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Global Warming Effects On Tropical Lizards

Martha Munoz starting the all-anole morning with a comparison of the thermal niches of different species of Hispaniolan cybotoid anoles

Martha Munoz starting the all-anole morning with a comparison of the thermal niches of different species of Hispaniolan cybotoid anoles

The symposium “The Biological Impacts of Tropical Climate Warming for Ectothermic Animals,” was recently (Aug. 1-3) held in San Juan Puerto, and it was a great success. In a two-part post, I will provide a brief summary. Today will focus on four talks on the second morning, all of which focused on Anolis. In the next post, I will review the rest of the symposium.

Martha Muñoz began the day by talking about the thermal biology of cybotoid anoles (members of the cybotes species group) in Hispaniola. These species show a remarkable elevational range from sea level to over 3000 meters. Martha pointed out that in this respect, Hispaniola is a much better place to look at questions related to elevation than Puerto Rico, a comment greeted with jeering from much of the crowd. Nonetheless, she scoffed at the discussion of the “high elevation” A. gundlachi at 850 m. Why, A. shrevei, in Hispaniola doesn’t even occur that low! In any case, what Martha showed is that despite the great thermal differences in habitats at different elevations, the cybotoids maintained approximately the same body temperature at all sites and have the same preferred temperatures and critical thermal maxima. Clearly, they are using thermoregulatory behavior to buffer their thermal physiology from selection in different environments and, indeed, field observations show that high elevation species do bask more. However, anoles can’t thermoregulate at night, and there is where adaptive differentiation occurs: high elevation anoles can withstand lower temperatures than lower elevation species. To clinch the deal, Martha measured the temperatures lizards experience at night. Indeed, the species at high elevation experience temperatures that would kill low elevation species.

Luisa Otera showing a slide of her collaborator, George Gorman, in his cowboy salad days

Luisa Otera showing a slide of her collaborator, George Gorman, in his cowboy salad days

Luisa Otera spoke next on the “Effects of recent climate warming on the reproductive phenology of Puerto Rican Anolis lizards.” Luisa revisited sites at which George Gorman had examined A. cristatellus 40 years ago. Gorman had found that at higher elevations, female reproduction tapered off in the winter, whereas at lower elevations, they continue reproducing year-round. Her prediction was that with higher temperatures, reproduction should be extended in the winter at high elevations. For the most part, this prediction was confirmed, though surprisingly not so at the sea-level site.

Most surprising, in a new twist, Luisa found that female reproduction could vary over a very short spatial scale. In particular, if a lizard has a territory in the open with a lot of sun, it can breed year round, whereas it’s neighbor under the shade of trees a few meters away may not be able to do so in the winter. Perhaps this explains the contrary finding at the sealevel sites: greater tree cover may have actually made conditions worse.

Luisa pointed out that warming isn't always bad--for some lizards, it allows them to extend their breeding seasons

Luisa pointed out that warming isn’t always bad–for some lizards, it allows them to extend their breeding seasons

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Gunderson’s data show that even lizards with body temperatures outside of their preferred range are still quite active

Alex Gunderson spoke next on “Behavioral responses to climate change: natural selection on the thermal physiology of Anolis sagrei.” Perceptive readers will note that these three talks focused sequentially on the trunk-ground anoles of three different islands. Coincidence? You be the judge. In any case, in a very thought-provoking talk, Alex pointed out that much of the literature predicting the response of species to global warming focuses on the effect that higher temperatures will have on the time in which lizards can be active, which affects factors like food acquisition. However, Gunderson note that although activity time is usually treated as a binary variable—a lizard is either active or it isn’t—his extremely detailed behavioral data (299 focal observations), indicate that, in fact, the effect of temperature on activity is continuous rather than binary. Indeed, lizards engage in all major activities—eating, mating, fighting—at temperatures substantially outside (mostly below) their “preferred temperatures.” This finding calls for a re-thinking of how we model the effects of climate change on lizard populations—they may be forced to be active at temperatures they’re not so happy about, but they will do more than stay in their hidey-holes.

Next, Michael Logan reprised his talk on the “Rapid evolution in response to climate change: natural selection on the thermal physiology of Anolis sagrei” which he gave at the Evolution meetings five weeks previously. But here he had twice as much time to speak and correspondingly gave greater details. Since I’ve reported on the talk previously, I’ll just summarize here: in a very cool experiment, he moved brown anoles from a shady habitat to a much hotter one. Before doing so, he measured the performance curves of each lizard (i.e., how their ability to sprint was affected by temperature). His prediction was that individuals that could sprint at higher temperatures would be favored by natural selection in the new habitat. And sure enough, they were! By contrast, another population in a shaded habitat experienced no selection on thermal performance. If thermal sensitivity of sprinting is a heritable trait—a big if, Mike noted—this strong selection could suggest that populations might be able to adapt very rapidly to warming climates.

A New Confirmation Of Pair Bonding In Anolis Limifrons

Monogamy, or the formation of stable pair bonds between males and females for reproductive purposes, is thought to be relatively rare across animals. While social pair formation is observed (commonly in birds and occasionally in reptiles), genetic assessments of parentage have revealed that mating fidelity is infrequent. Social monogamy is therefore not equivalent to genetic monogamy. However, the reasons for the persistence of social monogamy despite promiscuous mating remain unclear.

Sleepy lizards are the best known example of pair-bonding in lizards

Sleepy lizards are the best known example of pair-bonding in lizards (photo by J. Todd Kemper)

A new paper by Alexis Harrison revisits one of the only examples of social pair-bonding known from anoles–a population of Anolis limifrons in the La Selva Biological Station in Costa Rica. While most anoles are polygynous, with the territory of one male overlapping the territories of several females, Talbot (1979) noticed that 70% of adult A. limifrons in La Selva were found in pairs of a single male and female in close proximity to each other. However, such pair bonding has not been documented in any other population of the species, making La Selva an intriguing outlier.

A pair of Anolis limifrons

A pair of Anolis limifrons (photo by Jason Weigner)

Anoles Link Spatially Distinct Terrestrial Food Webs – Part 1 Of 2

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LIke all the anoles in our study, a considerable fraction of A. equestris’ diet was derived from the flow of allochthonous resources into its habitat.

A. sagrei, probably the most common vertebrate in Florida perch low on trees making occasional forays to the ground to feed.

A. sagrei, probably the most common vertebrate in Florida perch low on trees making occasional forays to the ground to feed.

The ecological importance of small, terrestrial insectivores such as litter frogs and small geckos is a topic that I’ve been curious about for years. While my dissertation research does not include anything about it, I am still quite curious about how these small, diverse and abundant vertebrates fit into ecosystems. Anoles possess all of the attributes that seem to predispose them to strong interactions and soon after arriving in Miami to begin my Ph.D., I decided to launch a small, side-project using tried-and-true food web tools, stable isotopes and gut content analysis to try to illustrate if and how these small, rather inconspicuous predators might affect ecosystem structure and function. The results of this study were just published online in Functional Ecology.

Basically, we found that anoles couple adjacent food webs by consuming insects that move across habitat boundaries. While food web linkages are a potentially important ecological dynamic and our study yielded some unique findings, there are other bits of information for those more generally interested in anole biology. Therefore, I’ve decided to break this post into two parts. Part 1 deals with our primary findings and contextualizes them within current understanding of food web ecology linkages. It’s sort of a geeky treatment of the subject. Part 2 will illustrate some of the other data that we’ve collected that were not dealt with explicitly in the paper that will be of interest to, I suspect, AA readers.

Bidirectional trophic linkages couple canopy and understory food webs

Sean T. Giery,Nathan P. Lemoine, Caroline M. Hammerschlag-Peyer, Robin N. Abbey-Lee, and Craig A. Layman

1.  Cross-system resource flux is a fundamental component of ecological systems. Allochthonous material flows generate trophic linkages between adjacent food webs, thereby affecting community structure and stability in recipient systems.

2.  We investigated cross-habitat trophic linkages between canopy and understory food webs in a terrestrial, wooded, ecosystem in South Florida, USA. The focal community consisted of three species of Anolis lizards and their prey. We described interspecific differences among Anolis species in the strength and routing of these cross-habitat flows using stable isotope analysis, stomach content analysis, and habitat use data.

3.  All three Anolis species in this study consumed different prey, and occupied vertically distinct arboreal habitats. Despite these differences, carbon isotope and stomach content analysis revealed strong integration with understory and canopy food webs for all Anolis species. Modes of resource flux contributing to the observed cross-habitat trophic linkages included prey movement and the gravity-driven transport of detritus.

4.  Our study shows that terrestrial systems are linked by considerable bidirectional cross-system resource flux. Our results also suggest that considering species-specific interactions between predator and prey are necessary to fully understand the diversity of material and energy flows between spatially separated habitats.

MAp

The study system was dominated by St. Augustine grass and isolated Ficus trees.

Some basics – The community was composed of four anole species, Anolis sagrei, A. distichus, A. carolinensis*, and A. equestris. The study site was recently featured in AA. Generally, the purpose of the study was to describe variation among species in resource use using stomach contents, habitat use, and stable isotope analysis. But based on some initial observations and a bit of stable isotope data, we had considered that there might be a role for anoles in ecosystems via linking spatially distinct food webs. That is, anole diets might be sourced, in part, by primary production originating outside their respective microhabitats. Basically, we knew that anoles occupy distinct arboreal habitats, but when we examined the stomach contents of each, we found that some prey were from habitats spatially distinct from the ones used by each anole species (e.g., How do terrestrial grasshoppers get inside a canopy giant anole such as A. equestris?),which spawned a more in-depth investigation. Additionally, some initial stable isotope data strongly supported the same interpretation – that is, anole diets might be at least partially derived from allochthonous resources.

Ecological And Population Data On Some Little Known Ecuadorian Anoles

Ken Miyata–naturalist, fly-fisherman, and photographer extraordinaire–died tragically young 30 years ago at the age of 32. Among the many items of unfinished business was his gargantuan thesis, Patterns of Diversity in Tropical Herpetofaunas, 787 pages in length and entirely unpublished. The dissertation ranges far and wide over topics herpetological and ecological–check out the Table of Contents at the bottom of the post. Over the years, Ernest Williams tried to talk a number of scientists into guiding some of the chapters into print, but the task was too large and so it has remained shelf-bound.

Anolis peraccae. Photo by Luke Mahler.

Anolis peraccae. Photo by Luke Mahler.

After a recent trip to Ecuador, I happened to be looking at the thesis for other reasons (parts of it were incorporated into the description of A. lyra by Poe et al. in 2009) and came across Chapter 2. This multi-part section includes separate studies on the habitat use of three anole species at the Río Palenque field station (A. chloris, A. festae and A. peraccae) and population biology and dynamics of two other species elsewhere (A. boettiger and A. gemmosus). Miyata argued that little was known of the population biology of South American anoles. Thirty years on, the situation isn’t all that different.

Anolis chloris. Photo by Luke Mahler.

Anolis chloris. Photo by Luke Mahler.

As a result, the data presented by Miyata in 1983 are still very relevant today and deserve wider circulation. And for that reason, we decided to publish a lightly-edited version of parts Chapter 2 in the Bulletin of the Museum of Comparative Zoology, appropriate given that Miyata was a grad student in the Museum (this paper, like all other Bulletins of the MCZ, is available online). In addition, in an online supplementary file, a number of his friends) Jerry Coyne, Chuck Crumly, Ray Huey, Eric Larson, Greg Mayer and B Wu) provide reminiscences of Ken.

The paper ranges widely over matters of anole ecology, behavior, and population biology, providing data on five species for which almost nothing exists in the literature. The paper’s findings are summarized in the abstract:

Anolis festae. Photo by Luke Mahler.

Anolis festae. Photo by Luke Mahler.

Little is known about the ecology and natural history of South American anoles. This study reports the results of a variety of different studies on several relatively common species of Ecuadorian Anolis. In part I, habitat use and population density are compared among three species of Anolis that occur in sympatry at a number of sites in Ecuador. The three species—A. chloris, A. festae, and A. peraccae—are roughly the same body size. These species perch primarily on tree trunks, and A. chloris perches substantially higher than the other two species, which are similar in perch height. Large differences from one year to the next were observed both in mean perch height and in population densities.

Anolis gemmosus. Photo by Jonathan Losos

Anolis gemmosus. Photo by Jonathan Losos

In Part II, natural history, growth rates, and population densities are reported for two little known Anolis species, A. bitectus and A. gemmosus. Although the two species are from nearby regions and are similar in microhabitat use, they show more differences than similarities in most aspects of their biology. The species have similar ranges in active body temperatures, but A. bitectus is thermally passive, whereas A. gemmosus appears to thermoregulate. Populations of A. gemmosus tend to remain constant through time, whereas A. bitectus undergoes moderate population fluctuations. Both species exhibit little sexual size dimorphism, but in A. bitectus females are larger, and in A. gemmosus males are larger. Anolis bitectus has a fairly high characteristic growth rate, whereas that of A. gemmosus is quite low.

Microsoft Word - Table of Contents entire thesis.docxMicrosoft Word - Table of Contents entire thesis.docx

Evidence Suggests That Cloacas Carry Risk: Venereal Disease and Lizard-Parasite Coevolution

Anolis cristatellus wileyae - Does this pair need to worry about Cyrtosomum infections?

Anolis cristatellus wileyae – Does this pair from St. Thomas need to worry about Cyrtosomum infections?  Read on.

I wanted to write a few posts about parasites because hey – anoles have some really neat parasites! First up are the nematodes in the genus Cyrtosomum, which have been reported from several anoles and some other lizard taxa like Sceloporus and Cyclura. You might remember Cyrtosomum because C. penneri was the worm that AA-contributor Gerrut Norval and his colleagues used to infer that the Taiwanese population of A. sagrei originated from Florida and not Hawaii, something that wasn’t clear from sagrei molecular data (cool!).

Aside from pinworms (we’ll get to these another day), Cyrtosomum species are probably the most widespread nematode parasites in anoles. They’re really small (difficult to see without magnification), and occur in really large numbers in the lizards’ large intestines (many hosts have worm burdens of 100-200). Until recently, we knew very little about their life history – we knew that they could multiply within a single host individual via infective larvae, but we didn’t know how they moved between host individuals. Several authors (including Norval et al.) noted that Cyrtosomum species are only found in adult lizards, and suggested the possibility that these are sexually transmitted parasites.

Okay, let’s just take a moment… Worms, from sex. Yep.

Gabe Langford and his students tested this hypothesis in C. penneri, and

Biomechanics Shed Light On Differences In Signal Behaviour

ordWhy do closely related species sometimes differ in signalling behaviour, despite apparent similarities in the selection pressures that act on the signal? That question is addressed in a paper in Functional Ecology now available as an early view.

Comparing Anolis species from Jamaica that extend the dewlap rapidly with more slowly extending relatives from Puerto Rico, Ord, Collar and Sanger have modelled the performance of the dewlap and then simulated changes to the system to predict its effects on the speed of the dewlap extension. The predictions are then compared with data on both morphology from cleared and stained specimens and actual dewlap speeds for lizards recorded in the field.

The analyses show that morphological changes have affected the performance of the dewlap display in Jamaican and Puerto Rican anoles differently. Within islands structural changes have led to differences in dewlap speed among species, whereas differences between islands are the result of an increase in muscle contraction velocity present in Jamaican species, but absent in Puerto Rican species.

The study is an excellent example of how investigations into the biomechanics of motion-based visual displays can increase our understanding of differences in signal behaviour.

Anole Display Behavior: Posters At the Animal Behavior Meetings

The 50th annual conference of the Animal Behavior Society kicks off today in Boulder, Colorado. Anole presentations are few: only two posters, which begs the question, why aren’t more behavioral biologists studying anoles? Certainly, their behavior is easily observed and manipulated. And, indeed, some such work is conducted, but not nearly as much as one might expect given the ubiquity of the animals in the southeastern U.S. and throughout the neotropics. And, moreover, the behavioral work that is done is relatively infrequently published in the behavior literature or, apparently, reported at behavior meetings. Behaviorists, you’re missing the boat!

In any case, the sole anole reporter at ABS is Joe Macedonia, who is presenting two posters. The first is a comparison of the behavior of the odd gray-dewlapped green anoles with more ordinary, red-dewlapped populations, and the second is a study using anole robots to determine the relative importance of dewlap color and behavior in species recognition; this study has recently been published and we should be hearing more about it soon.

A Comparison of Headbob Display Structure in Gray-Dewlapped and Red-Dewlapped Anolis carolinensis

JM Macedonia, LE Cherry, DL Clark

Many species of diurnal lizards engage in motion displays, termed ‘pushups’ or ‘headbobs’. In the diverse genus Anolis, headbob display structure typically exhibits substantial interspecific, and in some cases population-level, variation. The green anole (Anolis carolinensis) exhibits a red-dewlapped (RD) form found throughout the southeastern USA, as well as a gray-dewlapped (GD) form that is restricted to southwest Florida. Prior research has shown that RD A. carolinensis produce headbob displays of three basic types (Type A, B, C) that vary primarily in display unit durations. Based on known genetic and physiological differences between the two dewlap color forms, we hypothesized that GD and RD males also would differ in headbob display temporal structure. We quantified 440 displays from 24 GD and 15 RD males, and found some, though not all, display units to differ significantly in duration between the two populations. Our results therefore indicate that stereotyped display behavior can be added to the list of known traits that differ between the gray-dewlapped and red-dewlapped forms of A. carolinensis.

Color and motion display discrimination in Anolis grahami: evidence from responses to lizard robots

JM Macedonia, DL Clark, DJ Kemp

Anolis lizards exhibit color and motion displays that are thought to mediate species recognition, but direct experimental support is limited. We used lizard robots in two field experiments to test the relative importance of dewlap color (calibrated using a computational visual model) and headbob display structure for species recognition in Anolis grahami on Bermuda. Results from experiment 1 revealed equivalent, significant decrements in responsiveness of 102 adult male subjects to color and motion display manipulations, relative to the conspecific robot control. Findings also suggested that dewlap hue, not brightness, was responsible for reduced subject response to non-control dewlap colors. In experiment 2 we presented 93 different A. grahami males with conspecific or heterospecific (Anolis extremus) robots that performed their own, or the other species’, headbob displays. Results revealed species-specific body/dewlap coloration to be more important than headbob display structure for species recognition. Although more work is needed, our findings support the proposition that interspecific variation in color and motion displays provides important cues for species recogntition in anoles.

The Incomplete Guide To The Wildlife Of Saint Martin

yokoyamaMark Yokoyama’s second edition is now out, and available for download for free. Or, if you want to go old school, hard copies are available for purchase on Amazon.

The 128 page guide covers both the native and introduced fauna of Saint Martin, with more than 500 photographs and considerable treatment of invertebrates as well as vertebrates.

Of course, the most important subject of the book are the anoles, two native and two introduced, each of which gets a page. Mark has published previously on the introduced anolesA. sagrei and A. cristatellus. Both for the moment are restricted in range–to a resort complex and a cruise ship terminal,  respectively. If they expand their ranges–and I’m betting they will–it will be interesting to see how they interact with the native A. gingivinus, as well as each other.

The image below on A. pogus will give you a feel for the book. Certainly a must-have if you’re going to St. Martin, and a nice-to-have even if you aren’t.

pogus

The Asian Twig Anole

Cophotis ceylanica. Photo by M. Wickramasinghe

Cophotis ceylanica. Photo by M. Wickramasinghe

It’s got a dewlap, too!

Those upstart Asian agamids are at it again, trying to out-anole anoles. We’ve already marveled at the dewlap of Sitana and its friends, which—I hesitate to say this—makes any anole dewlap look bland by comparison. Now can we all agree that this guy here, Cophotis ceylandica, is a twig anole’s twig anole?

Any way, the photo comes from a new paper that reports an observation of a jungle crow in a Sri Lankan park catching one of these guys, tearing it in half (grutesome!) and then eating it. And then it did it again three more times in the next half hour, two more C. ceylandica and a third, unidentified lizard. This was just one bird in a flock of 37, and guards at the park say they are quite prolific lizard catchers. The authors make the interesting point that jungle crow populations in the park appeared to have grown as a result of all of the garbage, and an incidental victim of this may be lizard populations.

German speakers, we need you again. Can you look at the attached paper and confirm that the two parts are German and English versions of the same text?

New Specimens Of The Interesting Anolis Salvini

salvini

In an interesting new paper in the journal Checklist (subtitled, the “journal of “species lists and distribution”), Bienentreu et al. report on 28 new specimens of A. salvini from western Panama.  On its face, the paper is simply a description of many new specimens of a little known species. But lurking within are a variety of fascinating tidbits.

First, A. salvini is a member of the pentaprion clade of twig anole-like mainland species. The authors note that previous work by Köhler subsumed A. vociferans into A. salvini, but no one seems to have noticed—maybe this paper will help.

Second, and perhaps most interesting, the authors note extensive variation in dewlap color within this species, as illustrated in the figure above: e-h are males, and i-l are females.This variation is striking and worthy of further investigation.

Lastly, third, the authors note that the species vocalizes when handled, and even provide a spectrogram. Very few anoles make sounds, a topic which has received very little attention.

distress call

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