Metrics details
Exploration is among one of the most studied of animal personality traits (i.e.
individual-level behavioural responses repeatable across time and contexts)
not all species show clear evidence of this personality trait
and this is particularly so for members of the Corvidae family
We assessed the exploratory behaviour of four food-caching corvid species: pinyon jays (Gymnorhinus cyanocephalus)
Clark’s nutcrackers (Nucifraga columbiana)
California scrub jays (Aphelocoma californica)
Contextual repeatability was assessed through examining behavioural measures during the Novel Environment task and the Novel Object task
whereas temporal repeatability was assessed by examining changes in these measures over repeated trials
an individual’s exploratory behaviour was not repeatable across contexts or over time
we found no evidence that exploration constitutes a personality trait for these species of corvid
We did find differences in exploratory behaviour
that may be explained by relative reliance on cached food
it is important to examine whether animals have repeatable behavioural responses to better understand how they cope with novel or changing environments
it is becoming increasingly important to understand how individuals explore novelty to better evaluate whether these environmental changes affect species differently
suggesting instead that exploration may be context-dependent
investigating corvids’ exploratory behaviour
provides us with an opportunity to understand the potential uniqueness of this bird family among other animal species
resulting in the presence of a great range of personalities within a population
in addition to those collected from Clark’s nutcrackers and pinyon jays in the current study
allowed us to more closely examine the contribution of relative sociality and feeding ecology to exploration in corvids
The current study aimed to investigate the exploratory behaviour of corvids at the individual level and species level
we examined whether an individual’s exploratory behaviour constituted a personality trait
we assessed the temporal repeatability and the contextual repeatability of an individual’s exploratory behaviour
we investigated whether corvids differed in their exploration by comparing the behavioural responses of four closely-related North American corvid species
and/or institutional guidelines for the care and use of animals were followed
Our research protocol was approved by University of Manitoba’s Animal Care Committee (#F2014-037) and complied with the guidelines set by the Canadian Council on Animal Care
All individuals were housed in individual cages (jays: 51 × 51 × 72 cm
width x depth x height; nutcrackers and magpies: 82 × 54 × 76 cm)
Both jay species were held in the same colony room
whereas nutcrackers and magpies were held in a species-specific colony room
Colony rooms were maintained at 22 °C with a 12:12 day-night cycle
Birds were given an ad libitum amount of water and grit during the study
Their regular diet consisted of parrot pellets
The experimental procedures used during the Novel Environment task for the scrub jays and magpies were the same as reported here
which was conducted in a room different from that used in the current study
Testing time of the day and order of individuals were randomized across species and individuals
All trials were video-recorded using an Everfocus® 1/3″ colour digital camera
and in the same locations for both environments
comprised of perches used in the birds’ home cages
Birds were never exposed to the artificial trees nor to the environments prior to the current experiment
Behavioural measures for the novel environment task (NE)
For each trial four dependent measures were recorded: (1) NE Exit Latency – duration in seconds from when the start box door was opened to when the individual exited (i.e.
when the bird’s entire body was out of the start box)
(2) NE First Visit Latency – duration in seconds for an individual to visit the first tree (i.e.
perching on at least one of a tree’s branches) from when it exited the start box
(3) NE Number of Trees – number of trees visited at least once
and (4) NE Number of Movements – number of “movements” made in the environment (i.e.
individual flying or walking from one location to another
with a minimum of two seconds latency between movements)
If an individual did not exit the start box within 20 minutes
it was given a NE Exit Latency of 1200 seconds; if an individual did not visit any of the trees within 20 minutes it was given a NE First Visit Latency of 1200 seconds and a NE Number of Trees of 0
All trials were conducted in the same environment as used during the first trial of the Novel Environment task
and the start box remained in the same position
The birds experienced a total of four trials
each with a different object placed at the centre of the environment
and visible from the start box (Trial 1: red cup
The objects were selected to be distinctive
and small enough to allow individuals to interact with them
Only pinyon jays and nutcrackers performed this task
Behavioural measures for the novel object task (NO)
three dependent measures were recorded: (1) NO Exit Latency – duration in seconds from the start of the trial to when the individual exited the start box (i.e.
(2) NO Approach Latency – duration in seconds from when the individual exited the start box to when it approached within a radius of 50 cm of the novel object
and (3) NO Duration Close – relative duration spent less than 50 cm from the object (i.e.
duration spent less than 50 cm from the object divided by duration spent outside of the start box [600 – NO Exit Latency])
If an individual did not exit the start box during a trial it was given a NO Exit Latency of 600 seconds; if a bird did not approach within 50 cm of an object
it was given a NO Approach Latency of 600 seconds and a NO Duration Close of 0
Alpha values of p < 0.05 were considered significant
To assess whether dependent variables measured the same behaviour
we performed Spearman correlations between all measures collected within each task with a Bonferroni correction
We conducted parametric bootstrapping (n = 1,000 loops) to estimate 95% confidence intervals
and likelihood ratio tests to calculate p values for each repeatability estimate
To determine the contextual repeatability of an individual’s exploratory behaviour across tasks
we performed Spearman correlations between all repeatable measures using the data collected during the first trial of each task with a Bonferroni correction
To compare the exploratory behaviours between corvid species
we performed Kruskal-Wallis tests on all variables for the Novel Environment task and Mann-Whitney tests on all variables for the Novel Object task
To compare the inter-individual variability between species
we performed Levene’s tests on all variables collected using the car package
and HSD Tukey’s tests for post-hoc comparisons using the dunn.test package
During the first trial of the Novel Environment task, thirty-eight birds (n = 12 pinyon jays, n = 12 nutcrackers, n = 7 scrub jays, and n = 7 magpies) were tested. We found differences in the behavioural variables collected in the four corvid species (see Table 1 for all species comparisons using Kruskal-Wallis tests)
Pinyon jays visited more trees than magpies (Dunn’s multiple comparison post-test: NE Number of Trees: p = 0.022) and nutcrackers made more movements than magpies (Dunn’s multiple comparison post-test: NE Number of Movements: p = 0.012)
Thirty-three birds (n = 10 pinyon jays, n = 10 nutcrackers, n = 7 scrub jays, and n = 6 magpies) participated in the second trial of the NE task. We found differences in the behavioural variables collected in the four corvid species (see Table 1 for all species comparisons)
Pinyon jays had a lower latency to exit the start box than nutcrackers (Dunn’s multiple comparison post-test: NE Exit Latency: p = 0.001)
scrub jays (Dunn’s multiple comparison post-test: NE Exit Latency: p = 0.013) and magpies (Dunn’s multiple comparison post-test: NE Exit Latency: p = 0.008)
Twenty-three birds (n = 11 pinyon jays, and n = 12 nutcrackers) participated in all four trials of the NO task. We found some differences in the behavioural variables between the two corvid species (see Table 2 for all species comparisons using Mann-Whitney tests)
Nutcrackers had a lower latency to exit the start box during the first trial
but pinyon jays had a lower latency to exit the start box during the second and third trials
Nutcrackers had a lower latency to approach the novel object during the third trial
For pinyon jays, NO Duration Close was negatively correlated with NO Exit Latency (rho = −0.44, p = 0.005; Table S5) and with NO Approach Latency (rho = −0.82, p < 0.001; Table S5)
Individuals that spent a proportionally longer duration close to the object had a shorter latency to exit the start box and a shorter latency to approach the object once out of the start box
For nutcrackers, NO Approach Latency was negatively correlated with NO Exit Latency (rho = −0.36, p = 0.011; Table S6) and with NO Duration Close (rho = −0.76, p < 0.001; Table S6)
indicating that individuals that had a shorter latency to approach the novel object had a longer latency to exit the start box and spent relatively more time close to the novel object
Individual behavioural differences for the four dependent variables collected during the Novel Environment task in the four corvid species
Significant repeatability estimates are indicated in bold
For individual magpies, NE Exit Latency was not repeatable across trials (NE Exit Latency: n = 6, R = 0.36 [95% CI: 0.00–0.92], p = 0.187), but NE First Visit Latency and NE Number of Movements were (NE First Visit Latency: n = 7, R = 0.90 [95% CI: 0.47–0.99], p < 0.001; NE Number of Movements: n = 6, R = 0.73 [95% CI: 0.00–0.91], p = 0.028; Fig. 1)
Repeatability for NE Number of Trees was not calculated as individuals only visited zero or one tree
Individual behavioural differences for the three dependent variables collected during the Novel Object task in the two corvid species
For nutcrackers, NO Exit Latency and NO Approach Latency were repeatable over trials (NO Exit Latency: n = 12, R = 0.54 [95% CI: 0.16–0.78], p < 0.001; NO Approach Latency: n = 12, R = 0.47 [95% CI: 0.08–0.69], p < 0.001), but NO Duration Close was not (NO Duration Close: n = 12, R = 0.00 [95% CI: 0.00-1.00], p = 1.000; Fig. 2)
correlations between both tasks using repeatable variables were non-significant: 1) NE First Visit and NO Exit Latency (rho = 0.252
and 2) NE Number of Movements and NO Exit Latency (rho = 0.030
correlations between repeatable variables between tasks were non-significant: 1) NE Number of Trees and NO Exit Latency (rho = 0.041
and 2) NE Number of Trees and NO Approach Latency (rho = −0.266
Inter-individual variability in four North American corvid species tested in the Novel Environment task: (a) NE Exit Latency
During the first trial of the Novel Object task
we found no differences in the amount of variability for each behavioural variable between pinyon jays and nutcrackers (NO Exit Latency: F1,21 = 0.736
p = 0.401; NO Approach Latency: F1,21= 0.612
p = 0.443; NO Duration Close: F1,17 = 0.798
The goals of our study were: (1) to determine the temporal and contextual repeatability of exploratory behaviour in corvids at the individual level
using two commonly-used exploration tasks (Novel Environment and Novel Object)
and (2) to compare exploration among corvid species
our overall results showed that an individual’s exploratory behaviour was not temporally repeatable
We also found that the behavioural measures of exploration at the individual level did not correlate between tasks
suggesting an individual’s exploratory behaviour was not contextually repeatable
these results suggest that the behaviour assessed during the two tasks did not constitute a personality trait
we found some differences in the exploratory behaviour at the species level
magpies visited significantly fewer trees and made fewer movements than pinyon jays or nutcrackers
pinyon jays and nutcrackers differed in their latency to exit the start box
inter-individual variability in exploratory behaviour significantly differed between magpies and pinyon jays
as well as between magpies and nutcrackers
we stress that future research should attempt to validate the tasks used or the study of animal personality
Although we did not directly examine the influence of sociality and foraging ecology on the exploratory behaviour of our four corvid species
this study provides a first insight into the factors underlying potential behavioural differences among these corvids
Future research is necessary to determine whether corvids generally show different patterns of exploratory behaviour
or if cache-reliance is driving these differences
Other potential explanations exist for the differences in the exploratory behaviour between magpies and the other corvid species we examined
Perhaps the most interesting may be related to the rearing environment of the birds
whereas the three other species were wild-caught as adults
the influence of developmental experiences on exploratory behaviour has not yet been examined in related corvid species
whether the pattern of results we found are affected by these early experiences will require future investigation
the current study assessed the repeatability of an individual’s exploratory behaviour during two commonly-used tasks for four species of corvid
Our results support recent findings that exploration is context-dependent
we showed that an individual’s exploratory behaviour as measured in these tasks does not seem to constitute a personality trait
as the temporal and contextual repeatability of the behavioural variables collected during the two tasks was low
We recommend that future research focus on validating tasks used to assess an individual’s exploratory behaviour
We also suggest that future studies focus on the context-dependency of exploratory behaviour by corvids
we found no supporting evidence that relative sociality
explains inter-individual variability in exploration
our results tend to support foraging ecology as an explanatory factor driving exploration
Data has been made available as Supplementary Material
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This research was supported by a University of Manitoba Graduate Fellowship to AV and by a Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grant to DMK (#4944-2017)
We thank Parisa Sepehri and Thomas Rawliuk for their help with video scoring
conducted the experiments and analyzed the data; A.V
The authors declare no competing interests
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations
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Behavioral Ecology and Sociobiology (2023)
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Volume 8 - 2020 | https://doi.org/10.3389/fevo.2020.571456
Perceived predation risk can elicit strong behavioral responses in potential prey
songbirds exhibit anti-predator behaviors under experimental conditions
we hypothesized that females of two ground-nesting songbird species
the Ovenbird (Seiurus aurocapilla) and the Hermit Thrush (Catharus guttatus)
would use naturally available cues of predation risk when selecting their nest site
thereby avoiding activity hotspots of Eastern Chipmunks (Tamias striatus)
a predator on songbird nests and fledglings
We mapped chipmunk detections and songbird nests over four successive years in study plots located in mature deciduous forest of New Brunswick
Chipmunk activity varied by an order of magnitude among study plots and years
Nests were built further away from chipmunk detections than expected by chance in some
the proportion of nests built within hotspots of chipmunk activity was four times lower in the two plots where chipmunk activity was highest
we did not find clear evidence that chipmunk avoidance provided fitness benefits
possibly because this behavior procured little protection at high chipmunk densities
The persistence of this avoidance behavior in our focal species of ground-nesting songbirds might be linked to the benefits it procures at intermediate chipmunk densities
the persistence of such behaviors in prey populations suggests that they are adaptive
we aimed to determine whether ground-nesting songbird females respond proactively to nest predation risk in the absence of artificial enhancement of stimuli
We hypothesized that females would assess nest predation risk when choosing a nest site
Hermit Thrushes settle on territory slightly earlier than Ovenbirds
but less is known about the cues they use to select their territory
we predicted that daily nest success of either focal species will be negatively related to chipmunk activity at the nest
we did not include harvest treatment in our models
We recorded Eastern Chipmunk locations and songbird nest positions from 2012 to 2015
territorial males were individually identified using color band combinations
We performed intensive nest searches within mapped Ovenbird territories and around locations where any sign of reproductive activity of the focal species had been detected during spot mapping
we followed Ovenbird males in each territory to determine their pairing status (i.e.
presence of a female or signs of reproductive activity)
we followed her to detect cues suggesting the presence of a nest (e.g.
individuals carrying nest material or food)
We also followed males carrying food and we performed intensive searches in areas where we had lost sight of them
nest searching was conducted every 2–3 days in each territory
Hermit Thrush nests were found incidentally while spot mapping birds or nest predators
or when conducting intensive nest searching within Ovenbird territories
and nest-searching methods were consistent among plots and years
the timing of Hermit Thrush nest building preceded that of Ovenbirds by ca
All nests were monitored every 2–3 days until depredated
All nests found (n = 104) were included in the analyses
A nest was considered abandoned if it was undamaged (before eggs were laid or if the eggs were left untouched)
but there were no signs of adult activity at or around the nest after three visits
A predation event was recorded when a nest was found empty or partially empty after eggs had been laid and prior to the expected fledging date
Although the spot mapping method we used to estimate Eastern Chipmunk activity does not yield an abundance estimate like capture-mark-recapture techniques
it provides an estimate of visual and aural cues available to songbirds
All survey protocols were approved by Université de Moncton’s Animal Care Committee
All manipulations were performed in accordance with the guidelines and regulations of the Canadian Council on Animal Care
Bivariate Ripley’s K-function is a point-event method that determines the scales at which two types of events (here
bird nest locations and chipmunk detections) are either spatially aggregated or segregated from each other
we used the coordinates of each chipmunk detection comprised within the 50% isopleth
Observed Ripley’s K values are computed at increasing radius r and are depicted as the black line in the plots of Ripley’s K against the radii
to assess the significance of Ripley’s K value calculated at increasing window sizes
we used the null hypothesis of complete spatial randomness (CSR) based on a Poisson distribution
We then used 99% confidence envelopes based on the CSR randomizations to determine the spatial relationship between the two types of points
black line) that are outside the confidence envelope (in gray) indicate either spatial aggregation
or spatial segregation when they fall below the envelope
Bivariate Ripley’s K-function was performed for each plot and year separately because both nest and chipmunk locations varied over time and space
We then estimated chipmunk activity using the kernel density function (Dale and Fortin, 2014) for each plot and for each year
Kernel density function was computed using fixed Gaussian kernels to map hotspots of chipmunk detections at a 10 m resolution scale for an area of 1km × 1 km using the kde (kernel density estimation) function of the Hawthorne’s Geospatial Modelling Environment with ArcGIS
We used the estimated value of chipmunk activity at each nest for our analyses on daily nest survival rate
Daily nest survival rate was calculated using logistic-exposure models (Shaffer, 2004) and binomial distribution
To determine whether chipmunk activity influenced fledging success of songbird nests
we modeled daily nest survival rate as a function of chipmunk activity (kernel value at the nest location)
and their interactions (fixed factors) with generalized linear models
Year was included as a fixed factor in our models as previous research in the same study plots and during the same years showed strong fluctuations in daily nest survival rate in Ovenbirds
which was negatively correlated with an index of chipmunk activity
We obtained p-values for each fixed factor using likelihood ratio tests of the model with the fixed factor of interest against the model without the fixed factor of interest
Parameter estimation was achieved using residual maximum likelihood
Spatiotemporal variability in Eastern Chipmunk activity
Kernel densities of eastern chipmunk detections (expressed as number of detections per hectare) in each study plot (25 ha) and year
Note that plot size was adjusted to allow direct comparisons
Black and white dots represent the locations of Ovenbird and Hermit Thrush nests
Bivariate Ripley’s K statistics and generalized linear model were obtained with R version 3.2.2 (R Core Team, 2015) using spatstat (Baddeley and Turner, 2005) and AICcmodavg packages (Mazerolle, 2015)
Spatial aggregation between the Eastern Chipmunk locations and the Hermit Thrush and Ovenbird nests
The gray 99% confidence envelope and red line indicate the null hypothesis of complete spatial randomness (CSR)
The black line indicates the observed Bivariate Ripley K values against Euclidean distance r
When the black line is below the confidence envelope
it indicates a significant negative spatial aggregated pattern
This spatial heterogeneity in chipmunk activity provided opportunities for songbirds to build their nests in areas with lower predation risk
these areas are not risk-free as other nest predators have larger home ranges that encompass those of songbirds
females of both focal species living at least 3 to 5 years would be expected to encounter years of high or intermediate Eastern Chipmunk activity during their lifetime
Figure 3. Distribution of Ovenbird territories, kernel densities of Eastern Chipmunk activity, and songbird nests found in study plot A. See Figure 1 for meaning of color coding
Ovenbird territory locations are shown by ellipses
Black dots represent Ovenbird nests and white dots
we did not have enough nests to evaluate avoidance of chipmunk activity for each bird species separately
may thus be an important component of nest site selection in songbirds
Our activity index may not have provided an accurate estimate of Eastern Chipmunk density
but our objective was to obtain a good approximation of the cues available to female songbirds when selecting their nest site
All datasets generated for this study are included in the article/Supplementary Material
The animal study was reviewed and approved by Simon Lamarre
and M-AV designed the methods and performed the experiment
and M-JF conducted the statistical analyses
This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (DG 2017-05102)
and New Brunswick Innovation Foundation to M-AV.
Irving Ltd Industrial Postgraduate Scholarship to AV
and by NBIF-STGM and FESR scholarships to M-LF
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest
We thank all field assistants who participated in data collection and J
Boisvert for her help with Kernel analyses
Desrochers provided valuable advice on statistical analyses
Kirk made helpful comments on the manuscript
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2020.571456/full#supplementary-material
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Fiola M-L and Villard M-A (2020) Do Female Songbirds Avoid a Mammalian Nest Predator When Selecting Their Nest Site
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