Abstract
Animals inhabiting montane gradients experience varying winter climates that may result in differential selection on survival-related traits. Higher elevations in temperate climates are characterized by harsher winters with greater and longer-lasting snow cover compared to lower elevations, potentially leading to stronger selection for traits that improve fitness under these harsher conditions. For food-caching mountain chickadees, Poecile gambeli, inhabiting harsh high elevation environments, individual variation in spatial cognitive abilities related to cache retrieval is associated with significant differences in overwinter survival. Compared to lower elevations, stronger predicted selection on traits needed for overwinter survival at higher elevations can be expected to result in higher adult annual survival despite harsher environmental conditions, indicating that individuals that survive their first winter are better suited to survive similar subsequent selection events. Here, we used a Bayesian hierarchical Cormack-Jolly-Seber (CJS) model to estimate and compare survival of adult mountain chickadees at higher and lower elevations over 3 years. We showed that adult survival was consistently higher at higher elevations despite much harsher environmental conditions, supporting our hypothesis that selection on overwinter survival-related traits (such as spatial cognition) is stronger at our high elevation study area than at lower elevations.
Significance statement
Understanding how environmental conditions are associated with different selection strengths on survival-related traits is an important question in behavioral ecology. Directly estimating differences in strength of selection is daunting, but comparing survival between environments may provide an alternative method. We tested for differences in adult survival in a resident food-caching species at higher and lower elevations varying in winter climate severity. These birds rely on food caches for winter survival, and juvenile birds with better spatial cognition (needed for cache retrieval) have higher survival during their first year at higher harsher elevations. Here, we report higher adult survival at higher elevations compared to lower elevations, despite much harsher winter environment. Such findings support our hypothesis for stronger selection in harsher winter conditions because individuals that survive their first year under stronger selection are better suited to survive subsequent selection events.
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References
Barbour MG, Minnich RA (2000) Californian upland forests and woodlands. In: Barbour MG, Billings WD (eds) North American terrestrial vegetation, 2nd edn. Cambridge University Press, New York, pp 16–202
Boag PT, Grant PR (1981) Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galapagos. Science 214:82–85. https://doi.org/10.1126/science.214.4516.82
Branch CL, Pravosudov VV (2020) Variation in song structure along an elevation gradient in a resident songbird. Behav Ecol Sociobiol 74:9
Branch CL, Kozlovsky DY, Croston R, Pitera AM, Pravosudov VV (2016) Mountain chickadees return to their post-natal dispersal settlements following long-term captivity. Behaviour 153:551–567. https://doi.org/10.1163/1568539x-00003363
Branch CL, Pitera AM, Kozlovsky DY, Bridge E, Pravosudov VV (2019a) Smart is the new sexy: female mountain chickadees increase reproductive investment when mated to males with better spatial cognition. Ecol Lett 22:897–903. https://doi.org/10.1111/ele.13249
Branch CL, Pitera AM, Kozlovsky DY, Sonnenberg BR, Benedict LM, Pravosudov VV (2019b) Elevation-related differences in the age structure of breeding birds suggest stronger selection at harsher elevations. Behav Ecol Sociobiol 73:143–146. https://doi.org/10.1007/s00265-019-2750-4
Bridge ES, Bonter DN (2011) A low-cost radio frequency identification device for ornithological research. J Field Ornithol 82:52–59
Cormack RM (1964) Estimates of survival from the sighting of marked animals. Biometrika 51:429–438. https://doi.org/10.1093/biomet/51.3-4.429
Croston R, Kozlovsky DY, Branch CL, Parchman TL, Bridge ES, Pravosudov VV (2016) Individual variation in spatial memory performance in wild mountain chickadees from different elevations. Anim Behav 111:225–234. https://doi.org/10.1016/j.anbehav.2015.10.015
Croston R, Branch CL, Pitera AM, Kozlovsky DY, Bridge ES, Parchman TL, Pravosudov VV (2017) Predictably harsh environment is associated with reduced cognitive flexibility in wild food-caching mountain chickadees. Anim Behav 123:139–149. https://doi.org/10.1016/j.anbehav.2016.10.004
Development Core Team R (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://doi.org/10.1007/978-3-540-74686-7
Ekman J (1989) Ecology of non-breeding social systems of Parus. Wilson Bull 101:263–288
Endler JA (1986) Natural selection in the wild. Princeton Univ Press, Princeton
Freas CA, LaDage LD, Roth TC, Pravosudov VV (2012) Elevation-related differences in memory and the hippocampus in mountain chickadees, Poecile gambeli. Anim Behav 84:121–127. https://doi.org/10.1016/j.anbehav.2012.04.018
Freas CA, Bingman K, LaDage LD, Pravosudov VV (2013) Untangling elevation-related differences in the hippocampus in food-caching mountain chickadees: the effect of a uniform captive environment. Brain Behav Evol 3:199–209. https://doi.org/10.1159/000355503
Gimenez O, Lebreton J, Choquet R, Pradel R (2017) R2ucare: goodness-of-fit tests for capture-recapture models. https://cran.r-project.org/package=R2ucare. Accessed 20 Feb 2019
Jansson C, Ekman J, von Brömssen A (1981) Winter mortality and food supply in tits Parus spp. Oikos 37:313–322
Jolly GS (1965) Explicit estimates from capture-recapture data with both death and immigration-stochastic model. Biometrika 52:225–248. https://doi.org/10.1093/biomet/52.1-2.225
Kershner EL, Walk JW, Warner RE (2004) Postfledging movements and survival of juvenile eastern meadowlarks (Sturnella magna) in Illinois. Auk 121:1146–1154
Kéry M, Schaub M (2012) Estimation of survival from capture–recapture data using the Cormack–Jolly–Seber model. In: Bayesian Population Analysis Using WinBUGS. Academic Press, New York, pp 172–238. https://doi.org/10.1016/b978-0-12-387020-9.00007-9
Kozlovsky DY, Branch CL, Freas CA, Pravosudov VV (2014) Elevation-related differences in novel exploration and social dominance in food-caching mountain chickadees. Behav Ecol Sociobiol 68:1871–1881
Kozlovsky DY, Branch CL, Pitera AM, Pravosudov VV (2018) Fluctuations in annual climatic extremes are associated with reproductive variation in resident mountain chickadees. R Soc Open Sci 5:171604. https://doi.org/10.1098/rsos.171604
Lack D (1954) The natural regulation of animal numbers. Oxford University Press, Oxford
McCallum DA, Grundel R, Dahlsten DL (1999) Mountain chickadee (Poecile gambeli), version 2.0. In: Poole AF, Gill FB (eds) The birds of North America online. Cornell Lab of Ornithology, Ithaca. https://birdsna.org/Species-Account/bna/species/mouchi. Accessed 28 Aug 2019
Meigs JB, Smith DC, Van Buskirk J (1983) Age determination of black-capped chickadees. J Field Ornithol 54:283–286
Morand-Ferron J, Quinn JL (2015) The evolution of cognition in natural populations. Trends Cogn Sci 19:235–237
Morand-Ferron J, Cole EF, Quinn JL (2016) Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges. Biol Rev 91:367–389
Munch SB, Mangel M, Conover DO (2003) Quantifying natural selection on body size from field data: winter mortality in Menidia menidia. Ecology 84:2168–2177. https://doi.org/10.1890/02-0137
Pitera AM, Branch CL, Bridge ES, Pravosudov VV (2018) Daily foraging routines in food-caching mountain chickadees are associated with variation in environmental harshness. Anim Behav 143:93–104. https://doi.org/10.1016/j.anbehav.2018.07.011
Plummer M (2003) JAGS: A program for analysis of Bayesian graphical models using Gibbs Sampling. DSC 2003 Working Papers. http://www.ci.tuwien.ac.at/Conferences/DSC-2003/. Accessed 03 Dec 2018
Pravosudov VV, Roth TC (2013) Cognitive ecology of food hoarding: the evolution of spatial memory and the hippocampus. Annu Rev Ecol Evol S 44:173–193. https://doi.org/10.1146/annurev-ecolsys-110512-135904
Pyle P (1997) Molt limits in north American passerines. N Am Bird Bander 22:49–89
Reznick DN, Butler MJ, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulata). 6. Differential mortality as a mechanism for natural selection. Evolution 50:1651–1660. https://doi.org/10.2307/2410901
Royce EB, Barbour MG (2001) Mediterranean climate effects. I. Conifer water use across a Sierra Nevada ecotone. Am J Bot 88:911–918. https://doi.org/10.2307/2657044
Seber GAF (1965) A note on the multiple-recapture census. Biometrika 52:249–260. https://doi.org/10.1093/biomet/52.1-2.249
Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317. https://doi.org/10.1159/000116516
Sonnenberg BR, Branch CL, Pitera AM, Bridge ES, Pravosudov V (2019) Natural selection and spatial cognition in wild food-caching mountain chickadees. Curr bBiol 29:670–676.e3. https://doi.org/10.1016/j.cub.2019.01.006
Su Y, Yajima M (2015) R2jags: Using R to run ‘JAGS’. https://cran.project.org/package=R2jags. Accessed 03 Dec 2018
Tello-Ramos MC, Branch CL, Pitera AM, Kozlovsky DY, Bridge ES, Pravosudov VV (2018) Memory in wild mountain chickadees from different elevations: comparing first-year birds with older survivors. Anim Behav 137:149–160. https://doi.org/10.1016/j.anbehav.2017.12.019
Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, Chicago
Williams GE, Wood PB (2002) Are traditional methods of determining nest predators and nest fates reliable? An experiment with wood thrushes (Hylocichla mustelina) using miniature video cameras. Auk 119:1126–1132. https://doi.org/10.2307/4090242
Acknowledgments
We thank Rebecca Croston and Maria Tello-Ramos, who also participated in data collection. Thank you to Jeff Brown and staff of Sagehen Experimental Forest field station (University of California Berkeley) for the assistance at our field site. Thank you to Perry Williams (University of Nevada, Reno) and Noah Benedict for the advice in designing and implementing the Bayesian model. We thank Associate Editor (Dr. Dustin Rubenstein) and two anonymous reviewers for the constructive criticisms and suggestions resulting in a significantly improved manuscript.
Funding
This research was supported by the National Science Foundation (NSF) grant IOS1351295 and IOS1856181 to VVP and Division of Biological Infrastructure grant 1556313 to ESB. CLB was supported by the NSF Doctoral Dissertation Improvement Grant 1600845.
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LMB, AMP, CLB, DYK, BRS, and VVP collected data during breeding and nonbreeding seasons across 4 years. ESB designed the RFID system and provided support throughout data collection. AMP coalesced data from multiple sources to construct presence dataset later used by LMB to construct the CR dataset. LMB conducted all analyses. LMB and VVP wrote the first draft of the manuscript. AMP, CLB, DYK, and BRS all contributed to the writing. VVP established the field system.
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To the best of our knowledge, no birds were harmed by the collection of this data. All procedures were in accordance with the University of Nevada, Reno Institutional Animal Care and Use Committee (protocol no. 00046 and 00603) and California Department of Fish and Wildlife Permit SC-5210 (DocID: D-0019571790-9).
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The data supporting this study are publicly available via GitHub at https://github.com/LMbenedict/Publications/.
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The authors declare that they have no competing interests.
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Communicated by D. Rubenstein
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Benedict, L.M., Pitera, A.M., Branch, C.L. et al. Elevation-related differences in annual survival of adult food-caching mountain chickadees are consistent with natural selection on spatial cognition. Behav Ecol Sociobiol 74, 40 (2020). https://doi.org/10.1007/s00265-020-2817-2
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DOI: https://doi.org/10.1007/s00265-020-2817-2