Scheloribatid Mites as the Source of Pumiliotoxins in Dendrobatid Frogs†

Abstract

The strawberry poison frog Dendrobates pumilio (Anura: Dendrobatidae) and related poison frogs contain a variety of dendrobatid alkaloids that are considered to be sequestered through the consumption of alkaloid-containing arthropods microsympatrically distributed in the habitat. In addition to ants, beetles, and millipedes, we found that adults of two species of oribatid mites belonging to the cohort Brachypylina, trophically a lower level of animal than ants and beetles, contain dendrobatid alkaloids. Gas chromatography/mass spectrometry (GC/MS) of hexane extracts of adult Scheloribates azumaensis (Oribatida: Acari) revealed the presence of not only pumiliotoxin 251D (8-hydroxy-8-methyl-6-(2'-methylhexylidene)-1-azabicyclo[4.3.0]nonane), but also precoccinelline 193C and another coccinelline-type alkaloid. From the corresponding extracts of an unidentified Scheloribates sp., pumiliotoxin 237A (8-hydroxy-8-methyl-6-(2'-methylpentylidene)-1-azabicyclo[4.3.0]nonane) was detected as a minor component, and identified by synthesis. The presence of related alkaloids, namely deoxypumiliotoxin 193H, a 6,8-diethyl-5-propenylindolizidine, and tentatively, a 1-ethyl-4-pentenynylquinolizidine, were indicated by the GC/MS fragmentation patterns, along with at least another six unidentified alkaloid components. Thus, one possible origin of pumiliotoxins, coccinellid alkaloids, and certain izidines found in poison frogs may be mites of the genus Scheloribates and perhaps related genera in the suborder Oribatida.

Oribatid mites as a major dietary source for alkaloids in poison frogs

“…Alkaloids have only recently been reported in mites, namely in two different species of scheloribatid mites cultured in Japan (12). Our study adds to these findings and illustrates that oribatid mites possess a tremendous diversity of alkaloids, many of which also occur in poison frogs and some that have not previously been reported in nature.…”

“…Precoccinelline is a well known alkaloid found in coccinellid beetles (9). Precoccinelline and another tricyclic alkaloid were recently reported from a Scheloribates species cultured in Japan (12). The most common tricyclic alkaloid in O. pumilio is 205B, which was not detected in any mite extract.…”

“…For example, the 5,8-I 207A was identified from two different mite samples on Isla Escudo, each of which contained mites from a different family (Scheloribatidae and Drymobatidae). Takada et al (12) reported that alkaloids in Scheloribates were adult-specific and not detectable in either the larval or nymphal instars, even though Only alkaloids that have been reported previously in poison frogs (6) Table 1). All contain branched carbon skeletons.…”

“…Their food generally consists of decaying higher plant material and saprophytic fungi (31,32), although stable isotope studies indicate that necrophagy or predation on small invertebrates is common, especially in tropical soils (32,33). Oribatid mites posses paired exocrine glands (34), called opisthonotal or oil glands, that secrete a wide range of organic compounds, including monoterpenes, sesquiterpenes, aromatics, aliphatic aldehydes, a ketone, fatty acids, fatty acid esters, an alkyl formate, and hydrocarbons (12,(35)(36)(37)(38)(39)(40)(41)(42). The functions of these compounds have been little studied but include alarm signals and chemical defenses (34,38).…”

“…For instance, scheloribatid mites from Isla Escudo ( indolizidines, three homopumiliotoxins, a pyrrolidine, and an unclassified alkaloid. Several classes of alkaloids have also been detected from two species of Scheloribates cultured in Japan (12). One species contained a pumiliotoxin and tricyclic alkaloids, and the other species contained a different pumiliotoxin, a deoxypumiliotoxin, a 5,6,8-I, and a 1,4-Q; four other alkaloids were detected but not identified (12).…”