The Swamp Orchestra: Acoustic Repertoire of Frogs

The Swamp Orchestra: Acoustic Repertoire of Frogs

Author: Iago Ferraz

Abstract: This paper discusses concepts related to bioacoustics within the behavior, ecology, and zoology of anuran amphibians: toads, tree frogs, and frogs. Conceptualizing terms associated with the complex dynamics of vocalizations of these animals that are linked to various behaviors directly or indirectly related to reproduction, the author also reports the results of six months of observation in a puddle in the Atlantic Forest region with observations that exemplify the study's subject matter.

Keywords: Bioacoustics, Anuran amphibians, Vocalizations, Breeding Behavior, Ethology, Frogs, Toads.

Introduction

One of the most fascinating aspects of anuran amphibians, commonly known as frogs, treefrogs, and toads, is that they do not simply exhibit indistinct and random vocalizations. Instead, each species possesses a repertoire of distinct calls, each used in different situations within the behavioral dynamics of the animal. This is an efficient form of communication and a crucial aspect of anurans' ethology and reproductive ecology. It also aids in taxonomy, as vocalizations can be a diagnostic characteristic in identifying and grouping species.

The classification of anuran calls varies in the literature, depending on the authorial perspective on which the work in question is based. Following the more conventional sense (sensu Duellman & Trueb, 1994), we can categorize the calls into announcement calls, reciprocity calls, release calls, and stress calls.

The present work will delve into bioacoustics in anuran amphibians, specifically relating it to the author's field observations and results in an Atlantic forest area in the state of Rio de Janeiro, Brazil.

The Calls

Undoubtedly, announcement calls are the most emblematic and crucial; these are the calls that males emit most of the time, often simultaneously, a behavior referred to as chorusing. The primary purpose of the announcement call is to serve as a mating song to attract females of the same species. However, it can also be a territorial vocalization, warning other males that a vigorous frog already occupies the territory. In both cases, the announcement call falls within courtship or breeding behavior, specifically exhibited by the males since only they are singers.

Although the general rule associates vocalization with males, in some species, a second type of call occurs, emitted by females in response to the male's announcement call when they are receptive to mating. This call is known as the reciprocity call.

The third classification of calls is the release call, an agonistic vocalization that frogs, especially males, emit when caught by other animals, our hands, or another male in an attempt at amplexus (anuran mating) between males. The signaling of the call serves as a release command.

Lastly, the stress call is a low-pitched vocalization produced by either sex, usually with an open mouth, in response to disturbance.

Despite the general classifications, they can further divide, once courtship, territorial, combat, mating, and breeding calls can vary significantly within the same species. 

The acoustic apparatus

To deal with such a diversity of calls, the vocal repertoires of their species, anurans are endowed with highly efficient characteristics. Their unique auditory system among animals captures vibrations from the substrate and sound from the air, with the aid of an efficient tympanic membrane (Figure 1), a middle ear or tympanic cavity, and an inner ear or labyrinthine membrane, which assists in balance. An anuran can detect rotations, gravity, and acceleration through the auditory apparatus. The tympanic membrane and the columella amplify sounds, and there is a high sensitivity in recognizing intraspecific sounds (Pough et al., 2014).

What makes vocalizations so diverse, whether within the same species (allowing differentiation of calls and their functions) or between different species (enabling species identification), is the multitude of structural forms that sound can take. 

Sometimes, the sound will be highly distinctive, and easily recognizable to the human ear, as is the case of Boana faber (Wied-Neuwied, 1821), where the announcement call sounds like the noise of a hammer hitting metal or wood. However, often, the call needs to be studied meticulously, in detail and transformed into graphics to visualize its characteristics. 

To achieve this, the following parameters are observed: call (the entire vocalization), call rate (frequency of call production), note (a sound unit), note repetition rate (frequency of note production), pulses (energy impulses in the temporal spectrum of the note), pulse rate (number of pulses per second or millisecond), spectral frequency (pitch of the call).

The generated graphs are called sonograms and oscillograms, which are visual representations of sound frequency over time or graphs showing the variation of sound amplitude over time, respectively.

Acoustic signals are generated by air from the lungs passing through the vocal cords and resonated by the vocal sac, which exists only in males (Pough et al., 2014). The efficiency of sound production can be influenced by various factors such as body size (typically, smaller animals vocalize at higher frequencies) and environmental parameters like temperature, humidity, and surrounding vegetation.

Some species have a single vocal sac (Figure 2.d), while others have a double vocal sac.

It is believed that there is a strong relationship between the environment and the variation in vocal sacs. For example, it has been observed that in species inhabiting bromeliads, the vocal sacs have been reduced, possibly due to the limited space (Norbertino, 2023).

Each species selects a vocalization site, which may be on the ground, at the water's edge, in vegetation, on rocks, among other possibilities. Species associated with noisy environments, such as waterfalls have developed an alternative mechanism to attract female attention, by using limb movements, a behavior known as visual signaling. For the species Hylodes nasus (Lichtenstein, 1823), for instance, a frog species associated with potentially noisy rivers, a repertoire of several visual signals have been observed (Apolinario et al 2021).

Figure 1: Tympana of Thoropa miliaris (Spix, 1824), Nyctimantis brunoi (Miranda-Ribeiro, 1920), and Rhinella ornata (Spix, 1824), respectively.

The other senses

Due to vocalizations, hearing is the most emblematic sense when studying the reproductive behaviors of these animals, but the other senses of anurans are also related to the whole process. The sense of smell in anurans, composed of nostrils and a vomeronasal organ, has chemoreceptive ability and aids in orientation and spatial location. 

Additionally, anurans have a broad field of vision and recognize different light wavelengths. Besides enabling the recognition of visual signals, such as courtship moves or body inflation (aggressive behavior among males), colors also serve as communication tools.

Anurans possess cells called chromatophores, which contain pigments. Xanthophores result in warm colors, such as red and yellow. Iridophores result in white and silver tones. Melanophores are endowed with melanin, which darkens the tones. The combination, absence, or presence of these pigments determine the colors of the animal. Regarding blue, and consequently its derivatives, like green, the origin is not these cellular pigments but rather a protein complex present in various parts of the body, not just in the skin. Pigmented cells have a certain plasticity and can alter the color of the animal, which occurs in response to environmental and hormonal changes. Regarding reproduction, in several species, the vocal sacs change color or become more pigmented during the reproductive period, indicating that besides singing, the color of the sac is also part of courtship behavior to attract the female.

Ecological interactions and reproductive success

Given that sound is such a crucial tool for the lifestyle of anurans, the acoustic space can be considered a resource, akin to water and food, and thus falls under the ecological laws of competition. If, within the same pond, during the same season and at the same intervals, multiple males from different species chorus simultaneously, a significant acoustic competition ensues. Competition represents a negative ecological relationship for both parties. Therefore, natural selection has often followed paths that reduce competition, and in the observations of this study, we can discern some strategies employed by the anurans in the observed area to mitigate competition.

Over six months of monitoring a pond, singer male activity was observed in every field night from the following species: Boana faber (Wied-Neuwied, 1821), Dendropsophus bipunctatus (Spix, 1824), Dendropsophus elegans (Wied-Neuwied, 1824), Leptodactylus latrans (Steffen, 1815) Phyllomedusa burmeisteri Boulenger, 1882.

All field nights occurred during rainy periods, suggesting that the species in question correlated their reproductive behavior with the rainy season or engaged in extended reproduction. The most striking strategy to avoid overlapping calls (observed acoustic space competition) was antiphony. Antiphony occurs when individuals sing synchronously, thereby avoiding the overlap of calls (Tandel et al., 2014). This was observed intraspecifically, where males of B. faber and L. latrans did not overlap their calls.

For B. faber, there was also a tendency not to overlap calls with other species. In 14 out of 18 choruses of B. faber, the species sang practically alone, during times when others were quieter.

The same was observed for P. burmeisteri. No chorus was observed, only isolated calls, but these also occurred when the activity of other species was lower.

In the case of D. elegans and D. bipunctatus, there was no tendency toward antiphony or waiting for a vacant acoustic niche; males sang vigorously even in intraspecific and interspecific overlap. Although this involves an energy expenditure, reproductive success is still ensured given the female's ability to finely recognize the call and differentiate it from that of her own species.

Reproductive success in the pond could be speculated by observing the following parameters: amplexus couples (D. bipunctatus and Boana semilineata (Spix, 1824)), tadpole encounters (B. faber, L. latrans, D. sp., and also Scinax sp.)), froglet encounters (D. elegans, L. latrans, and also Boana albomarginata (Spix, 1824)), and nest/eggs encounters (B. faber, L. latrans). No signs of reproductive success were found for P. burmeisteri; however, this species was considered challenging to observe, as its presence was only noted through calls and a single observation of a male in a tangle of vegetation.

The encounter of these signals shows that even while sharing the same puddle and partitioning resources, reproduction was somewhat successful between the species, highlighting how anurans are well adapted to cope with various challenges, particularly excelling in reproductive behaviors.

Species	Tadpoles	Couple in amplexus	Froglet	Nest/Eggs	Pond activity (Monitored species)
Boana albomarginata			X
Boana faber	X			X	X
Boana semilineata		X
Dendropsophus bipunctatus	?	X			X
Dendropsophus elegans	?		X		X
Dendropsophus sp.	X
Leptodactylus latrans	X		X	X	X
Phyllomedusa burmeisteri					X
Scinax sp.	X

Table 1: Indicators of reproductive activity and consequently, efficiency of vocalizations.

Figure 2: Some observed anurans: a. Boana faber b. Boana semilineata c. Boana albomarginata d-e. Dendropsophus bipunctatus f. Leptodactylus latrans.

During the six-month observation period from November 2023 to April 2024, the warm and rainy season in the Southern Hemisphere's seasonal cycle, all five target species (Boana faber, Dendropsophus bipunctatus, Dendropsophus elegans, Leptodactylus latrans, and Phyllomedusa burmeisteri) were recorded in activity in the same puddle and its surroundings every month.

Although an in-depth study of these dynamics, known as "community ecology studies," should be longer (generally at least one year), with environmental and behavioral parameters meticulously described and subjected to statistical analyses, the aim of these observations and their recording for this work was limited to providing practical examples of anuran vocalization behavior to support the topics addressed in this article.

It was also possible to observe a diversity of behaviors. The best-observed example was Dendropsophus bipunctatus vocalizing in vegetation at the edges of the puddle, at an average height of 60 ± cm, where they vocalize continuously with brief pauses to perform body rotations on their own axis. In contrast, Leptodactylus latrans were all observed vocalizing on the ground, with many intervals between calls and interrupting their singing upon noticing any movement or drastic change in the wind. Boana faber sings vigorously while hanging from bushes bordering the puddle with sturdier branches, as it is a heavier animal, and they demonstrate their chorus usually when other species are quieter, although there are moments of song overlap. Phyllomedusa burmeisteri did not form a chorus during the observation; that is, all males sang isolated from each other, in different spots and at different times.

Conclusion

Successfully, the previously observed results endorse the importance of bioacoustics for the reproduction of anuran amphibians and demonstrate how much natural selection and evolution have refined this behavior, allowing individuals of different species, with even dozens of singing males in each species, to share a single puddle and the same space of sound distribution. This is thanks to the female's ability to recognize the vibrations of her own species males due to the unique auditory system of anurans (Figure 1). Additionally, we emphasize the roles of male behaviors in this functioning, such as antiphony, the selection of vacant perches, and, if necessary, aggressive behaviors that expel less fit males from the area and reduce competition.

Furthermore, the widespread notion that anurans have the most varied reproductive modes among vertebrates can be observed in monitoring activities with these creatures. Just among the five target species of this study, there are at least four modes of oviposition: Boana faber constructs clay pools where amplexus and oviposition occur; Phyllomedusa burmeistere lays eggs on leaves which it subsequently folds into a case for the tadpoles to fall into the water when ready; Leptodactylus latrans creates a characteristic foam nest for egg deposition; the others follow the traditional method of ovipositing near or in a puddle.

In conclusion, we assert that puddles, swamps, and forests are true orchestras for anuran amphibians, which form their choruses with songs perfected by evolution over thousands of years and thus perpetuate their species, essential for maintaining the life we know due to the irreplaceable contribution of frogs, tree frogs, toads, and tadpoles in the food web, whether as predators or prey.

References                            

• Apolinario, J. S., Silva, S. P. C. E., & Santos, F. H. S. F. (2021). O complexo repertório de comunicação visual em Hyloides nasus (Amphibia: Anura: Hylodidae) e sua aplicação durante as interações sociais. Anais da Jornada Giulio Massarani de Iniciação Científica, Tecnológica, Artística e Cultural, Rio de Janeiro, RJ: UFRJ.

In their work, Apolinario and the other authors describe the complex repertoire of visual signals of Hyloides nasus and contextualize why visual communication is important in noisy environments.

• Duellman, W. E., & Trueb, L. (1994). Biology of Amphibians. JHU Press.

Duellman and Trueb are arguably the foremost figures in the field of amphibian biology, and this work serves as the primary reference for most scientists, students, and researchers in the field. It is a book that conceptualizes and provides explanations on various aspects of the biology, ecology, and behavior of anurans.

• Ferraz, I. (2024). Sistemática, morfologia, ecologia, comportamento e diversidade de anfíbios e répteis. UFRRJ.

In this general herpetology work, within the anurans topic, the author extensively describes how auditory, olfactory, and visual senses directly and indirectly influence the reproductive behavior and ecology of anurans.

• Frost, D. (2024). Amphibians of the World. American Museum of Natural History. https://amphibiansoftheworld.amnh.org/Amphibia/Anura/.

The largest and most up-to-date amphibian database in the world, which serves as a reference for species, showcasing their currently accepted nomenclature and associated works.

• Norbertino, K. N. (2023). Saco Vocal e Ambiente Reprodutivo. Herpeto Capixaba. Retrieved from https://www.herpetocapixaba.com.br/post/saco-vocal-e-ambiente-reprodutivo.

In this scientifically grounded publication from the renowned Brazilian group "HerpetoCapixaba," the author describes the differences in vocal sacs and exemplifies how the environment may have selected for these characteristics, information cited in this work.

• Pough, F. H., Heiser, J. B., & McFarland, W. N. (2014). A Vida dos Vertebrados. Atheneu.

This book is the most important current bibliography for general zoology studies regarding vertebrates, chordates, tetrapods, and so on, being the classic foundational bibliography for graduation zoology classes. It provides information and appropriate nomenclature for morphological and anatomical parts, descriptions of characteristics, and phylogenetic information about vertebrates, which includes anurans.

• Tandel,  M., Loibel, S., Oliveira, E., & Haddad, C. (2014). Diferenciação de 3 tipos de vocalizações (cantos) na espécie Brachycephalus pitanga. Revista da Estatística da Universidade Federal de Ouro Preto, 3(3), 374-386.

The work served as a reference to explain the concept and functioning of antiphony.

Observation - Please note that when citing scientific names, they are often followed by the name of an author, resembling a parenthetical*** reference, but in turn, it is not listed in the reference list. This occurs because they are not bibliographic references, but rather, the scientific name of the species includes its authorship reference. For example, although we use Felis catus as the scientific name for the domestic cat, the complete scientific name is Felis catus (Linnaeus, 1758). And academically, the full name must be written, at least the first time the species is mentioned.

***Not always parentheses are used, as in the case of Phyllomedusa burmeisteri Boulenger, 1882.