Postnatal Development of Subterranean Habits in Tuco-Tucos Ctenomys Talarum (Rodentia, Caviomorpha, Ctenomyidae)
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J Ethol DOI 10.1007/s10164-015-0453-5 ARTICLE Postnatal development of subterranean habits in tuco-tucos Ctenomys talarum (Rodentia, Caviomorpha, Ctenomyidae) 1 1,2 1,3 Alejandra Isabel Echeverrı´a • Laura Marina Biondi • Federico Becerra • Aldo Iva´n Vassallo1 Received: 14 September 2015 / Accepted: 18 November 2015 Ó Japan Ethological Society and Springer Japan 2015 Abstract Postnatal development of subterranean habits hindfeet as adults do. During lactancy individuals could was investigated in Los Talas’ tuco-tuco Ctenomys construct a simple burrow to shelter, and first burrow talarum, a subterranean caviomorph rodent endemic from construction occurred in the absence of either a burrowing South America. Since in this species, some key morpho- demonstrator or an early subterranean environment (a natal functional traits related to scratch-digging behaviour—a burrow). However, certain features of the complex burrow form of underground progression—are already present system that characterize this species, such as lateral bran- during early ontogeny and develop progressively, we pre- ches and nest chamber, just appeared after weaning. The dicted that this behaviour expresses early during postanatal time elapsed until animals started to dig and the time development and its performance enhances gradually from dedicated to underground activities varied with age, pups to adults. The process of acquisition of different decreasing and increasing, respectively. In sum, our results behaviours associated to the construction of a burrow show that—in C. talarum—immature digging behaviour system was recorded in 11 individuals, each one coming gets expressed early during ontogeny, and develops pro- from different litters, inside a terrarium filled with natural gressively. The role of the early ability to build its own soil. We found that scratch-digging and burrowing beha- burrow and its possible function influencing the develop- viours expressed early during postnatal development, par- ment of musculoskeletal traits and on efficiency for such ticularly, during lactancy. The digging of a ‘‘true burrow’’ conduct is discussed. clearly preceded the dispersal age, with a high inter-indi- vidual variability, from 18 (lactancy) to 47 (post-weaning) Keywords Postnatal ontogeny Á Scratch-digging postnatal days. Pups could lose the soil using their fore- behaviour Á Subterranean rodents Á Tuco-tucos claws and remove the accumulated substrate using their Introduction & Alejandra Isabel Echeverrı´a [email protected] For altricial animals, the initial phase in the ontogeny represents a stage of great vulnerability because younglings 1 Grupo Morfologı´a Funcional y Comportamiento, Instituto de Investigaciones Marinas y Costeras, Universidad Nacional de have to learn and refine survival and reproductive skills Mar del Plata, Consejo Nacional de Investigaciones (Kirkton and Harrison 2006). Thus, investigating beha- Cientı´ficas y Te´cnicas, Dea´n Funes 3250, 2do. Piso, vioural changes during an organism’s development may 7600 Mar del Plata, Argentina provide insights into both the evolution of these behaviours 2 Grupo Vertebrados, Instituto de Investigaciones Marinas y and the differential ecology of various life stages (Stamps Costeras, Universidad Nacional de Mar del Plata, Consejo 2003). For small rodents, running and hiding are the main Nacional de Investigaciones Cientı´ficas y Te´cnicas, Dea´n Funes 3250, 3er. piso, 7600 Mar del Plata, Argentina strategies to protect themselves from predators and burrows offer an excellent protection against most of them (Trill- 3 Max Planck Weizmann Center for Integrative Archaeology and Anthropology, Max Planck Institute for Evolutionary mich et al. 2003). On the other hand, digging (i.e., to Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany breakup and remove the soil) and burrowing (i.e., to hide in 123 J Ethol burrows, to construct by tunnelling or to progress by or as axial tunnel representing 48 % of the total length, a single if by digging) are common behaviours in many mammals, nest, and a variable number of lateral blind and foraging particularly in arid and semi-arid ecosystems (Nevo 1999; tunnels; Antinuchi and Busch 1992). Although increasing Whitford and Kay 1999). Moreover, the possession of a evidence suggests that several complex behaviours in burrow with stable temperatures underground is especially higher vertebrates are socially transmitted from mother to critical for surviving in zones with great temperature offspring, it was shown that vertical social transmission is fluctuations on the ground surface (Kinlaw 1999). For not essential for the development of subterranean habits in mammals that evolved to live underground, burrows play C. talarum (Vassallo 2006). This rodent is solitary and an important role in their interactions with the environment highly territorial, both sexes and all ages displaying a low (Reig et al. 1990; Lacey et al. 2000), since they serve a vagility, whose individuals do not share burrows except for number of purposes (e.g., thermoregulation, procurement females and their offspring (up until the time of dispersing) and storage of foods, facilitation of social interactions and or at the moment when mating occurs (Busch et al. 1989). mating; see for examples, Fleming and Brown 1975; Elli- Nestlings stay inside the natal burrow during a *2 months son 1995; Ebensperger and Blumstein 2006). Accordingly, period (Zenuto et al. 2002a), which probably determines a subterranean lifestyle has become advantageous for small the species-typical early environmental conditions. They mammals in different phylogenetic lineages, not only show a long gestation period [95 days; (Zenuto et al. because it provides a stable environment but also a shelter 2002b)], and females raise pups in isolation (i.e., without against predators (Antinuchi et al. 2007; Zelova´ et al. any male or conspecific cooperation), which are rather 2010). altricial with respect to the developmental stage at birth Caviomorph rodents (Rodentia, Hystricognathi) repre- (Zenuto et al. 2002a; Cutrera et al. 2003). sent one of the most diverse clades of rodents in terms of Although there are studies on digging behaviour of adult ecology, life history, body size, and locomotor habits tuco-tucos (Camı´n et al. 1995; Giannoni et al. 1996; Vas- (Mares and Ojeda 1982; Vassallo and Antenucci 2015). For sallo 1998), the literature contains little information con- example, the Superfamily Octodontoidea includes aquatic, cerning its postnatal development. Our goal was to arboreal, terrestrial, fossorial, and completely subterranean investigate the postnatal development of subterranean species with wide-ranging climbing and digging special- habits in C. talarum under semi-natural conditions by izations (Morgan 2009; and references therein). Particu- analysing: (i) the first appearance and time course of larly, echimyids (spiny rats) and ctenomyids (tuco-tucos) changes in the ability to break down and remove the soil are the most diverse families of South American cavio- and associated behaviours, (ii) the time course of changes morphs (Parada et al. 2011; Fabre et al. 2013). Ctenomys, in the architecture of the excavated burrow system. Dig- the only living genus of the family Ctenomyidae, is char- ging behaviour is a highly specialized and derived loco- acterized by a high species richness (*60 recognized liv- motor behaviour (Lessa et al. 2008) by which animals ing species; Parada et al. 2011). These species occur over a progress underground by breaking down and removing the wide geographical and environmental range, nevertheless soil. Evidence from postnatal development analyses of they all share adaptations to terrestrial and underground different modes of locomotion in rodents (see Eilam 1997) activity (Camı´n et al. 1995). Los Talas’ tuco-tuco (C. showed that those species with more specialized locomotor talarum Thomas, 1898) inhabits dunes and interdunes at behaviours (e.g., asymmetrical gaits: bound, gallop and Buenos Aires Province (Argentina) and spends most of its bipedal walk) exhibit them late during ontogeny, compared life within plugged burrows (Reig et al. 1990), located to more generalized modes (e.g., symmetrical gaits: lateral parallel to soil surface (Busch et al. 1989; Antinuchi and walk and trot). This fact is partly related to the acquisition Busch 1992). At the morphological level, adult tuco-tucos of certain morphological features (for example, propor- have a robust digging apparatus (forelimbs and skull), tionally longer hindlimbs in jumping species; see Eilam which is specially adapted for loosening and transporting 1997). However, Echeverrı´a et al. (2014) showed that—in the soil (Ferna´ndez et al. 2000; Mora et al. 2003; Morgan C. talarum—some morphological adaptations to scratch- and Verzi 2006; Verzi 2008). Vassallo (1998) found that, digging are already present during early postnatal onto- when confronted with sandy and friable soils, these tuco- geny—suggesting that they are prenatally shaped—and tucos exclusively use their forelimbs—scratch-digging—to develop progressively. Particularly, these authors have break down the soil. Conversely, when it is confronted with shown that the olecranon increasingly elongate, suggesting harder and clayey soils, they behaved as a scratch- and a gradual enhancement in the scratch-digging performance chisel-tooth digger, using also the incisors to dig. This due to an improvement in the mechanical advantage of species builds extensive and elaborated tunnel systems