7

Borneo’s Tadpole Heaven

I remember the walk clearly. It was August 2002, and my friend and colleague from Germany, Alex (now Professor Haas), then with the University of Jena, and I were slowly trudging up the summit trail at Kubah National Park. Night was just falling, and we had set out to find a good spot to find frogs, particularly their larval stages.

Having arrived in 1998, I was a new staff member at the brand-new Universiti Malaysia Sarawak, located near the city of Kuching, in Sarawak State, on the island of Borneo. My previous experience on the island had been in adjacent Brunei Darussalam, and my tadpole samples from the time were kept aside as I grappled to identify the often-complex (adult) frog fauna of the rainforests of that country. Now, with the arrival of a self-confessed tadpole guy, I was more hopeful of arriving at precise determinations. Alex, the son of a watchmaker, has both the eye and patience for small details, just what’s needed to study tadpoles.

Approaching what looked like the top of the ridge, we (at the time a fairly physically unfit duo) were relieved to hear frog calls. And not just one or two, as in most Bornean forests, but a crescendo of a multitude of species, some of them unknown to our fairly well-trained ears!

As we gravitated to the left of the trail, a few yards along a muddy bank led us to an incredible sight—a largish pond, the result of excavation for an arboretum and other horticultural activities, on whose edges and on overhanging plants and adjacent trees sat a multitude of species, some clearly recognizable, others not. Areas in the water were dense with tadpoles, feeding or coming to the surface en masse to take hasty gulps of air, avoiding the equally numerous dragonfly naiads out to eat them. Given that standing bodies of water of this size are a rarity on the island (and most species breed in far smaller water bodies, such as temporary puddles and oxbow lakes and depressions created when large trees are uprooted), we realized that here was a great site for future research.

Some words on the pond itself are in order. This unimpressive-looking, often muddy depression is irregularly oval, 25–40 m at its greatest length and 8–12 m at its maximum width. Depending on the season, it is 1.5–2 m deep and edged with a low earth embankment that offers a perfect habitat for a variety of anuran amphibians.

Kubah’s frog pond sits at the foot of the Gunung Serapi sandstone massif, within the Matang Range, from where we have recorded 70 species of amphibians. Here, in a relatively small area, are as many as a dozen species that breed, some simultaneously. Studies by our Malaysian and European students, Alex, and me have produced several papers and theses on life histories, new records, and taxonomic descriptions of species; some of the studies continue to this day. Work at the pond and its surrounding areas has been done, for instance, on the female advertisement calls of the Smooth Guardian Frog (Limnonectes palavanensis); the breeding biology of what must be one of the smallest rhacophorids, White-Eared Tree Frogs (Feihyla kajau); and multiple-male amplexus in the Harlequin Tree Frog (Rhacophorus pardalis).

It is here that we found the region’s smallest frog (breeding males less than 13 mm in snout–vent length), the Matang Narrow-Mouthed Frog (Microhyla nepenthicola), whose tadpoles develop exclusively in the pitchers of a particular species of Nepenthes (pitcher plant), and the Red Hot Chili Pepper Frog (Glyphoglossus capsus), an attractive frog that is olive dorsally and blood red on the throat region. A visiting sound enthusiast from Australia made recordings of the pond by night, highlighting the Mahogany Frog (Abovarana luctuosa), and the clip won a competition for the best sound in the world, organized by the lifestyle website, BeautifulNow.is!

Overall, a visit to the pond is never disappointing and is a great opportunity to see many large, charismatic species among the frog fauna of Borneo that are seldom seen elsewhere, such as the File-Eared Tree Frog (Polypedates otilophus), the Bornean Tree Frog (Rhacophorus borneensis), and the celebrated Wallace’s Tree Frog (R. nigropalmatus). In addition, not far from the pond itself, we have observed both species of caecilians known from the Matang Range, the Broad-Striped Caecilian (Ichthyophis asplenius) and the Biangular Caecilian (I. biangularis). However, it is the knowledge generated on the larval stages of amphibians here in the remote pond and its vicinity, in the middle of nowhere, that we find most fascinating.

One species encountered at the edge of Kubah’s frog pond does not actually use these waters to breed and instead shows unusual parental care. The Smooth Guardian Frog lays and fertilizes eggs in the moist leaf litter, dozens of meters from the nearest stream. It is the task of the males to attend to the eggs. Upon hatching, the tadpoles climb onto the back of the father, who carries them to the stream, where they develop and transform into little frogs. Farther away from the pond are several other species of frogs that have even less use for ponds and rivers. These include the bush frogs (Philautus) and the dwarf toads (Pelophryne), both completing development inside water-filled plant structures, from pitchers of the local species of pitcher plants (Nepenthes) to tree cavities. Both groups are endotrophic, obtaining all the energy required for growth and transformation into little frogs from the yolk supplied by the mother. Our favorite frog, the Matang Narrow-Mouthed Frog, also shows such adaptations. Its tadpoles, about 11 mm in maximum length, inhabit the pitcher plant Nepenthes ampullaria. Also endotrophic, it does not have an oral aperture and has a remarkably short gut, with only three bends. The tadpoles turn into little frogs within a fortnight.

Just behind the frog pond is a shallow, flat stream that flows over sand, draining into the torrential (and oddly named) Sungei Bawang (= Garlic River), where herpetologists have broken more than one bone trying to study the tadpoles that live in this dangerous (to humans) environment. In fact, the current is so fast that it’s a miracle any tadpole should occur here in the first place. Two groups of amphibians regularly utilize such environments: the slender stream toads (Ansonia) and the Bornean torrent frogs (Meristogenys). The tadpoles of both species show peculiar adaptations, including oral suckers and in some even belly suckers, to cling to smooth surfaces of rocks. Such is the efficiency of the suckers that it is sometimes a challenge for field investigators to pry the tadpoles loose from such places using bare hands (and nails)! To understand how suction is achieved in Meristogenys, we studied the abdominal and oral suckers by means of three-dimensional reconstructions of serial histological sections. Our observations show that the suckers are composed of muscles and ligaments attached to the skeletal structures, and some muscles attach directly to soft tissue, explaining their significant strength.

Also nearby, but in the quiet side pools or bends of such wild mountain rivers, are gentle habitats—deep pockets of rock, filled with dense leaf litter. These areas create yet another unusual condition: a world of near darkness, anoxic conditions, and low temperatures. In such microhabitats develop the larvae of yet another specialized frog, the so-called foot-flagging frogs (Staurois). The adults, which are chiefly diurnal, raise their legs to communicate with each other against the thunderous background of the cascading waterfall. Their tadpoles are eel-like, and as might be expected of the habitat occupied, they lack pigments. The tadpoles appear in shades of red, pink, and orange, and they panic when exposed to the light of day.

The tadpoles of the puddle or seep frogs (Occidozyga) occupy shallow depressions and can swallow entire insect larvae, a feat for an amphibian larva. Our studies on its morphology show adaptations such as a relatively small mouth and tunnel-like arrangement of structures that form the buccal cavity, suggestive of suction feeding that generates strong negative pressure, much like a vacuum cleaner. Tadpoles of the genus Leptobrachella, referred to as slender frogs, live in shallow but highly oxygenated waters flowing over fine rocky sediments. They can merrily enter and exit such microhabitats, flexing their heads and necks in a way mammals do and other tadpoles can only dream of. Again, our detailed morphological studies, looking at their cranial bones and associated muscles, show how this is achieved. The mobility of the head is attributed to the freeing of the notochord from the base of the cranium, as well as the articulation of the foramen magnum floor with the atlas, conditions unknown in other frogs. Further, certain trunk muscles reach far forward onto the skull. Finally, with a total of 35 vertebrae, these tadpoles are indeed very long! Those who find the Bornean Horned Frog (Pelobatrachus nasutus) bizarre would find the biology of their larval stages equally so. These tadpoles have an upward-directed oral disc that spreads under the surface film of the water, sucking in microscopic particles of food (including algal material, pollen, and perhaps also bacteria) by means of the branchial pump.

Frog biology is indeed engrossing, be it for researchers or the general public. And the natural history of their larval stages—with its quirks and outright strangeness—must be one of the most diverse in the entire vertebrate world. In the intervening years, the fame of the frog pond has spread far and wide, and in recent years, few but the wettest nights have deterred ecotourists and photographers to the pond. Many travel agencies specializing in wildlife tours in town even sell frog tours to the pond. An event we at Universiti Malaysia Sarawak conduct annually (since 2012) with partners, such as the Sarawak Forestry Corporation, is the International Bornean Frog Race. Holding the race, a photographic competition with a variety of other programs and sometimes other parallel events at Kubah centered around the frog pond, has been a great success. The pond provides plenty of frogs for participants to photograph, and the event highlights the importance of amphibians through the media. We cap entry to 100 persons to reduce impact on the environment. Up to 17 countries have been represented at a single year’s event, making it a truly international affair.

The fame of the frog pond at Kubah National Park, admirably managed by the Sarawak Forestry Corporation and the staff at Kubah, continues to draw researchers and has helped bring a sense of pride to the people of Sarawak regarding their natural heritage, including frogs, which are often deemed lesser than hornbills and orangutans. We are happy to be part of that journey.