All posts by Ambika Kamath

About Ambika Kamath

I'm a graduate student at Harvard University, interested in behavioural ecology and evolution.

How Do We Know What We Know? Sexual Selection, in Humans and in Lizards

Reposted from my blog.

Over the last few months, there’s been a slow-boiling battle underway between Holly Dunsworth and Jerry Coyne about the evolution of sexual dimorphism in humans, surrounding the question of why male and female humans, on average, differ in size. The battlefield ranged from blogposts to twitter to magazine articles. In a nutshell, Coyne argued that “sexual dimorphism for body size (difference between men and women) in humans is most likely explained by sexual selection” because “males compete for females, and greater size and strength give males an advantage.” His whole argument was motivated by this notion that certain Leftists ignore facts about the biology of sex differences because of their ideological fears, and are therefore being unscientific.

Dunsworth’s response to Coyne’s position was that “it’s not that Jerry Coyne’s facts aren’t necessarily facts, or whatever. It’s that this point of view is too simple and is obviously biased toward some stories, ignoring others. And this particular one he shares…has been the same old story for a long long time.” Dunsworth went on to propose, seemingly off the cuff, alternative hypotheses for sexual dimorphism in body size in humans that were focussed not on men but on women, as examples of the kind of hypothesis that is relatively rarely considered or tested in this field.

Though on the surface this battle may seem to be about specific biological facts (Coyne certainly tries to win by treating it that way), in reality this disagreement is, as Dunsworth argues, about the process by which hypotheses are tested and about how knowledge comes into existence. About which hypotheses are considered for testing in the first place. As a result, the two ended up arguing past each other quite a bit.

As I followed this whole exchange, I shook my head at the timing–I had a paper in preparation that was SO RELEVANT to the centre of this debate! That paper is now available as a preprint, so I can try to outline why I think that Dunsworth is right, and Coyne is being short-sighted. My argument has *nothing* to do with humans, however–I don’t know the human sexual selection literature well enough to weigh in on that. Instead, my argument is by analogy with our knowledge of mating systems in Anolis lizards.

Continue reading How Do We Know What We Know? Sexual Selection, in Humans and in Lizards

Insights from Three Years of Measuring Anolis sagrei Reproductive Success

Female Festive Anole (photo: Ambika Kamath)

Female Festive Anole (photo: Ambika Kamath)

Sexual dimorphism–differences between the sexes in what they look like–is rampant across animals. But how do these differences arise? Why and how might natural selection or sexual selection act differently on males and females? In a new paper from Duryea et al. (2016) published last month, we begin to see what answers to these questions look like in our very favourite organism, the festive anole, Anolis sagrei.

The data presented in this paper is unprecedented in anoles–by catching every lizard on Kidd Cay for four successive years, the authors assigned parentage to three generations of offspring, and thus assigned reproductive success to three generations of adults. Using these measures of reproductive success for males and females, they ask a straightforward question: is reproductive success correlated with body size, and do these relationships differ between males and females?

The results, however, are not straightforward: patterns of selection differ quite a bit across the three years of sampling, especially in females. But overall, we see directional selection on body size in males (bigger males father more offspring who survive to adulthood than smaller males), possibly explaining why male festive anoles are 30% larger than females.

We don’t yet understand the origins of sexual size dimorphism in anoles–why in particular, does the shape of selection on female body size vary so much? Do large males sire more offspring who survive to adulthood because they mate more often, or because their offspring are somehow better at surviving? Duryea et al. have propelled forward the state of our knowledge with a formidable dataset that raises exciting new questions.

Some Thoughts on Display Evolution in Fan-Throated Lizards

Some weeks ago, a paper I wrote on the display behaviour and morphology of fan-throated lizards was published early online at the Journal of Herpetology. Some unfortunate timing meant that my paper did not incorporate these lizards’ new taxonomy, recently published by V. Deepak and colleagues. In this post, I’m going to summarize my results, and explore them in the context of what we now know about Sitana (Agamidae) systematics.

Male fan-throated lizards (surprise, surprise) have fans under their throats that are displayed in a manner analogous to the Anolis dewlap. The appearance of the throat-fan varies dramatically across this group, from small and mostly white to large and blue, black, and orange. I wanted to answer two broad questions

  1. Does display behaviour vary with throat-fan morphology? In other words, if you have different tools with which to communicate, do you communicate differently?
  2. Can we examine morphological and environmental variation to deduce anything about how this variation in throat-fan morphology has evolved?
Figure 1 from my paper, showing sampled sites and throat-fan variants.

Figure 1 from my paper, showing sampled sites and throat-fan variants.

To address these two questions, I measured the display behaviour, morphology, and environment of eight populations of lizards, from three “throat-fan variants.” I found the following:

  1. The main axis of variation in display behaviour differed between the coloured-fan variant and everybody else. Displays were fewer and longer in the coloured-fan variant, and included more head twists. The same axis of display behaviour did not differ between the white-fan and the intermediate-fan variants, though there was variation in the frequency of head-bobs across populations with different-sized throat-fans. These differences in display behaviour make sense in light of morphology. Head twisting was more frequent in the variant with a large blue section on the throat-fan that appears iridescent. Head-bobs, which often co-occur with a fully extended throat-fan, were more frequent in the variant(s) with smaller throat-fans (see Figure 6 in my paper for more).
  2. Throat-fan elaboration (both size and colour) was paired with increased male-biased sexual size dimorphism, suggesting sexual selection as a likely selective force driving throat-fan variation.
  3. Habitat structure did not co-vary with throat-fan morphology, suggesting that the visual environment is unlikely to play much of a role in the maintenance of this variation in throat-fan morphology. But because these lizards all persist in human-modified landscapes, it is difficult to discern how important the visual environment was for the origin of dewlap diversification in this group.
Figure 2 from Deepak et al. 2016.

Figure 2 from Deepak et al. 2016.

Based on geography, I can tell that all three of the coloured-fan variant populations I sampled belong to the newly described Sarada darwinii. The white-fan populations are Sitana laticeps and Sitana spinaecephalus (+ one population I’m not sure about), and the northern and southern intermediate-fan populations are Sitana ponticeriana and Sitana visiri respectively. Recast in terms of these species delimitations, I found that:

  1. Display behaviour differs between the genera Sitana and Sarada. It doesn’t vary consistently with species within Sitana, though variation in head-bobbing should be explored further.
  2. There are two broad possibilities for throat-fan evolution in the group. One possibility is that throat-fan elaboration and a shift towards male-biased SSD has evolved independently twice, once in Sarada (Clade 1) and once in the South India/Sri Lanka clade (Clade 3 in the phylogeny) in Sitana. The other possibility is the reduction of dewlap size and colour in the west Indian Sitana clade (Clade 2). This question won’t be definitively answerable until we have a phylogeny that includes the remaining north-eastern species of Sitana as well as more species of the sister genus Otocryptis, which also vary in the presence and morphology of the throat-fan.

Before knowing about the phylogeny, I predicted that throat-fan elaboration had evolved twice in fan-throated lizards, based on a suite of differences between the coloured-fan variant (now Sarada) and the intermediate-fan variant (now Sitana Clade 3). The main ones are:

  1. Different display behaviour.
  2. Different allometric relationships between body size and throat-fan size, suggesting different ways in which throat-fans have gotten big.
  3. Different spectral reflectances from the blue and orange patches, plus the presence/absence of black on the throat-fan.
  4. The ability of Sitana, but not Sarada, to turn “on” and “off” the blue colour on their throat-fans (more about this in a future post!).

These differences now lead me to favour the first of the two possibilities outlined above: repeated, somewhat parallel evolution of throat-fan elaboration, as opposed to the loss of an elaborate throat-fan. Given that the sister genus Otocryptis has also either evolved or lost a throat-fan (throat-fans are present in O. nigristima and O. wiegmanni but not O. beddomi), this group is positively rife with lability in display evolution, offering all sorts of exciting possibilities for future research!

Nocturnal Behavior in the Green Anole

I’m currently reading a 274 page tome called “The Biology and Biodemography of Anolis carolinensis” by Robert E. Gordon. Dating back to 1956, this impressive piece of scholarship is Gordon’s Ph.D. thesis. Gordon collected the bulk of his data in biweekly nocturnal surveys of the demography and spatial ecology of two populations of green anoles. The surveys continued for over a year, and consequently, this document is filled with insights into these lizards’ ecology.

One sentence that caught my attention was this, from page 195:

Anolis activity is primarily diurnal, although movement and feeding were observed at night under conditions of bright moonlight.

We’ve had observations of anoles feeding at artificial lights before, but have any of you night-owl herpers observed something similar under natural light?

A figure from Gordon (1956). Can we bring back this elegant asymmetric bar graph plotting style?

A figure from Gordon (1956). Can we please bring back this elegant asymmetric bar graph plotting style?

 

A New Genus and Five New Species of Fan-Throated Lizards

 

Dewlap morphology and colouration of Fan-throated lizards. Clade 1: A. Sarada darwini sp. nov., B. Sarada deccanensis comb. nov., C. Sitana superba sp. nov.; Clade 2: D. Sitana spinaecephalus sp. nov., E. Sitana laticeps sp. nov.; Clade 3: F. Sitana ponticeriana, G. Sitana visiri sp. nov., H. Sitana cf. bahiri. Scale bar = 10 mm

Dewlap morphology and colouration of Fan-throated lizards. Clade 1: A. Sarada darwini sp. nov., B. Sarada deccanensis comb. nov., C. Sitana superba sp. nov.; Clade 2: D. Sitana spinaecephalus sp. nov., E. Sitana laticeps sp. nov.; Clade 3: F. Sitana ponticeriana, G. Sitana visiri sp. nov., H. Sitana cf. bahiri. Scale bar = 10 mm

V. Deepak and his colleagues from five different institutions in India have published a revision of the systematics of fan-throated lizards in India. This work nicely expands on the project of figuring out the diversity of this clade of magnificent lizards, following the description of two new species from Sri Lanka last year.

I’ll be writing more about this paper and these lizards in weeks to come, but for now, here’s a figure from the paper, and below, the abstract!

Abstract

We revise the taxonomy of the agamid genus Sitana Cuvier, 1829, a widely distributed terrestrial lizard from the Indian subcontinent based on detailed comparative analyses of external morphology, osteology and molecular data. We sampled 81 locations spread over 160,000 km<sup>2</sup> in Peninsular India including type localities, which represented two known and five previously undescribed species. Based on general similarity in body shape and dewlap all species were hitherto identified as members of the genus Sitana. However, Sitana deccanensis and two other morphotypes, which are endemic to north Karnataka and Maharashtra in Peninsular India, are very distinct from the rest of the known members of the genus Sitana based on their external morphology and osteology. Moreover, members of this distinct morphological group were monophyletic in the molecular tree, and this clade (clade 1) was sister to two well-supported clades (2 and 3) constituting the rest of the Sitana. The interclade genetic divergence in mtDNA between clade 1 and clades 2 and 3 was 21-23%, whereas clade 2 and clade 3 exhibited 14- 16% genetic divergence. Thus, we designate a new genus name “Sarada” gen. nov. for species represented in Clade 1, which also includes the recently resurrected Sitana deccanensis. We describe two new species in Sarada gen. nov. and three new species in Sitana. Similarity in the dewlap of Sitana and Sarada gen. nov. is attributed to similar function (sexual signaling) and similarity in body shape is attributed to a similar terrestrial life style and/or common ancestry.

Anole Barely Moves While Snail Speeds Past

Anyone who studies animals behaving in their natural environments knows just how long they can spend doing nothing much. This is most definitely true of anoles as well. My colleague Jon Suh learnt this first hand last summer while working with me on Anolis sagrei in Florida. I think his video (from data he collected on lizard display variation, and sped up by 500%) perfectly captures what it feels like to spend a long time watching a lizard doing almost nothing.

It’s Twins! Two Embryos in One Anolis sagrei Egg

For the last several months, I’ve been collecting eggs from 36 female Anolis sagrei from Gainesville, FL. This is for a project on linking the movement patterns and mating patterns of brown anoles. To be able to assess which males have mated with each of these females, I’ll be sequencing the DNA from the mothers, their offspring, and potential fathers, and then trying to figure out which males have fathered each female’s offspring. All this is to say that what I want from the eggs I’ve been collecting is the offspring’s DNA. To this end, I’ve been dissecting out embryos from eggs about ten days after laying, and storing the tissue for future genetic work.

So far, the females have laid over 300 eggs, and dissecting embryos out of them has gotten a little monotonous. So I didn’t pay any special attention to an egg that looked perhaps a bit bigger than normal. I was shocked, though, when two seemingly healthy embryos popped out of it!

Two embryos from a single brown anole egg

Two embryos from a single brown anole egg

My initial excitement waned when I realised that twins are not that rare in humans, but returned when two anole breeding experts (AA correspondents Thom Sanger and Anthony Geneva) said that they haven’t seen anything quite like this before. In Thom’s words, “I’ve only found two [twins] in over a decade of dissecting eggs, both were conjoined and inviable. I think you have something special.”

Have any of you seen anything like this before?

 

Movement Rates in Anolis carolinensis Redux (Or) We Need to Study Female Anoles!

Some months ago, I posted a quick analysis of a dataset from 2010 on the movement rates of green anoles (Anolis carolinensis) in the presence and absence of brown anoles (Anolis sagrei) on spoil islands in Mosquito Lagoon, FL. At Jonathan Losos’s urging, Yoel Stuart and I turned this blog post into a paper, which was recently published in Breviora.

The story has not changed since the blogpost (though the analyses are now slightly more sophisticated): male and female green anoles seem to respond differently in their movement behaviour to the presence of brown anoles. There are many possible reasons for these differences, discussed in the paper, that can be summarized as “variation in the motivation for movement between the sexes.” Do read the paper if you’re interested in further details, but be forewarned that we engage in quite a bit of speculation because of one simple fact: compared to what is known about movement rates of male anoles, we know much less about how movement rates in female anoles vary with microhabitat.* Similar disparities between what we know about males and females exist in other aspects of anole biology too.

Though the subject matter of our paper is rather niche (anole ecology pun intended), it contains one paragraph that I think is more broadly pertinent:

 Much more attention has been paid to the behavioral ecology of male anoles than to that of female anoles (Butler et al., 2007; Losos, 2009). Our results suggest that male and female anoles can differ in their behavioral responses to ecological pressures. Understanding the mechanisms leading to behavioral and ecological variation within a species will therefore depend upon documenting this variation in both males and females, a conclusion that is hardly surprising. It is disappointing that research on fundamental aspects of the biology of even organisms as well-studied as Anolis lizards remains largely focused on males

There are reasonable reasons for focussing research on males. Male anoles are indeed often easier to spot in the field, and are certainly easier to catch. And incorporating an effect of sex into our statisical models will require us to double our sample sizes. But in many species, observing and catching females isn’t so difficult as to excuse not studying them. For example, in the last month or so, my undergraduate collaborator Rachel Moon and field assistant Barbara Da Silva have measured the ecology and morphology of over 300 Anolis sagrei females—an enviable sample size in any circumstances.

Females have been ignored in all sorts of studies of all sorts of organisms. The absence of female subjects in biomedical trials, for instance, has far more serious consequences than the gaps in our knowledge of the biology of female anoles. Nonetheless, given that many of us are dedicating some portion of our lives to understanding these animals, making sure that we don’t ignore half of them seems like a worthwhile goal. IMG_3060

*This gap exists for two reasons: some previous studies don’t sample females, others sample both sexes but don’t distinguish between them.

Are Brown Anoles in Florida Really Driving Green Anoles to Extinction?

Tell almost anyone in Florida that you’re doing research on brown anoles (Anolis sagrei), and they’ll express some distaste for your study organism. “I don’t like them,” they’ll say, “they’re invasive. Aren’t they driving the native green anoles extinct?” Everyone—literally everyone who has lived in Florida for a whilewill tell you how their backyards used to be full of green anoles (Anolis carolinensis). Today, they report, these green anoles have disappeared and been replaced by the invading browns.

Green anoles, increasingly elusive in Florida

Green anoles, increasingly elusive in Florida

These backyard tales are supported by some scientific evidence for shrinking populations of green anoles . On spoil islands in Mosquito Lagoon, Dr. Todd Campbell documented precipitous declines in green anole densities following the experimental introduction of brown anoles [1]. In southwest Florida, Cassani et al. repeated surveys of reptile and amphibian abundance fifteen years apart, using identical methods in exactly the same locations [2].  They found a drop in green anole numbers and a sharp rise in brown anole numbers between 1995 and 2011. Based on their results, both Campbell and Cassani et al. suggest that the persistence of green anoles in Florida has been jeopardized by the invasion and spread of brown anoles.

But both Campbell and Cassani et al. acknowledge a second possible explanation for the apparent disappearance of the green anoles: the lizards may simply have shifted upwards, out of sight.* As Cassani et al. put it, “the hope remains that these lizards persist in the face of competition and predation from A. sagrei by shifting habitat use.” We already know that green anoles shift upwards at least a bit in the presence of brown anoles, and have evolved morphological features that likely help them survive at these higher perches [3]. Could green anoles have shifted so high as to be nearly invisible to us, from our vantage points near the ground?

A bead-tagged brown anole

A bead-tagged brown anole

When I started studying brown anoles in Gainesville, FL, in 2014, I was convinced that the green anoles were all gone. But as we spent many hours marking individual brown anoles and repeatedly surveying their habitat to re-spot them, we began to spot a few green anoles too. I guessed that these green anoles were the last few holdouts against the invaders, and that we were seeing the same individuals again and again. To prove this, all we needed to do was catch and individually mark these green anoles using permanent bead-tags, in exactly the same way that we were catching and marking the brown anoles. It didn’t seem like too much extra work, so once I realised that my 2015 fieldsite was also home to quite a few green anoles, we began catching and tagging them as well.

In two months of sampling,  we either caught or re-spotted green anoles a mere 52 times. In the same period and location, we caught or re-spotted brown anoles 4369 times, which certainly seems to suggest more brown anoles than green anoles in this site. But to compare the population sizes of brown and green anoles, you need to compare how often you see new, unmarked individuals relative to how often you see already-marked individuals for each species**. In the graphs below, I’ve plotted the total number of observations against the total number of marked individuals for both A. carolinensis and A. sagrei***, and then zoomed in to just the first 52 observations for both.

Accumulation curves

Zoomed in, you notice that the curves for the brown and green anoles look quite similar. If anything, we see more new individuals per observation for green anoles than for brown anoles. Neither of these curves has begun to plateau (i.e. we’re still seeing lots of new individuals), so we cannot quantify the difference in total population size of these two species. But these limited data suggest that this population of green anoles is not doing that badly.

The taller tree was home to at least three green anoles

The taller tree was home to at least three different green anoles

But if the population is doing okay, then why weren’t we spotting green anoles all that often? The most logical explanation is that the green anoles have shifted up to very high perches, and only rarely descend to heights at which we can observe and catch them easily. Moving a bit beyond the numbers, we find another piece of evidence that supports the idea of a perch height shift—of the 40 green anoles we caught, only eight were males!

We know that male anoles usually perch higher than female anoles [4], that female anoles will often search for and feed on insects on the ground, and that females must descend to the ground to lay their eggs. Males, on the other hand, often move to higher perches to display, seem to feed more opportunistically than females, and are not necessarily compelled to return to the ground after they hatch. Though sex ratios can deviate quite a bit from 1:1 in natural populations of anoles [5], it seems unlikely that a population of green anoles could be comprised of one male for every four females. Taking the sex differences in perch height into account, it makes sense that for every female green anole we spotted, there’s a male green anole perching really high up whom we simply did not see.

lizards

None of this means that green anole densities aren’t declining due to the presence of brown anoles in some habitats. In particular, because brown anoles can perch as high as 4 m off the ground, there may be many places in which green anoles previously thrived but where there is simply no “up” for them to escape to once the brown anoles arrive. I suspect that many backyards are exactly such places, and that some reports of local declines in green anole population sizes may in fact be well-founded.

But it’s also certainly possible that, in habitats with sufficiently tall trees, brown anoles are not driving green anoles to extinction. Instead, brown anoles may simply have precipitated a substantial upward shift in the perch height of green anoles towards their ancestral trunk-crown niche. It’s therefore possible that green anoles are thriving, just out of our sight. If that’s the case, then brown anoles don’t deserve quite so much of our animosity after all!

A brown anole perching pretty high.

A brown anole perching pretty high.

References:

[1] CAMPBELL, T.S. 2000. Analyses of the effects of an exotic lizard (Anolis sagrei) on a native lizard (Anolis carolinensis) in Florida, using islands as experimental units. Unpublished Ph.D. Thesis. Knoxville, USA, University of Tennessee

[2] CASSANI, J.R., D.A. CROSHAW, J. BOZZO, B. BROOKS, E.M. EVERHAM, D.W. CEILLEY, AND D. HANSON. 2015. Herpetofaunal community change in multiple habitats after fifteen years in a southwest Florida preserve, USA. PLoS One 10(5): e0125845.

[3] STUART, Y.E., T.S. CAMPBELL. P.A. HOHENLOHE, R.G. REYNOLDS, L.J. REVELL, AND J.B. LOSOS. 2014. Rapid evolution of a native species following invasion by a congener. Science 346: 463-466.

[4] SCHOENER, T.W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49: 704-726

[5] SCHOENER, T.W., AND A. SCHOENER. 1980. Densities, sex ratios, and population structure in four species of Bahamian Anolis lizards. Journal of Animal Ecology 49: 19-53.

*Cassani et al., in particular, trapped reptiles and amphibians in ground-level traps, and very likely missed many anoles. Campbell, however, did sample in arboreal habitats, and did not find this explanation compelling in the context of his study. Trees on the islands he sampled were relatively short (~6 m), “allowing the vertical habitat to be searched thoroughly with small binoculars and some healthy tree climbing.”

**The logic is this: once you’ve marked every individual in a population, you will only re-spot marked individuals and not see new individuals, and the size of your population  will be equal to the number of individuals you’ve marked. In reality, you’ll almost never mark every individual, but the rate at which you spot new individuals relative to the total number of individuals you observe (new and marked) can still be revealing. Say you have two populations, A and B. If population A is much smaller than population B, then you will reach the point of mostly re-spotting marked individuals and not seeing new individuals more quickly in population A than in population B.

We obviously could not catch every lizard, and we were better at catching brown anoles than green anoles, so don’t use these data for any serious estimates of population size. But, if anything, our relative inability to catch green anoles means that there are more green anoles in this site than we document.

***Sampling for A. sagrei began about a month before sampling for A. carolinensis, explaining the mismatch in numbers between graph and text.

Anole Research Cakes!

It’s been an eventful year in the Losos Lab–three members of the lab have successfully defended their Ph.D.s in 2014-2015! To celebrate their defences, lab member Talia Moore designed and made three wonderful cakes, each tailored to the research of the newly-minted Ph.D.

For Dr. Martha Muñoz, who studied the shift of high-altitude anoles’ perches from trees to rocks, we had this beauty:

photo 1

 

For Dr. Alexis Harrison, who studied the Anolis dewlap, primarily in A. sagrei:photo 2

And for Dr. Shane Campbell-Staton, who studies geographic variation in cold tolerance in the North American Anolis carolinensisa map with sampling locations rendered in sprinkles, and lizard popsicles!

shane cake

 

Brown Anole Eats a Fish!

This post is by Holly Brown, a grad student at UConn studying the visual ecology of wading birds.

The piscivorous brown anole

The piscivorous brown anole

I spent the day filming herons at the Florida Keys Wild Bird Center, in Key Largo, FL. While changing positions to get a better view of interesting foraging behaviors of a juvenile Little Blue Heron and a Snowy Egret — head-tilting and foot-raking, respectively — I noticed a mad dash on the ground, ahead of the path I walked. I looked down, and a little anole had scrambled from the shoreline over to take cover in some mangrove roots, which were protruding out of the mud. I didn’t think much of this at first. I continued to walk along the shoreline, to follow a foraging white morph Great Blue Heron. I began to walk back toward the territory of the little anole, and noticed, yet again, a mad dash at ground level, from the shoreline into the mangrove roots. Thinking it might be odd to see an anole at the water’s edge I tried to find the well-camouflaged lizard amidst the vegetation. What I found was a lizard the size of an anole, but with a seemingly large, round head. Upon further examination, I realized that it was two heads–one anole head and one fish head! The anole had caught a minnow, and the poor little minnow’s head was sticking out of its mouth…gills still flapping and all.

I study herons because I am interested in how vision-based predators compensate for visual challenges, such as glare or refraction, while hunting across the air-water interface. I may need to start studying anoles as well!

Video of a Fight Between Two Female Brown Anoles

Compared with our extensive knowledge of male-male interactions, we know very little about how females interact with one another. Adding to a growing set of observations, here is some video (taken by my field assistant and seasoned anole videographer Jon Suh) of two bead-tagged female brown anoles mid-battle.

Both females are recent arrivals to this particular tree, and the lizard that remains on the tree at the end is marginally bigger than the one who leaves. Though I don’t think we witnessed the full interaction, I think it’s interesting that the females didn’t use their dewlaps in the course of this fight. This seems to match up with Ellee Cook’s description of a fight between two female A. gundlachiThe use of the dewlap by females has been observed during male-female interactions in A. cristatellusA. armouri  and a few other species, but also during female-female interactions in some Central American anoles. Clearly we’ve got a long way to go before we characterize and understand agonistic encounters and display behaviour in female anoles!

A Sad Mystery: Dying Green Anoles In Gainesville

At the risk of developing the reputation of being the harbinger of bad news, I’m here to report what seems to be an epidemic of sorts afflicting the green anoles in Gainesville, FL. In the last two years in this town, veteran AA correspondent Thom Sanger and I have noticed a number of very sickly and dead Anolis carolinensis. Here are some photos from last summer:

A sickly green anole that died the next morning. Photo by Thom Sanger.

A sickly green anole that died the next morning. Photo by Thom Sanger.

Picture1

We saw these animals in the later summer months, and Thom wondered if they might have died from ingesting insects that had been contaminated with insecticides sprayed to control mosquitoes. But a few days ago, my field assistant Jon Suh saw another mysteriously dead green anole, and it’s too early in the year for it to be explained by pesticide. This was in my fieldsite in the UF campus, where I haven’t seen any cats. The lizard also didn’t appear to have any botflies or other large parasites on it (though I’m not sure what that blue spot is…).

DSCN0133

It’s worth noting that we have seen no dead brown anoles in the same sites, so it appears that the cause of these lizards’ demise is species specific. Also, we haven’t noticed any dead lizards in the state parks just outside the city, so it seems to be specific to urban areas. Does anyone have any ideas about what might be afflicting these lizards?

Two New Species of Fan-Throated Lizards from Sri Lanka

Fan-throated lizards (Sitana) are one of the Indian Subcontinent’s most widespread and charismatic lizards, found in many of the region’s drier, scrubbier habitats. Not surprisingly, lizards across this vast range vary dramatically, most strikingly in the size and coloration of the throat-fans for which they’re named. Everyone has long suspected that the lizards in this genus must belong to several different species, and Sitana taxonomy has been long overdue for an upheaval.

Coloured-fanned, intermediate-fanned, and white-fanned male Sitana ponticeriana. Photographs by Shrikant Ranade, Jahnavi Pai, and Jitendra Katre respectively.

Sitana from India. Photographs by Shrikant Ranade, Jahnavi Pai, and Jitendra Katre.

The beginning of the revolution is finally here! Amarasinghe et al. (2015) have just published descriptions of two new species of fan-throated lizards, both from Sri Lanka. The authors also clarify some of the very confusing taxonomic and nomenclatural history of Sitana, paving the way for a comprehensive revision of the whole genus.

As is customary, the species descriptions of Sitana bahiri and S. devakai presented in this paper are based largely on morphological traits, including scale counts and throat-fan size, and I refer you to the paper for the details. The two species also differ in where they’re found, the former restricted to south-eastern Sri Lanka, the latter to the north of the island, separated by the Mahaweli River and surrounding wetter regions. Most interestingly, from my perspective, the authors suggest that S. bahiri and S. devakai differ in the coloration of their throat-fan. Sitana devakai is said to have brighter red coloration as well as a black patch on the throat-fan, whereas S. bahiri is described to have lighter orange coloration and no black patch.

Sitana bahiri and Sitana devakai, two newly described species from Sri Lanka (photos from Amarasinghe et al 2015).

Sitana bahiri and Sitana devakai, two newly described species from Sri Lanka (photos from Amarasinghe et al 2015).

I’m not sure I’m completely convinced of this difference in coloration. Though the differences are apparent in the examples shown above, another photo of S. bahiri shows some black coloration on the throat-fan (Figure 2 in the paper). I’ve also seen variation from bleached orange to deep orange, if not red, coloration within a single population of Sitana in southern India (in what Amarasinghe et al. refer to as Sitana cf. devakai):

Sitana Dewlaps

Variation in orange coloration on the throat-fan of Sitana from the southern tip of India

The need of the hour for Sitana taxonomy is not only more comprehensive geographic sampling across the whole range of this genus but also close examination of intra-population variation. Moreover, phylogenetic methods for delimiting species and discovering  relationships between species will be necessary to understand both morphological evolution  and biogeographic patterns in this group. The two species described by Amarasinghe et al. (2015), as well as their clarifications of the descriptions of S. deccanensis and S. ponticeriana, are just the start of an exciting period for Sitana systematics, so stay tuned!

Movement Rates and Microhabitat in Anolis carolinensis

In an earlier post on anole foraging mode, Jonathan Losos remarked that “much remains to be learned about the specifics of anole foraging and how it differs among species.” One thing we do know, however, about fine-scale variation in foraging mode is that it can depend on microhabitat. Both interspecific and intraspecific variation in movement rates in anoles suggest that low-perching anoles in trunk-ground habitats move less frequently than high-perching anoles in arboreal trunk-crown habitats (Lister and Aguayo 1992; Cooper 2005; Johnson et al. 2008)

One reason that anoles may shift from low to high perches is the presence of a congener. In the spoil islands of Mosquito Lagoon, FL, Anolis carolinensis occurs either on its own or in sympatry with A. sagrei, and recent research by Stuart, Campbell and colleagues showed that the green anoles perch higher on two-species islands than on one-species islands. Back in 2010 as a field assistant on this project, I collected some data on the foraging mode of green anoles on five of these islands, to test the prediction that allopatric A. carolinensis that inhabit lower perches in trunk-ground microhabitats have lower movement rates than sympatric A. carolinensis that occupy higher perches in trunk-crown microhabitats. I used the standard measure of movement per minute (MPM) to quantify foraging mode from a total of 204 lizards (78 females and 126 males, 110 lizards from one-species islands and 94 from two-species islands).

Movement data are messy and MPM varies a lot across individuals, with coefficients of variation within islands ranging from 41% to 74%. Moreover, when one watches lizards go about their lives, one readily realizes that they move for many reasons other than to feed and that MPM is therefore better interpreted as an index of activity than as a measure of foraging per se (Perry 2007).

I found that females show the predicted increase in MPM with increased perch height when sympatric with A. sagrei, while males show the opposite pattern, with higher MPM in the absence of A. sagrei (there was something of an interaction between A. sagrei presence and sex in the ANOVA on island means of MPM for males and females; F1,1=4.02, p=0.09).

 

Means of island means of MPM for male and female green anoles in one-species and two-species islands in Mosquito Lagoon, FL.

Means of island means of MPM for male and female green anoles in one-species and two-species islands in Mosquito Lagoon, FL.

That males and females differ behaviorally in their response to A. sagrei is perhaps not surprising, as males and females have different motives for movement during the breeding season. Male anoles spend a majority of their time in the breeding season engaged in social interactions and forage only opportunistically. Females, on the other hand, spend most of their time foraging in both the breeding and the non-breeding seasons (Lister and Aguayo 1992; Jenssen et al. 1995; Nunez et al. 1997). The increase in MPM in sympatric females relative to allopatric females therefore suggests that lizards forage more actively at higher perches. In contrast, the decreased movement rates of males on two-species islands might result from male territories being smaller on two-species islands than on one-species islands, with fewer movements required to defend these territories.

Aside from these speculations, the results shown here only allow one to conclude that movement behaviour is complex. Discerning why an individual is moving at any given time, coupled with much larger sample sizes than obtained here, including repeated measurements of the same individuals moving in different contexts, will be crucial to furthering our understanding of fine-scale variation in movement rates and its relationship with microhabitat

IMG_3060

Citations

Cooper WE (2005) Ecomorphological variation in foraging behaviour by Puerto Rican Anolis lizards. Journal of Zoology 265: 133-139

Jenssen TA, Greenberg N, Hovde KA (1995) Behavioral profile of free-ranging male lizards, Anolis carolinensis, across breeding and post-breeding seasons. Herpetological Monographs 9: 41 – 62

Johnson MA, Leal M, Schettino LR, Lara AC, Revell LJ, Losos JB (2008) A phylogenetic perspective on foraging mode evolution and habitat use in West Indian Anolis lizards. Animal Behavior 75: 555-563

Lister BC, Aguayo AG (1992) Seasonality, predation, and the behaviour of a tropical mainland anole. Journal of Animal Ecology 61: 717-733

Nunez SC, Jenssen TA, Ersland K (1997) Female activity profile of a polygynous lizard (Anolis carolinensis): evidence of intersexual asymmetry. Behaviour 134: 205-223

Perry G (2007) Movement patterns in lizards: measurement, modality, and behavioral correlates. In: Reilly SM, McBrayer LB, and Miles DB (eds.) Lizard Ecology. Cambridge University Press, Cambridge pp 13-48

A Failed Anole Predation Attempt

In the wake of the distressing news that even monkeys eat anoles with abandon, it’s a relief to see that there are at least some creatures that try to eat anoles, but fail. A 1979 report in The Wilson Bulletin by van Riper et al.  describing the the habits of the Red-Whiskered Bulbul in Hawaii, says this about these birds’ attempts at saurophagy:

On August 3rd 1977, a bulbul was observed chasing a large (ca. 20 cm in length) chamelion (Anolis sp.) in a circular pattern down an octopus tree; it was unsuccessful in capturing the reptile.

Such a vivid image, one that’s noteworthy for two reasons. First, while data on successful predation events are rare, descriptions of failed predation attempts are even rarer.  As bulbuls are mostly frugivorous, it isn’t too surprising that this lizard got away.

Second, like the battle between anoles and day geckos that we’re all eagerly anticipating, this interaction between two invasives, a New World lizard and an Old World bird, epitomizes the Anthropocene.

Red Whiskered Bulbul in southern India. Photo by adrashajoisa on Wikimedia.

Red Whiskered Bulbul in southern India. Photo by adrashajoisa on Wikimedia.

Rapid Evolution in Anolis carolinensis Following the Invasion of Anolis sagrei

If the biology of Anolis lizards is a puzzle, then a new paper by Yoel Stuart, Todd Campbell and colleagues is a crucial piece. It’s a puzzle piece that not only contains a wealth of information when held up on its own, but also brings clarity to a broader picture of anole biology when fitted into place.

Anolis carolinensis on small spoil-islands in Florida are the subject of Stuart et al. (2014)

Anolis carolinensis on small spoil-islands in Florida are the subject of Stuart et al. (2014)

A tight relationship between microhabitat and morphology characterizes variation across Anolis species in the Caribbean.  Anole biologists have long suspected that negative interactions, such as competition, are responsible for driving different species into different microhabitats, with subsequent morphological  adaptation to these microhabitats over evolutionary time. But pinning down interspecific interactions as the cause of evolutionary divergence in microhabitat and morphology has been difficult.

Why is establishing this causality challenging?  Upon observing a pattern of consistent differences between populations of a species that occur in sympatry and allopatry with an interacting species, it seems logical to attribute this pattern to the presence of the interacting species. But many processes other than an evolutionary response to negative interspecific interactions can generate such a pattern–environments may differ between sympatric and allopatric populations in a way that drives the observed divergence, individuals from sympatric populations may all be similar only because they  are closely related to each other, the divergence may be a consequence of phenotypic plasticity, or most dishearteningly, the whole pattern may simply be due to chance.

Ruling out these alternatives seems a gargantuan undertaking. Indeed, as Stuart and Losos (2013) point out, in a review that serves as a nice companion piece to this study, only a small fraction of studies describing patterns of divergence between sympatric and allopatric populations tackle the problem of eliminating these alternatives and can thus conclude with confidence that interspecific interactions cause the divergence they observe. But Stuart et al. (2014) take on the challenge.

Like recent research by Helmus et al. (2014) that exploits human-mediated anole dispersal to test classic principles of island biogeography, Stuart et al.’s (2014) research is rooted firmly in the Anthropocene. Occupying centrestage is the interaction between Anolis carolinensis, native to the United States, and Anolis sagrei, a relatively recent invader. The stage itself comprises small man-made spoil islands in Florida, created in the 1950s. When Todd Campbell began this study in the 1990s, A. carolinensis occurred on many of these little islands. Campbell introduced A. sagrei to three islands, and watched how, over the next three years, A. sagrei numbers rose steadily and A. carolinensis shifted higher into the trees on invaded islands, while continuing to perch at lower heights on nearby un-invaded islands.

Lead authors Yoel Stuart and Todd Campbell boating between spoil islands in FL

Lead authors Yoel Stuart and Todd Campbell boating between spoil islands in FL

This rapid shift in microhabitat spurred Stuart and Campbell to return to the islands 15 years later (with a team of field assistants, of whom I was one!) to ask if A. carolinensis on invaded islands had subsequently diverged morphologically from conspecifics on un-invaded islands. By this time, A. sagrei had spread widely. Nevertheless, they found five un-invaded islands. A. carolinensis still perched lower on these un-invaded islands than on nearby invaded islands.

Across Caribbean anoles, species perching higher up on trees have larger toepads and more lamellae on these toepads than do species perching closer to the ground. Recapitulating this interspecific difference, Stuart et al. (2014) found that A. carolinensis on invaded islands had evolved larger toepads and more lamellae than lizards on un-invaded islands in about 20 generations, rapidly establishing a pattern of character displacement. But is this pattern caused by the presence of A. sagrei?

It seems almost criminal to squish into one paragraph everything that Stuart et al. (2014) did to rule out alternative explanations for the pattern of divergence. They reared hatchlings from invaded and un-invaded islands to rule out phenotypic plasticity as a cause for divergence, sequenced a mind-bogglingly large number of SNP loci to establish that A. carolinensis on invaded islands were not closely related to each other, and conducted intensive habitat surveys to rule out environmental differences between invaded and un-invaded islands. This mountain of work supports the idea that the presence of A. sagrei has driven the evolutionary divergence among sympatric and allopatric populations of A. carolinensis. It’s this mountain of work that makes Stuart et al. (2014) a tremendously satisfying paper. We now have a much firmer basis from which to suggest that interspecific interactions have driven patterns of ecomorphological diversification across Caribbean anoles.

But I personally think that this study’s most exciting implications arise from it defining more clearly a part of the anole biology puzzle that still remains relatively empty, namely our understanding of within-population, among-individual variation in microhabitat use and morphology, and the consequences of this variation for behavioural interactions. This summer I came across an A. carolinensis and A. sagrei perched together thus:

A. carolinensis perched below A. sagrei on the University of Florida campus in Gainesville.

A. carolinensis perched below A. sagrei on the University of Florida campus in Gainesville.

These particular lizards couldn’t care less for Stuart et al.’s (2014) findings–clearly, the effect demonstrated in this study is a population-level effect. But this leaves us with a gap between behavioural interactions and eco-evolutionary dynamics–how exactly do we transition from individual A. carolinensis that are content to perch below A. sagrei to a population-level shift in A. carolinensis perch height in the presence of A. sagrei? Reassuringly, the divergence that Stuart et al. (2014) document is so rapid that this question becomes tractable–their results  emphasize an opportunity to integrate behavioural timescale with eco-evolutionary timescales. We can now examine individual interspecific behavioural interactions  among anoles, safe in the knowledge that ecological and evolutionary responses are not far behind.

 

Editor’s Note (October 28, 2014): Yoel Stuart provides the first perspon perspective on the study on eco-evolutionary dynamics

Editor’s Note II (November 3, 2014): The most thorough press coverage of this paper was in the Orlando Sentinel which as an added bonus had two animated talking anoles explaining the results.

Editor’s Note III (November 4, 2014): Yoel Stuart provides a more in-depth description of the study on the Howard Hughes Medical Institute’s The Conversation

More Morphological Oddities in Anolis sagrei

A few months ago, I shared with you some of the odder morphological variations my field assistants and I encountered while measuring Anolis sagrei in Gainesville, FL. We went on to measure quite a few more lizards, and saw quite a few more oddities, as well as some fairly gruesome injuries. Here are some of my favourite examples:

1. A far better picture of a doubly-regenerated tail.

double regeneration

2. A jaw injury that resulted in the left and right sides of the jaws being dissociated from each other.

jaw injury

3. A cut hyoid. I imagine this lizard was no longer able to extend his dewlap.

hyoid

4. A nasty head injury. We saw this lizard three or four more times after we measured him, and his wound seemed to have healed up completely.

head injury

5. A brutal leg injury.

IMG_0430

6. A male with not only an impressive tail crest but also some nice red tail coloration.

tail crest

 

ABS 2014: A Novel Social Behaviour in Uromastyx Lizards

I’m a big believer in the utility of watching animals in their natural environment, and it’s therefore no surprise that one of my favourite talks at the Animal Behaviour Society 2014 meeting was based on many, many hours of painstaking observation of Uromastyx ornata lizards in the rocky, arid cliffs of the Eilat Mountains in Israel. Amos Bouskila of Ben Gurion University presented an exciting outcome of this tremendous observation effort—a novel social behaviour in the Ornate Spiny Tailed Lizard, a large agamid that ranges from Egypt to Saudi Arabia. Here’s a video  of this behaviour (starts at roughly 0:55) for National Geographic, filmed by Eyal Bartov.

This novel behaviour comprises an interaction between a male and a female, and includes the following steps:

1. The female flips over onto her back (or is pushed onto her back by the male, as in the video above).

2. The male walks over the female’s body a few times

3. The female rights herself and moves away.

The sequence of events can be initiated by either the male or the female (though it’s predominantly female initiated), occurs both before and after copulation, and continues to occur well into the nesting season. Bouskila therefore rejects the notion that the behaviour is related to copulation, and speculates that it instead relates to chemical signalling (males have enlarged femoral pores in this species) and that it functions to maintain pair bonds between these long-lived lizards. Further observation will tell if this exciting hypothesis holds true!

ABS 2014: Social Learning in an Australian Skink

Martin Whiting of Macquarie University began his talk at the Animal Behaviour Society 2014 meeting by lamenting how little we know about the social lives of lizards, especially when compared with mammals, certain insects and fish, and most of all, those pesky other reptiles, birds. But the more we examine lizard social behaviour and cognition, the more apparent it becomes that these animals are capable of substantially more complexity than we previously thought possible. Whiting presented some recent research on the Eastern Water Skink, Eulamprus quoyii, that bolsters this view.

Eastern Water Skink, from the Whiting Lab Page

Though not often social, many lizards, including Eastern Water Skinks, live at densities high enough to allow individuals to be within sight of each other. This is a sufficient prerequisite for social learning, defined as learning a task by observing others and modifying one’s own behaviour accordingly. Whiting asked whether Eastern Water Skinks were capable of social learning by training “demonstrater” individuals to perform certain tasks, letting “observer” individuals watch these demonstraters, and then measuring whether this exposure to the demonstraters enhanced the observers’ success at the task at hand.

The answers to Whiting’s questions were not simple. First, age matters—young individuals were twice as likely to demonstrate social learning than old individuals. Second, the task matters—lizards learnt to associate a colour with a food reward by watching others, but the prerequisite task of actually flipping over the coloured cap to access a mealworm was not spurred by observing other individuals do the same.

In the future, Whiting and his students hope to conduct similar experiments with a variety of lizard species that differ in their degree of sociality. These experiments will definitively address the role of learning in shaping the social lives of lizards, and I can’t wait to see they find!