In August, we published a paper in the Caribbean Journal of Science entitled, “Sleeping Behavior of the Secretive Puerto Rican Twig Anole, Anolis occultus.” Check out our new post on the Chipojo Lab blog about the paper!
Levi Storks, Manuel Leal. 2020. Sleeping Behavior of the Secretive Puerto Rican Twig Anole, Anolis occultus. Caribbean Journal of Science 50(1):178–87.
A Brown Anole (Anolis sagrei) attempts to make a meal of a large centipede.
Anoles eat a wide variety of food items present in their environments, including all sorts of arthropods, and, occasionally, smaller anoles! We might expect that anoles would choose safe, appropriately-sized prey that would reduce chances of injury and guarantee a meal. However, some anoles, including brown anoles (Anolis sagrei), have been seen taking on potential prey that are either quite large (enough that we might foresee trouble actually swallowing the prey item) or poisonous or venomous, such as caterpillars and centipedes.
Another attempt at subduing the centipede.
Margaret Griffis O’Brien, a contributor to iNaturalist, recently observed just such a showdown on the mean streets of Miami between a brown anole and a centipede nearly its own body size. The anole made repeated attempts to take down the centipede before it was scared away from its potential meal by an intervening automobile. The centipede was injured enough from the battle that it was unable to leave the road and later in the day was found flattened by the continued traffic. The centipede, either an eastern bark centipede or the invasive Rhysida longipes, was a member of the family Scolopendridae, a group of centipedes known to possess powerful and painful (to humans, at least!) venoms.
The anole’s predation attempt was characterized by a lot of waiting for opportune moments to attack followed by quick strikes at the centipede.
Given that large, venomous centipedes have been documented in the diet of A. sagrei previously, it would be interesting to know if anoles are able to consume centipedes without being envenomated, how susceptible they are to centipede venom, and whether consuming these large, potentially dangerous prey items is advantageous for these lizards.
All photos by Margaret Griffis O’Brien.
Interspecific Interactions Between Two Species of Invasive Lizards in an Urban Environment; Camila Rodriguez-Barbosa and Steve Johnson
An extensive body of work has addressed the eco-evolutionary impacts of the Northern Curly-tailed Lizard (Leiocephalus carinatus) on Brown Anoles (Anolis sagrei) (much of it receiving coverage right here, here, and here on Anole Annals!). These species co-occur not only on many Caribbean islands where much of this research has taken place, but also within the urban matrix of southern Florida, where both species are introduced.
Camila Rodriguez-Barbosa and Steve Johnson investigated the impacts of curlies on brown anoles in shopping centers in southern Florida where both species were plentiful. Camila first collected baseline data on anole and curly populations at eight sites before embarking on a quest to eliminate curlies from four of her sites. Over the next four months, she removed over 300 (!) curlies from these sites, many of which had brown anole remains in their stomachs.
She found that this removal had serious consequences for brown anoles. Compared to anoles from shopping centers where curlies were unchanged, A. sagrei at removal sites experienced higher survival and consequently greater abundances. These anoles also shifted to lower perches once curlies were removed, mirroring results from previous work which show that the introduction of curlies leads to brown anoles occupying higher perches to escape this dangerous predator. Camila’s work suggests that brown anole/curly-tailed lizard interactions may be similar even in very different habitats and provides a fascinating look at lizard life (and death) in the urban sprawl of southern Florida.
Figure 1. Knight anoles (Anolis equestris) are large, arboreal, and highly frugivorous lizards native to Cuba and introduced to Miami, Florida in the mid-20th century. This adult female was found perched on the trunk of a strangler fig (Ficus aurea) in Miami, Florida, a common sight in south Florida. Strong jaws and a large gape enable knight anoles to consume a range of large food items including snails, locusts, small vertebrates (occasionally), and some moderate-sized fruit. Photo by S. Giery.
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).
Figure 2. Adult knight anoles (Anolis equestris) often inhabit the crowns of royal palms (Roystonea regia) in Florida and Cuba. Note the numerous ripe fruits above this displaying male photographed at our study site in Coral Gables, Florida (A). Roystonea regia seedlings resulting from seeds passed naturally by a wild-caught A. equestris. Both seeds were planted at the same time, but germinated nearly 130 days apart (B). Adult royal palms can reach 30m high and are an ecologically and economically important plant throughout their range (C). Photos by J. Stroud (A & B) and S. Zona (C).
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.
In the most recent issue of Herp Review, Anole Annals stalwarts Kevin de Queiroz and Jonathan Losos documented their account of observing an adult female grass-bush anole (Anolis pulchellus) consume a dwarf gecko (Sphaerodactylus macrolepis) on Guana Island, British Virgin Islands. The authors share their detailed report below:
Many primarily insectivorous lizards will eat other vertebrates on occasion, a behavior that has been reported in many species of Anolis. One unifying generality is that such carnivory is size structured, with the predator usually being substantially larger than the prey (Gerber 1999. In Losos and Leal [eds.], Anolis Newsletter V, pp. 28–39. Washington University, Saint Louis, Missouri). Not surprisingly, reports of anole carnivory pertain primarily to middle-sized and larger anoles. Here we report carnivory by a small anole of the species A. pulchellus. To our knowledge, this is the first instance of carnivory reported for this species and one of few for any similar-sized anole (the record noted by Henderson and Powell 2009. Natural History of West Indian Reptiles and Amphibians. University Press of Florida, Gainesville, Florida. 495 pp. is based on the observations reported here).
Fig. 1. Female Anolis pulchellus in the process of ingesting a
Sphaerodactylus macrolepis.
We observed a female A. pulchellus (SVL ca. 38 mm) capture and consume a Sphaerodactylus macrolepis (SVL ca.18 mm) in the leaf litter at approximately 1430 h on 25 September 2006, on Guana Island, British Virgin Islands, near the head of the Liao Wei Ping Trail at roughly 18.47916°N, 64.57444°W (WGS 84). The anole jumped from a low perch (ca. 20 cm above the ground) to the ground and bit the gecko, which escaped and fled 15–20 cm to the opening of an ant nest. The anole attacked the gecko again, seized it in its mouth and carried it approximately 10 cm up a vine, a distance of 15–20 cm from the site of attack. Initially, the anole held the gecko upside down (i.e., dorsal surface facing down), biting it between the fore and hind limbs on the left side. Eventually the anole worked its grasp posterior to the base of the tail, still on the left side. At this point, parts of both the base of the tail and the left hind limb were in the anole’s mouth (Fig. 1). The anole then manipulated the gecko so that it was no longer upside down, but rotated about its long axis by roughly 90 degrees (the ventral surface of the gecko was then oriented forward relative to the anole) at which point it was biting the gecko at the base of the tail and possibly by the left hind limb; the anole eventually manipulated the gecko so that it held it tail-first in its mouth, dorsal side up, at which point the anole proceeded to ingest the gecko tail first (during this time, the tail itself broke off and was carried away by ants, which had been biting the gecko in several places since shortly after it was
captured by the anole). Total time from capture to complete ingestion was approximately five minutes.
Predation on Sphaerodactylus geckos has been reported in anoles of only a few species, none of which are as small as Anolis pulchellus (Henderson and Powell 2009. Natural History of West Indian Reptiles and Amphibians. University Press of Florida, Gainesville, Florida. 495 pp.). However, given the size discrepancy between the lizards in these two clades and their extensive coexistence across the Caribbean, we suspect that such interactions may occur with some frequency. Moreover, the high population densities of some Sphaerodactylus geckos (e.g., Rodda et al. 2001. J. Trop. Ecol. 17:331–338) and the diurnal activity of several species (Allen and Powell 2014. Herpetol. Conserv. Biol. 9:590–600) suggest that they may be important prey items for anoles.
References
– Allen, K.E. and Powell, R., 2014. Thermal biology and microhabitat use in Puerto Rican eyespot geckos (Sphaerodactylus macrolepis macrolepis). Herpetological Conservation and Biology, 9(3), pp.590-600.
– Gerber 1999. In Losos and Leal [eds.], Anolis Newsletter V, pp. 28–39. Washington University, Saint Louis, Missouri
– Henderson and Powell 2009. Natural History of West Indian Reptiles and Amphibians. University Press of Florida, Gainesville, Florida. 495 pp.
– Rodda, G.H., Perry, G.A.D., Rondeau, R.J. and Lazell, J., 2001. The densest terrestrial vertebrate. Journal of Tropical Ecology, 17(02), pp.331-338.
Lead author, Kirsten Tyler, reports on her recent Journal of Herpetology paper with K. Winchell and L. Revell:
Urbanization creates drastic changes to habitats leading to differences in microclimate, perch characteristics and distribution, and ecological communities (competitors, prey, and predators) when compared to natural (forest) habitats. Studies have found increased rates of mortality of many urban species due to generalist urban-tolerant predators such as raccoons, feral cats, and domestic animals (Ditchkoff 2006). Anolis lizards are able to voluntarily drop their tails (“autotomize”) when challenged by a predator, enabling their escape in many instances. The maimed lizards are able to regenerate their lost tails, though the replacement tail is a rod of cartilage and not the original bony vertebrae. The regenerated tail portions are often a different color and texture, and the lack of vertebrae / cartilage rod are clearly visible in X-rays.
We hypothesized that autotomy rates would be more similar between urban areas in different municipalities than to natural areas in the same municipality due to similar predator regimes in urban sites across the island. We compared the frequency and pattern (number of caudal vertebrae remaining) of caudal autotomy of A. cristatellus between urban and natural areas in Puerto Rico.
X-rays of our samples with an intact tail (A) and an autotomized tail (B).
We sampled A. cristatellus from paired natural and urban sites in four Puerto Rican municipalities: San Juan, Mayagüez, Ponce, and Arecibo. The natural sites were high quality natural forests and the urban sites were high-density residential areas. Urban sites were dominated by asphalt and other impervious surfaces, had sparse tree cover, and a large fraction of potential perches were manmade surfaces such as walls and fences. We scored 967 X-rays from these eight sites for caudal autotomy and counted the number of remaining tail vertebrae. We tested for an effect of urbanization on caudal autotomy by fitting a logistic regression model with municipality (San Juan, Mayagüez, Ponce, Arecibo) and site type (urban, natural), and their interactions, as model factors, and body size as a covariate.
Our data shows that lizards found in urban sites have a larger probability of having autotomized tails.
Interestingly, we found higher rates of autotomy in all urban populations compared to nearby natural areas. Differences in autotomy might be explained by differences in predator density and efficiency (Bateman 2011). For example, inefficient predators (those that more often than not fail to capture their prey) tend to leave behind more lizards with broken and regenerated tails (Schoener 1979). In addition, a greater abundance of predators could result in more predation attempts. Unfortunately, we did not collect data on predator abundances or community composition, so we cannot distinguish between these (non-mutually exclusive) explanations. Higher rates of autotomy in urban areas could thus reflect any of a variety of factors, including (but not restricted to) inefficient predators in urban areas, a shortage of refuges offering protection from predators, or an increase in predator density.
For lizards with autotomized tails, we found no significant difference in caudal vertebrae number between urban and natural sites.
Lastly, we did not find that lizards with autotomized tails in urban areas had lost more (or less) of their original tail to caudal autotomy. Since regenerated tails cannot be autotomized past the original break point (i.e. cartilage cannot autotomize), this suggests that lizards in urban areas are no more likely to be subject to multiple unsuccessful predation attempts (resulting in caudal autotomy) than lizards in natural forest. Future investigation quantifying predation attempts or predator community composition in urban and forest habitats could help us better understand the source of this intriguing pattern.
References:
BATEMAN, P. W., AND P. A. FLEMING. 2011. Frequency of tail loss reflects variation in predation levels, predator efficiency, and the behaviour of three populations of brown anoles. Biological Journal of the Linnean Society 103:648–656.
DITCHKOFF, S. T. 2006. Animal behavior in urban ecosystems: modifica- tions due to human-induced stress. Urban Ecosystems 9:5–12.
SCHOENER, T. W. 1979. Inferring the properties of predation and other injury-producing agents from injury frequencies. Ecology 60:1110–1115.
Curly tail with brown anole tail visible from its mouth
Kayaking to cays
I was recently in Abaco, Bahamas with Losos lab post-doc Oriol LaPiedra and Ph.D. candidate Darío Fernández-Bellon from University College Cork, Ireland, to carry out some behavioral studies of Anolis sagrei on the island and its surrounding small cays. We kayaked (a highly recommended transportation mean for its lesser-impact on the marine ecosystem, not having to rely on the tide schedule, while allowing you to see rays and sharks and sea turtles!) our way out to islands that are known to have A. sagrei naturally existing alone, or with one of their natural predators, Leiocephalus carinatus.
Curly-tailed lizards are known to prey on A. sagrei and can have significant impact on anole behavior and adaptation. Twice I observed Leiocephalus capturing and consuming A. sagrei, one of which was an adult male and the other an adult female. We have also noticed that the A. sagrei on these island tend to perch higher and are seldomly seen on rocks or leveled ground compared to those on islands without curly tails, so this behavior could be an effect of Leiocephalus being present.
A female red-winged blackbird with a A. sagrei in its beak
On a different island where Leiocephalus were absent, A. sagrei are still under predation pressure, this time by red-winged blackbirds nesting on the island. We observed a female blackbird with an A. sagrei in its beak waiting for us to leave the island so that it can feed its chicks. This observation suggests that A. sagrei on islands without Leiocephalus might still be under predation pressure by other species that might not be present on the island at all times. Also, predation pressure exerted by an aerial predator differs from that by a terrestrial predator or if both predators are present, so this might be a factor in morphological or behavioral changes in these lizards on these islands.
Anolis sagrei on one of the small cays
Other interesting observations include A. sagrei density on islands seems to be unintuitive. Some small islands with fewer perches hosted many more adult males and females than large islands did. Sizes of individuals also seem to vary greatly between different islands: small cay A. sagrei seem to be, on average, larger than those on mainland Abaco. Personally, I am unable to note major differences between islands which might have resulted in these observations. I’m excited to see if the data we’ve collected will give more insight into these observations as well as other behavioral results that will come from this study!
While visiting relatives last week in Fort Myers (FL), anole enthusiast and avid wildlife photographer Kyle Wullschleger noticed a commotion among the trees while on an afternoon hike in a small neighbourhood nature preserve. On closer inspection he witnessed a group of red-bellied woodpeckers (Melanerpes carolinus) foraging on surrounding cypress trees, with a couple eventually appearing with their apparent target–non-native Cuban brown anoles (A. sagrei). He recalls some of the details:
“The photos from the sequence aren’t all that fantastic because I cropped in so it really just shows the behavior. The whole sequence the woodpecker was basically just slamming the anole against the tree and then trying to pick it apart – it was hard to tell what exactly it was doing, but I believe it eventually swallowed it whole before flying away–it hopped behind the tree so I couldn’t see it anymore.”
“There were at least five birds all moving up and down the lower third of the cypress trees just around the boardwalk I was on. They were moving around the trees without really knocking the wood, so maybe they were purposefully targeting anoles? I only saw successful predation twice, but the brush is so thick–it’s obviously happening quite a bit.”
Sean Giery had previously discussed the main avian predators of anoles in urban South Florida, but woodpeckers didn’t make the list. Woodpeckers do occur in urban areas of South Florida; a new one to add to the list?
Here is a video taken by University of Miami PhD student Joanna Weremijewicz at the Fairchild Tropical Botanical Gardens in Miami, FL last Friday (20th March 2015). There have been lots of posts talking about the predation potential of egrets (and other wading birds) on anoles here on AA similar to this (1,2,3,4), but I think this could be the first one recording predation of A. cristatellus? Cool video!
Macho de Anolis huilae acechando una presa.
Observaciones realizadas en mi finca (Ibagué – Colombia) de un macho de Anolis huilae acechando su presa y una hembra predando su presa. He tenido la oportunidad de observar individuos de ésta especie cazando orugas, larvas y moscas y, la manera como ellos invierten algún tiempo para acechar a sus presas para capturarlas . Aún se desconoce la dieta exacta de esta especie de lagarto endémico de la cordillera Central de Colombia.
Predación por parte de una hembra de Anolis huilae
Editor’s note: Google translates the passage above as follows. It’s amazing how good this programs are getting!:
Observations made on my farm (Ibague - Colombia) of a male Anolis huilae stalking his prey and a female predating its prey. I have had the opportunity to observe individuals of this species hunting caterpillars, larvae and flies and how they spend some time to stalk their prey to catch them. The exact diet of this species of lizard endemic to Central Cordillera of Colombia is still unknown.
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