On August 3rd 1977, a bulbul was observed chasing a large (ca. 20 cm in length) chamelion (Anolis sp.) in a circular pattern down an octopus tree; it was unsuccessful in capturing the reptile.
Such a vivid image, one that’s noteworthy for two reasons. First, while data on successful predation events are rare, descriptions of failed predation attempts are even rarer. As bulbuls are mostly frugivorous, it isn’t too surprising that this lizard got away.
If the biology of Anolis lizards is a puzzle, then a new paper by Yoel Stuart, Todd Campbell and colleagues is a crucial piece. It’s a puzzle piece that not only contains a wealth of information when held up on its own, but also brings clarity to a broader picture of anole biology when fitted into place.
Anolis carolinensis on small spoil-islands in Florida are the subject of Stuart et al. (2014)
A tight relationship between microhabitat and morphology characterizes variation across Anolis speciesin the Caribbean. Anole biologists have long suspected that negative interactions, such as competition, are responsible for driving different species into different microhabitats, with subsequent morphological adaptation to these microhabitats over evolutionary time. But pinning down interspecific interactions as the cause of evolutionary divergence in microhabitat and morphology has been difficult.
Whyis establishing this causality challenging? Upon observing a pattern of consistent differences between populations of a species that occur in sympatry and allopatry with an interacting species, it seems logical to attribute this pattern to the presence of the interacting species. But many processes other than an evolutionary response to negative interspecific interactions can generate such a pattern–environments may differ between sympatric and allopatric populations in a way that drives the observed divergence, individuals from sympatric populations may all be similar only because they are closely related to each other, the divergence may be a consequence of phenotypic plasticity, or most dishearteningly, the whole pattern may simply be due to chance.
Ruling out these alternatives seems a gargantuan undertaking. Indeed, as Stuart and Losos (2013) point out, in a review that serves as a nice companion piece to this study, only a small fraction of studies describing patterns of divergence between sympatric and allopatric populations tackle the problem of eliminating these alternatives and can thus conclude with confidence that interspecific interactions cause the divergence they observe. But Stuart et al. (2014) take on the challenge.
Like recent research by Helmus et al. (2014) that exploits human-mediated anole dispersal to test classic principles of island biogeography, Stuart et al.’s (2014) research is rooted firmly in the Anthropocene. Occupying centrestage is the interaction between Anolis carolinensis, native to the United States, and Anolis sagrei, a relatively recent invader. The stage itself comprises small man-made spoil islands in Florida, created in the 1950s. When Todd Campbell began this study in the 1990s, A. carolinensis occurred on many of these little islands. Campbell introduced A. sagrei to three islands, and watched how, over the next three years, A. sagrei numbers rose steadily and A. carolinensis shifted higher into the trees on invaded islands, while continuing to perch at lower heights on nearby un-invaded islands.
Lead authors Yoel Stuart and Todd Campbell boating between spoil islands in FL
This rapid shift in microhabitat spurred Stuart and Campbell to return to the islands 15 years later (with a team of field assistants, of whom I was one!) to ask if A. carolinensis on invaded islands had subsequently diverged morphologically from conspecifics on un-invaded islands. By this time, A. sagrei had spread widely. Nevertheless, they found five un-invaded islands. A. carolinensis still perched lower on these un-invaded islands than on nearby invaded islands.
Across Caribbean anoles, species perching higher up on trees have larger toepads and more lamellae on these toepads than do species perching closer to the ground. Recapitulating this interspecific difference, Stuart et al. (2014) found that A. carolinensis on invaded islands had evolved larger toepads and more lamellae than lizards on un-invaded islands in about 20 generations, rapidly establishing a pattern of character displacement. But is this pattern caused by the presence of A. sagrei?
It seems almost criminal to squish into one paragraph everything that Stuart et al. (2014) did to rule out alternative explanations for the pattern of divergence. They reared hatchlings from invaded and un-invaded islands to rule out phenotypic plasticity as a cause for divergence, sequenced a mind-bogglingly large number of SNP loci to establish that A. carolinensis on invaded islands were not closely related to each other, and conducted intensive habitat surveys to rule out environmental differences between invaded and un-invaded islands. This mountain of work supports the idea that the presence of A. sagrei has driven the evolutionary divergence among sympatric and allopatric populations of A. carolinensis. It’s this mountain of work that makes Stuart et al. (2014) a tremendously satisfying paper. We now have a much firmer basis from which to suggest that interspecific interactions have driven patterns of ecomorphological diversification across Caribbean anoles.
But I personally think that this study’s most exciting implications arise from it defining more clearly a part of the anole biology puzzle that still remains relatively empty, namely our understanding of within-population, among-individual variation in microhabitat use and morphology, and the consequences of this variation for behavioural interactions. This summer I came across an A. carolinensis and A. sagrei perched together thus:
A. carolinensis perched below A. sagrei on the University of Florida campus in Gainesville.
These particular lizards couldn’t care less for Stuart et al.’s (2014) findings–clearly, the effect demonstrated in this study is a population-level effect. But this leaves us with a gap between behavioural interactions and eco-evolutionary dynamics–how exactly do we transition from individual A. carolinensis that are content to perch below A. sagrei to a population-level shift in A. carolinensis perch height in the presence of A. sagrei? Reassuringly, the divergence that Stuart et al. (2014) document is so rapid that this question becomes tractable–their results emphasize an opportunity to integrate behavioural timescale with eco-evolutionary timescales. We can now examine individual interspecific behavioural interactions among anoles, safe in the knowledge that ecological and evolutionary responses are not far behind.
Editor’s Note (October 28, 2014): Yoel Stuart provides the first perspon perspective on the study on eco-evolutionary dynamics
A few months ago, I shared with you some of the odder morphological variations my field assistants and I encountered while measuring Anolis sagrei in Gainesville, FL. We went on to measure quite a few more lizards, and saw quite a few more oddities, as well as some fairly gruesome injuries. Here are some of my favourite examples:
1. A far better picture of a doubly-regenerated tail.
2. A jaw injury that resulted in the left and right sides of the jaws being dissociated from each other.
3. A cut hyoid. I imagine this lizard was no longer able to extend his dewlap.
4. A nasty head injury. We saw this lizard three or four more times after we measured him, and his wound seemed to have healed up completely.
5. A brutal leg injury.
6. A male with not only an impressive tail crest but also some nice red tail coloration.
I’m a big believer in the utility of watching animals in their natural environment, and it’s therefore no surprise that one of my favourite talks at the Animal Behaviour Society 2014 meeting was based on many, many hours of painstaking observation of Uromastyx ornata lizards in the rocky, arid cliffs of the Eilat Mountains in Israel. Amos Bouskila of Ben Gurion University presented an exciting outcome of this tremendous observation effort—a novel social behaviour in the Ornate Spiny Tailed Lizard, a large agamid that ranges from Egypt to Saudi Arabia. Here’s a video of this behaviour (starts at roughly 0:55) for National Geographic, filmed by Eyal Bartov.
This novel behaviour comprises an interaction between a male and a female, and includes the following steps:
1. The female flips over onto her back (or is pushed onto her back by the male, as in the video above).
2. The male walks over the female’s body a few times
3. The female rights herself and moves away.
The sequence of events can be initiated by either the male or the female (though it’s predominantly female initiated), occurs both before and after copulation, and continues to occur well into the nesting season. Bouskila therefore rejects the notion that the behaviour is related to copulation, and speculates that it instead relates to chemical signalling (males have enlarged femoral pores in this species) and that it functions to maintain pair bonds between these long-lived lizards. Further observation will tell if this exciting hypothesis holds true!
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.
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.
August 2014 is a good month for behavioural biologists in North America: at the start of the month, the International Society for Behavioral Ecology and the Animal Behavior Society are holding conferences in quick succession in New York City and Princeton respectively. However, Anolis lizards are pitifully underrepresented at these meetings: of the hundreds of talks at these two meetings, a total of zero–yes, zero–are about anoles. This is a tad surprising–plenty of people study the behaviour of anoles, and I was expecting some presentations at these meetings. I’ll be at ABS talking about Sitana, and would love to meet other anole behaviour enthusiasts, so please let me know in the comments below if you’ll be there.
That said, lizards aren’t too badly represented at these meetings: there will be talks or posters on Draco, Psammophilus, Phrynocephalus, Sceloporus, Crotaphytus, Podarcis and Tupinambis.I’ll be blogging about the lizard presentations from ABS, so stay tuned for a behavioural bonanza!
The wonderful Phrynocephalus mystaceus. Photo by Antoshin Konstantin from Wikimedia.
I’m doing fieldwork with Anolis sagrei in Gainesville, FL, this summer. We now have about 125 lizards measured and marked, and have come across a number of interesting morphological oddities in these lizards. Most interesting so far is this doubly regenerated tail, i.e. there appear to be two spots at which the tail has regenerated, which means a regenerated tail must have broken and regenerated again.
A doubly regenerated tail in a male Anolis sagrei in Gainesville, FL.
Approximately three minutes before we noticed this tail, my field assistant Christian Perez asked me if double regenerations were possible, and I confidently said “no.” As Jonathan Losos puts it in Lizards in an Evolutionary Tree, “when a tail regenerates, the new portion of is made of a rod of cartilage and thus lacks the intravertebral breakage planes that enable an unregenerated tail to autotomize.” So how did this double regeneration happen? Anyone seen this before?
The next oddity is this male with a mysteriously shortened upper jaw:
A shortened upper jaw in a male Anolis sagrei in Gainesville, FL.
Third, we have a partially discoloured dewlap:
A discoloured dewlap in Gainesville, FL
And finally, here’s an addition to our collection (1, 2) of multiply tailed lizards:
A double tail in an Anolis sagrei in Gainesville, FL.
If you’re in the field looking for lizards, knowing where they sleep can be tremendously useful. Anyone who’s tried catching an anole at night knows how much easier this can be than catching it during the day. When I began working with Sitana, therefore, I was keen to locate where these lizards slept. Being primarily terrestrial, it made sense that they would sleep under rocks, in cracks in the ground, or buried beneath grass, bushes, or leaf litter. I had some indirect evidence for the utilization of these locations as sleeping sites–I had seen lizards emerging from and retreating to these locations early in the morning and late in the evening, respectively.
However, I did not expect that fan-throated lizards would sleep completely in the open on the ground. Yet that is precisely what my colleague Divyaraj Shah recently observed. You can see the lizard’s head pointing downwards, resting on the ground below–he does not seem disturbed at this point.
Is it common for terrestrial lizards to sleep in open, unsheltered spots?
