Short Communication |
Corresponding author: Fillipe Pedroso-Santos ( fillipepedrosodossantos@gmail.com ) Academic editor: Eva Ringler
© 2021 Fillipe Pedroso-Santos, Carlos Eduardo Costa-Campos.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Pedroso-Santos F, Costa-Campos CE (2021) Anti-predator behaviour of Rhinella major (Müller and Hellmich 1936), with insights into the Rhinella granulosa group. Herpetozoa 34: 195-200. https://doi.org/10.3897/herpetozoa.34.e66909
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In anurans, the different types of anti-predator behaviour have been documented in isolation, but some species have shown synergistic strategies in different situations. The display of these types of behaviour may be related to the types of predators in the habitat, which boost defensive responses in their prey. However, most reports are mostly opportunistic and punctual observations, not systematic. Here, we report the occurrence of anti-predator behaviour in the toad Rhinella major (Müller and Hellmich 1936) (Amphibia, Anura, Bufonidae) in the face of different handling modes. Probably the disturbance caused by handling had elicited a predator deterrence response in the individual, causing it to rapidly exhibit such behaviour. These conditions are discussed along with an overview of anti-predator behaviour in species of the R. granulosa group and we re-interpreted these strategies for two species in the group.
anuran behaviour, Bufonidae, ethogram, gape-limited predator, handling
Several species of anuran amphibians have evolved different types of anti-predator behaviour synergistically with phylogenetic and morphological traits, for example, related to body size, colour patterns and toxin production. This selection is driven by a variety of vertebrate and invertebrate predators that prey on amphibians (
The different types of anti-predator behaviour have been documented in isolation (see
Currently, the defensive types of behaviour of Rhinella major (Müller and Hellmich 1936) have been reported, informally, from observations of two predatory events. First, the lung inflation (referred to as “puffing up the body”) and secretory products of skin glands (adhesive) were reported by
The Rhinella granulosa group is comprised of small and medium-sized morphologically distinct toads, characterised by heavily ossified skulls, keratinised cephalic crests and keratinised tubercles of varying sizes on the body (
R. major is a terrestrial species of moderate size (Snout-vent length 35.8–72.8 mm in adult males and 33.9–81.1 mm in adult females), distributed in the Chaco Region of Argentina, Paraguay and Bolivia and in open areas along the Rivers Madeira, Beni, Amazonas, Tapajos and Xingu in Brazil (
We conducted field observations at night from 1900 h to 2200 h, between August 2018 and July 2019, in urban areas in the Municipalities of Macapá (0.0083°S, 51.0953°W, datum WGS84) and Santana (0.03589°S, 51.16077°W, datum WGS84), in Amapá State, Brazil. The field observations were performed once a week by a researcher, totalling a sampling effort of 144 hours/man. The areas sampled are characterised by abandoned properties and lots, with open environments and temporary lentic water bodies and an equatorial climate with annual precipitation of 2850 mm and average annual temperatures ranging from 27.6–38.0 °C (
Types of anti-predator behaviour of Rhinella major were observed during cautious approach and during and after the manual capture close to the substrate (the toads were lifted approximately 20 cm from the substrate). One of us (FPS) approached the frogs and, after 5 min of observations, handled them simulating a predator attack. Each individual was handled only once in different and random ways, with handling lasting approximately 10 min. The individuals were subjected to only one of the following modes of handling: grabbing them on the dorsum/dorsolateral, by the inguinal and cloacal regions, by the head and by the limbs. For each mode of handling, a repetition of 10 times of use was considered. Combinations of handling types and the selection of their use were not considered in this study to avoid confounding toad responses. Individuals who exhibited a posture resembling a dead organism, with their ventral region turned upwards on the hand or when placed on the substrate and with their limbs held close to body or relaxed were recorded as death-feigning. Likewise, individuals who inflated themselves were recorded as body inflation and those who displayed full or partial extension of the fore- or hind limbs were recorded as stretching of limbs. All terms used to define these types of behaviour followed
This study was conducted with all due ethical procedures and permission from the Brazilian wildlife regulatory service (SISBIO #48102).
Of 65 sampled individuals, the percentage of toads displaying potential anti-predator behaviour was 67.70% (n = 44). The most frequently observed behaviour for R. major that appeared in isolation was either death feigning (55.88%, n = 19, Fig.
As for the way of handling individuals with the kind of behaviour displayed by them, only the handling by the limbs did not present any defensive response (100.0%, n = 15). Individuals handled by the head displayed only death feigning behaviour (50.0%, n = 3); three individuals (50.0%) did not display defensive responses. Those handled by the inguinal and cloacal regions displayed only body inflation behaviour (66.66%, n = 4); two individuals (33.34%) did not display defensive responses. We observed that defensive responses were more frequent and variable when individuals were handled by the dorsum/dorsolateral region; only one individual did not display any defensive responses (see Fig.
To our knowledge, the data presented here demonstrate the first formal record of anti-predator behaviour in R. major. Yet, we do not know if these types of behaviour are effective against its natural predators. However, we expect this species to employ the same behaviour already recorded for the R. granulosa group due to morphological and habitat similarities. The death feigning behaviour in synergy observed in R. major is similar to the report of R. pygmaea (referred to as “death feigning in isolation” by
In the genus Rhinella Fitzinger, 1826, death feigning is not formally described to occur in synergy with body inflation (see
Anti-predator defences of species in the Rhinella granulosa group. * Re-interpreted behaviour.
Species | Anti-predator defences | Reference |
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Rhinella major | Skin secretion |
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Skin secretion in synergy with Body inflation |
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Death feigning | This study | |
Body inflation | This study | |
Death feigning in synergy with Body inflation | This study | |
Body inflation in synergy with Stretching of limbs | This study | |
Rhinella granulosa | Body inflation in synergy with Stretching of limbs* |
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Body inflation |
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Rhinella pygmaea | Death feigning in synergy with Body inflation* |
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Body inflation in synergy with Stretching of limbs* |
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Rhinella humboldti | Skin secretion in synergy with Body inflation |
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Although body inflation behaviour is a recognised defensive strategy of anurans against predation attempts by snakes (
Regarding the modes of handling used in our study with the kind of behaviour displayed by the individuals, it is most likely that the disturbance caused by handling had elicited a predator deterrence response in the individual, causing it to rapidly exhibit such behaviour. Therefore, this condition would be better related to the learning of avoidance of detection and subjugation in the condition as prey. Thus, we suggest that body inflation behaviour, displayed when grasped by the inguinal and cloacal regions, may have been a developed mechanism for individuals of R. major for defence against a gape-limited predators, such as snakes, because such behaviour would make the process of subjugation or swallowing difficult. Even though some vertebrates (e.g. snakes and lizards) tend to prey on toads through headfirst ingestion, a low frequency of this mode of ingestion can be recorded for some lineages (see
Furthermore, we did not observe escape behaviour in R. major during our study. In fact, species of the genus Rhinella are relatively heavy and escape behaviour can be an inefficient alternative when it comes to highly mobile predators. Additionally, cryptic species may increase the likelihood of being detected if they escape (
As a final comment, although cryptic patterns were not the focus of this study, we reiterate that further studies are needed to evaluate the importance of selective pressure on phenotypic divergence amongst populations of R. major. This species, like the others in the group, can confuse predators guided only by vision because the dorsal cryptic pattern is similar to the complex background of its habitats. Therefore, our observations may support investigations of this nature. In addition, we encourage the necessity of experimental studies involving video traps to better evaluate the importance of defensive responses for prey detection and avoidance learning can be evaluated for different predator taxa.
We are grateful to Daniela C. Rößler for proofreading and for valuable comments on the earlier draft of the manuscript and the two anonymous reviewers who kindly reviewed and provided cordial criticisms to our work. FPS received a fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) during this study (process 134760/2018-2).