On march 19, 2013, Jonathan Losos wrote about Anolis heterodermus in this blog, on a post called “Adventures with Phenacosaurus”: “…I have to comment on the little-studied thermal biology of this species. The weather when we were there was usually overcast with the sun occasionally bursting out. Temperatures were usually in the 16-20̊ range. And the lizards were active! Moreover, we were at only about 2600 meters, but I have heard reports of them being found as high as 4000 meters! Clearly, a study on the thermal biology of this species would be fascinating!” One year later, I began to investigate this topic on A. heterodermus.
All my life I’ve loved reptiles, but only recently as part of my undergraduate studies in biology in the National University of Colombia, have I started in the herpetological world with Drs. Adriana Jerez and Martha Calderón. I was particularly intrigued by the thermal biology of these organisms. Soon I discovered that I’ve always lived in a high-elevation, cold city, Bogotá, in a neotropical country, Colombia, making the reptile species around me, which are ironically unknown, perfect models for questions about thermoregulation in reptiles.
A female Anolis heterodermus
As I tried to decide which of these species would be my model for my undergraduate thesis, I realized that my professors and some of my colleagues had already started to study some of the high-elevation species, like the high-Andean snake Atractus crassicaudatus, the microteiid Anadia bogotensis, and the collared tropidurids Stenocercus trachycephalus and S. lache. I realize now that my choice of the high-Andean lizard Anolis heterodermus for my study was one of the best decisions of my life as a biologist.
Between 2014 and 2015, I carried out my undergraduate thesis research under the direction of Dr. Martha Calderón on thermoregulation of Anolis heterodermus in Tabio, a town at 2650 m asl, close to Bogotá, Colombia. During my research, Martha, my colleagues and I had the opportunity to know Dr. Barry Sinervo and his group, who helped us with equipment and suggestions for our projects. Finally, in 2017, after my thesis was approved and I obtained my biology university degree, Martha and I published my first article.
Measuring an individual of Anolis heterodermus with calipers
Anolis heterodermus lives in a cold, low-quality thermal habitat that gets worse in wet seasons. Surprisingly, during the wet season, Anolis heterodermus copes succesfully with this seasonal variation and adjusts behaviorally to thermoregulate more actively to compensate for the reduction in the thermal quality of the habitat. In this way, these lizards match achieve their preferred temperatures just as in dry season. This match also occurs mostly at midday, particularly in sunny perch sites, confirmed by operative temperature data, which suggests that A. heterodermus is a heliothermic species. Additionally, sexes and ages are not different in their thermal traits, such as body and preference temperatures.
Study site: Tygüa Magüe Ecopark, Tabio, Colombia, at 2650 m asl.
But the most incredible trait of this species is its capacity to take advantage of the few sunny hours and sunny microhabitats to thermoregulate, taking into account that the tropical high-elevation ecosystems like the high-andean shrubs and forest, and subparamo and paramo not always are cold environments, but have large thermal fluctuation during the day too, which is reflected in the wide range of body (16.6-31.9°C) and preferred (19.1-30.2°C) temperatures. Definitely Anolis heterodermus is a very plastic thermoregulating species, as it has to be, because it is the anole species found at the highest altitude known.
Urbanization is intensifying worldwide, and while some species tolerate and even exploit urban environments, many others are excluded entirely from this new habitat. Understanding the factors that underlie tolerance of urbanization is thus of rapidly growing importance. Here, we examine urban tolerance across a diverse group of lizards: Caribbean members of the neotropical genus Anolis. Our analyses reveal that urban tolerance has strong phylogenetic signal, suggesting that closely related species tend to respond similarly to urban environments. We propose that this characteristic of urban tolerance in anoles may be used to forecast the possible responses of species to increasing urbanization. In addition, we identified several key ecological and morphological traits that tend to be associated with tolerance in Anolis. Specifically, species experiencing hot and dry conditions in their natural environment and those that maintain higher body temperatures tend to have greater tolerance of urban habitats. We also found that tolerance of urbanization is positively associated with toepad lamella number and negatively associated with ventral scale density and relative hindlimb length. The identification of factors that predispose a species to be more or less urban tolerant can provide a starting point for conservation and sustainable development in our increasingly urbanized world.
Reproductive physiology and behavior is mainly regulated by the hypothalamus-pituitary-gonad (HPG) axis, although abnormal thyroid hormone (TH) levels alter HPG axis activity. Seasonally breeding animals, such as green anole lizards (Anolis carolinensis), undergo drastic hormonal and behavioral changes between breeding and non-breeding seasons, with increased sex steroid hormones, larger gonads and increased reproductive behaviors during the breeding compared to non-breeding seasons. Relatively less is known regarding the regulation of gonadal TH in seasonal reproduction. We examined whether the gonadal expression of enzymes involved in TH activation are altered in concert with seasonal reproduction. Type 2 deiodinase (Dio2) mRNA, the TH activating enzyme, was upregulated in breeding compared to non-breeding testes, while type 3 deiodinase (Dio3) mRNA, the TH deactivating enzyme, was upregulated in breeding ovaries. To study the association between the HPG axis and local activation of TH, we manipulated the HPG axis during the non-breeding season by subcutaneously injecting luteinizing hormone (LH) and follicle stimulating hormone (FSH) in male lizards. We found that acute LH and FSH injections induced many aspects of breeding, with increased testes size and testosterone levels. Surprisingly, Dio3 was upregulated in the testes after LH and FSH injections, while Dio2 mRNA levels were unchanged. These results suggest that there might be different roles for local TH activation in developing and maintaining fully mature and functional gonads. Our findings continue to support the role for TH in regulating reproduction.
We are looking for a field assistant to help us conduct behavioural research on Anolis sagrei on small dredge-spoil islands near Ft. Pierce, FL, from April 22 to May 21. Daily activities include searching for and observing marked lizards as well as collecting habitat data. We will work long hours on most days (beginning 7-8am). Applicants should be prepared for hot and humid work conditions as well as travel on a small boat. Applicants must be comfortable handling lizards and using binoculars and should be adaptable to changing plans. All expenses (airfare, food, lodging) will be covered and a stipend will be provided.
If interested, please contact Ambika Kamath: ambikamath@gmail.com and Nick Herrmann: nicholas.carl.herrmann@gmail.com with a
brief letter describing why you are interested in this position and any relevant research experience along with your CV and the names and contact information of a professional reference whom we may contact by email. We will review applications as they arrive until the position is filled.
Vertebrate fossils embedded in amber represent a particularly valuable paleobiological record as amber is supposed to be a barrier to the environment, precluding significant alteration of the animals’ body over geological time. The mode and processes of amber preservation are still under debate, and it is questionable to what extent original material may be preserved. Due to their high value, vertebrates in amber have never been examined with analytical methods, which means that the composition of bone tissue in amber is unknown. Here, we report our results of a study on a left forelimb from a fossil Anolis sp. indet. (Squamata) that was fully embedded in Miocene Dominican amber. Our results show a transformation of the bioapatite to fluorapatite associated with a severe alteration of the collagen phase and the formation of an unidentified carbonate. These findings argue for a poor survival potential of macromolecules in Dominican amber fossils.
Stan Rand’s Super 8 Film from the 1972 Malpelo Expedition
Kevin de Queiroz
Research Zoologist and Curator of Amphibians and Reptiles
National Museum of Natural History, Smithsonian Institution
This film was made by Austin Stanley Rand (1932–2005), a biologist at the Smithsonian Tropical Research Institute (STRI) (1964–1997), during a six-day expedition to Malpelo Island, a small (1.2 km2), remote, oceanic island located some 500 km west of the Colombian mainland, in late February and early March of 1972. The Expedition involved 17 scientists from STRI, the republics of Colombia and Panamá, and several US universities, as well as the assistance of the United States Navy. The scientific findings of the Expedition were published in the series Smithsonian Contributions to Zoology (Number 176) in 1975, in a volume edited by Jeffrey B. Graham (1941–2011), one of the STRI biologists who participated in the Expedition. The volume contains 14 articles, five of which are on the lizards of Malpelo, including three on the endemic Anolisagassizi, two on the endemic Diploglossus millepunctatus (one of which is also on A. agassizi), and one describing a new endemic species of leaf-toed geckos, Phyllodactylus transversalis. As a result of prompting from George Gorman, who participated in the Expedition, and Jonathan Losos, I obtained a digital copy of the film from the Smithsonian Archives with the help of Archivist Ellen Alers. The film is a little under 11 minutes long and there is no audio. The notes about the contents of the film below were prepared mostly from information in the Malpelo Expedition Volume, with some additions based on web searches and input from George Gorman. Literature citations are for articles in the Smithsonian Contributions to Zoology Malpelo Expedition Volume unless otherwise indicated. Thanks to George Gorman and Ross Kiester for comments on an earlier version.
0:10: Adult male Anolis agassizi, Malpelo or Agassiz’s Anole. The species was named by Smithsonian Zoologist Leonard Stejneger in 1900 after Alexander Agassiz, leader of an 1891 Expedition aboard the USS Albatross that visited Malpelo and collected the first specimens.
0:20: Map showing the location of Malpelo Island (ca. 500 km west of mainland Colombia).
0:29: The USS York County (US Navy). This De Soto County-class Tank Landing Ship transported the Expedition participants from Panama to Malpelo and back.
0:32: Ship deck (the ship was decommissioned later that same year, 1972).
0:40: Crew members of the USS York (sweeping the deck).
0:46: A. Ross Kiester (Ph.D. 1975, Harvard University, Advisor: Ernest E. Williams; STRI Predoctoral Fellow, 1970–1971). Kiester authored a paper in the Malpelo Expedition Volume on the natural history of the endemic anguid lizard species Diploglossus millepunctatus.
0:53: George C. Gorman (Ph.D. 1968, Harvard University, Advisor: E. E. Williams; UCLA professor at the time of the Expedition) lying on deck. Gorman co-authored three articles in the Malpelo Expedition Volume, including one on the natural history, behavior and ecology of Anolis agassizi and another on the chromosomes of Anolis agassizi and Diploglossus millepunctatus.
1:00: Several Anolis agassizi licking a cut orange. The anoles are very abundant on the island. In the Malpelo Expedition Volume, Rand et al. (1975) estimated the population density to be 1 anole/5-10 square meters and a total population of at least 100,000 anoles on the small island.
1:11: Malpelo Island from the southeast (?).
1:20: Part of island closer up. The sides are very steep and landing is difficult.
1:27: Close-up of rock (island surface). The island is composed primarily of igneous rock and is of volcanic origin. Very few large (vascular) plants occur there, though several species of mosses and lichens are present.
1:33: Aerial view of island (from the northwest). The Expedition produced a new map of the island (see Kiester and Hoffman, 1975).
1:39: Map showing the topography of the ocean floor. Malpelo is part of Malpelo Ridge and is the only island on that ridge.
1:45: Nazca Booby (Sula granti). This is most abundant breeding bird species on Malpelo (Pitman et al., 1995, The marine birds of Malpelo Island, Colombia. Colonial Waterbirds 18:113–119, wherein it is called Sula dactylatra). The population was estimated by Pitman et al. (1995) to be 24,000 individuals. Referred to in the Malpelo Expedition Volume as Masked or Blue-faced Boobies, Sula dactylatra granti.
1:50: Seabirds flying. Other bird species known from Malpelo include Red-billed Tropicbirds, Red-footed Boobies, Black and Brown Noddies, White Terns, and Great and Magnificent Frigatebirds (Pitman et al., 1995).
2:00: Diploglossus millepunctatus, a Dotted or Malpelo Galliwasp. This is an anguid lizard species endemic to Malpelo.
2:02: Preserved specimens of Phyllodactylus transversalis, Malpelo Leaf-toed Geckos. This was a new species discovered on the Malpelo Expedition and described in the Malpelo Expedition Volume by Raymond B. Huey (Ph.D. 1976; Harvard University, Advisor: Ernest E. Williams).
2:06: This shot seems to show the abundance of anoles in a small area. Anolis agassizi was found not to be territorial, unlike most of its close relatives, and to exhibit relatively little intraspecific aggression.
2:21: Anole on a camera illustrating tameness and/or curiosity. Rand et al. reported that they often approached observers and unusual objects.
2:24: Clipboard with a map of Malpelo showing the routes taken by the exploration party (compare with Figure 4 in Kiester and Hoffman, 1975).
2:26: Anoles in a scuffle (chase and display).
2:32: Anoles on equipment (again showing abundance and curiosity).
2:37: Anoles at orange, licking, numerous individuals. Oranges were put out after the researchers noticed that the anoles seemed attracted to the color orange (Kodak film package, cap of suntan lotion container). The anoles normally eat insects, primarily ants and beetles (Rand et al., 1975).
3:21: Large marked male anole performing a headbob display. Marking was used to estimate home ranges.
3:30: More headbobs (different individual?). This is a typical anole display. The Malpelo anoles performed it infrequently compared to other anole species.
3:37: Large marked male A. agassizi performing more head bobs and dewlap extension. Malpelo anoles have relatively small dewlaps.
3:50: Attacks another male.
3:53: Nuchal crest and dewlap extended. This species has a relatively small dewlap, likely related to its lack of territoriality and reduced aggression.
4:04: Two males displaying and biting. The closer one appears to be tethered.
4:15: Males with jaws locked. Despite these cases, at least some of which appear to involve instigation by the researchers, aggression was found to be low in this species (Rand et al., 1975).
4:21: Male anole. Rosario Castañeda (2010, Ph. D. dissertation, George Washington University) found A. agassizi to be ecomorphologically divergent from other Dactyloa-clade species in having an exceptionally large number of toepad lamellae.
4:31: Anoles (some of which are marked) at orange. Note that the anoles do not attempt to monopolize this resource by displaying at each other or chasing each other away (Rand et al., 1975). The larger ones with the black heads are males.
4:47: Series of preserved Anolis agassizi specimens. No hatchlings were found during the Expedition, suggesting seasonal reproduction (Rand et al., 1975).
4:57: Dissected Anolis specimen showing testes. Probably one of the large males with a black head and nuchal crest.
5:02: Dissected Anolis specimen showing an egg. A little over 50% of the sampled females had oviducal eggs or enlarging follicles (Rand et al., 1975).
5:06: Testes again. Rand et al. (1975) found that some large males lack male secondary sexual characters (black head and erect nuchal crest) and have regressed testes (obviously, this isn’t one of them).
5:11: Back at the orange. The anoles both lick and bite the orange.
5:28: Dissected gut cavity. Possibly showing fat bodies or perhaps this is the male morph with regressed testes or perhaps showing the darkly pigmented peritoneum, a characteristic of lizards that live in areas of high insolation (Rand et al., 1975).
5:35: Back at the orange again.
5:51: Part of island with ocean in background (and birds). The shot pans to a small boat that was presumably used to transport the researchers to the island from the large ship.
6:02: Endemic Malpelo land crab, Johngarthia malpilensis. (Referred to in the Malpelo Expedition Volume as Gecarcinus malpilensis.)
6:08: Crab interaction with Diploglossus. D. millepunctutus is one of the largest anguids and one of the largest Diploglossus species. It is known to feed on dead crabs (Kiester, 1975).
6:24: Anolis agassizi male (marked).
6:30: A researcher tying a hookless fishing fly on fishing line. Ross Kiester thinks that the researcher may be William M. Rand, brother of A. Stanley Rand and co-author of the article on Anolis agassizi in the Malpelo Expedition Volume (Rand et al., 1975).
6:33: Anoles trying to capture the fly. Malpelo anoles are known to eat real flies (Diptera).
6:45: Anoles with green chuckles candy. The “Chuckles Experiment” was undertaken to test for a color preference (Rand et al., 1975). The results indicated a preference for orange and yellow Chuckles candies over red and green ones and even more so over black ones. Rand et al. speculated that this preference could be related to feeding on the yolks of broken seabird eggs.
6:52: Setting out red Chuckles candy.
6:54: Anoles on rock (more Chuckles).
6:59: Anole with red and orange Chuckles candies.
7:15: This sequence shows anoles drinking from a crevice, as reported in the Malpelo Expedition Volume by Rand et al. (1975). There are many small seeps, springs and rock pools on the island (Rand et al., 1975). Other experiments have shown that Malpelo anoles are not particularly tolerant of water loss (Rand et al., 1975).
7:43: More drinking.
7:57: Taking body temperature via the cloaca (a standard herpetological method). Rand et al. (1975) found that A. agassizi exhibits similar body-temperature preferences to other anoles.
8:05: Part of island (from boat?).
8:10: Anole runs and stops in the shade. Anoles were active during most of the day in the shade and didn’t spend much time basking (Rand et al., 1975).
8:24: Back at the half orange.
8:38: Anoles flee and a Diploglossus approaches. The Galliwasp is known to prey on anoles, but anoles are not its primary food source (Rand et al., 1975). On the other hand, Rand et al. reported that 85% of the Malpelo Anoles had regenerated tails.
8:49: Anoles.
8:52: Diploglossus departs. This is probably the individual mentioned by Rand et al. (1975) that repeatedly approached the orange when anoles were present, but did not eat the orange.
8:57: Large male anole moving up rock.
9:05: Diploglossus millepunctatus.
9:09: Anole running.
9:12: Diploglossus running. I assume that the anole is running from the galliwasp rather than the other way around.
9:17: Land crab (Johngarthia malpilensis).
9:20: Land crab and Diploglossus. Malpelo Galliwasps are known to feed on dead crabs (Kiester, 1975).
9:26: Nazca Boobies (Sula granti), adult and chick.
9:28: Diploglossusmillepunctatus. Kiester (1975) reported that when a booby chick squawks upon return of the parent to the nest, nearby galliwasps immediately run to the vicinity of the birds and will snatch and eat any fishes that are dropped.
9:33: Nazca Boobies (adult and chick) again.
9:36: Diploglossus eating a crab claw.
9:40: Two Diploglossus eating a dead crab.
9:46: Anoles back at the half orange (zoom out).
10:20: Close up of anoles at orange again.
10:40: Different shot of anoles at orange (some dart in and out).
In August 2019, while feeding a captive colony of brown anoles (Anolis sagrei) in Dr. Daniel Warner’s lab at Auburn University, I noticed a female anole crouching on the side of her nesting pot. Upon closer inspection, I realized she had dug a hole in the soil and was perched above it- apparently preparing to lay an egg. Gently prying up the lid of the cage, I snapped a few photos of this (somewhat still mysterious) event.
During the subsequent observations of this female in the lab, she laid an egg on the topsoil; however, jumping from the nesting pot, she knocked the freshly oviposited egg into the hole she created. She then returned to the nesting pot and looked to be positioning the egg within the hole (see video attached). This behavior has been previously documented in Anolis species (Propper et al. 1991; Stamps 1976) and suggests that females may provide additional influence on offspring survival and phenotype through egg-positioning.
Nest sites are critically important for embryonic development and resulting offspring phenotype (Tiatragul et al. 2019; Reedy, Zaragoza, and Warner 2013). The sequence of nesting events (i.e., oviposition, “egg-rolling” [Tokarz and Jones 1979]) may also assist females in choosing a nest-site that will maximize the survival of her offspring. While female nesting behavior has long been documented in scientific literature, it was interesting to see such (what I think of as) cryptic anole behavior! Thanks for letting me spy in on you little one!
References
Propper, Catherine R., Richard E. Jones, Matthew S. Rand, and Harriet Austin. 1991. “Nesting behavior of the lizard Anolis carolinensis.” Journal of Herpetology 25 (4): 484. https://doi.org/10.2307/1564774.
Reedy, Aaron M., David Zaragoza, and Daniel A. Warner. 2013. “Maternally chosen nest sites positively affect multiple components of offspring fitness in a lizard.” Behavioral Ecology 24 (1): 39–46. https://doi.org/10.1093/beheco/ars133.
Stamps, Judy A. 1976. “Egg retention, rainfall and egg laying in a tropical lizard Anolis Aeneus.” Copeia 1976 (4): 759–64. https://doi.org/10.2307/1443460.
Tiatragul, Sarin, Joshua M. Hall, Nathaniel G. Pavlik, and Daniel A. Warner. 2019. “Lizard nest environments differ between suburban and forest habitats.” Biological Journal of the Linnean Society 126 (3): 392–403. https://doi.org/10.1093/biolinnean/bly204.
Tokarz, Richard R., and Richard E. Jones. 1979. “A study of egg-related maternal behavior in Anolis Carolinensis (Reptilia, Lacertilia, Iguanidae).” Journal of Herpetology 13 (3): 283–88. https://doi.org/10.2307/1563320.
Male Anolis carolinensis lizards will fight and form social dominance hierarchies when placed in habitats with limited resources. Dominance may procure benefits such as priority access to food, shelter or partners, but may also come with costs, such as a higher risk of injuries due to aggressive interaction, a higher risk of predation or a higher energetic cost, all of which may lead to an increase in stress. While most research looks at dominance by using dyadic interactions, in our study we investigated the effect of dominance in a multiple male group of A. carolinensis lizards. Our results showed that dominant males in a multiple male group had priority access to prey and potential sexual partners but may run a higher risk of predation. We could not confirm that dominant males in a multiple male group had a higher risk of injuries from aggressive interactions or a higher energetic cost by being dominant. Overall our results seem to indicate that dominant male A. carolinensis lizards in a multiple male group obtain clear benefits and that they outweigh the disadvantages.
The egg tooth is a hatching adaptation, characteristic of all squamates. In brown anole embryos, the first tooth that starts differentiating is the egg tooth. It develops from a single tooth germ and, similar to the regular dentition of all the other vertebrates, the differentiating egg tooth of the brown anole passes through classic morphological and developmental stages named according to the shape of the dental epithelium: epithelial thickening, dental lamina, tooth bud, cap and bell stages. The differentiating egg tooth consists of three parts: the enamel organ, hard tissues and dental pulp. Shortly before hatching, the egg tooth connects with the premaxilla. Attachment tissue of the egg tooth does not undergo mineralization, which makes it different from the other teeth of most squamates. After hatching, odontoclasts are involved in resorption of the egg tooth’s remains. This study shows that the brown anole egg tooth does not completely conform to previous reports describing iguanomorph egg teeth and reveals a need to investigate its development in the context of squamate phylogeny.
