A naturalist's various thoughts on the frog genus Breviceps, part 2

(writing in progress)

...continued from https://www.inaturalist.org/journal/milewski/69039-a-naturalist-s-various-thoughts-on-the-frog-genus-breviceps-part-1#

I would like to review the genus Breviceps and interpret it relative to several themes, including myrmecophagy.
 
If you live in Cape Town, Breviceps is an important frog to know about. It has a centre of endemism in the Fynbos Biome. Breviceps persists in gardens (e.g. common on Middle Campus of UCT, which has no vestige of the original vegetation), so the species are somewhat adaptable despite their narrow endemism.
 
The general biogeographical pattern of Breviceps is: restricted to southern Africa sensu lato, but remarkably widespread across the range of rainfall and temperatures within southern Africa. Although Breviceps does occur in the southern Namib, it fails to penetrate the driest part of the Kalahari, i.e. the southwest Kalahari in the South African part of Kgalagadi Transfrontier Park. Breviceps occurs in dense forest and at high altitudes. What’s interesting is that it is virtually the only frog in some environments in southern Africa, e.g. the Namib and the Knysna forests away from streams.
 
The secret of survival of Breviceps in arid climates is emergence only after rain; and even in mesic summer-rainfall areas, the season of activity is restricted. For example, near Pietermaritzburg, Breviceps adspersus emerges in September (variable from year to year). “The majority of forms emerge only after heavy rains...even in moist areas, forms such as Breviceps adspersus, Phrynomantis bifasciatus and Cacosternum boettgeri [all of which tend to eat termites/ants] normally (but not invariably) emerge only after the heavy rains have set in...Breviceps adspersus does not normally call and is not found above ground after December, despite wet weather and frequent downpours during the ensuing four months...the widespread forms which extend into arid areas, namely Breviceps a. adspersus..., are those forms whose emergence in moister areas coincides with wet conditions to an unusually close degree. It is probably on account of this unusually strong response to rainfall that these forms are able to colonise the arid areas of southern Africa.”
 
Breviceps contributes a far greater percentage of the southwest Cape frog fauna than of the tropical South African frog fauna. I.e. it is one of the few tropical genera of frogs that persists in full force all the way to the southern tip of Africa.
 
The most consistent feature of Breviceps, apart from its extremely short face and extreme ability to inflate when threatened, is its breeding by ‘direct development’, independent of surface water. It is an extremely terrestrial genus of frogs, in breeding on land and in having lost the ability to swim. Breviceps and Pyxicephalus (or is that Tomopterna?) are the only two amphibian genera whic are represented over the main expanse of the Kalahari.
 
Breviceps burrows extremely efficiently, albeit by the normal method for frogs, i.e. using the hind feet (it has large inner metatarsal tubercles) and descending into the earth backwards. Breviceps has been found 4-5 feet below ground.
 
The eggs of Breviceps are large and few.
 
Nobody seems to know to what extent the southwestern Cape spp. of Breviceps concentrate on termites. Skaife, in his book on Amitermes atlanticus, illustrates Breviceps rosei and mentions that it eats termites, as does the blind snake Typhlops delalandei.
 
Body size varies considerably among spp. of Breviceps. The maximum snout-vent lengths are as follows, in order of decreasing body size: B. adspersus 59 mm, B. poweri 47.5 mm, B. mossambicus 43 mm, B. montanus 31 mm, B. rosei vansoni 30 mm. In the life-size illustrations of Passmore & Carruthers (1979), Breviceps adspersus is shown to have a length of 32 mm, while B. mossambicus is shown to have a length of 36 mm, both of which I take as typical sizes rather than maximum sizes.
 
Here are some notes from Rose W (1950) The reptiles and amphibians of southern Africa. Maskew Miller, Cape Town.
 
Breviceps gibbosus: “They will eat earthworms, insects and mealworms. In some districts the appear to feed mainly on termites, but in other localities these are only to a limited extent available.”
 
Breviceps rosei: “Though we found her under a decaying Restio tuft, in our opinion she was wont to range about at night, trotting about, dabbing her somewhat slender tongue at the grubs and small insects her downcast eyes would bring more clearly to her view. One which we have at present feeds readily on termites and can deal effectively with worms several times its own length.”
 
Breviceps montanus is common near Hermanus and is smaller even than B. rosei.
 
Breviceps adspersus: abundant in Natal and Zululand “where they are quite the most important enemies of the termites. The quantity they exterminate annually must be prodigious.” (I assume that Rose was referring to alates, not workers or soldier termites.)
 
My interpretation: I don’t see Breviceps as a myrmecophagous genus, and I don’t think ‘myrmecophagous’ is a particularly useful description even for those spp., such as B. adspersus, which do eat mainly termites (mainly alates). Instead, what makes Breviceps so unusual among the frogs of the world is that it combines spending most of its time underground with an independence from surface water during breeding. The fact that B. adspersus times its emergence to coincide with the rains is not in itself surprising, for a frog, but what is surprising is that it does not use the heavy rainfall to breed by means of free-living tadpoles. So the specialisation is mainly developmental rather than dietary.
 
And, because Breviceps burrows with its hind feet, it can’t really be described as particularly specialised or aberrant in terms of its digging. Certain frogs around the world that dig with their forelimbs and snouts, and that truly is specialised and aberrant among frogs.
 
What I clearly see for the first time today, despite having studied Breviceps for at least the last 25 years, is that no other frog anywhere else on Earth combines direct development, an extremely short face (eyes above the mouth instead of behind the mouth), and digging backwards with the hind feet. Rhinophrynus of Mexico, a myrmecophage, has an extremely narrow mouth but breeds in water. Arenophryne and Myobatrachus of Western Australia are myrmecophages and have direct development but dig forwards, with the fore limbs. Hemisus of Africa is probably myrmecophagous and has a narrow mouth but digs forward and breeds in water, at least after a period of development on land. Notaden of Australia is myrmecophagous and can inflate the body to some degree, and has a rather short face, but breeds in water. Nasikabatrachus is a true myrmecophage, with an extremely specialised mouth, and takes termites mainly underground (like Myobatrachus). I’m not sure whether it burrows forward or backward, but its tadpoles are aquatic.
 
The bottom line is that I’ve abandoned any view that I might have had of Breviceps as myrmecophage. Breviceps probably evolved from the mainly myrmecophagous family Microhylidae, but its specialisations do not lie in diet. What exactly the central specialisation in the genus is, and why it is so distinctively southern African, require further thought. I suspect that the best way to understand Breviceps will be in terms of the predation pressures under which it lives in southern Africa?

Sorting out eye size in Breviceps spp.:

Breviceps spp. vary considerably, including in eye size. I am starting to get a sense of how eye size varies within Breviceps.

The first thing to realise is that there is considerable variation in body size within the genus in South Africa, the largest species (B. gibbosus of Cape Town) weighing 5-10-fold more than the smallest (Breviceps rosei vansoni of Agulhas area).

One would expect the largest spp. to have proportionately small eyes and this is in fact what one finds.

The really large-eyed spp., namely B. macrops and B. namaquensis, are of medium size.

So, I conclude that some of the variation in eye size is ‘real’, i.e. remains after correction for adult body sizes.

In fact, the specific epithet ‘macrops’ means ‘big-eyed’ and the large eyes are mentioned in the scientific descriptions of B. macrops and B. namaquensis.

The two spp. (B. macrops and B. namaquensis) of the subNamib dunes from Namaqualand to the Orange River mouth area have particularly eyes. By contrast, B. verrucosus from Natal has particularly small eyes.

I find it interesting that if anything it is the smaller-eyed spp. (including B. gibbosus) that have the flattest faces.

This seems to indicate that the flatness of the faces in this genus is not just an effect of the eyes being much larger than in other subterranean frogs such as Myobatrachus, Arenophryne, Rhinophryne, Nasikabatrachus and Hemisus.

Breviceps gibbosus: SVL up to 5.9 cm. This species, which occurs in Tokai, is the largest in the genus and the small appearance of its eyes are partly explained by this body size.
 
https://hardakerwildlife.files.wordpress.com/2011/09/20110913durbanville-caperainfrog.jpg
 
B. gibbosus:
http://www.buckhambirding.co.za/wp/wp-content/uploads/2012/07/Cape-Rain-Frog-20120626.jpg
 
B. gibbosus:
https://capefroggers.files.wordpress.com/2014/04/m_dsc_0349-2.jpg
 
Breviceps verrucosus: SVL up to 5.3 cm (FOREST in Natal)
http://biodiversityfocused.co.za/wp-content/uploads/2015/02/Plaintive-Rain-Frog-Breviceps-verrucosus-1.jpg

B. verrucosus:
http://calphotos.berkeley.edu/imgs/512x768/0000_0000/1104/0117.jpeg
 
B. verrucosus:
http://calphotos.berkeley.edu/imgs/512x768/0000_0000/0211/3124.jpeg

B. verrucosus:
http://calphotos.berkeley.edu/imgs/512x768/0000_0000/0211/3125.jpeg
 
Breviceps namaquensis: up to SVL 4.3 cm. There is no doubt that the eyes are proportionately far larger than in B. gibbosus and B. verrucosus, even after discounting for body size differences. Note that the white sclera is visible.
 
http://i.ytimg.com/vi/7I6T38I8BNk/maxresdefault.jpg

B. namaquensis:
https://hardakerwildlife.files.wordpress.com/2012/10/018-20120930wcnp-namaquarainfrog.jpg

B. namaquensis:
http://featuredcreature.com/wp-content/uploads/2013/02/url.jpeg

B. namaquensis:
http://i814.photobucket.com/albums/zz70/LouranceKlose/_MG_2097Bnamaquensis_zps1293f7c2.jpg
 
B. namaquensis:
https://s-media-cache-ak0.pinimg.com/originals/e6/c0/ca/e6c0cad4fd5ea1abdd1db757a7c87442.jpg

Breviceps macrops:
http://www.boldsystems.org/pics/_w300/AMPSA/DNA_259%2B1353604132.JPG

Breviceps verrucosus:
http://www.boldsystems.org/pics/_w300/AMPSA/PEM_A10570%2B1353604140.JPG
 
Video clip inadvertently illustrating dexterity in Breviceps:

Please see this footage of Breviceps and termites: https://www.youtube.com/watch?v=mISMwN-0ggE.
  
This is from Attenborough’s ‘Life in Cold Blood’, his BBC documentary made in 2008 on herps.

The footage shows Breviceps adspersus eating termite workers, which I’m sure was set up by the film crew as opposed to just stumbling on a Breviceps naturally doing this. I think that the reality is that Breviceps adspersus usually eats the alates, not the workers.

Not only have Breviceps adspersus and B. mossambicus been recorded taking termites alates as their main food, but these frogs have no way to dig into termitaria or termite mounds to expose the workers in the way shown.

So, a lot of this footage is set-up and has to be taken with a grain of salt; no doubt it was in a terrarium inside a tent at their base camp.
 
In my notes from 25 years ago, I have discovered a similar point I noticed about a previous wildlife documentary, made two decades before this one by Attenborough.

The documentary I refer to is ‘Lions of the African Night’, made by David and Carol Hughes for National Geographic, and the footage I refer to is of Breviceps adspersus in Kruger National Park (not in inflated mode at all, but instead completely deflated and unalarmed) eating worker termites.

The footage showed, as in the case of this more recent footage by Attenborough’s team, the rather long tongue of the Breviceps adspersus as the frog flicks this deftly out to snap up the termite workers one by one.
 
My point is that, in at least two documentaries filmed in South Africa at least two decades apart (I viewed the Nat Geo one in Nov. 1991), film crews used the same technique to show Breviceps adspersus eating worker termites: they dug up a colony and kept the frogs captive in order to set them up eating the insects.

The fact that the Breviceps accepted the opportunity is no indication that Breviceps adspersus often eats workers. I think the staple diets of this Breviceps is termite alates.
 
You can see the footage of Breviceps from minute 30 in the 49-minute documentary https://www.youtube.com/watch?v=km4eXL8ATsI . Surprisingly, the full documentary is available free on the web.
 
The other footage of frogs is a reason to keep watching the documentary from this point, even if you don’t have time to watch the whole thing (which I recommend).
 
At minute 36 there is extraordinary footage of Chiromantis xerampelina, the only real example of a tree frog in Kruger Park, producing a foam nest communaly. Although Chiromantis is the closest thing in southern Africa to Ranoidea, no member of that genus has anything like this sort of specialised reproductive behaviour. No Ranoidea makes a foam nest, least of all out of the water; no Ranoidea inseminates eggs communally like this; and no Ranoidea deposits its eggs on plants well above the pool.
 
There is also footage of Afrixalus exhibiting dexterity in folding a grass leaf to make a tube for its eggs.
 
The footage of a spider eating Hyperolius is also noteworthy. And you can also see Africa’s only aposematic frog, Phrynomantis.

to be continued in https://www.inaturalist.org/journal/milewski/69062-a-naturalist-s-various-thoughts-on-the-frog-genus-breviceps-part-3#...
 
(writing in progress)

Publicado el 14 de agosto de 2022 por milewski