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RESEARCH PAPER

Sex-Biased Senescence in a Polygynous Bat SpeciesSabine Greiner*, Martina Nagy†, Frieder Mayer†, Mirjam Kn€ornschild‡, Heribert Hofer* &Christian C. Voigt*

* Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

† Museum f€ur Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Berlin, Germany

‡ Institute of Experimental Ecology, University of Ulm, Ulm, Germany

Correspondence

Sabine Greiner, Physikalisch-Technische

Bundesanstalt, Bundesallee 100, 38116

Braunschweig, Germany

E-mail: greiner@izw-berlin.de

Received: July 23, 2013

Initial acceptance: September 17, 2013

Final acceptance: November 10, 2013

(M. Herberstein)

doi: 10.1111/eth.12193

Keywords: individual fitness contribution,

reproduction, senescence, survival, trade-off,

tropical bat

Abstract

Bats live substantially longer than any other similar-sized mammal

despite high metabolic rates during flight. The underlying causes for the

longevity of bats and the question whether bats exhibit signs of senes-

cence – a progressive deterioration in performance – are still unclear.

Here, we describe rates of senescence in individual annual fitness, sur-

vival and reproduction using survival and recruitment data collected over

an 18-yr period from 77 males and 81 females in a wild population of Sac-

copteryx bilineata (greater sac-winged bat), a polygynous species inhabiting

colonies where female groups are defended each by a territorial male. In

individuals older than 4 yr of age, individual fitness contribution, sur-

vival and recruitment declined with increasing age in males but not in

females. Rates of senescence in annual individual fitness and in reproduc-

tion of males were at least an order of magnitude higher than those of

females. This finding might be explained by the ‘disposable soma theory’

that attributes senescence to an optimal allocation of resources to somatic

maintenance and competing traits such as reproduction. The rate of

senescence in the survival of males was also significant but of the same

order of magnitude as the (non-significant) rate of females. Unlike many

other polygynous mammals, greater sac-winged bats show little overt

male–male competition. As senescence in survival was only weak in

males, our results are consistent with the theories for polygynous mam-

mals, which view the trade-off between male investment in physical

traits for intense male–male competition against survival as a major

source of the decline of male survival with age. This is the first study to

demonstrate sex-specific senescence rates in a wild population of a small,

long-lived mammalian species.

Introduction

Senescence is the increase in the probability of death

and the decline in fitness caused by an accumulation

of physiological degradation with increasing age (Mo-

naghan et al. 2008). The previously widely held idea

that senescence is primarily a phenomenon of

humans (Hayflick 1995) and that animals usually die

before showing signs of senescence (Comfort 1979;

Williams 1992) has been replaced by the recent recog-

nition that senescence is probably widespread across

vertebrate taxa (Promislow 1991; Jones et al. 2008).

The long-standing belief that birds do not age (Lack

1954; Williams 1992) was disproved by newer studies

that revealed senescence to be present in avian species

as well (Holmes & Austad 1995; Jones et al. 2008),

although in general it seems that birds senesce at

lower rates than mammals (Bennet & Owens 2002).

As senescence impairs rather than improves an

individual’s fitness, there should be strong selection

against it. Three major theories explain the evolution

and persistence of senescence. The ‘mutation accu-

mulation theory’ predicts that deleterious mutations

may accumulate within the genome when the force

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH 1

Ethology

of natural selection to eliminate accumulations of

germ-line mutations with late-acting deleterious

effects is too weak because only few individuals of

advanced age are still alive to experience the deleteri-

ous effects of such mutations (Medawar 1952). The

‘antagonistic pleiotropy theory’ is an extension of this

theory and attributes senescence to a decline in the

strength of natural selection with increasing age when

mutations have beneficial effects early in life but may

be deleterious later (Williams 1957; Hamilton 1966).

A third theory, the ‘disposable soma theory’, is based

on trade-offs in optimal resource allocation between

somatic maintenance and other traits (Kirkwood

1977; Kirkwood & Austad 2000). A decline in func-

tion would then result from the age-dependent accu-

mulation of unrepaired metabolic damage and the

investment into costly repair mechanisms would

reduce resource allocation to other traits such as

reproduction (Kirkwood 2005).

Within mammals, bats substantially exceed the lon-

gevity predicted on the basis of their body size (Wil-

kinson & South 2002), that is, they live longer than

other similar-sized mammals (Austad & Fischer 1991;

reviewed by Brunet-Rossinni & Austad 2004). They

share many life history traits with large, long-lived

mammals, such as slow growth rates, long gestation

periods and the production of few and relatively large

offspring. Based on these traits, they lie at the slow

end of the fast–slow life history continuum (Barclay &

Harder 2003). The exceptional longevity of bats is

unusual as they exhibit high mass-specific metabolic

rates, which are thought to reduce longevity accord-

ing to the ‘rate of living’ theory (Pearl 1928; Calder

1985). High metabolic rates are supposed to result in

an accumulation of toxic by-products and an increase

in oxidative damage with age (Sohal & Weindruch

1996). It was therefore argued that the exceptional

longevity of bats is linked to their reduced energy

expenditure during hibernation (Bourliere 1958;

Sacher 1977) and an improved ability to cope with

oxidative stress compared with other taxa (Salmon

et al. 2009). On the other hand, metabolic rates of

bats may rise up to 20-fold during flight (Racey &

Speakman 1987), providing plenty of opportunity to

accumulate toxic by-products, and tropical species do

not enjoy the benefits of hibernation, yet are long-

lived as well (Austad & Fischer 1991). Because the

ability to fly substantially reduces the risk of being

killed by terrestrial predators, low predation pressure

could reduce selection for rapid maturity and repro-

duction and promote the evolution of delayed senes-

cence in bats (see review by Munshi-South &

Wilkinson 2010).

Studies of senescence in wild animal populations

are rare, particularly in small and cryptic animals

such as bats, and more longitudinal studies are

required to improve our understanding of the under-

lying causes of senescence (Nussey et al. 2008). Here,

we present the first longitudinal, sex-specific analysis

of the survival and reproductive performance in a

small free-ranging bat, the greater sac-winged bat

S. bilineata Temminck 1838 (Emballonuridae) from

the data collected in Central America over a period

of 18 yr. We asked whether there is evidence of

senescence in these bats by monitoring the annual

survival and reproductive outcome and by calculat-

ing annual fitness contribution of each individual

(Coulson et al. 2006; Jones et al. 2008). If there is

senescence in small bats, we would expect a decrease

in reproductive performance or survival with increas-

ing age, and if the ageing process is sex-biased, we

would expect sex-specific differences in the rates of

senescence measured as reproductive fitness and

survival.

Methods

Study Species

Saccopteryx bilineata, a widespread 8-g bat from low-

land Neotropical regions, has a harem polygynous

social system. Colonies can contain up to 50 individu-

als and are subdivided into smaller social units, the

so-called harems (Bradbury & Emmons 1974). Harem

territories consist on average of two to four females

defended by an adult territorial male. These societies

remain stable throughout the whole year and terri-

tory boundaries over several years. Male S. bilineata

either defend a territory with females (harem males)

or live, without females, in the periphery of harems

(non-harem males). All males, either harem males or

non-harem males, are able to reproduce successfully

(Bradbury & Emmons 1974; Heckel & von Helversen

2002). Harem males only sire 30% of the juveniles in

their harem, but their reproductive output is still

higher than that of non-harem males (Heckel & von

Helversen 2002). Individuals sexually mature at the

age of 6 mo (Tannenbaum 1975), and most males

take over harems at an average age of 2 yr (Voigt &

Streich 2003). The mating season is restricted to the

period from the end of November to the end of

December (Greiner et al. 2011). Saccopteryx bilineata is

characterised by male-biased philopatry and female-

biased dispersal (Bradbury & Emmons 1974; Nagy

et al. 2007), and individuals reach an average age of

7 yr (Tannenbaum 1975). In our long-term database,

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH2

Sex-Biased Senescence S. Greiner et al.

the maximum-recorded longevity for male S. bilineata

is 10 yr and for females 11 yr.

Census

Our main study colony was situated in an abandoned

building close to La Selva Biological Station (10°26′N;83°59′W) which lies within the Caribbean lowlands of

Costa Rica. In addition, smaller colonies in the same

study area were sampled. The colonies were surveyed

from approximately June to August and from Novem-

ber to January each year between 1995 and 2012. All

bats in the colonies were marked with coloured and

numbered plastic bands (AC Hughes Ltd, Sussex, UK,

size: XCL). Each year, we used a different colour for

the main band imprinted with individual numbers

and used, in addition, a second band containing dif-

ferent colours. With these colour combinations, we

were able to identify individuals from up to 3 m.

Females were marked on the left and males on the

right forearm. Since all offspring born in the colonies

were marked within the first weeks after birth, we

were able to include the specific age of individuals in

our analysis. Immigration into colonies usually hap-

pened at the age of 5–8 mo, when the early age of

individuals was detectable based on the appearance of

the epiphyseal gaps. In addition, females of the juve-

nile cohort were detectable during their first mating

season by the size and shape of their nipples. Thus,

exact ages could also be determined for colony immi-

grants. During capture, tissue samples were taken

from the wing membrane for genetic paternity analy-

ses. Detection probability in S. bilineata is very high:

during the mating season, harem males and non-

harem males were almost always encountered at their

harem territory. For harem males, a detection proba-

bility of 98% and for non-harem males, a detection

probability of 85% were reported (Voigt et al. 2007).

Females were similarly loyal to their roosting territory

and showed a probability of being present of 91% at a

given day during the mating season (Voigt & Schwar-

zenberger 2008).

Determination of Individual Fitness Contribution and

Rates of Senescence

Data on annual survival and number of offspring were

used from individuals of known age to calculate the

individual fitness contribution (IFC) for a given age

(Coulson et al. 2006; Jones et al. 2008). IFC is defined

as the sum of annual survival and recruitment. Sur-

vival for a specific age class was 0 if the individual died

between time t and t + 1, and 1 if it had survived to

time t + 1. Census time t for survival was 31 Decem-

ber, which roughly coincides with the end of the

mating season. Recruitment was defined as the num-

ber of offspring produced between the censuses at

times t and t + 1, which were recruited into the adult

population. Number of offspring was assessed in

females by genetic maternity analysis and by observ-

ing whether or not the offspring was suckled. In

males, number of offspring was assessed by genetic

paternity analysis of the newborn in the colonies. We

used 11 highly polymorphic microsatellite markers

(Heckel et al. 2000) to genotype 1036 individuals

caught between 1994 and 2011 at La Selva Biological

Station. Of these bats, 377 were juveniles born in our

study colonies. All individuals were genotyped at least

at 10 loci, and genotypes were 99.2% complete.

Paternity analysis followed the protocol described in

detail by Heckel & von Helversen (2003) and Nagy

et al. (2012) using CERVUS 2.0 (Marshall et al. 1998)

and CERVUS 3.0 (Kalinowski et al. 2007) as described

in Nagy et al. (2012). Maternity was determined by

nursing observations in the field and affirmed by

genetic analyses. All adult males captured in La Selva

were treated as putative fathers unless their death was

known. We simulated 100 000 offspring with an error

rate of 0.01 (as estimated from known mother–off-spring pairs) and a proportion of 90% sampled candi-

date males with CERVUS 3.0 (Kalinowski et al. 2007;

Nagy et al. 2012). Simulations were performed for

two confidence levels (80% and 95%). The exclusion

probability for paternity averaged 99.99% (Heckel &

von Helversen 2002; Nagy et al. 2012). We assigned

the most likely males as fathers and allowed for one

mismatch per parent–offspring pair.

Means of IFC, survival and recruitment were plot-

ted against age for each year of age. Owing to the ani-

mal’s fidelity to the roosting site, detection probability

was high, although for some individuals data on

recruitment or on survival were not available for all

age classes. In this case, the estimates for recruitment

and individual fitness would be minimum estimates,

that is, be right-censored data. For age classes that

contained right-censored data, the mean for this par-

ticular age class was calculated with the help of the

Kaplan–Meier estimator for the survivorship function

within a survival analysis (Parmar & Machin 1995).

In total, data were available from 77 males and 81

females (in total 158 individuals), with sample sizes

varying among age classes. We calculated linear and

quadratic polynomial regressional models using the

least-squares method for each parameter and for the

three data sets of males, females and all individuals

(combined data from males and females) separately.

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH 3

S. Greiner et al. Sex-Biased Senescence

All models were weighted by total sample size, that is,

each age class mean was weighted by the percentage

of data points the age class contributed to the entire

data set on which the means were based on. We then

tested whether regression coefficients (slopes) deviated

significantly from zero. We also compared linear and

quadratic polynomial models to assess which model

better explained the relationship between fitness

parameters (recruitment, survival and IFC) and age, by

looking at the significance of the regression coefficients

and the Akaike information criterion (AIC) score

(Burnham & Anderson 2002) for each model.

If a linear model was the better option to explain

the development of a fitness parameter with age, rates

of senescence were determined by ordinary least-

squares regression using the means for all ages. If a

quadratic polynomial was the better choice, we

selected the age class with the peak value for a partic-

ular fitness parameter as the minimum age for which

the rate of senescence was calculated by ordinary

least-squares regression (Jones et al. 2008). Data were

log-transformed if criteria for parametric testing were

not met. For log transformation, we replaced values of

0 by 0.1. All models were again weighted by total

sample size, that is, each age class mean was weighted

by the percentage of data points the age class contrib-

uted to the entire data set on which the means were

based on. Negative slopes of the linear regression that

differed significantly from zero were defined as a sig-

nificant rate of senescence. All data were analysed

using SYSTAT 13 (Systat Software Inc., Richmond,

USA).

Results

The Development of Fitness Measures with Age

The development of individual fitness parameters

with age differed between males and females; the data

set for all individuals (males and females combined)

mirrored the pattern of males. For males and for all

individuals, both reproduction and total annual IFC

first improved with age before both declined with

higher age, as reflected by a quadratic polynomial

equation. In males, only few individuals reproduced

successfully at the age of one. Recruitment then

increased and was highest at the age of four; after-

wards recruitment declined with increasing age

(Fig. 1e). Correspondingly, males and all individuals

reached a peak in IFC at the age of four, whereas no

peak in any of the three parameters was detectable in

females (Fig. 1). In males and all individuals, survival

declined in a linear fashion with age (Table 1).

Most females reproduced successfully already at the

age of one and reproductive success continued on the

same level until death (Fig. 1f). In females, no fitness

parameter significantly changed with age (Fig. 1,

Table 1).

Senescence Rates in IFC, Recruitment and Survival

Rates of senescence were reflected in the slopes of

least-square linear regressions calculated for the rela-

tionship between IFC, survival or recruitment and age

(Table 2). As the recruitment and IFC reached a peak

at the age of 4 yr in males and all individuals, we cal-

culated least-square linear regressions only for indi-

viduals older than 3 yr of age. For all other data sets,

we calculated least-square linear regression over all

age classes. For all individuals, there were significant

rates of senescence in reproduction (slope = �0.223,

p = 0.006, Table 2), IFC (slope = �0.177, p = 0.021,

Table 2) and a significant but weak senescence in

survival (slope = �0.041, p = 0.036, Table 2). The

significant senescence rates for reproduction and IFC

observed here were probably a consequence of the

senescence rates found in males for reproduction

(slope = �0.36, p = 0.009; Table 2; Fig. 1e) and IFC

(slope = �0.423, p = 0.036, Table 2; Fig. 1a). Senes-

cence in survival was also significant but weak

(slope = �0.063, p = 0.025, Table 2; Fig. 1c) when

including all age classes in the analysis. In females,

there were no significant rates of senescence at all.

The numerical value for the decline in IFC was more

than 15 times lower in females (slope = �0.026,

p = 0.121, Table 2; Fig. 1b) than in males. In females,

senescence in reproduction was also not detectable

(slope = �0.001, p = 0.957, Table 2; Fig. 1f) and

senescence rate for survival was also not significant

(slope = �0.024, p = 0.178, Table 2; Fig. 1d).

Discussion

Our data on survival and reproduction collected for

S. bilineata over an 18-yr period demonstrated strongly

sex-dependent senescence rates in a free-ranging tropi-

cal bat population. The annual IFC and the reproduc-

tive performance significantly declined with age only

in males but not in females. Senescence in survival

was weak in males but still significant, and no evidence

for senescence in survival was found in females. Sex-

specific senescence rates have been previously reported

in mammals (Mason et al. 2011; Tafani et al. 2013),

but – to the best of our knowledge – our analysis

demonstrates for the first time a sex-biased difference

in senescence in a small-sized, free-ranging mammal.

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH4

Sex-Biased Senescence S. Greiner et al.

(a) (b)

(c) (d)

(e) (f)

Fig. 1: Relationship between mean individual fitness contribution (IFC) (a, b), survival (c, d) and reproductive success expressed as recruitment (e, f)

and age in male (left) and female (right) greater sac-winged bats Saccopteryx bilineata. Dots represent the means and bars represent the lower and

upper confidence intervals (95%). Confidence intervals are not given for sample sizes = 1 and also not for survival (c, d) because these data were of a

binary nature.

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH 5

S. Greiner et al. Sex-Biased Senescence

In general, reproductive senescence seems to be

more common in birds and large mammals than in

small mammals (Jones et al. 2008). However, the

meta-analysis of Jones et al. (2008) did not include

bats, a mammalian group that shares many life history

traits with large mammals. Our data on S. bilineata

show that males experience an increase in reproduc-

tive success until they reach the age of four. At that

time, most adult males have already taken over a

harem territory (Voigt & Streich 2003). This increase

is then followed by a decline in reproductive success

with advancing age. Such an effect was not detectable

in females, which produced offspring for the first time

after arriving in the colony at the age of one and then

continued to produce a single offspring each year

until they died (Voigt et al. 2008). Even though

reproductive performance decreased in male S. biline-

ata, neither sex showed a post-reproductive life period

that has only been observed in captive mammals and

not in birds (Ricklefs et al. 2003).

A reduction in reproductive success at older ages in

males has in general been attributed to an intense

intra-sexual competition among polygynous males

and the costs of enhancing competitive success (Wil-

liams 1957; Stearns 1992; Clutton-Brock & Isvaran

2007). A higher investment of males into competition

for mates possibly reduces the ability to invest in sub-

sequent years (Clutton-Brock 1984; Preston et al.

2011). Indeed, a decline in age-specific reproductive

success is more likely in males than in females of

polygynous species, whereas in monogamous species,

no difference or only slight sex-specific differences in

reproductive success have been detected (Clutton-

Brock & Isvaran 2007). These generalisations are

mostly based on species where male–male competi-

tion for mates involves physical conflict and where

morphological parameters, for example, body size, are

essential for male mating success. In this respect,

greater sac-winged bats are unusual in that (1) males

rarely fight over females using physical combat but

instead queue for access to harems (Voigt & Streich

2003); (2) male body size is inversely related to repro-

ductive success (Voigt et al. 2005) and (3) males

attempt to attract females with an elaborate cocktail

of chemical substances, mixed and stored daily in a

sac-like organ located in their front wing membrane

and presented to females during complex and stereo-

typic hovering flights (Voigt & von Helversen 1999). If

there is an age-related element in male mate competi-

tion, it is therefore most likely to be related to the pro-

duction and secretion of stimulating substances or the

endurance required for the energetically costly daily

Table 1: Comparison of quadratic and linear curve fits for individual fitness contribution (IFC), reproductive success (= recruitment = RECR) and sur-

vival (SURV) for all individuals (males and females combined), males only and females only. Significant regression coefficients are highlighted by bold

letters. Quadratic polynomials were better at describing the data for IFC, RECR and SURV in all individuals, and for IFC and RECR in males. Linear mod-

els were better at describing the data for SURV in males and for all three parameters in females. We used the corrected Akaike information criterion

(AICc) score

Group All Males Females

Parameter (y) IFC RECR SURV IFC RECR SURV IFC RECR SURV

Linear model: y = Constant + b1 * (age��x )

R2 0.150 0.019 0.406 0.416 0.283 0.484 0.245 0.001 0.192

Constant 1.857 1.509 0.969 1.661 0.919 0.966 1.947 0.938 0.981

Slope 0.073 0.024 �0.041 0.162 0.214 �0.063 �0.026 �0.001 �0.024

df 1,9 1,9 1,9 1,8 1,8 1,8 1,9 1,9 1,9

F 1.59 0.18 6.15 1.67 3.16 7.50 2.93 0.01 2.14

p 0.239 0.683 0.035 0.232 0.114 0.025 0.121 0.957 0.178

AIC(c) �11.08 �11.70 �37.06 5.98 4.31 �27.22 �39.66 �51.74 �36.86

Quadratic model: y = Constant + b1 * (age��x ) + b2 * (age��x)2

R2 0.734 0.622 0.578 0.899 0.855 0.567 0.303 0.017 0.374

Constant 2.403 1.731 0.690 2.972 2.347 0.581 1.779 0.938 0.807

b1 Slope – linear �0.127 �0.162 �0.006 �0.212 �0.159 �0.036 �0.009 �0.005 0.004

p 0.062 0.036 0.798 0.020 0.126 0.298 0.724 0.758 0.858

b2 Slope – quadratic �0.0517 �0.0473 0.0097 �0.1241 0.1135 0.0098 0.0044 �0.0011 0.0082

p 0.0030 0.0073 0.1087 0.0002 0.0012 0.285 0.441 0.725 0.166

df 1,9 1,9 1,9 1,8 1,8 1,8 1,9 1,9 1,9

F 11.03 6.57 5.48 31.06 20.63 4.58 1.74 0.07 2.39

p 0.0050 0.0205 0.0317 0.0003 0.0012 0.053 0.237 0.935 0.154

AIC(c) �18.61 �16.94 �35.58 �9.02 �5.67 �22.97 �35.30 �46.68 �34.42

�x 6.0 6.0 6.0 5.5 5.5 5.5 6.0 6.0 6.0

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH6

Sex-Biased Senescence S. Greiner et al.

hovering flights. Reproductive senescence in males

may also be caused by straightforward female mate

choice if, all else being equal, females favour younger

males. We do not (yet) have evidence to either refute

or confirm this idea.

In contrast to the highly significant reproductive

senescence in males, our data did not indicate a strong

rate of senescence in survival in males older than 3 yr

of age and no survival senescence in female S. bilineat-

a. Across polygynous vertebrates, survival is often

reduced in males (Stearns 1992; Clutton-Brock & Isv-

aran 2007). This is usually explained with reference

to intense male–male competition over mates, and

the idea that the ability of individuals to compete suc-

cessfully is traded against their survival since most

behavioural traits that enhance reproductive success

are energetically costly or risky (Trivers 1972). If such

trade-offs are particularly pronounced in polygynous

males with intense physical combat or where larger

body size is an advantage, then male greater sac-

winged bats should show little difference in mortality

from females, which is what our data suggest. In this

sense, our results are consistent with the idea that the

trade-off in investment in male–male competition

against survival should be more pronounced in spe-

cies with intense and physical male–male competi-

tion. However, our sample sizes in older age classes

were low, and therefore, our interpretation on sur-

vival senescence in S. bilineata has to be treated with

caution.

We currently do not know the sources of mortality

in S. bilineata. Also, we do not know whether a slow

deterioration of physiological functions leads to death

or whether the probability of a sudden death

increases, while overall physiological parameters do

not change or change only slightly. Conceivably, flap-

ping flight, the prerequisite to foraging and many

other life-supporting activities in greater sac-winged

bats, and bats in general, may require a high level of

physiological performance that does not allow any

deterioration to take place without catastrophic con-

sequences for an individual’s survival. This has also

been suggested for birds that maintain high levels of

physiological condition and performance until death

(Ricklefs 2008). We therefore expect both males and

females of S. bilineata to maintain relatively high lev-

els of investment into maintenance until death. How

does this relate to investment in reproduction? Our

major finding that only males exhibit reproductive

senescence, whereas females continue to reproduce

on the same level until death may be explained by

sex-specific differences in metabolic resource alloca-

tion with age. If males of S. bilineata invest more into

somatic maintenance and less into reproduction with

older age, then senescence in reproductive perfor-

mance but not in survival would be the consequence.

However, our data indicate also a survival senescence

in males and we cannot completely rule out a survival

senescence in females due to the low sample sizes in

older age classes. Hence, although our data give a

valuable insight into the senescence pattern of a small

tropical mammal, it might be too early to draw firm

inferences about the underlying mechanisms.

In general, our study is consistent with the predic-

tions of the ‘disposable soma theory’ (Kirkwood 1977;

Kirkwood & Austad 2000) that attributes senescence

to an optimal resource allocation to either somatic

maintenance or competing traits such as reproduc-

tion.

The long lifespan of bats might also be explained by

this theory, as species exposed to a low extrinsic mor-

tality, such as bats with their ability to fly, are able to

invest resources into growth and somatic mainte-

nance rather than into early reproduction (Munshi-

South & Wilkinson 2010), allowing the evolution of

retarded ageing.

Table 2: Regression coefficients (slopes) as estimates of the annual rate

of senescence in individual fitness contribution (IFC), reproductive suc-

cess (= recruitment = RECR) and survival (SURV) for female and male

greater sac-winged bats Saccopteryx bilineata. Rates of senescence,

that is, slopes, which deviated significantly from zero, are highlighted in

bold

Parameters IFC RECR SURV

All

R2 0.615 0.745 0.404a

Slope �0.177 �0.223 �0.041

df 1,6 1,6 1,9

F 9.60 17.55 6.10a

p 0.021 0.006 0.036a

Age classes >3 yr >3 yr All

Males

R2 0.620a 0.774 0.484

Slope �0.423 �0.360 �0.063

df 1,5 1,5 1,8

F 8.15a 17.13 7.50

p 0.036 0.009 0.025

Age classes >3 yr >3 yr All

Females

R2 0.245 0.0003b 0.192

Slope �0.026 �0.001b �0.024

df 1,9 1,9 1,9

F 2.93 0.003b 2.14

p 0.121 0.957b 0.178

Age classes All All All

aLog-transformed data.bData could not be transformed.

Ethology 119 (2013) 1–9 © 2013 Blackwell Verlag GmbH 7

S. Greiner et al. Sex-Biased Senescence

Acknowledgements

The authors thank all colleagues who contributed to

data collection. The Organization for Tropical Studies

(OTS) and La Selva Biological Station are acknowl-

edged for providing the necessary infrastructure to

conduct our fieldwork in Costa Rica. We are thankful

to Dan Nussey and one anonymous reviewer for valu-

able comments that helped improve the manuscript.

Animal treatment followed the Guide for the Care

and Use of Laboratory Animals of the National Insti-

tutes of Health. The use of animals complied with the

current laws of the country and was reviewed and

approved by the Animal Care Review Committee of

SINAC, the Sistema Nacional de Areas de Conservac-

i�on in San Jose, Costa Rica and the Ministerio del

Ambiente y Energia, Costa Rica (permit no.: 272-

2003-OFAU, 135-2004-OFAU, 022-2005-OFAU, 108-

2006-SINAC, 147-2007-SINAC, 183-2008-SINAC).

Financial support was provided by the Deutsche Fors-

chungsgemeinschaft (Vo 890), the DAAD, the Ilse and

Dr. Alexander Mayer Stiftung, the German Merit

Foundation and the Leibniz Institute for Zoo and

Wildlife Research, Berlin.

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