4 DISCUSSION
Male Sakhalin taimen returned to the spawning grounds of the Karibetsu
River several days earlier than their female counterparts. Conversely,
the males departed from these sites later than the females after
spawning, resulting in a longer stream residence for males. Earlier
arrival at breeding sites by males
(protandry) has been documented
for some migratory fishes (e.g. Sinnatamby et al., 2018; Šmejkal et al.,
2017; Tibblin et al., 2016), and is generally explained by the mate
opportunity hypothesis that predicts that earlier arriving males of
polygynous species at breeding areas increase their opportunity to mate
with females (Morbey & Ydenberg, 2001). The earlier arrival and longer
residence at the spawning grounds by the male Sakhalin taimen likely
resulted in their lower rate of spawning across consecutive years
(Fukushima & Rand, 2021). Therefore, even though the operational sex
ratio can be temporarily skewed toward males earlier and again later in
the season, the overall sex ratio of active spawners was female biased,
according to our fish sampling
and videotaped records of individual fish (Rand & Fukushima, 2014).
The number of tributaries Sakhalin taimen entered for spawning
significantly influenced departure timings from tributary sites, such
that individuals, especially males, spawning in two tributaries were on
average later to depart from the last tributary than those spawning in a
single tributary. However,
subsequent arrival downstream at Site L was not influenced by the number
of tributaries they entered, indicating that fish spawning in multiple
tributaries tended to catch up with individuals with which they
previously comigrated before
spawning and restore cohesive groups during the downstream migration.
Sakhalin taimen migration timing was also different at the diel scale,
between sexes and between ascent and descent in females. Male Sakhalin
taimen were largely diurnal during both ascent and descent of the
mainstem of the Karibetsu River, whereas females were diurnal during
ascent but more likely to be nocturnal during descent. This may be
explained by the propensity of male salmonids to be less risk averse
than females during the spawning season (Fleming, 1996). Our model
predicted that both sexes tended to migrate during night-time when
departing from tributaries later in the season. Decreased water levels,
especially in small streams, would increase the visibility of the
post-spawners to predators during daytime (Finlay et al., 2020), which
is a likely explanation for our observations.
Female Sakhalin taimen displayed remarkable intra-individual
repeatability in seasonal migration timing between 2018 and 2019 at all
migration stages. Their departure timing was repeatable even at the diel
scale during MS3. Furthermore, the females descended the mainstem in a
chronological order very similar to that observed during their ascent,
despite most of them spawning in different tributaries in the interim.
Therefore, Sakhalin taimen, at least females, can be characterized by
highly synchronized movements during the spawning migration, and strong
fidelity to arrival and departure timings at specific waypoints along
their migration pathways. Meta-analysis on studies of behavioral
repeatability in various animal taxa have revealed that, except for mate
preference, females are generally
more consistent in their behavior than males (Bell et al., 2009).
Individual-level consistency in migratory behavior has been rarely
quantified for salmonids despite the long history of scientific
investigation into their migration at the species or population level.
This is in part due to the fact that the literature on salmonid
migrations has largely focused on Pacific salmon (Oncorhynchusspp.), which nearly all die after the first spawning (Groot & Margolis,
1991). Even well-studied iteroparous salmonids have rates of repeat
spawning so low (e.g. less than 10% in steelhead O. mykiss[Keefer et al., 2008; Leider et al., 1986], 11% in Atlantic salmonSalmo salar [Fleming, 1998]) that they also are considered
functionally semelparous (Penny
& Moffitt, 2013), making it impractical to investigate their long-term
behavioral consistency in spawning at the individual level.
There was a significant correlation in both water temperature and water
level measured in the Karibetsu mainstem between 2018 and 2019 in
specific time windows relative to the arrival timing of female Sakhalin
taimen in the spawning tributaries. Apart from the statistical
significance of the correlations, the facts that the two critical time
windows overlapped and particularly that their time lags (8.3 and 9.3
days) were very similar indicate that individual females became
responsive to the two environmental signals during similar time periods
in locations where the fish might have lingered before initiating
migration upstream. The estimated mean travel time (approx. 12 days) by
the females from the river mouth to the spawning ground exceeded the
time lags of the critical time windows, leading to a counterintuitive
conclusion that fish made the decision to initiate upstream migration
and left the river mouth “before” the environmental conditions were
met. However, it should be noted
that this travel time was most likely over-estimated because it was
derived by extrapolating the
observed swimming speed (1.98 km day–1) between
waypoints in the headwater area. This speed could be biased low given
that fish are expected to swim slower through upper river reaches (Gauld
et al., 2016) due to steeper elevation gradients, faster currents, and
more numerous natural and unnatural obstacles, like debris jams and
culverts, than they encounter in the lower reaches of the Karibetsu
mainstem. If a more realistic
(i.e. faster) estimate of swimming speed was available for the lower
reaches, their travel time would likely have been much shorter and
coincided more closely with the critical time windows than what is
displayed in Fig. 5. Our presumption that the Sakhalin taimen spawners
started upstream migration from the river mouth is justifiable according
to a provenance study based on stable isotope analysis of otoliths
(Fukushima et al., 2019). Strontium isotope ratios in the otolith
samples of juvenile Sakhalin taimen collected throughout the Sarufutsu
River drainage indicated that their mothers were inhabiting brackish
waters prior to their spawning migration.
The time scale that Sakhalin taimen responded to temperature and water
level appears to be different. The time window during which the fish
responded to water level was much longer
(6 days) than that for
temperature (1.7 days), suggesting that river flow not only cued the
start of migration but also continually influenced fish movements
en route to the spawning ground,
whereas water temperature cued migration with little influence
thereafter. Simmons et al. (2021) observed that out-migrating Atlantic
salmon smolts were significantly influenced by changes in water
temperature early in the run with much less influence afterwards, but
that changes in river discharge exerted stronger influences on the
migration towards the end of the run.
Although water temperature and stream discharge have long been
recognized as the key drivers of salmonid migrations (Dahl et al., 2004;
Quinn et al., 1997; Rand et al., 2006), few studies have investigated
individual variability in response to these environmental drivers. To
our knowledge no studies have examined how individuals might respond
uniquely to water temperature, but given the influence of river flow on
migration speed and successful passage, it is plausible that they
respond differently among individuals to river flows that cue migration.
Body size likely plays an important role, in which migration of larger
individuals is cued at higher river flows. Under a scenario of
a falling hydrograph, during
which salmonids commonly ascend rivers for spawning (Jonsson et al.,
2018; Rand et al., 2006), the migration of larger fish upriver could be
cued earlier in the season. Rand and Fukushima (2014) noted a trend of
decreasing size of Sakhalin taimen migrating upstream on the basis of
sonar observations. However, the earlier arrival of larger fish may be
simply due to the greater capability of larger fish to migrate faster
(Jonsson et al., 1991).
We found no evidence that coordinated movements and repeatable behaviors
of Sakhalin taimen were rooted in social interactions. Although there
were comigrating, same-sex pairs both ascending and descending the
Karibetsu mainstem, we found no evidence that these pairs were cohesive
during tributary entry or departure. However, the slightly smaller
number of female pairs spawning in the same tributaries than expected by
chance (albeit non-significant) may be indicative of some degree of
conspecific repulsion and may help minimize competition for spawning
space and thus redd
superimposition (Fukushima et al., 1998). It should be emphasized that
although the splitting of comigrating individuals into different
tributaries could be viewed as straying, between-year consecutive return
rates to the same tributaries were high (>80%) and likely
a result of fine-tuned homing capabilities (Fukushima & Rand, 2021).
The relatively small sample size of tagged individuals as well as the
limited spatial extent over which fish movements were examined, relative
to the species’ entire migration range, may have made it difficult to
identify social interactions in the migratory behavior of this species.
Female and male Sakhalin taimen consistently differed in migration
behaviors including seasonal and diel timings of arrival and departure,
the degree to which the migration timings were coordinated and
repeatable, reliance on environmental cues to initiate migration, the
frequency of comigration, and swimming speed. Furthermore, female
Sakhalin taimen have a higher rate of consecutive spawning than males
(Fukushima & Rand, 2021). All these behavioral differences between
sexes point to the hypothesis that female and male Sakhalin taimen may
have different degrees of migratory connectivity (Webster et al., 2002).
Although our study focused on the spawning migration period, we suspect
that migration connectivity would also be an important process during
other life-history stages. Migratory connectivity—the extent to which
individuals of a migratory population behave in unison (Torniainen et
al., 2014)—has been suggested to operate over the entire life cycle in
some salmonid populations. For example, individual coded-wire-tagged
steelhead released as juveniles at similar times and locations were
recovered in the same fishing operation in distant locations in the
North Pacific Ocean (McKinnell et al., 1997). Schools of migratory brook
trout S. fontinalis contained significantly more kin than
expected by chance for periods of up to 4 years (Fraser et al., 2005).
This migratory connectivity can be reinforced as individuals age and
become more experienced (Tibblin et al., 2016), or it can be passed on
to succeeding generations through learning by recruits or younger
individuals from older and more experienced ones (MacCall et al., 2019).
Thus, the connectivity can differ between different age-groups and
developmental or life-history stages, a phenomenon known as differential
migration (Briedis & Bauer, 2018).
Differential migration between
sexes in salmonids is exemplified by the migration protandry discussed
above. Furthermore, a higher
likelihood of adopting an anadromous life history in females than in
males, a pattern often observed in salmonids with facultative migratory
strategies, is an extreme example of sex-specific differential migration
(Ferguson et al., 2019; Jonsson & Jonsson, 1993). Although anadromy is
not obligatory, and resident populations of Sakhalin taimen exist,
depending on river systems (Zimmerman et al., 2012), facultative or
partial migration is yet to be reported from any rivers with the
species, including the Karibetsu River. Nonetheless, our observations in
this and previous studies suggest that even though Sakhalin taimen are
broadly categorized as anadromous in this river system, there seems to
be sex-specific differential migration in which females likely have
stronger migratory connectivity than their male counterparts, enabling
the females to better minimize variability in migration timing and form
cohesive groups of migrants composed of the same members across years.
The causes and consequences of the observed coordinated movements,
migratory consistency, and the associated between-sex differences in
migratory behaviors in Sakhalin taimen would be better elucidated by
further research focusing on migratory connectivity, not just during the
breeding stage but also during non-breeding stages of their life.