Discussion
This paper documents substantial en route mortality of migrating
summer Chum Salmon a major tributary of the Yukon River, the Koyukuk
River, in Alaska during the summer of 2019. Although the true numbers of
fish that died during this event and the proximate mechanisms of the
mortality are not known, available evidence points to a
temperature-mediated phenomenon. Comparisons of body size between
individuals that successfully accomplished their migrations vs. those
that died en route revealed evidence of size-selective mortality
favoring larger body sizes, but whether this reflects direct selection
acting on size or indirect selection acting on correlated phenotypic
traits is unclear. The ultimate question of how this event will impact
future summer Chum Salmon production in subsequent years remains to be
seen. The lower than average escapement counts observed on the major
spawning grounds of Henshaw Creek and the Gisasa River suggests that theen route mortality event was substantial enough to impact the
number of spawners surviving at the population level, which raises
conservation concerns should die-offs become more frequent and/or
greater in severity.
Over a thousand dead fish were counted along a 250 km section of the
Koyukuk River during a rapid-response survey on July 26-27, 2019. This
work would not have been possible without the invaluable observations of
local residents and the use of social media to communicate among
communities and with scientists and managers. Local residents have
always been the first responders to extreme events, and mechanisms to
support communities’ on-going stewardship of the river and its salmon
are needed more than ever. The magnitude of the die-off is unknown, but
likely substantial given several lines of evidence. First, the survey
occurred over a short time period (ca. 1.5 days) and over a relatively
small portion of the migratory path. Second, according to local
residents and the observed state of carcasses decomposition, it was
clear that the survey occurred after the peak of the event, suggesting
that counts would have been higher if we had been able to survey the
river a few days earlier. Third, carcass counts while traveling were an
unknown, but obviously minor, fraction of the number deposited on shore,
which in turn is an unknown fraction of the total number that died
throughout the drainage. Given the scarcity of data, it is impossible to
estimate what the total fraction of the returning fish succumbed toen route mortality. However, observed counts at the two major
spawning grounds were below average (Fig. 5), which is attributed by
managers to the warm temperatures and observed en route mortality
(Brenner et al. 2020). Between 1999 and 2018, Henshaw Creek had averaged
159,000 spawners and between 1994 and 2018 Gisasa River averaged 66,736
spawners. The observations of 34,342 and 19,099 spawners were the fourth
smallest on record for both Henshaw Creek and the Gisasa River. It is
possible that the anomaly between average and observed escapements was
larger for the Henshaw Creek population given the greater energetic
demands for populations that must travel further upstream to spawning
grounds compared to other populations (Crossin et al. 2004) in addition
to the difference in accumulated time in stressful migrating conditions
(Hinch et al. 2012).
Although the proximate mechanisms of this en route mortality
event are not known, existing evidence is strongly consistent with
temperature-mediated effects observed in other locations (Hinch et al.
2012). First, hypoxic conditions may have contributed to the stress of
migrants given that measurements of dissolved oxygen indicated
approximately 87% saturation. It is important to note that migrating
individuals require substantially more oxygen than individuals that are
not actively migrating (Brett 1972). Second, summer Chum Salmon
returning to the Koyukuk were approximately 8 days later than average
(Brenner et al. 2020), which is consistent with the widely observed
pattern of delayed migrations in other systems during periods of
anomalously warm water. For example, Chinook Salmon in the Klamath River
during 2002 entirely ceased migration when the water temperature rose
above ca. 20 degrees C, which in turn increased their densities in cool
water holding refugia and contributed to the spread of pathogens,
particularly Ich and columnaris that ultimately inflicted mass mortality
(Strange 2010, 2013). Third, observed water temperatures during the time
of the survey averaged 17.1°C, which is above the optimum temperature
for migration and is known to put individuals at risk of increased
mortality from pathogens such as F. columnare (Holt et al. 1975).
Approximately a third of the carcasses were noted to have patches of
fungal growth, consistent with earlier infections with columanaris or
other bacterial pathogen (Fig. 3), but formal pathology was not
conducted. Future rapid response surveys should be prepared to take
pathology samples to provide diagnostic disease assessments.
Importantly, the individual fish we sampled as carcasses on the mainstem
Koyukuk had already traveled 900 km from the mouth of the Yukon River
and it is likely that the accumulated time traveling in warm water,
combined with delayed migration increased the susceptibility to
pathogens, similar to en route mortality events in the Fraser
River and Columbia River.
We detected evidence of size-selective mortality, where individuals that
died en route were approximately 4% shorter than individuals
that survived to the spawning grounds at the Henshaw Creek weir (Fig.
4). This pattern was observed in both males and females and was
estimated to be strong selection compared to a global database of
standardized selection differentials (Siepielski et al. 2017). However,
several important caveats with the analysis are necessary. First, like
many analyses of selection this one is plagued by small and unbalanced
sample sizes (68 dead vs. 553 alive). Randomization simulations
conducted on the combined dataset (alive + dead) revealed that the level
of selection observed was likely to occur 1 out of every 4 times due to
chance alone. Second, the carcass survey occurred over a much narrower
range of dates than the observations at the weir, which may bias results
particularly because the size and age of individuals returning to
spawning grounds often covaries with run timing (Quinn et al. 2015).
Indeed, the size of returning individuals to the Henshaw Weir declined
significantly throughout the run (p<0.001), but date explained
little of the variance (6%) in size. However, analyses using a
date-truncated dataset from the Henshaw weir revealed similar patterns
of size selection with large fish being favored to return, and thus the
pattern was consistent while including the potential effect of run
timing. Third, it is not clear whether size selectivity is the result of
direct selection acting on body size or is the result of both direct and
indirect selection acting on correlated phenotypic traits such as
physiological tolerances and others that comprise a migratory phenotype.
The selection analysis here assumes only direct selection, which is
likely not true. Future work to survey carcasses throughout the run and
to gather additional phenotypic measurements would be needed to formally
calculate selection gradients that allow quantification of direct and
indirect influences on selection.
Will the en route mortality that occurred in 2019 have a lasting
consequence on the populations in the Koyukuk River and how might
populations adapt to warming? While this event gives cause for concern
given it appears to have resulted in substantially below average spawner
escapements, there are also reasons for optimism. Pacific salmon are
remarkably productive and resilient in the face of disturbance (Hilborn
et al. 2003) and there is little evidence that small spawner numbers can
result in positive density-density dependent effects, also known as
Allee Effects or depensation (Cunningham et al. 2013). The variable age
of adult migrants contributing to any one return year (e.g. fish that
spent 2, 3, or 4 winters at sea) provides a natural buffer that will
likely dampen (or mask) the true effect of the die-off in future years
(Schindler et al. 2010). In contrast, species such as pink salmon
(O. gorbuscha ) that all mature at two years of age, might be
particularly vulnerable to mortality events. Consistent with
observations from other systems in the southern part of the Pacific
salmon range, it seems the most obvious response to this and potential
future events are shifts in run timing by adults to avoid migrations
during stressful periods (Quinn and Adams 1996). Indeed, run timing and
migratory behavior, which reflect both plastic and genetic components,
are predicted to shift earlier in many systems (Crozier et al. 2011;
Reed et al. 2011a). Of course the extent to which run timing may shift
is a function of the strength of selection and heritability in addition
to plasticity (Carlson and Seamons 2008; Reed et al. 2011b). It is
important to recall, however, that run timing is in part also shaped by
the selection acting on other parts of the life history, such as the
timing of spawning given the water temperature during incubation
(Brannon et al. 2004). This presents potential conflicts, as selection
may favor earlier return timing on the adult life history to avoid
stressful water temperatures, whereas warming should select forlater timing given the relationship with temperature, embryo
development, and match-mismatch dynamics. This dynamic selection
tug-of-war is worthy of additional exploration using eco-evolutionary
modeling.
While the short-term or long-term consequences of 2019 remains to be
seen and understood, it is increasingly clear that regional warming
throughout Alaska and the Arctic is likely to make these events more
frequent and of greater severity. Preparations need to be made to avoid,
to the extent possible, surprises like this that are on the horizon.
This stark reality underscores the need to protect habitats that serve
as the template for life history variation that buffers against
disturbance (Moore et al. 2014), ensure migrating individuals have
natural options to seek thermal refugia in cooler waters during
stressful periods (Armstrong et al. 2016), and support local human
communities to continue being the first responders and stewards of
salmon, without which all of us would be impoverished.