Category: New Research Page 4 of 66

From Winchell et al. (2020): Anoles throughout the Caribbean differ in their tolerance to urbanization. Red colors = urban tolerant, blue colors = intermediate tolerance, green colors = urban intolerant.

Seven years ago I asked for the help of Anole Annals readers as I started to think about how different species of anoles throughout the Caribbean tolerate urbanization. This question, it turned out, was a lot more complex than I had originally anticipated! The idea was simple, find out which species are in urban areas and to what extent they use urban habitat elements, then determine if there is an evolutionary signal in urban tolerance and what traits are correlated with urban tolerance. Many hours of troubleshooting and brainstorming with my coauthors Klaus Schliep, Luke Mahler, and Liam Revell (and years later) and this study is finally out in the journal Evolution: Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade.

Anolis lineatopus, one of many urban tolerant anoles (photo K. Winchell)

Inventorying urban species

To figure out which anole species are tolerant of urbanization, my initial plan was to survey researchers and the literature to score each of the 100+ Caribbean species based on their presence in different types of urban habitats and their habitat use. Although I got a lot of great feedback from this original survey, it left a lot of gaps in the dataset. I needed to find a more objective way to assess urban tolerance.

With the help of Klaus Schliep and Luke Mahler, we decided to examine location records in museum collections (via GBIF) to determine which species had been observed (collected) in urban environments. Because we suspected museum records might be biased towards non-urban habitats, we also examined location records from the citizen science database iNaturalist, which we suspected might be biased in the opposite direction (i.e., people photograph things where they live). For each record, we looked at satellite imagery and scored the observation as urban or non-urban, then tallied the total number of observations and the total number of urban observations per species.

Even with these two data sources, we noticed gaps in our data for some species. So we included a third source, Henderson & Powell’s (2009) book on the Natural History of West Indian Amphibians and Reptiles. This fantastic reference (highly recommended!) gives detailed natural history information and summarizes key features of every anole (and other Caribbean herps) in the Caribbean. Of course, this is more subjective than the location-based data, so Luke and I came up with a scoring system that assigned a set number of urban tolerant or avoid “points” based on key descriptors. For example, if a species was described as being common around houses and often observed on buildings, it would get points for being tolerant of urbanization. In contrast, a species described as having a restricted range and intolerance of anthropogenic disturbance, it would get points for being intolerant.

Analyzing urban tolerance in a phylogenetic framework

We combined these disparate data sources into a logistic model with parameters we set based on the number of urban observations we would need to be certain of urban tolerance and how many total observations we would need to be certain of our species assessment. This resulted in a probability of being an urban avoider or urban tolerant for each species, which we used as our prior probabilities for these states in our phylogenetic model. We then reconstructed ancestral states and missing tip states for urban tolerance in 131 species of Caribbean anoles.

Of course, we don’t mean to say that we attempted to reconstruct the evolution of urban habitat use — anoles are far older than urbanization! Instead, we wanted to understand the evolution of the behavioral, physiological, ecological, and morphological traits traits that influence whether a species will exploit or avoid urban habitat when it arises. The threshold model is well-suited for this type of complex trait. The threshold model assumes that a discrete trait is determined by a combination of continuously valued characteristics. These characteristics may be measurable, unmeasurable, or even unknown. As a taxon accumulates specific trait changes, the species is pushed incrementally closer and closer to the discrete state change (in this case urban tolerance), and the more recently this discrete character state has flipped, the more likely a reversal to the previous state could occur. From this model we can extract a single continuously valued trait, the liability, that underlies the complex trait of urban tolerance.

Urban tolerance in Caribbean anoles, from Winchell et al. (2020).

Traits of urban species

So what did we find? To start, urban tolerance appears to be widespread in Caribbean anoles and has a strong phylogenetic signal. Because of that, we suggest that our approach may be used to predict urban tolerance of species that either have yet to encounter urbanization or for which we are lacking information. This application could be particularly useful for determining which species are likely to be intolerant of urbanization and thus should be prioritized in conservation efforts. At the other end of the urban tolerance scale, we caution that our approach should not be used to predict species that are robust to anthropogenic habitat loss, but rather that it might be useful to identify species that are promising for future urban ecology and evolution studies.

Finally, we used the liability score for each species to try to get a better understanding of what those traits underlying urban tolerance are exactly. Using PGLS we looked for correlations between the liability and a suite of ecological and phenotypic traits. We found that species that are more tolerant of urbanization had higher field body temperatures, fewer ventral scales, more rear lamellae, shorter hindlimbs, and experience warmer and drier climates within their native range. These traits may be key “pre-adaptations” enabling species to colonize urban habitats as they arise and to take advantage of anthropogenic niche space (i.e., on and around buildings). For example, urban habitats tend to be hotter and drier than nearby forest sites, so it makes sense that species with larger ventral scales, higher field body temperatures, and which experience hotter and drier temperatures in their non-urban range would be predisposed to tolerate urban habitats. Similarly, lamellae are important for clinging to smooth surfaces, which may be particularly beneficial in urban habitats dominated by smooth anthropogenic surfaces.

Lastly, we found, somewhat to our surprise, that no one ecomorph seems to be best suited for urban environments. Based on our experience, we had thought that trunk-ground anoles would be more likely to tolerate urbanization, but it turns out that there are a lot of trunk-ground anoles that are intolerant of urbanization and a lot of species from other ecomorphs that are tolerant (think A. equestris or A. distichus)!

Salmonella in Japan’s Green Anoles

By Nick Herrmann

On April 25, 2020

In All Posts, Introduced Anoles, New Research

When I hear or read Salmonella, I think of my mom explaining to my 7-year-old self why I shouldn’t eat raw chicken (to be clear, I never expressed interest in doing this, but lesson learned nonetheless). According to the U.S. Centers for Disease Control and Prevention, most instances of Salmonella bacteria making people sick do in fact result from transmission by food. But Salmonella infection can come from other sources, including direct contact with living animals, particularly reptiles (including birds which, in case you haven’t heard, are reptiles). So I was only a little surprised when I came across a recent paper in the Journal of Veterinary Medical Science, based in Japan, documenting the prevalence of Salmonella in the green anole, Anolis carolinensis, on Okinawa Island, Japan.

Of the 706 green anoles from Okinawa Island whose intestinal contents were analyzed for Salmonella presence between 2009 and 2014, only 2.1% tested positive. That number is low compared with published results for green anole populations in Florida (7.5%), Chichi Island in Japan (34.2% – this study was highlighted here on Anole Annals when it came out in 2013), and Guam (76.2%). I’m struck by how much these percentages vary. Green anoles have been in Florida for millions of years, whereas populations in the other locations have only been established for tens of years. The authors hypothesize that infection rate in recently introduced populations should correlate with how long the population has been established. Testing this hypothesis will require data from more populations. It also appears that we know little about whether anoles are affected by carrying Salmonella, although a quick search did reveal this study involving the brown anole, Anolis sagrei.

All told, we have a lot to learn about anoles and Salmonella. In the meantime, please protect yourself from Salmonella infection by following basic food safety precautions: refrigerate foods adequately, wash fruits and vegetables and cook meat and eggs thoroughly, and clean potentially contaminated cookware and utensils with soap and water. Most importantly, WASH YOUR HANDS, although I assume that like me, you are already doing this approximately a hundred times per day (for those of you reading this in the future, I’m not a weirdo. We’re in the middle of a pandemic).

For those who may be interested, green anoles became established in and around Japan several decades ago and are considered an ecologically disruptive pest. If you want to read more, here are links to some old Anole Annals posts on various topics related to the region’s green anoles: trapping efforts, population age structure, range expansion. Enjoy!

Anolis cristatellus Journal Cover!

By Kristin Winchell

On April 15, 2020

Hot off the press — the latest anole journal cover! In this issue of Nature Ecology & Evolution, Shane Campbell-Staton and I led a team of researchers to explore the effects of urban heat islands on anoles. We found that not only can urban Anolis cristatellus tolerate higher temperatures than their forest counterparts, but also identified genomic regions associated with divergent thermal tolerance. Check out a summary of this work at the urban evolution blog I co-edit, Life in the City: Anoles Adapt to Beat the Urban Heat.

In the Eye of the Beholder: How Do Anoles Respond to Human Clothing Color?

By Lindsey Swierk

On January 13, 2020

In New Research

Water anole (Anolis aquaticus), Costa Rica

Have you ever wondered how your clothing color affects how many anoles you see and catch on a given day? When we go out herping, a lot of us favor some sort of clothing color scheme – whether it’s conscious or subconscious, scientific or superstitious. Since anoles have such excellent color vision, and since they’re so sensitive to the signaling colors of the individuals they interact with, this makes sense, right?

(a) Water anole dewlap; (b) Orange and blue shirts; and (c) green shirts worn in this study.

Bree Putman (Cal. State San Bernardino), Andrea Fondren (an undergraduate researcher), and I teamed up to determine if there was any truth behind the superstition. In an effort to understand how anthropogenic colors affect the behavior of lizards, we designed a study to test whether researcher shirt color would influence the sighting and capture rates of water anoles (Anolis aquaticus). Male water anoles have large orange dewlaps, which is their most conspicuous sexual signal. Using a modified version of the species confidence hypothesis, we predicted that water anoles would be least fearful of anthropogenic colors that most closely resembled the color of their own sexual signals (orange). To test this, a group of us spent the summer surveying water anole populations wearing three different shirt colors: orange, blue, and green. We carefully allocated shirt colors to research teams and study sites, planning it out in advance so that all shirt colors were worn by all researchers and used at all sites evenly in the study.

Our results, published in Biotropica, may make you rethink your own field shirt color choices. Both our sighting rates and our capture rates of water anoles were significantly higher when wearing orange shirts – matching the color of water anole dewlaps. Lizards likely have sensory biases for colors used in their species-specific displays, and we found that this translates into clear differences in behavioral responses to anthropogenic colors. On some level, I think many of us expected that the green shirts, which camouflaged us beautifully in the forest, would have been the most successful. Not so. Looking more broadly, Bree Putman’s previous study on western fence lizards (Sceloporus occidentalis) helps to solidify the idea that lizards are biased toward anthropogenic colors that they themselves “wear.” Western fence lizards have blue sexual signals and – corresponding nicely to our water anole results – these lizards are less fearful of researchers wearing blue clothing. Taken together, these findings remind us that placing a human perspective on animal perception can sometimes lead to flat out wrong conclusions.

As ecotourism is on the rise, it’s worthwhile to consider how the anthropogenic stimuli that ecotourists bring into a species’ native habitat can affect species behavior and survival. Reducing a species’ exposure to more frightening stimuli (such as unfamiliar colors) can reduce stress and disturbance. Something for the ecotourism community to consider as researchers continue to explore ways to minimize disturbance of natural populations, while promoting sustainable use of natural areas.

As for me, it looks like I’ll be buying quite a few orange shirts this year.

SICB 2020: Artificial Light Keeps Green Anoles Hungry!

There are so many great anole talks at SICB 2020, I’d be remiss if I didn’t take this opportunity to shed some light on some of our fantastic undergraduate researchers, who turned out in force to Austin this year! As I’m sure Dr. Kristin Winchell will tell you, anole lizards make awesome model organisms for studying the effects of city life and urbanization on wildlife.

Cities can be dangerous though. A lot of different urban environments will present wildlife that have not lived in cities with numerous pressures they might not have faced before, such as different surfaces and substrates on which to run, different temperatures, and even new predators. One of the relatively new pressures that goes along with city life is light at night, and artificial light to boot. If you’ve ever been too disturbed by light during the moonlight hours to sleep and rest, imagine how small lizards feel!

To address the effects of this pressure on green anoles (Anolis carolinensis), Michelle D’Alessandro, an undergraduate student at the University of Scranton working in the lab of Dr. Chris Howey, measured the effects of artificial light at night (I’m just going to call it ALAN) They exposed anoles to ALAN and described the effects of artificial light on metabolism in green anoles. Initially, they did not find any differences between metabolic rates when lizards were exposed to ALAN, however after a sufficient time period, anoles exposed to ALAN increased their metabolic rates during the evening, but not during the day! During this experiment, they also found that ALAN anoles were far hungrier and ate more often than lizards that weren’t exposed to light at night. The term ‘midnight snack’ definitely comes to mind here! Michelle suggests that much like when humans get exposed to changes in sleeping patterns, anoles undergo some energetic changes, causing them to eat more and having to burn more energy. Maybe next time think twice about keeping that porch light on during the waning hours of the evening- give the wildlife some much needed rest.

SICB 2020: Variation in Anole Sperm and Testis Morphology

Another star undergrad alert! If you’ve ever followed the work that comes out of Dr. Michele Johnson’s lab at Trinity University, you’ll know that she produces some incredible science and some even-more incredible undergraduate researchers. Isabela Carson is no exception!

Isabela’s poster was focused on studying intraspecific variation in lizard sperm and testis morphology- she described differences in the size and shape of different testis and sperm features for 6 different species of anole. A lot of this work was founded on Dr. Ariel Kahrl’s dissertation work on describing sperm evolution in anole lizards, and her collaborations with Dr. Johnson’s lab and students always produce some awesome talks and posters wherever they are presented. Isabela wanted to know if longer sperm are produced from lizard species that have larger seminiferous tubules- the part of the testis where sperm are produced, matured, and transported. She found an inconsistent pattern across anole lizards where larger tubules don’t always produce longer sperm.

In talking with Isabela, she noted that there are some big inconsistencies between the external morphology of testes and the sperm they produce, and that there might be some larger ecological or evolutionary patterns at work that go into describing how sperm evolve in different species. I would bet that one day we are going to have data on testis shape and size and sperm length for all anolis species, and there are going to be some awesome patterns and studies that come out of that work. And we definitely have to give heaps of credit to the awesome biologists who are working towards it!

SICB 2020: Artificial Light Doesn’t Influence Immune Responses in Green Anoles

The Howey lab showed up to work at SICB 2020! In keeping with the theme of how urbanization and artificial light at night (ALAN) impacts wildlife populations, Elizabeth Kenny, an undergraduate researcher at the University of Scranton performed a study to describe the influence of artificial light on the immune response in green anoles (Anolis carolinensis).

The researchers used a test for immune response called a phytohemagglutinin test (PHA-L), where they injected the hindlimbs of green anoles with PHA-L and measured how much the foot swelled after both a 24 and a 48h hour period. But rest assured! PHA-L tests are temporary, only induce localized swelling, and have no larger impacts on the health of the organism; it’s sort of like if you’ve ever had a tuberculosis test done at your local physician. Interestingly, Elizabeth found no difference in swelling between green anoles exposed to ALAN and to green anoles that had not been exposed to ALAN. However, Elizabeth suggested that green anoles could respond sufficiently to ALAN by changing how they use the energy within their bodies and where they allocated those limited energetic stores, which provides a lot of support for the work of Michelle D’Allesandro and Meg McGrath. Altogether, the three undergraduate researchers of the Howey lab created a convincing and interesting story about how urban environments influence the energetics and physiology of city-dwelling lizards. Great stuff!

SICB 2020: City Anoles Have Bigger Toes!

Urbanization was a big theme at SICB 2020 this year, and studies of how city life influences wildlife populations are really important to help us understand the effects of human activity on natural environments and animals. One of the most rapid ways in that city-dwelling animals can adapt to these new environments is by changing the shape and size of various morphological traits.

Anoles in their natural habitat do tend to be tree-dwelling, or arboreal lizards, and they spend a lot of time climbing to find food resources, regulate their body temperature, and do other ecological activities. A lizard that relies so much on climbing performance frequently uses its claws and toe pads in its climbing ventures, so one of the first changes that city anoles might exhibit is changes in toe pad or claw shape to better climb on slick city surfaces (say that 3 times fast!). To get at this question, Bailey Howell from the Mississippi University for Women, along with her co-authors Travis Hagey and Kristin Winchell, compared urban crested anoles (Anolis cristatellus) to forested crested anoles and found that toe pads in urban anoles are longer and wider than toe pads from lizards in natural environments.

Bailey goes on to discuss that these toe pads that have an increased area might be better for urban anoles to climb on slicker and smoother substrates found in city environments. Bailey is going to continue adding to her dataset by incorporating more anoles and testing additional hypotheses such as measuring performance differences between urban and forested anoles. Stay tuned for more urban anole work!

SICB 2020: Gene Expression Can Lead to Size Dimorphism in Anole Lizards