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.

中文翻译：

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玻利维亚灰猴（Plecturocebus donacophilus）对人为噪声梯度的反应：行为和激素相关性

近几十年来，全球城市扩张和森林砍伐导致非人类灵长类动物迅速减少。然而，人们对这些动物能在多大程度上容忍道路交通和人类在其栖息地中出现的人为噪音知之甚少。我们在玻利维亚圣克鲁斯德拉谢拉 (Santa Cruz de la Sierra) 附近的一个促进生态旅游的公园中，研究了居住在距离繁忙高速公路越来越远的六个家庭群。我们绘制了群体运动图，对 titis 的行为进行了采样，从每个研究组中收集了粪便样本，并进行了实验，在这些实验中，我们使用了一个人体模型来模拟人类入侵他们的家园。我们假设暴露于更高水平的人为噪音和人类存在的山雀群对人体模型的反应较弱，并且与处于最少干扰区域的群相比，它们的粪便皮质醇浓度更高。声压测量和对 titis 家范围内声景的系统监测证实了噪声梯度的存在，最好通过均方根 (RMS) 和中值振幅 (M) 声学指数来表征；重要的是，人为噪声和人类存在共同变化。研究小组居住在小而重叠的家庭范围内，他们大部分时间都在休息，并优先使用较低的森​​林层进行旅行，并优先使用较高的森林层进行觅食。焦点采样分析表明，成对移动所花费的时间与噪声成反比，在 44 dB(A) 至 52 dB(A) 的最小声压梯度内发生的行为变化。然而，粪便样本的经验证的酶免疫测定检测到令人惊讶的低皮质醇浓度，与 RMS 和 M 指数中观察到的变化无关。最后，蒂蒂斯对人体模型的反应根据我们的预期而有所不同，与高速公路相比，远处人群的警报声更大。因此，我们的研究表明，通过对人类存在的习惯化，警报呼唤减少，并表明 titis 对人为噪音的适应能力几乎没有生理压力的证据。与在 RMS 和 M 指数中观察到的变化无关。最后，蒂蒂斯对人体模型的反应根据我们的预期而有所不同，与高速公路相比，远处人群的警报声更大。因此，我们的研究表明，通过对人类存在的习惯化，警报呼唤减少，并表明 titis 对人为噪音的适应能力几乎没有生理压力的证据。与在 RMS 和 M 指数中观察到的变化无关。最后，蒂蒂斯对人体模型的反应根据我们的预期而有所不同，与高速公路相比，远处人群的警报声更大。因此，我们的研究表明，通过对人类存在的习惯化，警报呼唤减少，并表明 titis 对人为噪音的适应能力几乎没有生理压力的证据。