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.
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.
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.
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.
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 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.
For the past eight years, my lab has conducted intensive research on green anoles (Anolis carolinensis) in Palmetto State Park in Luling, Texas, about an hour east of San Antonio. This park is beautiful – it’s centered around a swampy area dominated by dwarf palmettos (Sabal minor), and the San Marcos River flows through it. We’ve marked lizards and mapped their home ranges, watched their behavior, measured their morphology and parasite loads, and so much more. In past years, we’ve calculated that the density of green anoles in the park is approximately 0.04 lizards/m2, or about four adult lizards in every 10m x 10m area. We could regularly get sample sizes of around 150 lizards for behavioral studies in the park, but we very rarely collected animals from the park – we left them where we found them!
But this year is different. On three field trips to the park this summer, we have found very few green anoles. On our first visit this year in May, we spent 16 person-hours searching for lizards and found four green anoles. On our second visit in early June, we spent 14 person-hours searching and found eight. Last week, we spent another 12 person-hours and found only two. We see green anoles all over the city of San Antonio, and the students in my team are all skilled lizard spotters and catchers, so this isn’t due to inexperience. Also, we see other species of lizards all over the park – most commonly, Texas spiny lizards, little brown skinks, and house geckos– as well as garter snakes, copperheads, and cottonmouths. We also see tons of frogs.
Garter snake eating a tree frog, at Palmetto State Park. Other herps are thriving there!
So what happened to the anoles? We’ve considered a number of possibilities. The first thing we thought of was the possibility of feral cats – but we haven’t seen any cats in the park, and we think cats should have the same effect on the other herp species. What if the insect population had crashed? But again, that would affect the other lizards, snakes, and frogs too. This isn’t a year of particular drought or excess rain (and in previous wet and dry years, we’ve still seen lots of anoles), and the vegetation throughout the park largely looks the same as it has in the past. Perhaps an anole-specific disease has spread through this population?
In any case, the paucity of anoles in the park this year suggests that there won’t be many next year either, as there’s almost no one around laying eggs. It’s a bummer, because we’ve had such success here in the past.
Any ideas to explain this, AA readers?
Work we’ve published from our previous research in Palmetto State Park:
Dill, A.K., T.J. Sanger, A.C. Battles and M.A. Johnson. 2013. Sexual dimorphisms in habitat-specific morphology and behavior in the green anole lizard. Journal of Zoology 290: 135-142.
Battles, A.C., T.K. Whittle, C.M. Stehle, and M.A. Johnson. 2013. Effects of human land use on prey availability and body condition in the green anole lizard, Anolis carolinensis. Herpetological Conservation and Biology 8: 16-26.
Bush, J.M., M.M. Quinn, E.C. Balreira, and M.A. Johnson. 2016. How do lizards determine dominance? Applying ranking algorithms to animal social behavior. Animal Behaviour 118: 65-74.
Stehle, C.M., A.C. Battles, M.N. Sparks, and M.A. Johnson. In revision. Prey availability affects territory size, but not territorial display behavior, in green anole lizards. Acta Oecologica.
Late Breaking: one last Evolution 2017 post! Last weekend during the Evolution meeting, I had a chance to chat with Iris Holmes (Ph.D. student, University of Michigan) about the poster she presented. Initially not on our watch list because of the lack of “anole” in the description, my eye caught the dewlapping lizard perched at the top of her poster from across the room.
Iris presented her work on gut microbiomes of two groups of lizards: anoles and ameivas. She wanted to know if different taxa have different gut microbiomes and to what extent diet influences bacterial composition of gut microbiomes. Her collaborator (Ivan Monagan) collected scat samples from 22 Anolis dollfusianus and 9 Ameiva from an agricultural area in the Soconosco region of Chiapas, Mexico. Together, they then sequenced both the gut bacteria and the digesting prey with two 16S primers. Iris chose to target the prey as well because she wanted to know if they were eating different things and how different stages of digestion influence gut bacteria communities.
Iris found that there were no clear differences between the gut microbiomes of anoles and ameivas. Both species had gut microbiomes dominated by three main phyla: Proteobacteria, Firmicutes, and Bacteroidetes. Little is currently known about how these bacteria relate to digestion and health in reptiles, but Iris commented that we can make some guesses based on studies in other taxa. Proteobacteria are a disease indicator in mammals, but appear to be normal in reptiles and birds. Firmicutes and Bacteroidetes are both important for digestion of carbohydrates and fats (respectively) in mammals. Iris found that there was a loose correlation between the amount of prey consumed and the abundance of Bacteroidetes, suggesting these bacteria also play a role in digestion in lizards. She also found that there was an apparent tradeoff between the Proteobacteria and the two other groups – sequence abundance of proteobacteria was negatively correlated with abundance of Bacteroidetes and Firmicutes. Overall, this is an interesting first step in understanding the gut microbiomes of reptiles and how they differ (or don’t) between groups.
I’m hoping that some of you out there have been collecting Basal Metabolic Rate or Resting Metabolic Rate data on Caribbean anoles!
I’m working with a group of scientists on a large-scale comparative database on circulating hormones in free-living vertebrates – we call our collaboration HormoneBase – and we’re hoping to look at relationships between hormone levels and metabolism. (We’ll be presenting some of this work at the Society of Integrative and Comparative Biology meeting in January 2018 – check out our symposium announcement here!) We have a good list of anole species in the database, thanks to the work of Jerry Husak and Matt Lovern (2014), but it seems that very little metabolism rate data are available for these species. Do you know of such data, or do you have them – published or unpublished? If so, please contact me (mjohnso9@trinity.edu)!
Reference:
Husak JF and MB Lovern. 2014. Variation in steroid hormone levels among Caribbean Anolis lizards: endocrine system convergence? Hormones and Behavior 65:408-415.
Figure 1. Landmarks (black point circled in white) and sliding landmarks (black points) used in the geometric morphometric analysis.
The knowledge of the past squamate fauna of the Guadeloupe islands (French Lesser Antilles) dramatically increased these last years in the framework of two European paleontological research programs. New archaeological and paleontological excavations (about which I previously talked) have been conducted and led to the discovery of thousands of squamate remains allowing to complete the pioneering works conducted by G. K. Pregill in the 90’s (Pregill et al., 1994). Results obtained on iguanas (Bochaton et al., 2016b), galliwasps (Bochaton et al., 2016a), ameivas (Bochaton et al., 2017a) and other taxa (Bailon et al., 2015; Bochaton et al., 2015; Boudadi-Maligne et al., 2016) point to high extirpation and extinction rates, mainly taking place during the last centuries after the European colonization of the archipelago and probably in relation to introduction of exogenous competitors and predators, as well as the practice of intensive agriculture.
In the middle of all of these extinctions, anoles, which are still very common in Guadeloupe, appeared to be kind of indestructible and were apparently not impacted at all by recent anthropogenic disturbances. However, the study of a huge assemblage of anole remains from Marie-Galante Island dated from Late Pleistocene to the 14th century reveals that this first impression was far from true.
Nearly 30,000 anole remains coming from several deposits were investigated using a combination of morphological and morphometric approaches. Size estimations (see Bochaton, 2016; Bochaton and Kemp, 2017) indicate that whatever the stratigraphic layer they come from, fully mature individuals range in three groups of Snout-Vent Length (SVL) size (Figure 2).
Figure 2. SVL reconstructed on the basis of fully mature humeri (N = 66) with the results of a mixture analysis indicating a trimodal distribution. MTMS1, minimal theoretical maximal size obtained from the smallest fully mature humerus; MTMS 2, minimal theoretical maximal size obtained from the largest immature humerus; MTMS 3, minimal theoretical maximal size obtained from the smallest mature humerus included in the intermediately sized group.
These SVLs partly match those of the females (max 75mm SVL) and males (max 120 mm SVL) of the modern solitary Marie-Galante anole (Anolis ferreus). However, a third group of fossil specimens of very large size reaching 150mm SVL also occurred in the deposits and has no modern counterpart on the island. Still, morphological analysis indicates that these large specimens were also A. ferreus. A geometric morphometric analysis (Figure 1, above) was also conducted on dentaries of Marie-Galant fossils and included in a modern sample of Lesser Antillean anoles.
Figure 3. Two first axes of the PCA conducted on shape data collected for fossil and modern A. ferreus dentaries showing a diminution of morphological variability between fossil and modern anoles.
This analysis reveals a strong heterogeneity of the morphology of the dentary mostly depending of their size (allometry). The three fossil size groups are however closer to modern A. ferreus than to any other modern taxa and are linked by a common allometric relationship between their size and shape which differs from modern A. ferreus. The morphological variability of the fossil dentaries is also higher than that of modern A. ferreus (Figure 3).
These results indicate that all fossils are likely to correspond to A. ferreus. However, fossil representatives are more morphologically variable in terms of size, shape, and allometry than modern A. ferreus.The morphology of fossil A. ferreus remained stable during more than 30,000 years before an abrupt change that occurred during the last centuries. There is, however, a void of fossil data during the modern period which precludes linking this reduction of morphological variability between fossil and modern A. ferreus to a distinct event. Yet, this phenomenon is contemporaneous to the numerous extinction events documented on Marie-Galante and is thus very likely to be also related to the anthropization of the island.
This study also provides a strong argument again the hypothesis of the past occurrence of a second anole species smaller than modern A. ferreus on Marie-Galante and used to explain the large size reached nowadays by this insular solitary anole.
More details can be found in the publication of this work:
Bailon, S., C. Bochaton, and A. Lenoble. 2015. New data on Pleistocene and Holocene herpetofauna of Marie-Galante (Blanchard Cave, Guadeloupe Islands, French West Indies): Insular faunal turnover and human impact. Quaternary Science Reviews 128:127–137.
Bochaton, C. 2016. Describing archaeological Iguana Laurenti, 1768 (Squamata: Iguanidae) populations: size and skeletal maturity. International Journal of Osteoarchaeology 26:716–724.
Bochaton, C., and M. E. Kemp. 2017. Reconstructing the body sizes of Quaternary lizards using Pholidoscelis Fitzinger, 1843 and Anolis Daudin, 1802 as case studies. Journal of Vertebrate Paleontology 37:e1239626.
Bochaton, C., R. Boistel, F. Cassagrande, S. Grouard, and S. Bailon. 2016a. A fossil Diploglossus (Squamata, Anguidae) lizard from Basse-Terre and Grande-Terre islands (Guadeloupe, French West-Indies). Scientific Report 28475:1–12.
Bochaton, C., S. Grouard, R. Cornette, I. Ineich, A. Tresset, and S. Bailon. 2015. Fossil and subfossil herpetofauna from Cadet 2 Cave (Marie-Galante, Guadeloupe Islands, F. W. I.): Evolution of an insular herpetofauna since the Late Pleistocene. Comptes Rendus Palévol 14:101–110.
Bochaton, C., S. Bailon, I. Ineich, M. Breuil, A. Tresset, and S. Grouard. 2016b. From a thriving past to an uncertain future: Zooarchaeological evidence of two millennia of human impact on a large emblematic lizard (Iguana delicatissima) on the Guadeloupe Islands (French West Indies). Quaternary Science Reviews 150:172–183.
Bochaton, C., R. Boistel, S. Grouard, I. Ineich, A. Tresset, and S. Bailon. 2017a. Evolution, diversity and interactions with past human populations of recently extinct Pholidoscelis lizards (Squamata: Teiidae) from the Guadeloupe Islands (French West-Indies). Historical Biology.
Boudadi-Maligne, M., S. Bailon, C. Bochaton, F. Cassagrande, S. Grouard, N. Serrand, and A. Lenoble. 2016. Evidence for historical human-induced extinctions of vertebrate species on La Désirade (French West Indies). Quaternary Research 85:54–65.
Pregill, G. K., D. W. Steadman, and D. R. Watters. 1994. Late Quaternary vertebrate faunas of the Lesser Antilles: historical components of Caribbean biogeography. Bulletin of Carnegie Museum of Natural History 30:1–51.
Major Anole Annals contributor Martha Muñoz gave a brilliant talk at the Evolution meeting as an awardee of a well-deserved ‘Young Investigator’ award from the American Society of Naturalists. In her talk, Muñoz discussed how two classic papers by Janzen (1967) and Huey et al. (2003) influenced the way she thinks about the interplay between behavior, physiology, and evolution. Not surprisingly, Anolis lizards played a leading role in her exposition.
Martha Muñoz introduces the Cybotoid Anoles.
Martha’s talk, entitled “Janzen’s hypothesis meets the Bogert effect: a synthesis nearly 100 years in the making”, started by describing Janzen’s hypothesis. In short, Janzen (1967) predicted that physiological differences among populations across altitudinal bands would be stronger in tropical mountains than in temperate ones. The main argument was that populations can more easily adapt to a given temperature range in tropical environments because these ranges are stable throughout the year, whereas the temperatures of different altitudinal bands overlap more in temperate areas due to seasonal variation.
Martha explains how day and night temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.
Expanding on Janzen’s idea, Muñoz hypothesized that diurnal and nocturnal temperature variation in a single tropical mountain could also generate differences in physiological divergence among lowland and highland populations. The idea was that daytime temperatures were variable with overlap across elevation (similar to the seasonal picture in temperate areas) and nighttime temperatures were more constant and differed between elevations (similar to the seasonal picture in tropical areas).
To test this, Martha sampled populations in the Dominican Republic at sites ranging in elevation from sea level to 2400m. She then analyzed heat and cold tolerance of several species of anoles from the Anolis cybotes group. Results on cold tolerance (CT min) seem to agree with Janzen’s hypothesis: cold tolerance strongly covaries with altitude at night, with higher elevation populations having lower critical thermal minimums. Interestingly, however, heat tolerance (measured as CT max) was not at all associated with elevation.
Why did Janzen’s hypothesis fail to explain the evolution of heat tolerance across the altitudinal range? This question led to a key point of Muñoz’s talk: Janzen’s hypothesis might fail to predict evolution of CT max because it is agnostic about behavior. In the case of ‘cybotoid’ anoles, lizards from different altitudes could actively adjust their habitat use to achieve optimal temperatures. As a consequence, thermoregulatory behavior could forestall evolution of physiology in heat tolerance. By studying habitat use across different elevations, Muñoz showed that, although anoles behave as thermo-conformers at low elevations, they clearly thermoregulate at high elevations. In other words, anoles were at similar temperatures to the average available substrates in lowlands but their body temperatures were significantly higher than perches at higher elevation.
Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)
This was at least partially explained by habitat use differences: anoles at high elevations perched most frequently on boulders, which are on average about 5º C warmer than trees –the most used substrate in low altitudes. In fact, 90% of the trees Martha sampled at these high elevation sites were lower in temperature than the preferred temperature of the lizards! These data indicate that anoles from the A. cybotes group have buffered natural selection in physiology by means of behavioral adjustments –a phenomenon known as the Bogert effect (also called behavioral inertia; Bogert 1949).
Finally, the talk had a third part. And yes, it got even more interesting! Due to the observed habitat use differences in high latitudes, Muñoz and her collaborators predicted that although behavior could buffer physiological evolution on heat tolerance, it could spur evolutionary change in ecologically-relevant morphological traits (the behavioral drive hypothesis). Specifically, they predicted that increased use of boulders (for thermoregulation) at high elevations should drive morphological shifts in traits related to boulder use: head and limb morphology. They found evidence for these hypothesized morphological differences: high elevation lizards had higher head heights and longer hindlimb, in agreement with functional predictions. Finally, a captive breeding experiment confirmed that these differences were the consequence of genetic changes and not simply due to developmental plasticity.
Martha’s research is a great example of how, as Huey said, studying behavior can be crucial to improve our understanding of evolutionary processes. We are looking forward to hear about future research from the Muñoz lab, which is about to open at Virginia Tech!
Muñoz, M.M., Losos, J.B. Thermoregulation simultaneously promotes and forestalls evolution in a tropical lizard. (Accepted pending minor revision). American Naturalist.
In his Masters thesis conducted in Simon Lailvaux’s lab at the University of New Orleans and presented this week at Evolution 2017, David Weber used a multiyear data set of Anolis carolinensis lizards’ locations and morphology as well as a DNA-based pedigree to investigate the effects of body size and relatedness on the spatial distribution of these lizards. Specifically, he set out to test three hypotheses: first, are males’ home ranges larger than females’ home ranges? Second, are bigger males more likely to be surrounded by smaller males that are related to them? And third, is there any evidence for the inheritance of home ranges from parent to offspring?
Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.
Lizard locations were sampled in an urban New Orleans park twice a year, in the fall and in the spring, from 2010 to 2015. The dataset included over 800 individuals, and what struck me most about these data was that, of these 800+ individuals, fewer than 100 were observed often enough to estimate home range volumes–death and dispersal can rule these lizards’ lives! Male and female home range volumes did not differ significantly (and the trend was in the direction of females moving over larger areas, which concurs with data from Robert Gordon’s 1956 thesis on green anoles, but with little else, I think). Curiously, smaller neighbours of the biggest males were less related to them than were males found farther away, suggesting that male anoles don’t preferentially tolerate their kin over non-kin. And though philopatry (aka site fidelity aka staying the same place) was rare overall, females were a bit more likely to co-occur with their male offspring than males were. In a result that conforms to traditional wisdom, Weber found that the biggest males in the site seemed to avoid each other, potentially spacing themselves as far apart as possible.
Following a kind shout-out to my and Jonathan Losos’ recent paper on Anolis territoriality or the lack thereof, Weber chose to interpret his results as making sense only outside of a territorial framework. Unsurprisingly, I concur with this decision entirely, and am excited to see where Weber goes with this idea in the publications resulting from this mammoth dataset!
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).
