Martin Whiting of Macquarie University began his talk at the Animal Behaviour Society 2014 meeting by lamenting how little we know about the social lives of lizards, especially when compared with mammals, certain insects and fish, and most of all, those pesky other reptiles, birds. But the more we examine lizard social behaviour and cognition, the more apparent it becomes that these animals are capable of substantially more complexity than we previously thought possible. Whiting presented some recent research on the Eastern Water Skink, Eulamprus quoyii, that bolsters this view.
Eastern Water Skink, from the Whiting Lab Page
Though not often social, many lizards, including Eastern Water Skinks, live at densities high enough to allow individuals to be within sight of each other. This is a sufficient prerequisite for social learning, defined as learning a task by observing others and modifying one’s own behaviour accordingly. Whiting asked whether Eastern Water Skinks were capable of social learning by training “demonstrater” individuals to perform certain tasks, letting “observer” individuals watch these demonstraters, and then measuring whether this exposure to the demonstraters enhanced the observers’ success at the task at hand.
The answers to Whiting’s questions were not simple. First, age matters—young individuals were twice as likely to demonstrate social learning than old individuals. Second, the task matters—lizards learnt to associate a colour with a food reward by watching others, but the prerequisite task of actually flipping over the coloured cap to access a mealworm was not spurred by observing other individuals do the same.
In the future, Whiting and his students hope to conduct similar experiments with a variety of lizard species that differ in their degree of sociality. These experiments will definitively address the role of learning in shaping the social lives of lizards, and I can’t wait to see they find!
When I think of colour and pattern in lizards, I tend to think about showy visual displays. An example that springs to mind is this fantastic footage of Draco lizards using multiple appendages as colourful signals.
But despite all the effort an individual lizard puts into signalling to conspecifics, it must constantly remain wary of predators. Mimicry and camouflage are tried and tested means by which to evade predation, but little effort has been made to quantify the colours and patterns that may help lizards escape being eaten. Research presented by Danielle Klomp from the University of New South Wales at the Animal Behaviour Society 2014 meeting addresses this question in Draco cornutus, a South East Asian agamid lizard that uses the patagium, an extendable membrane attached to elongated rib bones, to glide from tree to tree.
Sampling in two populations of D. cornutus, Klomp noticed that though individuals in the two populations had identical dewlaps, they differed substantially in the colour and pattern of the patagium. Remarkably, the colours exhibited in each population seemed to perfectly match the colour of falling leaves of trees in the same habitat.
Patagia and falling leaves from two populations of Draco cornutus. Photos by Danielle Klomp.
By measuring spectral reflectances as well as the proportions of black on lizard patagia, falling leaves, foliage, and dead leaves, and accounting for how these colours might appear to predatory birds, Klomp demonstrated that in both colour and pattern, D. cornutus patagia in each population most closely matched falling leaves in the same population. This suggests that Draco are especially vulnerable to predation while gliding, and have undergone strong natural selection to mimic non-prey items in the particular environment they experience while gliding.
Here’s a link to Klomp’s poster from the International Society for Behavioural Ecology 2014 conference, and here’s a link to a blogpost about some very cool technology that Klomp used to make her poster come alive while presenting it.
Wouldn’t this be great? Maybe there’s one out there, still waiting to be discovered.
We’ve discussed the crisis concerning Jamaica’s Goat Islands previously. This film is the work of Robin Moore. Read more about the film and the efforts to preserve Jamaica’s iguanas on National Geographic‘s Newswatch. More relevant videos can be viewed at the Save Goat Islands website.
Here’s the first lizard talk from the Animal Behavior Society meetings! This is a guest post from Holly Brown, who studies visual and foraging ecology in herons at UConn.
Eye structure is remarkably similar among vertebrates. Therefore, one might, understandably, imagine human visual experiences to be representative of visual experiences across vertebrate taxa. However, this is not the case. Two important differences between mammalian and non-mammalian vertebrate vision are that, unlike us, the latter are able to move their eyes independently of one another, and they seem to lack stereopsis. Stereopsis is the ability to view the two independent images generated from each eye as a single image, which ought to make depth perception easier, and thus aid in important tasks such as capturing prey.
So instead of studying mammals, Gadi Katzir and his team of collaborators from the University of Haifa, Israel, are studying chameleons to better understand vertebrate vision.
Common Chameleon by Benny Trapp from Wikimedia
One of their recent experiments was aimed at finding out whether or not chameleons could simultaneously track two prey items independently with each eye, and if so, how independently (of one another) were the eyes able to move. They found that chameleons could simultaneously track different prey items with each eye, but at some point, they would always make a choice to converge both eyes onto their eventual prey target. Furthermore, they found that chameleons never struck at prey with their eyes still diverged. By pursuing this line of research, Katzir and his team may be able to glean insights as to how stereopsis may have evolved.
AA readers may remember from previous AA blog posts (here and here) that we have been tackling the field of anole palaeontology; the wonderful world of Amber Encased Anoles. This month, the first paper has been published in the Zoological Journal of the Linnean Society, on the Mexican amber fossil Anolis electrum (from the collection of UC Museum of Paleontology, Berkeley). And what a fossil!
The amber fossil (left) and x-ray CT reconstruction (right) of one of the two Mexican amber fossils of Anolis electrum. An ant (Azteca sp.) lies behind the right hindfoot. Part of the torso is also preserved (bottom of image). Morphobank images M323739 & M323741.
Kevin Chovanec of East Tennessee Sate University presented one of the most surprising and important posters at the JMIH conference this summer. In his poster, Kevin provides solid fossil evidence for the oldest crown group anole. Working with samples discovered along the Gulf Coast of Florida, Kevin found abundant and well-preserved fossil remnants from anoles. Apparently this material has been around for a while, but has been neglected as attention at these localities focused on identification of mammalian fossils. Kevin has identified the remains of what appear to be at least two species of anoles in deposits that are dated as 26-28 Ma and at least one species in deposits that are 19 Ma. None of this material possesses the traits that are diagnostic for members of the carolinensis series (the only group of extant anoles that was endemic to the United States prior to a wave of recent introductions). His work suggests the existence of a multi-species anole fauna dating back to the Oligocene. A phylogenetic analysis suggests that Kevin’s fossils are members of the anole crown group, but it is not possible to place them with any more phylogenetic precision. He did note, however, that they also lack the transverse vertebral processes that are diagnostic for the β anoles (a.k.a. Norops). The work Kevin presented was part of his masters project at East Tennessee State. I can’t wait to see what other insights emerge from Kevin’s work!
Anole jeans! Now marked down to $25. Get ‘em while they last!
Extensive googling reveals that the jeans are made by Nice Work Textile Jeans, Inc.
Long time AA readers will know that anoles frequently pop up in haute couture, perhaps most recently when Tommy Bahama created an anole-colored T-shirt.
Distribution records for Anolis cristatellus in Costa Rica reported in 2011 AA post.
Four years ago, we reported on the distribution of the Puerto Rican crested anole all along the Caribbean coast of Costa Rica. We also found the species inland, as far west as Turrialba and Siquerres, but not Guapiles (see map to right). A year later, we returned for a quick follow-up as part of a herpetology course spring break trip to Costa Rica. The weather wasn’t great and we failed to find cresteds in any place not previously reported; however, observations of brown basilisks, another sun-loving species, suggested that the weather was suitable enough, and that perhaps the absence of the anoles was real.
Two years later, this past March, another herpetology class trip ensued, and so another expedition was launched to Guapiles and environs. The team included AA correspondent Katie Boronow, an award-winning senior with expertise on A. cristatellus, and a sophomore in training for Miami field work this summer (more on them in posts to come).
And the results???
As mentioned in the previous post, the journal Herpetological Review is an excellent resource for anole natural history information. A frequent contribution is range extensions, often by county, for both native and introduced species. Range extensions are important pieces of information for biologists, as accurate county-level distributional data is crucial in many important exercises, such as mapping species richness in a region or identifying range boundaries (and then asking why the range ends in certain areas). This quarter’s issue has the following two range extensions.
Christopher Thawley and Fern Graves report a new county record for Anolis carolinensis in Bullock Co., Alabama, just south of Auburn. This apparently fills a hole in the confirmed range of the species in that part of Alabama.
Cory Adams and friends report an extension of Anolis sagrei range in Angelina Co., Texas. Interestingly, this specimen, as well as a specimen from Nacogdoches, Texas, were found in potted plants in Home Depot and Lowe’s garden departments. The authors posit that these animals turning up in East Texas are not range extensions, as in owing to the expansion of individuals from established ranges, but instead are the result of novel introductions facilitated by interstate transport of goods such as potted plants. If this is the case, these animals could have come from anywhere, not just the invasion front along the Gulf states. In other words, if the potted plants are coming from, say, Florida, then these animals would be leapfrogging their established conspecifics to potentially start new colonies and expand the range.
Adams, CK, D. Saenz, and JD Childress. 2014. Anolis sagrei (Brown Anole). Distribution. Herpetological Review 45: 282.
Thawley, CJ and F. Graves. 2014. Anolis carolinensis (Green Anole). Distribution. Herpteological Review 45: 282.
The journal Herpetological Review, published by the society for the Study of Amphibians and Reptiles, frequently has interesting anecdotal reports of natural history observations of anoles. This quarter’s edition has two: nocturnal activity in Anolis cristatellus and prey stealing behavior in Anolis sagrei. Here is a synopsis:
Dean and Jennifer Metcalfe report on nocturnal behavior of A. cristatellus wileyae observed (while perhaps on vacation) at the Nanny Cay Resort and Marina on Tortola, British Virgin Islands. The authors observed that the subject anole had navigated the interior of their hotel room in near darkness after dusk, selecting a nocturnal perching site on a lampshade. They suggest that this is similar behavior to that of an anole selecting an arboreal perch site at dusk. Two questions come to mind though. First, whether the room was completely dark- as the authors acknowledge that some light might have been entering the room- and whether the animal came from the outside into the room to perch or was residing in the room. Second, the author mentioned that this was the only anole seen on Tortola during her brief stay, which is also a bit unusual as the species should be abundant there. This might not add much to our understanding of anoles, but it certainly raises some questions about the co-habitation of humans and anoles.
The second note comes from David Delaney, a master’s student in Dan Warner’s lab at UAB, and friends, who report on an opportunistic A. sagrei in Ormond Beach, Florida. The anole had apparently been observing a predation attempt of a spider-wasp on a funnel-web spider. To summarize, the wasp attacked and envenomed the spider, captured it, and began dragging it across the ground. At this point the anole jumped to the ground, grabbed the spider, and took it up the tree to eat it. The wasp, likely disappointed, fled the area to hunt again.
Metcalfe, DC and JE Metcalfe. 2014. Anolis cristatellus wileyae (Vrigin islands Crested Anole). Nocturnal Activity. Herpetological Review 45: 323-324.
Delaney, DM et al. 2014. Anolis sagrei (Brown Anole). Prey stealing behavior. Herpetological Review 45: 324-325.
Hanna Wegener, a student with Jason Kolbe at the University of Rhode Island (and an Anole Annals contributor), presented a poster at JMIH on her efforts to identify the factors that drive morphological differentiation among Anolis sagrei populations found on 16 Bahamian islands near Staniel Cay. Hanna investigated morphometric, ecological, genetic, and demographic variation among these populations and, unlike many previous studies, considered variation in both males and females. Although Hanna did find significant morphometric variation among islands and between sexes, she did not find the significant correlation between morphometric variation and habitat use reported in prior work. She also did not find a significant relationship between morphometric and genetic variation. She did, however, find that population density influences morphometric variation, with lizards living at higher population densities having significantly longer heads than those found on lower density islands. Because these lizards on densely populated islands are also more likely to exhibit evidence of injury from other anoles (e.g., loss of limbs, digits, or claws), it is possible that their longer heads may indicate a response to intra-specific competitive interactions. However, interpretation of these results remains complicated because there is not a direct connection between injury and intra-specific competition, and the lizards on densely populated islands had longer heads, but not the wider heads that would have been expected if the goal of their morphometric shift was to increase bite force. Hanna undoubtedly has many more exciting questions to investigate with her ongoing research.
Great photos on Adventures Down South
Where do anoles poop? Will they chase laser points? Find out on Casey Gilman’s new blog on her Florida field research, Adventures Down South. Meanwhile, Chipojolab keeps the world abreast of goings-on in the Leal Lab. Most recently–Leal back in the Bahamas and multiple lab members cavorting in Puerto Rico! And Ambika Kamath’s afoot with her field crew in Gainesville, dodging frisbees and fire ants in quest of the wily festive anole. Finally, at Lizard and Friends, Michele Johnson talks about Puerto Rican anoles that are biting off more than they can chew. Or are they?
Do you have a blog on your research? If so, let us know!
Field laboratory in Puerto Rico. Read all about it in Chipojolab.
In a poster at JMIH 2014, Jonathan Clinger of Austin Peay State University found that spermiogenesis (the final step of spermatogenesis during which spermatids develop into mature spermatozoa) in Anolis sagrei is fairly similar to that previously reported in A. carolinensis.
Andrew Battles from the Kolbe Lab gave a talk at JMIH presenting data on performance-habitat relationships comparing lizard performance on rough and smooth surfaces. The data were collected on Guana Island in the British Virgin Islands using Anolis cristatellus and A. stratulus as study species. Andrew and his advisor, Jason Kolbe, were interested in whether lizards perform differently on artificial and natural surfaces.
Major differences between natural and artificial habitats
They used three different running tracks (37°-incline rough track, 90°-incline rough track, 90°-incline smooth track), assuming that artificial surfaces are smoother than natural ones. The rough tracks consisted of a board covered in window screen and the smooth track was a plain 2-by-4 board. They used a high-speed camera to measure maximum velocity, how often a lizard paused during the run and how often it slipped. While both species ran significantly slower, paused and slipped more often on the smooth surface, A. cristatellus performed even worse than A. stratulus. Andrew and Jason then conduced a field survey to test whether lizards in a human-modified habitat use both artificial and natural perches. In addition, they rated roughness of natural and artificial perches. When both types of perches were available, lizards used artificial perches more often than natural ones.
In human-modified habitats, lizards were found mostly on artificial perches
This is surprising, because artificial perches are significantly smoother than natural ones and lizards perform worse on smooth surfaces. Possible explanations are that other factors such as food availability and/ or predation may drive habitat selection on artificial substrates.
Following up on yesterday’s post, more research results from the Warner Lab on egg incubation were presented at JMIH. Corey Cates, a masters student from the Warner Lab, presented his data on developmental plasticity in Anolis sagrei. He used an experimental approach to test whether lizards incubated under dry conditions would survive better in a dry habitat than lizards incubated under moist conditions and vice versa. The idea for the study came from the observation that habitat and substrate differs among small islands in Florida. Some islands are scarcely vegetated and have dry substrate consisting of broken shells. Other islands are more densely vegetated and have dark soil that contains organic matter.
Corey collected 128 breeding pairs from four islands and incubated the eggs using the two different substrates. He also tested two different moisture conditions (wet and dry). He found that lizards incubated under wet conditions hatch on average 4-5 days later and hatchlings were significantly heavier than those incubated under dry conditions. In addition, lizards hatch significantly later when incubated in the soil substrate, which retains moisture longer than the broken shells. Corey further tested whether lizards raised under dry conditions have higher desiccation tolerance than lizards from wet conditions. He measured body mass before and after keeping the lizards in a desiccation chamber. Lizards that had developed under wet conditions lost 5% more mass than lizards developed under dry conditions.
Hatchlings incubated under wet conditions lost significantly more mass than hatchlings incubated under dry conditions.
This suggests, that plastic responses to different developmental conditions have an effect on physiological traits that might increase survival in a specific habitat. To test this, Corey then released the hatchlings on four experimental islands and measured hatchling survival using a recapture method.
Significantly more hatchlings survived in the open, arid habitat when eggs were incubated under dry conditions.
He found that significantly more hatchlings survived in open, arid habitats when eggs were incubated under dry conditions. No effect of incubation condition on hatchling survival was found in the shaded, moist habitat.
Yesterday at JMIH, Phillip Pearson reported results from work conducted with his thesis adviser at the University of Alabama, Birmingham Daniel Warner. Pearson investigated the impact of incubation environment on the brown anole (Anolis sagrei), and the effects of incubation in shaded versus open habitat and early versus late season in particular. Pearson reported several significant differences between the eggs (and resulting hatchlings) incubated under these two conditions. He specifically reported longer incubation intervals under early season and shaded conditions, smaller hatchling size under shaded conditions and better performance of hatchlings at 1 and 3 weeks for the eggs incubated under the late season regime. Performance of hatchlings was quantified as their speed and the number of times they stopped during a performance trial. This work is the latest in a string of interesting studies from the Warner Lab on the impact of incubation conditions on anoles. I was going to provide links to previous posts on Anole Annals about the Warner Lab‘s work, but there are so many that I’ll just suggest that you type “Warner” into the search box at the top of the page and enjoy for yourself.
I saw two talks on brown anoles in the same session this afternoon at JMIH. The second reported on the response of brown anoles (A. sagrei) to potential avian predators. Lisa Cantwell presented results of her work with Joe Altobelli and Sandy Echternacht on the behavior of brown anoles exposed to the calls of potential avian predators in a controlled laboratory environment. Cantwell has previously reported that anoles respond more strongly to the calls of predator birds than to white noise or non-predator birds (see also prior work on A. cristatellus in response to predator and non-predatory birds). Cantwell played the calls of four bird species to captive brown anoles and monitored their reactions. The four birds in the study included one species that co-occurs with, and preys upon, A. sagrei: the American Kestrel. The other birds were species that do not co-occur with A. sagrei: the White-rumped Falcon (gotta love the ornithologists and their descriptive common names), the Shikra, and the Lesser Kestrel (this name seems kind of demeaning and should probably be changed). Cantwell tested if the anoles responded more to the predator that they or their ancestors have likely encountered in nature than to the calls of predators that they or their ancestors have likely never encountered. The types of reactions that were viewed as indicative of increased vigilance in the lizards included head shifts, eye opening, and movement around the enclosure. Although Cantwell found that the lizards responded to all of the various bird stimuli at a similar level to white noise, she hypothesized that this resulted from hyper-vigilance in a contrived laboratory environment. She also reported that the lizards responded significantly more quickly to the American Kestrel and that they remained vigilant for twice as long in response to this sympatric predator than they did in response to the non-sympatric predators.
I caught my first anole talk at this year’s Joint Meeting of Ichthyologists and Herpetologists in Chattanooga, Tennessee. James Stroud presented the results of work with Ken Feeley on modeling the niche of the brown anole (Anolis sagrei). Using data acquired from GBIF, Stroud showed that the environmental conditions experienced by brown anoles in their introduced range are outside of the environmental conditions experienced by brown anoles on Cuba. Stroud discussed how these data from the invasive range of the brown anole might be used to develop a more accurate model of this species’ fundamental niche. This is a work in progress.
There is considerable variation in phallus morphology among the major groups of amniotes (phallus used herein to be inclusive of both the penis and clitoris). Just for starters, while most clades – including mammals, birds, turtles, and crocodilians – have a single midline phallus, squamates have paired hemiphalluses. Although herpetologists have long appreciated morphological variation in the hemipenis for its systematic value, understanding the nuances of anatomical homology, homoplasy, and novelty at this larger scale has not been as widely addressed. Recently, the Cohn lab of the University of Florida (of which I am now a member) undertook this challenge from a developmental perspective, studying development of external genitalia in representatives of each reptilian clade: the ball python (Python regius), the pond slider (Trachemys scripta), three duck species, the American alligator (Alligator mississippiensis), and who else, but the green anole (Anolis carolinensis). A synthetic review of the complete series will have to wait for another post, but reprints of each paper are available on the lab’s website to hold over the most curious. But because of the growing interest in anole nether regions, I will briefly highlight the recent findings regarding hemiphallus development in the green anole.
Fig. 2 of Gredler et al. illustrating the development of paired genital and cloacal swellings.
The Wade lab has previously shown that both male and female green anoles develop similar hemiphalluses during the early stages of genital morphogenesis, which then later differentiate into sex-specific reproductive structures. Building upon this observation, Gredler et al. described the embryology of the green anole hemiphallus from the earliest stages of morphogenesis through sexual differentiation. Hemiphallus development begins around the time of oviposition when three sets of paired swellings appear between the cloaca and the developing hindlimb bud, reminiscent of what is observed in other amniote clades. These swellings expand and meet at the midline to form the external lips of the cloaca or remain lateral to the cloaca and mature into the hemiphalluses. Following morphogenesis, the male hemipenis continues to elongate as it forms its distinctive lobes and sulcus spermaticus while the female hemiclitores gradually regress into the cloaca. Further details of the developmental anatomy of internal reproductive structures and gene expression patterns of several key molecules associated with genital morphogenesis are described in the paper.
Fig. 4 of Gredler et al. illustrating sexual differentiation of the hemiphalluses. Red arrow highlights the formation of the sulcus spermaticus.
Although there is some variation among squamates in the relative timing of the emergence and fusion of the paired swellings associated with hemiphallus development, these results are largely consistent with classical embryological descriptions of squamate genitalia (summarized by Raynaud and Pieu in Biology of the Reptila volume 15). But the revival of this body of literature in a comparative and molecular context brings new research questions to our collective table. As discussed by Gredler et al., the seemingly modular relationship between the genital swellings, cloaca, and limb buds may be particularly interesting in the context of repeated body elongation and limb loss among squamates. Better understanding of the relationship between cloacal and phallus development may also shed new light on the mechanisms of reproductive isolation, the coevolution of male and female reproductive organs, and evolving patterns of sexual conflict. Furthermore, there remain open many mechanistic questions regarding the molecular patterning of the hemiphalluses and which processes are hormone dependent that can now be more thoroughly addressed using the newly available sex-specific molecular markers. Considering the growing literature on hemipenis variation and expanding access to genomic resources in Anolis, these may be particularly fruitful areas for future investigation.