Skip to main content

Advertisement

SpringerLink
Log in

Cold birds under pressure: Can thermal substitution ease heat loss in diving penguins?

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Thermoregulation could represent a significant fraction of the total energy budget of endotherms under unfavourable environmental conditions. This cost affects several traits of the ecology of an organism such as its behaviour, distribution, or life history. Heat produced by muscle contraction during activity can be used to pay for heat loss or thermoregulation in many species (known as “thermal substitution”). This study seeks to unite the effects of temperature, depth, and activity on the energetic costs of endotherm divers using the Magellanic penguin as model species and to evaluate whether penguins may benefit from thermal substitution. This species operates under highly variable temperature and depth conditions along its breeding range and provides an ideal natural experiment. A developed thermodynamic model describing foraging activity predicted that the major element affecting heat loss was depth, exacerbated by temperature. Birds living in colder waters are predicted to be able to minimize costs by executing shallower dives and benefit from thermal substitution by swimming faster, particularly during deeper dives. The model was evaluated in two contrasting scenarios: (1) when birds swim near the surface commuting to the foraging areas and (2) when birds dive to depth to forage. Activity data from tags on free-living penguins indicated two of these predictions were apparent; penguins generally travelled faster while commuting at the surface in colder waters, while birds from warmer water colonies dived deeper while foraging. Contrary to predictions, however, penguins swam slower at deeper depths during both descent and ascent phases of foraging dives. These results suggest that penguins may benefit from thermal substitution by swimming faster when birds perform shallow dives commuting to and back from foraging areas, but they provide no evidence of behavioural response (via swimming faster) for thermoregulation when diving to depth to forage. Reasons for this are discussed and include the relevance of prey abundance in 3-d space and maximizing dive duration by conserving oxygen reserves. The way the bird operates will have profound consequences for the energy needed and therefore necessary energy acquisition rates. Expansion of our findings to other diving endotherms might help explain both global activity patterns and energy flow in ecosystems.

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

References

  • Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Intregr Comp Biol 44:498–509

    Article  Google Scholar 

  • Bannasch R, Wilson RP, Culik B (1994) Hydrodynamic aspects of design and attachment of a back-mounted device in penguins. J Exp Biol 194(1):83–96

    Google Scholar 

  • Baudinette R, Gill P (1985) The energetics of flying and paddling in water: locomotion in penguins and ducks. J Comp Physiol B Biochem Syst Environ Physiol 155:373–380

    Article  Google Scholar 

  • Bevan R, Boyd I, Butler P, Reid K, Woakes A, Croxall J (1997) Heart rates and abdominal temperatures of free-ranging South Georgian shags, Phalacrocorax georgianus. J Exp Biol 200:661–675

    Google Scholar 

  • Boersma PD, Rebstock GA, Frere E, Moore SE (2009) Following the fish: penguins and productivity in the South Atlantic. Ecol Monogr 79:59–76

    Article  Google Scholar 

  • Boyd IL (2002) Estimating food consumption of marine predators: Antarctic fur seals and macaroni penguins. J Appl Ecol 39:103–119

    Article  Google Scholar 

  • Brody S (1945) Bioenergetics and growth. Reinhold, New York

    Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Buckley LB, Hurlbert AH, Jetz W (2012) Broad-scale ecological implications of ectothermy and endothermy in changing environments. Glob Ecol Biogeogr 21:873–885

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Casarsa L (2005) Morfología y comportamiento de los cardúmenes de sardina fueguina (Sprattus fuegensis) en dos sectores característicos del Atlántico Sudoccidental. Bachellor thesis, Mar del Plata

  • Ciancio EJ, Botto F, Frere E (2015) Combining a geographic information system, dietary and habitat preferences, and stable isotope analysis to infer Magellanic Penguin diet in their austral distribution. Emu. doi:10.1071/MU14032_AC

    Google Scholar 

  • Culik B, Wilson R (1991) Energetics of under-water swimming in Adelie penguins (Pygoscelis adeliae). J Comp Physiol B 161:285–291

    Article  Google Scholar 

  • Culik BM, Wilson RP (1992) Field metabolic rates of instrumented Adélie penguins using double-labelled water. J Comp Physiol B Biochem Syst Environ Physiol 162:567–573

    Article  Google Scholar 

  • Culik B, Wilson R, Bannasch R (1994) Underwater swimming at low energetic cost by Pygoscelid Penguins. J Exp Biol 197:65–78

    Google Scholar 

  • Culik BM, Putz K, Wilson RP, Allers D, Lage J, Bost CA, Le Maho Y (1996) Diving energetics in king penguins (Aptenodytes patagonicus). J Exp Biol 199:973–983

    CAS  Google Scholar 

  • De Vries J, Van Eerden MR (1995) Thermal conductance in aquatic birds in relation to the degree of water contact, body mass, and body fat: energetic implications of living in a strong cooling environment. Physiol Zool 68:1143–1163

    Article  Google Scholar 

  • Enstipp MR, Grémillet D, Jones DR (2006) The effects of depth, temperature and food ingestion on the foraging energetics of a diving endotherm, the double-crested cormorant (Phalacrocorax auritus). J Exp Biol 209:845–859

    Article  Google Scholar 

  • Fahlman A, Schmidt A, Handrich Y, Woakes AJ, Butler PJ (2005) Metabolism and thermoregulation during fasting in king penguins, Aptenodytes patagonicus, in air and water. Am J Physiol Regul Integr Comp Physiol 289:670–679

    Article  Google Scholar 

  • Fort J, Porter WP, Grémillet D (2009) Thermodynamic modelling predicts energetic bottleneck for seabirds wintering in the northwest Atlantic. J Exp Biol 212:2483–2490

    Article  Google Scholar 

  • Frere E, Gandini P, Lichstein V (1996) Variación latitudinal en la dieta del Pinguino de Magallanes Spheniscus magellanicus. Ornitología Neotropical 7:35–41

    Google Scholar 

  • Gaesser GA, Brooks GA (1975) Muscular efficiency during steady-rate exercise: effects of speed and work rate. J Appl Physiol 38:1132–1139

    CAS  Google Scholar 

  • Garthe S, Ludynia K, Hüppop O, Kubetzki U, Meraz J, Furness R (2012) Energy budgets reveal equal benefits of varied migration strategies in northern gannets. Mar Biol 159:1907–1915

    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, Tuschy I, Kierspel M (1998) Body temperature and insulation in diving great cormorants and European shags. Funct Ecol 12:386–394

    Article  Google Scholar 

  • Groscolas R (1986) Changes in body mass, body temperature and plasma fuel levels during the natural breeding fast in male and female emperor penguins Aptenodytes forsteri. Comp Biochem Physiol B 156(4):521–527

    Google Scholar 

  • Handrich Y, Bevan RM, Charrassin JB, Butler PJ, Ptz K, Woakes AJ, Lage J, Maho YL (1997) Hypothermia in foraging king penguins. Nature 388:64–67

    Article  CAS  Google Scholar 

  • Hansen JE, Martos P, Madirolas A (2001) Relationship between spatial distribution of the Patagonian stock of Argentine anchovy, Engraulis anchoita, and sea temperatures during late spring to early summer. Fish Oceanogr 10:193–206

    Article  Google Scholar 

  • Hilborn R, Mangel M (1997) The ecological detective: confronting models with data. Princeton University Press, New Jersey

    Google Scholar 

  • Hind AT, Gurney WS (1997) The metabolic cost of swimming in marine homeotherms. J Exp Biol 200:531–542

    CAS  Google Scholar 

  • Hinke J, Trivelpiece W (2011) Daily activity and minimum food requirements during winter for gentoo penguins (Pygoscelis papua) in the South Shetland Islands, Antarctica. Polar Biol 34:1579–1590

    Article  Google Scholar 

  • Hudson DM, Bernstein MH (1981) Temperature regulation and heat balance in flying white-necked ravens, Corvus cryptoleucus. J Exp Biol 90(1):267–281

    Google Scholar 

  • Humphries MM, Careau V (2011) Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution. Intregr Comp Biol 51:419–431

    Article  Google Scholar 

  • Humphries MM, McCann KS (2014) Metabolic ecology. J Anim Ecol 83:7–19

    Article  Google Scholar 

  • Kaseloo PA, Lovvorn JR (2005) Effects of surface activity patterns and dive depth on thermal substitution in fasted and fed lesser scaup (Aythya affinis) ducks. Can J Zool 83:301–311

    Article  Google Scholar 

  • Kaseloo P, Lovvorn J (2006) Substitution of heat from exercise and digestion by ducks diving for mussels at varying depths and temperatures. J Comp Physiol B Biochem Syst Envir Physiol 176:265–275

    Article  CAS  Google Scholar 

  • Kojeszewski T, Fish FE (2007) Swimming kinematics of the Florida manatee (Trichechus manatus latirostris): hydrodynamic analysis of an undulatory mammalian swimmer. J Exp Biol 210:2411–2418

    Article  Google Scholar 

  • Kooyman GL, Gentry RL, Bergman WP, Hammel HT (1976) Heat loss in penguins during immersion and compression. Comp Biochem Physiol A Comp Physiol 54:75–80

    Article  CAS  Google Scholar 

  • Kvadsheim PH, Folkow LP, Blix AS (2005) Inhibition of shivering in hypothermic seals during diving. Am J Physiol-Regul Integr Comp Physiol 289:326–331

    Article  Google Scholar 

  • Kvist A, Lindstrom A, Green M, Piersma T, Visser GH (2001) Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413:730–732

    Article  CAS  Google Scholar 

  • Le Maho Y (1977) The emperor penguin: a strategy to live and breed in the cold: morphology, physiology, ecology, and behavior distinguish the polar emperor penguin from other penguin species, particularly from its close relative, the king penguin. Am Sci 65:680–693

    Google Scholar 

  • Liwanag HEM, Williams TM, Costa DP, Kanatous SB, Davis RW, Boyd IL (2009) The effects of water temperature on the energetic costs of juvenile and adult California sea lions (Zalophus californianus): the importance of skeletal muscle thermogenesis for thermal balance. J Exp Biol 212:3977–3984

    Article  CAS  Google Scholar 

  • Lovvorn JR (2007) Thermal substitution and aerobic efficiency: measuring and predicting effects of heat balance on endotherm diving energetics. Philos Trans R Soc Lond B Biol Sci 362:2079–2093

    Article  CAS  Google Scholar 

  • Luna-Jorquera G, Culik BM (2000) Metabolic rates of swimming Humboldt penguins. Mar Ecol Prog Ser 203:301–309

    Article  CAS  Google Scholar 

  • Luque S (2007) Diving behaviour analysis in R. R News 7:8–15

    Google Scholar 

  • McCafferty DJ, Moncrieff JB, Taylor IR (1997) The effect of wind speed and wetting on thermal resistance of the barn owl (Tyto alba). I: total heat loss, boundary layer and total resistance. J Therm Biol 22:253–264

    Article  Google Scholar 

  • McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol Part A Mol Integr Physiol 144:381–394

    Article  CAS  Google Scholar 

  • Mcnab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, New York

    Google Scholar 

  • McNamara J, Ekman J, Houston IA (2004) The effect of thermoregulatory substitution on optimal energy reserves of small birds in winter. Oikos 105:192–196

    Article  Google Scholar 

  • Mitchell JW (1976) Heat transfer from spheres and other animal forms. Biophys J 16:561–569

    Article  CAS  Google Scholar 

  • Peters G (1997) Die Regulation der Verdauugsprozesse bei Pinguinen (Spheniscidae). PhD thesis. Christian-Albrechts University Kiel

  • Pinheiro JC, Bates DM (2001) Mixed-effects models in S and S-PLUS. Springer, New York

    Google Scholar 

  • Ponganis P, Van Dam R, Knower T, Levenson D (2001) Temperature regulation in emperor penguins foraging under sea ice. Comp Biochem Physiol A Comp Physiol 129:811–820

    Article  CAS  Google Scholar 

  • Ponganis PJ, Van RP, Levenson DH, Knower T, Ponganis KV, Marshall G (2003) Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice. Comp Biochem Physiol A Comp Physiol 135:477–487

    Article  CAS  Google Scholar 

  • Porter WP, Gates DM (1969) Thermodynamic equilibria of animals with environment. Ecol Monogr 39:227–244

    Article  Google Scholar 

  • Porter WP, Vakharia N, Klousie WD, Duffy D (2006) Po’ouli landscape bioinformatics models predict energetics, behavior, diets, and distribution on Maui. Intregr Comp Biol 46:1143–1158

    Article  CAS  Google Scholar 

  • Prinzinger R, Pressmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol A Comp Physiol 99:499–506

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. In: Computing RFfS (ed), Vienna, Austria

  • Richman SE, Lovvorn JR (2011) Effects of air and water temperatures on resting metabolism of auklets and other diving birds. Physiol Biochem Zool 84:316–332

    Article  Google Scholar 

  • Sala JE, Wilson RP, Frere E, Quintana F (2012) Foraging effort in Magellanic penguins in coastal Patagonia, Argentina. Mar Ecol Prog Ser 464:273–287

    Article  Google Scholar 

  • Schiavini A, Yorio P, Gandini P, Raya Rey A, Boersma D (2005) Los pingüinos de las costas argentinas: estado y Conservación. El Hornero 20(1):5–23

    Google Scholar 

  • Schmidt Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Schmidt A, Alard F, Handrich Y (2006) Changes in body temperatures in king penguins at sea: the result of fine adjustments in peripheral heat loss? Am J Physiol-Regul Integrat Comp Physiol 291:608–618

    Article  Google Scholar 

  • Scolaro JA, Wilson RP, Laurenti S, Kierspel M, Gallelli H, Upton J (1999) Feeding preferences of the Magellanic Penguin over its breeding range in Argentina. Waterbirds 22:104–110

    Article  Google Scholar 

  • Sparling CE, Fedak MA, Thompson D (2007) Eat now, pay later? Evidence of deferred food-processing costs in diving seals. Biol Lett 3:95–99

    Article  Google Scholar 

  • Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726–746

    Google Scholar 

  • Stahel C, Nicol S (1982) Temperature regulation in the little penguin, Eudyptula minor, in air and water. J Comp Physiol B Biochem Syst Environ Physiol 148:93–100

    Article  Google Scholar 

  • Takahashi A, Dunn MJ, Trathan PN, Croxall JP, Wilson RP, Sato K, Naito Y (2004) Krill-feeding behaviour in a chinstrap penguin compared to fish-eating in Magellanic penguins: a pilot study. Mar Ornithol 32:47–54

    Google Scholar 

  • Tucker VA (1975) The energetic cost of moving about: walking and running are extremely inefficient forms of locomotion. Much greater efficiency is achieved by birds, fishes and bicyclists. Am Sci 63:413–419

    CAS  Google Scholar 

  • Walsberg GE, King J (1978) The relationship of the external surface area of birds to skin surface area and body mass. J Exp Biol 76(1):185–189

    Google Scholar 

  • Williams TD (1995) The penguins: Spheniscidae. In: Perrins CM, Bock WJ, Kikkawa J (eds) Bird families of the world. Oxford University Press, Oxford, p 295

    Google Scholar 

  • Wilson RP, Culik BM (1991) The cost of a hot meal: facultative specific dynamic action may ensure temperature homeostasis in post-ingestive endotherms. Comp Biochem Physiol A Physiol 100:151–154

    Article  CAS  Google Scholar 

  • Wilson RP, Grémillet D (1996) Body temperatures of free-living African penguins (Spheniscus demersus) and bank cormorants (Phalacrocorax neglectus). J Exp Biol 199:2215–2223

    CAS  Google Scholar 

  • Wilson RP, Hustler K, Ryan PG, Burger AE, Noldeke EC (1992) Diving birds in cold water: do Archimedes and Boyle determine energetic costs? Am Nat 144(2):179–200

  • Wilson RP, Pütz K, Grémillet D, Culik BM, Kierspel M, Regel J, Bost CA, Lage J, Cooper J (1995) Reliability of stomach temperature changes in determining feeding characteristics of seabirds. J Exp Biol 198:1115–1135

    Google Scholar 

  • Wilson RP, Putz K, Peters G, Culik B, Scolaro JA, Charrassin J-B, Ropert-Coudert Y (1997) Long-term attachment of transmitting and recording devices to penguins and other seabirds. Wildl Soc Bull 25:101–106

    Google Scholar 

  • Wilson RP, Adelung D, Latorre L (1998) Radiative heat loss in gentoo penguin (Pygoscelis papua) adults and chicks and the importance of warm feet. Physiol Biochem Zool 71(5):524–533

    CAS  Google Scholar 

  • Wilson RP, Ropert-Coudert Y, Kato A (2002) Rush and grab strategies in foraging marine endotherms: the case for haste in penguins. Anim Behav 63:85–95

    Article  Google Scholar 

  • Wilson RP, Kreye JM, Lucke K, Urquhart H (2004) Antennae on transmitters on penguins: balancing energy budgets on the high wire. J Exp Biol 207:2649–2662

    Article  Google Scholar 

  • Wilson RP, Scolaro JA, Grémillet D, Kierspel MAM, Laurenti S, Upton J, Gallelli H, Quintana F, Frere E, Muller G, Straten MT, Zimmer I (2005) How do Magellanic penguins cope with variability in their access to prey? Ecol Monogr 75:379–401

    Article  Google Scholar 

  • Wilson RP, Shepard ELC, Liebsch N (2008) Prying into the intimate details of animal lives: use of a daily diary on animals. Endang Species Res 4:123–137

    Article  Google Scholar 

  • Wilson RP, Shepard ELC, Gomez Laich A, Frere E, Quintana F (2010) Pedalling downhill and freewheeling up; a penguin perspective on foraging. Aquat Biol 8:193–202

    Article  Google Scholar 

  • Wilson RP, McMahon CR, Quintana F, Frere E, Scolaro A, Hays GC, Bradshaw CJ (2011) N-dimensional animal energetic niches clarify behavioural options in a variable marine environment. J Exp Biol 214:646–656

    Article  Google Scholar 

  • Yorio P, Quintana F, Dell'Arciprete P, González-Zevallos D (2010) Spatial overlap between foraging seabirds and trawl fisheries: implications for the effectiveness of a marine protected area at Golfo San Jorge, Argentina. Bird Conserv Int 20:320–334

    Article  Google Scholar 

  • Zuur A, Ieno E, Walker N, Saveliev A, Smith G (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

This research was founded by Agencia de Promoción Científica y Tecnológica (PICT 2010-203), CONICET (PIP 11220110100634) and Wildlife Conservation Society. We thank A. Gagliardini and J. Baba for assistance in satellite image analysis A. Rivas made great comments to the manuscript and model. All device deployments were performed under permits of Dirección de Fauna y Flora Silvestre of Chubut and Consejo Agrario of Santa Cruz.

Author information

Authors and Affiliations

  1. IBIOMAR, Centro Nacional Patagónico, Blvd. Brown 2915, 9120, Puerto Madryn, Chubut, Argentina

    Javier Ernesto Ciancio, Flavio Quintana & Juan Emilio Sala

  2. Wildlife Conservation Society, Amenabar 1595, C1426AKC, Ciudad Autónoma de Buenos Aires, Argentina

    Flavio Quintana

  3. Biosciences, College of Science, Swansea University, Swansea, SA2 8PP, UK

    Rory P. Wilson

Authors
  1. Javier Ernesto Ciancio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Flavio Quintana
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan Emilio Sala
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rory P. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javier Ernesto Ciancio.

Additional information

Responsible Editor: S. Garthe.

Reviewed by Undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ciancio, J., Quintana, F., Sala, J. et al. Cold birds under pressure: Can thermal substitution ease heat loss in diving penguins?. Mar Biol 163, 43 (2016). https://doi.org/10.1007/s00227-016-2813-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2813-2

Keywords

Search

Navigation