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Phenological advancement in arctic bird species: relative importance of snow melt and ecological factors

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Abstract

Previous studies have documented advancement in clutch initiation dates (CIDs) in response to climate change, most notably for temperate-breeding passerines. Despite accelerated climate change in the Arctic, few studies have examined nest phenology shifts in arctic breeding species. We investigated whether CIDs have advanced for the most abundant breeding shorebird and passerine species at a long-term monitoring site in arctic Alaska. We pooled data from three additional nearby sites to determine the explanatory power of snow melt and ecological variables (predator abundance, green-up) on changes in breeding phenology. As predicted, all species (semipalmated sandpiper, Calidris pusilla, pectoral sandpiper, Calidris melanotos, red-necked phalarope, Phalaropus lobatus, red phalarope, Phalaropus fulicarius, Lapland longspur, Calcarius lapponicus) exhibited advanced CIDs ranging from 0.40 to 0.80 days/year over 9 years. Timing of snow melt was the most important variable in explaining clutch initiation advancement (“climate/snow hypothesis”) for four of the five species, while green-up was a much less important explanatory factor. We found no evidence that high predator abundances led to earlier laying dates (“predator/re-nest hypothesis”). Our results support previous arctic studies in that climate change in the cryosphere will have a strong impact on nesting phenology although factors explaining changes in nest phenology are not necessarily uniform across the entire Arctic. Our results suggest some arctic-breeding shorebird and passerine species are altering their breeding phenology to initiate nesting earlier enabling them to, at least temporarily, avoid the negative consequences of a trophic mismatch.

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References

  • Angelstam P, Lindström E, Widén P (1984) Role of predation in short-term population fluctuations of some birds and mammals in Fennoscandia. Oecologia 62:199–208

    Article  Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178

    Article  Google Scholar 

  • Blums P, Nichols JD, Hines JE, Lindberg MS, Mednis A (2005) Individual quality, survival variation and patterns of phenotypic selection on body condition and timing of nesting in birds Individual quality, survival variation and patterns of phenotypic selection on body condition and timing of nesting in birds. Oecologia 143:365–376

    Article  PubMed  Google Scholar 

  • Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298

    Article  CAS  PubMed  Google Scholar 

  • Both C, Artemyev AV, Blaauw B, Cowie RJ, Dekhuijzen AJ, Eeva T, Enemar A, Gustafsson L, Ivankina EV, Järvinen A, Metcalfe NB, Nyholm NEI, Potti J, Ravussin P-A, Sanz JJ, Silverin B, Slater FM, Sokolov LV, Török J, Winkel W, Wright J, Zang H, Visser ME (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc R Soc B 271:1657–1662

    Article  PubMed Central  PubMed  Google Scholar 

  • Both C, Van Turnhout CAM, Bijlsma RG, Siepel H, Van Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc B 277:1259–1266

    Article  PubMed Central  PubMed  Google Scholar 

  • Burnham KR, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Byrkjedal I (1980) Nest predation in relation to snow-cover: a possible factor influencing the start of breeding in shorebirds. Ornis Scand 11:249–252

    Article  Google Scholar 

  • Crick HQP, Sparks TH (1999) Climate change related to egg-laying trends. Nature 399:423

    Article  CAS  Google Scholar 

  • Crick HQP, Dudley C, Glue DE, Thomson DL (1997) UK birds are laying eggs earlier. Nature 388:526

    Article  CAS  Google Scholar 

  • Doxa A, Robert A, Crivelli A, Catsadorakis G, Naziridis T, Nikolaou H, Jiguet F, Theodorou K (2012) Shifts in breeding phenology as a response to population size and climatic change: a comparison between short- and long-distance migrant species. Auk 129:753–762

    Article  Google Scholar 

  • Drever MC, Clark RG, Derksen C, Slattery SM, Toose P, Nudds TD (2012) Population vulnerability to climate change linked to timing of breeding in boreal ducks. Glob Change Biol 18:480–492

    Article  Google Scholar 

  • Dunn PO (2004) Breeding dates and reproductive performance. In: Moller AP, Fiedler W, Berthold P (eds) Birds and climate change. Advances in ecological research, vol 35. Elsevier, San Diego, CA, pp 67–85

  • Dunn PO, Winkler DW (2010) Effects of climate change on timing of breeding and reproductive success in birds. In: Moller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, UK, pp 113–128

    Google Scholar 

  • Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283

    Article  Google Scholar 

  • Epstein HE, Raynolds MK, Walker DA, Bhatt US, Tucker CJ, Pinzon JE (2012) Dynamics of aboveground phytomass of the circumpolar Arctic tundra during the past three decades. Environ Res Lett 7:1–12

    Article  Google Scholar 

  • Farmer A, Holmes RT, Pitelka FA (2013) Pectoral Sandpiper (Calidris melanotos) In: Poole A, Gill F (eds) The birds of North America online. Accessed 10 Sept 2013

  • Gaston AJ, Gilchrist HG, Mallory ML, Smith PA (2009) Changes in seasonal events, peak food availability, and consequent breeding adjustment in a marine bird: a case of progressive mismatching. Condor 111:111–119

    Article  Google Scholar 

  • Gilg O, Sittler B, Hanski I (2009) Climate change and cyclic predator–prey population dynamics in the high Arctic. Glob Change Biol 15:2634–2652

    Article  Google Scholar 

  • Gilg O, Kovacs KM, Aars J, Fort J, Gauthier G, Grémillet D, Ims RA, Meltofte H, Moreau J, Post E, Schmidt NM, Yannic G, Bollache L (2012) Climate change and the ecology and evolution of Arctic vertebrates. Ann NY Acad Sci 1249:166–190

    Article  PubMed  Google Scholar 

  • Grabowski M, Doyle FI, Reid DG, Mossop D, Talarico D (2013) Do arctic nesting birds respond to earlier snowmelt? A multi-species study in north Yukon, Canada. Polar Biol 36:1097–1105

    Article  Google Scholar 

  • Green GH, Greenwood JJD, Lloyd CS (1977) The influence of snow conditions on the date of breeding of wading birds in northeast Greenland. J Zool 183:311–328

    Article  Google Scholar 

  • Hinzman LD, Bettez ND, Bolton RW, Chapin FS, Dyurgerov MB, Fastie CL, Griffith B, Hollister RD, Hope A, Huntington HP, Jensen AM, Jia GJ, Jorgenson T, Kane DL, Klein DR, Kofinas G, Lynch AH, Lloyd AH, McGuire AD, Nelson FE, Oechel WC, Osterkamp TE, Racine CH, Romanovsky VE, Stone RS, Stow DA, Sturm M, Tweedie CE, Vourlitis GL, Walker MD, Walker DA, Webber PJ, Welker JM, Winker KS, Yoshikawa K (2005) Evidence and implications of recent climate change in northern Alaska and other Arctic regions. Clim Change 72(2):251–298

    Article  Google Scholar 

  • Hinzman LD, Deal CJ, McGuire AD, Mernild SH, Polyakov IV, Walsh JE (2013) Trajectory of the Arctic as an integrated system. Ecol Appl 23:1837–1868

    Article  PubMed  Google Scholar 

  • Høye TT, Post E, Meltofte H, Schmidt NM, Forchhammer MC (2007) Rapid advancement of spring in the high arctic. Curr Biol 17:449–451

    Article  Google Scholar 

  • Hussell DJT, Montgomerie R (2002) Lapland Longspur (Calcarius lapponicus) In: Poole A, Gill F (eds) The birds of North America, no. 656. The Birds of North America, Inc. Philadelphia

  • Intergovernmental Panel on Climate Change (IPCC) (2007) Climate change 2007: the physical basis. Summary for policymakers. Contribution of Working Group I to the 4th Assessment Report of the IPCC. IPCC Secretariat, Geneva

  • Ji L, Wylie B, Ramachandran B, Jenkerson C (2010) A comparative analysis of three different MODIS NDVI datasets for Alaska and adjacent Canada. Can J Remote Sens 36:149–167

    Article  Google Scholar 

  • Klaassen M, Lindström Å, Meltofte H, Piersma T (2001) Ornithology-Arctic waders are not capital breeders. Nature 413:794

    Article  CAS  PubMed  Google Scholar 

  • Lehikoinen E, Sparks TH (2010) Changes in migration. In: Møller AP, Fiedler W, Berthold P (eds) Effects of climate change on birds. Oxford University Press, Oxford, UK, pp 89–112

    Google Scholar 

  • Liebezeit JR, Zack SW (2008) Point counts underestimate the importance of arctic foxes as avian nest predators: evidence from remote video cameras in Arctic Alaskan oil fields. Arctic 61:153–161

    Google Scholar 

  • Liebezeit JR, Smith PA, Lanctot RB, Schekkerman H, Tulp I, Kendall SJ, Tracy DM, Rodrigues RJ, Meltofte H, Robinson JA, Gratto-Trevor C, McCaffery BJ, Morse J, Zack SW (2007) Assessing the development of shorebird eggs using the flotation method: species-specific and generalized regression models. Condor 109:32–47

    Article  Google Scholar 

  • Liebezeit JR, Kendall SJ, Martin P, Payer D, Johnson CB, McDonald T, Wildman A, Brown S, Streever W, Zack S (2009) Influence of human development and predators on nest survival of tundra birds, Arctic Coastal Plain Alaska. Ecol Appl 19:1628–1644

    Article  CAS  PubMed  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS system for mixed models, 2nd edn. SAS Institute Inc, Cary, NC

    Google Scholar 

  • Martin TE (1993) Nest predation and nest sites: new perspectives on old patterns. Bioscience 43:523–532

    Article  Google Scholar 

  • Martin K, Wiebe KL (2004) Coping mechanisms of alpine and arctic breeding birds: extreme weather and limitations to reproductive resilience. Integr Comp Biol 44:177–185

    Article  PubMed  Google Scholar 

  • McKinnon L, Nol E, Juillet C (2013) Arctic-nesting birds find physiological relief in the face of trophic constraints. Sci Rep 3:1816. doi:10.1038/srep01816

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meijer T, Drent R (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414

    Article  Google Scholar 

  • Meltofte H, Høye TT, Schmidt NM, Forchhammer MC (2007a) Differences in food abundance cause inter-annual variation in the breeding phenology of High Arctic waders. Polar Biol 30:601–606

    Article  Google Scholar 

  • Meltofte H, Piersma T, Boyd H, McCafferey B, Ganter B, Golovnyuk VV, Graham K, Gratto-Trevor C, Morrison RIG, Nol E, Rosner H, Schamel D, Schekkerman H, Soloviev MY, Tomkovich PS, Tracy DM, Tulp I, Wennerberg L (2007b) Effects of climate variation on the breeding ecology of Arctic shorebirds. Monogr Greenl (Biosci) 59:1–48

    Google Scholar 

  • Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P (2008) Bird migration times, climate change, and changing population sizes. Glob Change Biol 14:1959–1972

    Article  Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Phil Trans R Soc B 365:3177–3186

    Article  PubMed Central  PubMed  Google Scholar 

  • Morrison RIG, Hobson KA (2004) Use of body stores in shorebirds after arrival on high Arctic breeding grounds. Auk 121:333–344

    Article  Google Scholar 

  • Morton ES (1971) Nest predation affecting the breeding season of the clay-colored robin, a Tropical songbird. Science 171:920–921

    Article  CAS  PubMed  Google Scholar 

  • Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386:698–702

    Article  CAS  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–40

    Article  CAS  PubMed  Google Scholar 

  • Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refuelling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415

    Article  CAS  PubMed  Google Scholar 

  • Poole AF, Stettenheim P, Gill FB (eds) (2003) The birds of North America: life histories for the 21st century. The Academy of Natural Sciences, Philadelphia, and the American Ornithologists’ Union, Washington, DC

  • Post E, Forschhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Phil Trans R Soc B 363:2369–2375

    Article  PubMed Central  PubMed  Google Scholar 

  • Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Høye TT, Ims RA, Jeppesen E, Klein DR, Madsen J, McGuire AD, Rysgaard S, Schindler DE, Stirling I, Tamstorf MP, Tyler NJC, van der Wal R, Welker J, Wookey PA, Schmidt NM, Aastrup P (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358

    Article  CAS  PubMed  Google Scholar 

  • Ralph CJ, Geupel GR, Pyle P, Martin TE, DeSante DF (1993) Handbook of field methods for monitoring landbirds. Gen. Tech. Rep. PSW-GTR-144. Albany, California: Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture

  • Reed B, Brown JF, Vanderzee D, Loveland TR, Merchant JW, Ohlen DO (1994) Measuring phenological variability from satellite imagery. J Veg Sci 5:703–714

    Article  Google Scholar 

  • Rodrigues R (1994) Microhabitat variables influencing nest-site selection by tundra birds. Ecol Appl 4:110–116

    Article  Google Scholar 

  • Root TR, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    Article  CAS  PubMed  Google Scholar 

  • Rubega MA, Schamel D, Tracy DM (2000) Red-necked Phalarope (Phalaropus lobatus). In: Poole A, Gill F (eds) The birds of North America, no. 538. The Birds of North America, Philadelphia

  • SAS Institute Inc (2008) SAS/STAT® 9.2 User’s Guide. Cary, NC: SAS Institute, Inc

  • Smith NV, Saatchi SS, Randerson JT (2004) Trends in high northern latitude soil freeze and thaw cycles from 1988 to 2002. J Geophys Res 109:D12101. doi:10.1029/2003JD004472

    Article  Google Scholar 

  • Smith PA, Gilchrist HG, Smith JNM (2007) Effects of nest habitat, food, and parental behaviour on shorebird nest success. Condor 109:15–31

    Article  Google Scholar 

  • Smith PA, Gilchrist HG, Forbes MR, Martin J-L, Allard K (2010) Inter-annual variation in the breeding chronology of arctic shorebirds: effects of weather, snow melt and predators. J Avian Biol 41:292–304

    Article  Google Scholar 

  • Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, Liston GE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert arctic tundra to shrubland. Bioscience 55:17–26

    Article  Google Scholar 

  • Swets D, Reed BC, Rowland JD, Marko SE (1999) A weighted least-squares approach to temporal NDVI smoothing. In: Proceedings of the 1999 ASPRS Annual Conference, From Image to Information, Portland Oregon, May 17–21, 1999, Bethesda, MD: American Society for Photogrammetry and Remote Sensing, CD-ROM

  • Thackeray SJ, Sparks TH, Frederiksen M, Burth S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Carvalho L, Clutton-Brock T, Dawson A, Edwards M, Elliott JM, Harrington R, Johns D, Jones ID, Jones JT, Leech DI, Roy DB, Scott WA, Smith M, Smither RJ, Winfield IJ, Wanless S (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313

    Article  Google Scholar 

  • Tracy DM, Schamel D, Dale J (2002) Red Phalarope (Phalaropus fulicarius) In: Poole A, Gill F (eds) The birds of North America, no. 698. The Birds of North America, Philadelphia

  • Travis JM (2003) Climate change and habitat destruction: a deadly anthropogenic cocktail. Proc R Soc B 270:467–473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Troy DM (2000) Shorebirds. In: Truett JC, Johnson SR (eds) The natural history of an Arctic oil field, development and the biota. Academic Press, San Diego, pp 277–303

    Chapter  Google Scholar 

  • Tulp I, Schekkerman H (2008) Has prey availability for arctic birds advanced with climate change? Hindcasting the abundance of tundra arthropods using weather and seasonal variation. Arctic 61:48–60

    Google Scholar 

  • U.S. Geological Survey (2011) eMODIS Alaska Product Guide Online, Department of Interior, U.S. Geological Survey Earth Resources Observation and Science (USGS/EROS), Version 1.0, pp 1–21. http://dds.cr.usgs.gov/emodis/Alaska/

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272:2561–2569

    Article  PubMed Central  PubMed  Google Scholar 

  • Walker DA, Everett KR, Webber PJ, Brown J (1980) Geobotanical atlas of the Prudhoe Bay region, Alaska. United States Army Corps of Engineers. Cold Regions Research and Engineering Laboratory. CRREL report 80-14. Hanover, NH

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • Weidinger K, Král M (2007) Climatic effects on arrival and laying dates in a long-distance migrant, the collared flycatcher Ficedula albicollis. Ibis 149:836–847

    Article  Google Scholar 

  • Wiklund CG (1984) Reproductive synchrony in the fieldfare (Turdus pilaris) in relation to spring arrival, nest predation and nestling starvation. Behav Ecol Sociobiol 15:311–316

    Article  Google Scholar 

  • Winkler DW, Dunn PO, McCulloch CE (2002) Predicting the effects of climate change on avian life-history traits. PNAS 99:13595–13599

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank the many field assistants who collected data for this study. We also thank BP Alaska [Exploration] Inc., ConocoPhillips Alaska, Inc., and the North Slope Borough for logistic support. The funders that made this study possible include: Alaska Department of Fish and Game Partner Program, Bureau of Land Management, Disney Conservation Awards, Kresge Foundation, Liz Claiborne/Art Ortenberg Foundation, U.S. Fish and Wildlife Neotropical Migratory Bird Conservation Act grants, U.S. Fish and Wildlife Avian Influenza Surveillance grants, WCS private donors, and the U.S. Geological Survey’s (USGS) Changing Arctic Ecosystem Initiative that is supported by funding from the Wildlife Program of the USGS Ecosystem Mission Area. We thank Kyle Hogrefe for preparation of the study area figure. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Liebezeit, J.R., Gurney, K.E.B., Budde, M. et al. Phenological advancement in arctic bird species: relative importance of snow melt and ecological factors. Polar Biol 37, 1309–1320 (2014). https://doi.org/10.1007/s00300-014-1522-x

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