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Muscle map on scapulocoracoid of Anolis insolitus

Morphology of the Scapulocoracoid of Anolis Ecomorphs

 

From the onset of my scientific career I have been fascinated by the pectoral girdle. In its structural and functional diversity it is barely rivaled by any other skeletal part of the tetrapod body. Anoles, in particular, employ their forelimbs not only in locomotion, but also in various routines of display, grooming, feeding, or mating. It is likely that the different functional roles fulfilled by the pectoral limb and girdle impose varying, and potentially opposing, selective pressures onto the evolution of its structural form.

Jane Peterson briefly alluded to the structural variance displayed by the different anole ecomorphs, relating them to specific locomotor requirements by providing brief descriptions in her thesis (1973) and the First Anolis Newsletter (1974). However, beyond this initial work, and a few qualitative assessments in papers regarding phylogenetically informative characters, very little is known about the variability of the anole pectoral girdle.

right scauplocoracoid of Jamaican anoles

Right scapulocoracoid of three anole species, representative of the Jamaican lineage. The arrow denotes anterior. (via Tinius et al. 2020)

In many ways, our recent publication in the Annals of Anatomy (Tinius et al. 2020) is a dream come true (at least for me), as it allowed us to finally visualise the patterns of morphological variation that Peterson (1974) could only communicate in descriptions. Because the shoulder girdle is comprised of multiple elements that are mobile with respect to one another, this paper only investigated one of its moieties: the scapulocoracoid. This paired structure spans the entire height of the body wall, is comprised of developmentally very different compounds, and directly connects the forelimb to a midline element, the presternal plate. These attributes made it a great starting point for our investigations of the pectoral girdle.

In describing the scapulocoracoid of two non-anoline iguanids, Polychrus and Pristidactylus, we anchored our comparisons in two well-studied and closely related lizards. We then expanded on this anatomical framework by comparing all representatives of the monophyletic Jamaican anole radiation to their respective ecomorph representatives on Puerto Rico and Hispaniola. We tried to take full account of the variability of the scapulocoracoid by examining it both qualitatively, in images and comparative description, and quantitatively, through geometric morphometric analysis.

CVA of the right scapulocoracoid of Anolis ecomorphs

Canonical Variate Analysis (CVA) of the right scapulocoracoid of Greater Antillean anoles, including warp image of the scapulocoracoid denoting shape changes along CV1 and CV2. (via Tinius et al. 2020)

We found that regardless of potential phylogenetic constraints on skeletal morphology, morphospatial occupancy differs markedly between ecomorph groups. Unexpectedly, twig anoles show the most distinctive shape of the scapulocoracoid, with a relatively tall scapula and anteroposteriorly short coracoid, similar to the situation found in chameleons (Fischer et al. 2010). But despite a significant overlap in morphospatial occupancy, the other three ecomorphs examined (trunk-ground, trunk-crown, and crown-giant) also exhibit trends towards a specialized scapulocoracoid morphology, such as a relatively wide/cylindrical scapulocoracoid in trunk-ground anoles.

These variations in form likely impact the size and vectors of muscles attaching to the scapulocoracoid. One muscle group that is likely particularly impacted by the differences in scapulocoracoid form is the M. serratus anterior. This muscle group originates laterally on the cervical ribs and inserts on the medial aspect of the suprascapula. The M. serratus anterior group stabilizes the scapulocoracoid during locomotion and protracts/retracts it along the body wall. The anteroposteriorly more extensive suprascapula of crown-giant anoles likely facilitates more forceful scapular retraction, through the relatively greater attachment area for this muscle and the anterior disposition of its insertion area. Contrastingly, the relatively tall scapula of twig forms likely allows for a greater moment arm acting through this muscle group, while the anteroposteriorly short suprascapula facilitates more precise protraction/retraction of the scapulocoracoid.

Muscle map on scapulocoracoid of Anolis insolitus

Right scapulocoracoid of Anolis insolitus in a) lateral, and b) medial view, showing the attachment sites of major muscle groups that act upon the scapulocoracoid. (via Tinius et al. 2020)

My only regret about this project is the exclusion of Cuban anoles, which markedly limited our ability to compare patterns in a wider phylogenetic context. Most of the crown-giant and trunk-crown anoles examined belong to their own ecologically homogenous clade, making it impossible to discern ecological from morphological signal.

The Jamaican Anolis clade provides a glimpse into what might be achieved with a phylogenetically broader sample, as it represents four major ecomorph groups (five, if you attribute A. opalinus to the trunk group) plus two non-ecomorph species within a seven-species radiation. Despite the relatively young age of the Jamaican clade, its ecomorph representatives exhibit a push towards specialized morphologies of the scapulocoracoid, even if this level of specialization is markedly smaller than in their Puerto-Rican and Hispaniolan relatives. A future widening of our sample should allow us to answer some intriguing questions regarding the retention and diversification of ecomorphologically specialized forms within distinct phylogenetic lineages.

Literature cited

Fischer, M.S, Krause, C. & Lilje, K.E. (2010): Evolution of chameleon locomotion, or how to become arboreal as a reptile.─ Zoology, 113:67-74.

Peterson, J.A. (1973): Adaptation for arboreal locomotion in the shoulder region of lizards.─ Ph.D. thesis, University of Chicago.

Peterson, J.A. (1974) [In:] Williams, E.E. (ed.) The First Anolis Newsletter. Cambridge, Massachusetts: Museum of Comparative Zoology, Harvard University.

Tinius, A., Russell, A.P., Jamniczky, H.A. & Anderson, J.S. (2020): Ecomorphological associations of scapulocoracoid form in Greater Antillean Anolis lizards.─ Annals of Anatomy, 231; doi.org/10.1016/j.aanat.2020.151527.

Sleeping Behavior of the Puerto Rican Twig Anole, Anolis occultus

In August, we published a paper in the Caribbean Journal of Science entitled, “Sleeping Behavior of the Secretive Puerto Rican Twig Anole, Anolis occultus.” Check out our new post on the Chipojo Lab blog about the paper!

Levi Storks, Manuel Leal. 2020. Sleeping Behavior of the Secretive Puerto Rican Twig Anole, Anolis occultus. Caribbean Journal of Science 50(1):178–87.

Invasive Green Anole on Japanese Island Implicated in Butterfly Extinction

We’ve previously had posts about green anoles, Anolis carolinensis, introduced to the Ogasawara Islands, and the efforts to eradicate them. Now a report has implicated the anoles in the possible extinction of a butterfly species. Here’s an article from the japan times:

Blue Japanese butterfly endemic to Ogasawara Islands feared extinct

The Environment Ministry said Thursday that a species of small butterfly endemic to Japan’s southern islands is feared to have gone extinct because all artificially bred butterflies and worms of its type have died.

In the butterfly’s natural habitats, in the Ogasawara Islands some 1,000 km south of Tokyo, no individuals from the species have been confirmed since 2018, the ministry said.

Unless the blue butterfly measuring just over 1 cm long is found in the wild, it will be the first butterfly species native to Japan to go extinct.

The ministry believes that a decline in the butterfly population is at least partially attributable to foreign lizards on the remote islands.

Efforts to preserve the species, known as Celastrina ogasawaraensis, had been under way since 2005 by Tama Zoological Park in western Tokyo and also at a facility in Shinjuku Gyoen National Garden in the capital since last October.

But all of the butterflies and worms raised at these facilities died in July and earlier this month, the ministry said, adding that repeated inbreeding might have led to an accumulation of hazardous genes, ultimately causing death.

The small butterfly is currently categorized as endangered on the Environment Ministry’s Red List. The ministry is expected to decide whether the species should now be listed as extinct.

The Ogasawara Islands are known as the Galapagos Islands of Asia due to their unique flora and fauna after eons of separation from any continent.

While the remote islands are growing popular as a tourist spot for beautiful subtropical scenery and whale watching, limited access via a 24-hour ship voyage available only once once per week helps to preserve the wildlife and natural ecosystems.

The volcanic islands, now administered by the Tokyo Metropolitan Government, belonged to the United States after World War II before being returned to Japan in 1968.

Green Anole Eats Brown Anole

Four-year-old Dany Leffler noticed the goings-on in his backyard in Houston just minutes from downtown.

Down the hatch!

Interview on Lizard Science and Racism

Carlos Guarnizo along with several other scientists created Ciencia Café, pa’ Sumercé, which is a space where citizens can access first-hand (directly from researchers) excellent research in science and technology that Colombians are doing inside and outside the country. At the same time, this space offers scientists and researchers the opportunity to meet citizens and understand the concerns and interests of the public; all of this through respectful dialogue, promoting an appreciation for science and technology by encouraging everyone to participate.

Two weeks ago, I was invited to one of the interviews from Ciencia Café, pa’ Sumercé, in which I talk about two different things that are not necessarily exclusive: science and racism. During the interview, Carlos asked me about why I decided to study biology and lizards, especially, he was interested in knowing how I ended up doing a Ph.D. with Jonathan Losos. After I talked about that part of my professional life, Carlos asked me about the BLM movement and its consequences in Colombia. I told him that despite the miles apart that Colombia is from the USA, we – the black community – suffer from the same kind of discrimination (punctual and systemic racism) in our daily bases, and I also told him that it is important to talk about racism in our families and in our work areas. At the end of the interview, I told a short story about how the Anolis chloris photo I took in 2016 ended up as the cover image in Evolution in 2019.

#DidYouAnole? – Anolis porcatus

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Hey!
I’m taking a break for two weeks, but instead of leaving you without a post for two weeks in a row, here’s Anolis porcatus which I mentioned I had tweeted about the week before my first post!

Anolis porcatus is the Cuban Green anole. A trunk-crown anole with a dewlap ranging in colour from reddish to pink. Like it’s name says, it’s from Cuba but it has now been introduced to Florida, Brazil and Hispanola. And one was found in the… Canary Islands?? I’m jealous. That sounds like a great vacation.

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As you’ve seen from pictures, Anolis carolinensis and A. porcatus look extremely similar (for obvious reasons now haha).

Well that’s because, they’re the same species. As discussed in the Anolis carolinensis post, the American Green anole is not a distinct species.

I’ve mentioned that I’ve been going though the proposed series of anoles called the carolinensis series. They’re all trunk-crown anoles and look very similar, even identical like the American Green and Cuban Green. Some of the members are found in Cuba & that’s where their common ancestor is thought to originate.

The idea was that Anolis porcatus made its way to America a very long time ago and then, due to speciation, along came A. carolinenis. But because the two can interbreed, that means there’s no reproductive isolation, doesn’t it? That’s not all, but you can read about it from Dr. Losos’ post and the paper itself!

I hope you all have a great week!! I’ll see you on September 3rd. Thank you so much for reading!

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Photo by Jesús Reina Carvajal

San Antonio Celebrates Its Green Anoles

From the pages of the San Antonio Express-News (August 12, 2020):

S.A.’s Common Critters: Nothing common about the green anole, San Antonio’s most common lizard

Sarah Baade practically considers anole lizards her personal gardeners. The green little reptiles have a knack for keeping her company at her San Antonio home while she tends to her front yard tomatoes and backyard squash, poking out their slender heads from under her plants to stare at her.

She calls it a mutually beneficial relationship. The anoles eat any pesky bugs, and Baade rewards them with a free drink whenever she waters her gardens.

But there’s something else these simpatico green thumbs share: The joy of silence.

“It’s kind of my peaceful quiet time,” said Baade, who works as an audiologist. “They are my peaceful, quiet companions when I’m gardening.”

Anole lizards, the most common lizards in and around San Antonio, may not make much noise, but they sure make an impression — especially now as we see them more often while we spend more time in and around the house. And take it from another anole fan, one who’s studied them for nearly 20 years, there’s nothing common about this so-called common lizard.

“I think they’re incredibly charismatic,” said Michele Johnson, a biology professor at Trinity University who runs the kid-friendly website, lizardsandfriends.org. “I think that they’re a really interesting lizard because they seem so familiar, and yet there’s still things about them that we haven’t figured out yet.”

Here are some familiar and not so familiar facts about the anole.

Tomato, tomato. Anole, anole. San Antonio is home to the Carolina anole (Anolis carolinensis), sometimes just referred to as the green anole.

Anole is pronounced “ah-NOH-lee”, though Johnson noted most scientists say anole like “ah-NOLE.” She doesn’t think there’s one right way to say the name.

Anoles range beyond the Carolinas. The Carolina anole is native to North America and ranges across the southeastern United States, from around the middle of Texas east and up through the Carolinas. The lizard prefers warm and moist environments with trees, though you’re sure to spot them just about anywhere else there’s foliage, from forests and roadsides to lawns and doorsteps.

It’s easy being green. The Carolina anole also is known as the green anole for its bright, verdant color. The anole can change color into shades of brown, but that doesn’t make it a chameleon. Chameleons are not found in the Americas. Rather, anoles belong to the iguana family of reptiles.

Hey, baby, do you like my camo? Yes, an anole’s ability to change color can help it blend in with its surroundings, which is great for hunting insects and avoiding predators. But most anoles change color as a sign of dominance or sexual attraction, rather than trying to blend in.

“We know for sure it’s not camouflage,” Johnson said. “There’s been several studies.”

Little green men and women. Male and female anoles look almost exactly alike save for two distinguishing features. The female often sports a white dorsal stripe along her back, while the male displays a larger throat fan, or dewlap, that’s bright red and three times the size of the female’s fan.

Long tails, short bodies, short life spans. Anoles range in size from 5 to 8 inches long, and more than half of that is tail. Anoles live only around two to three years in the wild. The lizards are popular pets though, and can live up to seven years in captivity.

Days spent in the trees. Anoles are diurnal, meaning they’re active in the daytime. They’re also arboreal, meaning they live in trees.

They really toe the line. Johnson noted anoles have big toe pads that allow them to cling to surfaces.

They also cut and run. An anole will shed its tail to escape a predator. The twitching limb serves as a distraction for the lizard’s escape. A new tail will grow back, though not as long or as colorful as the original.

A bug’s life for breakfast, lunch and dinner. Anoles eat all sorts of insects, including moths, crickets, ants and spiders.

Keep off the dudes’ turf. Male anoles are extremely territorial and will fight other males to preserve their areas for themselves.

Self-reliant hatchlings. A few weeks after mating, a female anole will lay her first egg, then lay another every other week until she reaches around 10 eggs. The hatchlings then emerge 30 to 45 days later. The babies must fend for themselves without mother or father to care for them.

“I know that they had babies in my front garden because I’ve seen the babies,” Baade said. “It’s cool to see them scurry around.”

The anole is one of the X-Men. The Marvel comic book character Anole is one of the lesser-known mutants to join the heroic X-Men. The openly gay young hero exhibits lizardlike traits and abilities, including green scaly skin and the power to grow back lost limbs.

A first in genome sequencing. As part of scientists’ efforts to better understand the evolution of various animals, the green anole was the first reptile to have its entire genome sequenced. Johnson said the lizard was chosen because it has a small body and a fast reproduction time — and it’s way easier to keep in a lab than, say, a crocodile or snapping turtle.

She noted that sequencing the green anole has since led to a better understanding of such processes as forming eggs and regenerating tails. Take that, GEICO Gecko.

Living High with a Cool-Cold Anole – Part II

Illustration of Anolis heterodermus on a Frailejon inflorescence (Espeletia grandiflora). Illustration: Sebastian Perez.

Continuing with my adventure with Phenacosaurus (see Part 1 here), during the process of publishing papers from my thesis about thermoregulation in the high Andean lizard Anolis heterodermus , I realized that I only studied  one population of this species, but some populations living above 3000 meters of elevation in the subparamo and paramo tropical andes ecosystems, as well as others that are below 2600 m. Furthermore, Martha and I evaluated only thermoregulation, but other thermal traits remains unknown. Despite not having grants and without have been a postgraduate thesis, I decided to expand my research and study whether  thermoregulation, thermal tolerances and thermal sensitivity vary with elevation. I expected to find that at high elevation, lizards would be more active thermoregulators, eurythermal and cold tolerant, as happens in other Anolis lizards like the cristatellus and cybotes species groups.

To investigate these questions, I took new data during 2016 with Martha Calderón at two new localities: Chicaque Natural Park, a cloud forest reserve at 2000-2600 m elevation, and Matarredonda Ecological Park, a subparamo to paramo reserve at 3200-3400 m elevation. This time we invited our colleague and Martha Msc. student Felipe Paternina, who had done his thesis research on thermoregulation and extinction risk by climate change in the high-Andean nocturnal snake Atractus crassicaudatus. We also took data on Gachancipa, a municipality close to Tabio. At the beginning of this year, after the Covid-19 Pandemic, fortunately our second paper was published in the Journal of Thermal Biology.

 

Chicaque Natural Park (left) and Matarredonda Ecological Park (right) 

First of all, we did not find changes in thermal preference range between the three localities. Similarly, cold tolerance (CTmin) and thermal performance breadth were similar along the elevational gradient. Nevertheless, the most exciting discovery was that cold tolerance (CTmin) is very low (4.4°C in Matarredonda) and thermal performance ranges are wide. Surprisingly, CTmin in Chicaque, the lowest altitude, was 6.2°C, even though the potential lowest body temperatures at night could be only 10°C (calculated as operative temperatures with our null-models of Anolis heterodermus). This clue makes us think that maybe cold tolerance is constant due to a niche conservatism: during Pleistocene glaciations, Andean ecosystems were colder than now, and maybe this trait did not evolve when climate became warmer because there is no selective pressure for that. Definitely, Anolis heterodermus is the king mountain of anoles (in fact, it has a co-osified cranial crown).

 

Vertical thermal gradient to measure thermal preference of Anolis heterodermus. Figure from Méndez-Galeano & Calderón-Espinosa (2017)

Null model of Anolis heterodermus to measure operative temperatures in the field; in this case, the model was placed on a potential perch.

As well as with cold tolerance and thermal preference, critical thermal maximum and thermal sensitivity did not change with elevation; however, thermoregulation does: at both low and high elevations, this species has to face thermal constrains, like a cold and narrow temperature range of the Chicaque cloud forest due to its canopy cover, or the extreme fluctuating temperatures, with tendency to the coolest regimes in our study, in the Matarredonda subparamo. To deal with that, individuals become thermoconformers, contrasting in this mode with the seasonal trends in thermoregulation in Tabio. We attribute this change to the fact that seasonal changes can be behaviorally compensated with active thermoregulation, but elevational changes are more extreme, and the species have to resign to be active at suboptimal temperatures and exist under the cold range of this extreme ecosystem.

Measuring locomotor performance to assess thermal sensitivity on Anolis heterodermus. There is a very slow lizard, which the local people call “The Andean Chameleon.”

Thermoregulatory adjustments also exist at other temporal scales, such as day-by-day. At the highest elevation, subparamo and paramo days could be extremely different from one day to the next; on some days, the sun could burn your face, while on other days, you could not see anything due to the cloud cover. So, we evaluated thermorregulation between these regimes, too, and observed that on cloudy days, Anolis heterodermus remained a thermoconformer, but on sunny days, the thermal quality of the habitat offered some optimal microhabitats, and this species takes advantage by changing from thermoconformity to active thermoregulation on a daily temporal scale. Undoubtedly, this species is a thermo-oportunist, plastic in its thermoregulation, and showing us that general patterns observed at only one scale do not always tell the complete story.

Our findings placed this species closer to the static hypothesis of the evolution of thermal physiology due to behavioral buffering on selection, better known as “The Bogert Effect.” Also, thermoregulation is so dynamic, that Anolis heterodermus can be an active thermoregulator in high thermal quality habitats (or times) and a thermoconformer when the habitat become so cold or so fluctuating that thermoregulation is not feasible.

Other reptiles from the Bogotá Savannah, Eastern Cordillera of Colombia, which could be at extinction risk by climate change and which we study in our research group. From left to right: Anadia bogotensis, Atractus crassicaudatus*, Riama striata, Stenocercus trachycephalus. Photos: *Uber Rozo, Guido Fabian Medina.

Now, after all of this, the cold reign of our highland king is threatened by climate change, the effect of which could be devastating for tropical biota, especially to endemic species. Climate change puts high-elevation reptiles in a vulnerable situation due to a restricted possibility to distributional displacements, taking them to a dead end, upwards, what is called “the mountaintop extinctions.” Now it is our responsibility to, at least, predict the potential extinction risk by climate change of Anolis heterodermus and other co-distributed reptiles with our thermal data in order to prevent the possible loss of our cool-cold anole forever. Stay tuned for the final part of this trilogy of the thermal biology of Anolis heterodermus, our Andean chameleon.

 

Cites:

Méndez-Galeano, M. A., & Calderón-Espinosa, M. L. (2017). Thermoregulation in the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) at high elevation in the Eastern Cordillera of Colombia. Iheringia. Série Zoologia 107.

Méndez-Galeano, M. A., Paternina-Cruz, R. F., & Calderón-Espinosa, M. L. (2020). The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia. Journal of Thermal Biology 89: 102498.

#DidYouAnole – Anolis longiceps

File:Anolis longiceps lizard.jpg - Wikimedia Commons

Photo by USFWS R. Colon

Hope you are all having a great week!

I have searched high and low for this anole and now I’m here to present to you, Anolis longiceps.

This anole is found only on Navassa Island. Navassa is 76 km west of Haiti, has an area of 5.4 km² and is uninhabited (by humans). The introduction of cats and dogs, as well as goats that contribute to the destruction of vegetation, have led to the Navassa Anole being listed as Vulnerable by the IUCN. The island also had faced habitat degradation from mining.

Navassa Anole males can get up to 83 mm (SVL), while the females are at about 76 mm. Some have light spotting which is yellow-ish in their green phase and white in their dark phase.

The name longiceps means “longhead” and refers to the anole’s snout which is described as long and tapering to a point, much like A. maynardi. Its dewlap is orange with white scales.

These pictures appear to be of the holotype (a specimen used to describe and name a new species) from the Smithsonian Institution’s Division of Amphibians and Reptiles at the NMNH.
There don’t seem to be any other pictures I can find of this anole, but if you are aware of any, please let me know!

Anolis Lizards that Colonize Islands without Other Anoles Lose Their Parasites and Thrive: Experimental Study in Panama

Anolis apletophallus. Photo credit: Dario – https://www.inaturalist.org/photos/31736257

From a press release from the Smithsonian Tropical Research Institute:

When the U.S. flooded Panama’s Chagres River valley in 1910, Gatun Lake held the record as the world’s biggest reservoir. This record was surpassed, but researchers at the Smithsonian Tropical Research Institute (STRI), who are now studying invading lizards on the tiny islands that dot the lake, discovered that islands with native lizards act as another kind of reservoir, harboring the parasites that control invaders. The study, published in the journal Biology Letters, is valuable experimental evidence that biodiversity is better, making ecosystems more resistant to invasion.

As part of another study to find out how many generations it takes for slender anole lizards (Anolis apletophallus) to adapt to climate change, a research team led by Christian Cox, a visiting scientist at STRI from Florida International University, and Mike Logan from the University of Nevada, Reno, transplanted lizards from the tropical forest on the mainland to the islands, which tend to be hotter and drier. Before the transplant, they did a general health check of the lizards that included counting the number of parasites (mites) on their bodies.

When they came back several times during the next two years to see how the lizards were doing in their new habitats, they recounted the number of mites.

“We found that on the islands with no resident species of anole lizard, the slender anole lizards that were transplanted to the islands lost their mites within a single generation, and the mites are still gone several generations later (up until the present),” Cox said. “Indeed, individual founding lizards that had mites during the initial transplant had no mites when they were later recaptured. In contrast, anole lizards that were transplanted to an island with another resident (native) species of anole lizard kept their mites for three generations, and some of the founders on the two-species island never lost their mites.”

“Our study turned out to be a large-scale experimental test of the enemy release hypothesis,” said Logan, who did this work as a three-year STRI/Tupper postdoctoral fellow. “Often, when an invasive animal shows up in a new place, all of its pathogens and parasites are left behind or do not survive, giving it an extra survival advantage in the new place: thus the term enemy release.”

The team also found that the two-species island had lower density and lower biomass per unit area of the invasive lizard species, indicating that the continued presence of the mites may be keeping their populations under control.

“Our study is a clear example of something that conservationists have been trying to communicate to the public for some time,” Logan said. “Diverse native communities sometimes function as ‘enemy reservoirs’ for parasites and diseases the keep down the numbers of invaders.”

Funding for this study was provided by the Smithsonian Institution, Georgia Southern University, the Theodore Roosevelt Memorial Foundation and the American Museum of Natural History.

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