Anolis Sagrei In The Mexican Interior

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A view of our hotel from the parking lot, right in front of the spot where the brown anole was lounging.

A view of our hotel from the parking lot, right in front of the spot where the brown anole was lounging.

On our recent trip to Mexico, we had been warned that brown anoles were spreading beyond the coast, and sure enough, we found ’em. The photo above is a female A. sagrei we spotted in the parking lot of our point five-star hotel located in downtown Chinantla, Veracruz, Mexico. The photo ain’t pretty, but the ID is unmistakeable: them’s Cuban emigres, doing just fine in the Mexican heartland.

 

map chinantla mexico - Google MapsWe actually found brown anoles at two spots in Chinantla. The other was a small, bright green pained shack near the intersection of the highway and the main road through town. A bunch of female and juveniles brown anoles were running up and down the walls of the shack, easily seen from the side of the road. You can’t miss it, not only due to its bright color, but also because of the transit police standing in front, randomly waving over cars–especially those driven by oddly-attired biologists–and then finding problems with their registration or what-not. In fact, you’ll have plenty of time to watch the anoles as the officers explain at great length why they will have to impound the car, even though it is a rental and you are five hours from Veracruz, where your flight leaves the next morning, because the car’s tax certificate for 2013 is not plastered to the back window. You’ll probably be distracted by your colleague on her cell-phone berating the rental car office, but stay focused, even when–finally–the police officers realize (as the rental car people predicted) that it is possible to pay the registration tax, on the spot, in cash, and without being given a receipt. Any way, that’s where to look for brown anoles in Chinantla.

Hertz Rent-a-Car won't make that mistake again!

Hertz Rent-a-Car won’t make that mistake again!

The Anole Community Of Los Tuxtlas, Mexico

Anolis barkeri. Photo by J. Losos

Anolis barkeri. Photo by J. Losos

As part of its ongoing studies of Central and South American anoles, Team Mainland—fresh off successful field work in Colombia and Venezuela earlier this year, traveled to the Veracruz, Mexico to sample that state’s anole fauna. Joined by Anne-Claire Fabre, Victor Jiménez, and Ramón Martínez, Team Mainland worked at the fabled Estación de Biología Tropical Los Tuxtlas, home to eight or nine (depending on which paper you read) species of anoles. The goal of the trip was to characterize the ecology, behavior, and morphology of the species residing at the station. Although all anoles are interesting in their own right, as we know, not all anoles are created equal. And, indeed, there was one special species we had our heart set on seeing: the large aquatic anole, Anolis barkeri.

Anolis barkeri. Photo by J. Losos

Anolis barkeri. Photo by J. Losos

Anolis barkeri. Photo by

Anolis barkeri. Photo by Victor Jimenez.

And lo and behold, we saw them! Aided by Bob Powell’s advice to visit his old field site, a lovely stream located several kilometers from the station, we spent several days observing the antics of these gorgeous anoles, the largest of the mainland aquatics. And by antics, I mean primarily sitting around doing nothing, though they did flash their gorgeous red dewlaps occasionally (alas, not caught by camera, but several times on video—stay tuned once they get processed). Actually, they were sometimes quite active, running rapidly from one place to another. Like other mainland aquatics, these guys hang out right next to streams, and when threatened will sometimes jump in. They don’t go swimming away, though, at least not in our observations (which agree with others); rather, they immediately go to the nearest water-land interface and hang out, hoping they have not been detected.

Our trip occurred in early August, at the end of both the reproductive and dry seasons. We were told that it had been a particularly dry dry season, which may explain some of the observations. For example, A lemurins is supposed to be very common, but we didn’t see a one. Also, males of two other common species, A. sericeus and A. rodriguezi, were few and far between. This was surprising, but perhaps these—like many mainland species—are primarily annual, that is, with a lifespan averaging less than a year.  Perhaps the males, spent by their exertion, are all dead, explaining why we saw so few of them. That was a classic hypothesis borne of field observations, but the Malice of Nature did not intervene to refute it. A number of people suggested that A. barkeri is only found in shaded streams; in the open, it is pushed out by basilisks. “Find a basilisk,” we were told, “and you won’t find A. barkeri.” For the record, we did find several small basilisks along the stream, though only in open, sunny spots in the otherwise well-shaded watercourse. The A. barkeri were found on logs and rocks, always near the water. They didn’t impress me as brilliant swimmers, but could immediately climb onto rocks—very good graspers, with long arms and sharp claws.

I was particularly curious to learn more about A. sericeus.

Potted Plants And Invasive Lizards: A Case Study

Could a lizard stowaway on a succulent?

We hear a lot about invasive anoles–A. sagrei and others–showing up all over the place: Singapore, Taiwan, you  name it. But how do they get there? I was recently reminded of an article by Gad Perry and colleagues in the journal Iguana (now Reptiles and Amphibians: Conservation and Natural History–a quarterly journal available online and worth a look). Perry et al. examined a barge delivering a large number of potted plants to the small island of Guana in the British Virgin Islands. The plants came initially from Florida, but had been sitting in a nursery on a nearby island for at least ten days. What would they contain?

To find out, the investigators laboriously inspected the plants, all 220+ of them, one by one. And sure enough, there were stowaways: six juvenile Puerto Rican crested anoles (A. cristatellus); a dwarf gecko, Sphaerodactylus macrolepis; also, an immature spider, three snails and nests of the red fire ant. In addition, the barge carrying the cargo contained two other lizards, Ameiva exsul.

And remember, this is one just one shipment. Now, in this case, all of the lizards were natives, as were most of the invertebrates. But imagine all of the plants being shipped out from Florida, containing brown anoles, Cuban treefrogs, and who knows what else? My prediction: it’s just a matter of time before brown anoles are everywhere in the urban tropical world.

Another Observation Of Nectivory In Anolis

Following previous threads documenting nectivory in various Anolis (1, 2, 3), here is another account recently observed in south Florida, from Florida International University’s palm botanist Scott Zona in Miami:

This American green anole was methodically going along an inflorescence of one of the palms (Ptychosperma macarthurii) in my back yard licking the nectar droplet from the tip of each pistillode. This palm is an exotic ornamental from New Guinea and northern Australia but is widely cultivated around the world. It is monoecious (male and female flowers on the same inflorescence) but strongly dichogamous (separation in time). The male flowers open first. The lizard was lapping up a droplet of nectar that is excreted by the long, slender pistillode (sterile pistil) in each male flower. I watched him for several minutes (and have lots more photos). The lizard was very methodical about going to every flower, climbing to another branch, and then exhibiting the same feeding behavior. It is unlikely that the lizard would be a pollinator, because of the strong dichogamy; however, female flowers also secrete nectar, so if the same anole were to find another inflorescence in the female phase, it could affect pollination.

American green anole (Anolis carolinensis) feeding on the nectar of a palm inflorescence in south Florida

American green anole (Anolis carolinensis) feeding on the nectar of a palm inflorescence in south Florida

Nectivory in anoles has been well summarised in a previous post, in which Ambika Kamath noted that they had observed a a female licking palm flowers in south Florida but regrettably never got a picture – well it may have been a year and 3 months, but here’s one!

With the wealth of introduced anoles in south Florida, I wonder if this feeding behaviour has been observed in other species but not yet documented – the ecologically similar A. porcatus and A. chlorocyanus seem likely candidates…

If anyone would like more information on this, or has a keen interest in palms, please feel free to email Scott directly.

Evidence From VD That Small Territorial Males May Be Successfully Mating

The parasite in question. Photo from an Anole Annals post by Gerrut Norval.

Recently, Bryan Falk wrote an interesting report on how nematode parasites are passed from one anole to another by sexual contact. He summarized a fascinating paper by Langford et al. in the Journal of Parasitology that convincingly demonstrated this phenomenon. In reading that paper, I found one idea they suggested in the Discussion to be particularly intriguing. I’ll let them describe it:

“Our finding that C. penneri” (the nematode parasite) “is transmitted by copulation has some interesting implications for the host’s reproductive and behavioral biology. Anolis sagrei reproduces in a female-defense polygyny, wherein large males (e.g., SVL = 50 mm) establish and maintain territories containing multiple, relatively small females (Schoener and Schoener, 1980). In Anolis mating systems, young males are generally thought to have little mating success because they are excluded from females by large territorial males (Losos, 2009). In contrast, our parasitological results suggest that small male lizards are copulating with mature females and becoming infected with a sexually transmitted parasite. Thus, our results provide some support for the female mimicry hypothesis (Orrell and Jenssen, 2003) and/or the ‘‘dear enemy’’ phenomenon (Paterson, 2002) in anoles. This insight into A. sagrei reproduction should encourage anologists to reconsider the role of covert and satellite males in anole mating systems where C. penneri infects small male lizards. In conclusion, the major contribution of our study is the establishment of copulation as the route of transmission for C. penneri between lizards and the discovery of both ecological and physiological host specificity in these worms.This study also provides insight into the host’s biology, specifically support for the female mimicry hypothesis in anoles proposed by Orrell and Jenssen (2003).”

I queried Gabriel Langford, “just how small are these infected males?” He responded: “We sampled an evenly distributed group of females and males that ranged from a few days old to large (male SVL 68mm) adults. If memory serves (I’m on my tablet, no data in front of me), at least 35 of the 87 males fell into the range of 34-50 mm. Also, we had several males just above (infected) and below (uninfected) the 34 mm cut-off, which allowed us to be fairly confident about this number in A. sagrei.”

These results suggest that even quite small males may be mating, even though they are far too small to hold a territory. The idea that “sneaker” males may exist in anole populations has been suggested before, but not demonstrated. The occurrence of such matings has all kinds of interesting implications for anole sexual selection and evolution.

Rapid Color Change In Anoles

Anolis gundlachi. Photo by  Alejandro Sanchez.

Anolis gundlachi. Photo by Alejandro Sanchez.

Anolis gundlachi 10 seconds later. Photo by Alejandro Sanchez.

Anolis gundlachi 10 seconds later. Photo by Alejandro Sanchez.

West Indian photographer and natural historian extraordinaire Father Alejandro Sanchez sent in these photos, commenting “I took these two pics less than 10 seconds apart from each other – the time it took for me to modify the flash’s settings. Yet the lizard noticeably changed color patters in such a short time, surely for being scared by my proximity. Anolis gundlachi is one of my favorites.”

And note those blue eyes!

Anole Sculpture

IMG_2598IMG_2599On our recent field trip to Mexico, we were joined by AA contributor Ramon E. Martinez-Grimaldo. Ramon kindly gave me this lovely sculpture of Anolis sagrei. It’s the nicest anole sculpture I’ve ever seen! It’s made of resin and the artist is Luis Ivan Huerta. Check out his website;  in the section “dermoplastias,” he put a picture of the anole’s sculpture. Perhaps Luis will see this post and tell us whether it’s possible to order other anole creations!

Thorny-Headed Worm Parasites In Anoles: Host Manipulation, Complex Life Cycle, And Recent Expansion

These termites might infect anoles with a thorny-headed worm parasite.

Broken Caribbean termite nest.  These termites may infect anoles with a thorny-headed worm parasite, Oncicola venezualensis.

Among the many anole parasites are the acanthocephalans, or thorny-headed worms, which in anoles are typically found as encysted larvae in the body cavity, muscle, or under the skin. One of these acanthocephalans – Oncicola venezualensis – is relatively common in anoles on the Puerto Rican Bank, and is the main character in one of my favorite anole-parasite stories. The story has three parts: 1) how the parasite gets into anoles, 2) how it continues its life cycle beyond anoles, and 3) the mystery of when it all began.

In addition to anoles, O. venezualensis larvae occur in the Caribbean termites Nasutitermes acajutlae on the Puerto Rican Bank, which is a partially submerged landmass comprised of Puerto Rico and all the Spanish, U.S., and British Virgin Islands except St. Croix. These termites construct protective nests and foraging tubes in which they live (see photo), and each individual termite belongs to a morphologically distinct caste. Most are in either the soldier or worker caste, and soldiers are larger than workers, aggressive, and armed with big mandibles. These two castes also have slight color differences – worker termites have yellow heads, whereas soldier termites have dark yellow heads.

Anoles eat termites, and O. venezualensis manipulates both the behavior and appearance of its termite hosts in order to increase the likelihood that the parasitized individuals will be preyed on by anoles (Fuller et al. 2003). Infected termites behave carelessly when compared to their uninfected peers. When a foraging tube is broken, for example, the parasitized workers arrive quickly and then linger, a behavior that makes them more susceptible to predation by anoles. Infected termites also look different, as the head color of infected workers changes to a pale yellow. This increases the difference in appearance between the parasitized workers and the aggressive soldiers, and anoles presumably try to avoid eating soldiers (remember that anoles are smart decision-makers!). The color-changing strategy is effective – in feeding trials with Anolis cristatellus where the lizards were presented with petri dishes containing both parasitized and parasite-free workers, the lizards consistently preferred the light-colored parasitized termites.

After the anole ingests a termite infected with O. venezualensis, the parasite encysts (i.e., forms a cytacanth) somewhere outside of the host’s gastrointestinal tract. In anoles it remains in its larval form, unable to complete its life cycle, and waits for the lizard to be ingested by its definitive host where it will mature into an adult and undergo sexual reproduction. The identity of O. venezualensis‘s definitive host remained elusive for some time. Two primary suspects were mongooses and the pearly-eyed thrashers, since both eat anoles and are common on the Puerto Rican Bank. But, O. venezualensis remains in its larval form in both of these hosts (Nickol et al. 2006). The mystery was solved a couple of years ago – it’s cats! Fuller and Nickol (2011) necropsied a feral cat on St. John and found 87 adult worms. The life cycle for O. venezualensis is now understood to be termite → lizard or bird → cat, then begins again when termites ingest parasite eggs in cat feces. The mongooses aren’t eaten by cats, and so are dead-end hosts for the parasites.

For me, learning that the cat is the definitive host was a head-scratcher. We know that cats eat anoles, and feral cats are abundant on the Virgin Islands, particularly St. Thomas. But, it’s hard to imagine how a parasite with a complex life cycle of at least three hosts (termites, anoles/birds, cats) became invasive across so many islands. It’s also possible that a different, native anole-eater also serves as the definitive host. Bats are the only extant native mammal species on the Virgin Islands, and we know that some bat species eat anoles. Perhaps bats are the original definitive hosts? In any case, the populations of O. venezualensis have likely increased in recent times due to the introduction of cats on those islands, and whether that’s had any effect on the anole populations is unknown.

Weird Urban Perches

There is quite a bit of evidence that anoles like to display from relatively high perches (e.g. references in this paper), a tendency that seems to cross over to their Old World counterparts, the agamids (e.g. Sitana ponticeriana, as outlined here). The hypothesized reason for this choice is that displaying from high perches enables lizards to be maximally visible to conspecifics, ensuring that broadcast displays are heeded by the neighbours. This summer, my field assistant Divyaraj Shah spotted a Calotes versicolor in Kutch, India, displaying from the most exposed perch I’ve ever seen a lizard on. See if you can spot it below:

Spot the displaying Calotes versicolor

Spot the displaying Calotes versicolor

 

Anole Eats Morpho Butterfly

Photo by David Herasimtschuk

Photo by David Herasimtschuk

David Herasimtschuk took this striking photo along the Rio Carbon near the town of Bribri in Costa Rica. Here’s what happened: “The story of how I photographed this image was very bizarre. I was working my way up a stream with the intent to film poison frogs along the bank, and I saw the blue morpho floating down the stream. It was fluttering and still alive, but was being harassed by a school of very hungry fish. Feeling sorry for the animal and curious to see a blue morpho up close I pulled it out of the water. At that point it wasn’t doing to well, but I felt bad throwing it back in the stream, so I placed it on a branch thinking if it might be able to rest and dry off. I then left to film frogs, and came back about a half an hour later. When I returned the butterfly was gone.  Initially I thought it had survived and flew off, but then I saw a bright blue shape in the mouth of stream anole a couple feet from where I had placed it. It was a strange set of events, and it definitely reinforced my belief that when you live in a tropical forest everything wants to eat you.”

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