Helminths Associated with Anolis fuscoauratus in Highland Marshes of the Brazilian Semi-Arid Region

New literature alert!

In Journal of Helminthology
dos Santos Mesquita, de Oliveira, Perez, and Ávila

Abstract

Helminthological studies may contribute with valuable information on host biology and conservation. Herein, we provide new data on helminths infecting the lizard Norops fuscoauratus, testing one of the factors considered most important in parasitic ecology: host size. We analysed 25 specimens of N. fuscoauratus from three highland marshes in the Brazilian semi-arid. Eight taxa of helminths belonging to Nematoda, Trematoda and Acanthocephala were found. Physaloptera sp. showed the higher prevalence (40%), with a mean intensity of infection of 3.3 ± 1.46 (1–16) and mean abundance 1.32 ± 0.65 (0–16). Norops fuscoauratus represents four new host records for the helminths Cyrtosomum sp., Pharyngodon travassosiStrongyloides sp. and Centrorhynchus sp. There is no relationship of host body size (P = 0.79) and mass (P = 0.50) with parasite richness. In addition, the present study contributes to the knowledge of the parasitic fauna of N. fuscoauratus and the Neotropical region.

Read the full article here!

Free Online Course: Landscaping for Lizards

On Wednesday, May 20 at 4:00PM EDT, the University of Florida IFAS Extension Service is hosting a free online course! Here’s the event description from the website.

Learn about how you can landscape for lizards! We will cover many of the species you may see in Northeast Florida, the many benefits to having them around, and what you can do you in landscape and garden to support and protect them.

This is a free online course but registration through Eventbrite is required and the class is limited in size to 80 participants.

The cover photo for the event features a green anole (Anolis carolinensis, also pictured above), so expect some discussion of our beloved anoles. If you attend, please comment below and let us know what you learned!

You can register for the course here.

Anoles Love It When Ant and Termite Nests Get Opened

Lepidoterist and keen naturalist Andrei Sourakov from the Florida State Museum posted this photo on Twitter.

This is actually an effective, if somewhat mean to the little insects, way of watching anoles, as Stan Rand noted in his 1975 paper of A. agassizi: “In the West Indies, a well-established method for attracting large numbers of anoles is to break open a termite nest. Under such conditions, large numbers will often gather and feed actively with little aggressive interaction.”

 

Another Great Anole Journal Cover!

Another one bites the dust for Team Anole! The cover image of the most recent issue of the Proceedings of the National Academy of Sciences is a beautiful green anole (Anolis carolinensis), which accompanies a study in the same issue investigating the evolutionary effects of hurricanes on anole toepads by Colin Donihue et al.

Congrats too to Neil Losin for taking this fabulous photo!

Donihue, C.M., Kowaleski, A.M., Losos, J.B., Algar, A.C., Baeckens, S., Buchkowski, R.W., Fabre, A.C., Frank, H.K., Geneva, A.J., Reynolds, R.G., Stroud, J.T., Velasco, J.A., Kolbe, J.J., Mahler, D.M., Herrel, A. 2020. Hurricane effects on Neotropical lizards span geographic and phylogenetic scales. Proceedings of the National Academy of Sciences, 117 (19): 10429-10434

Biological Invasions Lead to Increased Aggressiveness in Endemic Lizards

Male of A. oculatus (background), displaying to the conspecific robot (foreground). Credit: Claire M.S. Dufour

Invasive species can have large negative effects on the environment and the economy, and this is a major driver of research interest. We want to understand what makes invasive species succeed or fail, so that we can tip the balance in favor of native counterparts. Increasingly, biological invasions are also recognized for their research value. These “accidental experiments” can help us answer questions about community assembly, species interactions and evolution (Losos et al. 1993; Stuart et al. 2014; Stroud 2019).

Much of the research on introduced species has focused on obtaining information that can help us predict the next invasion event. This includes efforts to understand pathways of invasion (which can be done using population genetic data) or to identify the traits that make invasive species so successful (which can be done by comparing invasive and non-invasive taxa). Less research has focused on what happens shortly after an invasive species gains a foothold. In particular, we know little about early behavioral interactions between invasive and native species. Might these exchanges determine invasion outcomes and patterns of spread?

Enter the anoles of Dominica

In a recent paper, Dufour and collaborators address this gap using native and invasive anoles in Dominica. The authors built lizard robots that mimic the morphology and display behavior of the invasive species (A. cristatellus) and the endemic species (A. oculatus). With these robots, they tested the responses of A. oculatus males when presented with conspecific and heterospecific displays. The authors used sites where both species are found, and sites where only the endemic is found. Therefore, they could contrast the responses of A. oculatus with and without prior experience with the invader.

Interspecific fight between A. oculatus (left) and A. cristatellus (right). Credit: Claire M.S. Dufour

Robots elicited the expected response. In addition, A. oculatus could discriminate a conspecific robot from a heterospecific robot. Intriguingly, a response to heterospecific displays was recorded even in A. oculatus populations with no prior experience with A. cristatellus. This finding is surprising given the lack of shared evolutionary history of the two species, and remains to be explained. Lastly, A. oculatus males that co-occur with A. cristatellus had a more aggressive display response.

A. oculatus are typically larger and are expected to be the dominant species during aggressive encounters (Dufour et al. 2018a,b). Therefore, it is possible that observed behavioral shifts will impact species coexistence and ultimately decide the long-term outcome of this invasion. Read all about Claire’s exciting new study!

 

Hot Nests and Thermal Stress: Why Do Animals Die when They Get Hot?

A hatching brown anole.

Temperature is probably the most studied environmental factor that influences living things; however, you might be surprised to learn that we still don’t have a solid understanding of why things die when they get hot. If you recall your intro biology, you’ll remember that proteins and cell membranes fall apart when they get hot, and that is often the explanation for death at high temperatures. But, there are several reasons to question this explanation. For example, complex organisms (e.g. plants and animals) universally have lower heat tolerance than simple organisms (e.g. bacteria), despite using the same basic biochemical building blocks (i.e. proteins and membranes). Moreover, complex organisms often die at temperatures lower than those that cause proteins and membranes to fall apart.

One explanation has gained a lot of traction in recent years: the oxygen-and capacity-limited thermal tolerance concept (what a mouth full!). This concept posits that as your body heats up, you need more oxygen; however, you eventually get so hot that you can’t get enough oxygen to survive.  There is growing evidence that oxygen limitation explains thermal tolerance for reptile eggs. Several studies show that when eggs are incubated in low oxygen conditions, their heat tolerance is lower (e.g. Smith et al., 2015); however, we still don’t know much about embryo metabolism at near-lethal temperatures, which would vastly improve our understanding of embryo heat tolerance.

In a recent study (Hall and Warner, 2020), we (I and Dr. Dan Warner, who was recently awarded the distinction of “Outstanding Mentor” by Auburn University – well deserved) sought to better understand the factors that determine heat tolerance of reptile embryos. We used eggs from our good friend, the brown anole (Anolis sagrei). Using 1-hour heat shocks, we measured the lethal temperature of embryos (~45.3 °C). We then monitored heart rate and metabolism of eggs across temperature, including near-lethal temperatures.

Figure 1. Heart rate of brown anole eggs across temperature.

As embryos approach the lethal temperature, heart rate and CO2 production increase (Figure 1), but oxygen consumption plateaus (Figure 2). Therefore, eggs need more and more energy as they heat up, but they are eventually unable to support their energy needs via aerobic respiration. Without enough oxygen, energy production is less efficient. These data indicate that oxygen is limited at near-lethal temperatures and provides additional support for the oxygen-and capacity-limited thermal tolerance concept for reptile eggs.

Figure 2. Oxygen consumption across temperature for brown anole eggs.

Many aspects of human-induced global change cause increases in temperature (e.g. deforestation, urbanization, climate change), potentially heating lizard nests and exposing embryos to thermal stress. The results of our study make progress toward understanding how embryos respond to extreme temperatures, which is important to understand how reptile populations will respond to global change.

Hall, J.M. and Warner, D.A., 2020. Thermal sensitivity of lizard embryos indicates a mismatch between oxygen supply and demand at near-lethal temperatures. Journal of Experimental Zoology, in press. https://doi.org/10.1002/jez.2359

Smith, C., Telemeco, R.S., Angilletta Jr, M.J. and VandenBrooks, J.M., 2015. Oxygen supply limits the heat tolerance of lizard embryos. Biology letters11(4), p.20150113.

Lighting Up Anoles at Night!

anolis lizard lit up by artificial lighting at night

Photo by James Stroud

How we perceive and interact with the world is strongly shaped by natural light. How much light there is at a given time determines whether we’re sleepy or awake, and whether we’re bracing for winter or excited for long summer days. The annual switch to daylights savings time shows us how even a small shift in our perceived light cycle can disrupt our internal clocks!

 

The amount of illumination an animal experiences – its photoperiod – is also vitally important in nature, from determining sleep cycles to the seasonal timing of reproduction. However, the increasing urbanization of natural habitats has led to huge shifts in the exposure of wildlife to light due to the use of electric lighting at night in urban areas. This artificial light at night has the potential to seriously affect the life cycle of many organisms through, for example, changes in endocrine function, melatonin production, and reproductive timing. On the other hand, artificial lighting at night may also have positive effects in some cases: organisms that forage or hunt at night, for instance, may have increased perception of prey and greater success in obtaining nutrients.

In a recent paper, Thawley and Kolbe investigate the effect of artificial light at night on one of our favorite species of lizards, Anolis sagrei. Using captured anoles from a wild population in a forested area with low levels of artificial lighting at night, they use laboratory experiments to see the effects of this artificial lighting on the anole’s body condition, glucocorticoid levels, and reproductive cycles.

The authors found that artificial lighting at night actually increased the growth rate of anoles in captivity! Females under ‘artificial light at night’ condition grew 1.8 times faster than their counterparts experiencing the ‘dark at night’ condition, and males grew 1.2 times more! This suggests that artificial lighting at night could have a huge biological consequences for this species. As the authors hypothesized, the female anoles exposed to artificial lighting at night also started laying eggs much earlier than their control counterparts. In particular, smaller females under artificial lighting at night managed to produce similar total egg output to that of larger females, potentially representing a tremendous gain in reproductive fitness for these smaller individuals.

All this would seem to suggest that artificial lighting might be a boon for Anolis sagrei! However, the authors suggest some caution in this interpretation, as their experimental set-up did not include foraging costs or predation – both of which could also interact with the effects of artificial lighting to create downsides for Anolis sagrei in these new lit-up urban environments.

Overall, this paper is an illuminating look at how the artificial lighting at night associated with increased urbanization can impact the lives of Anolis sagrei – I encourage you to check it out!

Citation: Thawley, Christopher J., and Jason J. Kolbe. 2020. Artificial light at night increases growth and reproductive output in Anolis lizards. Proceedings of the Royal Society B 287.1919: 20191682. [https://doi.org/10.1098/rspb.2019.1682]

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!

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