Author: Ambika Kamath Page 2 of 6

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.

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

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?

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. 

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

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 while—will 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

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

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.

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 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.

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.

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.

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:

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

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

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

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.

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. gundlachi. The use of the dewlap by females has been observed during male-female interactions in A. cristatellus, A. 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!

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.

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…).

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?

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.

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).

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):

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!

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; F_1,1=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.

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

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