Adult male A. cristatellus in survey position on a tree next to an urban street. Photo credit: Renata Brandt
Walking down “Red Road” in Pinecrest neighborhood of Miami, FL, it is hard to miss a myriad of lizards on trees and street lamps. Among the many city-dwelling residents, the Cuban brown anole (A. sagrei) and the Puerto Rican crested anole (A. cristatellus) are seen virtually everywhere. While there is evidence that anoles are adapting to urban landscapes, most past studies have focused on adult stages (Kolbe et al., 2012; Winchell et al., 2016; Lapiedra et al., 2017) and early life stages have been largely ignored. Our recently published study in the Journal of Thermal Biology (Tiatragul et al., 2017) was the first to address how anole embryos could facilitate establishment of populations in cities.
The transformation of natural habitats into urban landscapes dramatically alters thermal environments, which in turn, can impact local biota. For ectothermic organisms that are oviparous (like anoles), developing embryos are particularly sensitive to these altered environments because they cannot behaviorally thermoregulate and are largely left to the mercy of their surrounding environment. Yet, we know little about how thermal environments in urban and forested areas affect embryo development and hatchling phenotypes.
Mean incubation duration is shorter when eggs are incubated at urban temperatures (hotter). See publication for full results.
To determine if embryos from urban and forested sites are adapted to their respective thermal environments, we incubated eggs with temperature regimes that mimic likely nest conditions in both urban and forested environments. Our results show that for two species (A. sagrei and A cristatellus), urban thermal environments accelerated development, but had no impact on egg survival or any hatchling phenotypic traits measured (including body size, running performance, and locomotor behavior). Furthermore, there is no evidence that embryos from either habitat are adapted to their respective thermal environments. Rather, this lack of major effects suggests that both anole species are physiologically robust to novel environments. This may explain their success in establishing populations in human-modified landscapes.
Physiological adaptation by embryos are not required for a population to establish successfully. Maternal behaviors, like maternal nest site selection could shield embryos from lethal conditions. Hence, our next study is going to involve quantifying maternally selected nest sites in the urban and forested landscapes.
Anolis sagrei has successfully invaded several countries including the United States, Mexico, some Caribbean islands, and even Taiwan and Singapore in Asia. As an invasive species, brown anoles can reach high population densities, expand their range rapidly, and have a negative effect on native species of lizards.
Now, this tree lizard has gone further. A group of Ecuadorian herpetologists recently discovered some individuals of this species in two localities on the Pacific coast of Ecuador. These individuals also represent the first record of this invasive species in South America.
A juvenile male individual of Anolis sagrei found in Ecuador
World map showing the distribution of Anolis sagrei. Green spots correspond to native distribution, blue spots non-native distribution, and the red star corresponds to the new records from Ecuador.
Individuals were found in an urban area with a mix of native and introduced species of plants. Although an established population has not been confirmed, this finding certainly represents a potential threat to local species of lizards from Ecuador, home to 38 species of anoles. A note reporting this discovery is in publication process.
Acknowledgments
Thanks to Omar Torres-Carvajal who helped with the post.
Several anole species have become established outside of their native ranges as a result of human-mediated transportation, being introduced to Japan, Singapore, Taiwan, Hawaii, the continental U.S., and beyond. Alien anoles can have major impacts on the ecological communities that they invade, for instance leading to local extinction of arthropod taxa and displacing native anole species. It is therefore key to detect and report instances of introduction by these potentially aggressive invaders, as well as to document their geographic spread in colonized regions. In a recent paper, we report on the presence of Anolis porcatus, a species native from Cuba, in coastal southeastern Brazil, using DNA sequence data to support species identification and examine the geographic source of introduction.
Anolis porcatus collected in Brazil, and comparison with the native anole A. punctatus. A, male A. porcatus showing green coloration. B, male A. porcatus showing brown coloration. C, the pink dewlap of male A. porcatus. D, female A. porcatus. E, male A. punctatus, a native anole species. F, the yellow dewlap of male A. punctatus. Picture credits: A–D, Mauro Teixeira Jr.; E, Renato Recoder.
Perhaps embarrassingly, this study started with Facebook. On August 2015, Ricardo Samelo, an undergraduate Biology student at the Universidade Paulista in Santos, posted a few pictures of an unknown green lizard in the group ‘Herpetologia Brasileira.’ A heated debate about the animal’s identity took place, with people eventually agreeing on Anolis carolinensis. On my way to Brazil to join the Brazilian Congress of Herpetology, I contacted Ricardo (but only after properly hitting the ‘like’ button) and proposed to examine whether the exotic anole was established more broadly in the Baixada Santista region.
To our surprise, local residents knew the lizards well, with some people quite fond of the ‘lagartixas’ due to their pink dewlap displays. People could often tell when the anoles were first noticed in the vicinities – ‘six months’, ‘nine months’, ‘one year ago’ –, suggesting a rather recent presence. Guided by these informal reports, we sampled sites in the municipalities of Santos, São Vicente and Guarujá, where we found dozens of lizards occupying building walls, light posts, fences, debris, trees, shrubs, and lawn in residential yards, abandoned lots, and alongside streets and sewage canals. It was clear that the alien anoles are doing great in human-modified areas; the high density of individuals across multiple sites, as well as the presence of juveniles with various body sizes, seem to suggest a well-established reproductive population.
Sites in the Baixada Santista in southeastern coastal Brazil where introduced A. porcatus were detected. 1, Guarujá. 2, Santos. 3, São Vicente. Green indicates Atlantic Forest cover; gray indicates urban areas; black indicates water bodies.
By reading and bugging experienced anole researchers about the Anolis carolinensis species group, I learned about paraphyly among species, hybridization, and unclear species diagnosis based on external morphology. As a result, my PhD supervisor, Dr. Ana Carnaval, and I decided to recruit Leyla Hernandez, by the time an undergraduate student in the Carnaval Lab at the City University of New York, to help generate DNA sequences to clarify the species identity, and perhaps track the geographic source of introduction in Brazil. To our surprise, a phylogenetic analysis found Brazilian samples to nest within Anolis porcatus, a Cuban species that has also been introduced to Florida and the Dominican Republic. Brazilian A. porcatusclustered with samples from La Habana, Matanzas, and Pinar del Río, which may suggest a western Cuban source of colonization. Nevertheless, Brazilian specimens are also closely related to a sample from Coral Gables in Florida, which may suggest that the Brazilian population originated from lizards that are exotic elsewhere.
Phylogenetic relationships of A. porcatus introduced into Brazil (indicated in red), inferred using MrBayes based on a mitochondrial DNA locus. Purple indicates samples of A. porcatus invasive elsewhere (Florida and the Dominican Republic). Blue indicates native Atlantic Forest anole species. Asterisks indicate posterior probability >0.95. Picture depicts a male A. porcatus collected in São Vicente, Brazil.
The presence of A. porcatus in the Baixada Santista may be related to the country’s largest seaport complex, the Porto de Santos, in this region. Numerous storage lots for intermodal shipping containers were situated near sites where the lizards were detected, and in one instance we found the animals sheltered inside an open container. An exotic green anole (identified as A. carolinensis) was previously found in Salvador in Brazil’s northeast; like Santos, Salvador hosts a major seaport complex, which may indicate that the exotic anoles reached Brazil after being unintentionally transported by ships bringing goods from overseas – perhaps twice independently.
It is currently unclear whether A. porcatus will be able to expand into the surrounding coastal Atlantic Rainforest, or into more open natural settings such as shrublands in the Cerrado domain. It is also unknown whether this species will have negative impacts on the local ecological communities. In Brazil, introduced A. porcatus may potentially compete with other diurnal arboreal lizards, such as Enyalius,Polychrus, Urostrophus, and the native Anolis. Five native anoles inhabit the Atlantic Forest (for sure): A. fuscoauratus, A. nasofrontalis, A. ortonii, A. pseudotigrinus, and A. punctatus. While none of them is currently known to occur in sympatry with A. porcatus, the worryingly similar A. punctatus has been reported for a site in Bertioga located only 50 kilometers from the site in Guarujá where we found the exotic anoles.
To properly evaluate the potentially invasive status of A. porcatus in Brazil, we hope to continue assessing the extent of its distribution and potential for future spread, as well as to gather data about whether and how A. porcatus will interact with the local species – especially native Brazilian anoles. This seemingly recent, currently expanding colonization also represents an exciting opportunity for comparisons with other instances of introduction of A. porcatus, as well as the closely-related A. carolinensis, based on ecological and phenotypic data.
Studying such mysterious alien anoles in Brazil was made much more tractable through advice from Jonathan Losos and Richard Glor. Thank you!
Figure from a new paper by Yasumiba et al. illustrating how LAGs in the cross sections of bones can be used to infer lizard age.
Anolis carolinensis is a disruptive invasive species in the Osagawara Islands near Japan, a UNESCO World Natural Heritage site. It was first recorded on the island of Chichi-jima in the 1960’s and has since spread to surrounding islands. A recent post on Anole Annals describes efforts to improve the effectiveness of adhesive lizard traps on the islands by using cricket bait.
A new paper by Yasumiba et al. improves our understanding of these invasive A. carolinensis by quantifying their longevity and growth rates using skeletochronology.
At the JMIH in New Orleans this past July, the 100th anniversary celebration of the ASIH was held at the Rock ‘n’ Bowl, where music, food, drink, dancing, and bowling were enjoyed by all. But for those who were alert on their way in, there was an added bonus: anoles! Or, at least, one anole, spotted by Quynh Quach and corralled by Kristin Winchell.
As other attendees file in, Quynh and Kristin spot their quarry in the bushes.
Taking a picture of the crowd filing in, I serendipitously caught our two intrepid anoleers about to make the catch in the bushes to the right of the entrance. Kristin made the grab, and displayed her catch.
Kristin displays the catch.
It was, of course, Anolis sagrei, the invasive Cuban species which has been spreading through the southeastern US for more than 80 years now. He was a nice-sized adult male, typical of the nominate form that occurs through most of the species’ US range. The edificarian habitat– in bushes at the edge of a parking lot next to a building– is also typical of where invasive sagrei can be found.
Adult male Anolis sagrei, New Orleans, Louisiana, 10 July 2016.
An appreciative crowd gathered.
Eager anolologists immortalize the NOLA anole in pixels.
Female green anole (Anolis carolinensis) photographed in June 2016 in Golf Las Americas (28°03 ̍43.5 ̎N, 16°43 ̍06.3 ̎N), in Tenerife island (Canary Islands, Spain) [left picture; uploaded to Facebook by: G. Frías García].; Right photo extracted from Neotropico Foundation].
In August 2013, a Cuban green anole (A. porcatus) was collected and given to insular authorities in the same locality [right picture; extracted from Fundación Neotropico]. According to this foundation, a small reproductive population of the Cuban green anole was established there at that time for some years. No precise data exist on the individual abundance or distribution of any of these species even though they could become invasive at some point and impact the natural ecosystems of these highly biodiverse islands. There is a lack of information on how these species have arrived to Tenerife, although they might be related to the commerce of plants to the islands, which are mainly imported to create tropical-looking gardens in touristic areas. According to the Invasive Species Database of the Canary Islands, other species of anoles such asA. sagrei, A. allogus andA. equestris have been reported at least once in the Canary Islands, all of them in Tenerife.
At JMIH 2016, I chatted with Johanna Wegener, a graduate student at the University of Rhode Island in Jason Kolbe’s lab, about her poster detailing her work identifying hybridization between Anolis carolinensis and A. porcatus in southern Florida.
Interspecific hybridization in anoles is thought to be fairly rare, with the best-known example being hybridization between Anolis carolinensis (native to the southeastern U.S.) and A. porcatus (native to Cuba) in southern Florida. I was surprised to learn how little we know about this rumored hybrid zone.
A. porcatus was likely introduced into Florida within the last few decades, but the striking morphological similarities between A. carolinesis and A. porcatus make anecdotal reports of hybridization hard to confirm. Wegener conducted the first genetic analyses of hybridization between A. carolinesis and A. porcatus. She genotyped 18 nuclear microsatellites from green anoles in Florida (Palm Beach and South Miami) and western Cuba and conducted a STRUCTURE analysis and found support for three genetic clusters consisting of Cuban A. porcatus, and two Floridian groups (one from Palm Beach and one from South Miami). With the addition of the mitochondrial ND2 marker, she found that the South Miami population had both A. carolinensis and A. porcatus haplotypes. Interestingly, there appeared to be very few recent hybrids; instead, the hybrid group appeared distinct from either parent group, suggesting that hybridization has been occurring for several generations.
In addition, Wegener looked at the variation in A. porcatus and A. carolinensis markers in each hybrid individual and found examples of some parent markers being retained at high proportions in the hybrids, possibly suggesting the retention of beneficial parent alleles in the hybrids.
Given that this study was only conducted at two sites in Florida, the exciting next step of this study is to better quantify the genetic makeup of hybrids across southern Florida and map out the hybrid zone.
While exploring the grounds of Fairchild Tropical Botanical Gardens with Janson Jones this past weekend, we extremely fortunately happened upon a large adult male Cuban knight anole (A. equestris) in full displaying swing. Despite the fact that knight anoles have an impressively large dewlap, I have often found this to be a relatively rare event, as large crown-giant species tend to display less than other smaller and more active species. This individual was displaying at a height of ~15 m, just below the fronds of a large Royal Palm (Roystonea regia). We didn’t see any other neighboring knight anoles, so were unsure if this was a directed or passive display series. In all, this lizard performed perhaps 4-5 sets of dewlap displays (each comprising of 4-5 dewlap extensions) before stopping and retreating back into the canopy.
Anoles typically follow a predictable and repeated pattern of display that gradually increases in intensity. Initially, and rather lethargically, an individual will nonchalantly raise its head and extend its dewlap without much extra effort (stage a); described below from Losos (2009).
Adapted from Losos (2009), which itself is adapted from Losos (1985). Aggressive behavior of A. marconoi showing three stages of increasing display intensity – note stage (c) include full body elevation alongside simultaneous tail and dewlap extensions.
This then escalates to include a slight body raise (stage b).
And ultimately results in a dramatic finale – in full display all limbs will be extended to raise both their body from the substrate (in this case the trunk of a palm tree) and elevate their tail (stage c). In the following picture you can see this final stage of displaying where intensity peaks – albeit in this individual with a regenerated (and rather stubby) tail.
The Lesser Antillean island of Saba (Caribbean Netherlands) harbors a unique anole species, Anolis sabanus, of which the males are easily distinguishable by their striking skin pattern. This endemic species is the only anole species found on the island, but is abundant within its native range of only 13 km2. Last April, a male individual was found outside of Saba on the neighboring island of St. Eustatius (Caribbean Netherlands) marking the first ever recorded exotic introduction of Anolis sabanus.
Anolis sabanus (Saban anole). Source: The Reptile Database.
While visiting relatives last week in Fort Myers (FL), anole enthusiast and avid wildlife photographer Kyle Wullschleger noticed a commotion among the trees while on an afternoon hike in a small neighbourhood nature preserve. On closer inspection he witnessed a group of red-bellied woodpeckers (Melanerpes carolinus) foraging on surrounding cypress trees, with a couple eventually appearing with their apparent target–non-native Cuban brown anoles (A. sagrei). He recalls some of the details:
“The photos from the sequence aren’t all that fantastic because I cropped in so it really just shows the behavior. The whole sequence the woodpecker was basically just slamming the anole against the tree and then trying to pick it apart – it was hard to tell what exactly it was doing, but I believe it eventually swallowed it whole before flying away–it hopped behind the tree so I couldn’t see it anymore.”
“There were at least five birds all moving up and down the lower third of the cypress trees just around the boardwalk I was on. They were moving around the trees without really knocking the wood, so maybe they were purposefully targeting anoles? I only saw successful predation twice, but the brush is so thick–it’s obviously happening quite a bit.”
![Anolis carolinensis (left) and A. porcatus (right), introduced to Tenerife, Canary Islands. [Left photo by G. Frías García; Right photo extracted from Neotropico Foundation].](https://i0.wp.com/www.anoleannals.org/wp-content/uploads/2016/07/Picture.jpg?resize=629%2C472&ssl=1)
