Abstract
Most shorebirds depend on coastal habitats for much of their life cycle. The quality and diversity of feeding areas during the wintering period directly condition their winter survival, subsequent migration, and breeding success. During their wintering in France, shorebirds use intertidal areas for feeding, both in daylight and at night, depending on the availability of mudflats during the tidal cycle. In this context, we studied whether the bar-tailed godwit (Limosa lapponica) shows contrasting foraging behaviors and distributions between day and night in response to differences in visual capacities, prey availability, potential predation risk, and human activities. We carried out a fine-scale GPS tracking of birds at one of their main wintering sites along the French Atlantic coast. We predicted smaller foraging home ranges at night because of limits for godwits to detect prey visually, suggesting more sediment probing and less movement. Godwits used the entire time window when they have access to intertidal areas, but they faithfully selected distinct diurnal and nocturnal feeding areas using a low number of patches. This variability in space use highlights differences in selection of habitats, such as seagrass beds selected by most of the tracked godwits by day and used much less at night. In addition, distinct feeding distributions of monitored birds revealed interindividual variability in habitat selection, even more by night, most likely to reduce intraspecific competition. We therefore urge greater consideration of the night distribution of birds, rarely evaluated in shorebird studies, to define areas and habitats of importance to future management and conservation measures.
Similar content being viewed by others
References
Abrahams, M.V., and L.M. Dill. 1989. A determination of the energetic equivalence of the risk of predation. Ecology 70 (4): 999–1007. https://doi.org/10.2307/1941368.
Aubouin, Naïs. 2014. Etude de la distribution et des stratégies de survie hivernale de populations migratrices d’oiseaux limicoles en vue d’actions de conservation en région Poitou Charentes: exemple de la Barge rousse Limosa lapponica. Msc Thesis Université de Montpellier 64p.
Bajjouk, T., B. Guillaumont, N. Michez, B. Thouin, C. Croguennec, J. Populus, J. Louvel-Glaser, V. Gaudillat , C. Chevalier, J. Tourolle and D. Hamon. 2015. Classification EUNIS, Système d’information européen sur la nature : Traduction française des habitats benthiques des Régions Atlantique et Méditerranée. Vol. 1. Habitats Littoraux. IFREMER/DYNECO/AG/15‐02/TB1. https://archimer.ifremer.fr/doc/00271/38222/.
Bijleveld, A.I., J.A. van Gils, J. van der Meer, A. Dekinga, C. Kraan, H.W. van der Veer, and T. Piersma. 2012. Designing a benthic monitoring programme with multiple conflicting objectives. Methods in Ecology and Evolution 3 (3): 526–536. https://doi.org/10.1111/j.2041-210X.2012.00192.x.
BirdLife International. 2015. European red list of birds.
BirdLife International. 2017. Limosa lapponica (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017: e.T22693158A111221714. https://dx.doi.org/10.2305/IUCN.UK.2017-1.RLTS.T22693158A111221714.en.
Bocher, P., T. Piersma, A. Dekinga, C. Kraan, M.G. Yates, T. Guyot, E. Folmer, and G. Radenac. 2007. Site-and species-specific distribution patterns of molluscs at five intertidal soft-sediment areas in Northwest Europe during a single winter. Marine Biology 151 (2): 577–594. https://doi.org/10.1007/s00227-006-0500-4.
Burger, J., and L. Niles. 2013. Shorebirds and stakeholders: effects of beach closure and human activities on shorebirds at a New Jersey coastal beach. Urban Ecosystem 16 (3): 657–673. https://doi.org/10.1007/s11252-012-0269-9.
Burton, N.H.K., and M.J.S. Armitage. 2005. Differences in the diurnal and nocturnal use of intertidal feeding grounds by Redshank Tringa totanus. Bird Study 52 (2): 120–128. https://doi.org/10.1080/00063650509461381.
Calenge, C. 2011. Exploratory analysis of the habitat selection by the wildlife in R: the adehabitatHS package. Office national de la chasse et de la faune sauvage, Saint Benoist 78610. Auffargis, France. Available at: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.473.208&rep=rep1&type=pdf.
Calenge, C. 2015. Home range estimation in R: the adehabitatHR package. Saint Benoist, Auffargis, France: Office national de la classe et de la faune sauvage.
Calenge, C., and A.B. Dufour. 2006. Eigenanalysis of selection ratios from animal radio-tracking data. Ecology 87 (9): 2349–2355. https://doi.org/10.1890/0012-9658(2006)87[2349:EOSRFA]2.0.CO;2.
Colwell, M.A., and S.L. Landrum. 1993. Nonrandom shorebird distribution and fine-scale variation in prey abundance. The Condor 95 (1): 94–103. https://doi.org/10.2307/1369390.
Colwell, M.A., T. Danufsky, N.W. Fox-Fernandez, J.E. Roth, and J.R. Conklin. 2003. Variation in shorebird use of diurnal, high-tide roosts: How consistently are roosts used? Waterbirds 26 (4): 484–493. https://doi.org/10.1675/1524-4695(2003)026[0484:VISUOD]2.0.CO;2.
Cramp, S., K.E.L. Simmons, D.C. Brooks, N.J. Collar, E. Dunn, R. Gillmor, P.A.D. Hollom, et al. 1983. Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic: 3. Waders to gulls. Oxford University Press: Oxford. ISBN 0-19-857506-8, 913 pp.
Cunningham, S.J., J.R. Corfield, A.N. Iwaniuk, I. Castro, M.R. Alley, T.R. Birkhead, and S. Parsons. 2013. The anatomy of the bill tip of kiwi and associated somatosensory regions of the brain: comparisons with shorebirds. PloS One 8. Public Library of Science: e80036. https://doi.org/10.1371/journal.pone.0080036.
De Azuaje, L.M.R., S. Tai, and R. McNeil. 1993. Comparison of rod/cone ratio in three species of shorebirds having different nocturnal foraging strategies. The Auk: 110 (1): 141–145. Retrieved November 19, 2020, from http://www.jstor.org/stable/4088244.
De Boer, W.F., and F.A. Longamane. 1996. The exploitation of intertidal food resources in Inhaca Bay, Mozambique, by shorebirds and humans. Biological Conservation 78 (3): 295–303. https://doi.org/10.1016/S0006-3207(96)00050-X.
Delany, S., D. Scott, T. Dodman, and D. Stroud. 2009. The wader atlas: an atlas of wader populations in Africa and Western Eurasia.
Demongin, L. (2016). Identification guide to birds in the hand. Cambridge: Cambridge University Press. 392 pp.
Dias, M.P., F. Peste, J.P. Granadeiro, and J.M. Palmeirim. 2008. Does traditional shellfishing affect foraging by waders? The case of the Tagus estuary (Portugal). Acta Oecologica 33 (2): 188–196. https://doi.org/10.1016/j.actao.2007.10.005.
Dias, M.P., J.P. Granadeiro, and J.M. Palmeirim. 2009. Searching behaviour of foraging waders: does feeding success influence their walking? Animal Behaviour 77 (5): 1203–1209. https://doi.org/10.1016/j.anbehav.2009.02.002.
Dodd, S.L., and M.A. Colwell. 1996. Seasonal variation in diurnal and nocturnal distributions of nonbreeding shorebirds at North Humboldt Bay, California. The Condor 98 (2): 196–207.
Dugan, P.J. 1981. The importance of nocturnal foraging in shorebirds: a consequence of increased invertebrate prey activity. In Feeding and survival strategies of estuarine organisms, ed. N.V. Jones and W.J. Wolff, 251–260. Boston, MA: Springer US. https://doi.org/10.1007/978-1-4613-3318-0_19.
Duijns, S., N.A. Hidayati, and T. Piersma. 2013. Bar-tailed godwits Limosa l. lapponica eat polychaete worms wherever they winter in Europe. Bird Study 60 (4): 509–517. https://doi.org/10.1080/00063657.2013.836153.
Duijns, S., J.A. Van Gils, B. Spaans, J. ten Horn, M. Brugge, and T. Piersma. 2014. Sex-specific winter distribution in a sexually dimorphic shorebird is explained by resource partitioning. Ecology and Evolution 4 (20): 4009–4018. https://doi.org/10.1002/ece3.1213.
Dwyer, R.G., S. Bearhop, H.A. Campbell, and D.M. Bryant. 2013. Shedding light on light: benefits of anthropogenic illumination to a nocturnally foraging shorebird. Journal of Animal Ecology 82 (2): 478–485. https://doi.org/10.1111/1365-2656.12012.
Esser, W., S. Vöge, and K.-M. Exo. 2008. Day-night activity of intertidal invertebrates and methods to estimate prey accessibility for shorebirds. Senckenbergiana Maritima 38 (2): 115–122. https://doi.org/10.1007/BF03055286.
Evans, P.R. 1986. Correct measurement of the wing-length of waders. Wader Study Group Bull 48: 11.
Evans, A. 1987. Relative availability of the prey of wading birds by day and by night. Marine Ecology Progress Series 37: 103–107.
Goss-Custard, J.D., A.D. West, M.G. Yates, R.W.G. Caldow, R.A. Stillman, L. Bardsley, J. Castilla, M. Castro, V. Dierschke, S.E.A. Durell, G. Eichhorn, B.J. Ens, K.M. Exo, P.U. Udayangani-Fernando, P.N. Ferns, P.A.R. Hockey, J.A. Gill, I. Johnstone, B. Kalejta-Summers, J.A. Masero, F. Moreira, R.V. Nagarajan, I.P.F. Owens, C. Pacheco, A. Perez-Hurtado, D. Rogers, G. Scheiffarth, H. Sitters, W.J. Sutherland, P. Triplet, D.H. Worrall, Y. Zharikov, L. Zwarts, and R.A. Pettifor. 2007. Intake rates and the functional response in shorebirds (Charadriiformes) eating macro-invertebrates. Biological Reviews 81 (4): 501–529. https://doi.org/10.1111/j.1469-185X.2006.tb00216.x.
Granadeiro, J.P., M.P. Dias, R.C. Martins, and J.M. Palmeirim. 2006. Variation in numbers and behaviour of waders during the tidal cycle: implications for the use of estuarine sediment flats. Acta Oecologica 29 (3): 293–300. https://doi.org/10.1016/j.actao.2005.11.008.
Gunnarsson, T.G., J.A. Gill, J. Newton, P.M. Potts, and W.J. Sutherland. 2005. Seasonal matching of habitat quality and fitness in a migratory bird. Proceedings of the Royal Society B: Biological Sciences 272 (1578): 2319–2323. https://doi.org/10.1098/rspb.2005.3214.
Gunnarsson, T.G., J.A. Gill, P.W. Atkinson, G. Gélinaud, P.M. Potts, R.E. Croger, G.A. Gudmundsson, G.F. Appleton, and W.J. Sutherland. 2006. Population-scale drivers of individual arrival times in migratory birds. Journal of Animal Ecology 75 (5): 1119–1127.
Handel, C.M., and R.E. Gill. 1992. Roosting behavior of premigratory dunlins (Calidris alpina). The Auk 109 (1): 57–72. https://doi.org/10.2307/4088266.
Hilton, G.M., G.D. Ruxton, and W. Cresswell. 1999. Choice of foraging area with respect to predation risk in redshanks: the effects of weather and predator activity. Oikos 87 (2): 295–302. https://doi.org/10.2307/3546744.
Johnson, D.H. 1980. The comparison of usage and availability measurements for evaluating resource preference. Ecology 61 (1): 65–71. https://doi.org/10.2307/1937156.
Kelsey, M.G., and M. Hassall. 1989. Patch selection by dunlin on a heterogeneous mudflat. Ornis Scandinavica (Scandinavian Journal of Ornithology) 20 (4): 250–254. https://doi.org/10.2307/3676488.
Kie, J.G., J. Matthiopoulos, J. Fieberg, R.A. Powell, F. Cagnacci, M.S. Mitchell, J.-M. Gaillard, and P.R. Moorcroft. 2010. The home-range concept: are traditional estimators still relevant with modern telemetry technology? Philosophical Transactions of the Royal Society B: Biological Sciences 365 (1550): 2221–2231. https://doi.org/10.1098/rstb.2010.0093.
Kuwae, T. 2007. Diurnal and nocturnal feeding rate in Kentish plovers Charadrius alexandrinus on an intertidal flat as recorded by telescopic video systems. Marine Biology 151 (2): 663–673.
Lafferty, K.D. 2001. Birds at a Southern California beach: seasonality, habitat use and disturbance by human activity. Biodiversity and Conservation 10 (11): 1949–1962.
Last, K.S., and P.J.W. Olive. 2004. Interaction between photoperiod and an endogenous seasonal factor in influencing the diel locomotor activity of the benthic polychaete Nereis virens Sars. The Biological Bulletin 206 (2): 103–112. https://doi.org/10.2307/1543541.
Laver, P.N., and M.J. Kelly. 2008. A critical review of home range studies. Journal of Wildlife Management 72 (1): 290–298. https://doi.org/10.2193/2005-589.
Lourenço, P.M., A. Silva, C.D. Santos, A.C. Miranda, J.P. Granadeiro, and J.M. Palmeirim. 2008. The energetic importance of night foraging for waders wintering in a temperate estuary. Acta Oecologica 34 (1): 122–129. https://doi.org/10.1016/j.actao.2008.04.005.
Mallory, M.L., and C.D. Gilbert. 2008. Leg-loop harness design for attaching external transmitters to seabirds. Marine Ornithology 36: 183–188.
Manly, B.F., L. McDonald, D.L. Thomas, T.L. McDonald, and W.P. Erickson. 2002. Resource selection by animals: statistical design and analysis for field studies. Berlin: Springer Science & Business Media.
Martin, G. 1990. Birds by night. Poyser Monographs. London: Poyser. Retrieved November 19, 2020, from https://doi.org/10.5040/9781472596956.
Martin, G.R. 2012. Through birds’ eyes: insights into avian sensory ecology. Journal of Ornithology 153 (S1): 23–48. https://doi.org/10.1007/s10336-011-0771-5.
McNamara, J., and A. Houston. 1980. The application of statistical decision theory to animal behaviour. Journal of Theoretical Biology 85 (4): 673–690. https://doi.org/10.1016/0022-5193(80)90265-9.
McNeil, R., and J.R. Rodriguez. 1996. Nocturnal foraging in shorebirds. International Wader Studies 8: 114–121.
McNeil, R., P. Drapeau, and J.D. Goss-Custard. 1992. The occurrence and adaptive significance of nocturnal habits in waterfowl. Biological Reviews 67 (4): 381–419. https://doi.org/10.1111/j.1469-185X.1992.tb01188.x.
McNeil, R., O. Díaz Díaz, and I. Liñero A., and J. R. Rodríguez S. 1995. Day- and night-time prey availability for waterbirds in a tropical lagoon. Canadian Journal of Zoology 73 (5): 869–878. https://doi.org/10.1139/z95-102.
Morrison, G., N.C. Davidson, and J. Wilson. 2007. Survival of the fattest: body stores on migration and survival in red knots Calidris canutus islandica. Journal of Avian Biology 38 (4): 479–487.
Mouritsen, K.N. 1993. Diurnal and nocturnal prey detection by dunlins Calidris alpina. Bird Study 40 (3): 212–215. https://doi.org/10.1080/00063659309477185.
Mouritsen, K.N. 1994. Day and night feeding in dunlins Calidris alpina: choice of habitat, foraging technique and prey. Journal of Avian Biology 25 (1): 55–62. https://doi.org/10.2307/3677294.
Navedo, J.G., and J.A. Masero. 2007. Measuring potential negative effects of traditional harvesting practices on waterbirds: a case study with migrating curlews. Animal Conservation 10 (1): 88–94. https://doi.org/10.1111/j.1469-1795.2006.00076.x.
Nolet, B.A., and W.M. Mooij. 2002. Search paths of swans foraging on spatially autocorrelated tubers. Journal of Animal Ecology 71 (3): 451–462. https://doi.org/10.1046/j.1365-2656.2002.00610.x.
Pienkowski, M.W. 1983. Changes in the foraging pattern of plovers in relation to environmental factors. Animal Behaviour 31 (1): 244–264. https://doi.org/10.1016/S0003-3472(83)80195-X.
Piersma, T., P. de Goeij, and I. Tulp. 1993. An evaluation of intertidal feeding habitats from a shorebird perspective: towards relevant comparisons between temperate and tropical mudflats. Netherlands Journal of Sea Research 31 (4): 503–512. https://doi.org/10.1016/0077-7579(93)90062-W.
Piersma, T., R.E. Gill, P. de Goeij, A. Dekinga, M.L. Shepherd, D. Ruthrauff, and L. Tibbitts. 2006. Shorebird avoidance of nearshore feeding and roosting areas at night correlates with presence of a nocturnal avian predator. Bulletin-Wader Study Group 109: 73–76.
Pitelka, F.A. 1979. Shorebirds in marine environments (No. 598.8 SHO). Cooper Ornithological Society, 261 pp.
Prater, A.J., J.H. Marchant, and J. Vourinen. 1977. Guide to the identification and ageing of Holartcic waders. British Trust for Ornithology, Tring, UK.
Puttick, G.M. 1984. Foraging and activity patterns in wintering shorebirds. Behavior of Marine Animals: Current Perspectives in Research.
Pyle, P. 2008. Identification guide to North America birds. Part II: Anatidae to Alcidae. Slate Creek Press, Point Reyes Station, California, 836 pp.
Quaintenne, G., J.A. van Gils, P. Bocher, A. Dekinga, and T. Piersma. 2010. Diet selection in a molluscivore shorebird across Western Europe: does it show short- or long-term intake rate-maximization? Journal of Animal Ecology 79 (1): 53–62. https://doi.org/10.1111/j.1365-2656.2009.01608.x.
Rogers, D.I., P.F. Battley, T. Piersma, J.A. Van Gils, and K.G. Rogers. 2006. High-tide habitat choice: insights from modelling roost selection by shorebirds around a tropical bay. Animal Behaviour 72 (3): 563–575. https://doi.org/10.1016/j.anbehav.2005.10.029.
Rohweder, D.A. 2001. Nocturnal roost use by migratory waders in the Richmond River estuary, northern New South Wales, Australia. Stilt: 40: 23–28.
Rojas, L.M., R. McNeil, T. Cabana, and P. Lachapelle. 1999. Diurnal and nocturnal visual capabilities in shorebirds as a function of their feeding strategies. Brain, Behavior and Evolution 53 (1): 29–43. https://doi.org/10.1159/000006580.
Rompré, G., and R. McNeil. 1996. Variability in day and night feeding habitat use in the willet Catoptrophorus semipalmatus during the non-breeding season in northeastern Venezuela. Wader Study Group Bulletin 81: 82–87.
Rosa, S., A.L. Encarnação, J.P. Granadeiro, and J.M. Palmeirim. 2006. High water roost selection by waders: maximizing feeding opportunities or avoiding predation? Ibis 148 (1): 88–97. https://doi.org/10.1111/j.1474-919X.2006.00497.x.
Santos, C.D., A.C. Miranda, J.P. Granadeiro, P.M. Lourenço, S. Saraiva, and J.M. Palmeirim. 2010. Effects of artificial illumination on the nocturnal foraging of waders. Acta Oecologica 36 (2): 166–172. https://doi.org/10.1016/j.actao.2009.11.008.
Schmaltz, L., G. Quaintenne, L. Couzi, and J. Dupuy. 2019. Comptage des Oiseaux d’eau à la mi-janvier en France. Résultats 2019 du comptage Wetlands International. LPO Bird-Life France - Service Connaissance, Wetlands International, Ministère de la Transition écologique et solidaire. 25 pp. & annexes 104 pp., Rochefort.
Schuler, K.L., G.M. Schroeder, J.A. Jenks, and J.G. Kie. 2014. Ad hoc smoothing parameter performance in kernel estimates of GPS-derived home ranges. Wildlife Biology 20 (5): 259–266. https://doi.org/10.2981/wlb.12117.
Sitters, H.P. 2000. The role of night-feeding in shorebirds in an estuarine environment with specific reference to mussel-feeding oystercatchers. PhD thesis, Edward Grey Institute, Department of Zoology. University of Oxford, Oxford.
Sitters, H.P., P.M. Gonzalez, T. Piersma, A.J. Baker, D.J. Price, H.P. Sitters, P.M. González, A.J. Baker, and D.J. Price. 2001. Day and night feeding habitat of red knots in Patagonia: profitability versus safety? Journal of Field Ornithology 72 (1): 86–95. https://doi.org/10.1648/0273-8570-72.1.86.
Smith, K.W., J.M. Reed, and B.E. Trevis. 1999. Nocturnal and diurnal activity patterns and roosting sites of green sandpipers Tringa ochropus wintering in southern England. Ringing & Migration 19 (4): 315–322. https://doi.org/10.1080/03078698.1999.9674200.
Stephens, D., and J.R. Krebs. 1986. Foraging theory. Vol. 1. Princeton: Princeton University Press. https://doi.org/10.2307/1381654.
Thomas, K., R.G. Kvitek, and C. Bretz. 2003. Effects of human activity on the foraging behavior of sanderlings Calidris alba. Biological Conservation 109 (1): 67–71. https://doi.org/10.1016/S0006-3207(02)00137-4.
Triplet, P., S. Le Dréan Quénec’hdu, and R. Mahéo. 2010. La Barge rousse Limosa lapponica hivernant en France (1977-2009). Alauda 78: 207–216.
Turpie, J.K., and P.A.R. Hockey. 1993. Comparative diurnal and nocturnal foraging behaviour and energy intake of premigratory grey plovers Pluvialis squatarola and whimbrels Numenius phaeopus in South Africa. Ibis 135 (2): 156–165. https://doi.org/10.1111/j.1474-919X.1993.tb02827.x.
van de Kam, J., B. Ens, T. Piersma, and L. Zwarts. 2004. Shorebirds: an illustrated behavioural ecology. KNNV Publishers, Utrecht, The Netherlands.
van Gils, Jan A., I.W. Schenk, O. Bos, and T. Piersma. 2003. Incompletely informed shorebirds that face a digestive constraint maximize net energy gain when exploiting patches. The American Naturalist 161 (5): 777–793. https://doi.org/10.1086/374205.
Van Winkle, W. 1975. Comparison of several probabilistic home-range models. The Journal of Wildlife Management 39 (1): 118–123. https://doi.org/10.2307/3800474.
VanDusen, B.M., S.R. Fegley, and C.H. Peterson. 2012. Prey distribution, physical habitat features, and guild traits interact to produce contrasting shorebird assemblages among foraging patches. PLoS One 7 (12): e52694. https://doi.org/10.1371/journal.pone.0052694.
Verger, F. 2005. Marais maritimes et estuaires du littoral français. Paris, Belin, 335 pp.
West, A.D., J.D. Goss-Custard, S.E.A. Le V. dit Durell, and R.A. Stillman. 2005. Maintaining estuary quality for shorebirds: towards simple guidelines. Biological Conservation 123 (2): 211–224. https://doi.org/10.1016/j.biocon.2004.11.010.
Worton, B.J. 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70 (1): 164–168. https://doi.org/10.2307/1938423.
Zharikov, Y., and G. Skilleter. 2003. Depletion of benthic invertebrates by bar-tailed godwits Limosa lapponica in a subtropical estuary. Marine Ecology Progress Series 254: 151–162. https://doi.org/10.3354/meps254151.
Acknowledgments
We thank Jérôme Jourde for his help in determining the benthic macrofauna, Tania Damany and Sébastien Comarmond for their help with sample processing, and Françoise Amélineau and Chloé Tanton for their help during bird capture/marking sessions. We also thank all the volunteers who participated in bird captures and sediment sampling. We thank Christine Dupuy and Christel Lefrançois for the logistic support.
Funding
This work has been supported by the ECONAT project funded by the Contrat de Plan Etat-Région and the CNRS and the European Regional Development Fund (QUALIDRIS project). This work was also funded by the ANR Pampas (ANR-18 CE32-0006) and the Ligue pour la Protection des Oiseaux.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All work adheres to the legal requirements of the countries in which it was carried out and meets ethical and animal welfare guidelines.
Additional information
Communicated by James Lovvorn
Supplementary Information
ESM 1
(PDF 217 kb)
Rights and permissions
About this article
Cite this article
Jourdan, C., Fort, J., Pinaud, D. et al. Nycthemeral Movements of Wintering Shorebirds Reveal Important Differences in Habitat Uses of Feeding Areas and Roosts. Estuaries and Coasts 44, 1454–1468 (2021). https://doi.org/10.1007/s12237-020-00871-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-020-00871-5