Tolerance to Urbanization is Widespread in Anoles

From Winchell et al. (2020): Anoles throughout the Caribbean differ in their tolerance to urbanization. Red colors = urban tolerant, blue colors = intermediate tolerance, green colors = urban intolerant.

Seven years ago I asked for the help of Anole Annals readers as I started to think about how different species of anoles throughout the Caribbean tolerate urbanization. This question, it turned out, was a lot more complex than I had originally anticipated! The idea was simple, find out which species are in urban areas and to what extent they use urban habitat elements, then determine if there is an evolutionary signal in urban tolerance and what traits are correlated with urban tolerance. Many hours of troubleshooting and brainstorming with my coauthors Klaus Schliep, Luke Mahler, and Liam Revell (and years later) and this study is finally out in the journal Evolution: Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade.

Anolis lineatopus, one of many urban tolerant anoles (photo K. Winchell)

Inventorying urban species

To figure out which anole species are tolerant of urbanization, my initial plan was to survey researchers and the literature to score each of the 100+ Caribbean species based on their presence in different types of urban habitats and their habitat use. Although I got a lot of great feedback from this original survey, it left a lot of gaps in the dataset. I needed to find a more objective way to assess urban tolerance.

With the help of Klaus Schliep and Luke Mahler, we decided to examine location records in museum collections (via GBIF) to determine which species had been observed (collected) in urban environments. Because we suspected museum records might be biased towards non-urban habitats, we also examined location records from the citizen science database iNaturalist, which we suspected might be biased in the opposite direction (i.e., people photograph things where they live). For each record, we looked at satellite imagery and scored the observation as urban or non-urban, then tallied the total number of observations and the total number of urban observations per species.

Even with these two data sources, we noticed gaps in our data for some species. So we included a third source, Henderson & Powell’s (2009) book on the Natural History of West Indian Amphibians and Reptiles. This fantastic reference (highly recommended!) gives detailed natural history information and summarizes key features of every anole (and other Caribbean herps) in the Caribbean. Of course, this is more subjective than the location-based data, so Luke and I came up with a scoring system that assigned a set number of urban tolerant or avoid “points” based on key descriptors. For example, if a species was described as being common around houses and often observed on buildings, it would get points for being tolerant of urbanization. In contrast, a species described as having a restricted range and intolerance of anthropogenic disturbance, it would get points for being intolerant.

Analyzing urban tolerance in a phylogenetic framework

We combined these disparate data sources into a logistic model with parameters we set based on the number of urban observations we would need to be certain of urban tolerance and how many total observations we would need to be certain of our species assessment. This resulted in a probability of being an urban avoider or urban tolerant for each species, which we used as our prior probabilities for these states in our phylogenetic model. We then reconstructed ancestral states and missing tip states for urban tolerance in 131 species of Caribbean anoles.

Of course, we don’t mean to say that we attempted to reconstruct the evolution of urban habitat use — anoles are far older than urbanization! Instead, we wanted to understand the evolution of the behavioral, physiological, ecological, and morphological traits traits that influence whether a species will exploit or avoid urban habitat when it arises. The threshold model is well-suited for this type of complex trait. The threshold model assumes that a discrete trait is determined by a combination of continuously valued characteristics. These characteristics may be measurable, unmeasurable, or even unknown. As a taxon accumulates specific trait changes, the species is pushed incrementally closer and closer to the discrete state change (in this case urban tolerance), and the more recently this discrete character state has flipped, the more likely a reversal to the previous state could occur. From this model we can extract a single continuously valued trait, the liability, that underlies the complex trait of urban tolerance.

Urban tolerance in Caribbean anoles, from Winchell et al. (2020).

Traits of urban species

So what did we find? To start, urban tolerance appears to be widespread in Caribbean anoles and has a strong phylogenetic signal. Because of that, we suggest that our approach may be used to predict urban tolerance of species that either have yet to encounter urbanization or for which we are lacking information. This application could be particularly useful for determining which species are likely to be intolerant of urbanization and thus should be prioritized in conservation efforts. At the other end of the urban tolerance scale, we caution that our approach should not be used to predict species that are robust to anthropogenic habitat loss, but rather that it might be useful to identify species that are promising for future urban ecology and evolution studies.

Finally, we used the liability score for each species to try to get a better understanding of what those traits underlying urban tolerance are exactly. Using PGLS we looked for correlations between the liability and a suite of ecological and phenotypic traits. We found that species that are more tolerant of urbanization had higher field body temperatures, fewer ventral scales, more rear lamellae, shorter hindlimbs, and experience warmer and drier climates within their native range. These traits may be key “pre-adaptations” enabling species to colonize urban habitats as they arise and to take advantage of anthropogenic niche space (i.e., on and around buildings). For example, urban habitats tend to be hotter and drier than nearby forest sites, so it makes sense that species with larger ventral scales, higher field body temperatures, and which experience hotter and drier temperatures in their non-urban range would be predisposed to tolerate urban habitats. Similarly, lamellae are important for clinging to smooth surfaces, which may be particularly beneficial in urban habitats dominated by smooth anthropogenic surfaces.

Lastly, we found, somewhat to our surprise, that no one ecomorph seems to be best suited for urban environments. Based on our experience, we had thought that trunk-ground anoles would be more likely to tolerate urbanization, but it turns out that there are a lot of trunk-ground anoles that are intolerant of urbanization and a lot of species from other ecomorphs that are tolerant (think A. equestris or A. distichus)!

The Highest Kingdom of Anolis: Thermal Biology of the Andean lizard Anolis heterodermus Over an Elevational Gradient in the Eastern Cordillera of Colombia

New literature alert!

In Journal of Thermal Biology
Méndez-Galeano, Paternina-Cruz, and Calderón-Espinosa

Abstract

Vertebrate ectotherms may deal with changes of environmental temperatures by behavioral and/or physiological mechanisms. Reptiles inhabiting tropical highlands face extreme fluctuating daily temperatures, and extreme values and intervals of fluctuations vary with altitude. Anolis heterodermus occurs between 1800 m to 3750 m elevation in the tropical Andes, and is the Anolis species found at the highest altitude known. We evaluated which strategies populations from elevations of 2200 m, 2650 m and 3400 m use to cope with environmental temperatures. We measured body, preferred, critical maximum and minimum temperatures, and sprint speed at different body temperatures of individuals, as well as operative temperatures. Anolis heterodermus exhibits behavioral adjustments in response to changes in environmental temperatures across altitudes. Likewise, physiological traits exhibit intrapopulation variations, but they are similar among populations, tended to the “static” side of the evolution of thermal traits spectrum. The thermoregulatory behavioral strategy in this species is extremely plastic, and lizards adjust even to fluctuating environmental conditions from day to day. Unlike other Anolis species, at low thermal quality of the habitat, lizards are thermoconformers, particularly at the highest altitudes, where cloudy days can intensify this strategy even more. Our study reveals that the pattern of strategies for dealing with thermal ambient variations and their relation to extinction risks in the tropics that are caused by global warming is perhaps more complex for lizards than previously thought.

 

Méndez-Galeano, M. A., Paternina-Cruz, R. F., & Calderón-Espinosa, M. L. (2020). The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia. Journal of Thermal Biology, 89, 102498.

Anole Annals Has a New Look!

You spoke, we listened. We’ve been working hard behind the scenes to renovate Anole Annals. Yesterday we unveiled a new look, but not just that — comments are working again!

Please bear with us over the next few days as we work out the minor issues with this transition. And if you have any ideas of ways to improve the site, let us know by email or comment below, or better yet, consider joining our board of editors to get in on the behind the scenes action!

Anole Humor

Hot Eggs Don’t Lead to Adults Tolerant of Higher Temperatures

Writing in Biology Letters recently, Alex Gunderson (Tulane University) leads a study revealing that incubation temperature does not underlie the thermal tolerance limits of resulting lizards; individuals which hatch from eggs incubated in hot conditions are not able to withstand hotter air temperatures as adults, relative to lizards hatched from cooler incubation temperatures. A preliminary discussion of the relationship between incubation conditions and adult thermal physiology was put forward as a potential explanation for observed divergence in thermal physiology between crested anoles (A. cristatellus) in Puerto Rico and an introduced population in Miami, Florida USA (Leal & Gunderson 2012), “Additional studies are needed to explore the possibility that incubation temperature can influence the [thermal tolerance limits] CTmin of A. cristatellus.” Below is the abstract and the main figure from the paper, enjoy!

Abstract
Extreme heat events are becoming more common as a result of anthropogenic global change. Developmental plasticity in physiological thermal limits could help mitigate the consequences of thermal extremes, but data on the effects of early temperature exposure on thermal limits later in life are rare, especially for vertebrate ectotherms. We conducted an experiment that to our knowledge is the first to isolate the effect of egg (i.e. embryonic) thermal conditions on adult heat tolerance in a reptile. Eggs of the lizard Anolis sagrei were incubated under one of three fluctuating thermal regimes that mimicked natural nest environments and differed in mean and maximum temperatures. After emergence, all hatchlings were raised under common garden conditions until reproductive maturity, at which point heat tolerance was measured. Egg mortality was highest in the warmest treatment, and hatchlings from the warmest treatment tended to have greater mortality than those from the cooler treatments. Despite evidence that incubation temperatures were stressful, we found no evidence that incubation treatment influenced adult heat tolerance. Our results are consistent with a low capacity for organisms to increase their physiological heat tolerance via plasticity, and emphasize the importance of behavioural and evolutionary processes as mechanisms of resilience to extreme heat.

 

Figure 2.

Eggs at different temperatures did not produce adults capable of tolerating different temperatures. Here, Fig 1. shows the upper limits of heat tolerance of adult brown anoles (A. sagrei) hatched from eggs incubated under different thermal treatments.

Leal, M. and Gunderson, A.R., 2012. Rapid change in the thermal tolerance of a tropical lizard. The American Naturalist180(6), pp.815-822.
Gunderson, A.R., Fargevieille, A. and Warner, D.A., 2020. Egg incubation temperature does not influence adult heat tolerance in the lizard Anolis sagreiBiology Letters16(1), p.20190716.

Hurricane Effects on Neotropical Lizards Span Geographic and Phylogenetic Scales

New literature alert!

In PNAS
DonihueKowaleski, Losos, Algar, Baeckens, Buchkowski, Fabre, Frank, GenevaReynolds, Stroud, Velasco, Kolbe, Mahler, and Herrel

Abstract

Extreme climate events such as droughts, cold snaps, and hurricanes can be powerful agents of natural selection, producing acute selective pressures very different from the everyday pressures acting on organisms. However, it remains unknown whether these infrequent but severe disruptions are quickly erased by quotidian selective forces, or whether they have the potential to durably shape biodiversity patterns across regions and clades. Here, we show that hurricanes have enduring evolutionary impacts on the morphology of anoles, a diverse Neotropical lizard clade. We first demonstrate a transgenerational effect of extreme selection on toepad area for two populations struck by hurricanes in 2017. Given this short-term effect of hurricanes, we then asked whether populations and species that more frequently experienced hurricanes have larger toepads. Using 70 y of historical hurricane data, we demonstrate that, indeed, toepad area positively correlates with hurricane activity for both 12 island populations of Anolis sagreiand 188 Anolis species throughout the Neotropics. Extreme climate events are intensifying due to climate change and may represent overlooked drivers of biogeographic and large-scale biodiversity patterns.

 

Are Anoles with Re-grown Tails Easier to Catch?

In reporting a case of tail bifurcation in a Bahamian brown anole (A. sagrei) from south Eluethera, Sebastian Hoefer and Nathan Robinson (The Cape Eleuthera Island School), write in Herpetology Notes proposing so!

“Another interesting observation was that this individual was particularly easy to capture and did not attempt to escape. The lack of avoidance could be explained by the anole being stunned due to stress at the time of capture. Alternatively, it could be that multiple tails infer higher energetic costs than a single tail. In turn, this could negatively affect the individual’s activity patterns or ability to avoid predators.”

 

 

Hoefer, S. and Robinson, N.J., 2020. Tail bifurcation in a Brown Anole, Anolis sagrei (Duméril & Bibron, 1837). Herpetology Notes13, pp.333-335.

Dominance and Anoles: It’s Risky at the Top, But Worth It

Two anoles duking it out. Photo from sciencesource.com

Give the elaborate and charistmatic behaviours of our favourite lizards — anoles — many researchers have attempted to piece apart the intricacies of anole social dynamics. In a recent study in Zoology, Glenn Borgmans (University of Antwerp) tests whether dominant adult male American green anoles (A. carolinensis) – dominant in relation to other males – are actually at an advantage, for example by establishing priority access to food or other resources, or if risks associated with being the big boss in town outweigh any perceived benefits, like an increased likelihood of injury due to aggressive male-male interactions. You can read all about it here!

 

Abstract
Male Anolis carolinensis lizards will fight and form social dominance hierarchies when placed in habitats with limited resources. Dominance may procure benefits such as priority access to food, shelter or partners, but may also come with costs, such as a higher risk of injuries due to aggressive interaction, a higher risk of predation or a higher energetic cost, all of which may lead to an increase in stress. While most research looks at dominance by using dyadic interactions, in our study we investigated the effect of dominance in a multiple male group of A. carolinensis lizards. Our results showed that dominant males in a multiple male group had priority access to prey and potential sexual partners but may run a higher risk of predation. We could not confirm that dominant males in a multiple male group had a higher risk of injuries from aggressive interactions or a higher energetic cost by being dominant. Overall our results seem to indicate that dominant male A. carolinensis lizards in a multiple male group obtain clear benefits and that they outweigh the disadvantages.

Dominant lizards ate more food items (left; A) and hid less (right; B) than more submissive individuals.

Borgmans, G., Van den Panhuyzen, S. and Van Damme, R., 2020. The (dis) advantages of dominance in a multiple male group of Anolis carolinensis lizards. Zoology139, p.125747.

Salmonella in Japan’s Green Anoles

When I hear or read Salmonella, I think of my mom explaining to my 7-year-old self why I shouldn’t eat raw chicken (to be clear, I never expressed interest in doing this, but lesson learned nonetheless). According to the U.S. Centers for Disease Control and Prevention, most instances of Salmonella bacteria making people sick do in fact result from transmission by food. But Salmonella infection can come from other sources, including direct contact with living animals, particularly reptiles (including birds which, in case you haven’t heard, are reptiles). So I was only a little surprised when I came across a recent paper in the Journal of Veterinary Medical Science, based in Japan, documenting the prevalence of Salmonella in the green anole, Anolis carolinensis, on Okinawa Island, Japan.

Of the 706 green anoles from Okinawa Island whose intestinal contents were analyzed for Salmonella presence between 2009 and 2014, only 2.1% tested positive. That number is low compared with published results for green anole populations in Florida (7.5%), Chichi Island in Japan (34.2% – this study was highlighted here on Anole Annals when it came out in 2013), and Guam (76.2%). I’m struck by how much these percentages vary. Green anoles have been in Florida for millions of years, whereas populations in the other locations have only been established for tens of years. The authors hypothesize that infection rate in recently introduced populations should correlate with how long the population has been established. Testing this hypothesis will require data from more populations.  It also appears that we know little about whether anoles are affected by carrying Salmonella, although a quick search did reveal this study involving the brown anole, Anolis sagrei.

All told, we have a lot to learn about anoles and Salmonella. In the meantime, please protect yourself from Salmonella infection by following basic food safety precautions: refrigerate foods adequately, wash fruits and vegetables and cook meat and eggs thoroughly, and clean potentially contaminated cookware and utensils with soap and water. Most importantly, WASH YOUR HANDS, although I assume that like me, you are already doing this approximately a hundred times per day (for those of you reading this in the future, I’m not a weirdo. We’re in the middle of a pandemic).

For those who may be interested, green anoles became established in and around Japan several decades ago and are considered an ecologically disruptive pest. If you want to read more, here are links to some old Anole Annals posts on various topics related to the region’s green anoles: trapping efforts, population age structure, range expansion. Enjoy!

Does Breeding Season Variation Affect Evolution of a Sexual Signaling Trait in a Tropical Lizard Clade?

New literature alert!

In Ecology and Evolution
Gray, Barley, Hillis, Pavón‐Vázquez, Poe, White

Abstract

Sexually selected traits can be expected to increase in importance when the period of sexual behavior is constrained, such as in seasonally restricted breeders. Anolis lizard male dewlaps are classic examples of multifaceted signaling traits, with demonstrated intraspecific reproductive function reflected in courtship behavior. Fitch and Hillis found a correlation between dewlap size and seasonality in mainland Anolis using traditional statistical methods and suggested that seasonally restricted breeding seasons enhanced the differentiation of this signaling trait. Here, we present two tests of the Fitch–Hillis Hypothesis using new phylogenetic and morphological data sets for 44 species of Mexican Anolis. A significant relationship between dewlap size and seasonality is evident in phylogenetically uncorrected analyses but erodes once phylogeny is accounted for. This loss of strong statistical support for a relationship between a key aspect of dewlap morphology and seasonality also occurs within a species complex (A. sericeus group) that inhabits seasonal and aseasonal environments. Our results fail to support seasonality as a strong driver of evolution of Anolis dewlap size. We discuss the implications of our results and the difficulty of disentangling the strength of single mechanisms on trait evolution when multiple selection pressures are likely at play.

 

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