Cardiovascular and Immune Systems

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In a Class of Their Own

Part of the book series: Fascinating Life Sciences ((FLS))

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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.

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References

  • Abdalla MA, King AS (1975) The functional anatomy of the pulmonary circulation of the domestic fowl. Respir Physiol 23:267–290

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Adair BM (2000) Immunopathogenesis of chicken anemia virus infection. Dev Comp Immunol 24:247–255

    Article  CAS  PubMed  Google Scholar 

  • Akester AR (1964) Radiographic studies of the renal portal system in the Domestic Fowl (Gallus domesticus). J Anat 98:365–376

    CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Khalaifah H, Al-Nasser A (2018) Cytokines as effective elements of the avian immune system. J Microbiol Genet 2018:2574–7371

    Google Scholar 

  • Al-Saffar TM, Al-Mawla ED (2008) Some hematological changes in chickens infected with ectoparasites in Mosul. Iraqi J Vet Sci 22:95–100

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Altshuler DL, Dudley R (2002) The ecological and evolutionary interface of hummingbird flight physiology. J Exp Biol 205:2325–2336

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Anderson HL, Brodsky IE, Mangalmurti NS (2018) The evolving erythrocyte: red blood cells as modulators of innate immunity. J Immunol 201:1343–1351

    Article  CAS  PubMed  Google Scholar 

  • Apanius V (1998) Stress and immune defense. Adv Study Behav 27:133–153

    Article  Google Scholar 

  • Arad Z, Midtgard U, Bernstein MH (1989) Thermoregulation in Turkey Vultures: vascular anatomy, arteriovenous heat exchange, and behavior. Condor 91:505–514

    Article  Google Scholar 

  • Asghar M, Hasselquist D, Bensch S (2011) Are chronic avian haemosporidian infections costly in wild birds? J Avian Biol 42:530–537

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ashley NT, Weil ZM, Nelson RJ (2012) Inflammation: mechanisms, costs, and natural variation. Annu Rev Ecol Evol Syst 43:385–406

    Article  Google Scholar 

  • Atkinson CT, LaPointe DA (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg 23:53–63

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Atkinson CT, Thomas NJ, Hunter DB (eds) (2009) Parasitic diseases of wild birds. Wiley, New York

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bairlein F, Totzke U (1992) New aspects on migratory physiology of trans-Saharan passerine migrants. Ornis Scand 23:244–250

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Banerjee V, Banerjee M (1977) Variations of erythrocyte number and haemoglobin content of a migratory bird: Philomachus pugnax (Linnaeus). Zool Anz 199:261–264

    CAS  Google Scholar 

  • Barnas GM, Rautenberg W (1990) Shivering and cardiorespiratory responses during normocapnic hypoxia in the pigeon. J Appl Physiol 68:84–87

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Barske J, Eghbali M, Kosarussavadi S, Choi E, Schlinger BA (2019) The heart of an acrobatic bird. Comp Biochem Physiol A 228:9–17

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bernstein MH (1989) Temperature and oxygen supply in the avian brain. In: Wood SC (ed) Comparative pulmonary physiology. Dekker, New York, pp 343–368

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bischoff SC (2009) Physiological and pathophysiological functions of intestinal mast cells. Semin Immunopathol 31:185–205

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bishop CM, Butler PJ (1995) Physiological modeling of oxygen consumption in birds during flight. J Exp Biol 198:2153–2163

    Article  CAS  PubMed  Google Scholar 

  • Black CP, Tenney SM (1980) Oxygen transport during progressive hypoxia in high-altitude and sea-level waterfowl. Respir Physiol 39:217–239

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Boggs DF, Butler PJ, Wallace SE (1998) Differential air sac pressures in diving Tufted Ducks (Aythya fuligula). J Exp Biol 201:2665–2668

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bordel R, Haase E (1993) Effects of flight on blood parameters in homing pigeons. J Comp Physiol B 163:219–224

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Boström JE, Dimitrova M, Canton C, Håstad O, Qvarnström A, Ödeen A (2016) Ultra-rapid vision in birds. PLoS ONE 11:e0151099

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Burggren WW (2013) Cardiovascular development and angiogenesis in the early vertebrate embryo. Cardiovasc Eng Technol 4:234–245

    Article  PubMed  Google Scholar 

  • Burmeister AR, Marriott I (2018) The interleukin-10 family of cytokines and their role in the CNS. Front Cell Neurosci 12:458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burmester T, Hankeln T (2004) Neuroglobin: a respiratory protein of the nervous system. News Physiol Sci 19:110–113

    CAS  PubMed  Google Scholar 

  • Burmester T, Hankein T (2009) What is the function of neuroglobin? J Exp Biol 212:1423–1428

    Article  CAS  PubMed  Google Scholar 

  • Burmester T, Hankeln T (2014) Function and evolution of vertebrate globins. Acta Physiol 211:501–514

    Article  CAS  Google Scholar 

  • Butler PJ (2001) Diving beyond the limits. News Physiol Sci 16:222–227

    CAS  PubMed  Google Scholar 

  • Butler PJ (2004) Metabolic regulation in diving birds and mammals. Respir Physiol Neurobiol 141:297–315

    Article  PubMed  Google Scholar 

  • Butler PJ (2016) The physiological basis of bird flight. Philos Trans R Soc B 371:20150384

    Article  Google Scholar 

  • Butler PJ, Jones DR (1982) The comparative physiology of diving. Adv Comp Physiol Biochem 8:179–364

    Article  CAS  PubMed  Google Scholar 

  • Butler PJ, Jones DR (1997) Physiology of diving birds and mammals. Physiol Rev 77:837–899

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Campbell TW (1988) Avian hematology and cytology, 1st edn. Iowa State University Press, Ames, IA

    Google Scholar 

  • 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

    Google Scholar 

  • Campbell TW (2015) Avian hematology and cytology, 4th edn. Wiley, Hoboken, NJ

    Book  Google Scholar 

  • Campbell TW, Ellis CK (2007) Avian and exotic animal hematology and cytology, 3rd edn. Blackwell Publications, Ames, IA

    Google Scholar 

  • Carey C, Morton ML (1976) Aspects of circulatory physiology of montane and lowland birds. Comp Biochem Physiol 54A:61–74

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Casadevall A, Dadachova E, Pirofski L-A (2004) Passive antibody therapy for infectious diseases. Nat Rev Microbiol 2:695–703

    Article  CAS  PubMed  Google Scholar 

  • Chawla A (2010) Control of macrophage activation and function by PPARs. Circ Res 106:1559–1569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Clark NJ (2018) Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide. Glob Ecol Biogeogr 27:744–755

    Article  Google Scholar 

  • Clark P, Boardman WSJ, Raidal SR (2009) Atlas of clinical avian hematology. Wiley-Blackwell, Chichester, UK

    Google Scholar 

  • Coke RL, West GD, Hoover JP (2004) Hematology and plasma biochemistry of captive Puna Ibis (Plegadis ridgewayi). J Wildl Dis 40:141–144

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Cornick JL, Jensen J (1992) Anesthetic management of Ostriches. J Am Vet Med Assoc 200:1661–1666

    CAS  PubMed  Google Scholar 

  • Cotter PF (2022) A microscopic study on morphology of reactive thrombocytes in duckling. J World’s Poult Res 12:142–150

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Cuervo JJ, Møller AP, De Lope F (2007) Haematocrit is weakly related to condition in nestling Barn Swallows Hirundo rustica. Ibis 149:128–134

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cuperus T, Coorens M, van Dijk A, Haagsman HP (2013) Avian host defense peptides. Dev Comp Immunol 41:352–369

    Article  CAS  PubMed  Google Scholar 

  • Dantzler WH (1989) Comparative physiology of the vertebrate kidney. Springer, New York

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dawson RD, Bortolotti GR (1997) Are avian hematocrits indicative of condition? American Kestrels as a model. J Wildl Manag 61:1297–1306

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Diamond JM, Karasov WH, Phan D, Carpenter FL (1986) Digestive physiology is a determinant of foraging bout frequency in hummingbirds. Nature 320:62–63

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Donnelly RE, Sullivan KA (1998) Foraging proficiency and body condition of juvenile American Dippers. Condor 100:385–388

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dragon S, Baumann R (2003) Hypoxia, hormones, and red blood cell function in chick embryos. News Physiol Sci 18:77–82

    CAS  PubMed  Google Scholar 

  • Dufva R (1996) Blood parasites, health, reproductive success, and egg volume in female Great Tits Parus major. J Avian Biol 27:83–87

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Dzialowski EM, Crossley DA (2015) The cardiovascular system. In: Scanes CG (ed) Sturkie’s avian physiology. Academic Press, Cambridge, MA, pp 193–283

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Elkins N (1983) Weather and bird behaviour. T & AD Poyser Ltd, Calton

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552

    Article  Google Scholar 

  • Faraci FM (1986) Circulation during hypoxia in birds. Comp Biochem Physiol 85:613–620

    Article  CAS  Google Scholar 

  • Faraci FM (1991) Adaptations to hypoxia in birds: how to fly high. Annu Rev Physiol 53:59–70

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Favilla AB, Costa DP (2020) Thermoregulatory strategies of diving air-breathing marine vertebrates: a review. Front Ecol Evol 8:555509

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ferdous F, Scott TR (2015) A comparative examination of thrombocyte/platelet immunity. Immunol Lett 163:32–39

    Article  CAS  PubMed  Google Scholar 

  • Flajnik MF (2002) Comparative analyses of immunoglobulin genes: surprises and portents. Nat Rev Immunol 2:688

    Article  CAS  PubMed  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fuxjager MJ, Schuppe ER (2018) Androgenic signaling systems and their role in behavioral evolution. J Steroid Biochem Mol Biol 184:47–56

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gallardo MH, Bickham J, Honeycutt RL, Ojeda RA, Kohler N (1999) Discovery of tetraploidy in a mammal. Nature 401:341

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gannes LZ (2001) Comparative fuel use of migrating passerines: effects of fat stores, migration distance, and diet. Auk 118:665–677

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Genovese KJ, He H, Swaggerty CL, Kogut MH (2013) The avian heterophil. Dev Comp Immunol 41:334–340

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Glomski CA, Pica A (2011) The avian erythrocyte: its phylogenetic odyssey. Science Publishers, Enfield, NH

    Google Scholar 

  • Goossens KE, Ward AC, Lowenthal JW, Bean AGD (2013) Chicken interferons, their receptors and interferon-stimulated genes. Dev Comp Immunol 41:370–376

    Article  CAS  PubMed  Google Scholar 

  • Graham AC, Temple RM, Obar JJ (2015) Mast cells and influenza a virus: association with allergic responses and beyond. Front Immunol 6:238

    Article  PubMed  PubMed Central  Google Scholar 

  • Green JA, Butler PJ, Woakes AJ, Boyd IL (2003) Energetics of diving in Macaroni Penguins. J Exp Biol 206:43–57

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Grogan KB, Fernández RJ, Barranón FJR, Espinosa JG (2007) A brief review: avian immune system. Merial, Gainesville, GA

    Google Scholar 

  • Grubb BR (1983) Allometric relations of cardiovascular function in birds. Am J Physiol 245:H567–H572

    CAS  PubMed  Google Scholar 

  • Grubb B, Jorgensen DD, Conner M (1983) Cardiovascular changes in the exercising Emu. J Exp Zool 104:193–201

    CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Guillaumet A, Paxton EH (2019) Evaluating community-level response to management actions across a diverse Hawaiian forest bird community. Ecol Appl 29:e01953

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Halsey LG, Butler PJ, Blackburn TM (2006) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287

    Article  PubMed  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harr KE (2002) Clinical chemistry of companion avian species: a review. Vet Clin Pathol 31:140–151

    Article  PubMed  Google Scholar 

  • Harris BS, O’Brien TX, Gourdie RG (2002) Coronary arteriogenesis and differentiation of periarterial Purkinje fibers. Tex Heart Inst J 29:262–270

    PubMed  PubMed Central  Google Scholar 

  • Hart B (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12:123–137

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Hartman FA (1961) Locomotor mechanisms of birds. Smithson Misc Collect 143:1–91

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Hassanpour H, Shamsabadi MG, Dehkordi IN, Dehkordi MM (2014) Normal electrocardiogram of the Laughing Dove (Spilopelia senegalensis). J Zoo Wildl Med 45:41–46

    Article  PubMed  Google Scholar 

  • Hatch MI, Smith RJ, Owen JC (2010) Arrival timing and hematological parameters in Gray Catbirds (Dumetella carolinensis). J Ornithol 151:545–552

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hempleman SC, Powell FL, Prisk GK (1992) Avian arterial chemoreceptor responses to steps of CO2 and O2. Respir Physiol 90:325–340

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Hirsowitz LA, Fell K, Torrance JD (1977) Oxygen-affinity of avian blood. Respir Physiol 31:51–62

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Holz PH (1999) The reptilian renal portal system – a review. Bull Assoc Reptil Amphib Vet 9:4–9

    Google Scholar 

  • Hong JM, Kim TJ, Shin DH, Lee JS, Joo IS (2013) Cardiovascular autonomic function in lateral medullary infarction. Neurol Sci 34:1963–1969

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Huang L, Appleton JA (2016) Eosinophils in helminth infection: defenders and dupes. Trends Parasitol 32:798–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Janeway CA, Travers P, Walport M, Capra JD (1999) Immunobiology: the immune system in health and disease. Current Biology Publications, London

    Google Scholar 

  • Jenni-Eiermann S, Jenni L (1991) Metabolic responses to flight and fasting in night migrating passerines. J Comp Physiol B 161:465–474

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jensen KH, Kim W, Holbrook NM, Bush JWM (2013b) Optimal concentrations in transport systems. J R Soc Interface 10:20130138

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Josephson B (1980) Aging and sexing Snowy Owls. J Field Ornithol 51:149–160

    Google Scholar 

  • Joyce W (2018) Flying is not for the small-hearted. J Exp Biol 221:jeb169912

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Kharin SN (2004) Depolarisation and repolarization sequences of ventricular epicardium in chickens (Gallus gallus domesticus). Comp Biochem Physiol A 137:237–244

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kilgore DL, Bernstein MH, Schmidt-Nielsen K (1973) Brain temperature in a large bird, the rhea. Am J Phys 225:739–742

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Klasing KC (1998) Avian macrophages: regulators of local and systemic immune responses. Poult Sci 77:983–989

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60:19–32

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Laguë SL (2017) High-altitude champions: birds that live and migrate at altitude. J Appl Physiol 123:942–950

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larson TA (2018) Sex steroids, adult neurogenesis, and inflammation in CNS homeostasis, degeneration, and repair. Front Endocrinol 9:205

    Article  Google Scholar 

  • Lasiewski RC, Calder WA (1971) A preliminary allometric analysis of respiratory variables in resting birds. Respir Physiol 11:152–166

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lefranc MP, Lefranc G (2020) Immunoglobulins or antibodies: IMGT® bridging genes, structures and functions. Biomedicines 8:319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Liknes ET, Swanson DL (2011) Phenotypic flexibility of body composition associated with seasonal acclimatization in passerine birds. J Therm Biol 36:363–370

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lutz PL (1980) On the oxygen affinity of bird blood. Am Zool 20:187–198

    Article  CAS  Google Scholar 

  • Machida N, Aohagi Y (2001) Electrocardiography, heart rates, and heart weights of free-living birds. J Zoo Wildl Med 32:47–54

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Maina JN (2015) The design of the avian respiratory system: development, morphology and function. J Ornithol 156:41–63

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Martin LB (2009) Stress and immunity in wild vertebrates: timing is everything. Gen Comp Endocrinol 163:70–76

    Article  CAS  PubMed  Google Scholar 

  • Martínez-de la Puente J, Santiago-Alarcon D, Palinauskas V, Bensch S (2021) Parasite of the month: Plasmodium relictum. Trends Parasitol 37:355–356

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mathieu-Costello O, Agey PJ (1997) Chronic hypoxia affects capillary density and geometry in pigeon pectoralis muscle. Respir Physiol 109:39–52

    Article  CAS  PubMed  Google Scholar 

  • Matthieu-Costello O, Suarez RK, Hochachka PW (1992) Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle. Respir Physiol 89:113–132

    Article  Google Scholar 

  • Maxwell MH, Robertson GW (1995) The avian basophilic leukocyte: a review. Worlds Poult Sci J 51:307–325

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michel CC, Curry FE (1999) Microvascular permeability. Physiol Rev 79:703–761

    Article  CAS  PubMed  Google Scholar 

  • Midtgård U (1982) Patterns in the blood vascular system in the pelvic limb of birds. J Zool 196:545–567

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Milsom WK, Johansen K, Millard RW (1973) Blood respiratory properties in some Antarctic birds. Condor 75:472–474

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Minias P (2015) The use of haemoglobin concentrations to assess physiological condition in birds: a review. Cons Physiol 3:cov007

    Article  Google Scholar 

  • Minias P (2020) Ecology and evolution of blood oxygen-carrying capacity in birds. Am Nat 195:788–801

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Møller AP (1990) Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis. J Evol Biol 3:319–328

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Møller AP, Erritzoe J (2000) Predation against birds with low immunocompetence. Oecologia 122:500–504

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

  • 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

    Article  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Morton ML (1994) Hematocrits in montane sparrows in relation to reproductive schedule. Condor 96:119–126

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Murrant CL, Sarelius IH (2015) Local control of blood flow during active hyperaemia: what kinds of integration are important? J Physiol 593:4699–4711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mutua MP, Muya S, Gicheru MM (2016) Protective roles of free avian respiratory macrophages in captive birds. Biol Res 49:29

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Navarro J, Votier SC, Phillips RA (2014) Diving capabilities of diving petrels. Polar Biol 37:897–901

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Norte AC, Ramos JA, Sampaio HL, Sousa JP, Sheldon BC (2010) Physiological condition and breeding performance of the Great Tit. Condor 112:79–86

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • O’Toole ET, Hantgan RR, Lewis JC (1994) Localization of fibrinogen during aggregation of avian thrombocytes. Exp Mol Pathol 61:175–190

    Article  PubMed  Google Scholar 

  • Odum EP (1945) The heart rate of small birds. Science 101:153–154

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Oppliger A, Christe P, Richner H (1996) Clutch size and malaria resistance. Nature 381:565

    Article  CAS  PubMed  Google Scholar 

  • Ordway GA, Garry DJ (2004) Myoglobin: an essential hemoprotein in striated muscle. J Exp Biol 207:3441–3446

    Article  CAS  PubMed  Google Scholar 

  • Owen JC (2011) Collecting, processing, and storing avian blood: a review. J Field Ornithol 82:339–354

    Article  Google Scholar 

  • Owen JC, Moore FR (2006) Seasonal differences in immunological condition of three species of thrushes. Condor 108:389–398

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Palm EC, Newman SH, Prosser DJ, ** migratory flyways in Asia using dynamic Brownian bridge movement models. Mov Ecol 3:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul S, Lal G (2017) The molecular mechanism of natural killer cells function and its importance in cancer immunotherapy. Front Immunol 8:1124

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Pendl H, Tizard I (2016) Immunology. In: Speer BL (ed) Current therapy in avian medicine and surgery. Elsevier, St. Louis, MO, pp 400–432

    Chapter  Google Scholar 

  • Pennycuick CJ (1998) Computer simulation of fat and muscle burn in long-distance bird migration. J Theor Biol 191:47–61

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ponganis PJ (2015) Diving physiology of marine mammals and seabirds. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ponganis PJ, Meir JU, Williams CL (2010) Oxygen store depletion and the aerobic dive limit in Emperor Penguins. Aquat Biol 8:237–245

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Powell C, Lill A, Johnstone CP (2013) Body condition and chronic stress in urban and rural Noisy Miners. Open Ornithol J 6:25–31

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pryke SR, Rollins LA (2012) Mothers adjust offspring sex to match the quality of the rearing environment. Proc R Soc B 279:4051–4057

    Article  PubMed  PubMed Central  Google Scholar 

  • Pryke SR, Rollins LA, Griffith SC (2011) Context-dependent sex allocation: constraints on the expression and evolution of maternal effects. Evolution 65:2792–2799

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Qureshi MA, Heggen CL, Hussain I (2000) Avian macrophage: effector functions in health and disease. Dev Comp Immunol 24:103–119

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Ramiro AR, Nussenzweig MC (2004) Aid for AID. Nature 430:980–981

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs RE (1992) Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci USA 89:4722–4725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Romero LM, Gormally BMG (2019) How truly conserved is the “well-conserved” vertebrate stress response? Integr Comp Biol 59:273–281

    Article  CAS  PubMed  Google Scholar 

  • Rothenberg ME, Hogan SP (2006) The eosinophil. Annu Rev Immunol 24:147–174

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Santhakumar D, Rubbenstroth D, Martinez-Sobrido L, Munir M (2017) Avian interferons and their antiviral effectors. Front Immunol 8:49

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Scanes CG (2015) Blood. In: Sturkie’s avian physiology, 6th edn. Elsevier, New York

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Scheuerlein A, Ricklefs RE (2004) Prevalence of blood parasites in European passeriform birds. Proc R Soc B 271:1363–1370

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Scholander PF (1940) Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter 22:1–131

    Google Scholar 

  • Scott MG, Hancock RE (2000) Cationic antimicrobial peptides and their multifunctional role in the immune system. Crit Rev Immunol 20:407–431

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Sedlmayr JC, Witmer LM (2002) Rapid technique for imaging the blood vascular system using stereoangiography. Anat Rec 267:330–336

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Shiels HA (2022) Avian cardiomyocyte architecture and what it reveals about the evolution of the vertebrate heart. Philos Trans R Soc B 377:20210332

    Article  CAS  Google Scholar 

  • Shiels HA, Galli GLJ (2014) The sarcoplasmic reticulum and the evolution of the vertebrate heart. Physiology 29:456–469

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirkiä PM, Qvarnström A (2021) Adaptive coloration in Pied Flycatchers (Ficedula hypoleuca)—the devil is in the detail. Ecol Evol 11:1501–1525

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith FM (1994) Blood pressure regulation by aortic baroreceptors in birds. Physiol Zool 67:1402–1425

    Article  Google Scholar 

  • Smith KD, Barber CA (2012) Hematocrit does not indicate condition in nestling or adult European Starlings. Wilson J Ornithol 124:788–792

    Article  Google Scholar 

  • Smith KG, Hunt JL (2004) On the use of spleen mass as a measure of avian immune system strength. Oecologia 138:28–31

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Snyder GK, Sheafor BA (1999) Red blood cells: centerpiece in the evolution of the vertebrate circulatory system. Am Zool 39:189–198

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Soulsbury CD, Dobson J, Deeming DC, Minias P (2022) Energetic lifestyle drives size and shape of avian erythroctyes. Integr Comp Biol 62:71–80

    Article  CAS  PubMed  Google Scholar 

  • Spronk HMH, Govers-Riemslag JWP, ten Cate H (2003) The blood coagulation system as a molecular machine. BioEssays 25:1220–1228

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Stephenson A, Adams JW, Vaccarezza M (2017) The vertebrate heart: an evolutionary perspective. J Anat 231:787–797

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Storz JF (2007) Hemoglobin function and physiological adaptation to hypoxia in high-altitude mammals. J Mammal 88:24–31

    Article  Google Scholar 

  • Sutcliffe JF (1986) Black fly host location: a review. Can J Zool 64:1041–1053

    Article  Google Scholar 

  • Svoboda O, Bartunek P (2015) Origins of the vertebrate erythro/megakaryocytic system. Biomed Res Int 2015:632171

    Article  PubMed  PubMed Central  Google Scholar 

  • Swanson DL (1990) Seasonal variation of vascular oxygen transport in the Dark-eyed Junco. Condor 92:62–66

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tadjalli M, Ghazi SR, Parto P (2009) Gross anatomy of the heart in Ostrich (Struthio camelus). Iran J Vet Res 10:21–27

    Google Scholar 

  • Taha AA, Abdel-Magied EM, King AS (1983) Ultrastructure of aortic and pulmonary baroreceptors in the Domestic Fowl. J Anat 137:197–207

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Tavernier P, Sagesse M, Van Wettere A, Redig P (2005) Malaria in an Eastern Screech Owl (Otus asio). Avian Dis 49:433–435

    Article  PubMed  Google Scholar 

  • Tizard I (2002) The avian antibody response. Semin Avian Exotic Pet Med 11:2–14

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3:133–146

    Article  CAS  PubMed  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other Haemosporidia. CRC Press, Boca Raton, FL

    Google Scholar 

  • Valkiūnas G, Iezhova TA (2018) Keys to the avian malaria parasites. Malar J 17:212

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Warr GW, Magor KE, Higgins DA (1995) IgY: clues to the origins of modern antibodies. Immunol Tod 16:392–398

    Article  CAS  Google Scholar 

  • Warrington R, Watson W, Kim HL, Antonetti FR (2011) An introduction to immunology and immunopathology. Allergy Asthma Clin Immunol 7:S1

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westneat DF, Birkhead TR (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc B 265:1065–1073

    Article  PubMed Central  Google Scholar 

  • Wigley P, Kaiser P (2003) Avian cytokines in health and disease. Braz J Poult Sci 5:1–14

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Williams TD (2012) Physiological adaptations for breeding in birds. Princeton Univ Press, Princeton, NJ

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wong AD, Ye M, Levy AF, Rothstein JD, Bergles DE, Searson PC (2013) The blood-brain barrier: an engineering perspective. Front Neuroeng 6:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodbury RA, Hamilton WF (1937) Blood pressure studies in small animals. Am J Physiol 119:663–674

    Article  Google Scholar 

  • Wright TJ (2014) Myoglobin adaptation in terrestrial and diving birds and mammals. Ph.D. dissertation, Texas A&M University, College Station, TX

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496:445–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Yang D, Wan Y (2019) Molecular determinants for the polarization of macrophage and osteoclast. Semin Immunopathol 41:551–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zaefarian F, Abdollahi MR, Cowieson A, Ravindran V (2019) Avian liver: the forgotten organ. Animals 9:63

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Calvert RA, Sutton BJ, Doré KA (2017) IgY: a key isotype in antibody evolution. Biol Rev 92:2144–2156

    Article  PubMed  Google Scholar 

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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

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