Abstract
Birds have high metabolic rates and so require an efficient cardiovascular system that provides their cells and tissues with sufficient oxygen. Birds are also exposed to a wide variety of pathogens and so require an effective immune system. In this chapter, the structure and function of the avian cardiovascular system are explained, including how the blood transports oxygen and carbon dioxide. Adaptations that allow some birds to fly at high altitudes where there is less oxygen and to dive under water when breathing is not possible are discussed. The specific functions of the formed elements in bird blood, including red blood cells, thrombocytes, and white blood cells, are also described. The various components of the avian immune system are described and the various ways that the immune system acts against pathogens and their toxins are explained in detail. The structure and function of the avian heart and blood vessels are explained, as is the process by which the flow of blood to different tissues and organs varies as needed to ensure that blood flow matches changes in metabolic activity.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abdalla MA, King AS (1975) The functional anatomy of the pulmonary circulation of the domestic fowl. Respir Physiol 23:267–290
Abdel-Magied EM, King AS (1978) The topographical anatomy and blood supply of the carotid body region of the Domestic Fowl. J Anat 126:535–546
Abdolmaleki M, Yeap SK, Tan SW, Satharasinghe DA, Bello MB, Jahromi MZ, Bejo MH, Omar AR, Ideris A (2018) Effects of Newcastle disease virus infection on chicken intestinal intraepithelial natural killer cells. Front Immunol 9:1386
Adair BM (2000) Immunopathogenesis of chicken anemia virus infection. Dev Comp Immunol 24:247–255
Akester AR (1964) Radiographic studies of the renal portal system in the Domestic Fowl (Gallus domesticus). J Anat 98:365–376
Al-Khalaifah H, Al-Nasser A (2018) Cytokines as effective elements of the avian immune system. J Microbiol Genet 2018:2574–7371
Al-Saffar TM, Al-Mawla ED (2008) Some hematological changes in chickens infected with ectoparasites in Mosul. Iraqi J Vet Sci 22:95–100
Alsafy MAM, El-Gendy SA, Enany S, Amine M (2009) Anatomical studies on the atrioventricular valves of the Ostrich heart (Struthio camelus). J Vet Anat 2:67–83
Altimiras J, Lindgren I, Giraldo-Deck LM, Matthei A, Garitano-Zavala Á (2017) Aerobic performance in tinamous is limited by their small heart. A novel hypothesis in the evolution of avian flight. Sci Rep 7:15964
Altshuler DL, Dudley R (2002) The ecological and evolutionary interface of hummingbird flight physiology. J Exp Biol 205:2325–2336
Amat JA, Rendón MA, Ramírez JM, Hortas F, Arroyo GM, Garrido A, Rendón-Martos M, Pérez-Hurtado A (2009) Hematocrit is related to age but not to nutritional condition in Greater Flamingo chicks. Eur J Wildl Res 55:179–182
Anderson HL, Brodsky IE, Mangalmurti NS (2018) The evolving erythrocyte: red blood cells as modulators of innate immunity. J Immunol 201:1343–1351
Apanius V (1998) Stress and immune defense. Adv Study Behav 27:133–153
Arad Z, Midtgard U, Bernstein MH (1989) Thermoregulation in Turkey Vultures: vascular anatomy, arteriovenous heat exchange, and behavior. Condor 91:505–514
Asghar M, Hasselquist D, Bensch S (2011) Are chronic avian haemosporidian infections costly in wild birds? J Avian Biol 42:530–537
Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:436–438
Ashley NT, Weil ZM, Nelson RJ (2012) Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43:385–406
Atkinson CT, LaPointe DA (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg 23:53–63
Atkinson CT, Van Riper C III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution, and behaviour. Oxford University Press, New York, pp 19–48
Atkinson CT, Dusek RJ, Lease JK (2001) Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii Amakihi. J Wildl Dis 37:20–27
Atkinson CT, Thomas NJ, Hunter DB (eds) (2009) Parasitic diseases of wild birds. Wiley, New York
Baccari GC, Pinelli C, Santillo A, Minucci S, Rastogi RK (2011) Mast cells in nonmammalian vertebrates: an overview. Int Rev Cell Mol Biol 290:1–53
Bairlein F, Totzke U (1992) New aspects on migratory physiology of trans-Saharan passerine migrants. Ornis Scand 23:244–250
Bańbura J, Bańbura M, Glądalski M, Kaliński A, Markowski M, Michalski M, Nadolski J, Skwarska J, Zieliński P (2011) Body condition parameters of nestling Great Tits Parus major in relation to experimental food supplementation. Acta Ornithol 46:207–212
Banerjee V, Banerjee M (1977) Variations of erythrocyte number and haemoglobin content of a migratory bird: Philomachus pugnax (Linnaeus). Zool Anz 199:261–264
Barnas GM, Rautenberg W (1990) Shivering and cardiorespiratory responses during normocapnic hypoxia in the pigeon. J Appl Physiol 68:84–87
Barrientos S, Brem H, Stojadinovic O, Tomic-Canic M (2014) Clinical application of growth factors and cytokines in wound healing. Wound Repair Regen 22:569–578
Barske JK (2013) Sexual selection and adaptations for performance of an elaborate courtship display by the Golden-collared Manakin (Manacus vitellinus). Ph.D. diss, Univ California, Los Angeles, CA
Barske J, Eghbali M, Kosarussavadi S, Choi E, Schlinger BA (2019) The heart of an acrobatic bird. Comp Biochem Physiol A 228:9–17
Barve S, Dhondt AA, Mathur VB, Cheviron ZA (2016) Life-history characteristics influence physiological strategies to cope with hypoxia in Himalayan birds. Proc R Soc B 283:20162201
Bauchinger U, McWilliams SR (2010) Extent of phenotypic flexibility during long-distance flight is determined by tissue-specific turnover rates: a new hypothesis. J Avian Biol 41:603–608
Beadell JS, Atkins C, Cashion E, Jonker M, Fleischer RC (2007) Immunological change in a parasite-impoverished environment: divergent signals from four island taxa. PLoS ONE 2:e896
Bean AGD, Lowenthal JW (2022) Avian cytokines and their receptors. In: Kaspers B, Schat KA, Göbel TW, Vervelde L (eds) Avian immunology, 3rd edn. Academic Press, London, pp 249–276
Beaufrére H, Ammersbach M, Tully TN Jr (2013) Complete blood cell count in Psittaciformes by using high-throughput image cytometry: a pilot study. J Avian Med Surg 27:211–217
Bensch S, Hellgren O, Pérez-Tris JR (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome B lineages. Mol Ecol Resour 9:1353–1358
Bernstein MH (1989) Temperature and oxygen supply in the avian brain. In: Wood SC (ed) Comparative pulmonary physiology. Dekker, New York, pp 343–368
Bevan RM, Butler PJ, Woakes AJ, Boyd IL (2002) The energetics of Gentoo Penguins, Pygoscelis papua, during the breeding season. Funct Ecol 16:175–190
Birkhead TR, Fletcher F, Pellatt EJ (1998) Sexual selection in the Zebra Finch Taeniopygia guttata: condition, sex traits and immune capacity. Behav Ecol Sociobiol 44:179–191
Bischoff SC (2009) Physiological and pathophysiological functions of intestinal mast cells. Semin Immunopathol 31:185–205
Bishop CM (1997) Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power input of flying animals. Philos Trans R Soc B 352:447–456
Bishop CM, Butler PJ (1995) Physiological modeling of oxygen consumption in birds during flight. J Exp Biol 198:2153–2163
Black CP, Tenney SM (1980) Oxygen transport during progressive hypoxia in high-altitude and sea-level waterfowl. Respir Physiol 39:217–239
Blount JD, Houston DC, Møller AP, Wright J (2003) Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds. Oikos 102:340–350
Boggs DF, Butler PJ, Wallace SE (1998) Differential air sac pressures in diving Tufted Ducks (Aythya fuligula). J Exp Biol 201:2665–2668
Boggs DF, Baudinette RV, Frappell P, Butler PJ (2001) The influence of locomotion on air sac pressures in Little Penguins. J Exp Biol 204:3582–3586
Bonadiman SF, Stratievsky GC, Machado JA, Albernaz AP, Rabelo GR, DaMatta RA (2009) Leukocyte ultrastructure, hematological and serum biochemical profiles of Ostriches (Struthio camelus). Poult Sci 88:2298–2306
Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379
Bordel R, Haase E (1993) Effects of flight on blood parameters in homing pigeons. J Comp Physiol B 163:219–224
Borras A, Cabrera J, Senar JC (2010) Hematocrit variation in response to altitude changes in wild birds: a repeated-measures design. Condor 112:622–626
Boström JE, Dimitrova M, Canton C, Håstad O, Qvarnström A, Ödeen A (2016) Ultra-rapid vision in birds. PLoS ONE 11:e0151099
Boukens BJ, Kristensen DL, Filogonio R, Carreira LB, Sartori MR, Abe AS, Currie S, Joyce W, Conner J, Opthof T, Crossley DA II, Wang T, Jensen B (2019) The electrocardiogram of vertebrates: evolutionary changes from ectothermy to endothermy. Prog Biophys Mol Biol 144:16–29
Bowers EK, Hodges CJ, Forsman AM, Vogel AL, Masters BS, Johnson BGP, Johnson LS, Thompson CF, Sakaluk SK (2014) Neonatal body condition, immune responsiveness, and hematocrit predict longevity in a wild bird population. Ecology 95:3027–3034
Broughton JM (1994) Size of the bursa of Fabricius in relation to gonad size and age in Laysan and Black-footed albatrosses. Condor 96:203–207
Brown CR, Brown MB (2002) Spleen volume varies with colony size and parasite load in a colonial bird. Proc R Soc B 269:1367–1373
Brown TJ, Hammers M, Taylor M, Dugdale HL, Komdeur J, Richardson DS (2021) Hematocrit, age, and survival in a wild vertebrate population. Ecol Evol 11:214–226
Burggren WW (2013) Cardiovascular development and angiogenesis in the early vertebrate embryo. Cardiovasc Eng Technol 4:234–245
Burmeister AR, Marriott I (2018) The interleukin-10 family of cytokines and their role in the CNS. Front Cell Neurosci 12:458
Burmester T, Hankeln T (2004) Neuroglobin: a respiratory protein of the nervous system. News Physiol Sci 19:110–113
Burmester T, Hankein T (2009) What is the function of neuroglobin? J Exp Biol 212:1423–1428
Burmester T, Hankeln T (2014) Function and evolution of vertebrate globins. Acta Physiol 211:501–514
Butler PJ (2001) Diving beyond the limits. News Physiol Sci 16:222–227
Butler PJ (2004) Metabolic regulation in diving birds and mammals. Respir Physiol Neurobiol 141:297–315
Butler PJ (2016) The physiological basis of bird flight. Philos Trans R Soc B 371:20150384
Butler PJ, Jones DR (1982) The comparative physiology of diving. Adv Comp Physiol Biochem 8:179–364
Butler PJ, Jones DR (1997) Physiology of diving birds and mammals. Physiol Rev 77:837–899
Butler PJ, Turner DL, Al-Wassia A, Bevan RM (1988) Regional distribution of blood flow during swimming in the Tufted Duck (Aythya fuligula). J Exp Biol 135:461–472
Buzala M, Slomka A, Janicki B, Ponczek MB, Żekanowska E (2017) Review: the mechanism of blood coagulation, its disorders and measurement in poultry. Livest Sci 195:1–8
Campbell TW (1988) Avian hematology and cytology, 1st edn. Iowa State University Press, Ames, IA
Campbell TW (1994) Hematology. In: Ritchie BW, Harrison GJ, Harrison LR (eds) Avian medicine: principles and application. Wingers Publishing, Lake Worth, FL, pp 176–198
Campbell TW (2015) Avian hematology and cytology, 4th edn. Wiley, Hoboken, NJ
Campbell TW, Ellis CK (2007) Avian and exotic animal hematology and cytology, 3rd edn. Blackwell Publications, Ames, IA
Carey C, Morton ML (1976) Aspects of circulatory physiology of montane and lowland birds. Comp Biochem Physiol 54A:61–74
Carlson HC, Sweeny PR, Tokaryk JM (1968) Demonstration of phagocytic and trephocytic activities of chicken thrombocytes by microscopy and vital staining techniques. Avian Dis 12:700–715
Carvalho AR Jr, Diniz RM, Suarez MAM, Figueiredo CSS, Zagmignan A, Grisotto MAG, Fernandes ES, da Silva LCN (2018) Use of some asteraceae plants for the treatment of wounds: from ethnopharmacological studies to scientific evidences. Front Pharmacol 9:784
Carvalho-Paulo D, Neto JBT, de Oliveira TCG, de Sousa AA, dos Reis RR, dos Santos ZA, de Lima CM, de Oliveira MA, Said NM, Freitas SF, Sosthenes MCK (2021) Microglial morphology across distantly related species: phylogenetic, environmental and age influences on microglia reactivity and surveillance states. Front Immunol 12:2330
Casadevall A, Dadachova E, Pirofski L-A (2004) Passive antibody therapy for infectious diseases. Nat Rev Microbiol 2:695–703
Chawla A (2010) Control of macrophage activation and function by PPARs. Circ Res 106:1559–1569
Chico V, Nombela I, Puente-Marín S, del Mar Ortega-Villaizan M (2018) Nucleated red blood cells contribute to the host immune response against pathogens. IntechOpen. https://doi.org/10.5772/intechopen.80545
Cichon M, Sendecka J, Gustafsson L (2003) Age-related decline in humoral immune function in Collared Flycatchers. J Evol Biol 16:1205–1210
Clark NJ (2018) Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide. Glob Ecol Biogeogr 27:744–755
Clark P, Boardman WSJ, Raidal SR (2009) Atlas of clinical avian hematology. Wiley-Blackwell, Chichester, UK
Coke RL, West GD, Hoover JP (2004) Hematology and plasma biochemistry of captive Puna Ibis (Plegadis ridgewayi). J Wildl Dis 40:141–144
Conklin JR (2011) Extreme migration and the annual cycle: individual strategies in New Zealand Bar-tailed Godwits. Ph.D. dissertation, Massey University, Palmerston North, New Zealand
Cornell A, Gibson KF, Williams TD (2017) Physiological maturity at a critical life-history transition and flight ability at fledging. Funct Ecol 31:662–670
Cornick JL, Jensen J (1992) Anesthetic management of Ostriches. J Am Vet Med Assoc 200:1661–1666
Cotter PF (2022) A microscopic study on morphology of reactive thrombocytes in duckling. J World’s Poult Res 12:142–150
Crossin GT, Phillips RA, Wynne-Edwards KE, Williams TD (2013) Postmigratory body condition and ovarian steroid production predict breeding decisions by female Gray-headed Albatrosses. Physiol Biochem Zool 86:761–768
Cuervo JJ, Møller AP, De Lope F (2007) Haematocrit is weakly related to condition in nestling Barn Swallows Hirundo rustica. Ibis 149:128–134
Cuervo JJ, Soler JJ, Avilés JM, Pérez-Contreras T, Navarro C (2011) Experimental feeding affects the relationship between hematocrit and body mass in Spotless Starling (Sturnus unicolor) nestlings. J Ornithol 152:201–206
Cuperus T, Coorens M, van Dijk A, Haagsman HP (2013) Avian host defense peptides. Dev Comp Immunol 41:352–369
Dantzler WH (1989) Comparative physiology of the vertebrate kidney. Springer, New York
Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772
Dawson RD, Bortolotti GR (1997) Are avian hematocrits indicative of condition? American Kestrels as a model. J Wildl Manag 61:1297–1306
de Angeli Dutra D, Fecchio A, Braga ÉM, Poulin R (2021) Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents. Int J Parasitol 51:877–882
de Carvalho LR, Macêdo Farias L, Nicoli JR, Silva MCF, Corsino ATSM, de Lima LA, Redondo RAF, Ferreira PCP, Pinto MEBM (2003) Dominant culturable bacterial microbiota in the digestive tract of the American Black Vulture (Coragyps atratus) and search for antagonistic substances. Braz J Microbiol 34:218–224
de Geus ED, Jansen CA, Vervelde L (2012) Uptake of particulate antigens in a nonmammalian lung: phenotypic and functional characterization of avian respiratory phagocytes using bacterial or viral antigens. J Immunol 188:4516–4526
de Kok-Mercado F, Habib M, Phelps T, Gregg L, Gailloud P (2012) National Science Foundation – visualization challenge. http://www.nsf.gov/news/special_reports/scivis/winners_2012.jsp
deGraw WA, Kern MD, King JR (1979) Seasonal changes in the blood composition of captive and free-living White-crowned Sparrows. J Comp Physiol 129:151–162
DeGroote LW, Rodewald PG (2010) Blood parasites in migrating wood-warblers (Parulidae): effects on refueling, energetic condition, and migration timing. J Avian Biol 41:147–153
Diamond JM, Karasov WH, Phan D, Carpenter FL (1986) Digestive physiology is a determinant of foraging bout frequency in hummingbirds. Nature 320:62–63
Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgūnas M, Bukauskaitė D, Zehtindjiev P, Ilieva M, Shapoval AP, Bolshakov CV, Markovets MY (2015) Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol 148:1–16
Diniz CG, Magalhaes NGM, Sousa AA, Santos C, Diniz DG, Lima CM, Oliveira MA, Paulo DC, Pereira PDC, Sherry DF, Picanco-Diniz CW (2016) Microglia and neurons in the hippocampus of migratory sandpipers. Braz J Med Biol Res 49:20155005
Donnelly RE, Sullivan KA (1998) Foraging proficiency and body condition of juvenile American Dippers. Condor 100:385–388
Dora D, Arciero E, Hotta R, Barad C, Bhave S, Kovacs T, Balic A, Goldstein AM, Nagy N (2018) Intraganglionic macrophages: a new population of cells in the enteric ganglia. J Anat 233:401–410
Dragon S, Baumann R (2003) Hypoxia, hormones, and red blood cell function in chick embryos. News Physiol Sci 18:77–82
Dufva R (1996) Blood parasites, health, reproductive success, and egg volume in female Great Tits Parus major. J Avian Biol 27:83–87
Dussan FAO (2011) Modelling of the avian immune system for the optimization of specific antibody production. Ph.D. dissertation, Universidad Nacional de Colombia, Bogotá, Colombia
Dzialowski EM, Crossley DA (2015) The cardiovascular system. In: Scanes CG (ed) Sturkie’s avian physiology. Academic Press, Cambridge, MA, pp 193–283
Ekino S, Arakawa H, Sonoda K, Noguchi K, Inui S, Yokoyama H, Kodama Y (2012) The origin of IgG-containing cells in the bursa of Fabricius. Cell Tissue Res 348:537–550
Elkins N (1983) Weather and bird behaviour. T & AD Poyser Ltd, Calton
Ellerby DJ, Henry HT, Carr JA, Buchanan CI, Marsh RL (2005) Blood flow in guinea fowl Numida meleagris as an indicator of energy expenditure by individual muscles during walking and running. J Physiol 564:631–648
Emmenegger T, Bensch S, Hahn S, Kishkinev D, Procházka P, Zehtindjiev P, Bauer S (2021) Effects of blood parasite infections on spatiotemporal migration patterns and activity budgets in a long-distance migratory passerine. Ecol Evol 11:753–762
Esbaugh AJ, Tufts BL (2006) The structure and function of carbonic anhydrase isozymes in the respiratory system of vertebrates. Respir Physiol Neurobiol 154:185–198
Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552
Faraci FM (1986) Circulation during hypoxia in birds. Comp Biochem Physiol 85:613–620
Faraci FM (1991) Adaptations to hypoxia in birds: how to fly high. Annu Rev Physiol 53:59–70
Faraci FM, Kilgore DL, Fedde MR (1984) Oxygen delivery to the heart and brain during hypoxia: Pekin Duck vs. Bar-headed Goose. Am J Physiol 247:R69–R74
Favilla AB, Costa DP (2020) Thermoregulatory strategies of diving air-breathing marine vertebrates: a review. Front Ecol Evol 8:555509
Fecchio A, Clark NJ, Bell JA, Skeen HR, Lutz HL, De La Torre GM, Vaughan JA et al (2021) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Glob Ecol Biogeogr 30:2393–2406
Fedde MR, Orr JA, Shams H, Scheid P (1989) Cardiopulmonary function in exercising Bar-headed Geese during normoxia and hypoxia. Respir Physiol 77:239–252
Ferdous F, Scott TR (2015) A comparative examination of thrombocyte/platelet immunity. Immunol Lett 163:32–39
Flajnik MF (2002) Comparative analyses of immunoglobulin genes: surprises and portents. Nat Rev Immunol 2:688
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622
Foo YZ, Nakagawa S, Rhodes G, Simmons LW (2017) The effects of sex hormones on immune function: a meta-analysis. Biol Rev 92:551–571
Fox AD, Kahlert J (2005) Changes in body mass and organ size during wing moult in non-breeding Greylag Geese Anser anser. J Avian Biol 36:538–548
Froget G, Butler PJ, Woakes AJ, Fahlman A, Kuntz G, Le Maho Y, Handrich Y (2004) Heart rate and energetics of free-ranging King Penguins (Aptenodytes patagonicus). J Exp Biol 207:3917–3926
Fuxjager MJ, Schuppe ER (2018) Androgenic signaling systems and their role in behavioral evolution. J Steroid Biochem Mol Biol 184:47–56
Gabanyi I, Muller PA, Feighery L, Oliveira TY, Costa-Pinto FA, Mucida D (2016) Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164:378–391
Gaidica M, Dantzer B (2020) Quantifying the autonomic response to stressors—one way to expand the definition of “stress” in animals. Integr Comp Biol 60:113–125
Gallardo MH, Bickham J, Honeycutt RL, Ojeda RA, Kohler N (1999) Discovery of tetraploidy in a mammal. Nature 401:341
Gallo SSM, Ederli NB, Bôa-Morte MO, Oliveira FCR (2015) Hematological, morphological and morphometric characteristics of blood cells from rhea, Rhea americana (Struthioniformes: Rheidae): a standard for Brazilian birds. Braz J Biol 75:953–962
Gannes LZ (2001) Comparative fuel use of migrating passerines: effects of fat stores, migration distance, and diet. Auk 118:665–677
Gayathri KL, Hegde SN (2006) Alteration in haematocrit values and plasma protein fractions during the breeding cycle of female pigeons, Columba livia. Anim Reprod Sci 91:133–141
Genovese KJ, He H, Swaggerty CL, Kogut MH (2013) The avian heterophil. Dev Comp Immunol 41:334–340
Ghoddusi M, Kelly WR (2004) Ultrastructure of in situ perfusion-fixed avian liver, with special reference to structure of the sinusoids. Microsc Res Tech 65:101–111
Gleeson DJ, Blows MW, Owens IPF (2005) Genetic covariance between indices of body condition and immunocompetence in a passerine bird. BMC Evol Biol 5:61
Glomski CA, Pica A (2011) The avian erythrocyte: its phylogenetic odyssey. Science Publishers, Enfield, NH
Goossens KE, Ward AC, Lowenthal JW, Bean AGD (2013) Chicken interferons, their receptors and interferon-stimulated genes. Dev Comp Immunol 41:370–376
Graham AC, Temple RM, Obar JJ (2015) Mast cells and influenza a virus: association with allergic responses and beyond. Front Immunol 6:238
Green JA, Butler PJ, Woakes AJ, Boyd IL (2003) Energetics of diving in Macaroni Penguins. J Exp Biol 206:43–57
Gregory TR (2001) The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cell Mol Dis 27:830–843
Grilo ML, Vanstreels RET, Wallace R, García-Párraga D, Braga ÉM, Chitty J, Catão-Dias JL, Madeira de Carvalho LM (2016) Malaria in penguins–current perceptions. Avian Pathol 45:393–407
Grogan KB, Fernández RJ, Barranón FJR, Espinosa JG (2007) A brief review: avian immune system. Merial, Gainesville, GA
Grubb BR (1983) Allometric relations of cardiovascular function in birds. Am J Physiol 245:H567–H572
Grubb B, Jorgensen DD, Conner M (1983) Cardiovascular changes in the exercising Emu. J Exp Zool 104:193–201
Guglielmo CG, Williams TD (2003) Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the Western Sandpiper (Calidris mauri). Physiol Biochem Zool 76:84–98
Guillaumet A, Paxton EH (2019) Evaluating community-level response to management actions across a diverse Hawaiian forest bird community. Ecol Appl 29:e01953
Gupta P, Vishnudas CK, Robin VV, Dharmarajan G (2020) Host phylogeny matters: examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India. Parasit Vectors 13:1–13
Hahn S, Bauer S, Dimitrov D, Emmenegger T, Ivanova K, Zehtindjiev P, Buttemer WA (2018) Low intensity blood parasite infections do not reduce the aerobic performance of migratory birds. Proc R Soc B 28:20172307
Halsey LG, Butler PJ, Blackburn TM (2006) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
Handrich Y, Bevan RM, Charrassin J-B, Butler PJ, Ptz K, Woakes AJ, Lage J, Le Maho Y (1997) Hypothermia in foraging King Penguins. Nature 388:64–67
Harash G, Richardson KC, Alshamy Z, Hünigen H, Hafez HM, Plendl J, Al Masri S (2019) Heart ventricular histology and microvasculature together with aortic histology and elastic lamellar structure: a comparison of a novel dual-purpose to a broiler chicken line. PLoS ONE 14:e0214158
Harr KE (2002) Clinical chemistry of companion avian species: a review. Vet Clin Pathol 31:140–151
Harris BS, O’Brien TX, Gourdie RG (2002) Coronary arteriogenesis and differentiation of periarterial Purkinje fibers. Tex Heart Inst J 29:262–270
Hart B (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12:123–137
Härtle S, Magor KE, Göbel TW, Davison F, Kaspers B (2014) Structure and evolution of avian immunoglobulins. In: Schat K, Kaspers B, Kaiser P (eds) Avian immunology. Elsevier, Amsterdam, The Netherlands, pp 103–120
Härtle S, Magor KE, Göbel TW, Davison F, Kaspers B (2022) Structure and evolution of avian immunoglobulins. In: Kaspers B, Schat KA, Göbel TW, Vervelde L (eds) Avian immunology, 3rd edn. Academic Press, London, pp 101–119
Hartman FA (1961) Locomotor mechanisms of birds. Smithson Misc Collect 143:1–91
Harvey TC, Raichle ME, Winterborn MH, Jensen J, Lassen NA (1988) Effect of carbon dioxide in acute mountain sickness: a rediscovery. Lancet 8612:639–641
Hassanpour H, Shamsabadi MG, Dehkordi IN, Dehkordi MM (2014) Normal electrocardiogram of the Laughing Dove (Spilopelia senegalensis). J Zoo Wildl Med 45:41–46
Hatch MI, Smith RJ, Owen JC (2010) Arrival timing and hematological parameters in Gray Catbirds (Dumetella carolinensis). J Ornithol 151:545–552
Hawkes LA, Batbayar N, Bishop CM, Butler PJ, Frappell PB, Meir JU, Milsom WK, Natsagdorj T, Scott GS (2017) Goose migration over the Himalayas: physiological adaptations. In: Prins HHT, Namgail T (eds) Bird migration across the Himalayas: wetland functioning amidst mountains and glaciers. Cambridge University Press, Cambridge, UK, pp 241–253
Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG, Kim KS, Lima MR, Martin L, Palinauskas V, Ricklefs R (2015) Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography 388:842–850
Hempleman SC, Powell FL, Prisk GK (1992) Avian arterial chemoreceptor responses to steps of CO2 and O2. Respir Physiol 90:325–340
Hillman SS, Hedrick MS (2015) A meta-analysis of in vivo vertebrate cardiac performance: implications for cardiovascular support in the evolution of endothermy. J Exp Biol 218:1143–1150
Hirsowitz LA, Fell K, Torrance JD (1977) Oxygen-affinity of avian blood. Respir Physiol 31:51–62
Hodges RD (1979) The blood cells. In: King AS, McLelland J (eds) Form and function in birds, vol 1. Academic Press, New York, pp 361–379
Holz PH (1999) The reptilian renal portal system – a review. Bull Assoc Reptil Amphib Vet 9:4–9
Hong JM, Kim TJ, Shin DH, Lee JS, Joo IS (2013) Cardiovascular autonomic function in lateral medullary infarction. Neurol Sci 34:1963–1969
Hõrak P, Jenni-Eiermann S, Ots I, Tegelmann L (1998) Health and reproduction: the sex-specific clinical profile of Great Tits (Parus major) in relation to breeding. Can J Zool 76:2235–2244
Huang L, Appleton JA (2016) Eosinophils in helminth infection: defenders and dupes. Trends Parasitol 32:798–807
Iannello A, Debbeche O, Martin E, Attalah LH, Samarani S, Ahmad A (2006) Viral strategies for evading antiviral cellular immune responses of the host. J Leukoc Biol 79:16–35
Ilgūnas M, Bukauskaitė D, Palinauskas V, Iezhova TA, Dinhopl N, Nedorost N, Weissenbacher-Lang C, Weissenböck H, Valkiūnas G (2016) Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malar J 15:256
Ishtiaq F (2021) Ecology and evolution of avian malaria: implications of land use changes and climate change on disease dynamics. J Indian Inst Sci 101:213–225
Jamaati H, Mortaz E, Pajouhi Z, Folkerts G, Movassaghi M, Moloudizargari M, Adcock IM, Garssen J (2017) Nitric oxide in the pathogenesis and treatment of tuberculosis. Front Microbiol 8:2008
Janeway CA, Travers P, Walport M, Capra JD (1999) Immunobiology: the immune system in health and disease. Current Biology Publications, London
Jenni-Eiermann S, Jenni L (1991) Metabolic responses to flight and fasting in night migrating passerines. J Comp Physiol B 161:465–474
Jenni-Eiermann S, Jenni L (1998) What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biologia e Conservazione Della Fauna 102:312–319
Jenni-Eiermann S, Jenni L, Kvist A, Lindstrom A, Piersma T, Visser GH (2002) Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205:2453–2460
Jensen B, Wang T, Christoffels VM, Moorman AFM (2013a) Evolution and development of the building plan of the vertebrate heart. Biochim Biophys Acta 1833:783–794
Jensen KH, Kim W, Holbrook NM, Bush JWM (2013b) Optimal concentrations in transport systems. J R Soc Interface 10:20130138
Johansen K, Berger M, Bicudo JEPW, Ruschi A, de Almeida PJ (1987) Respiratory properties of blood and myoglobin in hummingbirds. Physiol Zool 60:2689–2278
Jones PJ (1983) Haematocrit values of breeding Red-billed Queleas Quelea quelea (Aves: Ploceidae) in relation to body condition and thymus activity. J Zool 201:217–222
Josephson B (1980) Aging and sexing Snowy Owls. J Field Ornithol 51:149–160
Joyce W (2018) Flying is not for the small-hearted. J Exp Biol 221:jeb169912
Jubril AJ, Olushola G, Adekola AA, Antia R (2021) Haematological profile of naturally infected haemoparasite positive and negative Japanese Quails (Coturnix coturnix japonica). Sahel J Vet Sci 18:21–26
Kalmbach E, Griffiths R, Crane JE, Furness RW (2004) Effects of experimentally increased egg production and laying dates in the Great Skua Stercorarius skua. J Avian Biol 35:501–514
Kharin SN (2004) Depolarisation and repolarization sequences of ventricular epicardium in chickens (Gallus gallus domesticus). Comp Biochem Physiol A 137:237–244
Kilgas P, Tilgar V, Mänd R (2006) Hematological health state indices predict local survival in a small passerine bird, the Great Tit (Parus major). Physiol Biochem Zool 79:565–572
Kilgore DL, Bernstein MH, Schmidt-Nielsen K (1973) Brain temperature in a large bird, the rhea. Am J Phys 225:739–742
Kilpatrick AM, LaPointe DA, Atkinson CT, Woodworth BL, Lease JK, Reiter ME, Gross K (2006) Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii Amakihi (Hemignathus virens). Auk 123:764–774
Kilpimaa J, Alatalo RV, Siitari H (2004) Trade-offs between sexual advertisement and immune function in the Pied Flycatcher (Ficedula hypoleuca). Proc R Soc B 271:245–250
Klasing KC (1998) Avian macrophages: regulators of local and systemic immune responses. Poult Sci 77:983–989
Klika E, Scheuermann DW, De Groodt-Lasseel MHA, Bazantova I, Switka A (1996) Pulmonary macrophages in birds (Barn Owl, Tyto tyto alba), domestic fowl (Gallus gallus f. domestica), quail (Coturnix coturnix), and pigeons (Columba livia). Anat Rec 246:87–97
Knower Stockard T, Heil J, Meir JU, Sato K, Ponganis KV, Ponganis PJ (2005) Air sac PO2 and oxygen depletion during dives of Emperor Penguins. J Exp Biol 208:2973–2980
Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60:19–32
Kozłowski J, Czarnołęski M, François-Krassowska A, Maciak S, Pis T (2010) Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals. Biol Lett 6:792–796
Kozlu T, Sari EK, Bozkurt YA, Altunay H (2011) A comparative study on the histological structure of the spleen in the Ostrich (Struthio camelus), the kestrel (Falco tinnunculus) and the Osprey (Pandion haliaetus). Acta Biol Hung 62:113–121
Kranen RW, Van Kuppevelt TH, Goedhart HA, Veerkamp CH, Lambooy E, Veerkamp JH (1999) Hemoglobin and myoglobin content in muscles of broiler chickens. Poult Sci 78:467–476
Kroneman J, Faber J, Wolschrijn C, Christoffels V, Jensen B (2019) Comparative analysis of avian hearts provides little evidence for variation among species with acquired endothermy. J Morphol 280:395–410
Laaksonen T, Fargallo JA, Korpimäki E, Lyytinen S, Valkama J, Pöyri V (2004) Year-and sex-dependent effects of experimental brood sex ratio manipulation on fledging condition of Eurasian Kestrels. J Anim Ecol 73:342–352
Laguë SL (2017) High-altitude champions: birds that live and migrate at altitude. J Appl Physiol 123:942–950
Laguë SL, Chua B, Alza L, Scott GR, Frappell PB, Zhong Y, Farrell AP, McCracken KG, Wang Y, Milsom WK (2017) Divergent respiratory and cardiovascular responses to hypoxia in Bar-headed Geese and Andean birds. J Exp Biol 220:4186–4194
Landys-Ciannelli MM, Jukema J, Piersma T (2002) Blood parameter changes during stopover in a long-distance migratory shorebird, the Bar-tailed Godwit Limosa lapponica taymyrensis. J Avian Biol 33:451–455
Lansford R, Rugonyi S (2020) Follow me! a tale of avian heart development with comparisons to mammal heart development. J Cardiovasc Dev Dis 7:8
Larson TA (2018) Sex steroids, adult neurogenesis, and inflammation in CNS homeostasis, degeneration, and repair. Front Endocrinol 9:205
Lasiewski RC, Calder WA (1971) A preliminary allometric analysis of respiratory variables in resting birds. Respir Physiol 11:152–166
Lee-Cruz L, Cunningham AA, Martínez P, Cruz M, Goodman SJ, Hamer KC (2016) Prevalence of Haemoproteus sp. in Galápagos Blue-footed Boobies: effects on health and reproduction. Parasitol Open 2:e1
Lefranc MP, Lefranc G (2020) Immunoglobulins or antibodies: IMGT® bridging genes, structures and functions. Biomedicines 8:319
Lenfant C, Johansen K, Torrance JD (1970) Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9:277–286
Leon-Velarde F, Sanchez J, Bigard AX, Brunet A, Lesty C, Monge C (1993) High altitude tissue adaptation in Andean Coots: capillarity, fibre area, fibre type and enzymatic activities of skeletal muscle. J Comp Physiol B Biochem Syst Environ Physiol 164:52–58
Li MO, Wan YY, Sanjabi S, Robertson A-KL, Flavell RA (2006) Transforming growth factor-β regulation of immune responses. Annu Rev Immunol 24:99–146
Liknes ET, Swanson DL (2011) Phenotypic flexibility of body composition associated with seasonal acclimatization in passerine birds. J Therm Biol 36:363–370
Lill A, Rajchl K, Yachou-Wos L, Johnstone CP (2013a) Are haematocrit and haemoglobin concentration reliable body condition indicators in nestlings: the Welcome Swallow as a case study. Avian Biol Res 6:57–66
Lill A, Yachou-Wos L, Johnstone CP (2013b) Are haematocrit and haemoglobin concentration reliable indicators of body condition in adult Welcome Swallows. Emu 113:93–98
Linde A, Ross CR, Davis EG, Dib L, Blecha F, Melgarejo T (2008) Innate immunity and host-defense peptides in veterinary medicine. J Vet Intern Med 22:247–265
Lindstrom A, Kvist A, Piersma T, Dekinga A, Dietz MW (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight. J Exp Biol 203:913–919
Lindström KM, Foufopoulos J, Pärn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proc R Soc B 271:1513–1519
Lobato DN, Braga EM, Belo NDO, Antonini Y (2011) Hematological and parasitological health conditions of the Pale-breasted Thrush (Turdus leucomelas) (Passeriformes: Turdidae) in southeastern Brazil. Zoologia (Curitiba) 28:771–776
Lownie TJR, Jubinville I, Williams TD, Phillips RA, Crossin GT (2022) Varying aerobic capacity in relation to breeding stage and reproductive success in giant petrels (Macronectes spp.). Comp Biochem Physiol A 266:111155
Lu Y, James TN, Bootsma M, Terasaki F (1993) Histological organization of the right and left atrioventricular valves of the chicken heart and their relationship to the atrioventricular Purkinje ring and the middle bundle branch. Anat Rec 235:74–86
Lu M, Lee Y, Lillehoj HS (2023) Evolution of developmental and comparative immunology in poultry: the regulators and the regulated. Dev Comp Immunol 138:104525
Lutfullah G, Abid Ali S, Abbasi A (2005) Molecular mechanism of high altitude respiration: primary structure of a minor hemoglobin component from Tufted Duck (Aythya fuligula). Biochem Biophys Res Commun 326:123–130
Lutz PL (1980) On the oxygen affinity of bird blood. Am Zool 20:187–198
Machida N, Aohagi Y (2001) Electrocardiography, heart rates, and heart weights of free-living birds. J Zoo Wildl Med 32:47–54
Madej JP, Chrząstek K, Piasecki T, Wieliczko A (2013) New insight into the structure, development, functions and popular disorders of bursa Fabricii. Anat Histol Embryol 42:321–331
Maginniss LA, Bernstein MH, Deitch MA, Pinshow B (1997) Effects of chronic hypobaric hypoxia on blood oxygen binding in pigeons. J Exp Zool 277:293–300
Maher MA (2019) Descriptive anatomy of hepatic and portal veins with special reference to biliary duct system in broiler chickens (Gallus gallus domesticus): a recent illustration. Braz J Poult Sci 21:1–12
Maina JN (2015) The design of the avian respiratory system: development, morphology and function. J Ornithol 156:41–63
Makanya AN (2017) Development of the airways and the vasculature in the lungs of birds. In: Maina JN (ed) The biology of the avian respiratory system. Springer, Cham, Switzerland, pp 147–178
Martin LB (2009) Stress and immunity in wild vertebrates: timing is everything. Gen Comp Endocrinol 163:70–76
Martínez-de la Puente J, Santiago-Alarcon D, Palinauskas V, Bensch S (2021) Parasite of the month: Plasmodium relictum. Trends Parasitol 37:355–356
Marzal A, De Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545
Mathieu-Costello O, Agey PJ (1997) Chronic hypoxia affects capillary density and geometry in pigeon pectoralis muscle. Respir Physiol 109:39–52
Matthieu-Costello O, Suarez RK, Hochachka PW (1992) Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle. Respir Physiol 89:113–132
Maxwell MH, Robertson GW (1995) The avian basophilic leukocyte: a review. Worlds Poult Sci J 51:307–325
McKibben JS, Harrison GJ (1986) Clinical anatomy with emphasis on the Amazon Parrot. In: Harrison GJ, Harrison LR (eds) Clinical avian medicine and surgery. W. B. Saunders, Philadelphia, PA, pp 31–66
Medeiros MCI, Hamer GL, Ricklefs RE (2013) Host compatibility rather than vector–host-encounter rate determines the host range of avian Plasmodium parasites. Proc R Soc B 280:20122947
Meir JU, Milsom WK (2013) High thermal sensitivity of blood enhances oxygen delivery in the high-flying Bar-headed Goose. J Exp Biol 216:2172–2175
Meir JU, Stockard TK, Williams CL, Ponganis KV, Ponganis PJ (2008) Heart rate regulation and extreme bradycardia in diving Emperor Penguins. J Exp Biol 211:1169–1179
Meir JU, York JM, Chua BA, Jardine W, Hawkes LA, Milsom WK (2019) Reduced metabolism supports hypoxic flight in the high-flying Bar-headed Goose (Anser indicus). eLife 8:e44986
Michel CC, Curry FE (1999) Microvascular permeability. Physiol Rev 79:703–761
Midtgård U (1982) Patterns in the blood vascular system in the pelvic limb of birds. J Zool 196:545–567
Miguel RDS, Reinaldo RCPS, Fraga KB, Galvão APO, Silva JAC, Xavier JE, Magalhães CP (2014) Morphological and morphometric analysis from the heart of Caracara plancus (Carcará). J Morphol Sci 31:225–227
Milenkaya O, Weinstein N, Legge S, Walters JR (2013) Variation in body condition indices of Crimson Finches by sex, breeding stage, age, time of day, and year. Conserv Physiol 1:cot020
Milsom WK, Johansen K, Millard RW (1973) Blood respiratory properties in some Antarctic birds. Condor 75:472–474
Minias P (2014) High glucose concentrations are associated with symptoms of mild anaemia in Whiskered Terns: consequences for assessing physiological quality in birds. J Ornithol 155:1067–1070
Minias P (2015) The use of haemoglobin concentrations to assess physiological condition in birds: a review. Cons Physiol 3:cov007
Minias P (2020) Ecology and evolution of blood oxygen-carrying capacity in birds. Am Nat 195:788–801
Minias P, Kaczmarek K, Wlodarczyk R, Janiszewski T (2013) Hemoglobin concentrations in waders vary with their strategies of migration: a comparative analysis. Comp Biochem Physiol 165:7–12
Minias P, Wlodarczyk R, Plasecka A, Kaczmarek K, Janiszewski (2014) Ecological, physiological, and morphological correlates of blood hemoglobin concentration in a migratory shorebird. Physiol Biochem Zool 87:771–781
Møller AP (1990) Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis. J Evol Biol 3:319–328
Møller AP, Erritzoe J (1996) Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50:2066–2072
Møller AP, Erritzoe J (2000) Predation against birds with low immunocompetence. Oecologia 122:500–504
Monaghan P, Nager RG, Houston DC (1998) The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc R Soc B 265:1731–1735
Moreno J, Sanz JJ, Arriero E (1999) Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female Pied Flycatchers Ficedula hypoleuca. Proc R Soc B 266:1105–1109
Moreno J, Yorio P, Garcia-Borboroglu P, Potti J, Villar S (2002) Health state and reproductive output in Magellanic Penguins (Spheniscus magellanicus). Ethol Ecol Evol 14:19–28
Morrison ES, Ardia DR, Clotfelter ED (2009) Cross-fostering reveals sources of variation in innate immunity and hematocrit in nestling Tree Swallows Tachycineta bicolor. J Avian Biol 40:573–578
Morton ML (1994) Hematocrits in montane sparrows in relation to reproductive schedule. Condor 96:119–126
Müller MS, Vyssotski AL, Yamamoto M, Yoda K (2017) Heart rate variability reveals that a decrease in parasympathetic (‘rest-and-digest’) activity dominates autonomic stress responses in a free-living seabird. Comp Biochem Physiol A 212:117–126
Murrant CL, Sarelius IH (2015) Local control of blood flow during active hyperaemia: what kinds of integration are important? J Physiol 593:4699–4711
Mutua MP, Muya S, Gicheru MM (2016) Protective roles of free avian respiratory macrophages in captive birds. Biol Res 49:29
Nager RG, Monaghan P, Houston DC (2001) The cost of egg production: increased egg production reduces future fitness in gulls. J Avian Biol 32:159–166
Narkkong N-A, Aengwanich W, Tanomthong A (2010) Morphological observations of the thrombocyte of White-bellied Sea Eagle Haliaeetus leucogaster. Comp Clin Pathol 19:263–267
Natarajan C, Jendroszek A, Kumar A, Weber RE, Tame JR, Fago A, Storz JF (2018) Molecular basis of hemoglobin adaptation in the high-flying Bar-headed Goose. PLoS Genet 14:e1007331
Navarro J, Gonzalez-Solis J, Viscor G (2007) Nutritional and feeding ecology in Cory’s Shearwater Calonectris diomedea during breeding. Mar Ecol Prog Ser 351:261–271
Navarro J, Votier SC, Phillips RA (2014) Diving capabilities of diving petrels. Polar Biol 37:897–901
Navia A, Tejos R, Yañez R, Cuadra A, Dagnino B (2021) Optimizing the chicken wing anatomy: nomenclature review and description for microsurgery and supermicrosurgery training. J Reconstr Microsurg 38:e1–e2
Nespolo RF, González-Lagos C, Solano-Iguaran JJ, Elfwing M, Garitano-Zavala A, Mañosa S, Alonso JC, Altimiras J (2018) Aerobic power and flight capacity in birds: a phylogenetic test of the heart-size hypothesis. J Exp Biol 221:jeb162693
Nganvongpanit K, Kaewkumpai P, Kochagul V, Pringproa K, Punyapornwithaya V, Mekchay S (2020) Distribution of melanin pigmentation in 33 organs of Thai black-bone chickens (Gallus gallus domesticus). Animals 10:777
Norte AC, Ramos JA, Sampaio HL, Sousa JP, Sheldon BC (2010) Physiological condition and breeding performance of the Great Tit. Condor 112:79–86
O’Dwyer TW, Buttemer WA, Priddel DM (2007) Differential rates of offspring provisioning in Gould’s Petrels: are better feeders better breeders? Aust J Zool 55:155–160
O’Toole ET, Hantgan RR, Lewis JC (1994) Localization of fibrinogen during aggregation of avian thrombocytes. Exp Mol Pathol 61:175–190
Odum EP (1945) The heart rate of small birds. Science 101:153–154
Oglesbee BL, Hamlin RL, Klingaman H, Cianciola J, Hartman SP (2001) Electrocardiographic reference values for macaws (Ara species) and cockatoos (Cacatua species). J Avian Med Surg 15:17–22
Oppliger A, Christe P, Richner H (1996) Clutch size and malaria resistance. Nature 381:565
Ordway GA, Garry DJ (2004) Myoglobin: an essential hemoprotein in striated muscle. J Exp Biol 207:3441–3446
Owen JC (2011) Collecting, processing, and storing avian blood: a review. J Field Ornithol 82:339–354
Owen JC, Moore FR (2006) Seasonal differences in immunological condition of three species of thrushes. Condor 108:389–398
Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp Parasitol 120:372–380
Palm EC, Newman SH, Prosser DJ, ** migratory flyways in Asia using dynamic Brownian bridge movement models. Mov Ecol 3:3
Paul S, Lal G (2017) The molecular mechanism of natural killer cells function and its importance in cancer immunotherapy. Front Immunol 8:1124
Peguero JG, Presti SL, Perez J, Issa O, Brenes JC, Tolentino A (2017) Electrocardiographic criteria for the diagnosis of left ventricular hypertrophy. J Am Coll Cardiol 69:1694–1703
Pendl H, Tizard I (2016) Immunology. In: Speer BL (ed) Current therapy in avian medicine and surgery. Elsevier, St. Louis, MO, pp 400–432
Pennycuick CJ (1998) Computer simulation of fat and muscle burn in long-distance bird migration. J Theor Biol 191:47–61
Perni S, Iyer VR, Franzini-Armstrong C (2012) Ultrastructure of cardiac muscle in reptiles and birds: optimizing and/or reducing the probability of transmission between calcium release units. J Muscle Res Cell Motil 33:145–152
Peters GW, Steiner DA, Rigoni JA, Mascilli AD, Schnepp RW, Thomas SP (2005) Cardiorespiratory adjustments of homing pigeons to steady wind tunnel flight. J Exp Biol 208:3109–3120
Petit M, Clavijo-Baquet S, Vézina F (2017) Increasing winter maximal metabolic rate improves intrawinter survival in small birds. Physiol Biochem Zool 90:166–177
Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80:623–631
Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415
Piersma T, van der Velde M (2012) Dutch House Martins Delichon urbicum gain blood parasite infections over their lifetime, but do not seem to suffer. J Ornithol 153:907–912
Piersma T, Everaarts JM, Jukema J (1996) Build-up of red blood cells in refueling Bar-tailed Godwits in relation to individual migratory quality. Condor 98:363–370
Ponganis PJ (2015) Diving physiology of marine mammals and seabirds. Cambridge University Press, Cambridge, UK
Ponganis PJ, Stockard TK, Meir JU, Williams CL, Ponganis KV, Van Dam RP, Howard R (2007) Returning on empty: extreme blood O2 depletion underlies dive capacity of Emperor Penguins. J Exp Biol 210:4279–4285
Ponganis PJ, Meir JU, Williams CL (2010) Oxygen store depletion and the aerobic dive limit in Emperor Penguins. Aquat Biol 8:237–245
Potti J (2007) Variation in the hematocrit of a passerine bird across life stages is mainly of environmental origin. J Avian Biol 38:726–730
Potti J, Moreno J, Merino S, Frías O, Rodríguez R (1999) Environmental and genetic variation in the haematocrit of fledgling Pied Flycatchers Ficedula hypoleuca. Oecologia 120:1–8
Powell C, Lill A, Johnstone CP (2013) Body condition and chronic stress in urban and rural Noisy Miners. Open Ornithol J 6:25–31
Pretorius E, Vieira WA, Oberholzer HM, Auer REJ (2009) Comparative scanning electron microscopy of platelets and fibrin networks of human and different animals. Int J Morphol 27:69–76
Prosheva VI, Kaseva NN (2016) Location and functional characterization of the right atrioventricular pacemaker ring in the adult avian heart. J Morphol 277:363–369
Protasi F, Sun X-H, Franzini-Armstrong C (1996) Formation and maturation of the calcium release apparatus in develo** and adult avian myocardium. Dev Biol 173:265–278
Pryke SR, Rollins LA (2012) Mothers adjust offspring sex to match the quality of the rearing environment. Proc R Soc B 279:4051–4057
Pryke SR, Rollins LA, Griffith SC (2011) Context-dependent sex allocation: constraints on the expression and evolution of maternal effects. Evolution 65:2792–2799
Pryke SR, Astheimer LB, Griffith SC, Buttemer WA (2012) Covariation in life-history traits: differential effects of diet on condition, hormones, behavior, and reproduction in genetic finch morphs. Am Nat 179:375–390
Qureshi MA, Heggen CL, Hussain I (2000) Avian macrophage: effector functions in health and disease. Dev Comp Immunol 24:103–119
Ramírez-Plascencia O, Acosta-Hernández ME, García-García F (2019) The role of neuroglobin in brain function and sleep–wake cycle. In: Murillo-Rodriguez E (ed) The behavioral, molecular, pharmacological, and clinical basis of the sleep-wake cycle. Academic Press, New York, NY, pp 85–102
Ramiro AR, Nussenzweig MC (2004) Aid for AID. Nature 430:980–981
Ramsis MN, El-Gammal SM, Abo-El-Sooud K, Swielim GA (2021) Anatomical studies on the arterial blood supply of the pelvic limb of geese. Adv Anim Vet Sci 9:604–614
Ratcliffe MJH, Härtle S (2014) B cells, the bursa of Fabricius and the generation of antibody repertoires. In: Schat KA, Kaspers B, Kaiser P (eds) Avian immunology. Academic Press, Paris, France, pp 65–89
Rehman ZU, Meng C, Umar S, Mahrose KM, Ding C, Munir M (2017) Mast cells and innate immunity: master troupes of the avian immune system. Worlds Poult Sci J 73:621–632
Resano-Mayor J, Hernández-Matías A, Real J, Parés F, Moleón M, Mateo R, Ortiz-Santaliestra ME (2016) The influence of diet on nestling body condition of an apex predator: a multi-biomarker approach. J Comp Physiol B 186:343–362
Ricklefs RE (1992) Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci USA 89:4722–4725
Rodman GP, Ebaugh FG Jr, Spivey Fox MR, Chambers DM (1957) The life span of the red blood cell and the red blood cell volume in the chicken, pigeon and duck as estimated by the use of Na2Cr51O4. Blood 12:355–366
Romero LM, Gormally BMG (2019) How truly conserved is the “well-conserved” vertebrate stress response? Integr Comp Biol 59:273–281
Rothenberg ME, Hogan SP (2006) The eosinophil. Annu Rev Immunol 24:147–174
Ruiz G, Rosenmann M, Fernando Novoa F, Sabat P (2002) Hematological parameters and stress index in Rufous-collared Sparrows dwelling in urban environments. Condor 104:162–166
Sakaluk SK, Wilson AJ, Bowers EK, Johnson LS, Masters BS, Johnson BGP, Vogel LA, Forsman AM, Thompson CF (2014) Genetic and environmental variation in condition, cutaneous immunity, and haematocrit in House Wrens. BMC Evol Biol 14:242
Santhakumar D, Rubbenstroth D, Martinez-Sobrido L, Munir M (2017) Avian interferons and their antiviral effectors. Front Immunol 8:49
Santiago-Alarcon D, Palinauskas V, Schaefer HM (2012) Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev 87:928–964
Scanes CG (2015) Blood. In: Sturkie’s avian physiology, 6th edn. Elsevier, New York
Schepelmann K (2005) Erythropoietic bone marrow in the pigeon: development of its distribution and volume during growth and pneumatization of bones. J Morphol 203:21–34
Scheuerlein A, Ricklefs RE (2004) Prevalence of blood parasites in European passeriform birds. Proc R Soc B 271:1363–1370
Schoenle LA, Kernbach M, Haussmann MF, Bonier F, Moore IT (2017) An experimental test of the physiological consequences of avian malaria infection. J Anim Ecol 86:1483–1496
Scholander PF (1940) Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter 22:1–131
Scott MG, Hancock RE (2000) Cationic antimicrobial peptides and their multifunctional role in the immune system. Crit Rev Immunol 20:407–431
Scoville SA, Doherty JP (2017) Baseline hematocrit values in birds: an important tool for monitoring exposure to polycyclic aromatic hydrocarbons. Environ Pollut Protect 2:145–152
Sedlmayr JC, Witmer LM (2002) Rapid technique for imaging the blood vascular system using stereoangiography. Anat Rec 267:330–336
Seymour RS, Blaylock AJ (2000) The principle of Laplace and scaling of ventricular wall stress and blood pressure in mammals and birds. Physiol Chem Zool 73:389–405
Sheridan JA, Beissinger SR, Hughes CR (2004) Weak association between measures of health and reproductive success in Green-rumped Parrotlets (Forpus passerinus) in Venezuela. Auk 121:717–725
Shiels HA (2022) Avian cardiomyocyte architecture and what it reveals about the evolution of the vertebrate heart. Philos Trans R Soc B 377:20210332
Shiels HA, Galli GLJ (2014) The sarcoplasmic reticulum and the evolution of the vertebrate heart. Physiology 29:456–469
Signore AV, Tift MS, Hoffmann FG, Schmitt TL, Moriyama H, Storz JF (2021) Evolved increases in hemoglobin-oxygen affinity and Bohr effect coincided with the aquatic specialization of penguins. Proc Natl Acad Sci USA 118:e2023936118
Sirkiä PM, Qvarnström A (2021) Adaptive coloration in Pied Flycatchers (Ficedula hypoleuca)—the devil is in the detail. Ecol Evol 11:1501–1525
Smith FM (1994) Blood pressure regulation by aortic baroreceptors in birds. Physiol Zool 67:1402–1425
Smith KD, Barber CA (2012) Hematocrit does not indicate condition in nestling or adult European Starlings. Wilson J Ornithol 124:788–792
Smith KG, Hunt JL (2004) On the use of spleen mass as a measure of avian immune system strength. Oecologia 138:28–31
Smith FM, West NH, Jones DR (2000) The cardiovascular system. In: Whittow GC (ed) Sturkie's avian physiology, 5th edn. Academic Press, San Diego, CA, pp 41–231
Snyder GK, Sheafor BA (1999) Red blood cells: centerpiece in the evolution of the vertebrate circulatory system. Am Zool 39:189–198
Sol D, Jovani R, Torres J (2003) Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135(542):547
Šolc D (2007) The heart and heart conducting system in the kingdom of animals: a comparative approach to its evolution. Exp Clin Cardiol 12:113
Sommer JR (1995) Comparative anatomy: in praise of a powerful approach to elucidate mechanisms translating cardiac excitation into purposeful contraction. J Mol Cell Cardiol 27:19–35
Sommer JR, Johnson EA (1969) Cardiac muscle: a comparative ultrastructural study with special references to frog and chicken hearts. Zeit Zellforsch Micro Anat 98:437–468
Soulsbury CD, Dobson J, Deeming DC, Minias P (2022) Energetic lifestyle drives size and shape of avian erythroctyes. Integr Comp Biol 62:71–80
Spronk HMH, Govers-Riemslag JWP, ten Cate H (2003) The blood coagulation system as a molecular machine. BioEssays 25:1220–1228
Stephenson R, Evans BK, Jones DR (1996) Physiological mechanisms for underwater endurance: Canada Goose (Branta canadensis) versus Pekin Duck (Anas platyrhynchos). J Comp Physiol B 166:46–54
Stephenson A, Adams JW, Vaccarezza M (2017) The vertebrate heart: an evolutionary perspective. J Anat 231:787–797
Stockard TK, Heil J, Meir JU, Sato K, Ponganis KV, Ponganis PJ (2005) Air sac PO2 and oxygen depletion during dives of Emperor Penguins. J Exp Biol 208:2973–2980
Storz JF (2007) Hemoglobin function and physiological adaptation to hypoxia in high-altitude mammals. J Mammal 88:24–31
Sutcliffe JF (1986) Black fly host location: a review. Can J Zool 64:1041–1053
Svoboda O, Bartunek P (2015) Origins of the vertebrate erythro/megakaryocytic system. Biomed Res Int 2015:632171
Swanson DL (1990) Seasonal variation of vascular oxygen transport in the Dark-eyed Junco. Condor 92:62–66
Swanson DL, Vézina F (2015) Environmental, ecological and mechanistic drivers of avian seasonal metabolic flexibility in response to cold winters. J Ornithol 156:377–388
Tadjalli M, Ghazi SR, Parto P (2009) Gross anatomy of the heart in Ostrich (Struthio camelus). Iran J Vet Res 10:21–27
Taha AA, Abdel-Magied EM, King AS (1983) Ultrastructure of aortic and pulmonary baroreceptors in the Domestic Fowl. J Anat 137:197–207
Takekawa JY, Heath SR, Douglas DC, Perry WM, Javed S, Newman SH, Suwal RN, Rahmani AR, Choudhury BC, Prosser DJ, Yan B, Hou Y, Batbayar N, Natsagdorj T, Bishop CM, Butler PJ, Frappell PB, Milsom WK, Scott GR, Hawkes LA, Wikelski M (2009) Geographic variation in Bar-headed Geese Anser indicus: connectivity of wintering areas and breeding grounds across a broad front. Wildfowl 59:100–123
Tavernier P, Sagesse M, Van Wettere A, Redig P (2005) Malaria in an Eastern Screech Owl (Otus asio). Avian Dis 49:433–435
Tizard I (2002) The avian antibody response. Semin Avian Exotic Pet Med 11:2–14
Townsend AK, Wheeler SS, Freund D, Sehgal RNM, Boyce WM (2018) Links between blood parasites, blood chemistry, and the survival of nestling American Crows. Ecol Evol 8:8779–8790
Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3:133–146
Valkiūnas G (2005) Avian malaria parasites and other Haemosporidia. CRC Press, Boca Raton, FL
Valkiūnas G, Iezhova TA (2018) Keys to the avian malaria parasites. Malar J 17:212
van Oers K, Richardson DS, Sæther SA, Komdeur J (2010) Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection? J Ornithol 151:69–77
Vervelde L, Matthijs MGR, Van Haarlem DA, de Wit JJ, Jansen CA (2013) Rapid NK-cell activation in chicken after infection with infectious bronchitis virus M41. Vet Immunol Immunopathol 151:337–341
Vinkler M, Schnitzer J, Munclinger P, Votýpka J, Albrecht T (2010) Haematological health assessment in a passerine with extremely high proportion of basophils in peripheral blood. J Ornithol 151:841–849
Wagner EC, Stables CA, Williams TD (2008) Hematological changes associated with egg production: direct evidence for changes in erythropoiesis but a lack of resource dependence? J Exp Biol 211:2960–2968
Warr GW, Magor KE, Higgins DA (1995) IgY: clues to the origins of modern antibodies. Immunol Tod 16:392–398
Warrington R, Watson W, Kim HL, Antonetti FR (2011) An introduction to immunology and immunopathology. Allergy Asthma Clin Immunol 7:S1
Weber RE, Jessen T-H, Malte H, Tame J (1993) Mutant hemoglobins alpha 119-Ala and beta 55-Ser: functions related to high-altitude respiration in geese. J Appl Physiol 75:2646–2655
West NH, Langille BL, Jones DR (1981) Cardiovascular system. In: King AS, McLelland J (eds) Form and function in birds. Academic Press, New York, pp 235–339
Westerdahl H, Waldenstrom J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc B 272:1511–1518
Westneat DF, Birkhead TR (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc B 265:1065–1073
Wigley P, Kaiser P (2003) Avian cytokines in health and disease. Braz J Poult Sci 5:1–14
Wigley P, Hulme SD, Barrow PA (1999) Phagocytic and oxidative burst activity of chicken thrombocytes to Salmonella, Escherichia coli and other bacteria. Avian Pathol 28:567–572
Williams TD (2012) Physiological adaptations for breeding in birds. Princeton Univ Press, Princeton, NJ
Williams TD, Challenger WO, Christians JK, Evanson M, Love O, Vezina F (2004) What causes the decrease in haematocrit during egg production? Funct Ecol 18:330–336
Wong AD, Ye M, Levy AF, Rothstein JD, Bergles DE, Searson PC (2013) The blood-brain barrier: an engineering perspective. Front Neuroeng 6:7
Woodbury RA, Hamilton WF (1937) Blood pressure studies in small animals. Am J Physiol 119:663–674
Wright TJ (2014) Myoglobin adaptation in terrestrial and diving birds and mammals. Ph.D. dissertation, Texas A&M University, College Station, TX
Wright AK, Ponganis KV, McDonald BI, Ponganis PJ (2014) Heart rates of Emperor Penguins diving at sea: implications for oxygen store management. Mar Ecol Prog Ser 496:85–98
Wu L, Sun Y, Li M, Li Y, Yao Y, Liu X, Hao Y, Li D, Wu Y (2016) Molecular cloning and 3D structure prediction of myoglobin and cytoglobin in Eurasian Tree Sparrow Passer montanus. J Ornithol 157:493–504
Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496:445–455
Yamamoto M, Kato A, Ropert-Coudert Y, Kuwahara M, Hayama S, Naito Y (2009) Evidence of dominant parasympathetic nervous activity of Great Cormorants (Phalacrocorax carbo). J Comp Physiol A 195:365–373
Yang D, Wan Y (2019) Molecular determinants for the polarization of macrophage and osteoclast. Semin Immunopathol 41:551–563
Yap KN, Tsai OHI, Williams TD (2019) Haematological traits co-vary with migratory status, altitude and energy expenditure: a phylogenetic, comparative analysis. Sci Rep 9:6351
Yatime L, Bajic G, Schatz-Jakobsen JA, Andersen GR (2016) Complement regulators and inhibitors in health and disease: a structural perspective. In: Howard KA, Vorup-Jensen T, Peer D (eds) Nanomedicine. Springer, New York, pp 13–42
Yogamaya B, Prafulla KM (2016) Haematology of Grey Heron (Ardea cinerea) and Black Crowned Night Heron (Nycticorax nycticorax) oi Chilika Wetland. Indian J Biol 3:151–156
Zaefarian F, Abdollahi MR, Cowieson A, Ravindran V (2019) Avian liver: the forgotten organ. Animals 9:63
Zepeda Mendoza ML, Roggenbuck M, Vargas KM, Hansen LH, Brunak S, Gilbert MTP, Sicheritz-Pontén T (2018) Protective role of the vulture facial skin and gut microbiomes aid adaptation to scavenging. Acta Vet Scand 60:61
Zhang X, Calvert RA, Sutton BJ, Doré KA (2017) IgY: a key isotype in antibody evolution. Biol Rev 92:2144–2156
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2023 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Ritchison, G. (2023). Cardiovascular and Immune Systems. In: In a Class of Their Own. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-031-14852-1_6
Download citation
DOI: https://doi.org/10.1007/978-3-031-14852-1_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-14851-4
Online ISBN: 978-3-031-14852-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)