Introduction
Acoustic communication is widely used by animals to transmit information
through sounds. These sounds are produced by an emitter (source) and are
propagated in the environment, causing some response in the receivers
(Kime, 2000; Wells, 2000). In environments where acoustic signals
propagate, transmission can be hampered by other different sounds,
causing stress, irritability, reduced fitness, in addition to being
associated with other risk situations (Grenat et al., 2019; Leon et al.,
2019; Troianowski et al., 2017). There are three main types of sound
noise that interfere with the transmission and detection of the species’
acoustic signal: abiotic (environmental), such as the presence of winds,
rains, streams and ocean tides (Caldart et al., 2016); biotic, produced
by intra and interspecific individuals that can form dense social groups
(Lengagne, 2008); and anthropic, which are related to acoustic pollution
caused by humans, such as the flow of automobiles on highways, civil
construction machinery, air transport, ships and boats (Cunnington &
Fahrig, 2010, 2013). The interference caused by these noises can
negatively influence the fitness of individuals, and consequently affect
populations and communities (Hanna et al., 2014; Hoskin & Goosem,
2016). Over the last few decades, there has been an increase in studies
on the effects of noise on the acoustic communication of organisms
(Gomes et al., 2022; Grenat et al., 2019). One of the groups of animals
most affected by human noise are anuran amphibians, which use acoustic
signals as their main form of communication (Gomes et al., 2022; Wells,
2007).
During the breeding period, most anurans form dense aggregations in
water bodies (Wells, 2007). Communication between frogs occurs mainly
through the emission of different types of vocalizations (Toledo et al.,
2015), however, the most emitted acoustic signal is the advertisement
call, which has the main function of attracting reproductive partners
and delimiting territories (Guerra et al., 2018; Toledo et al., 2015;
Wells, 2007). The calls of conspecific individuals (and also of other
species) can represent biotic sound noises that interfere in the local
acoustic space. Thus, males in vocalization activity must avoid the
overlapping of these acoustic signals (e.g., temporal and spectral
parameters) in some way (Bittencourt et al., 2016; Herrera-Montes &
Aide, 2011). Dense choruses of males in vocalizing activity may also
lead to limitations in the ability of females to choose reproductive
partners (Wollerman & Wiley, 2002).
In addition to biotic noises, more attention has recently been directed
to anthropic noises. This type of noise alters the conditions of the
acoustic environment of many habitats, creating new environmental
pressures that directly affect many animals that communicate
acoustically, including frogs (Barber et al., 2010; Desrochers &
Proulx, 2017; Knight & Swaddle, 2011; Sabah et al., 2017), birds
(Bermúdez-Cuamatzin et al., 2009; Herrera-Montes & Aide, 2011;
Slabbekoorn & Ripmeester, 2008) and marine mammals (Melcón et al.,
2012; Moore & Clarke, 2002; Stocker, 2002). Among the anthropic noises,
highways are considered the biggest source of noise pollution, producing
sounds with high energies concentrated in low frequencies (<5
kHz) (Warren et al., 2006). The urban expansion, and consequently the
road network, not only decreases the availability of habitats but also
increases the amount of human noise, causing negative effects on the
transmission and reception of sound between conspecifics (Bittencourt et
al., 2016; Sun & Narins, 2005), and may even reduce the chances of
survival of individuals (Gomes et al., 2022; Herrera-Montes & Aide,
2011). However, the species show several solutions to solve the problems
in the communication limitation imposed by the noises, such as, changing
the temporal and spectral acoustic parameters of the calls to reduce the
noise masking effect (Cunnington & Fahrig, 2010, 2013; Grenat et al.,
2019).
Among the strategies used by anurans to reduce or avoid the overlap
between biotic and anthropic noises on their calls, there are changes in
amplitude (Halfwerk et al., 2016; Parris et al., 2009; Yi & Sheridan,
2019), frequency (Caorsi et al., 2017; Cunnington & Fahrig, 2010),
duration (Zhao et al., 2021) and emission rate (Hanna et al., 2014;
Kaiser & Hammers, 2009; Legett et al., 2020). These changes can be
advantageous when the individuals are under external influences, since
the acoustic signals indicate the physical condition of the individuals.
Therefore, they must be transmitted in the best possible way in the
environment (Cunnington & Fahrig, 2010; Kime, 2000), just as the
acoustic adaptation hypothesis predicts (Goutte et al., 2018; Morton,
1975). Thus, changes in parameters of the call may indicate an
adaptation in response to noise, but they may generate additional
fitness costs, negatively affecting survival and reproductive success
(Herrera-Montes & Aide, 2011). It is often difficult to find evidence
that suggests that changes in the calls of individuals observed in
nature are caused by a single factor (Grenat et al., 2019), as
variations and/or adjustments in acoustic parameters can be influenced
by the environment (abiotic factors; (Kime et al., 2000)), size of
choirs (social factors; (Gambale & Bastos, 2014; Morais et al., 2012))
and/or level of human noise (Caorsi et al., 2017). Therefore, there may
be confounding factors when trying to explain changes in behavior if the
study does not consider the multiple biological and environmental
aspects to which individuals are exposed.
Biotic factors (body size, weight, predation and abundance of males in
vocalization activity) and abiotic factors (temperature, humidity and
vegetation heterogeneity) influence the anurans vocalizations in
different ways. For example, body size influences the spectral structure
(frequency) of the call, so that larger individuals present calls with
lower frequencies (Kohler et al., 2017). Thus, acoustic signals provide
reliable information about male body size (Bastos et al., 2011; Morais
et al., 2012). The number of individuals in the chorus influences the
intensity of the call as males increase sound pressure to promote
greater attractiveness (Bastos & Haddad, 2002; Morais et al., 2012). As
frogs are ectothermic animals, temperature influences the metabolic
rate, reflecting changes in the temporal parameters of calls, such as
duration and emission rate (Bastos & Haddad, 2002; Furtado et al.,
2016). All these aspects must be considered in bioacoustics studies to
avoid bias in the interpretation of results.
Since human activities have impacted the behavior of amphibians in
different ways, in this work we evaluated whether the call of a Yellow
Heart-tongued Frog species is affected by noise pollution produced by
car traffic on highways and by the noise of conspecifics in the chorus.
We hypothesized that (1) males exposed to anthropic noise (road traffic)
will present a higher dominant frequency of the advertisement call to
decrease or avoid signal masking, and that (2) males that vocalize in
conspecific choruses with higher density of individuals will present
higher values in the temporal parameters of the call (e.g., longer call
duration and intensity) to increase the efficiency in signal
transmission (and reduce or avoid overlapping of the call) in the
environment. For this, we compared the acoustic parameters of
advertisement calls of males of Phyllodytes luteolus(Wied-Neuwied, 1821) from natural and urban environments, and in the
presence of loud and quiet choruses. Phyllodytes luteolus is an
excellent model organism to test these hypotheses because it is a common
species, forms reproductive choruses, uses acoustic signals as the main
form of communication and is found in bromeliads in natural and urban
environments (Forti et al., 2017; Salles & Silva-Soares, 2010).