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Fitness and hormonal correlates of social and ecological stressors of female yellow-bellied marmots

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The effects of social and ecological stressors on female reproductive success vary among species and, in mammals, previous reviews have identified no clear patterns. However, few studies have simultaneously examined the relation between social rank and stressors and the relationships among rank, stressors and reproductive success. We used a long-term data set to study free-living facultatively social yellow-bellied marmots, Marmota flaviventris, to isolate the relationship between female social dominance rank and faecal glucocorticoid metabolite (FGM) levels (our measure of basal stress) in adult females. In addition, we examined whether rank and FGM levels were associated with reproductive success by quantifying the probability of an individual successfully weaning a litter and, for those who did, litter size. High-ranking females had lower FGM levels and larger litters. However, females with the highest FGM levels were significantly more likely to wean a litter. Importantly, body condition (as measured by previous year's mass) was also positively associated with breeding and with weaning larger litters. Thus, although low-ranking females probably experienced more social stressors than high-ranking females and although adult females often delayed their first reproduction until they were of a sufficient mass, our results suggest that elevated baseline FGM levels failed to mediate reproductive suppression. Perhaps, in species like marmots that have only a single chance per year to reproduce, reproductive suppression should be rare. These results highlight the importance of social status, body condition and predator abundance on determining reproductive success in highly seasonal breeders.
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Fitness and hormonal correlates of social and ecological stressors of
female yellow-bellied marmots
Daniel T. Blumstein
a
,
b
,
*
, Kathryn N. Keeley
a
, Jennifer E. Smith
c
a
Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, U.S.A.
b
The Rocky Mountain Biological Laboratory, Crested Butte, CO, U.S.A.
c
Department of Biology, Mills College, Oakland, CA, U.S.A.
article info
Article history:
Received 22 February 2015
Initial acceptance 20 March 2015
Final acceptance 30 September 2015
Available online
MS. number: A15-00144R2
Keywords:
ecological stressor
glucocorticoid
reproductive success
reproductive suppression
social rank
social stressor
yellow-bellied marmot
The effects of social and ecological stressors on female reproductive success vary among species and, in
mammals, previous reviews have identied no clear patterns. However, few studies have simultaneously
examined the relation between social rank and stressors and the relationships among rank, stressors and
reproductive success. We used a long-term data set to study free-living facultatively social yellow-bellied
marmots, Marmota aviventris, to isolate the relationship between female social dominance rank and
faecal glucocorticoid metabolite (FGM) levels (our measure of basal stress) in adult females. In addition,
we examined whether rank and FGM levels were associated with reproductive success by quantifying
the probability of an individual successfully weaning a litter and, for those who did, litter size. High-
ranking females had lower FGM levels and larger litters. However, females with the highest FGM
levels were signicantly more likely to wean a litter. Importantly, body condition (as measured by
previous year's mass) was also positively associated with breeding and with weaning larger litters. Thus,
although low-ranking females probably experienced more social stressors than high-ranking females
and although adult females often delayed their rst reproduction until they were of a sufcient mass, our
results suggest that elevated baseline FGM levels failed to mediate reproductive suppression. Perhaps, in
species like marmots that have only a single chance per year to reproduce, reproductive suppression
should be rare. These results highlight the importance of social status, body condition and predator
abundance on determining reproductive success in highly seasonal breeders.
©2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
In vertebrates, the hypothalamicepituitaryeadrenal (HPA) axis
modulates reactions to stressors by producing glucocorticoid hor-
mones and restoring homeostasis (Reeder &Kramer, 2005).
Glucocorticoid production upon encountering a stressor varies
among species and among individuals and may be a repeatable trait
within individuals (Martínez-Mota, Valdespino, Rebolledo, &
Palme, 2008; Ramamoorthy &Cidlowski, 2013; Rensel &Schoech,
2011; Smith, Monclús, Wantuck, Florant, &Blumstein, 2012;
Tilbrook, Turner, &Clarke, 2000). Glucocorticoid responses may
be inuenced by a number of factors, including social factors (e.g.
there are documented relationships between social rank and
glucocorticoid levels; discussed below), factors associated with
body condition (Williams, Kitaysky, Kettle, &Buck, 2008) and
ecological factors (e.g. predators and food availability; Creel,
Dantzer, Goymann, &Rubenstein, 2013).
The relationship between dominance and glucocorticoids is
particularly complex, varying enormously with respect to the
species involved, the breeding system, ecological contexts and the
means by which rank is achieved and maintained (Creel et al.,
2013). It is generally accepted that in relatively closed societies,
socially dominant individuals have better access to resources and
mates than do subordinates (Appleby, 1980) and that dominants
may direct aggressive behaviour (including aggressive threats) to-
wards subordinates to maintain their rank, discourage retaliatory
attacks or cause eviction (Ellis, 1995; Stockley &Bro-Jørgensen,
2011). However, even though socially dominant individuals
benet from their increased priority of access to resources due to
their social status and, often as a result, reproductive dominance
(dened here as increased reproductive success), high-ranking in-
dividuals may experience high costs associated with the mainte-
nance of social rank (Creel, 2001; Gesquiere et al., 2011; Muller &
Wrangham, 2004). For instance, reproductively dominant females
*Correspondence: D. T. Blumstein, Department of Ecology and Evolutionary
Biology, University of California, 621 Young Drive South, Los Angeles, CA 90025-
1606, U.S.A.
E-mail address: marmots@ucla.edu (D. T. Blumstein).
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
http://dx.doi.org/10.1016/j.anbehav.2015.11.002
0003-3472/©2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 112 (2016) 1e11
among cooperatively breeding mammals, such as in African wild
dogs, Lycaon pictus (Creel, 2001), meerkats, Suricata suricatta
(Carlson et al., 2004), ringtailed lemurs, Lemur catta (Cavigelli,
1999; Cavigelli, Dubovick, Levash, Jolly, &Pitts, 2003), wolves,
Canis lupus (Sands &Creel, 2004; but see McLeod, Moger, Ryon,
Gadbois, &Fentress, 1996), and common marmosets, Callithrix
jacchus (Saltzman, Schultz-Darken, Schefer, Wegner, &Abbott,
1994) have higher glucocorticoid levels than do conspecic sub-
ordinates. This is probably because reproductively dominant fe-
males are involved in more agonistic interactions to maintain their
high rank than are subordinates. Conversely, other studies have
found that socially subordinate individuals may experience
elevated glucocorticoid levels compared to their dominant coun-
terparts, perhaps due to reduced access to food and social support,
frequent harassment and reproductive suppression (Cavigelli &
Chaudhry, 2012). Such a pattern is seen in some primates
(reviewed by Abbott et al., 2003), alpine marmots, Marmota mar-
mota (Hackl
ander, M
ostl, &Arnold, 2003), African elephants, Lox-
odonta africana (Foley, Papageorge, &Wasser, 2001), and spotted
hyaenas, Crocuta crocuta (Goymann et al., 2001). In addition to
these opposite patterns, other studies have found no relationships
between female social rank and glucocorticoid levels (ringtailed
lemurs: Starling, Charpentier, Fitzpatrick, Scordato, &Drea, 2010;
meerkats: Barrette, Monfort, Festa-Bianchet, Clutton-Brock, &
Russell, 2012; common marmoset monkeys: Abbott, 1984; golden
lion tamarins, Leontopithecus rosalia:Bales, French, Hostetler, &
Dietz, 2005; Syrian hamsters, Mesocricetus auratus:Chelini,
Palme, &Otta, 2011; baboons, Papio hamadryas ursinus:
Crockford, Wittig, Whitten, Seyfarth, &Cheney, 2008; white rhi-
noceros, Ceratotherium simum simum:Metrione &Harder, 2011;
mandrills, Mandrillus sphinx:Setchell, Smith, Wickings, &Knapp,
2008; Ethiopian wolves, Canis simensis:van Kesteren et al., 2013).
Notably, we have listed multiple studies that documented
different patterns for the same species, such as in ringtailed lemurs,
meerkats and common marmosets. Given this variation and the
multitude of studies suggesting different patterns, generalizations
about social rank and glucocorticoid levels are not obvious.
Furthermore, because high glucocorticoid levels are a plausible
mechanism of reproductive failure (Bonier, Martin, Moore, &
Wingeld, 2009; Johnson, Kamilaris, Chrousos, &Gold, 1992;
Moberg, 1985; Munck, Guyre, &Holbrook, 1984; Sapolsky, 1992;
Scarlata et al., 2012; Welsh &Johnson, 1981), it is meaningful to
look beyond the rankestress relationship to better understand the
direct relationships between stressors and reproductive success. In
particular, female reproductive success can be meaningful to
examine because of the frequently high rates of reproductive failure
in female mammals (Wasser &Barash, 1983). In many group-living
animals, not all individuals breed or produce surviving offspring,
and reproductive suppression is a common reason for this (Abbott,
1987; Arnold &Dittami, 1997; Kaplan, Adams, Koritnik, Rose, &
Manuck, 1986; Rood, 1980; Wasser &Barash, 1983). In some sys-
tems, the socially dominant female is also the reproductively
dominant female. Furthermore, because socially subordinate fe-
males are usually the ones that are reproductively suppressed, it is
often inferred that suppression is a direct result of social stressors
caused by the unpredictable harassment, intimidation, evictions and
violence by the reproductively dominant female(s) (Abbott et al.,
2003; Hackl
ander et al., 2003; Louch &Higginbotham, 1967;
Mendl, Zanella, &Broom, 1992; Young et al., 2006). Reduced ac-
cess to food resources, although indirect, could be another mecha-
nism of suppression (Ellis, 1995), especially since dominant females
have better body condition than their subordinates due to increased
access to food (Huang, Wey, &Blumstein, 2011).
Whereas social subordinates may have reduced reproductive
success because of the actions of more dominant individuals,
suppressing others may itself be costly and may therefore not be
always be favoured by natural selection. Indeed, Bell, Nichols,
Gilchrist, Cant, and Hodge (2012) found that when socially domi-
nant banded mongooses, Mungos mungo, suppressed subordinates,
the offspring born to dominant females weighed less than those
born to dominant females that did not suppress others. To avoid
such costs, female reproductive suppression is absent altogether in
some carnivores, such as in the African lions, Panthera leo, living in
egalitarian societies, because aggression is hypothesized to be
disadvantageous and cub survival depends on cooperative defence
against infanticidal males (Packer, Pusey, &Eberly, 2001).
There is therefore substantial variation among and within spe-
cies in the relationships between stress and reproduction. Some
studies have reported links between low social rank, high stress
and suppression (Hackl
ander et al., 2003; Louch &Higginbotham,
1967; Wasser &Barash, 1983), while others have found no rela-
tionship between reproductive success and a female's glucocorti-
coid levels (Beehner, Nguyen, Wango, Alberts, &Altmann, 2006;
Sapolsky, Romero, &Munck, 2000; Setchell et al., 2008;
Weingrill, Gray, Barrett, &Henzi, 2004). Given this variation
among species, it is difcult to make generalizations among taxa.
Empirical studies that simultaneously track multiple social and
ecological variables in free-living wild mammals are therefore
warranted to tease apart the mechanisms and tness correlates of
femaleefemale competition.
We studied the relationship between social rank and faecal
glucocorticoid metabolite (FGM) levels and the relationship be-
tween glucocorticoid levels and reproduction in plural breeding
yellow-bellied marmots, Marmota aviventris. Yellow-bellied mar-
mots are an interesting system in which to study this because they
are facultatively social and hibernate throughout the winter, which
creates an important constraint on tness (Armitage, 1998, 2010,
2014). Marmot colonies contain one to multiple matrilines of
adult females and their offspring. Cooperation and competition
within colonies is concentrated within family groups. Close kin
exchange the highest rates of afliative and agonistic interactions;
these patterns emerge early in ontogeny at the pup stage and
persist into adulthood (Smith, Chung, &Blumstein, 2013). On
average, fewer than 50% of females wean a litter in a given year (e.g.
Blumstein &Armitage, 1998). Prior research suggests that younger
and less dominant adult females may be reproductively suppressed
(e.g. 2-year-old females reproduce only 34% of the time), and may
thus reproduce at later ages, especially if they remain in the same
groups as their reproductively dominant mothers (Armitage, 1998,
2010). Interestingly, delaying the age of rst reproduction beyond
the age of 2 years, however, is rare, and body mass, rather than age,
per se, is a strong predictor of reproductive success among adults
(Lenihan &Vuren, 1996). Previous studies have also shown that
environmental variation (Schwartz, Armitage, &Vuren, 1998), age
(Ozgul, Oli, Olson, Blumstein, &Armitage, 2007), predation pres-
sure (Monclús, Tiulim, &Blumstein, 2011) and parity (e.g. if the
animal has previously produced offspring or not; see Oli &
Armitage, 2003) can inuence reproductive success. Thus, we
therefore employed a holistic approach here to integrate these
variables into a single study based on almost a decade's worth of
eld data to isolate the effects of rank and stress on female
reproduction.
Our study builds upon earlier research on this species to address
fundamental and highly debated questions. First, after controlling
for variation in environmental factors, age classes, predation pres-
sure, colony size and breeding status, we aimed to understand the
specic relationship between social rank and FGM level (our vali-
dated measure of baseline stress; Smith et al., 2012) in adult female
marmots. Second, we aimed to understand whether FGM levels
were associated with reproductive success by investigating each
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e112
individual's probability of breeding as well their annual reproduc-
tive success, which we measured as the number of emergent
young.
Based on what is known about the social system of yellow-
bellied marmots, we predicted the following. Because individuals
are facultatively social and live in groups that can be described by
dominance hierarchies, we expected a relationship between social
rank and the degree to which individuals experienced stressors.
Thus, if femaleefemale competition is a stressor, then we expected
variation in FGM levels as a function of female social rank, and we
predicted that (socially) low-ranking reproductively mature fe-
males in this plural breeding species should have higher gluco-
corticoid levels than those of socially dominant females. Huang
et al. (2011) previously found no effect of an individual's overall
social dominance rank (based on outcomes of agonistic interactions
with all adult male and female group-mates) on reproductive
success of adult female marmots. Nevertheless, theory predicts that
female reproductive success should be most strongly shaped by
intrasexual competition among female mammals in social systems
in which females compete within matrilines (Stockley &Bro-
Jørgensen, 2011).
Here we therefore inquired whether femaleefemale competi-
tion (measured as adult female agonistic rank, after controlling for
group size; see Huang et al., 2011, and methods below) in combi-
nation with interindividual variation in responses to stressors may
together explain previously documented patterns of reproductive
suppression observed among adult female yellow-bellied marmots
(e.g. Armitage, 1998, 2014). Stressors triggered by femaleefemale
competition in combination with ecological stressors may together
explain reproductive failure and/or skew among adult female
marmots if reproductive success is reduced as a consequence of low
social rank and/or elevated FGM levels. We therefore predicted that
females with elevated FGM levels (i.e. young, low-ranking females),
low body mass and increased exposure to predators would have the
lowest reproductive success. Because we expected larger colonies
to attract more predators within an active season, we also included
colony size and its interaction with predator abundance as pre-
dictor variables in our models. While larger females are dominant
to smaller females, there was substantial variation in our data set to
permit us to isolate the effect of these variables statistically (none of
the correlations among mass, rank and predators exceeded 0.25).
METHODS
Field Methods
To determine the relationships among social rank, stress and
reproductive suppression, we studied the social interactions of
yellow-bellied marmots in and around the Rocky Mountain Bio-
logical Laboratory (RMBL, 38
57N, 106
59W) in Gunnison County,
Colorado, U.S.A. (Armitage, 2010; Blumstein, 2013). For these ana-
lyses, we focus on data collected on wild individuals over 9 years
(2003e2011) at ve colony sites (Bench, Gothic Townsite, Picnic,
Marmot Meadow, and River) located in and around the RMBL.
Colony sites are geographical locations that contain one or more
marmot social groups; social groups are dened by space use
overlap and contain one or more breeding age females (who are
related), typically a single male, young of the year, and predispersal
yearlings of both sexes.
We live-trapped marmots in Tomahawk traps that we placed
around marmot burrow entrances for a few consecutive days every
other week. At each trapping event, we recorded an individual's
mass, sex, age, reproductive status (by scoring nipple development
as present,swollenor lactating;Armitage &Wynne-Edwards,
2002; we conservatively estimated that 9% of females that failed
to wean a litter were scored as lactating) and collected faeces
(when present). The rst time a subject was trapped, we collected a
hair sample for subsequent parentage assignment (Blumstein, Wey,
&Tang, 2009). Marmots were also marked permanently with ear-
tags the rst time they were captured and their dorsal pelage was
dyed (and redyed when required) with a unique fur mark for visual
recognition from afar (see Armitage, 1982).
Social Factors Affecting Glucocorticoid Levels
Glucocorticoid metabolites can be reliably extracted from
marmot faeces (Smith et al., 2012). We opportunistically collected
faeces at trapping events and stored them on ice in plastic bags.
Samples were frozen within 2 h of collection at 20
C and steroid
hormones were extracted within 6 months of collection at the
University of California Los Angeles (details in Monclús et al., 2011;
Smith et al., 2012). Details of sample preparation and glucocorticoid
assay are in Appendix A of Blumstein, Patton, and Saltzman (2006).
We collected faecal samples each time an individual defecated in a
trap or in a bag. To be conservative, we only used the rst faecal
sample collected from each weekly trapping session to assess basal
FGM levels (N¼278; mean ±SD ¼30.8 ±15.79 samples/year). We
did this because repeated capture can result in trap stress and
elevated FGM levels in marmots (Smith et al., 2012). For each in-
dividual (N¼60; mean ±SD ¼14.1 ±6.33 individuals/year), we
calculated the annual glucocorticoid measure by averaging the
combination of each of these single samples collected from each
biweekly trapping session.
To determine an individual's social rank, we observed marmots
both in the morning (0700e1000 hours) and in the afternoon
(1600e1900 hours), when marmots are most active (Armitage,
1962). We observed marmots at distances of 20e150 m (Huang
et al., 2011) to avoid inuencing the marmots' behaviour. We
observed marmots in all ve colonies for a total of 8762 h over the 9
years (mean ±SD ¼973.6 ±246.30 h/year). Because social groups
and colonies vary in their composition annually through births,
deaths and dispersal, we analysed the data for each colony sepa-
rately for each year. Colonies contained one or more social groups,
dened by space use overlap, and also varied annually. Following
Huang et al. (2011), we calculated rank based on the subset of in-
dividuals in a colony that were observed to interact; for females,
these almost always were restricted to other social group members.
During observations, we recorded both afliative and agonistic
interactions, although for this study, we focused only on agonistic
interactions because we were interested in the link between
aggressive interactions and stress response. We dened agonistic
interactions as those that were aggressive and accompanied by
biting, chasing or ghting (see ethogram in Wey &Blumstein,
2012). For each social interaction, we recorded the instigator and
the victim, as well as the winner and the loser of the interaction.
These data allowed us to calculate social dominance hierarchies for
adult females using the Clutton-Brock index (CBI).
For a given subject, the CBI considers the total number of wins
and losses against each opponent (Clutton-Brock, Albon, Gibson, &
Guinness, 1979). The CBI is more applicable to the study of yellow-
bellied marmots than other metrics of dominance, like David's
score (DS), or the frequency-based dominance index (FDI), because
it is better suited for species with relatively few observed in-
teractions and does not use the rate of interaction in its calculation
(Bang, Deshpande, Sumana, &Gadagkar, 2010). The index is dened
as CBI ¼(Bþbþ1)/(Lþlþ1), where Bis the total number of
losers(individuals that previously lost an interaction) that an in-
dividual has beaten,bis the total number of individuals that the
losers(B)havebeaten,Lis the total number of winners(in-
dividuals that previously won an interaction) that have beatenthe
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e11 3
individual, and lis the total number of individuals that have
beatenthe winners(L).
Using the CBI, we then calculated relative rank, a measure that
accounts for differences in the number of individuals in a hierarchy
by standardizing each rank with respect to the total number of
individuals (Huang et al., 2011). We ordered the CBI values from
lowest to highest and then divided absolute rank by the total
number of individuals. In the relative ranking data, the lowest rank
was always zero and the highest rank was always one for each
hierarchy.
We determined social rank based solely the two-way in-
teractions between females that were of reproductive age (2 years
or older; Oli &Armitage, 2003). In our calculations we excluded
male interactions because our objective was to understand
reproductive suppression in females only. For the 9 years and the
45 colony-years (each of ve colonies studied over 9 years) ana-
lysed, all had sufcient two-way interactions to allow us to
calculate ranks for one or more social groups based on our pa-
rameters of age and sex. However, there were some dominance
hierarchies that could not be used because there were no observed
interactions to base rank upon because breeding-age females in the
group were not observed to interact aggressively with each other.
For our analyses we assume that rank relationships were stable
within years. However, social rank very well could change from
year to year given differences in group composition and agonistic
interactions.
The Relationship between Glucocorticoid Levels and Reproductive
Success
Our second goal was to understand what factors inuenced
breeding, and specically whether stress (as measured by FGM
level) was a likely mechanism underlying reproductive success. We
examined this in two ways: rst, by testing whether glucocorticoid
metabolite levels affected the probability of breeding and second,
by testing whether glucocorticoid metabolite levels and/or female
social rank best predicted the number of young weaned (a measure
of annual reproductive success). Because litters from different fe-
males may be mixed (Armitage, 1989; Olson, Blumstein, Pollinger,
&Wayne, 2012), we assigned offspring to their mother's molecu-
larly (details in Blumstein et al., 2009). Briey, we extracted DNA
from hair and used 12 microsatellite markers to assign maternity
using Cervus 3.0 (Kalinowski, Taper, &Marshall, 2007) with 95%
condence (see Blumstein, Lea, Olson, &Martin, 2010). Our pedi-
gree included 60 adult females (ca. 14 individuals were studied
each year) and their 306 conrmed offspring.
Statistical Analysis
We tted generalized linear mixed-effects models (GLMMs) to
evaluate our questions. Following Smith et al. (2012), FGM levels
were ln transformed. To study the relationship between social rank
and stress, our dependent variable was the annual FGM level. For
this model, we entered each set of predictor variables associated
with each trapping event (time of day, day of the year; see below)
for which FGMs were collected to assess their effects on average
annual FGM values for each subject based on a Gaussian distribu-
tion. To study the relationship between social stress and the
probability of breeding, our dependent variable was whether a fe-
male successfully weaned a litter; these effects were modelled
using the binomial distribution. To study the relationship between
social stress and litter size, our dependent variable was the number
of offspring weaned; these effects were modelled using the Poisson
distribution.
Each model contained nine xed effects, each of which was
entered as a separate predictor variable (rather than as an annual
measure so as to capture seasonal factors that might inuence
variation in FGM values), as follows: (1) whether or not the indi-
vidual reproduced in the previous year; (2) the hour the gluco-
corticoid sample was collected (there is seasonal and daily variation
in FGM; Smith et al., 2012); (3) an individual's mass at the current
trapping event (i.e. when the particular faeces were collected for
FGM extraction); (4) the date the glucocorticoid sample was
collected; (5) an individual's body mass as estimated on 15 August
the previous year (because previous year's mass is correlated with
reproductive success: Lenihan &Vuren, 1996; for a description of
the linear mixed modelling approach used to estimate body mass,
see Ozgul et al., 2010); (6) the number of predators seen during
observations between April and July that year (the number of
predators encountered can inuence FCM levels: Boonstra, Hik,
Singleton, &Tinnikov, 1998; Monclús et al., 2011); (7) colony size;
(8) female relative rank and/or (9) female rank and FGM levels,
depending on the model tested.
In addition, because female marmots can reproduce at 2 years of
age but may be reproductively suppressed (Blumstein &Armitage,
1999), we tested for the effects of age by creating a binary variable
that separated potentially reproductive females into two cate-
gories: 2 years old versus >2 years old. We tested for all two-way
interactions and only included these terms when it increased the
t of our model using the Akaike Information Criterion (AIC).
Each model also contained three random effects: the colony that
an individual belonged to, female identity and year. These were
included to explain location, individual and seasonal differences
that may account for variation in FGM levels. We tested for two-
way interactions and retained interaction terms only when doing
so increased the t of our model (within 2 AIC values of our best
model). Values for excluded terms were based on adding each term
to our nal models. We set our alpha to 0.05 and report the results
of two-tailed tests.
We elected to not analyse our data with a formal path analysis
because to do so we would have had to remove about 15% of our
data and risk overtting a structural equation model. Given the
relatively small effect sizes we report from the GLMM (see below),
we wished to retain as much power as possible and thus conducted
the GLMM.
Ethical Note
All procedures were approved under research protocol ARC
2001-191-01 as well as permits issued by the Colorado Division
of Wildlife. The research protocol was approved by the University
of California Los Angeles Animal Care Committee on 13 May 2002
and renewed annually. After trapping, individuals were released
immediately at the trap location. Marmots were in traps no
longer than 2e3 h, and typically for much less time than that.
Traps were shaded with vegetation on warm days. Marmot
handling was brief (typically 5e15 min depending upon the data
to be collected) and marmots were not injured during handling.
All marmots were handled while inside of a conical cloth-
handling bag to reduce stress. We swabbed ears with alcohol
before tagging individuals to reduce the chance of infection.
Observations were conducted at distances chosen to not overtly
affect marmot behaviour.
RESULTS
Our nal data set contained 147 breeding events from 60 unique
adult female marmots, collected over 9 years and from our ve
colonies (mean ±SD ¼15.8 ±10.34 breeding events/year). There
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e114
were a total of 485 pups weaned over the 9 years from all females
(mean ±SD ¼53.9 ±40.37 pups weaned/year). Main predators
that visited the sites included black bears, Ursus americanus, coy-
otes, Canis latrans, mountain lions, Puma concolor, red foxes, Vulpes
vulpes, and various raptors. On average (±SD), we detected and
identied predators at these colony sites on 19 ±12.87 days/year,
but this varied by colony.
Factors Affecting Glucocorticoid Levels
After controlling for variation accounted for by our random
variables, six of our xed effects and one interaction between them
signicantly explained variation in average annual faecal gluco-
corticoid metabolite levels (Table 1). When considered together,
FGM levels signicantly increased when females were heavier in
the previous year (Fig. 1a), when they were 2 years old (rather than
>2 years; Fig.1a), when they were of lower rank (Fig. 2), when there
were more predators in the area (Fig. 1b) and when they were
found in larger colonies (Table 1,Fig. 1b). This was the case after
controlling for the day of sample collection; FGM levels declined
across the season (Table 1). Colony size modulated the effect of
predator abundance (Table 1). The addition of other interactions
did not signicantly explain variation in FGM levels. All random
effects were signicant (year:
c
21
¼224.7, P<0.0001; colony:
c
21
¼13.7, P¼0.0002; marmot identity:
c
21
¼26.5, P<0.0001).
Table 1
Factors affecting faecal glucocorticoid metabolite levels in female yellow-bellied
marmots
Fixed effects Estimate±SD P
Reproduced in previous year 0.0617±0.4616 0.8935
Hour of faecal sample collection 0.0006±0.0034 0.8401
Mass at current trapping event 0.0001±0.0001 0.1305
Day of year of faecal sample collection 0.0018±0.0009 0.0480
Mass in previous year 0.0002±0.0001 <0.0001
2 years of age 0.2323±0.0409 <0.0001
Relative female social rank ¡0.1269±0.0524 0.0162
Predator abundance 0.0277±0.0079 0.0005
Colony size 0.0129±0.0033 <0.0001
Predator abundance)colony size ¡0.0005±0.0001 0.0001
Signicant outcomes are shown in bold.
120
130
140
150
160
170
180
190
(a)
(b)
200
2 years,
light before
>2 years,
light before
2 years,
heavy before
>2 years,
heavy before
Faecal glucocorticoid metabolites (ng/g faeces)
N = 50
N = 80
N = 58
N = 85
120
130
140
150
160
170
180
190
200
Small colony,
low
p
redation
Large colony,
low
p
redation
Small colony,
hi
g
h
p
redation
Large colony,
hi
g
h
p
redation
N = 60
N = 62 N = 29
N = 122
Figure 1. Mean faecal glucocorticoid metabolite concentration in female yellow-
bellied marmots as a function of (a) age (2 years old vs >2 years old) and previous-
year body mass (light before: 2500e3500 g; heavy before: 3500e4500 g) and (b)
colony size (small: <50 marmots; large: >50 marmots) and predator abundance (low:
<22 predators; high: >22 predators). We entered body mass, colony size and predator
abundance as continuous variables directly into our statistical model (Table 1). Sample
sizes above bars indicate the number of faecal samples for females in each category.
Error bars represent raw standard errors around the mean for each category (for
illustrative purposes).
0
0.5
1
1.5
2
2.5
3
3.5
4
4.5
80
100
120
140
160
180
200
220
240
260
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1
Relative social rank of adult females (from low to hi
g
h)
Number of
p
u
p
s survivin
g
to weanin
g
Faecal glucocorticoid metabolites (ng/g faeces)
Figure 2. Effects of relative social rank on faecal glucocorticoid metabolite concen-
tration (open circles) and number of pups surviving to weaning (black circles) in fe-
male yellow-bellied marmots ranked from lowest (0) to highest (1). Error bars
represent raw standard errors around the mean for each category (for illustrative
purposes).
Table 2
Factors affecting the probability that adult female yellow-bellied marmots suc-
cessfully weaned a litter
Fixed effects Estimate±SE P
Reproduced in previous year 136.8±63.940 0.0324
Hour of faecal sample collection 0.020±0.073 0.7817
Mass at current trapping event 0.002±0.001 0.2650
Day of year of faecal sample collection 0.001±0.022 0.9709
Mass in previous year 0.005±0.001 <0.00001
2 years of age ¡3.058±0.943 0.0012
Relative female social rank 0.481±1.346 0.7207
Predator abundance 0.109±0.046 0.0177
Colony size 0.658±0.224 0.0033
Faecal glucocorticoid metabolite (FGM) level 6.474±3.155 0.0402
FGM levels)colony size ¡0.116±0.045 0.0105
FGM levels)reproduced in previous year ¡30.450±13.740 0.0267
Signicant outcomes are shown in bold.
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e11 5
The Relationships Between Glucocorticoid Levels and Reproductive
Success
After controlling for a variety of variables that might inuence
the probability of breeding, six of our xed effects and two in-
teractions between them explained signicant variation in proba-
bility that adult female marmots reproduced (Table 2). The
variability of these data was consistent with that expected for the
binomial distribution (e.g. the dispersion parameter of 0.311 was
less than 1). Females were more likely to wean a litter if they were
heavier in the previous August (Fig. 3), if they lived in larger col-
onies (Figs. 4b and 5a), if they had higher FGM levels (Fig. 5a, b) and
if they reproduced in previous years (Table 2,Fig. 5b). Adult females
were also signicantly less likely to wean a litter if they were 2
years of age (rather than >2 years; Fig. 3), and less likely to wean a
litter when more predators were present (Table 2,Fig. 4a). There
were signicant negative interactions between FGM levels and
both colony size and whether or not a female weaned a litter in the
previous year (Table 2). However, reproductive failure could not be
explained by social rank, a variable that failed to explain whetheran
adult female weaned a litter (Table 2). All random effects were
signicant (year:
c
21
¼13.3, P¼0.0003; colony:
c
21
¼24.2,
P<0.0001; marmot identity:
c
21
¼48.6, P<0.0001).
In contrast, the number of pups weaned was inuenced by four
measured main effects, including social rank, and three interactions
(Table 3). The variability of these data was consistent with that
expected for the Poisson distribution (e.g. the dispersion parameter
of 0.784 was less than 1). Weaning litter sizes were larger when
females were of higher social rank (Fig. 2), they had higher FGM
levels (Table 3,Fig. 6a), they lived in larger colonies (Fig. 6a), they
reproduced in the previous year (Fig. 6b) and they were heavier in
the previous year (Fig. 7a). The effect of FGM levels on litter size,
however, was modulated by colony size and whether or not a fe-
male reproduced in the previous year (Table 3). For marmots that
successfully reproduced the previous year, litters were larger if
females were heavier when trapped in the previous August prior to
hibernation, and if they were of higher relative social rank within
their colonies (Table 3). Similarly, for 2-year-olds, litters were
smaller as predator abundance increased (Table 3,Fig. 7b). As with
the tendency to wean a litter or not, all random effects were sig-
nicant (year:
c
21
¼39.5, P<0.0001; colony:
c
21
¼61.0,
P<0.0001; marmot identity:
c
21
¼128.0, P<0.0001).
DISCUSSION
To better understand the inuences of social stressors and their
associations with reproductive success, we investigated the prob-
ability of weaning a litter and the annual reproductive success of 60
female yellow-bellied marmots studied over 9 years. Importantly,
0.2
0.3
0.4
0.5
0.6
0.7
0.8
2 years,
li
g
ht before
>2 years,
li
g
ht before
2 years,
heav
y
before
>2 years,
heav
y
before
Proportion of adult females that reproduced
N = 50
N = 80
N = 58
N = 85
Figure 3. Effects of previous-year body mass (light before: 2500e3500 g; heavy
before: 3500e4500 g) and age (2 years old vs >2 years old) on the probability that
female yellow-bellied marmots would wean a litter in the current year. We entered
body mass as a continuous variable directly into our statistical model (Table 2). Sample
sizes above bars indicate the number of females sampled in each category. Error bars
represent raw standard errors around the mean for each category (for illustrative
purposes).
0.46
0.48
0.5
0.52
0.54
0.56
0.58
0.6
0.62 (a)
(b)
Low predation High predation
N = 122
N = 151
0.46
0.48
0.5
0.52
0.54
0.56
0.58
0.6
0.62
Small colony Large colony
Proportion of adult females that reproduced
N = 89
N = 184
Figure 4. Effects of (a) predator abundance (low: <22 predators; high: >22 predators)
and (b) colony size (small: <50 marmots; large: >50 marmots) on the probability that
adult female yellow-bellied marmots would wean a litter in the current year. We
entered colony size and predator abundance as continuous variables directly into our
statistical model (Table 2). Sample sizes above bars indicate the number of females
sampled in each category. Error bars represent raw standard errors around the mean
for each category (for illustrative purposes).
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e116
we found that as a female's social rank increased, her FGM levels
signicantly decreased, but this was a relatively small effect that
was only detected after controlling for other variables that
explained variation in FGM levels. This is notable because similar
patterns have also been documented in many cooperative breeders
(Cavigelli &Chaudhry, 2012). From this nding, we infer that low-
ranking females experience more stressors than high-ranking fe-
males. Indeed, social competition among female kin is intense
within matrilines; social competition emerges early in ontogeny
and persists into adulthood (Smith et al., 2013).
Social rank also inuenced the number of offspring successfully
weaned in a season (but not reproductive failure), with high-
ranking producing the most offspring. Our nding that females
with high social status, based on agonistic interactions, produced
more offspring than did low-ranking females has similarly been
documented in ungulates (e.g. mountain goats, Oreamnos
americanus:C^
ot
e&Festa-Bianchet, 2001), carnivores (e.g. spotted
hyaenas: Holekamp, Smale, &Szykman, 1996) and primates (e.g.
gelada baboons, Theropithecus gelada:Dunbar &Dunbar, 1977).
Low-ranking females may produce fewer offspring because of dif-
ferences in access to resources, amount of social support, body
condition, group size and/or increased agonistic interactions
(Abbott et al., 2003; Appleby, 1980; Cabezas, Blas, Marchant, &
Moreno, 2007; Foley et al., 2001; Hackl
ander et al., 2003).
Taken together, our ndings about stresslevels and reproduc-
tive output are therefore in accordance with classic captive studies
on aggresion, rank and physiological stress responses that support
the stress of subordinationhypothesis (reviewed by Creel et al.,
2013). However, high FGM levels were also correlated with
increased reproductive success: higher FGM levels were correlated
with increased likelihood of successful reproduction as well as litter
size. This nding is inconsistent with many ndings of no rela-
tionship between stress levels and reproductive success (reviewed
in: Boonstra, 2013; Creel, 2001; Sapolsky et al., 2000). Our ndings
are important because they support the emerging view, such as
that expressed recently by Creel et al. (2013), that the effects of
social stressors on the HPA axis are complex. Our empirical ndings
therefore contribute to important data from wild populations of
mammals necessarily to advance this area of science forward.
Social rank was correlated with our measure of physiological
stress, but it failed to predict the probability of breeding. The re-
lationships we identied between FGM and social rank and FGM
and reproductive success may at rst appear contradictory (high-
ranking females had lower FGM levels and the probability of
breeding was positively correlated with FGM, suggesting that high-
ranking females have a lower probability of breeding). However,
our nding that females living in large colonies had elevated annual
FGM levels and produced the most offspring is likely attributed to a
surge in glucocorticoids during reproduction. In adult female
marmots, FGM levels vary with reproductive state and are highest
during pregnancy and lactation (Smith et al., 2012). Ebensperger
et al. (2011) found similar results in degus, Octodon degus.In
particular, adult female cortisol levels appear to rise as offspring are
weaned, which seems to be associated with an increased pro-
pensity to produce alarm calls (Blumstein, Steinmetz, Armitage, &
Daniel, 1997), but not with other factors such as group size or
number of females. Perhaps the measure of probability of breeding
(whether or not the female weaned pups) should include pups lost
before the pups' emergence. Unfortunately, such assignments are
nearly impossible for obligate hibernators, such as marmots, under
0.35
0.4
0.45
0.5
0.55
0.6
0.65
0.7
0.75 (b)
Low FGMs,
no re
p
rod.
High FGMs,
no re
p
rod.
Low FGMs,
re
p
roduced
High FGMs,
re
p
roduced
Proportion of adult females that reproduced
N = 83
N = 120
N = 30
N = 40
0.35
0.4
0.45
0.5
0.55
0.6
0.65
0.7
(a)
0.75
Low FGMs,
large colony
Low FGMs,
small colony
High FGMs,
large colony
High FGMs,
small colony
N = 68
N = 45 N = 116
N = 44
Figure 5. Effects of faecal glucocorticoid metabolite concentration (low FGMs:
<128 ng/g faeces; high FGMs: 128 ng/g faeces), (a) colony size (large: >50 marmots;
small: <50 marmots) and (b) reproductive success in the previous year on the prob-
ability that female yellow-bellied marmots would wean a litter in the current year. We
entered FGM and colony size as continuous variables directly into our statistical model
(Table 2). Sample sizes above bars indicate the number of females sampled in each
category. Error bars represent raw standard errors around the mean for each category
(for illustrative purposes).
Table 3
Factors affecting the number of yellow-bellied marmot pups surviving to weaning
Fixed effects Estimate±SE P
Reproduced in previous year 34.97±13.32 0.0087
Hour of faecal sample collection 0.0102±0.0132 0.4372
Mass at current trapping event 0.0002±0.0002 0.1366
Day of year of faecal sample collection 0.0031±0.0035 0.3872
Mass in previous year 0.0008±0.0002 0.0002
Relative female social rank 0.5259±0.2539 0.0384
2 years of age 0.2652±0.3363 0.4303
Predator abundance 0.0078±0.0081 0.3341
Colony size 0.1964±0.0444 <0.00001
Faecal glucocorticoid metabolite
(FGM) level
2.218±0.6253 0.0004
FGM levels)colony size ¡0.0355±0.0091 <0.00001
FGM levels)reproduced in
previous year
¡9.0480±2.875 0.0016
Mass at current trapping event
)reproduced in previous year
0.0021±0.0009 0.0146
2 years of age)predator abundance ¡0.0788±0.0181 <0.00001
Signicant outcomes are shown in bold.
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e11 7
natural conditions. This would require live-trapping of marmots
with bait that would prematurely prime metabolic processes prior
to snow-melt and the start of the growing season in their high-
elevation habits. Such an effort would not only confound the
reproductive outputs, but would probably be dangerous for the
marmots. Given some uncertainty about the cause of preweaning
failure (litter reabsorption versus preweaning predation), we
elected to dene breeders as those who successfully weaned a
litter, but we recognize that at least 9% of females that failed to
wean a litter were scored as lactating. We therefore call for future
research in a more controlled setting than is possible under eld
conditions, such as in a laboratory, to unravel these complex pat-
terns. Additional studies may therefore be able to disentangle the
relative effects of preweaning predation and reabsorption to
explain these seemingly contradictory results.
These inconsistent patterns may also suggest that female
reproductive outcomes in yellow-bellied marmots are more
strongly mediated by ecological factors than by stressors associated
with social status. Indeed, an individual's mass from the previous
year was correlated with increased FGM levels and both metrics of
reproductive success. Our nding here that FGM levels increased
with the number of predator visits is consistent with a growing
body of evidence revealing the potential sublethal effects of pred-
ators on prey (e.g. Brooks, Gaskell, &Maltby, 2009; Creel &
Christianson, 2008; Pangle, Peacor, &Johannsson, 2007). Our
nding that the probability of weaning a litter decreased as the
observed number of predators increased is consistent with studies
showing that high predator-induced stressdirectly impairs
reproductive function in snowshoe hares, Lepus americanus
(Boonstra et al., 1998; Sheriff, Krebs, &Boonstra, 2009). Given that
marmots consistently reside at the same burrows, marmots may
similarly suffer from sublethal effects from predator-induced
stressors. In contrast, Creel, Winnie, and Christianson (2009)
found that wolf presence limits reproduction in elk, Cervus
0
0.5
1
1.5
2
2.5
3
3.5 (b)
2 years,
low
redation
>2 years,
low
redation
2 years,
hi
h
redation
>2 years,
hi
h
redation
N = 60 N = 62
N = 48
N = 103
0
0.5
1
1.5
2
2.5
3
3.5 (a)
Light now,
no reprod.
Heavy now,
no reprod.
Light now,
reproduced
Heavy now,
reproduced
Number of pups surviving to weaning
N = 126
N = 77
N = 43
N = 27
Figure 7. Effects of (a) current-year body mass (light now: 1000e3000 g; heavy now:
3001e5000 g) and previous-year reproductive success and (b) predator abundance
(low: <22 predators; high: >22 predators) and female age (2 years old vs >2 years old)
on the number of offspring that female yellow-bellied marmots weaned in the current
year. We entered body mass as a continuous variable directly into our statistical model
(Table 3). Sample sizes above bars indicate the number of females sampled in each
category. Error bars represent raw standard errors around the mean for each category
(for illustrative purposes).
1
1.2
1.4
1.6
1.8
2
2.2
2.4
2.6
2.8
3
Low FGMs,
small colony
High FGMs,
small colony
Low FGMs,
large colony
High FGMs,
large colony
Number of pups surviving to weaning
N = 45
(a)
(b)
N = 44
N = 68
N = 116
1
1.2
1.4
1.6
1.8
2
2.2
2.4
2.6
2.8
3
Low FGMs,
no re
p
rod.
High FGMs,
no re
p
rod.
Low FGMs,
re
p
roduced
High FGMs,
re
p
roduced
N = 83
N = 120 N = 30
N = 40
Figure 6. Effects of faecal glucocorticoid metabolite concentration (low FGMs:
<128 ng/g faeces; high FGMs: 128 ng/g faeces), (a) colony size (large: >50 marmots;
small: <50 marmots) and (b) previous-year reproductive success on the number of
offspring that female yellow-bellied marmots weaned in the current year. We entered
FGM and colony size as continuous variables directly into our statistical model
(Table 3). Sample sizes above bars indicate the number of females sampled in each
category. Error bars represent raw standard errors around the mean for each category
(for illustrative purposes).
D. T. Blumstein et al. / Animal Behaviour 112 (2016) 1e118
elaphus; wolves drive elk to forage on suboptimal diets. Perhaps
ecological factors associated with foraging decisions also inuence
body mass, which, in turn, inuences FGM levels and reproductive
success in marmots. Moreover, because predator abundance may
also contribute directly to pup mortality via predation, carefully
designed eld experiments are needed to investigate the mecha-
nisms responsible for this observed pattern in marmots and other
rodents.
Rodent reproductive success often increases with age in wild
mammal populations (King &Allain
e, 2002; King, Festa-Bianchet,
&Hateld, 1991). Accordingly, 2-year-old marmots (the age of
reproductive maturity; Oli &Armitage, 2003) in the current study
had higher FGM levels and were less likely to reproduce than older
females. Thus, 2-year-old females, which are often socially and
reproductively subordinate to their mothers, might delay their age
of rst reproduction. Armitage (1998) suggested that older adult
female marmots may reproductively suppress 2-year-olds. How-
ever, because we found no interactions between being a 2-year-old
and FGM levels, it is unlikely that FGM mediates reproductive
failure. Instead, we found an interesting, nonadditive effect of
predator abundance on the number of offspring weaned by 2-year-
olds and by older females. That is, 2-year-olds appeared to be
particularly sensitive to the risks of high predator abundance,
rearing disproportionally small litters under the risk of high pre-
dation. This raises the possibility that 2-year-olds are most
vulnerable to the nonlethal effects of predators and/or the least
prepared to successfully protect their offspring from predators.
Because adult females belonging to both age categories apparently
similarly perceived large numbers of predators as intense stressors
(additive effect of predators on FGM levels of females that were 2
years old and >2 years old), our ndings are instead most consis-
tent with the notion that the loss of offspring born to inexperienced
mothers is due to direct predation rather than to nonlethal effects
of mothers being stressedby high predator abundance.
Moreover, the signicant interaction between body mass and
whether an individual reproduced the previous year highlights the
importance of condition-related factors affecting reproductive
success. Thus, the reproductive skew that Armitage (1998) pro-
posed may be due to factors other than social rank, such as female
body condition and predator abundance found to be important in
our current study. By contrast, for males, Huang et al. (2011)
identied a correlation between rank and reproductive success.
Further study of maleemale competition is clearly warranted.
As reviewed in the Introduction, differences in stress level,
dominance rank and reproductive success are seen among taxa,
and even within species. These connections are clearly complex,
and research has found both positive and negative relationships
between social stress and reproductive success (Bonier et al., 2009;
Brann &Mahesh, 1991; Crespi, Williams, Jessop, &Delehanty,
2013). There are multiple potential causes for these variable re-
lationships. For example, Brann and Mahesh (1991) noted that
reproductive outcome is in part a function of whether the stress is
acute or chronic because acute stressors may facilitate corticoste-
roid production and enhance fertility. By contrast, chronic stressors
may have a more inhibitory effect on reproduction, by preventing
sexual maturation and impairing pregnancies.
Although it may be premature to make generalizations about
the effects of stressors and social rank on reproductive success, our
study highlights the value of longitudinal empirical studies relating
three features of social living in relevant ecological contexts: social
rank, baseline stress and reproductive success. Whether socially
induced or induced through predator threat, females that enter
hibernation at low body mass may reduce their investment in
young to conserve valuable resources. Perhaps in species that only
have a single chance per year to reproduce, like marmots, socially
mediated reproductive suppression should be rare, and thus, social
rank or other social stressors may only reduce offspring number
rather than restrict annual reproductive bouts altogether. Regard-
less, these results highlight the importance of body condition and
other environmental factors, such as predator abundance, on the
reproductive success of highly seasonal breeders.
Acknowledgments
We thank all the marmoteers since 2001 who helped collect
these data. D.T.B was supported by the National Geographic Society
(grant number 8140-06), the University of California Los Angeles
(Faculty Senate and the Division of Life Sciences), a Rocky Mountain
Biological Laboratory research fellowship, and by the National
Science Foundation (IDBR-0754247 and DEB-1119660 to D.T.B., as
well as DBI 0242960 and 0731346 to the Rocky Mountain Biological
Laboratory). J.E.S. was supported by funds from Faculty Develop-
ment Funds and from the Provost's Ofce at Mills College as well as
by fellowships from the American Association of University
Women, the Institute for Society and Genetics at the University of
California Los Angeles and the American Philosophical Society. We
also thank several anonymous referees whose astute comments
helped us improve previous versions of this manuscript.
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Nuestros resultados sugieren que muchas especies de aves en Granada hacen un uso significativo de los paisajes rurales y agrícolas de baja intensidad y tales hábitats deben ser tenidos en cuenta en la conservación de las comunidades de aves. La conservación de las comunidades de aves terrestres residentes en esta región requerirá el mantenimiento de un mosaico de tipos de hábitats naturales y antropogénicos y la colaboración entre un amplio abanico de agentes gubernamentales y no gubernamentales. Palabras clave agricultura, conservación, Granada, isla, selección de hábitat, terrestre Résumé Utilisation des milieux anthropiques et naturels par les oiseaux dans un petit État insulaire en développement • Les oiseaux des petits États insulaires en développement (SIDS) sont particulièrement menacés par l’expansion agricole et urbaine ainsi que par le changement climatique. Dans ces États, il est toutefois difficile de mettre en place des mesures de gestion et d’atténuation appropriées, car les données sur l’écologie et la conservation sont rarement disponibles. Pour mieux comprendre l’utilisation des milieux naturels et anthropiques par les espèces d’oiseaux sédentaires dans un SIDS néotropical, nous avons mené une étude systématique à l’échelle de la communauté sur la répartition, la diversité et l’abondance des oiseaux terrestres de la Grenade. Pour la plupart des espèces, les densités observées étaient plus élevées dans les zones cultivées et les prairies secondaires, et plus faibles dans les forêts humides d’altitude et les forêts secondaires. Toutefois, certaines espèces dont l’état de conservation est préoccupant – comme le Caliste dos-bleu (Tangara cucullata), endémique à l’échelle régionale, le Tyran bavard (Myiarchus nugator), ainsi que tous les nectarivores – préféraient les forêts humides d’altitude et les forêts secondaires. Les nectarivores avaient tendance à éviter les milieux urbains. Nos résultats montrent que de nombreuses espèces d’oiseaux de la Grenade utilisent de manière non négligeable les milieux ruraux comprenant des zones d’agriculture peu intensive, et que ces habitats devraient être pris en compte dans la conservation des communautés d’oiseaux. La conservation des communautés d’oiseaux terrestres sédentaires dans cette région requiert le maintien d’une mosaïque de milieux naturels et anthropiques, ainsi qu’une collaboration entre un large éventail d’acteurs gouvernementaux et non gouvernementaux. Mots clés agriculture, conservation, Grenade, île, sélection de l’habitat, terrestre
... Additionally, there is evidence that the direction of the relationship between GCs and performance can also depend on individual attributes, such as body condition, sex or reproductive status and reproductive tactics (Tilbrook et al. 2000, Ricklefs and Wikelski 2002, Wey et al. 2015, Blumstein et al. 2016, Vuarin et al. 2019. Under high energy demands triggered by elevated GC concentration, high quality individuals are more likely to prevent themselves from reaching allostatic overload and may perform better than poor quality ones. ...
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Environmental fluctuations force animals to adjust glucocorticoids (GCs) secretion and release to current conditions. GCs are a widely used proxy of an individual stress level. While short-term elevation in GCs is arguably beneficial for fitness components, previous studies have documented that the relationship between long-term baseline GCs elevation and fitness components can vary according to ecological and individual factors and according to the life-history of the species studied. Using longitudinal data on roe deer Capreolus capreolus from two populations facing markedly different environmental contexts, we tested whether baseline GC levels negatively correlate with body mass-a trait positively associated with demographic individual performance-on the short-to long-term. In support, higher baseline GC concentrations were associated to lighter body mass, both measured during the same capture event, in adults of both populations. Overall, we showed that despite the marked environmental and demographic differences between populations and despite the between-sex differences in life history (i.e. reproductive tactics), the relationship between body mass and GCs is consistent across environmental contexts, but might differ according to the life history stage of an individual. This work opens promising perspectives to further explore the relationship between GC and fitness-related traits according to life history stages in free-ranging mammals across seasonal and environmental contexts. The timing and context-dependence of GC levels highlight the complexity of studying stress responses in the wild.
... We included the individual attributes age, sex, mass and location because survival is multi-causal and we wished to account for important attributes with known fitness implications [77][78][79]. Group size was included due to its relationship with fitness correlates in this system [35,44]. Predation index is a binary variable calculated by whether the number of predators observations at that colony was below or above the median number of predator observations across all colony areas in that year [80], providing a value relative to all other years [42]. ...
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For social animals, group social structure has important consequences for disease and information spread. While prior studies showed individual connectedness within a group has fitness consequences, less is known about the fitness consequences of group social structure for the individuals who comprise the group. Using a long-term dataset on a wild population of facultatively social yellow-bellied marmots ( Marmota flaviventer ), we showed social structure had largely no relationship with survival, suggesting consequences of individual social phenotypes may not scale to the group social phenotype. An observed relationship for winter survival suggests a potentially contrasting direction of selection between the group and previous research on the individual level; less social individuals, but individuals in more social groups experience greater winter survival. This work provides valuable insights into evolutionary implications across social phenotypic scales.
... We know that marmots become more socially selective as they age (Wey and Blumstein 2010; Smith et al. 2013) and these early behavioral patterns (e.g., play bouts) likely predict later dominance status . However, while we have known that high-ranking adult female marmots are more stressed and have larger litter sizes than low-ranking ones (Blumstein et al. 2016), the physiological correlates of dominance rank at adulthood is poorly understood for male marmots. ...
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The benefits of dominance may not come without costs, particularly for males. For example, the “immunocompetence handicap hypothesis” states that males with enhanced mating success allocate resources to enhance reproductive output at a cost to their current health, whereas the “resource quality hypothesis” predicts that high-ranking males may benefit from increased reproduction and good health. While the predictions from each have been well tested in captive animals and in a variety of highly social primates, fewer studies have been carried out in free-living, facultatively social animals. Using adult male yellow-bellied marmots (Marmota flaviventer), we evaluated predictions of these hypotheses by examining the relationship between social rank and two health indicators–fecal corticosterone metabolite (FCM) levels, and neutrophil/lymphocyte (N/L) ratios–after accounting for variation explained by age, body mass, and seasonality. We found that higher-ranking males tended to have a lower N/L ratio (reflecting good health) than lower-ranking individuals, whereas FCM levels were not significantly related to rank. In addition, heavier male marmots had lower N/L ratios, while body mass was not associated with FCM levels. We also found that older adult males had lower FCM levels (reflecting less physiological stress) but higher N/L ratios than younger adults. Finally, we found that FCM levels decreased as the active season progressed and FCM levels were associated with the time of the day. Overall, our results suggest that socially-dominant male marmots enjoyed better, not worse health in terms of lower N/L ratios.
... We know that traits reflecting social networks in the marmots are heritable [44] and can negatively impact longevity [45]; and, while we know that older females are less social [42], we are aware of no previous studies that have specifically focused on latelife variation in social behaviour. As for life-history traits, we know that stress hormone levels (faecal glucocorticoid metabolites), which negatively affect marmot survival [46], are negatively associated with age [47], as is vigilance behaviour, but only when adults are in good body condition [48]. In addition, separate studies have found evidence in support of senescence in reproduction and body mass [18,49], and of a terminal decrease in body mass [18]. ...
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Studies in natural populations are essential to understand the evolutionary ecology of senescence and terminal allocation. While there are an increasing number of studies investigating late-life variation in different life-history traits of wild populations, little is known about these patterns in social behaviour. We used long-term individual based data on yellow-bellied marmots ( Marmota flaviventer ) to quantify how affiliative social behaviours and different life-history traits vary with age and in the last year of life, and how patterns compare between the two. We found that some social behaviours and all life-history traits varied with age, whereas terminal last year of life effects were only observed in life-history traits. Our results imply that affiliative social behaviours do not act as a mechanism to adjust allocation among traits when close to death, and highlight the importance of adopting an integrative approach, studying late-life variation and senescence across multiple different traits, to allow the identification of potential trade-offs. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’
Preprint
The yellow-bellied marmot (Marmota flaviventer) study at the Rocky Mountain Biological Laboratory near Crested Butte, Colorado, USA is the world's second longest study of free-living mammals. Quantifying physiological stress is essential for understanding their health, reproductive success, and survival in a variable environment. Historically, we used a validated radioimmunoassay (RIA) to measure fecal glucocorticoid metabolites (FGMs). Given the costs and risks of working with radioisotopes, we have shifted to a more sustainable method. Here we evaluate the suitability of two competitive enzyme-linked immunosorbent assays (ELISA) from Cayman Chemical Company (CCC) and Arbor Assays (AA) to measure corticosterone levels in FGMs. The findings revealed that the AA ELISA, unlike the CCC ELISA, consistently matched the RIA in terms of accuracy across high and low corticosterone concentrations, demonstrated superior assay parameters, showed the highest correlations with RIA results and effectively captured the annual variations in FGM concentrations, indicative of its reliability for use in longitudinal studies. We further analytically validated the usage of the AA ELISA for FGMs, confirming its efficacy without matrix effects, thus establishing its suitability for ongoing and future studies of FGMs in marmots. The transition to the AA ELISA from the RIA ensures continued data integrity while enhancing safety and environmental sustainability.
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This paper updates and extends Dewsbury's (1982) review of the literature on dominance and reproductive success (RS). The findings from approximately 700 studies are included, over two thirds of which were unavailable to Dewsbury. In order to give a highly condensed and yet meaningful overview, the main findings are represented in four tables, one for male nonprimates, one for female nonprimates, one for male primates, and one for female primates. In the tables for males, findings are analyzed in terms of six different indicators of RS, and in the tables for females, in terms of eight RS indicators.Outside the primate order, evidence largely supported the hypothesis that high-ranking males enjoy greater RS than do subordinate males. For females, studies are more evenly divided between those supporting the hypothesis that high rank and RS are positively correlated and those indicating no significant rank-RS relationship. This may reflect both the lower saliency of hierarchical relationships among females, as well as the lower variability in RS among females, relative to males.Among primates, a complex picture has emerged, especially in the case of males. Much of the complexity appears due to the importance of age and seniority in affecting dominance rank. Also, in some primate species, female preferences for sex partners seem to have little to do with the male's dominance rank, at least at the time mating takes place. Nevertheless, the majority of studies suggest that high- to middle-ranking males have at least a slight lifetime reproductive advantage over the lowest ranking males.
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The Columbia Basin pygmy rabbit (Brachylagus idahoensis) is critically endangered and the focus of a captive-breeding program. However, reproductive success in captivity to date has not been sufficient to sustain reintroduction efforts. The goal of this study was to investigate patterns of fecal progestagen and glucocorticoid excretion in females during mating, gestation, and lactation and identify hormonal relationships to reproductive success. Fresh fecal samples were collected from 48 adult, female rabbits over 3 breeding seasons at a frequency of 47 samples per week. Results showed that a large (17-fold) increase in progestagen concentrations 1 day after mating provides a reliable means of determining if a successful mating occurred. In general, higher glucocorticoid concentrations during the breeding season, specifically during mating and gestation, were associated with lower reproductive success. Females that failed to conceive during the breeding season had higher glucocorticoid and lower progestagen baseline concentrations than females that did conceive. Glucocorticoid excretion during late gestation, but not lactation, was negatively associated with litter success, suggesting it affects offspring survival more during the prenatal than the postnatal period. Progestagen and glucocorticoid concentrations at the end of gestation were positively related to litter size, which may be an important factor in juvenile survival. In summary, higher concentrations of fecal glucocorticoids during the breeding season were associated with reduced conception rates and survival of subsequent litters. Ultimately, identifying what factors cause elevated glucocorticoids in pygmy rabbits could provide opportunities to alleviate negative stressors and increase the reproductive output of the captive population.
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Whenever individuals live in stable social groups and not all individuals breed, group members may breed cooperatively. While well-documented in a variety of birds and mammals, there is some controversy over whether, and to what degree, sciurid rodents breed cooperatively. We identify cooperative breeding when: individuals delay dispersal beyond reproductive maturity, reproduction in mature individuals is suppressed, and when non-breeders provide alloparental care. In this paper we note that the 14 species of marmots (Marmota spp.), large ground-dwelling sciurid rodents found throughout the Northern Hemisphere, provide an excellent taxon in which to study the evolution of cooperative breeding. Marmot species fit none, some, or all of the attributes of cooperative breeding. Most interestingly, delayed dispersal and alloparental care may be de-coupled interspecifically, and possibly intraspecifically, making marmots an excellent taxon for additional study. Environmental harshness increases maturation time and is associated with dispersal delayed beyond reproductive maturity. The opportunity to gain direct fitness may be associated with gaining indirect fitness by alloparental behavior. In addition to its theoretical attraction, cooperative breeding has profound implications for conservation and management of species that breed cooperatively. To maximize marmot production, managers and breeders need to pay particular attention to social group structure to prevent the expression of reproductive suppression. If cooperative breeding results from an environmental constraint, habitat modifications may increase the percent of females that breed.
Book
Focusing on the physiological and behavioral factors that enable a species to live in a harsh seasonal environment, this book places the social biology of marmots in an environmental context. It draws on the results of a forty-year empirical study of the population biology of the yellow-bellied marmot near the Rocky Mountain Biological Laboratory in the Upper East River Valley in Colorado, USA. The text examines life-history features such as body-size, habitat use, environmental physiology, social dynamics, and kinship. Considerable new data analyses are integrated with material published over a fifty-year period, including extensive natural history observations, providing an essential foundation for integrating social and population processes. Finally, the results of research into the yellow-bellied marmot are related to major ecological and evolutionary theories, especially inclusive fitness and population regulation, making this a valuable resource for students and researchers in animal behavior, behavioral ecology, evolutionary biology, ecology and conservation.
Chapter
Reproduction can serve as a barometer of animal well-being. Whenever a group of animals stops reproducing, researchers begin to examine various aspects of their well-being. Do they have sufficient food? Are they too crowded? Is housing adequate? Are the animals being stressed? Scientists feel justified in making this correlation between well-being and successful reproduction, because reproduction is one of the most basic drives for all animals. When an animal fails to reproduce, not only is its genetic potential lost, but survival of an entire group may be jeopardized. To prevent such a consequence, an animal will make considerable physiological sacrifices to ensure reproductive success; only the most severe threats to its well-being will prevent the animal from reproducing.
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Chronic activation of the stress axis caused by long‐term uncontrollable and unpredictable factors in the environment has been regarded as causing maladaptive and/or pathological effects, both by those studying animals in the laboratory and in nature. While pathology may apply to the former, I argue that it does not apply to the latter. Our thinking on the role of chronic stress in animals in nature has been heavily influenced by biomedical research, but much less so by the ecological and evolutionary context within which animals actually function. I argue that when such stressors occur (e.g. periods of high predation risk, food limitation, prolonged severe weather, social conflict, etc.), although the animal may be chronically stressed, its responses are adaptive and continue to promote fitness. Chronic stressors in nature can be subdivided into whether they are reactive (direct physiological challenges threatening homeostasis and not requiring cognitive processing – for example, food limitation) or anticipatory (perceived to be threatening and requiring cognitive processing – for example, high predation risk). For anticipatory stressors, their impact on the animal should not be based on their absolute duration (they may be acute), but rather by the duration of their physiological consequences. The anticipatory stressor of persistent high predation risk does not elicit chronic stress in all prey classes. Cyclic snowshoe hare and arctic ground squirrels exhibit evidence of chronic stress when predator numbers are high, but cyclic vole and noncyclic elk populations do not. I suggest that chronic stress has evolved to benefit the fitness of the former and not the later, with the key factors being lifespan and life history. I propose that chronic stress evolves in a species only if it is adaptive.