JMIH 2017: Nobody Gets Tired of Looking for Anoles!

Amy Yackely Adams presents at JMIH 2017.

Amy Yackel Adams presents at JMIH 2017.

All anole field biologists have been there, right? It’s the middle of the night, and you’re walking around the forest searching for sleeping lizards in the trees. You’re probably wearing a headlamp, so the bugs are flying around your face, and your eyes start to strain as you get sleepy and you’re entering hour three or four of the search. This searcher fatigue could lead to the kinds of unintentional bias that can interfere with our research. But there’s good news when it comes to anoles, as Amy Yackel Adams, a statistician with the USGS in Fort Collins, Colorado, reported on the last day of JMIH.

Dr. Yackel Adams works with a Rapid Response Team whose goal is to prevent the spread of the worst invasive species. When a report came in of a sighting of a brown tree snake on the island of Saipan (in the Northern Mariana Islands, western Pacific Ocean), the team of experienced herpers deployed to Saipan and began intensive nightly surveys to assess the possibility of a brown tree snake population there.  Luckily, they didn’t find any of these snakes in the surveys, but they did log 20,000+ sightings of other vertebrates! These included emerald tree skinks, several species of geckos, a variety of small mammals, and the green anole (Anolis carolinensis). Dr. Yackel Adams saw an opportunity to use this rich dataset to statistically test for two types of bias that could occur in such surveys – searcher fatigue (both across the 4-hour nightly searches, and across the up-to-31 day deployment), and searcher bias in taxon detection.

The team of 29 searchers covered a total of 387 km of transects during the 31 days, and found a total of 5,800 sleeping green anoles during this time. (Wow!!) In terms of short-term searcher fatigue, there was a slight decrease in tree skink and mammal sightings as the night progresses, and gecko sightings were generally stable over the night, but far MORE green anoles were sighted in the later hours of the night. And over the long term, skinks and anoles were MORE likely to be detected the more nights a searcher worked, and there was no evidence of long-term searcher fatigue.  So, that’s why my take-home message was “nobody gets tired of looking for anoles!”

There was, however, significant taxonomic bias among the searchers – for example, the skink-to-anole sighting ratios ranged from 0.86 to 9.5. Dr. Yackel Adams concluded that this type of bias could be a real problem for certain kinds of studies, and we should be aware that differences among sightings by our survey team members could be potentially problematic in statistical analyses.

If West Indian Weevils Colonized the Mainland 19 Million Years Ago, Were Norops Anoles Along for the Ride?

Exophthalmus scalaris. Credit: symbiota4.acis.ufl.edu/scan

Exophthalmus scalaris. Credit: symbiota4.acis.ufl.edu/scan

In their 2008 review  “Are islands the end of the colonisation road?” Bellemain and Ricklefs (2008) concluded that oceanic islands could be important sources of colonisation of mainland continental areas and cited anoles of the Norops clade as a notable success. There are more than 5 times as many Norops clade species in Central and northern South America as in the West Indies; the 23 extant Caribbean species in the clade are distributed in Cuba and Jamaica with one species in Grand Cayman (Nicholson et al, 2005). Data in Nicholson et al (2005) gave support to the reverse colonisation hypothesis, but did not offer specific dating for the colonisation.

New analyses of 65 species in the Exophthalmus weevil genus complex (Zhang et al 2017) have turned up results that are of significance in understanding the biogeographic history of Caribbean anole dispersal and diversification. Like anoles of the Norops clade, the weevils show reverse colonization (island-to-continent), with diversification on the mainland and diversification within the islands. The data also give some support for overwater dispersal as the factor best explaining ancient between-island distribution.

Zhang et al’s best fit biogeographic model gives an estimate of 19Ma for a jump dispersal of Exophthalmus, most likely from Hispaniola,  which went on to diversify into more than 40 species in Central America.   So – did the anoles and the weevils make their journeys to the mainland around the same time and under similar conditions? Can this weevil study and the techniques it uses to arrive at its conclusions inform anole evolution and dispersal?

References

Bellemain, E and RE Ricklefs (2008) Are islands the end of the colonisation road? Trends Ecol Evol. 2008 Aug; 23(8):461-8. doi: 0.1016/j.tree.2008.05.001. Epub 2008 Jun 26.   (Correction to citation numbering: Trends Ecol Evol. 2008 Oct; 23(10):536-7).

Nicholson, KE, RE Glor, JJ Kolbe, A Larson, S Blair Hedges, JB Losos (2005) Mainland colonization by island lizards.  Journal of Biogeography 32 (6), 929-938.

Zhang, G, U Basharat, N Matzke, NM Franz (2017) Model selection in statistical historical biogeography of Neotropical insects—The Exophthalmus genus complex (Curculionidae: Entiminae). Molecular Phylogenetics and Evolution, 109, 226-239. DOI: 10.1016/j.ympev.2016.12.039.

JMIH 2017: Brown Anoles Thrive under Artificial Night Light

Chris Thawley presents at JMIH 2017.

Chris Thawley presents at JMIH 2017.

For most of the history of life on earth, the only sources of light at night were the moon and stars. Yet with the invention and rapid spread of electric light, species around the world now face a novel evolutionary pressure: artificial light at night, or ALAN. Artificial light likely has an especially strong effect on animals in city habitats, such as the urban-adapted brown anole lizard, Anolis sagrei. Chris Thawley and Jason Kolbe at the University of Rhode Island set out to determine whether brown anoles were negatively impacted by ALAN.

In addition to their abundance in urban environments, brown anoles are a particularly good species for this study.  Previous studies of brown anoles have shown that photoperiod influences the onset of reproduction at the beginning of the breeding season, and that several behavioral traits change under artificial light. In addition, work by Moore and Menaker has shown that pineal production of melatonin in this species is significantly altered by photoperiod.  So, would ALAN influence brown anole growth and reproduction?

Chris and Jason collected lizards from south Florida and set up a lab experiment where some lizards experienced a normal photoperiod, and others were exposed to ALAN that mimicked landscape lighting. Their results were quite unexpected! ALAN actually increased female growth, resulted in eggs laid earlier in the season, and increased the reproductive output of small females – but did not affect the number or mass of eggs or hatchlings.  And, ALAN females did not exhibit more stress (measured via circulating corticosterone) than control females.

So are brown anoles just superlizards? Do they have no trade-offs that result from ALAN? Chris suggested that it’s possible that such trade-offs may appear in studies over a longer time period, or in traits not measured here. Or, perhaps ad libitum food and the absence of predators in the lab remove the costs of ALAN. Or, maybe these really are indefatigable lizards!

JMIH 2017: Removal of Curly-tailed Lizards Increases Survival of Urban Brown Anoles

CRodriguez_JMIH2017

Interspecific Interactions Between Two Species of Invasive Lizards in an Urban Environment; Camila Rodriguez-Barbosa and Steve Johnson

An extensive body of work has addressed the eco-evolutionary impacts of the Northern Curly-tailed Lizard (Leiocephalus carinatus) on Brown Anoles (Anolis sagrei) (much of it receiving coverage right here, here, and here on Anole Annals!). These species co-occur not only on many Caribbean islands where much of this research has taken place, but also within the urban matrix of southern Florida, where both species are introduced.

Camila Rodriguez-Barbosa and Steve Johnson investigated the impacts of curlies on brown anoles in shopping centers in southern Florida where both species were plentiful. Camila first collected baseline data on anole and curly populations at eight sites before embarking on a quest to eliminate curlies from four of her sites. Over the next four months, she removed over 300 (!) curlies from these sites, many of which had brown anole remains in their stomachs.

She found that this removal had serious consequences for brown anoles. Compared to anoles from shopping centers where curlies were unchanged, A. sagrei at removal sites experienced higher survival and consequently greater abundances. These anoles also shifted to lower perches once curlies were removed, mirroring results from previous work which show that the introduction of curlies leads to brown anoles occupying higher perches to escape this dangerous predator. Camila’s work suggests that brown anole/curly-tailed lizard interactions may be similar even in very different habitats and provides a fascinating look at lizard life (and death) in the urban sprawl of southern Florida.

JMIH 2017: Brown Anole Reproductive Output Varies Seasonally

TMitchell_JMIH2017

Tim Mitchell, Josh Hall, and Daniel Warner: Seasonal Shifts in Anolis sagrei Reproduction Invoke Challenges for Scientific Reproducibility

Sometimes a scientist just needs hundreds of hatchling anoles for an experiment. Tim Mitchell found himself in this position recently, and, like a good lizard ecologist, he started breeding colonies of anoles in the lab to produce eggs to incubate until hatching. As he created three different breeding colonies from brown anoles (Anolis sagrei) in central Florida, one each in February, June, and September, Tim found that he had also created an ideal situation in which to examine how the reproductive condition and output of brown anoles varies across the breeding season.

Tim, along with his coauthors Josh Hall and Dan Warner, found that females produced eggs with significantly greater mass later in the breeding season. These eggs took longer to produce than those earlier in the year (a greater interclutch interval), and the eggs resulted in hatchlings that had higher mass in relation to the weight of their eggs. These reproductive differences remained even after accounting for the fact that female anoles were also larger and heavier later in the year.

These findings suggest that female A. sagrei may shift their reproductive effort from producing a higher quantity of eggs (i.e., more, smaller eggs resulting in smaller hatchlings) in the beginning of the breeding season, to producing higher quality eggs (i.e., fewer, larger eggs resulting in larger offspring) later in the breeding season. Tim’s findings also stress the importance of investigating and accounting for seasonal differences when examining reproductive output in lizards.

 

JMIH 2017: Costa Rican Anole Ecology

JMIH

Greetings from Austin, Texas, and the Joint Meeting of Ichthylogists and Herpetologists! Chris Thawley and I have appointed ourselves to be your AA reporting team from JMIH, and we’re aiming to post updates from each of the 8 anole talks and posters at this meeting.

Brian Holt

Brian Folt

On the first day of the conference, there were two exciting talks on the ecology of Costa Rican anoles. The first was by Brian Folt, a graduate student in Craig Guyer’s lab at Auburn, who developed a model of predator-prey co-occurrence where one of the prey were anoles (Anolis (Norops) humilis) and the predators were…spiders?!  Yes, wandering spiders, or ctenids, can prey upon the small anoles on the forest floor. (The other putative prey were poison dart frogs, who have a relatively similar life history to anoles.) Brian performed an extensive field study in 14 plots at La Selva Biological Station, conducting visual encounter surveys for anoles, frogs, and spiders, and recording arthropods in leaf litter samples. He used two-species occupancy models to determine how prey were affected by the presence of the predator and by resource abundance in the leaf litter. The result? Anole occupancy was lower where spiders were absent, and the detection probability of anoles was higher when spiders were present and detected. This suggests that anoles are responding behaviorally, such that they may increase their vigilance when predators are around.

Michelle Thompson

Michelle Thompson

I then ran across the conference center to catch the next anole talk – a terrific presentation by Michelle Thompson, a graduate student in Maureen Donnelly’s lab at Florida International University. Michelle studied whether thermal quality differed across the stages of forest succession, and how that affected Anolis (Norops) humilis and A. (N.) limifrons distributions. She worked across transects of pasture, secondary forest, and old growth forest in both upland and riparian sites. Michelle measured the thermal quality of each habitat, the thermal preferences of the lizards, and the location and abundance of the lizards. She found that thermal quality was lowest in the pasture sites, as temperatures were frequently higher than the lizards prefer. Yet, in these pasture sites, riparian habitat with remnant trees provided a thermal refuge for the lizards. This kind of work can help us understand why and how species may respond differently to human-caused alterations in habitat structure and temperature in our changing world.

Stay tuned for updates from JMIH, and follow the #JMIH17 hashtag on twitter for more herp-related news!

Book Review Rebuttal: Are Honduran Anoles Overly Split?

Two years ago, McCranie and Kohler published The Anoles of Honduras: Systematics, Distribution, and Conservation(available on Amazon for under twenty bucks and downloadable for free on the Museum of Comparative Zoology website).

In turn, two mostly favorable reviews were published. However, one of the reviews, by Levi Gray, did question whether a number of anole species recognized from small distributions in Honduras should be recognized as valid species, rather than just as populations of species that are widespread throughout Central America.

Writing in Zootaxa, Randy McCranie has now responded to this point, forcefully arguing that the species should be recognized and challenging his critics to present their own data if they feel otherwise. You’ll have to read Gray’s review and McCranie’s rebuttal yourself to decide what you think. Gray made his skepticism clear, he also did clearly call for more research to address the question.

More on the Lizard Species Whose Dewlap Differs from One Side to the Other

dewlaps

These pages have previously told the tale of Anolis lineatus, the species whose dewlap is different on one side compared to the other. Now the work has been published in Breviora. Like all publications of the Museum of Comparative Zoology, the paper can be downloaded from the museum’s publications webpage.

The research project was actually explained in a delightful video put together by the three joint first authors, all of whom are headed to college this fall.

curious case

A Green Anole That’s Blue

Photo by Carissa Wickens

Photo by Carissa Wickens

Eileen Wickens, who just finished the fourth grade in north central Florida, is a lizard-catching machine and particularly adept at nabbing blue-colored green anoles (Anolis carolinensis). Here’s the story, relayed by her mom, Carissa:

The teal lizards do seem rare as we have only seen a few. We had one at our house last spring and the photo I sent you was taken at our horse teaching unit in Gainesville. We were running an equine behavior trial that day (we’re actually investigating startle phenotypes and genetics in our Quarter Horse herd), and I saw the lizard as we were packing up our gear. My daughter is very good at spotting and catching them, so we will definitely keep our eyes out and would be happy to provide a specimen for your genetic research if we can. I’ve attached the photo of the lizard we had at the house last spring. The green anoles are scare in our neighborhood and on campus compared to the brown anoles (short snouts with distinct, dorsal diamond or striped markings). They seem to far outnumber the greens. 

From our brief observations of those two blue lizards this past year it does not appear they turn the bright green you see on the other Carolina Anoles, but it would be good to observe them for a longer period of time to be certain. 

Local Adaptations and Signal Function in Sympatric Lizards

Figure 1 - Long-nosed (Gowidon longirostris) dragon performing a territorial.

Figure 1 – Long-nosed (Gowidon longirostris) dragon performing a territorial.

In the Greater Antilles, lizard radiations have produced the same suite of ecomorphs on different islands as a consequence of adaptations to similar environments. In the same way, species that use motion-based signals, and occur in sympatry, would be expected to develop similar adaptations to enhance signal efficacy as they are frequently exposed to the same environment (e.g. background noise). Additionally, sympatric species often develop mechanisms to ensure they can distinguish between conspecifics and heterospecifics, particularly if they are closely related. This means that potentially opposing selective pressures might be at work for such systems.

Agamid lizards are widespread across the Australian mainland, and species distributions regularly overlap, especially in arid and rocky habitats. We analysed the motion-based signals of two pairs of sympatric species of Australian agamids to consider how they maintain reliable communication, while at the same time they avoid misidentification during signalling interactions. We calculated the speed distributions of the motion produced by lizard signals, and also by the environment (i.e. background noise). We then compared these two sources of motion to obtain a measure of signal-noise contrast, which indicates how much the signals stand out from the background and is therefore a proxy for signal efficacy (see Ramos & Peters 2017a).

The ring-tailed dragon (Ctenophorus caudicinctus) and the long-nosed dragon (Gowidon longirostris; Figure 1) are often found in sympatry in south Northern Territory and southeast Western Australia, around gorges and rocky outcrops. We recorded territorial displays at West MacDonnell National Park, in Northern Territory. The two species differed in display complexity (example of displays by all four species) and motor pattern use, as well as overall morphology (Figure 2). Interestingly, the speeds produced during their displays (Figure 3) and their signal-noise contrast scores were strikingly similar. Not only that, but their scores indicate that the signals from both species are highly effective in the context of the plant environment. These results demonstrate similar adaptations to their shared environment, while maintaining species recognition cues through morphology and overall display appearance.

The core motor patterns refer to HB = head bob, LW = limb wave, PU = push up, TC = tail coil, and TF = tail flick (Ramos and Peters 2016). Ctenophorus caudicinctus has been observed performing limb waves, but this motor pattern is not present during its territorial displays. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

Figure 2 – Habitat, average snout-vent length and known repertoire of core motor patterns for both species pairs. The core motor patterns refer to HB = head bob, LW = limb wave, PU = push up, TC = tail coil, and TF = tail flick. Ctenophorus caudicinctus has been observed performing limb waves, but this motor pattern is not present during its territorial displays. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

The military mallee dragon (Ctenophorus fordi) and the painted dragon (Ctenophorus pictus) are very common in arid and semiarid sandy areas of northwest Victoria, South Australia, and southwest Queensland. We recorded displays at Ngarkat Conservation Park in South Australia, where they are often found in sympatry. These two species are much closer in appearance, but their display complexity and motor pattern use were just as contrasting as in the previous pair of lizards (Figure 2). In addition, the speeds produced during their displays and their signal-noise contrast scores were considerably higher in the painted dragon (Figure 3). We suggest this difference is related to the lack of territoriality in mallee dragons. This species is not known to protect territories or perform aggressive displays, so the motivation to produce conspicuous signals is likely to be reduced compare to its territorial relatives.

Figure 2 - Comparisons of the motion speed distributions for all species. Kernel density functions for a) Ctenophorus caudicinctus (red) and Gowidon longirostris (black), and b) C. fordi (red) and C. pictus (black), averaged within species. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

Figure 3 – Comparisons of the motion speed distributions for all species. Kernel density functions for a) Ctenophorus caudicinctus (red) and Gowidon longirostris (black), and b) C. fordi (red) and C. pictus (black), averaged within species. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

In this study we were able to show that the ring-tailed and long-nosed dragon perform displays with almost identical motion speed distributions and signal-noise contrast scores, despite utilising very different territorial displays (see Ramos & Peters 2017b for more details). In the case of the other sympatric pair, motion speed distributions and signal-noise contrast scores appeared to be much higher in the painted dragon than in the non-territorial mallee dragon. This difference in social behaviour could be key to explaining why the signals of the sympatric C. caudicinctus and G. longirostris seem equally well adapted to their local environmental noise, as evidenced by their equally high signal-noise contrast scores, but the signals produced by C. fordi and C. pictus do not. Thus, the selective pressure to generate signals with high efficacy appears to be mediated by signal function, at least in this context.

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