BańburaM., SkwarskaJ., ZielińskiP., and BańburaJ. (2009) Haemoglobin concentration and body condition of nestlings Great Tits Parus major: a comparison of first and second broods in two contrasting seasons. Ibis, 151, 667–676.
25.
KhanN., and RobertK. (2013) Does sex matter? Differential responses to corticosterone administration in the zebra finch. Zool., 116, 293–299.
26.
KilgasP., MändR., MägiM., and TilgarV. (2006) Hematological parameters in brood-rearing Great Tits in relation to habitat, multiple breeding and sex. Comp. Biochem. Physiol. A, 144, 224–231.
27.
Kostelecka-MyrchaA., and JaroszewiczM. (1993) The changes in the values of red blood indices during the nestling development of the house martin Delichon urbica. Acta Ornithol., 28, 39–46.
28.
LambrechtsM.M., AdriaensenF., ArdiaD.R., ArtemyevA.V., AtiénzarF., BańburaJ., BarbaE., BouvierJ-Ch., CamprodonJ., CooperC.B., DawsonR.D., EensM., EevaT., FaivreB., GaramszegiL.Z., GoodenoughA.E., GoslerA.G., GrégoireA., GriffithC.G., GustafssonL., JohnsonL.L., KaniaW., KeišsO., LlambiasP.E., MainwaringM.C., MändR., MassaB., MazgajskiT.D., MøllerA.P., MorenoJ., Naef-DaenzerB., NilssonJ.-Å, NorteA.C., OrellM., OtterK.A., ParkC.R., PerrinsC.R., PinowskiJ., PorkertJ., PottiJ., RemesV., RichnerH., RytkönenS., ShiaoM.-T., SilverinB., SlagsvoldT., SmithH.G., SoraceA., StenningM.J., StewartI., ThompsonC.F., TryjanowskiP., TörökJ., van NoordwijkA.J., WinklerD.W., and ZianeN. (2010) The design of artificial nestboxes for the study of secondary hole-nesting birds: A review of methodological inconsistencies and potential biases. Acta Ornithol., 45, 1–26.
29.
LandysM. M., RamenofskyM., and WingfieldJ. C. (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocr., 148, 132–149.
30.
LillA., RajchlK., Yachou-WosL., and JohnstoneC.P. (2013a) Are haematocrit and haemoglobin concentration reliable body condition indicators in nestlings: the Welcome Swallow as a case study. Avi. Biol. Res., 6, 57–66.
31.
LillA., Yachou-WosL., and JohnstoneC.P. (2013b) Are haematocrit and haemoglobin concentration reliable indicators of body condition in adult Welcome Swallows?Emu, 113, 93–98.
32.
MarkowskiM., BańburaM., KalińskiA., MarkowskiJ., SkwarskaJ., WawrzyniakJ., ZielińskiP., CyżewskaI., and BańburaJ. (2014) Spatial and temporal variation of lead, cadmium, and zinc in feathers of great tit and blue tit nestlings in central Poland. Arch. Environ. Con. Tox., 67, 507–518.
33.
MaronM., GouldingW., EllisR.D., and Mohd-TaibF.S. (2012) Distribution and individual condition reveal a hierarchy of habitat suitability for area-sensitive passerine. Biodivers. Conserv., 21, 2509–2523.
34.
MiniasP. (2014) High glucose concentrations are associated with symptoms of mild anaemia in Whiskered Terns: consequences for assesing physiological quality in birds. J. Ornithol., 155, 1067–1070.
35.
MiniasP., and KaczmarekK. (2013) Concentration of plasma metabolites as predictors of nestling condition in the Great Cormorant (Phalacrocorax carbo sinensis). Ornis Fenn., 90, 142–150.
36.
NadolskiJ., SkwarskaJ., KalińskiA., BańburaM., ŚniegulaR., and BańburaJ. (2006) Blood parameters as consistent predictors of nestling performance in great tits (Parus major and P. caeruleus) in the wild. Comp. Biochem. Physiol., A, 143, 50–54.
37.
O'BrienE.L., MorrisoB., and JohnsonL.S. (2001) Assesing the effects of haematotophagous ectoparasites on the health of nestling birds: haematocrit vs haemoglobin levels in House wrens parasitised by blow fly larvae. J. Avian Biol., 32, 73–76.
38.
OtsI., MuramagiA., and HõrakP. (1998) Haematological health state indices of reproducing great tits: methodology and sources of natural variation. Funct. Ecol., 12, 700–707.
39.
ParteckeJ., SchwablI., and GwinnerE. (2006) Stress and the city: urbanization and its effects on the stress physiology in european blackbirds. Ecol., 87, 1945–1952.
40.
PilnyA.A., and LoungR. (2005) Diabetes mellitus in a chestnut- fronted macaw (Ara severa). J. Avian. Med. Surg., 19, 297–302.
41.
PolakofS., MommsenT.P., and SoengasJ.L. (2011) Glucosensing and glucose homeostasis: From fish to mammals. Comp. Bioch. Physiol. B, 160, 123–149.
Remage-HealeyL., and RomeroM.L. (2001) Corticosterone and insulin interact to regulate glucose and trigliceride levels during stress in a bird. Am. J. Physiol. Reg. Integ. Comp. Physiol., 281, R994–R1003.
44.
RomeroM.L., and Remage-HealeyL. (2000) Daily and seasonal varition in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen. Comp. Endocr., 119, 52–59.
45.
RuizG., RosenmannM., NovoaF.F., and SabatP. (2002) Hematological parameters and stress index in rufous-collared sparrows dwelling in urban environments. Condor, 104, 162–166.
46.
ScanesC.G., and BraunE. (2013) Avian metabolism: its control and evolution. Front. Biol., 8, 134–159
47.
Schmidt-NielsenK. (1990) Animal physiology: adaptation and environment.Oxford University Press, Oxford.
48.
SergentN., RogersT., and CunninghamM. (2004) Influence of biological and ecological factors on hematological values in wild Little Penguins, Eudyptula minor. Comp. Bioch. Physiol. B, 138, 333–339.
49.
SimmonsP., and LillA. (2006) Development of parameters influencing blood oxygen carrying capacity in the welcome swallow and fairy martin. Comp. Bioch. Physiol. A, 143, 459–468.
50.
SłtomczyńskiR., KalińskiA., WawrzyniakJ., BańburaM., SkwarskaJ., ZielińskiP., and BańburaJ. (2006) Effects of experimantal reduction in nest micro-parasite and macro-parasite loads on nestling hemoglobin level in tits Parus caeruleus. Acta Oecol., 30, 223–227.
51.
SmithK.D., and BarberC. (2012) Hematocrit does not indicate condition in nestling or adult european starlings. Wilson J. Orn., 124, 788–792.
52.
StierK.S., AlmasiB., GaspariniJ., PiaultR., RoulinA., and JenniL. (2009) Effects of corticosterone on innate and humoral immune functions and oxidative stress in barn owl nestlings. J. Exp. Zool., 212, 2084–2090.
53.
SweazeaK.L., McMurtryJ.P., ElseyR.M., RedigP., and BraunE. (2014) Comparison of metabolic substrates in alligators and several birds of prey. Zool., 117, 253–260.
54.
Wallner-PendletonE.A., RogersD., and EppleA. (1993) Diabetes mellitus in a red-tailed hawk (Buteo jamaicensis). Avian Pathol., 22, 631–635.
55.
WhittowG.C. (2000) Sturkie's avian physiology.Academic Press, San Diego.
56.
WinklerA.S., MarsdenJ., ChaudhuriK.R., HambleyH., and WatkinsP.J. (1999) Erythropoietin depletion and anaemia in diabetes mellitus. Diabetic Med., 16, 813–819.
