Endemic to Madagascar, radiated tortoises are Critically Endangered due largely to poaching for the illegal pet trade

Looking at how corticosterone changes in a tortoise, scientists uncover two distinct personality types in the radiated tortoise

Biologists argue that individual animals consistently react to different circumstances based on their personality

A 350-kilometer drive away from the frenzy of the nearest city, the thatched desert village of Lavavolo, Madagascar seems to lie in infinite stillness. But homeostasis is never a given. Even this tiny, thatched town with its own sparse, spiny forests offers chaos, natural and manmade. In return, biology – and biologists – have developed a key survival tactic: the ability to improvise.

“There is almost no more remote a place than southern Madagascar,” Dr. Andrea Currylow, a conservation consultant and adjunct assistant professor at the University of Southern California said. “No power, no stores, no garbage dumps, nothing.”

Currylow hangs out here to study how radiated tortoises (Astrochelys radiata) – one of the world’s most endangered reptiles – deal with their surroundings. Even for southwest Madagascar’s endemic and venerated radiated tortoises, which locals say harbor ancestral souls, 15 million years of residency in these parts doesn’t free the species from existential threats. Locals slash-and-burn what’s left of the habitat, and poachers from outside Lavavolo systematically capture about 50,000 individuals annually for the exotic pet trade or to sell as rare meat for expensive palates. Generous estimates predict these Critically Endangered animals may hold out for another 20 years.

In a bygone era, radiated tortoises dealt with surprises all on their own. A nerve-wracking brush between two males during the breeding season might end with one disgraced loser flipped upside down. The kick of a lumbering zebu cattle can also send a tortoise flying, even crack their shells. Many species automatically unleash a slew of hormones in response to such indignities, including corticosterone, or CORT. A few minutes into a stressful event, CORT spills into the bloodstream, altering the function of various body systems. It allows hearts to race, directs white blood cells to damaged tissues, and can linger around long enough to stimulate appetites, so animals fill up in expectation of the next showdown.

Researchers often compare how much CORT exists in the bloodstream of males versus females, juveniles versus adults, or between animals in habitats with different levels of food availability or predators. Within these groupings, individuals might differ significantly in their levels of stress response, muddying the average. Variability isn’t necessarily the best news for a wildlife researcher hoping for clear numbers to describe male hormone levels, or to define how much a fragmented habitat changes species’ stress levels.

“I think your average endocrinologist, like your average scientist in almost any area of the life sciences mostly pays attention to average and means,” said Robert Sapolsky, a hormone scientist and neurology professor at Stanford University. “All that variability is [a] sign of, ‘Bummer, we need to do the experiment again’ or ‘I need to clean up the variables’ or ‘I’m never gonna get this grant if I don’t get the data cleaner.’”

However, Currylow’s latest look at radiated tortoises in Conservation Physiology reflects ecology’s increasing attention to correlated behaviors of individual animals and how behavioral types may survive in a changing world. Maybe variation in CORT is more than background noise. Maybe radiated tortoises have unique personalities worth exploring.

Lavavolo’s unpredictable conditions challenge biologists’ flexibility, too.

“If you want to do lab-oriented fieldwork, you gotta bring and make your lab with what you got,” Currylow said. “I once used the motor and charged battery from a dremel tool to spin the centrifuge drum when days of rain caused my [solar] power supply to drain. It’s a day-by-day, sometimes hour-by-hour problem-solving game.”

Currylow’s lab-on-wheels sought to discover how wild tortoises’ CORT levels responded to industry-standard handling procedures. Like many other chelonians studied before them, the Lavavolo tortoises suddenly found themselves flipped, measured, weighed, and epoxied with a radio transmitter. Unable to escape in the hands of a human throughout the 20-minute process, the tortoises had no recourse but to deploy their hormonal stress responses. The field crew drew a few blood samples to later isolate CORT and measure how its levels changed before and after the procedure. Currylow averaged those rates of change together to find the radiated tortoises’ general CORT response to handling.

Just as the speciously static landscape of Lavavolo seems to offer no change, at first glance, the CORT averages seemed to suggest that 20 minutes of handling did not create much of a stress response. Currylow was skeptical. The mean value didn’t come close to justifying the extreme variability in the raw data. Plus, she had two years’ worth of information on the same tortoises movement and activity around the habitat, and certain behaviors were linked, somehow.

“What I said to myself when I lumped all my data together to get that ‘golden mean’ to explain my study was; ‘really?’ I looked at [the] data and my bullshit detector went off. I sought another explanation for the CORT results and found that they correlated with all sorts of other ecological trends,” Currylow said.

Challenging the mean, she found that animals’ individual CORT levels differed so dramatically that they fit into either a “strong” or “mild” stress response category. Those in the “strong” response category had much more CORT in their bloodstream than the “mild” group even before handling. Currylow then averaged the stress response within both reaction types. The “strong” response tortoises’ CORT levels had shot up 131 percent after handling. The “mild” group’s had shot up 57 percent.

When an animal’s particular behavior in one setting consistently correlates to behaviors in other settings, that’s personality. The Lavavolo study found evidence for these correlated behaviors. There were the reactive personalities: tortoises whose CORT spiked significantly also seemed anxious and reactive in other areas of their lives. They were lighter for their size and more often found resting. They did not move around their habitat as frequently as the mild CORT group, but had larger home ranges. Conversely, the mild CORT tortoises proactively explored their environment, though they had smaller home ranges, and boasted denser, healthier body types.

With only nine tortoises, the sample size was small, but the findings did reflect researchers’ increasing attention to hormonal variation between individual animals and how it influences both species survival and a greater understanding of animal personalities.

Personality does not have to be genetically determined or lifelong, either. Currylow noted that some of the reactive tortoises were still growing into adulthood, a life stage when stress naturally runs high for many species (you know the feeling). Their home territories were perhaps larger because they were often looking for a peaceful place to grow, the study posits. Or, recovery from disease or stress over food and water might have caused others to wander farther over the course of the two years but conserve more energy and spend more time in one place from day to day.

“Animal personality” is no longer the domain of known charismatics, like Jane Goodall’s chimps.

UC Davis behavioral ecologist Andrew Sih wrote in a 2008 publication of Advances in the Study of Behavior, that the reason we know so much about the personalities of primates as individuals, is not “that they have ‘more personality than other animals,’” but, rather, because researchers studied the same few animals for so long and so closely that their personalities became glaringly obvious.

In the case of chelonian studies, researchers might miss the links between a behavior and physiological functioning, especially if studies are one-dimensional or brief.

“I am certain that without those other [behavioral] data, I would have completely overlooked any personality trends,” Currylow says.

The research also highlights an emerging view that studying a behavior in silos is not enough to actually understand it. Sih wrote that the traditional approach to studying one behavior at a time stems from a perspective that “natural selection favors optimal behavior in every situation.” However, animals don’t confront every issue successfully. Their personalities can enable them in some settings, limit them in others. If an animal is behaving in a sub-optimal way, it can help ecologists to know how that behavior might be tied to other personality characteristics.

For example, a shy, reactive tortoise in a relatively safe habitat might miss out on spotting a scrumptious shrub if it’s spending most of its time resting.

“It doesn’t always go one way, though,” Currylow said. “Those animals which are strongly reactive to stressors may avoid dangerous situations while others might not notice that they were about to be attacked.”

One of the takeaways for Currylow is the importance of differences between individuals.

“Simply having variation in whatever population you are investigating is always a good thing that should be strived for,” she says. “Variation is what allows evolution to work. It provides a source from which to draw from if something goes awry in a population.”

In southern Madagascar, personality variance only takes species so far. The human population boom engulfs the desert forest and the taste for forbidden meat and exotic pets indiscriminately depletes the endemic and sacred radiated tortoises. Thousands of tortoises confiscated from poachers constantly pour into the nation’s conservation centers, already at full capacity, requiring NGOs to quickly identify the least stressful relocation plan. Informed strategies concerning hormonal and behavioral differences become more important, while the opportunity to learn how personalities shape, and are shaped by, evolution becomes rarer, more precious.

“For my money,” Sapolsky said, “inter-individual variation is just the most interesting thing in biology.”



Banner image: Radiated tortoise at Arboretum d’ Antsokay, Toliara, Madagascar. Image by Bernard Dupont via Wikimedia Commons.

Citations:

Currylow, A. F. T., Louis, E. E., & Crocker, D. E. (2017). Stress response to handling is short lived but may reflect personalities in a wild, critically endangered tortoise species. Conservation Physiology. https://doi.org/10.1093/conphys/cox008.

Hudson, R. (2013). Troubled times for the Radiated Tortoise (Astrochelys radiata). https://doi.org/10.3854/crm.6.a13p67

Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How Do Glucocorticoids Influence Stress Responses? Integrating Permissive, Suppressive, Stimulatory, and Preparative Actions*. Endocrine Reviews.

Sih, A., Bell, A., & Johnson, J. C. (2004). Behavioral syndromes: An ecological and evolutionary overview. Trends in Ecology and Evolution. https://doi.org/10.1016/j.tree.2004.04.009

Sih, A., & Bell, A. M. (2008). Chapter 5 Insights for Behavioral Ecology from Behavioral Syndromes. Advances in the Study of Behavior. https://doi.org/10.1016/S0065-3454(08)00005-3