Skip to main content
SpringerLink
Log in

Heat-related massive chick mortality in an Imperial Cormorant Leucocarbo atriceps colony from Patagonia, Argentina

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Climate change has exacerbated the frequency and severity of heat waves, which on occasion lead to mass mortalities. Here, we report a massive mortality event in Imperial Cormorant Leucocarbo atriceps chicks that took place during December 2016 at Punta León, one of the two largest colonies (> 6000 pairs) and the northernmost colony for the species in coastal Patagonia, Argentina. During a 2-day period, we estimate that approximately 86.5% of the chicks died. Our results suggest that the mortality event was heat-related, as consequence of an intense heat wave during the brooding period. During two consecutive days, chicks between 12 and 19 days old were exposed to air temperatures above the historical mean of maxima for a total of 25 h. On one of these days, the air temperature reached a maximum of 38.1 °C with records above 35 °C sustained during four consecutive hours. Chicks were found dead throughout the colony, mostly in the nests with no evidence of external injuries other than occasional scavenging by seagulls. Acute mortality from disease was ruled out based on clinical presentation and negative results for avian influenza virus, saxitoxins, and domoic acid (two common marine toxins). Our work underscores the importance of long-term studies in understanding heat associated breeding failure of one of the largest Imperial Cormorant colonies along its breeding range in coastal Patagonia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and material

Data are available on request to the corresponding author.

Code availability

(software application or custom code) not applicable.

References

  • Abraham CL, Evans RM (1990) The development of endothermy in American white pelicans. Condor 101:832–841

    Article  Google Scholar 

  • Albright TP, Mutiibwa D, Gerson AR, Smith EK, Talbot WA, O’Neill JJ, McKechnie AE, Wolf BO (2017) Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc Natl Acad Sci 114:2283–2288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartholomew GA, Lasiewski RC, Crawford EC (1968) Patterns of panting and gular flutter in cormorants, pelicans, owls, and doves. Condor 70:31–34

    Article  Google Scholar 

  • Bengtsson H (2017) matrixStats: functions that apply to rows and columns of matrices (and to vectors). R package version 0.52.2. https://github.com/HenrikBengtsson/matrixStats

  • Berteaux D, Humphries MM, Krebs CJ, Lima M, McAdam AG, Pettorelli N, Réale D, Saitoh T, Tkadlec E, Weladji RB, Chr SN (2006) Constraints to projecting the effects of climate change on mammals. Clim Res 32:151–158

    Article  Google Scholar 

  • Bodenstein B, Beckmen K, Sheffield G, Kuletz K, Van Hemert C, Berlowski B, Shearn-Bochsler V (2015) Avian cholera causes marine bird mortality in the Bering Sea of Alaska. J Wildlife Dis 51:934–937. https://doi.org/10.7589/2014-12-273

    Article  CAS  Google Scholar 

  • Boyles JG, Seebacher F, Smit B, McKechnie AE (2011) Adaptive thermoregulation in endotherms may alter responses to climate change. Integr Comp Biol 51:676–690

    Article  PubMed  Google Scholar 

  • Bryant DM, Furness RW (1995) Basal metabolic rates of North Atlantic seabirds. Ibis 137:219–226

    Article  Google Scholar 

  • Chen H, Li Y, Li Z, Shi J, Shinya K, Deng G, Qi Q, Tian G, Fan S, Zhao H, Sun Y, Kawaoka Y (2006) Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol 80:5976–5983. https://doi.org/10.1128/JVI.00110-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Conradie SR, Woodborne SM, Cunningham SJ, McKechnie AE (2019) Chronic, sublethal effects of high temperatures will cause severe declines in southern African arid-zone birds during the 21st century. Proc Natl Acad Sci 116:14065–14070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook TR, Jewel OJD, Chivell W, Bester M (2012) An albino cape cormorant Phalacrocorax capensis. Mar Ornithol 40:72–77

    Google Scholar 

  • Cook TR, Martin R, Roberts J, Häkkinen H, Botha P, Meyer C, Sparks E, Underhill LG, Ryan P, Sherley RB (2020) Parenting in a warming world: thermoregulatory responses to heat stress in an endangered seabird. Conserv Physiol 8:coz109

    Article  PubMed  PubMed Central  Google Scholar 

  • Crawford RJM, Allwright DM, He CW (1992) High mortality of Cape Cormorants (Phalacrocorax capensis) off western South Africa in 1991 caused by Pasteurella multocida. Colon Waterbirds 15:236–238. https://doi.org/10.2307/1521458

    Article  Google Scholar 

  • Crick HQ (2004) The impact of climate change on birds. Ibis 146:48–56

    Article  Google Scholar 

  • D’Agostino VC, Krock B, Degrati M, Sastre V, Santinelli N, Krohn T, Hoffmeyer MS (2019) Occurrence of toxigenic microalgal species and phycotoxins accumulation in mesozooplankton in Northern Patagonian gulfs, Argentina. Environ Toxicol Chem 38:2209–2223

    Article  CAS  PubMed  Google Scholar 

  • De Lisle GW, Stanislawek WL, Moors PJ (1990) Pasteurella multocida infections in rockhopper penguins (Eudyptes chrysocome) from Campbell Island, New Zealand. J Wildlife Dis 26:283–285

    Article  Google Scholar 

  • Descamps S, Ramírez F, Benjaminsen S, Anker-Nilssen T, Barrett RT, Burr Z, Christensen-Dalsgaard S, Erikstad KE, Irons DB, Lorentsen SH, Mallory ML, Roberston GJ, Reierten TK, Strøm H, Varpe Ø, Lavergne S (2019) Diverging phenological responses of Arctic seabirds to an earlier spring. Glob Change Biol 25:4081–4409

    Article  Google Scholar 

  • Dunn EH (1976) Development of endothermy and existence energy expenditure of nestling Double-crested Cormorants. Condor 78:350–356

    Article  Google Scholar 

  • Frere E, Quintana F, Gandini P (2005) Cormoranes de la costa patagónica: estado poblacional, ecología y conservación. Hornero 20:35–52

    Google Scholar 

  • Furness RW, Monaghan P (1989) Seabird feeding ecology. In: Seabird ecology. tertiary level biology. Springer, Boston, pp 23–34. https://doi.org/10.1007/978-1-4613-2093-7_3

  • Gabrielsen GW, Mehlum F, Karlsen HE (1988) Thermoregulation in four species of arctic seabirds. J Comp Physiol B 157:703–708

    Article  Google Scholar 

  • Glibert PM, Icarus Allen J, Artioli Y, Beusen A, Bouwman L, Harle J, Holmes R, Holt J (2014) Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis. Glob Change Biol 20:3845–3858. https://doi.org/10.1111/gcb.12662

    Article  Google Scholar 

  • Grémillet D, Boulinier T (2009) Spatial ecology and conservation of seabirds facing global climate change: a review. Mar Ecol Prog Ser 391:121–137

    Article  Google Scholar 

  • Grémillet D, Kuntz G, Woakes AJ, Gilbert C, Robin JP, Le Maho Y, Butler PJ (2005) Year-round recordings of behavioural and physiological parameters reveal the survival strategy of a poorly insulated diving endotherm during the Arctic winter. J Exp Biol 208:4231–4241

    Article  PubMed  Google Scholar 

  • Hochscheid S, Grémillet D, Wanless S, du Plessis MA (2002) Black and white under the South African sun: are juvenile Cape gannets heat stressed? J Therm Biol 27:325–332

    Article  Google Scholar 

  • IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.)]. IPCC, Geneva, Switzerland

  • IPCC (2021) Climate change 2021: the physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change [Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B (eds)]. Cambridge University Press (In Press)

  • Jaeger A, Lebarbenchon C, Bourret V, Bastien M, Lagadec E, Thiebot J-B, Boulinier T, Delord K, Barbraud C, Marteau C, Dellagi K, Tortosa P, Weimerskirch H (2018) Avian cholera outbreaks threaten seabird species on Amsterdam Island. PLoS ONE 13:e0197291. https://doi.org/10.1371/journal.pone.0197291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenouvrier S, Desprez M, Fay R, Barbraud C, Weimerskirch H, Delord K, Caswell H (2018) Climate change and functional traits affect population dynamics of a long-lived seabird. J Anim Ecol 87:906–920

    Article  PubMed  Google Scholar 

  • Jones T, Parrish JK, Peterson WT, Bjorkstedt EP, Bond NA, Ballance LT, Bowes V, Hippfner JM, Burgess HK, Dolliver JE, Lindquist K, Lindsey J, Nevins HM, Roberston RR, Roletto J, Wilson L, Joyce T, Harvey J (2018) Massive mortality of a planktivorous seabird in response to a marine heatwave. Geophys Res Lett 45:3193–3202. https://doi.org/10.1002/2017GL076164

    Article  Google Scholar 

  • Keogan K, Daunt F, Wanless S, Phillips RA, Walling CA, Agnew P, Ainley DG, Anker-Nilssen T, Ballard G, Barret RT, Barton KJ (2018) Global phenological insensitivity to shifting ocean temperatures among seabirds. Nat Clim Change 8:313–318

    Article  Google Scholar 

  • Kuiken T (1999) Review of Newcastle disease in cormorants. Waterbirds 22:333–347

    Article  Google Scholar 

  • Lasiewski RC, Snyder GK (1969) Responses to high temperature in nestling double-crested and pelagic cormorants. Auk 86:529–540

    Article  Google Scholar 

  • Malacalza VE (1984) Aves Guaneras. Relevamiento de especies en tres cormoraneras continentales de la Provincia del Chubut (Argentina) (Pelecaniformes-Phalacrocoracidae). Centro Nacional Patagónico 84:1–13

    Google Scholar 

  • McKechnie AE, Wolf BO (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Lett 6:253–256

    Article  PubMed  Google Scholar 

  • McKechnie AE, Rushworth IA, Myburgh F, Cunningham SJ (2021) Mortality among birds and bats during a extreme heat event in easter South Africa. Austral Ecol 46:687–691

    Article  Google Scholar 

  • McLeod AI (2011) Kendall: Kendall rank correlation and Mann-Kendall trend test. R package version 2.2. https://CRAN.R-project.org/package=Kendall

  • Mitchell D, Snelling EP, Hetem RS, Maloney SK, Strauss WM, Fuller A (2018) Revisiting concepts of thermal physiology: predicting responses of mammals to climate change. J Anim Ecol 87:956–973

    Article  PubMed  Google Scholar 

  • Molini M, Aikukutu G, Roux JP, Kemper J, Ntahonshikira C, Marruchella G, Khaiseb S, Cattoli G, Dundon WG (2020) Avian influenza H5N8 outbreak in African Penguins (Spheniscus demersus), Namibia, 2019. J Wildlife Dis 56:214–218. https://doi.org/10.7589/2019-03-067

    Article  CAS  Google Scholar 

  • Nelson B (2005) Pelicans, cormorants, and their relatives. Oxford University Press, Oxford

    Google Scholar 

  • Osborne OE, Hara PD, Whelan S, Zandbergen P, Hatch SA, Elliott KH (2020) Breeding seabirds increase foraging range in response to an extreme marine heatwave. Mar Ecol Prog Ser 646:161–173

    Article  Google Scholar 

  • Oswald SA, Arnold JM (2012) Direct impacts of climatic warming on heat stress in endothermic species: seabirds as bioindicators of changing thermoregulatory constraints. Integr Zool 7:121–136

    Article  PubMed  Google Scholar 

  • Ovaskainen O, Skorokhodova S, Yakovleva M, Sukhov A, Kutenkov A, Kutenkova N, Shcherbakov A, Meyke E, Delgado MdM (2013) Community-level phenological response to climate change. Proc Natl Acad Sci 110:13434–13439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950–2010. PLoS ONE 10:e0129342

    Article  PubMed  PubMed Central  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Piatt JF, Parrish JK, Renner HM, Schoen SK, Jones TT, Arimitsu ML, Kuletz KJ, Bodenstein B, García-Reyes M, Duerr RS et al (2020) Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014–2016. PLoS ONE 15:e0226087. https://doi.org/10.1371/journal.pone.0226087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porter WP, Kearney M (2009) Size, shape, and the thermal niche of endotherms. Proc Natl Acad Sci 106:19666–19672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692

    Article  PubMed  Google Scholar 

  • Quintana F, Wilson RP, Prandoni N, Svagelj WS, Gómez-Laich A (In press) Long-term ecology studies in Patagonian seabirds: a review with the Imperial Cormorant as a case study. In: Helbling W, Villafañe V, Narvarte M, Gonzalez R (eds) Global change in Atlantic coastal Patagonian ecosystems: a journey through time. Springer, Berlin

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing: 2019, Vienna, Austria. https://www.r-project.org

  • Schreiber EA, Burger J (2001) Seabirds in the marine environment. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Washington, pp 19–34

    Chapter  Google Scholar 

  • Shumway SE, Allen SM, Boersma PD (2003) Marine birds and harmful algal blooms: sporadic victims or under-reported events? Harmful Algae 2:1–17. https://doi.org/10.1016/S1568-9883(03)00002-7

    Article  Google Scholar 

  • Smit B, Zietsman G, Martin RO, Cunningham SJ, McKechnie AE, Hockey PAR (2016) Behavioural responses to heat in desert birds: implications for predicting vulnerability to climate warming. Clim Change Responses 3:1–14. https://doi.org/10.1186/s40665-016-0023-2

    Article  Google Scholar 

  • Somveille M, Dias MP, Weimerskirch H, Davies TE (2020) Projected migrations of southern Indian Ocean albatrosses as a response to climate change. Ecography 43:1683–1691

    Article  Google Scholar 

  • Svagelj W, Quintana F (2011) Breeding performance of the Imperial Shag (Phalacrocorax atriceps) in relation to year, laying date and nest location. Emu 111:162–165

    Article  Google Scholar 

  • Sydeman WJ, Poloczanska E, Reed TE, Thompson SA (2015) Climate change and marine vertebrates. Science 350:772–777

    Article  CAS  PubMed  Google Scholar 

  • Uhart M, Karesh W, Cook R (2008) ¿Es el Mar Patagónico un ecosistema saludable? In: Estado de Conservación del Mar Patagónico y Áreas de Influencia. Foro para la Conservación del Mar Patagónico y Áreas de Influencia. Latingráfica, Buenos Aires, pp 303–324. http://www.marpatagonico.org

  • Urban MC (2015) Accelerating extinction risk from climate change. Science 348:571–573

    Article  CAS  PubMed  Google Scholar 

  • Van Hemert C, Schoen SK, Wayne Litaker R, Smith MM, Arimitsu ML, Piatt JF, Holland WC, Ransom Hardison D, Pearce JM (2020) Algal toxins in Alaskan seabirds: evaluating the role of saxitoxin and domoic acid in a large-scale die-off of Common Murres. Harmful Algae 92:101730. https://doi.org/10.1016/j.hal.2019.101730

    Article  CAS  PubMed  Google Scholar 

  • Waller LJ, Underhill LG (2007) Management of avian cholera Pasteurella multocida outbreaks on Dyer Island, South Africa, 2002–2005. Afr J Mar Sci 29:105–111. https://doi.org/10.2989/AJMS.2007.29.1.9.74

    Article  Google Scholar 

  • Whittow GC, Tazawa H (1991) The early development of thermoregulation in birds. Physiol Zool 64:1371–1390

    Article  Google Scholar 

  • Wilson C, Sastre AV, Hoffmeyer M, Rowntree VJ, Fire SE, Santinelli NH, Diaz Ovejero S, D´AgostinoMarónDoucette VCFGJ et al (2016) Southern right whale (Eubalaena australis) calf mortality at Península Valdés, Argentina: are harmful algal blooms to blame? Mar Mamm Sci 32:423–451

    Article  CAS  Google Scholar 

  • Work TM, Barr B, Beale AM, Fritz L, Quilliam MA, Wright JL (1993) Epidemiology of domoic acid poisoning in brown pelicans (Pelecanus occidentalis) and Brandt’s cormorants (Phalacrocorax penicillatus) in California. J Zoo Wildl Med 24:54–62

    Google Scholar 

  • Yorio P, Quintana F, Campagna C, Harris G (1994) Diversidad, abundancia y dinámica espacio-temporal de la colonia mixta de aves marinas en Punta León, Patagonia. Ornitol Neotrop 5:69–77

    Google Scholar 

  • Yorio P, Frere E, Gandini P, Harris G (1998) Atlas de la distribución reproductiva y abundancia de aves marinas del litoral patagónico Argentino. Fundación Patagonia Natural and Wildlife Conservation Society

  • Yorio P, Frere E, Gandini P, Conway W (1999) Status and conservation of seabirds breeding in Argentina. Bird Conserv Int 9:299–314

    Article  Google Scholar 

  • Yorio P, Pozzi L, Herrera G, Punta G, Svagelj WS, Quintana F (2020) Population trends of Imperial Cormorants (Leucocarbo atriceps) in northern coastal Argentine Patagonia over 26 years. Emu 120:114–122

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Pierre Anton Pistorius, Dr. Katrin Ludynia, one anonymous referee, and the editor Dr. Dieter for their suggestions that improved the manuscript. We express our gratitude to Tinio Resnik who reported the cormorant mortality on December 17th, 2016. We also thank La Chola, Miguel, Nicolás Prandoni, and Estancia El Pedral for assistance in various aspects of this research. We acknowledge Dr. Takashi Yamamoto for the pictures taken at the colony on our visit on December 20th, 2016. We specially thank W. Helbling for helpful comments on early versions of the manuscript and N. Montoya from Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP) for her help with the toxicological analysis. Logistical and institutional support was provided by the Instituto de Biología de Organismos Marinos (IBIOMAR-CONICET) and the One Health Institute, University of California, Davis. We thank the Ministerio de Desarrollo Territorial y Sectores Productivos and the Secretaría de Turismo de la Provincia de Chubut, Argentina, for the permits to work at Punta León protected area (permit 2016: 096-SsCyAP/16).

Funding

This study was funded by grants from the National Agency for Scientific and Technological Promotion of Argentina (PICT 2013 – 1229), the National Institute of Allergy and Infectious Diseases (NIAID) Center for Research on Influenza Pathogenesis (CRIP) (contract HHSN272201400008C), and the Instituto Nacional de Tecnología Agropecuaria (INTA) (PNSA 1115052 and PNSA 1115056).

Author information

Authors and Affiliations

  1. Instituto de Biología de Organismos Marinos, Consejo Nacional de Investigaciones Científicas y Técnicas, Puerto Madryn, Chubut, Argentina

    Flavio Quintana & Luciana Gallo

  2. One Health Institute, School of Veterinary Medicine, University of California, Davis, USA

    Marcela M. Uhart

  3. Instituto Nacional de Investigación y Desarrollo Pesquero, Mar del Plata, Buenos Aires, Argentina

    María Belén Mattera

  4. Instituto de Virologia, Centro de Investigación en Ciencias Veterinarias y Agronómicas, Instituto Nacional de Tecnología Agropecuaria, Castelar, Buenos Aires, Argentina

    Agustina Rimondi

  5. Departamento de Ecología, Genética y Evolución & Instituto de Ecología, Genética y Evolución de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

    Agustina Gómez-Laich

Authors
  1. Flavio Quintana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcela M. Uhart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luciana Gallo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Belén Mattera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Agustina Rimondi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Agustina Gómez-Laich
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FQ, AGL, and MU conceptualized the initial research question. AGL, MU, and LG collected the data. AGL completed statistical analysis with the help of FQ. MBM performed the toxicological analysis, and AR performed the virological testing. FQ wrote the original manuscript. AGL, MU, and LG contributed to reviewing and editing. FQ and MU acquired funding. All authors read and approved the manuscript.

Corresponding author

Correspondence to Flavio Quintana.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest/competing interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quintana, F., Uhart, M.M., Gallo, L. et al. Heat-related massive chick mortality in an Imperial Cormorant Leucocarbo atriceps colony from Patagonia, Argentina. Polar Biol 45, 275–284 (2022). https://doi.org/10.1007/s00300-021-02982-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-021-02982-6

Keywords

Search

Navigation