Phenological shifts conserve thermal niches in North American birds and reshape expectations for climate-driven range shifts

Edited by Hugh P. Possingham, University of Queensland, St. Lucia, Australia, and approved October 10, 2017 (received for review April 14, 2017)
November 13, 2017
114 (49) 12976-12981
Commentary
Shifts in time and space interact as climate warms
Michael C. Singer

Significance

Climate warming poses two major challenges for birds: exposure to higher temperatures and disruption of the synchrony between nesting and resource emergence. To cope, birds are expected to track temperature by moving to cooler areas and to track resource emergence by breeding earlier. We show that these two responses are intertwined. Earlier breeding can substitute for range shifts by reducing temperatures during critical breeding-season life-history events. We show that early-summer temperatures affect nesting success in North American birds and that Californian birds breed ∼1 wk earlier today than a century ago. Thus, without shifting geographically, birds now nest at similar temperatures as they did a century ago, which might reshape both the need and the opportunity for range shifts.

Abstract

Species respond to climate change in two dominant ways: range shifts in latitude or elevation and phenological shifts of life-history events. Range shifts are widely viewed as the principal mechanism for thermal niche tracking, and phenological shifts in birds and other consumers are widely understood as the principal mechanism for tracking temporal peaks in biotic resources. However, phenological and range shifts each present simultaneous opportunities for temperature and resource tracking, although the possible role for phenological shifts in thermal niche tracking has been widely overlooked. Using a canonical dataset of Californian bird surveys and a detectability-based approach for quantifying phenological signal, we show that Californian bird communities advanced their breeding phenology by 5–12 d over the last century. This phenological shift might track shifting resource peaks, but it also reduces average temperatures during nesting by over 1 °C, approximately the same magnitude that average temperatures have warmed over the same period. We further show that early-summer temperature anomalies are correlated with nest success in a continental-scale database of bird nests, suggesting avian thermal niches might be broadly limited by temperatures during nesting. These findings outline an adaptation surface where geographic range and breeding phenology respond jointly to constraints imposed by temperature and resource phenology. By stabilizing temperatures during nesting, phenological shifts might mitigate the need for range shifts. Global change ecology will benefit from further exploring phenological adjustment as a potential mechanism for thermal niche tracking and vice versa.

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Acknowledgments

We are indebted to the pioneering work and careful record keeping of Joseph Grinnell and his associates, including his wife Hilda Grinnell. We thank the volunteers who collected the nesting data for this study through the Cornell Laboratory of Ornithology’s Nest Box Network, The Birdhouse Network, NestWatch, the Smithsonian Migratory Bird Research Center’s Neighborhood NestWatch, and various state nest monitoring projects that have contributed their data. We also thank the volunteers who conduct the US Geological Survey Breeding Bird Survey. Initial inspiration to examine phenological shifts in the Grinnell Resurvey data emerged from discussions of M.W.T. with Malin L. Pinsky. Pinsky, Scott K. Robinson, and two anonymous reviewers provided valuable comments on the manuscript. The present analyses were supported by the University of Connecticut and National Science Foundation (NSF; Grant EF 1703048). Data on phenology in California were collected as part of the Grinnell Resurvey Project, which was primarily funded by the NSF (Grant DEB 0640859) and California Energy Commission (Grant PIR-08-001), with support from the US National Park Service; Museum of Vertebrate Zoology; and Department of Environmental Science, Policy and Management at the University of California, Berkeley.

Supporting Information

Appendix (PDF)

References

1
C Parmesan, Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37, 637–669 (2006).
2
BR Scheffers, et al., The broad footprint of climate change from genes to biomes to people. Science 354, aaf7671 (2016).
3
C Moritz, et al., Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322, 261–264 (2008).
4
I-C Chen, JK Hill, R Ohlemüller, DB Roy, CD Thomas, Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).
5
ML Pinsky, B Worm, MJ Fogarty, JL Sarmiento, SA Levin, Marine taxa track local climate velocities. Science 341, 1239–1242 (2013).
6
EE Cleland, I Chuine, A Menzel, HA Mooney, MD Schwartz, Shifting plant phenology in response to global change. Trends Ecol Evol 22, 357–365 (2007).
7
AJ Miller-Rushing, RB Primack, Global warming and flowering times in Thoreau’s Concord: A community perspective. Ecology 89, 332–341 (2008).
8
MW Tingley, WB Monahan, SR Beissinger, C Moritz, Birds track their Grinnellian niche through a century of climate change. Proc Natl Acad Sci USA 106, 19637–19643 (2009).
9
JM Sunday, AE Bates, NK Dulvy, Thermal tolerance and the global redistribution of animals. Nat Clim Change 2, 686–690 (2012).
10
MD Schwartz, R Ahas, A Aasa, Onset of spring starting earlier across the Northern Hemisphere. Global Change Biol 12, 343–351 (2006).
11
HL Cayton, NM Haddad, K Gross, SE Diamond, Do growing degree days predict phenology across butterfly species? Ecology 96, 1473–1479 (2015).
12
C Both, et al., Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc Biol Sci 271, 1657–1662 (2004).
13
NK Lany, et al., Breeding timed to maximize reproductive success for a migratory songbird: The importance of phenological asynchrony. Oikos 125, 656–666 (2015).
14
P Dunn, DW Winkler, Climate change has affected the breeding date of tree swallows throughout North America. Proc Biol Sci 266, 2487–2490 (1999).
15
J Lenoir, JC Gégout, PA Marquet, P de Ruffray, H Brisse, A significant upward shift in plant species optimum elevation during the 20th century. Science 320, 1768–1771 (2008).
16
MC Urban, Climate change. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).
17
BR Scheffers, et al., Increasing arboreality with altitude: A novel biogeographic dimension. Proc Biol Sci 280, 20131581 (2013).
18
ME Visser, LJM Holleman, P Gienapp, Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147, 164–172 (2006).
19
C Both, M van Asch, RG Bijlsma, AB van den Burg, ME Visser, Climate change and unequal phenological changes across four trophic levels: Constraints or adaptations? J Anim Ecol 78, 73–83 (2009).
20
PO Dunn, AP Møller, Changes in breeding phenology and population size of birds. J Anim Ecol 83, 729–739 (2014).
21
C Both, ME Visser, Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411, 296–298 (2001).
22
TE Martin, Food as a limit on breeding birds: A life-history perspective. Annu Rev Ecol Syst 18, 453–487 (1987).
23
TP Hahn, KW Sockman, CW Breuner, ML Morton, Facultative altitudinal movements by mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) in the Sierra Nevada. Auk 121, 1269–1281 (2004).
24
EH Dunn, The timing of endothermy in the development of altrical birds. Condor 77, 288–293 (1975).
25
M Nichelmann, B Tzschentke, Ontogeny of thermoregulation in precocial birds. Comp Biochem Physiol A Mol Integr Physiol 131, 751–763 (2002).
26
MW Tingley, MS Koo, C Moritz, AC Rush, SR Beissinger, The push and pull of climate change causes heterogeneous shifts in avian elevational ranges. Global Change Biol 18, 3279–3290 (2012).
27
MW Tingley, SR Beissinger, Cryptic loss of montane avian richness and high community turnover over 100 years. Ecology 94, 598–609 (2013).
28
N Strebel, M Kéry, M Schaub, H Schmid, Studying phenology by flexible modelling of seasonal detectability peaks. Methods Ecol Evol 5, 483–490 (2014).
29
R Bonney, et al., Citizen science: A developing tool for expanding science knowledge and scientific literacy. Bioscience 59, 977–984 (2009).
30
JL Greño, EJ Belda, E Barba, Influence of temperatures during the nestling period on post-fledging survival of great tit Parus major in a Mediterranean habitat. J Avian Biol 39, 41–49 (2008).
31
RY Conrey, SK Skagen, AA Yackel Adams, AO Panjabi, Extremes of heat, drought and precipitation depress reproductive performance in shortgrass prairie passerines. Ibis 158, 614–629 (2016).
32
WA Cox, 3rd FR Thompson, JL Reidy, J Faaborg, Temperature can interact with landscape factors to affect songbird productivity. Glob Change Biol 19, 1064–1074 (2013).
33
JW Pearce-Higgins, SM Eglington, B Martay, DE Chamberlain, Drivers of climate change impacts on bird communities. J Anim Ecol 84, 943–954 (2015).
34
I Pipoly, V Bókony, G Seress, K Szabó, A Liker, Effects of extreme weather on reproductive success in a temperate-breeding songbird. PLoS One 8, e80033 (2013).
35
I Catry, AMA Franco, WJ Sutherland, Adapting conservation efforts to face climate change: Modifying nest-site provisioning for lesser kestrels. Biol Conserv 144, 1111–1119 (2011).
36
RD Dawson, CC Lawrie, EL O’Brien, The importance of microclimate variation in determining size, growth and survival of avian offspring: Experimental evidence from a cavity nesting passerine. Oecologia 144, 499–507 (2005).
37
G Rapacciuolo, et al., Beyond a warming fingerprint: individualistic biogeographic responses to heterogeneous climate change in California. Glob Change Biol 20, 2841–2855 (2014).
38
; Intergovernmental Panel on Climate Change Climate Change 2013: The Physical Science Basis (Cambridge Univ Press, Cambridge, UK, 2015).
39
V Devictor, et al., Differences in the climatic debts of birds and butterflies at a continental scale. Nat Clim Change 2, 121–124 (2012).
40
C Parmesan, G Yohe, A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).
41
J Lenoir, et al., Going against the flow: Potential mechanisms for unexpected downslope range shifts in a warming climate. Ecography 33, 295–303 (2010).
42
RG Pearson, TP Dawson, Predicting the impacts of climate change on the distribution of species: Are bioclimate envelope models useful? Global Ecol Biogeogr 12, 361–371 (2003).
43
BG Freeman, AM Class Freeman, Rapid upslope shifts in New Guinean birds illustrate strong distributional responses of tropical montane species to global warming. Proc Natl Acad Sci USA 111, 4490–4494 (2014).
44
DH Janzen, Why mountain passes are higher in the tropics. Am Nat 101, 233–249 (1967).
45
CD Thomas, JJ Lennon, Birds extend their ranges northwards. Nature 399, 213 (1999).
46
JE Brommer, The range margins of northern birds shift polewards. Ann Zool Fennici 41, 391–397 (2004).
47
C Parmesan, et al., Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399, 579–583 (1999).
48
B Zuckerberg, AM Woods, WF Porter, Poleward shifts in breeding bird distributions in New York State. Global Change Biol 15, 1866–1883 (2009).
49
DR Easterling, et al., Climate extremes: Observations, modeling, and impacts. Science 289, 2068–2074 (2000).
50
JW Morley, RD Batt, ML Pinsky, Marine assemblages respond rapidly to winter climate variability. Glob Change Biol 23, 2590–2601 (2017).
51
MW Tingley, SR Beissinger, Detecting range shifts from historical species occurrences: New perspectives on old data. Trends Ecol Evol 24, 625–633 (2009).
52
CT Rota, Jr RJ Fletcher, RM Dorazio, MG Betts, Occupancy estimation and the closure assumption. J Appl Ecol 46, 1173–1181 (2009).
53
AE Gelfand, et al., Modelling species diversity through species level hierarchical modelling. J R Stat Soc Ser C Appl Stat 54, 1–20 (2005).
54
RM Dorazio, JA Royle, B Söderström, A Glimskär, Estimating species richness and accumulation by modeling species occurrence and detectability. Ecology 87, 842–854 (2006).
55
BL Brock, RM Inman, Use of latitude-adjusted elevation in broad-scale species distribution models. Intermt J Sci 12, 12–17 (2006).
56
T Slagsvold, Bird song activity in relation to breeding cycle, spring weather, and environmental phenology. Ornis Scand 8, 197–222 (1977).
57
A Keast, The annual cycle in a vocalization context: A comparison of the eastern yellow robin Eopsaltria australis and jacky winter Microeca leucophaea. Emu 94, 230–238 (1994).
58
J Hegelbach, R Spaar, Annual variation in singing activity of the song thrush (Turdus philomelos), with comments on high postbreeding song output. J Ornithol 141, 425–434 (2000).
59
CW de Keyzer, NE Rafferty, DW Inouye, JD Thomson, Confounding effects of spatial variation on shifts in phenology. Glob Chang Biol 23, 1783–1791 (2017).
60
MM Thornton, et al., Daymet: Annual Climate Summaries on A 1-km Grid for North America, Version 3 (ORNL DACC, Oak Ridge, TN). Available at https://doi.org/10.3334/ORNLDAAC/1343. Accessed March 22, 2017. (2016).
61
MM Nice, Nesting success in altricial birds. Auk 74, 305–321 (1957).
62
JR Sauer, WA Link, JE Fallon, KL Pardieck, Jr DJ Ziolkowski, The North American Breeding Bird Survey 1966–2011: Summary analysis and species accounts. North Am Fauna 79, 1–32 (2013).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 49
December 5, 2017
PubMed: 29133415

Classifications

Submission history

Published online: November 13, 2017
Published in issue: December 5, 2017

Keywords

  1. nesting
  2. thermal niche
  3. climate change
  4. Sierra Nevada
  5. birds

Acknowledgments

We are indebted to the pioneering work and careful record keeping of Joseph Grinnell and his associates, including his wife Hilda Grinnell. We thank the volunteers who collected the nesting data for this study through the Cornell Laboratory of Ornithology’s Nest Box Network, The Birdhouse Network, NestWatch, the Smithsonian Migratory Bird Research Center’s Neighborhood NestWatch, and various state nest monitoring projects that have contributed their data. We also thank the volunteers who conduct the US Geological Survey Breeding Bird Survey. Initial inspiration to examine phenological shifts in the Grinnell Resurvey data emerged from discussions of M.W.T. with Malin L. Pinsky. Pinsky, Scott K. Robinson, and two anonymous reviewers provided valuable comments on the manuscript. The present analyses were supported by the University of Connecticut and National Science Foundation (NSF; Grant EF 1703048). Data on phenology in California were collected as part of the Grinnell Resurvey Project, which was primarily funded by the NSF (Grant DEB 0640859) and California Energy Commission (Grant PIR-08-001), with support from the US National Park Service; Museum of Vertebrate Zoology; and Department of Environmental Science, Policy and Management at the University of California, Berkeley.

Notes

This article is a PNAS Direct Submission.
See Commentary on page 12848.

Authors

Affiliations

Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269;
Peter N. Epanchin
Office of Global Climate Change, US Agency for International Development, Washington, DC 20523;
Steven R. Beissinger
Department of Environmental Science, Policy & Management, University of California, Berkeley, CA 94720;
Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: J.B.S. and M.W.T. designed research; J.B.S., P.N.E., S.R.B., and M.W.T. performed research; J.B.S. and M.W.T. analyzed data; and J.B.S., P.N.E., S.R.B., and M.W.T. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Phenological shifts conserve thermal niches in North American birds and reshape expectations for climate-driven range shifts
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 49
    • pp. 12839-E10605

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