Cristian E. Schleich

Subterranean Rodents: News from Underground

Across the globe, in all continents but Australia and Antarctica, at least 250 extant rodent species (38 genera, 6 families – according to the classification applied) spend most of their lives in self-constructed burrows (Table 1.1, Fig. 1.1). Their subterranean ecotope is dark, microclimatically stable, hypoxic and hypercapnic, and deprived of most sensory cues available aboveground. The burrows offer shelter from predators and climatic extremes, but digging is energetically costly, and the yield of foraging is relatively low, because the productivity of the subterranean ecotope is rather low and the food resources (roots and underground plant storage organs like bulbs and tubers) are mostly unpredictably and unevenly scattered. These so-called subterranean rodents are specialized in multiple aspects for their unique way of life in which most events like foraging, mating, and breeding take place underground. Animals that inhabit underground selfmade tunnels, but also forage (predominantly) above ground, are called fossorial. Needless to say, a continuum exists between fossorial and subterranean rodents, and in the present volume a categorical differentiation is mostly ignored on purpose. Another mammalian group sharing the same ecotope, but feeding on invertebrates, are subterranean non-rodent mammals likemarsupial moles, certain armadillos, as well as “insectivore” moles (e.g. Talpidae) and golden moles (Chrysochloridae). Although the title of the book emphasizes that the focus is on subterranean rodents, we also encouraged the authors to glance at recent findings from studies on other subterraneanmammals, and we hope that the reader will profit from this. Most subterranean rodent taxa have already been scientifically described in the golden ages of alpha taxonomy 100–200 years ago (and, e.g. the blind mole-rat Spalax and the mole-vole Ellobius talpinus in 1770), and many subterranean dwellers have been familiar to local people for ages (Spalax

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

Abstract. The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat.

BULLAR VOLUME IN SUBTERRANEAN AND SURFACE-DWELLING CAVIOMORPH RODENTS

Abstract Bullar volume was estimated by external measurements for the subterranean genus Ctenomys (Rodentia, Ctenomyidae) and 24 species of surface-dwelling caviomorphs. Bullae were larger in Ctenomys than in caviomorphs. Larger bullar size may reflect good low-frequency audition and could be an adaptation for subterranean vocal communication. Estimated bullar volume of the Pliocene rodent Actenomys was intermediate between that of Ctenomys and surface-dwelling caviomorphs, in agreement with the presumed intermediate subterranean lifestyle of Actenomys.

Retinal photoreceptors of two subterranean tuco-tuco species (Rodentia, Ctenomys): morphology, topography, and spectral sensitivity.

Traditionally, vision was thought to be useless for animals living in dark underground habitats, but recent studies in a range of subterranean rodent species have shown a large diversity of eye features, from small subcutaneous eyes to normal‐sized functional eyes. We analyzed the retinal photoreceptors in the subterranean hystricomorph rodents Ctenomys talarum and Ctenomys magellanicus to elucidate whether adaptation was to their near‐lightless burrows or rather to their occasional diurnal surface activity. Both species had normally developed eyes. Overall photoreceptor densities were comparatively low (95,000–150,000/mm2 in C. magellanicus, 110,000–200,000/mm2 in C. talarum), and cone proportions were rather high (10–31% and 14–31%, respectively). The majority of cones expressed the middle‐to‐longwave‐sensitive (L) opsin, and a 6–16% minority expressed the shortwave‐sensitive (S) opsin. In both species the densities of L and S cones were higher in ventral than in dorsal retina. In both species the tuning‐relevant amino acids of the S opsin indicate sensitivity in the near UV rather than the blue/violet range. Photopic spectral electroretinograms were recorded. Unexpectedly, their sensitivity profiles were best fitted by the linear summation of three visual pigment templates with λmax at 370 nm (S pigment, UV), at 510 nm (L pigment), and at 450 nm (an as‐yet unexplained mechanism). Avoiding predators and selecting food during the brief aboveground excursions may have exerted pressure to retain robust cone‐based vision in Ctenomys. UV tuning of the S cone pigment is shared with a number of other hystricomorphs. J. Comp. Neurol. 518:4001–4015, 2010.

FUNCTIONAL MORPHOLOGY OF THE MIDDLE EAR OF Ctenomys talarum (RODENTIA: OCTODONTIDAE)

Abstract The middle ear of the solitary subterranean rodent Ctenomys talarum was studied. The most significant features observed were the enlarged middle-ear cavity, a round and larger eardrum without pars flaccida, no connection between malleus and the tympanic bone, partial fusion of malleus with incus, a nearly flat stapedial footplate, absence of stapedial artery, reduced tensor tympani, and absence of stapedial muscle. Some of these features are shared with unrelated subterranean rodents like Spalax ehrenbergi and geomyids, possibly as adaptations for low-frequency hearing.

Juvenile vocalizations ofCtenomys talarum (Rodentia: Octodontidae)

We analysed the physical structure and functional interpretation of juvenile vocalizations ofCtenomys talarum Thomas, 1898. Two sounds, one true vocalization (care-elicitation call) and one mechanical sound (nursing sound) were recorded during the nestling period. Care-elicitation calls were emitted by isolated pups and caused the mother to respond by immediately approaching the pups to take care of them. This maternal response to the care-elicitation calls ofC. talarum pups, together with the production of these vocalizations during the first weeks after birth, when pups depend exclusively on their mother to obtain food and maintain their body temperature, give preliminary support for the recent theory that care-elicitation cries are honest advertisements of offspring need.

Acoustic Communication in Subterranean Rodents

Why study acoustic communication? And why in subterranean rodents? There are several reasons for studying acoustic communication in this particular group of mammals. First, acoustic communication is of great importance to the organization of animal societies. Animals use vocal signals to elicit specific behaviors, initiate contacts with conspecifics, identify individuals or species, signalize status (reproductive, dominance, territorial), solicit food, warn against predators, and coordinate reproductive efforts (courtship, copulation solicitation, physiological synchrony). Beyond the intra-specific level, acoustic signals are also an important factor in reproductive isolation and speciation processes. Furthermore, vocal communication can be a useful instrument for explaining general evolutionary principles. Signal structure and function are shaped by several factors, such as characteristics of the environmental channel in which the signal is transmitted and the physiological and morphological properties of both, the sender and the receiver. Thus, the characteristics of the vocal signals usually demonstrate the kind, intensity and process of natural selection. Why in subterranean rodents? The answer to this question is intimately linked to the particular environment in which they live. The subterranean ecotopehas influenced the evolutionof the sensory biology of subterranean rodents. As seen in the previous chapter, the dark and monotonous subterranean environment limits the transmission of most signals and cues,

Energetic expenditure during vocalization in pups of the subterranean rodent Ctenomys talarum

Theoretical signaling models predict that to be honest, begging vocalizations must be costly. To test this hypothesis, oxygen consumption was measured during resting and begging (i.e., vocalizing) activities in pups of the subterranean rodent Ctenomys talarum by means of open-flow respirometry. No statistical differences in individual oxygen consumption between resting and calling pups ranging in age from day 2 to day 20 were found. Given these data, begging calls of C. talarum could not be considered as honest advertisements of offspring need, contrary to what suggested by the behavioral observations of the mother and pups during the nestling period.

Sound transmission and burrow characteristics of the subterranean rodentCtenomys talarum (Rodentia: Ctenomyidae)

Males of tuco-tucoCtenomys talarum Thomas, 1898 use particular burrow’s entrances to emit their territorial vocalization. Therefore we studied the internal structure of these entrances and the possible effect on the emission and propagation of airborne sounds. Externally, the burrow entrances used by tuco-tucos males to vocalize were characterized by the absence of sand mounds around their openings. Internally, most of the burrow’s entrances consisted of a main, relatively straight, tunnel of 30–40 cm length, with a diameter of 5.7–6.4 cm. After passing through the burrow’s entrance, the low-frequency components of an artificial signal played back inside the tunnel were not only less attenuated but also amplified (measured at 10–30 cm from the burrow opening). Therefore, the emission of territorial vocalizations inside the particular burrow’s entrances may be considered as a complex adaptative behavior, in which burrow structure improves the signal emission and propagation. Moreover, this work also showed thatC. talarum’s territorial vocalization seems to be adequate for long, inter-burrow communication, since its physical characteristics (high amplitude and low main frequency) are concomitant with the frequencies that are better transmitted in the natural habitat of this species of subterranean rodent.

Prenatal predatory stress in a wild species of subterranean rodent: Do ecological stressors always have a negative effect on the offspring?

In pregnant females, a failed predatory event not only induces individual responses but also represents a significant change in the developmental environment of the offspring, which may lead to modifications in their phenotype that may persist at different stages of life. We evaluate whether prenatal exposure to predatory cues affects anxiety behavior, behavioral response to predator cues, stress response to immobilization, and immune response to sheep red blood cells (SRBC) and phytohemagglutinin (PHA) in juveniles of the subterranean rodent Ctenomys talarum. We found that prenatal predator stress (PPS) (1) increased juvenile anxiety-like behaviors and the appearance of antipredator behaviors, (2) did not affect the response of offspring to predatory stressors, and (3) did not influence the physiological response of juveniles to stressors (immobilization) nor the immunological responses to SRBC and PHA challenges. This work shows the influence of PPS on the development of behavioral responses in the offspring, whom displayed a state of anxiety and behavioral changes associated with decreased locomotor activity and avoidance behaviors. Thus, these individuals prenatally exposed to predatory cues show behavioral adaptations that may contribute to avoid predators in the adult life.