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

详细信息    查看全文

• 作者：Javier Ernesto Ciancio ; Flavio Quintana ; Juan Emilio Sala ; Rory P. Wilson
• 刊名：Marine Biology
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：163
• 期：2
• 全文大小：1,305 KB
• 参考文献：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 44:498–509CrossRef
  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
  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 155:373–380CrossRef
  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
  Boersma PD, Rebstock GA, Frere E, Moore SE (2009) Following the fish: penguins and productivity in the South Atlantic. Ecol Monogr 79:59–76CrossRef
  Boyd IL (2002) Estimating food consumption of marine predators: Antarctic fur seals and macaroni penguins. J Appl Ecol 39:103–119CrossRef
  Brody S (1945) Bioenergetics and growth. Reinhold, New York
  Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRef
  Buckley LB, Hurlbert AH, Jetz W (2012) Broad-scale ecological implications of ectothermy and endothermy in changing environments. Glob Ecol Biogeogr 21:873–885CrossRef
  Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837
  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
  Culik B, Wilson R (1991) Energetics of under-water swimming in Adelie penguins (Pygoscelis adeliae). J Comp Physiol B 161:285–291CrossRef
  Culik BM, Wilson RP (1992) Field metabolic rates of instrumented Adélie penguins using double-labelled water. J Comp Physiol B Biochem Syst Environ Physiol 162:567–573CrossRef
  Culik B, Wilson R, Bannasch R (1994) Underwater swimming at low energetic cost by Pygoscelid Penguins. J Exp Biol 197:65–78
  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
  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 68:1143–1163CrossRef
  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 209:845–859CrossRef
  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 289:670–679CrossRef
  Fort J, Porter WP, Grémillet D (2009) Thermodynamic modelling predicts energetic bottleneck for seabirds wintering in the northwest Atlantic. J Exp Biol 212:2483–2490CrossRef
  Frere E, Gandini P, Lichstein V (1996) Variación latitudinal en la dieta del Pinguino de Magallanes Spheniscus magellanicus. Ornitología Neotropical 7:35–41
  Gaesser GA, Brooks GA (1975) Muscular efficiency during steady-rate exercise: effects of speed and work rate. J Appl Physiol 38:1132–1139
  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 159:1907–1915CrossRef
  Grémillet D, Boulinier T (2009) Spatial ecology and conservation of seabirds facing global climate change: a review. Mar Ecol Prog Ser 391:121–137CrossRef
  Grémillet D, Tuschy I, Kierspel M (1998) Body temperature and insulation in diving great cormorants and European shags. Funct Ecol 12:386–394CrossRef
  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
  Handrich Y, Bevan RM, Charrassin JB, Butler PJ, Ptz K, Woakes AJ, Lage J, Maho YL (1997) Hypothermia in foraging king penguins. Nature 388:64–67CrossRef
  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 10:193–206CrossRef
  Hilborn R, Mangel M (1997) The ecological detective: confronting models with data. Princeton University Press, New Jersey
  Hind AT, Gurney WS (1997) The metabolic cost of swimming in marine homeotherms. J Exp Biol 200:531–542
  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 34:1579–1590CrossRef
  Hudson DM, Bernstein MH (1981) Temperature regulation and heat balance in flying white-necked ravens, Corvus cryptoleucus. J Exp Biol 90(1):267–281
  Humphries MM, Careau V (2011) Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution. Intregr Comp Biol 51:419–431CrossRef
  Humphries MM, McCann KS (2014) Metabolic ecology. J Anim Ecol 83:7–19CrossRef
  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 83:301–311CrossRef
  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 176:265–275CrossRef
  Kojeszewski T, Fish FE (2007) Swimming kinematics of the Florida manatee (Trichechus manatus latirostris): hydrodynamic analysis of an undulatory mammalian swimmer. J Exp Biol 210:2411–2418CrossRef
  Kooyman GL, Gentry RL, Bergman WP, Hammel HT (1976) Heat loss in penguins during immersion and compression. Comp Biochem Physiol A Comp Physiol 54:75–80CrossRef
  Kvadsheim PH, Folkow LP, Blix AS (2005) Inhibition of shivering in hypothermic seals during diving. Am J Physiol-Regul Integr Comp Physiol 289:326–331CrossRef
  Kvist A, Lindstrom A, Green M, Piersma T, Visser GH (2001) Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413:730–732CrossRef
  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
  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 212:3977–3984CrossRef
  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 362:2079–2093CrossRef
  Luna-Jorquera G, Culik BM (2000) Metabolic rates of swimming Humboldt penguins. Mar Ecol Prog Ser 203:301–309CrossRef
  Luque S (2007) Diving behaviour analysis in R. R News 7:8–15
  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 22:253–264CrossRef
  McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol Part A Mol Integr Physiol 144:381–394CrossRef
  Mcnab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, New York
  McNamara J, Ekman J, Houston IA (2004) The effect of thermoregulatory substitution on optimal energy reserves of small birds in winter. Oikos 105:192–196CrossRef
  Mitchell JW (1976) Heat transfer from spheres and other animal forms. Biophys J 16:561–569CrossRef
  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
  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 129:811–820CrossRef
  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 135:477–487CrossRef
  Porter WP, Gates DM (1969) Thermodynamic equilibria of animals with environment. Ecol Monogr 39:227–244CrossRef
  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 46:1143–1158CrossRef
  Prinzinger R, Pressmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol A Comp Physiol 99:499–506CrossRef
  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 84:316–332CrossRef
  Sala JE, Wilson RP, Frere E, Quintana F (2012) Foraging effort in Magellanic penguins in coastal Patagonia, Argentina. Mar Ecol Prog Ser 464:273–287CrossRef
  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
  Schmidt Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge
  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 291:608–618CrossRef
  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 22:104–110CrossRef
  Sparling CE, Fedak MA, Thompson D (2007) Eat now, pay later? Evidence of deferred food-processing costs in diving seals. Biol Lett 3:95–99CrossRef
  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
  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 148:93–100CrossRef
  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
  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
  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
  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
  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 100:151–154CrossRef
  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
  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
  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
  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
  Wilson RP, Ropert-Coudert Y, Kato A (2002) Rush and grab strategies in foraging marine endotherms: the case for haste in penguins. Anim Behav 63:85–95CrossRef
  Wilson RP, Kreye JM, Lucke K, Urquhart H (2004) Antennae on transmitters on penguins: balancing energy budgets on the high wire. J Exp Biol 207:2649–2662CrossRef
  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 75:379–401CrossRef
  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 4:123–137CrossRef
  Wilson RP, Shepard ELC, Gomez Laich A, Frere E, Quintana F (2010) Pedalling downhill and freewheeling up; a penguin perspective on foraging. Aquat Biol 8:193–202CrossRef
  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 214:646–656CrossRef
  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 20:320–334CrossRef
  Zuur A, Ieno E, Walker N, Saveliev A, Smith G (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRef
  
• 作者单位：Javier Ernesto Ciancio (1)
  Flavio Quintana (1) (2)
  Juan Emilio Sala (1)
  Rory P. Wilson (3)
  
  1. IBIOMAR, Centro Nacional Patagónico, Blvd. Brown 2915, 9120, Puerto Madryn, Chubut, Argentina
  2. Wildlife Conservation Society, Amenabar 1595, C1426AKC, Ciudad Autónoma de Buenos Aires, Argentina
  3. Biosciences, College of Science, Swansea University, Swansea, SA2 8PP, UK
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Ecology
  Biomedicine
  Oceanography
  Microbiology
  Zoology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1793

文摘

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.