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Didelphimorphia: Didelphidae) Inhabiting the Brazilian Cerrado

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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 a 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 b 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. © 2014 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. 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 1616-5047/© 2014 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved. 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 2 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 2 monthly, during four consecutive nights, from August 2010 to April significantly
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