And we’re open to suggestions for new species to feature on a lovely wrist fob. Suggest away!
Here at Anole Annals, we’re all familiar with the replicated evolution of different anole ecomorph types in the Greater Antilles. However, divergence into these different ecomorph classes is not enough to explain how the group became so speciose on these islands. Additional factors must therefore have promoted speciation throughout the history of the group.
One potential factor is the flashy anole dewlap. Dewlap diversification across anoles has led to the remarkable array of dewlap color, pattern and size we see today. If dewlap differences did indeed drive speciation in anoles, or are involved with the maintenance of species boundaries, we might expect that as differences in dewlap color and pattern increases between species, genetic differentiation will also increase through fewer hybridization events.
In our study that just came out in the Journal of Herpetology, Rich Glor, Anthony Geneva, Sabina Noll and I set out to test this using two widespread species from the Anolis distichus species complex, A. distichus and A. brevirostris. These two species co-occur in many locations on Hispaniola and, while they often differ in dewlap color where they do co-occur (yellow with an orange patch vs. all pale yellow), in other areas, they co-occur with similarly pale dewlaps. Using mitochondrial DNA, microsatellite and AFLP data, we investigated patterns of genetic differentiation at four sites: two where the species differ in dewlap color, one where the species share the same dewlap color, and another where pale dewlapped A. brevirostris co-occurs with two A. distichus subspecies (one with a similarly pale dewlap and the other with an orange dewlap).
In general, we found that A. distichus and A. brevirostris looked like “good species,” with strong genetic differentiation and little evidence of hybridization, even at a site where they share the same dewlap color. This suggests that dewlap color differences are not associated with genetic differentiation in a manner one might expect if dewlaps were involved in the speciation process or in maintaining species boundaries. However, at the site where A. brevirostris co-occurs with two A. distichus subspecies with both similar and dissimilar dewlap colors, we found some evidence of hybridization and the species were not as highly genetically differentiated. This discrepancy suggests that site-specific factors could be influencing the dewlap’s role in speciation or maintaining species boundaries. For example, as Leo Fleishman’s and Manuel Leal’s work has shown (e.g. 1, 2, 3), the dewlap’s effectiveness as a signal is dependent on the light environment. Further understanding about the environmental differences among our study sites, how species utilize the available light microhabitats within each site, and how the dewlap looks to anoles at each site could provide more insight into our findings.
On the other hand, perhaps we need to be looking beyond the dewlap and focusing instead on whole signaling displays. Anole behavioral displays can also be strikingly different among species (e.g. 1) and may instead be the key to understanding species diversification in Greater Antillean anoles.
When someone first asked me about the major predators of anoles, my first thought was to talk about curly-tailed lizards (Leiocephalus carinatus) in the Caribbean, vine snakes (Oxybelis spp.) in the neotropics [see my previous post on anole predation by O. aeneus at La Selva], and birds. I think that as herpetologists, we tend to fall into the trap of thinking of invertebrates as “lesser” taxa to be preyed upon by small vertebrates like lizards, and in turn for small vertebrates to be eaten by larger vertebrates.
I, too, when thinking about how selective pressures shape morphological variation in mainland and island habitats turned to fellow herps and birds as the primary predation pressure for mainland anoles. However, it wasn’t until I arrived in Costa Rica that I discovered the high prevalence of voracious arthropods, and I realized that our beloved lizards had much more to fear!
In a single night at La Selva, I could easily find dozens of large wandering spiders (Ctenidae), and if I pointed my headlamp higher in the trees I could see eyeshine from hundreds of spiders. Given the high density of large ctenids at La Selva, it is not unlikely that anoles and small tree frogs constitute a major portion of their diet. In fact, I wouldn’t be surprised if large arthropods are one of the most common predators of mainland anoles in some regions.
The same might be the case for giant mantids of the genera Macromantis and Phasmomantis, and conocephaline katydids sporting fearsome mandibles (e.g. Copiphora spp.). Since the invasive Chinese mantids (Tenodera sinensis) in North America are well documented to prey on hummingbirds almost equal in size to the mantids [see Nyffeler et al. 2017], surely larger and bulkier species in the neotropics can take lizards much smaller than themselves. Even though wandering spiders and conehead katydids are primarily nocturnal hunters, I have heard many stories of these arthropods being implicated in anole and tree frog predation. Research looking into how ctenids and nocturnal katydids forage would help determine if they can actually detect sleeping anoles or if predation events occur from the arthropods simply running in to the anoles while on the move.
If anyone here on Anole Annals has any anecdotal or photographic records, please comment below.
To throw a twist on this discussion, is it possible for a spider to prey on a lizard two and a half times its size? A new paper about a vertebrate-eating jumping spider (Salticidae) describes just that! Considering arthropods as possible major players in anole predation could shed light on behavioral and ecological studies of mainland anoles.
Here are a few more spider photos to wrap up this blog post.
Getting good pictures of lizard toepads in the field can be tricky. Flatbed scanners are heavy and don’t take well to transit bumps and bruises, and getting a digital camera to focus on the toe, not the glass, requires surgical precision on the manual focus ring. I’ve just found a new solution for an iPhone (or GooglePixel, if that’s how you roll), and I’m eager to share.
You’ll notice that when the camera is facing up the iPhone screen is facing down. Obviously this makes it difficult to snap the photo—enter the app WiFiCam. This app enables you to type the phone’s IP address into your web browser and remotely trigger the camera, as long as both devices are on the same wifi. It’s very simple, and the price was right (free!).
And so here’s the whole shebang:
(Don’t forget to keep a tissue handy for wiping up lizard poop!)
And not to bury the lede, but the results are fantastic (see above).
A few things to note:
One last thought: Moment also has a fisheye lens that might do a really nice job of canopy cover photos in the field. That’s on my short list of things to experiment with in the near future!
I’d love to hear your thoughts on how to improve the system in the comments.
I recently saw these four anoles on a trip to Costa Rica. All four were sighted in La Fortuna in the province of Alajuela. They were sighted on July 18th and 19th, all within a few meters of a forested stream. I have some ideas about their ID’s, but am not completely sure. Can anyone help me with their identification?
This first anole was found on a tree trunk near the stream at night, while the second one was found on a pole in the morning. Both Anolis lionotus?
This third one was found on a low shrub in the morning. Anolis limifrons?
The fourth anole was found on a low-growing shrub at night. Anolis lemurinus?
Thank you in advance for your help.
Shane Campbell-Staton had fortuitously measured the thermal physiology of a number of populations of the green anole, Anolis carolinensis, the summer before 2014’s Polar Vortex. So, he went back and examined the survivors. And sure enough, in the most southerly populations, those most strongly affected by the cold snap, natural selection had occurred. Shane tells Scientific American all about it in this podcast. The nifty figure above comes from the University of Illinois’ press release.
We reported recently that knight anoles (Anolis equestris) have shown up in the T&C. Here’s more on the story from B Naqqi Manco, the Terrestrial Ecologist at the Department of Environment and Maritime Affairs, Turks and Caicos Islands Government:
Cuban knight anoles are currently known from two sites on Providenciales: Vicinity of Beaches Resort in The Bight and Amanyara Resort on Northwest Point. Both populations showed up after the importation of large trees for landscaping from Miami. The properties are both irrigated pretty heavily to keep the bigger trees going. The tree imports were brought in before the Department of Agriculture was fully operative, so unfortunately things got in at that time that probably shouldn’t have made it through.
I don’t have confirmation of the knight anoles breeding, but I know The Bight population has been spreading with individuals having been found on adjacent properties and in a nearby residential neighbourhood. I would be very surprised if they’re not breeding on either site. Unfortunately we don’t have the capacity to monitor them well but this is something we want to keep a closer eye on and it would make a worthwhile research project for a student or intern.
Thus far, they have not been reported from any other island or cay.
The 11th Latin American Congress of Herpetology is underway right now at the Museo de Zoología QCAZ at Pontificia Universidad Católica del Ecuador. Although I could not attend, I have been following the meeting vicariously as attendees have been using the Twitter hashtag #latinherps to document the meeting. From those tweets alone, it appears the meeting has featured a series of fantastic talks, including many on anoles. If you are not a Twitter user you can still follow along by clicking more below to see all tweets from the Congress. Finally to Congress attendees, if any of you are interested, it would be great to have you contribute Anole Annals posts (or even comments below) on talks from the meeting.
Two recent talks at JMIH 2017 shed light on key morphological characters in anoles: toe pad shape and limb length. Travis Hagey presented his work which looks to shed light on why lizard toe pads are shaped the way that they are and addresses whether gecko and anole toe pads are convergent structures. Working with a team of undergraduates, Travis used geometric morphometrics to analyze the structure of toepads in a diverse group of geckos and anoles. Travis found that anole and gecko toe pads have a similar range of values for traits such as the placement of pads on the toes and the shape of the toes (skinny or fat) in relation to claws. However, anole toe pads formed a distinct cluster indicating that they occupy a unique area of trait space not used by geckos. This finding suggests that the divergent evolutionary history of anoles and geckos has resulted in independent evolutionary explorations of toe pad shape.
Immediately following Travis’ talk, Robin Andrews presented work investigating the embryological development of morphological characters in diverse lizard species. In anoles, consistent differences in the morphology of divergent species support the existence of different anole ecomorphs. Previous research by Sanger and colleagues has shown that the differences in limb-length between anoles of different ecomorphs have their origins early in embryonic development. These early differences in limb length continue throughout the development of anoles into hatchlings and adult forms, a pattern known as transpositional allometry.
Robin compared patterns of limb, tail, and head growth in early stage embryos of four different lizard species, including a chameleon, two geckos, and the brown anole (Anolis sagrei). She found that species-specific differences in limb and tail lengths were exhibited as soon as limb and tail buds emerged from the body and were both best characterized by the same pattern, transpositional allometry. Embryonic head growth, however, showed no specific pattern. Robin’s findings suggest that the adaptive evolution of adult morphology in anole ecomorphs as well as other diverse lizard species is underpinned by developmental reprogramming.
Travis Hagey, Jordan Garcia, Oacia Fair, Nikki Cavalieri, and Barb Lundrigan: Variation in Lizard Adhesive Toe Pad Shape
Robin Andrews: Developmental Origin of Limb Size Variation in Lizards
All anole field biologists have been there, right? It’s the middle of the night, and you’re walking around the forest searching for sleeping lizards in the trees. You’re probably wearing a headlamp, so the bugs are flying around your face, and your eyes start to strain as you get sleepy and you’re entering hour three or four of the search. This searcher fatigue could lead to the kinds of unintentional bias that can interfere with our research. But there’s good news when it comes to anoles, as Amy Yackel Adams, a statistician with the USGS in Fort Collins, Colorado, reported on the last day of JMIH.
Dr. Yackel Adams works with a Rapid Response Team whose goal is to prevent the spread of the worst invasive species. When a report came in of a sighting of a brown tree snake on the island of Saipan (in the Northern Mariana Islands, western Pacific Ocean), the team of experienced herpers deployed to Saipan and began intensive nightly surveys to assess the possibility of a brown tree snake population there. Luckily, they didn’t find any of these snakes in the surveys, but they did log 20,000+ sightings of other vertebrates! These included emerald tree skinks, several species of geckos, a variety of small mammals, and the green anole (Anolis carolinensis). Dr. Yackel Adams saw an opportunity to use this rich dataset to statistically test for two types of bias that could occur in such surveys – searcher fatigue (both across the 4-hour nightly searches, and across the up-to-31 day deployment), and searcher bias in taxon detection.
The team of 29 searchers covered a total of 387 km of transects during the 31 days, and found a total of 5,800 sleeping green anoles during this time. (Wow!!) In terms of short-term searcher fatigue, there was a slight decrease in tree skink and mammal sightings as the night progresses, and gecko sightings were generally stable over the night, but far MORE green anoles were sighted in the later hours of the night. And over the long term, skinks and anoles were MORE likely to be detected the more nights a searcher worked, and there was no evidence of long-term searcher fatigue. So, that’s why my take-home message was “nobody gets tired of looking for anoles!”
There was, however, significant taxonomic bias among the searchers – for example, the skink-to-anole sighting ratios ranged from 0.86 to 9.5. Dr. Yackel Adams concluded that this type of bias could be a real problem for certain kinds of studies, and we should be aware that differences among sightings by our survey team members could be potentially problematic in statistical analyses.
In their 2008 review “Are islands the end of the colonisation road?” Bellemain and Ricklefs (2008) concluded that oceanic islands could be important sources of colonisation of mainland continental areas and cited anoles of the Norops clade as a notable success. There are more than 5 times as many Norops clade species in Central and northern South America as in the West Indies; the 23 extant Caribbean species in the clade are distributed in Cuba and Jamaica with one species in Grand Cayman (Nicholson et al, 2005). Data in Nicholson et al (2005) gave support to the reverse colonisation hypothesis, but did not offer specific dating for the colonisation.
New analyses of 65 species in the Exophthalmus weevil genus complex (Zhang et al 2017) have turned up results that are of significance in understanding the biogeographic history of Caribbean anole dispersal and diversification. Like anoles of the Norops clade, the weevils show reverse colonization (island-to-continent), with diversification on the mainland and diversification within the islands. The data also give some support for overwater dispersal as the factor best explaining ancient between-island distribution.
Zhang et al’s best fit biogeographic model gives an estimate of 19Ma for a jump dispersal of Exophthalmus, most likely from Hispaniola, which went on to diversify into more than 40 species in Central America. So – did the anoles and the weevils make their journeys to the mainland around the same time and under similar conditions? Can this weevil study and the techniques it uses to arrive at its conclusions inform anole evolution and dispersal?
Bellemain, E and RE Ricklefs (2008) Are islands the end of the colonisation road? Trends Ecol Evol. 2008 Aug; 23(8):461-8. doi: 0.1016/j.tree.2008.05.001. Epub 2008 Jun 26. (Correction to citation numbering: Trends Ecol Evol. 2008 Oct; 23(10):536-7).
Nicholson, KE, RE Glor, JJ Kolbe, A Larson, S Blair Hedges, JB Losos (2005) Mainland colonization by island lizards. Journal of Biogeography 32 (6), 929-938.
Zhang, G, U Basharat, N Matzke, NM Franz (2017) Model selection in statistical historical biogeography of Neotropical insects—The Exophthalmus genus complex (Curculionidae: Entiminae). Molecular Phylogenetics and Evolution, 109, 226-239. DOI: 10.1016/j.ympev.2016.12.039.
For most of the history of life on earth, the only sources of light at night were the moon and stars. Yet with the invention and rapid spread of electric light, species around the world now face a novel evolutionary pressure: artificial light at night, or ALAN. Artificial light likely has an especially strong effect on animals in city habitats, such as the urban-adapted brown anole lizard, Anolis sagrei. Chris Thawley and Jason Kolbe at the University of Rhode Island set out to determine whether brown anoles were negatively impacted by ALAN.
In addition to their abundance in urban environments, brown anoles are a particularly good species for this study. Previous studies of brown anoles have shown that photoperiod influences the onset of reproduction at the beginning of the breeding season, and that several behavioral traits change under artificial light. In addition, work by Moore and Menaker has shown that pineal production of melatonin in this species is significantly altered by photoperiod. So, would ALAN influence brown anole growth and reproduction?
Chris and Jason collected lizards from south Florida and set up a lab experiment where some lizards experienced a normal photoperiod, and others were exposed to ALAN that mimicked landscape lighting. Their results were quite unexpected! ALAN actually increased female growth, resulted in eggs laid earlier in the season, and increased the reproductive output of small females – but did not affect the number or mass of eggs or hatchlings. And, ALAN females did not exhibit more stress (measured via circulating corticosterone) than control females.
So are brown anoles just superlizards? Do they have no trade-offs that result from ALAN? Chris suggested that it’s possible that such trade-offs may appear in studies over a longer time period, or in traits not measured here. Or, perhaps ad libitum food and the absence of predators in the lab remove the costs of ALAN. Or, maybe these really are indefatigable lizards!
An extensive body of work has addressed the eco-evolutionary impacts of the Northern Curly-tailed Lizard (Leiocephalus carinatus) on Brown Anoles (Anolis sagrei) (much of it receiving coverage right here, here, and here on Anole Annals!). These species co-occur not only on many Caribbean islands where much of this research has taken place, but also within the urban matrix of southern Florida, where both species are introduced.
Camila Rodriguez-Barbosa and Steve Johnson investigated the impacts of curlies on brown anoles in shopping centers in southern Florida where both species were plentiful. Camila first collected baseline data on anole and curly populations at eight sites before embarking on a quest to eliminate curlies from four of her sites. Over the next four months, she removed over 300 (!) curlies from these sites, many of which had brown anole remains in their stomachs.
She found that this removal had serious consequences for brown anoles. Compared to anoles from shopping centers where curlies were unchanged, A. sagrei at removal sites experienced higher survival and consequently greater abundances. These anoles also shifted to lower perches once curlies were removed, mirroring results from previous work which show that the introduction of curlies leads to brown anoles occupying higher perches to escape this dangerous predator. Camila’s work suggests that brown anole/curly-tailed lizard interactions may be similar even in very different habitats and provides a fascinating look at lizard life (and death) in the urban sprawl of southern Florida.
Sometimes a scientist just needs hundreds of hatchling anoles for an experiment. Tim Mitchell found himself in this position recently, and, like a good lizard ecologist, he started breeding colonies of anoles in the lab to produce eggs to incubate until hatching. As he created three different breeding colonies from brown anoles (Anolis sagrei) in central Florida, one each in February, June, and September, Tim found that he had also created an ideal situation in which to examine how the reproductive condition and output of brown anoles varies across the breeding season.
Tim, along with his coauthors Josh Hall and Dan Warner, found that females produced eggs with significantly greater mass later in the breeding season. These eggs took longer to produce than those earlier in the year (a greater interclutch interval), and the eggs resulted in hatchlings that had higher mass in relation to the weight of their eggs. These reproductive differences remained even after accounting for the fact that female anoles were also larger and heavier later in the year.
These findings suggest that female A. sagrei may shift their reproductive effort from producing a higher quantity of eggs (i.e., more, smaller eggs resulting in smaller hatchlings) in the beginning of the breeding season, to producing higher quality eggs (i.e., fewer, larger eggs resulting in larger offspring) later in the breeding season. Tim’s findings also stress the importance of investigating and accounting for seasonal differences when examining reproductive output in lizards.
Greetings from Austin, Texas, and the Joint Meeting of Ichthylogists and Herpetologists! Chris Thawley and I have appointed ourselves to be your AA reporting team from JMIH, and we’re aiming to post updates from each of the 8 anole talks and posters at this meeting.
On the first day of the conference, there were two exciting talks on the ecology of Costa Rican anoles. The first was by Brian Folt, a graduate student in Craig Guyer’s lab at Auburn, who developed a model of predator-prey co-occurrence where one of the prey were anoles (Anolis (Norops) humilis) and the predators were…spiders?! Yes, wandering spiders, or ctenids, can prey upon the small anoles on the forest floor. (The other putative prey were poison dart frogs, who have a relatively similar life history to anoles.) Brian performed an extensive field study in 14 plots at La Selva Biological Station, conducting visual encounter surveys for anoles, frogs, and spiders, and recording arthropods in leaf litter samples. He used two-species occupancy models to determine how prey were affected by the presence of the predator and by resource abundance in the leaf litter. The result? Anole occupancy was lower where spiders were absent, and the detection probability of anoles was higher when spiders were present and detected. This suggests that anoles are responding behaviorally, such that they may increase their vigilance when predators are around.
I then ran across the conference center to catch the next anole talk – a terrific presentation by Michelle Thompson, a graduate student in Maureen Donnelly’s lab at Florida International University. Michelle studied whether thermal quality differed across the stages of forest succession, and how that affected Anolis (Norops) humilis and A. (N.) limifrons distributions. She worked across transects of pasture, secondary forest, and old growth forest in both upland and riparian sites. Michelle measured the thermal quality of each habitat, the thermal preferences of the lizards, and the location and abundance of the lizards. She found that thermal quality was lowest in the pasture sites, as temperatures were frequently higher than the lizards prefer. Yet, in these pasture sites, riparian habitat with remnant trees provided a thermal refuge for the lizards. This kind of work can help us understand why and how species may respond differently to human-caused alterations in habitat structure and temperature in our changing world.
Stay tuned for updates from JMIH, and follow the #JMIH17 hashtag on twitter for more herp-related news!
Two years ago, McCranie and Kohler published The Anoles of Honduras: Systematics, Distribution, and Conservation(available on Amazon for under twenty bucks and downloadable for free on the Museum of Comparative Zoology website).
In turn, two mostly favorable reviews were published. However, one of the reviews, by Levi Gray, did question whether a number of anole species recognized from small distributions in Honduras should be recognized as valid species, rather than just as populations of species that are widespread throughout Central America.
Writing in Zootaxa, Randy McCranie has now responded to this point, forcefully arguing that the species should be recognized and challenging his critics to present their own data if they feel otherwise. You’ll have to read Gray’s review and McCranie’s rebuttal yourself to decide what you think. Gray made his skepticism clear, he also did clearly call for more research to address the question.
These pages have previously told the tale of Anolis lineatus, the species whose is different on one side compared to the other. Now the work has been published in Breviora. Like all publications of the Museum of Comparative Zoology, the paper can be downloaded from the museum’s publications webpage.
The research project was actually explained in a delightful video put together by the three joint authors, all of whom are headed to college this fall.