Cortisol profiles in sockeye salmon: Sample bias and baseline values at migration, maturation, spawning, and senescence

Fisheries Research 154 (2014) 38–43

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Cortisol profiles in sockeye salmon: Sample bias and baseline values at migration, maturation, spawning, and senescence M.R. Baker a,∗ , C.H. Vynne b a b

School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA 98195, USA National Fish and Wildlife Foundation, 1133 Fifteenth Street, N.W. Suite 1100, Washington, DC 20005, USA

a r t i c l e

i n f o

Article history: Received 17 January 2013 Received in revised form 13 January 2014 Accepted 22 January 2014 Available online 6 March 2014 Keywords: Pacific salmon Sampling bias Stress Cortisol Reproductive maturation

a b s t r a c t Accurate and controlled methods to measure physiological stress are crucial to effectively monitor and assess the health of wildlife populations and evaluate resilience to external stressors. Glucocorticoids, particularly cortisol, are frequently used to measure stress in fish. While measurements of cortisol concentrations provide a powerful indicator of physiological stress, there are important considerations in accurately measuring and interpreting results. We assessed methods to capture and sample wild populations of salmonids and evaluated potential biases from sampling disturbance. We present results of a stress series and suggest approaches to mitigate bias associated with sampling disturbance. Studies on physiological stress in salmonids often focus on particular life stages (e.g. outward migration to marine waters, return migration to freshwater systems), or processes (e.g. fisheries interactions, spawning success), characterized by dramatic physiological challenges related to the developmental stage of the fish and the external environment. Such pressures influence baseline cortisol levels and complicate efforts to interpret the effects of additional external stressors. We present a profile for naturally occurring shifts in cortisol levels at migration, reproductive maturation, spawning, and senescence. This profile provides a crucial baseline for use as reference in evaluating physiological stress in Pacific salmon during crucial life stages. Our findings provide guidance for sampling wild salmonids and highlight the need for caution in interpreting cortisol in the context of physical challenges and physiological developments relevant to their complex life history. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Despite extensive research on physiological stress in captive stocks of salmonids, relatively few studies have analyzed stress in wild stocks, due to difficulty sampling and controlling environmental effects. Extensive natural and anthropogenic stressors challenge wild salmon populations, including interactions with commercial and recreational fisheries, physical impediments to migration, pollutants, habitat loss, natural shifts in habitat and conditions, oscillations and variability in climate, and anthropogenic climate change. Throughout much of their historical range, salmon populations are listed as threatened or endangered (Ford et al., 2010). Means to accurately measure and effectively interpret blood chemistry to assess effects of stressors have direct utility toward effective management and monitoring of salmon populations

∗ Corresponding author. Current address: Joint Institute for the Study of the Atmosphere and Ocean, University of Washington, Resource Ecology and Fisheries Management Division, Alaska Fisheries Science Center, NOAA Fisheries, 7600 Sand Point Way NE, Building 4, Seattle, WA 98115, USA. Tel.: +1 206 794 7515. E-mail addresses: [email protected], [email protected] (M.R. Baker), [email protected] (C.H. Vynne). 0165-7836/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fishres.2014.01.015

(Cooke et al., 2012). We evaluate methods for capture and extraction of blood from wild fish, while minimizing sampling bias. We also provide baseline values for cortisol concentrations in sockeye salmon (Oncorhynchus nerka) at various stages of reproductive maturity to inform analyses of external stressors in the context of migration, reproductive maturation, spawning, and senescence. Whether anthropogenic or naturally occurring, external stressors may have profound implications for the health and dynamics of fish stocks and the persistence, conservation, rebuilding, and management of wild populations (Pankhurst and Van Der Kraak, 1997). Both acute (Maule and VanderKooi, 1999) and chronic (Pickering and Pottinger, 1989) stressors have been shown to have detrimental effects on fish. Physiological stress may alter behavior (Schreck et al., 1997; Wingfield and Ramenofsky, 1999), lower immune responses (Balm, 1997; Maule et al., 1989), increase metabolic costs (Pankhurst and Van Der Kraak, 1997), and impair responses to physical challenges (Davis, 2006). Physiological stress may also inhibit sexual maturation (Carragher et al., 1989; Baker et al., 2013a) and reproductive function (reviewed in Pankhurst and Van Der Kraak, 1997; Schreck, 2010). Repeated exposure to acute stressors and prolonged exposure to chronic stressors disrupt endocrine processes (Sumpter et al., 1987) and may decrease gamete quality

M.R. Baker, C.H. Vynne / Fisheries Research 154 (2014) 38–43

and reduce larval viability (Campbell et al., 1992; Kubokawa et al., 1999). Cortisol is the major corticosteroid in salmonids (Billard and Gillet, 1981; Donaldson, 1981). The circulating level of cortisol is commonly used as an indicator of stress (Barton and Iwama, 1991; Wendelaar Bonga, 1997; Davis, 2010; Raby et al., 2012). Plasma level increases in cortisol are positively correlated with stress and do not reflect diurnal rhythms (Fagerlund et al., 1995). Cortisol therefore serves as a sensitive indicator of the severity of particular stressors. Yet caution is warranted in interpreting plasma cortisol concentrations as a metric for stress and condition in the context of secondary physiological processes and environmental challenges (Baker et al., 2013b). Many external stressors impact Pacific salmon at the juvenile stage, when fish migrate from freshwater to the ocean as smolts, or at the adult stage, when mature fish return to freshwater to spawn. Both life stages are also characterized by complex physiological processes that complicate interpretation of blood chemistry assays (Donaldson and Fagerlund, 1968; Mesa et al., 1998). At migration and spawning, salmon are subject to environmental stressors related to their transition from salt to fresh water habitat, the physical demands of migration, gonadal development, sexual maturation, competition for territory and mates, and the onset of senescence (Robertson and Wexler, 1960). Adult salmonids demonstrate sustained increases in cortisol in association with migration and sexual maturation (e.g. McBride et al., 1986; Carruth et al., 2000). In the case of extreme migrations, corticosteroid levels parallel those associated with chronic stress (Fagerlund, 1967; Fagerlund et al., 1995). Differentiating between natural and anthropogenic stressors and understanding the consequences of additional stressors at these critical life stages is imperative to effective approaches to restoration and sustainable management. 1.1. Purpose and approach We investigated the following research questions: (1) what is an appropriate protocol to measure baseline levels of cortisol, given challenges to sampling wild populations in the field; (2) what are baseline levels of cortisol during the crucial stages of migration, reproductive maturation, spawning, and senescence. The former provides guidance to unbiased sampling of cortisol in wild Pacific salmon. The later provides a baseline for cortisol during migration and spawning and informs our understanding of external stressors in the context of complex physiological processes that occur at this life stage. 2. Material and methods 2.1. Cortisol assays Cortisol concentrations in blood plasma were measured using a double antibody radioimmunoassay kit (DSL-2000) from Diagnostic System Laboratories, Inc., Webster, TX. Dilutions of plasma produced a curve parallel to the standard curve. Inter-assay variation was 6.4%. Intra-assay variation was 2.7%.

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Fish were sampled in-river or at the spawning stream (Fig. 1), using a beach seine. Fish were transferred to the lethal anesthetic bath until respiratory failure, and extracted when motionless. Blood was collected from the caudal vasculature into heparinized tubes. Clark et al. (2011) recently demonstrated that cortisol levels are not affected by lethal procedures (i.e. live versus recently sacrificed salmon) nor method of blood extraction (i.e. caudal puncture versus cannulated procedures). Blood samples were maintained on ice and, within hours, plasma was separated by centrifugation (1200–1500 rpm), transferred to 1.5 mL Eppendorf microcentrifuge vials, and stored at −80 ◦ C until analyzed.

2.3. Sampling protocol for analyses of sampling bias (stress series) To determine potential bias from sampling disturbance, sockeye salmon were sampled from a common school aggregated at the mouth of a spawning stream (Pick Creek, 59◦ 33 02.40 N, 159◦ 03 51.21 W). Sampling disturbance included the time from the initiation of the beach seine set to collection of the blood sample. All fish were sampled in a common set, but spent different amounts of time awaiting removal to lethal anesthesia bath, biopsy, and termination. Blood samples were collected at 2, 5, 10, and 20 min. Equal numbers of males and females were sampled at each interval.

2.4. Sampling protocol for analyses of cortisol at reproductive stages To better understand cortisol levels in the context of reproductive maturation and spawning, we sampled sockeye salmon at multiple maturation stages. Fish were sampled at: (i) in-river migration (early-stage maturation, males and females n = 42); at the mouth of spawning stream (late-stage maturation, males and females n = 44); and in-stream (mature, spawning, and senescent stages, females only n = 82). Mean sampling time (initial disturbance until deposition in a lethal anesthetic bath) was 5.92 ± 1.79 (SD) min for in-river sampling (immature migrating stage) and 7.1 ± 1.4 min at the mouths of spawning streams (maturing stage). In-stream sampling (mature, spawning, senescent stages) occurred in <2 min.

2.5. Assessing maturation via coloration and egg development To interpret the relationship between cortisol and reproductive maturation, we also assessed coloration in fish, which is related to the release of androgens (Idler et al., 1961). At maturity, sockeye salmon exhibit differential coloration from the immature ocean phase (Fig. 1), flushing carotenoid and lipophilic pigments from muscle to skin, shifting from silver coloration to deep red (Smirnov, 1958; Idler et al., 1961); Skin also thickens and scales are resorbed (Burgner, 1991). Fish were categorized by color and scale absorption (silver = none, blush = partial, red = complete). All females were also dissected to determine reproductive phase and egg development (Fig. 2).

2.2. General sampling protocol Staging equipment was prepared and processing stations established prior to initiation of each sampling sequence. Heparin ammonium salt (Sigma–Aldrich, 5000 IU mL−1 ), an anticoagulant was applied to 15 ml sample collection tubes (150 ␮L heparin solution). Anesthetic baths of tricaine methanesulfonate (MS222, 300 mg L−1 ) buffered with sodium bicarbonate (NaHCO3 , 500 mg L−1 ) were designed to induce rapid anesthesia but maintain vital functions until blood was collected.

3. Theory To investigate sampling disturbance on plasma cortisol in wild salmon, we conducted a stress series to quantify sampling bias and determine time intervals that avoid bias. To develop baseline physiological profiles informative to analyses of external stressors at migration, maturation, spawning or senescence, we characterized cortisol levels at these stages in Bristol Bay, Alaska sockeye salmon.

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M.R. Baker, C.H. Vynne / Fisheries Research 154 (2014) 38–43

Fig. 1. Location of sampling at river (Wood River 59◦ 15 11 N 158◦ 34 32 W, bottom figure) and spawning stream (Pick Creek 59◦ 33 00 N 159◦ 04 18 W, top figure) in Bristol Bay, Alaska.

4. Results and discussion 4.1. Effects of sampling protocol on plasma cortisol levels analyzed via implementation of stress series Due to latency in the corticosteroid response to an acute stressor, it is possible to measure baseline levels within a narrow timeframe of initial disturbance (Wedemeyer et al., 1990; Gamperl et al., 1994). Mean response latency in a measurable increase in plasma cortisol in teleost fishes is 12.5 min (reviewed in Pankhurst, 2011) and has been estimated at 15 (Fagerlund, 1967) or 20 min (Kubokawa et al., 2001); recovery to resting levels occurs within 6 h of the cessation of the stressor for most species (reviewed in Pankhurst, 2011). Resting levels of cortisol for Pacific salmon not under duress range 0–25 ng ml−1 (Fagerlund, 1967; McBride et al., 1986; Pickering and Pottinger, 1989). In our analysis, baseline rates of plasma cortisol at 2 min from disturbance (minimum time required to sample fish at spawning streams) were 7.7 ± 1.3 (SE, ng ml−1 ). Relative to this baseline, plasma cortisol rates increased slightly at five (20.4 ± 4.1 ng ml−1 ) and ten

Fig. 2. Sockeye salmon (Oncorhynchus nerka) at in-river migration (early-stage maturation, left) and spawning stream (late-stage maturation and spawning, right). At migration sockeye salmon remain largely silver with prominent scales, but at maturation, resorb their scales and flush red; at senescence color fades and tail fins appear worn.

(22.2 ± 5.3 ng ml−1 ) min after disturbance but remained within the range of reported baseline resting levels (0–25 ng ml−1 ) (Fagerlund, 1967; McBride et al., 1986; Pickering and Pottinger, 1989). Cortisol levels further increased at 20 min (40.0 ± 5.3 ng ml−1 ) (Fig. 3). Significant differences were observed across time intervals (ANOVA, F3,23 = 9.89, P < 0.000). Tukey HSD post hoc tests determined significant differences (P < 0.036) at 20 min, but not in sampling intervals < 10 min. Our results suggest sampling disturbance precipitated increases in cortisol levels almost immediately, but with a pronounced delay in the magnitude of that increase. Thus a tightly controlled sampling routine within a narrow timeframe of initial disturbance will allow the measurement of baseline levels. Further analyses should examine the elevation of cortisol <10 min from disturbance. 4.2. Cortisol levels according to sex In agreement with other studies of maturing Pacific salmon (Donaldson and Fagerlund, 1968; 1970), we found plasma cortisol levels in females to be elevated relative to males. Specifically, differences were noted between sexes at spawning streams (ttest, t20 = 6.4, P < 0.000), such that females were elevated 500% relative to males. As a result all subsequent analyses of cortisol were conducted separately for each sex. Previous studies have shown 17␤-estradiol enhances while testosterone and 11ketotestosterone suppress the cortisol response to a stressor (Sumpter et al., 1987; Pottinger et al., 1996; Pottinger and Carruck, 2000). In general, females exhibit a greater corticosteroid response than males (McBride et al., 1986) but at maturity appear less sensitive to acute stressors (Mazeaud et al., 1977; Kubokawa et al., 2001). This may be due to the role of cortisol in final oocyte maturation, ovulation (Jalabert, 1976) and spawning (Bry, 1985). In sockeye salmon the dynamics and magnitude of the corticosteroid response to stress are influenced by sexual maturity and sex-specific

M.R. Baker, C.H. Vynne / Fisheries Research 154 (2014) 38–43

Females

Males

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0 0

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Time from Initial Disturbance (min) Fig. 3. Results (mean ± SE) of a stress series conducted on sockeye salmon (Oncorhynchus nerka) to determine time frames in which samples might be collected without incurring bias related to sampling disturbance. Sampling disturbance was defined as the duration of time from initial disturbance until termination via lethal anesthesia and collection of sample for analysis of blood plasma cortisol. Sample sizes (N = 6) were consistent across groups. Significant differences (*) were noted at 20 min (Tukey HSD post hoc test, P < 0.036).

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0

modulation of stress responsiveness (Fagerlund and Donaldson, 1969; Donaldson and Fagerlund, 1970). Gonadal steroids have been associated with maturity-related modulation of stress responsiveness. Previous studies have shown 17␤-estradiol-17 (E2) enhances while testosterone and 11-ketotestosterone suppress the cortisol response to a stressor (Sumpter et al., 1987; Pottinger et al., 1996).

4.3. Cortisol and reproductive stage: profile in migrating, maturing, spawning and senescent salmon Sexual maturation in salmonids is associated with variety of morphological, physiological and behavioral changes influenced by the release of gonadal steroids (Idler et al., 1961; Pottinger et al., 1996). Past research suggests plasma cortisol at maturation may reach levels comparable to those measured during periods of chronic stress (Hane et al., 1966; Fagerlund, 1967). Other analyses of Pacific salmon have documented cortisol to increase at freshwater entry and peak at or immediately following spawning, with progressive increases from maturing to spawning and senescent fish (Schmidt and Idler, 1962; Fagerlund, 1967; Donaldson and Fagerlund, 1968). Our results corroborate these findings. Low levels were noted at migration, rising at maturation, spawning and senescence. Significant differences were noted (ANOVA, F4,124 = 26.7, P < 0.000) between all stages (Tukey HST post hoc P < 0.016) except maturing at stream mouth and instream (Fig. 4). Our cortisol profile across maturation stages closely matched other studies in this system (Carlson, S. unpublished data), but differed from studies of landlocked sockeye salmon, which showed only minor variation between stages (Carruth et al., 2000). Our results also differed from sockeye salmon challenged by strenuous migrations, which had pronounced increases in cortisol levels at migration (Fagerlund, 1967; Donaldson and Fagerlund, 1972). In all studies, however, plasma cortisol levels were similar at maturing (10–53 ng ml−1 ), spawning (50–200 ng ml−1 ), and senescent (200–600 ng ml−1 ) stages.

Ma

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Fig. 4. Profiles of plasma cortisol concentrations for sockeye salmon (Oncorhynchus nerka) at migration, maturation (eggs partially or entirely retained within the skein), spawning (established red sites with eggs loose in body cavity), and senescence (worn tail and fine, <100 eggs in body cavity) in females (N = 19–37) and at migration, and maturation in males (N = 14–25). Box plot boxes contain the first and third quartiles of the data; the line within the box denotes the median and whiskers contain the 5th and 95th percentiles. Significant differences in the mean are indicated by asterix on x-axis labels.

4.4. Cortisol and sexual maturation: interpreting cortisol response in context of salmon life histories Analyses of salmon at transitional stages must account for naturally occurring shifts in cortisol profiles. Adult salmonids exhibit a sustained increase in cortisol levels in association with sexual maturation and riverine migration (e.g. McBride et al., 1986; Carruth et al., 2000; Westring et al., 2008). In our analysis, cortisol levels increased in correlation with shifts in coloration and scale resorption, both processes associated with sexual maturation (ANOVA, F2,81 = 55.1, P = 0.001, Fig. 5). Tukey HSD post hoc tests determined significant differences between red and silver/blush females (P = 0.001) and differences between silver and red males (P = 0.003). As fish complete sexual maturation, responsiveness to external stressors diminishes (Hane et al., 1966), due to an attenuated corticosteroid stress response (Fagerlund and Donaldson, 1969; Kubokawa et al., 1999, 2001) and increased metabolic clearance of cortisol (Donaldson and Fagerlund, 1972; Sumpter et al., 1987; Dickhoff, 1989). Also, during in-river migration, salmon are subject to increased predation, anthropogenic challenges, thermal stress (Crossin et al., 2008; Cooke et al., 2012) and pathogen exposure (Donaldson and Fagerlund, 1968; Mesa et al., 1999). These have important implications for the utility of cortisol as a measure of external stressors at late-stage maturation in Pacific salmon.

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M.R. Baker, C.H. Vynne / Fisheries Research 154 (2014) 38–43

70

*

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Blood Plasma Cortisol (ng mL )

60

50

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* 10

* 0 Silver

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Fig. 5. Cortisol and coloration: Cortisol levels in fish at both migration (in-river) and late-stage maturation (stream mouth) stages combined (males, dark bars; females, light bars). Cortisol levels increase in accordance with coloration associated with reproductive maturity, suggesting that the use of cortisol as a metric for chronic stressors is complicated by maturation processes; mean ± SE (ng mL−1 ).

4.5. Summary Our results are intended to serve as a guide in sampling populations of wild salmonids for physiological stress and to mitigate biases in analyses of plasma cortisol related to sampling disturbance. We also present a profile for naturally occurring shifts in cortisol levels at migration, reproductive maturation, spawning, and senescence and highlight important considerations in measuring and interpreting cortisol as indicator of physiological stress. While the magnitude and duration of the cortisol response varies with species (reviewed in Barton, 2002), population (Pottinger and Moran, 1993), and environmental conditions (Pickering and Pottinger, 1983), this profile provides an informative baseline for use as reference in evaluating external stressors to Pacific salmon during migration and spawning. We expect these results will inform efforts to evaluate effects of natural and anthropogenic stressors at these crucial life stages and support effective monitoring and sustainable management of Pacific salmon populations. Acknowledgments We gratefully acknowledge D.E. Schindler for supporting analyses in the field and assisting with study design and implementation. We thank S. Wasser, K. Forsgren, G. Young, and P. Swanson for consultation and D. DeAvila for laboratory analysis. We also thank G. Holtgrieve, C. Ruff, L. Rogers, P. Lisi, A. Hilborn, J. Armstrong, S. Kroitz, G. Young, J. Bennis, K. Bentley, C. Boatright, J. Carter, D. Dougherty, M. Haraldsson, C. Gowell, J. Mudra, A. Paulsen, and T. Reed for assistance in collecting and processing samples. Financial support for this research was provided by the Gordon and Betty Moore Foundation, the National Science Foundation Biocomplexity Program, and the School of Aquatic and Fishery Sciences. References Baker, M.R., Swanson, P., Young, G., 2013a. Injuries from non-retention in gillnet fisheries suppress reproductive maturation in escaped stocks. PLoS One 8, e69615, http://dx.doi.org/10.1371/journal.pone.0069615.

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