Dietary Alkaloid Sequestration in a Poison Frog: An Experimental Test of Alkaloid Uptake in Melanophryniscus stelzneri (Bufonidae)

Abstract

Several lineages of brightly colored anurans independently evolved the ability to secrete alkaloid-containing defensive chemicals from granular glands in the skin. These species, collectively referred to as 'poison frogs,' form a polyphyletic assemblage that includes some species of Dendrobatidae, Mantellidae, Myobatrachidae, Bufonidae, and Eleutherodactylidae. The ability to sequester alkaloids from dietary arthropods has been demonstrated experimentally in most poison frog lineages but not in bufonid or eleutherodactylid poison frogs. As with other poison frogs, species of the genus Melanophryniscus (Bufonidae) consume large numbers of mites and ants, suggesting they might also sequester defensive alkaloids from dietary sources. To test this hypothesis, fruit flies dusted with alkaloid/nutritional supplement powder were fed to individual Melanophryniscus stelzneri in two experiments. In the first experiment, the alkaloids 5,8-disubstituted indolizidine 235B' and decahydroquinoline were administered to three individuals for 104 days. In the second experiment, the alkaloids 3,5-disubstituted indolizidine 239Q and decahydroquinoline were given to three frogs for 153 days. Control frogs were fed fruit flies dusted only with nutritional supplement. Gas chromatography/mass spectrometry analyses revealed that skin secretions of all experimental frogs contained alkaloids, whereas those of all control frogs lacked alkaloids. Uptake of decahydroquinoline was greater than uptake of 5,8-disubstituted indolizidine, and uptake of 3,5-disubstituted indolizidine was greater than uptake of decahydroquinoline, suggesting greater uptake efficiency of certain alkaloids. Frogs in the second experiment accumulated a greater amount of alkaloid, which corresponds to the longer duration and greater number of alkaloid-dusted fruit flies that were consumed. These findings provide the first experimental evidence that bufonid poison frogs sequester alkaloid-based defenses from dietary sources.

Ant and Mite Diversity Drives Toxin Variation in the Little Devil Poison Frog

“…Some defended organisms produce their own chemical defenses, while others sequester toxins from external sources (Casewell et al 2013;Olivera et al 1985;Saporito et al 2009Saporito et al , 2012. An example of toxin sequestration among vertebrates is poison frogs, which accumulate alkaloid toxins from arthropod prey (Daly et al 1994a, b;Hantak et al 2013;Saporito et al 2009). Compared to invertebrates, far less is known about how vertebrate species acquire chemical defenses from external sources.…”

Morphological and transcriptomic analyses reveal three discrete primary stages of postembryonic development in the common fire salamander, Salamandra salamandra

“…These salamanders are able to biosynthesize their own steroidal alkaloids, such as samandarine and samandarone (Habermehl & Haaf, ; Schöpf, ; Vences et al., ). This separates them from poison frogs whose alkaloids are largely of exogenous origin (Daly et al., ; Daly, Garraffo, Hall, & Cover, ; Hantak et al., ; Smith et al., ) and from tetrodotoxin‐containing salamanders and frogs, where the origin of these toxin is still not clear (e.g., Kudo et al, , Yotsu‐Yamashita, Toennes, & Mebs, ). Other amphibians (e.g., common toads) are known to synthesize steroidal toxins (bufadienolides, non‐alkaloids) which, like salamander alkaloids, are also derivatives of cholesterol (Garraffo and Gross, ; Habermehl & Haaf, ).…”

Taxonomic distribution of defensive alkaloids in Nearctic oribatid mites (Acari, Oribatida)

“…Composed of five independent evolutionary lineages, poison frogs are recognized by a shared ability to sequester defensive alkaloids from dietary arthropods, including ants, beetles, millipedes and, most recently discovered, oribatid mites (Saporito et al 2009(Saporito et al , 2012Hantak et al 2013). These frog lineages include certain dendrobatids from Central and South America, bufonids from South America (Melanophryniscus), mantellids from Madagasgcar, myobatrachids from Australia (Pseudophryne) and, most recently, miniaturized eleutherodactylid frogs from Cuba ).…”