Didelphimorphia: Didelphidae) Inhabiting the Brazilian Cerrado

Mammalian Biology 80 (2015) 1–6

Contents lists available at ScienceDirect

Mammalian Biology

jou rnal homepage: www.elsevier.com/locate/mambio

Original Investigation

Semelparity in a population of Gracilinanus agilis

(Didelphimorphia: Didelphidae) inhabiting the Brazilian cerrado

a b,∗

Gabriel P. Lopes , Natália O. Leiner

Programa de Pós-Graduac¸ ão em Ecologia e Conservac¸ ão de Recursos Naturais, Laboratório de Ecologia de Mamíferos, Instituto de Biologia, Universidade

Federal de Uberlândia, Uberlândia, MG, Brazil

Laboratório de Ecologia de Mamíferos, Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, MG, Brazil

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

Article history: Although reproducing once in a lifetime (i.e. semelparity) is considered rare among vertebrates, it has

Received 20 February 2014

evolved at least ﬁve times in two distantly related marsupial families; the Australian Dasyuridae and

Accepted 31 August 2014

South American Didelphidae. The major aim of this research was to describe the population dynamics,

Handled by Heiko G. Rödel

reproductive strategy and associated life-history traits of the agile gracile mouse opossum, Gracilinanus

Available online 6 September 2014

agilis, in order to position the species along the fast-slow life-history continuum. Sampling was carried

out through mark-recapture, from August 2010 to April 2013, in a Brazilian area of cerrado. Reproductive

Keywords:

activity was seasonal and synchronized among females, and occurred from July to January/February. After

Didelphidae

Life-history mating, population size decreased due to male disappearance, which seems to be explained by post-

mating male die-off. Phylogenetic predisposition toward semelparity in Gracilinanus lineage and intense

Male die-off

Reproductive strategy competition for females may contribute to male die-off, as indicated by several evidences such as male-

Sex ratio biased sex ratio, signs of aggression in reproductive males, and a pronounced gain in male body mass and

size prior to mating. Although two litters were produced, most females disappeared after weaning their

young, indicating post-reproductive senescence and resulting in discrete, non-overlapping generations,

characterizing semelparity in this population of G. agilis.

Introduction formed by Antartica, during the Cretaceous-Palaeogene (Nilsson

et al. 2004; Beck et al. 2008). These families of carnivorous mar-

Organisms present a variety of reproductive strategies, orga- supials, although distantly related (Cockburn 1997; Cardillo et al.

nized in a spectrum that ranges from iteroparity at one extreme 2004), present several similarities in their life-history (Springer

to semelparity at the other end of the continuum (Stearns 1992). et al. 1998), such as the adoption of a semelparous life cycle, which

The vast majority of species are iteroparous, reproducing sev- is surprisingly common among these families (Cockburn 1997).

eral times over a lifetime. On the other hand, a few species Among dasyurids, at least ﬁve genera present semelparity, which

present a semelparous breeding strategy, participating in only is characterized by stress-related male die-off after a short, highly

one breeding event (Cole 1954), which is usually followed by synchronized breeding season (Oakwood et al. 2001; Bradley 2003).

a massive post-reproductive mortality of individuals leading to Females may survive to participate in a second reproductive event,

discrete, nonoverlapping generations. Although common among although they usually present a decline in fecundity during the

invertebrates and plants (Stearns 1992; Lesica and Young 2005), second event (Cockburn 1997).

this strategy is considered rare among vertebrates (Crespi and Teo Although a great deal is known about the reproductive strate-

2002); even so it can be found in several marsupial species. gies of dasyurid marsupials and the physiological causes of male

Australian dasyurids and South American didelphids repre- die-off (Bradley 2003; Naylor et al. 2008), little is known about

sent two distantly related marsupial families, sharing common didelphid reproductive strategies and associated life-history traits.

ancestors that dispersed from South America, via a land bridge Recent studies reports a semelparous life cycle in the eastern short-

tailed opossum Monodelphis dimidiata (Baladrón et al. 2012), the

Brazilian gracile mouse opossum Gracilinanus microtarsus (Martins

∗ et al. 2006b), the gray slender mouse opossum Marmosops incanus

Corresponding author. Tel.: +55 3432182806.

(Lorini et al. 1994) and the São Paulo slender mouse opossum Mar-

E-mail addresses: [email protected] (G.P. Lopes), [email protected]

(N.O. Leiner). mosops paulensis (Leiner et al. 2008). In contrast to their Australian

http://dx.doi.org/10.1016/j.mambio.2014.08.004

2 G.P. Lopes, N.O. Leiner / Mammalian Biology 80 (2015) 1–6

counterparts, a few neotropical didelphids present cases of obligate third superior molar fully functional were considered sub-adults

semelparity, in which both males and females show a 100% mor- (P3/M3) and individuals with complete dentition (P3/M4) were

tality after mating and weaning respectively (Leiner et al. 2008; considered adults.

Baladrón et al. 2012), or partial semelparity, in which mortality Permission to trap and handle Didelphidae was issued by SIS-

increases after the mating period, but a few individuals of both BIO/ICMBio (Brazil) to Natalia Leiner (Permit Number: 22629-1)

sexes may survive to breed in the following year (Martins et al. and all trapping and handling of didelphids agreed with the ethical

2006b). principals on animal research as regulations of National Advice of

The agile gracile mouse opossum Gracilinanus agilis is a small Control and Animal Experimentation (CONCEA/Brazil). The proto-

(20–45 g), solitary, arboreal mouse opossum (Gardner 2007), col was approved by the Ethics Committee on Use of Animals of the

inhabiting the cerrado areas in southeastern Brazil. Its diet is com- Federal University of Uberlândia, Brazil (permit number: 152/13).

posed mainly of insects, although fruits may act as an important

food source during the dry season, especially for reproductive

Data analysis

females (Lamberto 2011; Camargo et al. 2014). Reproduction is

usually synchronized among individuals and a biased sex-ratio

The sex ratio (SR = number of males/number of males + females)

toward males has already been reported in previous populations

of sexually mature G. agilis individuals was calculated separately

(Aragona and Marinho-Filho 2009; Andreazzi et al. 2011). Because

for each year (2011 and 2012). Bias in sex ratio was evaluated

the adoption of this extreme reproductive strategy may vary among

through chi-square tests, with Yates correction. Population size was

populations of the same species (Lorini et al. 1994; Mills and Bencini

estimated monthly through the minimum number known alive

2000; Oakwood et al. 2001), the aim of this paper is to describe

(MNKA). Survival rates were estimated for the periods between

the population dynamics of G. agilis in a Brazilian area of cerrado,

consecutive sessions by the Jolly-Seber method (Seber 1986), sep-

with special emphasis on its reproductive mode and associated

arately for each sex. In this way, population was considered closed

life-history traits.

during trapping sessions and open between trapping sessions,

similarly to Pollock’s robust design (Pollock 1982). Differences in

Materials and methods body weight were compared between males and females using

a Mann–Whitney test, due to heterogeneity of variances, and

Study site between immature (juveniles) and sexually mature individuals

of both sexes, using separate analysis of variance for juveniles

The study was conducted at Estac¸ ão Ecológica do Panga and adults. Differences between non-reproductive (May–June) and

◦ ◦ ◦ ◦

(19 09 20–19 11 10 S and 48 23 20 –48 24 35 W, MG), a 409.5 ha reproductive males (July–December) were evaluated using a t-test,

cerrado fragment in the south region of Uberlândia municipality, and between non-reproductive (May–June), reproductive/mating

Minas Gerais state, Brazil. Climate in the area is characterized by (July–August) and lactating females (September–February) were

a dry winter from April to September and a wet summer from tested using an ANOVA with a posteriori Tukey tests.

October to March. Mean annual temperature is approximately

◦

22 C and average annual rainfall is about 1650 mm. Sampling of

Results

the G. agilis population was carried out in a cerrado sensu stricto

site, covered by secondary-growth herbaceous vegetation, which is

From August 2010 to April 2013, 124 individuals of G. agilis

dominated by Miconia albicans (Cardoso et al. 2009). Few, sparsely

were captured, including 82 males and 42 females, during 8040

distributed trees, compose the arboreal stratum.

trap-nights. In 2011, sex ratio (proportion of males) was 0.76

(20 reproductive males and 6 reproductive females), indicating

Capture of individuals a male-biased sex ratio ( = 6.50, P = 0.010), while in 2012 the

proportion of males (SR) was 0.6 (27 reproductive males and 13

In order to capture G. agilis individuals, trapping was carried out reproductive females), and the test revealed that sex ratio was not

monthly, during four consecutive nights, from August 2010 to April signiﬁcantly different from 1:1 ( = 0.83, P = 0.36). Females pre-

2013. From August 2010 to June 2012, Sherman traps were set in a senting signs of reproductive activity were captured from July to

grid of 0.96 ha, composed of ﬁve parallel transects of 120 m, spaced January/February. Since didelphid gestation lasts approximately

20 m apart. At each transect, seven capture stations with 2 traps 13–15 days (Tyndale-Biscoe and Renfree 1987), probably mat-

each (one on the ground and other in the understory) were placed ing started in July, while in August/September all females were

20 m apart. From July 2012 to April 2013, an additional 120 m tran- pregnant or lactating. Recently weaned pups (10–14 g) were ﬁrst

sect was included in the trapping grid. Following this addition, the captured in November, suggesting that weaning took place 3–4

trapping grid was then composed of six parallel transects, each months after gestation. In the following year, a few juveniles

containing eight instead of seven trap stations 20 m apart; thus (about 16–18 g) were also observed in April/May, indicating that

totaling a 1.4 ha grid with 96 traps baited with a mixture of banana, a few females may have produced a second, late litter. However,

oatmeal, peanut butter and bacon. Traps were checked daily, and it is important to notice that usually females suffered a nearly

all captured individuals were individually marked with numbered complete turnover of individuals during the breeding season. In

ear-tags. this way, it seems that some females mated in the beginning

Sex, body mass, breeding status and age class were evaluated for of the breeding season (July/August) and weaned their litters

each individual, which were then released in the same point of cap- in November/December, disappearing from the population after-

ture. Breeding status was evaluated based on external characters, wards, while a few mated from October to December, and weaned

such as perforated vagina and presence of swollen nipples or milk their litters in April/May. The same pattern of reproduction was

production as indicators of female reproduction and scrotal testes repeated every year, with a strong breeding synchrony among adult

as a sign of male sexual maturity. Age class was estimated follow- females in the population (Table 1).

ing Macedo et al. (2006), who proposed a method based only on In both years, the number of individuals (N2011 = 26 individ-

the eruption of the last superior molars. In this way, those individuals, N2012 = 40 individuals) was higher from June to October, which

uals presenting only the ﬁrst and second fully functional superior corresponded to most of the dry season. After October, there was

molars (P3/M1 or M2) were considered juveniles, those with the a drastic decrease in the observed number of individuals, which

G.P. Lopes, N.O. Leiner / Mammalian Biology 80 (2015) 1–6 3

Table 1

Monthly percentage of G. agilis individuals belonging to different age classes (adult, subadult and juvenile) and their respective breeding status at Estac¸ ão Ecológica do Panga

(Brazil) from January 2011 to April 2013. We excluded August–December 2010, since we captured only reproductive adults in this period, and sampling was not possible in

November 2011. Asterisks indicate months were only females were captured.

Month Adult Subadult Juvenile

Reproductive Non-reproductive Reproductive Non-reproductive

January 100

February 100

March 100

April 75 25

May 83.3 13.66

June 50 50

July 81.25 18.75

August 50 50

September 100

October 100

December 100

January 100*

February 50* 50

March 75 25

April 58 42

May 87.5 12.5

June 25 66.66 8.33

July 78.5 21.5

August 70 30

September 100

October 100

November 60 40

December 33.3* 66.6

January 25* 75

February 100

March 50 50

April 58 42

corresponded to the reduced number of adult males, due to belonging to 2011, 2012, 2013 cohorts were captured in January

a decrease in their survival between September and October, 2011 (18–20 g), February 2012 (19–21 g) and November 2012

resulting in the complete disappearance of these individuals (10–14 g), respectively. Adults from these cohorts were only cap-

between November and December (Fig. 1). By this period, tured after June/July (Table 1). In this way, each generation was

captured males presented signs of reduced body condition, discrete and presented a complete lack of overlap.

such as fur loss, wounds and high endoparasite infestation Sexually mature individuals (adults and subadults) were heavier

(Strona & Leiner, unpublished results). Adult females also pre- than juveniles (Mann–Whitney U test: U58 = 6.35, P < 0.001; Fig. 2A),

sented a decrease in their numbers, but most adult females although the initial gain in body weight occurred in July, dur-

survived until January or February (Fig. 1), with the excep- ing the mating period in males (t = −11.68, df = 38, P < 0.001;

tion of a single female that survived until April in 2013. Fig. 2B). Among females, body mass also increased during repro-

After male mortality, only juvenile males were trapped, which duction (F2,27 = 17.04, P < 0.001), and signiﬁcant differences were

were followed by sub-adults. The same phenomenon occurred found between the three categories (Fig. 2C). Lactating females

with females, after their disappearance. The ﬁrst individuals were heavier (mean body weight = 30.2 g) than non-reproductive

Fig. 1. Monthly ﬂuctuations in population size and survival of G. agilis individuals at Estac¸ ão Ecológica do Panga (Brazil) from August 2010 to April 2013. Abundance of

individuals (gray bars) was estimated using the MNKA and survival of both males (lines with triangles) and females (lines with circles) by Jolly-Seber.

4 G.P. Lopes, N.O. Leiner / Mammalian Biology 80 (2015) 1–6

Discussion

Our ﬁndings support the positioning of G. agilis in the fast-end of

the life history continuum, indicating the adoption of a semelparous

breeding strategy. First, the population suffered a reduction in

numbers after the mating season, more precisely from September

to October, which was largely explained by the disappearance of

adult males from the population. The lack of male immigration, the

reduced post-mating survival and several signs of decreased body

condition, such as fur loss, high endoparasite infestation (Strona

and Leiner, unpubl.) and the presence of wounds in the captured G.

agilis males, argues in favor of male die-off. In several marsupial

species, semelparity is characterized by male post-reproductive

die-off (Braithwaite and Lee 1979), in which males present sim-

ilar patterns of reduced body condition after the mating season

(Martins et al. 2006b; Leiner et al. 2008; Naylor et al. 2008) and usu-

ally die due to stress-related pathologies associated with increased

competition for the opposite sex and energetic constraints (Bradley

2003). Among Australian dasyurids, females participate in a sec-

ond reproductive event, although they show decreased fecundity

(Cockburn 1997). In the studied population, although two litters are

produced during the breeding season, each female seems to disap-

pear after weaning their offspring, similarly to M. paulensis (Leiner

et al. 2008). However, partial semelparity, in which a small group

of males and females can take part in another breeding event, may

also occur within didelphids, such as G. microtarsus (Martins et al.

2006b). Due to small sample size and lower female capture rates,

there is a slight possibility that our sampling design failed to detect

a few surviving individuals, especially females that could partic-

ipate in a second breeding event. Regardless of this caveat, male

post-mating die-off, female post-reproductive senescence (sensu

Cockburn 1997) and seasonal population age structure resulted

in discrete, nonoverlapping generations in the studied population,

thus characterizing semelparity in G. agilis.

Reproductive activity of G. agilis started by the end of June and

lasted until February. Mating apparently started in July/August and

lasted until December, and weaning took place in November and

April/May. As already demonstrated in other didelphids, energeti-

cally demanding phases of reproduction (i.e. lactation and weaning)

are usually restricted to periods of high food supply (Quental et al.

2001; Martins et al. 2006a; Leiner et al. 2008), with several stud-

ies showing the effect of the mother’s body condition on offspring

success (Gonzalez and Claramut 2000; Jonsson et al. 2002). In the

studied population, most females weaned their litters during the

wet season, which is usually associated with higher food supply,

while a few females mated in the late breeding season with debil-

itated males, weaning their litters in the dry season (April/May),

which usually corresponds to a food shortage period. In this way,

we suggest that juveniles belonging to the ﬁrst litter may experi-

ence higher survival than those belonging to the late litter, although

future studies should be done in this direction.

Population studies focusing on sex ratios of didelphid marsu-

Fig. 2. Body mass (g) of G. agilis males and females, belonging to adult and juve- pials indicate that sex-biases vary according to year and locality

nile age classes (A), G. agilis subadult and adult males during the non-breeding (Fernandez et al. 2003). Previous research with G. agilis have already

(May–June) and breeding season (from July to December) (B), and G. agilis females

described male-biased sex ratios in cerrado populations (Aragona

during the non-breeding (May–June), mating (July–September) and lactation period

and Marinho-Filho 2009), which is corroborated by our results.

Although several factors may contribute to skewed adult sex ratio,

letters indicate signiﬁcant differences between the analyzed groups.

we suggest that these biases were due to differential detectabil-

ities between the sexes (Donald 2011). The higher mobility of G.

(mean body weight = 21.5, Tukey test: P < 0.001, Fig. 2C) and repro- agilis males (Lopes 2014) may inﬂuence their capture rate, and then

ductive/mating females (mean body weight = 26 g, Tukey test: play a part in the observed male bias in 2011 and a higher num-

P = 0.025), while mating females presented larger body mass ber of males when compared to females in 2012, although the bias

than non-reproductive females (Tukey test: P = 0.028). Sexual size was not signiﬁcant. However, competition between adult and juve-

dimorphism occurred among juveniles (F1,23 = 4.74, P = 0.040) and nile females could also play a role in the observed male-biased sex

among adults (F1,32 = 8.40, P = 0.007), with males always presenting ratio, as already discussed in Antechinus swainsonii (Cockburn et al.

larger body weight than females. 1985).

G.P. Lopes, N.O. Leiner / Mammalian Biology 80 (2015) 1–6 5

Males experienced a gain in body mass prior to mating season, Acknowledgements

while female body mass increased during lactation, resulting in a

strong sexual size dimorphism during the reproductive season. The We thank A.L.S. Strona, S.T. Cardoso, J.M. Lamberto and P.

increase in body mass was accompanied by an increase in body Antunes for their help in ﬁeldwork. Two anonymous review-

size in both sexes during the reproductive period. Usually, among ers and M.V. Vieira provided valuable suggestions that improved

polygynous and promiscuous small mammals, males compete for the ﬁnal version of this manuscript. We are also indebted to

females and their reproductive success is based on body size and Programa de Pós-Graduac¸ ão em Ecologia e Conservac¸ ão de Recur-

mass (Clutton-Brock 1989; Oakwood 2002). Previous studies with sos Naturais/UFU for logistical support, and Coordenac¸ ão de

marsupials have already demonstrated that larger males are supe- Aperfeic¸ oamento de Pessoal do Nível Superior (CAPES) for spon-

rior competitors, gaining access to more females and fathering most soring G.P. Lopes. This study was funded by research grants

young (Ryser 1992; Holleley et al. 2006). This pronounced change provided by FAPEMIG CRA-04023/10, CNPq (PELD 403733/2012-0)

in body size and mass among G. agilis reproductive males may and FAPEMIG PACCSS/CRA-30058/12.

be associated to competition between males (see Baladrón et al.

2012), which is proposed as one of the driving forces of a semel-

parous reproductive strategy (Holleley et al. 2006). On the other

References

hand, female gain in body mass seems to be associated to the ener-

getic costs of reproduction, especially lactation, and body growth. Andreazzi, C.S., Rademaker, V., Gentile, R., Herrera, H.M., Jansen, A.M., D’Andrea, P.S.,

Body mass reﬂects female nutritional status, hence larger females 2011. Population ecology of small rodents and marsupials in a semi-deciduous

tropical forest of the southeast Pantanal, Brazil. Zoologia 28, 762–770.

may be more successful in producing large litters and rearing their

Aragona, M., Marinho-Filho, J., 2009. História natural e biologia reprodutiva de mar-

offspring (Gonzalez and Claramut 2000; Price-Rees et al. 2012).

supiais no Pantanal, Mato Grosso, Brasil. Zoologia 26, 220–230.

Since G. agilis females usually participate in a single breeding event, Baladrón, A.V., Malizia, A.I., Bó, M.S., Liébana, M.S., Bechard, M.J., 2012. Population

dynamics of the southern short-tailed opossum (Monodelphis dimidiata) in the

assuring offspring survival and improving reproductive success is

Pampas of Argentina. Aust. J. Zool. 60, 238–245.

crucial.

Beck, R.M.D., Godthelp, H., Weisbecker, V., Archer, M., Hand, S.J., 2008. Australia’s

Male die-off in dasyurids is attributed to intense competition oldest marsupial fossils and their biogeographical implications. PLoS ONE 3,

pe1858.

for females, due to the short, synchronized mating period. Fierce

Boonstra, R., 2005. Equipped for life: the adaptive role of the stress axis in male

competition leads to an adaptive stress response, characterized

mammals. J. Mammal. 86, 236–247.

by failure of the negative glucocorticoid feedback system, which Bradley, A.J., 2003. Stress, hormones and mortality in small carnivorous marsupi-

als. In: Jones, M., Dickman, C.R., Archer, M. (Eds.), Predators with Pouches: The

culminates in massive mortality of males due to immunosuppre-

Biology of Carnivorous Marsupials. CSIRO Publishing, Melbourne, Australia, pp.

sion, parasite infestation, lost of weight and organ degeneration 254–267.

(Boonstra 2005). The factors involved in male post-mating mor- Braithwaite, R.W., Lee, A.K., 1979. A mammalian example of semelparity. Am. Nat.

113, 151–155.

tality within didelphids remain unresolved. However, there is

Camargo, N.F., Ribeiro, J.F., De Camargo, A.J.A., Vieira, E.M., 2014. Diet of the

sounding evidence in G. agilis to suggest that intense male com-

gracile mouse opossum Gracilinanus agilis (Didelphimorphia: Didelphidae) in a

petition might play a role. First, males display signs of aggression, neotropical savanna:intraspeciﬁc variation and resource selection. Acta Theriol.

such as wounds, during the end of the mating season. Moreover, 59, 183–191.

Cardillo, M., Bininda-Emmons, O.R.P., Boakes, E., Purvis, A., 2004. A species-level

males exhibit an increase in testis size during this period (mean

phylogenetic supertree of marsupials. J. Zool. 264, 11–31.

scrotal width during the breeding period = 13.4 mm and during the

Cardoso, E., Moreno, M.I., Bruna, E.M., Vasconcelos, H.L., 2009. Mudanç as fitofi-

non-breeding period = 9.8 mm), probably linked to higher testos- sionômicas no Cerrado: 18 anos de sucessão ecológica na Estac¸ ão Ecológica do

Panga, Uberlândia – MG. Caminhos de Geograﬁa 10, 254–268.

terone concentrations, which usually contribute to aggressiveness

Clutton-Brock, T.H., 1989. Mammalian mating systems. Proc. R. Soc. Lond. B 236,

(Bradley 2003; Naylor et al. 2008). Didelphid mating systems and 339–372.

spatial organization, with males moving more during the breed- Cockburn, A., 1997. Living slow and dying young: senescence. In: Saunders, N., Hinds,

L. (Eds.), Marsupials. University of New South Wales Press, Sydney, Australia, pp.

ing season and female territoriality (Croft and Eisenberg 2006;

163–174.

Leiner and Silva 2009), should increase male energy expenditure

Cockburn, A., Scott, M.P., Dickman, C.R., 1985. Sex ratio and intrasexual kin compe-

and favor agonistic interactions due to the increased encoun- tition in mammals. Oecologia 66, 427–429.

Cole, L.C., 1954. The population consequences of life-history phenomena. Q. Rev.

ters between males. Second, male-biased sex ratios is consistent

Biol. 29, 103–137.

with intense male competition for females, once adult sex ratio

Crespi, B.J., Teo, R., 2002. Comparative phylogenetic analysis of the evolution of

is a key factor controlling sexual selection and inﬂuencing mat- semelparity and life history in salmonid ﬁshes. Evolution 56, 1008–1020.

Croft, D.B., Eisenberg, J.F., 2006. Behaviour. In: Armati, P., Dickman, C.R., Hume, I.

ing systems (Parker and Simmons 1996; Kokko and Jennions

(Eds.), Marsupials. Cambridge University Press, Cambridge, United Kingdom, pp.

2008). Third, males present several signs of decreased body con-

229–298.

dition by the end of the reproductive period, which are similar to Donald, P.F., 2011. Lonely males and low lifetime productivity in small populations.

their Australian counterparts (Naylor et al. 2008), although their Ibis 453, 465–467.

Fernandez, F.A.S., Barros, C.S., Sandino, M., 2003. Biased sex ratio in populations of

physiological and immunological changes require further inves-

the wooly mouse opossum Micoureus demerarae. Nat. Conserv. 1, 78–84.

tigation. Finally, since mating started during the dry season, it

Fisher, D.O., Dickman, C.R., Jones, M.E., Blomberg, S.P., 2013. Sperm competition

is possible that low resource availability in this period associ- drives the evolution of suicidal reproduction in mammals. Proc. Natl. Acad. Sci.

U. S. A., 1–5.

ated with competition for females could contribute to stress, as

Gardner, A.L., 2007. Order didelphimorphia. Mammals of South America. In: Gard-

already suggested by Fisher et al. (2013) to explain Antechinus

ner, A.L. (Ed.), Marsupials, Xenarthrans, Shrews and Bats, vol. 1. University of

breeding strategy; hence, leading to male debilitation and even- Chicago Press, Chicago, USA, pp. 1–126.

Gonzalez, E.M., Claramut, S., 2000. Behavior of captive short-tailed opossums Mon-

tually die-off by the end of the mating season. However, G. agilis

odelphis dimidiata (Wagner, 1847) (Didelphimorhia: Didelphidae). Mammalia

male post-mating die-off and female post-reproductive senes-

64, 281–285.

cence could also be explained by a phylogenetic predisposition Holleley, C.E., Dickman, C.R., Crowther, M.S., Oildrouyd, B.P., 2006. Size breeds suc-

cess: multiple paternity, multivariate selection and male semelparity in a small

toward semelparity in didelphids and dasyurids, as pointed out

marsupial, Antechinus stuartii. Mol. Ecol. 15, 3439–3448.

by Oakwood et al. (2001). Actually, this reproductive mode was

Jonsson, P., Hartikainen, T., Koskela, E., Mappes, T., 2002. Determinants of reproduc-

already described in two distinct didelphid lineages, one includ- tive success in voles: space use in relation to food and litter size manipulation.

Evol. Ecol. 16, 455–467.

ing Gracilinanus and Marmosops and other including Monodelphis

Kokko, H., Jennions, M.D., 2008. Parental investment, sexual selection and sex ratios.

(Palma 2003), indicating that it may have evolved in their ances-

J. Evol. Biol. 21, 919–948.

tor, and then suffered multiples losses, or separately in each Lamberto, J.M., 2011. Dieta de Gracilinanus agilis (Didephimorphia: Didelphidae) e

lineage. Rhipidomys sp. (Rodentia: Cricetidae) em uma área de cerrado stricto sensu na

6 G.P. Lopes, N.O. Leiner / Mammalian Biology 80 (2015) 1–6

Estac¸ ão Ecológica do Panga, Uberlândia, MG. Monograﬁa. Universidade Federal Oakwood, M., Bradley, A.J., Cockburn, A., 2001. Semelparity in a large marsupial.

de Uberlândia Uberlândia. Proc. R. Soc. Lond. B 268, 407–411.

Leiner, N.O., Setz, E.Z.F., Silva, W.R., 2008. Semelparity and factors affecting the Oakwood, M., 2002. Spatial and social organization of a carnivorous marsupial

reproductive activity of the brazilian slender opossum (Marmosops paulensis) Dasyurus hallucatus (Marsupialia: Dasyuridae). J. Zool. 257, 237–248.

in Southeastern Brazil. J. Mammal. 89, 153–158. Palma, R.E., 2003. Evolution of American marsupials and their phylogenetic rela-

Leiner, N.O., Silva, W.R., 2009. Territoriality in female slender opossums (Marmosops tionships with Australian metatherians. In: Jones, M., Dickman, C.R., Archer, M.

paulensis) in the Atlantic forest of Brazil. J. Trop. Ecol. 25, 671–675. (Eds.), Predators with Pouches: The Biology of Carnivorous Marsupials. CSIRO

Lesica, P., Young, T.P., 2005. A demographic model explains life-history variation in Publishing, Melbourne, Australia, pp. 21–29.

Arabis fecunda. Funct. Ecol. 19, 471–477. Parker, G.A., Simmons, L.W., 1996. Parental investment and the control of sexual

Lopes, G.P., (Master’s dissertation) 2014. Estratégia reprodutiva e organizac¸ ão espa- selection predicting the direction of sexual competition. Proc. R. Soc. Lond. B

cial de uma populac¸ ão de Gracilinanus agilis (Didelphimorphia: Didelphidae) 263, 315–321.

na Estac¸ão Ecológica do Panga, em Uberlândia/MG. Universidade Federal de Pollock, K.H., 1982. A capture-recapture design robust to unequal probability of

Uberlândia, Uberlândia, Brazil. capture. J. Wildl. Manage. 46, 752–757.

Lorini, M.L., Oliveira, J.A., Persson, V.G., 1994. Annual age structure and reproductive Price-Rees, S.J., Congdon, B.C., Krockenberger, 2012. Size delays female senescence

patterns in Marmosa incana (Lund, 1841) (Didelphidae, Marsupialia). Mamm. in a medium sized marsupial: the effects of maternal traits on annual fecun-

Biol. 59, 65–73. dity in the northern brown bandicoot (Isoodon macrourus). Aust. Ecol. 37,

Macedo, J.S., Loretto, D., Vieira, M.V., Cerqueira, R., 2006. Classes dentárias e de 313–322.

desenvolvimento em marsupiais: um método de análise para animais vivos em Quental, T.B., dos Santos, F.A., Dias, A.T.C., Rocha, F.S., 2001. Population dynamics of

campo. Mastozool. Neotrop. 13, 133–136. the marsupial Micoureus demerarae in small fragments of Atlantic Coastal Forest

Martins, E.G., Bonato, V., da Silva, C.Q., dos Reis, S.F., 2006a. Seasonality in repro- in Brazil. J. Trop. Ecol. 17, 339–352.

duction, age structure and density of the gracile mouse opossum Gracilinanus Ryser, J., 1992. The mating system and male mating success of the Virginia opossum

microtarsus (Marsupialia: Didelphidae) in a Brazilian cerrado. J. Trop. Ecol. 22, (Didelphis virginiana) in Florida. J. Zool. 228, 127–139.

461–468. Seber, G.A.F., 1986. A review of estimating animal abundance. Biometrics 42,

Martins, E.G., Bonato, V., da Silva, C.Q., dos Reis, S.F., 2006b. Partial semelparity in 267–292.

the neotropical didelphid marsupial Gracilinanus microtarsus. J. Mammal. 87, Springer, M.S., Westerman, M., Kavanagh, J.R., Burk, A., Woodburne, M.O., Kao, D.J.,

915–920. Krajewski, C., 1998. The origin of the Australasian marsupial fauna and the phy-

Mills, H.R., Bencini, R., 2000. New evidence of facultative maledie-off in island popu- logenetic afﬁnities of the enigmatic monito del monte and marsupial mole. Proc.

lations of dibblers, Parantechinus apicalis. Aust. J. Zool. 48, 501–510. R. Soc. Lond. B 265, 2381–2386.

Naylor, R., Richardson, S.J., McAllan, B.M., 2008. Boom and bust: a review of the Stearns, S.C., 1992. The evolution of life histories. Oxford University Press, Oxford,

physiology of the marsupial genus Antechinus. J. Comp. Physiol. B 178, 545–562. United Kingdom.

Nilsson, M.A., Armason, U., Spencer, P.B.S., Janke, A., 2004. Marsupial relationships Tyndale-Biscoe, H., Renfree, M.B., 1987. Reproductive physiology of marsupials.

and a timeline for marsupial radiation in South Gondwana. Gene 340, 189–196. Cambridge University Press, New York, USA.