Invasive Anole Evolution

One of the major challenges of studying evolution is that animals tend to evolve over time periods that extend far beyond the lifetimes of the scientists who study them. Evolutionary biologists generally make do with reconstructing evolutionary histories via clues left over in the present, and with decades of technological innovation and creative science, this approach has led to a robust patchwork of theory. That said, it is always nice when a capable scientist is blessed with a rare opportunity to study evolution in nature in real time. One of the most memorable papers I've come across in recent years happens to be written about exactly this kind of blessing. Stroud et al.'s "Observing character displacement from process to pattern in a novel vertebrate community," from November 2024, is the fascinating result of the kind of crafty and opportunistic science that I find exhilarating. 

The paper rests on a significant body of theoretical work on adaptive radiation, which is a subject that is a little broad to be covered thoroughly in a casual blogpost (and probably beyond my capability in any format). For those unfamiliar with the concept and looking for some resources to check out, I recommend starting with the work of Dolph Schluter, i.e. the adaptive radiation GOAT, and/or Peter and Rosemary Grant's prolific research on the Darwin's finch study system. Darwin's finches are the textbook example of an adaptive radiation, but other famous examples exist, for instance the cichlids of the central African crater lakes, the silverswords of Hawaii, and--most relevant to today's paper--the Anolis lizards of the Caribbean.

Stroud et al.'s 2024 paper builds upon theoretical work done particularly by Jonathan B Losos on the Anolis lizard system, and I would therefore be remiss if I didn't at least mention Losos' classic 1998 paper "Contingency and Determinism in Replicated Adaptive Radiations of Island Lizards." In this paper Losos shows that on each major Caribbean island, several species of anoles exist and fall into consistent "ecomorphs," or categories of behavior, habitat use, and corresponding morphological characteristics. On each island, anoles consistently occupy six distinct microhabitats that Losos defined as "crown-giant, grass-bush, trunk, trunk-ground, and twig," based on which parts of trees these arboreal lizards primarily spend their time. Observing a system with such remarkably consistent ecomorphs across multiple islands and dozens of species, Losos judged only two explanations to be feasible: either anoles evolved once into these distinct niches and then spread from island to island (which would be the parsimonious option), or anoles colonizing each island were repeatedly and separately driven into the same ecomorph categories. If the former hypothesis were true, anoles in each ecomorph would be more related to anoles in the same ecomorph class across islands, whereas if the latter hypothesis were true, this pattern would not be detected. After some genetic tests, Losos showed that anole relatedness was no stronger among ecomorph classes across islands than across species within islands, and the likelihood of these patterns being driven by repeated and regular adaptive radiation skyrocketed. 

Using genetics and carefully collected behavioral and morphological data, Losos provided strong evidence of some degree of determinism in evolution, as well as the power of adaptive radiations in generating diverse natural forms. While a massive contribution to science, Losos' conclusions still relied on a theoretical reconstruction of past events, leaving adaptive radiation-heads such as myself yearning for real-time, observational confirmation. This is where Stroud et al. 2024 (finally) comes into the picture. Stroud and his collaborators were busy studying invasive anoles in South Florida when one of his study sites that initially only had brown anoles (Anolis sagrei) was invaded and eventually dominated by crested anoles (Anolis cristatellus). Stroud jumped on the opportunity to observe the early phases of these novel competitive interactions, as these two species don't overlap in their native ranges. He and his collaborators observed that while in allopatry, both crested and brown anoles were happy to spend their time occupying similar regions of the lower sections of tree trunks, only spending 2% of their time on the ground. In Lososian terms, both species instantiated the same ecomorph class. In sympatry however, Stroud et al. were able to show that cristatellus individuals moved further up the trunk and sagrei further down, to the point where sagrei individuals were observed spending an average of 33% of their time on the ground. Novel competition had driven these anoles into separate ecomorphs! Aside from these behavioral observations, Stroud et al. showed that the newly ground-dwelling sagrei had developed significantly longer fore and hindlimbs, a result that conforms perfectly to the morphological characterizations made by Losos of Caribbean ground-dwelling ecomorphs. 

Fully-fledged adaptive radiations such as those found among anoles in the Caribbean may take thousands of years to develop, and what Stroud and his collaborators observed was character displacement, which is only a first step towards radiation. However, it is a crucial step, and one that is rarely observed so clearly in nature. The way that the results conform so exactly to the theoretical work laid out by Losos and others is also a lovely vindication of theory. Aside from these great qualities, as a biologist currently working in Florida, I also particularly love this paper because it draws a beautiful result from the invasive disaster zone that is South Florida and interrupts the steady stream of doomsday-level invasive news coming from that region with a terrifically exciting bit of science. 

Works Cited:

Stroud, J.T., et al. Observing character displacement from process to pattern in a novel vertebrate community. Nat Commun 15, 9862 (2024). https://doi.org/10.1038/s41467-024-54302-1
   
Losos, J. B., et al. Contingency and determinism in replicated adaptive radiations of Island Lizards. Science, vol. 279, no. 5359 (1998). https://doi.org/10.1126/science.279.5359.2115.

Snail Kites Prefer Escargot?

Two weeks ago I observed something quite unusual during a Snail Kite survey. I was tasked with meeting the project's Kissimmee area crew to survey a section of the Kissimmee river with them. As field lead of the state wide Snail Kite monitoring crew, I'm used to making some long drives to get to our daily surveys, but this site was only fifteen minutes from our field house. Basking in the luxury of a short drive, I rolled out of bed at the civilized hour of seven a.m., and met the crew for what I expected would be a short and kite-less survey. Kissimmee River can be an incredible spot to see kites when the river floods and creates a healthy floodplain. A rushing river is not much use to a Snail Kite, but when the grassy plains surrounding a river channel flood, shallow, vegetation-rich conditions can arise and provide perfect foraging habitat. A good rule of thumb for kite activity is too little water=no snails, while too much water=too deep for kites to successfully hunt snails. Anyway, in the fall the river floods, and in October we counted nearly 150 kites in one survey, which was among the highest counts we achieved in the state all month. Over the rest of the year however, water levels tend to drop, and our monthly surveys reflect the degraded conditions. Over winter, with water levels clearly already dwindling, we could muster a fifty kite survey, but across our last three spring and summer surveys, the river banks looked bone dry and we counted one measly, probably confused and disoriented kite. I had no reason to expect my most recent survey to be any different. 

As we launched our boat I planned to be on the water for no more than three hours, but rounding a bend in the river six miles in, I was rudely shocked. We came upon a section of the river where land managers had clearly done a prescribed burn recently, and my colleague Melisa pointed to a kite perched on some vegetation. "Oh nice," I thought, "at least we'll have one kite this survey." Shutting the boat off and pulling up to a steep river bank to inspect the bird more closely, I called out to Sandy, who on this day was recording data for us, and I asked her to note one un-banded male kite on the datasheet. Melisa quickly and politely contradicted me by pointing out that the bird was actually a banded female kite. Slightly embarrassed, I double check, and am filled with righteous indignation when I realize I had not made any mistake! My kite had orange legs unmarked by the color bands we apply, a fully blue head, striking red eyes, a bright orange cere, and could not have been anything but adult male. Before I had a chance to argue, it became clear that we were simply looking at different birds. After a cursory scan of the burnt area of the river bank, the three of us realized there were not one, not two, but dozens of kites present. 

What the hell was going on? Prescribed burns provide a whole bunch of ecological benefits, but I had never heard of them helping Snail Kites. Everything I knew about the species told me they need nice, shallow, freshwater wetlands where they can hunt live snails, but here I was watching them in a half mile section of bone dry, scorched, floodplain, scavenging dead apple snails. Melisa and I disembarked on the river bank while Sandy was left with the unenviable task of hanging back to make sure our airboat didn't float away down the river. Sensing I was witnessing an unusual ecological event, I took pictures of the chalky, scorched snail shells and their boiled meat, along with the coal-black mud and stripped bases of plant stems that the dead snails were resting on top of, and then I got to work counting kites. When so many kites are swirling around, actively hunting (or scavenging in this case), and territorially chasing each other, my job becomes quite tricky. In moments like these it's crucial to have a cool, calm, and collected voice assisting you, and luckily, as I was stressing myself out trying to keep track of which kites I had counted and which I hadn't got to yet, Melisa was my guiding light. With her help, after about an hour and a half, we were pretty confident in our count of fifty three total birds. 

After finally getting an accurate count, we continued with the remaining thirty miles of our survey track down the river channel, which turned out about as I expected it to that morning. The unburned river banks were lush and thick, and while beautiful to look at, would have completely concealed the scant puddles of water where apple snails may or may not have been eking out an existence, preventing kite foraging. We saw only two other kites for the rest of our survey. On my drive home that afternoon, I texted my boss to see if she had ever heard of kites scavenging dead snails on this scale, and she hadn't. Performing a cursory literature search online, I did not find any published accounts of such behavior either. 

Hopefully we'll be able to publish some account of this experience in a scientific journal, and maybe more experienced scientists than I can shed some light on this. For what it's worth, with my two years of involvement in this project, my best guess would be that the terrible drought plaguing the state is probably the root cause of this novel foraging strategy. Already, over the last few months, we have been making note of increased instances of unusual foraging. While apple snails make up ~99% of Snail Kite's typical diet, lately, we've observed unusually high instances of them deviating and eating musk turtles, dead fish, a few dead birds, some kind of large crab (pictured below), and now this scorched snail feeding frenzy. We have also observed some fierce intraspecific fighting, which I'm told is also generally uncommon for these kites, and may be another sign of resource scarcity and increased competition. Concealed within the excitement of observing a new and unexpected behavior, it's hard to avoid feeling that the root cause is related to degrading kite conditions throughout the state. 

Curious Side Effects of Invasive Species

I am currently working as the field crew lead of the University of Florida’s Snail Kite monitoring project, which comes with several perks. The most obvious is that I have the daily privilege of getting to zip around on airboats through beautiful, remote, wetland habitat across the southern half of Florida. I spend hours a day observing and occasionally handling and banding Snail Kites, which are unique and beautiful birds that I can’t imagine ever tiring of watching. On our crew we sometimes joke about how they lack the intimidating presence of a typical bird of prey; they’re simply too goofy. While they spend their days deftly plucking apple snails from fresh water marshes, unthreatening to anything other than their mollusk victims (outside of the rare times they find an unlucky musk turtle to gruesomely excavate and consume), in this cruel and unforgiving world of ours they still get relentlessly mobbed by grackles and red-winged blackbirds, as if they were any other egg-stealing, fledgling-hunting, run-of-the-mill bird of prey. Their strained, nasal, almost mechanical calls are another incongruity separating them from their raptor relatives, but as with their other quirks, they are simply delightful. It’s definitely worth a Google if you’ve never heard the various calls they make, by the way.    

Young male Snail Kite with a musk turtle. ~99% of their diet is made up of apple snails but they will rarely catch other prey.

Getting back to the point, one of the other major benefits of my job is that I get to be part of one of the longest running wildlife monitoring projects in the country, and I can claim some association with the incredible wealth of research that biologists in the lab have been putting out about Snail Kites for decades. A few years ago, the UF Snail Kite lab published a paper that was exciting enough to generate a certain amount of mainstream attention. Cattau et al.’s 2018 paper, “Rapid morphological change of a top predator with the invasion of novel prey,” has been covered by all sorts of outlets including the New York Times. The paper is an elegant and reassuring example of what the daily toil of my field crew and the many field crews before us can contribute to. Cattau et al. analyzed the previous 11 years of meticulously collected nestling morphological data and coupled it with quantitative genetic analyses to show conclusively that since the invasion of the larger Chinese apple snail species into Florida in the late 2000s, Snail Kites had grown significantly larger beaks, talons, and tarsi. A fascinating result, especially given that in 2007, just 11 years before Cattau et al.’s paper, Snail Kite researchers Darby et al. published “Food-handling Difficulties for Snail Kites Capturing Non-native Snails,” in which they recount numerous observations of kites dropping the significantly larger Asian snails and otherwise failing to extract their meat. In a matter of a mere 11 years, researchers went from worrying about invasive snails acting as ecological traps that could hurt the kite population, to showing clearly that kites have adapted in a very short time span and are now actually benefiting from their new invasive prey.

A crucial and underrepresented detail I want to highlight from the paper is that the researchers make it very clear that these morphological changes come not quite from strict evolution but from phenotypic plasticity. The quantitative genetic analyses they used show that the genetic components of these traits did not significantly change over their study period. This suggests that “cryptic genetic variation,” e.g. preexisting variation in the population that is only made visible phenotypically by some novel environmental condition, is primarily behind the rapid shift. Researchers point to the increased overall growth rate in kite nestlings in areas with higher invasive snail availability as an indication that this richer food source may be triggering a shift to longer beaks and talons somewhat incidentally. They also highlight that these traits show a high degree of “additive genetic variance,” which is the genetic heritability component that is uncluttered by epistatic and dominance effects and otherwise known as “narrow-sense heritability.” This is good news for the kites since it means that real evolution in the form of genetic change may be easier/faster to generate in these traits, compared to a situation where more complicated dominance and epistatic hierarchies among alleles were involved and slowing down the adaptive process.  

Even though phenotypic plasticity is not technically evolution, this rapid morphological change is an incredible example of how the complex web of interactions between genes, phenotypes, and the environment is always changing and bringing about unique forms of life. Human beings are challenging wildlife in ways that go beyond habitat degradation and destruction and include the reshuffling of wildlife interactions via the promulgation of invasive species, and native wildlife must be resilient. In many cases these changes only bring devastation, but it is nice from time to time to read about a positive case, especially when it involves a species as unique and wonderful as the Snail Kite.

Citations:

Cattau, C.E., Fletcher Jr, R.J., Kimball, R.T. et al. Rapid morphological change of a top predator with the invasion of a novel prey. Nat Ecol Evol 2, 108–115 (2018).

Darby, Philip C., David J. Mellow, and Miranda L. Watford. Food-handling difficulties for Snail Kites capturing non-native apple snails. Florida Field Naturalist 35.3 (2007): 2.