Abstract
The potential effects of global warming on the allis shad population were tested by combining a time series of spawning acts with expected thermal survival rates for embryos and larvae until 14 days post hatching. The yearly mean survival of spawn for each reproductive season was calculated and an index of reproductive efficiency based on this survival rate was proposed. The randomness of the spawning tactics was evaluated by shuffling the spawn acts time series. This approach was applied to the Gironde-Garonne-Dordogne (south-west France) population, which recently collapsed. The yearly mean thermal survival of spawn is slightly variable at approximately 55% over 2003–2012 despite fluctuating temperatures. An especially low survival (35%) was recorded for the last season (2013). For eight of the 11 reproductive seasons, the index of reproductive efficiency was high (> 80%) and largely above indices obtained by a random spawning tactic. Therefore shad are able to adopt an efficient spawning tactic to anticipate favourable thermal conditions for survival of their offspring. However, thermal behavioural rules still need to be expanded to understand the failures in their reproduction efficiency.





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Acolas ML, Begout Anras ML, Veron V et al (2004) An assessment of the upstream migration and reproductive behaviour of allis shad (Alosa alosa L.) using acoustic tracking. ICES J Mar Sci 61(8):1291–1304. https://doi.org/10.1016/j.icesjms.2004.07.023
Acolas ML, Veron V, Jourdan H et al (2006) Upstream migration and reproductive patterns of a population of Allis shad in a small river (L’Aulne, Brittany, France). ICES J Mar Sci 63(3):476–484. https://doi.org/10.1016/j.icesjms.2005.05.022
Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27(4):249–268. https://doi.org/10.1016/S0306-4565(01)00094-8
Aprahamian MW, Aprahamian CD (2001) The influence of water temperature and flow on year class strength of twaite shad (Alosa fallax fallax) from the river Severn, England. Bull Fr Pêche Piscic 362(363):953–972
Baglinière JL, Sabatié MR, Alexandrino P et al (2000) Les aloses: une richesse patrimoniale à conserver et à valoriser. In: Baglinière JL, Elie P (eds) Les aloses (Alosa alosa et Alosa fallax spp. ). Cemagref Editions - INRA Editions, pp 263–275
Béguer M, Beaulaton L, Rochard E (2007) Distribution and richness of diadromous fish assemblages in western Europe: large scale explanatory factors. Ecol Freshw Fish 16(2):221–237. https://doi.org/10.1111/j.1600-0633.2006.00214.x
Beitinger TL, Bennett WA, McCauley RW (2000) Temperature tolerances of north American freshwater fishes exposed to dynamic changes in temperature. Environ Biol Fish 58(3):237–275. https://doi.org/10.1023/A:1007676325825
Belliard J, Marchal J, Ditche JM, Tales E, Sabatié R, Baglinière JL (2009) Return of adult anadromous allis shad (Alosa alosa L.) in the river seine, France: a sign of river recovery? River Res Appl 25(6):788–794. https://doi.org/10.1002/rra.1221
Boisneau P, Mennesson-Boisneau C, Bagliniere JL (1990) Description d’une frayère et comportement de reproduction de la grande alose (Alosa alosa L.) dans le cours supérieur de la Loire. Bull Fr Pêche Piscic 316:15–23
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85(7):1771–1789. https://doi.org/10.1890/03-9000
Cassou-Leins F, Cassou-Leins JJ (1981) Recherches sur la biologie et l’halieutique des migrateurs de la Garonne et principalement de l’alose, Alosa alosa L. Thèse de doctorat, Sciences agronomiques, E.N.S.A. Toulouse
Cassou-Leins JJ, Cassou-leins F, Boisneau P, Bagliniere J-L (2000) La reproduction. In: Bagliniere JL, Elie P (eds) Les Aloses (Alosa alosa et Alosa fallax spp.): Ecobiologie et variabilité des Populations, Inra-Cemagref. pp 73–92
Chambers RC, Leggett WC (1996) Maternal influences on variation in egg sizes in temperate marine fishes. Am Zool 36(2):180–196. https://doi.org/10.1093/icb/36.2.180
Chanseau M, Castelnaud G, Carry L et al (2004) Essai d’évaluation du stock de géniteurs d’alose Alosa alosa du bassin versant Gironde-Garonne-Dordogne sur la période 1987-2001 et comparaison de différents indicateurs d’abondance. Bull Fr Pêche Piscic 374:1–19. https://doi.org/10.1051/kmae/2004023
Clayton DA (1978) Socially facilitated behavior. Q Rev Biol 53(4):373–392. https://doi.org/10.1086/410789
Collin S, Rochard E (2012) Projet de tableau de bord de la grande alose du bassin versant Gironde-Garonne-Dordogne, méthodes, résultats et perspectives de la démarche. Rapport Irstea, centre de Bordeaux
Crecco VA, Savoy TF (1985) Effects of biotic and abiotic factors on growth and relative survival of young American shad, Alosa sapidissima in the Connecticut river. Can J Fish Aquat Sci 42(10):1640–1648. https://doi.org/10.1139/f85-205
Crecco V, Savoy T (1987) Review of recruitment mechanisms of the American shad: the critical period and match-mismatch hypotheses reexamined. Am Fish Soc Symp 1:455–468
Crecco V, Savoy T, Gunn L (1983) Daily mortality rates of larval and juvenile American shad (Alosa sapidissima) in the Connecticut River with changes in year-class strength. Can J Fish Aquat Sci 40(10):1719–1728. https://doi.org/10.1139/f83-199
Crozier LG, Hutchings JA (2014) Plastic and evolutionary responses to climate change in fish. Evol Appl 7(1):68–87. https://doi.org/10.1111/eva.12135
Crozier LG, Hendry AP, Lawson PW, Quinn TP, Mantua NJ, Battin J, Shaw RG, Huey RB (2008) Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon. Evol Appl 1(2):252–270. https://doi.org/10.1111/j.1752-4571.2008.00033.x
Durham BW, Wilde GR (2006) Influence of stream discharge on reproductive success of a prairie stream fish assemblage. Trans Am Fish Soc 135(6):1644–1653. https://doi.org/10.1577/T05-133.1
Gaillagot A, Carry L (2014) Suivi de la reproduction de la grande alose sur la Garonne en 2014. Rapport MIGADO, Le Passage http://oai.eau-adour-garonne.fr/oai-documents/60949/GED_00000000.pdf
Golovanov VK (2013) Ecophysiological patterns of distribution and behavior of freshwater fish in thermal gradients. J Ichthyol 53(4):252–280. https://doi.org/10.1134/S0032945213030016
Houde ED (1989) Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87:471–495
Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15(2):56–61. https://doi.org/10.1016/S0169-5347(99)01764-4
Hundt M, Scharbert A, Weibel U, Kuhn G, Metzner K, Jatteau P, Pies A, Schulz R, Gergs R (2015a) First evidence of natural reproduction of the Allis shad Alosa alosa in the river Rhine following re-introduction measures. J Fish Biol 87(2):487–493. https://doi.org/10.1111/jfb.12721
Hundt M, Schiffer M, Weiss M, Schreiber B, Kreiss CM, Schulz R, Gergs R (2015b) Effect of temperature on growth, survival and respiratory rate of larval allis shad Alosa alosa. Knowl Manag Aquat Ecosyst 416(416):27. https://doi.org/10.1051/kmae/2015023
Hyle AR, McBride RS, Olney JE (2014) Determinate versus indeterminate fecundity in American shad, an anadromous clupeid. Trans Am Fish Soc 143(3):618–633. https://doi.org/10.1080/00028487.2013.862178
ICES (2014) Report of the workshop on lampreys and shads 27-29 November 2014 Lisbon Portugal
Jatteau P, Fraty R (2012) Etude de la tolérance à l’hypoxie des juvéniles de grande alose (Alosa alosa). Irstea
Jatteau P, Drouineau H, Charles K, Carry L, Lange F, Lambert P (2017) Thermal tolerance of allis shad (Alosa alosa) embryos and larvae: modelling and potentials applications. Aquat Living Resour 30:2. https://doi.org/10.1051/alr/2016033
Jonsson B, Jonsson N (2009) 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. J Fish Biol 75(10):2381–2447. https://doi.org/10.1111/j.1095-8649.2009.02380.x
Kennedy RJ, Crozier WW (2010) Evidence of changing migratory patterns of wild Atlantic salmon Salmo salar smolts in the river bush, Northern Ireland, and possible associations with climate change. J Fish Biol 76(7):1786–1805. https://doi.org/10.1111/j.1095-8649.2010.02617.x
Lambert TC (1990) The effect of population structure on recruitment in herring. J Cons ICES J Mar Sci 47(2):249–255. https://doi.org/10.1093/icesjms/47.2.249
Lanoux A, Etcheber H, Schmidt S, Sottolichio A, Chabaud G, Richard M, Abril G (2013) Factors contributing to hypoxia in a highly turbid, macrotidal estuary (the Gironde, France). Environ Sci Process Impacts 15(3):585–595. https://doi.org/10.1039/C2EM30874F
Lassalle G, Rochard E (2009) Impact of twenty-first century climate change on diadromous fish spread over Europe, North Africa and the Middle East. Glob Change Biol 15(5):1072–1089. https://doi.org/10.1111/j.1365-2486.2008.01794.x
Lassalle G, Béguer M, Beaulaton L, Rochard E (2008) Diadromous fish conservation plans need to consider global warming issues: an approach using biogeographical models. Biol Conserv 141(4):1105–1118. https://doi.org/10.1016/j.biocon.2008.02.010
Lassalle G, Crouzet P, Rochard E (2009) Modelling the current distribution of European diadromous fishes: an approach integrating regional anthropogenic pressures. Freshw Biol 54(3):587–606. https://doi.org/10.1111/j.1365-2427.2008.02135.x
Leggett WC, Whitney RR (1972) Water temperature and the migrations of American shad. Fish Bull 70:659–670
Lorda E, Crecco VA (1987) Stock-recruitment relationship and compensatory mortality of American shad in the Connecticut river. Am Fish Soc Symp 1:469–482
Martin Vandembulcke D (1999) Dynamique de population de la grande alose (Alosa alosa, L. 1758) dans le bassin versant Gironde-Garonne-Dordogne (France): analyse et prévision par modélisation. Thèse de doctorat, Ecole Nationale Polytechnique
Martin J, Rougemont Q, Drouineau H, Launey S, Jatteau P, Bareille G, Berail S, Pécheyran C, Feunteun E, Roques S, Clavé D, Nachón DJ, Antunes C, Mota M, Réveillac E, Daverat F (2015) Dispersal capacities of anadromous Allis shad population inferred from a coupled genetic and otolith approach. Can J Fish Aquat Sci 72(7):991–1003. https://doi.org/10.1139/cjfas-2014-0510
Mennesson-Boisneau C, Aprahamian MW, Sabatié MR, Cassou-Leins JJ (2000) Biologie des aloses : remontée migratoire des adultes. In: Baglinière JL, Elie P (eds) Les aloses (Alosa alosa et Alosa fallax spp.): écobiologie et variabilité des populations. Cemagref, Inra Éditions, Paris, pp 55–72
Mion JB, Stein RA, Marschall EA (1998) River discharge drives survival of larval walleye. Ecol Appl 8(1):88–103. https://doi.org/10.1890/1051-0761(1998)008[0088:RDDSOL]2.0.CO;2
Moss SA (1970) The responses of young American shad to rapid temperature changes. Trans Am Fish Soc 99(2):381–384. https://doi.org/10.1577/1548-8659(1970)99<381:troyas>2.0.co;2
Murua H, Kraus G, Saborido-Rey F, Wittames PR, Thorsen A, Junquera S (2003) Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. J Northwest Atl Fish Sci 33:33–54. https://doi.org/10.2960/J.v33.a3
Nack CC, Limburg KE, Miller D (2015) Assessing the quality of four inshore habitats used by post yolk-sac Alosa sapidissima (Wilson 1811) in the Hudson River: a prelude to restoration. Restor Ecol 23(1):57–64. https://doi.org/10.1111/rec.12122
Ochi H (1986) Breeding synchrony and spawning intervals in the temperate damselfish Chromis notata. Environ Biol Fish 17(2):117–423. https://doi.org/10.1007/BF00001741
Olney JE, McBride RS (2003) Intraspecific variation in batch fecundity of American shad: revisiting the paradigm of reciprocal latitudinal trends in reproductive traits. In: Limburg K, Waldman JR (eds) Biodiversity, status, and conservation of the world’s shads. Am. Fish. Soc. Symp., pp 185–192
Pigliucci M (1996) How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends Ecol Evol 11(4):168–173. https://doi.org/10.1016/0169-5347(96)10008-2
Quinn TP, Adams DJ (1996) Environmental changes affecting the migratory timing of American shad and sockeye salmon. Ecology 77(4):1151–1162. https://doi.org/10.2307/2265584
Reichard M, Jurajda P (2004) The effects of Elevated River discharge on the downstream drift of young-of-the-year cyprinid fishes. J Freshw Ecol 19(3):465–471. https://doi.org/10.1080/02705060.2004.9664921
Reynolds WW (1978) The final thermal preferendum of fishes: shuttling behavior and acclimation overshoot. Hydrobiologia 57(2):123–124. https://doi.org/10.1007/BF00016455
Rochard E (2001) Migration anadrome estuarienne des géniteurs de grande alose Alosa alosa, allure du phénomène et influence du rythme des marées. BFPP - Bull Francais Peche Prot Milieux Aquat 362–363:853–867
Ross R, Bennett R, Backman T (1993) Habitat use by spawning adult, egg, and larval American shad in the Delaware River. Rivers 4:227–238
Rougier T, Lambert P, Drouineau H, Girardin M, Castelnaud G, Carry L, Aprahamian M, Rivot E, Rochard E (2012) Collapse of allis shad, Alosa alosa, in the Gironde system (southwest France): environmental change, fishing mortality, or Allee effect? ICES J Mar Sci J Cons 69(10):1802–1811. https://doi.org/10.1093/icesjms/fss149
Rougier T, Lassalle G, Drouineau H, Dumoulin N, Faure T, Deffuant G, Rochard E, Lambert P (2015) The combined use of empirical and mechanistic species distribution models benefits low conservation status species. PLoS One 10(10):e0139194. https://doi.org/10.1371/journal.pone.0139194
Roule L (1922) La migration reproductrice et la protandrie de l’alose feinte (Alosa finta L.) Ann Sci Nat Zool 5:61–76
Roule L (1923) Notes sur les aloses de la Loire et de l’Aquitaine. Bull Société Cent Aquic Fr 30:14–22
Savoy TF, Crecco VA (1988) The timing and significance of density-dependent and density-independent mortality of American shad, Alosa sapidissima. Fish Bull 86:467–481
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3(3):259–268. https://doi.org/10.2307/2389364
Stoll S, Probst WN, Eckmann R, Fischer P (2010) A mesocosm experiment investigating the effects of substratum quality and wave exposure on the survival of fish eggs. Aquat Sci 72(4):509–517. https://doi.org/10.1007/s00027-010-0152-9
Taverny C, Belaud A, Elie P, Sabatie MR (2000) Influence des activités humaines. In: Bagliniere JL, Elie P (eds) Les aloses (Alosa alosa et Alosa fallax spp.): écobiologie et variabilité des populations. INRA - Cemagref, Paris Antony, pp 227–248
Travade F, Carry L (2008) Effet de la canicule de 2003 sur les poissons migrateurs en Garonne et Dordogne - Réflexions sur l’effet des rejets thermiques de la centrale nucléaire de Golfech sur la Garonne. Hydroécologie Appliquée 16:169–189. https://doi.org/10.1051/hydro/2009008
Ulanowicz RE (1975) The mechanical effects of water flow on fish eggs and larvae. In: Saila SB (ed) Fisheries and energy production: a symposium. Lexington Books, Lexington, pp 77–87
Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B Biol Sci 275(1635):649–659. https://doi.org/10.1098/rspb.2007.0997
Walton SE, Nunn AD, Probst WN, et al (2017) Do fish go with the flow? The effects of periodic and episodic flow pulses on 0+ fish biomass in a constrained lowland river. Ecohydrology 10:n/a-n/a. doi:https://doi.org/10.1002/eco.1777
Wehrly KE, Brenden TO, Wang L (2009) A comparison of statistical approaches for predicting stream temperatures across heterogeneous landscapes. J Am Water Resour Assoc 45(4):986–997. https://doi.org/10.1111/j.1752-1688.2009.00341.x
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20(1):249–278. https://doi.org/10.1146/annurev.es.20.110189.001341
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This work was conducted with the financial support of the Conseil Régional de Nouvelle Aquitaine (FAUNA project) and Agence de l’Eau Adour-Garonne (SHAD’EAU project).
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Lambert, P., Jatteau, P., Paumier, A. et al. Allis shad adopts an efficient spawning tactic to optimise offspring survival. Environ Biol Fish 101, 315–326 (2018). https://doi.org/10.1007/s10641-017-0700-4
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DOI: https://doi.org/10.1007/s10641-017-0700-4


