Are 'herbivorous' tadpoles really microbe-eaters?

@tom-kirschey @saber_animal @amila_sumanapala @graytreefrog @danieleseglie @kaylyncullen @diogoprov @alexey_katz @sandboa

The free-swimming larvae of most frogs (class Amphibia, order Anura, https://en.wikipedia.org/wiki/Frog) worldwide are described as herbivorous. Whereas the adults eat animals (mainly invertebrates), the larvae of the same species of frogs are usually 'grazers'.

(So most naturalists might assume that any sentence combining ‘frogs’ and ‘microbes’ would probably refer to pathogens, particularly the recent epidemic of chytridiomycosis https://en.wikipedia.org/wiki/Chytridiomycosis. This infection, caused by the chytrid fungus Batrachochytrium dendrobatidis, has exterminated many species of amphibians.)

However, this view hardly stands up to scrutiny (see http://fwf.ag.utk.edu/mgray/wfs493/Altigetal2007.pdf and https://www.researchgate.net/publication/227600906_What_tadpoles_really_eat_Assessing_the_trophic_status_of_an_understudied_and_imperilled_group_of_consumers_in_freshwater_habitats).

The larvae (excluding those species in which the larval stage depends on yolk or egg-jelly laid down by the mother) of remarkably few species of frogs have ever been shown to be herbivorous or even omnivorous.

At least one species of frog in the family Dicroglossidae, namely Phrynoderma hexadactylum (https://www.inaturalist.org/taxa/1363721-Phrynoderma-hexadactylum), is known to eat leaves (e.g. those of Ceratophyllum demersum, https://www.inaturalist.org/taxa/60997-Ceratophyllum-demersum) as a staple in both the larval and mature stages. However, even this species has not been shown to be able to extract food energy from plant fibre (cellulose).

Furthermore, it has long been known that larval salamanders (https://en.wikipedia.org/wiki/Salamander) rely on small animals for food.

Therefore, a salient ecological pattern in amphibians is that extremely few species in this diverse class – living or extinct – are known to have specialised on a diet of green leaves (i.e. photosynthetic organs of the kingdom Plantae).

This distinction seems to have been overlooked because of confusion generated around the following points.

Firstly, algae have been called ‘plants’ despite belonging to a separate phylogenetic kingdom. Algae belong to the kingdom Protista (https://en.wikipedia.org/wiki/Protist), which includes both microbes and macrobes. By contrast, plants belong to the kingdom Plantae, which contains only macrobes.

This error matters because no plant is unicellular or can replicate as rapidly as the microscopic algae eaten by larval frogs.

Secondly, most larval frogs have a staple diet of the microbes – namely bacteria and unicellular algae – that frequently coat the surface of aquatic plants. The scraping off of this microbial plaque has led to confusion between the eating of microbes and the eating of macrobes.

Larval frogs are the only vertebrates in which there is a complex ‘dentition’ of keratin, the same protein as in hair and feathers. This can be explained by the fact that larval frogs are the most specialised scrapers of microbial plaques among all the vertebrates.

And thirdly, 'grazing’ should mean the eating of graminoid plants (i.e. Poaceae, Cyperaceae, Typhaceae, Juncaceae and other monocotyledonous angiosperms). Its indiscriminate use to describe algal or bacterial diets of larval frogs has added to the confusion.

The surprising truth seems to be as follows:
Although larval amphibians eat widely (from bacteria to animals, from suspended to sedimentary organisms, and from photosynthetic to non-photosynthetic species) they generally reject vascular plants. The brownish ‘detritus’ eaten by larval frogs consists of the relatively easily digested living cells of microbes rather than dead cells of plants.

Larval frogs can be kept in captivity on artificial diets consisting partly of plants (e.g. boiled spinach), but this does not necessarily mean that they would eat such material, raw, in the wild.

The wetlands typically inhabited by amphibians have an optimal combination of freshwater and gaseous oxygen in a seasonal regime. This effectively releases pulses of nutrients via decomposition by beneficial fungi. The nutrients in turn sustain various bacteria (https://en.wikipedia.org/wiki/Bacteria) and other microscopic organisms.

Re-assessing amphibians in this context:
It is particularly remarkable that, in their typical habitats, amphibians have achieved competitive superiority over other vertebrate classes (i.e. fishes, reptiles, birds and mammals) without directly harvesting the vegetation of sedges, reeds, rushes and marsh grasses.

This indicates that the productivity and fecundity of amphibians is generally based on larval consumption of the most rapidly replicating but least visible producers in wetlands, namely unicells and other microbes. The bodies of amphibians grow more efficiently than those of mammals or birds because amphibian blood remains cool, minimising the wastage of energy in respiration.

In summary:
What has kept amphibians competitive despite their primitive origins may be their continued exploitation of the extreme productivity of microbes. In the case of frogs this exploitation is direct because the staple diet of most larval frogs is microbes. In the case of salamanders the exploitation is indirect because the staple diet of larval salamanders is small animals that eat microbes.

Posted on June 9, 2022 08:03 AM by milewski