Anolis nubilus male and female from The Anoles of the Lesser Antilles.
In 1972, James “Skip” Lazell published a monograph on the Anoles of the Lesser Antilles including the species description of Anolis nubilus, an endemic anole restricted to the island of Redonda. His description of the animal and island, like the rest of the monograph, is colorful and evocative:
“The tiny islet is exceedingly steep-to, and rises nearly 1000 feet out of the sea. There is virtually no surrounding bank, and the full swell of the western North Atlantic pounds Redonda’s cliffs. A tiny, nearly vertical gut on the leeward side provides the only access to the top of the islet up the cliffs; great blocks of basalt lie at the foot of this gut and one’s original entrance to Redonda is made by jumping onto these blocks as the boat goes past them. It is about like jumping from a moving elevator onto a card table, except that elevators give more notice of directional reversals… but getting on is just the beginning. …
The top of Redonda is a rolling wold and a favorite place of innumerable nesting sea birds; the gut provides a route for their guano to descend the cliffs, and it dries to a thick powder there. Because of its lee-ward location, a chimney effect is produced in the gut, and the guano dust, mixed with the volcanic sand weathered from the parent rock, tends to rise when disturbed. As one toils up the gut under the tropical sun, one is accompanied by a cloud of this dust, which soon mingles with one’s own sweat to produce a wondrously aromatic and abrasive, though rather gluey, bath. At the top, jumbles of rocks and clumps of prickly pear rise gently to the old ruins, complete with a hedge of bougainvillea and a single tree. This is the home of Anolis nubilus. …
Surely Redonda once supported more vegetation, and presumably Anolis nubilus then had an easier life. The feral goats should be extirpated on this remarkable island, whose only known nonflying vertebrates are species found nowhere else on earth.”
Now, 45 years, 1 week, and 4 days later, I’m headed to Redonda to gather baseline lizard data on exactly such a goat extirpation.
Skip did miss one nonflying vertebrate in his account; Rattus rattus has taken up residence en masse on Redonda. The black rats are so plentiful now that they’ve taken to stalking the lizards on the island in daytime—“tiger rats,” according to Dr. Jenny Daltry, one of the researchers leading the island restoration effort. And so, the government of Antigua and Barbuda, in conjunction with numerous conservation NGOs including Flora and Fauna International, has decided to remove the goats and rats from Redonda in an attempt to restore the island and help its three endemic lizard species to recover.
Redonda is home to not just A. nubilus but also a jet black ground lizard, Ameiva atrata and an as-yet unnamed dwarf gecko, Sphaerodactylus sp. Presumably, A. nubilus would be perched high in vegetation avoiding the roving A. atrata; however, after centuries of goat grazing on Redonda, that vegetation has been reduced to a single Cassuarina tree. So, while that tree is likely swarming with anoles, most of the A. nubilus are spending their time hopping around the boulders of Redonda. Normally this would put them in range of the roving ground lizards, but it sounds as though both lizards should be more worried about those hungry black rats.
Fortunately for all of Redonda’s reptiles, as of a few weeks ago the goats on the island took a one-way ferry ride to new pastures (not a euphemism) and, well, starting soon the rats will be making their way to the great big garbage heap in the sky (definitely a euphemism). My goal is to get to Redonda and gather as much baseline data on the lizards as possible to see whether and how the lizard community changes on a goat-less, rat-free Redonda.
That’s no easy task, though. Here’s a picture of Redonda:
Photo credit: Dr. Jenny Daltry. I’m reasonably sure that’s the gut there, in the foreground of the image.
Believe it or not, that’s the pleasant side of the island. Here’s the other:
Photo credit: TopTenz.net
We decided that hauling a week’s worth of research and camping gear up Lazell’s gut (let alone jumping to that card-table basalt) was out of the question, so I’m going to be arriving by helicopter. As if the rats weren’t enough, Redonda has no source of fresh water so we’ll be carrying in food and drink for the 8 days on the island. No power either, so I’ve been putting together solar kits to try to get enough juice to run a computer and spectrophotometer.
All in all, it’s going to be an adventure! I’ll update Anole Annals when I return, but I’ll also be posting more frequent updates to my personal blog and twitter. I’d love to hear from you, especially if you have any tips for rat-proofing tents (seems more efficient to just bait the other ones, right?).
Citation: Lazell, J.D. 1972. The Anoles (Sauria, Iguanidae) of the Lesser Antilles. Bulletin of the Museum of Comparative Zoology. 143(1).
What a lovely festive (a.k.a., brown) anole!
For more on the new AMNH exhibit on Cuba, see our previous report.
h/t to Sandra Buckner for notifying us of this magazine cover.
It’s been a while since we updated this montage…and at least a few months since the last anole cover. Get to work, everyone! And let me know if we’ve missed any.
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.
Peter Uetz of the Reptile Database fame sends the following Valentine’s Day greetings:
If you or your significant other loves anoles, you may want to show her/him this hearty Anolis distichus (Figure 2960, above) on occasion of today’s Valentine’s Day. It clearly shows a heart on it’s head. Some other specimens such as the couple in Figure 3297 (right, from locality 1 in the Google map), also show a heart although it’s not as pronounced. Also note their blunt coloration which doesn’t seem to affect their affection.
Anolis distichus is pretty variable and even within this subspecies, A. d. dominicensis Reinhardt & Lütken 1863, to which all these specimen belong, there is considerable variation. By the way, the guy with the heart (Figure 2960) is from the same locality 3 as two other specimens which do not have a heart (Figures 2948 and 2968) although they display a similar shape on their heads. Figure 3087 shows yet another specimen for comparison, this time from locality 2.
2968
2948
3087
Various authors have described a dozen subspecies from Hispaniola (reviewed in Schwartz 1971, see map 2 from that paper). The northern half of Hispaniola is almost entirely in the hands of A. d. dominicensis, hence the specimens on the photos have been assigned to that subspecies.
Note that Glor & Laport 2012 elevated several Dominican subspecies of A. distichus to full species level, namely A. dominicensis, A. favillarum, A. ignigularis, A. properus, and A. ravitergum. The Reptile Database hasn’t followed this yet because their geographic sampling was limited to relatively few localities and they did not provide any updated diagnoses (but their recommendations have been recorded in the database). Also, there seems to be hybridization among several of these populations.
Photo localities:
2948: 3
2960: 3
2968: 3
3087: 2
3297: 1
Acknowledgments
Thanks to Miguel Landestoy and Luke Mahler who helped with the IDs.
References
Glor, Richard E.; Robert G. Laport 2012. Are subspecies of Anolis lizards that differ in dewlap color and pattern also genetically distinct? A mitochondrial analysis. Molecular Phylogenetics and Evolution 64 (2): 255-260. http://www.sciencedirect.com/science/article/pii/S1055790310004276
Schwartz, A. 1968. Geographic variation in Anolis distichus Cope (Lacertilia, Iguanidae) in the Bahama Islands and Hispaniola. Bull. Mus. comp. Zool. Harvard 137 (2): 255- 309. http://biodiversitylibrary.org/page/4784182
Schwartz, A. 1971. Anolis distichus. Catalogue of American Amphibians and Reptiles (108)
(used to be available online at ZenScientist, and maybe soon at the SSAR website again).
Anolis distichus in the Reptile Database
http://reptile-database.reptarium.cz//species?genus=Anolis&species=distichus
(an extended synonymy and distribution section will appear in the next database release)
The database entry also has another 43 references most of which are available online.
Any congress advertising with a horned anole (Anolis proboscis) must be worth attending. Check out the details at the conference website.
A new paper in Zootaxa aims to figure it out, based on the travel journals of its describer, Franz Werner. Here’s the paper’s abstract:
The eminent Austrian zoologist Franz Werner described several new species of amphibians and reptiles from America, including Anolis aequatorialis Werner, 1894 and Hylodes appendiculatus Werner, 1894. Both species were described based on single specimens, with no more specific type localities than “Ecuador” (Werner 1894a,b). After its description, A. aequatorialis remained unreported until Peters (1967) and Fitch et al. (1976) published information on its distribution and natural history. Anolis aequatorialis is currently known to inhabit low montane and cloud forest on the western slopes of the Andes from extreme southern Colombia to central Ecuador, between 1300 and 2300 m elevation (Ayala-Varela & Velasco 2010; Ayala-Varela et al. 2014; Lynch et al. 2014; D.F. Cisneros-Heredia pers. obs.). Likewise, Hylodes appendiculatus (now Pristimantis appendiculatus) remained only known from its type description until Lynch (1971) and Miyata (1980) provided certain localities and information on its natural history. Pristimantis appendiculatus is currently known to occur in low montane, cloud, and high montane forests on the western slopes of the Andes from extreme southern Colombia to northern Ecuador between 1460 and 2800 m elevation (Lynch 1971; Miyata 1980; Lynch & Burrowes 1990; Lynch & Duellman 1997; Frost 2016). To this date, the type localities of both species remain obscure. The purpose of this paper is to restrict the type localities of Hylodes appendiculatus Werner, 1894 and Anolis aequatorialis Werner, 1894 based on analyses of the travel journals of their original collector.
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. porcatus clustered 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!
Male (left) and female (right) brown anoles (sizes are not to scale)
Among their many contributions to evolutionary biology, anoles have historically been at the forefront of research on sexual dimorphism. Much of the recent work in this area focuses on a very general question – how do males and females express different phenotypes despite sharing essentially the same underlying genome?
Not surprisingly, the answer often depends on the type of scientist you ask. An endocrinologist might say that the development of sexual dimorphism requires hormones such as testosterone and estradiol. A quantitative geneticist might reply that it involves the reduction of genetic correlations between the sexes. A molecular geneticist might view the problem as one of regulating the expression of shared genes differently in each sex. Can anoles help us put these different perspectives together into a unified framework for sexual dimorphism?
To address this question, our lab at the University of Virginia teamed up with Christian Cox (Georgia Southern), Joel McGlothlin (Virginia Tech), and Daren Card, Audra Andrew, and Todd Castoe (University of Texas, Arlington). The full details are available in The American Naturalist, but here’s a quick rundown of the highlights:
We conducted a breeding study on a captive colony of Anolis sagrei, a species in which adult males average nearly three times the mass of females. We found that the extent to which males and females share heritable variation for body size starts out high early in life, but declines rapidly as sexual dimorphism emerges during development.
This breakdown of genetic constraint is mirrored by a sharp increase in the sex-biased expression of hundreds of autosomal genes in the liver, particularly those genes that regulate growth, metabolism, and cell proliferation. In other words, although male and female anoles share most of the same genes, each sex tweaks the expression of these genes in different ways as development progresses.
How do they do it? We also show that some of the patterns of male-specific gene expression that emerge later in life can be induced by treating juvenile females with testosterone. Putting these pieces together, we propose that hormones help male and female anoles regulate their shared genes in different ways, which allows them to attain dramatically different body sizes and also helps break down genetic correlations that would otherwise constrain their independent evolution. We hope that our study encourages other Anolis biologists to continue building connections between evolutionary genetics, developmental biology, and endocrinology!