Living Large in the City: Impacts of Urbanization on Anoles

Brown anoles (A. sagrei) thrive in urban environments.

More and more research is highlighting how living in cities impacts the organisms that exploit urban habitats. Some research in anoles even highlights how organism may be adapting via evolution to these novel urban habitats!

However, we still don’t know much about how urbanization impacts reptiles, and anoles are a great group in which to study these effects. A large team from the Kolbe lab at the University of Rhode Island set out to tackle the question of how living in cities can impact anoles by studying populations of both brown (A. sagrei) and crested anoles (A. cristatellus) in urbanized areas in Miami and remaining natural areas within the urban matrix. The team included two undergraduates at URI, Amanda Merritt and Haley Moniz (currently a MS student in Chris Feldman’s lab at UNR ) who were key contributors to the project.
We caught lizards at 7 different sites in the Miami area and measured their morphology, thermal preferences, and parasite loads. This research was recently published in the Journal of Urban Ecology.

We found that for all groups of anoles studied (male and female brown anoles, and male crested anoles), lizards living in the urbanized habitats were larger (see figure below), but showed no differences in body condition, or how much body mass they had per unit length. Larger body size can be associated with increased fitness in anoles, so the larger size of urban lizards could represent an advantage for anoles living in cities.

Lizards from urban (blue) habitats were larger than those from natural (green) habitats.

Despite cities being known to have higher temperatures (the urban heat island effect), including at our study sites, we found no differences in the temperatures that lizards from urban and natural sites preferred. Our preferred temp values were in line with those found for native range populations of these species, which suggests that we are not seeing adaptation of preferred body temperature to the warmer conditions in very urban parts of Miami. This means that lizards living in cities could end up having higher body temperatures than they would prefer, a potential cost to using urban environments, though see Andrew Battles’ recent paper for a more detailed look at this issue!

Lastly, we examined the presence of parasites in the body cavities of these lizards. Most of the parasites that we found were nematodes in the digestive tract, though we also found some pentastomids, crazy crustacean parasites, in the lungs of crested anoles! We found no difference in the presence of parasites in lizards from urban or natural sites, although brown anoles did consistently have parasites more often than crested anoles. When we looked at parasite infection intensity, or the number of parasites in lizards that had them, we did see that brown anoles in urban habitats had significantly higher parasite loads than those in natural habitats. This result indicates that increased parasitism could be a cost of living in cities for anoles, though it may vary from species to species.

Crested anoles from both urban (blue) and natural (green) habitats have similar levels of infection intensity (number of parasites) to brown anoles in natural habitats, but brown anoles in urban habitats show significantly higher levels of infection intensity.

Overall, our work suggests that there may be advantages (larger body size) and costs (non-optimal body temperatures, higher parasite loads) for anoles living in cities, and that these may vary even between species that are quite similar ecologically. Anoles are an emerging study system in urban ecology, so stay tuned for what should be a fascinating variety of papers on city-loving anoles in the near future!

Christopher J Thawley, Haley A Moniz, Amanda J Merritt, Andrew C Battles, Sozos N Michaelides, Jason J Kolbe; Urbanization affects body size and parasitism but not thermal preferences in Anolis lizards, Journal of Urban Ecology, Volume 5, Issue 1, 1 January 2019, juy031, https://doi.org/10.1093/jue/juy031

SquaMates Podcast: Anole Special Episode!

Recently, the guys over at SquaMates Podcast — a podcast about all things herpetological — asked if I would be interested in joining them for a special episode on anoles to discuss the recent Anolis Newsletter VII.  The podcast is hosted by Mark D. Sherz, Ethan Kocak, and Gabriel Ugueto, who was responsible for the wonderful drawing which graced the cover of ANVII.

The Anole Special, “Episode 8: The Last Anole”, has just gone live and you can listen to it at the link below. Here’s hoping the title isn’t true and there are many more anole episodes to come in the future!

SquaMates Ep. 8: The Last Anole

You can also subscribe to the SquaMates Podcast at any of the podcast streaming services below!

Apple Podcasts | Android | Google Podcasts | Stitcher | TuneIn | RSS | More

 

 

The Science of Species Delimitation: David Hillis Diagnoses What’s Being Done Right and Where the Field Is Headed

In a somewhat autobiographical romp through the history of species delimitation, David Hillis, in a recently published article in the Journal of Herpetology, details the state-of-the-field in terms of phylogenetic and species delimitation, detailing both the many advances that have been made over the last few decades, but also pointing out where things are out of whack and need some recalibration. There’s much more to the article than the figure above, but that’s a good place to start!

Anoles in the Hot Seat on the Ologies Podcast

UCLA professor Shane Campbell-Staton was recently interviewed on the science podcast  Ologies, hosted by Alie Ward. Shane is a thermophysiologist and anolologist (you may remember the stories about A. carolinensis and the polar vortex on AA a couple of years ago (here, here, and here). That’s not all Shane has going on though; his lab is branching out in lots of different directions (listen to learn about some cool/hot new projects) and he’s also hosting The Biology of Superheroes Podcast. As per usual, Shane’s interview is filled with jaw-dropping factoids (bees that cook their wasp predators), words of wisdom (write tomorrow’s to-do list every night before bed), lots of lizards, and many an endearing anecdote (though we never did find out who wins Superman vs. Ali).

You can listen to the full interview here, or on iTunes, Spotify, or wherever you get your podcasts.

Effects of Deforestation on Lizard Communities Differ at Low and High Elevations

 

Anolis landestoyi. Photo by Miguel Landestoy.

As reported by Science Daily:

Elevation matters when it comes to climate change, deforestation and species survival

Date:
February 25, 2019
Source:
University of Toronto
Summary:
A study examining the impact of deforestation on lizard communities in the Dominican Republic demonstrates differing outcomes at different elevations. In the lowlands, deforestation reduces the number of individuals, but not which species occur in an area. In the highlands, it’s the opposite. When the forest is cut down at higher elevations, the newly created pastures become filled with species found in the warmer lowlands. But locally adapted mountain lizards cannot survive as temperature rises.

University of Toronto student George Sandler was shocked to see the rainforest floor suddenly come to life around him, as if in a scene from an Indiana Jones movie.

“The forest floor started rustling around me,” says Sandler, “as dozens of crabs emerged from holes and crevices. Some were huge, the size of dinner plates. I even spotted a hermit crab climbing up a tree, lugging its heavy shell along with it.”

But Sandler wasn’t in the field to study crabs. He was in the Dominican Republic to take a census of the region’s Anolis lizard species for a study on the effects of deforestation being conducted by researchers Luke Mahler, Luke Frishkoff and collaborators. In the Caribbean nation, deforestation is the main form of natural habitat loss as residents cut down rainforest in order to produce charcoal, as well as create pastures for livestock and farmland for crops.

It is no surprise that deforestation has a profound effect on biodiversity; scientists have been studying this problem around the globe for decades. What is surprising is the difficulty they still face in making detailed predictions about which species survive, especially in relation to other factors such as climate change and natural local conditions.

Now, using the data collected in the census, the research team has discovered details about how Anolis lizards are being affected by the loss of their habitat.

“When it comes to predicting the effects of deforestation,” says Mahler, “elevation matters.”

Mahler is an assistant professor in the Department of Ecology & Evolutionary Biology (EEB) in the Faculty of Arts & Science at the University of Toronto. Frishkoff led the research while he was a postdoctoral fellow in Mahler’s lab at U of T and is lead author of the paper describing their findings, published today in Nature Ecology & Evolution; he is currently an assistant professor at the University of Texas at Arlington. Sandler and researchers from the National Museum of Natural History in Santo Domingo were also co-authors.

Mahler and Frishkoff analyzed populations of lizards in both lowland and highland regions affected by deforestation. Generally, the lowlands are warmer than the highlands due to altitude; also, forest canopy blocks direct sunlight, making forests at any altitude cooler than their immediate surroundings.

“It turns out that deforestation changes lizard communities in fundamentally different ways in the lowlands as compared to the highlands,” says Mahler. “In the lowlands, deforestation reduces the number of individuals, but not which species occur in an area. In the highlands, it’s the opposite.”

“When the forest is cut down at higher elevations,” says Frishkoff, “the newly created high elevation pastures become filled with species we saw down in the warmer lowlands. But, the locally adapted mountain lizards cannot survive.”

The invasion into the highlands by lowland-dwelling lizards was made possible by a combination of human activity and natural factors; i.e. deforestation and elevation respectively. Thanks to the altitude, the temperature of deforested fields in the highlands was comparable to the temperature of forested lowlands.

As it is in many regions around the world, the problem of deforestation in the Dominican Republic is dire. In 2016, Mahler announced the discovery of a previously unknown chameleon-like Anolis lizard on the island of Hispaniola. In the paper describing the discovery, Mahler and his co-authors recommended that the new species, dubbed Anolis landestoyi, be immediately classified as critically endangered because the lizard was threatened by illegal clear-cutting in the region.

Unlike the crabs that crowded around Sandler in the rainforest, the lizards were more elusive and difficult to survey. In order to obtain accurate counts, the students employed a technique known as mark-resight.

“We hiked out to our designated plots,” says Sandler, who was an undergraduate student while conducting the field work and is currently an EEB graduate student at U of T. “Then we walked around looking for lizards. We carried a paint spray gun filled with a non-toxic, water soluble paint — a different colour for each of the six observation periods. If we saw a lizard we would note the species, if it had any paint on it already, and the colour of the paint. Then we would spray the lizard with the paint gun we were carrying, a task that was a little tricky with some of the more skittish species!”

Paint on a lizard indicated that it had already been counted; and the number of unpainted lizards that were observed during each period allowed the researchers to calculate how many lizards were going uncounted.

“It’s not your typical summer job,” says Mahler. “Each survey is essentially a game in which you try to find all the lizards in an area and zap them with paint. It’s a messy affair, but we get great data from it.”

“Our results help us better understand the likely consequences of climate change and how it will interact with human land-use,” says Frishkoff.

For lowland forest Anolis lizards, deforestation just means a decline in abundance or relocating to the highlands. But for highland species, the situation is more critical. Unlike their lowland cousins, they have reached high ground already and in the face of deforestation have nowhere to go — a situation facing more and more species around the world.

“Our data suggest that while many lowland Anolis species might not be seriously affected by deforestation and the gradual warming brought about by climate change,” says Frishkoff, “the opposite is true for the unique mountain lizard species which do not tolerate land-use change well, and which are already on the top of the island.

“Land-use and climate change are a double whammy for these species. If we cut down the mountain forests these lizards have nowhere left to go. Gradual warming might push species up slope, but when you’re already at the top of the mountain, you can’t move any higher.”

Story Source:

Materials provided by University of TorontoNote: Content may be edited for style and length.


Journal Reference:

  1. Luke O. Frishkoff, Eveling Gabot, George Sandler, Cristian Marte, D. Luke Mahler. Elevation shapes the reassembly of Anthropocene lizard communitiesNature Ecology & Evolution, 2019; DOI: 10.1038/s41559-019-0819-0

Remembering Lourdes Rodriguez Schettino

Lourdes Rodriguez Schettino with Ada Chamizo and Rich Glor in 1999.

Our recent mention of Richard Etheridge’s death reminded us that we’d never noted the passing of Lourdes Rodriguez Schettino nearly two years ago, in March of 2017.

Lourdes was an expert on the lizards of Cuba, particularly the iguanid lizards, about which she truly wrote the book. She also was the lead author on a lovely book on Cuban herpetology (below).

Sadly, I am unaware of any obituaries of Lourdes in English, but  the Instituto de Ecología y Sistemática, where she worked for many years, has a nice summary of her life’s work, and there is a brief notice in Revista Colombiana de Ciencia Animal.

Lourdes Rodriguez Schettino in 1995.

 

 

Richard Etheridge, Founder of Anole Systematics, Passes Away

Word has belatedly reached Anole Annals’ ears that, sadly, Richard Etheridge passed away last month at the age of 89. Richard was not only a titan of lizard systematics, but the founder of anole systematics. Amazingly, the classic worked that is the foundation of all that has followed in anole systematics was his never-published PhD dissertation. Bobby Espinoza and Kevin de Queiroz wrote a biography of Richard’s career that was published a decade ago in Copeia and that, happily, is freely available.

Growth Rate in a Population of Anolis nebulosus from Tropical Dry Forest

Anolis nebulosus is an endemic species of Mexico. Its distribution occurs along the coasts of the Mexican Pacific, from Sinaloa to the Isthmus of Tehuantepec, but it enters the highlands a little bit in the Sierra Madre Occidental. At the end of the 80’s, very little was known about the natural history of populations of this species.

Our study was conducted at the Field Station Chamela, Jalisco México during a period from 1988-1990. It is believed that the growth rates of juveniles are restricted by available food resources. In animals that grow throughout the year, such as tropical lizards, it is believed that growth will be faster during the rainy season. Consequently, we wanted to know (a) if there are differences in growth rates between sexes of A. nebulosus; (b) whether growth rates vary among age classes, between dry and wet seasons, and between years; and (c) what extrinsic factors (e.g., environmental temperature, precipitation, and food availability) promote variation on growth rate of different age classes and sexes between seasons and years.

Our study shows the growth rate of males and females and feeding behavior; male grow faster than females; males reached sexual maturity at minimum SVL of 32 mm, while females at 35 mm of SVL; lizards live only one reproductive season, that is during rainy season–after that, they die. In 1989, juvenile males and females grew more in both seasons (rainy and dry) than adults; for 1990, there were no differences by season or between age classes.

The information that was presented about the growth of Anolis nebulosus in Ecology and Evolution  is part of the information I (ARB) have shared with my ex-graduate students, now doctors (Uriel Hernández-Salinas, Raciel Cruz-Elizalde, and Christian Berriozabal- Islands), as well as my colleague, Dr. Shai Meiri. This study opens a window on knowledge of the natural history of this fascinating species model.

 

Evolution of Claws in Greater Antillean Anoles

Much has been made about the role of convergent morphology in the partitioning of vertical habitat by Greater Antillean anole ecomorphs. In particular, the role of toepads in allowing anoles to utilize vertical habitat space has been the focus of abundant research. It is easy to see why, given the novelty of the toepad in anoles (and, of course, geckos). But when you look across the lizard tree, there plenty of arboreal lizards lack toepads entirely and instead rely on their claws for climbing.

Functional studies in other claw-bearing squamates provide some predictions for how claws may be related to habitat use. For example, studies have shown that highly curved claws perform better in performance trials of clinging strength (Zani 2000), and so we would expect that more arboreal species should have more highly curved claws. Yet claws remain a relatively neglected trait in anoles, despite the wealth of literature related to other aspects of their ecomorphology.

Is claw morphology related to habitat partitioning in anoles? Or is it really all about the toepad? In a recent publication, my coauthors and I set out to examine how claw morphology varies across the Greater Antillean anole radiation with these questions in mind. We measured the claws and toepads of 428 museum specimens across 57 species to test the prediction that claw morphology was related to habitat use in Greater Antillean anoles. Our sampling spanned every ecomorph present on each Greater Antillean island, as well as several non-ecomorph species.

First, we tested the prediction that arboreal species should have more curved claws than terrestrial species. This pattern has been observed in squamate reptiles broadly, but has not been tested within anoles. Unfortunately, only one truly terrestrial anole exists in the Greater Antilles, A. barbouri. Therefore, to increase our sampling, we included four terrestrial mainland species. As predicted, we found that terrestrial anoles had much flatter claws than arboreal species. Claw curvature was also positive correlated with perch height


Fig 1 PCA plot of first and second principal components for univariate claw measurements. Convex hulls are depicted for each Greater Antillean ecomorph and terrestrial species (both Greater Antillean and mainland) are labelled. Insets: (A) Superimposed means of geometric morphometric shape for terrestrial and arboreal species; (B) Boxplots of claw curvature measurements for arboreal and terrestrial species (*** P < 0.001).

Next, we tested the prediction that ecomorphs are differentiated by claw morphology. We found that ecomorph did predict claw morphology, but that differences were more pronounced for some ecomorphs. Notably, more terrestrial ecomorphs (trunk-ground) were differentiated from more arboreal ecomorphs (trunk and trunk-crown) in line with predictions. In the most extreme case, twig anoles appear to have dramatically reduced claws. Their claws were not only flatter, but also shorter and thinner relative to body size compared to all other ecomorphs. We can only speculate as to the reason that this might be the case. Perhaps claws are unimportant or an impediment in twig anole locomotion? Clearly, functional studies are required to fully understand the relationship between being a twig anole and claw morphology.

Finally, we tested for patterns of covariation, or phenotypic integration, between claw and toepad traits. Claw curvature was positively correlated with toepad width and lamella number, both traits that positively correlate with perch height and demonstrated to improve clinging performance in anoles. Other claw traits such as relative length and diameter did not correlate with toepad traits. This is perhaps unsurprising, as these traits also do not appear to be differentiated between more arboreal and terrestrial species. Given the developmental literature showing that terminal digit features are decoupled from the rest of the digit (Casanova and Sanz-Ezquerro 2007), our observed pattern of integration is unlikely to be the result of developmental linkage.

In conclusion, our data suggest that integration between claw curvature and toepad traits is driven by correlative selection due to structural habitat use. Our results strongly support the hypothesis that claws play an important role in the partitioning of vertical habitat within the adaptive radiations of anoles, and suggest that they are likely shaped by similar patterns of correlative selection that have driven the evolution of ecomorphs overall. Still, we have a lot to learn about how variation in claw shape influences actual locomotor performance in anoles. Claws are a trait just waiting for more research!

Casanova, J. C., and J. J. Sanz-Ezquerro. 2007. Digit morphogenesis: is the tip different? Dev. Growth Differ. 49:479–491.
Yuan, M. L., M. H. Wake, and I. J. Wang. 2019. Phenotypic integration between claw and toepad traits promotes microhabitat specialization in the Anolis adaptive radiation. Evolution 73:231–244.
Zani, P. A. 2000. The comparative evolution of lizard claw and toe morphology and clinging performance. Journal of Evolutionary Biology 13:316–325.

Where Do Anolis Lizards Lay Their Eggs?

Searching for anole eggs

In this southern city where the heat is on, and the parties last ‘til the break of dawn, residents are busy patrolling territories, showing off their physique, and courting each other. With all this activity going on, South Miami, FL surely takes the crown for the best people anole-watching destination. All these anoles surely have different stories for how they got to Miami, and some research has shed light on this issue. But what is unknown about anoles in this city is how they manage to proliferate when the temperature can be unforgiving to developing embryos (Sanger et al. 2018; Hall and Warner 2018).

Anolis lizards have attracted the attention of many anolologists that are mesmerized by their conspicuously beautiful dewlap displays, superb clinging abilities (Donihue et al. 2018; Winchell et al. 2018), and an urge to show off their physiology (Battles and Kolbe 2018). However, one aspect of their biology that is much less conspicuous is their nesting behavior. Even biologists that have devoted countless hours studying their behaviors know very little about where females lay eggs, what microhabitats they prefer, and how those nesting behaviors impact embryonic development. In this recently published study, we unveil the mystery of where these city slickers’ nests are located compared to their forest-dwelling counterparts.

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