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All about my mother: the complexities of maternally derived chemical signatures in otoliths.

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Connecting maternal migratory behavior with the behavior and ecology of their progeny can reveal important details in the ecology of a population. One method for linking maternal migration to early juvenile life-history is through maternal chemistry recorded in otoliths. Despite the wide use of maternal signatures to infer anadromy, the duration and dynamics of maternal otolith signatures are not well understood. Shifts in the elemental ratios and strontium isotope (87Sr/86Sr) chemistry in otoliths from juvenile Chinook salmon (Oncorhynchus tshawytscha) correlate with the timing of hatch and emergence respectively, indicating a chemical marker of these ontological stages. Additionally, analysis of maternal signatures show that maternally derived 87Sr/86Sr may be influenced by equilibration of the mother to freshwater, and in some cases the 87Sr/86Sr signatures of the eggs can shift significantly after being laid. These results provide guidance in separating maternal and juvenile signatures as researchers increasingly target early juvenile otolith chemistry. These results also caution against the use of 87Sr/86Sr alone as a marker of anadromy in populations with significant inland migrations.
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What did you say about my mother? The complexities of
maternally derived chemical signatures in otoliths.
Journal:
Canadian Journal of Fisheries and Aquatic Sciences
Manuscript ID
cjfas-2017-0341.R1
Manuscript Type:
Article
Date Submitted by the Author:
23-Mar-2018
Complete List of Authors:
Hegg, Jens; University of Idaho, Fish & Wildlife Sciences
Kennedy, Brian; University of Idaho,
Chittaro, Paul; National Marine Fisheries Service - NOAA
Is the invited manuscript for
consideration in a Special
Issue? :
N/A
Keyword:
MATERNAL EFFECTS < General, OTOLITHS < General, BIOGEOCHEMISTRY
< General, MIGRATION < General, SALMON < Organisms
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What did you say about my mother? The
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complexities of maternally derived
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chemical signatures in otoliths.
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Jens C. Hegg1*, Brian P. Kennedy1,2,3, Paul Chittaro4
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*jhegg@uidaho.edu
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1 Department of Fish & Wildlife Resources, 975 W. 6th Street, University of Idaho, Moscow, ID
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83844
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2 Department of Biology, Life Sciences South 252, University of Idaho, Moscow, ID 83844
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3 Department of Geology, McClure Hall 203, University of Idaho, Moscow, ID 83844
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4 National Oceanic and Atmospheric Administration, Northwest Fisheries Science Center, 2725
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Montlake Boulevard East, Seattle WA 98112
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Abstract
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Connecting maternal migratory behavior with the behavior and ecology of their progeny can
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reveal important details in the ecology of a population. One method for linking maternal
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migration to early juvenile life-history is through maternal chemistry recorded in otoliths.
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Despite the wide use of maternal signatures to infer anadromy, the duration and dynamics of
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maternal otolith signatures are not well understood. Shifts in the elemental ratios and strontium
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isotope (87Sr/86Sr) chemistry in otoliths from juvenile Chinook salmon (Oncorhynchus
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tshawytscha) correlate with the timing of hatch and emergence respectively, indicating a
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chemical marker of these ontological stages. Additionally, analysis of maternal signatures show
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that maternally derived 87Sr/86Sr may be influenced by equilibration of the mother to freshwater,
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and in some cases the 87Sr/86Sr signatures of the eggs can shift significantly after being laid.
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These results provide guidance in separating maternal and juvenile signatures as researchers
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increasingly target early juvenile otolith chemistry. These results also caution against the use of
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87Sr/86Sr alone as a marker of anadromy in populations with significant inland migrations.
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Introduction
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In many fish species migration is a facultative strategy, often encompassing various degrees of
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partial migration (Tsukamoto and Arai 2001, Secor and Kerr 2009, Chapman et al. 2011,
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Brodersen et al. 2014). Even within species and populations that are generally considered to be
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obligately migratory, the timing of migratory movements can be quite diverse (Isaak et al. 2003,
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Burke 2004, Hegg et al. 2015a). In many cases life-history characteristics such as growth rate
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and propensity to migrate are heritable, and understanding their expression in the context of
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fitness necessitates linking parent and progeny (Stewart et al. 2006, Thériault et al. 2007,
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Liberoff et al. 2014, 2015, Waples et al. 2017). Further, maternal effects and conditions early in
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life can have large effects on adoption of particular strategies by individual fish (Taylor 1990,
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Morinville and Rasmussen 2003). However, it can be difficult without genetic parentage
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information to link the life-history of the mother to her progeny. Further, understanding behavior
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and the effects of environment on juvenile fish can be difficult in fish too small to apply
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electronic tags.
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Otoliths provide a window into the link between mothers and progeny, as well as detailed
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juvenile information. An inner ear structure of bony fish, otoliths grow in size with the addition
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of daily layers of calcium carbonate (Campana and Thorrold 2001). These layers incorporate
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elements and isotopes that occasionally substitute into the calcium carbonate structure. Many of
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these elements and isotopes are recorded in proportion to the water the fish inhabits, creating a
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temporal and spatial record throughout its life (Kennedy et al. 1997, Thorrold et al. 1998,
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Campana 2005). Numerous studies have reported the presence of a maternal chemical signature
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in the core of otoliths using various chemical proxies, allowing researchers to infer some aspects
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of maternal location, spawning migration, and anadromy from their progeny (Kalish 1990, Volk
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et al. 2000, Miller and Kent 2009, Shippentower et al. 2011, Courter et al. 2013, Liberoff et al.
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2015). At the same time, otoliths provide information on juvenile natal location, movement,
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growth and condition in the layers just outside the zone of maternal influence near the otolith
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core (Thorrold et al. 1998, Walther and Thorrold 2010, Hamann and Kennedy 2012, Hegg et al.
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2013a, Schaffler et al. 2014, Shrimpton et al. 2014, Turner et al. 2015).
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Despite the amount of available research using these adjacent areas of the otolith, Veinott et al.
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(2014) highlight variability in some core signatures and a lack of conclusive agreement on the
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markers of maternal signature and its duration. Further, some assumptions of maternal chemical
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incorporation and duration in the otolith core are untested (Elsdon et al. 2008). Limburg et al.
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(2001) note that a lack of understanding of the duration of maternal signatures may affect their
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interpretation of Baltic sea trout that lack a freshwater phase. It is also unknown whether the
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maternal transition is related to underlying ontological changes in maturing fish which might
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provide further information on juvenile development. As the number of studies utilizing otolith
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chemistry to infer detailed juvenile movement patterns increase in frequency it is important to
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determine how to distinguish maternally-derived, versus environmentally-derived, chemical
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signatures of juvenile fish.
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The maternal signature is retained in the otolith because the egg is provisioned using nutrients
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derived from the mother. The larva obtains all of its nutrients from the yolk sac until it
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commences feeding, which occurs shortly after hatching, at which point the larva begins
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significant chemical exchange with the surrounding water (Hayes et al. 1946). Therefore, as the
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otoliths develop prior to hatching, its isotopic signature should reflect that of the mother (Kalish
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1990, Waite et al. 2008). If the mother has migrated from a location with a different chemical
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signature her eggs will retain a chemical signature related to her past location, attenuated by the
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degree to which her body chemistry has equilibrated with the chemistry of the spawning stream
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(Volk et al. 2000, Bacon et al. 2004). This has also been demonstrated as a marking technique,
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by exposing mothers to known isotopic signatures prior to spawning (Thorrold et al. 2006,
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Woodcock et al. 2013, De Braux et al. 2014). This maternally derived chemical information
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recorded in the otolith can then be used to infer information about the maternal provenance or
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behavior.
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The use of maternally-derived chemical signatures for the identification of marine influence in
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fish has been repeatedly demonstrated (Kalish 1990, Miller and Kent 2009, Liberoff et al. 2015).
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In most freshwater systems the concentration of strontium (Sr) is much lower than that of the
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ocean, providing a large and predictable shift in Sr/Ca in dissolved ions that is conserved
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between anadromous and resident fish (Kraus and Secor 2004, Brown and Severin 2009).
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However, examples exist showing that in some systems Sr/Ca is a poor indicator of ocean
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residence (Kraus and Secor 2004), that expected patterns of chemical signatures of ocean
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residence can be population specific (Hamer et al. 2015), and that Sr/Ca ratios change in relation
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to the time females spend in freshwater and the difficulty of the migration (Donohoe et al. 2008).
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It has also been demonstrated that maternal signatures are conserved in otolith 87Sr/86Sr
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signatures (Barnett-Johnson et al. 2008, Miller and Kent 2009, Hegg et al. 2013a). In contrast to
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Sr/Ca, however, the relationship between maternal 87Sr/86Sr values and juveniles is less well
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quantified. The assumption in anadromous species has been that 87Sr/86Sr maternal signatures
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follow the same mechanism as Sr/Ca, reflecting the global marine value of 0.70918 due to
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maternal investment in the yolk material (Courter et al. 2013). Several studies, however, have
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shown that migratory distance and migratory difficulty may influence the maternal 87Sr/86Sr
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signature (Volk et al. 2000, Bacon et al. 2004, Miller and Kent 2009). As more studies use
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87Sr/86Sr as a marker of maternal anadromy (Courter et al. 2013, Hodge et al. 2016), it is
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necessary to understand the dynamics of maternal chemistry in the otolith core, as well as the
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migratory conditions under which the assumptions of maternal chemical influence hold.
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Based upon a review of the otolith literature, the factors controlling the duration of the maternal
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signature have been largely unexplored. Many studies mention the need to avoid mistaking the
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period of maternal influence with the period of natal origin, or vice-versa (Barnett-Johnson et al.
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2008, 2010, Donohoe et al. 2008, Hegg et al. 2013a). However, determining the end of maternal
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chemical influence on the otolith has often been determined subjectively, often based on
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associations with microstructural checks, without a clear understanding of the link between
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microstructure and chemistry (Barnett-Johnson et al. 2008, Hegg et al. 2013a). Most studies of
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the microchemistry of the otolith core have focused on markers of the otolith primordium, rather
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than the extent of maternally derived influence, using various chemical ratios to calcium
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including barium (Ba/Ca), magnesium (Mg/Ca), and manganese (Mn/Ca) (Ruttenberg 2005,
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Macdonald et al. 2008).
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Late season spawning Chinook salmon (Oncorhynchus tshawytscha) in the Snake River of Idaho
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provide an ideal population for examining the presence and duration of the maternal otolith
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signature. Females in this population are entirely anadromous and individuals migrate long
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distances (500-1000 kms) inland to spawn over a narrowly defined period in October and
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November (Garcia et al. 2005). Prior work has characterized the isotopic variation across
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spawning areas in the basin, indicating that juvenile signatures are significantly different
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between spawning areas and that 87Sr/86Sr and Sr concentration in freshwater habitats are
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significantly different from the marine signature (Hegg et al. 2013a). These factors provide both
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a range of freshwater strontium concentrations to interpret otolith signatures, as well as the
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migration distance required to explore the degree that maternal marine signature varies from the
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global marine signature with inland migration.
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This study used individual otolith transects from a collection of known-origin, juvenile Fall
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Chinook salmon from both wild and hatchery sources to quantify the duration and stability of
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maternal signatures in otoliths. This work also investigates the variability in these signatures that
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may be due to the equilibration of mothers to river-specific chemical signatures prior to
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spawning, as well as changes in the microchemistry of the egg after deposition in the redd. Given
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the inland location of the population we hypothesized that maternal 87Sr/86Sr signatures would
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reflect some degree of freshwater influence. We used a multi-tracer approach, including ratios of
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Sr/Ca, Ba/Ca, Mn/Ca, and Mg/Ca as well as 87Sr/86Sr to examine the presence and duration of
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the maternal signature on the otolith. Further, we explored whether changes in each tracer were
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simultaneous, and thus indicative of a single event, or if individual tracers may signal different
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ontological time-points in the early life of fish. First, using the suite of chemical signatures we
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determine the presence and duration of a maternal marine signature in individual juvenile
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otoliths. Given the variability we quantify in maternal signatures, we then measure the spatial
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and temporal variability of maternal signatures across the study area.
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Methods
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Study System
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Fall Chinook salmon in the Snake River are listed as threatened under the Endangered Species
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Act (Good et al. 2005). The population inhabits low-elevation, mainstem habitats of the Snake
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River and its tributaries. The majority of spawning occurs in the free flowing Snake River
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between Asotin, Washington and Hells Canyon dam and in the Clearwater River (Garcia et al.
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2008). The main spawning areas in the Snake River are classified as “Upper”, above the
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confluence with the Salmon River, and “Lower”, in the free-flowing section below the Salmon
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River confluence to Asotin, WA. The watersheds of the basin are geologically heterogeneous
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with enough distinction to provide significant differences in water 87Sr/86Sr ratios between the
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major spawning reaches that can be used to classify fish to their natal location (Hegg et al.
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2013a, 2013b). Adult salmon migrate a minimum of 750 km to the main spawning areas in the
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Snake and Clearwater Rivers above the town of Lewiston, ID. The watershed is heavily
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influenced by hydropower with eight downstream dams, four on the Columbia River and 4 on
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the Snake River, creating slow moving reservoir habitat downstream of Lewiston, ID.
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The population is notable for a recent shift from a historically ubiquitous sub-yearling strategy,
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whereby individuals migrated shortly after emergence, toward a later, yearling strategy in
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response to anthropogenic changes to the river system (Connor et al. 2005, Williams et al. 2008).
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Studies have indicated that this change in juvenile life-history is likely heritable and under active
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selection in response to reservoirs and hydropower regulation that provide cool water
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opportunities during summer that did not exist historically (Williams et al. 2008, Waples et al.
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2017). A separate study seeks to quantify the spatially explicit outmigration behaviors (Hegg et
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al. In prep). However, to accurately assess early life-history behaviors using chemical proxies in
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otoliths, it is essential to determine the degree of maternal influences on the early chemistry of
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juvenile fish.
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Background Water Sample Collection
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Water samples were collected from 2008 through 2016 throughout the spawning range of Snake
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River Fall Chinook salmon to characterize the spatial and temporal variation in strontium
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isotopic chemistry within the basin (Figure 1). Samples were collected during baseflow periods
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in late summer and fall in all years to capture the most representative signature of water and rock
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interactions within each river. Starting in 2009, as resources permitted, samples were taken
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seasonally. Sampling began in the spring as soon as flows were safe to sample and included
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summer, and fall seasons to characterize the stability of the signatures. Additionally, in 2010,
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samples were taken in the Clearwater and Salmon Rivers at three periods encompassing the peak
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of the hydrograph to characterize seasonal variation observed in prior studies (Hegg et al. 2015b)
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Samples were collected in acid cleaned 125ml HDPE bottles according to established protocol
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(Kennedy et al. 2000). Samples were analyzed for 87Sr/86Sr isotope ratios on a Finnigan MAT
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262 Multi-Collector thermal ionization mass spectrometer (TIMS) as well as a Isotopix Phoenix
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TIMS. Throughout the research period, replicate analysis of the National Institute of Standards
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and Technology standard reference material (SRM-987) was used to determine the analytical
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error. The Finnegan MAT 262 yielded mean 87Sr/86Sr of 0.710231 (2SD = 0.000032, n=16), the
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Isotopix Phoenix yielded a mean 87Sr/86Sr of 0.710244 (2SD = 0.000009, n=89).
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Fish and Otolith Collection
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Wild juvenile fish (n=430) were captured using beach seines from spawning areas between the
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Snake and Clearwater Rivers as part of seasonal population surveys between April and August in
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years spanning 2007 to 2014 (Connor et al. 1998). Some of these fish (n=111) were PIT tagged,
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released, and recaptured at fish passage facilities at Lower Granite Dam on the Snake River
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during their downstream out-migration, providing two known locations for these fish (tagging
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site and recapture site). Juvenile fish were also collected from the two hatcheries that produce
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Fall Chinook in the Snake River basin. Hatchery fish were collected from Lyons Ferry Hatchery
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in 2009 and 2011 (n=28), and from Nez Perce Tribal Hatchery in 2011 and 2012 (n=35).
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Fish samples were kept frozen until otoliths could be removed through dissection. Otoliths were
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stored dry in polypropylene microcentrifuge tubes. Otoliths were then mounted on the sagittal
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plane on petrographic microscope slides using Crystalbond adhesive and ground by hand on fine
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grit Micromesh aluminum oxide sandpaper to reveal the otolith primordium and daily otolith
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increments. (Secor et al. 1992, Hegg et al. 2013a).
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Otolith Chemical Analysis
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Otoliths were analyzed for 87Sr/86Sr using a Finnigan Neptune (ThermoScientific) multi-collector
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inductively coupled plasma mass spectrometer coupled with a New Wave UP-213 laser ablation
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sampling system (LA-MC-ICP-MS). Analysis for trace element composition was conducted
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using an Element 2 (ThermoScientific) ICP-MS attached to the same laser ablation system. For
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each analysis method otoliths were analyzed using a transect moving from the edge of the otolith
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to the core. This transect was positioned approximately 90° from the sulcus on the dorsal side of
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the otolith to capture the area containing the clearest succession of rings from the edge to the
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core. The laser was set to ablate at a constant speed. For 87Sr/86Sr ratios the LA-MC-ICP-MS
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system was set to 10µm/second scan speed, 40µm laser spot size, and 0.262 second integration
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time. For trace element analysis, the laser was set to scan at 10µ/second, 30µm laser spot size,
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and a 1 second sampling time in the ICP-MS method. Samples were run using a dry flow of
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helium (He) through the sample chamber was approximately 0.8L/minute, which combined with
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.6L/min argon (Ar) before entering the plasma. Oxide formation rates were <1% Th/ThO2. The
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trace element analysis included the elements calcium (43Ca), strontium (86Sr), barium (138Ba),
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Magnesium (25Mg), and Manganese (55Mn).
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Strontium ratio data was corrected based on the global marine signature for each analysis day
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using a marine shell standard (mean 87Sr/86Sr = 0.709186, SD = 0.000077, n=535). Error across
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individual otoliths varies based on fish location and is best assessed on stable regions. The
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maternal period between the otolith core and 150µm is relatively stable across all otoliths. In our
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study the standard deviation of the 87Sr/86Sr signature in the maternal region averaged across all
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otoliths was 0.00095 (SD = 0.00063, n = 279).
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Elemental counts were corrected to the SRM 610 standard (Jochum et al. 2011). Correction was
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done using a ten second, within-run blank during which gas was flowing over the sample but the
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laser was not ablating. Blank counts were then subtracted from the measured concentration of
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SRM 610 for each element. All measurements were normalized to known CaO in SRM-10 and
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aragonite, to account for variations in laser ablation efficiency. Three standards were run for
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every 10-20 samples, and an average of the correction factor for these standards was used to
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correct those samples. Limits of detection (LOD) for each element were calculated as 3 X SD
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from the mean of all sample blanks during otolith analysis runs in which our samples were a part
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(n = 859). Detector problems affected approximately 15% of the samples, causing high blank
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values and increasing LOD for those samples. The LOD for all samples are included in
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parentheses. Expressed as a ratio of elements to calcium, detection limits were; Sr/Ca 0.0059
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(0.029) mm•mol-1, Ba/Ca 0.00036 (0.023) mm•mol-1, Mn/Ca 0.011 (0.031) mm•mol-1, and
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Mg/Ca 0.003 (0.022) mm•mol-1. A suitable solid standard with a similar matrix was not available
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to report accuracy and precision of elemental analyses.
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The edges of the otolith were identified within the data using a CUSUM algorithm on Sr and Ca
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counts, then confirmed visually. Extraneous data were trimmed beyond the edge of the otolith
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before reversing the sequence to form a data transect from the core to the edge. The distance of
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each data point from the core, in microns, was calculated using the scan speed and
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integration/sampling time of the laser and ICP-MS software.
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Statistical Analysis
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Water chemistry and otolith data were aggregated into chemically distinguishable reaches as
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detailed by Hegg et al. (2013a) with the inclusion of two groups for hatchery signatures. One
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chemically distinguishable river group is made up of the Clearwater and Salmon Rivers (CWS).
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A second group is the Lower Snake River (LSK), which extends downstream from the
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confluence of the Snake and Salmon Rivers downstream to the town of Asotin, WA. A third
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group is the Upper Snake River (USK) consisting of the Snake River upstream of the confluence
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with the Salmon River to Hells Canyon Dam. Finally, the Grande Ronde, Imnaha, and Tucannon
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Rivers, comprise the fourth river group. Each of these rivers, flowing from the south, runs over
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the Columbia River basalts, a geological formation of flood basalts (referred to collectively as
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the CRB river group). Finally, Lyons Ferry Hatchery (LFH) and Nez Perce Tribal Hatchery
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(NPTH) make up two separate groupings. Hatchery fish were analyzed separately despite the
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inability to distinguish these groups using 87Sr/86Sr in the past (Hegg et al. 2013a). This was done
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with the hope that multi-tracer data would help to distinguish these groups, and because we
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expected early juvenile or maternal microchemistry might differ from wild fish.
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Duration of Maternal Signature
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Otolith transects were analyzed graphically to determine the location of a change between
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maternally derived and post-hatch chemistry. Large, rapid, changes in element/calcium ratio in
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the early otolith allowed for statistical confirmation of the location of chemical change. To
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confirm the identified location on the otolith did, in fact, represent a significant change in
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elemental signature, the mean signature from 100µm of otolith growth before the identified
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change was compared to the mean signature 100µm after, for all fish within each river group.
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This comparison was done using a two-sided, paired t-test assuming unequal variance (a = 0.05)
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with Bonferroni correction for multiple comparisons. The chemical tracers that showed the most
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significant change across river groups were then used to develop a multivariate change-point
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algorithm to determine the otolith location of the maternal/natal change for individual fish.
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The maternal/natal transition in 87Sr/86Sr was less distinct and involved a gradual slope during
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the maternal period (See Variation in Maternal Signature section below), transitioning to a
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second slope during an extended equilibration period. We used a segmented regression approach
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to test for the presence of a transition in slope near 150µm, the point that we determined a
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transition graphically. We used the {segmented} package for R which uses a likelihood
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maximization approach to determine the optimal breakpoints in a linear model (Muggeo 2003,
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2008). We applied this algorithm to the segment of each otolith 87Sr/86Sr transect between 50µm
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and 250µm from the otolith core, encompass a range around the expected transition. The model
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fit was limited to a single breakpoint and each sample was limited to a maximum of 200
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iterations to converge on a breakpoint. If the model failed to converge it was assumed that the
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data did not contain a breakpoint and was instead best described by a simple linear model.
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Breakpoint analysis was only conducted for those river groups whose river signature was
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different from the expected maternal signature (somewhere between the global marine average
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and the Lower Snake River), since these were the only signatures likely to exhibit a sharp
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enough shift to test. Therefore, fish from Lyons Ferry Hatchery and the Lower Snake River were
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not tested. Breakpoint analysis was run on data smoothed with a centered, 20-point moving
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average. To ensure that smoothing did not affect results, breakpoint analysis was run across a
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range of smoothness from the raw data to 20-point smoothing at increments of 5-points.
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We also tested two change-point methods for their ability to identify the location of the
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maternal/natal chemical transition for individual otolith elemental ratios. Both were applied to
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the data between 150µm and 350µm from the core of each otolith. The first 150µm was excluded
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so as to avoid the known peak in Mn/Ca near the core (Brophy et al. 2004, Ruttenberg 2005),
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while covering the location on the otolith where the presumed maternal/natal change occurs. The
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first change-point method tested was the multivariate {ecp} package for R, that used the three
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most significant elemental tracers from the paired t-test above (James and Matteson 2014).
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Additionally, we applied a univariate change-point algorithm from the {changepoint} package
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for R (Killick and Eckley 2013). This univariate approach used only the most significant
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chemical tracer from the prior paired t-test. The univariate change-point algorithm was applied
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using the “AMOC” (At Most One Change-point) procedure and an asymptotic penalty, for
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changes in both mean and variance.
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Variation in Maternal Signature
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To determine the degree that maternal signatures vary we fit a linear model to the maternal
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87Sr/86Sr signatures of all known juvenile fish and the known average 87Sr/86Sr of the river in
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which they were captured. Under the null hypothesis that all fish maintain an ocean signature we
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would expect the slope of this regression to be zero, with an intercept of 0.70918, the global
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ocean signature. A significant slope other than zero, with an intercept other than 0.70918 would
330
indicate that maternal signatures vary with maternal equilibration to the spawning stream.
331
332
Stability of Maternal Signature
333
During the course of analysis, we noted that the mean 87Sr/86Sr in the early otolith (<150µm from
334
the otolith core) of the CWS and NPTH groups appeared to differ. This was striking because
335
contributing mothers of both groups inhabit similar water chemistries from the Clearwater River
336
prior to spawning. Further, we noted that otolith chemistry during this early period appeared to
337
change during development in both groups, with opposite slopes. Chemistry this early in the
338
otolith is likely to reflect chemistry in the egg (Boyd et al. 2010), a period whose rate of
339
chemical change has not been well studied and that some authors claim to be a closed system
340
chemically and isotopically (Volk et al. 2000, Elsdon et al. 2008). To test for differences
341
between these groups we tested the mean 87Sr/86Sr ratio between the CWS and NPTH groups
342
using a two-sample t-test. To test for isotopic change within the egg during this isotopically
343
“closed” period we also fit a linear model to the aggregate maternal data in each group to
344
determine the presence and magnitude of change in the maternal signal.
345
346
To support our findings, we calculated expected changes in the 87Sr/86Sr ratios of the egg under
347
seven scenarios of maternal equilibration and spawning water chemistry (Table 1). In these
348
scenarios, we tested four different maternal equilibration chemistries; mothers equilibrated to the
349
ocean, the Lower Snake River, the Clearwater River (as measured during Oct. & Nov.), and the
350
observed signature at the otolith core (0µm) for known NPTH juveniles taken from the linear
351
model above. For each of these maternal equilibration scenarios the change in 87Sr/86Sr was
352
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calculated assuming eggs were laid into Clearwater River water, or into water similar to the well
353
water used at NPTH. As a proxy for NPTH well water we used the signature for the Potlatch
354
River, a nearby river that is representative of the low 87Sr/86Sr basalt signature of the area.
355
356
The signature observed in the core of NPTH otoliths represents an “intermediate” signature
357
between the Lower Snake and the Clearwater Rivers, an indication that mothers may not be fully
358
equilibrated to the Clearwater River signature at spawning. This “intermediate” signature
359
provided a direct test of whether the changes we observed in the otoliths were supported by our
360
calculations.
361
362
Calculations were based on two-component isotope mixing models including both concentration
363
and isotope ratio differences (Faure and Mensing 2004 p. 350, equation 16.11). We calculated
364
the expected change in 87Sr/86Sr during the first 80 hours after fertilization, when the egg takes
365
on the majority of its external water (Loeffler and Løvtrup 1970). We then calculated the further
366
change in 87Sr/86Sr due to the small amount of water exchange during the period from
367
fertilization to hatch (0.33% of egg volume per day) as estimated by Loeffler and Løvtrup
368
(1970). Calculations were based on values available from the literature. We used egg Sr
369
concentration data for wild and hatchery steelhead from Kalish (1990), average egg volume in
370
Atlantic salmon from Rombaugh and Garside (1982), and changes in Atlantic salmon egg
371
volume over time from Leoffler and Løvtrup (1970). We assumed the number of days to hatch to
372
be 73, the average for the Clearwater River in 2013 (Bill Arnsberg, Nez Perce Tribal Fisheries,
373
pers. comm.).
374
375
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Results
376
377
Duration of Maternal Signature
378
379
Graphical analysis of otoliths by known natal location indicated that changes occurred at
380
consistent locations on the otolith for elemental ratios and 87Sr/86Sr, regardless of river group.
381
However, elemental ratios and 87Sr/86Sr did not change simultaneously. Instead 87Sr/86Sr
382
exhibited changes at different locations on the otolith than elemental ratios.
383
384
Strontium ratio appeared to exhibit an inflection point ~150µm from the otoliths core. This was
385
particularly noticeable in the signatures from the Clearwater, Grand Ronde, and NPTH river
386
groups. Breakpoints within each river group were approximately normally distributed, with no
387
group violating the assumption of normality (p > 0.4 for all groups, a = 0.05) using the Shapiro-
388
Wilkes normality test (Razali and Wah 2011). The mean breakpoint within the Clearwater River
389
was located at 151µm (SD = 22µm). Mean breakpoints for the Grande Ronde were 150µm (SD =
390
20µm). For NPTH the mean breakpoint was 148µm (SD=24µm). The median breakpoint for the
391
Upper Snake river group was 145µm (SD=24.9). Both the NPTH and USK groups exhibited a
392
second, smaller, group of breakpoints near 200µm as data smoothness decreased. The mean
393
breakpoint for all groups remained within 15µm across all smoothing profiles, though the results
394
became increasingly abnormally distributed as data smoothness decreased. The median
395
breakpoint remained relatively stable across groups regardless of smoothing, with the exception
396
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of NPTH and the Upper Snake river groups whose median increased to 180µm and 185µm
397
respectively on the raw data.
398
399
Elemental ratios, particularly Mn/Ca and Ba/Ca, showed a marked change beginning at 225µm
400
from the otolith core (Figure 2). These changes were less pronounced in fish from the hatchery.
401
Comparison of the 100µm segments on either side of 225µm using two-sided, paired t-tests
402
assuming unequal variance (a = 0.05) with Bonferroni correction showed that Mn/Ca was highly
403
significant for all groups, while Ba/Ca was significant for all river groups except hatchery fish
404
from LFH (Figure 3). Sr/Ca ratios were significantly different only for the USK and LSK groups
405
and LFH. Mg/Ca ratios showed no significant differences. Mn/Ca ratios were at or below LOD
406
in many samples during this period, however, the consistent pattern of increasing Mn/Ca after
407
225µm indicates this increase is likely biological despite low concentrations of Mn.
408
409
Multivariate change-point analysis on Mn/Ca and Ba/Ca ratios using the {ecp} package did not
410
provide consistent determination of the location of chemical change in individual otoliths.
411
Similarly, univariate change-point analysis on Mn/Ca using the {changepoint} package resulted
412
in inconsistent determination of the maternal/natal chemical shift at the individual level. Using a
413
value of 225µm appeared to describe the location of the maternal/natal transition as well or better
414
than change-point analysis. Individual variation in the magnitude of the chemical change, as well
415
as data noise, was likely to blame for the difficulty in determining logical change-points at the
416
individual level.
417
418
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Plots of 87Sr/86Sr for each non-hatchery river group showed changes in the signature at
419
approximately 150µm from the otolith core, as much as 100µm earlier than the location of
420
chemical changes in the elemental ratios (Figure 4). Following the initial change in 87Sr/86Sr ratio
421
after ~150µm the signature then began moving toward a second stable period near ~250-300µm.
422
The signature for LFH was consistent throughout the life of the fish, with no distinct changes.
423
Fish from NPTH began at a signature near 0.7096, before a sudden transition to a signature near
424
0.70918 around 150µm, before beginning near 300µm to move toward a signature near 0.7110
425
toward the end of their life.
426
427
Variation in Maternal Signatures
428
The regression of maternal signatures to the signatures of the rivers in which juveniles were
429
captured resulted in a significant linear model (p<0.00001, a=0.05) with the form,
430
431
!"#$%&"'()%
*+ ,)%
*- ( . ((/01234 5!"#$%&"'()%
*+ ,)%
*- 6 (/07893
432
433
Both the slope and intercept terms were highly significant (p<0.00001, a=0.05), providing
434
support for the alternate hypothesis that maternal signatures are different from the ocean
435
signature, and significantly influenced by the signature of the natal river. This effect is apparent
436
in the histogram of maternal signatures expressed in our study, with Clearwater and Grande
437
Ronde juveniles exhibiting maternal signatures that trend in the direction of their natal river from
438
the global marine average (Figure 5)
439
440
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Stability of Maternal Signatures
441
442
Despite mothers experiencing similar 87Sr/86Sr regimes, the maternal signatures of CWS and
443
NPTH juveniles were significantly different prior to 150µm in a two-sample t-test (p<0.00001).
444
CWS juveniles had a mean maternal 87Sr/86Sr signature of 0.7104, while NPTH juveniles had a
445
mean maternal 87Sr/86Sr signature of 0.7096 (Figure 6A).
446
447
Maternal signatures in both groups also showed significant, but opposing, slopes and intercept
448
values when a linear model was applied to the maternal data in each group, indicating changes in
449
chemistry within the egg (Figure 6B). The linear model fit to Clearwater River juveniles returned
450
an intercept of 87Sr/86Sr = 0.7101 (p=<0.00001, a=0.05) and a slope of .00000314 microns
451
(p=0.0016, a=0.05). Variability in the data was high (R2 = .0115). Juveniles from NPTH were fit
452
to a linear model with an intercept of 87Sr/86Sr = 0.7098 (p=<0.00001, a=0.05) and a slope of
453
-0.00000236 microns (p=0.0025, a=0.05). Variability in the NPTH juvenile data was also high
454
(R2 = 0.0102).
455
456
Our calculation of the expected change in egg maternal signatures indicated that 87Sr/86Sr can
457
exhibit changes nearing 0.0001 between the time eggs are laid and when they hatch in some
458
cases (Table 1). The degree of change was driven largely by concentration differences, with
459
mothers equilibrated to the high concentration of the ocean showing little change. The largest
460
change in 87Sr/86Sr signature (0.00094) was seen for mothers equilibrated to the “intermediate”
461
signature observed in NPTH fish, with eggs laid into NPTH well-water. This change,
462
interestingly, is very similar to the significant difference (0.0009) between the mean 87Sr/86Sr
463
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maternal signatures of the Clearwater and NPTH groups above (Figure 6A). In this case, the egg
464
changed its 87Sr/86Sr ratio by 0.00005 in the direction of the ambient water between initial
465
swelling and hatch, supporting our observation of a slope in maternal signatures in Clearwater
466
and NPTH juveniles (Figure 6B). In all cases approximately half of the 87Sr/86Sr ratio change
467
occurred in the first 80 hours after hatch, with the subsequent change occurring slowly during the
468
period after hatch, further supporting the observation of a slope in 87Sr/86Sr signature prior to
469
150µm in the otolith.
470
471
Discussion
472
473
Connecting maternal migratory behavior with the behavior and ecology of their progeny can
474
reveal important details in the ecology of a population. In the case of fish, the maternally derived
475
chemistry stored in the core of otoliths provides important clues about the behavior of mothers.
476
This maternally derived chemistry has been particularly effective as a signature to identify ocean
477
residence for partially migratory salmonid populations (Kalish 1990, Volk et al. 2000, Miller and
478
Kent 2009, Shippentower et al. 2011, Liberoff et al. 2015). Recent work has extended this tool,
479
using 87Sr/86Sr ratio to infer the degree of anadromy in multiple inland populations of steelhead
480
(Courter et al. 2013). Additional studies have cited a period of maternal influence near the core
481
of the otolith, however the duration and chemical makeup of this maternal signature is unclear
482
(Barnett-Johnson et al. 2008, Miller et al. 2011, Hegg et al. 2015b).
483
484
While the use of maternal Sr/Ca signature as a marker of anadromy has been validated (Kalish
485
1990, Zimmerman 2005), very little information is available regarding the duration of this
486
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maternal signature. Several elemental tracers have been proposed as markers of the otolith core,
487
including Ba/Ca and Mn/Ca, but the origin of these elevated elemental ratios may have more to
488
do with juvenile ontogeny and formation of the core itself than maternal behavior (Brophy et al.
489
2004, Ruttenberg 2005). Whether these elemental systems change in concert with a single
490
developmental stage, or whether there are asynchronous patterns of chemical changes during
491
development has not been tested.
492
493
The hatching of juvenile fish, or alternatively the moment of first exogenous feeding, is usually
494
cited as the ontological event that precipitates a change between maternal and natal chemical
495
signatures. The assumption made in most studies is articulated by Volk et al. (2000); that the egg
496
makes up a closed system reflecting the chemistry of the mother during the time at which the
497
eggs are sufficiently developed to close to outside chemical influence. Under this assumption,
498
the juvenile otolith only begins to equilibrate to the external chemistry of the river after hatching
499
when it begins to interact directly with the external environment. Some authors have extended
500
the assumption to conclude that the equilibration of 87Sr/86Sr must be correlated to the first
501
exogenous feeding (Barnett-Johnson et al. 2008).
502
503
Duration of the Maternal Signature
504
505
Our data indicate that Mn/Ca and Ba/Ca, and to a lesser degree Sr/Ca, appear to mark a sharp
506
transition in the otolith chemistry of juvenile fish at 225µm from the otolith core (Figure 2). The
507
simultaneous changes in these elements argue for an underlying ontological change in the
508
juvenile, however it is unclear whether this indicates hatch, the onset of exogenous feeding, or
509
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another physiological or external driver. There is considerable individual variation in the
510
magnitude and location of this change, however, making individual determination difficult and
511
indicating that individual conditions may play a large role in this chemical change.
512
513
The results of our 87Sr/86Sr analysis show that in contrast to elemental signatures, 87Sr/86Sr ratios
514
appear to change near 150µm from the otolith core, with a more gradual change in signature than
515
that seen for elemental ratios (Figure 4). At this point the signature moves steadily toward the
516
signature of the natal river, reaching a stable plateau between ~250µm and ~300µm depending
517
on the population. This change in signature is especially visible in juveniles from the CWS and
518
CRB groups, natal locations whose 87Sr/86Sr values are farthest from the global marine signature
519
and therefore might be expected to exhibit the fastest change toward equilibrium.
520
521
The difference in the timing of change between elemental and 87Sr/86Sr isotopic ratios was
522
interesting. Strontium ratios in our study began to change at 150µm, ~75µm earlier than do
523
elemental signatures (225µm). This distance corresponds to roughly 12 - 19 days, based on the
524
range of known Chinook growth rates in the basin (Zabel et al. 2010). Further, experimental
525
results indicate that otolith radius at emergence varies from 173µm to 259µm (Paul Chittaro,
526
unpublished data). It is reasonable, based on this difference in timing, to assume that the shift in
527
elemental ratios and 87Sr/86Sr are synchronized with different ontogenetic changes in the juvenile
528
fish.
529
530
Since hatching represents the first time the egg is capable of a large degree of ion exchange with
531
the surrounding water, the change in 87Sr/86Sr ratio at ~150µm likely represents hatching.
532
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Strontium and calcium uptake in juvenile fish begins to climb steadily after hatching, and
533
experimental results indicate that it is possible to isotopically mark non-feeding salmonid fry
534
using water spiked with 84Sr (Hayes et al. 1946, Yamada and Mulligan 1987, De Braux et al.
535
2014). Further, between 30 and 83% of strontium is incorporated into the otolith from the
536
surrounding water, enough to begin changing the 87Sr/86Sr signature once the fish begins
537
exchanging ions directly with the surrounding water through its gills and endothelium (Hayes et
538
al. 1946, Walther and Thorrold 2006).
539
540
Previous research indicates that the onset of exogenous feeding could be accompanied by a
541
change in elemental ratios. Experimental evidence indicates that the rate of strontium intake
542
increases to an even faster rate following first-feeding (Yamada and Mulligan 1987), and that
543
magnesium concentration also increases 12-15 days after juveniles hatch (Hayes et al. 1946).
544
The physiological changes that accompany the onset of exogenous feeding could change the
545
regulation of these elements in relation to calcium within the fish’s tissues, as well as changes
546
related to the intake of food sources with differing concentrations of elements as compared to
547
that of the yolk sac. The chemical change also broadly correlates with a first-feeding
548
microstructural check at 235-240µm determined by Barnett-Johnson (2007) in Chinook salmon
549
from California’s Central Valley.
550
551
Taken together our data suggest that both elemental ratios and 87Sr/86Sr ratios provide
552
information on maternally derived chemical influence on the otolith. However, the change from
553
maternal to natal chemistry in 87Sr/86Sr and elemental data appear to correspond to different
554
ontological stages. Changes in 87Sr/86Sr ratio appear to correspond to the hatching of the larval
555
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fish ~150µm, with equilibration continuing until sometime at, or soon after, the onset of
556
exogenous feeding. Elemental ratios of manganese, barium, and strontium appear to reflect the
557
onset of exogenous feeding at ~225µm with a more sudden shift to some equilibrium. While the
558
equilibration of 87Sr/86Sr seems to coincide with the change in elemental data, we have no
559
evidence to indicate that this is necessarily causal.
560
561
Variation in Maternal Signature
562
563
Although Sr/Ca in the core of the otolith can be used to determine maternal anadromy, long
564
inland migrations may attenuate the ocean-derived maternal signature, resulting in variation in
565
the maternal signature. Rieman et al. (1994) showed that Sr/Ca was an incomplete predictor of
566
resident and anadromous maternal behavior in juveniles from a population of O. nerka in Idaho,
567
900km from the ocean. Bacon et al. (2004) found that inland populations in the Pacific
568
Northwest had attenuated or nonexistent Sr/Ca and 87Sr/86Sr maternal signatures and Donohoe et
569
al. (2008) showed that a metric of migratory difficulty could explain attenuation of the maternal
570
signature.
571
572
This attenuation of maternal signature indicates that mothers who spend significant time in
573
freshwater equilibrate to some degree to the freshwater chemistry along their migratory path and
574
in the natal stream. This equilibration should also be reflected in maternally derived 87Sr/86Sr
575
ratios. Our results show that maternal 87Sr/86Sr signatures of juvenile Snake River fall Chinook
576
salmon do vary significantly from the global marine value (Figure 5). As might be expected, the
577
maternal signatures vary in the direction of the water chemistry of the natal stream, indicating a
578
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large degree of maternal equilibration, not just to the mainstem river in which they reside for
579
most of their upstream migration but to the spawning tributary itself. This is especially evident in
580
fish captured from the Clearwater and Grande Ronde Rivers, spawning reaches whose 87Sr/86Sr
581
signatures deviate considerably from the global marine signature, making these changes more
582
apparent. This variation in maternal 87Sr/86Sr signatures indicates that for inland populations,
583
maternal 87Sr/86Sr ratio does not correlate perfectly to marine residence of the mother.
584
585
This result, it seems, would argue that care should be taken in using 87Sr/86Sr as a marker of
586
maternal anadromy. However, Courter et al. (2013) used 87Sr/86Sr to infer the production of
587
anadromous juveniles in resident rainbow trout in the Yakima River, another inland system in
588
the Columbia River basin with similar inland migration distances. Their success may indicate
589
some degree of species or life-history specific retention of ocean signatures in spawning female
590
salmon. However, without an understanding of these hypothetical species or life-history specific
591
mechanisms, our results would suggest caution in interpreting maternal 87Sr/86Sr signatures from
592
the otoliths of populations with significant migration distances. This is particularly the case given
593
that our results indicate that the 87Sr/86Sr signature of the egg can vary from that of the mother,
594
and that the maternal signature may not be stable in all cases.
595
596
Stability of Maternal 87Sr/86Sr Signature
597
598
The apparent differences, and significant slope of change, in the maternal 87Sr/86Sr ratio of fish
599
from the Clearwater River and NPTH groups challenge the assumption made in many studies
600
that the egg is a closed system, reflecting only the chemical signature of the mother. Spawning
601
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females used as broodstock at NPTH are captured at Lower Granite dam and make up a random
602
subsample of the run (Milks and Oakerman 2016). They are then transported to the NPTH
603
complex where they are housed in Clearwater River water until they are spawned (Bill Arnsberg,
604
Nez Perce Tribal Fisheries, pers. comm). Adults who spawn naturally in the Clearwater River
605
move upstream past Lower Granite dam, through the remainder of the Snake River and into the
606
Clearwater River, spawning at a similar time. Thus, adults taken for broodstock at NPTH
607
ultimately spend as much, or perhaps more, time exposed to Clearwater River water as adults
608
who spawn naturally in the river. Despite the similar duration of time mothers are exposed to
609
high 87Sr/86Sr Clearwater River water, the mean maternal signature of NPTH juveniles is
610
significantly lower than that of juveniles originating in the Clearwater River (Figure 6A).
611
612
Because adult spawners experience similar water chemistries before spawning in both groups,
613
the discrepancy in their progeny’s maternal signature is best explained by changes in the isotopic
614
signature of the egg after spawning. The eggs of the two groups of fish do experience different
615
water chemistries between spawning and hatch, providing a mechanism for the observed
616
difference in maternal 87Sr/86Sr if the egg takes up Sr from the surrounding water.
617
618
While NPTH adults are kept in Clearwater River water before spawning, spawned eggs are
619
reared in a different water source. This water is a mix of water from the Clearwater River itself
620
and a well drawing from an aquifer below the river that changes through the year. As the river
621
level rises in the spring, the proportion of Clearwater River water increases (Bill Arnsberg, Nez
622
Perce Tribal Fisheries, pers. comm.). The Potlatch River and Lapwai Creek, both nearby low-
623
elevation streams influenced by the same basalt sources as the aquifer from which well water is
624
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taken, exhibit signatures of 0.7089 and 0.7068 respectively (Hegg, unpublished data). The
625
mixing of low 87Sr/86Sr ratio water influenced by the Columbia River basalts, and the higher
626
87Sr/86Sr water from the Clearwater River that is influenced by older metamorphic rocks
627
upstream, creates the characteristic movement from low 87Sr/86Sr ratio early in NPTH otoliths to
628
higher 87Sr/86Sr signatures more reflective of the Clearwater River as fish age (Figure 3).
629
Therefore, it is possible that the differing signatures of the water in which eggs at NPTH and in
630
the Clearwater River incubate is responsible for the difference we observed in their maternal
631
signatures.
632
633
The idea that the maternal signature of eggs might change seems to be in conflict with the idea
634
that the egg is a closed system (Volk et al. 2000). It is also in contrast to several studies showing
635
that the Sr/Ca chemistry of eggs does not change (Waite et al. 2008, Gabrielsson et al. 2012), and
636
that Sr/Ca signatures are inherited from mothers directly (Kalish 1990, Rieman et al. 1994).
637
However, it should be kept in mind that these studies have been conducted in fish with relatively
638
short spawning runs, whose strontium and calcium concentrations are relatively high compared
639
to the freshwater signatures into which their eggs are laid. Isotope ratio mixing is highly
640
dependent on the concentration of the sources being mixed (Faure and Mensing 2004).
641
Therefore, it would require a relatively large amount of fresh water introduction into the egg to
642
change either Sr/Ca or 87Sr/86Sr if the ocean-acquired maternal contribution is significantly
643
elevated.
644
645
Salmon eggs do take in as much as 12-15% of their volume in water during the first hours after
646
being laid, and external calcium is required during the process of water hardening, indicating that
647
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strontium would also be absorbed in proportion to its concentration in the water (Potts and Rudy
648
1969, Finn 2007). Further, the egg does not actively osmoregulate and continues to take on water
649
at an approximate rate of 1/300th of its mass per day (Loeffler and Løvtrup 1970). Recent
650
research has shown that eggs can be successfully tagged using isotopes of strontium and barium
651
during this initial uptake of water (De Braux et al. 2014, Warren-Myers et al. 2015). Thus,
652
changes to the 87Sr/86Sr signature is possible in the hours after eggs are laid, and before the
653
otolith is formed, creating a difference between the maternal signature of the juvenile otolith and
654
the true maternal signature of its mother at the time the egg was laid. Further, under certain
655
combinations of water and egg chemistry, the slow water exchange during development could
656
create changes in the 87Sr/86Sr signature during the period between water-hardening and hatch,
657
much as we observed in NPTH and Clearwater River juveniles.
658
659
Our calculations make clear that spawning females must equilibrate substantially to the
660
concentration of freshwater before the 87Sr/86Sr signature of the egg could be changed by influx
661
of freshwater (Table 1). The high concentration of Sr in ocean-equilibrated fish effectively
662
buffers changes in 87Sr/86Sr. But, for females that have substantially equilibrated to freshwater,
663
our calculations show that the 87Sr/86Sr signature of the egg can change up to 0.00086 within the
664
first 80 hours after being laid, and as much as 0.00091 by the time of hatch.
665
666
The largest calculated change between the mothers’ signature and the signature of the egg at
667
hatch was in the case testing NPTH equilibrated maternal signatures, with eggs laid into NPTH
668
well water. In this case the signature changed significantly, and, it should be noted that this
669
change is very close to the value of 0.0009 that we observed between the CWS and NPTH
670
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groups, an indication that our calculations are accurately representing the observed shift in
671
87Sr/86Sr for these fish.
672
673
Further, our data provide evidence that the signature of the egg can change significantly even
674
after the initial hours of water-hardening. This is shown by the significant slopes of 87Sr/86Sr
675
ratio during the maternal period in CWS and NPTH juveniles. Despite large amounts of
676
individual variation, CWS and NPTH maternal signatures show highly significant slopes moving
677
in the direction of equilibration to the ambient water, a positive slope in CWS fish and a negative
678
slope in NPTH juveniles (Figure 6B). This is further supported by our calculations showing that
679
a change in 87Sr/86Sr ratio in the fourth digit, well within the analytical precision, could be
680
expected in each case.
681
682
Conclusions
683
684
Maternally derived chemical signatures in fish otoliths, and Sr/Ca in particular, have been
685
instrumental in connecting maternal anadromy to the life-history of their progeny. More recently
686
researchers have begun to infer anadromy from maternally derived 87Sr/86Sr signatures as well.
687
At the same time researchers are examining ever more detailed early movement and life-stages
688
of juvenile fish. As more inferences are made from otoliths about the maternal and early juvenile
689
periods it is increasingly important to know when the maternal signature ends and juvenile
690
signature begins to avoid including erroneous chemical data that could bias results. Despite this
691
need, there has been little understanding of when the influence of maternally derived chemistry
692
ends on the otolith. Our study indicates that both elemental and 87Sr/86Sr ratios mark ontogenetic
693
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changes within larval fish. Further, these signals can be used to determine the end of maternal
694
influence, and the beginning of signatures derived from the water of the natal location. However,
695
our results show that 87Sr/86Sr and elemental data are asynchronous, and likely signal two
696
different ontogenetic changes in the developing fish. We believe it is likely that changes in
697
87Sr/86Sr signal hatching, while elemental signatures of Mn/Ca and Ba/Ca likely signal the onset
698
of exogenous feeding. Further, our results indicate that as female spawners equilibrate toward
699
freshwater concentrations, the 87Sr/86Sr signature of their eggs may shift after they are laid, and
700
in some cases significant changes can occur. Thus, eggs may not directly reflect the maternal
701
signature, complicating the use of 87Sr/86Sr as a method for determining maternal anadromy in
702
inland populations with significant migrations. Further work is needed to verify the duration and
703
stability of maternal signatures under varying elemental concentrations and signatures, and the
704
relationship of elemental signatures to early ontological changes in larval fish.
705
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Walther, B.D., and Thorrold, S.R. 2010. Limited diversity in natal origins of immature
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anadromous fish during ocean residency. Can. J. Fish. Aquat. Sci. 67(10): 1699–1707.
937
doi:10.1139/F10-086.
938
Waples, R.S., Elz, A., Arnsberg, B.D., Faulkner, J.R., Hard, J.J., Timmins-Schiffman, E., and
939
Park, L.K. 2017. Human-mediated evolution in a threatened species? Juvenile life-history
940
changes in Snake River salmon. Evol. Appl. (February). doi:10.1111/eva.12468.
941
Warren-Myers, F., Dempster, T., Fjelldal, P.G., Hansen, T., and Swearer, S.E. 2015. Immersion
942
during egg swelling results in rapid uptake of stable isotope markers in salmonid otoliths.
943
Can. J. Fish. Aquat. Sci. 72(5): 722–727. doi:10.1139/cjfas-2014-0390.
944
Williams, J.G., Zabel, R.W., Waples, R.S., Hutchings, J.A., and Connor, W.P. 2008. Potential
945
for anthropogenic disturbances to influence evolutionary change in the life history of a
946
threatened salmonid. Evol. Appl. 1(2): 271–285.
947
Woodcock, S.H., Grieshaber, C.A., and Walther, B.D. 2013. Dietary transfer of enriched stable
948
isotopes to mark otoliths, fin rays, and scales. Can. J. Fish. Aquat. Sci. 70(1): 14. NRC
949
Research Press. doi:10.1139/cjfas-2012-0389.
950
Yamada, S.B., and Mulligan, T.J. 1987. Marking nonfeeding salmonid fry with dissolved
951
strontium. Can. J. Fish. Aquat. Sci. 44(8): 1502–1506. NRC Research Press Ottawa,
952
Canada . doi:10.1139/f87-180.
953
Zabel, R., Haught, K., and Chittaro, P. 2010. Variability in fish size/otolith radius relationships
954
among populations of Chinook salmon. Environ. Biol. fishes 89(3): 267–278. Springer
955
Netherlands. doi:10.1007/s10641-010-9678-x.
956
Zimmerman, C.E. 2005. Relationship of otolith strontium-to-calcium ratios and salinity:
957
experimental validation for juvenile salmonids. Can. J. Fish. Aquat. Sci. 62(1): 88–97.
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CSIRO PUBLISHING. doi:10.1139/f04-182.
959
960
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Tables
962
963
Table 1 - Calculated change in 87Sr/86Sr in eggs between laying and hatch
964
965
The change in 87Sr/86Sr signature was calculated for six different scenarios of maternal
966
equilibration and laying location. In the table strontium concentrations increase from top to
967
bottom, and decrease from left to right. The largest changes within the egg were calculated for
968
scenarios with low maternal concentration and high concentration in the surrounding water (grey
969
outline). This indicates that concentration likely controls the change in strontium ratio of the egg.
970
Calculations were based on sampled water chemistry and values from the literature. Strontium
971
concentration in fish tissue was taken from Kalish et al. (1990), measured in ocean and
972
freshwater reared steelhead. Changes were calculated for the first 80 hours, when the egg takes
973
in the majority of external water, as well as the remaining 73 days of maturation (the average
974
estimated days to hatch for Clearwater River juveniles in 2013). The furthest right-hand column
975
represents the signature observed at the core of known NPTH juveniles, equilibrating to a
976
signature similar to the well-water used to rear NPTH eggs.
977
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Mother’s signature (starting signature of egg)
High Concentration
¾¾¾¾¾¾¾¾¾¾¾¾¾¾¾®
Low Concentration
Ocean
87Sr/86Sr = 0.70918
Sr ppm = 4.73
Lower Snake
87Sr/86Sr = 0.70956
Sr ppm = 0.88
Clearwater
87Sr/86Sr = 0.71321
Sr ppm = 0.88
Observed signature of
NPTH fish at 0
µ
m
87Sr/86Sr = 0.70981
Sr ppm = 0.88
Signature of Surrounding Water
Low Conc.
¬
¾¾
High Conc.
Potlatch (similar
to NPTH well
water)
87Sr/86Sr = 0.70891
Sr ppm = 0.15
First 80h = 0.00000
To hatch = 0.00001
Total
D
= 0.00001
First 80h = -0.00003
To hatch =-0.00003
Total
D
= 0.00006
First 80h = -0.0002
To hatch = -0.0002
Total
D
= -0.00040
First 80h = -0.00086
To hatch = -0.00005
Total
D
= -0.00091
Clearwater River
87Sr/86Sr = 0.71321
Sr ppm = 0.03
First 80h = 0.00001
To hatch = 0.00001
Total
D
= 0.00002
First 80h = 0.00003
To hatch = 0.00004
Total
D
= 0.00007
N/A
First 80h = 0.00004
To hatch = 0.00003
Total
D
= 0.00007
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Figures
979
980
Figure 1 - Water 87Sr/86Sr Chemistry of the Study Area
981
982
Water samples of 87Sr/86Sr within the range of Fall Chinook salmon in the Snake River basin
983
show distinct grouping between major river groups in the basin. Lyons Ferry Hatchery is located
984
on the Lower Snake River. The Nez Perce Tribal Hatchery is located on the Clearwater River.
985
Water within this hatchery is mixed from two sources, low 87Sr/86Sr well water and water from
986
the Clearwater River, depending on water conditions. Thus, care should be taken in interpreting a
987
single sample.
988
0.708
0.711
0.714
Clearwater/Salmon
G.R./Im./Tuc.
L.F. Hatchery
Lower Snake
N.P.T. Hatchery
Upper Snake
River Group
87Sr86Sr
River Reach/
Hatchery
Clearwater/Salmon
G.R./Im./Tuc.
L.F. Hatchery
Lower Snake
N.P.T. Hatchery
Upper Snake
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989
Figure 2 - Element to Calcium Ratios for Juvenile Fish from known locations
990
991
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Plots of individual element to calcium ratios (mm•mol-1), plotted by river and hatchery grouping,
992
show a shift in chemistry beginning at ~225µm from the otolith core (red line). This shift is most
993
apparent in Ba/Ca (A) and Mn/Ca (B), and less apparent in Sr/Ca (C) and Mg/Ca (D). Plots are
994
smoothed with a 10-point moving average and exclude high values on the y-axis to maintain
995
detail of the maternal/juvenile transition. Blue lines represent the smoothed average of all
996
individual transects using a generalized additive model.
997
998
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999
1000
Figure 3 - Differences in elemental ratios of maternal vs. juvenile periods
1001
1002
Boxplots show the difference in elemental ratios 100µm before and after the 225µm otolith
1003
radius. Asterisks indicate cases in which maternal signatures (red) were significantly different
1004
than natal signatures (blue) based on paired t-tests with Bonferroni correction for multiple
1005
comparisons.
1006
1007
Clearwater
Grande Ronde
L.F. Hatchery
Lower Snake
N.P.T. Hatchery
Upper Snake
0.000
0.005
0.010
0.0
0.5
1.0
0.000
0.005
0.010
0.015
0.6
0.8
1.0
1.2
Known Natal Location
Maternal
Natal
** *
** ***
* * * * **
Ba/CaMg/Ca
Mn/Ca
Sr/Ca
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1008
1009
Figure 4 - Strontium isotope ratios (87Sr/86Sr) of individual fish from known locations
1010
1011
Plots of individual 87Sr/86Sr transects show a relatively stable period from the core of the otolith
1012
to ~150µm from the otoliths core (purple vertical line). This region was not apparent in the
1013
Lyons Ferry and Lower Snake river groups, presumably due to the similarity in signature
1014
between maternal and natal water. After this point transects slowly equilibrate toward the
1015
expected 87Sr/86Sr value for their river group. Strontium ratio does not seem to change at 225µm
1016
(red vertical line) where elemental ratios show a change, indicating that 87Sr/86Sr may be
1017
recording a different ontological change within the developing fish. Fish from NPTH equilibrate
1018
toward an unknown well-water signature before moving upwards to signature reflecting the
1019
Clearwater river as river water is mixed with the hatchery well-water late in the season. Some
1020
late-season juveniles were removed from the Clearwater River plot for clarity (n=21) because
1021
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their transects followed a pattern of movement that suggested hatchery origin and acclimation in
1022
unknown water sources. The global marine signature, 0.70918, is noted for reference (horizontal
1023
blue line).
1024
1025
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1026
1027
Figure 5 - Variation in Maternal 87Sr/86Sr signature
1028
1029
Maternal 87Sr/86Sr signatures of known origin juvenile fish vary significantly from the global
1030
marine value of 0.70918 (dotted line). Individual fish are colored by their known location,
1031
showing that maternal signatures vary in the direction of the water chemistry of the natal stream
1032
of the fish (Figure 1). Means for each group are; Clearwater (0.71050), Grande Ronde (0.70845),
1033
Lyons Ferry Hatchery (0.70946), Lower Snake (0.70931), Nez Perce Tribal Hatchery (0.70964),
1034
Upper Snake (0.70920).
1035
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Figure 6 - Mean maternal signatures of hatchery and natural origin Clearwater juveniles
1037
1038
Despite NPTH adults being exposed to the same, or more, time in Clearwater River water, their
1039
progeny exhibit significantly lower 87Sr/86Sr maternal signatures (A) than juveniles spawned
1040
naturally in the Clearwater River (T-test, p<0.0001). Eggs at NPTH are reared in well-water, not
1041
Clearwater River water. Further, the maternal signatures of juveniles from each location exhibit
1042
significant slopes in the direction of the signature of their natal water sources, indicating
1043
equilibration of the egg signature before hatch (B). Dark blue lines represent the slope of the
1044
aggregate data, while grey shading represents confidence intervals for each regression.
1045
1046
1047
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0.708
0.711
0.714
Clearwater/Salmon
G.R./Im./Tuc.
L.F. Hatchery
Lower Snake
N.P.T. Hatchery
Upper Snake
River Group
87Sr86Sr
River Reach/
Hatchery
Clearwater/Salmon
G.R./Im./Tuc.
L.F. Hatchery
Lower Snake
N.P.T. Hatchery
Upper Snake
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0.00
0.01
0.02
0.03
0.04
0.05
0.00
0.01
0.02
0.03
0.04
0.05
Ba/Ca
Lower Snake Nez Perce Tribal Hatchery Upper Snake
Clearwater Grande Ronde Lyons Ferry Hatchery
0.00
0.01
0.02
0.03
0.04
0.05
0.00
0.01
0.02
0.03
0.04
0.05
Mn/Ca
Lower Snake Nez Perce Tribal Hatchery Upper Snake
Clearwater Grande Ronde Lyons Ferry Hatchery
0.0
0.5
1.0
1.5
2.0
0.0
0.5
1.0
1.5
2.0
Sr/Ca
Lower Snake Nez Perce Tribal Hatchery Upper Snake
Clearwater Grande Ronde Lyons Ferry Hatchery
0
300
600
900
0
300
600
900
0
300
600
900
0.0
0.5
1.0
1.5
0.0
0.5
1.0
1.5
Distance from otolith core
(
µm
)
Mg/Ca
Lower Snake Nez Perce Tribal Hatchery Upper Snake
Clearwater Grande Ronde Lyons Ferry Hatchery
(B)
(A)
(C)
(D)
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Clearwater
Grande Ronde
L.F. Hatchery
Lower Snake
N.P.T. Hatchery
Upper Snake
0.000
0.005
0.010
0.0
0.5
1.0
0.000
0.005
0.010
0.015
0.6
0.8
1.0
1.2
Known Natal Location
Maternal
Natal
** *
** ***
* * * * **
Ba/CaMg/Ca
Mn/Ca
Sr/Ca
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Nez Perce Tribal Hatchery Upper Snake
Lyons Ferry Hatchery Lower Snake
Clearwater Grande Ronde
0
100
200
300
400
500
600
700
800
900
1000
1100
0.703
0.705
0.707
0.709
0.711
0.708
0.710
0.712
0.708
0.709
0.710
0.709
0.710
0.711
0.712
0.713
0.714
0.715
0.707
0.708
0.709
0.710
0.711
0.712
0.709
0.710
0.711
0.712
Distance from otolith core
(
μ
m)
87
Sr
86
Sr
0
100
200
300
400
500
600
700
800
900
1000
1100
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0
10
20
30
40
0.707 0.709 0.711
Maternal
87
Sr
86
Sr
Number of Fish
Natal Location
Clearwater
Grande Ronde
Lyons Ferry
Hatchery
Lower Snake
Nez Perce Tribal
Hatchery
Upper Snake
Global Marine
Value
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0.704
0.708
0.712
0.716
Clearwater
N.P.T. Hatchery
Juvenile Natal Location
87Sr 86Sr
(A)
Clearwater
N.P.T Hatchery
0.7095
0.7100
0.7105
0 50 100 150
Distance from otolith core (µm)
87Sr 86Sr
(B)
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Animal migrations provide important ecological functions and can allow for increased biodiversity through habitat and niche diversification. However, aquatic migrations in general, and those of the world's largest fish in particular, are imperiled worldwide and are often poorly understood. Several species of large Amazonian catfish carry out some of the longest freshwater fish migrations in the world, travelling from the Amazon River estuary to the Andes foothills. These species are important apex predators in the main stem rivers of the Amazon Basin and make up the regions largest fishery. They are also the only species to utilize the entire Amazon Basin to complete their life cycle. Studies indicate both that the fisheries may be declining due to overfishing, and that the proposed and completed dams in their upstream range threaten spawning migrations. Despite this, surprisingly little is known about the details of these species' migrations, or their life history. Otolith microchemistry has been an effective method for quantifying and reconstructing fish migrations worldwide across multiple spatial scales and may provide a powerful tool to understand the movements of Amazonian migratory catfish. Our objective was to describe the migratory behaviors of the three most populous and commercially important migratory catfish species, Dourada ( Brachyplatystoma rousseauxii ), Piramutaba ( Brachyplatystoma vaillantii ), and Pira?ba ( Brachyplatystoma filamentosum ). We collected fish from the mouth of the Amazon River and the Central Amazon and used strontium isotope signatures ( ⁸⁷ Sr/ ⁸⁶ Sr) recorded in their otoliths to determine the location of early rearing and subsequent. Fish location was determined through discriminant function classification, using water chemistry data from the literature as a training set. Where water chemistry data was unavailable, we successfully in predicted ⁸⁷ Sr/ ⁸⁶ Sr isotope values using a regression-based approach that related the geology of the upstream watershed to the Sr isotope ratio. Our results provide the first reported otolith microchemical reconstruction of Brachyplatystoma migratory movements in the Amazon Basin. Our results indicate that juveniles exhibit diverse rearing strategies, rearing in both upstream and estuary environments. This contrasts with the prevailing understanding that juveniles rear in the estuary before migrating upstream; however it is supported by some fisheries data that has indicated the presence of alternate spawning and rearing life-histories. The presence of alternate juvenile rearing strategies may have important implications for conservation and management of the fisheries in the region.
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The chronological properties of otoliths are unparalleled in the animal world, allowing accurate estimates of age and growth at both the daily and the yearly scale. Based on the successes of calcified structures as environmental proxies in other taxa, it was logical that researchers should attempt to link otolith biochronologies with otolith chemistry. With the benefit of hindsight, this anticipation may have been naive. For instance, the concentrations of many elements are lower in the otolith than in corals, bivalves, seal teeth, or the other bony structures of fish, making them less than ideal for elemental analyses. Nevertheless, there is growing interest in the use of otolith chemistry as a natural tag of fish stocks. Such applications are directed at questions concerning fish populations rather than using the fish as a passive recorder of the ambient environment and do not rely upon any explicit relationship between environmental variables and otolith chemistry. The questions that can be addressed with otolith chemistry are not necessarily answerable with genetic studies, suggesting that genetic and otolith studies complement rather than compete with each other. Thus, we believe that otolith applications have the potential to revolutionize our understanding of the integrity of fish populations and the management of fish stocks.Les propriétés des otolithes sur le plan de la chronologie sont sans équivalent dans le monde animal, car elles permettent d'estimer avec précision l'âge et la croissance à une échelle tant quotidienne qu'annuelle. Étant donné les succès obtenus par l'emploi des structures calcifiées comme substituts des conditions environnementales chez d'autres taxons, il était logique pour les chercheurs de tenter de faire le lien entre la biochronologie et la chimie des otolithes. Rétrospectivement, cette approche peut sembler naïve. Par exemple, les concentrations de nombreux éléments sont plus faibles dans les otolithes que dans les coraux, les bivalves, les dents de phoques ou les autres structures osseuses des poissons, ce qui en fait de bien mauvais candidats à l'analyse élémentaire. Toutefois, on note un intérêt croissant pour l'emploi de la chimie des otolithes comme marque naturelle des stocks de poissons. De telles applications visent à répondre à des questions sur les populations de poissons plutôt qu'à utiliser les poissons comme enregistreurs passifs du milieu ambiant, et ne se fondent pas sur une relation explicite entre les variables environnementales et la chimie des otolithes. Les questions auxquelles peut répondre la chimie des otolithes ne sont pas nécessairement abordables par l'étude génétique, de sorte que les travaux sur les otolithes et les études génétiques vont se compléter plutôt que se concurrencer. Nous pensons ainsi que les applications de l'étude des otolithes peuvent révolutionner aussi bien notre compréhension de l'intégrité des populations de poissons que la gestion des stocks halieutiques.[Traduit par la Rédaction]
Article
Otolith marking with enriched stable isotopes via immersion is a recent method of batch marking larval fish for a range of research and industrial applications. However, current immersion times and isotope concentrations required to successfully mark an otolith limit the utility of this technique. Osmotic induction improves incorporation and reduces immersion time for some chemical markers, but its effects on isotope incorporation into otoliths are unknown. Here,wetested the effects of osmotic induction over a range of different isotope concentrations and immersion times on relative mark success and strength for 26Mg:24Mg, 86Sr:88Sr and 137Ba:138Ba on Atlantic salmon (Salmo salar) larvae. 71% and 100% mark success were achieved after 1 h of immersion for 86Sr (75 mg L-1) and 137Ba (30 mg L-1) isotopes, respectively. Compared with conventional immersion, osmotic induction improved overall mark strength for 86Sr and 137Ba isotopes by 26–116%, although this effect was only observed after 12 h of immersion and predominately for 86Sr. The results demonstrate that osmotic induction reduces immersion times and the concentrations of isotope required to achieve successful marks. Osmotically induced isotope labels via larval immersion may prove a rapid and cost-effective way of batch marking fish larvae across a range of potential applications.
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Determining the value of restocking wild fisheries with hatchery-reared fish requires the ability to identify and quantify the survival of hatchery fish after release. However, to obtain accurate estimates of survival rates, multiple fish identification techniques are often used, making the monitoring of restocking inefficient and costly. Here we test a new immersion marking method to determine its efficiency and cost effectiveness for marking millions of hatchery-reared Atlantic salmon (Salmo salar). Salmon eggs were marked during the egg swelling stage by immersing eggs in a solution containing seven enriched stable isotopes (134Ba, 135Ba, 136Ba, 137Ba, 86Sr, 87Sr, and 26Mg) for 2 h immediately after fertilisation. One hundred percent successful marks were detected in the otoliths of resulting larvae at a concentration of 1000 μg·L-1 for 136Ba and 100 μg·L-1 for 135Ba and 137Ba, with no detrimental effects on survival or health of egg and yolk sac larvae. We estimate that seven unique mark combinations can be made at a cost of $0.0001 to $0.0017 (US) per egg and conclude that marking via egg immersion is suitable for low cost, accurate marking of hatchery-reared salmonids destined for restocking purposes. © 2015, National Research Council of Canada. All Rights Reserved.
Article
The Atlantic Menhaden Brevoortia tyrannus is an important component of the estuarine and nearshore fish assemblages in the mid-Atlantic region. It serves as a forage species for many piscivorous fish, birds, and marine mammals as well as being subject to an important commercial fishery. Currently there is concern over low standing stocks and recruitment, yet few studies have addressed those concerns. We evaluated the effectiveness of using an otolith chemistry approach to identify juvenile menhaden nursery areas throughout the Chesapeake Bay over 2 years. If successful, an otolith chemistry approach is capable of addressing a number of hypotheses regarding the source and fate of recruits in a stock. We found multiple unique otolith chemistry signatures in menhaden collected in the Chesapeake Bay. Overall correct classification was 85% for the 2005 cohort and 95% for the 2006 cohort. The ratios of most trace element: Ca and stable isotope ratios were different among areas. In addition to spatial differences, both seasonal and annual temporal variation was present in the otolith chemistry. However, a discriminant function that included temporal variation resulted in reduced prediction accuracy (overall errors increased 7–10%). We found that our classification function, which was developed for multiple cohorts, can successfully predict group membership. We recommend additional evaluation of this strategy because of its potential application to data-poor stocks. Our data show that juvenile menhaden in the Chesapeake Bay can be reliably discriminated based on otolith chemistry signatures and that this approach can be used to critically evaluate the nursery contributions of the bay to the coastal adult stock of menhaden.Received July 11, 2013; accepted January 21, 2014