climate change; disturbance; engineering; fish; hydro ecology; hydropower; migration; river
Abstract :
[en] 1. Changes in migration timing, resulting from the alteration in river continuity or the
effect of climate change, can have major consequences on the population dynamics
of diadromous fish. Forecasting the phenology of fish migration is thus critically
important to implement management actions aimed at protecting fish during
their migration.
2. In this study, an 11-year monitoring survey of Atlantic salmon smolts (Salmo salar)
from the Ourthe River, Belgium, was analysed within a European Special Area of
Conservation to improve the understanding of environment-induced spring migration.
A logistic model was fitted to forecast smolt migration and to calculate phenological
indicators for management, i.e. the onset, end, and duration of
migration, while accounting for the influence of photoperiod, water temperature,
and hydrological conditions.
3. The results indicated that the photo-thermal units accumulated by smolts above a
7 C temperature threshold was a relevant proxy to reflect the synergistic effect
between temperature and photoperiod on smolt migration. After integrating the
effect of river flow pulses, the model accurately explained the inter-annual
changes in migration timing (R2 = 0.95). The model predictions provide decisive
management information to identify sensitive periods during which mitigation
measures (e.g. hydropower turbine shutdown, river discharge management)
should be conducted to promote smolt survival.
4. The model was used to predict phenological characteristics under future scenarios
of climate change. The results suggest a joint effect of hydrological alterations
and water warming. Temperature increases of 1–4 C were associated with earlier
initiation of migration, 6–51 days earlier, and spring flood events greatly
influenced the duration of the migration period. Accordingly, the combined
effects of human-induced modifications of the hydrological regimes and increasing
temperatures could result in a mismatch between the smolt and favourable
survival conditions in the marine environment.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Environmental sciences & ecology
Author, co-author :
Nils, Teichert; Station Marine de Dinard, Dinard, France
Benitez, Jean-Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire de Démographie des poissons et hydroécologie
Dierckx, Arnaud ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Département de Biologie, Ecologie et Evolution
Tétard, Stéphane; EDF R&D
De Oliveira, Eric; EDF R&D
Trancart, Thomas; Station Marine de Dinard, Dinard, France
Feunteun, Eric; Station Marine de Dinard, Dinard, France
Ovidio, Michaël ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire de Démographie des poissons et hydroécologie
Language :
English
Title :
Development of an accurate model to predict the phenology of Atlantic salmon smolt spring migration
Publication date :
August 2020
Journal title :
Aquatic Conservation
ISSN :
1052-7613
eISSN :
1099-0755
Publisher :
John Wiley & Sons, Hoboken, United States - New Jersey
Adler, D., Kelly, S.T., (2018) vioplot: Violin plot. R package version 0.3.0
Aldvén, D., Degerman, E., Höjesjö, J., Environmental cues and downstream migration of anadromous brown trout (Salmo trutta) and Atlantic salmon (Salmo salar) smolts (2015) Boreal Environment Research, 20, pp. 35-44
Antonsson, T., Gudjonsson, S., Variability in timing and characteristics of Atlantic salmon smolt in Icelandic Rivers (2002) Transactions of the American Fisheries Society, 131, pp. 643-655
Bardonnet, A., Baglinière, J.-L., Freshwater habitat of Atlantic salmon (Salmo salar) (2000) Canadian Journal of Fisheries and Aquatic Sciences, 57, pp. 497-506. , https://doi.org/10.1139/f99-226
Barry, J., Newton, M., Dodd, J.A., Lucas, M.C., Boylan, P., Adams, C.E., Freshwater and coastal migration patterns in the silver-stage eel Anguilla anguilla (2016) Journal of Fish Biology, 88, pp. 676-689
Berdahl, A., Westley, P.A.H., Quinn, T.P., Social interactions shape the timing of spawning migrations in an anadromous fish (2017) Animal Behaviour, 126, pp. 221-229
Bickford, S.A., Skalski, J.R., Reanalysis and interpretation of 25 years of Snake–Columbia River juvenile salmonid survival studies (2000) North American Journal of Fisheries Management, 20, pp. 53-68. , https://doi.org/10.1577/1548-8675(2000)020<0053:RAIOYO>2.0.CO
2
Birnie-Gauvin, K., Aarestrup, K., A call for a paradigm shift: Assumed-to-be premature migrants actually yield good returns (2019) Ecology of Freshwater Fish, 28, pp. 62-68. , https://doi.org/10.1111/eff.12431
Bonhomme, R., Bases and limits to using “degree day” units (2000) European Journal of Agronomy, 13, pp. 1-10
Canty, A., Ripley, B., (2017) boot: Bootstrap R (S-Plus) Functions. R package version 1.3-20, , &, R Package Version 1,.3–20
Chezik, K.A., Lester, N.P., Venturelli, P.A., Tierney, K., Fish growth and degree-days II: Selecting a base temperature for an among-population study (2014) Canadian Journal of Fisheries and Aquatic Sciences, 71, pp. 1303-1311. , https://doi.org/10.1139/cjfas-2013-0615
Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora (1992) Official Journal of the European Communities, L206, pp. 7-50
Cunjak, R.A., Comparative feeding, growth and movements of Atlantic salmon (Salmo salar) parr from riverine and estuarine environments (1992) Ecology of Freshwater Fish, 1, pp. 26-34. , https://doi.org/10.1111/j.1600-0633.1992.tb00004.x
Dingle, H., Drake, V.A., What is migration history? (2007) Bioscience, 57, pp. 113-121
Dolotov, S.I., The effects of water temperature on the migration of smolts of the Atlantic salmon Salmo salar L (2006) Journal of Ichthyology, 46, pp. S194-S203. , https://doi.org/10.1134/s0032945206110099
Donohue, K., Burghardt, L.T., Runcie, D., Bradford, K.J., Schmitt, J., Applying developmental threshold models to evolutionary ecology (2015) Trends in Ecology and Evolution, 30, pp. 66-77. , https://doi.org/10.1016/j.tree.2014.11.008
Dormann, C.F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., Lautenbach, S., Collinearity: A review of methods to deal with it and a simulation study evaluating their performance (2013) Ecography, 36, pp. 27-46. , https://doi.org/10.1111/j.1600-0587.2012.07348.x
Ebbesson, L.O.E., Ebbesson, S.O.E., Nilsen, T.O., Stefansson, S.O., Holmqvist, B., Exposure to continuous light disrupts retinal innervation of the preoptic nucleus during parr-smolt transformation in Atlantic salmon (2007) Aquaculture, 273, pp. 345-349. , https://doi.org/10.1016/j.aquaculture.2007.10.016
Fjeldstad, H.P., Alfredsen, K., Boissy, T., Optimising Atlantic salmon smolt survival by use of hydropower simulation modelling in a regulated river (2014) Fisheries Management and Ecology, 21, pp. 22-31. , https://doi.org/10.1111/fme.12044
Fjeldstad, H.P., Uglem, I., Diserud, O.H., Fiske, P., Forseth, T., Kvingedal, E., Järnegren, J., A concept for improving Atlantic salmon Salmo salar smolt migration past hydro power intakes (2012) Journal of Fish Biology, 81, pp. 642-663. , https://doi.org/10.1111/j.1095-8649.2012.03363.x
Gosset, C., Travade, F., Durif, C., Rives, J., Elie, P., Tests of two types of bypass for downstream migration of eels at a small hydroelectric power plant (2005) River Research and Applications, 21, pp. 1095-1105. , https://doi.org/10.1002/rra.871
Gross, M.R., Coleman, R.M., McDowall, R.M., Aquatic productivity and the evolution of diadromous fish migration (1988) Science, 239, pp. 1291-1293. , https://doi.org/10.1126/science.239.4845.1291
Handeland, S.O., Imsland, A.K., Björnsson, B.T., Stefansson, S.O., Long-term effects of photoperiod, temperature and their interaction on growth, gill Na+, K+-ATPase activity, seawater tolerance and plasma growth-hormone levels in Atlantic salmon Salmo salar (2013) Journal of Fish Biology, 83, pp. 1197-1209. , https://doi.org/10.1111/jfb.12215
Haraldstad, T., Kroglund, F., Kristensen, T., Jonsson, B., Haugen, T.O., Diel migration pattern of Atlantic salmon (Salmo salar) and sea trout (Salmo trutta) smolts: An assessment of environmental cues (2017) Ecology of Freshwater Fish, 26, pp. 541-551. , https://doi.org/10.1111/eff.12298
Helm, B., Visser, M.E., Schwartz, W., Kronfeld-Schor, N., Gerkema, M., Piersma, T., Bloch, G., Two sides of a coin: Ecological and chronobiological perspectives of timing in the wild (2017) Philosophical Transactions of the Royal Society B: Biological Sciences, 372. , https://doi.org/10.1098/rstb.2016.0246
Hvidsten, N.A., Heggberget, T.G., Jensen, A.J., Sea water temperatures at Atlantic salmon smolt entrance (1998) Nordic Journal of Freshwater Research, 74, pp. 79-86
Hvidsten, N.A., Jensen, A.J., Vivås, H., Bakke, Ø., Heggberget, T.G., Downstream migration of Atlantic salmon smolts in relation to water flow, water temperature, moon phase and social interaction (1995) Nordic Journal of Freshwater Research, 70, pp. 38-48
Ibbotson, A.T., Riley, W.D., Beaumont, W.R.C., Cook, A.C., Ives, M.J., Pinder, A.C., Scott, L.J., The source of autumn and spring downstream migrating juvenile Atlantic salmon in a small lowland river (2013) Ecology of Freshwater Fish, 22, pp. 73-81. , https://doi.org/10.1111/eff.12003
Jonsson, B., Jonsson, N., A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow (2009) Journal of Fish Biology, 75, pp. 2381-2447. , https://doi.org/10.1111/j.1095-8649.2009.02380.x
Jonsson, B., Jonsson, N., (2011) Ecology of Atlantic salmon and brown trout: Habitat as a template for life histories, , Dordrecht, The Netherlands, Springer
Jonsson, B., Ruud-Hansen, J., Water temperature as the primary influence on timing of seaward migrations of Atlantic salmon (Salmo salar) smolts (1985) Canadian Journal of Fisheries and Aquatic Sciences, 42, pp. 593-595. , https://doi.org/10.1139/f85-076
Jonsson, N., Jonsson, B., Time and size at seaward migration influence the sea survival of Salmo salar (2014) Journal of Fish Biology, 84, pp. 1457-1473. , https://doi.org/10.1111/jfb.12370
Karppinen, P., Jounela, P., Huusko, R., Erkinaro, J., Effects of release timing on migration behaviour and survival of hatchery-reared Atlantic salmon smolts in a regulated river (2014) Ecology of Freshwater Fish, 23, pp. 438-452. , https://doi.org/10.1111/eff.12097
Kuczynski, L., Chevalier, M., Laffaille, P., Legrand, M., Grenouillet, G., Indirect effect of temperature on fish population abundances through phenological changes (2017) PLoS ONE, 12. , https://doi.org/10.1371/journal.pone.0175735
Lagarde, R., Teichert, N., Boussarie, G., Grondin, H., Valade, P., Upstream migration of amphidromous gobies of La Réunion Island: Implication for management (2015) Fisheries Management and Ecology, 22, pp. 437-449. , https://doi.org/10.1111/fme.12142
Larinier, M., Environmental issues, dams and fish migration (2001) FAO Fisheries Technical Paper, 419, pp. 45-89
Larinier, M., Fish passage experience at small-scale hydro-electric power plants in France (2008) Hydrobiologia, 609, pp. 97-108. , https://doi.org/10.1007/s10750-008-9398-9
Larinier, M., Travade, F., Downstream migration: Problems and facilities (2002) Bulletin Français de la Pêche et de la Pisciculture, 364, pp. 181-207. , https://doi.org/10.1051/kmae/2002102
Mack, L., Andersen, H.E., Beklioğlu, M., Bucak, T., Couture, R.-M., Cremona, F., Birk, S., The future depends on what we do today – Projecting Europe's surface water quality into three different future scenarios (2019) Science of the Total Environment, 668, pp. 470-484. , https://doi.org/10.1016/j.scitotenv.2019.02.251
Marschall, E.A., Mather, M.E., Parrish, D.L., Allison, G.W., McMenemy, J.R., Migration delays caused by anthropogenic barriers: Modeling dams, temperature, and success of migrating salmon smolts (2011) Ecological Applications, 21, pp. 3014-3031. , https://doi.org/10.1890/10-0593.1
Martin, P., Rancon, J., Segura, G., Laffont, J., Boeuf, G., Dufour, S., Experimental study of the influence of photoperiod and temperature on the swimming behaviour of hatchery-reared Atlantic salmon (Salmo salar L.) smolts (2012) Aquaculture, 362-363, pp. 200-208. , https://doi.org/10.1016/j.aquaculture.2011.11.047
McCormick, S.D., Hansen, L.P., Quinn, T.P., Saunders, R.L., Movement, migration, and smolting of Atlantic salmon (Salmo salar) (1998) Canadian Journal of Fisheries and Aquatic Sciences, 55, pp. 77-92. , https://doi.org/10.1139/d98-011
McCormick, S.D., Lerner, D.T., Monette, M.Y., Nieves-Puigdoller, K., Kelly, J.T., Björnsson, B.T., Taking it with you when you go: How perturbations to the freshwater environment, including temperature, dams, and contaminants, affect marine survival of salmon (2009) American Fisheries Society Symposium, 69, pp. 195-214
McCormick, S.D., Shrimpton, J.M., Moriyama, S., Björnsson, B.T., Effects of an advanced temperature cycle on smolt development and endocrinology indicate that temperature is not a zeitgeber for smolting in Atlantic salmon (2002) The Journal of Experimental Biology, 205, pp. 3553-3560
McMaster, G.S., White, J.W., Hunt, L.A., Jamieson, P.D., Dhillon, S.S., Ortiz-Monasterio, J.I., Simulating the influence of vernalization, photoperiod and optimum temperature on wheat developmental rates (2008) Annals of Botany, 102, pp. 561-569. , https://doi.org/10.1093/aob/mcn115
McNamara, J.M., Barta, Z., Klaassen, M., Bauer, S., Cues and the optimal timing of activities under environmental changes (2011) Ecology Letters, 14, pp. 1183-1190. , https://doi.org/10.1111/j.1461-0248.2011.01686.x
Miller-Rushing, A.J., Høye, T.T., Inouye, D.W., Post, E., The effects of phenological mismatches on demography (2010) Philosophical Transactions of the Royal Society B: Biological Sciences, 365, pp. 3177-3186. , https://doi.org/10.1098/rstb.2010.0148
Neuheimer, A.B., Mackenzie, B.R., Explaining life history variation in a changing climate across a species' range (2014) Ecology, 95, pp. 3364-3375. , https://doi.org/10.1890/13-2370.1
Neuheimer, A.B., Taggart, C.T., The growing degree-day and fish size-at-age: The overlooked metric (2007) Canadian Journal of Fisheries and Aquatic Sciences, 64, pp. 375-385. , https://doi.org/10.1139/f07-003
Otero, J., L'Abée-Lund, J.H., Castro-Santos, T., Leonardsson, K., Storvik, G.O., Jonsson, B., Vøllestad, L.A., Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar) (2014) Global Change Biology, 20, pp. 61-75. , https://doi.org/10.1111/gcb.12363
Ovidio, M., Dierckx, A., Bunel, S., Grandry, L., Spronck, C., Benitez, J.P., Poor performance of a retrofitted downstream bypass revealed by the analysis of approaching behaviour in combination with a trapping system (2017) River Research and Applications, 33, pp. 27-36. , https://doi.org/10.1002/rra.3062
Ovidio, M., Kestemont, P., Dierckx, A., Benitez, J.-P., Mandiki, R., Neus, Y., Rollin, X., (2019) Rehabilitation effort for anadromous salmonids in the river Meuse basin. Achievements and new challenges, , Advances in the populations ecology of stream salmonids, 20-25 may 2019, Granada University, Spain
Persson, L., Kagervall, A., Leonardsson, K., Royan, M., Alanärä, A., The effect of physiological and environmental conditions on smolt migration in Atlantic salmon Salmo salar (2019) Ecology of Freshwater Fish, 28, pp. 190-199
Philippart, J.C., Micha, J.C., Baras, E., Prignon, C., Gillet, A., Joris, S., The Belgian project “Meuse Salmon 2000”. First results, problems and future prospects (1994) Water Science and Technology, 29, pp. 315-317. , https://doi.org/10.2166/wst.1994.0128
Pinder, A.C., Riley, W.D., Ibbotson, A.T., Beaumont, W.R.C., Evidence for an autumn downstream migration and the subsequent estuarine residence of 0+ year juvenile Atlantic salmon Salmo salar L., in England (2007) Journal of Fish Biology, 71, pp. 260-264. , https://doi.org/10.1111/j.1095-8649.2007.01470.x
(2018) R: A language and environment for statistical computing, , https://www.R-project.org/, R Foundation for statistical computing, Vienna, Austria. URL
Renardy, S., Benitez, J.P., Tauzin, A., Dierckx, A., Matondo, B.N., Ovidio, M., How and where to pass? Atlantic salmon smolt's behaviour at a hydropower station offering multiple migration routes (2020) Hydrobiologia, 847, pp. 469-485. , https://doi.org/10.1007/s10750-019-04108-w
Riley, W.D., Ibbotson, A.T., Beaumont, W.R.C., Adult returns from Atlantic salmon, Salmo salar, parr autumn migrants (2009) Fisheries Management and Ecology, 16, pp. 75-76. , https://doi.org/10.1111/j.1365-2400.2008.00643.x
Sandlund, O.T., Diserud, O.H., Poole, R., Bergesen, K., Dillane, M., Rogan, G., Vøllestad, L.A., Timing and pattern of annual silver eel migration in two European watersheds are determined by similar cues (2017) Ecology and Evolution, 7, pp. 5956-5966. , https://doi.org/10.1002/ece3.3099
Smith, D.R., Fackler, P.L., Eyler, S.M., Villegas Ortiz, L., Welsh, S.A., Optimization of decision rules for hydroelectric operation to reduce both eel mortality and unnecessary turbine shutdown: A search for a win–win solution (2017) River Research and Applications, 33, pp. 1279-1285. , https://doi.org/10.1002/rra.3182
Stefansson, S.O., Bjömsson, B.T., Hansen, T., Haux, C., Taranger, G.L., Saunders, R.L., Growth, parr–smolt transformation, and changes in growth hormone of Atlantic salmon (Salmo salar) reared under different photoperiods (1991) Canadian Journal of Fisheries and Aquatic Sciences, 48, pp. 2100-2108. , https://doi.org/10.1139/f91-249
Stefansson, S.O., Nilsen, T.O., Ebbesson, L.O.E., Wargelius, A., Madsen, S.S., Björnsson, B.T., McCormick, S.D., Molecular mechanisms of continuous light inhibition of Atlantic salmon parr-smolt transformation (2007) Aquaculture, 273, pp. 235-245. , https://doi.org/10.1016/j.aquaculture.2007.10.005
Stich, D.S., Bailey, M.M., Holbrook, C.M., Kinnison, M.T., Zydlewski, J.D., Catchment-wide survival of wild- and hatchery-reared Atlantic salmon smolts in a changing system (2015) Canadian Journal of Fisheries and Aquatic Sciences, 72, pp. 1352-1365. , https://doi.org/10.1139/cjfas-2014-0573
Stich, D.S., Kinnison, M.T., Kocik, J.F., Zydlewski, J.D., Krkošek, M., Initiation of migration and movement rates of Atlantic salmon smolts in fresh water (2015) Canadian Journal of Fisheries and Aquatic Sciences, 72, pp. 1339-1351. , https://doi.org/10.1139/cjfas-2014-0570
Strand, J.E.T., Hazlerigg, D., Jørgensen, E.H., Photoperiod revisited: Is there a critical day length for triggering a complete parr–smolt transformation in Atlantic salmon Salmo salar? (2018) Journal of Fish Biology, 93, pp. 440-448. , https://doi.org/10.1111/jfb.1376010.1111/jfb.13760
Sykes, G.E., Johnson, C.J., Shrimpton, J.M., Temperature and flow effects on migration timing of Chinook salmon smolts (2009) Transactions of the American Fisheries Society, 138, pp. 1252-1265. , https://doi.org/10.1577/t08-180.1
Taal, I., Kesler, M., Saks, L., Rohtla, M., Verliin, A., Svirgsden, R., Saat, S., Evidence for an autumn downstream migration of Atlantic salmon Salmo salar (Linnaeus) and brown trout Salmo trutta (Linnaeus) parr to the Baltic Sea (2014) Helgoland Marine Research, 68, pp. 373-377. , https://doi.org/10.1007/s10152-014-0395-2
Teichert, N., Trancart, T., Feunteun, E., Acou, A., Oliveira, E.D., Resolving the trade-off between silver eel escapement and hydropower generation with simple decision rules for turbine shutdown (2020) Journal of Environmental Management, 261. , https://doi.org/10.1016/j.jenvman.2020.110212
Tétard, S., Maire, A., Lemaire, M., De Oliveira, E., Martin, P., Courret, D., Behaviour of Atlantic salmon smolts approaching a bypass under light and dark conditions: Importance of fish development (2019) Ecological Engineering, 131, pp. 39-52. , https://doi.org/10.1016/j.ecoleng.2019.02.021
Thorstad, E.B., Havn, T.B., Sæther, S.A., Heermann, L., Teichert, M.A.K., Diserud, O.H., Økland, F., Survival and behaviour of Atlantic salmon smolts passing a run-of-river hydropower facility with a movable bulb turbine (2017) Fisheries Management and Ecology, 24, pp. 199-207. , https://doi.org/10.1111/fme.12216
Thorstad, E.B., Økland, F., Aarestrup, K., Heggberget, T.G., Factors affecting the within-river spawning migration of Atlantic salmon, with emphasis on human impacts (2008) Reviews in Fish Biology and Fisheries, 18, pp. 345-371. , https://doi.org/10.1007/s11160-007-9076-4
Thorstad, E.B., Whoriskey, F., Uglem, I., Moore, A., Rikardsen, A.H., Finstad, B., A critical life stage of the Atlantic salmon Salmo salar: Behaviour and survival during the smolt and initial post-smolt migration (2012) Journal of Fish Biology, 81, pp. 500-542. , https://doi.org/10.1111/j.1095-8649.2012.03370.x
Tomanova, S., Courret, D., Alric, A., De Oliveira, E., Tétard, S., Lagarrigue, T., Protecting efficiently sea-migrating salmon smolts from entering hydropower plant turbines with inclined or oriented low bar spacing racks (2018) Ecological Engineering, 122, pp. 143-152. , https://doi.org/10.1016/j.ecoleng.2018.07.034
Trancart, T., Acou, A., De Oliveira, E., Feunteun, E., Forecasting animal migration using SARIMAX: An efficient means of reducing silver eel mortality caused by turbines (2013) Endangered Species Research, 21, pp. 181-190. , https://doi.org/10.3354/esr00517
Whalen, K.G., Parrish, D.L., McCormick, S.D., Migration timing of Atlantic salmon smolts relative to environmental and physiological factors (1999) Transactions of the American Fisheries Society, 128, pp. 289-301. , https://doi.org/10.1577/1548-8659(1999)128<0289:mtoass>2.0.co
2
Zeiringer, B., Seliger, C., Greimel, F., Schmutz, S., River hydrology, flow alteration, and environmental flow (2018) Riverine ecosystem management, pp. 67-89. , S. Schmutz, &, J. Sendzimir, (Eds.),, Amsterdam, The Netherlands, Springer International Publishing
Zydlewski, G.B., Haro, A., McCormick, S.D., Evidence for cumulative temperature as an initiating and terminating factor in downstream migratory behavior of Atlantic salmon (Salmo salar) smolts (2005) Canadian Journal of Fisheries and Aquatic Sciences, 62, pp. 68-78. , https://doi.org/10.1139/f04-179
Zydlewski, G.B., Stich, D.S., McCormick, S.D., Photoperiod control of downstream movements of Atlantic salmon Salmo salar smolts (2014) Journal of Fish Biology, 85, pp. 1023-1041. , https://doi.org/10.1111/jfb.12509