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From the archives. One of the greatest <i>Anole Annals</i> posts of all times, because why not?

“You’ve gotta see this!” my fiancé Mark called to me one morning.  He was outside, which could mean only one thing: a wildlife encounter was underway.  Living in a semi-rural neighborhood in Florida, you never knew what you would see, from a mated pair of Sandhill Cranes walking down the street with their young, to Gopher Tortoises excavating burrows in the front yard.

I walked downstairs to the concrete area under our elevated house where Mark was staring at something on the ground.  I looked down to see a frog (Cuban Treefrog) with the tail of an A. carolinensis protruding from its gullet.

“I knew that lizard,” Mark said forlornly.

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I wanted to share an observation of communal basking of the Green Anole (Anolis carolinensis) from the western Highland Rim of Tennessee. The locality is near the northern extent of their range in middle Tennessee. On a warm January day this winter, I observed six (6) individuals basking in close proximity along an exposed tree branch. The overwintering habitat was a south-facing road cut.

Has anyone else observed this type of “communal” basking of anoles, either in the Green Anole (Anolis carolinensis) or other species?

Shelby Irwin, a junior in Michele Johnson’s lab at Trinity University, presented a poster on her summer research in Thomas Sanger’s lab at Loyola University examining hatchling behavior in Anolis sagrei after incubation in thermally stressful conditions. In the lab, Irwin and colleagues incubated A. sagrei eggs under a standard (27°C) and elevated (34°C) thermal regimes to investigate impacts on hatchling phenotype and behavior.

It has been previously noted that thermal stress during development can affect craniofacial development, but Shelby was interested in if there was also an impact on behavior of hatchlings. After hatching, lizards from both the standard and elevated thermal regimes were run through a gambit of exploratory (prey interactions, novel object, and open-field test) and social trials (conspecific and predator interactions). They found that “hot” hatchlings were less aggressive and exhibited less exploratory behaviors. Their findings add to the growing body of research investigating the impacts of a warming world, particularly with regards to sensitive periods in thermally sensitive species.

Recent increases in non-native species introductions by humans have spurred a flurry of research examining the subsequent impacts of species invasions. However, often times non-native species introductions go unnoticed until the species is already established. When predicting the effects of a species invasion, it is important to understand how population demographics change during the colonization and establishment stages. Amélie Fargevieille addressed this issue in her talk entitled “Population demographics of an invasive lizard following experimental introduction on small islands.”

Fargevieille and colleagues released adult Anolis sagrei onto islands off the northeast coast of Florida prior to the reproductive season and monitored survival and reproduction over the first reproductive season. The total density of lizards introduced to islands were the same, but four of their islands were introduced with male-biased populations and four with female-biased populations. They then examined the survival and reproduction of the descendants of the founding populations over the next two years. They found that male-biased and female-biased founding populations did not differ in survival rates. In addition, across all islands, juveniles had the highest mortality, which suggests that the ecological factors facilitating or deterring colonization in the earliest stages following an introduction play an important role in invasion biology. Looking forward to future work from Fargevieille and colleagues in the Warner lab!

Anolis shrevei. Photograph by Miguel Landestoy.

Post-doc Vincent Farallo presented work, co-authored by Martha Muñoz, in the behavioral physiology session on the importance of incorporating physiology and behavior when assessing how species, especially montane endemics, will be impacted by climate change. Vincent and Martha compared correlative models and mechanistic niche models to better understand how climate change may impact three anoles from the island of Hispaniola, Anolis shrevei, A. armouri, and A. cybotes. When predicting future ranges of these species using correlative modeling, Farallo and Muñoz saw that the ranges of the mountain-top endemics A. shrevei and A. armouri shrink, whereas the range of the widespread species A. cybotes remains the same under future climate change predictions. Comparing these findings to mechanistic niche modeling, which uses organismal physiology and behavior to help predict future activity times within current ranges, they found that all three species will increase activity times within the mountain-top endemic ranges.

To reiterate their findings, they showed that when incorporating behavior and physiology, montane endemic species will increase potential activity time under climate change.  However, their widespread competitor will also see increased activity, indicating the montane endemics are still likely at risk, but not directly from warming temperatures.  Understanding the mechanism of species decline will be critical for mitigating the impacts of climate change.

Despite the widespread use of anoles as model species for ecology, evolution, and behavior, we still have a relatively poor understanding of their nesting behavior and the factors that contribute to egg survival. This is unfortunate because past research demonstrates that egg survival can drive important measures of population demography (e.g. adult population density, Andrews 1982). Andrew DeSana, an undergrad from Seton Hill University, teamed up with the Warner lab to explore the possibility that marsh crabs (Armases cinereum) might serve as predators for brown anole eggs (Anolis sagrei). Because nest site selection by females may shield developing eggs from predators, he also wanted to know how several common nesting microhabitats might influence the depredation of eggs. He used both a lab and a field study to assess how the density of crab predators (no crabs, low crab density, and high crab density) and the nesting microhabitat of females (open sand, under palm fronds, and under leaf litter) might influence egg survival. He collected eggs from a breeding colony of anoles and placed them in these microhabitats in the presence of varying densities of crabs.

He found that marsh crabs readily prey upon anole eggs and that variation in egg survival was best explained by both crab density and the microhabitat where eggs develop. In both the lab and field study, eggs had the highest survival when placed under leaf litter and lower survival in the open and under palm fronds. Anecdotal data of crab behavior suggests that they don’t forage in the leaf litter and this may explain these results. Egg survival also decreased with increasing crab density. Thus, females nesting in leaf litter in habitats with low crab density would have greater reproductive success than those nesting in other microhabitats, especially if crab density is high. Future research will determine how the presence/absence of crabs influences female nesting behavior.

Andrews, R.M., 1982. Spatial variation in egg mortality of the lizard Anolis limifrons. Herpetologica, pp.165-171.

Many biologists are interested in understanding how temperature affects animals throughout ontogeny. Egg incubation experiments are often done to examine how nest temperatures influence embryo development. However, the information gleaned from these experiments are only useful when comparing ecologically relevant thermal regimes.

Mallory Turner, an undergraduate researcher in the Warner lab at Auburn University, examined how embryo development differs between incubator thermal regimes in Anolis cristatellus and A. sagrei. Nest temperatures peak at different times of the day due to differences in the local environment (e.g., habitat structure, shade, etc.). Turner examined how incubator thermal regimes that were uncentered and peak-centered influenced development. Nest temperature data were used to create two 24-hour diel cycles. Anole eggs were incubated in incubators programmed to mimic hourly nest temperature data with temperatures either uncentered (uncentered regime), or with hourly nest temperature data aligned temporally at thermal peaks (peak-centered regime). She examined how thermal regimes impacted incubation duration and offspring phenotype. Incubator thermal regime did not impact incubator duration, mass, or SVL in either anole species. Uncentered thermal regimes have lower maximum incubation temperatures compared to peak-centered regimes, although interestingly enough these differences do not appear to influence development.

Frequently phenotypic evolution is rapid on islands, resulting in many ecologically diverse species. Most of what we know about the faster evolution on islands has been through the examination of morphological diversity. By utilizing species-rich Anolis lizards, Dr. Martha Muñoz and collaborators were able to examine the island effect with regards to rates and patterns of evolution through a different lens: thermal physiological trait diversity. Muñoz et al. examined the evolutionary dynamics of cold tolerance, body temperature, and heat tolerance in island and mainland anoles. They discovered faster heat tolerance evolution in the mainland lineages, and that island and mainland anoles are evolving towards separate trait optima with island lizards having a higher upper thermal limit. A higher optima and slower evolutionary rates are consistent with the Bogert Effect, in which organisms are shielded from selection because of behavioral buffering such as thermoregulatory behavior. Cold tolerance did not differ between habitats, not surprisingly due the fact that lower physiological limits cannot be behaviorally buffered against selection. Despite island and mainland anoles occurring in similar thermal environments, island lizards thermoregulate more. Consequently, the ecological opportunity (fewer predators and/or competitors) provided on islands may be reducing the costs of thermoregulation and slowing down, rather than accelerating evolution of certain traits. This study highlights the importance of other phenotypic axes that organisms diversify along in an adaptive radiation, such as physiological diversification, and that behavior can elucidate or drive patterns shaping evolution.

The effect of temperature on biological processes and systems is one of the most studied topics in ecology. Despite a wealth of existing research, we still have a relatively poor understanding of what factors contribute to the thermal tolerance of complex organisms. Much research suggests that oxygen limitation at extreme temperatures is what determines the thermal limits of complex aquatic life; however, this hypothesis (i.e. Oxygen-and capacity-limitation of thermal tolerance; Pörtner 2010) has not proven very useful in explaining the thermal limits of terrestrial organisms. One reason is that there is a comparatively greater amount of oxygen in air vs water. Moreover, terrestrial organisms tend to have very efficient systems of ventilation (e.g., air sacs of birds and tracheal system of insects). Terrestrial vertebrate embryos, however, rely solely on diffusion of oxygen through a hard shell and, thus, their thermal limits may be set by oxygen limitation (Smith et al. 2015).

Sylvia Nunez and Thom Sanger set out to determine the relationship between oxygen availability and temperature for brown anole (Anolis sagrei) embryos. Previous work shows that thermal stress can induce embryo mortality and severe craniofacial malformations at incubation temperatures above 33 °C (Sanger et al. 2018). They used a factorial design (2 incubation temperatures: 27 °C and 33 °C; and 2 oxygen treatments: 10% O₂ and 21% O₂) and dissected eggs at day 14 or day 20 after oviposition to measure the effects of these treatments during morphogenesis and the growth phase of development, respectively. They found that hypoxia did not lower survival during these periods at 27 °C; however, survival was reduced for embryos incubated at 33 °C and under hypoxic conditions (i.e. 10% O₂). Furthermore, high temperatures and low oxygen resulted in various craniofacial malformations and increased incidences of cerebral blood-pooling. It appears that oxygen supply may limit the thermal tolerance of anole embryos, and these data support the findings of previous work in other lizard species (Smith et al. 2015). The next steps for the Sanger lab are to determine the cellular mechanisms that drive the results discovered in their current study.

Pörtner, H.O., 2010. Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. Journal of Experimental Biology, 213: 881-893.

Sanger, T.J., Kyrkos, J., Lachance, D.J., Czesny, B. and Stroud, J.T., 2018. The effects of thermal stress on the early development of the lizard Anolis sagrei. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 329:244-251.

Smith, C., Telemeco, R.S., Angilletta, M.J. and VandenBrooks, J.M., 2015. Oxygen supply limits the heat tolerance of lizard embryos. Biology letters, 11:20150113.

Different environments promote different life history strategies. The way an organism allocates resources in an environment can have large consequences on growth, reproduction, and immune function. Furthermore, energy allocation tradeoffs may differ between sexes. The energetic costs of immunity can differ between sexes due to differences in energetic demands and ecology. However, the reason some organisms exhibit sex-based energy allocation, and the causes of this phenomenon, remain enigmatic.

Zachariah Degon, an undergraduate student at Georgia Southern University, and colleagues examined the relationships between ectoparasite load, organ mass, fat body mass, and total body size in the Panamanian anole, Anolis apletophallus. Mainland populations of adult male (n=72) and female (n=34) A. apletophallus were sampled in Gamboa, Panama during the reproductive season. Each lizard was visually inspected for mites. The density of mites, and the location of each mite on the lizard body, were recorded. Lizards were dissected and all fat-storing organs were removed. Fat-storing organs included the fat bodies, livers, and gonads. Organs were dried and weighed before measuring organ mass. They found that overall males had more mites than females, and that this difference was driven by the high density of mites located on male dewlaps. Larger lizards, regardless of sex, had higher mite loads. Higher fat body mass was linked to decreased mite loads, although this was only true for male lizards. Liver mass had no effect on mite load in either species. However, mite load increased with ovary mass in females, but there was no relationship between testes mass and mite load in males.

Overall, sex-based differences in energy allocation may have important implications for maintaining immune function in variable environments. Male A. apletophallus had higher mite loads due to their heavily parasitized dewlaps. And interestingly, males with increased fat body masses had lower mite loads. This suggests that males may be allocating energy away from storage and towards increasing immune function.