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ARTICLE
Supplemental feeding may reduce responsiveness of Blackcapped Chickadees (Poecile atricapillus) to avian mobbing calls
during gap-crossing experiments
Jacob M. Bailey, Matthew W. Reudink, and Ken A. Otter

Abstract: Deforestation creates gaps in forest habitat, which can limit the movements of many avian species. Increased
predation risk associated with crossing open habitats is often considered the primary impediment to crossing gaps. However,
other factors such as energetic reserves may also inﬂuence these decisions. We conducted playback experiments before and after
supplemental feeding of Black-capped Chickadees (Poecile atricapillus (Linnaeus, 1766)) to investigate how energetic reserves
inﬂuenced gap-crossing decisions. Black-capped Chickadees were less likely to respond to playbacks, whether conducted within
forests or across gaps, after supplemental feeding. This suggests that energetic reserves may have less inﬂuence on gap-crossing
decisions than on the willingness of birds to respond to mobbing calls in general. We recommend that future studies investigating gap-crossing decisions using playbacks account for differences in resource availability among sampling locations, especially when making comparisons across discrete habitats.
Key words: Black-capped Chickadee, Poecile atricapillus, playback, gap-crossing decisions, energetic reserves, habitat fragmentation,
movement.
Résumé : La déforestation crée des trouées dans les habitats forestiers qui peuvent limiter les déplacements de nombreuses
espèces d’oiseaux. Le risque de prédation accru associé au franchissement d’habitats ouverts est souvent considéré comme étant
le principal obstacle au franchissement de trouées. D’autres facteurs, tels que les réserves énergétiques, peuvent toutefois aussi
inﬂuencer ces décisions. Nous avons mené des expériences de rediffusion de cris avant et après des supplémentations de
nourriture données à des mésanges à tête noire (Poecile atricapillus (Linnaeus, 1766)) aﬁn d’examiner l’inﬂuence des réserves
énergétiques sur les décisions de franchissement de trouées. Les mésanges à tête noire étaient moins susceptibles de répondre
à la rediffusion de cris, qu’elle soit effectuée dans la forêt et dans des trouées, après une supplémentation. Cela donne à penser
que les réserves énergétiques pourraient exercer moins d’inﬂuence sur les décisions de franchissement de trouées que sur la
volonté des oiseaux de répondre à des cris de houspillage en général. Nous recommandons que les études futures qui utilisent
la rediffusion de cris pour examiner les décisions de franchissement de trouées tiennent compte des différences de disponibilité
de ressources entre les lieux échantillonnés, en particulier lorsqu’il s’agit de comparer des habitats distincts. [Traduit par la
Rédaction]
Mots-clés : mésange à tête noire, Poecile atricapillus, rediffusion de cris, décisions de franchissement de trouées, réserves énergétiques,
fragmentation d’habitat, déplacement.

Introduction
Gaps in forest habitat resulting from fragmentation can affect
movement behaviours across a range of taxa (Haddad 1999; Villard
et al. 1999; Collinge 2000; Desrochers and Fortin 2000; Bélisle et al.
2001; Harris and Reed 2001; Ricketts 2001; Bakker and Van Vuren
2004; Riley et al. 2006; Duggan et al. 2012; Janin et al. 2012; Smith
et al. 2013; Poessel et al. 2014). Limited movements of forest songbirds across these gaps created by fragmentation (Desrochers and
Hannon 1997; Haddad 1999; Desrochers and Fortin 2000; Bélisle
et al. 2001; Harris and Reed 2001; Bélisle and Desrochers 2002) can
result in bird populations experiencing reduced connectivity between populations (Keller and Largiadèr 2003; Riley et al. 2006;
Adams and Burg 2015) and decreased juvenile dispersal (Beauchamp

et al. 1997; With et al. 1997). This could increase the vulnerability of
threatened or sensitive species.
The reluctance of songbirds to cross forest gaps is often attributed to a perception of increased risk of predation from avian
predators (e.g., hawks, falcons, and small owls) (Lima and Dill
1990; Rodríguez et al. 2001; Tellería et al. 2001; Desrochers et al.
2002). However, there is evidence that birds may consider factors
other than predation risk when making gap-crossing decisions;
ultimately, the decision of whether or not to cross a gap may
result from a balance between these other competing pressures.
For instance, energetic reserve levels may also play an important
role for birds when making gap-crossing decisions. Turcotte and
Desrochers (2003) demonstrated that birds in food-supplemented
forest fragments were less likely to venture into gaps than those

Received 6 June 2018. Accepted 13 August 2018.
J.M. Bailey and K.A. Otter.* Natural Resources and Environmental Studies, University of Northern British Columbia, 3333 University Way, Prince
George, BC V2N 4Z9, Canada.
M.W. Reudink. Department of Biological Sciences, Thompson Rivers University, 805 TRU Way, Kamloops, BC V2C 0C8, Canada.
Corresponding author: Ken A. Otter (email: ken.otter@unbc.ca).
*Present address: Ecosystem Science and Management Program, University of Northern British Columbia, 3333 University Way, Prince George, BC V2N 4Z9,
Canada.
Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink.
Can. J. Zool. 97: 680–684 (2019) dx.doi.org/10.1139/cjz-2018-0161

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Bailey et al.

in non-supplemented fragments. They suggested that decreased
energy stress, afforded by greater food access, reduced the energetic necessity to move in search of food and in turn made birds
less likely to take risks associated with gap-crossings. Their ﬁnding suggests that birds who do cross habitat gaps may be engaging
in a trade-off between foraging requirements and predation risk
(Lima and Dill 1990; Walther and Gosler 2001).
The primary goal of our study was to investigate how supplemental feeding, as a proxy for energetic reserves, inﬂuences avian
gap-crossing decisions. To test this, we conducted playback experiments before and after supplemental feeding during a concurrent
study (Bailey et al. 2018) investigating the gap-crossing decisions of
Black-capped Chickadees (Poecile atricapillus (Linnaeus, 1766)). We
predicted that birds would be less likely to engage in risky behaviour, such as responding to mobbing calls broadcast from across a
gap, if they occupied patches containing supplemental resources.
We expected birds in these habitats to be less motivated to take
risks, due to the higher resource availability provided by feeders.
We also predicted that there would be little change in the likelihood of birds to respond to mobbing playbacks within continuous
forest, even if supplemental feeders were available, because responding to these playbacks would not involve a gap-crossing.
Responding to mobbing trials within continuous forest would not
necessarily expose birds to elevated risk and therefore the tradeoff between risk and resources would be less inﬂuential on their
decisions.

Materials and methods
We conducted ﬁeldwork for this study within Prince George,
British Columbia, Canada (53.9049°N, 122.7667°W), between
October 2016 and March 2017. Black-capped Chickadees are a species that is resident in the fall and winter months in British Columbia and they will readily use bird feeders (Foote et al. 2010).
Gap-crossing behaviour of Black-capped Chickadees has been
studied extensively using playback experiments (Desrochers and
Hannon 1997; St. Clair et al. 1998; Desrochers and Fortin 2000;
Bélisle et al. 2001; Bélisle and Desrochers 2002; Turcotte and
Desrochers 2003; Groom 2006; Tremblay and St. Clair 2009;
St-Louis et al. 2014; Adams and Burg 2015), making them a useful
study species for our experiment.
We adapted our playback protocol from Tremblay and St. Clair
(2009) so our results would be comparable with past studies (St.
Clair 2003; Tremblay and St. Clair 2009). We conducted 22 playbacks at 11 different sites. Feeders were available at the different
sites between 18 and 45 days (mean 23 days); as part of a parallel
study (Bailey et al. 2018), feeders were established to band Blackcapped Chickadees with passive integrated transponder (PIT) tags
for radio frequency identiﬁcation (RFID) tracking and the variation in feeder availability reﬂected the time required for ﬂocks to
ﬁnd and consistently use feeders (approximately 4 to 20 days),
band the birds at the site (approximately 5 to 7 days), then conduct
7-day RFID-tracking trials. The majority of the variance between
sites was in the time required for ﬂocks to initially locate and
begin using feeders; once located, the mean number of days using
feeders was more similar between sites. Sites were selected where
a linear gap bisected forests, ranging in size from major walking
trails (10–20 m), small to large forest service roads (30–50 m),
through powerline transmission corridors (60–80 m). We selected
an origin location in the forest on one side of the gap that served
as the site of our starting playback. At each site, we conducted two
types of playbacks: (1) playbacks where the origin and destination
locations were on opposite sides of the gap (gap trials) and (2) playbacks where the origin and destinations were within continuous
forest on the same side of, and running parallel to, the gap, i.e.,
did not require movement into open habitat (forest trials). At each
site, we conducted both gap and forest playback trials prior to
supplemental feeding and then again at the end of the feeding

681

period. The playback distances at each site that we sampled were
the same for the gap and forest trials, ranging from 17 to 80 m
(distance was dictated by the size of the gap, as the origin location
was in the forest on one edge of the gap and the destination
location was in the edge of the forest on the immediate opposite
side of the gap; an equivalent distance was used for playbacks in
forest trials). We measured gap distances using a Bushnell
Yardage Pro Sport 600 laser range ﬁnder. At each successive site,
we alternated which trial type (gap or forest) was performed ﬁrst.
Playback protocol
Each playback trial was conducted by two observers, one at the
playback origin and the other at the playback destination. Each
observer had a speaker (Logitech X100) connected to an iPod
Touch that we used to broadcast a Black-capped Chickadee mobbing call. We placed each speaker roughly 1.5 m above the ground
and positioned it pointing in the direction of the other observer.
We standardized speaker volume across all trials (approximately
80 dB at 1 m) using a GoldLine SPL120 sound pressure meter. We
chose this volume because it is similar to natural calling and
because it was sufﬁciently loud to be audible to the second observer at all distances that we sampled.
We began each playback with a 30 s primer of Black-capped
Chickadee mobbing calls at the origin location, followed by 1 min
of silence. Next, we began playing the same mobbing call at the
origin location for up to a maximum of 6 min, or until no new
birds had arrived for 1 min. If no birds responded after the ﬁrst
2 min of the 6 min playback, then we stopped the playback for
2 min and restarted the trial. We repeated this protocol until birds
either began responding to the playback, or the entire 6 min
playback had elapsed with no birds responding (in the latter case,
the trials were aborted until the next day; see below). For a playback trial at the origin location to proceed to testing at the destination location, at least one bird had to have been attracted to
within 10 m of the origin speaker and indicate some form of
responsiveness to the mobbing call (i.e., calling or approaching
the speaker). Once these conditions had been met, the observer at
the origin turned their speaker off and moved to a location halfway between the origin and the destination speakers to observe
and record birds moving from the initial location to the destination speaker. Simultaneously, the observer at the destination
speaker began their mobbing call playback. We broadcasted the
mobbing call for 6 min continuously at the destination location.
Our criterion for a bird to successfully respond to the destination
call was the same as those used at the origin location. After the
ﬁrst playback type (gap or forest trial) was completed, we conducted the reciprocal trial immediately (typically within 1–5 min).
If only one or neither of the gap or forest playback trials was
successful in attracting birds to the origin location, then we
aborted the playback and attempted it again the following day.
For successful playbacks, we recorded the number of birds at the
initial location and the number of individuals that moved to the
destination location; we used this as the dependent variable in
our models.
Statistical analysis
We performed all statistical analyses using STATA version 14
(StataCorp LLC 2015). To analyze the responses of birds to our
playbacks, we constructed mixed-effects logistic regression models with binomial distributions and logit link functions. We used
the number of birds at the destination location (i.e., number of
bird that moved in response to playback) as our dependent variable and the number of birds at the origin location (i.e., total
number of bird responding to the initial playback) as a binomial
denominator. Therefore, for a single playback trial, each individual bird that approached the origin location was scored as either
successfully (1) or unsuccessfully (0) moving to the destination
location. To account for the potential for other birds to inﬂuence
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Fig. 1. The proportion of responses to destination playbacks across all playback distances for gap (circles) and forest (triangles) trials both
before feeding (left) and after feeding (right). After-feeding trials had much lower responses overall compared with before-feeding trials;
however, in the after-feeding trials, a few responses at large distances likely skewed our results to show a positive interaction between gaptrial playback responses and increased gap distance. Graphed data points are jittered to better illustrate overlapping points.

gap-crossing decisions of individuals, we included the total number of birds responding to the origin-location playback in each
individual playback as the binomial denominator (herein referred
to as the “response proportion”). This then uses the total number
of playbacks, rather than the total number of responding birds, as
our sample size for analysis. All of our models included a random
intercept for site to account for the two types of trials (gap trials
and forest trials) being performed at the same sites.
To conﬁrm assumptions that trial order (i.e., whether the ﬁrst
trial at a site was a gap playback or a forest playback) at a site did
not impact the overall responsiveness of birds to playbacks, we
used the response proportion for each trial as the dependent variable and the trial type that was performed ﬁrst at that site as a
categorical predictor variable (forest trial = 0; gap trial = 1). If trial
order was not found to affect response, we subsequently removed
this from further analysis.
To investigate how supplemental feeding inﬂuenced gapcrossing behaviours, we tested if playback responses differed before vs. after food supplementation. To test this, we used the
response proportion as the dependent variable and whether the
trial was performed before feeding or after feeding as a categorical predictor variable (before feeding = 0; after feeding = 1). To test
if this effect was only present during gap or forest trials, we partitioned the data into gap trials and forest trials and again tested
response proportion as the dependent variable and whether the
trial was performed before feeding or after feeding as a categorical predictor variable on both data sets. We also included number
of supplemental feeding days as a continuous predictor variable
for the after-feeding trials to see if differences in duration of food
supplementation inﬂuenced playback responses.
To ask whether gaps in forest habitat negatively impacted bird
movements, we used the response proportion as the dependent
variable, the trial type as a categorical predictor variable (forest
trial = 0; gap trial = 1), and the playback distance as a continuous
predictor variable. We looked at the interaction between playback type and distance because we suspected the effect of distance
on response proportion may only be evident during gap trials. In
this model, we used the response proportion as the dependent
variable, trial type and playback distance as predictor variables,
and included a trial type × playback distance interaction term. To
further investigate signiﬁcant interactions between trial type and
playback distance, we used the response proportion as the dependent variable and playback distance as a continuous predictor
variable for both gap trials and forest trials separately.

Animal care approval
This research was approved by the University of Northern British
Columbia’s Animal Care and Use Committee (protocol No. 2014-6)
and follows the guidelines of both the Association for the Study of
Animal Behaviour and the Canadian Council on Animal Care.

Results
The likelihood of birds responding to a playback was not inﬂuenced by which trial (gap or forest) we performed ﬁrst (Wald ␹2 =
0.06, n = 44, P = 0.81), so we did not use playback order as a random
effect in subsequent models. Birds were signiﬁcantly less likely to
respond to our destination speaker mobbing playbacks during the
after-feeding playback trials compared with the before-feeding
playback trials. This was true when we analyzed all trials together
(Wald ␹2 = 16.27, n = 44, P = 0.0001) and when we partitioned the
data into gap trials (Wald ␹2 = 10.77, n = 22, P = 0.001) and forest
trials (Wald ␹2 = 8.50, n = 22, P = 0.004; Fig. 1) separately.
For our before-feeding trials, we found no signiﬁcant interaction between playback distance and trial type (gap trials vs. forest
trials) (P = 0.72). We therefore dropped the nonsigniﬁcant interaction to derive our ﬁnal model. The full model including trial type
and playback distance was signiﬁcant (Wald ␹2 = 10.70, n = 22, P =
0.004), so we investigated the contributions of the variables to the
model. Increased playback distance did not inﬂuence the proportion of birds that responded to our playbacks (␤ = 0.003, z = 0.12,
P = 0.90). During the before-feeding trials, however, birds were
signiﬁcantly less likely to respond to mobbing playback when
doing so involved a gap-crossing (gap trials) than when they did
not (forest trials) (␤ = −2.12, z = −3.27, P = 0.001).
The ﬁnal model for after-feeding playback trials including the
number of feeding days, playback distance, trial type, and the
interaction between trial type and playback distance was signiﬁcant (Wald ␹2 = 11.67, n = 22, P = 0.02). The number of feeding days
had no inﬂuence on playback response probability (␤ = 0.037, z =
0.84, P = 0.40), whereas distance between the origin speaker and
the destination speaker had a moderate negative effect on response (␤ = –0.03, z = –1.70, P = 0.09). Again, birds were also significantly less likely to respond to gap-trial playbacks compared with
forest-trial playbacks (␤ = –5.87, z = –2.97, P = 0.003), but there was
also a signiﬁcant positive interaction between distance and trial
type (␤ = 0.08, z = 2.33, P = 0.02; Fig. 1). This interaction suggests
that birds were more likely to respond to gap-trial playbacks as
distance increased. However, when we investigated this interacPublished by NRC Research Press

Bailey et al.

tion further, playback distance on its own had no signiﬁcant effect on response probability during the after-feeding gap trials
(Wald ␹2 = 2.08, n = 11, P = 0.15) or the after-feeding forest trials
(Wald ␹2 = 2.25, n = 11, P = 0.13).

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Discussion
Black-capped Chickadees were signiﬁcantly less likely to respond to mobbing playbacks where the destination speaker involved crossing forest gaps compared with those where the
destination speaker was within the same forest patch. This supports the ﬁndings from previous studies, which showed that gaps
act as barriers to movement (Desrochers and Hannon 1997;
St. Clair et al. 1998; Desrochers and Fortin 2000; Bélisle et al. 2001;
Bélisle and Desrochers 2002; Turcotte and Desrochers 2003;
Groom 2006; Tremblay and St. Clair 2009; St-Louis et al. 2014;
Adams and Burg 2015). However, perhaps the most interesting
result of our study was the overall decrease in responsiveness to
approaching mobbing playbacks between our before-feeding trials and our after-feeding trials, as this decrease was seen in both
our gap trials and our forest trials. Because our before-feeding and
after-feeding trials were separated by at least 18 days, habituation
to playbacks is unlikely to explain the reduction in mobbing response. Also, because birds were less likely to respond after feeding regardless of which trial type (gap or forest) was preformed ﬁrst,
this also suggests that the reduction in after-feeding responses was
related to the food supplementation and not habituation to the mobbing call. One possibility is that food supplementation may have
diminished the risk-taking propensity of birds not just to gapcrossing, but to mobbing in general. Because mobbing is a risky
behaviour (Sordahl 1990), birds may have been less motivated to
respond to mobbing calls as the stimulus moved from the origin
speaker to the destination speaker. Birds may have perceived the
“predator” as having moved away as the stimulus shifted to the
destination speaker and thus was no longer potentially hampering access to a perceived food source near the origin speaker. As a
localized food source might reduce the total area the birds need to
travel, they may simply have chosen not to venture to the destination feeder to pursue the predator, regardless of whether or not
this involved a gap-crossing.
During our sampling period, the feeders that we used to supplement birds were also outﬁtted with RFID readers and many
birds in our study population were banded with PIT tags as part of
a concurrent study (Bailey et al. 2018). Results from the RFIDtracking study found that gaps in our study area do appear to
impede Black-capped Chickadee movements. When using RFID
feeders to track movement, the prime impediment to interfeeder
movement was when these involved crossing a gap, which was
exacerbated by the increasing gap size (Bailey et al. 2018). However, during RFID tracking, food supplementation did not inﬂuence bird movements within forests or across gaps. This ﬁnding is
in stark contrast to the overall decrease in responses to mobbing
playbacks after feeding in the current study. Movements recorded
between feeder visitations in Bailey et al. (2018) were recorded by
tracking birds over multiple days, though, as opposed to shortterm movements invoked via mobbing playbacks in the current
study. In conjunction, these ﬁndings suggest that resource availability may have less inﬂuence on reducing gap-crossings than it
does on responding to mobbing calls. However, as we were constrained by a relativity small sample size for our playback experiments, more work is needed to investigate the inﬂuence of
resource availability and bird energetic reserves on mobbing responses, speciﬁcally as they relate to use of mobbing calls in playback studies.
Our playback results run somewhat contrary to other playback studies; whereas others found that increased gap distance
imposed a greater impediment to movement (Desrochers and
Hannon 1997; Rodríguez et al. 2001; Harris and Reed 2001; Bélisle

683

and Desrochers 2002; Tremblay and St. Clair 2009), our study did
not ﬁnd this effect of gap distance. This may result from the
smaller gap distances used in our study (17–80 m) compared with
those of others (e.g., up to 160 m) (i.e., Desrochers and Hannon
1997). Had we been able to sample larger gap distances, differences in response probability may have been more pronounced,
but gaps of this size are not common in the hydro and forestry
right of ways used in our research. RFID tracking, though, did ﬁnd
that movements between feeders were reduced between even
these small gap distances (Bailey et al. 2018).
When we analyzed the after-feeding playback trials alone, we
found birds appeared more likely to respond to mobbing calls
during gap-trial playbacks as gap distance increased. This unexpected result was present for our after-feeding playback trials
only. However, this interaction appears to be due to a few outlier
responses where birds responded to our playbacks at higher rates
than would be expected at large gap distances, rather than an
overall trend of increasing responses with increased gap distance
(Fig. 1).
We recommend future studies looking at the effects of habitat
fragmentation using mobbing call playbacks take into account
differences in resource availability among sampling locations, especially when comparing responses across different habitats.
Birds in areas of differing resource availabilities may differ in
their propensities to respond to mobbing calls. If the goal of a
study is to compare responses across habitats, then differences in
resources may obscure results obtained through use of mobbing
call playbacks.

Acknowledgements
We thank those who volunteered their time to this project,
especially H. Scott, C. Brûlé, D. Powe, and E. Bonderud. We thank
the Catholic Diocese of Prince George for allowing access to their
private property. Funding for this project was provided by the
American Ornithological Society (J.M.B.), the Natural Sciences and
Engineering Research Council of Canada (NSERC) Engage Grant
(K.A.O.) in partnership with Environmental Dynamics Inc., and
NSERC Discovery Grants to K.A.O. and M.W.R. C. Johnson provided advice on models and on the manuscript itself. Two anonymous reviewers kindly provided comments that improved the
manuscript. This research was conducted within the traditional
territory of the Lheidli T’enneh First Nation.

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