Behavioral Ecology
doi:10.1093/beheco/arq137
Advance Access publication 30 August 2010
No direct fitness benefits of helping in
a cooperative breeder despite higher survival of
helpers
Jessica Meade and Ben J. Hatchwell
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK
Helpers in cooperatively breeding species may gain direct fitness benefits that increase their survival probability and/or reproductive success. However, survival and productivity may be influenced by many other factors, including variation in dispersal,
nepotistic interactions, or individual condition. High helper survival relative to nonhelpers has been reported in the long-tailed
tit Aegithalos caudatus, a cooperative breeder where helpers are failed breeders that redirect care toward kin. Using capturemark-recapture analysis of a long-term data set, we confirm this result and show that it is not attributable to differential dispersal.
Then, using only males with first-order relatives (to control for any effects of nepotism), we investigated the survival of 3 groups of
failed breeders (i.e., potential helpers): survival of helpers was highest (61%) but, contrary to predictions based on direct
benefits, survival of 2 categories of nonhelpers differed; those with helping opportunities had the lowest survival rate (24%),
whereas those without helping opportunities had intermediate survival (52%). We suggest that the groups varied in condition;
helpers are in good condition, males with helping opportunities who did not help are in poor condition, and nonhelpers without
helping opportunities comprise a mixture of birds in good and poor condition. This conclusion was supported by differences in
the timing of breeding (a proxy for condition) between groups: helpers bred earliest and nonhelpers with helping opportunities
bred latest. Furthermore, we found no evidence that helpers gained any future reproductive benefits. We suggest that condition
rather than benefits accrued as a direct result of helping influenced helper survival. Key words: condition, direct fitness, helper,
long-tailed tit, survival. [Behav Ecol 21:1186–1194 (2010)]
n cooperatively breeding species, helpers are individuals
that forego independent reproduction and care for the
young of others. This helping behavior can provide helpers
with direct and/or indirect fitness benefits. Direct fitness benefits enhance helpers’ own survival and/or reproductive success, whereas indirect fitness benefits are gained via kin
selection when cooperation is directed toward relatives and
increases either the productivity or survival of related breeders
(Hamilton 1964; Brown 1978; Cockburn 1998).
Helpers can gain direct survival benefits from group membership via 2 routes. First, helpers can work to ‘‘pay’’ breeders
for the privilege of remaining within their social group
(Gaston 1978), whereas individuals that do not help are expelled from the territory (e.g., Mulder and Langmore 1993;
Balshine-Earn et al. 1998). Second, under the assumption that
individuals in larger groups have a greater chance of survival,
helpers can gain direct survival benefits via group augmentation (Brown 1978; Kokko et al. 2001). If the presence of
a helper in a group leads to a larger group size via increased
productivity, then the survival of the entire group increases,
including that of the helper (Emlen 1991; Kokko et al. 2001).
This hypothesis has proved difficult to test directly, and consequently, there is currently no direct empirical evidence for
group augmentation as a key driver of cooperative breeding
(Wright 2007).
Though helping can theoretically lead to enhanced helper
survival, it is also likely to be costly to the helper in terms of
energy expenditure (e.g., Reyer 1984; Grantner and Taborsky
I
Address correspondence to J. Meade. E-mail: [email protected].
uk.
Received 10 February 2010; revised 8 July 2010; accepted 12
July 2010.
The Author 2010. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
1998), survival (e.g., Rabenold 1990), or future fecundity
(Clutton-Brock 1991; for review, see Heinsohn and Legge
1999). Indeed, condition-dependent caring has been demonstrated for helpers in cooperatively breeding meerkats
Suricata suricatta (e.g., Clutton-Brock et al. 1998; Russell
et al. 2003), and in experimental studies, helpers receiving
supplemental food increased their level of care (Eden 1987;
Boland et al. 1997). There is also some limited evidence that
the decision of whether to help or not help is influenced by
individual condition (Eden 1987; Emlen and Wrege 1988).
An individual’s quality may also influence helping decisions,
although there is disagreement over the direction of this potential effect. Several authors suggest that helpers are likely
to be high-quality individuals because delayed dispersal, one
of the prerequisites for helping in many group territorial cooperatively breeding species, is influenced by individual quality, with higher quality individuals remaining on the natal
territory (Black and Owen 1987; Strickland 1991; Ekman
et al. 2002; but see also Richner 1990). In contrast, Heinsohn
and Legge (1999) have argued that poor-quality individuals
with a low chance of future independent reproduction might
devote more time or effort to helping than higher quality
individuals. The idea that condition or quality might influence the decision to help or influence the amount of help
provided is of fundamental importance in determining the
fitness consequences of helping in cooperative breeders, yet
this issue has rarely been addressed (but see Schürch and Heg
2010).
The survival rates of helpers may also be affected by nepotism. In cooperative breeding systems where help is directed
at kin, helpers are necessarily more likely to have close relatives
in the population than nonhelpers. Nepotism could lead to
enhanced survival through several processes, including reduced parental aggression (Ekman et al. 2000; Griesser and
Meade and Hatchwell • Direct benefits do not explain higher helper survivorship
Ekman 2004), parental concession at food sources (Scott
1980; Barkan et al. 1986; Pravosudova et al. 2001), and nepotistic alarm calling (Sherman 1985; Ekman et al. 2000, 2004).
Related flock members may therefore have higher survival
rates than nonrelatives (Griesser et al. 2006), so high survivorship of helpers relative to nonhelpers may arise simply because they have more relatives in the population rather
than as a benefit of helping per se. Thus, helper survival is
potentially influenced not only by direct consequences of
helping but also by several other factors working in different
directions.
As well as potential survival benefits, helpers may also accrue
direct fitness benefits in the form of enhanced breeding
success, through various routes (Brown 1978; Emlen 1991;
Cockburn 1998; Dickinson and Hatchwell 2004). Helpers
can potentially gain breeding territories or breeding partners
(e.g., Reyer 1990), receive reciprocal help from the grown
offspring of helped broods (Wiley and Rabenold 1984), acquire experience of brood care (Skutch 1961), or gain access
to direct reproduction in the current brood (e.g., Richardson
et al. 2001). It has been suggested that the role of direct
fitness benefits has been neglected and that of indirect fitness
benefits overstated in explanations for the evolution of vertebrate cooperative breeding systems (Clutton-Brock 2002).
In this study, we use the cooperative breeding system of the
long-tailed tit Aegithalos caudatus to determine whether helpers accrue direct fitness benefits as a consequence of helping.
The long-tailed tit lends itself well to investigations of this sort
because unlike most other cooperatively breeding species,
long-tailed tit helpers are adults whose own breeding attempts
have failed and who show a strong tendency to redirect their
care toward close relatives (Russell and Hatchwell 2001; Nam
et al. 2010). Therefore, helping is not confounded by age
because individuals are able to switch back and forth between
breeding and helping throughout their lifetimes. Long-tailed
tits are also relatively short-lived, so differences in survival
are likely to be easier to detect than in many longer lived
cooperatively breeding species.
A previous study showed that long-tailed tit helpers have
higher survival rates than nonhelpers (McGowan et al.
2003), and the authors concluded that this increase in survival was due to a direct fitness benefit of helping, such as
winter group membership or preferential roosting positions
(Hatchwell et al. 2009). There are several alternative explanations for the relatively high survivorship of helpers. 1) Nonhelpers may disperse further than helpers, resulting in
the observed survival difference because in capture-markrecapture (CMR) studies death is not functionally different
from dispersal beyond study site boundaries. 2) Helpers may
survive better than nonhelpers through nonspecific nepotistic
effects of having close kin in the population rather than as
a consequence of helping per se. 3) Birds that choose to help
may be in relatively better condition than nonhelpers and
thus more likely to survive the winter.
We first repeat the analysis of the relative survival rates of
long-tailed tits of differing breeding status at the population
level by McGowan et al. (2003) with a substantially larger data
set. Second, we investigate the possibility of differential dispersal of failed breeders leading to ‘‘survival’’ differences.
Third, we examine the possibility that variation in condition
between helpers and nonhelpers could influence the observed survival rates while controlling for the presence of
close relatives in the population and hence any effects of
nepotism. The availability of first-order relatives with active
nests is known to be a critical factor in a long-tailed tit’s decision to help (Russell and Hatchwell 2001). For each failed
breeder, we were able to calculate whether or not a first-order
relative had an active nest that was available to be helped,
1187
following the failure of the unsuccessful breeders’ own breeding attempt. This allowed us to divide the failed breeders into
3 groups: helpers, nonhelpers that had the opportunity to
help, and nonhelpers that did not have the opportunity to
help. If the decision to help was independent of condition
and resulted in direct fitness benefits that enhanced survival,
then we expected the survival rate of helpers to be high, and
the survival rates of the 2 groups of nonhelpers to be equal
and lower. If the decision to help was influenced by condition,
then the survival rate of helpers was expected to be highest,
the survival rates of nonhelpers with the opportunity to help
to be lowest, and the survival rate of nonhelpers without the
opportunity to help to be intermediate (because this group is
likely to be a mixture of birds in good condition that would
have helped if the opportunity had arisen, and those in poor
condition that wouldn’t have helped given the opportunity).
Finally, we investigate whether helpers gain any direct fitness
benefit through enhanced future reproductive success.
METHODS
Study system
We used data collected between 1995 and 2009 from a study
population of 25–72 pairs of long-tailed tits in the Rivelin
Valley, Sheffield, UK (lat 5323# N, long 134# W). Each year,
all birds form monogamous breeding pairs in the early spring
and work together to build elaborate domed nests comprising
an outer structure of moss, lichen, plant fibers, and spider
silk, lined with up to 2600 feathers (Lack and Lack 1958;
Gaston 1973; Hansell 1993, 2000). The nests may take several
weeks to complete (McGowan et al. 2004). Nest sites are identified during nest building and once located, any un-ringed
birds are caught in mist nets, uniquely color-ringed, weighed,
and blood samples are taken from the brachial vein (under
UK Home Office Licence). Nests are closely monitored and
the timing of laying, clutch size, hatch date, brood size, and
fledge date are recorded. Clutch sizes range from 7 to 12 eggs
(typically 9–11). There are high levels of nest depredation at
all stages of nesting and if this occurs early enough in the
season, new nesting attempts are often made. We located
new nests in intensive searches of the field site. Some birds
whose own nesting attempts fail redirect their care and help
to feed the offspring of other pairs. Nestlings hatch synchronously and nests are observed from hatching (day 0) until
fledging (day 16–17) or failure, typically every second day
for 1 h, so that all carers at the nest can be identified. Nestlings in accessible nests are weighed, color-ringed, and blood
samples are taken on day 11. Blood samples are subsequently
used to sex adults and nestlings using molecular techniques
(Griffiths et al. 1998). Birds ringed as adults (i.e., immigrants
to the study population) were assumed to be 1-year olds at
time of ringing (this is a reasonable assumption as there is no
evidence that any significant dispersal occurs after a bird’s
first winter (McGowan et al. 2003). Birds were defined as
successful breeders if their brood fledged in a given year
(long-tailed tits are always single brooded). Long-tailed tit
helpers are typically male (85%) because males are more
philopatric than females (Sharp et al. 2008). Throughout
the analyses, a helper is defined as any bird observed feeding
offspring that were not in their own nest. Age is defined as the
age in years of birds in year n, and the number of relatives is
defined as the number of known first-order relatives present
in year n determined by pedigree information. Where there
were observations for the same bird from multiple years, 1
observation was randomly selected (excepting the CMR analysis). For more details about the species and study site, see
Hatchwell and Sharp (2006).
Behavioral Ecology
1188
Capture-mark-recapture analysis
To estimate the relative survival of individuals of differing
breeding status, we used a multistrata modeling approach
within Program MARK, a freely available CMR software developed by White and Burnham (1999). This program allows the
resighting history of individuals to be separated into different
strata or states (in this case breeding status), and the likelihood of re-encountering individuals can be determined by 3
probabilities: the probability of survival (U, defined as being
alive and available for recapture within the study area), the
resighting probability (P), and the probability of moving from
one state to another (w).
For this analysis, we included all birds from 1995 to 2009 of
known sex and breeding status throughout their adult lives
(n ¼ 333 males and 310 females). Each year, birds were classified as falling into 1 of 4 breeding status categories: a failed
breeder that did not help (F), a failed breeder that helped
(H), a successful breeder that was helped at the nest (A), and
a successful breeder that was not helped at the nest (N).
We did not expect the resighting probability to vary with
either sex or the previous year’s breeding status because the
sex ratio within the field site is ;50:50 and all birds attempt to
breed as a pair at the beginning of each season and therefore
are equally likely to be observed. The intensity of fieldwork
has been constant throughout the study, so the resighting
probability was assumed to be constant, apart from in 2001
when access to the field site was limited by restrictions imposed after an outbreak of foot and mouth disease. We therefore divided the resighting probability into 2 levels: 2001 and
the remaining years.
To understand the fitness consequences of helping, we examined the probability of moving from one breeding status
to another between years, allowing us to estimate the likelihood of an individual with a particular breeding status in year
n becoming a successful breeder in year n 1 1. We therefore
compared models where w (the probability of movement
from one state to another) was allowed to vary by breeding
status (F, H, A, N) and by sex (s).
Therefore, our general model was U((F,H,A,N)3s) P(2)
w((F,H,A,N)3s), where survival probability (the probability
that an individual is alive and available for recapture within
the study area) is allowed to vary with sex and with breeding
status, resighting probability has 2 levels (one for 1995–2000
and 2002–2009 and a second for 2001), and the probability of
moving from one breeding status to another varies with sex
and with the previous year’s breeding status. To assess the
goodness of fit of the general model, we calculated ĉ within
Program MARK. This provides an estimate of the overdispersion of the data (see White and Burnham 1999 for more details). The estimate of ĉ was 0.98. A value of ĉ close to 1
indicates that the data does not violate the basic rules of
a CMR modeling approach.
We considered the effect of breeding status on survival in 5
ways that specified relative survival rates according to status:
full breeding status effect in which each status could differ
(F, H, A, N); worker effect in which failed breeders differed
from other states in not having fed a brood to fledging (F,
H ¼ A ¼ N); breeder effect in which those birds raising their
own brood differed from those that did not (F ¼ H, A ¼ N);
successful breeder effect, as for breeder effect but helpers
and failed breeders were allowed to differ (F, H, A ¼ N); and
no breeding status effect where survival rate was unaffected by breeding status (F ¼ H ¼ A ¼ N). We also compared
models that allowed survival to vary with sex and breeding
status and models where the breeding status transitions
varied either between the 4 breeding statuses or by both
sex and breeding status. We therefore constructed and compared a total of 20 models. The final model selection is based
on corrected Akaike’s Information Criterion (AICc) that
considers the deviance and the number of estimated
parameters (see Burnham et al. 1987 and Lebreton et al.
1992 for detailed descriptions). The model with the lowest
AICc is deemed the best-fitting model. The top 10 bestfitting models are displayed in order of best fit in the results
(Table 1).
We then went on to perform a second analysis, this time taking advantage of the detailed nature of our data. Only male
birds with living first-order relatives throughout their lifetimes
were included in the analysis (n ¼ 135), and this time ‘‘failed
breeders that did not help’’ were further divided into 2 categories; those that had the opportunity to help first-order relatives with active nests and those that did not. We constructed
and compared 5 models. Birds were defined as falling into 4
states: successful breeders (regardless of whether they received help) (S), helpers (H), failed breeders that did not
have the opportunity to help (Fn), and failed breeders that
did have the opportunity to help but chose not to (Fo). The
probability of recapture remained set at 2 levels (2001 and the
remaining years), and the probability of changing state was
allowed to vary between breeding states. The models are displayed in order of best fit in the results (Table 2). The estimate of ĉ was 0.93 indicating that the basic rules of the CMR
modeling approach were not violated.
Table 1
Ten best-fitting models of the survival probability of adult long-tailed tits in relation to sex and breeding status, based on the corrected Akaike’s
Information Criterion (AICc). The best fitting model is shown in bold
1
2
3
4
5
6
7
8
9
10
Model
AICc
DAICc
AICc weight
Number of parameters
Deviance
F(F,H,A 5 N)P(2)w(F,H,A,N)
U(F,H ¼ A ¼ N)P(2)w(F,H,A,N)
U(F,H,A ¼ N)P(2)w((F,H,A,N)3s)
U(F,H ¼ A ¼ N)P(2)w((F,H,A,N)3s)
U(F,H,A,N)P(2)w(F,H,A,N)
U(F,H,A,N)P(2)w((F,H,A,N)3s)
U(F ¼ H ¼ A ¼ N)P(2)w(F,H,A,N)
U((F,H,A ¼ N)3s)P(2)w(F,H,A,N)
U((F,H ¼ A ¼ N)3s)P(2)w(F,H,A,N)
U(F ¼ H ¼ A ¼ N)P(2)w((F,H,A,N)3s)
2791.51
2791.99
2792.47
2792.83
2793.52
2794.54
2795.73
2795.99
2796.06
2796.44
0.000
0.482
0.963
1.321
2.009
3.031
4.220
4.483
4.551
4.930
0.233
0.183
0.144
0.120
0.085
0.051
0.028
0.025
0.024
0.020
17
16
29
28
18
30
15
20
18
27
1413.8
1416.4
1389.7
1392.1
1413.7
1389.6
1422.15
1412.1
1416.3
1397.8
U ¼ survival probability, P ¼ resighting probability, w ¼ breeding status transition probability, s ¼ sex, A ¼ helped successful breeder,
N ¼ unhelped successful breeder, H ¼ helper, F ¼ nonhelper, 3 ¼ interaction.
Meade and Hatchwell • Direct benefits do not explain higher helper survivorship
1189
Table 2
Five models of survival probability for adult male long-tailed tits with living first-order relatives displayed in order of best fit, based on the
corrected U 5 survival probability, P 5 resighting probability, c 5 breeding status transition probability, S 5 successful breeder, H 5 helper,
Fn 5 nonhelper without the opportunity to help, Fo 5 nonhelper with the opportunity to help. The best fitting model is shown in bold
1
2
3
4
5
Model
AICc
DAICc
AICc weight
Number of parameters
Deviance
F(S,H 5 Fn,Fo)P(2)w(S,H,Fn,Fo)
U(S,H,Fn,Fo)P(2)w(S,H,Fn,Fo)
U(S,H,Fn ¼ Fo)P(2) w(S,H,Fn,Fo)
U(S,H ¼ Fn ¼ Fo)P(2) w(S,H,Fn,Fo)
U(S,Fn,H ¼ Fo)P(2) w(S,H,Fn,Fo)
657.24
658.78
663.88
667.40
668.73
0.000
1.543
6.643
10.157
11.494
0.663
0.307
0.024
0.004
0.002
16
17
16
15
16
407.9
407.1
414.6
420.4
419.4
Breeding dispersal
In population studies conducted in finite study areas with porous boundaries, survival may be indistinguishable from dispersal. Therefore, to determine whether helping status
influenced breeding dispersal (i.e., dispersal between breeding events in different years), thereby confounding survival
estimates, we modeled dispersal distance within the study site
between year n and n 1 1 for male failed breeders in year n
that survived to year n 1 1. We focused on males because
a large majority of helpers are male (Hatchwell et al. 2004).
To investigate whether dispersal distance depended on helping status, we fitted a linear model. The dependent variable
was dispersal distance defined as the straight line distance (m)
between the final nest in year n and the first nest in year n 1 1
for each bird (n ¼ 116; 36 helpers and 80 nonhelpers). We
used the function boxcox in the R package car to transform
the response variable to facilitate normal and heteroscedastic
errors. The explanatory variables were helping status (helper
or nonhelper in year n), age, and population density in year
n 1 1. ‘‘Population density’’ was the total number of breeding
birds during the year n 1 1 breeding season, and we included
this as an explanatory variable because birds may have had to
travel further to find a suitable breeding location in years of
high population density.
Timing of breeding
To further investigate any effect of condition on the decision
to help, we used timing of breeding as a proxy for condition
in year n. We were unable to use a direct measure of body
condition such as fat storage or protein reserves (Gosler 1991)
because birds in the study population were caught only for the
purposes of ringing and therefore often as chicks or in a season previous to year n. Individuals in good condition are
known to breed earlier in the season than those in poor condition in many bird species (Perrins 1970; Ewald and Rohwer
1982; Davies and Lundberg 1985; Perrins and McCleery 1985;
Wright and Cuthill 1992; Wendeln 1997) and this is likely to
be the case in the long-tailed tit because they have a temporally
constrained breeding season (MacColl and Hatchwell 2002).
Furthermore, timing of breeding is likely to reflect the condition of males as well as females because both sexes invest very
heavily in building their complex nests over a period of several weeks (McGowan et al. 2004).
We used a subset of the data that included only male failed
breeders forming part of a pair for which the first clutch lay
date in year n was available (n ¼ 69; 22 helpers, 31 nonhelpers
(relative unavailable) and 16 nonhelpers (relative available).
We fitted a linear model using ‘‘relative lay date’’ defined as
a pair’s lay date in year n (first nesting attempts only) minus
the median first attempt lay date for all pairs in that year as
the dependent variable. This correction was performed to
control for the substantial annual variation in lay date caused
by variable spring temperature (MacColl and Hatchwell
2002). Thus, a negative lay date indicates birds that bred early
relative to the yearly median and a positive lay date indicates
birds that bred late. The explanatory variables were helping
status and age. ‘‘Helping status’’ was defined as 1 of 3 groups:
helpers, nonhelpers whose relatives had an active nest, and
nonhelpers whose relatives did not have an active nest in year
n. Age was included to control for any effect that age might
have on timing of breeding.
In order to examine whether the stage at which a bird failed
in its own breeding attempt influenced its helping decision, we
used the same data set to investigate whether the 3 types of
failed breeder differed in the stage (egg or chick) that their
most developed nest in year n reached before failure, using
a chi-squared test.
Future reproductive success
To investigate the future reproductive success of failed
breeders, we used 2 approaches. First, we modeled the likelihood that a failed breeder surviving to year n 1 1 would breed
successfully in year n 1 1 depending on their helping status in
year n (helper or nonhelper). Second, of those birds that did
breed successfully in year n 1 1, we investigated how many of
the offspring produced recruited successfully into the breeding population in year n 1 2. The latter approach is the best
measure of success because if helping in year n increases the
likelihood of having helpers in year n 1 1, the effect on reproductive success would be observed only in the recruitment
of offspring in year n 1 2 (Hatchwell et al. 2004).
To model the likelihood of breeding successfully in year
n 1 1 depending on helping status in year n, we fitted a generalized linear model with a binomial error and a logit link
function with a binary response variable of ‘‘bred successfully
in year n 1 1?’’ that took a value of 1 if the bird fledged chicks
in year n 1 1 and a value of 0 otherwise (n ¼ 119; 47 helpers
and 72 nonhelpers). The explanatory variables were helping
status, age, and number of relatives. Helping status was
whether the bird was a helper or a nonhelper in year n. Number of known relatives was included to control for any advantage of having associated with close kin overwinter that could
increase the likelihood of breeding successfully in year n 1 1.
For our second analysis, we had a much smaller sample size
due to the high annual mortality of adults and the low probability of successful breeding in year n 1 1 (n ¼ 44; 17 helpers
and 27 nonhelpers). We modeled the likelihood of recruiting
offspring into the breeding population in year n 1 2 based on
helping status in year n. Only those males that survived and
bred successfully in year n 1 1 were included. We used a generalized linear model with a binomial error and logit link
function. The binary response variable was ‘‘recruits in year
n 1 2’’ that took a value of 1 if male offspring from year n 1 1
recruited into the breeding population in year n 1 2 and
a value of 0 otherwise. Only male recruits were included because females are dispersive and very few recruit into the
breeding population within our study site; it is therefore
Behavioral Ecology
1190
difficult to estimate the survival and subsequent recruitment
of female offspring. The explanatory variables were helping
status, age, and winter rainfall in year n 1 1. ‘‘Winter rainfall
in year n 1 1’’ was included because this has been shown to
affect adult survival (Meade J, unpublished data) and therefore is likely to have an effect on the probability of offspring
surviving to year n 1 2.
RESULTS
CMR analysis
The final accepted model was the ‘‘successful breeder’’ model
where successful breeders (both helped and unhelped) had
the same likelihood of survival (0.51 6 0.03 standard error
[SE]), failed breeders that chose to help had the highest
survival probability of 0.59 6 0.04, and failed breeders that
did not help had the lowest survival probability of 0.45 6 0.02
(Table 1; Figure 1).
This analysis also calculates the likelihood of birds moving
from one breeding status to another. The best-fitting model
predicted a 0.28 6 0.05 SE probability that helpers would
breed successfully in year n 1 1 and a 0.32 6 0.03 probability
that nonhelpers would breed successfully in year n 1 1. When
this difference was examined in greater detail by running
a model with the likelihood of breeding successfully in year
n 1 1 set as equal for helpers and nonhelpers, this model was
more parsimonious than the previous model (AICc ¼ 2787.80
vs. 2791.51), indicating that there was no significant difference in the likelihood of breeding successfully in year n 1 1
between helpers and nonhelpers (P ¼ 0.31 6 0.03 for both
helpers and nonhelpers).
A second analysis was performed, including only male
breeders with first-order relatives in the population, to facilitate the division of failed breeders that did not help into
2 groups, those without relatives available to be helped, and
those with relatives available to be helped. When survival rates
were compared between successful breeders, helpers, and the
2 types of nonhelpers, we found that again helpers had the
highest survival rate of 61%, and failed breeders without available relatives had a survival rate of 52%; however, we found
that the best-fitting model (see Table 2; Figure 2) was 1 where
the survival rates of helpers and nonhelpers without available
relatives were not significantly different (0.56 6 0.08 SE) and
the survival rate for nonhelpers that had relatives available was
significantly lower (0.24 6 0.06). The survival rate of successful breeders was estimated as 0.51 (60.06), which is very similar to the estimate for the larger sample size. When the
likelihood of breeding successfully in year n 1 1 was compared for helpers and nonhelpers that did not have the opportunity to help in the same way as described above, we
found no significant difference between the 2. Both helpers
and nonhelpers that did not have the opportunity to help had
a likelihood of breeding successfully in year n 1 1 of 0.28 6
0.06. Nonhelpers that did have the opportunity to help had
a likelihood of breeding successfully in year n 1 1 of 0.20 6
0.13.
Breeding dispersal
Helping status in year n had no effect on breeding dispersal
distance between year n and n 1 1 (df ¼ 1, P ¼ 0.443). Helpers in year n dispersed on average 620 m 6 88 SE and nonhelpers dispersed on average 583 m 6 60. Therefore, there
was no indication that the effect of helping on the survival of
failed breeders (Figure 1) was confounded by differential
dispersal. Population density in year n 1 1 also had no effect
on dispersal distance (estimate ¼ 20.001, SE ¼ 0.004, df ¼ 1,
P ¼ 0.786), but we found that breeding dispersal distance
decreased significantly with age (estimate ¼ 20.240, SE ¼
0.120, df ¼ 1, P ¼ 0.044). Birds aged 1 in year n dispersed
on average 687 m 6 68 (n ¼ 69) between year n and year n 1
1, birds aged 2 in year n dispersed 471 m 6 79 (n ¼ 33), and
birds aged 3 or more in year n dispersed 431 m 6 116 (n ¼ 14;
all values from raw data).
Timing of breeding
Birds that chose to help in year n had started their own breeding attempts significantly earlier in the breeding season in
0.7
0.7
0.6
Predicted survival
Predicted survival
0.6
0.5
0.4
0.3
0.2
0.5
0.4
0.3
0.2
0.1
0.1
0.0
Successful breeder
0.0
Helper
Nonhelper
Nonhelper
(relative unavailable) (relative available)
Successful breeder
Helper
Nonhelper
Breeding status
Figure 1
The effect of breeding status on the survival probability (6SE) of
adult long-tailed tits. The values shown are the parameter values from
the best-fitting model (Table 1).
Breeding status
Figure 2
The effect of breeding status on the survival probability (6SE) of
adult male long-tailed tits with first-order relatives in the population.
The values shown are the parameter values from the best-fitting
model (Table 2).
Meade and Hatchwell • Direct benefits do not explain higher helper survivorship
3
n=22
n=31
n=16
Nonhelper
Nonhelper
Relative lay date
2
1
0
−1
−2
−3
Helper
(relative unavailable) (relative available)
Breeding status
Figure 3
Relative timing of breeding in year n in relation to subsequent
breeding status in the same year. Values are the mean values from the
raw data for each status 6 SE.
year n than those birds that chose not to help their available
relatives. Birds whose relatives were unavailable to be helped
had an intermediate timing of first nesting attempt (df ¼ 2,
P ¼ 0.019; Figure 3). This result was not confounded by age
(estimate ¼ 0.36, SE ¼ 0.53, df ¼ 1, P ¼ 0.486).
There was no difference between the 3 types of failed
breeders in the proportion of birds failing during the egg
phase and the proportion failing during the chick phase
(v2 ¼ 1.086, df ¼ 2, P ¼ 0.581).
Future reproductive success
Helping status in year n had no significant effect on the likelihood of breeding successfully in year n 1 1 (df ¼ 1, P ¼
0.123). Furthermore, the probability of breeding successfully
in year n 1 1 was not significantly affected by either the number of known first-order relatives in the population in year n
(estimate ¼ 20.06, SE ¼ 0.12, df ¼ 1, P ¼ 0.595) or by age
(estimate ¼ 0.14, SE ¼ 0.24, df ¼ 1, P ¼ 0.556). Similarly, we
found no significant effect of either helping status (df ¼ 1,
P ¼ 0.414), age (estimate ¼ 20.21, SE ¼ 0.38, df ¼ 1, P ¼
0.560), or winter rainfall in year n 1 1 (estimate ¼ 0.17,
SE ¼ 0.55, df ¼ 1, P ¼ 0.765) on whether or not year n 1 1
offspring survived to year n 1 2.
DISCUSSION
Using 14 years of data, we confirmed that at the population
level, long-tailed tit helpers have a significantly higher probability of survival than failed breeders that do not help (nonhelpers). When first reported by McGowan et al. (2003), this
result was interpreted as an indication that helpers gain direct
fitness benefits from helping that enhance their survival.
Here, we took advantage of the detailed nature of our data
set to test several other possible explanations for this relatively
high survival rate that need not include direct fitness benefits.
We also used our long-term data set to determine whether
helpers gained direct fitness benefits by increasing their future reproductive success. We first discuss alternative explan-
1191
ations for the increased survivorship of helpers relative to
nonhelpers and then the apparent absence of direct fitness
benefits from helping in this species.
One explanation for the survival difference between helpers
and nonhelpers could be differential dispersal between breeding seasons by the 2 categories of failed breeder. Survival in
CMR analyses is defined as ‘‘an individual being alive and
available within the study area for recapture,’’ so death
and dispersal are functionally the same. Individual strategies
of dispersal and cooperation are linked in some other cooperative breeders (e.g., Young et al. 2005; Ridley et al.
2008), but here, controlling for age and population density,
we found no difference in dispersal distance within our study
site for helpers and nonhelpers. We thus conclude that our
survival estimates are not confounded by dispersal.
A second explanation is that some form of nepotism affects
helper survival rates independently of helping because in the
long-tailed tit system, nonhelpers are less likely than helpers
to have first-order relatives in the population (Russell and
Hatchwell 2001). Such effects of nepotism on survival have
been extensively documented in cooperative and noncooperative species (Ekman et al. 2004). We did not test this
hypothesis directly, but to control for the possibility, we conducted analyses that included only those birds that had at
least 1 first-order relative in the population. Finally, variation
in condition or quality may affect failed breeders’ decisions of
whether or not to help. The status ‘‘helper’’ is the only status
that an adult long-tailed tit has the opportunity to actively
enter. Several studies have identified short-term costs to helping (Brown et al. 1982; Arnold 1990; Heinsohn and Cockburn
1994; Clutton-Brock et al. 1998), and there is evidence that
individual condition affects not only the work rate of helpers
(Eden 1987; Boland et al. 1997) but also the decision to help
(Eden 1987; Emlen and Wrege 1988). Therefore, we examined the hypothesis that the high survivorship of helpers relative to nonhelpers is a result of birds in better condition or of
higher quality being more likely to become helpers.
Helping behavior in long-tailed tits is kin selected (MacColl
and Hatchwell 2004), and the decision to help is determined
principally by the availability of a close relative with an active
nest (Russell and Hatchwell 2001; Nam et al. 2010). Because
we had detailed data including the timing of nesting failure
and pedigree information, we were able to divide failed
breeders into 3 groups: 1) birds with first-order relatives with
active nests available that chose to help; 2) birds with firstorder relatives with active nests that chose not to help even
though they had the opportunity to do so; and 3) birds with
first-order relatives in the population without active nests who
therefore did not have the opportunity to help. Modeling the
survival of these 3 groups allowed us to investigate the factors
causing the high survival rate of helpers. If high helper survival was caused solely by direct fitness benefits of helping, we
expected the survival of the 2 groups of nonhelpers to be
equal and lower than that of helpers. In fact, we found that
helpers have the highest survival (61%), but survival of the 2
groups of nonhelpers is not equivalent. Nonhelpers that have
relatives available to be helped have the lowest survival of
24%, whereas nonhelpers without relatives available have considerably higher survival of 52% which is not significantly different from the survival rate of helpers. We can also dismiss
the possibility that the decision of whether to help when given
the opportunity was related to the distance that potential
helpers had to travel in order to reach an active nest. The
mean distance traveled by helpers was 380 m 6 47 SE (n ¼
44), and the mean distance from the failed nest of nonhelpers
to the nearest active nest belonging to a first-order relative was
353 m 6 42 (n ¼ 48; generalized linear model controlling for
age: distance, P ¼ 0.780). The survival pattern observed is
Behavioral Ecology
1192
what would be expected if the decision to help was caused by
variation in individual condition or quality. Birds choosing to
help are individuals in good condition and have correspondingly high survival; birds that chose not to help available relatives are in poor condition and have a low survival rate; and
birds without relatives available to be helped are likely to be
a mixture of birds in good and poor condition and hence
would have an intermediate level of survival.
Individual condition or quality is a notoriously difficult
‘‘trait’’ to measure (Wilson and Nussey 2010), and we have
no direct metric in long-tailed tits. Therefore, we used timing
of breeding in year n as a proxy for condition or quality to
examine whether this life history trait differed between these
groups of failed breeders. We modeled the timing of breeding
of these 3 groups (controlling for age) and found that birds
that subsequently became helpers bred on average 3 days
earlier than those failed breeders that chose not to help available relatives (failed breeders without available relatives had
an intermediate relative timing of breeding). Long-tailed tits
are single brooded and have a highly constrained breeding
season (MacColl and Hatchwell 2002), the mean time interval
between the median first egg lay date of first clutches and first
egg lay date of final clutches is 30 days, with a range of 15–43
days (Hatchwell BJ and Meade J, unpublished data), so a difference of 3 days in the initiation of breeding may represent
a significant proportion of the breeding season. Our timing of
breeding results is consistent with the survival results and reinforce that the idea that the relatively high survival of helpers
compared with nonhelpers may be caused by differences in
condition rather than by birds accruing direct survival benefits from helping.
There are multiple routes through which helpers might gain
direct fitness benefits from helping (see Introduction), but the
ultimate test of the hypothesis is to examine whether the reproductive success of helpers is enhanced as a consequence of
their cooperative behavior. We found no evidence that helpers
gain any direct fitness benefit from helping via increased future fecundity. Birds that became helpers in year n had no
reproductive advantage over nonhelpers in year n 1 1; there
was no difference in the likelihood that failed breeders and
helpers would breed successfully in year n 1 1 nor was there
a difference in the chance of offspring from these successful
breeding attempts recruiting into the breeding population in
year n 1 2. This finding is perhaps unsurprising because many
of the hypothesized direct fitness benefits that helpers in cooperative breeding systems might accrue (Cockburn 1998) do
not apply to long-tailed tits. In terms of future direct benefits,
long-tailed tits are nonterritorial, so there is no possibility of
territory inheritance. Likewise, in the absence of territoriality,
helping cannot be interpreted as payment of rent (Gaston
1978). Most helping occurs between siblings (Russell and
Hatchwell 2001) and the high annual mortality rate reported
here also show that there is little potential for reciprocity from
helped broods. Higher reproductive success of helpers relative to nonhelpers would also be predicted if helpers gain
experience of breeding (Skutch 1961). This is most likely to
apply in long-lived species (e.g., Heinsohn 1991; Komdeur
1996), and this and previous studies have not found any
effect of age on reproductive parameters in long-tailed tits
(Hatchwell et al. 2004). Long-tailed tits also experience few
constraints in mate acquisition because all birds in our population breed each year (MacColl and Hatchwell 2002), so
there is little incentive to help in order to gain access to
a mate. We can also dismiss current reproduction by helpers
as a direct benefit. Helping occurs only during the nestling
phase in long-tailed tits, so eggs are fertilized long before any
potential acts of helping, and males would not have to help in
order to gain extrapair paternity. Levels of extrapair paternity
in the long-tailed tit are low in any case (Hatchwell et al.
2002). The only direct fitness benefit that might be gained
is that helpers may gain information about beneficial nest
positions (Hatchwell et al. 1999). Our analysis suggests that
this does not translate into higher reproductive success by
helpers, and it is not clear why individuals would need to help
in order to gain this information (Hatchwell and Sharp 2006).
In conclusion, using data from a long-term study, we found
that long-tailed tit helpers had a higher probability of overwinter survival than nonhelpers. However, our findings suggest
that the relatively high survivorship of helpers is not a consequence of helping per se but instead is likely to be caused by
differences in the condition of birds that choose to become
helpers and those that do not. Therefore, we think that helping in the long-tailed tit is unlikely to confer a benefit of increased survival on helpers. Moreover, we found no significant
positive effect of helping on future reproductive success. This
conclusion contrasts with the strong evidence for kin-biased
helping (Russell and Hatchwell 2001; Nam et al. 2010)
and substantial indirect fitness benefits gained by helpers
(MacColl and Hatchwell 2004) in this species’ cooperative
breeding system. Our study also highlights the importance
of considering individual quality or condition where possible
when investigating variation in either the probability of helping or the amount of care that helpers provide.
FUNDING
J.M. was supported by a Natural Environment Research
Council grant (NE/E006655-1) to B.J.H.
We thank Andy Bamford, Martin Fowlie, Nicky Green, Jin-Won Lee,
Andrew MacColl, Andy McGowan, Ki-Baek Nam, Dan Richardson,
Douglas Ross, Andy Russell, Stuart Sharp, and Michelle Simeoni for
invaluable assistance with data collection and Sheffield City Council,
Yorkshire Water, and the Hallamshire Golf Club for permission to
work on their land. We thank A. McGowan and 3 anonymous referees
for constructive comments on the manuscript and D. Gillespie, S.
Votier, and M. Trinder for helpful statistical advice. Long-term data
were collected under grants from Natural Environment Research
Council, Nuffield Foundation, Association for the Study of Animal
Behaviour, and the University of Sheffield, for which we are most
grateful.
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