Anuradha Batabyal and Maria Thaker in the IISc campus comparing the colours, size and bite marks on the bodies of their respective lizards to settle an argument about which among the two males is feistier. Photo: Devica Ranade
After submitting my PhD thesis on the biochemistry and molecular biology of a bacterial virus, I decided to turn my attention to the ecology and evolution of larger creatures. I had already been mesmerised by the Indian paper wasp (Ropalidia marginata). But I was also fascinated by the common house gecko (Hemidactylus frenatus). But I knew nothing about geckos.
My mentor Madhav Gadgil suggested that I spend some time at the Bombay Natural History Society (BNHS) to learn about geckos. J.C. Daniel, an authority on the Reptiles and Amphibians of India, and who was probably already the Director of BNHS by then, kindly invited me.
My tryst with geckos
And so it was that I took a train from Bangalore to Bombay and found myself in Daniel’s office on a Monday morning. He welcomed me and showed me racks and racks of preserved gecko specimens, and said I was free to study all I wanted. Seeing me with a suitcase in hand, he kindly asked me if I had a place to stay. I murmured that I did not. He seemed worried, but after a pause, he said in a hushed voice: let this be just between you, me, and the watchman; you can sleep on the floor in between the racks of specimens. And so I did.
I spent the next month sleeping among the racks at night, quietly slipping out in the morning, arriving at 10 am disguised as a day visitor, studying my geckos, going out conspicuously at 5 pm, and slipping back inconspicuously after 9 pm. The kindly watchman even shared his morning tea with me.
It was a lot of fun. I also fell in love with the city and enjoyed long walks, cheap restaurants and cheaper cinemas, and above all, the endlessly fascinating second-hand books on the pavements. Returning to Bangalore, I made some cages, caught some house geckos, had fun watching them fight and mate and lay eggs, and the cutest imaginable gecko babies break out of the smallest imaginable eggs.
To my wife’s horror, I made plans to stay up all night in our and our neighbours’ kitchens to study the ecology of the house gecko. But to her delight, my first love, the paper wasp, won me over. I have never conducted any serious research on lizards, but I have always had a soft corner for them. As a result, I have a large collection of lizard stories. These are some of my favourites. I mean stories of facts, not of fiction, although I have one favourite in fiction too – Karvalo, the story of a lizard hunt by the famous Kannada writer Poornachandra Tejaswi.
Lizards in the wild
During my brief romance with geckos, I read a monograph, The Life and Demography of the Side-Blotched Lizard, Uta stansburiana, by Donald W. Tinkle (1968). I was still too naïve in matters of ecology and demography to fully appreciate Tinkle’s results. But it was his way of working, his process of science that mesmerised me – so romantic and so different from the microbiology and molecular biology I was familiar with.
Donald Tinkle (1930-1980) studied a single lizard species for nine years, during which he marked 3,729 lizards in the field, captured and recaptured them 12,927 times in two study areas of about two acres each. In these study areas, he and his assistants combed the entire area at all hours of the day and located every lizard, time and again. They would sometimes focus on a particular lizard and follow it to observe its movements, migration, courtship and mating. They developed tricks to capture the lizards, weigh and measure them and release them back, but they also collected several thousand lizards for laboratory studies.
Tinkle’s work left a deep impression on me. His research has since been described as a classic “that established a foundation for demographic and life history studies for lizards, in particular, and for reptiles in general”. But I did not know that at that time.
What struck me was that it was something that even I could have done! Indeed, this is the kind of fun activity many of us did as children, and now I saw that this was scientific research. With a little training and discipline, I have no doubt that school kids can collect valuable scientific data and become knowledge producers if only we believed in them and in the value of this kind of research. Unfortunately, we condemn young people to remain as mere knowledge consumers for far too long in their lives.
Tinkle was also a great champion of long-term field ecological studies, though he himself died from cancer at the age of 49. It appears that we in India are finally waking up to the importance of such studies – my colleague Raman Sukumar has worked tirelessly to establish a Long-Term Ecological Observatories programme. This programme will operate at six sites “representing different biomes including the Northwestern Arid Zone, Western Himalaya, Eastern Himalaya, Central India, Western Ghats and Andaman and Nicobar Islands”.
Games lizards play
Lost in the fascinating world of paper wasps, I had all but forgotten about Uta stansburiana when these little lizards rushed back into my consciousness in 1996, complete with the image of Donald Tinkle running after them. In that year, Barry Sinervo of the University of California, Santa Cruz and Curt Lively of Indiana University, Bloomington, published their new study of this lizard in California. Their main interest was to understand how and why males of this species exist in three different throat colours – orange, yellow and blue. And why doesn’t natural selection retain the fittest of the three and eliminate the other two?
To understand why all three types of males persist through generations, we must observe and assess their behavioural strategies. Males with orange throats are aggressive and thus manage to maintain large territories to attract females. Males with blue throats are meeker and therefore maintain smaller territories and cooperate with other blue-throated males. Yellow-throated males are the meekest, resemble females, and hold no territories; instead, they masquerade as females, gain entry into other males’ territories, and manage to mate with the females who the territory owners have attracted.
We know of many examples where alternative phenotypes persist because they happen to have the same fitness. But here, the three types of males do not have the same fitness. Nevertheless, natural selection cannot eliminate two of the three types and retain only the best.
The secret to the persistence of such multiple morphs with unequal fitness is that natural selection is ‘frequency-dependent. This means that any type of male’s success depends on its proportion in the population with respect to the other types – fitness depends on the neighbours.
When orange males are common, they outcompete blue males but cannot defend themselves against the deceptive yellow males. So, the oranges go down, and the yellows go up in numbers. If the oranges go down, the blues are freed from the competition, and they increase in numbers. The yellows cannot sneak into the blues’ territories because the blues cooperatively ward off the sneakers from their smaller territories with multiple defenders. So, the yellows go down. When the yellows go down, the oranges are back in business. The net result is a cyclic variation in the preponderance of the three colour morphs.
One can say that the lizards are engaged in an evolutionary game. There is an elaborate mathematical toolkit to analyse such games, popular both in economics and evolutionary biology. The best-known name in economic game theory is John Forbes Nash, Jr. (1928-2015) of the Nash equilibrium and A Beautiful Mind fame. And the most famous name in evolutionary game theory is John Maynard Smith.
Rock paper scissors
The game of the side-blotched lizards is analogous to the familiar children’s game “rock-paper-scissors”. The rules of the game are that rock blunts scissors, scissors cut paper and paper wraps rock. Notice the analogy with orange males win over blue, blue males win over yellow and yellow males win over orange. The rock-scissors-paper game is a standard example in game theory to analyse games with three possible strategies.
Sinervo and Lively studied all three types of males’ reproductive success during 1990-95 in the inner Coast Range of California. As expected, no male morph was always the winner – blue males peaked in 1991, orange males in 1992, yellow males in 1993-1994 and blue males peaked again in 1995. This kind of oscillation is precisely what was predicted by their mathematical model that fitted the lizard data onto the dynamics of a rock-scissors-paper game. Side-blotched lizards are credited even today to be the best biological example of an evolutionary process governed by a simple children’s game’s rules.
The village of Hampi in Karnataka, which contains the ruins of the Vijayanagara Empire of the 14th century, is a very popular tourist site on account of its exquisitely carved temples and ruins of a bygone era. It is also a pilgrimage site for Hindus on account of the ancient Virupaksha temple dedicated to Lord Shiva. But I used to know a young man named Rajkumar Radder who visited Hampi more frequently than any tourist or pilgrim.
Raju, as we called him, was studying lizards towards his PhD under the mentorship of my colleagues Srinivas Saidapur and Bhagyashri Shanbhag at Karnatak University Dharwad. Raju did pioneering work (PDF) on the reproductive biology of the common garden lizard (Calotes versicolor) and the mechanism of sex determination in the Australian lizard (Bassiana duperreyi). Another species of interest to Raju was the South Indian rock agama (Psammophilus dorsalis), a very common lizard with a 10-12-cm body and a 20-cm tail. The males are larger than the females and gorgeously coloured during the breeding season, while the females are mottled and well camouflaged against the rocks.
One of Raju’s interests was to describe and understand the meanings of the many kinds of visual displays of the lizards, which he called the “language of lizards”. He documented their display repertoire to include push-ups or head-bobbing, tail raising, extension of the gular patch (brightly coloured skin under the throat), leg extension, arching of the back and dorsal flattening. Unfortunately, Raju passed away prematurely at the age of 35, bringing a temporary halt to research on these fascinating lizards of south India.
(View a tribute video here.)
Signalling with colours
I am delighted that my colleague Maria Thaker and her students have recently embarked on a long-term study of the south Indian rock agama. They have made many discoveries, and I would like to mention two of my favourites.
Everyone is familiar with the chameleon’s capacity to change colour to suit its background. This ability is present in many animals, including crustaceans, cephalopods, fishes, amphibians and reptiles. More impressive than changing colour to match the physical background is the ability of many animals to change colour to signal to rivals or mates. Signalling by changing colour has to be very dynamic in real-time.
In one set of studies, Anuradha Batabyal and Maria Thaker have focused on the ability of such dynamic, physiological colour change in the Indian rock agama. They brought wild-caught male and female lizards to the laboratory and staged encounters with members of the same or opposite sex while the lizards were surreptitiously monitored by a fibre-optic probe connected to a spectrometer. Thus, they quantitatively monitored changes in body colour and also the speed of the change.
When the males encountered females, the colour of the dorsal band on their body changed from yellow to orange or red and the lateral band from red to black. When they encountered other males instead, the colour change was different; the dorsal band changed to brighter yellow, and the lateral band changed to a more brilliant red. The intensity of the colour change was four times compared to the random change in control males that were monitored without such encounters. Besides, the colour change was more rapid during male-male encounters than male-female encounters.
That the males can change their body colour within seconds, differently in different parts of the body, and differently during courtship and aggressive interactions is a truly remarkable ability not recorded before in agamid lizards. This discovery opens up rich possibilities to study both the physiological and genetic mechanisms that orchestrate these changes, as well as the evolutionary significance of such an ability. What does it do to the fitness of a male to be able to change body colour rapidly, selectively and in a context-dependent manner? Does it make him more attractive to females and more frightening to other males? There are significant research opportunities ahead.
From country bumpkin to city slicker
Ecologists generally take great pride in studying forests and exotic places, the more pristine the better; few study the ecology of their backyard, the trees lining their streets and the lizards that run around them. It is somehow considered too silly for a serious scientist to be doing so.
Much of Anuradha and Maria’s research on rock lizards defies this stereotype. They extract rigorous scientific questions that can only be answered by studying urban animals and comparing them with their rural or forest counterparts. When animals move into urban habitats, they face new challenges, just as we do when moving from villages into cities – new enemies, new resources, and rapid spatial and temporal changes in the environment, requiring a new survival toolkit. How do lizards deal with these problems?
Anuradha and Maria have turned to their lizards to answer these questions. And to do so, they have been roaming in less disturbed habitats like the Antharagange forest range in the Kolar district of Karnataka and more disturbed habitats like construction sites in Bangalore. From both locations, they capture lizards by noosing them, house them in simple terraria in their laboratory and release the lizards back where they found them after the experiment.
In their study on the dynamic colour change I alluded to above, they also found, for example, that urban males changed colour more slowly and less dramatically. In another study, they found that on the matter of choosing safe shelters, urban males learn and unlearn more rapidly than rural males. In a third study, they showed that urban lizards have changed their behavioural strategies to suit the contingencies of their new environment: they take more risks, are less afraid of humans but choose their perches close to safety than rural lizards. These results open up a whole new set of questions about how urbanisation brings about these changes, are they really adaptive, are they reversible and so on.
Given the rates of urbanisation and the resulting habitat destruction and fragmentation worldwide, we may need to follow the lead provided by Anuradha and Maria to study rural-urban migrations and transformations of many species in many places. The knowledge so gained will become increasingly essential for the welfare of the animals and our own.
Maria Thaker has said, “Most of my anecdotes revolve around how impressed I am by their ability to shimmy just out of reach, and the fact that despite my decades of studying and catching lizards, they still outwit me with a tiny shift in position or posture. And nothing puts you in your place as a bite from one of these males.”
Anuradha said, “Despite many challenges, the love for wildlife and my passion for understanding animal behaviour helped me all along my PhD… My love for Psammophilus is a tad bit more because of their beautiful colour, and I am always fascinated with colourful animals (being an artist, colours inspire me a lot).”
I think it’s time we changed the canonical image of the scientist from that of an elderly, bearded man in a white coat to one of an intrepid young woman in the wilderness!