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Mammalian Biology xxx (2013) xxx–xxx

Contents lists available at SciVerse ScienceDirect

Mammalian Biology
journal homepage: www.elsevier.com/locate/mambio

Original Investigation

Life history of a neotropical marsupial: Evaluating potential contributions of

survival and reproduction to population growth rate
Mariana Silva Ferreira a,c,∗ , Maja Kajin a,c,d , Marcus Vinícius Vieira a,c , Priscilla Lóra Zangrandi a ,
Rui Cerqueira a,c , Rosana Gentile b
a
Laboratório de Vertebrados, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
b
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, RJ, Brazil
c
Departamento de Ecologia, Programa de Pós-Graduação em Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
d
Departamento de Ecologia, Programa de Pós-Graduação em Ecologia e Evolução, Instituto de Biologia Roberto Alcantara Gomes – IBRAG, Universidade do Estado do Rio de Janeiro,
Rio de Janeiro, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: The relative effect of survival and reproductive rates to population growth rate is expected to be similar
Received 28 August 2012 across species with similar life-histories. We employed a matrix population model and sensitivity and
Accepted 15 March 2013 elasticity analysis to assess the absolute and relative importance of age-specific survival and fertility
Available online xxx
to population growth rate of Didelphis aurita (Didelphimorphia, Didelphidae) in a rural area of Rio de
Janeiro, southeastern Brazil. The results were compared to expectations for mammals that mature early
Keywords:
and have short generation time, such as D. aurita. Prospective analysis showed that changes in pouch
Didelphidae
young and juveniles survival would have large effects on population growth rate, relative to other vital
Elasticity analysis
Fertility
rates, being the most critical time periods in the life cycle of D. aurita, whereas the effect of fertilities
Mammal were always low. These findings do not fit to the observed pattern in mammals that mature early, where
Matrix population model reproductive parameters have the largest relative influence on population growth rate. Although repro-
ductive rates were characterized by a relatively small influence on population growth rate, they are still
relevant because of their high variability and response to potential environmental disturbances. The first
application of matrix population models to a neotropical rainforest marsupial provides information on
marsupial demography and life-history strategy, increasing comprehension of this unknown group.
© 2013 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.

Introduction mammals, an increase in fertility should have a minor effect (Crooks

One of the central issues in life-history theory is how life his-
tory traits vary among individuals, and how this variation is related
to environmental conditions and fitness (Stearns 1992; Caswell
2001). A range of life-history strategies can be identified from the
interaction between vital rates, such as age-specific survival and
reproduction (Stearns 1992). The effect of changes in a vital rate
on population growth rate () should be dependent on the life-
history strategy of the population under study (Heppell et al. 2000;
Sæther and Bakke 2000; Oli and Dobson 2003; Stahl and Oli 2006).
An increase in fertility should have a larger effect on  in animals
that mature early, produce large litters and have short generation
time (Dobson and Oli 2001). On the other hand, in late maturing
∗ Corresponding author at: Laboratório de Vertebrados, Departamento de Ecolo-
gia, Universidade Federal do Rio de Janeiro, CP 68020, Ilha do Fundão, Rio de Janeiro,
RJ, CEP 21941-901, Brazil. Tel.: +55 21 2562 6314; fax: +55 21 2562 6313.
E-mail address: msferreira84@gmail.com (M.S. Ferreira).
et al. 1998; Corti et al. 2010).
Several authors have investigated the relative importance of
vital rates on  (e.g., Cole 1954; Stearns 1992), with more recent
studies using matrix population models (e.g., Heppell et al. 2000;
Oli and Dobson 2003; Stahl and Oli 2006). Prospective perturbation
analysis of matrix models quantifies the potential effect of small
changes in a vital rate on , either in absolute (sensitivity) or rela-
tive (elasticity) units, revealing the most critical time period in the
species’ life cycle (Caswell 2001). Sensitivity analysis is the appro-
priate tool to quantify the importance of vital rates for evolutionary
questions such as intensity and direction of selection, but it is not
appropriate to compare sensitivities of vital rates scaled differently
(de Kroon et al. 1986). Elasticity analysis, on the other hand, quan-
tifies the proportional change in  resulting from an infinitesimal
proportional change in a vital rate (de Kroon et al. 1986), hence
facilitating comparisons among them. In a study with 50 popula-
tions Heppell et al. (2000) concluded that  is influenced mainly
by fertility in mammals that mature early and have high reproduc-
tive rates (high elasticities for fertility and low elasticities for adult
survival), whereas adult survival is more determinant in mammals

1616-5047/$ – see front matter © 2013 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.mambio.2013.03.002

Please cite this article in press as: Ferreira, M.S., et al., Life history of a neotropical marsupial: Evaluating potential contributions of survival and
reproduction to population growth rate. Mammal. Biol. (2013), http://dx.doi.org/10.1016/j.mambio.2013.03.002
 ARTICLE IN PRESS
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that mature late and have low reproductive rates. This pattern was
further supported by Oli and Dobson (2003), compiling 142 stud-
ies of mammal populations. In addition, these authors found that
age at maturity was also important to  in populations with early
maturity and high reproductive rates, whereas juvenile and adult
survival had the largest relative influence on  in populations with
late maturity and low reproductive rates. Therefore, the relative
effect of vital rates to  is expected to be similar across species
with similar life-histories (Heppell et al. 2000; Stahl and Oli 2006).
The search for patterns on mammalian life histories is mostly
based on eutherian mammals (Promislow and Harvey 1990;
Heppell et al. 2000; Oli and Dobson 2003). Nonetheless, marsupials
show a great diversity of life history strategies (Dickman and Vieira
2006), and a “slow-fast continuum” in life history traits was also
observed in marsupials even after the effect of body size and phy-
logeny was controlled (Fisher et al. 2001). Didelphid marsupials, as
well as dasyurids, are positioned in the “fast” end of this continuum
compared to other marsupials because of their short life-spans,
large litter sizes and energy-rich diets (Fisher et al. 2001). How-
ever, demographic analysis and the potential effect of vital rates
on  for species at the fast end of the continuum are necessary to
determine if fertility has a larger effect on  indeed.
We analyzed the relative importance of vital rates on  in a
wild population of the neotropical marsupial Didelphis aurita Wied-
Neuwied, 1826 (Didelphimorphia, Didelphidae) using sensitivity
and elasticity analyses to assess how changes in reproductive and
age-specific survival rates would influence population growth rate
(Caswell 2001). Neotropical marsupials belong mostly to the order
Didelphimorphia (Kirsh et al. 1997), with more than 96 species
described, most of them rainforest species (Gardner 2008). How-
ever, sensitivity and elasticity analyses have not yet been employed
for a neotropical rainforest marsupial. We aimed to (1) determine
the importance of survival and fertility rates to  through elasticity
and sensitivity analysis, and (2) determine if this marsupial follows
the general pattern of early maturing mammals: high fertility and
low survival elasticities.
Material and methods
Study species
Didelphis aurita is a common and abundant marsupial in the
Coastal Atlantic Forest of Brazil (Fonseca and Robinson 1990;
D’Andrea et al. 1999; Gentile et al. 2000). Its distribution ranges
from northeastern Brazil, to southeastern Paraguay and northeast-
ern Argentina (Gardner 2008). This solitary opossum of nocturnal
habits weights an average of 1.5 kg, and it is known as a gen-
eralist species in its food habits (Freitas et al. 1997; Astúa de
Moraes et al. 2003), and habitat preferences (Fonseca and Robinson
1990; Freitas et al. 1997; Moura et al. 2005). Young are weaned
within approximately 100 days after birth and reach puberty within
approximately 170 days of age (Kajin et al. 2008). In Didelphis,
pregnancy time varies between 13 and 15 days (Reynolds 1952;
Tyndale-Biscoe and Mackenzie 1976), and two estrous usually
occur during a breeding season (Rademaker and Cerqueira 2006).
Frequently, D. aurita is the dominant species in small mammal
assemblages (Fonseca and Robinson 1990; Gentile et al. 2004;
Macedo et al. 2007; Bonecker et al. 2009), and can act as a com-
petitor and as an occasional intraguild predator of other small
mammals, having a major role in structuring small mammal assem-
blages (Fonseca and Robinson 1990; Moura et al. 2009).
Study area
The study was conducted in a rural area in the locality of
Pamparrão (22◦ 02 46 S, 42◦ 41 21 W) in the county of Sumidouro,
175 km from the city of Rio de Janeiro, southeastern Brazil (Fig. 1).
The original Atlantic Forest of Pamparrão has a long history of
anthropogenic disturbances, currently composed of small rural
properties with vegetable gardens, pasture lands, logging forests,
and few small Atlantic Forest fragments at hilltops. The region
has a humid-mesothermic climate (Nimer 1989) with mean mini-
mum and maximum monthly temperatures of 19.6 ◦ C and 27.4 ◦ C,

Fig. 1. Study area at Pamparrão valley located in the county of Sumidouro (emphasized in black), State of Rio de Janeiro, southeastern of Brazil. The map highlights the
relatively few small Atlantic Forest remnants present in the rural area (in gray) when compared to others counties of Rio de Janeiro.

Please cite this article in press as: Ferreira, M.S., et al., Life history of a neotropical marsupial: Evaluating potential contributions of survival and
reproduction to population growth rate. Mammal. Biol. (2013), http://dx.doi.org/10.1016/j.mambio.2013.03.002
 ARTICLE IN PRESS
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Fig. 2. Life cycle graph of the opossum Didelphis aurita, corresponding to the popu-
lation projection matrix. Nodes correspond to age classes: 1, juveniles; 2, subadults;
3, adults; 4, aged female and arrows represent the possible transitions between age
classes in which Px represent the age-specific survival rate, Fx represent fertility
rate and, mx , fecundity rate. Pouch young marsupials, age class 0, are incorporated
in the fertility transitions (Fx = P0 mx ). Note that animals in age class 1 are not able to
reproduce.
respectively. Total monthly rainfall varies between 0.6 and
462.9 mm, May to August being the driest months, and November to
March the wettest (data obtained from Instituto Nacional de Mete-
orologia do Rio de Janeiro – INMET). For a more detailed description
of the area see Gentile and Fernandez (1999) and Gentile et al.
(2000).
Field methods
Opossums were captured from June 1991 to July 1995 in 7 lin-
ear transects (A–G) in bimonthly trapping sessions. Transects A,
B, C and D had 15 trapping stations each, transects E and F had
10, and G had 5 trapping stations. A trapping session is comprised
of 5 consecutive nights in A, B, C, D, and 4 nights in E, F, G. Each
trapping station received 1 wire-mesh-live-trap on the ground
(32 cm × 18 cm × 20 cm). Trapping stations were spaced 13 m along
each transect, and total trapping effort was 12,250 trap-nights.
Traps were baited with a mixture of oat, banana, peanut butter, and
bacon spread on a manioc slice. Traps were checked every morning
and individuals captured for the first time were marked by tail tat-
tooing, and pouch young by toe-clipping (Twigg 1975). For each
animal we recorded trapping station, sex, body mass, head and
body length, tail length, reproductive condition, and tooth eruption
sequence following Gentile et al. (1995) and Macedo et al. (2006).
Animals were treated carefully following the guidelines for mam-
mals approved by the American Society of Mammalogists (Sikes
et al. 2011).
Estimation of vital rates
Age-specific survival rates (Px , x = 0, 1, 2, 3) and capture proba-
bilities were modeled using a modified Cormack-Jolly-Seber model
implemented in program MARK (Cooch and White 2009). In the set
of candidate models, we considered age and cohort as sources of
differences among individuals. A cohort was defined by a group
of individuals born in the same breeding season of the year (e.g.,
cohort 1992), and only capture histories of individuals first cap-
tured inside the pouch were considered for the analyses. Age was
determined based on the pattern of tooth eruption, which also
correspond to distinct developmental stages (Gentile et al. 1995;
Macedo et al. 2006) (Fig. 2). Individuals were classified into five
age classes: age class 0 comprises pouch young, lactating animals;
age class 1 non-reproductive juveniles, individuals with the first
(M1 ) or the second (M2 ) functional molar; age class 2 reproductive
subadults, individuals with the third (M3 ) functional molar; age
class 3 adults with complete dentition (P3 M4 ); and age class 4 aged
females, individuals with worn teeth cusps. Age and time are syn-
onymous in the models because each transition from one age class
Please cite this article in press as: Ferreira, M.S., et al., Life history of a neotropical marsupial: Evaluating potential contributions of survival and
reproduction to population growth rate. Mammal. Biol. (2013), http://dx.doi.org/10.1016/j.mambio.2013.03.002
3
to the next takes approximately four months in D. aurita, the same
period between encounter occasions (Cooch and White 2009).
Model selection started by accessing potential lack of fit
due to overdispersion of the most general model (i.e., model
({ϕ(age × cohort) p(age × cohort)})). A variance inflation factor (ĉ)
was estimated using a parametric bootstrap approach in program
MARK (Cooch and White 2009), obtained by dividing the deviance
estimated from the most general model with the mean of the 1000
simulated deviances computed in the bootstrap procedure. This
procedure revealed whether the global model could account for the
amount of variation in the data in which case, all the models nested
inside the global model would be fitted as well by definition. When
a lack of fit was detected (ĉ = / 1), model selection statistics were
adjusted according to the ĉ value, obtained from the simulations.
Models were compared based on Akaike’s information criterion
adjusted for small sample size (AICc) (Burnham and Anderson
1998). Delta AICc (difference between each model and the one with
the lowest AICc value), and AICc weight (evidence weight that the
model is the best model within the candidate set) are statistics
derived from AICc that form the basis for comparison among mod-
els (Burnham and Anderson 1998). Model-averaging techniques
were employed when more than one model had substantial sup-
port. In the case of overdispersion in the data, the quasi-Akaike
information criterion (QAICc) was employed (Anderson et al. 1994),
and derived statistics also were based on QAICc.
Fecundity rates (mx , x = 2, 3, 4) were estimated following Caswell
(2001). Using a pre-breeding matrix formulation, fertility rates (Fx ,
x = 2, 3, 4) were parameters composed by pouch young survival
(P0 ) and fecundity rate of each reproductive age class (Fx = P0 mx )
(Caswell 2001).
Sensitivity, elasticity and loop analysis
We converted D. aurita life cycle (Fig. 2) into a female-based,
age-classified matrix projection model and performed sensitivity
and elasticity analyses (Caswell 2001). Sensitivities were the par-
tial derivatives of  with respect to vital rates, which quantify the
potential impact of an absolute change in  with an infinitesimal
absolute change in a vital rate (Caswell 1978). Elasticities were the
proportional sensitivities, i.e., the effect of proportional changes
in a vital rate on . Pouch young survival (P0 ) and age-specific
fecundity rates (mx ) are lower-level parameters, not explicit in the
matrix elements (upper-level), but were part of the fertility rates
(Caswell 2001). Elasticities and sensitivities of lower-level param-
eters were calculated by chain-rule differentiation (Caswell 2001).
Lower-level elasticities generally do not sum to 1 as upper-level
elasticities do (de Kroon et al. 1986), so interpretation of results
based on effects on  must be done carefully (Caswell 2001).
In a life cycle graph, each loop represents a life-history pathway,
i.e., the options for individuals to complete their life cycles. To quan-
tify and compare the proportional effect of different life-history
pathways to  we used a method of loop analysis (van Groenendael
et al. 1994; Caswell 2001), which is based on the elasticity values
of the vital rates estimated previously. Four life history pathways
could be distinguished in the life cycle of D. aurita (Fig. 2): early
reproduction (1 → 2 → 1), adult reproduction (1 → 2 → 3 → 1), late
reproduction (1 → 2 → 3 → 4 → 1) and a self-loop, aged female sur-
vival (4 → 4). Each life history pathway has one unique transition
element and the elasticity of this transition is the characteristic
elasticity of the loop. All transitions in the loop had the same elastic-
ity value and when transitions are part of more than one pathway,
elasticity values are the summed characteristic elasticity of the
loops involved. The loop elasticity is the result of the character-
istic elasticity multiplied by the number of transitions present in a
loop. The sum of all loop elasticities must be equal to one.
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Fig. 3. Sensitivity and elasticity of population growth rate to changes in lower level (black bars) and upper level (white bars) parameters for the opossum Didelphis aurita. Px
represent the age-specific survival rate, Fx represent fertility rate and mx , fecundity rate. Age classes: 1, juveniles; 2, subadults; 3, adults; 4, aged female.
Matrix analyses were performed in R (version 2.13.0, R
Development Core Team 2011) with the package Popbio (Stubben
and Milligan 2007).
Results
During the study, we followed three cohorts: 1991, 1992 and
1993. Since females from the 1994 cohort were still alive at the end
of the study, data was not included in the analyses. A total of 88
pouch young females were marked and 16 (18.2%) individuals were
recaptured, hence most did not survive or were not recaptured later
in their lifetime. Half of the recaptured females reproduced, and
two of them were able to reproduce twice in one breeding season,
survive to the next breeding season, and produce a third litter. One
female was also able to reproduce three times in a breeding season,
and produce a fourth litter in the next breeding season.
Estimation of vital rates
Overdispersion was detected in the general model (ĉ = 1.98,
P < 0.05 in the parametric bootstrap), so we adjusted model selec-
tion statistics according to the ĉ estimate.
Model selection indicated differences in survival among age
classes and in capture probabilities among cohorts (supplemen-
tary material, Table S1). The lowest survival rate values were for
pouch young (parameter value ± SD) (0.191 ± 0.063), followed by
subadults (0.520 ± 0.215), aged females (0.552 ± 0.254), juvenile
(0.956 ± 0.11) and adults (0.962 ± 0.148). For fecundity rates, values
were higher for aged females (2.888 ± 0.192), followed by adults
(2.638 ± 0.851) and juveniles (0.500 ± 0.661). The estimated pop-
ulation growth rate () based on the dominant eigenvalue of the
population projection matrix was 0.973.
Sensitivity, elasticity and loop analysis
Regarding lower level parameters, the high sensitivity values
of pouch young survival (P0 ), almost 3 times as large as subadult
survival (P2 ), confirmed that first class survival has a higher effect
on  compared to the survival in higher classes (Fig. 3, left panel).
The sensitivity of  to fecundity rates was higher for aged females,
followed by subadults and adults (Fig. 3, left panel). Elasticity values
were higher for survival rates of early age classes (pouch young,
juvenile and subadult) and lower for fecundity rates (Fig. 3, right
panel).
Regarding upper level parameters, sensitivity of  to sur-
vival rates was higher for subadults (P2 ) and aged females (P4 –
Fig. 3, left panel). Sensitivity of  to reproductive transitions was
higher for subadults (F2 ), followed by aged females (F4 ) and adults
Please cite this article in press as: Ferreira, M.S., et al., Life history of a neotropical marsupial: Evaluating potential contributions of survival and
reproduction to population growth rate. Mammal. Biol. (2013), http://dx.doi.org/10.1016/j.mambio.2013.03.002
(F3 – Fig. 3, left panel). Similarly to the lower level parameters,
elasticity of  to survival rates showed that first age classes sur-
vival were the key transitions in the life cycle of D. aurita, with
 being far more sensitive to changes in the survival of these age
classes (juvenile and subadult) than to changes in fecundity rates
(Fig. 3, right panel), while elasticities of  regarding fertility rates
were lower than survival rates, with exception of adult survival
(P3 ), which had the same value of aged female fertility (F4 ) (Fig. 3,
right panel). Vital rates with the same elasticity value were also
observed when lower-level elasticities were computed. This hap-
pened because in a life cycle the summed incoming and outgoing
elasticities are equal. Since there is no self-loop on the first node
of the life cycle of D. aurita and the only transition from age class
4 is the late reproduction transition, they will result in the same
value. To confirm the importance of survival transitions to the life
cycle of D. aurita, summed survival elasticities were compared to
summed fertilities. Survival transitions had high elasticity values
than fertility transitions (0.77 and 0.23, respectively).
In loop analysis, late reproduction was the most important life-
history pathway (58.17%). The next highest loop elasticity was
aged females survival (18.95%) and adult reproduction pathway
(18.65%), followed by early reproduction pathway (4.21%), which
had a minor importance in terms of increasing .
Discussion
A strong selective pressure at weaning in D. aurita was revealed
by sensitivity analysis. Low estimates of pouch young survival
or weaning success on previous studies of didelphidae marsu-
pials are evidence that these initial stages are indeed the most
vulnerable in their life cycle (Caluromys philander and Philander
opossum, Charles-Dominique et al. 1981; Atramentowicz 1986,
1992; Didelphis marsupialis, Atramentowicz 1986; Sunquist and
Eisenberg 1993; Didelphis virginiana, Sunquist and Eisenberg 1993;
Hossler et al. 1994; Kanda and Fuller 2004; D. aurita, Kajin et al.
2008). Opossums are quite protected inside the pouch, but from
the moment they are left in the den to the moment they start
to forage, vulnerability increases. At weaning, juvenile opossums
show exploratory and dispersal behavior (Gillette 1980; Graipel
and Santos-Filho 2006), being more susceptible to predators and
even infanticide by adults (Raven, 1929; Lay 1942; Hopkins and
Forbes 1980; Atramentowicz 1992; Hossler et al. 1994; Cherem
et al. 1996).
The relative importance of life-history variables to  in the pop-
ulation here studied disagree with predictions of elasticity patterns
for early maturing mammals (Heppell et al. 2000; Oli and Dobson
2003). The life history of D. aurita should be more similar to species
that attain sexual maturity early, but it is characterized by low
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fertility elasticities, not fitting the expected pattern. This is not
the first study in disagreement with predictions for early maturing
mammals. For the Australian marsupial Onychogalae fraenata, elas-
ticity values were higher for adult survival (Fisher et al. 2000), and
in the American marsupial Thylamys elegans, adult and subadult
survival were more important than recruitment to  (Lima et al.
2001). It is important to note that none of the reviews of elastic-
ity patterns in mammals included demographic data of marsupials.
Thus, the general patterns described by Heppell et al. (2000) and
Oli and Dobson (2003) should be treated cautiously when applied
to marsupials.
The incorporation of all life history and demographic transitions
in the life cycle of D. aurita was essential to identify the critical
stages contributing to , similarly to observed by Radchuk et al.
(2013). Standardizations of transitions in life cycles to common
time frames are frequently necessary in comparative studies of
elasticities involving species with distinct age or stage structured
life histories (Crone 2001). For example, Heppell et al. (2000) pooled
age classes in 50 species of eutherian mammals so that interval
between age classes was 1 year in all species: in mammals that first
reproduce at age of 2 years or higher, age classes were pooled into
three classes (fecundity, juvenile survivorship and adult survivor-
ship), while in mammals that first reproduce at age of 1 year were
pooled in only two (fecundity and adult survivorship). Had we stan-
dardized age classes similarly, to 1 year intervals between classes,
we would not be able to detect the effect of juvenile survival, and
adult survival estimate would be based on a single female which
lived for more than 24 months. Furthermore, we would not have
been able to identify first age class survival as the most important
transition in the opossum’s life cycle.
The “slow” life history of D. aurita may be a result of regular inter-
val between reproductive events and fixed resource allocation to
litter production, with pouch young facing constant conditions, and
mortality of pouch young occurring mostly by mortality of moth-
ers. Reproduction in populations of D. aurita in the latitude of the
study area is markedly seasonal, being somewhat independent of
environmental conditions, with onset of breeding period triggered
by the variation of photoperiod (Cerqueira 2005; Rademaker and
Cerqueira 2006). Therefore, despite the circumstances, reproduc-
tion occurs at regular intervals (this study; Julien-Laferriere and
Atramentowicz 1990; Cerqueira et al. 1993; Hossler et al. 1994;
Kajin et al. 2008), and females appear to allocate the same amount
of reproductive resources in a litter of size 7 (mode) (7.33 ± 1.83)
(supplementary material, Figure S1), an strategy that seems to hold
in other populations of D. aurita (Davis 1945; Cerqueira et al. 1993;
Kajin et al. 2008). Pouch young stay in the pouch for ca. 100 days
(Rademaker and Cerqueira 2006) and after this period weaning of
young tend to coincide with optimal environmental conditions in
an attempt to maximize juvenile survival (Atramentowicz 1992;
Cerqueira 2005). Thus, the number of individuals entering the pop-
ulation through birth is approximately the same of weaned ones
(Rui Cerqueira, personal communication). Nonetheless, survival at
the end of this period seems to be very important, and individ-
uals that survive through the pouch young phase certainly have a
greater potential effect on . Thus, survival of these individuals is
critical in the life cycle of D. aurita.
Another reason for the “slow” life history of D. aurita is the high
variability of reproductive rates compared to variability of survival
rates. Vital rates can be phylogenetically or environmentally con-
strained (Oli et al. 2001), which means that they are difficult to
be perturbed. In our analysis, fertility rates varied markedly, espe-
cially for subadults and adults age classes, contrasting to the low
variability of the survival rates. Variance of vital rates is negatively
correlated with their elasticities (Pfister 1998; Sæther and Bakke
2000), hence the high variability in reproductive rates is a conse-
quence of their low elasticity, which will have the lowest effect on .
Please cite this article in press as: Ferreira, M.S., et al., Life history of a neotropical marsupial: Evaluating potential contributions of survival and
reproduction to population growth rate. Mammal. Biol. (2013), http://dx.doi.org/10.1016/j.mambio.2013.03.002
5
This also would explain the result of loop analysis, where late repro-
duction pathway contributes proportionally more to  than adult
and early reproduction that are less variable. Therefore, in spite of
the small relative influence of reproductive rates, they are still rele-
vant for population persistence and evolution because of their high
variability compared to pouch young and juvenile survival.
Prospective perturbation analysis of matrix models is a first step
taken to answer questions about life history and population dynam-
ics of D. aurita, and marsupials in general. In this regard, this is the
first application of sensitivity and elasticity analysis to a neotropical
rainforest marsupial. Contrary to expectations for elasticity based
on eutherian mammals, survival rates were most influential on 
in the population of D. aurita studied. The “slow” life history of D.
aurita may be a result of the fixed resource allocation to litter pro-
duction and regular interval between reproductive events, an effect
of the photoperiod. Since mortality of pouch young at the end of
this period is high and also linked to mortality of mothers, the indi-
viduals that survive and achieve the juvenile age class will have
the greatest relative influence on . Reproductive parameters are
also potentially important because of their high variability, which
allow response and adaptation in face of environmental perturba-
tions. Further studies should consider variance-based perturbation
analyses (LTRE – life table response experiments), which take into
account variability in vital rates. This five-year study of a population
of D. aurita, in addition to published studies for a few other marsu-
pials, suggest that the general pattern identified in eutherians may
not hold for marsupials, but sensitivity and elasticity analyses of
other marsupial species are necessary to test this hypothesis.
Acknowledgements
The authors thank Selina Heppell for suggestions on the anal-
ysis and three anonymous referees and the subject editor (Prof.
Dr. Heiko Rödel) for their helpful comments. We are also thank-
ful to Renato Crouzeilles for valuable comments and suggestions
in a early version of the manuscript, P.S. D’Andrea, C.H. Almeida,
C.E.V. Grelle and J.W.F. da Costa for help during the field work, Insti-
tuto Oswaldo Cruz (Fiocruz), CNPq, FAPERJ, CAPES (PNPD grant to
M.K.) and “Projeto Nacional de Ações Integradas, Público-privadas
para Biodiversidade - PROBIO II” for financial support, Sumidouro
Municipal Government for providing some operational facilities,
owners of the rural properties in Sumidouro and S. Serafim for
structural facilities during field work.
Appendix A. Supplementary data
Supplementary data associated with this article can be found,
in the online version, at http://dx.doi.org/10.1016/j.mambio.
2013.03.002.
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