Satellite-based environmental variables complement traditional variables in spatio-temporal models of purple martin migration
Jason R. Courter A * , Zhen Liu B , Naresh Neupane C , Ali Arab B and Joe Siegrist DA Department of Natural Sciences, Malone University, Canton, OH, USA.
B Department of Mathematics and Statistics, Georgetown University, Washington, DC, USA.
C Department of Biology, Georgetown University, Washington, DC, USA.
D Purple Martin Conservation Association, 301 Peninsula Drive, Suite 6, Erie, PA 16505, USA.
Abstract
As advanced satellite-based environmental data become widely accessible, emerging opportunities exist to understand avian lifecycle events at continental scales. Although this growing toolbox offers much promise, an abundance of options may appear overwhelming to ecologists and point to the need for interdisciplinary collaborations to develop and interpret complex, spatio-temporal models.
Here, we demonstrate that satellite-based environmental variables complement conventional variables in spatio-temporal phenology models. The objective of this case study was to assess the degree to which including more sophisticated, satellite-based greenness data in association with a customised growing degree-day metric, can improve traditional phenological models based solely on monthly temperature and precipitation.
Using 2001–2018 purple martin (Progne subis) first arrival dates (n = 49 481) from the Purple Martin Conservation Association, we develop a predictive model for their first arrival dates on the basis of traditional temperature and precipitation values from ground-based meteorological stations, the MODIS satellite-based greenness index, and a more sophisticated growing degree-day metric. We used a Bayesian framework to construct 10 spatio-temporal candidate models on the basis of different combinations of predictor variables and our best model included a combination of both traditional and customised MODIS-based variables.
Our results indicated that purple martins arrive earlier when greening occurs earlier than the mean, which is also associated with warmer spring temperatures. In addition, wetter February months also predicted earlier martin arrivals. There was no directional change in purple martin first arrival dates from 2001 to 2018 in our study region.
Our results suggest that satellite-based environmental variables complement traditional variables such as mean monthly temperature and precipitation in models of purple martin migratory phenology.
Including emerging and conventional variables in spatio-temporal models allows complex migratory changes to be detected and interpreted at broad spatial scales, which is critical as Citizen Science efforts expand. Our results also pointed to the importance of assembling interdisciplinary research teams to assess the utility of novel data products.
Keywords: first-arrival dates, climate change, growing degree-days, moderate resolution imaging spectroradiometer (MODIS), phenology, purple martin, remote-sensing, spatio-temporal models.
References
Arab A, Courter JR, Zelt J (2016) A spatio-temporal comparison of avian migration phenology using Citizen Science data. Spatial Statistics 18, 234-245.
| Crossref | Google Scholar |
Banner KM, Irvine KM, Rodhouse TJ (2020) The use of Bayesian priors in ecology: the good, the bad and the not great. Methods in Ecology and Evolution 11, 882-889.
| Crossref | Google Scholar |
Barraquand F, Ezard THG, Jørgensen PS, Zimmerman N, Chamberlain S, Salguero-Gomez R, Curran TJ, Poisot T (2014) Lack of quantitative training among early-career ecologists: a survey of the problem and potential solutions. PeerJ 2, e285.
| Crossref | Google Scholar |
Berra EF, Gaulton R (2021) Remote sensing of temperate and boreal forest phenology: a review of progress, challenges and opportunities in the intercomparison of in-situ and satellite phenological metrics. Forest Ecology and Management 480, 118663.
| Crossref | Google Scholar |
Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441, 81-83.
| Crossref | 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. Proceedings of the Royal Society B: Biological Sciences 277, 1259-1266.
| Crossref | Google Scholar |
Briedis M, Hahn S, Adamík P (2017) Cold spell en route delays spring arrival and decreases apparent survival in a long-distance migratory songbird. BMC Ecology 17, 11.
| Crossref | Google Scholar |
Butler CJ (2003) The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America. Ibis 145, 484-495.
| Crossref | Google Scholar |
Callaghan CT, Poore AGB, Major RE, Rowley JJL, Cornwell WK (2019) Optimizing future biodiversity sampling by citizen scientists. Proceedings of the Royal Society B: Biological Sciences 286, 20191487.
| Crossref | Google Scholar |
Cheke RA, Tratalos JA (2007) Migration, patchiness, and population processes illustrated by two migrant pests. BioScience 57, 145-154.
| Crossref | Google Scholar |
Chen M, Shi W, Xie P, Silva VBS, Kousky VE, Wayne Higgins R, Janowiak JE (2008) Assessing objective techniques for gauge-based analyses of global daily precipitation. Journal of Geophysical Research – Atmospheres 113, D04110.
| Crossref | Google Scholar |
Coelho MTP, Diniz-Filho JA, Rangel TF (2019) A parsimonious view of the parsimony principle in ecology and evolution. Ecography 42, 968-976.
| Crossref | Google Scholar |
Courter JR, Johnson RJ, Stuyck CM, Lang BA, Kaiser EW (2013a) Weekend bias in Citizen Science data reporting: implications for phenology studies. International Journal of Biometeorology 57, 715-720.
| Crossref | Google Scholar |
Courter JR, Johnson RJ, Bridges WC, Hubbard KG (2013b) Assessing migration of Ruby-throated Hummingbirds (Archilochus colubris) at broad spatial and temporal scales. The Auk 130, 107-117.
| Crossref | Google Scholar |
Dennis B (1996) Discussion: should ecologists become Bayesians? Ecological Applications 6, 1095-1103.
| Crossref | Google Scholar |
Dickinson JL, Zuckerberg B, Bonter DN (2010) Citizen science as an ecological research tool: challenges and benefits. Annual Review of Ecology, Evolution, and Systematics 41, 149-172.
| Crossref | Google Scholar |
Drake A, Rock CA, Quinlan SP, Martin M, Green DJ (2014) Wind speed during migration influences the survival, timing of breeding, and productivity of a neotropical migrant, Setophaga petechia. PLoS ONE 9, e97152.
| Crossref | Google Scholar |
Fraser KC, Silverio C, Kramer P, Mickle N, Aeppli R, Stutchbury BJM (2013) A trans-hemispheric migratory songbird does not advance spring schedules or increase migration rate in response to record-setting temperatures at breeding sites. PLoS ONE 8, e64587.
| Crossref | Google Scholar |
Fraser KC, Shave A, de Greef E, Siegrist J, Garroway CJ (2019) Individual variability in migration timing can explain long-term, population-level advances in a songbird. Frontiers in Ecology and Evolution 7, 324.
| Crossref | Google Scholar |
Fu Y, Zhang H, Dong W, Yuan W (2014) Comparison of phenology models for predicting the onset of growing season over the northern hemisphere. PLoS ONE 9, e0109544.
| Crossref | Google Scholar |
Gao F, Hilker T, Zhu X, Anderson M, Masek J, Wang P, Yang Y (2015) Fusing Landsat and MODIS data for vegetation monitoring. IEEE Geoscience and Remote Sensing Magazine 3, 47-60.
| Crossref | Google Scholar |
Gibb R, Shoji A, Fayet AL, Perrins CM, Guilford T, Freeman R (2017) Remotely sensed wind speed predicts soaring behaviour in a wide-ranging pelagic seabird. Journal of the Royal Society Interface 14, 20170262.
| Crossref | Google Scholar |
Gordo O (2007) Why are bird migration dates shifting? A review of weather and climate effects on avian migratory phenology. Climate Research 35, 37-58.
| Crossref | Google Scholar |
Haest B, Hüppop O, Bairlein F (2018a) The influence of weather on avian spring migration phenology: what, where and when? Global Change Biology 24, 5769-5788.
| Crossref | Google Scholar |
Haest B, Hüppop O, Bairlein F (2018b) Challenging a 15-year-old claim: The North Atlantic oscillation index as a predictor of spring migration phenology of birds. Global Change Biology 24, 1523-1537.
| Crossref | Google Scholar |
Hussell DJT (2003) Climate change, spring temperatures, and timing of breeding of tree swallows (Tachycineta bicolor) in southern Ontario. The Auk 120, 607-618.
| Crossref | Google Scholar |
Knudsen E, Lindén A, Both C, Jonzén N, Pulido F, Saino N, Sutherland WJ, Bach LA, Coppack T, Ergon T, Gienapp P, Gill JA, et al. (2011) Challenging claims in the study of migratory birds and climate change. Biological Reviews 86, 928-946.
| Crossref | Google Scholar |
La Sorte FA, Graham CH (2021) Phenological synchronization of seasonal bird migration with vegetation greenness across dietary guilds. Journal of Animal Ecology 90, 343-355.
| Crossref | Google Scholar |
La Sorte FA, Lepczyk CA, Burnett JL, Hurlbert AH, Tingley MW, Zuckerberg B (2018) Opportunities and challenges for big data ornithology. The Condor 120, 414-426.
| Crossref | Google Scholar |
Leinonen I, Kramer K (2002) Applications of phenological models to predict the future carbon sequestration potential of boreal forests. Climatic Change 55, 99-113.
| Crossref | Google Scholar |
Lin J, Liu X, Li K, Li X (2014) A maximum entropy method to extract urban land by combining MODIS reflectance, MODIS NDVI, and DMSP-OLS data. International Journal of Remote Sensing 35, 6708-6727.
| Crossref | Google Scholar |
Linek N, Brzęk P, Gienapp P, O’Mara MT, Pokrovsky I, Schmidt A, Shipley JR, Taylor JRE, Tiainen J, Volkmer T, Wikelski M, Partecke J (2021) A partial migrant relies upon a range-wide cue set but uses population-specific weighting for migratory timing. Movement Ecology 9, 63.
| Crossref | Google Scholar |
Marra PP, Francis CM, Mulvihill RS, Moore FR (2005) The influence of climate on the timing and rate of spring bird migration. Oecologia 142, 307-315.
| Crossref | Google Scholar |
Mayor SJ, Guralnick RP, Tingley MW, Otegui J, Withey JC, Elmendorf SC, Andrew ME, Leyk S, Pearse IS, Schneider DC (2017) Increasing phenological asynchrony between spring green-up and arrival of migratory birds. Scientific Reports 7, 1902.
| Crossref | Google Scholar |
McKinnon L, Picotin M, Bolduc E, Juillet C, Bêty J (2012) Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. Canadian Journal of Zoology 90, 961-971.
| Crossref | Google Scholar |
Mesaglio T, Callaghan CT (2021) An overview of the history, current contributions and future outlook of iNaturalist in Australia. Wildlife Research 48, 289-303.
| Crossref | Google Scholar |
Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P (2008) Bird migration times, climate change, and changing population sizes. Global Change Biology 14, 1959-1972.
| Crossref | Google Scholar |
Moreira FS, Regos A, Gonçalves JF, Rodrigues TM, Verde A, Pagès M, Pérez JA, Meunier B, Lepetit J-P, Honrado JP, Gonçalves D (2022) Combining citizen science data and satellite descriptors of ecosystem functioning to monitor the abundance of a migratory bird during the non-breeding season. Remote Sensing 14, 463.
| Crossref | Google Scholar |
Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences 105, 16195-16200.
| Crossref | Google Scholar |
Nebel S, Mills A, McCracken JD, Taylor PD (2010) Declines of aerial insectivores in North America follow a geographic gradient. Avian Conservation and Ecology 5, 1.
| Crossref | Google Scholar |
Neupane N, Goldbloom-Helzner A, Arab A (2021) Spatio-temporal modeling for confirmed cases of lyme disease in Virginia. Ticks and Tick-borne Diseases 12, 101822.
| Crossref | Google Scholar |
Neupane N, Peruzzi M, Arab A, Mayor SJ, Withey JC, Ries L, Finley AO (2022) A novel model to accurately predict continental-scale timing of forest green-up. International Journal of Applied Earth Observation and Geoinformation 108, 102747.
| Crossref | Google Scholar |
Pearce-Higgins JW, Eglington SM, Martay B, Chamberlain DE (2015) Drivers of climate change impacts on bird communities. Journal of Animal Ecology 84, 943-954.
| Crossref | Google Scholar |
Renner SS, Zohner CM (2018) Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annual Review of Ecology, Evolution, and Systematics 49, 165-182.
| Crossref | Google Scholar |
Rockwell SM, Wunderle JM, Sillett TS, Bocetti CI, Ewert DN, Currie D, White JD, Marra PP (2017) Seasonal survival estimation for a long-distance migratory bird and the influence of winter precipitation. Oecologia 183, 715-726.
| Crossref | Google Scholar |
Rosenberg KV, Dokter AM, Blancher PJ, Sauer JR, Smith AC, Smith PA, Stanton JC, Panjabi A, Helft L, Parr M, Marra PP (2019) Decline of the North American avifauna. Science 366, 120-124.
| Crossref | Google Scholar |
Rotics S, Kaatz M, Turjeman S, Zurell D, Wikelski M, Sapir N, Eggers U, Fiedler W, Jeltsch F, Nathan R (2018) Early arrival at breeding grounds: causes, costs and a trade-off with overwintering latitude. Journal of Animal Ecology 87, 1627-1638.
| Crossref | Google Scholar |
Saino N, Ambrosini R, Rubolini D, von Hardenberg J, Provenzale A, Hüppop K, Hüppop O, Lehikoinen A, Lehikoinen E, Rainio K, Romano M, Sokolov L (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proceedings of the Royal Society B: Biological Sciences 278, 835-842.
| Crossref | Google Scholar |
Sauer JR, Link WA, Hines JE (2020) The North American breeding bird survey, analysis results 1966–2019: US Geological Survey data release 10, P96A7675. 10.5066/P96A7675
Seidl R (2017) To model or not to model, that is no longer the question for ecologists. Ecosystems 20, 222-228.
| Crossref | Google Scholar |
Shariati Najafabadi M, Darvishzadeh R, Skidmore AK, Kölzsch A, Vrieling A, Nolet BA, Exo K-M, Meratnia N, Havinga PJM, Stahl J, Toxopeus AG (2015) Satellite-versus temperature-derived green wave indices for predicting the timing of spring migration of avian herbivores. Ecological Indicators 58, 322-331.
| Crossref | Google Scholar |
Si Y, Xin Q, Prins HHT, de Boer WF, Gong P (2015) Improving the quantification of waterfowl migration with remote sensing and bird tracking. Science Bulletin 60, 1984-1993.
| Crossref | Google Scholar |
Sockman J, Courter J (2018) The impacts of temperature, precipitation, and growing degree-days on first egg dates of eastern bluebird (Sialia sialis) and tree swallow (Tachycineta bicolor) in Ohio. The American Midland Naturalist 180, 207-215.
| Crossref | Google Scholar |
Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A (2002) Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society Series B: Statistical Methodology 64, 583-639.
| Crossref | Google Scholar |
Spiller KJ, Dettmers R (2019) Evidence for multiple drivers of aerial insectivore declines in North America. The Condor 121, duz010.
| Crossref | Google Scholar |
Tombre IM, Høgda KA, Madsen J, Griffin LR, Kuijken E, Shimmings P, Rees E, Verscheure C (2008) The onset of spring and timing of migration in two arctic nesting goose populations: the pink-footed goose Anser bachyrhynchus and the barnacle goose Branta leucopsis. Journal of Avian Biology 39, 691-703.
| Crossref | Google Scholar |
Tøttrup AP, Thorup K, Rainio K, Yosef R, Lehikoinen E, Rahbek C (2008) Avian migrants adjust migration in response to environmental conditions en route. Biology Letters 4, 685-688.
| Crossref | Google Scholar |
Trudgill DL, Honek A, Li D, Van Straalen NM (2005) Thermal time – concepts and utility. Annals of Applied Biology 146, 1-14.
| Crossref | Google Scholar |
Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society B: Biological Sciences 272, 2561-2569.
| Crossref | Google Scholar |
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Gudberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416, 389-395.
| Crossref | Google Scholar |
Wang C, Cao R, Chen J, Rao Y, Tang Y (2015) Temperature sensitivity of spring vegetation phenology correlates to within-spring warming speed over the Northern Hemisphere. Ecological Indicators 50, 62-68.
| Crossref | Google Scholar |
Watanabe S (2010) Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. Journal of Machine Learning Research 11, 3571-3594.
| Google Scholar |
Weisshaupt N, Arizaga J, Maruri M (2018) The role of radar wind profilers in ornithology. Ibis 160, 516-527.
| Crossref | Google Scholar |
Xie P, Chen M, Yang S, Yatagai A, Hayasaka T, Fukushima Y, Liu C (2007) A gauge-based analysis of daily precipitation over East Asia. Journal of Hydrometeorology 8, 607-626.
| Crossref | Google Scholar |
Youngflesh C, Socolar J, Amaral BR, Arab A, Guralnick RP, Hurlbert AH, LaFrance R, Mayor SJ, Miller DAW, Tingley MW (2021) Migratory strategy drives species-level variation in bird sensitivity to vegetation green-up. Nature Ecology & Evolution 5, 987-994.
| Crossref | Google Scholar |
Zhang X, Friedl MA, Schaaf CB, Strahler AH (2004) Climate controls on vegetation phenological patterns in northern mid-and high latitudes inferred from MODIS data. Global Change Biology 10, 1133-1145.
| Crossref | Google Scholar |
Zhu L, Guo Y (2022) Remotely sensed winter habitat indices improve the explanation of broad-scale patterns of mammal and bird species richness in China. Remote Sensing 14, 794.
| Crossref | Google Scholar |
Zuckerberg B (2008) Overcoming ‘analysis paralysis’. Frontiers in Ecology and the Environment 6, 505-506.
| Crossref | Google Scholar |