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

Abstract

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.

Noise intensity modulates the responses of mantled howler monkeys to anthropophony

“…Owls (California spotted owls, Strix occidentalis ; Mexican spotted owls, Strix occidentalis lucida ), for instance, do not show significant behavioral changes nor increases in physiological stress following playbacks of chainsaw noise at <60 dB (Delaney et al, 1999; Tempel & Gutiérrez, 2003), a contrast that could result from differences in auditory perception between birds and primates (Ball & Balthazart, 2021; Weisman et al, 2014). However, pygmy marmoset behavior is also not influenced by the intensity of simulated human speech (played back at 30, 60, and 78 dB: Sheehan & Papworth, 2019) and in Bolivian gray titi monkeys, from a total of eight response variables (including fGCM and social proximity), only time spent moving was negatively associated with noise intensity (Hernani Lineros et al, 2020). Considering that mantled howler monkeys have enhanced auditory sensitivity at lower frequencies compared to other primate species (Ramsier et al, 2019), they may be particularly susceptible to anthropogenic noise, which is typically low‐frequency (Barber et al, 2010; Francis et al, 2009).…”

“…First, at noisier locations black‐tufted marmosets ( Callithrix penicillata ) and black‐fronted titi monkeys ( Callicebus nigrifrons ) change the acoustics and temporal patterns of their vocalizations (Duarte et al, 2018; Santos et al, 2017). Second, black‐tufted marmosets, Bolivian gray titi monkeys ( Plecturocebus donacophilus ), and pygmy marmosets ( Cebuella pygmaea ) change their ranging behavior, by either avoiding or moving less in noisier areas (Duarte et al, 2011; Hernani Lineros et al, 2020; Sheehan & Papworth, 2019). Research in other animal groups suggests that these behavioral changes could impose fitness costs (e.g., Habib et al, 2006; Halfwerk et al, 2011; Kight & Swaddle, 2011), but the available evidence for primates neither informs on the physiological consequences of noise nor conveys information that can be used to design management actions aimed at increasing the welfare of individuals.…”

The influence of anthropogenic noise on the behavior of male mantled howler monkeys

“…Following Hernani Lineros et al (2020), we classified noise as: aerial traffic (aircrafts); human voice (normal conversation, laugh, loudspeaker, scream); recreation (firecracker, music, radio); tools/machinery (chainsaw, hammer, ladder, lawnmower, machete, sprinkler); traffic (boat, jet ski, horn, siren, vehicle); and unknown (when we could not identify the source of noise). We calculated rates of anthropogenic noise by dividing the number of recorded noises by sampling effort (in hours).…”

“…Nevertheless, our knowledge of the effects of anthropogenic noise on wild primates is scant. There is evidence that, in the presence of noise, primates: (i) change their vocalizations by calling less frequently (black tufted‐ear marmosets, Callithrix penicillata ; black‐fronted titi monkeys, Callicebus nigrifrons ; mantled howler monkeys, Alouatta palliata ), calling for longer (black tufted‐ear marmosets) or shorter (black‐fronted titi monkeys) periods, modifying the diel pattern of calling (black‐fronted titi monkeys), or by changing the acoustic attributes of vocalizations (black tufted‐ear marmosets) (Cañadas‐Santiago et al, 2020; Duarte et al, 2018; Santos et al, 2017); (ii) modify their movement patterns, by reducing (Bolivian gray titi monkeys, Plecturocebus donacophilus ) or increasing (mantled howler monkeys) time spent moving (Cañadas‐Santiago et al, 2020; Hernani Lineros et al, 2020), and by avoiding noise (black tufted‐ear marmosets: Duarte et al, 2011; pygmy marmosets, Cebuella pygmaea : Sheehan & Papworth, 2019); (iii) spend more time vigilant (mantled howler monkeys: Cañadas‐Santiago et al, 2020; pygmy marmosets: Sheehan & Papworth, 2019); (iv) spend less time resting and feeding (pygmy marmosets: Sheehan & Papworth, 2019); and (v) increase physiological stress levels (mantled howler monkeys: Cañadas‐Santiago et al, 2020; but see Hernani Lineros et al, 2020). Thus, all species examined to date respond to anthropogenic noise, although specific responses vary among taxa.…”

Pied tamarins change their vocal behavior in response to noise levels in the largest city in the Amazon

“…Nevertheless, such activity is also temporally structured, with animals calling more in the morning (Heymann, 1990;Norconk, 1990). Despite the importance of long calls to primate species, our knowledge of how, in the wild, their deployment is adjusted in response to anthropogenic noise, is limited (Duarte et al, 2011(Duarte et al, , 2018Gómez-Espinosa et al, 2022;Lineros et al, 2020;Santos et al, 2017).…”