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Learning capabilities enhanced in harsh environments: A common garden approach


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Previous studies have suggested that the ability to inhabit harsh environments may be linked to advanced learning traits. However, it is not clear if individuals express such traits as a consequence of experiencing challenging environments or if these traits are inherited. To assess the influence of differential selection pressures on variation in aspects of cognition, we used a common garden approach to examine the response to novelty and problem-solving abilities of two populations of black-capped chickadees (Poecile atricapillus). These populations originated from the latitudinal extremes of the species's range, where we had previously demonstrated significant differences in memory and brain morphology in a multi-population study. We found that birds from the harsh northern population, where selection for cognitive abilities is expected to be high, significantly outperformed conspecifics from the mild southern population. Our results imply differences in cognitive abilities that may be inherited, as individuals from both populations were raised in and had experienced identical environmental conditions from 10 days of age. Although our data suggest an effect independent of experience, we cannot rule out maternal effects or experiences within the nest prior to day 10 with our design. Nevertheless, our results support the idea that environmental severity may be an important factor in shaping certain aspects of cognition.
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Learning capabilities enhanced in harsh
environments: a common garden approach
Timothy C. Roth*, Lara D. LaDage and Vladimir V. Pravosudov
Department of Biology, University of Nevada, 1664 North Virginia Street, MS 314,
Reno, NV 89557, USA
Previous studies have suggested that the ability to inhabit harsh environments may be linked to advanced
learning traits. However, it is not clear if individuals express such traits as a consequence of experiencing
challenging environments or if these traits are inherited. To assess the influence of differential selection
pressures on variation in aspects of cognition, we used a common garden approach to examine the
response to novelty and problem-solving abilities of two populations of black-capped chickadees (Poecile
atricapillus). These populations originated from the latitudinal extremes of the species’s range, where we
had previously demonstrated significant differences in memory and brain morphology in a multi-
population study. We found that birds from the harsh northern population, where selection for cognitive
abilities is expected to be high, significantly outperformed conspecifics from the mild southern popu-
lation. Our results imply differences in cognitive abilities that may be inherited, as individuals from
both populations were raised in and had experienced identical environmental conditions from 10 days
of age. Although our data suggest an effect independent of experience, we cannot rule out maternal
effects or experiences within the nest prior to day 10 with our design. Nevertheless, our results support
the idea that environmental severity may be an important factor in shaping certain aspects of cognition.
Keywords: behavioural flexibility; environmental harshness; learning; neophobia;
natural selection; problem-solving
Animals living in energetically challenging (e.g. unpre-
dictable and/or harsh) environments should benefit from
advanced cognitive abilities (Dukas 1998; Shettleworth
1998,2009). One aspect of advanced cognition often
examined is behavioural flexibility or learning (Reader
2003), also termed plasticity or innovation (sensu Lefebvre
et al. 1997). Rather than a fixed response to a given stimu-
lus, behavioural flexibility allows for the expression of a
variety of different behavioural outcomes under different
contexts based on previous experiences (Dukas 1998;
Reader 2003). Such flexibility seems to be adaptive and
therefore has strong ecological and evolutionary relevance
(Price et al. 2003;Biernaskie et al. 2009). For example,
various aspects of learning or behavioural flexibility may
play key roles in the success of biological invasions (e.g.
Sol et al.2002,2005a;Martin & Fitzgerald 2005), the
occupation of anthropogenic environments (e.g.
Echeverria & Vassallo 2008), as well as in some of the
basic ecological differences between populations and
species (e.g. Greenberg 1983,1984,1990;Liker &
Bokony 2009). However, the ultimate source of the
production of these cognitive differences is poorly
understood. Can all individuals of the species express
advanced learning traits simply as a consequence of
experiencing a challenging environment, or are these
traits an inherited product of differential selection
pressures in these environments?
Evidence for the relationship between increased
learning capabilities and harsh environments has been
observed in numerous taxa. For example, in an intra-
specific comparison, Martin & Fitzgerald (2005) found
that an actively invading population of house sparrows
(Passer domesticus) had reduced levels of neophobia when
compared with a long-established population. Moreover,
several large-scale comparative analyses have shown posi-
tive relationships between living in anthropogenic habitats
(i.e. those characterized by novelty and complexity) and
feeding innovation in birds (Lefebvre et al. 1997;Sol
et al. 2005a) as well as mammals (Lefebvre et al. 2004).
Thus, taxa that more often show innovative foraging tac-
tics appear to be those that are more successful at
invading novel environments. These patterns have also
been shown to correlate with brain size (or forebrain
size), suggesting a morphological basis to the variance
in cognition (Lefebvre et al. 1997;Solet al.2005a). Unfor-
tunately, the comparative studies that make up the bulk of
the large-scale evidence for the environmental complexity–
cognition relationship (e.g. Lefebvre et al.1997,2004;Sol
et al.2002,2005a) only present a ‘snapshot’ of traits influ-
enced heavily by selection pressures in evolutionary history,
which are generally unknown. These comparisons cannot
be used to address the influence of specific experiences
and population-level selection pressures. To address the
effects of selection pressures on cognition, it may be
more effective to examine differences in populations that
are currently experiencing potentially different selection
The relationship between harsh environments and cog-
nitive abilities is not limited to learning. Theory suggests
that food-caching birds living in more harsh climates
should cache more and have better spatial memory than
those in more mild climates (Krebs et al. 1989;Sherry
*Author for correspondence (
Proc. R. Soc. B (2010) 277, 3187–3193
Published online 2 June 2010
Received 23 March 2010
Accepted 10 May 2010 3187 This journal is q2010 The Royal Society
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et al. 1989;Pravosudov & Grubb 1997;Pravosudov &
Lucas 2001). Indeed, previous work supports the basis
for this relationship between environmental harshness
and memory, as birds from higher latitudes (i.e. more
harsh climates) had better spatial memory (Pravosudov &
Clayton 2002), probably owing to increased demands for
accurate cache retrieval. Moreover, these behavioural
differences seem to have a neurological basis. We have
previously demonstrated a gradation of hippocampal attri-
butes across populations, where hippocampal size and
neuron number decrease with declining latitude
(Pravosudov & Clayton 2002;Roth & Pravosudov 2009).
Overall, then, there is strong theoretical and empirical evi-
dence supporting a relationship between environmental
severity and one aspect of cognition—spatial memory—
along a latitudinal gradient in food-caching birds.
We extend this logic from memory for cache retrieval
to learning. Because of the drastically lower temperatures,
shorter winter day length and greater precipitation
(snow cover) in the northern when compared with the
southern parts of their range (see Roth & Pravosudov
2009), northern populations of food-caching birds must
eat more to fulfil their daily energy requirements
(Pravosudov & Grubb 1997;Pravosudov & Lucas
2001), but have less daylight in which to do it and
encounter more obstacles (snow) that conceal food.
Traits that increase food acquisition rates and increase
the accuracy and speed of decision-making should be
adaptive under these time-limited and energetically
demanding conditions (Lefebvre et al. 1997;Pravosudov &
Grubb 1997;McLean 2001;Pravosudov & Lucas 2001;
Hills 2006; see also Sol et al. 2005b). It would be naive
to presuppose that selection should work on a single
behavioural/morphological trait. Instead, selection may
result in the enhancement of numerous cognitive traits
produced in various ways depending upon the selection
pressures in the population. The ultimate effect would
be that individuals with such traits might have a higher
probability of recovering food, and hence of survival
during the winter. Indeed, birds from the more harsh
northern populations tend to have larger telencephalic
regions relative to body mass (a trait associated with
enhanced cognitive abilities; Lefebvre et al.1997,2004;
Sol et al.2002,2005a) than those in the south. For
example, based on our previous study, the telencephalon
volume of chickadees from northern populations are
larger than those from southern populations (ordered
heterogeneity test: r
¼0.774, p,0.010; methods
from Rice & Gaines 1994; based on data from Roth &
Pravosudov 2009). Interestingly, body mass showed the
opposite trend with birds from southern populations
being significantly heavier than those from the north
(ordered heterogeneity test: r
¼0.899, p,0.001;
methods from Rice & Gaines 1994; based on mass data
in Roth & Pravosudov 2009). Note that we do not
intend to make causal statements about the overall or rela-
tive size of the brain and cognitive ability, but only point
out their association. See Roth et al.(2010)for a detailed
discussion of these topics.
The goal of this study was to examine the environ-
mental complexity cognition relationship using a
common garden approach in a food-caching model
system. To avoid the problems associated with comparing
different species (see Macphail 1996), yet to assess two
aspects of the cognitive abilities of different populations
experiencing differential selection pressures, we examined
the response to novel object and problem-solving tasks of
hand-raised black-capped chickadees (Poecile atricapillus).
We have chosen to work with the two populations at the
latitudinal extremes of the species’s range—Alaska (AK)
and Kansas (KS)—as they showed the largest morpho-
logical differences (in both relative hippocampal volume
and in telencephalon volume) along the previously
demonstrated multi-population gradient of environ-
mental harshness (Roth & Pravosudov 2009). Thus, it is
from these most geographically and climatically distinct
populations that we would expect to see the largest differ-
ences in learning, should they exist.
Our prediction was that birds from the climatically
harsh northern population (AK), which had the larger
brains in our previous work, would outperform conspeci-
fics from the more mild southern population (KS), which
had smaller brains. Given that these individuals were
raised in the laboratory and had experienced identical
environmental conditions (at least since day 10 after
hatching), difference between these populations may
suggest a component to learning that may potentially be
the result of differential selection pressures within their
respective populations.
(a)Collection sites
Black-capped chickadees (Poecile atricapillus) were collected
during late May and early June 2009 from nests at the latitu-
dinal extremes of their range (Anchorage, AK: 618100N,
1498530W; Manhattan, KS: 398080N, 968370W). Two
chicks were taken from each nest, with siblings used in the
two different tests (see below). At both sites, we collected
chicks from both natural nests and those in nest boxes (con-
structed from wood and PVC) in a wide range of habitats
from anthropogenic to very ‘natural’. Average temperatures
during the respective collection periods were as follows:
AK: max ¼18.3 +1.18C, min ¼7.2 +0.48C; KS: max ¼
24.8 +1.48C, min ¼8.7 +1.18C. The average day length
during collection was 1149 min for AK and 856 min for KS.
Chicks were approximately 10 days old at the time of col-
lection and were hand-raised indoors on site until they were
approximately 18 days old. To retain consistency in the
hand-raising environment between the two sites, T.C.R.,
assisted by the same technician, worked at both locations.
In addition, the indoor environment was as similar as pos-
sible. Temperature was maintained between 21 and 238C
and lighting conditions were similar and on the same sche-
dule (15 : 9, L : D), beginning the first day of collection.
Chicks were transported to the University of Nevada,
Reno, via ground (from KS) and air (from AK), in the same
containers (wood nesting boxes; see below). We attempted
to transport the chicks as rapidly as possible and control the
environment as much as possible during transportation.
(b)Hand-rearing and housing
All chicks were fed a diet of: Orlux Handmix formula
(Versele-Laga, Deinze, Belgium); wax worms (Pyralidae sp.);
meal worms (Tenebrio molitor); phoenix worms (Hermetia
illucens); crickets (Acheta domesticus); a slurry consisting of
dog food (Canidae, San Luis Obispo, CA), cat food (Natura
EVO, Santa Clara, CA), Orlux Insect Patee Premium and
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Orlux Handmix; and nut powder pellets consisting of
pulverized pine nuts (Pinus koraiensis), peanuts (Arachis hypo-
gaea), sunflower seeds (Helianthus sp.) and Insect Patee. Food
types were systematically cycled throughout the day and were
offered every 20 min during daylight hours, so the chicks from
both locations ate at approximately the same frequency and
for the same time period during the day. Food (same diet as
above less Handmix, all in whole form, plus Roudybush
Crumbles and Purina Game Starter) and water were provided
ad libitum after birds reached independence (approx. 3035
days after hatch).
During hand-rearing, chicks were housed in groups of
four to six individuals in 17 17 24 cm wooden boxes
filled with sawdust to simulate nest cavities. At the fledgling
stage (approx. 1820 days after hatch), chicks were housed
as sibling pairs in 120 42 60 cm wire cages. At the dis-
persal stage (approx. 60 days after hatching), all birds were
moved into a solitary, permanent arrangement in 60
42 60 cm wire cages. Sex was estimated via wing chord
measurements. To reduce aggression between males, birds
were placed in an M/F/F/M arrangement within a row of
four cages (all within visual contact). The populations were
systematically partitioned as AK/KS/AK/KS within these
rows, with siblings located in different rooms.
Beginning in early August and until mid-October,
the light cycle gradually shifted (approx. 0.5 h per week) to
9 : 15 (L : D). All tests occurred on this light cycle. Tests
began when birds were approximately five months old.
However, because of the asynchronous breeding of the two
populations, the AK birds were on average slightly less than
three weeks younger than the KS individuals (average age
at testing: AK, 20.8 weeks; KS, 23.7 weeks).
(c)Learning tests
We focused on two aspects of learning: problem-solving and
the response to novelty. Innovative problem-solving is a goal-
oriented form of learning, whereby an animal encounters a
novel problem with a known goal or reward (often food)
and must perform a series of novel steps to achieve the goal
(Dukas 1998; e.g. Webster & Lefebvre 2001;Keagy et al.
2009). The speed required to solve the task is frequently
used as an indication of the animal’s ability to learn (e.g.
Carlier & Lefebvre 1996). Habituation to a non-threatening
novel object can also be viewed as a form of this type of learn-
ing. Although a novel object may initially be perceived as
risky, through the process of examination the animal learns
that the object is not a threat. As learning is inherent to
both of these processes, the performance on these tasks prob-
ably reflects selection on the ability to learn (sensu Dukas 1998).
(i) Problem-solving test
Problem-solving tests were conducted approximately 2 h
after lights-on from 4 9 November 2009. This test was per-
formed with 24 birds (12 AK, 12 KS) from different nests.
The problem-solving test involved removing galvanized
steel washers (3.5 cm diameter, 1.5 cm diameter hole;
roughly equal to the mass of the birds, approx. 15 g) covered
with clear 3M acetate from a 3 5 grid of 1.5 cm wells
drilled into a wooden board (40 18 cm) containing wax
worms. All birds had been fully habituated to the boards
(total duration of prior exposure .30 h) in their home
cages. Birds were habituated to the washers for 8 h the day
prior to the test. During this habituation, washers were
secured to the boards (adjacent to, but not covering, the
wells) with double-sided tape so that they could be touched,
but not moved. Wax worms were offered in 8 of the 15 wells,
and habituation was considered successful if birds took all
wax worms (which occurred in all cases).
A pre-trial control occurred approximately 1 h before
lights-off the day prior to the test. During this control, one
wax worm was placed on each board, and we recorded the
latency to remove the worm (300 s max). The boards were
then removed. The following morning, birds were allowed
to feed for 1 h after lights-on, and then deprived of food
for 1 h before the problem-solving trial. The boards were
introduced into the cages with one wax worm in each of
the same eight wells as during the habituation period, but
now washers covered all 15 wells. The birds could see the
worms, but could only retrieve a worm by moving the
washer. The birds could not puncture the acetate.
The trials occurred in the home cages, with birds in the
cage row (i.e. two AK, two KS) tested simultaneously. All
trials were observed remotely with a live video feed to another
room and recorded using Sony DCR-SR300 and DCR-SR47
digital video cameras on tripods. We recorded the latency
(in seconds) to land on the board and the latency to take
the first worm (3600 s max). We considered the problem
solved when the bird had taken a worm. To control for
motivation, a post-trial control was performed. After
3600 s, one wax worm was placed on top of the board and
we recorded the latency to take the worm (300 s max).
(ii) Novelty test
Novelty tests were conducted 0.5 h after lights-on from 18 21
October 2009. This test was performed with 25 birds (12 AK,
13 KS) from different nests (siblings of the birds in the pro-
blem-solving test). All birds were deprived of food 0.5 h
prior to lights-off the evening before testing and until after
the test the following day (approx. 2 h after lights-on). Birds
were recorded using video as in the previous test. We recorded
the cumulative latency to approach and remove food (a single
wax worm) from a control (usual type 300 ml circular stainless
steel) and novel feeder (usual type feeder modified with paint
and protruding bolts) in an A : B : A (control : treatment : con-
trol) design. The feeders were placed in the centre of the home
cage floor and the birds were recorded for 300 s (during the
controls) and 1800 s (during the treatment). We recorded
the latency (in seconds) to touch the feeder, to sit on the
feeder and to take the worm from the feeder for both control
and treatment trials.
(d)Statistical analyses
Repeated-measures analysis of variance tests were used to
test the overall models for population (AK and KS) and
within-subject effects (controls and treatment). In addition,
we used planned comparisons to confirm that controls were
not significantly different within populations. We also com-
pared the habituation time in the novelty test (treatment
minus pre-control times) and the time to solve the problem
(latency to take the worm minus latency to land on the
board) with t-tests. Data were log-transformed for all ana-
lyses; raw data are presented in figures for clarity (means +
s.e. are reported;
Problem-solving was assessed by the time required to
remove a transparent, weighted cover from a well
Learning in harsh environments T. C. Roth et al. 3189
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containing a food item. The motivation to land on the
testing apparatus was assessed with pre- and post-treat-
ment trials of a single wax worm placed on the board.
The individuals from AK landed on the testing board,
uncovered the well and removed the wax worm signifi-
cantly faster than those from KS ( population: F
32.888, p,0.001; within-subject: F
¼181.825, p,
0.001; figure 1). There was no effect of motivation or
habituation to the experimental set-up, as there were no
differences between pre- and post-treatment times in
either population (AK: p¼0.092; KS: p¼0.320). The
time to solve the task (latency to eat minus latency to
land) was significantly longer for the KS population
¼25.340, p,0.001).
(b)Response to novelty
The response to novelty was assessed by the latency to
approach, sit on and finally take a food item from a
novel feeder. Motivation was controlled with both pre-
and post-treatment exposures of the same food item in
a familiar feeder. There was a large and significant differ-
ence between the two populations in the latency to
approach (population: F
¼13.691, p¼0.001;
within-subject: F
¼92.724, p,0.001), sit on
(population: F
¼12.359, p¼0.002; within-subject:
¼104.262, p,0.001) and take the food item
from (population: F
¼11.528, p¼0.002; within-
subject: F
¼142.876, p,0.001; figure 2) the novel
feeder . The individuals from the KS population took sig-
nificantly longer than those from the AK population to
approach (t
¼23.349, p¼0.003), sit on
¼22.972, p¼0.007) and take the wax worm from
¼23.159, p¼0.004) the novel feeder relative to
the pre-treatment control. Comparisons of the pre- and
post-treatment controls showed that motivation, the ten-
dency to feed on the floor of the cage and/or the testing
set-up did not play a substantive role in the results
(touch: AK, p¼0.181; KS, p¼0.019; sit: AK, p¼
0.146; KS, p¼0.014; take: AK, p¼0.027; KS, p¼
0.005; figure 2). Although we did see small, yet
significant, differences in some pre/post comparisons,
the latencies were lower in the post-trials in all cases.
This suggests some habituation in both populations
within the study, but these differences are very minor
relative to the overall treatment effect (figure 2).
We found significant differences in problem-solving and
neophobia between two populations originating from
drastically different environmental conditions. Our results
suggest that selection has produced variance in the ability
to learn (sensu Dukas 1998), as the chickadee population
from the more harsh environment (AK) were faster in
problem-solving and less neophobic relative to their
southern conspecifics (KS) despite being raised in identi-
cal environments since age 10 days post-hatch. Thus,
there seems to be the possibility of an inherited com-
ponent (genetic and/or maternal effects) to the speed of
latency (s)
pre land eat post
Figure 1. Latency to the completion of a problem-solving
task (removing a weighted, transparent cover from a well con-
taining a wax worm) in black-capped chickadees. Pre- and
post-treatment exposure of a wax worm on the testing appar-
atus controlled for motivation, the tendency to feed on the
floor of the cage and habituation to the testing set-up.
Filled circles, Kansas; open circles, Alaska.
latency to touch (s)
latency to sit (s)
latency to take worm (s)
re treatment
Figure 2. The response to novelty of black-capped chickadees
as assessed by the latency to (a) approach, (b) sit on and
(c) take a wax worm from a novel feeder. Pre- and post-
treatment exposure of a wax worm in a familiar feeder
controlled for motivation and the tendency to feed on the
floor of the cage. Filled circles, Kansas; open circles, Alaska.
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problem-solving and habituation to novelty within this
species, although we could not rule out any experiential
or environmental effects taking place prior to day 10,
when blind chicks were in a dark nest cavity. As both of
these traits are aspects of learning (Dukas 1998;Reader
2003;Lefebvre et al. 2004), our results suggest that selec-
tion may favour enhanced learning abilities in more
extreme climates, at least in this species.
We found differences in both of our measures of learn-
ing, suggesting that there may be a difference in the
selection pressures for these aspects of learning between
these populations from extremely different climates. This
does not imply, however, that all aspects of learning will
necessarily be different or that all aspects of cognition will
necessarily be superior in the more northern populations.
One very broad interpretation of our results could be that
selection might enhance all types of cognitive qualities in
more harsh climates. However, Pravosudov & Clayton
(2002) reported differences in spatial memory but not
colour memory in a two-population comparison in this
same species. This may suggest that the selection on cogni-
tion is quite complex, and differing selection pressures in
different populations must be considered thoroughly
(Dukas 1998;Shettleworth 1998). On the other hand,
the test for colour memory by Pravosudov & Clayton
(2002) was purposefully simplistic (a single colour) as the
goal of that study was to test for motivation to perform a
spatial task and not to test for differences in memory for
colour per se. Still, it is not to say that selection should
enhance all cognition. Rather, selection should enhance
cognitive abilities that may affect fitness under specific
environmental conditions. So, in the case of the food-
caching chickadee, selection for spatial memory (which is
important for successful cache recovery) has been shown
to be particularly important for the northern population,
but presumably under less selection in the southern popu-
lation (Pravosudov & Clayton 2002). Selection for colour
memory, however, may not be a function of climate in
this system as both populations seem to use it similarly
(Pravosudov & Clayton 2002). According to the adaptive
specialization hypothesis, specific differences observed
between the populations should be a function of the specific
selection regimes experienced by those populations.
Given that we have very specific predictions based on
our previous study of multiple populations along a latitu-
dinal gradient (Roth & Pravosudov 2009), we emphasize
that these results are not likely to be due to chance alone.
Our selection of the two populations in this study was
based on our previous multi-population studies of the
relationship between environmental harshness, memory
and brain morphology, as well as theoretical differences
(e.g. Pravosudov & Grubb 1997;Pravosudov & Lucas
2001;Pravosudov & Clayton 2002;Roth & Pravosudov
2009). As we had already shown the large-scale pattern
between the environment and the brain, our next objec-
tive was to examine the relevance of individual
experiences by comparing the differences in learning
capabilities between populations with maximal differ-
ences in brain morphology. Although the inclusion of
additional populations would have increased the scope
of our comparison, we were limited by logistical and
ethical constraints.
Our data suggest the possibility of an inherited effect
on learning; however, there are two important caveats to
this interpretation. First, owing to the logistical difficulty
of hand-raising very small birds, we collected chicks from
the nest at approximately 10 days of age. Thus, it is pos-
sible that experiences during early development (from
hatching to day 10) could have produced the observed
results. We think that this is unlikely as it is around day
10 that black-capped chickadees’ eyes begin to open,
and any experiences would have occurred in a dark nest-
ing cavity. Thus, the visual conditions that the two
populations experienced were probably very similar. How-
ever, we cannot rule out the possibility that thermal
differences or differences in parental feeding had an
effect on our results. Second, we cannot rule out the
possibility of maternal effects. It is possible that our
observed differences could have been due to physiological
decisions made by the mother prior to egg laying. For
example, stressed mothers may deposit increased levels
of corticosterone into their eggs to ‘prepare’ the young
for a challenging environment (Chin et al. 2009). This
possibility, in particular, may explain the differences in
response to novelty. It is possible that exposure to corti-
costerone during development may produce a response
in specific brain regions such as the amygdala, which
may affect neophobia responses (Burns et al. 1996). How-
ever, we argue that these maternal effects, should they
exist, are likely to be the result of selection as well. Thus,
it is still not the individual chicks’ experiences that produce
such effects. Moreover, differences in corticosterone
would not clearly explain the differences in problem-
solving abilities between the populations. Still, as a
consequence of these caveats, we interpret our results as
evidence of a possible inherited effect, since maternal
effects are an aspect of inheritance, but suggest that
future studies consider breeding experiments to fully dis-
sociate these factors.
Although one possible explanation of our results is a
heritable component to cognition, we acknowledge that
complex behaviours are probably the result of both inheri-
tance and experience. For example, Greenberg (1983,
1984) supports an experiential explanation for specific
responses such as neophobia. These studies suggest that
differences in foraging niches themselves may be the pro-
duct of ontogenetic experiences produced in part by
neophobia. Experiences may still be important and may
produce variation in addition to that generated through
inheritance. It is possible that the ultimate differences in
foraging niches created by experience as realized in
Greenberg’s (1984) study may be the result of genetic
differences in response to novelty between different
species. In other words, using Greenberg’s approach,
some of the ecological differences between generalists
and specialists may be due to genetic difference in
response to novelty. Ontogenetic experience may then
be the mechanism by which a particular species is ‘intro-
duced’ to (and maintained in) its habitat. This will
require further study.
Overall, our data suggest a large difference in some
aspects of the cognitive abilities of black-capped chicka-
dees that may be due in part to differential selection
pressures within different environments. Based on
theory and our previous work comparing brains of chick-
adees from multiple populations across a gradient of
environmental harshness, we suggest that these results
are probably due to the climatic severity of the
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environments. A complementary explanation is that the
observed differences are not the result of climatic harsh-
ness per se, but of range expansion. Several studies
suggest an important role of behavioural flexibility in
the success of biological invasions (Martin & Fitzgerald
2005). It is possible that the AK population has more
recently (on an evolutionary scale) been involved in
range expansion, at least since the retreat of the glaciers
during the last Ice Age (Harrap & Quinn 1995). Thus,
rather than an effect of current climatic conditions, the
AK population may possess faster learning skills owing
to their ancestors’ recent range expansion. It is important
to point out that the range expansion and environmental
harshness hypotheses are not mutually exclusive; both
could be relevant to our study system. Both of these
hypotheses, nevertheless, imply a selective component
to the differences between the populations, suggesting
that these cognitive traits are important, adaptive and
probably the product of natural selection rather than
individual experiences alone.
We are grateful to E. Horne, B. Van Slyke, K. Hampton and
Kansas State University’s Konza Prairie Biological Station
for their assistance at our Kansas site. We are also indebted
to C. Handel, V. Jorgensen, M. Pajot and the United States
Geological Survey’s Alaska Science Center for their
assistance at our Alaska site. C. Freas and J. Ream assisted
in nestling collection. C. Freas and G. Hanson assisted in
animal care and maintenance. We are also grateful to
K. Otter for logistical advice, and to our many colleagues
(too numerous to mention) for advice on hand-rearing
chickadees. This research was funded in part by grants
from the National Science Foundation (IOB-0615021) and
the National Institutes of Health (MH079892 and
MH076797). Birds were collected under United States
Fish and Wildlife (MB022532), Alaska (09-020), Kansas
(SC-039-2009) and Nevada (S30942) permits. This
research was supervised by the University of Nevada,
Reno, IACUC (protocol no. A05/06-35), and followed
all federal and local guidelines for the use of animals in
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... For example, despite the mechanisms of habituation are phylogenetically very old and their functioning is almost identical in most animal species (Rankin et al., 2009), the rate at which different individuals of the same species habituate to the repetition of the same stimulus varies significantly. Inter-individual differences in habituation have been found in a wide range of species from humans (Blanch et al., 2014;LaRowe et al., 2006;Mangan and O'Gorman, 1969;O'Gorman, 1977) and other primates (Allan et al., 2020) to birds (e.g., Roth et al., 2010), rats (e.g., Glowa and Hansen, 1994), and lizards (Rodríguez-Prieto et al., 2011. The origin of these differences is unknown. ...
... However, life-history is not the only reason for inter-individual differences in habituation. Differences in habituation can be inherited as demonstrated, for example, by Glowa and Hansen (1994); but see also Roth et al. (2010). The authors found that the habituation to a loud sound in three strains of rats (Ratticus norvegicus) selected based on the amplitude of their startle response (high-, intermediate-, and low-amplitude) differ in two aspects: the habituation rate (i.e., response decrement relative to the initial startle response) and the number of trials necessary to reach an asymptotic level of response, and complete habituation. ...
... While the study by Glowa and Hansen (1994) supports the notion that inter-individual differences in habituation are inherited, their results must be interpreted with caution as a genetic cause for inter-individual differences independent of experience cannot be completely ruled out. Indeed, even when it is possible to trace the genetic relatability between individuals of a species, altricial animals like rats (and the same holds true for the study that we cited by Roth et al., 2010 on black-capped chickadees, Poecile atricapillus) spend some amount of time with their parents after birth. Parental effects or experiences within the nest prior to the habituation test can have exerted considerable influence in shaping individuals' behaviour. ...
Habituation to novel stimuli has been associated with behavioural differences among individuals in numerous animal species. Because the habituation mechanisms depend on previous experiences with a stimulus, one would expect individuals to develop their habituation capacity based on the life experiences that also shape their behavioural traits. And indeed, in adult lizards, exploratory behaviour and body size correlates with habituation. However, here we show that the same factors correlate with habituation of domestic chicks reared under controlled laboratory conditions and tested in the first 3 days after hatching. This result indicates that the covariation between habituation, exploration, and body size does not necessarily depend on experience. Rather, it represents an innate association between exploratory behaviour and risk assessment, which may provide an immediate survival advantage to new-borns of this precocial avian species.
... For instance, climate variability has been advanced as a possible driver of among-species variation in cognition: species subjected to erratic precipitation or temperature regimes may require enhanced cognitive performance to deal with temporally fluctuating availability of resources (e.g., food, water, heat, shelter) and threats (e.g., predators, competitors) (Mettke-Hofmann 2014). Support for this idea has been found, for example, across populations of chickadees (Roth et al. 2010b;Freas et al. 2012) and chimpanzees (Kalan et al. 2020), and among bird species with brain size as a proxy of cognitive performance (Sol et al. 2005a;Schuck-Paim et al. 2008;Fristoe et al. 2017;Sayol et al. 2018). However, this effect can go either way. ...
... A fair number of studies have tested the above ideas by comparing the cognitive performance of species inhabiting contrasting environments (e.g., see review in Henke-von der Malsburg et al. 2020), but a number of issues complicate the interpretation of their results. First, many of these studies have used relative brain size as an anatomical proxy of cognition, an approach that is increasingly being criticized (Healy and Rowe 2007;Roth et al. 2010b; Cauchoix and Chaine 2016). Brain size, whether absolute or relative, may be a poor predictor of cognitive performance in general (Cauchoix and Chaine 2016) or of the specific cognitive skills under selection (Hartley et al. 2014). ...
Cognition is an essential tool for animals to deal with environmental challenges. Nonetheless, the ecological forces driving the evolution of cognition throughout the animal kingdom remain enigmatic. Large‐scale comparative studies on multiple species and cognitive traits have been advanced as the best way to facilitate our understanding of cognitive evolution, but such studies are rare. Here, we tested 13 species of lacertid lizards (Reptilia: Lacertidae) using a battery of cognitive tests measuring inhibitory control, problem‐solving, and spatial and reversal learning. Next, we tested the relationship between species’ performance and a) resource availability (temperature and precipitation), habitat complexity (NDVI) and habitat variability (seasonality) in their natural habitat, and b) their life‐history (size at hatching and maturity, clutch size and frequency). Although species differed markedly in their cognitive abilities, such variation was mostly unrelated to their ecology and life‐history. Yet, species living in more variable environments exhibited lower behavioural flexibility, likely due to energetic constrains in such habitats. Our standardised protocols provide opportunities for collaborative research, allowing increased sample sizes and replication, essential for moving forward in the field of comparative cognition. Follow‐up studies could include more detailed measures of habitat structure and look at other potential selective drivers such as predation. This article is protected by copyright. All rights reserved
... In this review, we bring together ideas from the traditionally disparate fields of cognitive ecology and disease ecology to examine evidence for infection-linked cognitive impairment, discuss why it may occur, and consider its ecological and evolutionary implications. In a century characterized by global changes that accelerate pathogen emergence [18,19] while simultaneously favoring cognitive flexibility [20,21], there is an urgent need to better understand the interactions between animal cognition and infection and their potential consequences for wild populations. ...
... Unfortunately, cognitive performance might be particularly important in degraded habitats if learning, flexibility, and innovation confer a survival advantage [21] and provide a cognitive buffer in stressful or novel environments [20,78]. Indeed, at the species level, innovation (estimated as the propensity to eat new foods or use novel feeding techniques) is associated with reduced global extinction risk and positive population trends in birds [79]. ...
Infectious disease is linked to impaired cognition across a breadth of host taxa and cognitive abilities, potentially contributing to variation in cognitive performance within and among populations. Impaired cognitive performance can stem from direct damage by the parasite, the host immune response, or lost opportunities for learning. Moreover, cognitive impairment could be compounded by factors that simultaneously increase infection risk and impair cognition directly, such as stress and malnutrition. As highlighted in this review, however, answers to fundamental questions remain unresolved, including the frequency, duration, and fitness consequences of infection-linked cognitive impairment in wild animal populations, the cognitive abilities most likely to be affected, and the potential for adaptive evolution of cognition in response to accelerating emergence of infectious disease.
... An alternative way to control for motivation could be to conduct motivation tests before a task and control for it during analysis, for example by measuring latency to approach a free food source (e.g. [74,76]) or through latency to approach the task apparatus out of choice (e.g. [77]). ...
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Metabolic rate determines life processes and the physiological requirements of an individual, and has recently been implicated as a driver of inter-individual variation in behaviour, with positive correlations associated with boldness, exploration and aggressive behaviours being recorded. While the link between metabolism and personality has been explored, little is known about the influence of metabolism on cognitive abilities. Here we used juvenile female chickens (Gallus gallus domesticus) to investigate the relationships between metabolic rate at rest, short-term memory, personality, and dominance. Resting metabolic rates of the chicks were measured over a three-week period, concurrently with measures of short-term memory using an analogue of the radial arm maze. We also measured latency to leave the shelter (boldness), neophobia (fear of novel objects) and dominance within a group, both before and after short-term memory trials. We found that metabolic rate did not explain inter-individual differences in short-term memory, personality traits or dominance, suggesting that energy allocated to these traits is independent of individual metabolic rate, and providing evidence for the independent energy-management hypothesis. Differences in short-term memory were also not explained by boldness or neophobia. Variation in behaviour in chicks, therefore, appears to be driven by separate, currently unknown variables.
... Reductions in learning and memory could affect any number of fitness-related traits in thrushes. The tests we used are related to resource acquisition, e.g., foraging and managing unpredictable environments 32,33 . Swainson's thrushes do not form pairs on the wintering grounds 39 , but difficulties acquiring resources on the wintering grounds could carry-over to spring migration and the breeding season, affecting hybrid survival on migration and reproductive success on the breeding grounds 40,41 . ...
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Hybrid zones can be used to identify traits that maintain reproductive isolation and contribute to speciation. Cognitive traits may serve as post-mating reproductive isolating barriers, reducing the fitness of hybrids if, for example, misexpression occurs in hybrids and disrupts important neurological mechanisms. We tested this hypothesis in a hybrid zone between two subspecies of Swainson’s thrushes (Catharus ustulatus) using two cognitive tests—an associative learning spatial test and neophobia test. We included comparisons across the sexes and seasons (spring migration and winter), testing if hybrid females performed worse than males (as per Haldane’s rule) and if birds (regardless of ancestry or sex) performed better during migration, when they are building navigational maps and encountering new environments. We documented reduced cognitive abilities in hybrids, but this result was limited to males and winter. Hybrid females did not perform worse than males in either season. Although season was a significant predictor of performance, contrary to our prediction, all birds learned faster during the winter. The hypothesis that cognitive traits could serve as post-mating isolating barriers is relatively new; this is one of the first tests in a natural hybrid zone and non-food-caching species. We also provide one of the first comparisons of cognitive abilities between seasons. Future neurostructural and neurophysiological work should be used to examine mechanisms underlying our behavioral observations.
... Также у них относительно больший передний мозг. Скорее всего, эти отличия врождённые: уровень кортизола не различается между популяциями, и лучшую обучаемость «северян» не объяснить материнским эффектом от стресса, переданным повышением кортизола в желтке яйца [Roth et al. 2010]. Больший мозг, лучшее решение проблемных задач и т. д. когнитивные «достижения» в урболандшафтах, на больших высотах, в других неблагоприятных средах обитания дают их носителям большую кладку, однако связаны с «платой» в виде повышенного риска гибели гнезда от хищников и других внешних воздействий (данные по большим синицам, черноголовым и горным гаичкам [Lefebre, Aplin, 2017]). ...
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We have studied important differences between the urbanization of "wild" species of birds and mammals and the domestication of domestic ones, together with the difference in stressors to which they adapt. In the first case, these are the most general characteristics of the urban environment - an extreme level of heterogeneity, instability and variability compared to any non-urban landscapes. It requires "urban" birds to quickly change nesting sites, feeding habitats, feeding methods and other features of biology in the wake of habitat changes, local and citywide, with the development of the ability to predict them, live, constantly "jumping from ice floe to ice floe" as opposed to sustainability existence in "rural" or "forest" populations. In the second, it is simply a change in the reaction to people, equipment, and animal care from an anxious-defensive to a friendly-interesting one. In the process of urbanization of "wild" species of birds, the brain increases, as in other variants of extreme habitats. Cognitive progress is achieved by each "urban" individual independently, due to the developing impact of the urban environment on its psyche, thanks to the growth of the possibilities for evaluating and predicting its dynamics using precursor signals. Therefore, it is preceded by an increase in the courage of individuals, a better differentiation of stimuli by them, a separation of significant ones from all the others (to which indifference is growing). On the contrary, during domestication, the brain decreases, cognitive progress in the new environment is achieved due to the “cooperative thinking”, social “prompts” of people and relatives. Behavioral changes during the urbanization of "wild" species are also sharply different from domestic ones. An analysis of aggression, defensive, exploratory behavior, attitudes towards the novelty of "urban" birds and mammals shows that they do not become "kind" or "trustful" (as happened with domestic animals). On the contrary: their aggression increases, along with courage and a better response to potential danger, a more accurate differentiation of it from “just anxiety”, to which they become more indifferent. As the species urbanizes, the behavior of each of the individuals becomes more diverse. Aggression, courage, flight from potential danger or vice versa, taking risks, exploring new places and objects no longer characterize individuals, but situations. All behavior is made as flexible and contextual as possible, with better recognition of the specifics of the situation, better choice of the mode of action, more accurate “dosing” of reactions according to the goal. This is the developing role of the urban environment. Urbanization destroys the behavioral syndrome: the correlations existing in the original populations between exploration, courage, aggression, risk taking, and in some cases other parameters. The launches of the forms of behavior characterized by each of these features in "urban" birds are mutually independent, in contrast to "rural" individuals. This maximizes the accuracy of the choice of behavior in a problem situation and its switching to another according to the situation, which is opposite to the changes associated with domestication and inconsistent with their explanation based on the D.K. Belyaev model. Urbanization changes the life strategy in a completely different way than domestication. The strategy of the newly formed urban population in the r-K-continuum shifts towards a “more pronounced K” compared to the initial one, due to a set of changes that mutually determine and reinforce each other: 1) Population growth occurs to a greater extent due to the lengthening of the average life expectancy, while reducing the reproduction of individuals (partly similar to the demography of Homo sapiens); 2) The primacy of future reproduction in the best conditions, with a directed movement to search for them “following the dynamics of the urban environment”, compared with the maximum reproductive effort “here and now”; 3) Greater “fractionality” of the reproductive potential of “urban” individuals, subdivided into a greater number of breeding attempts compared to the original population, with greater mobility and contextuality of each of them. Domesticated species behave in the opposite way and shift the strategy towards the "r-pole" of the continuum. A partly similar result during urbanization and domestication is achieved by opposite changes in the life strategy, behavior, cognitive characteristics, attitudes towards humans, and other aspects of the "natural history" of the species. The “individuality genes” DRD4 and SERT, which are under positive selection during urbanization, do not participate in domestication-related changes in the genome. On this basis, an evolutionary scenario for the urbanization of "wild" species is proposed, explaining on the same basis both differences and similarities with domestication. Modern cities, their expansion and association into groups (urbanization) are very interesting as arenas of the fastest microevolutionary processes that "separate" the urban population from the original and adapt it mainly to the most general features of the urban environment, but only gradually, then, and not completely - to specific influences that it "dumps" on individuals of this species. This happens in each region separately: the newly formed populations in different cities change parallel to each other (the same is true for urbanization changes in different, completely unrelated species), but do not approach each other in any way, remaining genetically closer to the local initial ones than to urban populations in other regions. Human-modified ("man-made") landscapes create extreme habitats, cities are its quintessence. We consider the adaptation of "wild" species of birds, partly mammals, to such changes, occurring through directed invasion into it and rapid changes in the population structure, ecology and behavior of individuals, restoring viability in new conditions and facilitating their even greater development, with penetration into areas, all more and more modified by man. The settlement of the urban environment is the culmination of all processes of this kind. Microevolution goes faster here than in natural landscapes (the faster, the stronger the transformation, with a maximum in the urban environment), but "gets stuck" at the stage of adaptation. Form formation - the appearance of "urban" subspecies, species, etc. - does not happen, despite the growing separation of "urban" populations from the original ones.
... procuring food from novel source, eating novel items; Griffin, Netto, and Peneaux 2017) is often found in urban birds (Audet, Ducatez, and Lefebvre 2016) and mammals (Mangalam and Singh 2013). It has been argued that pressure to innovate stems from inhabiting harsher, more complex, unique environments (Roth, LaDage, and Pravosudov 2010;Kozlovsky, Branch, and Pravosudov 2015), but few such studies have explored this innovative ability in multiple contexts. Griffin, Netto, and Peneaux (2017) reviewed the literature on innovation in urban birds and found in six of eight studies that urban birds showed a higher level of innovation than their rural counterparts. ...
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Recent human-induced transformations to the environment are significantly impacting wild animal populations. Whereas some animals thrive due to these changes, others are being extinguished. Many studies have attempted to identify behavioural traits (e.g. personality, diet versatility, cognition) that allow some animals to succeed in human-dominated landscapes, but few have studied multiple traits or environmental contexts concurrently, despite the fact that different environments may require different types of behavioural performance. We presented house finches (Haemorhous mexicanus) captured from urban, suburban, and rural sites with two different environmental problems to solve (escaping from a confinement and finding food in multiple feeding structures) and measured the success and speed of solving the challenge as well as activity levels and stress behaviours of the birds. We found that urban birds were better at solving the escape challenge, but there was no difference in finding a hidden food source. In addition, we found that birds who solved the escape challenge were more active than those who did not solve this problem, although we observed no such behavioural difference in the food challenge. These results indicate that, because problem-solving challenges can vary across environments, certain types of innovation may be prioritized over others in urban-dwelling species.
... Furthermore, behavioral ecologists have independently found the same pattern within non-human primates (Navarrete et al., 2016), birds (e.g. Roth et al., 2010;Sol et al., 2010) and other species (Gillooly & McCoy, 2014;Jiang et al., 2015), giving the theory parsimony. In particular, the evidence from birds shows that the relationship between absolute latitude or winter temperature to brain size is only present in non-migrating birds, a prediction of the cold winters theory that is difficult to explain otherwise. ...
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Since Lynn and Vanhanen's book IQ and the Wealth of Nations (2002), many publications have evidenced a relationship between national IQ and national prosperity. The strongest statistical case for this lies in Jones and Schneider's (2006) use of Bayesian model averaging to run thousands of regressions on GDP growth (1960-1996), using different combinations of explanatory variables. This generated a weighted average over many regressions to create estimates robust to the problem of model uncertainty. We replicate and extend Jones and Schneider's work with many new robustness tests, including new variables, different time periods, different priors and different estimates of average national intelligence. We find national IQ to be the "best predictor" of economic growth, with a higher average coefficient and average posterior inclusion probability than all other tested variables (over 67) in every test run. Our best estimates find a one point increase in IQ is associated with a 7.8% increase in GDP per capita, above Jones and Schneider's estimate of 6.1%. We tested the causality of national IQs using three different instrumental variables: cranial capacity, ancestry-adjusted UV radiation, and 19 th-century numeracy scores. We found little evidence for reverse causation, with only ancestry-adjusted UV radiation passing the Wu-Hausman test (p < .05) when the logarithm of GDP per capita in 1960 was used as the only control variable.
Selective pressures emerging from the environmental complexity shapes variation in vertebrate brain size. Generally, larger brains are linked to better cognitive abilities under complex environments. However, the general assumption that species with larger brains have better cognitive abilities remains heavily controversial, and it is also lack of experimental support. Here, we investigated whether larger-brained individuals displayed increased foraging and escaping abilities by designing three standardized experiments where we provided the tasks of foraging and escaping for individuals in three species of the paddy frogs. The results showed that successful individuals with foraging and escaping had relatively larger brains than unsuccessful ones for all experiments. We provided new experimental evidence for whole-brain size as a predictor of cognitive abilities in the paddy frogs. Our findings support the claim that brain size can reflect an animal’s foraging and escaping abilities and enhance our understanding of larger brains evolved with better cognitive abilities in frogs.
The cognitive abilities of birds are remarkable: hummingbirds integrate spatial and temporal information about food sources, day-old chicks have a sense of numbers, parrots can make and use tools, and ravens have sophisticated insights in social relationships. This volume describes the full range of avian cognitive abilities, the mechanisms behind such abilities and how they relate to the ecology of the species. Synthesising the latest research in avian cognition, a range of experts in the field provide first-hand insights into experimental procedures, outcomes and theoretical advances, including a discussion of how the findings in birds relate to the cognitive abilities of other species, including humans. The authors cover a range of topics such as spatial cognition, social learning, tool use, perceptual categorization and concept learning, providing the broader context for students and researchers interested in the current state of avian cognition research, its key questions and appropriate experimental approaches.
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Adaptive views of learning predict that natural selection should lead to differences in specialized learning abilities between animals that face different ecological pressures. Group-living is thought to favour social learning, but previous comparative work suggests that differences between gregarious feral pigeons (Calumba livia) and territorial Zenaida doves (Zenaida aurita) exceed the specialized effect on social tasks predicted by the adaptive hypothesis. In this paper, we show that group-foraging Zenaida doves from Barbados learn an individual shaping task more quickly than territorial Zenaida doves from a site 9 km away. These results suggest that the scramble competition associated with group-foraging favours several types of learning, both social and non-social, and that its effects are more wide-ranging than previously thought. Since genetic isolation between Zenaida dove populations is highly unlikely, the results also suggest that differences in foraging ecology may lead to different learned responses to local reward contingencies as well as natural selection for different genotypes affecting learning. In some cases, the standard comparative prediction of ecologically-correlated learning differences may therefore not distinguish between adaptive specialization and general process theories.
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In the temperate zone, permanent-resident birds and mammals that do not hibernate must survive harsh winter conditions of low ambient temperature, long nights, and reduced food levels. To understand the energy management strategy of food-hoarding birds, it has been hypothesized that such birds respond to increased starvation risk by increasing the number of their hoards rather than by increasing their fat reserves and that they cache early in the day and retrieve their caches later to achieve fat reserves necessary to survive the night. We tested these hypotheses by observing the responses in captivity of a caching bird, the tufted titmouse (Parus bicolor), to the combined influenced of reduced predictability of food and naturally) occurring ambient temperature and photoperiod. When the food supply was unpredictable, birds significantly increased both internal fat reserves at dusk and external food caches. Initially leaner birds tended to increase their fat reserves to a greater extent and initially fatter birds tended to cache more food and to fly significantly less. Half the birds also increased their dawn and mean daily body mass. All birds tended to forage, gain body mass, and cache food at significantly lower rates in the morning and at significantly higher rates in the evening. Cache retrieval showed the opposite trend, with birds retrieving most of their caches in the morning. Our results do not support the hypothesis that caching birds increase caching rate but not body mass under an unpredictable food regime. Instead fat reserves and food caches are both important complementary sources of energy in food-hoarding birds. Energy management by wintering birds occurs in response to a number of biotic and abiotic factors acting simultaneously; thus future models must incorporate independent variables in addition to the state of the food supply and time of day.
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Neophobia, or the hesitancy to approach a novel food item, object, or place, is an important factor influencing the foraging behavior of animals. Environmental factors (e.g. rapid anthropogenic changes, migration into new habitats) are associated with novelty in feeding ecology and may affect neophobic responses. Mechanisms that underlie the differential neophobic response may involve complex interactions with the environment: post-fledging experience in a greater diversity of habitats or in habitats that are more complex may contribute to reduced neophobia. In a previous study, it was observed that some urbanized species, in particular house sparrows (Passer domesticus) and shiny cowbirds (Molothrus bonariensis) show high levels of neophobia. This study was carried out in a suburban marsh of Cortaderia selloana, a relatively simple and predictable ecosystem as compared to urban areas. For this reason, in the present study, we explored novelty responses of bird species inhabiting an urban area, representing a complex environment. The results were compared to those obtained previously in the suburban marsh. We found unexpectedly high levels of neophobia in house sparrows, but shiny cowbirds showed a somewhat neophilic response. In the presence of novel objects, house sparrows tended to enter the feeders alone, while shiny cowbirds tended to forage in groups. We found no differences in latencies to forage or in visit duration between habitat types, but the proportion of individuals that visited the feeders when novel objects were present was lower in the urban area for house sparrows and eared doves (Zenaida auriculata). The results are discussed in the context of invasion success and feeding innovation in shiny cowbirds.
The effects of bilateral excitotoxic lesions of 3 major sources of afferents to the ventral striatum (nucleus accumbens) were compared on an open field test of food neophobia allowing the choice between familiar and novel food. Whereas lesions of the basolateral amygdala and ventral subiculum had qualitatively similar effects to reduce food neophobia (although not affecting the latency to eat), amygdala lesions increased and the ventral subiculum decreased locomotor activity. In contrast, damage to the ventromedial prelimbic prefrontal cortex only affected initial food choice and latency measures. By comparison, excitotoxic lesions of the nucleus accumbens itself and intra-accumbens infusion of the N-methyl-D-aspartate (NMDA) receptor antagonist AP5 increased activity and attenuated food neophobia. Results are discussed in terms of the role of limbic and prefrontal neuronal networks converging in the nucleus accumbens to control different aspects of the behavioral response to novelty.
This paper reviews behavioural, neurological and cognitive correlates of innovation at the individual, population and species level, focusing on birds and primates. Innovation, new or modified learned behaviour not previously found in the population, is the first stage in many instances of cultural transmission and may play an important role in the lives of animals with generalist or opportunistic lifestyles. Within-species, innovation is associated with low neophobia, high neophilia, and with high social learning propensities. Indices of innovatory propensities can be calculated for taxonomic groups by counting the frequency of reports of innovation in published literature. These innovation rate data provide a useful comparative measure for studies of behavioural flexibility and cognition. Innovation rate is positively correlated with the relative size of association areas in the brain, namely the hyperstriatum ventrale and neostriatum in birds, and the neocortex and striatum in primates. Innovation rate is also positively correlated with the reported variety of tool use, as well as interspecific differences in learning. Current evidence thus suggests similar patterns of cognitive evolution in primates and birds. [ABSTRACT FROM AUTHOR] Copyright of Animal Biology is the property of VSP International Science Publishers and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
A new testing procedure is described concerning ordered alternative hypotheses when three or more populations are categorized by class. The test is specifically designed for use in complex testing applications frequently found in biological research where the isotonic regression and Jonckheere-Terpstra test cannot readily be applied. The test has both parametric and nonparametric applications. Significance tables for the test are provided for both large and small sample sizes, and a power analysis relative to isotonic regression is described for the case of the one-way layout.
During the winter in Panama, ie. during the nonbreeding season, the bay-breasted warbler Dendroica castanea is a generalized forager compared to the chestnut-sided warbler D. pensylvanica. Individuals of 4 other species of Dendroica (caerulescens, coronata, magnolia, tigrina) were tested in similar experiments to see how bay- breasted and chestnut-sided warblers compared with the genus as a whole. Consistent with field observations, chestnut-sided warblers obtained hidden mealworms from fewer unfamiliar objects than did bay- breasted warblers. They approached a similar number of objects, but were more timid and ambivalent. Individuals of all 6 species of Dendroica had consistent rankings in how rapidly they fed at the model microhabitats. This variation had a species-specific component, with bay-breasted warblers feeding most rapidly and chestnut-sided warblers feeding most hesitantly. The number of microhabitats visited by a warbler is thus the result of a dynamic interaction of attraction and fear. Individuals and species with greater aversion to novel foraging situations may be more specialized than less neophobic warblers.-from Author
The hypothesis that quantitative differences in neophobia underlie varitaion in ecological plasticity was tested by comparing feeding responses of wild-caught immature song, Melospiza melodia, and swamp, M. georgiana, sparrows in captivity. The song sparrow is a habitat generalist and good colonizing species, while the swamp sparrow specializes on marsh habitats. As predicted by the neophobia hypothesis, captive swamp sparrows showed a greater hesitancy to feed in the presence of a variety of novel objects than did song sparrows. Swamp sparrows made significantly more approaches to the food source without feeding when a novel object was present. There was a consistent difference in latency among individuals within each species. Habituation reduced latencies in the most neophobic sparrows, but sometimes almost a week of constant exposure was required before swamp sparrows fed without hesitation.
The links between ecology, behavioural plasticity and brain size are often tested via the comparative method. Given the problems in interpretating comparative tests of learning and cognition, however, alternative measures of plasticity need to be developed. From the short notes section of nine ornithological journals, two separate, exhaustive data sets have been collated on opportunistic foraging innovations in birds of North America (1973-1993;N=196) and the British Isles (1983-1993;N=126). Both the absolute and relative frequencies (corrected for species number per order) of innovations differ between bird orders in a similar fashion in the two geographical zones. Absolute and relative frequency of innovations per order are also related to two measures of relative forebrain size in the two zones. The study confirms predicted trends linking opportunism, brain size and rate of structural evolution. It also suggests that innovation rate in the field may be a useful measure of behavioural plasticity.