Response of Bolivian gray titi monkeys (Plecturocebus donacophilus) to an anthropogenic noise gradient: behavioral and hormonal correlates

Worldwide urban expansion and deforestation have caused a rapid decline of non-human primates in recent decades. Yet, little is known to what extent these animals can tolerate anthropogenic noise arising from roadway traffic and human presence in their habitat. We studied six family groups of titis residing at increasing distances from a busy highway, in a park promoting ecotourism near Santa Cruz de la Sierra, Bolivia. We mapped group movements, sampled the titis’ behavior, collected fecal samples from each study group and conducted experiments in which we used a mannequin simulating a human intrusion in their home range. We hypothesized that groups of titi monkeys exposed to higher levels of anthropogenic noise and human presence would react weakly to the mannequin and show higher concentrations of fecal cortisol compared with groups in least perturbed areas. Sound pressure measurements and systematic monitoring of soundscape inside the titis’ home ranges confirmed the presence of a noise gradient, best characterized by the root-mean-square (RMS) and median amplitude (M) acoustic indices; importantly, both anthropogenic noise and human presence co-varied. Study groups resided in small, overlapping home ranges and they spent most of their time resting and preferentially used the lower forest stratum for traveling and the higher levels for foraging. Focal sampling analysis revealed that the time spent moving by adult pairs was inversely correlated with noise, the behavioral change occurring within a gradient of minimum sound pressures ranging from 44 dB(A) to 52 dB(A). Validated enzyme-immunoassays of fecal samples however detected surprisingly low cortisol concentrations, unrelated to the changes observed in the RMS and M indices. Finally, titis’ response to the mannequin varied according to our expectation, with alarm calling being greater in distant groups relative to highway. Our study thus indicates reduced alarm calling through habituation to human presence and suggests a titis’ resilience to anthropogenic noise with little evidence of physiological stress.

piloerection while looking at the mannequin. She emits a short alarm call (~3 s) and then leaves.

GROUP 3 -MFJIB
Trial # 2 Date: 02/15/18 Start time: 6:00; no wind, sunny End time: 7:20 Mannequin: north facing Test duration: 20 min 6:59-7:00 Adult female is the first to observe the mannequin from a vantage point in a Eucalyptus tree, at a distance of ~4 m and ~5 m above ground. She starts emitting soft, high-pitched calls while watching the dummy. The juvenile and infant appear together and observe the dummy from behind the branches. Then, appears the adult male and they all start emitting chirrups. They all climb up to the tree top (~5 m).
Then the juvenile starts producing chirrups. 7:01-7:04 Focal group remains silent while watching the mannequin. The adult female goes down and looks directly at the dummy. The adult male stands behind her mate who adopts a defensive posture, shrinking her back and ruffling her coat, staggering from side to side without calling. They do not leap to another tree. 7:05-7:08 Adult female approaches the mannequin to a distance of ~4 m. She stands ~2 m above ground. She is hiding among the branches of a Eucalyptus tree and adopts a defensive posture, hunching her back with signs of piloerection. The adult male starts producing solo song in response to the duet of a neighboring pair. They don't move to another tree. 7:08-7:10 Adult female approaches and inspects the dummy ~3 m away. She stands ~2 m above ground. The juvenile arrives, followed by the two infants. The adult male shows up last and approaches the dummy with a defensive posture. They all walk away and climb in the Eucalyptus trees, behind. At 7:10, the adult male starts producing solo song for approximately 15 s. Finally, they all climb up to the canopy and move back, avoiding the decoy before crossing to another tree. 8:08-8:14 Adult female appears and sees the mannequin but ignores it. She goes behind the infant while circumnavigating the dummy. At a height of ~4 m, just when she is behind the dummy, she emits a short alarm call. As a result, the infant runs away and disappears among the tangles of lianas. The adult male is not yet visible.
8:14-8:21 Adult female looks at the mannequin from between the branches of the trees at a distance of ~5 m and ~4 m high. However, she does not emit any call and start eating leaves. All individuals regroup to forage on leaves. Finally, the adult male stops eating and moves towards the mannequin, followed by the female and the infant. All individuals pass the dummy at a distance of ~2 m and at a height of ~3 m.
None of them seems to be scared or intimidated.   The mannequin was put under the sleeping tree of the group, which is ~6 m above ground. At 06:58 an alarm call was heard but the caller could not be identified due to height and obstructing foliage. Then, all individuals descend at a height of ~5 m and move in the opposite direction to the dummy and finally cross the path. Only the adult male stops briefly (5 s) to observe the dummy in a defensive position, arching his back and showing piloerection.