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Article
Individual Nest Site Preferences Do Not Explain Upslope
Population Shifts of a Secondary Cavity-Nesting Species
Elisa J. Abeyta 1, *, Andrew W. Bartlow 2, Charles D. Hathcock 1and Jeanne M. Fair 2
Citation: Abeyta, E.J.; Bartlow, A.W.;
Hathcock, C.D.; Fair, J.M. Individual
Nest Site Preferences Do Not Explain
Upslope Population Shifts of a
Secondary Cavity-Nesting Species.
Animals 2021,11, 2457. https://
doi.org/10.3390/ani11082457
Academic Editor: Mathew Crowther
Received: 28 July 2021
Accepted: 19 August 2021
Published: 21 August 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
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iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Environmental Stewardship, Los Alamos National Laboratory, Los Alamos, NM 87545, USA;
hathcock@lanl.gov
2Biosecurity and Public Health, Los Alamos National Laboratory, Los Alamos, NM 87545, USA;
abartlow@lanl.gov (A.W.B.); jmfair@lanl.gov (J.M.F.)
*Correspondence: ejabeyta@lanl.gov
Simple Summary:
Environmental changes such as climate change have affected wildlife species
behavior and geographic ranges globally. We analyzed nesting data of western bluebirds to determine
whether the link between geographic range shifts of a western bluebird population in New Mexico,
USA is due to individual adaptations or changes occurring at a larger scale. We looked at location
data of marked and recaptured nestlings and adults that nested within our study area. We found that
individual choices have no impact on the geographic range shift being observed in this population,
suggesting that population-level processes, such as emigration and immigration, may be the main
cause of these shifts.
Abstract:
Geographic ranges of plants and animals are shifting due to environmental change. While
some species are shifting towards the poles and upslope in elevation, the processes leading to these
patterns are not well known. We analyzed 22 years of western bluebird (Sialia mexicana) data from
a large nest box network in northern New Mexico at elevations between 1860 m and 2750 m. This
population has shifted to higher elevations over time, but whether this is due to changes in nesting
behavior and preference for higher elevation within the population or driven by immigration is
unclear. We banded adults and nestlings from nest boxes and examined nesting location and elevation
for individual birds captured two or more times. Most recaptured birds nested at the same nest
boxes in subsequent years, and the number of birds that moved upslope did not significantly differ
from the number that moved downslope. Fledglings moved greater distances and elevations than
adults, but these movements were not upslope specific. Female fledglings showed greater changes in
elevation and distance compared to male fledglings, but again, movements were not consistently
upslope. The upslope shift in this population may be due to birds immigrating into the population
and not from changes in individual nesting behavior.
Keywords:
behavioral plasticity; dispersal distance; elevation change; range shift; climate change;
long-term monitoring; western bluebird
1. Introduction
Populations of plants and animals are responding to anthropogenic environmental
change worldwide [
1
–
4
]. Climate change and changes to habitats mean that species must
adapt to new environmental conditions [5] or shift their geographic ranges to match their
preferred climate regimes (i.e., niche conservatism; [
6
]). Not all species have the ability to
adapt quickly enough in the face of environmental change, making these populations more
likely to undergo range shifts [
7
]. If a species can neither adapt nor shift its distribution
because of geographic constraints, it may be vulnerable to local extinction [6,8]. This may
be especially true for species that are range-restricted and for species that may already
be pushed to the limits of their climatic or geographic niche; for example, species on
mountaintops [9,10].
Animals 2021,11, 2457. https://doi.org/10.3390/ani11082457 https://www.mdpi.com/journal/animals
Animals 2021,11, 2457 2 of 12
Climatic niches encompass the biotic and abiotic conditions where a species can persist
over time and space [
11
] and are important to consider with the current rates of climate
changes that are occurring worldwide. As climates change, niches also change, and a
species must respond in order to persist. The effects of climate change and climate niches
on geographic range shifts of populations and communities are still unpredictable, but
general movement upslope and towards the poles has been observed in many species [
12
].
For example, Ref. [
13
] showed that the range of 14 out of 28 small mammal species in
Yosemite National Park monitored for over a century significantly increased in elevation
by an average of 500 m. Identifying whether range shifts occur through population-
level processes, such as changes to reproductive success or dispersal (e.g., immigration
and emigration), or through individual behaviors (e.g., changing nesting locations), can
provide important information about which conservation efforts and mitigation tools
should be implemented.
Despite geographic range shifts being documented more frequently, the processes
behind these shifts have not been fully investigated. Bird species respond to environmental
change in different ways; some adapt quickly through behavioral plasticity (e.g., timing
of reproduction, resource use, microhabitat selection) or more slowly via evolution (i.e.,
genetic changes in the population). Species that do not adapt can contract, expand, or shift
their geographic ranges [
9
,
14
–
18
]. Birds have been shown to move to higher latitudes and
along elevational gradients; however, elevational shifts are not always predictable. Some
species have shifted upslope, while others have shifted downslope [2,19–22].
Colonization and establishment events in new areas are critical for elevation shifts
and can occur through two main processes [
23
,
24
]. First, individuals can shift their nesting
preferences by using information about past breeding sites and choosing a new site the
next year [
24
]. Thus, upslope and downslope population shifts occur when individual
birds return to the same site to breed, but select and colonize higher or lower elevation
nesting sites, respectively. Second, range shifts can occur as immigrants move into the area
or fledglings disperse and nest near their natal area; but in doing so, they nest at different
elevations because they are tracking preferred climatic conditions [
23
]. This kind of range
shift occurs through population dispersal processes even though individual birds may nest
in the same location year after year. Range shifts result from processes happening at the
“leading edge” of a species distribution [
15
]. Studies suggest that range shifts could be
due to pioneering individuals at the leading edge having different behaviors, morphology,
or physiology that provide them the capacity to successfully expand beyond their typical
range [25–29].
The western bluebird (Sialia mexicana) is a secondary cavity-nesting species in western
North America that has a broad distribution up to 2900 m in elevation [
30
]. They are
insectivorous, and the populations in and around our study area in northern New Mexico
are residents or short-distance migrants. They are valuable indicators of ecosystem health
because of their relatively quick responses to environmental change [
31
]. Throughout their
range, males are the more philopatric sex and return to the natal site to breed or to help pro-
vision their parents’ nests, while females are the main dispersers [
32
,
33
]. Fledgling males
either disperse to a new population to compete for a territory, or they inherit a territory
from parents or relatives [
28
]. Over the past 19 years on the Pajarito Plateau, western blue-
birds have not shifted the timing of their breeding even though spring temperatures have
increased [
22
]. They have, however, shifted their nesting sites to higher elevations by an
average increase of 5 m per year [
22
]. It is currently unknown if these elevational changes
occurred through changes in individual behaviors of nesting preferences or through dis-
persal processes. Here, we analyze recapture data from 1997 to 2019 to understand changes
in nesting elevation and dispersal distances in individual western bluebirds. Our data
come from a nest box network that provides nesting sites for secondary cavity-nesting
species, mostly occupied by bluebirds dispersed over an elevational range from 1860 m to
2750 m. The recapture data consist of adult birds that were captured two or more times
and newly banded fledglings that have returned to the breeding site one or more times
Animals 2021,11, 2457 3 of 12
after fledging. Therefore, we were able to address the key question concerning individual
nesting over time and test hypotheses regarding age and sex, both of which are important
in nest site preference and postnatal dispersal. We tested the hypothesis that individual
birds nest higher in elevation each consecutive year, thereby contributing to population
shifts in elevation over time. Our null hypothesis was that individual birds do not nest
higher in elevation each year, which would suggest that individual behavior is not the main
process contributing to population shifts. We also tested hypotheses regarding differences
between adults and fledglings and between male and female fledglings to document any
differences in behavior. The first hypothesis was that fledglings will have greater changes
in elevation and greater dispersal distances than adults, and that the average changes
will be in the upslope direction. Regarding male and female fledglings, we compared
elevational changes and dispersal distances from their natal areas to their new nesting sites.
Because males are the philopatric sex, we hypothesized that female fledglings will show
greater elevational changes and greater dispersal distances than male fledglings, and that
these changes will tend towards upslope movement.
2. Materials and Methods
2.1. Study Location
This study was conducted at Los Alamos National Laboratory (LANL) and surround-
ing areas in Los Alamos, New Mexico, USA (35.09222
◦
N, 106.3242
◦
W, WGS84). The
laboratory occupies ~103 km
2
and is located on the Pajarito Plateau on the eastern flanks
of the Jemez Mountains (see Musgrave et al. [
34
] for a recent map of nest box locations).
The plateau is made up of narrow mesas, separated by steep-sided canyons. The primary
habitats encompassed in the study area are predominantly pinyon-juniper forests and
ponderosa pine (Pinus ponderosa) forests. Pinyon-juniper forests mainly comprise one-seed
juniper (Juniperus monosperma) and pinyon pine (Pinus edulis) trees.
2.2. Field Work and Data Collection
In this study, we analyzed 22 years of data for western bluebirds using a network
of nest boxes. We collected data from recaptured birds between the years 1997 and 2019.
Western bluebirds were the main target species for the avian nest box network because
they nest in secondary cavities. All of the nest boxes were located in pinyon-juniper or
ponderosa pine forests between 1860 and 2750 m in elevation. Data collection for this
network has been ongoing since 1997 using over 500 wooden nest boxes in 49 different
sampling locations. Not all 49 sites were in operation simultaneously; a subset of these
were monitored each year due to changes in staff over the years, inactive sites, or difficulty
of accessing the nest boxes. A total of 350 to 550 boxes were monitored in any given year
during this study. Commercial, standard-sized, wooden nest boxes that had a front-facing
hinged door were used, allowing us the ability to collect data on the nest and its occupants.
Nest boxes were placed ~50 m apart and mounted 2 m above ground.
During the breeding season, nest boxes in the network were monitored continuously
by researchers. They were checked once every 2 weeks unless they were identified as being
active. A nest was considered active if there was nesting material or eggs inside. When an
active nest was identified, it was visited once every 5 days by researchers until nestlings
hatched. The nest was visited again when nestlings were between the ages of 10–15 days
old, so we could band each nestling. A last visit to the nest was to determine fledging
success. A successful nest was an empty nest that had no evidence of predation, such
as a flattened nest with an abundance of fecal matter within the box. A failed nest was
determined by evidence of abandonment or predation, such as a box that was broken by a
black bear (Ursus americanus), missing eggs, or had cracked eggs. At this time, the nest box
was cleaned out for a second clutch to be laid or for another pair to nest. Data collected on
the nests included clutch size, hatch date, sex, and whether the nest successfully fledged
young. Nestlings’ sex was determined by plumage color when they were 12 days or older,
by the amount of blue on the wing and tail [32,35,36].
Animals 2021,11, 2457 4 of 12
Many times, when a nest was active, females were captured in the nest box during
incubation and banded. These opportunistic captures make up a large portion of our
adult capture and recapture data. We recorded the sex and age and took morphometric
measurements, including wing length, tail length, and mass. To obtain data on the parents
that were not in nest boxes when they were visited, mist nets were set up near an active
nest box to capture, band, and collect data on each adult. These adults were measured the
same way as the individuals that were captured opportunistically. Data collectors acted
in accordance with the Guidelines for the Use of Wild Birds in Research (Fair et al., 2010),
and the approved Institutional Animal Care and Use Committee protocol. All New Mexico
State and Federal Scientific Permits were obtained for all years of the project.
2.3. Statistical Analysis
We compiled all records of birds captured two or more times. This dataset contains
the band numbers, dates of capture and recapture, nest box locations, ages, and sexes
of adults and newly banded and fledged bluebirds (hereafter referred to as fledglings)
between the years 1997 and 2019. These records were compiled to include the year, age, sex,
location, and elevation of each nest box each year the bird was captured. For consistency,
all fledglings that were banded in the nest were considered adults the next year(s) they
were recaptured. Therefore, the adult category was made up of “after hatch year”’, “second
year”, and “after second year” birds.
Elevation and distances between nest boxes (straight-line distances) were obtained
using a geographic information system (Google Earth Pro 2020, version 7.3.3.7786, Google
LLC, Mountain View, CA, USA). Data were visualized at the individual bird level for
changes in elevation in subsequent years. To determine the positive, negative, and absolute
changes in elevation from one year to the next, we used each bird movement or recapture
as a data point. We used a linear model to test whether individual nesting increased in
elevation over time (model residuals were normally distributed).
We used linear mixed models (LMM) and model selection to find the best variables
that predicted both changes in distance and changes in elevation (absolute change in
elevation). Our predictor variables were initial nesting elevation, year initially captured,
sex, and age (fledgling/adult). We included initial nesting elevation to determine if where
a bird initially nested predicted where it nested subsequently. Our random effect was bird
ID. Year was not included as a random effect because it explained very little variation. We
tested for multicollinearity using variance inflation factor (VIF) and found that all variables
had values less than 3. We ran all combinations of models with an interaction between sex
and age, and ranked the models using Akaike Information Criterion (AICc). Models with
delta AICc values less than 2 were considered similar models in terms of predictability.
Variables were considered significant if 95% confidence intervals did not cross zero. Models
were run using the lme4 package [
37
], and model selection was performed using the
MuMIn package [38].
We used chi-square tests to compare numbers of adults and fledglings and numbers
of males and females to determine whether there were differences between groups in
upslope and downslope shifts. Differences in elevation and distance between nest boxes
were tested using Mann–Whitney U tests. Elevation and distance data were not normally
distributed; and therefore, we opted to use non-parametric statistics. For those analyses for
which birds were recaptured multiple times, we used a linear mixed model with bird ID
as a random effect to test for these differences. All data analyses were completed in the
statistical software program R (version 3.6.1 [
39
]). Data were visualized using the ggplot2
package [40].
3. Results
We recaptured a total of 182 individual bluebirds from 1997 to 2019, which consisted
of 95 adults and 87 birds that were captured initially as fledglings. Of the 182 individuals,
there were 148 birds that were recaptured only once. Twenty-nine birds were recaptured
Animals 2021,11, 2457 5 of 12
twice and 4 birds were recaptured three times. One individual was recaptured four times.
These totals do not include same-year recaptures. These recaptures resulted in 222 data
points (148 + 58 + 12 + 4) on potential individual bird movements (135 adults and 87
fledglings; Table 1). Each bird was plotted according to the year in which it was initially
captured and then subsequently recaptured with the corresponding elevation of the nest
box in which it nested for that year (Figure 1a). Birds that were first banded as fledglings
were recorded at the location of their parents’ nests. These fledglings were considered
adults the next year(s) they were captured.
Table 1.
The numbers of movements that were upslope, downslope, and showed no change for
adults and fledglings. Both adults and fledglings have been split into males and females.
Number of
Upslope Shifts
Number of
Downslope
Shifts
Number
Showing No
Change
Total
Adults 34 30 71 135
Males 14 9 21 44
Females 20 21 50 91
Fledglings 34 31 22 87
Males 24 24 22 70
Females 10 7 0 17
Total 68 61 93 222
Most individuals nested at approximately the same elevation year after year. However,
a few birds changed elevation dramatically between subsequent nesting periods, both
in the upslope and downslope directions (Figure 1a). From 2000 to 2019, birds generally
nested at higher elevations later in the study period (i.e., 2011 to 2019) compared to the
early part of the study period (i.e., 2000 to 2010). To test for an increase in elevation over
time, we calculated the mean nesting elevation for each recaptured bird and plotted this
against the last year each bird was captured (Figure 1b). All birds were adults because
banded fledglings were considered adults when they were recaptured during a subse-
quent year. There was a significant positive relationship between year and elevation (LM:
estimate = 15.69, SE ±1.21, t = 12.93, p< 0.001, R2= 0.48; Figure 1b).
For absolute change in elevation, the top linear mixed model included sex and age.
This model was greater than 2 delta AICc units from the next model. In this model, age
(adults: estimate [95% CIs] =
−
11.65 [
−
16.34 to
−
7.48]; SE = 1.99; df = 73.60; t =
−
5.87) and
sex (females: estimate [95% CIs] = 10.98 [5.46 to 16.43]; SE = 2.76; df = 196.49; t = 3.97) were
both significant. Fledglings and females had greater changes in elevation than adults and
males, respectively. For change in distance, the top models included sex, age, and year.
This model was greater than 2 delta AICc units from the next model. Age (age, adults:
estimate [95% CIs] =
−
287.26 [
−
440.18 to
−
170.49]; SE = 54.48; df = 38.13; t =
−
5.27) and
sex (sex, females: estimate [95% CIs] = 466.84 [236.54 to 694.14]; SE = 115.69; df = 184.68;
t = 4.04
) were both significant in this model, while year was not significant (estimate [95%
CIs] = −6.69 [−27.04 to 13.76]; SE = 10.43; df = 163.99; t = −0.64).
We calculated the change in elevation, or lack of change, from the initial nest location
to the subsequent nest location for adults and fledglings (Figure 2) and for male and female
fledglings (Figure 3). The biggest upslope change in elevation for a bird between recapture
years was 152.1 m, and the biggest downslope change in elevation was 93.8 m. Both
of these were female fledglings. There were 68 upslope movements and 61 downslope
movements (Table 1). There were 93 movements with no change in elevation, meaning
they nested in the same nest box each capture (Table 1). There was no significant difference
in the absolute elevation change between upslope movements and downslope movements
(LMM: estimate =
−
1.18
±
2.18, df = 23.61, t =
−
0.54, p= 0.60). The greatest distance moved
between nest boxes was 4.5 km, by a female fledgling in the downslope direction.
Animals 2021,11, 2457 6 of 12
Animals 2021, 11, x FOR PEER REVIEW 6 of 12
Figure 1. (a) The movement of nesting locations by elevation for individual birds year to year. Or-
ange circles depict a bird that was banded as a nestling, and blue circles depict adults. Movements
of an individual bird (n = 182) are tracked by dotted lines. (b) Linear regression of nesting elevation
over time for recaptured birds (n = 182). Dots represent the mean (±SE) nesting elevation per bird.
There was a significant positive relationship over time (LM: estimate = 15.69, SE ± 1.21, t = 12.93, p <
0.001, R2 = 0.48). Area shaded blue is the 95% confidence interval.
For absolute change in elevation, the top linear mixed model included sex and age.
This model was greater than 2 delta AICc units from the next model. In this model, age
(adults: estimate [95% CIs] = −11.65 [−16.34 to −7.48]; SE = 1.99; df = 73.60; t = −5.87) and
sex (females: estimate [95% CIs] = 10.98 [5.46 to 16.43]; SE = 2.76; df = 196.49; t = 3.97) were
both significant. Fledglings and females had greater changes in elevation than adults and
males, respectively. For change in distance, the top models included sex, age, and year.
This model was greater than 2 delta AICc units from the next model. Age (age, adults:
estimate [95% CIs] = −287.26 [−440.18 to −170.49]; SE = 54.48; df = 38.13; t = −5.27) and sex
Figure 1.
(
a
) The movement of nesting locations by elevation for individual birds year to year. Orange
circles depict a bird that was banded as a nestling, and blue circles depict adults. Movements of an
individual bird (n= 182) are tracked by dotted lines. (
b
) Linear regression of nesting elevation over
time for recaptured birds (n= 182). Dots represent the mean (
±
SE) nesting elevation per bird. There
was a significant positive relationship over time (LM: estimate = 15.69, SE
±
1.21, t = 12.93, p< 0.001,
R2= 0.48). Area shaded blue is the 95% confidence interval.
Animals 2021,11, 2457 7 of 12
Animals 2021, 11, x FOR PEER REVIEW 7 of 12
(sex, females: estimate [95% CIs] = 466.84 [236.54 to 694.14]; SE = 115.69; df = 184.68; t =
4.04) were both significant in this model, while year was not significant (estimate [95%
CIs] = −6.69 [−27.04 to 13.76]; SE = 10.43; df = 163.99; t = −0.64).
We calculated the change in elevation, or lack of change, from the initial nest location
to the subsequent nest location for adults and fledglings (Figure 2) and for male and fe-
male fledglings (Figure 3). The biggest upslope change in elevation for a bird between
recapture years was 152.1 m, and the biggest downslope change in elevation was 93.8 m.
Both of these were female fledglings. There were 68 upslope movements and 61
downslope movements (Table 1). There were 93 movements with no change in elevation,
meaning they nested in the same nest box each capture (Table 1). There was no significant
difference in the absolute elevation change between upslope movements and downslope
movements (LMM: estimate = −1.18 ± 2.18, df = 23.61, t = −0.54, p = 0.60). The greatest
distance moved between nest boxes was 4.5 km, by a female fledgling in the downslope
direction.
Figure 2. Age differences in elevational changes between nesting locations from one year to the next
for each bird captured two or more times (n = 222). Each point represents an individual bird move-
ment. An individual can have multiple points if it was captured more than two times. Orange circles
depict a bird that was banded as a fledgling, and blue circles depict adults. The size of each point
corresponds to the straight-line distance between nest boxes. Inset: Mean (±SE) elevation difference
(absolute values) between fledglings and adults. Fledglings changed elevation more than adults
(LMM: estimate = −8.48 ± 1.83, df = 90.97, t = −4.64, p < 0.001).
Figure 2.
Age differences in elevational changes between nesting locations from one year to the next for each bird captured
two or more times (n= 222). Each point represents an individual bird movement. An individual can have multiple points
if it was captured more than two times. Orange circles depict a bird that was banded as a fledgling, and blue circles
depict adults. The size of each point corresponds to the straight-line distance between nest boxes. Inset: Mean (
±
SE)
elevation difference (absolute values) between fledglings and adults. Fledglings changed elevation more than adults (LMM:
estimate = −8.48 ±1.83, df = 90.97, t = −4.64, p< 0.001).
The numbers of adult (n= 64) and fledgling (n= 65) movements that were upslope and
downslope did not significantly differ (Chi-square test: X
2
< 0.001, df = 1, p= 1.0;
Table 1
),
meaning that adults and fledglings did not show patterns in how they were moving
between boxes. However, when numbers of adults and fledglings that did not move were
included, there was a significant difference between adults and fledglings (Chi-square test:
X
2
= 16.21, df = 2, p< 0.001; Table 1). Specifically, more adults remained at the same nest
box than fledglings (71 adults vs. 22 fledglings). There was a significant difference in the
absolute change in elevation between adults and fledglings (LMM:
estimate = −8.48 ±1.83,
df = 90.97, t =
−
4.64, p< 0.001; Figure 2inset); fledglings changed elevation more than
adults. In those fledglings that moved to different nest boxes, there was no significant
difference between upslope elevation changes and downslope elevation changes (Mann–
Whitney U: W = 579, p= 0.50). Likewise, there was no significant difference between
upslope and downslope elevation changes for adults (LMM: estimate = 0.14
±
1.59, df
= 11.57, t = 0.086, p= 0.93), meaning that there were no patterns in elevation shifts for
individual birds. Adults and fledglings differed significantly in the straight-line distance
traveled between nest boxes (LMM: estimate =
−
218.61
±
50.72, df = 50.45, t =
−
4.31,
p< 0.001; Figure 2); fledglings moved significantly greater distances than adults.
The changes in elevation between male and female fledglings were also compared
(Figure 3). Out of the 87 fledglings that returned to breed in the same general area, 70
(80.4%) were male. There was not a significant difference between the numbers of male and
female fledglings that shifted upslope and downslope (Chi-square test: X
2
= 0.118,
df = 1,
p= 0.73;
Table 1). However, when numbers of males and females that did not move were
included, there were significantly more males (n= 22) than females (n= 0) that did not
Animals 2021,11, 2457 8 of 12
move (Chi-square test: X
2
= 7.63, df = 2, p= 0.02; Table 1). There was a significant difference
between fledgling male and female absolute changes in elevation (Mann–Whitney U test:
W = 719, p< 0.001; Figure 3inset); females changed elevation more than males. Male and
female fledglings differed significantly in the straight-line distance traveled between nest
boxes (Mann–Whitney U test: W = 772, p< 0.001), such that females dispersed farther than
males (Figure 3).
Animals 2021, 11, x FOR PEER REVIEW 8 of 12
Figure 3. Sex differences in elevational changes between nesting locations from one year to the next
for fledglings captured twice (n = 87). Each point represents an individual bird movement. Green
circles depict females, and blue circles depict males. The size of each point corresponds to the
straight-line distance between nest boxes. Inset: Mean (±SE) elevation difference (absolute values)
between males and females. Females changed elevation more than males (Mann–Whitney U test: W
= 719, p < 0.001).
The numbers of adult (n = 64) and fledgling (n = 65) movements that were upslope
and downslope did not significantly differ (Chi-square test: X2 < 0.001, df = 1, p = 1.0; Table
1), meaning that adults and fledglings did not show patterns in how they were moving
between boxes. However, when numbers of adults and fledglings that did not move were
included, there was a significant difference between adults and fledglings (Chi-square
test: X2 = 16.21, df = 2, p < 0.001; Table 1). Specifically, more adults remained at the same
nest box than fledglings (71 adults vs. 22 fledglings). There was a significant difference in
the absolute change in elevation between adults and fledglings (LMM: estimate = −8.48 ±
1.83, df = 90.97, t = −4.64, p < 0.001; Figure 2 inset); fledglings changed elevation more than
adults. In those fledglings that moved to different nest boxes, there was no significant
difference between upslope elevation changes and downslope elevation changes (Mann–
Whitney U: W = 579, p = 0.50). Likewise, there was no significant difference between
upslope and downslope elevation changes for adults (LMM: estimate = 0.14 ± 1.59, df =
11.57, t = 0.086, p = 0.93), meaning that there were no patterns in elevation shifts for indi-
vidual birds. Adults and fledglings differed significantly in the straight-line distance trav-
eled between nest boxes (LMM: estimate = −218.61 ± 50.72, df = 50.45, t = −4.31, p < 0.001;
Figure 2); fledglings moved significantly greater distances than adults.
The changes in elevation between male and female fledglings were also compared
(Figure 3). Out of the 87 fledglings that returned to breed in the same general area, 70
(80.4%) were male. There was not a significant difference between the numbers of male
and female fledglings that shifted upslope and downslope (Chi-square test: X2 = 0.118, df
= 1, p = 0.73; Table 1). However, when numbers of males and females that did not move
were included, there were significantly more males (n = 22) than females (n = 0) that did
Figure 3.
Sex differences in elevational changes between nesting locations from one year to the next for fledglings captured
twice (n= 87). Each point represents an individual bird movement. Green circles depict females, and blue circles depict
males. The size of each point corresponds to the straight-line distance between nest boxes. Inset: Mean (
±
SE) elevation
difference (absolute values) between males and females. Females changed elevation more than males (Mann–Whitney U
test: W = 719, p< 0.001).
Some of the fledglings did not change elevation and were even captured from the
same nest box in which they were born. Twenty-two male fledglings came back to the
same nest the following year. In addition, out of the 34 birds captured more than two times,
14 were initially captured as fledglings. Of these 14 fledglings, 12 (87.5%) were male, the
philopatric sex.
4. Discussion
Environmental changes are causing birds to change behaviors, adapt to these changes,
or shift their geographic ranges [
20
,
21
,
24
]. Geographical range shifts can be due to individ-
ual movements each year or through colonization and establishment events at the leading
edge of a species distribution. The main goal of this study was to understand elevational
changes and dispersal distances of individual western bluebird adults and fledglings in
subsequent years. Knowing how species are responding to environmental changes will
help predict behavioral responses and aid in management practices in the future.
We found no patterns in individual changes from year to year. The number of indi-
vidual movements in the downslope direction was similar to that in the upslope direction.
Likewise, the magnitude of change in elevation was the same in the downslope direction
Animals 2021,11, 2457 9 of 12
as the upslope direction. Most birds nested in the same nest box year after year, especially
adult birds. This is contrary to our first hypothesis that individual birds nest at higher
elevations each year and that these changes contribute to population shifts over time. We
saw a general upslope pattern in nesting over time (Figure 1b), which is the same pattern
documented in the same population in Wysner et al. [
22
] and consistent with other patterns
in birds globally [
15
,
19
,
41
,
42
]. Our results suggest that this shift over 22 years was not
caused by consistent changes in individuals’ nesting preferences year to year.
We cannot reject our second hypothesis, which was that immigrating individuals are
tracking preferred climate conditions and nesting higher, on average, than the current
population. Although we have no data regarding the proportion of birds immigrating
to the area, this scenario seems likely for three reasons. First, adult birds that re-nest
and breed the following year generally nest in the same general location (i.e., at the same
elevation). Second, fledglings that returned to the same area to breed showed greater
elevation changes, and distances traveled, the following year than adults. However, these
fledglings showed similar elevational changes upslope as downslope. This is also contrary
to our hypothesis that fledgling movements would be consistently upslope. Third, site
fidelity of fledglings is fairly low in our population, suggesting that the majority of birds
have immigrated from other populations.
Pioneering individuals have been shown to have different traits than other members
of the population for birds, reptiles, amphibians, and mammals [
25
,
43
–
45
]. Morpholog-
ical, behavioral, and physiological traits may predispose certain individuals to disperse
farther [
25
–
27
]. It is currently unclear if bluebirds that nest higher in our population have
different traits that make them predisposed to disperse farther, especially upslope into the
leading edge of population expansion. In an expanding population of western bluebirds in
the northwestern United States, dispersal is biased toward highly aggressive males [
28
,
29
].
Western bluebird fledglings can acquire nest sites and territories from parents and relatives,
or they can disperse to a new population and compete for their own territory [
28
]. Based
on our data, it seems that fledglings are staying near their parents’ nest and territory rather
than dispersing upslope to the leading edge of the population. Bluebirds that immigrate
to the population and nest at higher elevations may be more aggressive dispersers or are
simply tracking local climatic conditions upon arrival.
The fledglings that returned to breed were mostly males (80.4%). Male fledglings
moved significantly less in elevation and distance the year after they fledged compared to
female fledglings. This is similar to other studies that have shown male western bluebirds
to be philopatric to their natal site [
32
,
35
,
46
], and is consistent with our hypothesis. Males
are known to return to their natal site to help their parents raise young, and can even help
their parents with a second nest in the same season [
33
,
35
,
47
]. By helping, these helper
males increase their, and their parents’, inclusive fitness [
48
]. Although, females showed
greater elevational changes than males, the magnitude of changes was the same in the
upslope and downslope direction, contrary to our hypothesis. A future question to address
would be whether males and females differ in their immigration rates, and whether there
are sex differences in pioneer individuals at the leading edge of range shifts.
Our sample size was relatively small despite the long timespan for which we collected
data. We have banded 6597 bluebirds since this nest box network was initiated, and
have a recapture rate of 3.4%. However, this is based on actively mist-netting adults
near nest boxes as well as opportunistic recaptures (i.e., grabbing adults off the nest).
Future work will involve tracking nestlings using radio transmitters to compare male
and female dispersal and determine where fledglings disperse to. Fledglings, particularly
males, may come back to their parents’ nest to help and may also have their own nest.
However, the majority of fledglings disappear from our study area and may disperse
into new populations. In this population, there is generally high fledging success, even
when parasitized by nest parasites [
34
]. After fledging, predation is a large risk factor for
fledglings and may also contribute to why we may see less recaptures of fledglings [49].
Animals 2021,11, 2457 10 of 12
5. Conclusions
Changes to plant and animal distributions are difficult to predict because behavioral,
morphological, and physiological traits vary greatly between individual species. We found
that the western bluebirds in this study did not significantly move upslope or downslope in
elevation year to year in response to environmental change. This suggests that geographic
range shifts are not occurring at the individual level, but rather through immigrants nesting
at higher elevations, although more research is needed to explicitly test this hypothesis.
Future work should focus on understanding the traits of bluebirds at the upslope edge of
the range compared to the rest of the population on the Pajarito Plateau [
50
]. This would
provide more information regarding potential mechanisms for species range shifts, as
predictions on a per species basis still remain a challenge.
Author Contributions:
Conceptualization, J.M.F., C.D.H. and A.W.B.; methodology, C.D.H. and
J.M.F.; formal analysis, A.W.B. and E.J.A.; investigation, E.J.A., C.D.H. and J.M.F.; resources, J.M.F.
and C.D.H.; data curation, E.J.A., C.D.H., J.M.F. and A.W.B.; writing—original draft preparation,
E.J.A. and A.W.B.; writing—review and editing, C.D.H. and J.M.F.; visualization, A.W.B. and E.J.A.;
supervision, C.D.H. and J.M.F.; project administration, C.D.H. and E.J.A.; funding acquisition, C.D.H.
and J.M.F. All authors have read and agreed to the published version of the manuscript.
Funding:
This research was funded by the Environmental Restoration Program, Los Alamos Na-
tional Security, LLC, operator of the Los Alamos National Laboratory under Contract No. DE-A52-
06NA25396 with the U.S. Department of Energy and Triad National Security, LLC, current operator
of Los Alamos National Laboratory, under Contract No. 89233218CNA000001.
Institutional Review Board Statement:
Data collectors acted in accordance with the Guidelines
for the Use of Wild Birds in Research (Fair et al., 2010), and the approved Los Alamos National
Laboratory’s Institutional Animal Care and Use Committee protocol. All New Mexico State and
Federal Scientific Permits were obtained for all years of the project.
Data Availability Statement:
The datasets generated during and/or analyzed during the current
study are available from the corresponding author on reasonable request.
Acknowledgments:
We thank the interns, technicians, and staff past and present who have helped
in this long-term study.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.
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