Javier Lobon Rovira, a graduate student working on geckos, decided to up his game and pay attention to anoles. Here’s what resulted! The lizards were found on 24th of August in the surroundings of Gainesville, Florida, displaying from a tree branch around one meter high. He found a second specimen close by sleeping at night on a small bush close to a water pond.
Photo: Kerry Ross, iNaturalist
Hello and welcome to my first post since officially starting as a grad student!
I think I’ve got my schedule down and we can get back to regular weekly anoles. Love that for us!
This week’s anole, Anolis gingivinus is also called the Anguilla Bank anole or Anguilla anole and is endemic to Anguilla and its satellite islands.
The Anguillan anole is reported to adapt well to anthropogenic effects on its habitat (Hailey et al, 2011) and to different niches, although its ecomorph affinities lie closest to being trunk-ground. They also seem to be abundant despite being heavily preyed on by American kestrels.
Photo: John Sullivan, iNaturalist
Male Anguillan anoles have an average SVL of 72mm and females have an average of 53mm. They are usually olive to greyish in colour with bright orange dewlaps, and have bold dorsal and lighter flank stripes. They also occasionally sport some green on their lower halves and males may have darker marbled spotting along their bodies. Anolis gingivinus are insectivorous but like many other anoles will eat smaller lizards.
Photo: Rozilber, iNaturalist
New Paper: Disentangling Controls on Animal Abundance: Prey Availability, Thermal Habitat, and Microhabitat Structure
DOI: https://doi.org/10.1002/ece3.7930
Above: Male Anolis bicaorum, endemic to the island of Utila (photo credit Tom Brown).
Why are there more anoles in this plot? This is the question that we continually asked ourselves whilst setting up our 2018 survey plots on the small island of Utila, Honduras, home of the endemic Anolis bicaorum (pictured above). So in 2019 we set out from Heathrow airport, kitted up with A LOT of equipment, for our second field season, based at Kanahau Utila Research and Conservation Facility, with one of the goals being to look into just that (see previous Anole Annals posts on Utila and its anoles).
Above Left: Getting ready to leave Heathrow (photo: Adam Algar). Above Right: Miraculously all the field kit all safely arrived at Houston stopover.
We all know that such factors as the thermal environment, prey resources and structural habitat play important roles in the lives of our beloved anoles. And we also know that you can go to one spot and be overrun with anoles, but go to a seemingly similar spot nearby and find none (usually when the field season is drawing to a close and you still don’t have a large enough sample size). But how are these aspects of anole biology linked? Specifically what determines their abundance, and its variation, at fine scales? While ecological niche theory is well developed, empirical evidence for which factors are most important, and how they interact, is still rare for many taxa, including anoles. Given rapid environmental change, understanding the drivers and mechanisms governing abundance is now more important than ever.
We measured the abundance of the endemic Anolis bicaorum across thirteen 20x20m plots along a tropical habitat gradient, using standard mark-recapture methods, based on Heckel & Roughgarden (1979). Within these plots, we also measured factors relating to the thermal habitat suitability (using 3D printed models fitted with iButtons), structural habitat (perch surveys), canopy cover (leaf area index) and prey availability (arthropod biomass and diversity). We then used N-mixture models and path analysis to disentangle direct and indirect effects of these factors on anole abundance.
Above Left: Emma setting up 3D printed anole thermal models. Above Right: Tom out collecting 3D printed anole replica models (photo credits Adam Algar).
We first decided on several measures for each niche factor which could determine the suitability of the habitat for the anoles. For the thermal environment, we first determined the thermal preference (Tpref) range of A. bicaorum, following Battles and Kolbe (2018). We then calculated two indices to quantify the thermal habitat quality of each plot. The first was the percent of model hours that operative temperatures (from 3D models) were within the Tpref range over the 36-hour study period for each plot. The second was the total number of degrees (°C) that the models deviated from the Tpref range across all models throughout the survey period for each plot, which included the total degrees, the degrees above and degrees below the Tpref range.
Above: Many of the anoles were “side-eye” pros
As a measure of structural microhabitat quality we determined both perch availability by counting surveys and the plot basal area (a measure of stand density), across all tree trunks, palm stems and fence posts in the plot.
Above: A. bicaorum predating on an unidentified spider (Araneae).
For prey availability, we measured arthropod biomass (g) and diversity (Simpson and Shannon’s) from a combination of leaf litter sieving and sweep-net samples taken in each plot. Sweep-net and leaf-litter samples were combined for plot level analyses.
We also measured mean leaf area index (LAI) in each plot using an Accupar LP80 ceptometer. LAI is the one-sided area of leaves per unit ground area and is a measure of canopy density; it is expected to influence thermal environment via the interception of solar radiation (Campbell & Normal 1998; Algar et al 2018).
After we determined reasonable measures of habitat suitability for each factor, we examined univariate relationships between A. bicaorum abundance and each of our habitat variables (percent of time within Tpref, deviation from Tpref, perch number, basal area, arthropod biomass, arthropod diversity and LAI) by including each predictor as a covariate in a multinomial-Poisson mixture model of abundance. The results of the most significant and strongest relationships can be seen in the figure below.
Above: Relationships between Anolis bicaorum abundance and individual niche metrics in forest plots across Utila, Honduras. Relationships were estimated using multinomial Poisson mixture models with a constant detection rate across plots. All variables are scaled to a mean of zero and unit variance; (a) reflects thermal habitat quality, (b) reflects structural habitat quality, (c) reflects prey availability and (d) reflects canopy cover.
We used these models to select a subset of these variables (one representing habitat structure, one prey availability, and one thermal quality) for subsequent path analysis; we also included LAI as the sole measure for canopy cover. We used the path analysis to evaluate the relative strength of direct and indirect effects on abundance. As we could not estimate indirect paths within a single multinomial-Poisson mixture model, we estimated abundance for the path analysis from a multinomial Poisson mixture model that included no environmental covariates, held detection rate constant, and permitted abundance to vary by plot. The results of the path analysis can be seen in the figure below.
Above: Direct and indirect effects of niche axes on A. bicaorum abundance. (a) Values are standardized path coefficients; line width is proportional to the strength of the effect, solid lines indicate statistically significant pathways. ε, unexplained variation. (b) The total effects of covariates on abundance. NP: number of perches; PB: prey biomass; LAI: mean leaf area index; TP: time within Tpref range.
Our results showed that thermal habitat quality and prey biomass both had positive direct effects on anole abundance. However, thermal habitat quality also influenced prey biomass, leading to a strong indirect effect on abundance. Thermal habitat quality was primarily a function of canopy density, measured as leaf area index (LAI). Despite having little direct effect on abundance, LAI had a strong overall effect mediated by thermal quality and prey biomass.
We have demonstrated the interconnectedness of abiotic and biotic components that determine habitat quality and animal abundance. Rather than identify a single strong control on abundance, we found key abiotic factors (canopy cover and thermal environment) affect abundance through multiple pathways and have effects that are mediated by biotic interactions and the niche of the focal species. In particular, our results suggest alignment of thermal niches across multiple trophic levels results in strong indirect effects of thermal environment on anole abundance. Losses of thermal habitat quality, particularly due to canopy loss, may thus have greater effects than appreciated when only direct effects are considered.
Our results demonstrate the role of multidimensional environments and niche interactions in determining animal abundance and highlight the need to consider interactions between thermal niches and trophic interactions to understand variation in abundance, rather than focusing solely on changes in the physical environment. Identifying the factors responsible for population change along habitat gradients will improve our understanding of how multidimensional environments and niches interact to determine population abundance. Which is more important than ever in this ever-changing world.
You can read the full paper here.
If you have any questions or just an interest in the work, please feel free to contact me emma.a.higgins@hotmail.com.
I would also just like to thank everyone again who was involved in this project, it was a lot of hard work, but great fun and it couldn’t have been done without the team effort.
Above: Part of the field team, helping process what is certainly not an anole, whilst setting up survey plots (photo credit Adam Algar).
References
Algar, A.C. et al. 2018. Remote sensing restores predictability of ectotherm body temperature in the world’s forests. – Glob. Ecol. Biogeogr. 27: 1412-1425. https://doi.org/10.1111/geb.12811
Campbell, G. S., and J. M. Norman. 1998. An introduction to environmental biophysics. 2nd edition. -Springer-Verlag, New York.
Battles, A.C. and Kolbe, J.J. 2018. Miami heat: Urban heat islands influence the thermal suitability of habitats for ectotherms. – Glob. Change Biol. 25: 562–576. https://doi.org/10.1111/gcb.14509
Heckel, D.G. and Roughgarden, J., 1979. A Technique For estimating the Size of Lizard Populations .Published by : Wiley on behalf of the Ecological Society of America Stable URL : http://www.jstor.org/stable/1936865 References Linked refere 60, 966–975.
Lizards with sticky toepads have a greater clinging ability. Above, the tree canopy specialist American green anole (Anolis carolinensis). (Credit: Getty Images)
Data from 2,600 lizard species worldwide indicate that those with sticky toepads prevail.
Many lizards are phenomenal climbers. Their sharp, curved claws are ideal for clinging to tree trunks, rocks, and other rough surfaces. However, in the precarious world of tree tops—filled with slippery leaves and unstable branches—three peculiar groups of lizards possess the remarkable evolutionary accessory of sticky pads on their fingers and toes.
Sticky toepads have independently evolved in geckos, skinks, and Anolis lizards—producing tree acrobats specially adapted to life in the forest canopy. Scientists have long considered sticky toepads an “evolutionary key innovation” that allow arboreal lizards to interact with the environment in ways that many padless lizards cannot.
Yet, some lizards without toepads have adopted the canopy lifestyle, an observation that has puzzled scientists for decades. Biologists Aryeh Miller and James Stroud at Washington University in St. Louis set out to find if lizards with toepads had an evolutionary advantage for life in the trees relative to their padless counterparts.
“Lizards with toepads have a greater ecological advantage in the arboreal environment,” says Miller, a graduate student in the evolution, ecology, and population biology program at Washington University in St. Louis and lead author of the study. “Toepads are essentially a biological superpower for lizards to access new resources that lizards without toepads cannot.”
“We found that lizards with sticky feet dominate the arboreal environment. Once adapted to life in the trees, they rarely leave,” says Stroud, a postdoctoral research associate and the senior author of the paper. “Conversely, lizards without sticky toepads frequently transition away from living in trees to living on the ground.”
The study appears in Systematic Biology.
“Scientists have long wondered about the role that the origin of key innovation plays in subsequent evolutionary diversification. Lizards are an excellent type of organism for such studies due to their exceptional species richness and the incredible extent of anatomical variation and habitat use,” says Jonathan Losos, professor of biology and director of the university’s Living Earth Collaborative.
Using a recently published database of habitat use for nearly every lizard species across the globe, the researchers were able to perform a comprehensive analysis of toepad evolution in the context of lizard habitat use—for the first time, the evolutionary relationships between which lizards live in trees and which do not became clear.
“Miller and Stroud have developed an elegant new approach to understand this diversity and the role that anatomical evolution plays in shaping the great diversity of lizard kind. This work will be a model for researchers working on many types of plants, animals, and microbes,” Losos adds.
Miller, who led the analysis, is the first to find that species have evolved for specialized life in trees at least 100 times in thousands of lizards. In other words, it is evolutionarily easy for a lizard to become a tree lizard.
What’s difficult is sticking around (pun intended!). Toepads don’t evolve until after lizards get into the trees, not before. And padless lizards will leave trees at a high frequency—much higher than padbearing lizards.
“There are hundreds of lizards living in the trees, but over evolutionary time many of those species end up leaving for life on the ground because, presumably, they interact with these padded lizards that have a greater advantage,” Stroud says.
The next step in this research is to find out exactly what padbearing lizards can do that their padless relatives can’t. Scientists can learn about this by watching the animals in their natural habitat.
“Analyzing evolutionary relationships can tell us a lot, but next we need to go out into nature—to see what parts of the environment the lizards use and why these evolutionary relationships exist,” Miller says.
Dominican House Wren (Troglodytes aedon rufescens) holding a juvenile Puerto Rican crested anole (Anolis cristatellus). Photo by M.P. van den Burg.
New literature alert!
Predation on the nonnative Puerto Rican crested anole (Anolis cristatellus) by the Dominican House Wren (Troglodytes aedon rufescens) on the Commonwealth of Dominica
In The Wilson Journal of Ornithology
van den Burg & Brisbane
Abstract
Predation on vertebrate species by insect-eating birds is rarely recorded, with only one report for the House Wren (Troglodytes aedon). On 4 January 2019, we observed a Dominican House Wren (T. a. rufescens) consume a juvenile of the nonnative Puerto Rican crested anole (Anolis cristatellus) in Roseau, Commonwealth of Dominica. This observation suggests the Dominican House Wren could additionally prey on the endemic Dominican anole (Anolis oculatus). This record aids our understanding of the ecosystem-wide impact of the A. cristatellus invasion.
Read the full article here, available as First Cite.
Cockroach positioned on head of Anolis fuscoauratus, on 29 March 2019 in the Ecuadorian Amazon. Photo by Javier Aznar González de Rueda
New literature alert!
Lachryphagy by cockroaches: reptile tears to increase reproductive output?
In Neotropical Biodiversity
van den Burg & Aznar González de Rueda
Abstract
Lachryphagy, or tear-feeding, is generally considered as supplementary feeding by invertebrates with a long proboscis to acquire essential nutrients. Commonly reported vertebrate host species of lachrypaghic interactions are humans and birds, and in reptiles concern large species: turtles and crocodiles, with one report from an iguanid host. Here, we report tear-feeding by a cockroach, a species lacking a proboscis, on a small squamate species, Anolis fuscoauratus. We address how the nutritional needs for the reproductive cycle may force cockroaches to explore any dietary source with essential nutrients. In addition to birds, our report adds Anolis as invertebrate predators that are visited by lachryphagous invertebrates, interactions that may be restricted to nights to reduce predation risk for the feeding invertebrates. This report extends tear-feeding behavior to proboscis-lacking invertebrates, and to small squamate hosts, and demonstrates that lachryphagy on reptilian hosts is not restricted to diurnal occurrence. Overall, this observation suggests that similar interactions could be far more frequent.
Turns out that it happens more commonly than you might think! Here’s the latest report from The Bulletin of the Chicago Herpetological Society, a ferruginous pygmy-owl eating a clouded anole in Mexico.
A biologist at The University of Texas at Arlington is studying the diversity of anole lizard species in the Caribbean islands to gain insight into why some species are common, while others are rare and possibly at risk for extinction.
The National Science Foundation awarded Luke Frishkoff, assistant professor of biology, a $1.1 million grant to investigate the reptile’s ecological niches, the set of conditions in which an organism can survive and reproduce.
Anoles with a broad niche thrive in a range of ecological conditions; those with a narrow niche are specialized to live in environments that meet their precise biological needs. Knowing the lizards’ niche characteristics will help scientists identify which species are in danger of dying out.
“We are in the middle of an extinction crisis right now, and some species are more likely to go extinct in the next 100 years than others,” Frishkoff said. “Among researchers, there is a common assumption that specialization is a predicting factor for extinction. The narrower the niche, the less likely it is that a species could survive.”
Frishkoff will collaborate with Martha Muñoz, a thermal biologist at Yale University, and Luke Mahler, an evolutionary biologist at the University of Toronto, to examine three aspects of the animal’s niche: diet, where they live among vegetation and how they interact with temperature.
The team’s findings will inform researchers’ strategies to conserve vulnerable species. As a community ecologist fascinated by the question of why various types of animals choose to live where they do, Frishkoff has a driving ambition to preserve the world’s biological diversity.
“When we go hiking and observe the plants and animals that are assembled there, I feel a deep sense of mystery,” Frishkoff said. “For me, the deepest motivation is to understand the rules by which life exists in these complex ecosystems.”
Frishkoff said humans can learn a lot from anoles about how to sustain life on earth.
“These lizards are a treasure trove of knowledge about ecology and evolutionary history, and they are a great model for understanding the fundamental properties of life on earth,” Frishkoff said.
Photo: Chase G Mayers, iNaturalist
On the island of Puerto Rico this trunk-crown anole is locally called lagartijo manchando, but is also known as: the Puerto Rican spotted anole, spotted anole, banded anole, saddled anole, salmon lizard, barred anole, St. Thomas anole and chameleon.
They are possibly the most abundant anole in Puerto Rico but can also be found on the British Virgin Islands and US Virgin Islands. They can be spotted in a number of different habitats including urban environments, though they occupy buildings at a lower frequency than Anolis cristatellus. In Puerto Rico they can often be found in Tabonuco trees.
Photo: Steve Maldonado Silvestrini, iNaturalist
Spotted anoles are active foragers with an apparent preference for ants.
Males have an SVL of 40-44mm, and females an average of 46mm. They have large orange dewlaps that fade into yellow closer to the margins but female dewlaps are smaller and grey with orange near the throat. Spotted anoles are typically brown or pale gray with pale and dark coloured spots along its body. Unlike some of the anoles found in Puerto Rico, they don’t permanent crests but have a nuchal crest that they raise during antagonistic interactions and otherwise ridges down their backs. There is also a patch behind their eyes that darkens during these interactions as well, much like in Green anoles.
Photo: larsonek, iNaturalist
Despite being on opposite sides of the world and separated by millions of years of evolution, Draco and Anolis lizards have converged on many common adaptive solutions.
It has long been suspected that the Draco lizards of Southeast Asia were ecological analogues of the Anolis lizards in the Caribbean. But it has only been recently that we’ve started to truly figure out just how similar these two groups actually are. Especially exciting has been the discovery of how lizards in both groups have converged on remarkably similar adaptations: natural selection appears to repeat itself, time and time again.
The classic textbook scenario in anoles is adaptive convergence in ecomorphology, which reflects where lizards tend to hang out in the environment. This is particularly obvious in the adaptation of Anolis limb morphology to different types of perches. I’m not sure we can say whether Draco exhibit the same ecomorphs as Caribbean anoles just yet, but Draco do exhibit the same adaptive changes in limb morphology as the anoles of the Caribbean.
Then there’s the obvious case of the dewlap, which has evolved separately in both Anolis and Draco as a key component of their territorial and courtship displays.
Most Anolis and Draco lizards also rely heavily on elaborate sequences of head-bobs in these displays as well.
This in itself isn’t unusual. Many lizards head-bob and push-up over territory and mates. Up to now, however, Caribbean Anolis lizards were the only ones known to tailor their display movements to ensure detection. For any visually communicating animal, visual “noise” from windblown vegetation and poor ambient light make it difficult to see visual signals. Anolis lizards were exceptional because they actively monitored environmental conditions and exaggerated their body movements when it was visually noisy (e.g., on windy days) or extended the duration of their displays when light levels diminished (e.g., on cloudy days or deep inside a forest).
There are a countless ways lizards might produce a conspicuous signal. Many Australian and Chinese lizards add arm-waves or elaborate tail-flicks or simply rely on colourful ornamentation that stands out well in the environment. Many North American lizards rely on performing lots of head-bobs or positioning themselves to accentuate a colourful badge on their throat or sides. But anoles seemed unique in both the complexity of their visual displays and their capacity to modify their behaviour to the prevailing conditions in the environment.
But after years of studying Anolis on Jamaica and Puerto Rico, and then even more years studying Draco in the Philippines, Borneo and Malaysia, we have now discovered more astonishing parallels between the two lizard groups that extends beyond just morphology.
Southeast Asian Draco lizards exhibit virtually identical strategies for coping with visually difficult environments as do the Caribbean Anolis lizards. Draco use the dewlap in the same way as the anoles, and change the speed (or exaggeration of movements) and the duration of displays in the same way as anoles, and this capacity to tailor displays to the conditions of the environment has also tended to precede what seems to have been adaptive divergences in display behaviour among species.
To discover all this, we had to study many different species of Draco and Anolis (11 and 12 species respectively), including hundreds and hundreds of lizards (727 to be precise), and then conduct thousands and thousands of hours of video analysis (13,310 hours – !!).
To be perfectly honest, what I was hoping to document from all this work was how differences in evolutionary history between the Anolis and Draco had shaped the trajectory of display evolution. Sure, Draco had evolved a dewlap like Anolis, but how that dewlap has been morphologically constructed was quite different between the two groups. I had become quite interested in these so-called “many-to-one, form-to-function” outcomes in evolution, and I was aiming to show something similar for display behaviour.
To be clear, there were differences in how Anolis and Draco lizards responded to environmental conditions, and how plastic changes in behaviour have contributed to display differentiation among species. In fact, the head-bob component of the territorial display has been entirely lost in some Draco species.
But the similarities were stunning and outweighed the differences by a large margin. Even the loss of headbobs in some Draco have intriguing similarities to how some Anolis species have shifted their display effort to the dewlap, which seems to be a more energetically efficient means of producing a conspicuous, complex visual display, than the more tiresome head-bob and push-up movements.
We have also confirmed experimentally in anoles that the manner in which Anolis lizards tailor their displays does actually improve display detection in visually difficult environments. This took a lot of work in itself and required the development of a robotic playback system, but this is now ancient history.
But to complete the loop, a similar type of playback experiment needed confirm the same adaptive benefit in Draco.
Some years ago we had conducted a lengthy field experiment using robot playbacks that were designed to test the response of Draco lizards to different coloured dewlaps. That experiment showed little effect of dewlap colour on detection, but a tangible effect that once lizards saw the dewlap, they used it to evaluate the species identity of the signaller.
I was in the lab one day looking at these old Draco robots to get some inspiration for designing a new system for some other crazy idea I had. As I was fiddling with the mechanism, I noticed that the robots weren’t exactly the same, with the lever controlling the dewlap of one being slightly longer than another. This meant the display probably differed in speed between the robots. These things happen and I didn’t think much of it at the time. The treatments used in the field experiment were systematically inter-changed across the robots to make sure this type of thing didn’t cause any problems.
Later, however, it occurred to me that perhaps this might offer a serendipitous opportunity to confirm the adaptive benefit of at least one of the key convergences exhibited by Draco lizards. I downloaded the data from the original study from its dryad repository, extracted the response times of lizards to the two robots that differed in dewlap speed, and sure enough, detection times were much quicker to the robot with the faster dewlap display.
The top panel (a) shows the differences in dewlap speed between the two robots, while the bottom panel (b) shows the detection time of free living Draco melanopogon.
If you’re interested in a short video introduction to this work, or want to know more about how these findings relate to our general understanding of adaptation and animal communication, you’ll find some answers in this 5 minute video below.
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