Form and function of long-range vocalizations in a Neotropical fossorial rodent: the Anillaco Tuco-Tuco (Ctenomys sp.)

The underground environment poses particular communication challenges for subterranean rodents. Some loud and low-pitched acoustic signals that can travel long distances are appropriate for long-range underground communication and have been suggested to be territorial signals. Long-range vocalizations (LRVs) are important in long-distance communication in Ctenomys tuco-tucos. We characterized the LRV of the Anillaco Tuco-Tuco (Ctenomys sp.) using recordings from free-living individuals and described the behavioral context in which this vocalization was produced during laboratory staged encounters between individuals of both sexes. Long-range calls of Anillaco tuco-tucos are low-frequency, broad-band, loud, and long sounds composed by the repetition of two syllable types: series (formed by notes and soft-notes) and individual notes. All vocalizations were initiated with series, but not all had individual notes. Males were heavier than females and gave significantly lower-pitched vocalizations, but acoustic features were independent of body mass in males. The pronounced variation among individuals in the arrangement and number of syllables and the existence of three types of series (dyads, triads, and tetrads), created a diverse collection of syntactic patterns in vocalizations that would provide the opportunity to encode multiple types of information. The existence of complex syntactic patterns and the description of soft-notes represent new aspects of the vocal communication of Ctenomys. Long-distance vocalizations by Anillaco Tuco-Tucos appear to be territorial signals used mostly in male-male interactions. First, emission of LRVs resulted in de-escalation or space-keeping in male-male and male-female encounters in laboratory experiments. Second, these vocalizations were produced most frequently (in the field and in the lab) by males in our study population. Third, males produced LRVs with greater frequency during male-male encounters compared to male-female encounters. Finally, males appear to have larger home ranges that were more spatially segregated than those of females, suggesting that males may have greater need for long-distance signals that advertise their presence. Due to their apparent rarity, the function and acoustic features of LRV in female tuco-tucos remain inadequately known

Nocturnal to Diurnal Switches with Spontaneous Suppression of Wheel-Running Behavior in a Subterranean Rodent.

Several rodent species that are diurnal in the field become nocturnal in the lab. It has been suggested that the use of running-wheels in the lab might contribute to this timing switch. This proposition is based on studies that indicate feed-back of vigorous wheel-running on the period and phase of circadian clocks that time daily activity rhythms. Tuco-tucos (Ctenomys aff. knighti) are subterranean rodents that are diurnal in the field but are robustly nocturnal in laboratory, with or without access to running wheels. We assessed their energy metabolism by continuously and simultaneously monitoring rates of oxygen consumption, body temperature, general motor and wheel running activity for several days in the presence and absence of wheels. Surprisingly, some individuals spontaneously suppressed running-wheel activity and switched to diurnality in the respirometry chamber, whereas the remaining animals continued to be nocturnal even after wheel removal. This is the first report of timing switches that occur with spontaneous wheel-running suppression and which are not replicated by removal of the wheel

Circadian phase and intertrial interval interfere with social recognition memory

A modified version of the social habituation/dis-habituation paradigm was employed to examine social recognition memory in Wistar rats during two opposing (active and inactive) circadian phases, using different intertrial intervals (30 and 60 min). Wheel-running activity was monitored continuously to identify circadian phase. To avoid possible masking effects of the light-dark cycle, the rats were synchronized to a skeleton photoperiod, which allowed testing during different circadian phases under identical lighting conditions. In each trial, an infantile intruder was introduced into an adult`s home-cage for a 5-minute interaction session, and social behaviors were registered. Rats were exposed to 5 trials per day for 4 consecutive days: oil days I and 2, each resident was exposed to the same intruder; on days 3 and 4, each resident was exposed to a different intruder in each trial. I he resident`s social investigatory behavior was more intense when different intruders were presented compared to repeated presentation of the same intruder, suggesting social recognition memory. This effect was stronger when the rats were tested during the inactive phase and when the intertrial interval was 60 min, These findings Suggest that social recognition memory, as evaluated in this modified habituation/dis-habituation paradigm, is influenced by the circadian rhythm phase during which testing is performed, and by intertrial interval. (C) 2008 Elsevier Inc. All rights reserved.CAPESCoordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)FAPESPFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)CNPqConselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq

Modeling natural photic entrainment in a subterranean rodent (Ctenomys aff. knighti), the Tuco-Tuco.

Subterranean rodents spend most of the day inside underground tunnels, where there is little daily change in environmental variables. Our observations of tuco-tucos (Ctenomys aff. knighti) in a field enclosure indicated that these animals perceive the aboveground light-dark cycle by several bouts of light-exposure at irregular times during the light hours of the day. To assess whether such light-dark pattern acts as an entraining agent of the circadian clock, we first constructed in laboratory the Phase Response Curve for 1 h light-pulses (1000lux). Its shape is qualitatively similar to other curves reported in the literature and to our knowledge it is the first Phase Response Curve of a subterranean rodent. Computer simulations were performed with a non-linear limit-cycle oscillator subjected to a simple model of the light regimen experienced by tuco-tucos. Results showed that synchronization is achieved even by a simple regimen of a single daily light pulse scattered uniformly along the light hours of the day. Natural entrainment studies benefit from integrated laboratory, field and computational approaches

Simultaneous measurements of daily rhythms in oxygen consumption (V˙O2), body temperature (T_b), gross motor and wheel-running activity of tuco-tucos.

<p>Left: temporal series collected when the animal was inside the respirometry chamber, with and without a running-wheel. Shaded areas indicate dark phases and white areas light phases. Right: actograms across experimental conditions. Pink and blue backgrounds indicate data from animals inside the respirometry chamber, with and without access to wheels, respectively. (A) Representative individual that did not switch phase inside the respirometry chamber. Pink line in the left figure indicates introduction of the wheel to the chamber. (B) Representative individual that switched from nocturnal to diurnal inside the respirometry chamber. There was a 7-day interval outside the respirometry chamber before the wheel introduction due to technical problems. Pink broken line in the right figure separates days with and without wheels. General conditions: LD12:12 (L = 200–250 lux), 25±2°C and food <i>ad libitum</i>.</p

Wheel-running, mean T_b and mean Oxygen consumption of tuco-tucos in relation to diurnality indexes.

<p>Measurements for each individual (N = 9), across the stages of the experiment including days outside (white squares) and inside (black square) the respirometry chamber both with and without (grey squares) running-wheels. (A) Mean daily wheel-running levels are associated with nocturnality. (B) Mean body temperatures during each stage. There is no clear correlation with D-Indices. (C) Mean <math><mrow><msub><mrow>V<mo>˙</mo>O</mrow><mn>2</mn></msub></mrow></math> during each stage. There is no clear correlation with D-Indices. (D) Mean amount of general activity per day during each stage. There is no clear correlation with D-Indices.</p

Schematic view of different phase switch patterns associated with the presence of running wheels.

<p>Based on: [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref001" target="_blank">1</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref039" target="_blank">39</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref056" target="_blank">56</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref057" target="_blank">57</a>] for <i>Octodon degus</i>; [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref002" target="_blank">2</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref038" target="_blank">38</a>] for <i>Arvicanthis niloticus</i>; [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref003" target="_blank">3</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref058" target="_blank">58</a>] for <i>Acomys russatus</i>; [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref004" target="_blank">4</a>] for <i>Meriones ungiculatus</i>; [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref009" target="_blank">9</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140500#pone.0140500.ref010" target="_blank">10</a>] for <i>Ctenomys</i> aff. <i>knighti</i>. *For each species, field data were collected using different methods and do not necessarily reflect activity patterns of whole populations.</p

Dynamics of the model oscillator under different simulated light-regimens.

<p>The upper-left actogram presents the oscillator in a free-running condition, under a simulated constant darkness (DD). The following graphs show the oscillator under simulated pulse regimens. Except for the DD condition, values over the actograms indicate the duration, in hours, of the time-interval I when the pulses occur. Pulse-times are represented by white dots over the gray background representing a simulated dim background illumination. A consistent 24 h-period is only visualized up to the time-window duration of 12 h. The abscissas for all actograms are the same as indicated under the “I₌12 h” graph.</p

Photic Phase Response Curve (PRC) of the tuco-tuco.

<p>A: Representative phase-shifts in response to light-pulses. The actograms show three examples of free-running rhythms of tuco-tucos under DD conditions and different phase-shift responses of the rhythms elicited by a single 1 h-light-pulse (1000 lux) on day 28 (open circle). In each graph, the phase of activity onsets after the pulse (lower dashed line) is compared to the phase of activity onsets previous to the pulse (upper dashed line). In response the light stimuli, activity phase was either advanced (left graph), delayed (middle graph) or unshifted (right graph). Values on the upper left of each graph are quantifications, in hours, of the phase-shift responses. The upper right numbers are identification codes for individual animals. B: The magnitudes of phase-shift responses are plotted against the time of the applied light-pulse. The time axis is represented in a standardized time-scale (circadian time). Inset: single values for each of the phase-shift responses. Outer graph: mean phase-shifts ±1 standard deviation for every 3 CT’s. Both graphs illustrate the dependence of the magnitude and sign of phase-shift on the time of the pulse.</p

Synchronization of the wheel-running activity rhythm of a tuco-tuco by light dark cycles LD 1∶23 (A) and LD 12∶12 (B).

<p>The data is depicted in actograms, with times of running-wheel activity (black and dark-gray marks) represented along the days. Dark-gray marks represent free-running rhythms in the first 15 days in DD. White rectangles drawn in the graphics during the LD cycles represent the hours of lights-on. Both light-dark cycles LD 1∶23 and LD 12∶12 synchronize the rhythms of tuco-tucos to a 24 h-period. Figure B was modified from Valentinuzzi et al. (2009) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068243#pone.0068243-Valentinuzzi1" target="_blank">[1]</a>.</p