Canadian Journal of Fisheries and Aquatic Sciences Trade-offs in the adaptation towards hatchery and natural conditions drive survival, migration, and angling vulnerability in a territorial fish in the wild Journal: Canadian Journal of Fisheries and Aquatic Sciences Manuscript ID cjfas-2018-0256.R1 Manuscript Type: Article Date Submitted by the 09-Nov-2018 Author: Complete List of Authors: Tsuboi, Jun-ichi; Fisheris Research Agency, National Research Institute of Aquaculture Kaji, Kohichi; Yamanashi Prefectural Fisheries Technology Center Baba, Shinya; Logics of Blue Arlinghaus, Robert; Humboldt University of Berlin, Adaptation,Draft Captive breeding, Hatchery-induced selection, Stocking, Keyword: Territorial behaviour Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/cjfas-pubs Page 1 of 47 Canadian Journal of Fisheries and Aquatic Sciences 1 Trade-offs in the adaptation towards hatchery and natural conditions drive 2 survival, migration, and angling vulnerability in a territorial fish in the wild 3 4 Jun-ichi Tsuboi, Kohichi Kaji, Shinya Baba, and Robert Arlinghaus 5 6 J. Tsuboi. * Yamanashi Prefectural Fisheries Technology Center, Kai, Yamanashi 7 400-0121, Japan 8 e-mail: [email protected] 9 K. Kaji. Yamanashi Prefectural Fisheries Technology Center, Kai, Yamanashi 10 400-0121, Japan 11 e-mail: [email protected] 12 S. Baba. Logics of Blue, Hyogo, 650-0025, Japan 13 e-mail: [email protected] 14 R. Arlinghaus. Department of Biology and Ecology of Fishes, Leibniz-Institute of 15 Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, 16 Germany; Division of Integrative Fisheries Management, Albrecht-Daniel-Thaer 17 Institute of Agricultural and Horticultural Sciences, Department for Crop and Animal 18 Sciences, Faculty of Life Sciences, Humboldt-Universität zu Berlin, Invalidenstrasse 19 42, 10115 Berlin, Germany. 20 e-mail: [email protected] 21 22 Corresponding author: 23 Jun-ichi Tsuboi 24 National Research Institute of Fisheries Science, Japan Fisheries Research and https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 2 of 47 25 Education Agency, Nikko, Tochigi 321-1661, Japan. 26 Phone: +81-288-55-0055 27 Fax: +81-288-55-0064 28 e-mail: [email protected] 29 30 *Present address: National Research Institute of Fisheries Science, Japan Fisheries 31 Research and Education Agency, Nikko, Tochigi 321-1661, Japan 32 33 34 Draft https://mc06.manuscriptcentral.com/cjfas-pubs Page 3 of 47 Canadian Journal of Fisheries and Aquatic Sciences 35 Abstract 36 Hatchery fish to support capture fisheries need to thrive in both hatchery and natural 37 environments. We conducted joint experiments in both environments with individuals 38 stemming from multiple generations held in captivity to test the performance of 39 hatchery-reared ayu (Plecoglossus altivelis). Ayu has an annual, herbivorous, territorial 40 and amphidromous riverine fish native to Japan of high importance to recreational 41 fisheries. Hatchery fish of the 1st hatchery generation exhibited poor growth and highest 42 malformation rates relative to the 2nd and following hatchery generations. The 1st 43 generation offspring stocked into a natural stream also showed low survival and poor 44 vulnerability to angling, suggesting that maladaptation to the hatchery environment 45 explained the performance in the wild.Draft By contrast, offspring of the 7th to 9th 46 generations exhibited high growth in the hatchery environment, but when stocked into 47 the wild they also exhibited low survival, maladapted migratory behaviour, and again 48 poor vulnerability to angling. Consequently, intermediate generations held in captivity 49 were found to offer the best fisheries performance and can thus be recommended for 50 enhancements to support recreational fisheries. 51 52 Keywords Adaptation; Captive breeding; Hatchery-induced selection; Stocking; 53 Territorial behaviour https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 4 of 47 54 Introduction 55 Stocking of hatchery-reared fish has been frequently applied in fisheries 56 enhancements and conservation, particularly in freshwater environments (Cowx 1994; 57 Lorenzen et al. 2012). Stocking programs are successful if hatchery-fish survive and 58 grow in the wild, contributing to fisheries catch or maintaining threatened or declining 59 populations. However, rapid environmental change from natural to artificial conditions 60 is expected to drive rapid evolutionary change (reviewed by Bay et al. 2017). Indeed, 61 hatchery selection negatively affects fitness in the wild, particularly in salmonids (Araki 62 et al. 2007; Christie et al. 2014, 2016, 2018). The hatchery environment offers strikingly 63 different selection pressures to natural conditions (e.g., in terms of chemical conditions, 64 density of fish, access to food, presenceDraft of predators, parasite load), such that adaptation 65 to the hatchery environment can be expected to exert rapid fitness effects on genotypes, 66 gene expression and phenotype development (Araki et al. 2008; Christie et al. 2016; 67 Uusi-Heikkilä et al. 2017). Hatchery selection effects leading to trait divergence among 68 hatchery and natural populations likely accumulate over generational time, but are most 69 severe early on in the adaptation process to artificial conditions (Araki et al. 2007, 2008) 70 and may occur even within the first generation in captivity through epigenetic effects 71 (Christie et al. 2016). In particular, hatchery selection has been shown to rapidly modify 72 phenotypic variance and mean trait values involved in maturation and growth and 73 associated behavioural and physiological traits considered important for efficient 74 biomass production in aquaculture settings (Huntingford 2004; Kostow 2004). In this 75 study, we followed Teletchea and Fontaine (2014) and defined domestication as the 76 gradual adaptation of an organism to living conditions that are determined by some 77 form of human intervention. Releasing highly domesticated fishes into the wild https://mc06.manuscriptcentral.com/cjfas-pubs Page 5 of 47 Canadian Journal of Fisheries and Aquatic Sciences 78 promises high mortality post release (Lorenzen 2006), at the possible benefit of high 79 return to the fisheries catch when large, recruited fishes are stocked that are immediately 80 targeted by recreational anglers (Mezzera and Largiadèr 2001; Baer et al. 2007; 81 Lorenzen et al. 2012). 82 Although a range of studies have shown that hatchery fish have lower fitness (e.g., 83 survival) in the wild (Lorenzen 2000, 2006), it is less clear which phenotypic traits are 84 exactly affected and which fitness components – behaviour, growth, survival or 85 reproduction – are altered alone or in combination in hatchery selection (e.g., Brown 86 and Day 2002; Miller et al. 2004; Araki and Schmid 2010). Moreover, from an 87 anthropocentric perspective, the current body of literature suggests that some traits 88 important to fisheries may even benefitDraft from hatchery selection – notably individual 89 vulnerability to capture, and by the same token population-level catchability, which is 90 often found to be higher in domesticated phenotypes compared to wild phenotypes 91 because domesticated fish are more explorative, bolder and grow faster, in turn showing 92 greater food intake rates and vulnerability to angling (Lorenzen et al. 2012; Klefoth et al. 93 2012, 2013). Thus, although hatchery selection should lower natural fitness, it should at 94 the same time benefit vulnerability to fishing, assuming that fish that are stocked are 95 morphologically vulnerable to fishing gear (Lennox et al. 2017). However, no studies 96 have quantified the trade-offs among natural and hatchery selection in terms of natural 97 and fisheries performance over several generations in captivity when these fish are 98 stocked into the wild to support recreational fisheries catch. 99 In stock enhancements, hatchery-reared fish are released to be recaptured after 100 stocking after some period in the wild (Lorenzen et al. 2012). Hatchery fish are usually 101 more-exploratory and bolder than wild conspecifics, and as a result hatchery fish are https://mc06.manuscriptcentral.com/cjfas-pubs Canadian Journal of Fisheries and Aquatic Sciences Page 6 of 47 102 often highly vulnerable to angling gear (Klefoth et al. 2012, 2013; Härkönen et al. 2014, 103 2016; Koeck et al. in press; reviewed in Lennox et al. 2017 and Arlinghaus et al. 2017). 104 Because domestication changes all of these traits, domesticated fish of both salmonids 105 and cyprinids were indeed found to be more readily captured than less domesticated fish 106 (Mezzera and Largiadèr 2001; Klefoth et al. 2012), leaving behind individuals, which 107 are less explorative and more timid (Alós et al. 2016; Tsuboi et al. 2016; Arlinghaus et 108 al. 2017). The fact that vulnerability to angling is a function of domestication relates to 109 a range of behavioural and physiological traits that co-vary with adaption to artificial 110 environments and that render domesticated fish a good model for trait complexes 111 affecting vulnerability to angling (Klefoth et al. 2012, 2013; Arlinghaus et al. 2017). 112 According to recent reviews andDraft empirical studies, passive gear types, such as gill 113 nets or rod-and-reel, are supposed to selectively catch bold,