Author: Joshua Hall

I am a postdoctoral fellow in Dan Warner's lab at Auburn University. More about me and my research interests can be found on my website: www.devoeco.weebly.com

Sperm of Anolis sagrei. Picture by Ariel Kahrl.

Caribbean anoles are making their way to Florida in all sorts of ways. Swimming across the sea is not one of them; however, once they arrive, some consistent and interesting patterns begin to emerge for something that swims inside them.

Sperm morphology can vary widely among individuals and between species, and this variation can be due to both intrinsic (genetic) and environmental factors. Large genetic variation in a trait means that the raw materials for evolution are abundant, and populations can diverge over space and time in relatively few generations. Much of this variation, however, could also be the result phenotypic plasticity since the environment that males experience during their lifetime can impact the shape and size of their sperm. Although previous studies have documented how sperm morphology can differ among populations, no studies have determined how introduction into novel habitats might influence this morphology.

Novel environments can influence traits through adaptive evolution, plastic responses to new conditions, or through random changes in gene frequencies (genetic drift and/or founder effects). Random changes in gene frequencies are likely to occur when populations expand into a new range because the founding population tends to be small and thus the gene pool is limited. By studying independent evolutionary trajectories (e.g. multiple species, or independent populations of the same species), we can rule out random changes in gene frequencies if the patterns we find are consistent among groups. As usual, anoles make excellent models for this work.

Ariel Kahrl and Bob Cox examined testis size and sperm morphology (head length, midpiece length, and tail length) for three species of Caribbean anoles (A. cristatellus, A. distichus, and A. sagrei) in their native ranges (Puerto Rico, Dominican Republic, Bahamas, respectively) as well as in Florida where each species is naturalized.

Although the results differed among species for some measures of sperm morphology, they found a few consistent patterns: sperm from introduced anoles had shorter tails and longer midpieces than those collected from native congeners (Figure 1). Furthermore, introduced populations had smaller testes than those from the native range.

Anolis spermatozoa (A). Population means 6 SE calculated from individual mean values (across 15 cells per male) for length of the sperm head, midpiece, and tail in native (black symbols) and introduced (white symbols) populations of three species of Anolis lizards. Significant differences between populations (P < 0.05) were determined using Tukey’s HSD test and are noted with an asterisk.

Figure 1. Anolis spermatozoa (A). Population means +/- SE calculated from individual mean values (across 15 cells per male) for length of the sperm head, midpiece, and tail in native (black symbols) and introduced (white symbols) populations of three species of Anolis lizards. Significant differences between populations (P < 0.05) were determined using Tukey’s HSD test and are noted with an asterisk.

There are two main reasons that differences in sperm morphology between native and introduced populations are probably not the result of random genetic shifts. First, the size of the midpiece and tail correlate with swimming speed in sperm. The midpiece of the sperm is the housing unit for the mitochondria which powers the cell as it moves, and the length of the tail can directly influence the speed at which the sperm swims (longer tail = greater speed). Because the observed changes in morphology likely impact function, adaptive evolution may be the source of these population differences. Second, the observed differences between the native and introduced populations are fairly consistent among species. Were these changes due to genetic drift or founder effects, it is unlikely that all three species would demonstrate similar changes in morphology. This pattern is more indicative of convergent evolution or phenotypic plasticity because the south Florida environment may generate similar plastic responses in all three species.

What is left to be determined are the proximate causes of these changes in sperm morphology. The observed changes could be due to the process of introduction per se, or they could be caused by unique features of the south Florida environment. Conveniently, many anole species have been introduced to new areas on multiple, independent occasions. Adding more species from other introductions (e.g. green anoles in Hawaii; brown anoles in California or Taiwan) would provide further insight.

Kahrl, A.F. and Cox, R.M., 2017. Consistent Differences in Sperm Morphology and Testis Size between Native and Introduced Populations of Three Anolis Lizard Species. Journal of Herpetology, 51(4), pp.532-537. http://www.bioone.org/doi/abs/10.1670/16-184

A Bit of Extra Swag? Unusual Color Spot on a Brown Anole

By Joshua Hall

On March 20, 2017

In All Posts

Figure 1. Male brown anole with an unusual orange spot on the shoulder.

In the past, numerous anole enthusiasts have posted photos of atypical color variants (1, 2, 3, 4). While sampling small spoil islands in the intracoastal waterway last October, I caught a male brown anole with an unusual splash of color on the shoulder (Fig 1). Reports of sagrei that are completely orange have been noted (5, 6); however, those animals appear to represent a more intense version of the ‘rusty red’ that many of these lizards commonly display on their bodies, particularly on the head. The orange on this male, however, is unlike anything I’ve seen on a brown anole, save for the coloration outlining the dewlap. I’m curious to know if anyone has seen something like this before.

City Lizards Are Hesitant Feeders

By Joshua Hall

On March 4, 2017

In New Research

Figure 1. Anolis cristatellus male in survey position.

Foraging behavior reflects a trade-off between the benefits of obtaining vital resources and the potential costs of energy expenditure, missed mating opportunities, and predation. Through time, selection should canalize foraging behaviors that optimize fitness within a given environment, but novel habitats, like urban landscapes, may require behavior to change. For example, human-landscape modification often results in significant reductions in structural complexity of habitat as compared to natural areas, potentially leaving individuals with a greater sense of perceived vulnerability as they venture out to feed. Moreover, these landscapes can alter the diversity and density of predators in ways that might leave prey with a greater sense of perceived predation risk.

In a recent paper in Urban Ecosystems, Chejanovski et al (2017) sought to quantify differences in foraging behavior between anoles from urban areas and those from more natural, forested locations. They utilized two trunk-ground anoles: Anolis sagrei in Florida and A. cristatellus in Puerto Rico. In both urban and natural habitats, they located male lizards in survey posture (Fig 1), which indicates an individual is likely searching for food, and placed a tray with mealworms on the ground at a fixed distance from the perch. They measured each lizard’s latency to feed which was the time it took to the lizard to descend from its perch and capture a mealworm.

Because the availability of complex habitat structure and the proximity of predators might both influence foraging behavior, they experimentally manipulated perch availability for A. sagrei and predator presence for A. cristatellus in both urban and natural habitats. For A. sagrei, they provided half the individuals with two extra perches between the lizard’s original position and the food tray. For A. cristatellus, they manipulated perceived predation risk by placing a static bird model on the opposite side of the feeding tray from half the lizards.

Additionally, they measured several other factors that might influence foraging behavior: the number of available perches within a fixed radius of each lizard – increased habitat complexity might result in lower perceived predation risk; perch height of each individual – those that perch lower to the ground may be more motivated to feed and those that perch higher may be satiated; estimates of body temperature by placing a copper model at the original position of each lizard – body temperature can influence locomotor function and this may have consequences for how easily a lizard can escape predation and play a role in its perceived risk. They also measured the density of conspecifics in the immediate vicinity and noted when conspecific individuals captured mealworms from the feeding tray.

Finally, they measured SVL and mass for a representative sample of each population (urban and natural) in order to calculate body condition. Trade-offs between costs and benefits of foraging decisions can be influenced by satiation of hunger, and body condition, which increases with food consumption, may indicate the extent to which individuals are well-fed.

For both species, lizards from urban areas had a longer latency to feed and demonstrated lower overall response rates to food trays; many individuals never attempted to capture a mealworm in the allotted time (20 minutes). For A. sagrei, habitat (urban vs. natural) best explained feeding latency, but perch height and the presence of conspecifics were also important determinants of feeding latency for A. cristatellus. Individuals perching lower had shorter latency, and latency was shorter when a conspecific attempted to feed from the tray. Neither experimental perch availability nor perceived predation risk (bird model) had any influence on foraging behavior. In both species, individuals from the forest were smaller (SVL) and less massive than those from the city. Body condition was higher for urban A. sagrei but did not differ between natural and urban habitats for A. cristatellus.

Differences in foraging behavior for male A. cristatellus between natural and urban habitats.

Because of the reduced availability of perches and structural complexity in urban habitats, urban lizards could have generally higher perceived predation risk and this might explain their reluctance to feed; however, experimental perch availability did not influence foraging behavior for A. sagrei and an artificial predator had no effect on A. cristatellis. The latter may simply reflect that the experimental predator was stationary and a moving predator may have elicited different results.

It is possible that foraging differences reflect food availability in urban vs natural habitats, and thus motivation to forage. Urban anoles had higher body condition and may be generally better fed than those from the forest; however, the authors found no significant correlation between individual body condition and latency to feed. It is also possible that mealworms represent a novel food source for urban anoles, and this resulted in a hesitance to initiate feeding since many animals are reluctant to approach novel objects/ food (neophobia).

In summary, this study demonstrates that differences do exist in foraging behavior for two distantly related species of anoles between urban and forested habitats. The increased latency to feed observed in urban anoles could be due to perceived predation risk, foraging motivation, neophobia, or some combination. What is left to be determined is the extent to which these behavioral differences might be adaptive in their respective habitats.

Honduran Anole Identification

By Joshua Hall

On August 30, 2016

In All Posts

I have been working my way through McCranie and Kohler’s guide to Honduran anoles and thought I would pull out some old photos from when I did some romping about Honduras a decade ago. At the time I had little interest in anoles and barely noticed them on my trips to Honduras (O foolishness of youth!). These photos below, however, represent a species I remember seeing frequently. I believe it is Norops lemurinus but without a specimen in hand it is difficult to use a dichotomous key. I was hoping someone more familiar with this part of the world could offer confirmation or correction. I was on the northern coast a few miles east of Balfate, less than 50 m above sea level.

I took my first trip to Honduras in 2004 at the age of 19 and made six more trips over the next eight years. Unfortunately, what I remember most was how the landscape changed so drastically from one year to the next as more and more people, mostly ‘norteamericanos,’ moved in to extract any and all resources from the land. At 19, I could hardly take one step through the long grasses on my way to the beach without scattering a half dozen lizards. I remember that so vividly! By the time I hit my late 20’s the grasses were replaced with a coconut grove and a size-able complex of condominiums (built by and, I assume, advertised to Canadians).

Of course, there are still plenty of herps around and about: when last I left, the cane toads and hemidactylids were doing just fine.

Three-Legged Green Anole

By Joshua Hall

On June 24, 2016

In Natural History Observations

There are several previous posts concerned with lizards missing feet or limbs (1, 2, 3). At the risk of being monotonous, here is another. I caught this male green anole (Anolis carolinensis) in Auburn, AL this morning (6.24.16). He was sitting on someone’s porch railing at my apartment complex. In addition to his front left limb he was missing 2 fingers on the front right hand and one on the back left foot. He has no other signs of damage, however, not even any evidence of a regenerated tail. I think what sets this example apart from ones previously given is that the entire limb is missing. There is only a tiny nub of bone at the shoulder, and a small flap of skin. Interestingly, the tiny nub moves back and forth beneath the skin when he runs, as if the entire limb were still present and useful.

We (Warner Lab) have had lizards hatch without limbs in the past. We even had one (A. cristatellus) hatch this year with 6 limbs (three front right arms). It is possible that this carolinensis never developed this limb to begin with; however, the tiny flailing nub and flap of skin make me feel that is not the case. Anyhow, this guy seems fat and happy and still moves pretty fast, despite the handicap.

This Anole’s Signal is…Multimodal?

By Joshua Hall

On April 8, 2016

In New Research

Female Anolis sagrei

In recent months, there has been a lot of talk on the Auburn campus about multimodal signals. Diana Hews gave a phenomenal seminar to the Biology Department last November about complex signaling in Sceloporus lizards, and just last week Eileen Hebets told a similar story about signaling behavior in a group of invertebrates, amblypygids. The latter lecture prompted a momentary side conversation between a Warner Lab postdoc, Tim Mitchell, and me concerning the apparent lack of multimodality in Anolis signaling. Ironically, I just ran across a 2016 publication by Baeckens et al that forced me to eat crow, albeit only a tiny bit of crow.

Anoles, like most iguanians, have been labeled as “visual only” signalers and for good reason. Anoles lack the epidermal glands that secrete the typical chemicals used in lizard chemosensing. Rather, anoles are known widely as models for communication for their reliance on visual signals (which have been demonstrated to be quite complex despite being unimodal) and are also characterized by a low baseline rate of tongue-flicking, even when considered against the backdrop of other visually oriented iguanians. Additionally, previous experiments conducted with A. carolinensis found no significant evidence of chemosensory function in prey selection, assessment of opponents, or in mate choice (Jaslow & Pallera, 1990; Forster et al., 2005; Orrel & Jenssen, 2002). The question of whether or not anoles utilize chemical signals seems to be one answered; however, Baeckens et al have conducted a simple but convincing study that might demonstrate the converse.

Lizard Populations Offer Fresh Look at Island Biogeography

By Joshua Hall

On February 22, 2016

In Introduced Anoles, New Research

Female Anolis sagrei, Palm Coast, Florida

Any observant individual has noticed and possibly even been astonished by the incredible densities that some insular anole populations (i.e. A. sagrei) can achieve. Islands necessarily create a unique combination of environmental factors, several of which have traditionally been suggested as reasons that insular species are capable of attaining such densities. Species richness tends to be quite low on islands and so the diversity of predators remains low and there are fewer other species with which to compete for resources. A lack of predation pressure and competition can allow a species to more broadly utilize a traditionally occupied niche or even evolve to fill new regions of adaptive space, further utilizing resources in ways that increase population growth. A newly published meta-analysis of lizard densities across the globe confirms some of what we already knew about island biogeography, but also challenges some traditional thinking on the subject.

Communication in Context: Signal Plasticity and Novel Environments

By Joshua Hall

On February 11, 2016

In New Research

Anolis gundlachi from The Reptile Database

Plasticity is the ability of one genotype to produce multiple phenotypes under different environmental conditions. Once considered a hindrance to the study of evolution, plasticity is now thought to be one basic way organisms may persist in novel habitats long enough for adaptation to occur. Because of its propensity for rapid change, behavioral plasticity is considered one of the most effective ways that organisms can adjust to new surroundings. In some circumstances, behavioral changes can even be immediate. In example, some populations of birds can alter their vocalizations when singing against the backdrop of city noise pollution (Potvin and Mulder, 2013). This ability to instantaneously respond to external stimuli is known as contextual plasticity, and it may be a powerful tool by which organisms adapt to novel conditions.

A new paper by Ord et. al., explores the potential use of contextual plasticity in social communication using species of Puerto Rican Anoles. Anoles use visual signals (head bobbing, pushups, and dewlapping) to communicate with one another, and previous research has noted that these signals are in competition with background visual noise (i.e. presence/movement of leaves and visual obstructions) and their reception is more challenging under low light conditions (Ord et.al., 2007). Anoles must adjust their signaling behavior in order to compete with distractions in their environment. The point of visual signaling is to be seen, so a positive relationship exists between mean visual noise and signaling speed and a negative relationship between mean display duration and mean light levels. See the decibel chart which is used to measure the intensity of a sound.

Urban Hibernacula

By Joshua Hall

On February 2, 2016

In All Posts

Urban environments often create a diversity of novel habitats that differ from natural areas in thermal variance and spatial organization. Sometimes this results in a broader range of usable microhabitats for species able to thrive in human-disturbed areas. A few days ago I discovered such a microhabitat in an unlikely place. Last October, after getting mucked up seining for turtles in a slow moving Alabama stream, I quickly rinsed my muddy boots with a water hose and tossed them absentmindedly into a sunny spot to dry. There they remained until I went out a few days ago (January 30) with my daughter to look for green anoles coming out to enjoy a brief break in winter weather. Temperatures for the day were expected to reach the upper 60’s° F. Even in midwinter, green anoles (Anolis carolinensis) will sometimes emerge from their hibernacula to sun if the weather is right. As we walked outside, I noticed such an individual emerging from one of my steel-toe boots; he was covered in a dry layer of mud that most likely still lined the insole from my turtle trip last fall. He was quite sluggish so my daughter (3 ½) was able to inspect him for a moment before he got spooked and scurried off to a sunny brick wall some distance away. This was the only anole we found for several hours, so we called it quits and went looking for salamanders. Later that evening, once the sun was long down and temperatures had returned to a squamate-chilling 52° F, my skepticism got the best of me, and I returned to the boot for another look. After probing around a bit I found what I was looking for: a little green lizard had returned to bed down for the rest of the mild Alabama winter.