Rock agamas are lizards that live on rocky hills of peninsular India. They are also found in the suburbs of north Bengaluru.

A research group is studying the urban rock agamas and comparing them to those from rural areas to understand how these species react when their habitats are taken over by cities.

Retaining areas in the city which resembled their natural habitat could be ways for cities like Bengaluru to retain their rock agamas and other diverse animal species.

Imagine your home, a vast open space with gentle hillocks, grassy fields and massive boulders, is slowly encroached upon by a growing city, hungry for land. The hills are levelled, grassy fields are cordoned off into neat little plots of land to be sold for houses and apartments. For the Indian rock agama, Psammophilus dorsalis, this is an increasingly common reality.

Maria Thaker’s research group from the Centre for Ecological Sciences (CES) at the Indian Institute of Science, Bengaluru have been studying how they are coping with this new reality.

Thaker explained that her lab was interested in understanding the best combination of physical features, physiological processes and behaviours for the same species in different environments. “And we study that by picking species that live under varying selection pressures,” she said.

As the name suggests, rock agamas are lizards that live on rocky hills of peninsular India. However, they are also found in the suburbs of north Bengaluru. These urban habitats are a mix of houses, interspersed with empty plots invaded by lantana. Some lots have concrete compound walls. The agamas were restricted to these empty lots, where they bask perched on the walls.

It was the perfect study species for the lab. A lizard with dramatically different circumstances: a rural (and natural) environment and an increasingly urban one.

When their habitats are taken over by cities animals can react in two different ways, according to ecologists. Some animals like crows and rats exploit the new landscape, feeding on food waste. Others adapt and cope with the changing circumstances.

Where did the rock agamas fall? To answer this question, Maria Thaker and her research group began comparing the urban rock agamas to those from rural areas in Kolar district, about 60 kms from Bengaluru city. They compared the lizards’ diet, strategies for escaping predation, levels of social interactions and physiological health and found some important differences in the city dwellers and their country cousins.

Food, shelter and colour

One of the first studies from Thaker’s group tried to find out if urban and rural lizards were eating the same food and more importantly if they had similar body conditions. Shashank Balakrishna and others established that urban and rural agamas were eating similar foods, mainly ants, although the rural lizards ate a more varied diet. Surprisingly, urban lizards were bigger and had a higher Body Mass Index (BMI) than rural lizards. The researchers speculate that this was because rural lizards had to move much more to find prey, compared to the urban lizards.

Meanwhile, Madhura Amdekar, another researcher from the lab, placed models of rock agamas in urban and rural areas and measured the number of predator attacks on them. The ongoing study (yet to be published) showed no difference in the number of attacks. Anuradha Batabyal then set out to see if the urban and rural agamas would react differently to the same threat – her presence. Batabyal would approach the lizards, while her colleague measured how close she could go before they fled.

It was the males that responded to differently. Rural males fled much sooner than urban males. The latter allowed Batabyal to approach much closer suggesting that urban agamas were less flighty and more relaxed than rural agamas, even though predation threats were not necessarily different.

“I feel they [urban males] are actually more habituated to human presence and that is why they don’t consider humans to be potential predators and thus let you approach much closer to them,” Batabyal speculated, adding that urban lizards also had several hiding places, thanks to human construction and debris in empty plots of land.

“These lizards have learnt to use the urban landscape to their advantage and thus can spend more time outside and when really needed can quickly hide,” added Batabyal.

Courtship in the city

When matters of food and safety are dealt with, animals typically focus on their reproductive goals. Like most animals, adult male rock agamas become extremely colourful during the breeding season. Richly hued males attract the attention of females and rival males, signalling their superior prowess and territory size to both. But unlike most other animals, Batabyal and Thaker discovered that these lizards could actively change the colours they produced.

The males would become orange on their back and black on their sides, belly and all four limbs when displaying to females. But when a rival male appeared on the scene the courting male would go from orange to yellow on the back and from a black to bright orange on the belly.

These colour shifts can be rapid. The lizards would typically start changing colour within 10 seconds of a rival male or a female turning up.

“Till this time only chameleons were known to show such dramatic colour change among reptiles, so this was a major finding,” said Batabyal.

Batabyal found however that compared to rural males, urban male agamas were much slower to change colours when a female appeared. Their mating colours were also less rich compared to the rural lizards. These colour differences matched their other behaviours; urban males were also more reticent in their interactions with females. They displayed less to females than rural males did.

The lab then went one step further and tried to understand this behaviour from the “inside out.” “Behaviours like courtship or aggression cannot be expressed unless specific hormones are expressed,” explained Thaker. “Inside out means, I need to not just look at the outcome but the process that generates that outcome.”

To understand what inside the male agama was driving their behaviour, in experiments, the researchers introduced the rural and urban male agamas to female suitors and male rivals, and then measured two hormones. Testosterone, the sex hormone and corticosterone, the stress hormone. Thaker explained that during the breeding season, animals like rock agamas routinely maintain high levels of testosterone. High levels help the males to react quickly to any mating opportunities or fighting, so that they can make the most of a short, intense breeding season.

Corticosterone is elevated after any stressful situation to make sure that the body can mobilise energy to recover from the stress situation and then to bring it back to homeostasis or equilibrium. This stress can also come from aggressive social interactions. As expected, all the test subjects spiked up their testosterone levels when they saw both rivals and suitors. But while rural males maintained these high testosterone levels as Thaker had explained, urban males quickly brought down the testosterone levels rapidly after any interactions.

More interestingly, even before any stressful social interaction urban males already had much higher levels of the stress hormone corticosterone than rural males. And after social interactions with females and rival males, urban males had to produce even more corticosterone for their body to recover.

“Which means,” said Thaker, “it takes more corticosterone to maintain homeostasis in a lizard in the city. Which means they’ve already shifted their physiology to a world that’s more stressful. And it takes even more for them to recover from social interactions.”

Could this mean that the urban males were participating somewhat half-heartedly in the mating game? Not trying too hard with a female or being too aggressive with a rival male?

Batabyal is not sure. “As the territories are quite big in [sic] rural males, they need to be on their toes to keep the females in their territory and also fight off other males who might invade,” she said. She also pointed out that urban males were restricted to smaller territories and more crowded conditions than rural males which might affect their interactions.

“It might be that having duller colours or being less responsive does not really matter because they always have females available and they have learnt to share resources with other males as well, so they don’t fight all the time,” said Batabyal. “Also, the urban habitat is divided in such a way that the lizards are stuck to these small pockets and don’t have an option to go and look for other suitable territories very well. Thus, they are stuck with the neighbours they have,” she added.

Health in the city

Amdekar agrees that the proximity might play an important role in the male lizards and found some physiological basis for this. Amdekar decided to compare the health of the urban and rural izards to see if differences in behaviour matched with differences in physiological health.

She measured the body condition (i.e. weight and length) of the lizards from both habitats for parasites. She checked them for parasites and measured their immune response and the amount of plasma testosterone.

Straight off, urban males showed a lower level of testosterone in their blood compared to rural males, which Amdekar suspected supports Batabyal’s point. “If testosterone levels are high, males may engage in more fights and this can be physically costly to them. We speculate that having lower testosterone levels may be a mechanism to avoid the costs of constantly engaging in social interactions.”

Again, Amdekar found no major health cost to the urban male agama living human habitats. “I almost expected to find urban lizards in extremely poor health compare to rural lizards. It was interesting that it was not the case and the urban and lizards differed in only some physiological measures,” she said. Indeed, urban males had largely similar immune responses and ectoparasites as rural males. There seemed to major negative effect to the health of these lizards. “This was interesting to me and re-instated the importance of studying both behaviour and physiology.”

Kristin Winchel, a postdoctoral researcher from the Washington University, St Louis, who is not connected with any of this work, said, “I thought the use of physiological measures to complement traditional (body condition) metric of health was novel and a great idea.”

Winchell studied a lizard species called the Puerto Rican crested anole lizards in urban and forest habitats of the island of Puerto Rico, found some similarities. “The take-home from both of these studies seems to be that lizards that do well in urban environments are not in ill health,” she said.

Although these results suggest that urban rock agamas were indeed adapting to urbanisation, Winchell proposed other explanations could not be ruled out. “An alternative hypothesis could be that lizards in the urban environments have not changed at all because there is no reason to (i.e., the environments do not differ in ways that matter for the health metrics tested).” She also wondered if these health results would be consistent if the lab had studied multiple populations of urban and rural lizards.

Perhaps these could be future questions for the Thaker lab. Thaker emphasised that these lizards were likely to hold her lab’s attention for a while. “The fact that there’s so much variation is interesting to us,” she said. “And our job as ecologists is to understand how the variation comes to be and whether that variation matters. We’re having fun trying to understand the colour. We know that their behaviours are changing. Anu [Batabyal] is already working on how smart they are. So, we know that cognition is different in these two places. This lizard [urban] is different from every aspect we look at.”

While they explore more questions, how can cities like Bengaluru retain their rock agamas? Amdekar suggested retaining areas in the city which resembled their natural habitat, “areas with rocks and boulders, and scrub vegetation.”

Thaker felt it could be even simpler. “So, if you don’t pave everything, we leave some soil so they can put eggs down and if we don’t destroy the insect community with pesticide or remove all plants these lizards will coexist with us. It’s perching on walls! Which means we can still build without too much of a problem,” she said. “And that is wonderful because they are really interesting, very beautiful, iconic animals in the city. It’s nice to see that they are coping, because there’s a lot of hope that they will be around for a very very long time. We should just not muck up the environment to a point where we lose them.”

CITATION

Batabyal, A., & Thaker, M. (2019). Social coping styles of lizards are reactive and not proactive in urban areas. General and comparative endocrinology, 270, 67-74.

Winchell, K. M., Briggs, D., & Revell, L. J. (2019). The perils of city life: patterns of injury and fluctuating asymmetry in urban lizards. Biological Journal of the Linnean Society, 126(2), 276-288.

Amdekar, M. S., Kakkar, A., & Thaker, M. (2018). Measures of health provide insights into the coping strategies of urban lizards.

Batabyal, A., & Thaker, M. (2017). Signalling with physiological colours: high contrast for courtship but speed for competition. Animal Behaviour, 129, 229-236.

Batabyal, A., Balakrishna, S., & Thaker, M. (2017). A multivariate approach to understanding shifts in escape strategies of urban lizards. Behavioral ecology and sociobiology, 71(5), 83.

Balakrishna, S., Batabyal, A., & Thaker, M. (2016). Dining in the city: dietary shifts in Indian rock agamas across an urban–rural landscape. Journal of Herpetology, 50 (3), 423-428