The Day’s Edge team combined with lizard behavior guru Manuel Leal–what could be better? Turns out that anoles have amazing navigation abilities, able to make incredible journeys over vast distances. Check it out, in either English (above) en español (below).
I remember the first knight anole (Anolis equestris) I ever caught. Details about how I caught it are gone, but I certainly remember the resulting bloody thumb. I was impressed and intrigued by the force and stamina of its bite – I needed to study this critter (fig. 1). Motivated by the recent publication of a short paper on knight anole diets, below, I break down a few years of research into the trophic ecology of the knight anole into a brief recount of what my collaborators and I have found.
Preliminary observations on knight anole trophic ecology
Following that first encounter I conducted a simple study of anole diet and habitat use around the Florida International University (FIU) campus in North Miami. In general, the findings showed some sensible results: Cuban brown anoles (A. sagrei; trunk-ground) perched low and ate a wide variety of terrestrial insects, Hispaniolan bark anoles (A. distichus; trunk) skittered up and down the trunk and ate – almost exclusively – ants, and Cuban knight anoles (A. equestris; crown-giant) ate larger food items than the other two species and tended to stay in the canopy (Giery et al. 2013). Again, this pattern of diet and habitat use was expected except for one thing – the composition of knight anole diet. Prior to embarking on the study, I had expected, based on their large size, strong bite force, the abundance of smaller anoles, and a few anecdotal accounts, that these powerful lizards would be eating lots of anoles. Surely these were the T-Rex of the trees and their direct interaction with other anoles was a predatory one. Yet in all the knight anoles that I dissected in this first study (n =21), not a single one contained vertebrate remains. Instead, nearly half of the diet (by volume) was fruit, specifically strangler figs (Ficus aurea; look to Supplemental table 1 for summary diet data). Our stable isotope data corroborate these observations – rather than the enriched 15N signature we‘d expect from an anole predator, the isotope data suggested similar trophic levels for brown, bark, and knight anoles. So what gives? Where was the evidence for a swaggering, arboreal meat-a-saurus?
Years later, James Stroud and I assessed the stomach contents of more knight anoles (n = 10) from a different site in Miami (Fairchild Tropical Botanic Gardens. James had directly observed knight anoles eating three different species of anoles there (1,2,3,4) and so we thought another look at their diet would be interesting. Once again, the majority of gut contents consisted of fruit, this time from royal palm trees (Roystonea regia). In fact the only evidence for vertebrate prey in this population was a 1 cm section of green anole tail. These data supported earlier observations (Brach 1976; Dalrymple 1980, Giery et al. 2013) demonstrating that fruit is a major component of knight anole diet, and vertebrates aren’t. It seemed that the canopy superpredator role I’d imagined for knight anoles was increasingly less likely. In fact, in all three previous examinations of knight anole diet, few instances of vertebrate predation by knight anoles are observed (table 1). The evidence spoke, knight anoles were sharp-toothed, veggie-sauruses with a deliberate, powerful bite.
An opportunity presents itself
Understanding the trophic ecology of anoles has been an ongoing project of mine for some time, the paper that we’ve just published in Food Webs (Giery et al. 2017) would not have come without the serendipitous post-capture … deposition … of a few seeds. An adult male passed two royal palm seeds which were planted post-haste in the greenhouse at FIU. It took a few months but the seeds eventually geminated, demonstrating that seeds consumed by knight anoles are viable and suggesting a role as seed dispersers (fig 2).
We felt that these data filled an important gap in our understanding of how anoles interact with other species. Certainly, the literature (e.g., Herrel et al. 2004; Losos 2009) and our data from Florida (Giery et al. 2013, 2017), Bermuda (Stroud, unpublished), and The Bahamas (Giery, unpublished) show that frugivory is widespread and sometimes quite common in anoles. Yet, the fact that seeds remain viable after passing through the guts of anoles presents a new facet to their interactions with plants. For more about what we know about lizard-plant interactions go ahead and check out the references in our paper (there’s good stuff from Europe, and recently, the Galapagos).
Whether the interaction we illustrate in our paper is ecologically important (i.e., increasing germination rates via ingestion and/or dispersal) requires substantially more study. Yet, the relationship between knight anoles and royal palms has been noted for nearly a century in Cuba suggesting their interaction is more widespread than just Florida. For example, Barbour and Ramsden (1919) remarked on the frequent coexistence of royal palm and knight anoles in Cuba. Interestingly, these early works often focused on the potential consumption of vertebrate prey, despite reports from Cubans that knight anoles often ate fruit – a bias matching my own preconceptions about the nature of this great anole:
“As to the food of the great Anolis [equestris] we know but little; it is surely insectivorous and Gündlach records that he once heard the shrill scream of a tree frog Hyla and found that it had been caught by one of these lizards. The country people all declare that they feed largely upon fruit, especially the mango; it is not improbable that this idea arises from the fact that they are frequently found in mango trees. We have always imagined that this circumstance was due in part at least to the excellent cover offered by the splendid growth of rich green foliage of the Cuban mango trees; it, however, has been seen eating berries (Ramsden). With good luck one may occasionally see two males of this fine species chasing one another about, making short rushes and charges at each other, accompanied by much tossing of heads and display of brilliant dewlaps When this mimic battle takes place about the smooth green top of the trunk of a stately Royal Palm, it is a sight not easily forgotten.” from Barbour and Ramsden 1919.
Anyways, we hope our short paper does two things. First, we hope that our summary of knight anole diet in Florida accurately illustrates their trophic ecology. Second, seed dispersal of native trees (royal palm and strangler fig) by an introduced vertebrate represents an interesting contrast to the negative effects usually attributed to introduced species (e.g., brown anole). We hope our observations highlight the diverse relationships between anoles and plants in the Caribbean region. Finally, we realize that our data are merely suggestive and effective seed dispersal by anoles has yet to be demonstrated. Nevertheless, we’re excited by the potential for new research directions stimulated by our observations.
Giery, S.T., Vezzani, E., Zona, S., Stroud, J.T. 2017. Frugivory and seed dispersal by the invasive knight anole (Anolis equestris) in Florida, USA. Food Webs 11: 13-16.
As you have heard before on Anole Annals, the Lizards On The Loose project involves middle school students conducting anole surveys in their back yards, school grounds, and local parks throughout South Florida. You can read more about the background and early results of this project in an earlier AA post which summarizes my talk at the Ecological Society of America’s (ESA) 2016 annual meeting.
Well, now we have updated results! Chris Thawley, a postdoc in Jason Kolbe’s lab and new member of the Lizards On The Loose team, has produced this video which explains what we have learned from the new data collected by students during their 2016-17 surveys. One species that we are particularly interested in is the Puerto Rican crested anole (Anolis cristatellus), whose distribution in Miami has been closely monitored since their introduction in the 1970s (see Kolbe et al. 2016 for a review of this species’ range dynamics in Miami). To our amazement, middle school students identified populations of crested anoles that were brand new to us! Watch below for more information:
By Andres Marmol and Ignacio Moore
A new study by Diego R. Quirola and collaborators about the enigmatic Ecuadorian proboscis anole has been published a few weeks back. In this study, the authors report new ontogenic and social behaviour data regarding males of this amazing lizard and its most noticeable character: the proboscis. But before going into the data, lets draw a short background.
Of all the Ecuadorian reptiles, Anolis proboscis is arguably the most remarkable. Originally described by Peters and Orcés in 1956, this elusive species was not seen for almost 50 years and was believed to be extinct, until 2005 when a group of ornithologists spotted and photographed a male (see Almendáriz and Vogt, 2007; see this previous post for a discussion of this history). Since then, a number of researchers have been interested in this lizard. However, a major question remained unclear regarding the species’ most notable character: how do males use the fleshy rostral appendage in social interactions?
Ernest E. Williams (1979) gave the first reliable hypothesis around this question in his taxonomic analysis of the proboscis anoles (of which there are two additional species; see more details in Williams, 1979). Based on collected male specimens, he proposed that the proboscis was the result of sexual selection. Two main questions required an answer to support William’s hypothesis: (1) do females also have the proboscis (Females were unknown at that time)?; and (2) how is the proboscis used by these lizards (No data on the natural history of the species had been described particularly regarding social interactions).
The first part of the riddle was solved in 2010 when the females were discovered confirming that the proboscis was only observed in males (see Yánez-Muñoz et al., 2010 for a proper description). Documenting the behaviour of the species in nature, however, was a greater challenge —as anyone that has attempt to study animal behavior knows— due to both the cryptic coloration of the species and its elusive nature. Two more years went by before the first insights about the natural history of the species were known — Losos et al. (2012) described the habitat use, diet, and activity patterns, whereas Poe et al. (2012) reported anecdotal observations of intra- and intersexual social behavior of the species and some uses of the proboscis. Despite these advances, more detailed observations of the species’ social behavior were needed. And more importantly, the use of the proboscis remained undescribed.
This point is where the new publication becomes relevant. By using a semi-natural environment where males and females were placed, the authors were able to record social interactions for the first time in this species. In particular, the study describes the agonistic behaviour between males, including the displays and the proboscis function during the encounter. The study provides a complete description of the courtship and mating behavior, reporting for the first time a female display during male-female interactions. As a bonus, the research reports the ontogeny of the rostral appendage.
Among the highlights of the paper include the description of four different displays that the males appear to use. Most interesting is the behaviour termed “proboscis flourishing”: a display composed of stereotyped lateral movements of the head that appear to be a way to present the rostral appendage to the female counterpart. The authors discuss the possibility that females can be assessing males by using this display as it was only observed during male-female encounters and before chasing—another new report of the reproductive behaviour of the species—occur (Video 1, Supplementary material).
In the last ten years, knowledge about this enigmatic anole has increased substantially thanks to the contribution of studies like Quirola et al. In particular, is clear that the rostral appendage has no direct use in physical combat. However, there is still a long way to go before we understand why and how this exaggerated trait evolved. Other variables regarding proboscis morphology, such as size or straightness, could be possible characters that may be honest indicators of quality and/or may confer an advantage against other males during agonistic behaviors. One thing is sure: we have only scratched the surface of the mystery of the evolution of the proboscis and this fascinating lizard.
ALMENDÁRIZ, A. C. & VOGT, C. 2007. Anolis proboscis (SAURIA: POLYCHROTIDAE), UNA LAGARTIJA RARA PERO NO EXTINTA. Politécnica, 27, 157-9.
LOSOS, J. B., WOOLLEY, M. L., MAHLER, D. L., TORRES-CARVAJAL, O., CRANDELL, K. E., SCHAAD, E. W., NARVÁEZ, A. E., AYALA-VARELA, F. & HERREL, A. 2012. Notes on the Natural History of the Little-Known Ecuadorian Horned Anole, Anolis proboscis. Breviora, 1-17.
POE, S., AYALA, F., LATELLA, I. M., KENNEDY, T. L., CHRISTENSEN, J. A., GRAY, L. N., BLEA, N. J., ARMIJO, B. M. & SCHAAD, E. W. 2012. Morphology, Phylogeny, and Behavior of Anolis proboscis. Breviora, 1-11.
WILLIAMS, E. E. 1979. South American Anoles: The Species Groups. 2. The Proboscis Anoles (Anolis laevis Group). Breviora, 449, 1-19.
YÁNEZ-MUÑOZ, M., URGILÉS, M. A., ALTAMIRANO, M. B. & CÁCERES, S. S. R. 2010. Redrescripción de Anolis proboscis: Peters & Orcés (Reptilia: Polychrotidae), con el descubrimiento de las hembras de la especiey comentarios sobre su distribución y taxonomía. Avances en Ciencias e Ingeniería, 2, 1-14.
The latest work on genetic differentiation and species status within the Anolis distichus group has just been published by MacGuigan, Geneva and Glor in Ecology and Evolution. In line with previous work from the Glor lab, the study finds evidence for seven distinct evolutionary lineages worthy of recognition as species, and further finds that variation in dewlap color in some cases does not correlate with geographic isolation. Finally, geographic isolation seems to play a key role in genetic divergence.
Here’s the abstract, followed by a few comments:
Delimiting young species is one of the great challenges of systematic biology, particularly when the species in question exhibit little morphological divergence. Anolis distichus, a trunk anole with more than a dozen subspecies that are defined primarily by dewlap color, may actually represent several independent evolutionary lineages. To test this, we utilized amplified fragment length polymorphisms (AFLP) genome scans and genetic clustering analyses in conjunction with a coalescent-based species delimitation method. We examined a geographically widespread set of samples and two heavily sampled hybrid zones. We find that genetic divergence is associated with a major biogeographic barrier, the Hispaniolan paleo-island boundary, but not with dewlap color. Additionally, we find support for hypotheses regarding colonization of two Hispaniolan satellite islands and the Bahamas from mainland Hispaniola. Our results show that A. distichus is composed of seven distinct evolutionary lineages still experiencing a limited degree of gene flow. We suggest that A. distichus merits taxonomic revision, but that dewlap color cannot be relied upon as the primary diagnostic character.
The authors suggest that there are at least seven species within the distichus complex, but they suggest that it is premature to recognize them officially at this time. Nonetheless, Poe et al. in their recent Systematic Biology paper (hey! who’s going to write a post on this one?) recognize at least some of these taxa as distinct species.
Finally, I do have one tiny bone to pick. The authors state:
“Together these results suggest that dewlap color is not by itself a reliable diagnostic trait in the A. distichus complex, and perhaps in anoles more broadly.”
I take umbrage with the final statement, “and perhaps in anoles more broadly.” The distichus complex has always been recognized as the major exception to the idea that dewlap color variation relates to reproductive isolation. Consequently, demonstrating what has been suggested—with some evidence—for 40 years doesn’t necessarily argue against the role of the dewlap in reproductive isolation more generally. Now, you may quibble with the data underlying this general proposition, and it certainly is worthy of further study, but the results of this study confirm what was already recognized as an exception to this general rule..
With summer just around the corner (any day now, Boston!) that can only mean one thing – the annual ASN/SSE/SSB sponsored Evolution meeting is almost here! This year the anole community is attending in full force with 2 posters, 11 regular talks, and 2 symposium talks.
We regularly cover this meeting here at Anole Annals, and once again we are asking for YOU to help us out. If you will be attending Evolution and are interested in writing a short blog post about one or more of the talks or posters, send me an email (firstname.lastname@example.org) or comment below. I will give you all the information you need to get started and a little help on how to write a blog post for us if you haven’t done so before. We always appreciate the extra help and fresh perspectives.
For those of you not attending the meeting (or maybe still debating attending), here’s the current list of anole talks in the schedule. Are you particularly excited about a talk at Evolution this year? Did we miss a talk that should be on our list? Let us know in the comments!
|Are we wrong about territoriality in Anolis lizards?||A. Kamath|
|Evolutionary analysis of viral strains infecting a single anole species||S. Prado-Irwin|
|Deeply conserved genetic constraints influence adaptive radiation of Anolis lizards||J. McGlothlin|
|Macroevolution of the dewlap and diversification of Anolis lizards||T. Ingram|
|Using sexually antagonistic skewers to explore the genetic architecture of sexual dimorphism in Anolis lizards||R. Cox|
|Evaluating the evidence for protein coding convergence in phenotypically convergent anoles||R. Corbett-Detig|
|Variation in dominance traits and body condition in urban Anolis cristatellus||D. Briggs|
|Population trascriptomic analysis of ecologically differentiated, partially reproductively isolated Anolis lizards||A. Geneva|
|Natural selection in behavior? A field experiment with Anolis lizards from the Caribbean||O. Lapiedra|
|Temporal variation of anthropogenic perch use by populations of forest and urban lizards||K. Aviles-Rodriguez|
|The influence of relatedness and size on spatial structure in an urban population of Anolis carolinensis lizards||W. Weber|
|Urban adaptation in Lizards: Connecting phenotypic shifts with performance and survival||K. Winchell|
|Character displacement in evolutionary-novel Anolis lizards||J. Stroud|
|Does competition between the Dominican native Anolis oculatus and the invasive Anolis cristatellus drive changes in ecological, agonistic and reproductive traits?||C. Dufour|
|Population genomics of Anolis carolinensis transposable elements: insertion polymorphisms are abundant but rarely approach fixation||R. Ruggiero|
The following is taken from the Society for the Study of Amphibian and Reptile’s website:
Catalogue of American Amphibians and Reptiles
The Catalogue consists of accounts of taxa prepared by specialists, including synonymy, description, diagnosis, phylogenetic relationships, published descriptions, illustrations, distribution map, and comprehensive list of literature for each taxon. Over 900 accounts have been published since the initiation of the series in 1963. The series covers amphibians and reptiles of the entire Western Hemisphere. Previously, accounts were published as loose-leaf separates; beginning in 2013 accounts are published as on-line PDFs. All accounts are open access and are available for free download at the University of Texas Library Repository.
Just this week, one of the latest catalogue entries is for the little known Anolis ruibali of Cuba, written by Robert Powell, Javier Torres, and Nils Navarro Pacheco.
Poor Anolis, snack box of the jungle. Seems that just about anything will eat an anole. So, it’s not surprise to learn that the teid lizard Kentropyx calcarata joins the lizard of anole consumers. So report Franzini et al. in a recent report in Herpetology Notes. Anolis fuscoauratus was the unfortunate victim, the crime discovered by examination of stomach contents.
Consider two lizard species that differ in limb length, with one species having relatively longer legs than others. During development, how does this difference arise? Do the limbs start at the same length when they first appear in the embryo, but grow at a greater rate in the longer-legged species? Or is the initial limb bud longer in the embryo of the longer-legged species, and then the rate of growth the same in the two species, preserving the initial difference?
Thom Sanger’s elegant work showed that the latter answer is correct for Anolis: the limb buds of long-legged species start out longer and then grow in parallel with those of shorter-legged species.
But does this finding also hold when comparing across a broader range of lizards? Robin Andrews and Sable Skewes decided to find out, comparing embryos of a chameleon, two geckos, and the brown anole.
The answer: the same pattern as within anoles! And it applies to tail length (but not head length) as well as limbs.
hardinherpetologica: Interesting observation while walking through the woods. Found this #BoxTurtle eating a dead #GreenAnole. I’m assuming it was a scavenged find but the entire body was gone by the time I came upon the scene. #Neature
Has anyone else observed box turtles (or any other chelonian [I guess now testudine?]) interacting with anoles?
Thanks to the work of Roger Thorpe and colleagues, Lesser Antillean anoles are renowned as an example of adaptive geographic variation. On many islands in the Lesser Antilles, populations in wet areas, where vegetation is lush, are green in color, whereas those in more xeric areas tend to be a drab gray, often with markings on their back. This pattern is repeated on many different islands, the convergent geographic variation thus making a strong case for the adaptive basis of anole coloration.
In a new paper in PLoS One, Thorpe takes this work a step further, asking whether we can use the parallel patterns seen across Lesser Antillean islands to predict the coloration of an anole species on another island. The focal species is Anolis bonairensis, which occupies the extraordinarily dry island of Bonaire (see our previous posts on this species).
The prediction: A. bonairensis should be grayer and drabber than populations of anoles that occur at the driest sites on Lesser Antillean answers.
The answer: yes! Just as predicted, Anolis bonairensis is one drab lizard. Score one for evolutionary predictability!
Anolis bonairensis is represented by the red circles. The x-axis goes from aridity on the left to the most mesic on the right. As you can see, A. bonairensis‘s color and patterning is well-predicted by variation in other species.
Anolis biporcatus is, if I’m not mistaken, the largest mainland beta/Norops anoles, attaining a length of ca. 100 mm snout-vent. In addition, it has an enormous geographic distribution, ranging from southern Mexico to Ecuador. In a new paper in Salamandra, a team of New Mexican and Ecuadorian biologists headed by Janet Armstead have sliced off part of the species, raising the Ecuadorian/Colombian A. biporcatus parvauritus to species status. They make this decision based on a detailed analysis of morphology and molecular data. Their data also find deep genetic subdivisions within A. biporcatus in Costa Rica, suggesting that there may be more cryptic species awaiting recognition.
A key difference between the species is the color of the distal scales on the dewlap of males, white in biporcatus, black in parvauritus.
Note, too, that like many mainland anoles, the males and females have very different dewlaps.
Here’s the distribution of the two species:
We would like to introduce our recent paper on the invasive green anole (Suzuki-Ohno et al. 2017). In Japan, the green anole Anolis carolinensis invaded the Ogasawara Islands in 1960’s and Okinawa Island in 1980’s. In Ogasawara Islands, A. carolinensis expanded its range and had a significant negative impact on native species and the ecosystem. This becomes a big problem since Ogasawara Islands are designated as a natural heritage.
On Okinawa Island, A. carolinensis was first captured in 1989 and it did not expand its distribution until more than 25 years later, although its density is extremely high in the southern region. In the northern region of Okinawa Island, Yambaru area, native forests are preserved so that it is important to avoid the invasive effects of A. carolinensis. Thus, It is important to determine whether A. carolinensis has the potential to expand its distribution on Okinawa Island.
Phylogenetic analysis shows that the invader A. carolinensis originated in the western part of the Gulf Coast and inland areas of the United States. Interestingly, all of the invaded A. carolinensis in Ogasawara, Okinawa and Hawaii originated from the Gulf Coast and inland areas of the United States.
We used a species distribution model (MaxEnt) based on the distribution of native populations in North America to identify ecologically suitable areas on Okinawa Island. The MaxEnt predictions indicate that most areas in Okinawa Island are suitable for A. carolinensis. Therefore, A. carolinensis may have the potential to expand its distribution in Okinawa Island.
The predictions indicate that habitat suitability is high in areas of high annual mean temperature and urbanized areas. The values of precipitation in summer in the northern region of Okinawa Island were higher compared with those of North America, which reduced the habitat suitability in Okinawa Island. Adaptation to low temperatures, an increase in the mean temperature through global warming, and an increase in open environments through land development will likely expand the distribution of A. carolinensis in Okinawa Island. We think that invasive anoles (A. calrolinensis and A. sageri) prefer open habitats.
Therefore, we suggest that A. carolinensis should be removed by using traps and/or chemicals. In addition, we must continue to be alert to the possibility that city planning that increases open environments may cause their range to expand.
I’ve been looking through a lot of anole museum specimens lately, and I’ve noticed that many of them have pretty pronounced endolymphatic glands, which made me curious about their prevalence and function in anoles generally.
Endolymphatic glands serve as calcium reserves, and are present in many animals, including a number of reptile and amphibian clades. According to Etheridge (1959), these glands are present in anoles and a few of their close relatives (e.g. Polychrus), but not in any other Iguanians. But it looks like most of the research on their function (in reptiles) has focused on geckos. In geckos, the size of the glands has been shown to fluctuate in response to both stress and reproductive activity, supporting the idea that the stored calcium is used in egg production, both for the yolk and the shell (Brown et al. 1996, Lamb et al. 2017). However, in anoles and geckos, these glands are present in both males and females, so their function isn’t limited to providing calcium for eggs (Etheridge 1959, Bauer 1989, Lamb et al. 2017).
But I haven’t found much information on these glands in anoles. I personally haven’t noticed them in the wild, but so far I’ve found very pronounced glands in 13/66 museum specimens, and some of them are really striking (see photos)! So I’m curious to hear, how often do you other anole-ologists see these enlarged glands? Is there any other literature about their prevalence, seasonality, or function in anoles that I’ve overlooked? Seems like we might be lagging behind the gecko crowd on this topic!
Bauer A (1989) Extracranial Endolymphatic Sacs in Eurydactylodes ( Reptilia : Gekkonidae), with Comments on Endolymphatic Function in Lizards. J Herpetol 23:172–175.
Brown SG, Jensen K, DeVerse HA (1996) The Relationship Between Calcium Gland Size, Fecunduty and Social Behavior in the Unisexual Gecks Lepidactyluse Lugubris and Hemidactylus Garnotii. Int J Comp Psychol. doi: 10.5811/westjem.2011.5.6700
Etheridge R (1959) The relationships of the anoles (Reptilia: Sauria: Iguanidae) an interpretation based on skeletal morphology.
Lamb AD, Watkins-colwell GJ, Moore JA, et al (2017) Endolymphatic Sac Use and Reproductive Activity in the Lesser Antilles Endemic Gecko Gonatodes antillensis (Gekkota: Sphaerodactylidae). Bull Peabody Museum Nat Hist 58:17–29.
Liam Revell has developed a method, which he explains in Phytools.
A rose by any other name would still smell as sweet. But what if there’s an anole sleeping inside of it?
Michele Johnson (top) and Manuel Leal (bottom). For more on the Leal lab’s march-related activities, check out the post on Chipojolab.