Can Lizards Adapt to a Warming World? An Experimental Study Demonstrates Natural Selection for Performance at Warmer Temperatures

Anolis sagrei in the Bahamas. Photo by Christian Cox from the Washington Post

In these times of rapidly changing climates, a major question is whether species will be able to survive. Essentially, they have two options: either shift their geographic ranges to stay within their ancestral niches, or adapt to new circumstances. Or, of course, go extinct. In recent years, evolutionary biologists have come to realize that evolutionary change can occur very rapidly when selective pressures are strong. The question is whether it can occur rapidly enough to accommodate quickly changing environments.

A recent study suggested that many tropical lizards are imperiled by a warming world. This study suggested that lizard populations would not be able to adapt rapidly to warmer conditions, but the analysis wasn’t very detailed.

First author Mike Logan hard at work at the field site. Photo reprinted from the Washington Post

In a study that is the first of its kind, Mike Logan and colleagues at Dartmouth have investigated the selective forces that may impinge on lizards as the world warms. The study was conducted on the old workhouse, the brown anole, Anolis sagrei. In essence, what the researchers did was calculate the extent to which sprinting capability was affected by temperature in two populations, one in an area in the Bahamas currently occupied by the anoles, and another in a population transplanted to a warmer era that served as a surrogate for conditions that will be experienced under global warming.

The study was gargantuan in its scope. Each lizard was put through its paces a number of times at each of a number of temperatures. From these data, the researchers could establish the temperature at which each lizard ran fastest and the breadth of temperatures at which they ran reasonably fast (compared to their maximum), which is termed performance breadth. They then marked the animals and returned them to their habitats. They then returned three months later to recapture the lizards to see which had survived and which hadn’t, allowing them to see whether their sprint capability measures were acted upon by natural selection.

It turns out that a fair amount of variation exists in the lizards in terms of both optimal temperature and performance breadth. In the natural habitat in Georgetown, Great Exuma, Bahamas, there was no evidence of selection operating on any of their measures.

The transplant experiment was conducted a year later on the Bahamian island of Eleuthera, which is not all that far from Great Exuma. In this case, the thermal characteristics of the habitat from which lizards were taken were very similar to the study site on Abaco. However, the more open, exposed area into which the lizards were transplanted was several degrees warmer, and also more variable in temperature.

Lizards in the transplanted population experienced body temperatures 1.5 C higher than those in the reference population. When the researchers recaptured the lizards on Eleuthera, they found strong evidence for natural selection, and in the direction expected: lizards that performed better at higher temperatures survived better than those with lower performance optima, and those with a broader thermal range survived better than those more narrowly adapted. In other words, there was strong selection for adaptation to warmer conditions.

The big question is whether populations can adapt to such strong selection pressures. The authors didn’t measure the heritability of the traits—that is, the extent to which adults with higher temperature optima produce offspring with similarly high optima, and such heritability is crucial to predicting evolutionary response. Nonetheless, if these traits have levels of heritability equivalent to that of other thermal performance traits in other species, the authors argue, then the brown anole may well be able to adapt evolutionarily to the warming predicted to occur in the next century.

This paper received a lot of attention in the press and blogosphere. For example, nice articles appeared in the Washington Post and on Scientific American‘s website.

More Morphological Oddities in Anolis sagrei

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.

double regeneration

2. A jaw injury that resulted in the left and right sides of the jaws being dissociated from each other.

jaw injury

3. A cut hyoid. I imagine this lizard was no longer able to extend his dewlap.

hyoid

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.

head injury

5. A brutal leg injury.

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6. A male with not only an impressive tail crest but also some nice red tail coloration.

tail crest

 

The Dewlap of Cophosaurus texanus

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Here at Anole Annals, we can appreciate a good dewlap. In particular, a pair of agamid clades, namely the genera Draco and Sitana + Otocryptis, arguably do extensible throat fans even better than Anolis. But dewlaps are actually found in many other iguanian lizards, covered by AA posts here and here.

Today I thought I’d share a lesser-known dewlap, that of Cophosaurus texanus, known as the greater (greatest?) earless lizard, and a legitimate candidate for best lizard coloration if you ask me. In my experience, these lizards don’t often dewlap, but will occasionally hit you with a few push-ups, and reliably wag their striped tails at you before darting away — though they are upstaged in this latter respect by Callisaurus draconoides. On a recent walk in the Rincon mountains near Tucson, Arizona, I encountered a particularly saucy individual, and thought I would share.

Here’s a series of photos showing a pushup/dewlap combo being delivered. By the way, Cophosaurus texanus are known to display at potential predators (see Dial 1986, American Naturalist 127:1).

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Another shot, the dewlap is being retracted here:

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As far as dewlaps go, its not the most impressive, but there certainly looks to be some cartilaginous rod action involved, as in Anolis. But wait – notice anything unusual in the above photos? Yes, there looks to be a parasite peeking out through the lizard’s nostril. Here’s a closer look:

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Pretty gnarly. I’m not sure what the parasite is, it looks to me like it could be a maggot (hey, speaking of maggots, remember anole throat maggots?). Hope I didn’t just ruin anyone’s lunch!

Anyway, if you’re interested in learning more about Cophosaurus, here is an excellent write-up written by Robert Bezy and provided by the Tucson Herp Society.

Globalization and the 50-Year-Old Predicted Reorganization of Anole Biogeography

helmus_etal_fig2I caught an anole lizard and tossed it ten feet or so out into the water. To my dismay, it popped to the surface, swam expertly back to the shelter of the trees, and climbed up a mangrove trunk. Well, I continued, suppose a full hurricane blew an anole so far away on open water it couldn’t get back. Our little experiment shows that it could swim to the nearest islet if it were not too far away.

So wrote E.O. Wilson (1995 p. 271, Warner Books, NY) in his autobiography, Naturalist, reflecting on his island defaunation work with Daniel Simberloff. From his ‘little experiment’ (I can hear animal care committees cringing), Wilson postulated that anoles could, if they had to, disperse from island to island across open water. Whether anoles can cross water, however, isn’t that important. Rather, what’s important is that they rarely do. Anoles’ status as a symbol of island biogeography and adaptive radiation is largely due to the fact that isolation and the resulting low gene flow among islands set the stage for in situ speciation and adaptive radiation. In fact, much of what we (and island biogeography in general) owe to anoles, we owe because they don’t swim so well. And they don’t colonize new islands very often.

Or rather, they didn’t.

A new paper in Nature by Matt Helmus, with AA stalwarts Luke Mahler and Jonathan Losos, shows how human-mediated dispersal of anoles among Caribbean islands is reorganizing anole biogeography in a very predictable way. I suspect many who have worked on anole island biogeography, me included, have considered what to do about recent introductions and have often, like me, dropped them out of a dateset with the goal of trying to discern the ‘natural’ pattern. Helmus et al., however, saw the spate of recent anole introductions across the Caribbean as an opportunity, rather than a nuisance. Their great leap came from realizing that this reorganization of anole Caribbean biogeography should be predictable from the basic tenets of island biogeography theory.

Based on MacArthur and Wilson’s equilibrium theory, adaptive radiation theory and drawing on Losos and colleagues’ past work from 1993 and 2000, Helmus et al. predicted three patterns: 1) Species-impoverished islands (for their size) should have more exotics than more saturated islands, 2) The phylogenetic diversity of islands should increase due to exotic establishment, and 3) Human-mediated introductions should degrade richness–(geographic) isolation relationships. In short, they found evidence consistent with all of these patterns. Furthermore, they showed that economics that has replaced distance as the key determinant of island isolation. Needless to say, these are very exciting results that have supplied a key test, at biogeographic scales, of some classic theory*. It’s a must read.

This paper is also important because it shows how ‘blue skies’, curiosity-driven science can help us understand and, most importantly, predict how human activity will impact ecological systems. Did MacArthur and Wilson know, more than half a century ago, that their work would predict how increasing globalization and trade embargoes would affect modern biodiversity? I doubt it (cue someone pointing out in the Comments the exact line in the ETIB where they do predict this). However, regardless of whether they knew it at the time, this is exactly what their theory has done. As Helmus et al. state (p. 545): “Our results support the theory that it is the influence of geographic area and isolation on … speciation and colonization that fundamentally determine island biodiversity”. However, as they crucially find, what we now need to do is rethink how we define ‘isolation’. We can’t leave ourselves out of the equation any more. It’s economics, not geography, that matters now. Thus, not only does Helmus et al.’s paper test a long-standing theory, but it provides a clear example of the importance of fundamental scientific theory for understanding and predicting ecological dynamics in the ‘Anthropocene’.

In conclusion, the observation that humans are moving anoles — and other taxa — around faster than they could make their own way will come as a surprise to no one. But finding that the subsequent reorganization of life can be predicted by island biogeographic theory is fantastic (it should be pretty clear by this point that I like this paper. A lot). So if you haven’t read the paper, you should. I know it’s a terrible cliché to call a study ‘elegant’. So I won’t. I’ll call it damn elegant.

*I can’t help but mention that Helmus et al.’s findings were mostly based on good old-fashion OLS regression and ANOVA, and visualized using simple scatterplots – No fancy-shmancy statistical machismo here (phylogenetics aside). Just a clear set of predictions that could be parsimoniously tested. Chapeau.

Editor’s note #1: nice summaries of this paper have been written by Ed Yong’s Phenomena: Not Exactly Rocket Science blog and by Emily Singer in the new online Science magazine Quanta.

Editor’s note #2: The paper grabbed the cover of Nature.

Helmus et al. cover

This, in turn, joins a long list of recent science journal covers sporting an anole:

covers

Male Brown Anoles Disperse Farther than Females

sagrei dispersalUnderstanding dispersal—the extent to which organisms move from their place of birth—is of obvious importance in understanding many aspects of the natural history of a species, such as how related individuals are in a population or how genetically distinct one population is from another. Despite the intensive study on Anolis, however, very little is known about their dispersal. This is particularly surprising for species like the green and brown anoles, which are so common in so many places. Now, in a very nice experimental study in Behavioral Ecology, Calsbeek and colleagues have shed light on dispersal in the brown anole in the Bahamas.

Basically, the study went like this: the authors collected a bunch of gravid females from a variety of sites on a single, small island in the Bahamas. They got the lizards to lay eggs in the lab and hatched them out, then released them within three weeks of hatching back on their mom’s island. Each lizard was individually marked. The researchers then returned the following spring to find which animals had survived and how far they had moved. Then, they returned again in the fall to see how these survivors fared over the following summer and whether subsequent survival in this second period varied as a function of the distance they had dispersed in the first period.

There are a lot of interesting specific details and I encourage you to read the paper, but the broader story is this:

1. Males dispersed substantially further than females

2. Surviving males grew faster than surviving females

3. Survival of the lizards was low

4. Among females that survived the first period, those that had dispersed shorter distances survived better in the second period

Surprisingly little is known about the extent of anole dispersal, and so this paper is an important advance. As far as I’m aware, dispersal of only two other anoles have been studied. Here’s a summary from Lizards in an Evolutionary Tree:

“Little is known about the dispersal of anoles. One study of A. limifrons found that most lizards dispersed very little and that the home ranges of many individuals moved little from the juvenile to adult age. The maximum dispersal distance, measured as distance from the center of the juvenile home range to the center of the adult home range, based on 148 individuals, was 45 meters. Both the mean and extremes were greater for males than for females (Andrews and Rand, 1983). Anolis limifrons is a small and short-lived mainland species; it is always possible that larger, longer-lived species may disperse further.

The only other data come from Anolis aeneus, which moves as much as 150 meters or more after hatching to occupy open clearings (Stamps, 1983b, 1990). Ultimately, the lizards move back into shadier areas when they reach subadult size, although it is not known whether they return to the vicinity of their hatching site.

A number of arboreal species are known to disperse across open ground between trees (Trivers, 1976; Hicks and Trivers, 1983; Losos and Spiller, 2005).

A Taxonomic Epiphany Regarding Anolis utowanae (Not Really)

I awoke to a placid summer day in Cambridge, Massachusetts, on 3 August of 2013. My hosts at the aptly named Friendly Inn had prepared a sumptuous breakfast, which I had again slept through before embarking on my then-daily walk to the Museum of Comparative Zoology. As I strolled on, my concerns vacillated between the upcoming Catalina Wine Mixer and the validity of the lizard name Anolis utowanae, an enigmatic name associated with a single specimen ostensibly from Mazatlan, Mexico. Perhaps distracted by the excitement of the coming social season portended by the Mixer, I wandered a bit longer than usual and entered a quaint shop of letters on Massachusetts Avenue. The shop had on display a historical map featuring the population growth of the Pacific shipping ports shortly after the completion of the Panama Canal in 1914. As I gazed on that map, I experienced an epiphany regarding A. utowanae. What if Thomas Barbour, the describer of this problematic species, had in fact collected the specimen earlier, on the other side of the canal in the West Indies? My jubilance at this realization was such that I could not help but engage the curious shopkeep.

“Sir, with this display, do you realize what you’ve done?” I asked, gesturing towards the map.

The shopkeep stared at me, wide-eyed in bated anticipation.

“You have helped solve one of the great mysteries of Mexican anole taxonomy, ” I told him.

His pride was palpable as I exited the shop and proceeded hurriedly to the Museum to test my hypothesis.

The above narrative is largely but not completely true. It is a fact that I was in Cambridge in August 2013, I did walk to the MCZ every day, and I often thought about the Catalina Wine Mixer during my morning walk. But the important part—the part that might make this story a passable introduction to a scientific paper 80 years ago—is patently false. There was no epiphany about A. utowanae. Rather, my suspicion of the status of this name had been growing ever since I’d gotten serious about Mexican anoles. The time at MCZ just gave me the material to write a paper establishing this species as a junior synonym (Poe 2014; available now for free on the Breviora website!).

Figure 1. Thomas Barbour. He would hide his disgust if he weren't so disappointed in you. (Photo: Marine Biological Laboratory, Woods Hole, Massachusetts)

Figure 1. Thomas Barbour. He would hide his disgust if he weren’t so disappointed in you. (Photo: Marine Biological Laboratory, Woods Hole, Massachusetts)

Some readers of Anole Annals are likely aware of the story of Anolis utowanae. The species was described in 1932 with type locality near Mazatlan, Mexico. In the ensuing years, no additional specimens were procured despite the accessibility of the type locality and a lot of interest in Sinaloan herps. Thomas Barbour (Figure 1), of MCZ and anole fame and one of the kings of the Rich White Guy on a Yacht period of herpetological exploration, began the Anolis utowanae species description with a detailed story of the collection of the type specimen. Here it is:

On a day last spring, April 10, 1931, while driving with Mrs. Barbour and my daughter, Mary, to a finca some miles north of Mazatlan, we stopped in a dusty lane to let a herd of calves pass by. The herd was followed by a barefooted Indian who trudged wearily behind them through the deep dust. He carried in his hand a long lashed whip and from time to time he snapped it viciously and in so doing killed the lizards on rocks or fence posts by his way with most extraordinary skill. We watched him some time quite fascinated. I asked him what on earth he was pocketing these lizards for. He looked at me with surprise and then added, “I am taking them home to feed my cats.” I bought what he had for a few cents. It was obvious that he felt quite certain that he had been dealing with a person of unsound mind as he walked on looking at the coins, for it surely had never occurred to him that such small game had a cash value. Among these lizards one, I feel quite certain, is unknown.

                    —-Barbour (1932), description of Anolis utowanae

Thomas Barbour’s story of the discovery of A. utowanae shares some qualities with my epiphany story. His treatment is at least partially untrue and, more particularly, I am convinced that the important part of Barbour’s story—that he obtained a new species of lizard on an April day in 1931 in Mazatlan—is false. But I am getting ahead of myself.

I was at MCZ in August of 2013 to collect additional data on some projects in my lab that require information on every species of Anolis. Thus, I was addressing important questions like “how many toe lamellae does Anolis granuliceps have?” (answer: about 15) and “how many scales are across the snout at the second canthals in the parvauritus version of Anolis biporcatus? (answer: 11.5). In the context of this work, we must make a decision on every species of Anolis: Valid or Not? These decisions go beyond simple literature searches; we really are trying to predict what species are likely to end up valid in the foreseeable future. For example, we are not going to include Anolis ibague Williams 1975 in our key to Anolis, because we have visited the type locality of ibague (Ibague, Tolima, Colombia) and found several individuals of the supersimilar and earlier-described species Anolis sulcifrons, some displaying the purportedly unusual headscales of the type specimen (a juvenile female) of A. ibague (sorry, Ernest). We could include A. ibague in our analyses—virtually any list of Anolis species would include this name—but if there are no traits to distinguish ibague and sulcifrons, and we are fairly certain ibague is a junior synonym of sulcifrons…would such an approach really be scientifically responsible?

I mention the example of Anolis ibague because A. utowanae was a similar case, but with a more concrete answer. When I was at MCZ in 2013, we were finishing an electronic key to all Mexican Anolis and we needed to know whether the name utowanae is valid. Some recent work (Kohler, 2012; Nieto et al. 2013) had cleared up several other Mexican anole names, but A. utowanae remained an enigma. With the MCZ type specimen (MCZ 31035) in front of me, I gave myself two nights to figure this out.

The key ingredients to elucidating the status of Anolis utowanae were 1) the wonderful MCZ anole collection (Figure 2); 2) the nearly equally wonderful MCZ herpetology library, including texts by Barbour; 3) the excellent paper by Henderson and Powell (2004); 4) my electronic (Lucid) key to Anolis; 5) my lab’s inability to find A. utowanae during a stop near Mazatlan in 2011 (not the safest place to be walking around at night looking for anoles); and 6) later, the diary of Thomas Barbour’s daughter Mary (Leaves from my Diary, 1932). Oh, and the kindness and hospitality of Joe Martinez, Tsuyoshi Takahashi and Jonathan Woodward (Messrs. Losos and Rosado usually are equally tolerant hosts, but they were absent during this particular visit).

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Figure 2. As most Anole Annals readers know, MCZ has a fantastic anole collection. Here are some of the specimens I examined during my visit.

Put these elements together and you get my paper published this month in Breviora. I will spare you the time of reading the paper and summarize: Thomas Barbour apparently collected the Anolis utowanae specimen during his stop on Grand Cayman during the earlier part of a family voyage from Miami to Baja Mexico via the Panama Canal on a yacht called the Utowana. That is, Anolis utowanae = A. conspersus (Figure 3), and the skepticism of workers like Stuart, McDiarmid, and Lieb regarding the status of this name is validated. The lizard-whipping incident described in the paper probably actually occurred, but evidently involved a different lizard than the A. utowanae specimen. At some point Barbour mistakenly attributed a Grand Cayman anole to Mexico. Specifically, he associated an Anolis conspersus with the event where he and daughter Mary met a local cattle farmer in Mazatlan. How did this switch happen? Continue reading

And So the Carnage Is Resumed …

A brown anole (Anolis sagrei) male from Santzepu, Chiayi County, southwestern Taiwan.

A brown anole (Anolis sagrei) male from Santzepu, Chiayi County, southwestern Taiwan.

The Taiwanese authorities will once again launch a campaign to try to eradicate the brown anole in southwestern Taiwan. By paying a bounty of N.T.D 3 per collected lizard, they hope to encourage residents to help remove these lizards. They have funds for about 100 000 lizards, but I am afraid that is most likely not enough! The known distribution of this species in southwestern Taiwan is ca. 237 hectares. In my opinion the distribution most likely exceeds that. Those in the know are aware that these lizards can attain great densities. In one study, we found that they can attain densities of about 2900 lizards / ha. So, even if the average density is just 1/10 of that they do not have enough funds.
In addition to that, some religious groups are against the killing of animals and I have found that they do not permit the capture of these lizards on their properties. Even in areas where the capturing of the lizards is permitted, it is difficult to collect all the individuals present. Anolis sagrei that have escaped after being captured tend to flee from a perceived threat at greater distances, which means that such individuals could persist in an area without the collectors being aware of them. These lizards are also opportunistic and can utilize a variety of natural and man-made structures as shelters, many of which would hinder the capture of lizards. In addition to that, some agricultural practices such as the use of greenhouses can act as reservoirs for these lizards. It is thus not surprising that in spite of the large numbers of lizards removed to date, A. sagrei still exists in the southwestern and eastern study site and seems to be expanding its distribution range in Taiwan.

An Anolis sagrei male sheltering in an electrical control unit in an agricultural area in the southwestern Santzepu, Chiayi County, southwestern Taiwan (note the sympatric Hemidactylus frenatus on one of the electrical wires).

An Anolis sagrei male sheltering in an electrical control unit in an agricultural area in the southwestern Santzepu, Chiayi County, southwestern Taiwan (note the sympatric Hemidactylus frenatus on one of the electrical wires).

An Anolis sagrei sheltering in a drainage pipe (right) of a concrete roadside embankment in Santzepu, Chiayi County, southwestern Taiwan.

An Anolis sagrei sheltering in a drainage pipe (right) of a concrete roadside embankment in Santzepu, Chiayi County, southwestern Taiwan.

So my money is on the lizards! Because the distribution of A. sagrei in Taiwan is fairly extensive and the species disperses very easily, the eradication of A. sagrei in Taiwan is impractical. Efforts should rather focus on managing this species.

My opinion is that one of the best ways to do so is by manipulating habitats and making them unsuitable for A. sagrei to inhabit, and so hinder the spread of this species in Taiwan and limit its population growth. The cultivation of crops such as rice (Oryza sativa) and taro (Colocasia esculenta), which are unsuitable habitats for these lizards, should be encouraged in agricultural areas where these lizards are known to occur. Also, since broadleaf forests in Taiwan are likely unsuitable habitats for A. sagrei, greater efforts should be made to re-establish and conserve large areas of broadleaf forests in disturbed lowland areas of Taiwan. This would not only contribute to the conservation of native forest species, but such areas will also function as reservoirs for species like Japalura swinhonis that can compete with A. sagrei, as well as being barriers for its spread.

Dwarf Boa Versus Giant Twig Anole

Figure 1. Sequence of the unsuccessful predation by Tropidophis melanurus on Anolis porcus. See Torres et al. 2014 for the full description. Photos by Carlos Pérez-Penichet.

Snake predation on anoles has been widely documented on this blog (1, 2, 3, 4, 5, 6). Torres and colleagues, writing in Herpetology Notes, add to this collection with stunning pictures of a dusky dwarf boa, Tropidophis melanurus, constricting an Anolis porcus, a member of the Chamaeleolis clade.  While the individuals were found entwined on the ground, they likely fell out of nearby tree since A. porcus is a highly arboreal species. The anole was ultimately spared an unpleasant fate, but it was unclear whether the lizard was too big for the snake to consume or if the snake was disturbed by the observers.

Torres, J., C. Pérez-Penichet, and O. Torres. 2014. Predation attempt by Tropidophis melanurus (Serpentes, Tropidophiidae) on Anolis porcus (Sauria, Dactyloidae). Herpetology Notes 7: 527-529.

Bolder Lizards Drop Their Tails More Readily to Compensate for Risky Behavior

(editor’s note: this video was added by the editor. Decide for yourself whether it illustrates the experimental approach described below)

It’s no secret that grabbing a lizard by its tail will often times leave you with the tail rather than the lizard. Why? Because the tail would simply break off. The voluntarily shedding of the tail in lizards (tail autotomy) has fascinated herpetologists ever since the 70s, and it didn’t take long for those people to notice that the propensity for tail autotomy varies extensively among species, conspecific individuals, or even within the same individual at different developmental stages. Four decades have passed, what might be responsible for the variation in tail autotomy is still not entirely clear. In a recent paper, we tried to solve a piece of the puzzle by testing the hypothesis that lizards might autotomize the tail with different propensities to compensate for their intrinsic risk-taking tendency.

Our idea was simple: bolder lizards, due to their behavioral tendency, tend to expose themselves more to higher predation risk. Therefore, selection might favor higher propensities for tail autotomy in bolder lizards as a compensation mechanism. We were also interested in knowing how food availability in the environment might affect tail autotomy. So, we caught a bunch of juvenile brown anoles from the same population in New Orleans and assigned them into two dietary groups: low versus high food availability. After the lizards reached adulthood, we picked out the males and examined the relationship between boldness and the propensity for tail autotomy. (In case you wonder how we measured the propensity for tail autotomy, we refer you to a paper by Stanley Fox, who contributed greatly to our knowledge of tail autotomy.)

And here’s what we found:

The relationship between boldness and the propensity for tail autotomy in the brown anole lizards

Bolder lizards did autotomize their tails more readily as a means to compensate for their risk-prone personality, but only in the group raised with abundant food. Our results helped explain why lizards from the same population autotomized the tail with different propensity. Moreover, our study highlighted the role of food availability in the cost-benefit dynamics of tail autotomy, which has never been explicitly discussed or tested before. Aside from those exciting implications for the study of tail autotomy, our results also have important bearings on broader topics such as the evolution of trait compensation and animal personality. If you are interested in knowing more about this project, check out our recent paper:

CHI-YUN KUO, DUNCAN J. IRSCHICK and SIMON P. LAILVAUX. (2014). Trait compensation between boldness and the propensity for tail autotomy under different food availabilities in similarly aged brown anole lizards. Functional Ecology DOI: 10.1111/1365-2435.12324

Seasonal Shifts in Relative Density of the Lizard Anolis polylepis (Squamata, Dactyloidae) in Forest and Riparian Habitats

displaying on leaf

A. polylepis displaying dewlap.

A commonly observed, but little studied, aspect of tropical herpetology is the seasonal shift in some species’ relative abundance in forested habitat and adjacent, nearby streams. The general pattern is that during the dry season, some species of forest frogs, lizards, and snakes seem easier to detect along streams than in the forest and vice versa during the wet season. Despite this intuitively unsurprising seasonal shift in macrohabitat use being noticed in the 1960s by researchers like Jay Savage and Norm Scott, there has been little work done to document it. In an upcoming issue of the Journal of Herpetology is a paper titled: Seasonal Shifts in Relative Density of the Lizard Anolis polylepis (Squamata, Dactyloidae) in Forest and Riparian Habitats.

The difficulty in documenting seasonal macrohabitat shifts is twofold. First, field sampling must encompass both seasons and be continuous. Second, simultaneous sampling needs to occur in both forest and streams across seasons. For many tropical herpetologists, the opportunity and time for such a study do not come about often. In December 1999, I had this opportunity when I spent three years studying the herpetofauna along the south-central Pacific coast of Costa Rica. I was a young, precocious and budding herpetologist and wanted to understand the ecological habits of all the local amphibians and reptiles. So, out of curiosity I set up transects in a 25-hectare forest patch and a stream that ran through the forest at the Tropical Forestry Initiative (TFI) research station. For 29-months, with the help of field assistants (Deborah Merritt and Yemaya Maurer St. Clair) we sampled the transects regularly, documenting and observing species diversity and habitat use in the forest and stream. While I was organizing the data, an interesting pattern emerged in regard to Anolis polylepis. Of all of the species in the local lizard fauna, A. polylepis showed the strongest seasonal shift in relative density between the two habitats!

Anolis polylepis is the most common anole along the Pacific coast of Costa Rica, reaching densities of up to 300 individuals per hectare (Andrews 1971; Scott 1976). The species can be found in a wide variety of forested habitats ranging from old growth forest to gardens with ample shade trees. In my experience, the only necessary habitat requirement for A. polylepis is shade from a closed canopy. The high density and generalist habits of A. polylepis make it a wonderful study species.

Like many forest anoles, A. polylepis is active in the understory during the day. However, obtaining accurate population counts can be difficult because individuals are wary and can be difficult to detect. For example, A. polylepis will jump to the ground or circle around a tree when observed. This avoidance behavior can be problematic when attempting to obtain reliable counts by increasing the likelihood of missing a lizard. To counter this difficulty, I surveyed for A. polylepis at night, which facilitated easier detection. Anolis polylepis, like many species of anoles, sleeps visibly on leaf tops, twigs, branches and vines from 0.5 to 4 meters above the ground. Thus, it is easier to obtain better counts of relative density for some anole species when lizards are sleeping and inactive. Nocturnal surveys can be very informative for addressing certain questions related to anole biology.

In total, 41 nocturnal surveys were conducted between January 2001 and February 2002, covering one wet and one dry season. We found significant seasonal differences in A. polylepis relative densities between the wet and dry season. During the dry season, A. polylepis density was 0.052 lizards per meter in the stream and 0.010 lizards per meter in the forest. This pattern reversed in the wet season when stream relative density was 0.002 lizards per meter and forest relative density was 0.036 lizards per meter. This seasonal change in relative abundance suggests that wet-dry seasonality influences macrohabitat use in A. polylepis in Costa Rica.

One major limitation of our study was that we did not use mark-recapture. Use of such an approach would give insight into the individual movements associated with our observed patterns. For example, we could test whether lizards are moving large distances to the stream during the dry season, or whether deep forest lizards are moving to moist microhabitats within the forest such as tree buttresses, to name two possibilities.

As with many pilot field projects, ours documents a novel pattern, but raises additional questions. Future work on this issue should extend to other species and regions and use mark-recapture or radio telemetry to elucidate the details of seasonal migrations. An understanding of seasonal movements in environments with distinct wet and dry seasons has implications for how anoles and other herps can tolerate the harsh dry season.

References:

Andrews, R.M. 1971. Food resource utilization in some tropical lizards. Unpubl. PhD diss. University of Kansas, Lawrence.

Scott, N.J. 1976. The abundance and diversity of the herpetofauna of tropical forest litter. Biotropica 8:41-58.

A. polylepis on tree trunk.

Sleeping A. polylepis. Courtesy of Cesar Barrio Amoros.

Sleeping A. polylepis. Courtesy of Cesar Barrio Amoros.

 

 

Anoles (Sort of) Eat Mice

geckoeatsmouse

After last week’s report about Tokay geckos consuming small rats, readers may be concerned that their favorite lizard is lacking a little in the predator department. Fear no longer! In this recent article, Torres and Acosta describe an Anolis porcatus observed carrying a dead house mouse. While the authors suspect that the mouse was disoriented by venom pellets when it was caught (and that the mouse was probably too big for the lizard to consume), it still goes to show that anoles have plenty of killer instinct. This plucky A. porcatus is especially impressive since almost all previous reports of predation by anoles on small vertebrates feature much larger crown giants.

Torres, J. and M. Acosta. 2014. Predation attempt by Anolis porcatus (Sauria, Dactyloidae) on Mus musculus (Rodentia, Muridae). Herpetology Notes 7:525-526.

How Anoles Respond to Toucans and Other Birds

James Christensen, a fabulous nature photographer and keen naturalist, made the following comment on the recent post about how anoles react to bird calls. However, the points are so important that they deserve a post of their own, so I’m reprinting them here:

I have spent many hours photographing wild anoles, especially here in Ecuador, and have learned a great deal about their behaviour while watching them through the viewfinder. When the wind picks up and begins to stir the surrounding foliage I can expect my subject to risk rapid movement – therefore, I probably won’t get a viable shot. Conversely, when toucans or furnarids become active in the vicinity I know that my anole will not venture an abrupt movement, so I squint through the viewfinder and start clicking the shutter. What I have noticed is that the anoles – e.g. Anolis gemmosus and A. proboscis – react not only to the calls of these birds, but also to the sound of their wingbeats. The usual response is a cessation of movement and an increased watchfulness; the anole sits very still and peers upward while discreetly swivelling its head. In the case of a very fit male A. gemmosus with whom I spent many hours – over a period of several weeks – upon the disappearance of avian predators he would begin to dewlap, frequently ‘emphatically’, seeming to reassert his local dominance in the wake of forced inactivity. It became clear to me that the sounds of nearby birds triggered a profound shift in behaviour, and that vision played a secondary role in the perception of avian threats – as every neotropical birder knows, foraging birds are heard more readily than seen.

Concerning the above study, it perhaps bears noting that the American Kestrel is not a highly vocal bird, and that it is likely to remain silent while hunting. I have frequently observed toucans apparently hunting in shrubby forest margins, where no fruit-bearing trees were evident and anoles were plentiful, and at such times the birds were always silent – only their deep wingbeats would betray them to a wary anole.

New Comprehensive Account of Everything about Tuatara

Alison Cree, one of the leading researchers on tuatara, has written a comprehensive account of everything we know–and would like to know–about toots. The book not only covers ecology, evolution, behavior, physiology and so on, but also the history of knowledge of tuatara as well as details on how they were perceived by the Maori. And, of course, the incredible conservation turnaround, which has led to reintroduction of tuatara to the New Zealand mainland after a half-millenium absence.

This fine volume can be purchased for a tad under US$75 plus shipping from the University of Canterbury Press.

Anole Apartment Invasion: What Can Be Done?

Anole in the house. Photo from Daffodil’s Photo Blog

AA reader Katharine from southern Florida writes:

“I live on the 4th floor of a 4-story concrete constructed condominium building (6 units to a floor) with catwalks in S.E. Fl.  In front of the ground floor walkway of our building there is landscaping & ligustrum trees that reach up to the 2nd floor with catwalks with overhead lights on in front of each doorway at night.

For some reason anole lizards seem to find their way more to my unit (when I open my entrance door they come in) than the others on the same floor all with the same ground floor foliage, trees & overhead lights. One also sees the feces they’ve left overnight in front of my unit and not the others.

It makes me wonder if these lizards travel as ants do, following a leader either by a scent or fluid left by the leader or previous lizard?  I’ve learned that these lizards are attracted both to light (obviously, the catwalk lights) & the greenery.  However,  the other units on the same floor under the same conditions don’t seem to have the same invasion.

I’ve done as much Google researching as I can but can’t seem to find an answer.  Do you have an answer or can you direct me where I can look.?  Obviously, I’m trying to find some way to deter or reroute their path.”

ABS 2014: A Novel Social Behaviour in Uromastyx Lizards

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!

Geckos Eat Rats

gecko eating rat

As lizards go, it’s hard to beat an anole. But geckos come pretty close. Anole Annals, of course, is dedicated to reporting all things anole, but until Gecko Gossip debuts, we feel it’s only polite to occasionally comment on geckonid happenings.

In that light, we were impressed to see the culinary prowess of the Tokay gecko, which apparently quite regularly preys on small rats in the Philippines. Read all about it in Herpetology Notes.

Anole Foraging Mode: New Data

An actively foraging anole on the prowl (A. tigrinus; photo by J. Losos)

An actively foraging anole on the prowl (A. tigrinus; photo by J. Losos)

Nearly 50 years ago, Eric Pianka proposed the idea that hunting animals forage in one of two ways, either actively foraging for prey or sitting-and-waiting for food to wander by. These ideas were initially promulgated with lizards in mind, and much of the research in the last half century has involved lizards. Anoles haven’t been a major player in the work, but their certainly have been some studies conducted on anoles.

This post is motivated by a paper published by Cooper et al. in Herpetology Notes last year in which new data are presented on six anole species, as well as for a variety of other species. The anole data conform both to previous data on the same species and studies on anoles in general: as lizards go, anoles are on the sit-and-wait end of the spectrum, moving relatively little (think about the other end of the spectrum, species like whiptail lizards which seem to move almost non-stop).

I was surprised in looking through the archives to see that we haven’t previously had a post on AA about foraging mode. Now we do! And for some background: I reviewed what we know about anole foraging in a five-page section of Lizards in an Evolutionary Tree. The take-home messages:

1. By comparison to other lizards, anoles don’t move much and would be considered sit-and-wait foragers;

2. Nonetheless, among anoles, some are much more active foragers than others;

3. Caribbean anoles are much more active than mainland species;

4. Much remains to be learned about the specifics of anole foraging and how it differs among species

And here are some highlights, from the footnotes:

“Some of the danger inherent in an active foraging mode was apparent in another observation of a female [A. valencienni] moving upside down on a bromeliad, searching for prey (quoting from Trivers’ field notes, p. 575): “. . . it seems to spot something on a neighboring bromeliad, also upside down. I too spot something on the second bromeliad. Starts to dart the 5 cm to the neighboring bromeliad but—as if forgetting it is upside down—it steps into thin air and falls 6 m to the ground. It appears to be uninjured.”

“Examples of this prey-catching behavior were provided for the relatively short-limbed A. carolinensis (under the name A. principalis) by Lockwood (1876, p. 7): “I have just been watching Nolie eying a fly which was walking on one of the glass panes of his house. He made a noiseless advance of about three or four inches; then followed a spring, when he was seen cleaving to the glass by his feet, and champing the captured fly. I saw him once intently watching the movements of a fly which was walking on the glass. As seemed evident to me by an ominous twitch of that little head, his mind was made up for a spring; but lo, there was a simultaneous makeup of mind on the part of the fly, which at this juncture flew towards the other side of the case. Then came—and how promptly—mental act number two of Anolis, for he sprang as the after-thought directed, and caught the insect on the fly.” Dial and Roughgarden (1995) report an anole jumping from a branch one meter above a spider web, catching the spider as it passed by, before landing in the vegetation below.”