Results
The δ13C values ranged from -17.58 to -11.46‰ and the
δ15N values ranged from 6.92 to 8.66‰ (Fig 2., see
Supplementary Table 2 for full dataset).
The experimental fish left the release compartment within 10-min in most
trials. The results of the GLMM showed that as a group the experimental
fish left the compartment quicker with subsequent trials, but activity
did not differ across days of the experiment (Table 1). Similarly, there
was little variation among individuals in activity but high in latency
to explore (Table 1).
The results from the generalized linear model of the estimated
intercepts and slopes of behavioral traits (latency to explore and
activity) and stable isotope values showed that the intercept of latency
to explore was correlated to δ13C values of both fin
and muscle. The effect was not large, R2 for both
tissue types was 0.16, p = 0.02 (see also Fig. 3). Other correlations
were not significant.
The calculated Euclidean distance between fin and muscle stable isotope
values varied between fish with a mean value of 0.74 and SD = 0.39. The
slope of latency to explore, as well as the interaction between slope
and intercept, explained variation in the distance (Table 2, Fig. 4).
The model R2 was 0.23 suggesting that the model
moderately reflected variation in the stable isotope distance. No
significant result was observed for activity.
Discussion The current result show that latency to explore, a common proxy for
boldness, assessed in a rapid laboratory array, correlated to
retrospective measures of threespine stickleback trophic niche.
Specifically, bolder fish had lower δ13C values (Fig.
3) and their stable isotope niche changed more over time (Table 2).
These results are among the first to support such a relationship.
The δ13C values
of bolder stickleback were consistently lower in both muscle and fins
(Fig. 2). Comparing isotopic values of multiple tissues allows
estimation of the relative temporal stability of the individual niche
(Phillips & Eldridge, 2006; Maruyama et al., 2017). It is currently
uncertain how much threespine stickleback fin and muscle differ in
turnover rates but estimates for bony fish commonly vary on the scale of
a few weeks to months (Willis et al 2013; Busst & Britton 2018; Barton
et al., 2019; Winter et al., 2019). The stickleback fin and muscle
stable isotope values were highly correlated (Fig. 3). The current study
did not include
δ13C values of
potential prey items within the lake, making inferences on how these
patterns relate to the diet of the fish difficult. However, based on
previous studies of stable isotope ecology in northern freshwater lakes
the lower δ13C
values are expected to indicate more pelagic foraging or foraging on
invertebrates that rely on pelagic production (France, 1995). Lower
δ13C values of bolder individuals could therefore be
consistent with a “landscape of fear” (Gaynor et al., 2019), that
shyer individuals keep to the more sheltered benthic habitat. It should
be noted that in the current experimental setting the intercept will
highly reflect initial boldness (latency to explore during the first
trial). Both in the current experiment and previous studies stickleback
from this population have been found to adjust or habituate to the
experiment as many individuals would initially be slow to explore but
become quicker in subsequent trials (Ólafsdóttir & Magellan, 2016;
Ólafsdóttir et al., 2014). Therefore, the current results should be
taken to indicate that initial shyness/boldness is correlated to
δ13C values, whether those individuals were
consistently shy/bold or adjusted their exploratory speed to context.
Boldness was also linked to change in stable isotope niche over time,
that is, to the difference between δ13C and
δ15N values in fin and muscle. Both the estimated
slope of latency to explore and the interaction of intercept and slope
had significant effect on the change in individual stable isotope niche
(Table 2). High positive slope (individuals that were initially shy but
progressively bold) was correlated to less change in stable isotope
niche (Table 2). This is also reflected by the significant interaction
effect and is, at least in part, explained by that initially shy
individuals will most often have (steep) negative slopes and vice versa.
Visualization of these effects can be seen in Fig. 4 and may indicate
that the pattern is largely driven by a few individuals. These results
highlight that the correlation of trophic niche and behavior can be
nuanced but also the need to consider not only the average behavior but
also plasticity when relating animal personality to foraging (Coomes et
al., 2021).
Based on the current data it is not possible to fully distinguish
between three underlying scenarios. First, innate boldness, as a general
trait expressed consistently in the laboratory and in the field, results
in different foraging patterns and those foraging patterns are reflected
in stable isotope values. Second, previous diet was unrelated to innate
behavior but induced the observed differences in behavior in the
laboratory, for example, through nutrient state or condition. The
experimental fish were deliberately chosen to be of approximately the
same size and weight, but more detailed variation of condition, fatty
deposits, lipid content etc., was not considered. Should previous diet
affect behavior the timing of behavioral test could highly determine the
results, for example, in the current study behavioral test were
conducted with only a single day for fish to adjusting to laboratory
conditions. This was necessary to limit the effect of the identical
laboratory diet on stable isotope values but could have augmented
variation on the boldness-shyness axis, as acclimatization has been
found to affect measures of behavioral traits (Biro, 2012; O’Neill et
al., 2018) but also resulted in increased variation in nutrient state.
Third, both growth rates and standard metabolic rate have been linked to
stable isotope turnover rate and are therefore reflected in stable
isotope values (Gorokhova, 2018; Scharnweber et al., 2021), although
these factors may explain less of the values than diet (Johnston et al.,
2021). Varying growth rates of the stickleback in the wild prior to
capture could have relevance for the current results, both in that
fast-growing individuals would be both bolder and with lower
δ13C values, without any causal link, but boldness and
growth could also have been correlated in the wild. It has been
previously supported that boldness, metabolic rate and growth could be
connected in a “pace of life” syndrome (Réale, 2010). Finally, it
should be noted that overall the relationship of behavior and stable
isotope niche in the current study was small and that no significant
correlations were found for activity or δ15N.