dart frog study 4
Arthropod Sources of Alkaloids
Many of the alkaloids sequestered in the skins of frogs appear to be obtained in their diet from arthropod sources. Six of the twenty classes of alkaloids detected in Dendrobatid frogs have been found in Myrmicine ants, with the highest number occurring in the genus Solenopsis (Diplorhoptrum) (Jones et al., 1999). The classes thus far detected in Myrmicine ants and Dendrobatid frogs are 2,5-dialkylpyrrolidines, 2,6-dialkylpiperidines, 3,5-dialkylpyrrolizidines, 3,5-dialkylindolizidines, 4,6-dialkylquinolizidines, and 2,5-dialkyldecahydroquinolines (Daly et al., 2000). A total of 18 individual compounds have been detected in both groups from these six classes (Daly et al., 2000). Alkaloid 195C and two decahydroquinolines have been found in a Brazilian Solenopsis (Diplorhoptrum) species and in the same proportions in Mantella betsileo. The discovery of three alkaloids in the same proportions in an ant and in frogs strongly suggests a dietary source for these and related compound in frog skin(Jones et al., 1999). Decahydroquinoline cis-195A has been found in Solenopsis (Diplorhoptrum) species and also in Dendrobatid and Mantella species (Jones et al.,1999). The 4,6-disubstituted quinolizidine, 195C, occurs in Dendrobatids from Panama, Costa Rica, Venezuela, Colombia, Peru, Brazil, and Ecuador and in the Madagascan Mantellas. This compound is identical to a quinolizidine found in a Solenopsis (Diplorhoptrum) species from Brazil. The only other occurrence of 4,6-disubstituted quinolizidines in nature is the plant alkaloid porantherilidine (Jones et al., 1999).
The Myrmicine ant species Monomorium pharaonis produces significant amounts of two alkaloids: a 3,5-disubstituted indolizidine, named monomorine-I, and trans-2-heptyl-5-(5-hexenyl)pyrrolidine. The pyrrolidine occurs in much higher concentrations than the indolizidine. A 3,5-disubstituted indolizidine, 195B, has been detected in the skin of some frogs but is usually a different isomer than monomorine-I. When Monomorium pharaonis was fed to frogs for seven weeks, monomorine-I was accumulated in the skin but none of the pyrrolidine was detected (Daly et al., 1994).
A study was done in Panama on Dendrobates auratus raised in outdoor cages and fed with arthropods contained in leaf litter collected from the same site as the parents. Fourteen of the forty alkaloids that were found in the parents were found in the terrarium raised offspring. Pumiliotoxins, allopumiliotoxins and histrionicotoxins were absent from the terrarium raised frogs but were major alkaloids in the parents (Daly et al., 2000). Ants collected from the site were found to contain several of the alkaloids that were found in the frogs. This important study was the first to find the same alkaloids in sympatric species of frogs and arthropods (Daly et al., 2000).
Several alkaloids from arthropods other than ants have been detected in Dendrobatids. A spiropyrrolizidine and a spiropyrrolidine have been found in millipedes and frogs. Two of the fifteen tricyclic coccinelline alkaloids that have been detected in frogs have also been found in beetles (Daly et al., 2000).
Evolutionary Significance of Alkaloids in the Dendrobatidae and Convergently Evolved Taxa
Specialization for a diet consisting mainly of myrmicine ants and other minute prey is an adaptation shared by the seven genera of alkaloid containing frogs (Caldwell, 1996). Frogs in the genus Dendrobates, whose species contain alkaloids, contained from 50% to 73% ants upon stomach analyses whereas the nontoxic genus Colostethus was found to contain from 12% to 16% ants (Caldwell, 1996). This difference seems to be due to prey preference not merely small body size (Caldwell, 1996). It has been suggested that genetic disposal toward a certain type of prey might determine in which assemblages these frogs could occur rather than interactions within assemblages determining the type of prey taken (Caldwell, 1996). Some costs are involved in microphagous and myrmecophagous specialization including rejection of suitable prey, digestion of heavily chitinous and toxic prey, and constant foraging (Toft, 1995). Several derived traits seem to be shared by alkaloid containing frogs. These traits include microphagous specialization, myrmecophagous specialization, small body size, aposematic coloration, diurnal activity patterns, narrowing of the head and tongue, and decrease in number of maxillary and vomerine teeth (Vences et al., 1997/98). These traits were found to be correlated in comparisons with sister groups, with Mantidactylus as the sister group for Mantella and Colostethus as the sister group for the four alkaloid containing genera of Dendrobatids. The number of traits correlated with diet specialization suggest that foraging ecology could be the storngest driving force in the adaptive radiation of Dendrobatid and other alkaloid containing genera (Toft, 1995). Caldwell (1996) suggested a sequence of events leading to the radiation of toxic species. Diet specialization on toxic ants necessitates the detoxification of prey, especially by excretion through the skin. This would be strengthened by natural selection, if the excretions are toxic to predators, leading to the sequestering of alkaloid toxins in the skin. This would lead to selection for aposematic coloration and then diurnal activity. The end result being the radiation of species. This trend seems to have occurred separately in four groups of anurans: Dendrobatidae, Mantellinae, Pseudophryne, and Melanophryniscus (Vences et al., 1997/98).
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