Reproductive biology of Río Negro tuco-tuco, Ctenomys rionegrensis (Rodentia: Octodontidae)

Abstract

Reproductive success depends on a precise synchronization of organisms’ activities with the environment, determining the evolution of mechanisms controlling reproductive behaviour. In temperate zones mammals exhibit pronounced seasonal reproduction because of thermoregulation costs imposed by low winter temperatures and limited food availability. Even occupying burrows that buffer external ambient conditions, these restrictions also affect subterranean rodents inhabiting these latitudes. Tuco-tucos (genus Ctenomys) are subterranean herbivorous rodents that have a Neotropical distribution between 17 and 54° of latitude S. Ctenomys rionegrensis is one of the three species occurring in Uruguay and generated interest due to chromatic polymorphism in a restricted area (50×60 km). Here we describe the timing of breeding in C. rionegrensis based on the reproductive status of free-living females and the proportion of juveniles in the population, and describe the characteristics of the estrous cycle of the species using cytological techniques. As expected, the data showed a clear seasonality in female breeding and provided evidence of the occurrence of post-partum estrous. The reproductive activity began in late austral autumn and the highest proportion of pregnant females was observed in winter. At the beginning of the austral spring, the prevalence of lactating females increased as a consequence of the first births and remained high until early summer. This pattern of breeding seasonality was clearly correlated with the annual temperature variation. The estrous cycle showed four phases characterized by both different cellular types and the abundance and appearance of mucus, which allows a clear determination of female's reproductive status.

Introduction

Reproductive behaviour has been traditionally approached emphasizing either proximal physiological mechanisms or evolutionary factors (Crews and Moore 1986). Mechanisms that allow individuals to optimize advantages of favourable environmental conditions for reproduction have evolved under two major categories of constraints: environmental (e.g. food availability or adequate breeding sites) and physiological (time for gamete maturation or offspring growth) (Crews and Moore 1986; Ims 1990). Reproductive success depends on a precise synchronization of organisms’ activities with the environment, determining the evolution of mechanisms controlling reproductive behaviour in which hormonal and social cues are involved. In temperate-zone environments, mammals exhibit pronounced seasonal reproduction because of thermoregulation costs imposed by low winter temperatures and limited food availability (Fournier et al. 1999; Bronson 1989). Even occupying burrows that buffer external ambient conditions (Altuna 1991; Sumbera et al. 2004), these restrictions also affect subterranean rodents inhabiting these latitudes. Therefore, environment physical factors as photoperiod, temperature and precipitation, which influence as well food availability, are key in determining the beginning and duration of the breeding season in these animals (Bronson, 1985, Bronson, 1989; Ims 1990; Fanjul et al. 2006). These particular conditions provide an interesting framework to generate information on the temporal pattern of reproduction in subterranean rodent species.

Tuco-tucos (genus Ctenomys), subterranean herbivorous rodents, have Neotropical distribution between 17 and 54° of latitude S., and occur in a wide ambient ranging from Andean steppes at 4000 m high to coastal sandy dunes in the Atlantic coast, prairies and deserts. In Uruguay, Ctenomys rionegrensis is one of the three species occurring in the country and has generated interest due to its chromatic polymorphism in a restricted area (50×60 km) in the southwest region of the Department of Río Negro. Although the Río Negro tuco-tuco has been specially considered when investigating genetic and geographic differentiation (D’Elía et al. 1998; Wlasiuk et al. 2003, D’Anatro and Lessa 2006) basic parameters of life history of this species such as reproductive seasonality or estrous cycle characteristics are unknown.

Within this genus, some generalizations have been proposed about reproduction, namely long pregnancies of around 100 days and induced ovulation by copulation (Zarrow and Clark 1968; Weir 1974; Weir and Rowlands 1974; Altuna et al. 1991; Camin 1999; Bennett et al. 2000; Fanjul and Zenuto 2008a). Mainly in the Argentinean species C. mendocinus (Rosi et al., 1996, Rosi et al., 1992) and C. talarum (Pearson et al. 1968; Malizia and Busch, 1991, Malizia and Busch, 1997; Malizia 1998; Zenuto et al., 2002, Zenuto et al., 1999, Zenuto et al., 2002; Fanjul et al. 2006) female reproductive parameters like pregnancy frequency and duration, litter size, and reproductive seasonality have been reported. Except in C. talarum (Malizia 1998; Fanjul et al. 2006; Fanjul and Zenuto 2008b) most of such studies are based on data obtained from autopsied animals because their subterranean habits prevent or make difficult direct behavioural studies in wild populations. However, a non-invasive study of the external features and vaginal cytology, combined with a long-time field study would allow us to determine accurately and to monitor reproductive status in females across time. Also, observations in captivity would contribute to know the estrous cycle. We hypothesize that females adjust their reproductive activity in relation to seasonal fluctuations in ambient conditions. Because in Ctenomys species reported, pregnancy last about 100 days (Pearson 1959; Weir 1974; Zenuto et al., 2002, Zenuto et al., 2002) we predict that reproductive activity begins in early winter, since births occur in spring when environmental conditions are favourable for pups’ development.

The aim of the present study was to determine the temporal pattern of breeding in Ctenomys rionegrensis, by assessing reproductive status in free-living females and proportion of juveniles in the population through a long-term study. Another objective was to investigate the characteristics of the estrous cycle in this species by non-invasive techniques at field and laboratory. In this study we diagnosed reproductive condition of females and described the reproductive seasonality in a Uruguayan species of Ctenomys using cytological techniques.