Anolis (Phenoacosaurus) heterodermus, a mainland anole that co-occurs with few or no other anole species
One of the most important questions in ecology and evolution is about the role of biotic interactions in driving phenotypic and behavioral changes across species. The insular Anolis species are a good model to address this kind of question due to their high abundance and pervasive ecological interactions across islands. Some insular species, however, live in isolation on small islands across the Pacific and Caribbean islands (21 species). These species have evolved similar morphologies across islands. For instance, Poe et al (1) found that body size evolved by exaptation (remember the classic Gould and Vrba 1982 paper) to colonize these small (and depauperate) islands successfully. By contrast, Poe et al. (1) showed that sexual size dimorphism (SSD) evolved by adaptation likely after island colonization to minimize intraspecific competition.
In brief, these solitary insular anoles evolved phenotypic (body size and SSD) traits by two different processes. Cool! But, what happens in mainland areas? Much work has been devoted to Caribbean species, but the mainland offers many more species and very little research has been conducted there to understand ecological and evolutionary processes. So, we decided to establish whether solitary ecology can be extended to mainland species or whether it is an island ecological phenomena.
The first problem that we had to resolve was trying to establish whether mainland species tend to live in geographical/ecological isolation as insular species. We adopted a novel concept in macroecology (the diversity field concept) developed by Mexican macroecologists (Hector Arita and Fabricio Villalobos see 2, 3) implemented here using extensive distributional information for almost all known Anolis species (377 spp), which I generated during my Ph.D. thesis (see 4 for an example using these maps). The diversity field concept allows us to establish how many species co-occur with a given species across its geographic range.
We calculated how many congeners can co-occur within the distributional area of each Anolis species using the range maps (see figure below). We divided mainland species into two groups: those co-occurring with few congeners (i.e., “solitary-like”, I had to say that his term did not like to reviewers, so we used a “species-poor” forms in the paper). Then, we test whether these “solitary-like” mainland species are different from other mainland species using a randomization approach. Our results revealed that “solitary-like” mainland species exhibit different traits from random mainland assemblages. These unique traits (i.e., uniform body size and greater SSD) suggest that solitary ecology from insular anoles can be extended to mainland settings.
Figure. Diversity fields for some Anolis species. Note that the diversity field is the set of richness values of co-occurring anoles inside each distributional area.
The next question was focused to establish whether similar (ecological and evolutionary) processes affected body size and SSD patterns in a similar way. We found that the phylogenetic position of body size and SSD shifts did not coincide and also with the evolutionary transitions to solitariness (i.e., reduced level of sympatry). We suggested that both traits are decoupled across the entire Anolis radiation and likely that both traits evolved exaptatively. In other words, it is possible to think that “solitary-like” species retained body size and SSD from their most recent common ancestors to facilitates the lonely life.
The paper is very short (less than 2500 words) and was published in the May number of Biology Letters(5).
In the most recent issue of Nature Ecology & Evolution, first-author Rob Pringle gives the inside skinny on the recent paper about the interaction of predation and competition among lizards (see the video description of the study).
Herewith, the essay:
I was heavily influenced by a handful of papers that were published during my first few years of graduate school. Some of these — Fine et al. (2004) on how herbivores promote habitat specialization in trees, Rooney et al. (2006) on food-web structure and stability — resonated because I could connect them to problems that I was working on. Others, such as Schmitz et al. (2004) on the ecological importance of predator-avoidance behavior, made an impression because they seemed to herald seismic shifts in the outlook of community ecology. And then there was a set of papers that captivated me with their sheer elegance: beautifully designed and executed field experiments that inspired me and made me jealous.
A string of papers by Tom Schoener, Dave Spiller, and Jonathan Losos belonged to this last category. There was a new one each year, with titles like “Predator-induced behaviour shifts and natural selection in field-experimental lizard populations” (2004) and “Island biogeography of populations: an introduced species transforms survival patterns” (2005). These studies used tiny cays in the Bahamas as arenas for a simple yet powerful experiment. On some islands, the investigators had introduced top predators — curly-tailed lizards (Leiocephalus carinatus), which occurred naturally on larger islands just a few stone-throws away from the experimental islands. A major aim of this work was to understand how the introduced predators affected populations of brown anoles (Anolis sagrei), which were native to the experimental islands.
The results were dramatic. Curly-tailed lizards are stocky, ground-dwelling animals, and they devastated brown-anole populations. The brown anoles that survived did so by climbing into the vegetation, beyond the reach of the curly-tails, and this behavioral shift was associated with natural selection on hindlimb length — an evolutionary consequence of predator-avoidance behavior. When I was a kid, we used to play a game called ‘the floor is lava’; if your feet touched the ground, you were dead. It seemed kind of like that for the brown anoles on these islands.
Left: Brown anole. Right: curly-tailed lizard. Photos: Jonathan Losos and Kiyoko Gotanda.
When I started a post-doc at the Harvard Society of Fellows in 2009, I met Losos and we started discussing ideas for a new experiment. I thought that a minor innovation on the earlier experiments could open up new conceptual territory. Losos said that he’d been wanting to do the same thing for years. To wit: if we introduced not just curly-tailed lizards, but also a second species of anole — green anoles (Anolis smaragdinus) — then we could ask questions about predation, competition, and the interaction between the two. Among other things, this design would enable us to test classic ideas about how predators affect the ability of competing prey species to coexist.
Green anole, characteristically perched on a thin branch in the canopy.
The risky thing about this idea was that so much of it had already been done to one degree or another. Previous work had painted a rich picture of the interaction between curly-tailed lizards and brown anoles — our odds of discovering something new on that front were low. And there were dozens of studies about competition between sympatric Anolis lizards. The novelty of our approach hinged on the interaction between predation and competition, which was a thin thread on which to hang such a massive undertaking. But I felt supremely confident that the experiment would work. Todd Palmer, Rowan Barrett, and a raft of other collaborators must have been confident too, because they joined me in setting up and monitoring the experiment.
Left: Aerial view of island 926; at left is a larger island, similar to those where we collected green anoles and curly-tailed lizards for introduction onto the experimental cays. Right: Naomi Man in ‘t Veld conducts a population census; squirt guns with water-soluble paint were used to mark lizards from a distance. Photos: Day’s Edge Productions and Kiyoko Gotanda.
By 2013, two full years into the study, my confidence was giving way to panic. I had started a job as an assistant professor in 2012; I was anxious about my professional survival, and I had ploughed large amounts of time and money into an experiment that did not seem to be working after all. The introduced curly-tailed lizards were firmly established in their new homes, and the brown anoles were responding by becoming more arboreal, as previous work had indicated they would. But the introduced green-anole populations seemed to be struggling. It looked as if they might die out, in which case our experiment would amount to a very expensive confirmation of the earlier work by Schoener, Spiller, and Losos. Our project had some original twists — Tyler Kartzinel was spearheading an effort to monitor the lizards’ diets using DNA metabarcoding — but it wasn’t at all clear that we would discover anything new or noteworthy.
Our break came in 2014, when it became clear that the green-anole populations were indeed thriving on some islands — just not on any of the islands with curly-tailed lizards. When we returned to the Bahamas in 2015, buoyed by the emerging results and freshly funded by the US National Science Foundation, we found that green anoles had disappeared on one island with curly-tailed lizards (the largest such island). Sometime during 2016, a second green-anole population vanished, this time from the smallest island with curly-tailed lizards. That left just two islands where green anoles still persisted in the presence of curly-tails, and one of those populations looked like it might soon join the list of casualties. Was this because the curly-tailed lizards were simply eating the green anoles to extinction on those islands? Probably not. The green anoles were highly arboreal; they rarely descended to the ground and instead moved by scampering through the twigs and leaves in the canopy. The chunky curly-tailed lizards, by contrast, lumbered across the ground, rarely climbing higher than 50 centimeters — and then only on the thickest of tree trunks. Indeed, the curly-tails didn’t seem to be eating many lizards of any kind. We saw them feasting on cockroaches, and occasionally snacking on fallen fruits and dead hermit crabs, but it wasn’t until 2016 that we finally saw one eat a small female brown anole. Isotopic analysis revealed that curly-tailed lizards actually occupied a slightly lower trophic position than did either anole species, which suggested that the top predator was subsisting more on insects than on other lizards.
Left: Curly-tailed lizard eating a cockroach; the lizard’s paint marks signify that it had been seen on the first two days of the three-day population census. Center: Mating green anoles were a welcome sight in 2013. Right: Green anole clinging to a thin twig, where we often found them, especially on islands with curly-tails. Photos: Kiyoko Gotanda and Rowan Barrett.
The more plausible explanation for our results was that the presence of curly-tailed lizards intensified competition between the two anole species within the predator-free arboreal refuges, and that this competition — not direct predation — was the primary reason why the introduced green-anole populations failed to increase on islands with curly-tailed lizards. Molecular analysis of fecal samples subsequently reinforced this impression. DNA metabarcoding produced evidence that curly-tailed lizards exacerbated the competition between brown and green anoles for insect prey. And a quantitative PCR assay — conducted by Charles Xu at the behest of one of the four very thoughtful reviewers for Nature — detected the DNA of brown and green anoles in just 4% of the curly-tailed lizards that we sampled. Curly-tailed lizards really were the top predators; they just didn’t catch anoles very often.
We concluded that indirect effects of the top predator destabilized the coexistence of competing prey species. In the landscapes of fear created by curly-tailed lizards, the clear niche partitioning exhibited by brown and green anoles on predator-free islands — a product of adaptive radiation — was no longer evident. Instead, these species were trapped together in the top story of the small islands, competing for the same space and food, afraid of getting burned by the hungry predators on the ground. Green anoles, despite being better adapted to arboreal life, got the shorter end of the stick (both literally and figuratively). This might be because brown anoles, as the incumbents on the islands, had greater strength in numbers. If we had introduced both brown and green anoles at identical starting numbers, would the green anoles have come out on top? Or, now that the combination of competition and predation has greatly diminished brown-anole populations, might green anoles stage a comeback? In 2018, we reintroduced green anoles on the two islands where they had been extirpated, with the hope of answering this question.
In any event, our findings ran counter to one of the motivating hypotheses of the project. Early studies, notably Bob Paine’s classic experiment in the rocky intertidal habitats of Makah Bay, suggested that predators tend to ameliorate competition between species at lower trophic levels by preventing any one species from becoming too abundant and excluding the others. Many ecologists, myself included, love this idea of ‘keystone predation’. Not only is it an elegant concept, but it also validates top predators as linchpins of ecological integrity. But when can we expect predators to play this role? In rocky intertidal communities, where keystone predation is a powerful force, sea stars feed on sessile invertebrates; but prey that are attached to the substrate have a limited ability to escape predators in space. In predator-prey interactions involving fast-moving prey that can rapidly adjust their behavior to avoid predators, I would expect keystone predation (sensu stricto, as opposed to the broader concept of ‘keystone species’) to be infrequent, and competition for enemy-free space to be both frequent and strong.
Left: The crew of the Sand Crab prepares to disembark on an island (from left: Naomi Man in ‘t Veld, Todd Palmer, Rowan Barrett, Tim Thurman). Center: When the Sand Crab got stuck at low tide, we had to walk (from left: Palmer, Pringle). Right: When the seas were rough, we contemplated our own mortality (from left: Palmer, Man in ‘t Veld, Pringle, Thurman). Photos: Kiyoko Gotanda and Rowan Barrett.
It has now been almost a decade from the conception to the publication of this work. What started out as a post-doc project has become an enduring annual ritual, and one that I have (usually) been able to enjoy thanks to a talented group of collaborator-friends: Palmer, Barrett, Kartzinel, and Xu, along with Tim Thurman, Kena Fox-Dobbs, Matt Hutchinson, Tyler Coverdale, Josh Daskin, Dominic Evangelista, Kiyoko Gotanda, Naomi Man in ‘t Veld, Hanna Wegener, and Jason Kolbe — and, of course, Schoener, Spiller, and Losos.
The research team left it all on the field. Tim Thurman (left) required stitches after one nasty fall; later (center), he was possibly sick (or simply didn’t want anybody to steal his water). Todd Palmer (right) was forced to become arboreal in his search for green anoles. Photos: Rowan Barrett and Kiyoko Gotanda.
The interdisciplinarity of this team enabled what is to me the most satisfying feature of our work. We were fortunate to have access to a replicated set of small cays on which to manipulate species composition. That is a rare opportunity and would have made for a nice study in itself. But by also integrating molecular assays (to quantify diet composition and intraguild predation) and stable-isotope analyses (to quantify trophic position and food-chain length), we were able to gain deeper insight into the mechanisms underlying the population dynamics. Indeed, without these additional assays, our suppositions about the relative importance of consumptive and non-consumptive effects would have been equivocal at best. Molecular techniques have fully entered the mainstream of ecology over the past decade, yet they are still rarely paired with the kind of manipulative field experiments that so inspired me as a first-year graduate student. The fusion of sound natural history, rigorous experimentation, and forensic mechanistic exploration offers tremendous power to resolve the kind of messy complexity that has long frustrated ecologists.
New paper in Nature examines the interaction between green anoles and brown anoles, and how the presence of the predatory curly-tailed lizard changes the balance. See also the commentary by Os Schmitz.
This colorful story in rhyme, for both children and adults, will put a smile on your face. You will observe the flamboyant Anatoly flaunting his magnificent dewlap to his female fan club and learn lots of solid facts about these fascinating and abundant little Floridian lizards.
When showing off, with his push-ups and head nodding, there is a crisis when he hits his dewlap on a rock. That red and yellow dewlap of his is now black and blue and he is more than depressed about it. His chance encounter with a Monarch butterfly sets him on the right path toward improving his character and not relying on looks for his popularity.
Yale Undergraduate Fiona Reed has designed a website in which you can answer a few question and determine which anole ecomorph you are. Give it a try! And then tell us what you are?
This is the best picture I took of a suspected A. pulchellus at Punta Borincua. The coloration and size seems consistent with A. pulchellus. Anyone think it might be something else?
This is the best pic I could get of what I believe is an A. stratulus at Punta Borincua. Note the single yellowish stripe down the back with black bars above the base of the tail. Does anyone know the identifying characteristics of A. stratulus?
Most visitors to Cayman Brac will likely not have noticed one of the island’s now established transplants: the Maynard’s anole.
This non-native lizard spends much of its time just out of eyesight, perched in the tree branches where its bright green colour blends with the foliage. The elusive anole, originally from Little Cayman, has captured the interest of researchers, intrigued by the insight the species can offer about evolution in island ecosystems.
And the Maynard’s anole is not the only island-hopping lizard on the minds of Cayman Islands researchers these days. While far from the invasive status of the prolific green iguana, the brown anole is also creating questions about the potential impact on Grand Cayman’s native blue anole.
Through separate studies – one carried out by Caymanian researcher Vaughn Bodden and another by National Geographic Society grantee Inbar Maayan – biologists are getting a better idea of how invasive species adapt and populate new territories.
Maynard’s anole in Cayman Brac
While the Maynard’s anoles in Cayman Brac are not far from their native home, Little Cayman, the lizard sheds light on how invasive species colonise new habitat.
Fortunately for Cayman Brac, the Maynard’s anole does not appear to pose a threat to the native Cayman Brac anole and has not shown potential for hybridisation.
“Based on similar invasions on other Caribbean islands, we expect the potential for a negative impact to be low. The native anole in Cayman Brac is found low on tree trunks and on the forest floor, while the introduced anole is predominantly found on upper tree trunks and in the canopy so direct interaction between the two species should be limited,” said Bodden, who studied the species while completing his bachelor’s in conservation biology at the University of Plymouth. He is now completing his master’s in biodiveristy and conservation at the University of Glasgow.
“Any impacts on the native anole are more likely to be indirect, such as a shift in habitat use to further avoid interacting with the introduced anole,” he added.
Researcher Inbar Mayaan captures lizards in Grand Cayman. – Photo: Jane Hakkonsson
The Maynard’s anole, first spotted in the Brac in 1987, does show signs of adaptation, however, when compared to its counterpart in Little Cayman.
Through fieldwork capturing and analysing the anoles in both Sister Islands, Bodden’s team, assisted by University of Plymouth lecturer Robert Puschendorf, found some interesting differences in their morphology and ecology. While the team hypothesised that the introduced anole might have developed longer hind legs – a trait that can aid dispersal and movement – their findings did not support this. In fact, they found much the opposite. The anole had instead developed longer forelimbs.
“Potential explanations for the rapid divergence could be that the founding individuals of the introduced population had a unique phenotype and these characteristics became exaggerated over time through the process of genetic drift, or that some habitat use characteristics that we did not measure on Cayman Brac are driving the morphological adaptation,” Bodden said.
Another interesting discovery about the introduced anole population was the presence of a parasite not previously recorded in the Sister Islands.
The source of this parasite remains unclear.
“The ectoparasites we found infecting A. maynardi [Maynard’s anole] have not been recorded in the Sister Islands, so this study provides the first evidence of its presence there. It is unclear whether the parasite species is native to both islands, invasive to both islands, or co-introduced from Little Cayman to Cayman Brac with its host,” Bodden said.
The Maynard’s anole is native to Little Cayman but introduced to Cayman Brac. – Photo: Vaughn Bodden
“We found that the introduced population [in Cayman Brac] had a reduced ectoparasite prevalence compared to the native population [in Little Cayman].”
The further researchers ventured from long-settled habitats, the lower the prevalence they found of the parasite.
This is something that may have benefited the introduced population and encouraged colonisation.
While the origin of the anole’s introduction to Cayman Brac is unclear, its presence there sends a reminder about the importance of safeguarding borders.
Due to the islands’ prevailing easterly trade winds, Bodden suspects the lizard had human rather than natural assistance in its introduction, possibly as a stowaway in a flight or boat.
“This is a unique situation where we have a species endemic to one of the Cayman Islands being introduced to another one of our islands. Fortunately, this introduction is not a major threat to the ecosystem in Cayman Brac, but it highlights the need for more vigilant bio-security control at our ports,” Bodden said.
“Unchecked cargo transportation provides a route for other invasive species, such as the green iguana, to be transported into or between the three islands.”
A female blue anole perches in Grand Cayman. – Photo: Inbar Maayan
Brown anole in Grand Cayman
Theories about how the brown anole, found endemically in Cuba and the Bahamas, arrived in Grand Cayman reinforce the call for careful biosecurity measures at ports. While researchers do not know exactly how the anole arrived here in the 1980s, its prevalence in the western end of Grand Cayman hints that it may have arrived through shipping.
Although Maayan, currently a Ph.D. candidate at Harvard University, did not find brown anoles in the numbers she had expected, she warned of complacency when it comes to invasive species.
“I was expecting them to be more of a problem than I saw, but it speaks to the importance of monitoring introduced and invasive populations,” she said.
Maayan said the brown anole should not be considered invasive in the same sense as the green iguana. But she cautioned that at a time, even the green iguana’s population numbers were much lower than they are now.
Much of the findings of her Grand Cayman research is not ready to share with the public, but she shared a few takeaways from her time on island.
Maayan described Cayman’s native blue anole as an incredibly charismatic and stunningly beautiful animal.
“They are a good ambassador for the Cayman Islands,” she said.
Maayan was interested in whether the presence of the brown anole had led to changes in the native anole’s habitat or physical characteristics. Physical changes in leg and head size, for example, could communicate competition between the species for habitat and resources.
An invasive male brown anole in Grand Cayman – Photo: Inbar Maayan
“The reason why these [island] species introductions are particularly useful is they mimic what we would see in evolutionary time,” she said.
“It gives a glimpse in a natural setting of when species come into contact and compete.”
With the help of local researchers, including Vaughn Bodden, Morgan Ebanks and Jane Haakonsson, she scouted out sites where just the Grand Cayman anole lived and sites where both species lived, for comparison.
Finding the brown anole was not as easy as she expected, however. While the lizard is found abundantly in Belize, where it is also an invasive species, this was not what Maayan observed in Grand Cayman.
Researchers sampled two sites heavily, taking data from more than 200 lizards. The team took data on habitat use of both species, and took measurements of the blue anole’s physical characteristics.
Maayan’s next step will be performing DNA analysis on the lizards to determine the level of migration and morphology.
Fortunately for the Grand Cayman anole, Maayan’s initial findings show little impact on how the lizard interacts with its native habitat.
While the brown anoles seemed to prefer perching in lower, sunnier areas, the Grand Cayman anole stuck to shadier natural areas. It would appear the lizards have adapted to separate habitats.
The full findings of Maayan’s research are expected to be released this summer, after the study has been reviewed and published by the National Geographic Society.
Anole Annals‘ woman in Florida, Karen Cusick, has photo-documented more interesting anole behavior (Karen has observed and photographed much interesting green and brown anoles behavior. Search this site for her name or “Daffodil’s Photo Blog” and you’ll find all kinds of interesting observations). oday I saw something I don’t think I’ve seen before, and I’m sending you a few photos. A big male brown anole was sitting in the sun on the upper rail of the fence when a big male green anole approached. He stopped about 6 inches away from the brown anole, and started bobbing his head and displaying his dewlap. The brown anole watched but didn’t react. The green anole moved closer and displayed again while the brown anole watched. Just as I was wondering if there would be a fight, the green anole suddenly ran past the brown anole along the rail and then down off the fence.
