Costs of attaining larger size prior to migration inferred from predation-caused wounds in an anadromous fish

Costs of attaining larger size prior to migration inferred from predation-caused wounds in an anadromous fish | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Costs of attaining larger size prior to migration inferred from predation-caused wounds in an anadromous fish Ryo Futamura, Kentaro Morita, Yoichiro Kanno, Jiro Uchida, Atsushi Okuda, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4289981/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Survival during migration typically depends on body size, in which smaller migrants suffer higher mortality. Thus, migratory animals are predicted to adopt growth tactics to attain large size before migration. Size-dependent growth patterns represent such a case, in which smaller migrants exhibit rapid growth and delay start of migration (extended pre-migration period) to attain a large body size to survive migration. To evaluate adaptiveness of such size-dependent growth patterns, it is crucial to understand costs associated with rapid growth and delayed migration start, since the adaptiveness of the size-dependent growth patterns cannot be solely explained by ecological demands of rapid growth and late migration start. However, potential costs remain largely unknown. Here, we focused on the trade-off between growth and survival, and investigated whether faster pre-migration growth rates and longer pre-migration periods incurred higher predation risk in masu salmon ( Oncorhynchus masou ), which exhibit size-dependent growth patterns. In a capture-mark-recapture survey examining predation-caused wounds as a proxy for predation risk, we found a non-significant effect of growth rate but a significantly positive effect of timing of migration initiation on the frequency of predation-caused wounds. In particular, migrants that stayed longer in the river had higher probabilities of having predation-caused wounds, especially inflicted by piscivorous birds. This implies that smaller migrants extend their stay in the river to attain larger size for surviving oceanic migration, although the extended stay in the river is costly in terms of increased predation risk. trade-off growth predation life-history salmonids Figures Figure 1 Figure 2 Figure 3 Introduction Many animals migrate to complete their life cycle (Dingle and Drake 2007 ; Alerstam and Bäckman 2018 ). Although they benefit substantially from migration, they also suffer high mortality during migration (Alerstam et al. 2003 ). Notably, smaller migratory individuals (migrants) suffer higher mortality during a risky migration trip (Sogard 1997 ; Alerstam et al. 2003 ; Oppel et al. 2015 ; Tucker et al. 2016 ; Gregory et al. 2019 ; Simmons et al. 2022 ). Thus, attaining large size before migration is critical for successful migration (Roff 1991 ). This suggests that migrants should adopt growth tactics to attain sufficiently large size to survive the migration (i.e., size-threshold) once they have decided to migrate (Arendt 1997 ). Indeed, previous research has documented potential growth tactics just prior to migration. For instance, smaller migrants exhibited higher growth rates and delayed migration (i.e., an extended pre-migration period) compared to their larger counterparts (Nicieza and Brana 1993 ; Bohlin et al. 1996 ; Dermond et al. 2019 ; Futamura et al. 2022 a). This combination of higher growth rates and extended pre-migration periods allow smaller migrants to achieve a greater size increment during the pre-migration period, enabling them to surpass a size threshold at the onset of migration. Given that smaller migrants face stronger ecological demands than larger ones, these size-dependent growth patterns can be interpreted as adaptive life history tactics. However, it is important to note that the adaptiveness of this growth pattern cannot be solely explained by the size-dependent ecological demands of growth placed on smaller migrants. If faster growth rates and longer pre-migration periods do not incur any cost, maximizing size increment before migration should be adaptive for migrants, regardless of body size. Therefore, to affirm the adaptive significance of the size-dependent growth pattern, it is necessary to understand the costs associated with faster growth and longer pre-migration periods. However, these potential costs remain largely unexplored. In this study, we addressed this knowledge gap by focusing on the trade-off between growth and survival (Stearns 1989 ). The trade-off between growth and survival is characterized by a positive correlation between size increment and mortality, where individuals attempting to achieve a larger size increment are subject to a higher mortality risk (Stearns 1989 , 1992 ; Mangel and Stamps 2001 ). This growth-survival trade-off has been documented in previous studies that explored genetic and plastic variation in growth rates among individuals (Anholt and Werner 1995 ; Gotthard 2000 ; Munch and Conover 2003 ; Biro et al. 2004 ). One well-known cause of this trade-off is the increased predation risk associated with behaviors that individuals adopt to achieve a larger size increment (Houston et al. 1993 ; Dmitriew and Rowe 2005 ). Individuals need to either increase their foraging activity or time to achieve larger size increment, (Werner and Anholt 1993 ; Damsgird and Dill 1998 ; Willette 2001 ), but these behaviors likely increase encounters with predators (Lima and Dill 1990 ; Brown and Kotler 2004 ; Verdolin 2006 ). In this study, we sought to evaluate whether the same processes operate during the pre-migration period of migrants. We examined whether migrants with a higher growth rate and longer growth period were subject to a higher predation risk before migration. This was done by investigating the frequency of wounds caused by predator attacks on masu salmon ( Oncorhynchus masou ) migrants. Masu salmon, endemic to East Asia, commonly exhibit partial migration, with populations consisting of both river-dwelling residents and anadromous migrants (Kato 1991 ). Residents remain in the river throughout their lives (Nakano 1995 ; Sakata et al. 2005 ). In contrast, migrants typically spend only the first 1–2 years in the river, during which they mostly stay in a limited habitat area in the upstream of the river (nursery habitat). Subsequent to the stay in the nursery habitat, migrants descend the middle and lower reaches of the river (river corridor) towards the ocean in spring (i.e., between April and July) to begin oceanic migration (Kato 1991 ). After spending a year in the resource-rich but high-risk ocean, migrants return to their natal river to spawn (Morita 2018 ). Migrants, particularly smaller ones, face size-selective mortality during oceanic migration (Miyakoshi et al. 2001 ; Shimoda et al. 2003 ; Miyakoshi 2006 ). Notably, we found size-dependent growth patterns among masu salmon migrants before oceanic migration, suggesting a growth tactic to avoid size-selective mortality during oceanic migration: smaller migrants had exhibited higher growth rates for half a year before they started oceanic migration and descended the river later than larger ones in the same seasons (Futamura et al. 2022 a). In this study, we hypothesized that a faster growth rate and a longer pre-migration period of masu salmon would accompany mortality costs due to increased predation risk in the river. More interpretively, we considered that these costs would result in the size dependence of growth rates and pre-migration periods. Specifically, the smaller migrants would not survive the risky oceanic migration unless they attained larger sizes before migration. Therefore, they would accelerate growth rates and extend the pre-migration periods, even if these growth tactics are accompanied by potentially higher costs. In contrast, the larger migrants would not need to invest in additional size growth to prepare for risky oceanic migration and minimize these potential costs. Accordingly, we tested the following two predictions. First, masu salmon migrants that exhibited higher growth rates just before oceanic migration (i.e., period between early spring and start of oceanic migration) would be exposed to higher predation risk than those exhibiting lower growth rates. Second, masu salmon migrants that started oceanic migration later would be exposed to higher predation risk than those who started earlier. To test these predictions, we conducted a capture-mark-recapture survey of masu salmon migrants in the pre-migration period and examined the frequency of the wounds due to predator attacks (i.e., hereafter called predation-caused wounds) as a proxy for predation risk (Fig. 1 ) (Reimchen 1988 , 1992 ; Davies et al. 1995 ; Polyakov et al. 2022 ). Material and Methods Study system Our study was conducted in a 12.2 km long spring-fed River, Horonai River (42°40′N, 141°35′E) located in Hokkaido, northern Japan (Fig. 2 ). This river is composed of three distinct reaches. The uppermost 5.3 km reach (6.9–12.2 km from the river mouth) is characterized with natural riverbank and secondary deciduous forest. The uppermost reach is the primary habitat of masu salmon residents and migrants, where migrants have their nursery habitat before descending the river. In this reach, masu salmon have been marked with a PIT-tag (12.0 mm × 2.12 mm, Oregon RFID, Inc) for an ongoing fish monitoring project since 2018. The middle river reach (4.6–6.9 km from the river mouth) is slow-moving and includes artificial impoundments and wetlands totaling 1.0 ha and a maximum depth of 2.5 m. This reach serves as a river corridor, where river-descending masu salmon migrants pass through after leaving the nursery habitat in the uppermost reach. In the middle reach, piscivorous brown trout ( Salmo trutta ) account for 70% of the fish (Futamura et al. unpublished data ) and water birds such as Great Egret ( Ardea alba ) and Common Merganser ( Mergus merganser ) are commonly observed (Futamura et al. personal observation ). Since this reach largely consists of artificial impoundments and wetlands, it appears favorable for piscivorous birds, which mainly forage in open waters with sparce overhanging trees (Tojo 1996 ). The lowermost reach (the lowermost 4.6 km section from the river mouth) flows through the urbanized landscape of Tomakomai City and artificially straightened for flood control. This reach regularly harbors only few salmonids and temporally function as river corridor for masu salmon during the season of river-descending. Capture-mark-recapture survey of migrants before river descending. We conducted a capture-mark-recapture survey in the uppermost reach in spring 2020 (18–26 Mar-2020). We collected masu salmon using a backpack electrofishing unit (300–400 V DC, model 12B, Smith-Root, Inc., Vancouver, WA, USA) with 3 mm mesh dipnets (30 cm wide). Fish were anesthetized by diluted eugenol (FA-100 DS Pharma Animal Health Co., Ltd.) to measure their fork length (FL) (nearest 1 mm) and body mass (nearest 0.1 g) and to check for bodily wounds (see later). We also examined whether fish had been previously identified by a PIT tag using a handy PIT-tag reader. Individuals without the PIT tag > 60 mm were tagged in this survey. The tag was inserted into the abdominal cavity through a small incision made with a clean scalpel. Fish were then allowed to recover from anesthesia and were released within 10 m of original capture. The number of masu salmon captured and identified by PIT tag was 1495 and individuals having predation-caused wounds was not found at this occasion. Capture survey on the river-descending migrants We captured migrants at the onset of oceanic migration by installing a fyke-net type trap in the middle reach (5.7 km from the river mouth) from 04 Apr to 24 Jul, 2020 (Fig. 2 ). Captured fish were anesthetized using eugenol (FA-100 DS Pharma Animal Health Co., Ltd.), and were measured for fork length (nearest 1 mm) and body mass (nearest 0.1 g). We checked for visual signs of smoltification (i.e., silverly body coloration and black pigmentation on the tip of the dorsal fin) and then took a photograph. A waterproof digital camera (TG-5, Olympus Co., Tokyo, Japan) was used to take photographs and document predation-caused wounds. Then, fish were held in a bucket filled with fresh river water to allow recovery from anesthesia and were released to the pool habitat just downstream of the trap. Detailed information on the migrant trap survey is described in Futamura et al. ( 2022 b). Using the photographs taken in the migrant trap survey, we examined whether wounds were inflicted by predators (predation-caused wounds) or not (handling-caused wounds). Three categories of predation-caused wounds were identified based on their characteristics. First, bill-shaped scars inflicted from either the ventral or dorsal side were identified as avian wounds (Fig. 1 a) (Reimchen 1988 ; Davies et al. 1995 ; Kortan et al. 2008 ). Second, a series of tooth-shaped scars inflicted from the front or the back of the body were identified as those caused by piscivorous fish (Fig. 1 b) (Reimchen 1988 , 1991 , 1992 ). Third, we could not identify all scars were inflicted by either a bill or tooth, and they were recorded as non-identified predation-caused wounds. If migrant had either of the predation-caused wounds, we defined that migrant had a predation-caused wound. Other wounds, such as large areas of missing scales or single linear scar, were classified as handling-caused wounds (i.e., capturing the fish by migrant trap and measurement) (Fig. 1 c). The identification of the wound types based on the scar characteristics can be difficult because scar patterns are sometimes unclear. This raises the concern that our categorization of the wound type might be incorrect. However, this concern is not an issue, as the occurrence patterns of handling-caused and predation-caused wounds were inconsistent. Although we observed a positive relationship between the timing of migration start and the frequency of predation-caused wounds (see Result), the relationship between migration timing and the frequency of handling-caused wound was negative (Fig. S1 ) (Table. S2) (see Online Resource 1 for detail). Definition of growth rate and pre-migration period To test whether higher growth rates before migration and longer pre-migration periods incurred higher predation risk, we defined growth rate during the pre-migration period using the data obtained from the capture-mark-recapture survey in early spring and migrant trap survey. As a metric of growth rate, we used relative growth rate adjusted for body size, because growth rate and predation highly depend on body size (Lugert et al. 2016 ). Relative growth rate was calculated from the residuals of the following linear model: ln (FL migration ) ~ ln (FL early spring ) + Δ t, in which FL migration is the size at the migrant trap survey, FL early spring is the size at early spring capture-mark-recapture survey and Δ t as elapsed dates between the two surveys. As a metric of the pre-migration period, we used the capture date at the migrant trap survey, which serves as an endpoint of the pre-migration period. Statistical analysis To assess the effects of relative growth rate and pre-migration period on the frequency of predation-caused wounds, we conducted our analysis in two procedures. First, we assessed the association between these variables and frequency of predation-caused wound regardless of their cause (i.e., bill-shaped, tooth-shaped, or not-identified). Then, we investigated the association between these variables and frequency of each type of predation-caused wounds (bill-shaped and tooth-shaped). The effect of relative growth rate and pre-migration period on predation-caused wounds were analyzed in separate models because of the sample size disparities (i.e., sample size for growth rate analysis is n = 119, sample size for pre-migration period analysis is n = 578). Growth period and relative growth rate were not significantly correlated with each other (Pearson’s r correlation, r = -0.03, P = 0.780). For the growth rate analysis, generalized linear model (GLM) with a binominal distribution and logit-link function (i.e., logistic regression) was employed to examine whether the frequency of the predation-caused wound at the onset of migration was determined by relative growth rate in spring. Similarly, logistic regression was employed to examine whether the frequency of the predation-caused wound at the migrant trap was affected by the pre-migration period and fork length at migrant trap. Because the interaction term, pre-migration period × fork length, did not improve the models in preliminary analyses, the interaction terms were dropped. Overall, we used six models on the analysis of the predation-caused wounds (i.e., three injury status [predation-caused wound regardless of cause, bill-shaped, and tooth-shaped] × two growth mechanisms [growth rate and pre-migration period]). In all models, the significance of the independent variables was evaluated by likelihood ratio test which was performed by using the maximum likelihood method. All statistical analysis was performed using R ver. 4.3.1. Result A total of 578 masu salmon migrants were captured in the migrant trap from 14-Apr to 16-Jun 2020. Among these, 51 had a bill-shaped predation-caused wound, 24 had a tooth-shaped predation-caused wound, 31 had a non-identified predation-caused wound, 186 had a handling-caused wound, 1 had both bill-shaped predation-caused wound and handling-caused wounds, 4 had both bill-shaped and tooth-shaped predation-caused wounds, and 281 had no wound (unscathed) (Table S1 ). These 578 individuals were used for the analysis of the pre-migration period. Of migrants captured in the migrant trap survey, 119 had been previously captured in the early-spring capture-mark-recapture survey): 10 had a bill-shaped wound, 2 had a tooth-shaped wound, 7 had a non-identified predation-caused wound, 32 had a handling-caused wound, 1 had both bill-shaped predation-caused wound and handling-caused wounds, and 67 had no wound (Table S1 ). These 119 individuals were used for the analysis of the relative growth rate. The frequency of predation-caused wound, regardless of its cause, tended to increase with the relative growth rate, but was not significant (χ 2 = 2.07, P = 0.150) (Table 1 ) (Fig. 3 a). The relative growth rate in spring was not significantly related to the frequency of bill-shaped predation-caused wound (χ 2 = 0.30, P = 0.586) or tooth-shaped predation-caused wound (χ 2 = 1.19, P = 0.276) (Table 1 ) (Fig. 3 c; Fig. 3 e). Table 1 Results of the logistic regression model predicting frequency of predation-caused wound. Estimates of independent variables are shown on the logit scale. Model formulae Independent variable Estimates Std. Error χ 2 value P Frequency of predation-caused wound (regardless of cause) ~ Intercept + Relative growth rate Intercept -1.64 0.25 Relative growth rate 9.71 6.94 2.07 0.150 Frequency of bill-shaped predation-caused wound ~ Intercept + Relative growth rate Intercept -2.30 0.32 Relative growth rate 4.64 8.60 0.30 0.586 Frequency of tooth-shaped predation-caused wound ~ Intercept + Relative growth rate Intercept -4.40 0.94 Relative growth rate 22.94 22.41 1.19 0.276 Frequency of predation-caused wound (regardless of cause) ~ Intercept + Pre-migration period + Fork length Intercept -9.66 2.07 Pre-migration period 2.23 × 10 − 2 9.44 × 10 − 3 5.76 0.016 Fork length 3.77 × 10 − 2 1.20 × 10 − 2 10.31 0.001 Frequency of bill-shaped predation-caused wound ~ Intercept + Pre-migration period + Fork length Intercept -12.73 2.82 Pre-migration period 4.44 × 10 − 2 1.33 × 10 − 2 12.13 < 0.001 Fork length 3.10 × 10 − 2 1.58 × 10 − 2 4.02 0.045 Frequency of tooth-shaped predation-caused wound ~ Intercept + Pre-migration period + Fork length Intercept -6.40 3.51 Pre-migration period -1.42 × 10 − 2 1.62 × 10 − 2 0.77 0.381 Fork length 4.02 × 10 − 2 2.14 × 10 − 2 3.67 0.055 The frequency of migrants with predation-caused wounds, regardless of its cause, significantly increased with the pre-migration period (χ 2 = 5.76, P = 0.016) (Fig. 3 b) and with the fork length (χ 2 = 10.31, P = 0.001) (Table 1 ). The frequency of migrants with bill-shaped predation-caused wound also significantly increased with the pre-migration period (χ 2 = 12.13, P < 0.001) (Fig. 3 d) and with the fork length (χ 2 = 4.02, P = 0.045) (Table 1 ). However, the frequency of migrants with tooth-shaped wound was not significantly related with either the pre-migration period (χ 2 = 0.77, P = 0.381) (Fig. 3 f) or the fork length (χ 2 = 3.67, P = 0.055) (Table 1 ). Discussion In many migratory species, small individuals at a certain timing before migration tend to grow faster and start migrating later than large individuals, which allows the small ones to reach a larger size before they start migration (Nicieza and Brana 1993 ; Bohlin et al. 1996 ; Dermond et al. 2019 ; Futamura et al. 2022 a). While the potential costs of faster growth and delayed migration explain why migrants don’t all maximize these size-increment factors, these costs have not been directly investigated. This study, using masu salmon migrants, tested the hypotheses that faster growth and delayed migration start increase predation risk for migrants in the pre-migration period. Our result could not support the hypothesis that faster growth in the pre-migration period caused greater predation risk. To the contrary, timing of migration start (i.e., date of capture at migrant trap) was significantly associated with the frequency of wounds. In particular, although the timing of migration start did not explain the frequency of the tooth-shaped wound, probability of inflicting bill-shaped predation-caused wound was higher in migrants with delayed migration start. These results suggest that masu salmon migrants that initiated oceanic migration later were exposed to higher predation risk mainly by the avian predators before migration. This implies that smaller migrants stayed longer in the river to attain a large size for surviving the oceanic migration despite the increased predation risk in the river. In contrast, larger migrants opted to leave the river sooner and avoided the predation risk. As the frequency of predation-caused wounds in migrants increased over time, it is possible that the higher probability of inflicting predation-caused wounds with late migration start is simply due to the later timing of the wound assessment (i.e., the day of capture in the migrant trap). However, this is unlikely to be a problem for our conclusion. This is because all migrants, regardless of when they were captured at the migrant trap, must pass through the high predation risk areas such as the lower reaches of the river, estuaries and coastal areas (Welch et al. 2011 ; Clark et al. 2016 ; Moore et al. 2021 ). If all migrants are exposed to at least the same degree of predation risk during the passage through such risky areas, regardless of the timing, migrants that initiate migration later experience higher predation risk as a whole. In this case, our conclusion that migrants with predator wounds at the time of capture are exposed to a higher predation risk before the start of oceanic migration remains valid. Our study revealed increased predation on migrants with longer pre-migration periods, particularly from piscivorous birds. This raises a further question: where and how do these migrants encounter this heightened predation risk before their journey? There are two potential hotspots for increased predation before migration: the uppermost reach where migrants spend until start of river-descending as a nursery habitat, and the middle reach which serve as a river corridor during descending the river. A survey of masu salmon residents, which was held right after the river-descending season of migrants (25–26 Jun-2020), indicates the former hypothesis is unlikely. In the survey, the residents remaining in the migrants’ nursery habitat (the uppermost river reach) exhibited no predation-caused wounds (i.e., total 509 residents had no predation-caused wounds) (Futamura et al., unpublished data ). This strongly suggests that migrants were facing increased predation risk while descending the river. This aligns with our frequent observations of piscivorous birds in the middle reaches of the Horonai River, lending support to the hypothesis. Notably, Great Egrets ( Ardea alba ) and Common Mergansers ( Mergus merganser ), rarely seen in the uppermost reach, were regularly present in the middle reach during the river-descending season of migrants (Futamura et al., personal observation ). In general, individuals with faster growth are more vulnerable to predation because active foraging to support faster grow also makes them more likely to be detected or encountered by predators (Lima and Dill 1990 ; Brown and Kotler 2004 ; Verdolin 2006 ). However, in our present study, we did not find statistically significant evidence of predation-related costs in migrants with higher growth rates. This does not necessarily mean that there are no costs associated with rapid growth before migration. While we focused on increased predation risk as a potential fitness cost of faster growth, other costs are also worth considering. For example, higher growth rates may incur physiological costs such as increased metabolic costs and impaired immune function (Stoks et al. 2006 ; Van Der Most et al. 2011 ). It is important to explore these potential long-term costs to fully understand the costs associated with rapid growth before migration. Smaller individuals typically face heavier predation pressure (Sogard 1997 ; Van Kooten et al. 2007 ; Takatsu et al. 2017 ; Stige et al. 2019 ), and this holds true similarly for migrating species (Alerstam et al. 2003 ; Oppel et al. 2015 ; Gregory et al. 2019 ; Simmons et al. 2022 ). In fact, our previous study provided evidence of such size-selective mortality in masu salmon migrants while descending the lower reaches (river corridor) of Horonai River (Futamura et al. 2022 b). However, our results contradicted this general pattern. Larger migrants showed a higher frequency of predation-caused wounds (Table 1 ). This pattern mirrors a similar finding in a previous study on predation-caused wounds of three-spine stickleback ( Gasterosteus aculeatus ) (Reimchen 1988 ). This seemingly paradoxical result may be explained by predator handling abilities. While piscivorous birds and fish can attack and capture prey across a wide size range, their ability to consume certain larger prey is limited by their gape size (“gape-limited”) (Moser 1986 ; Hambright 1991 ). Additionally, even with prey smaller than their gape, predators require time to handle and swallow them (Draulans 1987 ). This extended handling time provides larger migrants with a heightened chance of escape, even after initial capture. Consequently, larger migrants may inflict more predation-caused wounds due to these attempted attacks Our findings demonstrated that extending the pre-migration period incurs a fitness cost in the form of increased predation risk. However, this might not preclude the possibility that other mechanisms operate as costs of an extended pre-migration period. For example, a delay in the departure of migration likely results in decreased benefits of oceanic migration, because longer pre-migration period also translates to a shorter oceanic migration period and might miss the optimal timing of migration. During oceanic migration, salmonids can significantly increase their size by consuming abundant prey, which ultimately benefits reproduction (Gross et al. 1988 ; Maekawa and Nakano 2002 ) and the timing of migration affect the ocean survival (Jonsson and Jonsson 2009 ; Iida et al. 2018 ). Thus, to maximize resource gains, starting oceanic migration early can be crucial. Therefore, investigating such potential trade-off between oceanic growth and early departure, alongside predation costs, in masu salmon and other migratory species would be valuable in advancing our understanding of the factors that shape condition-dependent migration departure. Declarations ACKNOWLEDGEMENTS We thank Yuichi Matsuoka, Shoji Kumikawa, Hiroshi Sugiyama, Hiroyuki Takahashi, Susumu Igarashi, Tomoaki Sato, Yuto Sasaki for their support in fieldwork. Funding This work was supported by a JSPS KAKENHI grant to RF (22KJ0078) and OK (20K21439 and 22H02694). Conflicts of interest The authors declare that they have no conflict of interest. Ethics approval Our work conforms to the guidelines for the proper conduct of animal experiments in Japan and was approved by the committee for animal experiments in FSC of Hokkaido University (ID 2‐6). Consent to participate Not applicable Consent for publication Not applicable Availability of data and material All of the data analyzed in this study is deposited in Figshare (10.6084/m9.figshare.25638036). Code availability All of the R scripts is deposited in Figshare (10.6084/m9.figshare.25638036). Author contribution statement RF, KM, YK and OK conceived the ideas. 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Knowl Manag Aquat Ecosyst 01. https://doi.org/10.1051/kmae:2008006 Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. https://doi.org/10.1139/z90-092 Lugert V, Thaller G, Tetens J et al (2016) A review on fish growth calculation: Multiple functions in fish production and their specific application. Reviews Aquaculture 8:30–42. https://doi.org/10.1111/raq.12071 Maekawa K, Nakano S (2002) To sea or not to sea: A brief review on salmon migration evolution. Fish Sci 68:27–32. https://doi.org/10.2331/fishsci.68.sup1_27 Mangel M, Stamps J (2001) Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res Miyakoshi Y (2006) Evaluation of stock enhancement programs and stock assessment for masu salmon in Hokkaido, Northern Japan. Sci Rep Hokkaido Fish Hatch 60:1–64 Miyakoshi Y, Nagata M, Kitada S (2001) Effect of smolt size on post release survival of hatchery-reared masu salmon Oncorhynchus masou . Fish Sci 67:134–137. https://doi.org/10.1046/j.1444-2906.2001.00209.x Moore ME, Berejikian BA, Greene CM, Munsch S (2021) Environmental fluctuation and shifting predation pressure contribute to substantial variation in early marine survival of steelhead. Mar Ecol Prog Ser 662:139–156. https://doi.org/10.3354/meps13606 Morita K (2018) Ocean ecology of masu (cherry) salmon 1. Masu salmon group. In: Beamish R (ed) The ocean ecology of Pacific salmon and trout. American Fisheries Society, pp 697–730 Moser ME (1986) Prey profitability for adult Grey Herons Ardea cinerea and the constraints on prey size when feeding young nestlings. https://doi.org/10.1111/j.1474-919X.1986.tb02688.x . Ibis Munch SB, Conover DO (2003) Rapid growth results in increased susceptibility to predation in Menidia menidia . Evolution 57:2119–2127. https://doi.org/10.1111/j.0014-3820.2003.tb00389.x Nakano S (1995) Competitive interactions for foraging microhabitats in a size-structured interspecific dominance hierarchy of two sympatric stream salmonids in a natural habitat. Can J Zool 73:1845–1854. https://doi.org/10.1139/z95-217 Nicieza AG, Brana F (1993) Relationships among smolt size, marine growth, and sea age at maturity of Atlantic salmon ( Salmo salar ) in Northern Spain. Can J Fish Aquat Sci 50:1632–1640. https://doi.org/10.1139/f93-184 Oppel S, Dobrev V, Arkumarev V et al (2015) High juvenile mortality during migration in a declining population of a long-distance migratory raptor. Ibis 157:545–557. https://doi.org/10.1111/ibi.12258 Polyakov AY, Quinn TP, Myers KW, Berdahl AM (2022) Group size affects predation risk and foraging success in Pacific salmon at sea. Sci Adv 8:eabm7548. https://doi.org/10.1126/sciadv.abm7548 Reimchen TE (1988) Inefficient predators and prey injuries in a population of giant stickleback. Can J Zool 66:2036–2044. https://doi.org/10.1139/z88-299 Reimchen TE (1992) Injuries on stickleback from attacks by a toothed predator ( Oncorhynchus ) and implications for the evolution of lateral plates. Evolution 46:1224. https://doi.org/10.2307/2409768 Reimchen TE (1991) Trout foraging failures and the evolution of body size in stickleback. Copeia 1991:1098–1104. https://doi.org/10.2307/1446106 Roff DA (1991) Life history consequences of bioenergetic and biomechanical constraints on migration. Am Zool 31:205–216. https://doi.org/10.1093/icb/31.1.205 Sakata K, Takuya K, Takeshita N et al (2005) Movement of the fluvial form of masu salmon, Oncorhynchus masou masou , in a mountain stream in Kyushu, Japan. Fish Sci 71:333–341. https://doi.org/10.1111/j.1444-2906.2005.00969.x Shimoda K, Naito K, Nakajima M et al (2003) Marine survival and growth of masu salmon Oncorhynchus masou , in relation to smolt size. Nippon Suisan Gakkaishi 69:926–932. https://doi.org/10.2331/suisan.69.926 Simmons OM, Britton JR, Gillingham PK et al (2022) Predicting how environmental conditions and smolt body length when entering the marine environment impact individual Atlantic salmon Salmo salar adult return rates. J Fish Biol 101:378–388. https://doi.org/10.1111/jfb.14946 Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: A review. Bull Mar Sci 60:1129–1157 Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268. https://doi.org/10.2307/2389364 Stearns SC (1992) The Evolution Of Life Histories. Oxford University Press Stige LC, Rogers LA, Neuheimer AB et al (2019) Density- and size-dependent mortality in fish early life stages. Fish Fish 20:962–976. https://doi.org/10.1111/faf.12391 Stoks R, De Block M, McPeek MA (2006) Physiological costs of compensatory growth in a damselfly. Ecology 87:1566–1574. https://doi.org/10.1890/0012-9658(2006)87[1566:pcocgi]2.0.co;2 Takatsu K, Rudolf VHW, Kishida O (2017) Giant cannibals drive selection for inducible defence in heterospecific prey. Biol J Linn Soc Lond 120:675–684. https://doi.org/10.1111/bij.12912 Tojo H (1996) Habitat selection, foraging behaviour and prey of five heron species in Japan. Jap J Ornithol 45:141–158. https://doi.org/10.3838/jjo.45.141 Tucker S, Hipfner JM, Trudel M (2016) Size- and condition-dependent predation: A seabird disproportionately targets substandard individual juvenile salmon. Ecology 97:461–471. https://doi.org/10.1890/15-0564.1 Van Der Most PJ, De Jong B, Parmentier HK, Verhulst S (2011) Trade-off between growth and immune function: a meta‐analysis of selection experiments. Funct Ecol 25:74–80. https://doi.org/10.1111/j.1365-2435.2010.01800.x Van Kooten T, Persson L, De Roos AM (2007) Size-dependent mortality induces life-history changes mediated through population dynamical feedbacks. Am Nat 170:258–270. https://doi.org/10.1086/518947 Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464. https://doi.org/10.1007/s00265-006-0172-6 Welch DW, Melnychuk MC, Payne JC et al (2011) In situ measurement of coastal ocean movements and survival of juvenile Pacific salmon. Proceedings of the National Academy of Sciences 108:8708–8713. https://doi.org/10.1073/pnas.1014044108 Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272. https://doi.org/10.1086/285537 Willette TM (2001) Foraging behaviour of juvenile pink salmon ( Oncorhynchus gorbuscha ) and size-dependent predation risk. Fish Oceanogr 10:110–131. https://doi.org/10.1046/j.1054-6006.2001.00042.x Supplementary Files Predationwoundsubmissionsupplement.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4289981","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":319872120,"identity":"6837a12f-d315-4af2-93e7-3d260b0c8081","order_by":0,"name":"Ryo Futamura","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA6klEQVRIiWNgGAWjYDAC5gNInA9AzMZOSAtbAmMDhMHMwDgDQpOghZkHbC8BHeZtPOYPfuYczuef33/4tc2vbfJ8QNs+fMzBrUXmGI9hY++2w5YzjjGzWef23TZsA9omOXMbbi0S8j2GDbzbDhswALUY5/bcZgRqYWPmxaeFDWjLX6AWeZAWy57b9kRpaQbZYnCMmfkxw4/biURoYSucLbst3cDwWLIZY2/D7eQ2ZsZm/H5hY97w8e02awO5wwcff/jx57bt/Pbmgx8+4tGCDNgkGNtANDSiiAHMHxj+EK14FIyCUTAKRhAAAHXbTBhIivBVAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0000-0001-8128-3476","institution":"Hokkaido Daigaku","correspondingAuthor":true,"prefix":"","firstName":"Ryo","middleName":"","lastName":"Futamura","suffix":""},{"id":319872121,"identity":"622c489f-ce4d-418d-8d10-08128ccdcd7b","order_by":1,"name":"Kentaro Morita","email":"","orcid":"","institution":"Tokyo Daigaku","correspondingAuthor":false,"prefix":"","firstName":"Kentaro","middleName":"","lastName":"Morita","suffix":""},{"id":319872122,"identity":"f2d0dda6-e934-4898-86b1-70e79f8d76c9","order_by":2,"name":"Yoichiro Kanno","email":"","orcid":"","institution":"Colorado State University","correspondingAuthor":false,"prefix":"","firstName":"Yoichiro","middleName":"","lastName":"Kanno","suffix":""},{"id":319872123,"identity":"c8d09aec-1bcd-406e-80fd-28f568bd430c","order_by":3,"name":"Jiro Uchida","email":"","orcid":"","institution":"Hokkaido Daigaku","correspondingAuthor":false,"prefix":"","firstName":"Jiro","middleName":"","lastName":"Uchida","suffix":""},{"id":319872124,"identity":"fe4326a9-bc9f-457a-abd8-8e26a957ebed","order_by":4,"name":"Atsushi Okuda","email":"","orcid":"","institution":"Hokkaido Daigaku","correspondingAuthor":false,"prefix":"","firstName":"Atsushi","middleName":"","lastName":"Okuda","suffix":""},{"id":319872125,"identity":"5d04b2a1-c341-42bc-845f-1d702ca3b731","order_by":5,"name":"Osamu Kishida","email":"","orcid":"https://orcid.org/0000-0002-2663-8155","institution":"Hokkaido Daigaku","correspondingAuthor":false,"prefix":"","firstName":"Osamu","middleName":"","lastName":"Kishida","suffix":""}],"badges":[],"createdAt":"2024-04-18 23:11:34","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4289981/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4289981/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":60713166,"identity":"c83d240f-cab4-4669-b850-b6e30ceac4e3","added_by":"auto","created_at":"2024-07-19 20:32:47","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":143666,"visible":true,"origin":"","legend":"\u003cp\u003ePhotograph of the masu salmon migrants with wounds. \u003cstrong\u003e(a)\u003c/strong\u003eBill-shaped predation-caused wound (i.e., bill-shaped scar inflicted from either the ventral or dorsal side of the fish); \u003cstrong\u003e(b)\u003c/strong\u003e tooth-shaped predation-caused wound (i.e., several scars inflicted from the front or the back of the body); \u003cstrong\u003e(c)\u003c/strong\u003enon-identified predation-caused wound (i.e., large areas of missing scales).\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-4289981/v1/f12f39440ebbd5d3dfccf76a.png"},{"id":60713168,"identity":"1c06ba81-bc58-4f88-8ca6-a07bf420a397","added_by":"auto","created_at":"2024-07-19 20:32:47","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":306137,"visible":true,"origin":"","legend":"\u003cp\u003eMap of the Horonai River. The Horonai River consists of three distinct reaches. Uppermost reach (6.9–12.2 km from the river mouth (black solid line) is the primary habitat of masu salmon residents and migrants before descending the river, where they have a nursery habitat. Middle reach (4.6–6.9 km from the river mouth) (blue solid line) is the river corridor of the migrants, where they pass by during river-descending. The migrant trap was installed at the midstream of Horonai River (place in which 5.7 km from the river mouth) (black dot) to capture river-descending migrants. Lowermost reach (4.6 km section from the river mouth) (blue break line) flows through the urbanized landscape of Tomakomai City and temporally serves as a river corridor. The map is based on the digital map published by the Geospatial Information Authority of Japan.\u003c/p\u003e","description":"","filename":"floatimage2.png","url":"https://assets-eu.researchsquare.com/files/rs-4289981/v1/344cf00a9c23df749f75256c.png"},{"id":60713167,"identity":"930b1ca5-43ba-4c30-9c85-d993d7a69492","added_by":"auto","created_at":"2024-07-19 20:32:47","extension":"jpeg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":487816,"visible":true,"origin":"","legend":"\u003cp\u003eRelationship between the relative growth rate, endpoint of pre-migration period and the frequency of predation-caused wound. Regression line was predicted by logistic regression (see Table 1 for estimates). The shaded area represents the 95 % confidence interval of the fitted regression. The second Y-axis shows the number of individuals with wound (y = 1) and without wound (y = 0). Frequency of predation-caused wound regardless of the causes in relation to \u003cstrong\u003e(a)\u003c/strong\u003e relative growth rate and \u003cstrong\u003e(b) \u003c/strong\u003eendpoint of pre-migration period (i.e., date of capture in migrant trap); Frequency of bill-shaped predation-caused wound in relation to \u003cstrong\u003e(c)\u003c/strong\u003e relative growth rate and \u003cstrong\u003e(d) \u003c/strong\u003eendpoint of pre-migration period;\u003cstrong\u003e \u003c/strong\u003eFrequency of tooth-shaped predation-caused wound in relation to \u003cstrong\u003e(e) \u003c/strong\u003erelative growth rate and \u003cstrong\u003e(f) \u003c/strong\u003eendpoint of pre-migration period\u003c/p\u003e","description":"","filename":"floatimage3.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-4289981/v1/9d9f4da0c7cb914094ad09a4.jpeg"},{"id":62538366,"identity":"917a8323-4ffa-452c-9f0a-42fbb4b5c8a8","added_by":"auto","created_at":"2024-08-15 14:18:40","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1436265,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4289981/v1/0058d22e-1128-462b-aac9-539cb786903a.pdf"},{"id":60713169,"identity":"234cb122-3862-48ff-ba9f-f3e0c6235ca8","added_by":"auto","created_at":"2024-07-19 20:32:47","extension":"docx","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":100714,"visible":true,"origin":"","legend":"","description":"","filename":"Predationwoundsubmissionsupplement.docx","url":"https://assets-eu.researchsquare.com/files/rs-4289981/v1/6fb90580667d3a556c1e109d.docx"}],"financialInterests":"","formattedTitle":"Costs of attaining larger size prior to migration inferred from predation-caused wounds in an anadromous fish","fulltext":[{"header":"Introduction","content":"\u003cp\u003eMany animals migrate to complete their life cycle (Dingle and Drake \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Alerstam and B\u0026auml;ckman \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Although they benefit substantially from migration, they also suffer high mortality during migration (Alerstam et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2003\u003c/span\u003e). Notably, smaller migratory individuals (migrants) suffer higher mortality during a risky migration trip (Sogard \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e1997\u003c/span\u003e; Alerstam et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Oppel et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Tucker et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Gregory et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Simmons et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Thus, attaining large size before migration is critical for successful migration (Roff \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e1991\u003c/span\u003e). This suggests that migrants should adopt growth tactics to attain sufficiently large size to survive the migration (i.e., size-threshold) once they have decided to migrate (Arendt \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e1997\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIndeed, previous research has documented potential growth tactics just prior to migration. For instance, smaller migrants exhibited higher growth rates and delayed migration (i.e., an extended pre-migration period) compared to their larger counterparts (Nicieza and Brana \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1993\u003c/span\u003e; Bohlin et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e1996\u003c/span\u003e; Dermond et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Futamura et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2022\u003c/span\u003ea). This combination of higher growth rates and extended pre-migration periods allow smaller migrants to achieve a greater size increment during the pre-migration period, enabling them to surpass a size threshold at the onset of migration. Given that smaller migrants face stronger ecological demands than larger ones, these size-dependent growth patterns can be interpreted as adaptive life history tactics. However, it is important to note that the adaptiveness of this growth pattern cannot be solely explained by the size-dependent ecological demands of growth placed on smaller migrants. If faster growth rates and longer pre-migration periods do not incur any cost, maximizing size increment before migration should be adaptive for migrants, regardless of body size. Therefore, to affirm the adaptive significance of the size-dependent growth pattern, it is necessary to understand the costs associated with faster growth and longer pre-migration periods. However, these potential costs remain largely unexplored. In this study, we addressed this knowledge gap by focusing on the trade-off between growth and survival (Stearns \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e1989\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe trade-off between growth and survival is characterized by a positive correlation between size increment and mortality, where individuals attempting to achieve a larger size increment are subject to a higher mortality risk (Stearns \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e1989\u003c/span\u003e, \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e1992\u003c/span\u003e; Mangel and Stamps \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2001\u003c/span\u003e). This growth-survival trade-off has been documented in previous studies that explored genetic and plastic variation in growth rates among individuals (Anholt and Werner \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Gotthard \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Munch and Conover \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Biro et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). One well-known cause of this trade-off is the increased predation risk associated with behaviors that individuals adopt to achieve a larger size increment (Houston et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e1993\u003c/span\u003e; Dmitriew and Rowe \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). Individuals need to either increase their foraging activity or time to achieve larger size increment, (Werner and Anholt \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e1993\u003c/span\u003e; Damsgird and Dill \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Willette \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2001\u003c/span\u003e), but these behaviors likely increase encounters with predators (Lima and Dill \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; Brown and Kotler \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Verdolin \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). In this study, we sought to evaluate whether the same processes operate during the pre-migration period of migrants. We examined whether migrants with a higher growth rate and longer growth period were subject to a higher predation risk before migration. This was done by investigating the frequency of wounds caused by predator attacks on masu salmon (\u003cem\u003eOncorhynchus masou\u003c/em\u003e) migrants.\u003c/p\u003e \u003cp\u003eMasu salmon, endemic to East Asia, commonly exhibit partial migration, with populations consisting of both river-dwelling residents and anadromous migrants (Kato \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e1991\u003c/span\u003e). Residents remain in the river throughout their lives (Nakano \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Sakata et al. \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). In contrast, migrants typically spend only the first 1\u0026ndash;2 years in the river, during which they mostly stay in a limited habitat area in the upstream of the river (nursery habitat). Subsequent to the stay in the nursery habitat, migrants descend the middle and lower reaches of the river (river corridor) towards the ocean in spring (i.e., between April and July) to begin oceanic migration (Kato \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e1991\u003c/span\u003e). After spending a year in the resource-rich but high-risk ocean, migrants return to their natal river to spawn (Morita \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Migrants, particularly smaller ones, face size-selective mortality during oceanic migration (Miyakoshi et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Shimoda et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Miyakoshi \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). Notably, we found size-dependent growth patterns among masu salmon migrants before oceanic migration, suggesting a growth tactic to avoid size-selective mortality during oceanic migration: smaller migrants had exhibited higher growth rates for half a year before they started oceanic migration and descended the river later than larger ones in the same seasons (Futamura et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2022\u003c/span\u003ea).\u003c/p\u003e \u003cp\u003eIn this study, we hypothesized that a faster growth rate and a longer pre-migration period of masu salmon would accompany mortality costs due to increased predation risk in the river. More interpretively, we considered that these costs would result in the size dependence of growth rates and pre-migration periods. Specifically, the smaller migrants would not survive the risky oceanic migration unless they attained larger sizes before migration. Therefore, they would accelerate growth rates and extend the pre-migration periods, even if these growth tactics are accompanied by potentially higher costs. In contrast, the larger migrants would not need to invest in additional size growth to prepare for risky oceanic migration and minimize these potential costs. Accordingly, we tested the following two predictions. First, masu salmon migrants that exhibited higher growth rates just before oceanic migration (i.e., period between early spring and start of oceanic migration) would be exposed to higher predation risk than those exhibiting lower growth rates. Second, masu salmon migrants that started oceanic migration later would be exposed to higher predation risk than those who started earlier. To test these predictions, we conducted a capture-mark-recapture survey of masu salmon migrants in the pre-migration period and examined the frequency of the wounds due to predator attacks (i.e., hereafter called predation-caused wounds) as a proxy for predation risk (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e1\u003c/span\u003e) (Reimchen \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1988\u003c/span\u003e, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e1992\u003c/span\u003e; Davies et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Polyakov et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e"},{"header":"Material and Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy system\u003c/h2\u003e \u003cp\u003eOur study was conducted in a 12.2 km long spring-fed River, Horonai River (42\u0026deg;40\u0026prime;N, 141\u0026deg;35\u0026prime;E) located in Hokkaido, northern Japan (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e2\u003c/span\u003e). This river is composed of three distinct reaches. The uppermost 5.3 km reach (6.9\u0026ndash;12.2 km from the river mouth) is characterized with natural riverbank and secondary deciduous forest. The uppermost reach is the primary habitat of masu salmon residents and migrants, where migrants have their nursery habitat before descending the river. In this reach, masu salmon have been marked with a PIT-tag (12.0 mm \u0026times; 2.12 mm, Oregon RFID, Inc) for an ongoing fish monitoring project since 2018. The middle river reach (4.6\u0026ndash;6.9 km from the river mouth) is slow-moving and includes artificial impoundments and wetlands totaling 1.0 ha and a maximum depth of 2.5 m. This reach serves as a river corridor, where river-descending masu salmon migrants pass through after leaving the nursery habitat in the uppermost reach. In the middle reach, piscivorous brown trout (\u003cem\u003eSalmo trutta\u003c/em\u003e) account for 70% of the fish (Futamura et al. \u003cem\u003eunpublished data\u003c/em\u003e) and water birds such as Great Egret (\u003cem\u003eArdea alba\u003c/em\u003e) and Common Merganser (\u003cem\u003eMergus merganser\u003c/em\u003e) are commonly observed (Futamura et al. \u003cem\u003epersonal observation\u003c/em\u003e). Since this reach largely consists of artificial impoundments and wetlands, it appears favorable for piscivorous birds, which mainly forage in open waters with sparce overhanging trees (Tojo \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e1996\u003c/span\u003e). The lowermost reach (the lowermost 4.6 km section from the river mouth) flows through the urbanized landscape of Tomakomai City and artificially straightened for flood control. This reach regularly harbors only few salmonids and temporally function as river corridor for masu salmon during the season of river-descending.\u003c/p\u003e \u003cp\u003e \u003cem\u003eCapture-mark-recapture survey of migrants before river descending.\u003c/em\u003e \u003c/p\u003e \u003cp\u003eWe conducted a capture-mark-recapture survey in the uppermost reach in spring 2020 (18\u0026ndash;26 Mar-2020). We collected masu salmon using a backpack electrofishing unit (300\u0026ndash;400 V DC, model 12B, Smith-Root, Inc., Vancouver, WA, USA) with 3 mm mesh dipnets (30 cm wide). Fish were anesthetized by diluted eugenol (FA-100 DS Pharma Animal Health Co., Ltd.) to measure their fork length (FL) (nearest 1 mm) and body mass (nearest 0.1 g) and to check for bodily wounds (see later). We also examined whether fish had been previously identified by a PIT tag using a handy PIT-tag reader. Individuals without the PIT tag\u0026thinsp;\u0026gt;\u0026thinsp;60 mm were tagged in this survey. The tag was inserted into the abdominal cavity through a small incision made with a clean scalpel. Fish were then allowed to recover from anesthesia and were released within 10 m of original capture. The number of masu salmon captured and identified by PIT tag was 1495 and individuals having predation-caused wounds was not found at this occasion.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eCapture survey on the river-descending migrants\u003c/h2\u003e \u003cp\u003eWe captured migrants at the onset of oceanic migration by installing a fyke-net type trap in the middle reach (5.7 km from the river mouth) from 04 Apr to 24 Jul, 2020 (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Captured fish were anesthetized using eugenol (FA-100 DS Pharma Animal Health Co., Ltd.), and were measured for fork length (nearest 1 mm) and body mass (nearest 0.1 g). We checked for visual signs of smoltification (i.e., silverly body coloration and black pigmentation on the tip of the dorsal fin) and then took a photograph. A waterproof digital camera (TG-5, Olympus Co., Tokyo, Japan) was used to take photographs and document predation-caused wounds. Then, fish were held in a bucket filled with fresh river water to allow recovery from anesthesia and were released to the pool habitat just downstream of the trap. Detailed information on the migrant trap survey is described in Futamura et al. (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2022\u003c/span\u003eb).\u003c/p\u003e \u003cp\u003eUsing the photographs taken in the migrant trap survey, we examined whether wounds were inflicted by predators (predation-caused wounds) or not (handling-caused wounds). Three categories of predation-caused wounds were identified based on their characteristics. First, bill-shaped scars inflicted from either the ventral or dorsal side were identified as avian wounds (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e1\u003c/span\u003ea) (Reimchen \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1988\u003c/span\u003e; Davies et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Kortan et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). Second, a series of tooth-shaped scars inflicted from the front or the back of the body were identified as those caused by piscivorous fish (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e1\u003c/span\u003eb) (Reimchen \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1988\u003c/span\u003e, \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e1991\u003c/span\u003e, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e1992\u003c/span\u003e). Third, we could not identify all scars were inflicted by either a bill or tooth, and they were recorded as non-identified predation-caused wounds. If migrant had either of the predation-caused wounds, we defined that migrant had a predation-caused wound. Other wounds, such as large areas of missing scales or single linear scar, were classified as handling-caused wounds (i.e., capturing the fish by migrant trap and measurement) (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e1\u003c/span\u003ec).\u003c/p\u003e \u003cp\u003eThe identification of the wound types based on the scar characteristics can be difficult because scar patterns are sometimes unclear. This raises the concern that our categorization of the wound type might be incorrect. However, this concern is not an issue, as the occurrence patterns of handling-caused and predation-caused wounds were inconsistent. Although we observed a positive relationship between the timing of migration start and the frequency of predation-caused wounds (see Result), the relationship between migration timing and the frequency of handling-caused wound was negative (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e) (Table. S2) (see Online Resource 1 for detail).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eDefinition of growth rate and pre-migration period\u003c/h2\u003e \u003cp\u003eTo test whether higher growth rates before migration and longer pre-migration periods incurred higher predation risk, we defined growth rate during the pre-migration period using the data obtained from the capture-mark-recapture survey in early spring and migrant trap survey. As a metric of growth rate, we used relative growth rate adjusted for body size, because growth rate and predation highly depend on body size (Lugert et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Relative growth rate was calculated from the residuals of the following linear model: ln (FL \u003csub\u003emigration\u003c/sub\u003e)\u0026thinsp;~\u0026thinsp;ln (FL \u003csub\u003eearly spring\u003c/sub\u003e) + Δ t, in which FL \u003csub\u003emigration\u003c/sub\u003e is the size at the migrant trap survey, FL \u003csub\u003eearly spring\u003c/sub\u003e is the size at early spring capture-mark-recapture survey and Δ t as elapsed dates between the two surveys. As a metric of the pre-migration period, we used the capture date at the migrant trap survey, which serves as an endpoint of the pre-migration period.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eTo assess the effects of relative growth rate and pre-migration period on the frequency of predation-caused wounds, we conducted our analysis in two procedures. First, we assessed the association between these variables and frequency of predation-caused wound regardless of their cause (i.e., bill-shaped, tooth-shaped, or not-identified). Then, we investigated the association between these variables and frequency of each type of predation-caused wounds (bill-shaped and tooth-shaped). The effect of relative growth rate and pre-migration period on predation-caused wounds were analyzed in separate models because of the sample size disparities (i.e., sample size for growth rate analysis is n\u0026thinsp;=\u0026thinsp;119, sample size for pre-migration period analysis is n\u0026thinsp;=\u0026thinsp;578). Growth period and relative growth rate were not significantly correlated with each other (Pearson\u0026rsquo;s r correlation, r = -0.03, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.780). For the growth rate analysis, generalized linear model (GLM) with a binominal distribution and logit-link function (i.e., logistic regression) was employed to examine whether the frequency of the predation-caused wound at the onset of migration was determined by relative growth rate in spring. Similarly, logistic regression was employed to examine whether the frequency of the predation-caused wound at the migrant trap was affected by the pre-migration period and fork length at migrant trap. Because the interaction term, pre-migration period \u0026times; fork length, did not improve the models in preliminary analyses, the interaction terms were dropped. Overall, we used six models on the analysis of the predation-caused wounds (i.e., three injury status [predation-caused wound regardless of cause, bill-shaped, and tooth-shaped] \u0026times; two growth mechanisms [growth rate and pre-migration period]). In all models, the significance of the independent variables was evaluated by likelihood ratio test which was performed by using the maximum likelihood method. All statistical analysis was performed using R ver. 4.3.1.\u003c/p\u003e \u003c/div\u003e"},{"header":"Result","content":"\u003cp\u003eA total of 578 masu salmon migrants were captured in the migrant trap from 14-Apr to 16-Jun 2020. Among these, 51 had a bill-shaped predation-caused wound, 24 had a tooth-shaped predation-caused wound, 31 had a non-identified predation-caused wound, 186 had a handling-caused wound, 1 had both bill-shaped predation-caused wound and handling-caused wounds, 4 had both bill-shaped and tooth-shaped predation-caused wounds, and 281 had no wound (unscathed) (Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). These 578 individuals were used for the analysis of the pre-migration period. Of migrants captured in the migrant trap survey, 119 had been previously captured in the early-spring capture-mark-recapture survey): 10 had a bill-shaped wound, 2 had a tooth-shaped wound, 7 had a non-identified predation-caused wound, 32 had a handling-caused wound, 1 had both bill-shaped predation-caused wound and handling-caused wounds, and 67 had no wound (Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). These 119 individuals were used for the analysis of the relative growth rate.\u003c/p\u003e \u003cp\u003eThe frequency of predation-caused wound, regardless of its cause, tended to increase with the relative growth rate, but was not significant (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;2.07, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.150) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003ea). The relative growth rate in spring was not significantly related to the frequency of bill-shaped predation-caused wound (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;0.30, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.586) or tooth-shaped predation-caused wound (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;1.19, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.276) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003ec; Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003ee).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eResults of the logistic regression model predicting frequency of predation-caused wound. Estimates of independent variables are shown on the logit scale.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eModel formulae\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIndependent variable\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eEstimates\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eStd. Error\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eχ\u003csup\u003e2\u003c/sup\u003e value\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"6\" nameend=\"c6\" namest=\"c1\"\u003e \u003cp\u003eFrequency of predation-caused wound (regardless of cause)\u0026thinsp;~\u0026thinsp;Intercept\u0026thinsp;+\u0026thinsp;Relative growth rate\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIntercept\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-1.64\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.25\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eRelative growth rate\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e9.71\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e6.94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e2.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.150\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"6\" nameend=\"c6\" namest=\"c1\"\u003e \u003cp\u003eFrequency of bill-shaped predation-caused wound\u0026thinsp;~\u0026thinsp;Intercept\u0026thinsp;+\u0026thinsp;Relative growth rate\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIntercept\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-2.30\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.32\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eRelative growth rate\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4.64\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e8.60\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.30\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.586\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"6\" nameend=\"c6\" namest=\"c1\"\u003e \u003cp\u003eFrequency of tooth-shaped predation-caused wound\u0026thinsp;~\u0026thinsp;Intercept\u0026thinsp;+\u0026thinsp;Relative growth rate\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIntercept\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-4.40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0.94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eRelative growth rate\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e22.94\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e22.41\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.276\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"6\" nameend=\"c6\" namest=\"c1\"\u003e \u003cp\u003eFrequency of predation-caused wound (regardless of cause)\u0026thinsp;~\u0026thinsp;Intercept\u0026thinsp;+\u0026thinsp;Pre-migration period\u0026thinsp;+\u0026thinsp;Fork length\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIntercept\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-9.66\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.07\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePre-migration period\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2.23 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e9.44 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;3\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.76\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.016\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFork length\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3.77 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.20 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e10.31\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"6\" nameend=\"c6\" namest=\"c1\"\u003e \u003cp\u003eFrequency of bill-shaped predation-caused wound\u0026thinsp;~\u0026thinsp;Intercept\u0026thinsp;+\u0026thinsp;Pre-migration period\u0026thinsp;+\u0026thinsp;Fork length\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIntercept\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-12.73\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.82\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePre-migration period\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4.44 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.33 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e12.13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFork length\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3.10 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.58 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e4.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.045\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"6\" nameend=\"c6\" namest=\"c1\"\u003e \u003cp\u003eFrequency of tooth-shaped predation-caused wound\u0026thinsp;~\u0026thinsp;Intercept\u0026thinsp;+\u0026thinsp;Pre-migration period\u0026thinsp;+\u0026thinsp;Fork length\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIntercept\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-6.40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e3.51\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003ePre-migration period\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e-1.42 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.62 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.77\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.381\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFork length\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4.02 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e2.14 \u0026times; 10\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e3.67\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.055\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eThe frequency of migrants with predation-caused wounds, regardless of its cause, significantly increased with the pre-migration period (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;5.76, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.016) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003eb) and with the fork length (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;10.31, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.001) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The frequency of migrants with bill-shaped predation-caused wound also significantly increased with the pre-migration period (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;12.13, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003ed) and with the fork length (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;4.02, P\u0026thinsp;=\u0026thinsp;0.045) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). However, the frequency of migrants with tooth-shaped wound was not significantly related with either the pre-migration period (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;0.77, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.381) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e3\u003c/span\u003ef) or the fork length (χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;3.67, \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.055) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eIn many migratory species, small individuals at a certain timing before migration tend to grow faster and start migrating later than large individuals, which allows the small ones to reach a larger size before they start migration (Nicieza and Brana \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1993\u003c/span\u003e; Bohlin et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e1996\u003c/span\u003e; Dermond et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Futamura et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2022\u003c/span\u003ea). While the potential costs of faster growth and delayed migration explain why migrants don\u0026rsquo;t all maximize these size-increment factors, these costs have not been directly investigated. This study, using masu salmon migrants, tested the hypotheses that faster growth and delayed migration start increase predation risk for migrants in the pre-migration period. Our result could not support the hypothesis that faster growth in the pre-migration period caused greater predation risk. To the contrary, timing of migration start (i.e., date of capture at migrant trap) was significantly associated with the frequency of wounds. In particular, although the timing of migration start did not explain the frequency of the tooth-shaped wound, probability of inflicting bill-shaped predation-caused wound was higher in migrants with delayed migration start. These results suggest that masu salmon migrants that initiated oceanic migration later were exposed to higher predation risk mainly by the avian predators before migration. This implies that smaller migrants stayed longer in the river to attain a large size for surviving the oceanic migration despite the increased predation risk in the river. In contrast, larger migrants opted to leave the river sooner and avoided the predation risk.\u003c/p\u003e \u003cp\u003eAs the frequency of predation-caused wounds in migrants increased over time, it is possible that the higher probability of inflicting predation-caused wounds with late migration start is simply due to the later timing of the wound assessment (i.e., the day of capture in the migrant trap). However, this is unlikely to be a problem for our conclusion. This is because all migrants, regardless of when they were captured at the migrant trap, must pass through the high predation risk areas such as the lower reaches of the river, estuaries and coastal areas (Welch et al. \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Clark et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Moore et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). If all migrants are exposed to at least the same degree of predation risk during the passage through such risky areas, regardless of the timing, migrants that initiate migration later experience higher predation risk as a whole. In this case, our conclusion that migrants with predator wounds at the time of capture are exposed to a higher predation risk before the start of oceanic migration remains valid.\u003c/p\u003e \u003cp\u003eOur study revealed increased predation on migrants with longer pre-migration periods, particularly from piscivorous birds. This raises a further question: where and how do these migrants encounter this heightened predation risk before their journey? There are two potential hotspots for increased predation before migration: the uppermost reach where migrants spend until start of river-descending as a nursery habitat, and the middle reach which serve as a river corridor during descending the river. A survey of masu salmon residents, which was held right after the river-descending season of migrants (25\u0026ndash;26 Jun-2020), indicates the former hypothesis is unlikely. In the survey, the residents remaining in the migrants\u0026rsquo; nursery habitat (the uppermost river reach) exhibited no predation-caused wounds (i.e., total 509 residents had no predation-caused wounds) (Futamura et al., \u003cem\u003eunpublished data\u003c/em\u003e). This strongly suggests that migrants were facing increased predation risk while descending the river. This aligns with our frequent observations of piscivorous birds in the middle reaches of the Horonai River, lending support to the hypothesis. Notably, Great Egrets (\u003cem\u003eArdea alba\u003c/em\u003e) and Common Mergansers (\u003cem\u003eMergus merganser\u003c/em\u003e), rarely seen in the uppermost reach, were regularly present in the middle reach during the river-descending season of migrants (Futamura et al., \u003cem\u003epersonal observation\u003c/em\u003e).\u003c/p\u003e \u003cp\u003eIn general, individuals with faster growth are more vulnerable to predation because active foraging to support faster grow also makes them more likely to be detected or encountered by predators (Lima and Dill \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; Brown and Kotler \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Verdolin \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). However, in our present study, we did not find statistically significant evidence of predation-related costs in migrants with higher growth rates. This does not necessarily mean that there are no costs associated with rapid growth before migration. While we focused on increased predation risk as a potential fitness cost of faster growth, other costs are also worth considering. For example, higher growth rates may incur physiological costs such as increased metabolic costs and impaired immune function (Stoks et al. \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Van Der Most et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). It is important to explore these potential long-term costs to fully understand the costs associated with rapid growth before migration.\u003c/p\u003e \u003cp\u003eSmaller individuals typically face heavier predation pressure (Sogard \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e1997\u003c/span\u003e; Van Kooten et al. \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Takatsu et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Stige et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), and this holds true similarly for migrating species (Alerstam et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Oppel et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Gregory et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Simmons et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). In fact, our previous study provided evidence of such size-selective mortality in masu salmon migrants while descending the lower reaches (river corridor) of Horonai River (Futamura et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2022\u003c/span\u003eb). However, our results contradicted this general pattern. Larger migrants showed a higher frequency of predation-caused wounds (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). This pattern mirrors a similar finding in a previous study on predation-caused wounds of three-spine stickleback (\u003cem\u003eGasterosteus aculeatus\u003c/em\u003e) (Reimchen \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1988\u003c/span\u003e). This seemingly paradoxical result may be explained by predator handling abilities. While piscivorous birds and fish can attack and capture prey across a wide size range, their ability to consume certain larger prey is limited by their gape size (\u0026ldquo;gape-limited\u0026rdquo;) (Moser \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e1986\u003c/span\u003e; Hambright \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e1991\u003c/span\u003e). Additionally, even with prey smaller than their gape, predators require time to handle and swallow them (Draulans \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e1987\u003c/span\u003e). This extended handling time provides larger migrants with a heightened chance of escape, even after initial capture. Consequently, larger migrants may inflict more predation-caused wounds due to these attempted attacks\u003c/p\u003e \u003cp\u003eOur findings demonstrated that extending the pre-migration period incurs a fitness cost in the form of increased predation risk. However, this might not preclude the possibility that other mechanisms operate as costs of an extended pre-migration period. For example, a delay in the departure of migration likely results in decreased benefits of oceanic migration, because longer pre-migration period also translates to a shorter oceanic migration period and might miss the optimal timing of migration. During oceanic migration, salmonids can significantly increase their size by consuming abundant prey, which ultimately benefits reproduction (Gross et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1988\u003c/span\u003e; Maekawa and Nakano \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2002\u003c/span\u003e) and the timing of migration affect the ocean survival (Jonsson and Jonsson \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Iida et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Thus, to maximize resource gains, starting oceanic migration early can be crucial. Therefore, investigating such potential trade-off between oceanic growth and early departure, alongside predation costs, in masu salmon and other migratory species would be valuable in advancing our understanding of the factors that shape condition-dependent migration departure.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eACKNOWLEDGEMENTS\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe thank Yuichi Matsuoka, Shoji Kumikawa, Hiroshi Sugiyama, Hiroyuki Takahashi, Susumu Igarashi, Tomoaki Sato, Yuto Sasaki for their support in fieldwork.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis work was supported by a JSPS KAKENHI grant to RF (22KJ0078) and OK (20K21439 and 22H02694).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflicts of interest\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no conflict of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eOur work conforms to the guidelines for the proper conduct of animal experiments in Japan\u0026nbsp;and was approved by the committee for animal experiments in FSC of Hokkaido University (ID 2‐6).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and material\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll of the data analyzed in this study is deposited in Figshare (10.6084/m9.figshare.25638036).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCode availability\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll of the R scripts is deposited in Figshare (10.6084/m9.figshare.25638036).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor contribution statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eRF, KM, YK and OK conceived the ideas. All authors designed the methodology and collected the data. RF and OK analyzed the data and led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAlerstam T, B\u0026auml;ckman J (2018) Ecology of animal migration. Curr Biol 28:R968\u0026ndash;R972. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1016/j.cub.2018.04.043\u003c/span\u003e\u003cspan address=\"10.1016/j.cub.2018.04.043\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAlerstam T, Hedenstrom A, Akesson S (2003) Long-distance migration: evolution and determinants. 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Fish Oceanogr 10:110\u0026ndash;131. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1046/j.1054-6006.2001.00042.x\u003c/span\u003e\u003cspan address=\"10.1046/j.1054-6006.2001.00042.x\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"trade-off, growth, predation, life-history, salmonids","lastPublishedDoi":"10.21203/rs.3.rs-4289981/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4289981/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eSurvival during migration typically depends on body size, in which smaller migrants suffer higher mortality. Thus, migratory animals are predicted to adopt growth tactics to attain large size before migration. Size-dependent growth patterns represent such a case, in which smaller migrants exhibit rapid growth and delay start of migration (extended pre-migration period) to attain a large body size to survive migration. To evaluate adaptiveness of such size-dependent growth patterns, it is crucial to understand costs associated with rapid growth and delayed migration start, since the adaptiveness of the size-dependent growth patterns cannot be solely explained by ecological demands of rapid growth and late migration start. However, potential costs remain largely unknown. Here, we focused on the trade-off between growth and survival, and investigated whether faster pre-migration growth rates and longer pre-migration periods incurred higher predation risk in masu salmon (\u003cem\u003eOncorhynchus masou\u003c/em\u003e), which exhibit size-dependent growth patterns. In a capture-mark-recapture survey examining predation-caused wounds as a proxy for predation risk, we found a non-significant effect of growth rate but a significantly positive effect of timing of migration initiation on the frequency of predation-caused wounds. In particular, migrants that stayed longer in the river had higher probabilities of having predation-caused wounds, especially inflicted by piscivorous birds. This implies that smaller migrants extend their stay in the river to attain larger size for surviving oceanic migration, although the extended stay in the river is costly in terms of increased predation risk.\u003c/p\u003e","manuscriptTitle":"Costs of attaining larger size prior to migration inferred from predation-caused wounds in an anadromous fish","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-07-19 20:32:42","doi":"10.21203/rs.3.rs-4289981/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"63534fae-c1f5-454d-b10e-6aa8d6166997","owner":[],"postedDate":"July 19th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-08-15T14:10:32+00:00","versionOfRecord":[],"versionCreatedAt":"2024-07-19 20:32:42","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4289981","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4289981","identity":"rs-4289981","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}