Q&A Blog | World Lizard Day
Stanley Fox
Check out this World Lizard Day Q&A blog with Dr. Stanley Fox, an emeritus regents professor at Oklahoma State University and a true trailblazer in field experiments that reveal the intricacies of lizard societies, from development to evolution! Learn all about Dr. Fox’s experiences with being an avid researcher with contributions extending beyond lizards and spanning the herp community ecology, amphibian conservation, and the pressing influence of climate change on South American lizard populations.
Q&A Blog
Published August 14, 2023
All images provided courtesy of Dr. Stanley Fox.
Take a look at Dr. Fox’s homepage to learn more about his research and work!
As a scientist, what led you to study the field of herpetology? How did you find out you were interested in science and herpetology?
When I was a youngster growing up in rural northern Illinois, USA, I wanted to be a scientist, a detective, or a minister when I grew up. When I was maybe 7-8 years-old, I performed my first scientific experiment. I buried a pancake just outside our property and every day for maybe a week I dug it up to see what had happened. There was no replication, no control, no hypothesis, just a scientific curiosity. I guess the pancake began to deteriorate in that week until I could no longer find it; or maybe some wild animal dug it up and ate it. I don’t remember. But I still remember it was my first SCIENTIFIC EXPERIMENT. Then a few years later my mother received a call from our local pharmacist concerned that I might be making a bomb because I had bought some very fine powdered charcoal and some talcum powder at the drug store. When my mother asked me about this I told her, no bomb–I was dusting various surfaces for fingerprints: white talcum powder for prints on dark surfaces and black powdered charcoal for prints on light surfaces. I was playing detective. But note I was still oriented toward the scientific study of crimes, i.e., forensics. I lived on a huge plot of natural land with fields, forests, streams, and wildlife—an Illinois Tree Farm. My father was the managing forester of this land and also oversaw a sawmill there. My favorite pastime in all seasons was to walk that land, sometimes, fishing, sometimes hunting, but always observing the flora and fauna. In high school, my favorite class was biology and I loved dissecting animals. I even devised an apparatus from instructions in the section “The Amateur Scientist” at the back of every Scientific American magazine. This was an apparatus to measure the twitch of a leg muscle dissected from a recently sacrificed frog. I also devised a project with tissue culture, using muscle tissue from a house sparrow I had just shot with my BB gun and Petri dish plates spread with a blood agar for the tissue to grow on. I got the blood at the local hospital, probably not something you could do today! I majored in biology in college at the University of Illinois and remember when I was a Junior there, struggling to decide if I should focus on Ecology and Behavior or Molecular Biology. It was a struggle, but my heart won out and I pursued Ecology and Behavior and never looked back. The next summer, I got the opportunity to travel with my advisor and one of his graduate students to Churchill, Manitoba, Canada, on the Hudson’s Bay. The graduate student and I stayed the whole summer, but my advisor had to return to the university. While there, I designed and carried out a study of relative aggression of the Meadow Vole and the Collared Lemming. I even published it with my major advisor in a peer-reviewed journal, my first publication! My interest in herpetology surfaced at an early age. I grew up in northern Illinois and there were no lizards there, and very few snakes. That area is still called the “Great American Snake Desert.” There were turtles, frogs, and salamanders, but no lizards. Nevertheless, I was fascinated by lizards and procured one via a catalog order (none of the local pet stores had lizards back in that time)—a Green Anole. I remember when it arrived in a ventilated box in the mail that I excitedly dumped it into the bathtub to observe it. Fortunately, it couldn’t climb the slick tub walls, even though this species can climb up plaster or brick walls and other vertical surfaces. From my favorite nearby forest, I set up a beautiful terrarium with mosses, rocks, water, bark hides, and even a tiny pine seedling. The lizard’s favorite perching place was that tiny pine. Whenever our family would take vacations out West, I would always watch for lizards and even hand-capture them, or try to. In graduate school, I wanted to demonstrate Natural Selection, which at that time was thought difficult within a small time frame. I started off thinking to work with small mammals, but small mammals are hard to observe, mostly underground or in grass tunnels. Then I thought about birds, they are easy to observe. But they fly away. So I latched on to lizards–perfect, they are diurnal and easy to observe, they don’t fly away, and in fact usually stay their whole life in a small area. I completed my PhD dissertation on side-blotched lizards in West Texas, and demonstrated natural selection at three levels: genetic, morphological, and behavioral. I stayed with lizards all my career, with occasional forays off into frogs, snakes, turtles, and salamanders.
Left: Side-Blotched Lizard in Texas, USA (photo by Stanley Fox). Right: Chilean Liolaemus leopardinus mother caring for its offspring (photo by Stanley Fox)
Could you elaborate on your investigations into tail autotomy in lizards and how you are exploring the possibility of the tail’s role as a status signaling badge? What implications might this have for understanding lizard behavior?
It is well-known that body size is often closely related to dominance or successful defense of a territory in many kinds of animals. Lizards have long tails and many species have tail autotomy, the ability to release the tail if bitten by a predator, leaving the predator with just the tail while the main part of the lizard runs off and hides. Then over time, the tail regenerates (but never the backbone) so that it can be lost again if the need arrives. I got to thinking, in addition to the cost of reduced running ability without this organ of balance and perhaps loss of fat stored in the tail, perhaps another cost to tail loss is loss of social status, loss of dominance. So I performed some simple experiments, first establishing in laboratory dyadic encounters which lizard in size- and sex-matched replicate pairs of side-blotched lizards was dominant and which was subordinate. Then I allowed the dominant lizard to autotomize a good part of its tail following the simulated bite of a predator. I froze the tail and let all lizards recover for two weeks. Then I reintroduced the pairs in laboratory encounters to measure social status. Sure enough, the previous dominant lizard who had lost its tail significantly fell in social status. Then I waited for another two weeks and then reattached (glued) its thawed tail back to the tail base (regeneration takes several months). Control lizards were previously dominant lizards that lost their tails but did not get them glued back. Lo and behold, among females, the former dominant who lost its dominance once it lost its tail, regained its dominance when it got its tail back. Now, the tail was dead and could not be used in any way, but it gave the appearance to an opponent that she was facing a big adversary and gave way. So the tail can be interpreted as a status-signaling badge, something like a colored throat patch on some lizards, a badge because it is cheap and easy to manufacture, but powerful as a signal that the bearer is not one to be messed with. The lizard with its long tail casts a powerful signal of large body size, and since the tail is much cheaper to make than the whole body, or bulk of the lizard, it can be viewed as a status-signaling badge. Incidentally, it has been shown in other species that the bearer of a status-signaling badge still has to have the wherewithal to be dominant; in other words, an animal cannot just manufacture a cheap badge and expect to be respected. It has to have the other elements, like aggressiveness or fighting ability, to be dominant. But the badge helps to settle disputes quickly and without costly, escalated fighting. I mentioned that this regained dominance following tail loss and artificial replacement happened in females, but not males. Why? It turns out that dominance is integral to fitness (reproductive success, number of babies sired) in male side-blotched lizards in West Texas; they need to be dominant to secure a good territory and attract females. Females, however, will be courted and fertilized no matter what. Dominance is not that important to their fitness and they use the lack of a tail–really the total appearance of smaller body size–to signal that they can adopt an alternative subordinate social role and occupy inferior habitat. They don’t need to fight to gain a high social status because they will be fertilized and produce offspring no matter what. In addition, they can reduce injury risk and save on energy if they don’t engage in energetic fighting over social status. Males, on the other hand, must have high social status to increase their fitness—they don’t have alternate social roles—and tend to ignore the loss of the tail of an opponent as a signal of lowered social status.
Marking a Side-Blotched Lizard in the field in Texas, USA (photo by Matt Anderson)
As you’ve researched herp community ecology, particularly turtle communities, what ecological factors have you found to be influential in shaping these communities, and how might these insights contribute to conservation efforts?
Turtles, like animals in any community, need certain ecological or habitat conditions in order to survive, grow, and reproduce successfully. Some turtles need deep, slow water, while others need fast-flowing riffles. Some turtles are carnivores and some are omnivores or herbivores. Some need to bask a lot and so need floating logs or other basking places, whereas other species don’t. Subsequently, for a healthy diverse turtle community, one needs a diversity of habitats and microhabitats. If habitats are removed, changed, or degraded, elements (species) of the turtle community will greatly diminish or even disappear. Habitat alteration by humans, e.g., damming or channelizing streams or rivers, removing debris and floating logs, removing or altering streamside vegetation, fishing out certain fish species or introducing other fish species, facilitating heavy boating activity, plus many other anthropogenic activities, can greatly alter the habitats and microhabitats of turtles and negatively affect the turtle community. Turtles are long-lived, slow growers with slow replacement capacities and so are especially slow to recover from habitat loss or degradation. Another dimension that affects turtle conservation, probably more than other taxa, is that turtles are harvested for their meat or as pets, mostly being shipped overseas to foreign meat and pet markets. The negative effect on turtles is staggering. Many, many U.S. turtles are captured and sent to these far-away markets. If mostly the turtles are used for meat, like common snapping turtles and alligator snapping turtles, the largest individuals are preferred and removed. These larger individuals are the main breeders and those most responsible for maintaining the population. Consequently, population sizes fall and it takes a long time for younger age classes to reach larger sizes and take on the reproductive role of the big, removed turtles. Most states in the U.S. have realized this problem and made commercial turtle harvest illegal, but not all states, and commercial turtle trappers continue to harvest turtles (big and small turtles) surreptitiously.
Alligator Snapping Turtle (photo by Dan Moore)
With your knowledge of worldwide amphibian declines, what are some of the primary drivers of these declines, and how can society address and mitigate these threats?
As I mentioned in my answer above, habitat loss and degradation are the primary causes of the loss of biodiversity, and amphibians are no exception. It’s not just habitat loss, but also the loss of large tracts of habitat. Many species need unsegmented habitat to survive or to disperse from one patch of good habitat to another. For example, in pond-breeding frogs and salamanders, if some ponds are drained and filled in for farming or other human uses, then the average distance between ponds increases and individuals can’t successfully reach ponds that are too distant and separated by hostile habitat across which the frogs and salamanders can’t easily traverse. Additionally, many frogs and salamanders are philopatric, meaning that they come back to the same pond from which they themselves hatched and grew as larvae to breed as metamorphosed adults. What do they do if the pond no longer exists? An additional conservation threat unique to amphibians and not other taxa, is the appearance and spread of emerging infectious diseases that do not affect other animals. For example, a pair of fungal diseases like Bd (Batrachochytrium dendrobatidis) and B. salamandrivorans (Bsal), both chytrids that infect the skin of amphibians, cause infected animals to get sick and often die. Ranavirus is a viral disease that affects frogs. These diseases are found around the world and when they move through an area, they kill off many amphibian species; other species are not affected or affected very little. These amphibian diseases intrinsic just to amphibians, plus the normal threats of habitat loss and degradation, make amphibians the most endangered class of vertebrates. We have lost a third of our amphibian species on earth. What can be done to save amphibian species? It is possible to rid captive individuals of chytrid infections, so some species can be saved that way, followed by propagation in the laboratory. But many of the species under threat of extinction are poorly understood and not easy to breed in the laboratory, plus it is too many species for us to rely on this method. Often overlooked as a conservation measure applied to amphibians–because the threat of amphibian disease overshadows them–is the need to preserve habitat and improve habitat, i.e., habitat restoration. This, humans can do, and conservation groups worldwide are doing just that.
Taking a blood sample from a juvenile lizard without harm to the subject (photo by Stanley Fox)
You are involved in climate change research related to its effects on South American lizards. How are changing climatic conditions impacting lizard populations, and what measures can be taken to protect them?
There is no doubt that global climate change is seriously affecting our weather and climate, habitats, and the plants and animals that live in those habitats. Drastic natural climate change has happened before in geological history, but mostly happened way before humans inhabited earth and before the presence of the whole flora and fauna with which humans interact. This recent global climate change is human-induced, or anthropocentric. It is happening much faster than previous natural changes long ago before people even were around. In 1986, I completed a large field study of Liolaemus lizards along an elevational gradient in the Andes of South America when I spent my sabbatical year on a Fulbright fellowship in Chile. This was largely before the anthropogenic buildup of greenhouse gases and subsequent global climate change. The study exhaustively surveyed three study sites at 1,250, 1,980, and 2,760 m of elevation. We marked all the subjects on all three sites and characterized their social behavior, thermoregulatory behavior and thermal limits. Then under support from the National Geographic Society, we returned 30 years later (in 2016), after effects of global climate change had been in place. We resurveyed the same three sites and also three sister sites, each 200 m above its matching site. We observed some remarkable changes to the lizards and their thermoregulatory behavior, thermal limits, distribution, population sizes, and more. We expected to see that with increasing temperatures, species would move upslope in search of environments more like that to which they had evolved over the past thousands of years, and largely this is what we saw. Populations at the lowest sites had deceased the most, with all three species more abundant at the sister site 200 m higher. One species has almost disappeared from its original site. Populations at the highest site told a different story. These populations greatly increased in abundance and one species has even increased 23-fold, expanding into the original site from lower elevations where it had been found before. It has not reached the sister site 200 m above, however, Another species doubled its population size at the original site but is nearly absent 200 m above. The third species has also increased at the original site, but in 2016 was superabundant 200 m above with no competition from other species. In general, the lizards at the lowest sites have suffered the most, while those at the highest site have prospered and expanded their distributions upslope. Thirty years ago lizards at all sites showed a bimodal activity pattern with most activity in the morning. Thirty years later, activity at the lowest site was still bimodal, but with more activity in the late afternoon than in the morning. All six species increased their voluntary thermal maximal, four of them significantly so. Surprisingly, three species have significantly increased their body size, including the only two species that originally occupied the highest site. In summary, there have been numerous changes in elevational distribution, all upwards where the climate is more like it used to be before global climate change, and the lizards are now able to remain active at higher temperatures than before. All these changes also change the ecological dynamics of competition, predation, and resource use. Changes like these are happening all over the globe. There is little we can do about this locally other than protecting habitat and areas into which the lizards move, but the best thing we can do is to diminish our use of burning fossil fuels and emitting greenhouse gases into the atmosphere, which are responsible for global climate change and global warming. If we can indeed do this, our loss of biological diversity will be ameliorated.
Left: Liolaemus leopardinus in its natural habitat in the Chilean Andes (photo by Enrique Santoyo). Right: Juvenile male Collared Lizard with juvenile orange bars used in precocial sexual selection (photo by Stanley Fox)
In your field experimental approach, what specific techniques or methodologies have you found to be particularly effective in studying lizard behavior and ecology?
I firmly believe that animals should be studied in their natural environment and research should include experimental treatments in the natural environment whenever possible. However, the best research is that which also utilizes laboratory experiments and manipulations when multiple factors can be controlled. Nature is complex and it is hard to interpret results from field experiments when so many factors and variables can bias results. That’s why laboratory experiments are so important. But sometimes the results of laboratory experiments do not extrapolate to the field because important variables in nature do not exist in the laboratory. So, the best compromise is research that includes both and strives to make the laboratory experiments as naturalistic as possible.
Stanley Fox capturing lizards in the field in northern Oklahoma, USA (accidental photo from a game camera)
What are some of the most pressing questions or areas of research that you believe need further exploration in the field of behavioral and evolutionary ecology, specifically focusing on lizards and other reptile species?
Most of my career and interests have addressed basic questions, expanding our knowledge and understanding of evolutionary ecology, but I have also conducted applied research on conservation and human impacts on the ecology and behavior of reptiles, especially lizards. The disturbing thing about all this is that with constant threats to the very existence of many species, or less drastically, threats to the distribution and abundance of even many more species, using animals to explore and advance evolutionary and ecological theory is becoming more difficult because the very subjects are changing and even disappearing, and challenges to these animal species are constantly coming from anthropogenic pressures instead of natural ecological pressures historically important during the evolutionary history of these living things. This is not trivial, consider that we have lost a third of our world’s amphibian species in the last 40-50 years! Apart from this immediate concern, is the increasing study of variation in the field of behavioral and evolutionary ecology. We have transitioned from the study of fixed, limited topological categories of behavior and ecology to the study of variation of traits related to behavior and ecology. I hope this trend continues and grows. Variation is the root driver of evolution; even Darwin recognized this when he wrote The Origin of Species. Natural selection works only when there is variation. Let’s just hope there is enough variation in the traits and genes of contemporary plants and animals that most can adapt to the changing conditions humans have forced upon them. I know all of them cannot and many will disappear. But nature is strong and resilient, and I hope resilient enough to meet the anthropogenic challenges. OR, we can slowly diminish those challenges and learn to live with our natural world in a more harmonious state.