The dynamics of spawning acts by a semelparous fish and its associated energetic costs

10.24072/pcjournal.56 - Peer Community Journal, Volume 1 (2021), article no. e49.

Get full text PDF Peer reviewed and recommended by PCI

During the reproductive season, animals have to manage both their energetic budget and gamete stock. In particular, for semelparous capital breeders with determinate fecundity and no parental care other than gametic investment, the depletion of energetic stock must match the depletion of gametic stock, so that individuals get exhausted just after their last egg is laid and fertilized. Although these budgets are managed continuously, monitoring the dynamics of mating acts and energy expenditure at a fine temporal scale in the wild is challenging. This study aimed to quantify the individual dynamics of spawning acts and the concomitant energy expenditure of female Allis shad (Alosa alosa) throughout their mating season. Using eight individual-borne accelerometers for one month, we collected tri-axial acceleration, temperature, and pressure data that we analysed to i) detect the timing of spawning acts, ii) estimate energy expenditure from tail beat frequency and water temperature, and iii) monitor changes in body roundness from the position of the dorsally-mounted tag relative to the vertical plane. Female shad had a higher probability to spawn during warmer nights, and their spawning acts were synchronized (both individually and inter-individually) within each active night. They experienced warmer temperature, remained deeper, swan more slowly and spent less energy during daytime than night time. Over one month of spawning, they performed on average 15.75 spawning acts, spent on average 6 277 kJ and died with a significant portion of residual oocytes. The acceleration-based indicator of body roundness was correlated to condition coefficient measured at capture, and globally decreased through the spawning season, although the indicator was noisy and was not correlated to changes in estimated energy expenditure. Despite significant individual variability, our results indicate that female shad exhausted their energetic stock faster than their egg stock. Water warming will increase the rate of energy expenditure, which might increase the risk that shad die with a large stock of unspent eggs. Although perfectible, the three complementary analyses of acceleration data are promising for in situ monitoring of energy expenditure related to specific behaviour.

Published online:
DOI: 10.24072/pcjournal.56
Tentelier, Cédric 1, 2; Bouchard, Colin 1, 2, 3; Bernardin, Anaïs 2; Tauzin, Amandine 2; Aymes, Jean-Christophe 1, 2; Lange, Frédéric 1, 2; Recapet, Charlotte 1, 2; Rives, Jacques 1, 2

1 Pôle Gestion des Migrateurs Amphihalins dans leur Environnement, OFB, INRAE, AGROCAMPUS OUEST, UNIV PAU & PAYS ADOUR/E2S UPPA
2 Universite de Pau et des Pays de l’Adour, E2S UPPA, INRAE, ECOBIOP, Saint-Pée-surNivelle, France
3 Tour du Valat, Research Institute for the Conservation of Mediterranean Wetlands, Arles, France
     author = {Tentelier, C\'edric and Bouchard, Colin and Bernardin, Ana{\"\i}s and Tauzin, Amandine and Aymes, Jean-Christophe and Lange, Fr\'ed\'eric and Recapet, Charlotte and Rives, Jacques},
     title = {The dynamics of spawning acts by a semelparous fish and its associated energetic costs},
     journal = {Peer Community Journal},
     eid = {e49},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.56},
     url = {}
TI  - The dynamics of spawning acts by a semelparous fish and its associated energetic costs
JO  - Peer Community Journal
PY  - 2021
DA  - 2021///
VL  - 1
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.56
ID  - 10_24072_pcjournal_56
ER  - 
%0 Journal Article
%T The dynamics of spawning acts by a semelparous fish and its associated energetic costs
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.56
%F 10_24072_pcjournal_56
Tentelier, Cédric; Bouchard, Colin; Bernardin, Anaïs; Tauzin, Amandine; Aymes, Jean-Christophe; Lange, Frédéric; Recapet, Charlotte; Rives, Jacques. The dynamics of spawning acts by a semelparous fish and its associated energetic costs. Peer Community Journal, Volume 1 (2021), article  no. e49. doi : 10.24072/pcjournal.56.

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100060

[1] Acolas, M.; Bégout Anras, M.; Véron, V.; Jourdan, H.; Sabatié, M.; Baglinière, J. An assessment of the upstream migration and reproductive behaviour of allis shad (Alosa alosa L.) using acoustic tracking, ICES Journal of Marine Science, Volume 61 (2004) no. 8, pp. 1291-1304 | Article

[2] Acolas, M.; Véron, V.; Jourdan, H.; Bégout, M.; Sabatié, M.; Baglinière, J. Upstream migration and reproductive patterns of a population of allis shad in a small river (L'Aulne, Brittany, France), ICES Journal of Marine Science, Volume 63 (2006) no. 3, pp. 476-484 | Article

[3] Alexander, R. M. Physical aspects of swimbladder function, Biological Reviews, Volume 41 (1966) no. 1, pp. 141-176 | Article

[4] Anderson, S. S.; Fedak, M. A. Grey seal males: energetic and behavioural links between size and sexual success, Animal Behaviour, Volume 33 (1985) no. 3, pp. 829-838 | Article

[5] Baglinière J-L, ; Elie P, Les Aloses (Alosa alosa et Alosa fallax spp.): écobiologie et variabilité des populations, Editions Quae, (2000)

[6] Barton, K. Mu-MIn: Multi-model inference. R Package Version 0.12.2/r18., (2009)

[7] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Usinglme4, Journal of Statistical Software, Volume 67 (2015) no. 1, pp. 1-48 | Article

[8] Beamish, F. W. H.; Potter, I. C.; Thomas, E. Proximate Composition of the Adult Anadromous Sea Lamprey, Petromyzon Marinus, in Relation to Feeding, Migration and Reproduction, The Journal of Animal Ecology, Volume 48 (1979) no. 1, pp. 1-19 | Article

[9] Bengen GSH, Suivi de la maturation gonadique des aloses, Alosa alosa L. lors de leur migration en Garonne. PhD thesis, Toulouse, France: Institut national polytechnique ((1992))

[10] Bonnet, X.; Bradshaw, D.; Shine, R. Capital versus Income Breeding: An Ectothermic Perspective, Oikos, Volume 83 (1998) no. 2, pp. 333-342 | Article

[11] Borgia, G. Bower quality, number of decorations and mating success of male satin bowerbirds (Ptilonorhynchus violaceus): an experimental analysis, Animal Behaviour, Volume 33 (1985) no. 1, pp. 266-271 | Article

[12] Breine, J.; Pauwels, I. S.; Verhelst, P.; Vandamme, L.; Baeyens, R.; Reubens, J.; Coeck, J. Successful external acoustic tagging of twaite shad Alosa fallax (Lacépède 1803), Fisheries Research, Volume 191 (2017), pp. 36-40 | Article

[13] Brett, J.; Groves, T. Physiological Energetics, Fish Physiology, Elsevier, 1979, pp. 279-352 | Article

[14] Broell, F.; Taggart, C. T. Scaling in Free-Swimming Fish and Implications for Measuring Size-at-Time in the Wild, PLOS ONE, Volume 10 (2015) no. 12 | Article

[15] Brooks, M.; Kristensen, K.; Benthem, K.; Magnusson, A.; Berg, C.; Nielsen, A.; Skaug, H.; Mächler, M.; Bolker, B. glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling, The R Journal, Volume 9 no. 2 | Article

[16] Brown, D. D.; Kays, R.; Wikelski, M.; Wilson, R.; Klimley, A. Observing the unwatchable through acceleration logging of animal behavior, Animal Biotelemetry, Volume 1 (2013) no. 1 | Article

[17] Brownscombe, J. W.; Lennox, R. J.; Danylchuk, A. J.; Cooke, S. J. Estimating fish swimming metrics and metabolic rates with accelerometers: the influence of sampling frequency, Journal of Fish Biology, Volume 93 (2018) no. 2, pp. 207-214 | Article

[18] Casas, J.; Pincebourde, S.; Mandon, N.; Vannier, F.; Poujol, R.; Giron, D. Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid, Ecology, Volume 86 (2005) no. 3, pp. 545-554 | Article

[19] Cassou-Leins F, ; Cassou-Leins J-J, Recherches sur la biologie et l’halieutique des migrateurs de la Garonne et principalement l’alose: Alosa alosa . PhD thesis. Institut National Polytechnique de Toulouse ((1981))

[20] Castro-Santos, T.; Letcher, B. H. Modeling migratory energetics of Connecticut River American shad (Alosa sapidissima): implications for the conservation of an iteroparous anadromous fish, Canadian Journal of Fisheries and Aquatic Sciences, Volume 67 (2010) no. 5, pp. 806-830 | Article

[21] Chanseau, M.; Castelnaud, G.; Carry, L.; Martin-Vandembulcke, D.; Belaud, A. Essai d’evaluation du stock de géniteurs d’alose alosaalosa du bassin versant gironde-garonne-dordogne sur la periode 1987-2001 et comparaison de différents indicateurs d’abondance, Bulletin Français de la Pêche et de la Pisciculture (2004) no. 374, pp. 1-19 | Article

[22] Collins, P. M.; Halsey, L. G.; Arnould, J. P. Y.; Shaw, P. J. A.; Dodd, S.; Green, J. A. Energetic consequences of time‐activity budgets for a breeding seabird, Journal of Zoology, Volume 300 (2016) no. 3, pp. 153-162 | Article

[23] Craig, J. F.; Kenley, M. J.; Talling, J. F. Comparative estimations of the energy content of fish tissue from bomb calorimetry, wet oxidation and proximate analysis, Freshwater Biology, Volume 8 (1978) no. 6, pp. 585-590 | Article

[24] Csilléry, K.; Blum, M. G.; Gaggiotti, O. E.; François, O. Approximate Bayesian Computation (ABC) in practice, Trends in Ecology & Evolution, Volume 25 (2010) no. 7, pp. 410-418 | Article

[25] De Cuyper, A.; Clauss, M.; Carbone, C.; Codron, D.; Cools, A.; Hesta, M.; Janssens, G. P. J. Predator size and prey size-gut capacity ratios determine kill frequency and carcass production in terrestrial carnivorous mammals, Oikos, Volume 128 (2019) no. 1, pp. 13-22 | Article

[26] Duncan, A. E.; Torgerson-White, L. L.; Allard, S. M.; Schneider, T. An evaluation of infrared thermography for detection of bumblefoot (pododermatitis) in penguins, Journal of Zoo and Wildlife Medicine, Volume 47 (2016) no. 2, pp. 474-485 | Article

[27] Emlen, S. T.; Oring, L. W. Ecology, Sexual Selection, and the Evolution of Mating Systems, Science, Volume 197 (1977) no. 4300, pp. 215-223 | Article

[28] Fatin, D.; Dartiguelongue, J. Etude préliminaire de la reproduction des aloses en 1995 entre Tuilières et Mauzac sur la Dordogne (Rapport S.C.E.A.) (39pp), (1996)

[29] Føre, M.; Svendsen, E.; Økland, F.; Gräns, A.; Alfredsen, J. A.; Finstad, B.; Hedger, R. D.; Uglem, I. Heart rate and swimming activity as indicators of post-surgical recovery time of Atlantic salmon (Salmo salar), Animal Biotelemetry, Volume 9 (2021) no. 1 | Article

[30] Fürtbauer, I.; Mundry, R.; Heistermann, M.; Schülke, O.; Ostner, J. You Mate, I Mate: Macaque Females Synchronize Sex not Cycles, PLoS ONE, Volume 6 (2011) no. 10 | Article

[31] Gauthey, Z.; Freychet, M.; Manicki, A.; Herman, A.; Lepais, O.; Panserat, S.; Elosegi, A.; Tentelier, C.; Labonne, J. The concentration of plasma metabolites varies throughout reproduction and affects offspring number in wild brown trout (Salmo trutta), Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Volume 184 (2015), pp. 90-96 | Article

[32] Gleiss, A. C.; Wilson, R. P.; Shepard, E. L. C. Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure, Methods in Ecology and Evolution, Volume 2 (2011) no. 1, pp. 23-33 | Article

[33] Gochfeld, M. Mechanisms and Adaptive Value of Reproductive Synchrony in Colonial Seabirds, Behavior of Marine Animals, Springer US, Boston, MA, 1980, pp. 207-270 | Article

[34] Groscolas, R.; Viera, V.; Guerin, N.; Handrich, Y.; Côté, S. D. Heart rate as a predictor of energy expenditure in undisturbed fasting and incubating penguins, Journal of Experimental Biology, Volume 213 (2010) no. 1, pp. 153-160 | Article

[35] Heimpel, G. E.; Rosenheim, J. A. Egg Limitation in Parasitoids: A Review of the Evidence and a Case Study, Biological Control, Volume 11 (1998) no. 2, pp. 160-168 | Article

[36] Hendry, A. P.; Beall, E. Energy use in spawning Atlantic salmon, Ecology of Freshwater Fish, Volume 13 (2004) no. 3, pp. 185-196 | Article

[37] Hendry, A. P.; Berg, O. K. Secondary sexual characters, energy use, senescence, and the cost of reproduction in sockeye salmon, Canadian Journal of Zoology, Volume 77 (1999) no. 11, pp. 1663-1675 | Article

[38] Hicks, O.; Burthe, S.; Daunt, F.; Butler, A.; Bishop, C.; Green, J. A. Validating accelerometry estimates of energy expenditure across behaviours using heart rate data in a free-living seabird, Journal of Experimental Biology, Volume 220 (2017) no. 10, pp. 1875-1881 | Article

[39] Hruska, K. A.; Hinch, S. G.; Patterson, D. A.; Healey, M. C. Egg retention in relation to arrival timing and reproductive longevity in female sockeye salmon (Oncorhynchus nerka), Canadian Journal of Fisheries and Aquatic Sciences, Volume 68 (2011) no. 2, pp. 250-259 | Article

[40] Hughes, P. W. Between semelparity and iteroparity: Empirical evidence for a continuum of modes of parity, Ecology and Evolution, Volume 7 (2017) no. 20, pp. 8232-8261 | Article

[41] Idler, D. R.; Bitners, I. Biochemical studies on sockeye salmon during spawning migration: ii. cholesterol, fat, protein, and water in the flesh of standard fish, Canadian Journal of Biochemistry and Physiology, Volume 36 (1958) no. 8, pp. 793-798 | Article

[42] Ims, R. A. The ecology and evolution of reproductive synchrony, Trends in Ecology & Evolution, Volume 5 (1990) no. 5, pp. 135-140 | Article

[43] Jepsen, N.; Thorstad, E. B.; Havn, T.; Lucas, M. C. The use of external electronic tags on fish: an evaluation of tag retention and tagging effects, Animal Biotelemetry, Volume 3 (2015) no. 1 | Article

[44] Jonsson, N.; Jonsson, B.; Hansen, L. P. Changes in Proximate Composition and Estimates of Energetic Costs During Upstream Migration and Spawning in Atlantic Salmon Salmo salar, The Journal of Animal Ecology, Volume 66 (1997) no. 3, pp. 425-436 | Article

[45] Jovani, R.; Grimm, V. Breeding synchrony in colonial birds: from local stress to global harmony, Proceedings of the Royal Society B: Biological Sciences, Volume 275 (2008) no. 1642, pp. 1557-1564 | Article

[46] Kawabe, R.; Kawano, T.; Nakano, N.; Yamashita, N.; Hiraishi, T.; Naito, Y. Simultaneous measurement of swimming speed and tail beat activity of free-swimming rainbow trout Oncorhynchus mykiss using an acceleration data-logger, Fisheries Science, Volume 69 (2003) no. 5, pp. 959-965 | Article

[47] Kieffer, J. D. Limits to exhaustive exercise in fish, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Volume 126 (2000) no. 2, pp. 161-179 | Article

[48] Kirkendall, L. R. On Defining "Breeding Once", The American Naturalist, Volume 125 (1985) no. 2, pp. 189-204 | Article

[49] Koizumi, I.; Shimatani, I. K. Socially induced reproductive synchrony in a salmonid: an approximate Bayesian computation approach, Behavioral Ecology, Volume 27 (2016) no. 5, pp. 1386-1396 | Article

[50] Langkau, M. C.; Clavé, D.; Schmidt, M. B.; Borcherding, J. Spawning behaviour of Allis shad Alosa alosa : new insights based on imaging sonar data, Journal of Fish Biology, Volume 88 (2016) no. 6, pp. 2263-2274 | Article

[51] Leonard, J. B.; McCormick, S. D. Effects of migration distance on whole-body and tissue-specific energy use in American shad (Alosa sapidissima), Canadian Journal of Fisheries and Aquatic Sciences, Volume 56 (1999) no. 7, pp. 1159-1171 | Article

[52] Leonard, J. B. K.; Norieka, J. F.; Kynard, B.; McCormick, S. D. Metabolic rates in an anadromous clupeid, the American shad ( Alosa sapidissima ), Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, Volume 169 (1999) no. 4-5, pp. 287-295 | Article

[53] Mennesson-Boisneau C, ; Boisneau P, Migration, répartition, reproduction, caractéristiques biologiques et taxonomie des aloses (Alosa sp) dans le bassin de la Loire. PhD thesis Université de Rennes et Paris XII, (1990)

[54] Nagy, K. A.; Girard, I. A.; Brown, T. K. Energetics of free-ranging mammals, reptiles, and birds, Annual Review of Nutrition, Volume 19 (1999) no. 1, pp. 247-277 | Article

[55] Olney, J. E.; Denny, S. C.; Hoenig, J. M. Criteria for determining maturity stage in female american shad, alosa sapidissima, and a proposed reproductive cycle, Bulletin Français de la Pêche et de la Pisciculture (2001) no. 362-363, pp. 881-901 | Article

[56] Paumier, A.; Drouineau, H.; Carry, L.; Nachón, D. J.; Lambert, P. A field-based definition of the thermal preference during spawning for allis shad populations (Alosa alosa), Environmental Biology of Fishes, Volume 102 (2019) no. 6, pp. 845-855 | Article

[57] Pelster, B. Swimbladder function and the spawning migration of the European eel Anguilla anguilla, Frontiers in Physiology, Volume 5 | Article

[58] Petersson, E.; Järvi, T. ‘False orgasm’ in female brown trout: trick or treat?, Animal Behaviour, Volume 61 (2001) no. 2, pp. 497-501 | Article

[59] Pianka, E. R. Natural Selection of Optimal Reproductive Tactics, American Zoologist, Volume 16 (1976) no. 4, pp. 775-784 | Article

[60] R Development Core Team, R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria., (2008)

[61] Rands, S. A.; Houston, A. I.; Cuthill, I. C. Measurement of mass change in breeding birds: A bibliography and discussion of measurement techniques, Ringing & Migration, Volume 23 (2006) no. 1, pp. 1-5 | Article

[62] Robertson, D. R. The Role of Adult Biology in the Timing of Spawning of Tropical Reef Fishes, The Ecology of Fishes on Coral Reefs, Elsevier, 1991, pp. 356-386 | Article

[63] Roff D., Evolution of life histories: Theory and analysis, Springer Science & Business Media, (1993)

[64] Sakaji, H.; Hamada, K.; Naito, Y. Identifying spawning events of greater amberjack using accelerometers, Marine Biology Research, Volume 14 (2018) no. 6, pp. 637-641 | Article

[65] Schultz, D. L. Comparison of Lipid Levels during Spawning in Annual and Perennial Darters of the Subgenus Boleosoma, Etheostoma perlongum, and Etheostoma olmstedi, Copeia, Volume 1999 (1999) no. 4, pp. 906-916 | Article

[66] Stearns SC., The Evolution of life histories, OUP Oxford, (1992)

[67] Steinbach, P.; Gueneau, P.; Autuoro, A.; Broussard, D. Radio-pistage de grandes aloses adultes en Loire, Bulletin Français de la Pêche et de la Pisciculture (1986) no. 302, pp. 106-117 | Article

[68] Taverny C., Contribution à la connaissance de la dynamique des populations d’aloses: Alosa Alosa et Alosa Fallax dans le système fluvio-estuarien de la Gironde: pêche, biologie et écologie: étude particulière de la devalaison et de l’impact des activités humaines. Univ. Bordeaux 1 ((1991))

[69] Tentelier, C.; Larranaga, N.; Lepais, O.; Manicki, A.; Rives, J.; Lange, F. Space use and its effects on reproductive success of anadromous Atlantic salmon, Canadian Journal of Fisheries and Aquatic Sciences, Volume 73 (2016) no. 10, pp. 1461-1471 | Article

[70] Tétard, S.; Feunteun, E.; Bultel, E.; Gadais, R.; Bégout, M.-L.; Trancart, T.; Lasne, E. Poor oxic conditions in a large estuary reduce connectivity from marine to freshwater habitats of a diadromous fish, Estuarine, Coastal and Shelf Science, Volume 169 (2016), pp. 216-226 | Article

[71] Tsuda, Y.; Kawabe, R.; Tanaka, H.; Mitsunaga, Y.; Hiraishi, T.; Yamamoto, K.; Nashimoto, K. Monitoring the spawning behaviour of chum salmon with an acceleration data logger, Ecology of Freshwater Fish, Volume 15 (2006) no. 3, pp. 264-274 | Article

[72] Verdeyroux P, ; Guerri O, ; Chanseau M, ; Cazeaux J, ; Fauvel F, ; Bogun F, ; Desmoulin A, ; Tarrene C, ; Nicole T, ; Dubois A, ; Raynal J , Radio-telemetry study of the Allis shad (Alosa alosa) migration at Bergerac and Tuilières along the Dordogne river and at Golfech along the Garonne river from 2011 to 2014. Epidor, (2015)

[73] Wainwright, P. C.; Turingan, R. G. Evolution of Pufferfish Inflation Behavior, Evolution, Volume 51 (1997) no. 2, pp. 506-518 | Article

[74] Wilson, R. P.; Börger, L.; Holton, M. D.; Scantlebury, D. M.; Gómez‐Laich, A.; Quintana, F.; Rosell, F.; Graf, P. M.; Williams, H.; Gunner, R.; Hopkins, L.; Marks, N.; Geraldi, N. R.; Duarte, C. M.; Scott, R.; Strano, M. S.; Robotka, H.; Eizaguirre, C.; Fahlman, A.; Shepard, E. L. C. Estimates for energy expenditure in free‐living animals using acceleration proxies: A reappraisal, Journal of Animal Ecology, Volume 89 (2020) no. 1, pp. 161-172 | Article

[75] Wilson, R. P.; White, C. R.; Quintana, F.; Halsey, L. G.; Liebsch, N.; Martin, G. R.; Butler, P. J. Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant, Journal of Animal Ecology, Volume 75 (2006) no. 5, pp. 1081-1090 | Article

[76] Yamazaki, C.; Koizumi, I. High frequency of mating without egg release in highly promiscuous nonparasitic lamprey Lethenteron kessleri, Journal of Ethology, Volume 35 (2017) no. 2, pp. 237-243 | Article

Cited by Sources: