Does the Gender of an Observer Affect Lizard Behavior?

Hard at work studying lizards (from a previous AA post on best practices in lizard videotaping in the field)

The New York Times reported today on a recent paper in Nature Methods that indicated that stress levels of lab rats varied depending on whether the scientist in the room with them was a man or a woman. This effect existed even in response to t-shirts worn by a man or a woman.

This got me thinking: could the same factor effect lizard behavior studies? In many cases, anoles are studied by an observer quietly watching or recording lizards from a distance of a few meters. Many anole species seem unperturbed by the presence of observers and go about their activities in a seemingly natural way. But does the presence of an observer have an effect? Are they warier? Do they display less? And, more to the point, does the identity of the observer have an effect? Men are, on average, bigger than women, so might that matter? Some people are more fidgetty than others. Clothes? Facial hair? I am aware of a few studies on observer effects on lizard behavior (such as this one on the brown anole), but not many.

 

Anolis carolinensis in Alabama–What Do Green Anoles Do When Browns Aren’t Around?

carolinensis on pine alabamax

Something you don’t see every day: a green anole on a pine tree.

Through the years here at AA, we’ve had discussion of the habitat use of the common green anole. In particular, there is a persistent belief that before the brown anole emigrated from Cuba, green anoles used all manner of anole habitat, from the bottom of trees to the very top of the canopy. Once the browns arrived, however, greens seem to have repeated back up the tree, ceding the low perches to the browns.

This is a very nice story, and probably true, but it’s surprising how little documentation we have of the habitat use of green anoles in places where browns don’t occur. In fact, more generally, it is quite surprising just how little we know about the natural history of green anoles throughout their natural range. For such a common species, you’d think its biology would be extremely well-known, but that is far from the case.

A while back, Janson Jones referred to the green anoles in his then-neighborhood (he’s since moved) in Georgia as low-riders, a possible example of green anole habitat use in the absence of browns. With this in mind, I was delighted to get a chance to see what the greens are up to in Alabama, a state that is still mostly–at least for now–mostly brown anole free.

Across the street from Pi Kappa Kappa.

Across the street from Pi Kappa Kappa.

On the campus of the University of Alabam in Tuscaloosa, greens were moderately abundant when the sun was out. The fellow to the right was strutting his stuff on sorority row, but his comrades elsewhere were in similar habitats on trees, moving up to into the canopy when harassed by an old dude with an iPhone.

But then I had the good fortune to get taken to a nearby pine forest by whiptail lizard geneticist turned turtle biologist Peter Scott, a grad student at UA. Peter told me that he often saw (or, rather, heard) green anoles scurrying through the leaf litter when he approached, running to the nearest tree which it then ascended. It seemed unlikely, but sure enough, that’s where the greens we found were, down low, in very un-green anole-like habitat.

carolinensis in the litter Alabama

Alabama low-ridin’ green anole

Of course, these were just a few observations made over the course of a short hike one afternoon. But clearly there’s a lot to learn about green anoles–what they do in places without competitors, and how that changes when brown anoles arrive. Seems like a great project out there, just waiting for someone to do it.

 

More Orange-Headed Brown Anoles

sagrei orange headed heather stewart

We’ve had a series of posts on orangey brown anoles in Florida, but this most recent example is a stunner. Thanks to Heather Stewart for providing this photo of a fine male from Boca Raton, FL, photographed this past January. Heather pointed out that other brown anoles in the populations were quite normal looking.

Rampaging Wrens Chow Down on Green Anoles

Wrens seem like such harmless, friendly little birds. And with such a dainty little beak, how much damage could they do? Imagine our surprise, then, to learn that they may be voracious predators on our beloved anoles. Thanks to the observations of Roger Birkhead and Mark Benny, reported in the most recent issue of Herpetological Review, we now know the true nature of these little beasts. Here’s what they saw (Herpetological Review 45(1):123-124, 2014):

wren“On 14 August 2013 around 0730 h MCB was observing the birdfeeders and birdhouses at his residence (Harrison Co., Mississippi, USA; 30.387325°N, 89.021624°W, datum WGS84/NAD83) when he noticed a commotion near the potted plants on his front porch. An adult Carolina Wren (Thryothorus ludovicianus) was observed smacking and shaking something large and elongated. When the wren flew up to the nearby birdhouse it became apparent that it had a juvenile Anolis carolinenis in its beak which it quickly fed to its chicks. This behavior was observed for a second time at approximately 1130 h. A third anole was observed being fed to the chicks at 1619 h (Fig. 1). There were at least two exchanges of food missed while leaving the point of observation to retrieve and set up a camera, but were evidenced by long green tails protruding from the entrance hole of the birdhouse that were longer than the lizard in Fig. 1. Adult wrens were also seen bringing larger unidentifiable pieces of flesh assumed be the remains of a larger dismembered A. carolinensis. Similar behavior has been noted for vireos feeding on A. carolinenis (Sykes et al. 2007. Wilson J. Ornithol. 119:508–510). Additional observations were made on 15 August and 16 August of both whole lizards and parts being brought in by the adult wrens. Lizards are identified in the diet of the Carolina Wren as far back as 1916 (Beal et al. 1916. Common Birds of the Southeastern United States in Relation to Agriculture. Farmers Bulletin 755, 40 pp.), but no species identifications were provided. Generally, predation of vertebrates by passerine birds is considered uncommon (Lopes et al. 2005. Lundiana 6:57–66). This observation is the first documented record of A. carolinensis being consumed by Carolina Wrens and judging by the frequency of captures noted here this wren species may be a significant predator of anoles at least during the bird’s nesting season.”

Green Anoles Sunning in San Diego

Zookeeper Amber Carney sent these photos of what is likely Anolis carolinensis.  The lizards were spotted in Balboa Park, San Diego, CA, at 3pm on the 19th of April. They’ve been reported in Los Angeles but, to the best of my and Jonathan Losos’s knowledge, never in San Diego. Has anyone else observed wild anoles in San Diego? Range expansion!

This looks like a female to me.

This looks like a female to me.

A male, if I had to guess.

A male, perhaps.

Uncertain Future for the Jamaican Iguana

A few months back, we had a post on the conservation situation in Jamaica with particular emphasis on the Hellshire Hills, last redoubt of the Jamaican iguana. Now in the journal Oryx, Rick Van Veen and Byron Wilson of the University of the West Indies, along with Tandora Grant and Richard Hudson, of the San Diego and Fort Worth Zoos, respectively, express further concern of the situation. Most of the article can be viewed online; add “and the environmental conventions to which it is a signatory.” to the last line and you’ve got the whole article.

When You Can Not Get The Results You Expected, Use What You Can Get!

An adult Anolis sagrei male specimen from Santzepu, Sheishan District, Chiayi County, southwestern Taiwan.

An adult Anolis sagrei male specimen from Santzepu, Sheishan District, Chiayi County, southwestern Taiwan.

Field research does not always go the way we plan. My research partners and I were reminded of that in 2004, when we tried to use a mark-and-recapture method to determine the population sizes of brown anoles (Anolis sagrei) in a small betelnut palm (Areca catecha L) plantation in Santzepu, Sheishan District, Chiayi County, southwestern Taiwan. We ended up with too low recapture rates for our estimates. Still all was not lost! Of the lizards we did recapture, we were able to calculate monthly growth rates and monthly growth percentages. The results indicated that at least some individuals experienced active growth throughout the year. Our results also supported the findings of Schoener and Schoener (1978) and Cox et al. (2009) that smaller individuals of both sexes grew faster than larger conspecifics of the same gender, and that males grew faster than females. We also determined that growth rates of both sexes decreased during the peak reproductive period, suggesting that available energy is directed primarily to reproduction and the associated to behavior, and that energy is only directed towards growth once the requirements for reproduction are met.

The experience from this study convinced me again that it is important to collect as much data as possible when conducting field studies – it is hard to predict where it may come in handy at a later stage.

Estrogen Pathway Is Responsible for Facial Elongation

Why the long face?

Why the long face?

When most people think of vertebrate sexual dimorphism (differences between the sexes), they think of elephant seals or red deer. Most of us here, of course, think of the pronounced dimorphism in size and shape in many anole species. Indeed, anoles have served as excellent model systems for the study of sexual dimorphism, particularly the evolutionary forces that give rise to it. Although there has been significant progress since Darwin in our understanding of why sexual dimorphism evolves, we have made less progress in the HOW. That is, what mechanisms during development give rise to what are often extreme differences between the sexes when their genomes are so similar?

When we think of vertebrates where males are larger or shaped differently than females, and have weapons or ornaments, we almost immediately think of testosterone as a mechanism underlying the sex differences. Once sexual maturity happens, the testes start cranking out testosterone, thus causing a change in the male’s phenotypic trajectory. While there is certainly evidence for circulating testosterone to have this effect in some lizards, is this always the case, and does it apply to specific body parts and not just overall size? Aside from the circulating hormone, how are receptors involved in the development of dimorphism? In a new paper by Sanger et al., a novel developmental pathway of sexual dimorphism is described for lizards in the carolinensis clade, which are striking in their elongation of male faces relative to females.

Figure 1a. from Sanger et al. (2014), showing the differnces in head shape dimorphism among anole clades. Note the long male face in A. maynardi, a member of the carolinensis clade.

Figure 1a. from Sanger et al. (2014), showing the differences in head shape dimorphism among anole clades. Note the long male face in A. maynardi, a member of the carolinensis clade.

Sanger et al. tested whether sex differences in several different pathways led to the observed head shape dimorphism in A. carolinensis compared to two non-carolinensis species (A. cristatellus and A. sagrei) that exhibit shorter male faces. They show, using a combination of developmental and molecular genetic techniques, that the extreme elongation of male heads in carolinensis lizards is not due to an androgen pathway (i.e., testosterone) or the somatropic axis (i.e., insulin-like growth factor). Instead, they found a significant shift in the estrogen pathway. Specifically, at sexual maturity, males decrease expression of estrogen receptors (erβ), which is the beginning of a signaling cascade, ultimately resulting in up-regulation of genes involved in skeletogenesis in the skull of males.

Figure 4 from Sanger et al. (2014), showing the molecular pathway underlying facial elongation in A. carolinensis.

Figure 4 from Sanger et al. (2014), showing the molecular pathway underlying facial elongation in A. carolinensis.

This identification of a novel mechanism for the development of sexual dimorphism will certainly stimulate further evo-devo research in anoles and beyond. For starters, is the same pathway responsible for male facial elongation in other species in the carolinensis clade, or are more ‘traditional’ mechanisms operating there? This important research highlights that investigators need to consider all aspects of signaling systems, including circulating hormones, their receptors, and signal cascades that result from activation of a particular pathway. Clearly this paper by Sanger et al. is an excellent step in the right direction for understanding how developmental pathways lead to adult difference in anoles, and it will also steer other investigators to consider a diversity of developmental mechanisms in their quest to elucidate how adults end up the way they do.

Sanger TJ, Seav SM, Tokita M, Langerhans RB, Ross LM, Losos JB, Abzhanov A. 2014. The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards. Proceedings of the Royal Society B 281:20140329.

It’s Time to Retire the Use of the Term “Squamate” from Public Discourse

Let’s face it, “squamate” doesn’t work. It’s an ugly word, and most people don’t know what it means–if anything, it conjures up “squamous cell carcinoma,” a type of skin cancer.

Slide1 More importantly, the term is not needed. Squamate comes from the scientific order Squamata, the lizards and snakes. But we know that snakes evolved from lizards–they are one type of lizard. In other words, lizards do not form a monophyletic group; they are paraphyletic with respect to snakes.

Does this remind you of any other major group of vertebrate? Say, birds and dinosaurs? We all know that birds evolved from dinosaurs, they are a type of dinosaur; dinosaurs are paraphyletic with respect to birds. And so, what is the solution to this problem? We now realize that birds are dinosaurs, members of the Dinosauria. Indeed, failing to recognize birds as a type of dinosaur commits the sin of paraphyly, obscuring the fact that some dinosaurs (in the old sense) are more closely related to birds than they are to some other dinosaurs.

And so, for the same reason, we should start referring to snakes as one type of lizards and, in turn, when we use the term “lizard,” we should understand that we are referring to snakes as well. In other words “Lizard” = Squamata. And, hence, we have no need to use the term “squamate” in common discourse.

 

How Anoles Sense Heat

Ahh, that warmth feels good.

We all know that many anoles species are very good at behaviorally regulating their body temperature by moving from an area that is too hot or too cold to another area that is just right. But how do they actually judge the thermal properties of a particular microsite? There’s been a lot of work on the sensation of temperature in mammals, but not so much in reptiles.

Recently, Erkin Kurganov and colleagues at the National Institutes of Natural Sciences, in Okazaki, Japan began to rectify this shortcoming, and their paper has just been published in Pflügers Archiv – European Journal of Physiology. Here’s the abstract: 

Transient receptor potential ankyrin 1 (TRPA1) is a member of the large TRP super family of ion channels and functions as a Ca2+-permeable nonselective cation channel that is activated by various noxious stimuli. TRPA1 was initially identified as a potential mediator of noxious cold stimuli in mammalian nociceptive sensory neurons, while TRPA1s from nonmammalian vertebrates (snakes, green anole lizards, and frogs) were recently reported to be activated by heat, but not cold stimulus. In this study, we examined detailed properties of the green anole TRPA1 channel (gaTRPA1) related to thermal and chemical stimulation in whole-cell and single-channel recordings. Heat activates gaTRPA1 with a temperature threshold for activation of 35.8 °C, while heat together with allyl isothiocyanate (AITC), a chemical agonist, had synergistic effects on gaTRPA1 channel activation in that either the temperature threshold or activating AITC concentration was reduced in the presence of the other stimulus. Significant heat-evoked gaTRPA1 activation was observed in the presence but not absence of extracellular Ca2+. gaTRPA1 channels were also activated by heat and AITC in excised membrane patches with an inside-out configuration. By comparing the kinetics of heat- and AITC-evoked singlechannel currents, we defined similarities and differences of gaTRPA1 channel responses to heat and AITC. We observed similar current-voltage relationship and unitary amplitudes for heat- and AITC-evoked currents and found that heat-activated currents showed shorter durations of both open and closed times. Our results suggest that the gaTRPA1 channel is directly activated by heat and chemical stimuli.

 

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