Category: New Research Page 17 of 67

Of Rats and Reptiles: An Expedition to Redonda

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Anolis nubilus male and female from The Anoles of the Lesser Antilles.

In 1972, James “Skip” Lazell published a monograph on the Anoles of the Lesser Antilles including the species description of Anolis nubilus, an endemic anole restricted to the island of Redonda. His description of the animal and island, like the rest of the monograph, is colorful and evocative:

“The tiny islet is exceedingly steep-to, and rises nearly 1000 feet out of the sea. There is virtually no surrounding bank, and the full swell of the western North Atlantic pounds Redonda’s cliffs. A tiny, nearly vertical gut on the leeward side provides the only access to the top of the islet up the cliffs; great blocks of basalt lie at the foot of this gut and one’s original entrance to Redonda is made by jumping onto these blocks as the boat goes past them. It is about like jumping from a moving elevator onto a card table, except that elevators give more notice of directional reversals… but getting on is just the beginning. …

The top of Redonda is a rolling wold and a favorite place of innumerable nesting sea birds; the gut provides a route for their guano to descend the cliffs, and it dries to a thick powder there. Because of its lee-ward location, a chimney effect is produced in the gut, and the guano dust, mixed with the volcanic sand weathered from the parent rock, tends to rise when disturbed. As one toils up the gut under the tropical sun, one is accompanied by a cloud of this dust, which soon mingles with one’s own sweat to produce a wondrously aromatic and abrasive, though rather gluey, bath. At the top, jumbles of rocks and clumps of prickly pear rise gently to the old ruins, complete with a hedge of bougainvillea and a single tree. This is the home of Anolis nubilus. …

Surely Redonda once supported more vegetation, and presumably Anolis nubilus then had an easier life. The feral goats should be extirpated on this remarkable island, whose only known nonflying vertebrates are species found nowhere else on earth.”

Now, 45 years, 1 week, and 4 days later, I’m headed to Redonda to gather baseline lizard data on exactly such a goat extirpation.

Skip did miss one nonflying vertebrate in his account; Rattus rattus has taken up residence en masse on Redonda. The black rats are so plentiful now that they’ve taken to stalking the lizards on the island in daytime—“tiger rats,” according to Dr. Jenny Daltry, one of the researchers leading the island restoration effort. And so, the government of Antigua and Barbuda, in conjunction with numerous conservation NGOs including Flora and Fauna International, has decided to remove the goats and rats from Redonda in an attempt to restore the island and help its three endemic lizard species to recover.

Redonda is home to not just A. nubilus but also a jet black ground lizard, Ameiva atrata and an as-yet unnamed dwarf gecko, Sphaerodactylus sp. Presumably, A. nubilus would be perched high in vegetation avoiding the roving A. atrata; however, after centuries of goat grazing on Redonda, that vegetation has been reduced to a single Cassuarina tree. So, while that tree is likely swarming with anoles, most of the A. nubilus are spending their time hopping around the boulders of Redonda. Normally this would put them in range of the roving ground lizards, but it sounds as though both lizards should be more worried about those hungry black rats.

Fortunately for all of Redonda’s reptiles, as of a few weeks ago the goats on the island took a one-way ferry ride to new pastures (not a euphemism) and, well, starting soon the rats will be making their way to the great big garbage heap in the sky (definitely a euphemism). My goal is to get to Redonda and gather as much baseline data on the lizards as possible to see whether and how the lizard community changes on a goat-less, rat-free Redonda.

That’s no easy task, though. Here’s a picture of Redonda:

Photo credit: Dr. Jenny Daltry

Photo credit: Dr. Jenny Daltry. I’m reasonably sure that’s the gut there, in the foreground of the image.

Believe it or not, that’s the pleasant side of the island. Here’s the other:

Photo credit: TopTenz.net

Photo credit: TopTenz.net

We decided that hauling a week’s worth of research and camping gear up Lazell’s gut (let alone jumping to that card-table basalt) was out of the question, so I’m going to be arriving by helicopter. As if the rats weren’t enough, Redonda has no source of fresh water so we’ll be carrying in food and drink for the 8 days on the island. No power either, so I’ve been putting together solar kits to try to get enough juice to run a computer and spectrophotometer.

All in all, it’s going to be an adventure! I’ll update Anole Annals when I return, but I’ll also be posting more frequent updates to my personal blog and twitter. I’d love to hear from you, especially if you have any tips for rat-proofing tents (seems more efficient to just bait the other ones, right?).

Citation: Lazell, J.D. 1972. The Anoles (Sauria, Iguanidae) of the Lesser Antilles. Bulletin of the Museum of Comparative Zoology. 143(1).

Anolis sagrei Now in the Southern Hemisphere, First Record for South America

Anolis sagrei has successfully invaded several countries including the United States, Mexico, some Caribbean islands, and even Taiwan and Singapore in Asia. As an invasive species, brown anoles can reach high population densities, expand their range rapidly, and have a negative effect on native species of lizards.

Now, this tree lizard has gone further. A group of Ecuadorian herpetologists recently discovered some individuals of this species in two localities on the Pacific coast of Ecuador. These individuals also represent the first record of this invasive species in South America.

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 A juvenile male individual of Anolis sagrei  found in Ecuador

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World map showing the distribution of Anolis sagrei. Green spots correspond to native distribution, blue spots non-native distribution, and the red star corresponds to the new records from Ecuador.

Individuals were found in an urban area with a mix of native and introduced species of plants. Although an established population has not been confirmed, this finding certainly represents a potential threat to local species of lizards from Ecuador, home to 38 species of anoles. A note reporting this discovery is in publication process.

Acknowledgments

Thanks to Omar Torres-Carvajal who helped with the post.

Cuban Anolis porcatus introduced to Brazil (perhaps through Florida?)

Several anole species have become established outside of their native ranges as a result of human-mediated transportation, being introduced to Japan, Singapore, Taiwan, Hawaii, the continental U.S., and beyond. Alien anoles can have major impacts on the ecological communities that they invade, for instance leading to local extinction of arthropod taxa and displacing native anole species. It is therefore key to detect and report instances of introduction by these potentially aggressive invaders, as well as to document their geographic spread in colonized regions. In a recent paper, we report on the presence of Anolis porcatus, a species native from Cuba, in coastal southeastern Brazil, using DNA sequence data to support species identification and examine the geographic source of introduction.

Anolis porcatus collected in Brazil, and comparison with the native anole A. punctatus. A, male A. porcatus showing green coloration. B, male A. porcatus showing brown coloration. C, the pink dewlap of male A. porcatus. D, female A. porcatus. E, male A. punctatus, a native anole species. F, the yellow dewlap of male A. punctatus. Picture credits: A–D, Mauro Teixeira Jr.; E, Renato Recoder.

Anolis porcatus collected in Brazil, and comparison with the native anole A. punctatus. A, male A. porcatus showing green coloration. B, male A. porcatus showing brown coloration. C, the pink dewlap of male A. porcatus. D, female A. porcatus. E, male A. punctatus, a native anole species. F, the yellow dewlap of male A. punctatus. Picture credits: A–D, Mauro Teixeira Jr.; E, Renato Recoder.

Perhaps embarrassingly, this study started with Facebook. On August 2015, Ricardo Samelo, an undergraduate Biology student at the Universidade Paulista in Santos, posted a few pictures of an unknown green lizard in the group ‘Herpetologia Brasileira.’ A heated debate about the animal’s identity took place, with people eventually agreeing on Anolis carolinensis. On my way to Brazil to join the Brazilian Congress of Herpetology, I contacted Ricardo (but only after properly hitting the ‘like’ button) and proposed to examine whether the exotic anole was established more broadly in the Baixada Santista region.

To our surprise, local residents knew the lizards well, with some people quite fond of the ‘lagartixas’ due to their pink dewlap displays. People could often tell when the anoles were first noticed in the vicinities – ‘six months’, ‘nine months’, ‘one year ago’ –, suggesting a rather recent presence. Guided by these informal reports, we sampled sites in the municipalities of Santos, São Vicente and Guarujá, where we found dozens of lizards occupying building walls, light posts, fences, debris, trees, shrubs, and lawn in residential yards, abandoned lots, and alongside streets and sewage canals. It was clear that the alien anoles are doing great in human-modified areas; the high density of individuals across multiple sites, as well as the presence of juveniles with various body sizes, seem to suggest a well-established reproductive population.

Sites in the Baixada Santista in southeastern coastal Brazil where introduced A. porcatus were detected. 1, Guarujá. 2, Santos. 3, São Vicente. Green indicates Atlantic Forest cover; gray indicates urban areas; black indicates water bodies.

Sites in the Baixada Santista in southeastern coastal Brazil where introduced A. porcatus were detected. 1, Guarujá. 2, Santos. 3, São Vicente. Green indicates Atlantic Forest cover; gray indicates urban areas; black indicates water bodies.

By reading and bugging experienced anole researchers about the Anolis carolinensis species group, I learned about paraphyly among species, hybridization, and unclear species diagnosis based on external morphology. As a result, my PhD supervisor, Dr. Ana Carnaval, and I decided to recruit Leyla Hernandez, by the time an undergraduate student in the Carnaval Lab at the City University of New York, to help generate DNA sequences to clarify the species identity, and perhaps track the geographic source of introduction in Brazil. To our surprise, a phylogenetic analysis found Brazilian samples to nest within Anolis porcatus, a Cuban species that has also been introduced to Florida and the Dominican Republic. Brazilian A. porcatus clustered with samples from La Habana, Matanzas, and Pinar del Río, which may suggest a western Cuban source of colonization. Nevertheless, Brazilian specimens are also closely related to a sample from Coral Gables in Florida, which may suggest that the Brazilian population originated from lizards that are exotic elsewhere.

Phylogenetic relationships of A. porcatus introduced into Brazil (indicated in red), inferred using MrBayes based on a mitochondrial DNA locus. Purple indicates samples of A. porcatus invasive elsewhere (Florida and the Dominican Republic). Blue indicates native Atlantic Forest anole species. Asterisks indicate posterior probability >0.95. Picture depicts a male A. porcatus collected in São Vicente, Brazil.

Phylogenetic relationships of A. porcatus introduced into Brazil (indicated in red), inferred using MrBayes based on a mitochondrial DNA locus. Purple indicates samples of A. porcatus invasive elsewhere (Florida and the Dominican Republic). Blue indicates native Atlantic Forest anole species. Asterisks indicate posterior probability >0.95. Picture depicts a male A. porcatus collected in São Vicente, Brazil.

The presence of A. porcatus in the Baixada Santista may be related to the country’s largest seaport complex, the Porto de Santos, in this region. Numerous storage lots for intermodal shipping containers were situated near sites where the lizards were detected, and in one instance we found the animals sheltered inside an open container. An exotic green anole (identified as A. carolinensis) was previously found in Salvador in Brazil’s northeast; like Santos, Salvador hosts a major seaport complex, which may indicate that the exotic anoles reached Brazil after being unintentionally transported by ships bringing goods from overseas perhaps twice independently.

It is currently unclear whether A. porcatus will be able to expand into the surrounding coastal Atlantic Rainforest, or into more open natural settings such as shrublands in the Cerrado domain. It is also unknown whether this species will have negative impacts on the local ecological communities. In Brazil, introduced A. porcatus may potentially compete with other diurnal arboreal lizards, such as Enyalius, Polychrus, Urostrophus, and the native Anolis. Five native anoles inhabit the Atlantic Forest (for sure): A. fuscoauratus, A. nasofrontalis, A. ortonii, A. pseudotigrinus, and A. punctatus. While none of them is currently known to occur in sympatry with A. porcatus, the worryingly similar A. punctatus has been reported for a site in Bertioga located only 50 kilometers from the site in Guarujá where we found the exotic anoles.

To properly evaluate the potentially invasive status of A. porcatus in Brazil, we hope to continue assessing the extent of its distribution and potential for future spread, as well as to gather data about whether and how A. porcatus will interact with the local species – especially native Brazilian anoles. This seemingly recent, currently expanding colonization also represents an exciting opportunity for comparisons with other instances of introduction of A. porcatus, as well as the closely-related A. carolinensis, based on ecological and phenotypic data.

Studying such mysterious alien anoles in Brazil was made much more tractable through advice from Jonathan Losos and Richard Glor. Thank you!

To learn more: Prates I., Hernandez L., Samelo R.R., Carnaval, A.C. (2016). Molecular identification and geographic origin of an exotic anole lizard introduced to Brazil, with remarks on its natural history. South American Journal of Herpetology, 11(3): 220-227.

Habitat Disturbance Negatively Affects the Body Condition Index of Anolis antonii

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Anolis antonii from the agricultural area

Habitat disturbance is considered one of the most important threats to biodiversity. Particularly, anthropogenic disturbance for agricultural practices alters the original structure of Anolis habitats and consequently negatively affects their health and survival. Because the body condition index (BCI) is an effective indicator to assess the health of animals, we hypothesized that the BCI of the Colombian endemic lizard Anolis antonii from an undisturbed habitat (natural area) would be higher than that from the disturbed habitat (agricultural area).

We studied two populations of Anolis antonii from the municipality of Ibague, Tolima, Colombia: (1) a population from an agricultural area cultivated with coffee (Coffea arabica) and plantains (Musa paradisiaca), and (2) a population from a secondary forest, an anthropogenic-free area. We measured the snout-vent length (SVL) and body mass (BM) of adult anoles (males and females)and calculated BCI from the residuals of a linear regression between BM and SVL.

Fig 2. A) Forest habitat and B) Agricultural habitat of Anolis antonii (Ibagué – Colombia)

We found that the BCI of the lizard population from the agricultural area was significantly lower than that of the secondary forest population. Consequently, A. antonii from the secondary forest, with a higher BCI, might have a greater ability to compete for available resources and survive than those from the cultivated area. Thus, this work shows that anthropogenic disturbance negatively decreases the body conditions of A. antonii lizards, which might represent a forthcoming threat for its conservation, especially due to the current habitat deterioration of this species by agriculture activities.

Read the paper:

Gallego-Carmona, C.A., Castro-Arango, J.A. and Bernal-Bautista, M.H., 2016. Effect of Habitat Disturbance on the Body Condition Index of the Colombian Endemic Lizard Anolis antonii (Squamata: Dactyloidae). South American Journal of Herpetology 11(3):183-187.

Adult Male Density Influences Juvenile Microhabitat Use in Brown Anoles

Photographs of the housing conditions used in the experiment. (a) One of the experimental enclosures (with an artificial tree) surrounded by blinds on all sides (note, the front blind was pulled back to reveal the tree and cage). (b) Close-up of the available horizontal perches. (c) Juvenile Anolis sagrei with its identification number on the lateral body surface for visual identification.

Fig 1. Photographs of the housing conditions used in the experiment. (a) One of the experimental enclosures (with an artificial tree) surrounded by blinds on all sides (note, the front blind was pulled back to reveal the tree and cage). (b) Close-up of the available horizontal perches. (c) Juvenile Anolis sagrei with its identification number on the lateral body surface for visual identification.

For many animals, optimal habitats vary across age classes, and individuals shift habitat use as they age. While many studies have documented such age-specific habitat use, most are observational and do not identify the causal factors. In addition, we know that competition between species has been an important driver of habitat use in Anolis lizards. However, less is known about the role of competition on habitat use within species of anoles, especially between age classes.

Dan Warner and I previously found that adults use higher and thicker perches than juveniles at our field site in northeastern Florida (Delaney and Warner 2016). We hypothesized that this variation was a result of adults forcing juveniles to suboptimal habitat. Thus, we altered the density of adult males in mesh enclosures (Fig. 1) in the lab and monitored changes in juvenile microhabitat choice.

Anoles Are Habitat Specialists at the Individual Level Too

Anoles are probably best known for the ecomorph story: the presence of specialized species adapted to the same sets of structural microhabitats on different islands. Anoles in the Greater Antilles have contributed hugely to our understanding of both the evolutionary history and the contemporary ecology of communities of specialists.

While they are better known for specialization of species in communities, anoles have also contributed to our understanding of within-species ecological diversity. Around the same time that Ernest Williams was developing the ecomorph concept, Roughgarden (1972) used data from Lesser Antillean anoles to introduce a new framework for investigating the extent to which a population’s niche width (i.e. the diversity of habitats it uses or prey it eats) is determined by variation among individuals versus variation within individuals. For example, individuals in a population of Anolis roquet differ in the size of prey they consume, mainly because larger individuals can catch and ingest larger prey items. While Roughgarden’s early work set the stage for an explosion of studies of individual specialization over the past decade or two (reviewed in Araújo et al. 2011), surprisingly little work has been done to revisit individual specialization within species of anoles. In particular, we don’t know enough about how much individuals specialize in important aspects of microhabitat that differentiate ecomorphs, especially perch height and perch diameter.

"Gar" lived alone on my desk, so I don’t know if he was an individual specialist or not

“Gar” lived alone on my desk, so I don’t know if he was an individual specialist or not

Anole Annals contributors Ambika Kamath and Jonathan Losos have helped to fill this gap with a study just published online in Evolution. Ambika and her team spent a summer observing microhabitat use of a population of brown anoles (Anolis sagrei) in a forested park in Gainesville FL. They marked lizards with colored beads, and repeatedly recorded individual lizards’ perch height and diameter, compiling a total of over 1000 observations of 80 anoles. They grouped perch heights and perch diameters into classes, then compared the distribution used by each individual to the distribution used by the whole population (or to the distribution available to that individual) using a proportional similarity index. The mean value of this index gives a measure of the overall degree of individual specialization in a population, as lower overlap values tell us that individuals are specializing on a subset of the available perches.

SICB 2017: Are Anoles Less Stable When Running Without Using Claws?

Photo courtesy of Catalina Mantilla

Photo courtesy of Catalina Mantilla

This post was written by Brittney Ivanov, research technician in Michele Johnson’s lab at Trinity University.

Catalina Mantilla, a Ph.D. candidate at Florida International University working with Tonia Hsieh of Temple University, is interested in how anoles use their toepads and claws when they run. For most animals, movement on vertical perches such as tree trunks or buildings usually requires specialized morphologies to adhere to these substrates. While many species have evolved adaptations for moving through complex arboreal habits (e.g., prehensile tails or feet, sticky pads, spines), anoles evolved enlarged toepads and distinct claws, presumably to allow for better adhesion. The morphologies of these specialized structures can greatly impact performance; for example, greater toepad area is associated with greater clinging ability. Catalina wanted to better understand how toepads and claws work together to enhance running performance.

Catalina collected 17 males from four Anolis species (A. carolinensis, A. sagrei, A. cristatellus, and A. distichus). Each male was tested in four different running courses to test performance at difference inclines and on different substrates. Two of the courses were positioned at a 45° incline and two at a flat (0°) incline. Plexiglass covered one course at each incline to allow the use of toepads and eliminate the use of claws. Nylon mesh covered the other course at each incline to test the use of both toepads and claws. Performance was evaluated using mean relative sprint speed, relative stride length, and stride frequency.

Catalina found, unexpectedly, that when the lizards ran on the level plexiglass, they ran slower, took shorter strides, and increased their stride frequency compared to when they ran on the inclines. These results suggest that anoles are less stable when they can’t use their claws! in addition, these data support the idea that the combination of toepads and claws is important for their running performance. In the future, Catalina hopes to increase the number of species in this study to determine the effect of ecomorph on claw and toepad interactions during running, and to evaluate limb function changes when running across different inclines.

SICB 2017: How Anoles Climb Trees: Ecomorph Differences in Neuromuscular Function

Kathleen Foster presents her work to a packed room at SICB.

Kathleen Foster presents her work to a packed room at SICB.

Regular readers of AA will be familiar with the differences in microhabitat use that define the Anolis ecomorphs, but do species with such distinct structural habitats move differently on their specialized perches? In other words, does muscle function differ between the ecomorphs? In the very last session at this year’s SICB, Kathleen Foster, currently a postdoctoral researcher at the University of Ottawa studying the biomechanics of fish locomotion (come back to anoles, Kathleen!), presented a portion of her graduate work in Tim Higham’s lab at the University of California, Riverside, to address this question. She used high speed video to film five species of anoles running on broad and narrow perches at two angled inclines, combined with electromyography to record fore- and hindlimb muscle activity during running.

Photo courtesy of Kathleen Foster.

Photo courtesy of Kathleen Foster.

Kathleen found that all five species had greater motor unit recruitment on steeper inclines than on horizontal perches, and that muscle activity is shorter but begins more abruptly on inclines. Further, recruitment of the gastrocnemius (a “calf” muscle) was greater on broad perches, because the way lizards sit on narrow perches limits the function of this muscle. If you’ve seen how anoles position their feet on both sides of narrow perches, it’s easy to understand how this posture prevents effective propulsion by ankle extension. Kathleen also found several intriguing differences that distinguish trunk-ground species’ muscle function from trunk-crown and crown-giant species. The activity of the caudofemoralis (a limb retractor muscle in the hindlimb) changes more in trunk-ground species as a function of incline, and trunk-ground species use the biceps and gastrocnemius more in the early stance phase of propulsion than trunk-crown species.

Overall, these data help us understand how specialization in neuromuscular function can allow different anole species to successfully move through their varying habitats, and offer insight into how behavioral differences depend on the muscles that underlie them.

SICB 2017: Impacts of Urbanization on Morphology, Thermal Preference, and Parasitism

Chris Thawley at a crossroads.

Chris Thawley at a crossroads.

Urban environments are widespread and expanding across much of the earth, and this urbanization likely affects the flora and fauna in its path. Anoles are no exception and are frequently observed perching on anthropogenic structures. Thus, Chris Thawley, a post-doc in Jason Kolbe’s lab at the University of Rhode Island, and colleagues wondered how the abiotic and biotic changes in urban areas influence anole traits.

Thawley compared populations in urban and natural habitats of two species that we’re quite familiar with on Anole Annals – the Brown Anole (Anolis sagrei) and the Puerto Rican Crested Anole (Anolis cristatellus). Thawley found that A. sagrei prefers warmer temperatures than A. cristatellus, but that urban anoles do not differ in thermal preference than natural anoles for either species. Alternatively, urban male A. cristatellus and both sexes of urban A. sagrei were larger than their natural counterparts. As for parasites, A. sagrei had a higher parasite prevalence than A. cristatellus, but urban anoles did not differ from natural anoles in either species in parasite prevalence. However, for the A. sagrei that were parasitized, urban A. sagrei had higher parasite loads than natural A. sagrei.

These findings show that urbanization can influence anole morphology and parasite ecology. Thawley has just begun this work, and I look forward to seeing his future research on anole adaptation to urban environments!

SICB 2017: A Field Based Approach to Study Behavioral Flexibility

storks-poster-sicb-2017

Levi Storks explains his project in New Orleans.

Most animal learning studies have been conducted in the lab with the assumption that those findings are representative of behavior in the field. However, assessing behavior in the field increases ecological relevance. In addition, birds and mammals have received much of the attention in cognitive studies. Yet we on Anole Annals know that these lizards can be quite clever.

Levi Storks, a Ph.D. student in Manuel Leal’s lab at Mizzou, set out to address these issues by designing a method for testing behavioral flexibility in brown anoles (Anolis sagrei). Wild lizards in the Bahamas were allowed to feed unrestricted on a maggot placed in the middle of a testing apparatus in order to acclimate lizards to the structure. Storks then used a clear plastic tube to block the direct route to food, requiring lizards to move to either end to gain access. Lizards that successfully completed this task were then tested to see if they could associate unique patterns on the ends of the tube with single openings.

Storks found that a subset of lizards could successfully complete the first detour task, and lizards made fewer errors over the course of solving the detour task. These findings suggest brown anoles can learn and exhibit behavioral flexibility. Stay tuned for more of Levi’s work as he’ll be applying these methods to assess differences in behavioral flexibility between populations that vary in ecology!   

 

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