All’s well that ends well
A couple of days ago, we had a post about a poor anole frozen to death in wintry Texas. Today comes a report on Dust Tracks on the Web of another green anole incapacitated by unseasonable chill, but with a happier ending.
Male and female A. sagrei at the famous Soroa, Cuba locality.
Anole displays consist of conspicuous behaviors that are known to be used in multiple contexts, such as exhibiting territory ownership and territory defense, mate attraction and female receptivity, species recognition, and even predator deterrence. As most of you know, the display repertoire typically involves three major signal types: “dewlap extensions” (DE, pulsing of the throat fan or dewlap), “push-ups” (PU, up and down movement of the body and tail), and “head-nods” (HN, up and down movement of the head only). Although the visual display behavior in anoles has been extensively studied, the function of these three major signal types (DE, PU and HN) remains highly equivocal, and especially in the brown anole. Therefore, we decided to set up a behavioral experiment addressing DE, PU and HN signaling rates across diverse contexts, using the brown anole as study species.
Our study differed from previous ones in two main aspects. Whereas most other studies have focused on male signaling only, we looked to the three separate signal types in both male and female lizards. Secondly, our study is the first one to compare display rates across a wide range of contexts using the same individuals over again (repeated-measures design). This design could, however, only work under fully-controlled laboratory testing conditions. The diverse contexts we tested included predator, non-predator and several social interactions (i.e., mirror, male-male, male-female and female-male). For the predator and non-predator interactions, we used a living curly-tailed and equally-sized ocellated spiny-tailed lizard, respectively; the social context involved only conspecific interactions. Rather than examining display structure, we focused on the frequency with which each individual signal type was performed.
What did our results show? We found that brown anoles of both sexes exhibited higher display rates in the presence of conspecifics than when confronted with a predator or non-predator. DE, PU, and HN seem to be of main importance during brown anole social interactions, and thus not in predator deterrence. Whereas the females did not significantly raise display rates in response to a mirror or during intersexual interactions compared to a control situation, males did. The PU signal type only appears to play a major role for brown anole males during aggressive encounters. On the other hand, increased frequencies of all signal types during male-female interactions suggest that DE, PU, and HN are all essential for male courtship.
Staged intersexual interactions in the brown anole
Finally, we suggest that intersexual selection is probably a driving force for frequency-related dewlap use in both sexes (we found a very strong, but not significant, trend that females increased their DE frequency only during female-male interactions). In contrast, pronounced intersexual differences were detected for PU and HN rates within a social context. I would like to mention once more that all our behavioral experiments were conducted under controlled laboratory conditions and that caution is needed on the general interpretation of our findings.
To end, I would like to say that we did experience some difficulties in comparing our PU and HN results with results from previous studies on brown anole display behavior, due to an inconsistent terminology found in the literature. Authors have variously used the terms “nod,” “headnod,” “bob,” “headbob” and “pushup” to refer to the stereotyped bobbing display and it is not always clear which movements correspond exactly to which terms (e.g., only head movement, only front legs, whole body movement including/excluding tail). Partan et al. (2011) did a very nice job by discussing several bobbing display terms in her paper, but still we think there is need for a more consistent and defined “bobbing” terminology. In this way, pooling display datasets and comparing display results will become more efficient and accurate, which in turn may lead to better “anole science”!
Driessens, T., Vanhooydonck, B., Van Damme, R. 2014. Deterring predators, daunting opponents or drawing partners? Signaling rates across diverse contexts in the lizard Anolis sagrei. Behav Ecol Sociobiol 68:173–184.
This weekend I recently saw an adult male Cuban brown anole (Anolis sagrei) perching higher than I have ever observed – roughly 4m high!
Adult male Cuban brown anole (Anolis sagrei) perching uncharacteristically high
So anole aficionados, what dizzying heights have you observed trunk-ground anoles up to?
*My apologies for the poor quality of the zoomed in sections.
In species of Anolis where females have dewlaps, we know very little about exactly how females use their dewlaps. Losos (2009) describes this lamentable situation thus:
“Unfortunately, little is known about how females use their dewlaps, and the little information that is available from three species permits few generalities. Anolis carolinensis females only rarely use their dewlaps in intersexual displays (Jenssen et al., 2000), whereas female A. valencienni use their dewlaps primarily to discourage courting males, including those of other species (Hicks and Trivers, 1983). Both A. carolinensis and A. bahorucoensis females use their dewlaps in intrasexual displays (Orrell and Jenssen, 1998, 2003); in A carolinensis, females use the dewlap more at close range and less at long range in female-female interactions compared to dewlap use in male-male interactions (Jenssen et al., 2000; Orrell and Jenssen, 2003). Unfortunately, without more information on how females use their dewlaps, we will not be able to explain sexual dimorphism and dichromatism in anole dewlaps.”
Since then, Martha Muñoz has added an observation from A. armouri, but the numbers are still small.
Attempted forced copulation in Anolis cristatellus
In July 2013, I spent ten days observing A. cristatellus in Mayagüez, Puerto Rico, and can add one more species to the list of female anoles that use their dewlaps to dissuade males from mating with them. I was mapping male territories and counting male-male interactions in a park in one of Mayagüez’s fancier neighbourhoods, and came across a male chasing after a female. I sat down to watch the interaction, and was struck by how determined the female seemed to avoid mating with this male. You’ll notice how the male is biting the female much lower down the body than is normal during mating, indicating how the female is trying to get away. Her dewlap is completely extended during this interaction.
The chase went on for several minutes before the female ran to the end of a thin branch and another male showed up to chase the first male away. I proceeded to catch and mark this second male, and later observations revealed him to be the resident territory holder of the tree.
A little later, we caught a male in the tree adjacent to one in which the showdown occurred. In a fantastic stroke of luck that anyone whose work depends on identifying individual animals in the field will appreciate, we were able to determine that this male from the adjacent tree was in fact the first of the two males observed earlier.
How, you ask, did we perform this forensic wizardry? Observe the second tiny tail of the interloper attempting the forced copulation:
Caught red-handed!
I was showing these photos to Jonathan Losos the other day, and he immediately noted that the observation of a female using her dewlap was pretty rare. Of course, the obvious response was to write a blogpost about it, but then we realised that with Anole Annals‘ daily viewership of up to 1500, we could do more than just write a blogpost–we could do citizen science! So this, ladies and gentlemen, is an invitation to all of you to help build a dataset. It’s more than the usual request for participation and comments that I end many posts with–it’s a challenge to all of us AA readers to keep an eye and camera out for examples of females using their dewlaps, so that we can together figure out a pretty basic piece of Anolis biology.
We’ve done this sort of citizen science before, quite successfully: here’s Kristin Winchell’s call for data on urban anoles, and here’s the resultant analysis. And there’s all sorts of exciting natural history questions that would be impractical for individuals to tackle on their own, but that we can solve easily as a team. Let’s make this blog a citizen science hotspot!
Photo from http://www.frogtown.org/
For more than three decades, since the seminal work of Ray Huey, Al Bennett, and Steve Arnold, biologists have measured whole animal performance–how fast they run, how far they jump, how well they can swim–to understand how species are adapted to their environment. Work on anoles has been a prime example of how we can study differences among individuals and species to understand how natural selection works and why species living in different environments possess different morphologies (several AA posts have discussed this sort of work [e.g., 1, 2, 3]).
But a critical assumption of all of this research is that we can get animals to perform maximally. Otherwise, it’s tough to study what causes variation in maximal capabilities if animals aren’t performing maximally. The catch is: how do you tell if an animal is going all out? Sure, it’s easy to weed out the slackers, but distinguishing a lizard giving it his all from one going at, say, 90% of max…hard to tell.
In an important and entertaining paper, Henry Astley and colleagues provide some sobering information. The short story goes as follows, and you really should watch the video below for more details and some great images: biomechanicians have studied frog jumping for decades to understand how muscles work. Bullfrogs are known not to jump very well. The maximum jump ever recorded in the lab was only 1.3 m, whereas the much smaller Cuban treefrog can bound 1.7 m. The proffered explanation was that bullfrogs live on land and in the water, and so their morphology must be a compromise.
But…the Guinness Book of World Records claims that a bullfrog–Rosie the Ribeter, to be exact–once jumped 2.18 meters at the Calaveras County Fair. That’s 68% farther than any scientist had ever recorded in the lab. Sounds like a bunch of hooey, right? Well, just to debunk this nonsense, a bunch of Brown University biologists headed to sunny California to visit the County Fair, eat some cotton candy, and check out the frogs. And, lo and behold, it’s true–bullfrogs there regularly far exceed the lab record.
The story’s a lot more complicated–it turns out that there are “pro” frog jumpers–and I won’t go into the details; the paper is well worth a read, very entertaining and sobering for lab performance types (abstract here). But the short story is this: it seems that lab studies had massively underestimated how far bullfrogs can jump, calling into question many of the conclusions that had been reached about their physiology. Moreover, records for the maximum jump distance at the fair showed a steady increase for the first 50 years before levelling off for the last 30. This suggests that the people who jump the frogs (and some families have been doing this for generations) have only gradually learned exactly what conditions and behaviors maximally stimulate the frogs. And this suggests that lab scientists, who just guess at what may work best and tinker a little bit, may not have much of a chance of hitting on the right stimuli.
There’s been lots of great press coverage, too–just google “calaveras frog astley” or something like that. But, first, watch the video and go read the paper (I can email you a copy if you can’t access it online).
httpv://www.youtube.com/watch?v=QKFpvoez7_M
Two days ago, the Boston Globe had an article online,
Winter storm causes havoc in US South
“A winter storm that hit the southern United States yesterday all but paralyzed the city of Atlanta, stranding people in cars at stores and children at their schools. The storm only brought a few inches across the region but with the ice caused major problems in America’s southern region.”
Accompanying the article were 28 photos. The one above was #22, with the following caption: “Snow covers a dead lizard in Springville, Ala., on Jan. 28. (Mark Almond/Associated Press)”
CTmax, Tb, and CTmin of cybotoid anoles & env. temperature. Modified from Fig 2 in Muñoz et al.
AA contributor Martha Muñoz’s work on altitudinal variation in the cybotoid anoles has already netted her the Raymond B. Huey award and of course, been featured on AA. A big chunk of this work, co-first authored with Maureen Stimola, has just been published by the Proceedings of the Royal Society B. If you haven’t read it yet, check it out.
I love this paper. However, in the spirit of full disclosure, I’m completely biased as I happen of be one of the co-authors. But I’m sure I’d love it anyway. Why? In part because it tests a clear hypothesis using multiple lines of evidence and eliminates confounding explanations – characteristics every paper should have. It also has cool (or should I say hot?) results. However, more than this, I think this paper demonstrates the power of combining good ole’ fashioned (yet cutting edge) field work with macroecological and macroevolutionary models, demonstrating how these different approaches can really complement each other.
What did Muñoz and company find? Briefly, they looked at hot and cold tolerance (CTmax and CTmin) of six species of cybotoid anoles on Hispaniola, in relation to elevation. They found far more variation in CTmin than CTmax across species (and populations). By bringing in a little macroecology, they showed that CTmax isn’t correlated with environmental temperature, but CTmin is, i.e. when the going gets cold, the anoles get colder – sort of. The catch is that while CTmin strongly tracks temperature, daytime body temperature does not. This is a neat result in and of itself and fits well with a big, recent, data-mining paper showing similar trends across hundreds of both ecto- and endothermic species. But while it doesn’t have the breadth of that paper, Muñoz et al. were able to go further. Firstly, bringing in a little macroevolutionary analysis, they showed that yes, CTmin has actually evolved significantly faster than CTmax. Neat, but at this point you should be asking yourself, “What about acclimatization?” and “Is this just plasticity?” Muñoz et al. asked the same thing and headed back to the field. A lot of work later and the answer was no. An acclimation experiment rejected this possibility.
At this stage, most macroecological and macroevolutionary analyses would have to stop at the identification of a clear, and intriguing pattern of fast past evolution of cold tolerance along an elevation gradient, but little CTmax evolution. The Discussion of such a paper would suggest potential hypotheses to explain the pattern and that would be that. But Muñoz et al. again went further and, by working in the field to measure perch use and operative temperatures, worked out why . The key result showed that lizards can behaviourally thermoregulate to escape the heat, thus reducing selection on heat tolerance, i.e. the Bogert effect. However, the nighttime cold cannot be escaped (actually, it can, by moving to England where it hasn’t dipped below -2 deg C this winter. Enjoy that polar vortex America!), leading to selection on cold tolerance.
Like I said, very cool results and a real testament to the power of using field experiments and macroevolutionary models to inform each other and go beyond what each approach could do in isolation. So please read it, challenge it, and build on it.
Here’s a picture of an Anolis cristatellus I recently found in Miami (FL) with a strangely coloured dewlap (next to a more typical dewlap colour and pattern). I have no extra details other than I found one other individual that was similar close by, although with less grey. I have never seen it on any other cristatellus in the area. So strange I thought I would share!
Left: Atypical dewlap, Right: Typical dewlap
Although I intended to post this just because of my natural curiosity, it also gave me the added bonus of being able to annoy WordPress’s US-English spellcheck with my title!
Until now, Anolis omiltemanus was the only Mexican anole restricted to pine forests. However, in a new paper in Zootaxa, Gunther Köhler and colleagues have described a new species, A. peucephilis, from the southern Sierra Madre del Sur in southern Oaxaca, nearly 300 km from A. omiltemanus. The new species differs morphologically in a number of respects, most notably in its extremely short legs. It is also is divergent in mitochondrial DNA. All specimens were collected at night in pine trees at heights ranging from 2-10 meters. No specimens could be located during the day, suggesting that they are very cryptic, a common trait with short-legged anoles.
Wondering what the name means? Here’s what the paper says in its etymology section: “The name peucephilus is a compound adjective derived from peuke (Greek for pine) and philios (Greek for loving) referring to the obvious habitat preference of this species.”
Kindle readers, could you please check this out? The non-anole on the cover is not a promising start!