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Annual Review of Animal Biosciences

Volume 12, 2024

Illuminating the Mysteries of the Smallest Birds: Hummingbird Population Health, Disease Ecology, and Genomics

Abstract

Hummingbirds share biologically distinctive traits: sustained hovering flight, the smallest bird body size, and high metabolic rates fueled partially by nectar feeding that provides pollination to plant species. Being insectivorous and sometimes serving as prey to larger birds, they fulfill additional important ecological roles. Hummingbird species evolved and radiated into nearly every habitat in the Americas, with a core of species diversity in South America. Population declines of some of their species are increasing their risk of extinction. Threats to population health and genetic diversity are just beginning to be identified, including diseases and hazards caused by humans. We review the disciplines of population health, disease ecology, and genomics as they relate to hummingbirds. We appraise knowledge gaps, causes of morbidity and mortality including disease, and threats to population viability. Finally, we highlight areas of research need and provide ideas for future studies aimed at facilitating hummingbird conservation.

Keyword(s): avian, disease ecology, genomics, hummingbird, population health, Trochilidae
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2024-02-15
2024-05-02
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Literature Cited

  1. 1.
    Stephen C 2022. Wildlife Population Health Cham, Switz.: Springer Int. Publ
  2. 2.
    Ostfeld RS. 2018. Disease ecology. Oxford Bibliographies Oxford, UK: Oxford Univ. Press https://www.oxfordbibliographies.com/display/document/obo-9780199830060/obo-9780199830060-0128.xml
    [Google Scholar]
  3. 3.
    Dorland's Med. Dict 2023. Disease retrieved Oct. 11, 2023. https://www.dorlandsonline.com/dorland/definition?id=14449&searchterm=disease
  4. 4.
    Storfer A, Kozakiewicz CP, Beer MA, Savage AE. 2021. Applications of population genomics for understanding and mitigating wildlife disease. Population Genomics: Wildlife PA Hohenlohe, OP Rajora 357–83 Cham, Switz.: Springer Int. Publ
     [Google Scholar]
  5. 5.
    DeCandia AL, Dobson AP, vonHoldt BM. 2018. Toward an integrative molecular approach to wildlife disease. Conserv. Biol. 32:4798–807
     [Google Scholar]
  6. 6.
    Natl. Hum. Genome Res. Inst 2022. Epigenomics fact sheet https://www.genome.gov/about-genomics/fact-sheets/Epigenomics-Fact-Sheet
  7. 7.
    Natl. Hum. Genome Res. Inst 2022. Transcriptome fact sheet https://www.genome.gov/about-genomics/fact-sheets/Transcriptome-Fact-Sheet
  8. 8.
    Al-Amrani S, Al-Jabri Z, Al-Zaabi A, Alshekaili J, Al-Khabori M. 2021. Proteomics: concepts and applications in human medicine. World J. Biol. Chem. 12:557–69
     [Google Scholar]
  9. 9.
    Orozco Calambas EL, Calambas FO, Castillo Ordoñez WO. 2022. The hummingbird and the condor among the Nasa symbolize spirituality in the ceremony of the Saakhelu. J. Ethnobiol. 42:31–12
     [Google Scholar]
  10. 10.
    Fogden M, Taylor M, Williamson S. 2014. Hummingbirds: A Life-Size Guide to Every Species New York: Harper Design
  11. 11.
    Mesear T. 2016. Fastest Things on Wings: Rescuing Hummingbirds in Hollywood Boston: Mar. Books
  12. 12.
    Winkler DW, Billerman SM, Lovette IJ. 2020. Hummingbirds (Trochilidae), version 1.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  13. 13.
    Healy S, Calder WA. 2020. Rufous hummingbird (Selasphorus rufus), version 1.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  14. 14.
    Roy MS, Boesman PFD, Kirwan GM. 2020. Green-backed firecrown (Sephanoides sephaniodes), version 1.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  15. 15.
    Chai P, Kirwan GM. 2020. Bee hummingbird (Mellisuga helenae), version 1.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  16. 16.
    Clark CJ. 2020. Vervain hummingbird (Mellisuga minima), version 1.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  17. 17.
    Lasiewski RC, Weathers WW, Bernstein MH. 1967. Physiological responses of the giant hummingbird, Patagona gigas. Comp. Biochem. Physiol. 23:3797–813
     [Google Scholar]
  18. 18.
    Medrano F, Mallea MJS, Heynen I, Boesman PFD, Kirwan GM. 2022. Giant hummingbird (Patagona gigas), version 2.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  19. 19.
    Pearson OP. 1954. The daily energy requirements of a wild Anna hummingbird. Condor 56:6317–22
     [Google Scholar]
  20. 20.
    Suarez RK. 1992. Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48:6565–70
     [Google Scholar]
  21. 21.
    Altshuler DL, Dudley R. 2002. The ecological and evolutionary interface of hummingbird flight physiology. J. Exp. Biol. 205:Pt. 162325–36
     [Google Scholar]
  22. 22.
    Lasiewski RC, Lasiewski RJ. 1967. Physiological responses of blue-throated and Rivoli's hummingbirds. Auk 84:134–48
     [Google Scholar]
  23. 23.
    Rico-Guevara A, Rubega MA. 2017. Functional morphology of hummingbird bill tips: their function as tongue wringers. Zoology 123:1–10
     [Google Scholar]
  24. 24.
    Cuban D, Hewes AE, Sargent AJ, Groom DJE, Rico-Guevara A. 2022. On the feeding biomechanics of nectarivorous birds. J. Exp. Biol. 225:2jeb243096
     [Google Scholar]
  25. 25.
    Stoddard MC, Eyster HN, Hogan BG, Morris DH, Soucy ER, Inouye DW. 2020. Wild hummingbirds discriminate nonspectral colors. PNAS 117:2615112–22
     [Google Scholar]
  26. 26.
    Ward BJ, Day LB, Wilkening SR, Wylie DR, Saucier DM, Iwaniuk AN. 2012. Hummingbirds have a greatly enlarged hippocampal formation. Biol. Lett. 8:4657–59
     [Google Scholar]
  27. 27.
    Zenzal TJ Jr., Ward MP, Diehl RH, Buler JJ, Smolinsky J et al. 2021. Retreat, detour or advance? Understanding the movements of birds confronting the Gulf of Mexico. Oikos 130:5739–52
     [Google Scholar]
  28. 28.
    Carpenter FL, Hixon MA, Beuchat CA, Russell RW, Paton DC. 1993. Biphasic mass gain in migrant hummingbirds: body composition changes, torpor, and ecological significance. Ecology 74:41173–82
     [Google Scholar]
  29. 29.
    Eberts ER, Tattersall GJ, Auger PJ, Curley M, Morado MI et al. 2023. Free-living Allen's hummingbirds (Selasphorus sasin) rarely use torpor while nesting. J. Therm. Biol. 112:103391
     [Google Scholar]
  30. 30.
    Pandit PS, Bandivadekar RR, Johnson CK, Mikoni N, Mah M et al. 2021. Retrospective study on admission trends of Californian hummingbirds found in urban habitats (1991–2016). PeerJ 9:e11131
     [Google Scholar]
  31. 31.
    Louchart A, Tourment N, Carrier J, Roux T, Mourer-Chauviré C. 2008. Hummingbird with modern feathering: an exceptionally well-preserved Oligocene fossil from southern France. Naturwissenschaften 95:2171–75
     [Google Scholar]
  32. 32.
    Mayr G. 2007. New specimens of the early Oligocene Old World hummingbird Eurotrochilus inexpectatus. J. Ornithol. 148:1105–11
     [Google Scholar]
  33. 33.
    Bochenski Z, Bochenski ZM. 2008. An Old World hummingbird from the Oligocene: a new fossil from Polish Carpathians. J. Ornithol. 149:2211–16
     [Google Scholar]
  34. 34.
    Mayr G. 2022. Opisthocomiformes (hoatzins), “Columbaves” (doves, cuckoos, bustards, and allies), and Strisores (nightjars, swifts, hummingbirds, and allies). Paleogene Fossil Birds G Mayr 93–116 Cham, Switz: Springer Int. Publ
     [Google Scholar]
  35. 35.
    McGuire JA, Witt CC, Remsen JV, Corl A, Rabosky DL et al. 2014. Molecular phylogenetics and the diversification of hummingbirds. Curr. Biol. 24:8910–16
     [Google Scholar]
  36. 36.
    Bleiweiss R. 1998. Origin of hummingbird faunas. Biol. J. Linn. Soc. 65:177–97
     [Google Scholar]
  37. 37.
    Bleiweiss R, Kirsch JA, Matheus JC. 1997. DNA hybridization evidence for the principal lineages of hummingbirds (Aves:Trochilidae). Mol. Biol. Evol. 14:3325–43
     [Google Scholar]
  38. 38.
    McGuire JA, Witt CC, Altshuler DL, Remsen JV. 2007. Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Syst. Biol. 56:5837–56
     [Google Scholar]
  39. 39.
    McGuire JA, Witt CC, Remsen JV, Dudley R, Altshuler DL. 2009. A higher-level taxonomy for hummingbirds. J. Ornithol. 150:1155–65
     [Google Scholar]
  40. 40.
    Mendoza-Henao AM, Garcia-R JC. 2021. Neotropical biodiversity: hypotheses of species diversification and dispersal in the Andean mountain forest. The Andean Cloud Forest RW Myster 177–87 Cham, Switz: Springer Int. Publ
     [Google Scholar]
  41. 41.
    Tell L, Hazlehurst J, Bandivadekar R, Brown J, Spence A et al. 2021. Hummingbird (Family Trochilidae) Research: Welfare-Conscious Study Techniques for Live Hummingbirds and Processing of Hummingbird Specimens Lubbock: Mus. Tex. Tech Univ.
  42. 42.
    Sylvina TJ 2022. Animal Welfare Challenges in Research and Education on Wildlife, Non-Model Animal Species and Biodiversity: Proceedings of a Workshop Washington, DC: Natl. Acad. Press
  43. 43.
    Russell SM, Russell RO. 2019. The North American Banders’ Manual for Hummingbirds Point Reyes Station, CA: N. Am. Band. Counc
  44. 44.
    Hobson KA, Wassenaar LI, Milá B, Lovette I, Dingle C, Smith TB. 2003. Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia 136:2302–8
     [Google Scholar]
  45. 45.
    Supp SR, La Sorte FA, Cormier TA, Lim MCW, Powers DR et al. 2015. Citizen-science data provides new insight into annual and seasonal variation in migration patterns. Ecosphere 6:1art15
     [Google Scholar]
  46. 46.
    Wolf N, Smeltz TS, Cook C, Martinez del Rio C. 2022. Using stable isotopes in hummingbird breath to estimate reliance on supplemental feeders. Ecol. Evol. 13:2e9799
     [Google Scholar]
  47. 47.
    Bishop CA, Moran AJ, Toshack MC, Elle E, Maisonneuve F, Elliott JE. 2018. Hummingbirds and bumble bees exposed to neonicotinoid and organophosphate insecticides in the Fraser Valley, British Columbia, Canada. Environ. Toxicol. Chem. 37:82143–52
     [Google Scholar]
  48. 48.
    Góngora E, Cadena CD, Dussán J. 2016. Toxic metals and associated sporulated bacteria on Andean hummingbird feathers. Environ. Sci. Pollut. Res. Int. 23:2222968–79
     [Google Scholar]
  49. 49.
    Hiebert SM, Ramenofsky M, Salvante K, Wingfield JC, Gass CL. 2000. Noninvasive methods for measuring and manipulating corticosterone in hummingbirds. Gen. Comp. Endocrinol. 120:2235–47
     [Google Scholar]
  50. 50.
    Yamasaki YK, Graves EE, Houston RS, OConnor BM, Kysar PE et al. 2018. Evaluation of Proctophyllodes huitzilopochtlii on feathers from Anna's (Calypte anna) and black-chinned (Archilochus alexandri) hummingbirds: prevalence assessment and imaging analysis using light and tabletop scanning electron microscopy. PLOS ONE 13:2e0191323
     [Google Scholar]
  51. 51.
    Schweizer TM, DeSaix MG. 2023. Cost-effective library preparation for whole genome sequencing with feather DNA. Conserv. Genet. Resour. 15:121–28
     [Google Scholar]
  52. 52.
    Galvin AN, Pandit PS, English SG, Quock RC, Bandivadekar RR et al. 2022. Evaluation of minimally invasive sampling methods for detecting Avipoxvirus: hummingbirds as a case example. Front. Vet. Sci. 9:924854
     [Google Scholar]
  53. 53.
    Clark CJ, Rankin DT, Rudeen CE. 2022. Banding data show hummingbirds have high rates of hybridization. Ornithology 139:1ukab067
     [Google Scholar]
  54. 54.
    Celis-Murillo A, Malorodova M, Nakash E. 2022. North American bird banding program dataset 1960–2022 https://www.sciencebase.gov/catalog/item/632b2d7bd34e71c6d67bc161
    [Google Scholar]
  55. 55.
    Hadley AS, Betts MG. 2009. Tropical deforestation alters hummingbird movement patterns. Biol. Lett. 5:2207–10
     [Google Scholar]
  56. 56.
    Pavan LI, Jankowski JE, Hazlehurst JA. 2020. Patterns of territorial space use by shining sunbeams (Aglaeactis cupripennis), tropical montane hummingbirds. J. Field Ornithol. 91:1–12
     [Google Scholar]
  57. 57.
    Leimberger KG, Dalsgaard B, Tobias JA, Wolf C, Betts MG. 2022. The evolution, ecology, and conservation of hummingbirds and their interactions with flowering plants. Biol. Rev. 97:3923–59
     [Google Scholar]
  58. 58.
    Zenzal TJ Jr., Moore FR. 2018. Resource use and defence by ruby-throated hummingbirds during stopover. Behaviour 156:2131–53
     [Google Scholar]
  59. 59.
    Bandivadekar RR, Pandit PS, Sollmann R, Thomas MJ, Logan SM et al. 2018. Use of RFID technology to characterize feeder visitations and contact network of hummingbirds in urban habitats. PLOS ONE 13:12e0208057
     [Google Scholar]
  60. 60.
    English SG, Wilson S, Bandivadekar RR, Graves EE, Holyoak M et al. 2022. Quantifying phenology and migratory behaviours of hummingbirds using single-site dynamics and mark-detection analyses. Proc. Biol. Sci. 289:198220220991
     [Google Scholar]
  61. 61.
    Williamson JL, Witt CC. 2021. A lightweight backpack harness for tracking hummingbirds. J. Avian Biol. 52:9 https://doi.org/10.1111/jav.02802
    [Google Scholar]
  62. 62.
    Godoy LA, Tell LA, Ernest HB. 2014. Hummingbird health: pathogens and disease conditions in the family Trochilidae. J. Ornithol. 155:1–12
     [Google Scholar]
  63. 63.
    English SG, Bishop CA, Wilson S, Smith AC. 2021. Current contrasting population trends among North American hummingbirds. Sci. Rep. 11:18369
     [Google Scholar]
  64. 64.
    Drake A, Bishop CA, Moran AJ, Wilson S. 2022. Geographic and temporal variation in annual survival of a declining neotropical migrant hummingbird (Selasphorus rufus) under varying fire, snowpack, and climatic conditions. Front. Ecol. Evol. 10:825026
     [Google Scholar]
  65. 65.
    Blake CH. 1957. Diseases and injuries of Jamaican birds. Bird-Band 28:3157–59
     [Google Scholar]
  66. 66.
    Wood FD, Wood SF. 1937. Occurrence of haematozoa in some California birds and mammals. J. Parasitol. 23:2197
     [Google Scholar]
  67. 67.
    Backus L, Foss L, Tell LA. 2019. West Nile virus in hummingbirds in California, USA, 2005–17. J. Wildl. Dis. 55:4903–7
     [Google Scholar]
  68. 68.
    Bleitz D. 1958. Treatment of foot pox at a feeding and trapping station. Auk 75:4474–75
     [Google Scholar]
  69. 69.
    Michener H, Michener JR. 1936. Abnormalities in birds. Condor 38:3102–9
     [Google Scholar]
  70. 70.
    Bolte AL, Meurer J, Kaleta EF. 1999. Avian host spectrum of avipoxviruses. Avian Pathol 28:5415–32
     [Google Scholar]
  71. 71.
    Godoy LA, Dalbeck LS, Tell LA, Woods LW, Colwell RR et al. 2013. Characterization of avian poxvirus in Anna's hummingbird (Calypte anna) in California, USA. J. Wildl. Dis. 49:4978–85
     [Google Scholar]
  72. 72.
    Baek HE, Bandivadekar RR, Pandit P, Mah M, Sehgal RNM, Tell LA. 2020. TaqMan quantitative real-time PCR for detecting avipoxvirus DNA in various sample types from hummingbirds. PLOS ONE 15:6e0230701
     [Google Scholar]
  73. 73.
    Magagna M, Noland E, Tell LA, Purdin G, Rideout B et al. 2019. Histopathologic findings in free-ranging California hummingbirds, 1996–2017. J. Wildl. Dis. 55:2343–51
     [Google Scholar]
  74. 74.
    Adams NE, Bandivadekar RR, Battey CJ, Clark MW, Epperly K et al. 2023. Widespread gene flow following range expansion in Anna's hummingbird. Mol. Ecol. 32:123089–101
     [Google Scholar]
  75. 75.
    Moens MAJ, Valkiūnas G, Paca A, Bonaccorso E, Aguirre N, Perez-Tris J. 2016. Parasite specialization in a unique habitat: hummingbirds as reservoirs of generalist blood parasites of Andean birds. J. Anim. Ecol. 85:51234–45
     [Google Scholar]
  76. 76.
    Valkiūnas G. 2004. Avian Malaria Parasites and Other Haemosporidia Boca Raton, FL: CRC Press
  77. 77.
    Redig PT, Cruz-Martinez L 2009. Raptors. Handbook of Avian Medicine TN Tully, GM Dorrestein, AK Jones, JE Cooper 209–42 Edinburgh: W.B. Saunders, 2nd ed.
     [Google Scholar]
  78. 78.
    Samuel MD, Woodworth BL, Atkinson CT, Hart PJ, LaPointe DA. 2015. Avian malaria in Hawaiian forest birds: infection and population impacts across species and elevations. Ecosphere 6:6art104
     [Google Scholar]
  79. 79.
    Matta NE, Lotta IA, Valkiūnas G, González AD, Pacheco MA et al. 2014. Description of Leucocytozoon quynzae sp. nov. (Haemosporida, Leucocytozoidae) from hummingbirds, with remarks on distribution and possible vectors of leucocytozoids in South America. Parasitol. Res. 113:2457–68
     [Google Scholar]
  80. 80.
    Harrigan RJ, Sedano R, Chasar AC, Chaves JA, Nguyen JT et al. 2014. New host and lineage diversity of avian haemosporidia in the northern Andes. Evol. Appl. 7:7799–811
     [Google Scholar]
  81. 81.
    Galvin AN, Bradshaw AC, Myers BM, Tell LA, Ernest HB, Sehgal RNM. 2021. Low prevalence of haemosporidians in blood and tissue samples from hummingbirds. J. Parasitol. 107:5794–98
     [Google Scholar]
  82. 82.
    Mackenzie AM, Dudenhoeffer M, Bangoura B, Sehgal RNM, Tell LA et al. 2022. Prevalence and diversity of haemosporidians in a migratory high-elevation hummingbird in North America. Parasitol. Res. 121:2769–73
     [Google Scholar]
  83. 83.
    Glomski CA, Pica A. 2016. The Avian Erythrocyte: Its Phylogenetic Odyssey Boca Raton, FL: CRC Press
  84. 84.
    Williamson JL, Linck EB, Bautista E, Smiley A, McGuire JA et al. 2023. Hummingbird blood traits track oxygen availability across space and time. Ecol. Lett. 26:71223–36
     [Google Scholar]
  85. 85.
    Valkiūnas G, Iezhova TA. 2022. Keys to the avian Haemoproteus parasites (Haemosporida, Haemoproteidae). Malar. J. 21:269
     [Google Scholar]
  86. 86.
    Williams RAJ, Segovia-Hinostroza K, Ghersi BM, Gonzaga V, Peterson AT, Montgomery JM. 2012. Avian influenza infections in nonmigrant land birds in Andean Peru. J. Wildl. Dis. 48:4910–17
     [Google Scholar]
  87. 87.
    Oniki Y, Willis EO. 2000. Nesting behavior of the swallow-tailed hummingbird, Eupetomena macroura (Trochilidae, Aves). Braz. J. Biol. Rev. 60:4655–62
     [Google Scholar]
  88. 88.
    Nuñez-Rosas LE, Ramírez-García E, Lara C, Arizmendi M. 2018. Observación del parasitismo por moscas (Philornis bellus) en tres especies de colibríes del Occidente de México. Rev. Mex. Biodivers. 89:3847–53
     [Google Scholar]
  89. 89.
    Kitto GB, Wilson AC. 1966. Evolution of malate dehydrogenase in birds. Science 153:37421408–10
     [Google Scholar]
  90. 90.
    Gill FB, Gerwin JA. 1989. Protein relationships among hermit hummingbirds. Proc. Acad. Nat. Sci. Phila. 141:409–21
     [Google Scholar]
  91. 91.
    Bleiweiss R, Matheus JC. 1994. DNA-DNA hybridization evidence for subfamily structure among hummingbirds. Auk 111:18–19
     [Google Scholar]
  92. 92.
    García-Moreno J, Arctander P, Fjeldså J. 1999. Strong diversification at the treeline among Metallura hummingbirds. Auk 116:3702–11
     [Google Scholar]
  93. 93.
    Parker PG, Snow AA, Schug MD, Booton GC, Fuerst PA. 1998. What molecules can tell us about populations: choosing and using a molecular marker. Ecology 79:2361–82
     [Google Scholar]
  94. 94.
    Vianna CR, Hagen T, Zhang CY, Bachman E, Boss O et al. 2001. Cloning and functional characterization of an uncoupling protein homolog in hummingbirds. Physiol. Genom. 5:3137–45
     [Google Scholar]
  95. 95.
    Allendorf FW. 2017. Genetics and the conservation of natural populations: allozymes to genomes. Mol. Ecol. 26:2420–30
     [Google Scholar]
  96. 96.
    Lance SL, Hagen C, Glenn TC, Brumfield RT, Stryjewski KF, Graves GR. 2009. Fifteen polymorphic microsatellite loci from Jamaican streamertail hummingbirds (Trochilus). Conserv. Genet. 10:41195–98
     [Google Scholar]
  97. 97.
    Oyler-McCance SJ, Fike JA, Talley-Farnham T, Engelman T, Engelman F. 2011. Characterization of ten microsatellite loci in the broad-tailed hummingbird (Selasphorus platycercus). Conserv. Genet. Resour. 3:2351–53
     [Google Scholar]
  98. 98.
    van Dongen WFD, Vásquez RA, Winkler H. 2012. The use of microsatellite loci for accurate hybrid detection in a recent contact zone between an endangered and a recently-arrived hummingbird. J. Ornithol. 153:2585–92
     [Google Scholar]
  99. 99.
    Bailey IE, Segelbacher G, Healy SD, Hurly TA, Pemberton JM. 2013. Microsatellite variation in rufous hummingbirds (Selasphorus rufus) and evidence for a weakly structured population. J. Ornithol. 154:41029–37
     [Google Scholar]
  100. 100.
    Hillier LW, Miller W, Birney E, Warren W, Hardison RC et al. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:7018695–716
     [Google Scholar]
  101. 101.
    Zhang G, Li B, Li C, Gilbert MTP, Mello CV et al. 2014. Genomic data of the Anna's Hummingbird (Calypte anna. GigaScience Database http://gigadb.org/dataset/101004
    [Google Scholar]
  102. 102.
    Natl. Cent. Biotechnol. Inf 2023. Trochilidae (hummingbirds) genome https://www.ncbi.nlm.nih.gov/datasets/taxonomy/9242/
  103. 103.
    Baldwin MW, Toda Y, Nakagita T, O'Connell MJ, Klasing KC et al. 2014. Sensory biology. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345:6199929–33
     [Google Scholar]
  104. 104.
    Workman RE, Myrka AM, Wong GW, Tseng E, Welch J Jr., Timp W. 2018. Single-molecule, full-length transcript sequencing provides insight into the extreme metabolism of the ruby-throated hummingbird Archilochus colubris. GigaScience 7:3giy009
     [Google Scholar]
  105. 105.
    Gershman A, Hauck Q, Dick M, Jamison JM, Tassia M et al. 2023. Genomic insights into metabolic flux in hummingbirds. Genome Res 33:5703–14
     [Google Scholar]
  106. 106.
    Osipova E, Barsacchi R, Brown T, Sadanandan K, Gaede AH et al. 2023. Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds. Science 379:185–90
     [Google Scholar]
  107. 107.
    Salve BG, Kurian AM, Vijay N. 2023. Concurrent loss of ciliary genes WDR93 and CFAP46 in phylogenetically distant birds. R. Soc. Open Sci. 10:8230801
     [Google Scholar]
  108. 108.
    Waters PD, Patel HR, Ruiz-Herrera A, Álvarez-González L, Lister NC et al. 2021. Microchromosomes are building blocks of bird, reptile, and mammal chromosomes. PNAS 118:45e2112494118
     [Google Scholar]
  109. 109.
    Lewin HA, Richards S, Lieberman Aiden E, Allende ML, Archibald JM et al. 2022. The Earth BioGenome Project 2020: starting the clock. PNAS 119:4e2115635118
     [Google Scholar]
  110. 110.
    Rhie A, McCarthy SA, Fedrigo O, Damas J, Formenti G et al. 2021. Towards complete and error-free genome assemblies of all vertebrate species. Nature 592:7856737–46
     [Google Scholar]
  111. 111.
    Croville G, Le Loc'h G, Zanchetta C, Manno M, Camus-Bouclainville C et al. 2018. Rapid whole-genome based typing and surveillance of avipoxviruses using nanopore sequencing. J. Virol. Methods 261:34–39
     [Google Scholar]
  112. 112.
    Bensch S, Canbäck B, DeBarry JD, Johansson T, Hellgren O et al. 2016. The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biol. Evol. 8:51361–73
     [Google Scholar]
  113. 113.
    Barrow LN, Allen JM, Huang X, Bensch S, Witt CC. 2019. Genomic sequence capture of haemosporidian parasites: Methods and prospects for enhanced study of host-parasite evolution. Mol. Ecol. Resour. 19:2400–10
     [Google Scholar]
  114. 114.
    Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. 2008. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6:10776–88
     [Google Scholar]
  115. 115.
    Dutch R, Tell LA, Bandivadekar R, Vannette RL. 2022. Microbiome composition of Anna's hummingbirds differs among regions of the gastrointestinal tract. J. Avian Biol. 2022:3e02856
     [Google Scholar]
  116. 116.
    Lees AC, Haskell L, Allinson T, Bezeng SB, Burfield IJ et al. 2022. State of the world's birds. Annu. Rev. Environ. Resour. 47:231–60
     [Google Scholar]
  117. 117.
    Rosenberg KV, Dokter AM, Blancher PJ, Sauer JR, Smith AC et al. 2019. Decline of the North American avifauna. Science 366:6461120–24
     [Google Scholar]
  118. 118.
    Schmidt C, Hoban S, Hunter M, Paz-Vinas I, Garroway CJ. 2023. Genetic diversity and IUCN Red List status. Conserv. Biol. 37:4e14064
     [Google Scholar]
  119. 119.
    Gilpin ME, Soule ME 1986. Minimum viable populations: the processes of species extinctions. Conservation Biology: The Science of Scarcity and Diversity ME Soule 13–34 Sunderland, MA: Sinauer Assoc
     [Google Scholar]
  120. 120.
    Trail PW. 2022. Dying for love: illegal international trade in hummingbird love charms. Conserv. Sci. Pract. 4:6e12679
     [Google Scholar]
  121. 121.
    Brown JJ, Pascual M, Wimberly MC, Johnson LR, Murdock CC. 2023. Humidity—the overlooked variable in the thermal biology of mosquito-borne disease. Ecol. Lett. 26:71029–49
     [Google Scholar]
  122. 122.
    Betini GS, Malaj E, Donkersteeg C, Smith AC, Wilson S et al. 2023. Spatial variation in the association between agricultural activities and bird communities in Canada. Sci. Total Environ. 881:163413
     [Google Scholar]
  123. 123.
    Gonzalez AM, Espejo N, Armenteras D, Hobson KA, Kardynal KJ et al. 2023. Habitat protection and restoration: Win-win opportunities for migratory birds in the Northern Andes. Perspect. Ecol. Conserv. 21:133–40
     [Google Scholar]
  124. 124.
    Galetto L, Aizen M, Arizmendi M, Freitas B, Garibaldi L et al. 2022. Risks and opportunities associated with pollinators’ conservation and management of pollination services in Latin America. Ecol. Austral 32:055–076
     [Google Scholar]
  125. 125.
    Tinoco BA, Santillán VE, Graham CH. 2018. Land use change has stronger effects on functional diversity than taxonomic diversity in tropical Andean hummingbirds. Ecol. Evol. 8:63478–90
     [Google Scholar]
  126. 126.
    Hadley AS, Frey SJK, Robinson WD, Betts MG. 2018. Forest fragmentation and loss reduce richness, availability, and specialization in tropical hummingbird communities. Biotropica 50:174–83
     [Google Scholar]
  127. 127.
    Lara C, Feria-Arroyo TP, Dale J, Muñoz J, del Coro Arizmendi M et al. 2012. Potential effects of the climate change in the distribution of hummingbirds: a study case with hummingbirds from the genus Amazilia and Cynanthus. Ornitol. Neotropical 23:35–48
     [Google Scholar]
  128. 128.
    Prieto-Torres DA, Nuñez Rosas LE, Remolina Figueroa D, del Coro Arizmendi M. 2021. Most Mexican hummingbirds lose under climate and land-use change: long-term conservation implications. Perspect. Ecol. Conserv. 19:4487–99
     [Google Scholar]
  129. 129.
    Freeman BG, Scholer MN, Ruiz-Gutierrez V, Fitzpatrick JW. 2018. Climate change causes upslope shifts and mountaintop extirpations in a tropical bird community. PNAS 115:4711982–87
     [Google Scholar]
  130. 130.
    Carsen R. 1962. Silent Spring Boston: Houghton Mifflin Harcourt
  131. 131.
    Moreau J, Rabdeau J, Badenhausser I, Giraudeau M, Sepp T et al. 2022. Pesticide impacts on avian species with special reference to farmland birds: a review. Environ. Monit. Assess. 194:11790
     [Google Scholar]
  132. 132.
    Etterson MA, Paulukonis EA, Purucker ST. 2023. Using Pop-GUIDE to assess the applicability of MCnest for relative risk of pesticides to hummingbirds. Ecologies 4:1171–94
     [Google Scholar]
  133. 133.
    Bishop CA, Woundneh MB, Maisonneuve F, Common J, Elliott JE, Moran AJ. 2020. Determination of neonicotinoids and butenolide residues in avian and insect pollinators and their ambient environment in Western Canada (2017, 2018). Sci. Total Environ. 737:139386
     [Google Scholar]
  134. 134.
    Bishop CA, English SG, Maisonneuve F, Moran AJ, Higo HA et al. 2022. Temporal and spatial patterns of systemic insecticides in avian and insect pollinators and flowers in western Canada (2018, 2019). Environ. Adv. 8:100211
     [Google Scholar]
  135. 135.
    Graves EE, Jelks KA, Foley JE, Filigenzi MS, Poppenga RH et al. 2019. Analysis of insecticide exposure in California hummingbirds using liquid chromatography-mass spectrometry. Environ. Sci. Pollut. Res. 26:1515458–66
     [Google Scholar]
  136. 136.
    Filigenzi MS, Graves EE, Tell LA, Jelks KA, Poppenga RH. 2019. Quantitation of neonicotinoid insecticides, plus qualitative screening for other xenobiotics, in small-mass avian tissue samples using UHPLC high-resolution mass spectrometry. J. Vet. Diagn. Investig. 31:3399–407
     [Google Scholar]
  137. 137.
    English SG, Sandoval-Herrera NI, Bishop CA, Cartwright M, Maisonneuve F et al. 2021. Neonicotinoid pesticides exert metabolic effects on avian pollinators. Sci. Rep. 11:2914
     [Google Scholar]
  138. 138.
    Loss SR, Will T, Loss SS, Marra PP. 2014. Bird-building collisions in the United States: estimates of annual mortality and species vulnerability. Condor 116:18–23
     [Google Scholar]
  139. 139.
    King M, Giacinti J, Dubois S, Lair S, Parmley EJ, Jardine CM. 2023. Using wildlife rehabilitation and postmortem data to identify key causes of morbidity and mortality impacting the health and welfare of free-living wild animals in Canada. J. Wildl. Dis. 59:193–108
     [Google Scholar]
  140. 140.
    Contreras-Martínez S. 2015. Dinámica espacio-temporal de colibríes (Trochilidae), en bosques de pino-encino post-incendio en la Reserva de la Biosfera Sierra de Manantlán, Jalisco, México PhD Thesis Univ. Guadalajara Guadalajara, Mex.:
  141. 141.
    Alexander JD, Williams EJ, Gillespie CR, Contreras-Martínez S, Finch DM. 2020. Effects of restoration and fire on habitats and populations of western hummingbirds: a literature review RMRS-GTR-408 US Dep. Agric., For. Serv., Rocky Mt. Res. Stat. Ft. Collins, CO:
  142. 142.
    Robb GN, McDonald RA, Chamberlain DE, Bearhop S. 2008. Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front. Ecol. Environ. 6:9476–84
     [Google Scholar]
  143. 143.
    Fischer JR, Stallknecht DE, Luttrell P, Dhondt AA, Converse KA. 1997. Mycoplasmal conjunctivitis in wild songbirds: the spread of a new contagious disease in a mobile host population. Emerg. Infect. Dis. 3:169–72
     [Google Scholar]
  144. 144.
    Loss SR, Li BV, Horn LC, Mesure MR, Zhu L et al. 2023. Citizen science to address the global issue of bird-window collisions. Front. Ecol. Environ. 21:9418–27
     [Google Scholar]
  145. 145.
    Nyffeler M, Maxwell MR, Remsen JV. 2017. Bird predation by praying mantises: a global perspective. Wilson J. Ornithol. 129:2331–44
     [Google Scholar]
  146. 146.
    Choi J, Lee L, Maro A, Corl A, McGuire JA et al. 2023. Hummingbird ingestion of low-concentration ethanol within artificial nectar. R. Soc. Open Sci. 10:6230306
     [Google Scholar]
  147. 147.
    Lee C, Tell LA, Hilfer T, Vannette RL. 2019. Microbial communities in hummingbird feeders are distinct from floral nectar and influenced by bird visitation. Proc. R. Soc. B 286:189820182295
     [Google Scholar]
  148. 148.
    Clark CJ, Russell SM. 2020. Anna's hummingbird (Calypte anna), version 1.0. Birds of the World Ithaca, NY: Cornell Lab Ornithol
     [Google Scholar]
  149. 149.
    Handelman C, Kohn JR. 2014. Hummingbird color preference within a natural hybrid population of Mimulus aurantiacus (Phrymaceae). Plant Species Biol 29:165–72
     [Google Scholar]
  150. 150.
    Lumsdaine E. 2017. An examination of Allura Red AC as an additive to commercially produced hummingbird nectars Unpubl. thesis Univ. Calif. Davis:
  151. 151.
    De Paoli-Iseppi R, Deagle BE, Polanowski AM, McMahon CR, Dickinson JL et al. 2019. Age estimation in a long-lived seabird (Ardenna tenuirostris) using DNA methylation-based biomarkers. Mol. Ecol. Resour. 19:2411–25
     [Google Scholar]
  152. 152.
    West. Hummingbird Partnersh 2023. Restoration guides for maintaining and improving habitats for hummingbirds https://westernhummingbird.org/habitat/
/content/journals/10.1146/annurev-animal-021022-044308
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Illuminating the Mysteries of the Smallest Birds: Hummingbird Population Health, Disease Ecology, and Genomics
Annual Review of Animal Biosciences 12, 161 (2024); https://doi.org/10.1146/annurev-animal-021022-044308
/content/journals/10.1146/annurev-animal-021022-044308
/content/journals/10.1146/annurev-animal-021022-044308
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