Green Geckos and Fungal Frogs: the Herpetofauna of Ranomafana

In my mind Madagascar means geckos, especially the brilliant green day geckos of the genus Phelsuma, but this island is home to a lot more cold-blooded life. Ranomafana National Park alone contains 62 species of reptile and 98 of amphibian.

Enjoy this collection of reptiles and amphibians, known together as herpetofauna, making their way in the outskirts of Ranomafana ⎯ and a carnivorous fungal spore beginning to lurk within them.

Chameleons


On one of our early trapping missions, my attention was utterly occupied by running the GPS unit and navigating the viney, slippery mountainside. Menja had attention to spare, apparently, because she pointed up at this distance blue blob in the canopy. It was a Parson's chameleon (Calumma parsonii parsonii), one of the biggest and most colorful species!

This nose-horned chameleon (Calumma nasutum) was spotted by Zaka on a birding hike. It matched the color of its twig perfectly, and it slyly rotated to the far side from me and my camera. An intelligent habit for the chameleon, but infuriating for the photographer!

Finally I got him on the top of his twig by placing myself on both sides. Here he's looking green because he just walked off my blue-and-red plaid shirt (which I suppose was a bit much to match).

No matter how frightened he may have been, his top speed was a lazy stroll, and he didn't negotiate around barriers (like my hand), only over them.

Here he is disappearing into a dead fern, zig-zaggy brown stripes and all.

This is a brown leaf chameleon (Brookesia superciliaris), one of thirty magnificently-strange "leaf chameleons" endemic to Madagascar. Unlike their greenish, large, arboreal cousins, Brookesia crawl through the leaf litter and resemble dead leaves.

Like other chameleons, leaf chameleons have protruding eyes that can each point in a different direction to focus on two images at once. The entire eyeball is covered in a fused, muscular eyelid with only the pupil exposed.

I found this little guy, another brown leaf chameleon, while walking through a misty rainforest fragment near the village of Bevoahazo. A bit of mud fell and tumbled at my feet. Good thing I looked closer -- it was a chameleon!

Update: Rasolo the Artist, who you'll meet below, just sent me an incredible Scientific Reports article titled Widespread Bone-Based Fluorescence in Chameleons. Fluorescence is the ability to absorb light of a short wavelength and then emit light of a longer wavelength. In other words, if you shine light of one color on a fluorescent object, it glows a different color. This neat trick is common in marine organisms (like corals!) but rare in terrestrial animals. Naturally, Madagascar's chameleons of the genus Calumma decided to be the exception.

From the paper: "Tubercles arising from bones of the skull displace all dermal layers other than a thin, transparent layer of epidermis, creating a ‘window’ onto the bone... The fluorescence emits with a maximum at around 430 nm in blue colour which contrasts well to the green and brown background reflectance of forest habitats." We get nose-rings and tattoos, and all this time, you had glowing, neon-blue bone bumps peeking through skin-windows on your face? Cool, chameleons. You win.

Geckos


The ubiquitous peacock day gecko, Phelsuma quadriocellata. In this photo, two individuals are having a staring contest to determine who will rule this particular blade of sugar cane.

I caught this peacock day gecko snooping around our bananas. At first, she was upset to be in my hand, but then...

I put a little condensed milk on my finger, and she lapped it right up!

We often found this species licking sticky banana juice of the outside of our lemur traps.

I saw this Gray's leaf-toed gecko, Hemidactylus mercatorius, on the cement wall of Centre ValBio's parking lot and brought him inside. He escaped temporarily to bask on the warmth of an Apple laptop! Ah, Anthropocene habitats.

My friend Rasolo poses with the Gray's leaf-toed gecko. Rasolo is an extraordinary watercolor artist specializing in Malagasy wildlife. Check out his work (including an abundance of reptiles) here

Rasolo recently painted an ecosystemic poster of Ranomafana's reptiles, and his next project is even cooler. He's creating educational tools pulled straight from the poster. The Centre ValBio "My Rainforest, My World" project will be using these tools to teach about biodiversity in village primary schools. On the left is a Satanic leaf-tailed gecko pressed from a dead leaf with a custom-built cookie-cutter. (Kids will hide these biodegradable geckos around the forest and then try to find them, a lesson in camouflage.) On the right is an oragami Baron's mantella. (Kids will fold their own paper frogs, and choose to color them as their favorite endemic species.)

After learning about Rasolo's crafty herptiles, I was lucky to find both in the wild. Here is a Baron's mantella, Mantella baroni. (Yes, I know it's out of place in the gecko category, sorry not sorry.)
  
The Baron's mantella has a blue polka-dot belly, just like its origami model.

Here is a Satanic leaf-tailed gecko, Uroplatus fantasticus. Without the expert eyes of a guide, I would never have noticed that this reptile was anything but a leaf. The Uroplatus genus is made up of small species that resemble leaves and large species that imitate bark.

Since we're on the topic of leaf-tailed geckos, here is the crown jewel of my Madagascar experience: the mossy leaf-tailed gecko, Uroplatus sikorae.

This is one of those larger species, a bark imitator. Its body is fringed with a scalloped flap of skin that lays flat against the tree trunk, obscuring its outline to hide from predators.

These geckos always sleep head-down on exposed, lichen-graced tree trunks. This head-down position hides their open eyes (geckos lack eyelids) from hungry birds.

When I got too close, this ever-watchful piece of bark lifted its head ever so slightly, breaking the seal of its scalloped chin-flap. I backed off and let the wonderful animal go back to sleep.

Other Lizards


Ornate girdled lizard, Zonosaurus ornatus, missing the tip of its tail (hidden under a leaf).

Another ornate girdled lizard, basking and posing.

This Afro-Malagasy mabuya (Trachylepis sp.) is a kind of skink. These smooth, golden lizards skittered through the fern and sugarcane underbrush whenever the sun blasted through the rain clouds.

Snakes


Lateral water snake, Thamnosophis lateralis. This black snake with yellow racing stripes was a dime a dozen in the rice paddies and rainforest fragments.

I am in heaven here because Madagascar has no venomous snakes, just like my home in western Washington. I can pick up everything that slithers! Ironically, the Malagasy have a national phobia of snakes. Whenever I touch one, people stop to gape in horror and amazement. (An elderly man carrying a load of rice stopped to watch from a safe distance as Menja took this photo of me.)

One afternoon, two snakes peeked their swaying, sinister heads out of this hole in the ground. (One sank out of sight before the photo.)

Here's the hole---an ant nest! I sure wouldn't want to slither into the home of biting insects, but that's just me. I wonder if the snakes enjoy the formic-acid flavor of ants, or just their white eggs and larvae?

Madagascar tree boa, Sanzinia madagascariensis. Madagascar's boas are a delightful mystery. The boa family is native only to South America and Madagascar---not to continental Africa, not to Asia or India or Europe. How did that happen? One leading theory says that ancestral boas travelled from South America through present-day Antarctica (before it was so cold) and onto Madagascar while all were connected as the Gondwana supercontinent, over 180 million years ago (the Jurassic period). But recent DNA evidence suggests these "boas" might actually be more related to the Calabar pythons of Africa than to the boas of South America. Whether this snake tells a story of ancient migration or astounding convergent evolution, I love that humans haven't solved the mystery yet.

Can you see his thick, muscular, emerald body wrapping a branch?

A juvenile Madagascar tree boa. We found this slinky fellow crossing the road at night.

He was pumpkin-orange and calm as a cucumber.

He made a stylish bracelet, but he just wasn't practical to wear. Every time I put my hand down, he slithered right off!

Frogs


Frogs are the only amphibian present on Madagascar, and all 290 species are endemic. It's not easy for a wet-skinned amphibian to cross the salty Mozambique Channel and colonize an island! I've split these slimy-skinned hoppers into utterly unscientific categories for ease of enjoyment.

Frogs that Look Really Normal


I read in a guidebook (Madagascar Wildlife by Bradt Travel Guides, highly recommend) that a conservation group was accepting photos of any frog seen in Madagascar as part of a frog atlas project. Jazzed on citizen science, as always, I made sure to take a photo of every frog I saw. When I finally got around to posting the photos on iNaturalist.org for identification, I realized I had dozens of shots of the same guy: the Mascarene ridged frog, Ptychadena mascareniensis.

These frogs look like, well, quintessential frogs. You can't take ten steps through a rice paddy without disturbing one. A good example of how habitat alteration by humans doesn't always decrease biomass (the sheer number of frogs), but it does decrease biodiversity (the number of frog species).

You thought that was a big bullfrog, didn't you? Look how tiny!

Frogs that Like to Swim


The genus Boophis is endemic to Madagascar. These frogs are known for bug-eyes. With similar traits to the unrelated tree frogs of Africa and South America, they're a good example for convergent evolution. I stumbled on this pair in a cold, fast stream draining a steep sugarcane field. If you look past those glowing orange orbs, notice that this female has a male clasped to her back! The mating embrace of frogs is called "amplexus."

Update: the excellent folks over at iNaturalist.org have identified this frog as Boophis boehmei, Böhme's bright-eyed frog!

When I pointed my finger near the frogs to give a sense of scale, the female turned downward and swam half-heartedly into the sand. She never got more than her head covered... Fail.

A Mantidactylus species in the same stream.

A frog with a white belly... perhaps a different species of Mantidactylus.

Frogs that Look Like Dead Leaves


Once my guides noticed how I scrambled to photograph every leaping leaf, they started pointing out frogs right and left. Madagascar is famous for its Mantella genus, analogous with the poison dart frogs of South America, and it bug-eyed Boophis. But after those distinctive groups, there are still a whole mess of frogs that are best known for... looking like leaves.

See that dead leaf?

Yeah, it's a frog.

It's the aptly named Madagascar jumping frog, Aglyptodactylus madagascariensis.

A juvenile of the genus Gephyromantis.

A Fort Dauphin Madagascar frog, Mantidactylus melanopleura.

Another Fort Dauphin Madagascar frogwith my finger for scale.

A burrowing or stump-toed frog of the genus Rhombophryne (family Microhylidae, the narrow-mouth toads).

What a pointy nose you have, little burrowing frog.


Frogs that Climb Trees


This whitebelly reed frog (Heterixalus alboguttatus) was one of the most beautiful amphibians I've ever seen!

Another species of reed frog (Heterixalus sp.) or perhaps a light morph of the whitebelly reed frog. This genus does well in the longoza springing up in fallow plots left from slash-and-burn agriculture.

Another, smaller reed frog (Heterixalus sp.)

White grainy frog, Gephyromantis luteus? One night I went out for a solo frog hunt. I heard a loud PING, PING, PING sound, but when I approached, the sound stopped. I held still and searched with my flashlight all around me. After five minutes, I gave up and looked down at my feet to find the path. There on a leaf, inches from my face, was a big, brown treefrog! He'd been sitting there in silence the whole time.

This is a Pandanus frog, Guibemantis pulcher, sitting on---you guessed it---a pandanus leaf.

Here's a river of Pandanus in Ranomafana National Park. These stilt-rooted monocots are abundant in patches and along water. They're often called "pandanus palms" or "screw pines," but they're neither palms nor pines. The genus Pandanus contains 750 species spread across the Old World tropics.

Here's my hand with the Pandanus frog for scale.

A Betsileo reed frog, Heterixalus betsileo? This frog gave one strong impression: silver! Like a shimmering sardine or a newly polished spoon.

To tie this post in with emerging wildlife disease, I'll touch on something that's been on my mind since I arrived in Madagascar: chytrid.

During the World Congress of Herpetology in 1988, scientists realized a disquieting global pattern. All over the world, amphibians that had been common were disappearing for no apparent reason, often from inside protected areas. Soon after, the IUCN published a Global Amphibian Report showing that 43% of amphibian species were in decline, 32% were threatened, and 168 species were recently extinct. Strikingly, 100 of those extinctions were very recent, having occurred since 1980. Why?

I remember learning about this mystery as an eighth-grader visiting the Woodland Park Zoo. It was 2008, and zoos across America had declared it "The Year of the Frog" to raise awareness. I read a sign in the Day-Night Exhibit and felt a chill of terror at the disappearing frogs, and a thrill of wonder that we hadn't found the killer.

Since then, a prime suspect has emerged: a little organism first described in 1997. It's a skin fungus known as Batrachochytrium dendrobatidis, or Bd. This fungus causes a diseases called chytridiomycosis, or simply chytrid. Under a scanning electron microscope, the fungal zoospore looks like a beach ball with few nails bulging out from the inside.

Scanning electron micrograph of a frozen, intact Bd zoospore.
Image credit: CSIRO. CC BY 3.0 license.

Bd prefers a diet of keratin, a protein found in amphibian skin, which it breaks down with proteolytic enzymes like trypsin and chymotrypsin ⎯ the same enzymes found in our small intestine. It spreads stringy, root-like tendrils called rhizomes throughout the frog's skin to harvest keratin meals. That's where the real trouble starts for the frog. With their damp skin, even healthy frogs are constantly at risk of dehydration, and Bd rhizomes make it easier for frogs to dry out.

No one knows for sure where Bd comes from. Various strains have existed for a long time in Africa, Japan, and the eastern United States. One hypothesis states that the pandemic strain of Bd is native to Africa, and it began its global journey in the past century when African clawed frogs, Xenopus laevis, were exported from South Africa as laboratory models and pets.

Some regions of the world experienced sudden, massive die-offs in the 1980s when chytrid fungus arrived. This was the pattern with harlequin frogs of Costa Rica, the Yosemite toad and mountain yellow-legged frog of California, and dozens of Australian frog species.

Reading this pattern, conservationists began to worry about a zombie pandemic sweeping the planet: chytrid arrives, frogs die, repeat. But the story is more complicated than that. Chytrid has now been found on all continents (except Antarctica, where no amphibians live), and it isn't causing disease everywhere.

Large tracts of the world ⎯ Africa, Asia, and Europe ⎯ show high rates of infection but few die-offs, indicating that chytrid may be endemic there. Local amphibian species have probably lived alongside Bd for long enough to evolve defenses. In these regions, chytrid might hang out with frogs much like the common cold virus hangs out with us, causing intermittent sniffles but seldom death.

Then, there are those few islands where chytrid has not yet been found: Papua New Guinea, Fiji, the Solomon Islands, and the Seychelles (scattered next to Madagascar, where I am now). We don't know when chytrid will arrive, or what the consequences will be when it does.

Madagascar was on this chytrid-free list until recently. In 2015, a study published in Scientific Reports detected Bd in all four families of frog native to the island. The earliest positive samples were Mantidactylus species from 2010 and a Mascarene ridged frog (Ptychadena mascareniensis) in 2011. All these frogs were taken from the remote Makay massif, so it's puzzling how the fungus might have gotten there without hitting the human-population centers first.

Locations where Bd has been detected in Madagascar's frogs.
Image by Bletz. et al 2015 in Scientific Reports.

Since then, Bd has been detected in regions all across Madagascar, including Ranomafana National Park. I was particularly struck to read that one of the only positive tests in Ranomafana came from a Boophis reticulatus in Valohoaka, just across a river from the spot where I watched the pair of orange-eyed Boophis mating in a stream. I wonder if that couple was infected with chytrid? If their immune systems had warded off an infection? If their tadpoles will swim through a world where Bd spores overwhelm their fragile skin and shove them toward extinction?

Such dire predictions aren't really warranted given the evidence. As reports of Bd continue to come in from Madagascar, reports of diseased and dying frogs do not. Why? That's a mystery. Maybe a native strain of Bd has lurked here all along, avoiding notice by the eyes of science. Or maybe the Bd invasion just hasn't gotten a toehold yet, and the glory days of frog fungus in Madagascar are still to come.

Comments

  1. That mossy leaf-tailed gecko is INCREDIBLE!

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  2. You said there are no venomous snakes there, how about frogs? Other reptiles? Amazing examples of camouflage!
    Jeanette

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  3. Love these questions, Jeanette! Thanks for being my most faithful commenter from the start :)

    The short answer is no.

    There are only three species of venemous lizards in the world: the Gila monster (found in the Sonoran Desert), and the Mexican and Guatemalan beaded lizards. So the Malagasy lizards are safe (if you can catch em.)

    Frogs are not venemous but poisonous. (Venom is injected when the animal bites you; poison is ingested when you bite the animal.) Indeed the Mantella frogs are poisonous, like their analogs, the South American poison-dart frogs. Both genera get their alkaloid poisons from their insect prey: ants, termites, and fruit flies. But the poison-dart frogs are far more toxic than the Mantella. Cool!

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