Year: 2014 Page 23 of 31

A common concept in ecology is that predators have a strong influence on the behaviour of prey species. Anolis lizards have been used as a classic model system to investigate the effect of predator presence on the behavioural response of prey species. On small experimental islands in the Bahamas the manipulated introduction of curly-tailed lizards (Leiocephalus carinatus), a large terrestrial anole-predator, has resulted in brown anoles (Anolis sagrei) shifting higher up in the vegetation, presumably in an understandable effort to avoid being eaten (1, 2, 3). However, predator-prey interactions such as these which may shape community structure are often difficult to observe.

Here in Miami FL we have a rich and diverse, although largely non-native, lizard community. There are two species of “crown-giant” anoles, the Cuban knight anole (A. equestris) and the Jamaican giant anole (A. garmani), that could be potential predators of smaller anoles in the canopy of trees and upper half of tree trunks (although see Giery et al. 2013 for an empirical analysis that suggests this may not be the case). Additionally, there are several large, terrestrial lizards present which may be filling a similar role to curly-tails in the Bahamas.

Potential lizard predators in south Florida:

– *Red-headed agama (Agama agama)
– *Cuban knight anole (Anolis equestris)
– Jamaican giant anole (Anolis garmani)
– *Brown basilisk (Basiliscus vittatus)
– Spiny tailed iguana (Ctenosaura similis)
– Curly-tail lizard (Leiocephalus carinatus)
– Giant day gecko (Phelsuma grandis)
– Black and white tegu (Tupinambis merianae)

*Present at Fairchild Tropical Botanical Gardens

Earlier this afternoon, while taking a break from my office at Fairchild Tropical Botanical Gardens (a hot spot for any anologist visiting Miami; 1, 2, 3, 4) in a typical graduate student effort to put off work that I should be doing instead, fellow lab member Evan Rehm and I noticed some scuffling in a nearby bush. At around 2.5m, and admittedly on relatively precarious branches by this stage, sat an adult female African red-headed agama (A. agama) around 30cm from an adamantly motionless adult male Cuban brown anole (A. sagrei)! As we moved towards the bush the agama was quick to ungraciously thump itself to the floor, while the brown anole remained still. On closer inspection, it soon became apparent why both lizards were so high.

Adult male Cuban brown anole (A. sagrei) found ~2.5m high in Miami FL, supposedly following a predation attempt from an African red-headed agama (A. agama) – JStroud

The significance of tail loss/damage in a population is still debated. The classical view argues that high proportions of tail damage indicates high predation pressure, therefore prey populations are under high predation stress (1). Alternatively, high proportions of tail damage could indicate low predator efficiency, which would suggest prey populations are experiencing low predation stress (1, 2). But the debate doesn’t stop there! Having already lost a tail, a lizard may experience either a resulting increase or decrease in predation depending on the predator species and its associated foraging tactic (1).

The extent of tail damage is clearer in this photo. The lizard had autotomised the lower half of it’s tail however a secondary half-completed break is also evident – JStroud

African red-headed agamas (A. agama) are similar morphologically to curly-tailed lizards (L. carinatus), although are taxonomically distinct (Agamidae and Leiocephalidae, respectively). Predation of anoles by agamas in Miami has not previously been officially recorded, and the impact of these large predators remains unclear. Unlike in the Bahamas, there are multiple predators in the same geographic vicinity that anoles need to be aware of. For example, at Fairchild, brown anoles (A. sagrei) could be eaten from below by agamas, eaten at intermediate levels by basilisks and eaten from above by knight anoles!

South Florida is a tough place to be an anole!

Adult male African red-headed agama (A. agama) at Fairchild Tropical Botanical Gardens, Miami FL. The population of agamas is localised to the botanical gardens; the source remains unclear but is likely an introduction from the pet trade – JStroud

Spotlight on Cuban Anoles, Part I: Anolis bartschi

By Shea Lambert

On March 29, 2014

In All Posts

A juvenile Anolis bartschi scampers up a limestone boulder.

Recently, frequent Anole Annals contributor Martha Muñoz and I had the opportunity to visit Cuba as part of a licensed trip through the Harvard Museum of Natural History. During our two weeks on the island, we visited many localities and had the opportunity to photograph and observe some of Cuba’s most beautiful anoles. In the coming weeks, I’ll be spotlighting some of our favorites. All images presented are © Shea Lambert 2014.

First up: Cuba’s Western cliff anole, Anolis bartschi.

Knight Anole Eating Brown Anole

By Jonathan Losos

On March 28, 2014

In All Posts

Photo courtesy Marissa Pierce

Decoupled Muscle Activity and Kinematics in Green Anoles (Anolis carolinensis): New Research by Kathleen Foster and Tim Higham

By Kathleen Foster

On March 26, 2014

In New Research

Anolis carolinensis. Photo taken by Kathleen Foster.

Anoles are the indisputable poster children of ecomorphology. Morphological, behavioral, and performance data support classification of Anolis species into discrete ecomorphs on the Greater Antilles islands. In a large part, the basis of this classification is due to variables (e.g. limb length) that relate to differing locomotor abilities (i.e. speed and/or stability) on the various substrates that comprise the different areas of the arboreal habitat. However, until recently, we knew nothing about how the muscles that power locomotion in these species relate to their ability to cope with the challenges of moving in these different microhabitats.

In a recent paper in Proceedings of the Royal Society B, we used a combination of electromyography and 3D high-speed video to examine the impact of perch diameter and incline on limb kinematics and muscle activity in Anolis carolinensis. Our previous study in the Journal of Experimental Biology found a number of kinematic changes (e.g. increased limb flexion and depression) associated with increased stability on narrow surfaces, and we hypothesized increased recruitment in the muscles associated with those movements. Interestingly, this was not the case. Despite considerable kinematic modulation with change in perch diameter (63% of the 32 kinematic variables were significantly affected by perch diameter), there was very little change in muscle activity (2% of the 100 muscle activity variables). This decoupling of kinematics and muscle function raises a number of very interesting questions relating to the sensitivity of these muscles to changes in operating length and the degree to which this species is specialized for a particular microhabitat. It also highlights the complexity of the physiological basis of animal locomotion and emphasizes the need for caution when attempting to infer motor control from kinematics and vice versa.

An additional result that may significantly impact identification of habitat preference in Anolis lizards relates to the importance of variability, as opposed to magnitude, of muscle activity in describing the differences in how this species handled the different substrate conditions. Specifically, the muscles examined were less variable on the broad perch compared to the narrow perch and on the vertically, as opposed to horizontally, inclined perch. Locomotor stereotypy is generally believed to reflect locomotor specialization, although reduced variation of in muscle activity may also be achieved as a byproduct of near-maximal muscle recruitment. However, we have little support for this second option, as the muscles were neither approaching maximal stimulation nor vastly different in overall magnitude or recruitment. Therefore the greater stereotypy of muscle activity seen in the green anole as it moved on the broad, vertical condition may reflect a physiological preference for tree trunks, rather than the narrower and shallower substrates that comprise (on average) the trunk-crown region to which it is traditionally assigned.

It is clear that there remains a wealth of knowledge waiting to be unearthed in the Anolis system and this paper barely scratches the surface. It emphasizes how little we understand about the complex nature of animal locomotion and the relationship between the muscles that power locomotion and the movements we observe in the field. And the possibility that variability of muscle activity might be a useful tool to identify functional preference for microhabitat is tantalizing and deserves further attention, especially if it can be applied usefully to mainland Anolis species. The remainder of my dissertation will focus on fleshing out these and other aspects of muscle function through the comparison of ecomorphs of the Greater Antilles.

Kathleen L. Foster & Timothy E. Higham. (2012). How forelimb and hindlimb function changes with incline and perch diameter in the green anole, Anolis carolinensis. Journal of Experimental Biology 215: 2288-2300. (DOI: 10.1242/jeb.069856)

Kathleen L. Foster & Timothy E. Higham. (2014). Context-dependent changes in motor control and kinematics during locomotion: modulation and decoupling. Proceedings of the Royal Society B 281: 20133331. (DOI: 10.1098/rspb.2013.3331)

Transgenerational Effects Of Nutrition Observed In Anolis sagrei

By Thomas Sanger

On March 25, 2014

In New Research

Mothers affect the quality of their offspring. As humans, this seems obvious. For example, expecting mothers often take prenatal vitamins, limit their consumption of certain foods, and avoid kitty litter knowing that these minor environmental factors can affect the normal development of the fetus. Related statements could be made for the relationship of a mother and child after birth. Understanding the precise effects that parents have on their offspring has been of great interest to biologists from many disciplines as they disentangle the genetic and environmental factors that underlie differential survival and reproduction for individuals within a population (fitness). Because Anolis lizards can be easily maintained in captivity and their eggs readily manipulated they provide a useful model for the examination of maternal effects. Warner and Lovern took advantage of these qualities and tested the role of maternal body condition on offspring quality in the brown anole, Anolis sagrei.

A. sagrei from Cayman Brac

Nutritional stress is a well-studied example of how maternal condition may affect juvenile quality; if the mother is malnourished the quality of her egg yolk may suffer, which, in turn, affects embryonic development. The authors tested this hypothesis in A. sagrei by manipulating the amount of food gravid females received, feeding approximately 168 crickets per lizard in a “high-prey” treatment versus 84 crickets in a “low-prey” treatment distributed over 11 weeks. During this time the authors carefully assessed the number and size (mass) of the eggs and, subsequently, the quality (mass-and-snout to vent length) of the hatchlings. Impressively, the authors didn’t stop there. They also experimentally manipulated the amount of nutrition in a subset of eggs by removing yolk with a syringe. Followed by a battery of statistical models, this study is quite a nice physiological analysis that has evolutionary implications.

When comparing the two diet regimes, Warner and Lovern found that body condition does affect the quality of offspring; females maintained on the “low-prey” diet produced eggs 6.6% smaller than females raised on the “high-prey” diet. In turn, smaller eggs also tended to hatch more quickly and smaller eggs produced smaller hatchlings, both probably due to the lower amount of available nutrition (paradoxically, neither incubation time or hatchling mass was directly correlated with maternal prey availability). Low prey availability also results in hatchlings with slower growth rates. The experimental reduction of egg yolk supports the results of the prey availability study: hatchlings from yolk-reduced females were 8% shorter and 23% lighter and grew more slowly than those hatched from unmanipulated eggs. It is clear from their results that nutrition has an effect on hatchling quality well into life, after the obvious maternal effects have passed. There are a number of other interesting correlations (and statistical caveats) described within the text that may also be of interest to some readers.

Figure 5 from Warner and Lovern 2014.

What is becoming clear from studies like these is that environmental stressors can have lasting effects on organismal development that transcend generational boundaries. Mechanistic studies, such as those on the American alligator, illustrate that these effects are mediated by heritable methylation patterns of key regulatory genes. The stressors do not need to be long lasting; physiological responses can result from acute events that occur within key developmental windows, often when a particular organ is maturing. While stressing the embryo too far results in abnormal embryonic development, more subtle effects may not arise until late in life or subsequent generations. Anoles, and A. sagrei in particular, may provide a number of opportunities for environmental health research in the future. Studies such as the one described above could be performed to more precisely dissect the organ-specific effects of maternal nutritional stress or whether the effects dissipate with age. Similar to the alligator studies, eggs laid in polluted soils may allow opportunities for developmental toxicology research. Growing genomic resources may allow for examination of genome-wide and gene-specific methylation patterns within and outside of polluted habitats. The possibilities are broad and the impact cannot be predicted at this time, but the potential is there for much more detailed mechanistic research on the relationship between developmental physiology and the environment.

New Guide on How to Preserve Material for Genetic Studies

By Jonathan Losos

On March 24, 2014

In All Posts

Blurb: “This guide will allow nearly everyone with an interest in amphibians and reptiles to collect and store samples for genetic analyses. It is written at a level appropriate for people with a basic background in biology, including professional scientists moving into a new project as well as wildlife managers, conservation biologists, ecologists, and others working on herpetological projects. The book should also be useful for advanced undergraduates and graduate students just starting their research careers.”

See more at the SSAR book website.

Price: $11

Call for Assistance: Anolis sagrei

By Graham Reynolds

On March 21, 2014

In All Posts

Hi Everyone, a quick post to see if anyone out there is interested in contributing to a large ongoing project on Anolis sagrei. We are sampling this species throughout the (mostly) native range, and currently have 77 sampling locations represented. However, we are wondering if anyone would be able to help us fill some remaining gaps.
We are interested in adding additional tissue samples from Central America and the Bahamas. Here is an approximate range map with some desired localities (in blue):

Any help is greatly appreciated. I realize that collecting tissues (not to mention all the paperwork) is not a trivial task, so if you are interested in contributing samples please get in touch with me. We will keep AA posted on this project!

Anolis ortonii Displaying

By Jon Suh

On March 20, 2014

In Anole Videos, Natural History Observations

I had the opportunity to study abroad in Ecuador last year, an amazing experience which culminated in a one-month stay in the rainforest at the Tiputini Biodiversity Station located in Yasuni Biosphere Reserve. The most common species of anole there was Anolis ortonii, if you knew where to look. Despite several written accounts of A. ortonii being found close to the ground, I observed them in high abundance about 150 feet in the air at the top of a ceiba tree made accessible by a canopy tower.

My experience with Anolis displays in the wild is next to nothing, but from what little I’ve seen, this swaying seemed unusual to me. Perhaps the more experienced anolologists here can comment on this. Regardless, enjoy the video of a lesser-known mainland anole!

Turks and Caicos Anole: Anolis scriptus

By Graham Reynolds

On March 19, 2014

In Notes from the Field

Much of my research has been conducted on the herpetofauna of the Turks and Caicos Islands (TCI). Known to a chunk of the lay public in North America as a sweet honeymoon spot, the Turks and Caicos boast a wonderful assemblage of terrestrial reptiles, like these IUCN critically endangered TCI iguanas (Cyclura carinata):

Of course, we on AA prefer the smaller saurians, so I will draw your attention to the TCI anole (A. scriptus scriptus), a member of the Southern Bahamas Anole complex (A. scriptus).

Anolis s. scriptus, Big Ambergris Cay, TCI

Also known as the Silver Cay Anole, A. scriptus can be found across the southern Bahamas banks, including the Inaguas, Samana, Plana Cays, Mayaguana, and the Turks and Caicos Islands. I have previously posted about this understudied species (1,2), but spent a good bit of time observing them on my last research trip. They occur throughout the TCI archipelago, from the dense tropical dry forest of North Caicos, to the pine savannas of Middle Caicos and xeric outposts like the Ambergris Cays. They can also be found on nearly every vegetated rock cay.

Male, Big Ambergris Cay

The males have an attractive yellow wash on the underside, with an orange-yellow dewlap that is really striking in the bright sun. The males display from elevated perches, but are wary when approached by nosy researchers.

The females are more cryptic, both in coloration and in behavior. They often have a light stripe down the back, or occasionally darker crossbars perpendicular to the light stripe.

On Big Ambergris Cay, on the southeastern edge of the Caicos Bank, the anoles especially favor an irrigated area near a decorative plant nursery. They are voracious, taking down large prey like this cicada (Ollanata caicosensis) on the right. Hopefully this voraciousness extends to interspecific interactions, as the “Festive” anole (A. sagrei) has now firmly invaded at least one island on the Caicos Bank (1; more on this in a future post).

Phylogenetically, Anolis scriptus is nested firmly within the radiation of Puerto Rican Anoles (most recently). Most closely related to a trunk-ground clade containing A. cristatellus, A. desechensis, and A. ernestwilliamsi, the TCI Anole exhibits a curious distribution, although they really do resemble A. cristatellus. Much of the terrestrial herpetofauna of the TCI is likely derived from Hispaniola (See TOC on this post), so what did A. scriptus do to get to the TCI? Our recent research on the A. cristatellus clade suggests that A. scriptus most likely dispersed from Puerto Rico around the start of the Pliocene. This could have been accomplished completely over-water, as currents and hurricanes push flotsam in a northwesterly direction from Puerto Rico. Alternatively, the species could have island-hopped on the formerly emergent Silver, Mouchoir, and Navidad banks, now a famous calving ground for the Humpback Whale.

Although I have not visited, the Crooked-Acklins Bank is a curious intersection of Bahamian and southern Bahamian herpetofauna, where the range of the southern A. scriptus (nearby Plana Cays) meets the range of the northern A. sagrei (Crooked Island). Furthermore, the bank is the northern limit of the Southern Bahamas Boa (Chilabothrus chrysogaster), which is replaced just a few kilometers northwest on the Great Bahama Bank by C. strigilatus. Finally, the handsome endemic A. brunneus (1,2,3) occurs there.

Aerial Behavior by Anolis pentaprion

By Jonathan Losos

On March 18, 2014

In All Posts

Anolis pentaprion taxiing down the runway on a canopy tower at the La Selva Biological Station in Costa Rica. Photo by Vinicio Paniagua.

Draco, the flying dragon, has borrowed an anole dewlap, so it’s only proper that anoles return the favor by developing gliding capabilities. It’s been long rumored that Anolis pentaprion, a twig anole from Central America, will launch itself off of perches in canopy and glide away, but now Steve Overbauer, Vinicio Paniagua, Craig Guyer and Mo Donnelly have documented just that in an interesting herpetological natural history note that appeared in the last issue of last year’s volume of Herp Review (Vol. 44, pp. 677-678). Here’s what they have to say:

“Lizards with gliding or directed aerial descent behaviors are well known from the Old World Tropics (e.g., Draco, Ptychozoon), and snakes and frogs exhibiting these behaviors are found both in the Old and New World Tropics (Dudley et al. 2007. Annu. Rev. Ecol. Evol. Syst. 38:179–201). However, lizards showing directed aerial descent have not been reported from the New World Tropics. Here we report on directed aerial descent capability and behavior in Norops pentaprion, a canopy lizard from eastern Costa Rica, southern Nicaragua, and western Panama (Köhler 2010. Zootaxa 2354:1–18).

The initial discovery of this behavior in N. pentaprion was serendipitous in July 2001 when an individual was captured on a walk-up meteorological tower at canopy level (~ 25 m) at La Selva Biological Station in the Atlantic lowlands of Costa Rica. After identification, the animal was returned to the original location on the tower, but upon release to a horizontal tower brace, it executed a controlled aerial descent to a tree in the distance below. Individuals of N. pentaprion have been occasionally observed on our meteorological towers subsequent to our first observation of directed aerial descent. The lizards are typically at canopy level but are sometimes found well above the canopy on the highest levels of the towers (up to 42 m). While the typical response of N. pentaprion to the presence of personnel on the tower is to race down the tower or hide on the opposite side of vertical supports, the animals will occasionally jump from the tower to escape when approached. Since 2001 we have observed directed aerial descent by N. pentaprion from canopy towers on several occasions. In at least two instances the lizard landed at lower levels on the tower, but in other occurrences they covered substantial distance to adjacent trees including aerial rotations of near 180º. During more than one observation, animals appeared to glide with near-horizontal trajectories towards termination of the descent. Similar to some snakes, frogs, lizards, and ants showing directed aerial descent, N. pentaprion does not have strongly specialized features associated with gliding behavior such as skin flaps, skin extensions, or webbed feet. Norops pentaprion has a relatively flattened head and wide body. During aerial descent this lizard proceeds headfirst, with limbs partially extended and the body strongly flattened, a position that may take advantage of regions of relatively loose skin along the sides of the body (Guyer and Donnelly 2005. Amphibians and Reptiles of La Selva, Costa Rica, and the Caribbean Slope, Univ. California Press, Berkeley, California. 299 pp.).

At La Selva Biological Station this species is uncommon in the understory and is usually found on trees limbs. Norops pentaprion is a member of a closely-related group of anoline lizards subjected to a recent analysis of morphology and morphometrics (Köhler, op. cit.); these related taxa share similar body size characteristics with N. pentaprion and are frequently arboreal. Future observations of some of these species may result in the discovery of similar directed-aerial descent behavior. Canopy pioneer Donald Perry reported lizards with a rose dewlap parachuting between trees in the canopy in Costa Rican forests (Perry 1986. Life Above the Jungle Floor, Simon and Schuster, Inc. New York, New York. 170 pp.), but the species was not identified. In their description of Norops pentaprion, Guyer and Donnelly (op. cit.) indicated that parachuting behavior likely occurs in this species on the basis of our initial observations and those of Perry. Our repeated observations verify directed aerial descent in this species and confirm that the lizard observed by Perry was N. pentaprion, the only lizard in the region with magenta dewlap coloration.”