Defining frontiers in mite and frog alkaloid research

Raspotnig et al. [1] comment on our recent finding of skin alkaloids in miniaturized Eleutherodactylus frogs from Cuba, which might be taken up from the high proportion of mites among their prey [2]. They provide a summary of current knowledge about alkaloid content and alkaloid sequestering in oribatid mites, which provides a valuable basis for developing future studies. According to their comment, in mites, ‘alkaloids are known to occur only in certain restricted taxonomic groups of the derived cohort Brachypylina; these include certain families in Oripodoidea (Scheloribatidae, Drymobatidae, Mochlozetidae) and possibly also Galumnoidea (Galumnidae)’ [1].

In our study, we flagged several mite taxa as possible alkaloid sources [2] but did not suggest that necessarily all of these contain alkaloids; instead, some of these taxa were contained in multi-taxon mite samples that had jointly been extracted and positively screened for alkaloids in a previous study done in Costa Rica and Panama by Saporito et al. [3]. Most of the mixed mite samples that tested positively for alkaloids in fact contained brachypilines of the Scheloribatidae, Drymobatidae, Mochlozetidae and Galumnidae, but some did not: for instance, sample ‘Cayo Nancy 2’ was composed of representatives of the Trhypochthoniidae, Tectocepheidae, Epactozetidae and Mesostigmata, and sample ‘Bastimentos 1’ consisted of Trhypochthoniidae and Hypochthoniidae [3]. We insist that it will be worth extending future alkaloid screening to mite species other than brachypilines, based on the following arguments: (i) the diversity of species in tropical environments is overwhelming and extremely understudied, and no doubt many new mite species and their unknown life and natural histories await discovery; (ii) if alkaloids have not yet been detected in a genus, family or higher taxon of Acari, this does not necessarily exclude their occurrence in this taxon, especially when current knowledge is typically based on screening of a few species. This is exemplified by our discovery of alkaloid sequestering in the frog Eleutherodactylus iberia, a member of a very diverse clade in which other species have tested negative for alkaloids [4]; and (iii) based on our own unpublished data (S. Schulz, work in progress), we are aware of at least one non-oribatid mite species containing alkaloids, which exemplifies how widespread this trait can be among diverse animal lineages.

If we are to understand how food intake regulates the alkaloid composition and thereby the unpalatability of frogs, the following mite-specific priority questions need to be addressed: (i) which species of leaf litter mites and other arthropods actually contain alkaloids? (ii) are mite alkaloids species-specific, do they occur in all individuals of a mite species, and is there geographical variation in alkaloid composition? (iii) do oribatid mites produce alkaloids themselves, or do they acquire them with their food (i.e. from uptaken bacteria or plant material), or are symbiotic micro-organisms involved? (iv) what is the function of the mite alkaloids—do mites use these alkaloids to deter predators? (v) do mite individuals contain or produce predominantly or exclusively single alkaloid compounds, or a cocktail of various compounds? and (vi) do alkaloid-containing mites have different natural histories compared with their non-alkaloid-containing relatives?

Given that oribatid mites feed on decaying matter rather than being host-specific phytophages, it is unlikely that they ingest their alkaloids from consumed plants, and it is possible that they produce them de novo. Because these animals are not often brightly coloured, it is also unlikely that their alkaloids exclusively serve to deter visually oriented predators, as in such a case evolution of aposematic colour is to be expected. However, surprising scientific discoveries are not uncommon in biodiversity research and are also to be expected from studies into mite alkaloid production and function. From a herpetological point of view, it would be rewarding to ascertain if geographical variation in species composition and alkaloid content of mite communities is correlated with variation in alkaloid content and coloration of mite-eating frogs. Studying these questions in more detail will be an important step towards a better understanding of the mechanisms of alkaloid production and transfer in complex tropical food webs, and of their ecological relevance.