Abstract
More frequent and extreme heat waves threaten climate-sensitive species. Structurally complex, older forests can buffer these effects by creating cool microclimates, although the mechanisms by which forest refugia mitigate physiological responses to heat exposure and subsequent population-level consequences remain relatively unexplored. We leveraged fine-scale movement data, doubly labeled water, and two decades of demographic data for the California spotted owl (Strix occidentalis occidentalis) to (1) assess the role of older forest characteristics as potential energetic buffers for individuals and (2) examine the subsequent value of older forests as refugia for a core population in the Sierra Nevada and a periphery population in the San Bernardino Mountains. Individuals spent less energy moving during warmer sampling periods and the presence of tall canopies facilitated energetic conservation during daytime roosting activities. In the core population, where tall-canopied forest was prevalent, temperature anomalies did not affect territory occupancy dynamics as warmer sites were both less likely to go extinct and less likely to become colonized, suggesting a trade-off between foraging opportunities and temperature exposure. In the peripheral population, sites were more likely to become unoccupied following warm summers, presumably because of less prevalent older forest conditions. While individuals avoided elevated energetic expenditure associated with temperature exposure, behavioral strategies to conserve energy may have diverted time and energy from reproduction or territory defense. Conserving older forests, which are threatened due to fire and drought, may benefit individuals from energetic consequences of exposure to stressful thermal conditions.
Similar content being viewed by others
Availability of data and materials
The datasets used during the current study are available from the corresponding author on request.
Code availability
Codes used for statistics and occupancy models are available from the corresponding author on request.
References
Barrows CW (1981) Roost selection by spotted owls: an adaptation to heat stress. Condor 83:302. https://doi.org/10.2307/1367496
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Berigan WJ, Jones GM, Whitmore SA et al (2019) Cryptic wide-ranging movements lead to upwardly biased occupancy in a territorial species. J Appl Ecol 56:470–480. https://doi.org/10.1111/1365-2664.13265
Betts MG, Phalan B, Frey SJK et al (2018) Old-growth forests buffer climate-sensitive bird populations from warming. Divers Distrib 24:439–447. https://doi.org/10.1111/ddi.12688
Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83. https://doi.org/10.1038/nature04539
Briscoe NJ (2015) Tree-hugging behavior beats the heat. Temperature 2:33–35. https://doi.org/10.4161/23328940.2014.954420
Brunk KM, Gutiérrez RJ, Peery MZ et al (2023) Quail on fire: changing fire regimes may benefit mountain quail in fire-adapted forests. Fire Ecol 19:19. https://doi.org/10.1186/s42408-023-00180-9
Burnham KA, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Bütikofer L, Anderson K, Bebber DP et al (2020) The problem of scale in predicting biological responses to climate. Glob Change Biol 26:6657–6666. https://doi.org/10.1111/gcb.15358
Cade BS (2015) Model averaging and muddled multimodel inferences. Ecology 96:2370–2382. https://doi.org/10.1890/14-1639.1
Calder W, King JR (1974) Thermal and caloric relations of birds. In: Farner DS, King JR (eds) Avian biology. Academic Press, New York
California Forest Observatory (2020) A statewide tree-level forest monitoring system. Salo Sciences, Inc. San Francisco, CA. https://forestobservatory.com
Cayan DR, Maurer EP, Dettinger MD et al (2008) Climate change scenarios for the California region. Clim Change 87:21–42. https://doi.org/10.1007/s10584-007-9377-6
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. https://doi.org/10.1073/pnas.1821312116
Cruz-Neto AP, Andrade DV, Abe AS (2001) Energetic and physiological correlates of prey handling and ingestion in lizards and snakes. Comp Biochem Physiol A Mol Integr Physiol 128:513–531. https://doi.org/10.1016/S1095-6433(00)00332-9
Cunningham SJ, Martin RO, Hojem CL, Hockey PAR (2013) Temperatures in excess of critical thresholds threaten nestling growth and survival in a rapidly-warming arid savanna: a study of common fiscals. PLoS ONE 8:e74613. https://doi.org/10.1371/journal.pone.0074613
Cunningham SJ, Martin RO, Hockey PA (2015) Can behaviour buffer the impacts of climate change on an arid-zone bird? Ostrich J Afr Ornithol 86:119–126. https://doi.org/10.2989/00306525.2015.1016469
Cunningham SJ, Gardner JL, Martin RO (2021) Opportunity costs and the response of birds and mammals to climate warming. Front Ecol Environ 19:300–307. https://doi.org/10.1002/fee.2324
Davis KT, Dobrowski SZ, Holden ZA et al (2019) Microclimatic buffering in forests of the future: the role of local water balance. Ecography 42:1–11. https://doi.org/10.1111/ecog.03836
Daymet (1840) Daily Surface Weather Data on a 1-km Grid for North America, Version 4 R1. https://doi.org/10.3334/ORNLDAAC/2129
De Frenne P, Lenoir J, Luoto M et al (2021) Forest microclimates and climate change: importance, drivers and future research agenda. Glob Change Biol 27:2279–2297. https://doi.org/10.1111/gcb.15569
Dormann CF, Schymanski SJ, Cabral J et al (2012) Correlation and process in species distribution models: bridging a dichotomy. J Biogeogr 39:2119–2131. https://doi.org/10.1111/j.1365-2699.2011.02659.x
du Plessis KL, Martin RO, Hockey PAR et al (2012) The costs of keeping cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob Change Biol 18:3063–3070. https://doi.org/10.1111/j.1365-2486.2012.02778.x
Franklin AB, Anderson DR, Gutiérrez RJ, Burnham KP (2000) Climate, habitat quality, and fitness in northern spotted owl populations in Northwestern California. Ecol Monogr 70:539–590. https://doi.org/10.1890/0012-9615(2000)070[0539:CHQAFI]2.0.CO;2
Frey SJK, Hadley AS, Betts MG (2016) Microclimate predicts within-season distribution dynamics of montane forest birds. Divers Distrib 22:944–959. https://doi.org/10.1111/ddi.12456
Ganey JL, Balda RP, King RM (1993) Metabolic rate and evaporative water loss of Mexican Spotted and Great Horned Owls. Wilson Bull 105(4):645–656
Gessaman JA, Nagy KA (1988) Energy metabolism: errors in gas-exchange conversion factors. Physiol Zool 61:507–513
Glenn EM, Anthony RG, Forsman ED (2010) Population trends in northern spotted owls: Associations with climate in the Pacific Northwest. Biol Cons 143:2543–2552. https://doi.org/10.1016/j.biocon.2010.06.021
Gutiérrez RJ, Manley PN, Stine PA (2017) The California spotted owl: current state of knowledge. Gen Tech Rep PSW-GTR-254 Albany, CA: US Department of Agriculture, Forest Service, Pacific Southwest Research Station 254. https://doi.org/10.2737/PSW-GTR-254
Herbert C, Haya BK, Stephens SL, Butsic V (2022) Managing nature-based solutions in fire-prone ecosystems: competing management objectives in California forests evaluated at a landscape scale. Front Forests Global Change. https://doi.org/10.3389/ffgc.2022.957189
Hines J (2006) PRESENCE2. Software to estimate patch occupancy and related parameters. USGS-PWRC
Hobart BK, Jones GM, Roberts KN et al (2019) Trophic interactions mediate the response of predator populations to habitat change. Biol Conserv 238:108217. https://doi.org/10.1016/j.biocon.2019.108217
Hudson LN, Isaac NJB, Reuman DC (2013) The relationship between body mass and field metabolic rate among individual birds and mammals. J Anim Ecol 82:1009–1020. https://doi.org/10.1111/1365-2656.12086
Hulley GC, Dousset B, Kahn BH (2020) Rising trends in heatwave metrics across southern California. Earth Fut 8:e2020EF001480. https://doi.org/10.1029/2020EF001480
Jones GM, Gutiérrez RJ, Tempel DJ et al (2016) Using dynamic occupancy models to inform climate change adaptation strategies for California spotted owls. J Appl Ecol 53:895–905. https://doi.org/10.1111/1365-2664.12600
Jones GM, Ayars J, Parks SA et al (2022) Pyrodiversity in a warming world: research challenges and opportunities. Curr Landsc Ecol Rep. https://doi.org/10.1007/s40823-022-00075-6
Keppel G, Mokany K, Wardell-Johnson GW et al (2015) The capacity of refugia for conservation planning under climate change. Front Ecol Environ 13:106–112. https://doi.org/10.1890/140055
Kim H, McComb BC, Frey SJK et al (2022) Forest microclimate and composition mediate long-term trends of breeding bird populations. Glob Change Biol 28:6180–6193. https://doi.org/10.1111/gcb.16353
Kramer HA, Jones GM, Kane VR et al (2021) Elevational gradients strongly mediate habitat selection patterns in a nocturnal predator. Ecosphere 12:e03500. https://doi.org/10.1002/ecs2.3500
LaHaye WS, Zimmerman GS, Gutiérrez RJ (2004) Temporal variation in the vital rates of an insular population of spotted owls (Strix Occidentalis Occidentalis): contrasting effects of weather. Auk 121:1056–1069. https://doi.org/10.1093/auk/121.4.1056
Londe DW, Elmore RD, Davis CA et al (2021) Fine-scale habitat selection limits trade-offs between foraging and temperature in a grassland bird. Behav Ecol 32:625–637. https://doi.org/10.1093/beheco/arab012
MacKenzie DI, Nichols JD, Hines JE et al (2003) Estimating site occupancy, colonization, and local extinction when a species is detected imperfectly. Ecology 84:2200–2207. https://doi.org/10.1890/02-3090
Martin ME, Moriarty KM, Pauli JN (2020) Forest structure and snow depth alter the movement patterns and subsequent expenditures of a forest carnivore, the Pacific marten. Oikos 129:356–366. https://doi.org/10.1111/oik.06513
McCue MD, Bennett AF, Hicks JW (2005) The effect of meal composition on specific dynamic action in burmese Pythons (Python molurus). Physiol Biochem Zool 78:182–192. https://doi.org/10.1086/427049
McKechnie AE, Wolf BO (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Let 6:253–256. https://doi.org/10.1098/rsbl.2009.0702
Moen CA, Gutiérrez RJ (1997) California spotted owl habitat selection in the Central Sierra Nevada. J Wildl Manag 61:1281–1287. https://doi.org/10.2307/3802127
Morelli TL, Barrows CW, Ramirez AR et al (2020) Climate-change refugia: biodiversity in the slow lane. Front Ecol Environ 18:228–234. https://doi.org/10.1002/fee.2189
Morin DJ, Yackulic CB, Diffendorfer JE et al (2020) Is your ad hoc model selection strategy affecting your multimodel inference? Ecosphere 11:e02997. https://doi.org/10.1002/ecs2.2997
Moritz C, Agudo R (2013) The future of species under climate change: Resilience or decline? Science 341:504–508. https://doi.org/10.1126/science.1237190
Moyer-Horner L, Mathewson PD, Jones GM et al (2015) Modeling behavioral thermoregulation in a climate change sentinel. Ecol Evol 5:5810–5822. https://doi.org/10.1002/ece3.1848
Nagy KA (1983) The doubly labeled water method: a guide to its use. UCLA publication no. 12-1417
North MP, Kane JT, Kane VR et al (2017) Cover of tall trees best predicts California spotted owl habitat. For Ecol Manag 405:166–178. https://doi.org/10.1016/j.foreco.2017.09.019
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. https://doi.org/10.1038/nature01286
Pattinson NB, Thompson ML, Griego M et al (2020) Heat dissipation behaviour of birds in seasonally hot arid-zones: Are there global patterns? J Avian Biol. https://doi.org/10.1111/jav.02350
Peery MZ, Gutiérrez RJ, Kirby R et al (2012) Climate change and spotted owls: potentially contrasting responses in the Southwestern United States. Glob Change Biol 18:865–880. https://doi.org/10.1111/j.1365-2486.2011.02564.x
Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78:419–433. https://doi.org/10.1086/378926
Riddell EA, Iknayan KJ, Hargrove L et al (2021) Exposure to climate change drives stability or collapse of desert mammal and bird communities. Science 371:633–636. https://doi.org/10.1126/science.abd4605
Schulte PM (2015) The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment. J Exp Biol 218:1856–1866. https://doi.org/10.1242/jeb.118851
Schultner J, Welcker J, Speakman JR et al (2010) Application of the two-sample doubly labelled water method alters behaviour and affects estimates of energy expenditure in black-legged kittiwakes. J Exp Biol 213:2958–2966. https://doi.org/10.1242/jeb.043414
Secor SM (2001) Regulation of digestive performance: a proposed adaptive response. Comp Biochem Physiol a: Mol Integr Physiol 128:563–575. https://doi.org/10.1016/S1095-6433(00)00325-1
Secor SM, Faulkner AC (2002) Effects of meal size, meal type, body temperature, and body size on the specific dynamic action of the marine toad, Bufo marinus. Physiol Biochem Zool 75:557–571. https://doi.org/10.1086/344493
Shepard ELC, Wilson RP, Rees WG et al (2013) Energy landscapes shape animal movement ecology. Am Nat 182:298–312. https://doi.org/10.1086/671257
Sinervo B, Méndez-de-la-Cruz F, Miles DB et al (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899. https://doi.org/10.1126/science.1184695
Smith RB, Peery MZ, Gutiérrez RJ, Lahaye WS (1999) The relationship between spotted owl diet and reproductive success in the San Bernardino Mountains, California. Wilson Bull 111:22–29
Speakman JR (1993) How should we calculate CO2 production in doubly labelled water studies of animals? Funct Ecol 7:746–750
Speakman JR (1997) Doubly labelled water: theory and practice. Chapman & Hall, New York
Steel ZL, Jones GM, Collins BM et al (2022) Mega-disturbances cause rapid decline of mature conifer forest habitat in California. Ecol Appl 33:e2763. https://doi.org/10.1002/eap.2763
Steger GN, Munton TE, Johnson Kenneth A, Eberlein GP (2002) Demography of the California spotted owl in the sierra national forest and sequoia/kings canyon national parks. In: Proceedings of a symposium on the kings river sustainable forest ecosystem project: progress and current status. Gen. Tech. Rep. PSW-GTR-183, Albany, CA: Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture: 107-116
Stewart JAE, Perrine JD, Nichols LB et al (2015) Revisiting the past to foretell the future: summer temperature and habitat area predict pika extirpations in California. J Biogeogr 42:880–890. https://doi.org/10.1111/jbi.12466
Street GM, Rodgers AR, Fryxell JM (2015) Mid-day temperature variation influences seasonal habitat selection by moose. J Wildl Manag 79:505–512. https://doi.org/10.1002/jwmg.859
Tempel DJ, Gutiérrez RJ, Whitmore SA et al (2014) Effects of forest management on California Spotted Owls: implications for reducing wildfire risk in fire-prone forests. Ecol Appl 24:2089–2106. https://doi.org/10.1890/13-2192.1
Tempel DJ, Keane JJ, Gutiérrez RJ et al (2016) Meta-analysis of California Spotted Owl (Strix occidentalis occidentalis) territory occupancy in the Sierra Nevada: Habitat associations and their implications for forest management. Condor 118:747–765. https://doi.org/10.1650/CONDOR-16-66.1
Tempel DJ, Kramer HA, Jones GM et al (2022) Population decline in California spotted owls near their southern range boundary. J Wildl Manag 86:e22168. https://doi.org/10.1002/jwmg.22168
Tucker VA (1970) Energetic cost of locomotion in animals. Comp Biochem Physiol 34:841–846. https://doi.org/10.1016/0010-406X(70)91006-6
van de Ven TMFN, McKechnie AE, Cunningham SJ (2019) The costs of keeping cool: behavioural trade-offs between foraging and thermoregulation are associated with significant mass losses in an arid-zone bird. Oecologia 191:205–215. https://doi.org/10.1007/s00442-019-04486-x
Varner J, Horns JJ, Lambert MS et al (2016) Plastic pikas: behavioural flexibility in low-elevation pikas (Ochotona princeps). Behav Proc 125:63–71. https://doi.org/10.1016/j.beproc.2016.01.009
Veľký M, Kaňuch P, Krištín A (2009) Selection of winter roosts in the Great Tit Parus major: influence of microclimate. J Ornithol 151:147. https://doi.org/10.1007/s10336-009-0436-9
Verner J, Gutiérrez RJ, Gould GJ (1992) The California spotted owl: General biology and ecological relations. Chapter 4. In: Verner J, McKelvey KS, Noon BR, Gutierrez RJ; Gould GI Jr; Beck TW (eds) Technical coordinators 1992 the California spotted owl: a technical assessment of its current status Gen Tech Rep PSW-GTR-133 Albany, CA: Pacific Southwest Research Station, Forest Service, US Department of Agriculture; pp 55-77 133:55–77
Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc Biol Sci 275:649–659. https://doi.org/10.1098/rspb.2007.0997
Weathers WW, Hodum PJ, Blakesley JA (2001) Thermal ecology and ecological energetics of California spotted owls. Condor 103:678. https://doi.org/10.1650/0010-5422(2001)103[0678:TEAEEO]2.0.CO;2
Webster MD, Weathers WW (1989) Validation of single-sample doubly labeled water method. Am J Physiol Regul Integr Comp Physiol 256:R572–R576. https://doi.org/10.1152/ajpregu.1989.256.2.R572
Wilkinson ZA, Kramer HA, Jones GM et al (2022) Tall, heterogenous forests improve prey capture, delivery to nestlings, and reproductive success for Spotted Owls in southern California. Ornithol Appl. https://doi.org/10.1093/ornithapp/duac048
Wolf C, Bell DM, Kim H et al (2021) Temporal consistency of undercanopy thermal refugia in old-growth forest. Agric for Meteorol 307:108520. https://doi.org/10.1016/j.agrformet.2021.108520
Wolff CL, Demarais S, Brooks CP, Barton BT (2020) Behavioral plasticity mitigates the effect of warming on white-tailed deer. Ecol Evol 10:2579–2587. https://doi.org/10.1002/ece3.6087
Zuckerberg B, Ribic CA, McCauley LA (2018) Effects of temperature and precipitation on grassland bird nesting success as mediated by patch size. Conserv Biol 32:872–882. https://doi.org/10.1111/cobi.13089
Zulla CJ, Kramer HA, Jones GM et al (2022) Large trees and forest heterogeneity facilitate prey capture by California Spotted Owls. Ornithol Appl 124:duac024. https://doi.org/10.1093/ornithapp/duac024
Zulla CJ, Jones GM, Kramer HA et al (2023) Forest heterogeneity outweighs movement costs by enhancing hunting success and reproductive output in California spotted owls. Landsc Ecol. https://doi.org/10.1007/s10980-023-01737-4
Acknowledgements
We thank Tom Munton, Richard Tanner, Tony Lavictoire and Nora Holmes for their assistance in the field. We also thank Timothy Shriver for his expertise analyzing isotope ratios. We thank Brian Dotters for his generous review of this manuscript. Finally, we acknowledge that the research described in this paper was carried out on the land of the Nisenan, Miwok, Mono, Yokuts, Serrano, and Cahuilla, and we pay our respects to them as the original custodians of the land.
Funding
This research is based upon work supported by the National Science Foundation Graduate Research Fellowship Program (DGE-1747503 awarded to KM). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. This work was also supported by the USDA Forest Service Region 5, USFS Pacific Southwest Research Station, and the University of Wisconsin-Madison (Hatch WIS03069 awarded to MZP and BZ by Wisconsin Agricultural Research Station). None of the funders of this research had any influence on the content of the submitted manuscript, nor required approval of the final manuscript to be published.
Author information
Authors and Affiliations
Contributions
KM, BZ, JP, and MZP conceived the ideas and designed the methodology; KM, WB, CZ, ZW, and JB collected the data; KM constructed the manuscript and handled analyses. Historical data was provided by JK and RJ. All authors contributed to writing drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Ethics approval
All handling of animals in this study were done by trained individuals under the proper permitting (IACUC A005367-R02-A01). All institutional and national guidelines for the care of animals were followed.
Consent to participate/consent for publication
This article does not contain any studies with human participants.
Additional information
Communicated by Robert L Thomson.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
McGinn, K.A., Zuckerberg, B., Pauli, J.N. et al. Older forests function as energetic and demographic refugia for a climate-sensitive species. Oecologia 202, 831–844 (2023). https://doi.org/10.1007/s00442-023-05442-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-023-05442-6