Female Anolis sagrei
In recent months, there has been a lot of talk on the Auburn campus about multimodal signals. Diana Hews gave a phenomenal seminar to the Biology Department last November about complex signaling in Sceloporus lizards, and just last week Eileen Hebets told a similar story about signaling behavior in a group of invertebrates, amblypygids. The latter lecture prompted a momentary side conversation between a Warner Lab postdoc, Tim Mitchell, and me concerning the apparent lack of multimodality in Anolis signaling. Ironically, I just ran across a 2016 publication by Baeckens et al that forced me to eat crow, albeit only a tiny bit of crow.
Anoles, like most iguanians, have been labeled as “visual only” signalers and for good reason. Anoles lack the epidermal glands that secrete the typical chemicals used in lizard chemosensing. Rather, anoles are known widely as models for communication for their reliance on visual signals (which have been demonstrated to be quite complex despite being unimodal) and are also characterized by a low baseline rate of tongue-flicking, even when considered against the backdrop of other visually oriented iguanians. Additionally, previous experiments conducted with A. carolinensis found no significant evidence of chemosensory function in prey selection, assessment of opponents, or in mate choice (Jaslow & Pallera, 1990; Forster et al., 2005; Orrel & Jenssen, 2002). The question of whether or not anoles utilize chemical signals seems to be one answered; however, Baeckens et al have conducted a simple but convincing study that might demonstrate the converse.
Fig 1. (A) Male signaling behavior (DE – Dewlap, HN – Headbob, PU – pushup) and Tongue flicking (TE) in a control cage (white) and one previously occupied by a female (black). (B) Overall display behavior and Locomotor activity under both control and experimental conditions.
Each of 14 male A. sagrei were placed alone into an enclosure with opaque walls on all sides (though one wall was coated with a dark window film so males could be observed). This was done under two different conditions. On one occasion, the enclosure had been recently cleaned with ethanol and on the other, the cage had previously housed several female sagrei for at least eight hours. The females were then removed just five minutes prior to the male’s introduction. The placement of males in each treatment was randomized; however, each male was subjected to both conditions and cages were cleaned between trials. During each trial, the researchers measured the amount of signaling (number of headbobs, dewlaps, pushups) and exploratory behavior (number of tongue extrusions and locomotor behavior) performed by the male being tested. They found that males displayed significantly more dewlap extensions and headbobs as well as more tongue flicks and locomotor activity when placed in a novel cage that had recently housed female anoles than when placed in a control cage (Fig 1). This, they claim, “[constitutes] the first evidence of intersexual chemo-sensation in an anoline lizard.”
Though intriguing, these data cannot be separated from the immense body of literature that overwhelmingly demonstrates the reliance of anoles on visual communication. for example, even though males in this study performed many more displays when in a cage previously occupied by a female, other studies (i.e. Driessens, Vanhooydonck & Van Damme, 2013) demonstrate that signaling behavior can still be as much as nine times greater than that observed in the current study when males have visual contact with a female, and thus chemosensory functions that may be in play still pale in comparison to the use of visual signaling. What is yet to be determined is the ecological relevance of such signaling and the extent to which it may enhance visual signals. One proposed explanation for the importance of multimodal signaling is that each signal alone does not produce the magnitude of response that the two signals produce together. It will be for future studies to determine if visual signaling in anoline lizards is somehow enhanced by chemosensory function. The results of this study, however, are quite enticing and further illustrate why anoles make phenomenal models for studying communication.
assorted facets of the dewlap, in both sexes of Anolis sagrei. Behavioral Ecology and
Sociobiology 69:1251–1264
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Kurt Schwenk
Very nice summary Joshua! I think that one of the problems here is one that pops up everywhere—over-generalization. The notion that anoles are “anosmic” goes way back in the literature (at least to Armstrong, Gamble & Goldby, 1953) and the literature since has been, to some extent, guilty of affirmation bias. As a rule, when compared to most other squamate taxa, anoles are unquestionably down at the low-chemosensory/high visual end of things, but the point here is that not anoles are the same. When one starts looking at the histology of the vomeronasal organs, which I have some data on, there is more than trivial variation among species in its relative development. This is manifested in variation in rates of spontaneous tongue-flicking. I think we might end up being surprised about the level of chemoreception employed by some species. Joshua’s suggestion that there may be a synergy when combining signal types is right on, but it is also true that chemical signals are useful in many contexts that do not allow visual communication—and chemical signals persist in the environment for a relatively long time. So there may be stronger selection than we imagine for some species of anole to maintain functional vomeronasal systems. Certainly their gustatory (taste) system remains in full force (Schwenk, 1985). Almost nothing is known about nasal olfaction in the group, although it is true that their olfactory bulbs are very small (but again, no comparative data). So basically I’m saying that chemoreception is strong enough in anoles to suggest that Losos’ entire career has pretty much been pointless. Oh well.
George Gorman
An interesting analysis. This appears to demonstrate a response to an olfactory stimulus. But why test males with only females as former occupants?
Visual Male-Male interactions are easily induced experimentally with a mirror or a film loop… Couldn’t a chemical signal be triggering a defensive reaction ? Are the test males responding to conspecific females, or simply to conspecifics? And then carrying it one step further; what kind a response would you generate if the cages held females of other (closely related or distantly related) anole species…. or other unrelated lizards?
Josh Hall
George, you’ve pointed out several questions that I had when reading the study. Hard to overstate how simple the design was here. I think the simplicity may be one reason it wasn’t published in a higher impact journal. It would have been really easy to replicate the design across a variety of species. Well, I say that but these researchers are not from the same part of the world as anoles. I should rephrase and say it would have been easy to do a species comparison if you live in South Florida! The animals they utilized were actually collected in Florida and purchased from a pet store.
As alluded to by Kurt, anoles represent a diverse group and too much extrapolation occurs from studies done on carolinensis and the other few, yet intensively studied species. This seems like an understudied aspect of basic natural history in the group and maybe this simple paper will spark some interest and generate some new data.