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Adult vocalizations can develop following three alternative modes; by retention of juvenile vocalizations, through the modification of juvenile precursors or by a de novo appearance in adults. Vocalizations that develop from juvenile precursors may develop following two pathways; vocal learning (implying the ability of juveniles to modify their vocalizations based on an external auditory input) and/or vocal tract maturation (involving the improvement of the capacity of juveniles to generate progressively more adult-like vocalizations by the tuning of an innate motor program). The emission of adult vocalizations requires the synchronization of neuromuscular and anatomical structures, and the lack of maturation and/or precise coupling between them would lead to the production of abnormal vocalizations. Tuco-tucos (Ctenomys spp.) are subterranean rodents that produce territorial, high intensity long-range vocalizations (LRVs) of, broadband and low frequency that are essential for long-distance communication between individuals in different tunnel systems. Despite their importance, the developmental modes, pathways and developmental sequences of LRVs remain poorly understood. In adult Anillaco Tuco-Tucos (Ctenomys sp.) the LRV is composed by two types of syllables (series and individual notes) that are repeated a variable number of times. We studied the development of the LRV in 8 juveniles of the Anillaco Tuco-Tuco ranging from 14 to 108 days after birth. The LRV exhibited a mixed developmental mode: while series developed from juvenile precursors whose acoustic features gradually approached those of adults, individual notes appeared later in the ontogeny and de novo, with acoustic features undistinguishable from those of adults. Vocalizations became progressively longer, but the series types shown by adults were evident in juveniles at an early age. All three acoustic features of series (triad) notes studied correlated with age in both sexes (duration 90% increased through development, while bandwidth 90% and peak frequency decreased). LRV developed normally in juveniles acoustically isolated from adults, supporting the vocal tract maturation hypothesis and possibly rejecting the vocal learning hypothesis. Juveniles emmitted a higher proportion (7.4%) of abnormal vocalizations than adults (0.3%), as expected in the development of any complex behavior that requires practice to be mastered. The maturation of the LRV occurred well before the sexual maturation, presumably due to the protracted time needed to acquire or build a burrow system long before mating is possible. We propose that protracted vocal development is another component in the slow developmental strategy of Ctenomys and subterranean rodents in general.
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Acoustic parameters of triad notes and individual notes of juveniles males during vocal development
Acoustic parameters (duration 90%. bandwidth 90%. peak frequency) of triad notes and individual notes of juveniles males during 4 sampling weeks over 12 study weeks in relation to weight and adults males of the Anillaco Tuco-Tuco (Ctenomys sp.).
Acoustic parameters of triad notes and individual notes of juveniles females during vocal development
Acoustic parameters (duration 90%. bandwidth 90%. peak frequency) of triad notes and individual notes of juveniles females during 4 sampling weeks over 12 study weeks in relation to weight and adults females of the Anillaco Tuco-Tuco (Ctenomys sp.).
Spearman correlation values and significance levels of comparisons of selected acoustic parameters vs. age in the development of long-range vocalizations (LRVs) of juveniles of the Anillaco Tuco-Tuco (Ctenomys sp.). *P<0.05, **P<0.001, ns = P>0.1