Suffering in receivers: Negative effects of noise persist regardless of experience in female anurans

Abstract

Anthropogenic noise is widespread, and growing evidence suggests that it can negatively affect animals through many different mechanisms including masking of cues and signals, distraction, and aversion to noise. Acoustic masking has received the most attention from researchers and recent evidence suggests that masking effects can be mitigated by alteration of signal frequencies or amplitudes by signalers. Additionally, alteration can be a learned response via prior experience with noise exposure. However, it remains unclear whether distraction or aversive effects due to noise can be mitigated by prior experience with noise, especially among signal receivers. Here, we addressed this gap by separating mechanisms of noise disturbances on female phonotaxis towards male advertisement calls in anurans. To do this, we experimentally examined phonotaxis of gravid females that differ in their prior experience with noise under three acoustic manipulations: spectrally overlapping and non‐overlapping noise that either mask or do not mask male advertisement calls respectively, plus a silent control. We confirm two experience‐dependent responses of noisy‐site individuals relative to quiet‐site individuals: faster initiation of phonotaxis under non‐overlapping noise and a stronger aversive response against overlapping noise. However, we showed that, for both noisy‐ versus quiet‐site individuals, both overlapping and non‐overlapping noise treatments resulted in delayed initiation and disorientation of phonotaxis relative to silent control treatments. Our study provides the first evidence to demonstrate that, although prior experience appears to mitigate the negative effects of distraction or aversion to noise, prior experience falls short of fully compensating for disrupted orientation through phonotaxis. Additionally, although most studies have emphasized masking of biologically relevant cues and signals as the most prominent mechanism by which noise negatively affects wild organisms, we show that non‐overlapping noise, which cannot cause signal and cue masking, can have negative consequences via distraction or aversive responses. This finding suggests that noise impacts could extend well beyond contexts involving acoustic cue detection and discrimination and deserves increased attention by researchers. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13130/suppinfo is available for this article.

Why does noise reduce response to alarm calls? Experimental assessment of masking, distraction and greater vigilance in wild birds

“…Acoustic masking predicts that birds will flee to alarm calls during Non‐overlapping noise but not during Overlapping noise, while distraction implies a reduced response during either type of noise, compared to alarm calls alone, because both noise playbacks were of the same amplitude and lie well within avian hearing (Dooling, ). A similar logic has been used to discriminate the effects of masking and distraction on the foraging performance of bats in the presence of noise (Luo et al, ), and female frogs responding to male mating calls (Senzaki et al, ). A reduced response specifically during Overlapping noise could, however, also arise if birds were more vigilant during Overlapping noise, and so were aware that no predator was nearby and were therefore less likely to flee (Morris‐Drake et al, ).…”

“…However, understanding mechanisms is important because it can help predict effects of noise and suggest methods to ameliorate these effects (Francis & Barber, ). For example, remediation aimed at reducing acoustic masking may not solve problems of distraction or aversion (Luo, Siemers, & Koselj, ; Senzaki, Kadoya, Francis, Ishiyama, & Nakamura, ). Here, we focus on the mechanisms by which environmental noise can affect response to acoustic signals and thereby compromise communication.…”

“…While auditory masking is often assumed to be the primary mechanism by which noise reduces the response to acoustic signals including alarm calls, other mechanisms, including receiver distraction or changes in vigilance, could have similar effects on response (Brumm & Slabbekoorn, 2005;Francis & Barber, 2013;Senzaki et al, 2018). Noise could distract receivers and so compromise responses to other sensory input (Chan & Blumstein, 2011;Chan et al, 2010).…”

Traffic noise differentially impacts call types in a Japanese treefrog (Buergeria japonica)

“…In addition, understanding how males vocally respond to traffic noise is only one half of the picture when studying anthropogenic noise and communication. As male frogs adjust calling behavior to overcome acoustic masking from noise, female choice experiments are also needed to examine the effectiveness of these strategies (e.g., Senzaki, Kadoya, Francis, Ishiyama, & Nakamura, ; Wollerman & Wiley, ). Studies, therefore, that aim to address the interaction between male responses to noise and female choice in noise across multiple call types would provide a more in‐depth understanding of the impacts of anthropogenic noise on anuran species.…”

“…The same species (H. arborea), however, did not change calling behavior when examined in a different study (Lukanov et al, 2014). Similarly, gray treefrogs (Hyla versicolor) decreased their calling rates in response to noise in one study (Cunnington & Fahrig, 2010), but not in another female choice experiments are also needed to examine the effectiveness of these strategies (e.g., Senzaki, Kadoya, Francis, Ishiyama, & Nakamura, 2018;Wollerman & Wiley, 2002). Studies, therefore, that aim to address the interaction between male responses to noise and female choice in noise across multiple call types would provide a more in-depth understanding of the impacts of anthropogenic noise on anuran species.…”