Rodolfo Ruibal, R.I.P.

AA is sorry to learn of the passing of Rodolfo Ruibal, an eminent Cuban herpetologist based at UC-Riverside for many years. Rodolfo did important early work on thermal biology andsocial behavior of Caribbean anoles. For example, 1961 paper showed thermoconformity in some lizards (when everyone though that lizards always thermoregulate carefully), it showed that physiology can evolve faster than morphology, and it proposed that only thermoregulators (not thermoconformers) could invade the temp zone.

You can find transcripts from a 1998 interview with Rodolfo as part of a UC-Riverside history project. Here’s the obituary that recently appeared in UCR Today:

Professor Emeritus Rodolfo “Rudy” Ruibal, a founding member of UC Riverside’s Biology department whose passions included lizards, frogs and making beautiful jewelry, died Aug. 30 at the age of 88, just six months after the death of his wife of 68 years, Irene Shamu Ruibal.

“He was instrumental in forging the department in the directions and expertise that form its center now,” said Professor Michael Allen, chair of UCR’s biology department.

Ruibal was a native of Cuba who conducted research in several parts of South America with fellowships from the National Science Foundation and the John Simon Guggenheim Memorial Foundation. He was an early student of temperature regulation in reptiles and amphibians, said friend and colleague Professor Mark Chappell, and was also known for his work with water loss in amphibians and their ability to waterproof their skin by using waxy glandular secretions the animals wipe over themselves.

“He taught the Biology 161 course, on functional vertebrate morphology, or ‘Vert’ to generations of premeds and other life science students, and was renowned for both the clarity of his lectures and for his skill in drawing structures on the blackboard,” said Chappell.

During Ruibal’s 42 years at UCR, he helped establish the Philip Boyd Desert Research Center and spent a year as the acting director of UC MEXUS, created to stimulate teaching and research between California and Mexico. Ruibal also spent a year advising a man he much admired—UC President Clark Kerr—about faculty requests and concerns.

“He always had one faculty member in his office,” Ruibal said during an oral history interview in 1998. “It was his way of simply making sure his faculty were being treated by an academic who knew what the score was, rather than somebody who was just a bureaucrat.”

Ruibal’s life read like a novel. He was born in Cuba on Oct. 27, 1927, an only child who attended the same Jesuit school as Fidel Castro. The budding scientist had an early fascination for animals, said his son, Claude Ruibal of Zurich, Switzerland. Rudy Ruibal’s earliest memories were of watching fish swimming in the waters of Cuba, and chasing lizards in his yard, something his aunt remembered years later, when he returned to Cuba for research on an NSF grant project.

Reptiles and research always fascinated Ruibal, and he excelled at an early age. He enrolled in Harvard when he was just 16 years old, after completing high school at the prestigious McBurney School in Manhattan.

Ruibal took a break from Harvard when he was 18, to serve in the military at the tail end of World War II. But he returned to school a year later and married his wife, Irene, a secretary in the Department of Herpetology in the American Museum of Natural History.

By the time he was 21, Ruibal had finished his BA at Harvard and enrolled at Columbia University for graduate studies in biology. At 26, Ruibal completed his PhD and accepted a position at a new liberal arts college called UC Riverside, where Howard Spieth, one of his former professors at Columbia, had become the chair of the life science’s department, and would later become the university’s first chancellor.

Ruibal began teaching in the fall of 1954, the second semester for a school so new that it had no landscaping or trees. Their son was born the following year, in 1955. Claude Ruibal said his parents were loving but not overbearing. His father, he said, “was a thoughtful guy, a moral guy—very rational and not very emotional. I don’t think I ever heard my parents argue.”

His mother loved to cook and throw dinner parties, and they cultivated a diverse group of close friends—artists, business people, even the publisher of the newspaper. His father loved tennis, playing into his 80s, and did a lot of reading about history and politics.

Ruibal also was a noted local artist. Shortly after he arrived in Riverside, he successfully lobbied the Riverside Art Museum to have real nude models available for sketching (instead of women in bathing suits). He later branched into candle making, ceramics —complete with his own kiln—and finally, making brass and silver jewelry, which were top sellers at the Riverside Art Museum, Mission Inn Museum and other locations.

Anole Fashion: Dorsal Crests and Curlicue Tails

Daffodil’s Photo Blog has some nice photos of stylish anoles. Some anoles–the festive anole (A. sagrei) being a prime example, seem to have a penchant for sitting with their tails hanging in a lovely. Why do they do it? Got me.

We do know why they raise their dorsal crests–to look fearsome, as this mini-dinosaur does. How they do it, though, is another matter, when discussed previously in these pages (1,2).

Best Anole Dewlap of All Time?

sericeus

There are many contenders, but my favorite is Anolis sericeus, seen above from the Kanahau research station on the Honduran island of Utila, and another photo below from Chiapas, Mexico.

Age Structure of Invasive Green Anole Populations near Japan

Yasumiba et al 2016 Fig 1

Figure from a new paper by Yasumiba et al. illustrating how LAGs in the cross sections of bones can be used to infer lizard age.

Anolis carolinensis is a disruptive invasive species in the Osagawara Islands near Japan, a UNESCO World Natural Heritage site.  It was first recorded on the island of Chichi-jima in the 1960’s and has since spread to surrounding islands. A recent post on Anole Annals describes efforts to improve the effectiveness of adhesive lizard traps on the islands by using cricket bait.

A new paper by Yasumiba et al. improves our understanding of these invasive A. carolinensis by quantifying their longevity and growth rates using skeletochronology.

Field Notes from Long Island, Bahamas

smaragdinus-and-sagrei

Anolis smaragdinus (left) and Anolis sagrei (right) from Long Island, Bahamas. The individual on the right is marked as part of selection study.

This past August, two field assistants and I went to Long Island, Bahamas to collect data on sympatric populations of Anolis sagrei and Anolis smaragdinus as part of a natural selection study. Our primary study area is a small island (approximately 1000 ft x 200 ft) in the middle of a lake with relatively high densities of both species. While in the field we observed some interesting behaviors that I want to share with the AA community in hopes that you will find them interesting as well!

1) Frugivory by anoles was common at our study site, which had an abundant supply of small berries from black torch (Ertihalis fruticosa) and small-leaved blolly (Guapira discolor).  Anolis smaragdinus was usually the culprit, although we did we did see one adult male A. sagrei eating fruit.

2) We captured (and released) over 150 unique A. smaragdinus and later re-spotted several of those individuals. During a typical eight-hour day, we encountered 15-20 individuals, a surprisingly large portion of which were a male and a female in the same tree. These instances made a particularly strong impression on me when they were separated by long periods of not seeing any A. smaragdinus. I can think of multiple occasions in which we found a couple together, saw no individuals for another three hours, and then suddenly came across another couple. In several instances, there were three individuals in the same tree. I’m not aware of green anoles mate guarding, and unfortunately the data I have don’t have the resolution to provide much insight here, but the pattern was definitely striking.

smaragdinus-cannibalism

3) We observed an act of cannibalism in A.smaragdinus, a species for which cannibalism has not previously been reported (although it has reported for the closely related A. carolinensis). We captured an adult female, saw that she was eating something, and proceeded to lose our marbles after pulling a hatchling (pictured) out of her mouth. Acts of cannibalism by female anoles appear to be rather uncommon (see page 30 of this Anolis newsletter), making this observation perhaps the most intriguing of our adventure!

Lizards Running (and Slipping) in Ultra-Slo-Mo!

Day’s Edge Productions has done it again (again? see here and here).

JMIH 2016: Rock ‘n’ Bowl Anole

At the JMIH in New Orleans this past July, the 100th anniversary celebration of the ASIH was held at the Rock ‘n’ Bowl, where music, food, drink, dancing, and bowling were enjoyed by all. But for those who were alert on their way in, there was an added bonus: anoles! Or, at least, one anole, spotted by Quynh Quach and corralled by Kristin Winchell.

Quynh and Kristin spot their quarry.

As other attendees file in, Quynh and Kristin spot their quarry in the bushes.

Taking a picture of the crowd filing in, I serendipitously caught our two intrepid anoleers  about to make the catch in the bushes to the right of the entrance. Kristin made the grab, and displayed her catch.

Kristin displays the catch.

Kristin displays the catch.

It was, of course, Anolis sagrei, the invasive Cuban species which has been spreading through the southeastern US for more than 80 years now. He was a nice-sized adult male, typical of the nominate form that occurs through most of the species’ US range.  The edificarian habitat– in bushes at the edge of a parking lot next to a building– is also typical of where invasive sagrei can be found.

Adult male Anolis sagrei, New Orleans, Louisiana, 10 July 2016.

An appreciative crowd gathered.

Eager anolologists immortalize the NOLA anole in pixels.

Eager anolologists immortalize the NOLA anole in pixels.

I was glad to see it, because prior to this I had only seen Anolis carolinensis in New Orleans (more on this in a later post).

Quyhn and Kristin show off their catch.

Quynh and Kristin show off their catch.

 

Does Evolution or Ecology of Anolis Lizards Shape the Bacterial Communities Living in their Guts?

fig2ren2016

Figure 2 from Ren et al. 2016: “Diversity of Anolis gut microbiota as a function of host phylogeny. Each thin horizontal bar represents an individual lizard, with bacterial diversity (proportion of reads) coded at phylum, family, and genus.”

In recent years, the study of microbiomes – the communities of microorganisms living in certain environments or in association with hosts – has boomed. It’s long been understood that microorganisms (especially bacteria) can play a big role in host health, but recent work has also shown that microbes can have a huge impact on many other important facets of a host’s life, from growth and development to behavior. Despite the importance of these microbiomes, the ecological and evolutionary processes that shape them are still not very well understood.

In a recent study, Ren et al. (2016) decided to use our favorite model system to better understand the relationship between host and microbiome. As a classic example of an adaptive radiation, Anolis lizards provide an opportunity to test both ecological and evolutionary factors that might be influencing their microbiomes. In this study, the authors asked whether the evolutionary and ecological diversification of a host lineage (anoles) has structured the biodiversity of the gut microbiome community.

IMG_0455

A. evermanii and A. gundlachi sharing a perch

The authors used several approaches to address this question. First, they sampled gut microbiomes (using fecal samples) from six Puerto Rican anole species representing three ecomorphs: two trunk-crown sister species (A. evermanii and A. stratulus), two grass-bush sister species (A. pulchellus and A. krugi), and two trunk-ground species (A. cristatellus and A. gundlachi). They predicted that microbiomes of species of the same ecomorph would be more similar to one another than to species of different ecomorphs, reflecting an influence of either ecological similarity or phylogenetic relatedness on gut microbiome composition. Second, they sampled invasive populations of two trunk-ground species in Florida (A. cristatellus and A. sagrei) in sympatry and in allopatry to explore a) whether species that are phylogenetically distinct but ecologically similar have similar gut microbiomes and b) whether gut microbiome is influenced by the local environment. Lastly, they documented individual variation in gut microbiome composition over time by recapturing and resampling marked individuals.

The most striking result of the study was the huge amount of variability in gut microbiome composition between individuals (Fig 2, Ren et al. 2016). For example, on average, any two gut microbiomes only shared 7% of their bacterial OTUs (“Operational Taxonomic Units,” you can think of them as bacterial species). Such high variability from one individual to another is notable, compared to studies of other organisms.

In their analysis of the Puerto Rican anoles, the researchers found that gut microbiomes were more similar between conspecifics than between individuals of different species, but only weakly so. Perhaps more surprisingly, there was no difference in gut microbiome composition based on ecomorph. The authors suggest that this lack of distinction between ecomorphs may stem from the fact that most anoles are dietary generalists; although different ecomorphs do partition habitats, they still overlap in the types of arthropods that they consume, which could impact their gut microbiomes. The authors find further support for this conclusion in their separate analysis of temporal variation in A. sagrei. The composition of an individual’s gut microbial community fluctuated greatly over time, suggesting that transient factors (such as variability in diet) have a significant impact on the gut microbiome.

Interestingly, the two invasive trunk-ground species in Florida showed a much stronger pattern: despite being of the same ecomorph, the gut microbiomes of the two species were significantly different from one another. The authors suggest that the strong signal in these not-so-closely-related invasive anoles along with the weak signal in the closely-related Puerto Rican anoles might indicate that Anolis evolution could have impacted the diversification of the gut microbiome over long evolutionary timescales, but the Puerto Rican radiation just is too young for such microbiome divergence to have occurred. But it’s also possible that the difference in the microbiomes of the two invasive anoles is just a holdover from the source environments (Puerto Rico and Cuba) that has been maintained in their invasive ranges. To throw another wrench into the works, the authors also found that allopatric populations of one of the invasive species (A. cristatellus) were different from one another, while those of the other invasive species (A. sagrei) were not.

So does host ecology impact gut microbiome? Does host phylogeny? Or host environment? Ren et al.’s study suggests possibly yes to all, but with limited (and somewhat conflicting) evidence, it’s hard to draw any certain conclusions. Perhaps more poop from more branches of the Anolis tree will hold the answers.

 

Find the full paper here:
Ren, T. et al., 2016. Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards. Molecular Ecology.

Praying Mantis Eats Anole

carolinensis eaten by praying mantis

The stuff of science fiction horror stories. We’ve previously reported on spiders eating anoles [e.g., 1, 2 and type “spiders” into search bar for more], but reports of anolivory by other invertebrates are scarce. Some others (from p.141 of Lizards in an Evolutionary Tree): katydids, tarantulas, whip scorpions, and centipedes.

Ecology of the San Salvador Bark Anole (Anolis distichus ocior)

 An adult male San Salvador Bark Anole (Anolis distichus ocior) displaying. Photograph by Guillermo G. Zuniga.

An adult male San Salvador Bark Anole (Anolis distichus ocior) displaying.
Photograph by Guillermo G. Zuniga.

Dayton Antley and colleagues from Avila University, the home of AA stalwart Bob Powell, recently published a detailed study of the ecology of the San Salvador bark anole (Anolis distichus ocior) in IRCF Reptiles & Amphibians (an open-access herpetological journal, with this article available here). Anolis d. ocior is one of 17 recognized subspecies of the diverse distichus group, and is found on only San Salvador and Rum Cay (Henderson and Powell 2009).

Antley et al. assessed microhabitat use, activity patterns, and approach distances of A. d. ocior in an approximately 0.3ha study area on the grounds of the Gerace Research Centre, dominated by Tropical Almonds (Terminalia catappa), Papaya (Carica papaya), and Ficus trees.

A Google Map view of the Gerace Research Centre. The study site (24°07'05.2"N 74°27'50.9"W) is outlined in white.

A Google Map view of the Gerace Research Centre. The study site
(24°07’05.2″N 74°27’50.9″W) is outlined in white.

In assessing patterns of microhabitat use throughout the day, Antley et al. conducted surveys every two hours for two days from 0700h (about 40 min after sunrise) to 1900h (about 40 min before sunset). Size class, perch height and diameter, body orientation relative to the ground, and thermal microsite (sun/shade/mixed) were recorded for every observed lizard. In the following two days, approach distances were assessed. This was achieved by a surveyor, wearing neutrally-coloured clothing, approaching an undisturbed anole at a steady pace and recording the distance at which the lizard reacted. Over two additional days, 10-minute focal animal observations were conducted of individual adult lizards (including both males and females) at a distance of 5m. The number of movements (changes in location or orientation), head turns, and head bobs were recorded for all lizards, with dewlap displays and pushups being additional recorded for males.

Lizards were active throughout the day, with activity peaking in the early morning and before midday. This was compared to ambient air temperatures recorded 1m from the ground in a shaded and sheltered location. This result surprised the authors, as a second activity peak in late afternoon/early evening was expected, as has observed in other similar studies of bark anoles (e.g. Hillbrand et al. 2011).

Mean number of lizards active (bars) and mean ambient temperatures (dots) per time period. Temperature data were collected on two consecutive days.

Mean number of lizards active (bars) and mean ambient temperatures
(dots) per time period. Temperature data were collected on
two consecutive days.

Adult males experienced highest levels of arboreality during the middle of the day, while subadult males and adult females (grouped together as they can be hard to distinguish from distance) were highly variable (see figure below). Most lizards of all classes were found in the shade, which the authors attributed as evidence for thermal conformity, and facing downward towards the ground, a common trait in many anoles that is most commonly perceived to increase an individual’s ability to monitor potential predators, competitors, or mates. 43% of lizards, however, were observed facing upwards. The author’s note that this behavior is often interpreted as an individual prepared for escape; however as all lizards were observed from distance and undisturbed, they (admirably) explain that this result is difficult to interpret.

A: Mean perch heights (cm) of adult males (L) and subadult males and females (S); B: mean perch heights of adult males at different times of day; C: mean perch heights of subadult males and females at different times of day.

A: Mean perch heights (cm) of adult males (L) and subadult males and females (S); B: mean perch heights of adult males at different times of day;
C: mean perch heights of subadult males and females at different times of day.

Adult male lizards were bolder than smaller subadult males and females, and retreated at a much closer distance when approached by a surveyor (0.99m +/- 0.07m vs. 1.54m +/- 0.18m). Focal observations revealed no significant differences between adult males vs. subadult males/females in shared behaviors, although there was a high variation in the amount of displaying behavior between adult males. The average time spent conducting dewlap displays was 3%, although one male was recorded investing 47% of his time in a combination of dewlap extensions and pushup displays.

Using all survey data combined, Antley et al. estimate that A. d. ocior in this study plot had a population density of 593 individuals/ha, with lizards observed on all but four of the smallest trees surveyed. Antley et al. note that their density estimate is extremely conservative, and much lower than previously published estimates (e.g. 1.070-5,460 individuals/ha, Schoener and Schoener 1978). The authors suggest that the small size of the study plot may have contributed to the relatively low density.

In all, this is a charming (although admittedly short) study of the natural history of the San Salvador bark anole (A. d. ocior) – a great example of an undergraduate research project that follows through to publication!

References
– Antley, D.L. et al. 2016. Microhabitat, Activity, and Approach Distances of the San Salvador Bark Anole (Anolis distichus ocior). IRCF Reptiles & Amphibians 23(2): 75-81
– Henderson, R.W. and R. Powell. 2009. Natural History of West Indian Reptiles and Amphibians. University of Florida Press, Gainesville, Florida.
– Hillbrand, P.A., A.T. Sloan, and W.K. Hayes. 2011. The terrestrial reptiles of San Salvador Island, Bahamas. Reptiles & Amphibians 18: 154–166.
– Schoener, T.W. and A. Schoener. 1978. Estimating and interpreting body-size growth in some Anolis lizards. Copeia 1978: 390–405.

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