Mammalia (2006): 28 2006 by Walter de Gruyter Berlin New York. DOI 10.1515/MAMM.2006.

001
Article in press - uncorrected proof
2006/1
Comparative analysis of life-history traits in two species of
Calomys (Rodentia: Sigmodontinae) in captivity
Analyse comparative des traits dhistoire de vie de deux espe` ces de
Calomys (Rodentia: Sigmodontinae) en captivite
Luciana O. Araripe
1
, Paula Aprigliano
2
, Natalie
Olifiers
3,
*, Pavel Borodin
3,4
and Rui Cerqueira
2
1
Departamento de Gene tica e Evoluc a o, Instituto de
Biologia, Universidade Estadual de Campinas,
Unicamp, CP 6109, 13083-9790 Campinas, SP, Brazil
2
Laborato rio de Vertebrados, Departamento de
Ecologia, Universidade Federal do Rio de Janeiro,
21941-590, Rio de Janeiro, RJ, Brazil
3
Laborato rio de Biologia e Parasitologia de Mamferos
Silvestres Reservato rios, Departamento de Medicina
Tropical, Instituto Oswaldo Cruz, Av. Brasil 4365,
CP 926, 21040-360, Rio de Janeiro, RJ, Brazil,
e-mail: natolifiers@yahoo.com.br
4
Institute of Cytology and Genetics, Novosibirsk
630090, Russia
* Corresponding author
Abstract
We analyzed life-history traits (fertility, growth and rate of
postnatal development) in captive-bred colonies of two
closely related sympatric species: Calomys expulsus and
C. tener (Rodentia, Sigmodontinae). We found significant
differences between the species in growth rate and sev-
eral reproductive traits. C. tener had a smaller litter size
and litter mass, smaller proportion of litter mass to mater-
nal mass, lower growth rate and higher infant mortality.
We also found an apparent difference in correlation pat-
terns of life history parameters between the two species
of Calomys. The strong correlation between body size
and fecundity found in other studies of life history traits
and in selection experiments seems to be disrupted in
C. tener. We found a significant positive correlation
between maternal mass and litter size and mass only for
C. expulsus, which means that in C. tener the fertility of
females does not depend strongly on body mass. We
discuss inbreeding depression and stress reactions as
possible reasons for these results.
Keywords: Calomys; fertility; growth curve; litter size;
reproduction.
Re sume
Nous avons analyse les traits dhistoire de vie (fertilite ,
croissance et taux de de veloppement apre` s la naissance)
dans des colonies de deux espe` ces de rongeurs sym-
patriques e leve es en captivite : Calomys expulsus et C.
tener (Rodentia, Sigmodontinae). Nous avons trouve des
diffe rences significatives entre les espe` ces en ce qui
concerne le taux de croissance et divers traits reproduc-
tifs (nombre de petits, masse de la porte e, mortalite
infantile, etc.). C. tener a une porte e et un poids de cette
dernie` re plus petits et proportionnellement re duits par
rapport a` la masse de la me` re, un taux de croissance
plus petit et une plus grande mortalite infantile. Nous
avons aussi constate une apparente diffe rence dans les
patrons de corre lation des parame` tres dhistoire de vie
entre les deux espe` ces de Calomys. La corre lation forte
entre la taille du corps et la fe condite , qui est souvent
observe es dans les travaux concernant les traits dhis-
toire de vie et les expe riences de se lection, ne semble
pas e tre visible chez C. tener. La corre lation significative
entre le poids de la me` re dun co te et le nombre de petits
et la masse de la porte e dautre part nexiste que chez
C. expulsus, ce que veut dire que chez C. tener la fertilite
des femelles ne de pendrait pas de la masse du corps.
Lendogamie et la re ponse aux conditions de captivite
sont les possibles raisons dune telle diffe rence.
Mots cles: Calomys; courbes de croissance; fertilite ;
reproduction; taille de porte e.
Introduction
The life history of an animal species includes several fea-
tures related to reproduction and growth that are specific
to each taxon. Since these traits are fundamental com-
ponents of fitness, they are supposed to be strongly
influenced by natural selection (Gadgil and Bossert 1970,
Stearns 1992, Kawecki and Stearns 1993). The evolution
of life history may be constrained by developmental,
morphological and physiological variables. In addition, it
can be regarded as a result of selection for a set of co-
adapted characters determined by specific mortality
schedules. This may result in a common and rather con-
servative pattern of relationships between different life-
history traits (Harvey and Read 1988, Harvey et al. 1989,
Promislow and Harvey 1990, Kappeler 1996). However,
a variation in this pattern can be found between species
of the same genera and even within species. For these
reasons, a comparative analysis of life-history traits of
closely related species may provide an important insight
into the particular methods of adaptation of the species.
It is particularly interesting to compare species that live
in the same habitat and show different life strategies.
Studies on the life history of mammals are usually
based on field observations (Kravetz et al. 1981, Cutrera
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Figure 1 Locations of the occurrence of s Calomys expulsus
and d Calomys tener; sympatry between the species; hloca-
tion of Miranda. Data obtained from Bonvicino and Almeida
(2000) and from our database.
1989, Mills et al. 1992a,b). This approach is very effective
in describing a population or species in its original habitat
and is possibly useful in generating predictions. Labo-
ratory experiments provide the possibility of unraveling
the genetic and environmental components that might
account for any differences found (Stearns 1983, 1992,
Sebens 1987, West-Eberhard 1989). When representa-
tives of different populations or species are raised in the
same environment, it is possible to investigate differenc-
es in their bionomical responses to these conditions, and
build up an idea of their evolutionary divergence con-
cerning these traits (Boag and Boonstra 1988, Stamps
1993, Svensson 1997).
Another advantage of studying animals of different ori-
gins in captivity is the possibility of comparing their onto-
genetic trajectories using the real age of the individuals,
instead of any other trait correlated to age. Analysis of
complete ontogenetic paths may shed light on how dif-
ferences in growth patterns have evolved from differenc-
es in rates and the timing of growth and development
(Creighton and Strauss 1986, Fiorello and German 1997).
In this study we analyzed life-history traits (fertility,
growth and rate of postnatal development) in captive-
bred colonies of two related species: Calomys expulsus
and C. tener (Rodentia, Sigmodontinae). Both species
inhabit open vegetation of the Cerrado and Caatinga
biomes of Brazil. C. expulsus is distributed from Pernam-
buco to Minas Gerais, and C. tener from Bahia to Sa o
Paulo (Brazil). They are sympatric, at least in some parts
of Minas Gerais (Figure 1). Although C. expulsus was
considered a subspecies of C. callosus by Herskovitz
(1962) or a junior synonymous of C. callosus by Musser
and Carleton (1993), a recent study based on karyologic
and morphologic comparisons showed that both are val-
id species (Bonvicino and Almeida 2000). However, the
recent phylogenetic hypothesis proposed by Salazar-
Bravo et al. (2001) based on mitochondrial DNA does not
include C. expulsus. Bonvicino and Almeida (2000)
showed that this species and C. tener share the same
diploid number, although they are very different in size.
Material and methods
Breeding
Nine individuals of C. expulsus and 24 of C. tener were
used as founders of our captive breeding colony. Animals
were trapped in a rescue program during filling of the
reservoir of the Miranda hydroelectric station (208109S,
418449W; Minas Gerais State, Brazil; Figure 1, location of
Miranda) in August 1997. The colony was kept under
conventional conditions (temperature 22268C, humidity
70%, natural daylight) at the animal house of the Labo-
ratory of Vertebrates of the Federal University of Rio de
Janeiro. Animals were fed a standard diet composed of
fruits, roots, seeds and alfalfa.
All possible mating pairs were established among the
founders of each colony (4 females, 5 males in C. expul-
sus and 14 females, 10 males in C. tener). The breeding
program was scheduled to produce as many offspring as
possible and to avoid inbreeding. Breeding pairs were
kept together permanently. Males were replaced as soon
as pregnancy was detected. Thus, we were able to study
whether these species have post-partum estrus and to
take advantage of this to maximize the number and
genetic variability of litters produced by one female dur-
ing her reproductive life. After weaning (21 days), the off-
spring were separated by sex and placed in different
cages.
Data collection
On the day of birth, offspring were counted, weighed,
sexed and individually marked. The age at the appear-
ance of developmental traits (fur emergence, ears and
eyes opening, and incisor occlusion) was recorded for
each offspring. The age of vaginal opening in females
and of the appearance of scrotal testes in males was
registered and used as indicators of the age of puberty.
The age of first successful mating was recorded for
males and females. Gestation length was estimated as
the minimum interval between consecutive parturitions.
To detect the beginning of the reproductive phase,
recently weaned animals were mated to adults. All ani-
mals were weighed weekly, beginning from the day of
birth, to monitor their growth.
Statistical analysis
Frequency distributions of litter size at birth, age at
appearance of each developmental trait, and litter size at
weaning for both species were compared using the Kol-
mogorov-Smirnov test. The significance of deviations of
the sex ratio from 1:1 was tested by x
2
test corrected for
one degree of freedom using the Yates correction (Zar
1984). The weight of newborns was compared between
sexes and species using Students t-test. The ratio of
litter mass to maternal mass was compared between
species using Students t-test after arcsine-transforma-
tion. Postnatal mortality was estimated as the difference
between litter size at birth and at weaning for each spe-
cies. Spearman rank correlation coefficients between
parity, litter size, litter mass, mass of each young, aver-
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Table 1 Mean
"
SD (n) for fertility traits of C. expulsus and C. tener.
Trait C. expulsus C. tener Test
Litter size at birth 5.87
"
1.77 (38) 3.51
"
1.18 (45) KSs0.709**
Mass at birth, males, g 2.21
"
0.28 (82) 2.05
"
0.36 (44) ts2.561*
Mass at birth, females, g 2.07
"
0.34 (70) 1.95
"
0.34 (60) ts2.114*
Litter mass/maternal mass 0.37
"
0.09 (34) 0.28
"
0.11 (41) ts3.708**
Litter size at weaning 4.84
"
2.32 (18) 2.68
"
1.72 (40) KSs0.577**
*p-0.05.
**p-0.01.
age mass of neonates and maternal mass were
estimated.
Growth curves were adjusted for each individual older
than 150 days using the Gompertz sigmoid asymptotic
model (Winsor 1932, Zullinger et al. 1984, Begall 1997)
for weight data. The Gauss-Newton method and least-
square estimation were used for the fitting process:
-k(t-I)
-e
ysAe , (1)
where A is the asymptotic mass, k is the constant growth
rate, and I is the age at the first inflection point of the
growth curve, when the growth rate is maximum. These
parameters were estimated using the non-linear regres-
sion procedure of SYSTAT (Wilkinson 1990).
The three parameters of the model were compared
between sexes and species using two-way ANOVA. The
maximum growth rate and the age at the growth plateau
(scored as the age at which the rate decreased to 1% of
the maximum growth rate) were obtained from the Gom-
pertz derivative (Begall 1997, Fiorello and German 1997):
dy
-K(t-I)
-K(t-I) -e
sAke e . (2)
dt
The parameters were estimated using the same
numerical method as for Eq. (1).
Results
Reproduction
Over the experimental period, we obtained 38 litters with
223 offspring for C. expulsus and 45 litters with 158 off-
spring for C. tener. No sterile females and only one sterile
C. tener male were detected. At the beginning of our
study we observed that the females of C. tener (but not
of C. expulsus) attacked their male partners after giving
birth. To prevent this, we separated the C. tener couples
as soon as pregnancy was detected. This difference in
breeding technique made it difficult to compare breeding
efficiency between the species. However, the interval
between encounter of breeding partners and parturition
can be used as an indirect indicator of breeding efficien-
cy. This was significantly longer in C. tener (KS maximum
difference 0.295, p-0.05).
Females of C. expulsus showed post-partum estrus,
as 60% of effective matings occurred shortly after
females had given birth. We observed post-partum
estrus in all three cases when C. tener couples were
maintained throughout and after gestation.
Litter size at birth was significantly larger in C. expulsus
than in C. tener (Table 1). Sexual dimorphism in body
mass at birth was significant in C. expulsus (ts2.71,
p-0.001, but not in C. tener (ts1.53, p)0.05). The sex
ratio at birth did not differ from the expected 1:1 in either
species (C. expulsus x
2
s1.01, ps0.316; C. tener
x
2
s1.01, ps0.317). Newborn males and females of C.
expulsus were significantly bigger than those of C. tener
(Table 1). The ratio of litter mass to maternal mass on the
day of birth was significantly higher in C. expulsus (Table
1). Thus, C. expulsus females seem to have made rela-
tively higher investment into the total mass of their
embryos than C. tener. The maternal mass in C. expulsus
increased significantly with parity (ns21, Rs0.608,
p-0.01). However, in both species studied we found no
correlation between parity and litter size, average neo-
nate mass or proportion of males.
There was a significant positive correlation between
maternal mass on the date of birth and litter size, litter
total mass, and average young mass in C. expulsus. In
C. tener, these traits did not co-vary with maternal mass
(Table 2).
Postnatal mortality between the day of birth and wean-
ing (Table 1) was negligible in C. expulsus (KS maximum
difference 227, p)0.05), whereas C. tener displayed a
higher mortality rate (KS maximum difference 884.5,
p-0.05). The proportion of dead young did not correlate
with either litter size or litter mass in both species.
Development
The gestation period was similar in both species: the
minimum interval between successive births was
22 days. Most traits indicating pre-weaning development
appeared at the same age in both species (Table 3). Fur
emergence, ear and eye opening occurred somewhat
earlier in C. tener, but the difference was not significant.
In both species, the mode for the age of puberty was
approximately the same for males and females. However,
there was a significant difference in the distribution of
ages of puberty between the species (Table 3).
In a specific experiment, newly weaned animals were
mated to adults to estimate the minimum age for first
successful mating. In C. tener, this was 46 days in males
and 62 days in females, and in C. expulsus, it was
50 days in males and 40 days in females. Thus, the first
successful mating in both species occurred some days
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Table 2 Spearmans coefficients for correlations between life history traits in C. expulsus and C. tener.
C. expulsus C. tener
Lm Mm Lm Mm
Ls 0.90 (0.00) 0.61 (0.00) 0.93 (0.00) 0.13 (0.57)
Lm 1 0.77 (0.00) 1 0.27 (0.23)
A.m. neot 0.37 (0.10) 0.48 (0.03) 0.11 (0.63) 0.40 (0.07)
The probability of a random correlation is given in parentheses. Lm, litter mass; Mm, maternal mass; Ls, litter size; A.m. neot, average
mass of neonates.
Table 3 Age on emergence of developmental traits in C. expulsus and C. tener and comparison of the distributions.
Traits C. expulsus C. tener Comparison of the distributions
n Age (days) n Age (days) KS p
Range Mode Range Mode
Underfur, dorsal 15 No variation 0 23 No variation 0 - -
Underfur, ventral 21 04 2 20 04 2 0.089 1.000
Inferior incisors 18 47 6 28 311 6 0.165 0.908
Superior incisors 16 58 7 26 411 7 0.199 0.804
Fur, dorsal 16 26 5 33 26 3 0.397 0.062
Fur, ventral 12 47 5 21 46 5 0.238 0.743
Ear opening 21 37 7 28 38 5 0.290 0.219
Eye opening 14 69 8 26 59 7 0.203 0.782
Puberty, males 76 1648 22 57 1546 25 0.278 0.014
Puberty, females 45 2248 37 41 2450 36 0.299 0.036
Table 4 Mean
"
SD (n) for growth traits of males and females of C. expulsus and C. tener.
Trait C. expulsus C. tener
Males Females Males Females
Asymptotic mass, g (A) 39.0
"
7.7 (49) 39.1
"
8.2 (34) 19.6
"
4.9

(32) 24.5
"
7.7
,
* (40)
Growth rate (K) 0.035
"
0.011 (49) 0.028
"
0.007* (34) 0.035
"
0.016 (32) 0.034
"
0.016

(40)
Age at the inflexion point (I) 28.4
"
5.3 (49) 31.2
"
6.2* (34) 17.7
"
8.5

(32) 25.0
"
17.2
,
* (40)
Mass at the inflexion point, g 14.3
"
2.9 (49) 14.4
"
3.0 (34) 7.1
"
1.6

(31) 9.0
"
2.8
,
* (40)
Maximum rate of growth 0.485
"
0.131 (49) 0.391
"
0.096* (34) 0.244
"
0.089

(31) 0.270
"
0.094

(40)
Age of growth plateau, days 206.6
"
51.6 (49) 244.0
"
46.2* (34) 205.6
"
94.7 (31) 251.7
"
175.4 (40)
Mass at maturity, g 15.2
"
5.9 (49) 19.0
"
4.8* (32) 10.8
"
1.5

(32) 15.2
"
4.6
,
* (40)
Mass at weaning, g 10.0
"
2.8 (45) 10.2
"
3.3 (28) 8.2
"
1.2

(24) 9.7
"
1.9* (25)
Mass at birth/A 0.06
"
0.01 (46) 0.06
"
0.02 (33) 0.12
"
0.03

(24) 0.10
"
0.04

(30)
Mass at weaning/A 0.26
"
0.07 (45) 0.26
"
0.07 (28) 0.45
"
0.10

(24) 0.44
"
0.14

(25)
Mass at maturity/A 0.40
"
0.16 (49) 0.50
"
0.12* (32) 0.57
"
0.13

(32) 0.66
"
0.21

(37)

Significant difference within sex between species (p-0.05).

* Significant sex difference within species (p-0.05).
later than the appearance of anatomical indicators of
puberty.
Growth
Although males of C. expulsus were significantly heavier
than females at birth, there were no significant differenc-
es in asymptotic mass between the sexes (Table 4 and
Figure 2a). This could be due to the fact that the females
remained in the accelerated phase of growth for a longer
time, i.e., they had a greater (although not significantly)
I-parameter than males (Figure 2b). They also reached
the end of the growth period later (230 days) than males
(188 days). Thus, due to their lower growth rate, females
took more time to attain the same mass as males.
Males and females of C. tener did not differ signifi-
cantly either in body mass at birth or growth rate. How-
ever, the final mass in females was much greater than in
males (ts3.090, p-0.01). Males spent more time grow-
ing, but their period of accelerated growth was shorter.
Thus, the period of accelerated growth appears to be the
most critical parameter in determining the mass for this
species.
The interspecies difference in body mass was signifi-
cant at birth. During postnatal growth, this difference also
increased. Interestingly, this was not due to a difference
in general growth rate (K), which was approximately the
same in both species, but due to the time they spent in
the accelerated growth phase and the maximum growth
rate achieved (Figure 2b). These two parameters were
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Figure 2 (a) Growth curves for female (white) and male (black)
C. expulsus (squares) and C. tener (circles) fitted to the mean
values for individual parameters, calculated using the Gompertz
model. (b) Variation of the growth rates throughout ontogeny,
fitted by the Gompertz derivative.
Table 5 Average litter size in Sigmodontinae rodents.
Species Mean SD Source
Akodon cursor 4.2 1.6 Aulchenko et al. 2002
Bolomys lasiurus 5.0 1.4 Our unpublished data
C. callosus 5.5 Morrison et al. 1976
C. expulsus 5.9 1.8 Present study
C. laucha 5.3 Hodara et al. 1989
C. musculinus 5.47.6 Buzzio and Castro-Va zquez 2002
C. tener 3.6 1.2 Present study
Holochilus brasiliensis 3.1 Mello 1978
Holochilus sciureus 3.1 Twigg 1965
Nectomys squamipes 4.1 1.2 DAndrea et al. 1996
Oligoryzomys flavescens 5.2 0.3 Mills et al. 1992b
Oligoryzomys nigripes 4.8 1.5 Bonvicino et al. 2001
Rhipidomys mastacalis 3.7 1.7 Our unpublished data
significantly higher in C. expulsus the species with
greater final body mass. Another important point is that
the species differed in relative body mass of females on
the day of puberty: females of C. expulsus were signifi-
cantly heavier (Table 4). Differences between the species
in relative mass at birth, weaning and age of maturity
were mainly due to rapid and precocious growth of C.
tener.
Discussion
Our comparative study of life-history traits in two closely
related and sympatric species of Calomys revealed that
these species are similar in a set of traits that character-
ize their development. At the same time, they differ from
each other in litter size and body mass at birth, in growth
parameters, and in the way these traits are correlated to
each other.
It seems that the rate of development is an evolution-
arily conserved feature. For instance, gestation length,
i.e., the length of prenatal development, has been shown
to be well conserved within the genus Calomys (Mello
1978, de Villafane 1981, Hodara et al. 1989, Buzzio and
Castro-Va zquez 2002). External indicators of postnatal
development, such as ear and eye opening and fur emer-
gence, occurred somewhat earlier in C. tener, but there
was no significant difference in the frequency distribution
of ages at the appearance of these and other develop-
mental indicators. Representatives of both species
reached puberty at approximately the same age. This is
a surprising result considering the significant interspecies
differences in body mass and growth rate at the corre-
sponding periods of life. This suggests that postnatal
development follows a genetically stable timetable and
does not depend strongly on the growth rate in these
species. Data on C. musculinus, which is approximately
the same size as C. tener, show remarkably early matur-
ation (21 days) coincident with the weaning age (Mills et
al. 1992a, Buzzio and Castro-Va zquez 2002).
We found a notable difference between C. expulsus
and C. tener in the growth rate and several fecundity
traits (Table 1). Murid rodents have been considered as
opportunistic species because of their high reproductive
capability, which might have evolved as an adaptation to
high predator pressure occurring in cornfields and grass-
lands (Conaway 1971). Considering all these life-history
traits, C. tener seems to be a low-fitness species. Under
laboratory conditions, females of C. tener have smaller
litter size and litter mass, a lower litter mass/maternal
mass ratio, and higher infant mortality. Litter size, for
example, in C. tener is one of the smallest found among
Sigmodontinae species studied so far, and the smallest
within the genus Calomys (Table 5).
Another remarkable feature of C. tener is the drastic
disruption of the evolutionarily stable pattern of correla-
tion between fertility traits. There is much evidence of a
strong correlation between body size and fecundity from
studies of life-history traits (Millar 1981, Stearns 1983,
Harvey and Clutton-Brock 1985) and from selection
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experiments (Falconer 1989 and references therein). In C.
expulsus there was a significant positive correlation
between maternal mass and litter size and litter mass.
We did not find such a correlation for C. tener, which
means that female fertility does not depend strongly on
body mass in this species.
The process of adaptation and the necessity to maxi-
mize fitness leads to a strong interrelationship between
life-history traits (Millar 1981). One of the explanations for
these correlations is the energetic trade-off (Stearns
1992, Alexander 1999), i.e., an increase in one trait leads
to a decrease in others because of limitations in the
amount of energy available. In an evolutionary context,
these correlation complexes can be regarded as the
result of stabilizing selection, which leads to optimization
of ontogenetic homeostasis and consequently to the
masking of genetic variation of the traits involved in co-
adapted complexes (Schmalhausen 1949, Lerner 1954,
Mayr 1963).
Low fecundity and disruption of the evolutionarily sta-
ble correlation complex between fecundity traits in C.
tener could be an indication of inbreeding depression or
stress reactions of the captive breeding colony of this
species. Inbreeding may cause disruption of co-adaptive
gene complexes and a decrease in fertility (Mayr 1963).
Environmental stress is another factor that depresses fer-
tility (Lee and McDonald 1985). Although both species
were bred under the same laboratory conditions, their
response to these conditions might be different, due to
differences in behavior, physiology, territorial and nutri-
tional demands, etc. It is well known that some species
are very easy to breed in captivity, but others are not.
Thus, the low success showed by C. tener in breeding
could be an indication of a stress reaction this species
displays in captivity.
Acknowledgements
We thank Diego Astu a de Moraes, Francisca Almeida and Mar-
cus Vin cius Vieira for valuable comments on the manuscript.
Keeping and breeding all the specimens would not have been
possible without help from Nelio P. de Barros and the students
of the Laboratory of Vertebrates, UFRJ. This research was sup-
ported by grants and fellowships from the institutions CAPES,
CNPq, FAPERJ, FUJB, PROBIO/MMA and RFBR.
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