Differential responses of avian and mammalian predators to phenotypic variation in Australian Brood Frogs

PLOS ONE, Nov 2019

Anti-predator signaling is highly variable with numerous examples of species employing cryptic coloration to avoid detection or conspicuous coloration (often coupled with a secondary defense) to ensure detection and recollection. While the ends of this spectrum are clear in their function, how species use intermediate signals is less clear. Australian Brood Frogs (Pseudophryne) display conspicuous coloration on both their dorsum and venter. Coupled with the alkaloid toxins these frogs possess, this coloration may be aposematic, providing a protective warning signal to predators. We assessed predation rates of known and novel color patterns and found no difference for avian or mammalian predators. However, when Pseudophryne dorsal phenotypes were collectively compared to the high-contrast ventral phenotype of this genus, we found birds, but not mammals, attacked dorsal phenotypes significantly less frequently than the ventral phenotype. This study, importantly, shows a differential predator response to ventral coloration in this genus which has implications for the evolution of conspicuous signaling in Pseudophryne.

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Differential responses of avian and mammalian predators to phenotypic variation in Australian Brood Frogs

April Differential responses of avian and mammalian predators to phenotypic variation in Australian Brood Frogs J. P. Lawrence 0 1 Michael Mahony 1 Brice P. Noonan 0 1 0 University of Mississippi, Department of Biology, University, MS, United States of America, 2 University of Newcastle, School of Environmental and Life Sciences , Callaghan, NSW , Australia 1 Editor: Lesley Joy Rogers, University of New England , Australia , AUSTRALIA Anti-predator signaling is highly variable with numerous examples of species employing cryptic coloration to avoid detection or conspicuous coloration (often coupled with a secondary defense) to ensure detection and recollection. While the ends of this spectrum are clear in their function, how species use intermediate signals is less clear. Australian Brood Frogs (Pseudophryne) display conspicuous coloration on both their dorsum and venter. Coupled with the alkaloid toxins these frogs possess, this coloration may be aposematic, providing a protective warning signal to predators. We assessed predation rates of known and novel color patterns and found no difference for avian or mammalian predators. However, when Pseudophryne dorsal phenotypes were collectively compared to the high-contrast ventral phenotype of this genus, we found birds, but not mammals, attacked dorsal phenotypes significantly less frequently than the ventral phenotype. This study, importantly, shows a differential predator response to ventral coloration in this genus which has implications for the evolution of conspicuous signaling in Pseudophryne. - Data Availability Statement: All relevant data are within the paper and its supporting information files. Funding: This work was funded by the East Asia and Pacific Summer Institutes Fellowship program through the National Science Foundation grant no. OISE-1515149 to JPL (https://www.nsf.gov/pubs/ 2013/nsf13593/nsf13593.htm). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Introduction Phenotypic coloration and pattern in prey species often serves to evade or deter potential predators. These signals range from cryptic (i.e., background matching; [ 1 ]) to conspicuous (i.e., aposematism; [ 2 ]) with some signals serving both functions [ 3,4 ]. In some cases, how prey species utilize a phenotypic signal is easy to discern (i.e., cryptic coloration of many moths or conspicuous coloration of poison frogs), but in many cases, how signals are used is not clear [5]. Signal interpretation is dependent upon the observer and environmental conditions in which the signal is received. For example, there is experimental evidence that coloration in the Strawberry Poison Frog (Oophaga pumilio) is aposematic [ 6 ], however, when viewed by conspecifics, these colors can affect mate choice [ 7 ]. Even aposematism may be observer-specific as modeling has demonstrated that conspicuous signals to avian predators may not be conspicuous to other predators (i.e., crabs and snakes [ 8 ]). The duality of these signals can result in phenotypes that are complex, and perhaps not readily apparent as to how species use signals. Pseudophryne are small, terrestrial Australian frogs exhibiting dorsal coloration ranging from solid brown to brilliant yellow stripes on a black background (e.g., Fig 1A). As these frogs Competing interests: The authors have declared that no competing interests exist. possess distasteful alkaloid toxins [ 9,10 ], this coloration is thought to be aposematic [11]. However, some Pseudophryne species have little conspicuous coloration, often confined to inguinal flash marks. Research on Neotropical poison frogs (Dendrobatidae) suggests there may be an inverse relationship between toxicity and conspicuousness [ 12,13 ], and it is certainly possible that this may be true of Pseudophryne. Further complicating matters, however, is that all Pseudophryne have conspicuous blackand-white ventral patterns (Fig 1G). This coloration has also been hypothesized to function in an aposematic manner [ 11 ] as disturbed frogs are likely to freeze position and not right themselves if flipped upside down (pers. obs.). Unlike the Neotropics [ 6,14 ], mammals (e.g., marsupial predators such as quolls, possums, and Antechinus) may be important predators of these frogs that contribute to signal evolution. While dorsal yellows, reds, and oranges would be effective signals for birds which are sensitive to long wavelength colors [ 15,16 ], many Australian mammals have limited ability to perceive color [ 17 ], so high-contrast signals would likely be more effective at deterring predation. Alternatively, this black-and-white coloration could be disruptive, breaking up the shape of the frog [ 18 ]. We examined how predators in eastern Australia react to natural dorsal and ventral phenotypes both known and novel to the region. Material and methods This study was conducted in the Watagans Nat (...truncated)


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J. P. Lawrence, Michael Mahony, Brice P. Noonan. Differential responses of avian and mammalian predators to phenotypic variation in Australian Brood Frogs, PLOS ONE, 2018, Volume 13, Issue 4, DOI: 10.1371/journal.pone.0195446