[June 12 2012; 8:35 a.m.]. During a placid morning, a team from Herbios Group Panama observed an impressive image. We witnessed an Oxybelis aeneus (147 cm, 55 g) with an Anolis lionotus male (22.9 g) caught in her jaws. He was the breakfast meanwhile, his fellow female just observed the scene.
We were so happy to witness such an event, thinking about what was the male doing while the predator took the chance. Perhaps He was displaying to attract the cryptic female, or just was distracted while feeding! In any case the snake had the morning meal and the male paid the price.
Avid readers of this blog might have noticed that Jonathan Losos likes trying to get readers to confuse the white-fanned variant of the South Asian agamid lizard Sitana ponticeriana with the only toepad-less anole, Anolis onca. Indeed, the two lizards look quite similar:
Sitana ponticeriana, white-fanned variant, in Saswad, India
Anolis onca in Maracaibo, Venezuela. Photo by Jonathan Losos
Posts [1, 2, 3] detailing the habits and habitats of these two lizards point to a number of similarities between the species. Both occur in incredibly hot and windy environments. Both are primarily terrestrial, where they are very well-camouflaged, but are also observed perching on vegetation. The causes for the loss of A. onca’s toepads remain a mystery, and here I lay out some observations of S. ponticeriana’s behaviour that lead to a hypothesis for why A. onca might have lost it’s toepads.
Perch use in S. ponticeriana follows a predictable temporal pattern from about 8:00 a.m., when the lizards first emerge, to about 12:00 noon, the hottest part of the morning. Lizards perch primarily on rocks, if available, in the early morning while basking. During the middle of the morning, male lizards are found perching on and displaying from a variety of perches, including the ground, mud piles, rocks, twigs, and shrubs. By noon, however, lizards are often found resting in shrubs. Here are a couple of lizards resting:
Male Sitana ponticeriana, white-fanned variant, resting in the shrubs. Saswad, India.
Female Sitana ponticeriana, white-fanned variant, resting in the shrubs. Kutch, India.
But what happens when you chase lizards out of the shrubs in the heat of the day? Peak air temperatures at the site I was at this summer hovered around 40 degrees Celsius, and soil or rock surface temperatures were likely higher (they certainly felt so). Lizards that we chased out of shrubs onto the sand would run rapidly as usual, but when they paused, were often observed lifting the toes of their hind feet off the ground. Here are two photos–compare the toe positions on the hind foot to get a sense of the behaviour I’m referring to:
If the highest risk of heat exposure comes from the ground, any adaptation that reduces the transfer of heat from the ground to the lizard will be favoured. Such adaptation would explain S. ponticeriana’s behaviour of resting in vegetation during the hottest part of the day and lifting toes off the ground when forced onto hot terrestrial perches. Like most agamids, Sitana have very skinny toes, leaving a small surface area for transfer of heat from the ground. But what about A. onca? If the ancestral A. onca had typically anole-like toepads on moving to the beaches, they might have been at high risk of heat transfer from the sand when forced onto terrestrial perches in the heat of the day. This would lead to the evolution of reduced toepads to avoid such heat transfer. A temporal pattern of perch use in A. onca, similar to that of S. ponticeriana, would be the first piece of evidence useful for establishing what might be an exciting example of trans-continental convergence.
I was communicating recently with an eminent Gondwanan herpetologist, one who has published far and wide on many issues pertaining to many species. I remarked that it was time that he/she reached the pinnacle and worked on anoles. I received this response:
“To my mind, an anole is a little like a bicycle with training wheels – quite useful for youngsters to practice on and develop their skills. But just a pale shadow of the subtlety and sophistication of real lizards. They just make it too easy to get lots of papers in good journals, and discover neat things. Where’s the challenge?”
If I were a brown anole, I’d take offense at a flag like this, too!
Pat Shipman from the AA Little Cayman Bureau checks in:
The observation that anoles nod at inanimate objects (or possibly at anoles the observer hasn’t spotted) is not new.
A few days ago, I watched an adult male sagrei repeatedly unfurling his dewlap and displaying… at an orange landscaping flag that marks the location of a large septic pipe underground. What was most interesting is that the flag was fluttering in the breeze and that it was a shade of orange almost exactly the same as the sagrei’s dewlap. Alas, I did not have a camera handy to record this event.
Has anyone else noticed sagreis paying special attention to orange objects?
According to Williams and Rivero, the name occultus was chosen for the anole they described in 1965 because it means “hidden,” referring to the unexpected finding of a new species in such a well-trodden spot (“The discovery of so distinct a species in an island thought to be well known herpetologically and in which the anoles have received special attention must give us pause.”). But to the unknowledgeable, “occultus” sounds more mysterious, more preternatural, befitting such a spectral, gnome-like species that is so rarely seen and so little known.
On a recent trip to western Puerto Rico, I was fortunate to visit a locality where they can be found readily at night. In a short evening, we found five clinging to the ends of twigs (as well as a dozen green giants). Naively, I thought that I’d come back during the day and locate some to see where they live when they’re active, and what they do. Ha! Much, much easier said than done. How do you find a little, camouflaged gray match-stick of a lizard in the dense vegetational matrix that is a tropical forest? The answer: you don’t, and I didn’t.
I’m thirsty! Photo by J. Losos. For more on drinking occultus, check out Manuel Leal’s recent post on Chipojolab.
Indeed, there are almost no data on the natural history of this species, except where it sleeps. The little that we do know suggests that they are just what they look like–twig anoles. Some of the few that have been found have been on twigs, though a surprising several have been on leaves or ferns. They seem to creep slowly, though no one has published a good behavioral description.
Photo by J. Losos
Since the description of this species in 1965, there has only been one paper written on the diurnal natural history of this species, published by Preston Webster in 1969–44 years ago (go ahead, read it yourself)! Someone needs to go out and find these guys and see what they do! How to do it? Go find them at night and come back before dawn and watch them as they wake up and get out of bed. And here’s a bonus–George Gorman published a paper suggesting they sleep in pairs–that’s right, pair-bonding twig anoles!
Note that these photos were taken of animals captured and placed on twigs, as was the lizard which subsequently started drinking raindrops discussed on Chipojolab.
And here’s one acting like a real twig anole. Photo by J. Losos.
Up high displaying green anole. Photo from this website, which has some nice other reptile shots.
Many animals use different parts of their habitat for different activities–eating in one place, mating in another, and so on. This hasn’t been studied in many anoles, but has been documented in several. In addition, many species alter their habitat use in the presence of competitors, and this has been widely demonstrated in anoles. However, few have studied the interaction of the two phenomena: is the extent of behavioral partitioning among habitats affected by the presence of competitors?
To address this question, Ambika Kamath and colleagues studied green anoles on several islands in Mosquito Lagoon in the Intracoastal Waterway of Florida. In this area, a number of small “spoil” islands were created when the waterway was dredged half a century ago. These islands were quickly colonized by plants–and now are covered with very large trees–and then by green anoles. More recently, the invasive brown anoles have arrived on the scene on some of the islands.
Kamath et al., whose research was recently published in a paper in Breviora, chose four islands, two with brown anoles, two without (freely available, as are all MCZ publications, on the museum’s website). On these islands, they recorded habitat use and behavior. As predicted animals forage at lower heights than where they perch. One possible explanation is that they sit at vantage points looking for prey, then go down and catch them. And as predicted, males display at particularly high spots. The explanation here is not clear, but as reported recently for A. cuvieri, males seem to like to display higher than their rivals. Finally, once more as predicted, in the presence of brown anoles, green anoles shift upwards in all respects.
The interesting finding, however, is that the shift is essentially parallel for all activities. Animals move downward the same amount to capture prey and upward the same amount to display. This would suggest that there is not an optimal height for feeding or displaying, or perhaps that the optimal height changes in the presence of brown anoles. That would be readily understandable with regard to feeding–the voracious brown anoles probably vacuum up the low-lying food, so no point in dropping down as low to feed as in their absence. Why males continue to move up even higher is less obvious, though it may be just that competitors are now perching higher, so a male has to go higher yet to display above them.
This paper represents the sort of detailed behavioral study that is all too infrequent for anoles. How these lizards modulate their behavior in response to conditions is fascinating and often surprising. Much remains to be learned, and most anole species–well, at least in the Caribbean–are amenable to behavioral observation.
Ok, this post has nothing to do with Frank Sinatra other than his nickname. But what about blue eyes in anoles? They seem to pop up all over anole phylogeny. For example, in my recent trip to Puerto Rico, three anoles had cerulean peepers–A. evermanni and A. stratulus, which are closely related, and A. gundlachi, which is more phylogenetically distant. And blue eyes occur in other anoles, such as A. etheridgei from Hispaniola.
The observation raises two questions:
1) Just how phylogenetically widespread is the occurrence of blue eyes in anoles? I know I’ve noted blue-eyedness from time to time, but I haven’t get tracked and can’t remember in which species. I propose the Anole Annals community take it upon itself to compile a list of blue-eyed anoles. If you know of one, please post a comment and, even better, add a photo.
2) Why? I can’t believe there is an adaptive significance to having blue eyes per se. Is it genetically linked to some other adaptive trait? Could sexual selection have a role (though I don’t know of sexual dichromatism in eye color)? Other animals exhibit interspecific variation in eye color and I bet there’s a literature trying to explain it, but I’m not familiar with it. Would make an interesting project!
Some quick googling reminded me of a few other examples, below. Who am I missing? And does anyone have a good photo of blue-eyed etheridgei?
Rick Stanley photo #2 of a large Costa Rican anole
Award-winning nature photographer, naturalist, and undergraduate Rick Stanley spied this large anole in Costa Rica. Is it A. microtus? A.insignis? Something else?
Photo #1
Here’s what Rick had to say: “I encountered these impressive lizards on the Pacific Slope of the Cordillera Talamanca, on the border of Chirripo National Park, in the summer (wet season). They were between 1500 and 1600m elevation, in secondary forest habitat. Although sightings were about a month apart, all of the animals observed were in the same general area near the cabins.
Photo #3
Images 2/3 are of the same individual. Image 1 was taken nearby at an earlier date, so it could be the same individual as well. Image 4 is of a different, slightly smaller individual seen along with 2/3 (perhaps the female?). The male(?) displayed his dewlap at me- I think it was an aggressive gesture, because the female was out of sight by then. When I first saw him, he had a large clump of moss in his mouth that he proceeded to devour (chances are there was an insect in there as well).
Photo #4
The lizards were over a foot long including the tail, although I didn’t catch them and measure svl. The first time I sighted 1 it was sunning. Later, it changed color and appeared more like the individual in photos 2 and 3. Didn’t move much, as I found him in the same place the next day, hanging head down on some vines.
There is also some damage to the animal’s dewlap that isn’t part of the pattern.”
‘Sibling species’, an old term that has fallen out of use, refers to closely related species that are so similar that it is hard to tell them apart. The existence of such species raises the obvious question: How do the animals themselves tell one another apart? And indeed, this is an active area of research (Tibbetts & Dale 2007; Uy et al. 2009). Usually, the species differ in one or more traits (i.e. species recognition signals) detectable with the sensory modalities upon which they rely (e.g. raptors use visual signals, frogs use sound and electric fish use different patterns of electric discharge).
A more general question concerns how such differences evolve. Over the last decade, it has become increasingly evident that mating signals can evolve under simultaneous selection for two functions (Fleishman et al. 2009): (i) eliciting attention (i.e. detectability); and (ii) species identification (i.e. distinguishing conspecifics from non-conspecifics). Historically, species recognition has attracted a significant amount of research from evolutionary biologists based on the assumption that if hybrids suffer reduced fitness or cannot be produced at all, then natural selection should favour individuals bearing traits that prevent such matings. This idea—confusingly termed either reinforcement or reproductive character displacement—had a rocky time in the evolutionary literature for many years, though now it is widely accepted (Servedio & Noor 2003; Rundle and Nosil, 2005; Pfennig & Pfennig 2009).
Near the dawn of the era of molecular ecology, one of the first studies to employ molecular tools to study the evolution of species recognition signals was Webster & Burns’ (1973) study of the evolution of dewlap colour in Anolis lizards. Anoles possess a retractable flap of skin under the throat, termed as dewlap, that is used in courtship, aggressive interactions and even encounters with predators (reviewed in Losos 2009). Anoles can be found in communities of as many as 15 species, and sympatric species never have identical dewlaps, leading to the hypothesis that the dewlap is used in species identification (Rand & Williams 1970).
Webster and Burns studied a highly unusual pattern of dewlap distribution in the Hispaniolan bark anole, Anolis brevirostris, along a transect on the western coast of Haiti (Fig. 1, above). Starting in the south, the lizards have a white dewlap. Then, abruptly the dewlaps become intensely orange; moving northwards, the intensity and size of the orange spot diminishes until it has almost disappeared, whereupon again there is an abrupt transition back to intense orange coloration that characterizes the northernmost populations.
Using the tools of the day, Webster and Burns employed starch-gel electrophoresis to examine six geographically varying protein loci. Analysis of these data yielded three important discoveries. First, the populations sorted into three groups: the white-dewlapped forms in the south, the orange-dewlapped forms in the north and a third, intervening form that exhibited clinal variation in the proportion of white vs. orange in the dewlap. Second, at the point of contact between the groups in both the north and the south, adjacent populations did not share alleles at several loci. Third, within the middle, clinally varying group, populationsshowed little genetic differentiation despite the differences in dewlap colour among populations.
Webster and Burns concluded that they were dealing not with a single species, but three—subsequently, the middle populations were described as A. caudalis and the northern ones as A. websteri. More importantly, what had seemingly been an incoherent pattern of geographic variation in dewlap colour variation now had a clear explanation. The apposition of orange vs. white at both ends of A. caudalis’s range is most parsimoniously explained as the result of selection for differences in species recognition signals in sympatry. The fact that A. caudalis maintains the clinal variation in the face of possibly strong ongoing gene flow, as evidenced by the lack of genetic differentiation among populations, was interpreted as powerful evidence for ongoing natural selection favouring dewlap colour differences at the contact zones with the other species.
Given this provocative pattern and the great interest in evolutionary reinforcement, it is surprising that this example has not been subject to further investigation as molecular tools have developed over the past four decades. Undoubtedly, the transect’s occurrence in Haiti, a notoriously difficult place for fieldwork, has been a factor. Finally, however, this case study has come under further scrutiny.
On a trip in Haiti that was no doubt a story in itself, Lambert et al. revisited Webster and Burns’ transect and report in this issue of Molecular Ecology the results of their phylogenetic and phenotypic analyses. Examining variation at mitochondrial and nuclear loci, Lambert et al. have demonstrated that Webster and Burns pretty much got it exactly right. Chalk one up for old school electrophoresis! Not only do the three species each fall out as monophyletic, but, as with the allozymes, A. caudalis exhibits little interpopulation genetic differentiation, in contrast to the deep genetic structure apparent among populations in the other two species. Moreover, phenotypic examination of dewlap coloration reaffirmed the patterns of clinal variation within A. caudalis and the abrupt shifts in coloration between sympatric species at either end of its range (Fig. 2).
Lambert et al.’s study not only completely corroborates Webster and Burns’ conclusions, but adds several important new perspectives on this case study.
Ray Huey giving the first talk of the symposium, illustrating that present day temperatures are more suitable for A. cristatellus than A. gundlachi at the El Verde Field Station (the red circles show average temperature through the day now; the gray circles are for corresponding temperatures 40 years ago).
This is part II of my report on the the symposium “The Biological Impacts of Tropical Climate Warming for Ectothermic Animals,” which was recently (Aug. 1-3) held in San Juan Puerto. Previously I discussed several of the talks that focused on anoles; today I summarize the rest of the symposium (the program is listed here).
Symposium co-organizer Ray Huey kicked off the symposium with opening remarks, including some important background. The symposium was funded as part of a grant headlined by Huey to investigate the effect of global warming on Puerto Rican reptiles. Huey joined forces with Paul Hertz, George Gorman, and Brad Lister, all of whom had studied Puerto Rican anoles in the 1960’s and 70’s. The goal of the proposal was to revisit their study sites to see how things had changed in the intervening time, as the climate had warmed, including as much as 2 degree C at the El Verde Field Station. A particular species of focal interest was the forest interior montane anole, A. gundlachi. This species is adapted to low temperatures, whereas its close relative, A. cristatellus, thrives at warmer temperatures. Huey and colleagues speculated that as the forest warmed, it would become more suitable for cristatellus and less for gundlachi, resulting in a forest invasion by the former and the disappearance by gundlachi from lower elevation forests.
Imagine their surprise, then, when they found not only that cristatellus had made no inroads into the forest at El Verde, but that gundlachi, previously found only at higher elevations, could now be found at sea-level! Exactly the opposite of what had been predicted–what a conundrum!
Noted forest science Ariel Lugo explained this result clearly in the next talk. It turns out that Puerto Rico has experienced massive reforestation in the last 50 years. Consequently, even if the world is getting warmer, it is also getting more tree-covered, at least in Puerto Rico, and this latter effect has had a greater impact on gundlachi’s distribution, allowing it to occupy newly re-emerged forests at lower temperatures. An important lesson that warming is not the only thing going on in the world today and that we must consider other factors as well.
Barry Sinervo showing the grim news for lizard populations worldwide
Much of the rest of the day was pretty gloomy, with projections of massive ectotherm disappearance in the tropics as global temperatures rise (turtles, as well as lizards, as Barry Sinervo showed), the reason being that tropical species are often closer to their upper thermal limits, and so relatively small increases in temperature may push them over the edge. Michael Kearney’s talk was particularly notable in taking an extremely detailed mechanistic analysis of how increased temperatures affect all aspects of ectotherm biology through their entire life cycle. Such studies, though very elaborate, promise particularly rich insight into the specifics of how changing temperatures will affect ectotherms. One finding of particular interest is that the amount of shade available in a habitat will be critical: more shade = good; less shade = bad. In many cases, Kearney argued, it is not the warming per se, but the effect on vegetative cover that may be most significant in effecting species like lizards.
All of the talks were fascinating and I can’t discuss them all: a few particular points stick in my head: Mike Kaspari showing that the boundary layer of air around a surface is particularly important for small animals such as ants, that may experience temperatures as much as 10 degrees C higher than the air temperature a few centimers above the surface; symposium co-organizer Patricia Burrowes showing that changes in seasonality are extremely important, particularly with regard to host-pathogen dynamics; Carlos Navas discussing the relative importance of temperature and water availability for amphibians; Ana Carnival examining geographic patterns of genetic variation to understand responses to climate change in the past; and Brad Lister showing that anoles and almost everything else at his study site in the Luquillo Mountains have declined greatly in abundance in the last 40 years.
Have this many anole biologists ever been in the field together previously? And who are they? This photo was taken at the El Verde Field Station, site of James Stroud’s observations on rock-using canopy anoles.
[June 12 2012; 8:35 a.m.]. During a placid morning, a team from Herbios Group Panama observed an impressive image. We witnessed an Oxybelis aeneus (147 cm, 55 g) with an Anolis lionotus male (22.9 g) caught in her jaws. He was the breakfast meanwhile, his fellow female just observed the scene.
