Poison frogs, defensive alkaloids, and sleepless mice: critique of a toxicity bioassay

Weldon, Paul J.

doi:10.1007/s00049-017-0238-0

Cited by 16 publications

(10 citation statements)

References 28 publications

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“…No complete information exists about possibly differing toxicities of these peptides on a predator, except about the lethal dose (LD) for mice by intra-peritoneal injection: LD 50 ≈ 10 mg pergidin/kg, and 2 mg lophyrotomin/kg 35 , 94 . Such toxicity tests clearly do not reflect natural predatory-prey interactions 95 . We cannot exclude that the two compounds strongly differ in their feeding deterrence and/or toxicity, knowing however that these hepta- and octapeptides are closely related 35 , 36 .…”

Section: Methodsmentioning

confidence: 99%

Endogenous toxins and the coupling of gregariousness to conspicuousness in Argidae and Pergidae sawflies

Boevé

Nyman

Shinohara

et al. 2018

Sci Rep

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Phytophagous insects tend to be either cryptic and solitary, or brightly colored and gregarious, as a defense against vertebrate predators. Here, we tested whether potent defensive chemicals produced de novo by larvae of Argidae and Pergidae sawflies have influenced the evolutionary relationship between larval appearance and levels of gregariousness. Phylogeny-based correlation analyses indicated only a weak trend for solitary species to be cryptic, and for gregarious ones to be conspicuous. Numerous Argidae were cryptic–solitary or conspicuous–gregarious, whereas most Pergidae were conspicuous–gregarious. Both families also included not truly gregarious but aggregated species, i.e. with individuals more evenly distributed on the host plant. By considering two specific morphological traits, predominant body coloration and contrasting spots on body, each one was (weakly) associated with appearance but none with gregariousness, which reflects the functional relevance of appearance as a whole. Furthermore, Argidae can display alternate appearances during successive larval instars. Finally, an independent contrasts test showed no obvious correlation between two major toxic peptides. Our results point towards diversely combined patterns of linked ecological traits in these insects. By assuming that warning coloration is more warranted against vertebrate than invertebrate predators, we suggest that the occurrence itself of toxins allowed this diversity via differing predator guilds and environmental factors, to which these insects were confronted during evolution.

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Section: Methodsmentioning

confidence: 99%

Endogenous toxins and the coupling of gregariousness to conspicuousness in Argidae and Pergidae sawflies

Boevé

Nyman

Shinohara

et al. 2018

Sci Rep

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“…Mice are the standard test subjects in many toxicity studies because they are believed to be a good proxy for humans, but, given that mice are not considered a potential natural predator or closely related to any potential predator of poison frogs and defensive secretions are ingested, not injected, the ecological or evolutionary relevance of the effects of these injections on mice is unclear (for further discussion, see Bolton et al. ; Weldon ). That is, injection of skin secretions might be highly toxic to mice while ingestion might have little or no effect on potential avian, snake, or arthropod predators, or they might have no effect on mice, but be extremely effective at inhibiting pathogens across a broad spectrum.…”

mentioning

confidence: 99%

Comment on Amézquita et al. (2017) “Conspicuousness, color resemblance, and toxicity in geographically diverging mimicry: The pan-Amazonian frogAllobates femoralis”

Saporito

Grant

2018

Evolution

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Amézquita et al. (2017) recently concluded that species of the Allobates femoralis group are toxic to mice at levels equivalent to syntopic alkaloid-containing poison frogs, which they attributed to the presence of alkaloids in skin secretions. However, the chemical composition of skin secretions was not analyzed, and here we present additional data supporting the absence of alkaloids in skin secretions of the Allobates femoralis group. Instead, we suggest the observed toxicity was caused by the anesthetic benzocaine, which was applied to the buccal cavity to euthanize frogs prior to skin removal. We show that orally administered benzocaine is rapidly incorporated into the skin of species that sequester and do not sequester alkaloids, which casts doubt on the conclusion that Allobates femoralis group skin secretions are toxic and makes the results of experiments with alkaloid-containing species of Adelphobates and Ameerega uninterpretable. To prevent experimental errors and misinterpretations in studies of amphibian chemical defense, we encourage researchers to test the chemical composition of samples prior to experimentation, include all necessary controls to detect false positives, conduct small pilot studies for new methods, and consider the limitations of particular methods and their ability to address the intended research questions.

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“…Researchers are beginning to work on unpalatability assays of anuran toxins in invertebrates (34–36), but our unpalatability assay provides a practical assessment of distastefulness, as opposed to toxicity (33), of anuran alkaloids in avian predators in a controlled manner, without having to use live frogs (33, 37). While informative, toxicity assays do not give an evolutionary context to defensive compounds as predators experience these alkaloids through taste, not via toxicity effects in the bloodstream (38). Experiments with live frogs, on the other hand, do not account for interindividual or interpopulational differences in toxin profiles (as sampling complete alkaloid profiles is not possible with live frogs) or alkaloid amount, which we have found not to relate directly to unpalatability.…”

Section: Discussionmentioning

confidence: 99%

Weak warning signals can persist in the absence of gene flow

Lawrence

Rojas

Fouquet

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Aposematic organisms couple conspicuous warning signals with a secondary defense to deter predators from attacking. Novel signals of aposematic prey are expected to be selected against due to positive frequency-dependent selection. How, then, can novel phenotypes persist after they arise, and why do so many aposematic species exhibit intrapopulation signal variability? Using a polytypic poison frog (Dendrobates tinctorius), we explored the forces of selection on variable aposematic signals using 2 phenotypically distinct (white, yellow) populations. Contrary to expectations, local phenotype was not always better protected compared to novel phenotypes in either population; in the white population, the novel phenotype evoked greater avoidance in natural predators. Despite having a lower quantity of alkaloids, the skin extracts from yellow frogs provoked higher aversive reactions by birds than white frogs in the laboratory, although both populations differed from controls. Similarly, predators learned to avoid the yellow signal faster than the white signal, and generalized their learned avoidance of yellow but not white. We propose that signals that are easily learned and broadly generalized can protect rare, novel signals, and weak warning signals (i.e., signals with poor efficacy and/or poor defense) can persist when gene flow among populations, as in this case, is limited. This provides a mechanism for the persistence of intrapopulation aposematic variation, a likely precursor to polytypism and driver of speciation.

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Poison frogs, defensive alkaloids, and sleepless mice: critique of a toxicity bioassay

Cited by 16 publications

References 28 publications

Endogenous toxins and the coupling of gregariousness to conspicuousness in Argidae and Pergidae sawflies

Endogenous toxins and the coupling of gregariousness to conspicuousness in Argidae and Pergidae sawflies

Comment on Amézquita et al. (2017) “Conspicuousness, color resemblance, and toxicity in geographically diverging mimicry: The pan-Amazonian frogAllobates femoralis”

Weak warning signals can persist in the absence of gene flow

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