Read all about it in the (almost) latest from the October 2016 issue of Herpetological Review.
Category: All Posts Page 58 of 146
Travis in the Dominican Republic with Anolis fowleri. Photo by Luke Mahler.
Two recent talks at JMIH 2017 shed light on key morphological characters in anoles: toe pad shape and limb length. Travis Hagey presented his work which looks to shed light on why lizard toe pads are shaped the way that they are and addresses whether gecko and anole toe pads are convergent structures. Working with a team of undergraduates, Travis used geometric morphometrics to analyze the structure of toepads in a diverse group of geckos and anoles. Travis found that anole and gecko toe pads have a similar range of values for traits such as the placement of pads on the toes and the shape of the toes (skinny or fat) in relation to claws. However, anole toe pads formed a distinct cluster indicating that they occupy a unique area of trait space not used by geckos. This finding suggests that the divergent evolutionary history of anoles and geckos has resulted in independent evolutionary explorations of toe pad shape.
Immediately following Travis’ talk, Robin Andrews presented work investigating the embryological development of morphological characters in diverse lizard species. In anoles, consistent differences in the morphology of divergent species support the existence of different anole ecomorphs. Previous research by Sanger and colleagues has shown that the differences in limb-length between anoles of different ecomorphs have their origins early in embryonic development. These early differences in limb length continue throughout the development of anoles into hatchlings and adult forms, a pattern known as transpositional allometry.
Robin compared patterns of limb, tail, and head growth in early stage embryos of four different lizard species, including a chameleon, two geckos, and the brown anole (Anolis sagrei). She found that species-specific differences in limb and tail lengths were exhibited as soon as limb and tail buds emerged from the body and were both best characterized by the same pattern, transpositional allometry. Embryonic head growth, however, showed no specific pattern. Robin’s findings suggest that the adaptive evolution of adult morphology in anole ecomorphs as well as other diverse lizard species is underpinned by developmental reprogramming.
Travis Hagey, Jordan Garcia, Oacia Fair, Nikki Cavalieri, and Barb Lundrigan: Variation in Lizard Adhesive Toe Pad Shape
Robin Andrews: Developmental Origin of Limb Size Variation in Lizards
Exophthalmus scalaris. Credit: symbiota4.acis.ufl.edu/scan
In their 2008 review “Are islands the end of the colonisation road?” Bellemain and Ricklefs (2008) concluded that oceanic islands could be important sources of colonisation of mainland continental areas and cited anoles of the Norops clade as a notable success. There are more than 5 times as many Norops clade species in Central and northern South America as in the West Indies; the 23 extant Caribbean species in the clade are distributed in Cuba and Jamaica with one species in Grand Cayman (Nicholson et al, 2005). Data in Nicholson et al (2005) gave support to the reverse colonisation hypothesis, but did not offer specific dating for the colonisation.
New analyses of 65 species in the Exophthalmus weevil genus complex (Zhang et al 2017) have turned up results that are of significance in understanding the biogeographic history of Caribbean anole dispersal and diversification. Like anoles of the Norops clade, the weevils show reverse colonization (island-to-continent), with diversification on the mainland and diversification within the islands. The data also give some support for overwater dispersal as the factor best explaining ancient between-island distribution.
Zhang et al’s best fit biogeographic model gives an estimate of 19Ma for a jump dispersal of Exophthalmus, most likely from Hispaniola, which went on to diversify into more than 40 species in Central America. So – did the anoles and the weevils make their journeys to the mainland around the same time and under similar conditions? Can this weevil study and the techniques it uses to arrive at its conclusions inform anole evolution and dispersal?
References
Bellemain, E and RE Ricklefs (2008) Are islands the end of the colonisation road? Trends Ecol Evol. 2008 Aug; 23(8):461-8. doi: 0.1016/j.tree.2008.05.001. Epub 2008 Jun 26. (Correction to citation numbering: Trends Ecol Evol. 2008 Oct; 23(10):536-7).
Nicholson, KE, RE Glor, JJ Kolbe, A Larson, S Blair Hedges, JB Losos (2005) Mainland colonization by island lizards. Journal of Biogeography 32 (6), 929-938.
Zhang, G, U Basharat, N Matzke, NM Franz (2017) Model selection in statistical historical biogeography of Neotropical insects—The Exophthalmus genus complex (Curculionidae: Entiminae). Molecular Phylogenetics and Evolution, 109, 226-239. DOI: 10.1016/j.ympev.2016.12.039.
Two years ago, McCranie and Kohler published The Anoles of Honduras: Systematics, Distribution, and Conservation(available on Amazon for under twenty bucks and downloadable for free on the Museum of Comparative Zoology website).
In turn, two mostly favorable reviews were published. However, one of the reviews, by Levi Gray, did question whether a number of anole species recognized from small distributions in Honduras should be recognized as valid species, rather than just as populations of species that are widespread throughout Central America.
Writing in Zootaxa, Randy McCranie has now responded to this point, forcefully arguing that the species should be recognized and challenging his critics to present their own data if they feel otherwise. You’ll have to read Gray’s review and McCranie’s rebuttal yourself to decide what you think. Gray made his skepticism clear, he also did clearly call for more research to address the question.
These pages have previously told the tale of Anolis lineatus, the species whose dewlap is different on one side compared to the other. Now the work has been published in Breviora. Like all publications of the Museum of Comparative Zoology, the paper can be downloaded from the museum’s publications webpage.
The research project was actually explained in a delightful video put together by the three joint first authors, all of whom are headed to college this fall.
Photo by Carissa Wickens
Eileen Wickens, who just finished the fourth grade in north central Florida, is a lizard-catching machine and particularly adept at nabbing blue-colored green anoles (Anolis carolinensis). Here’s the story, relayed by her mom, Carissa:
The teal lizards do seem rare as we have only seen a few. We had one at our house last spring and the photo I sent you was taken at our horse teaching unit in Gainesville. We were running an equine behavior trial that day (we’re actually investigating startle phenotypes and genetics in our Quarter Horse herd), and I saw the lizard as we were packing up our gear. My daughter is very good at spotting and catching them, so we will definitely keep our eyes out and would be happy to provide a specimen for your genetic research if we can. I’ve attached the photo of the lizard we had at the house last spring. The green anoles are scare in our neighborhood and on campus compared to the brown anoles (short snouts with distinct, dorsal diamond or striped markings). They seem to far outnumber the greens.
From our brief observations of those two blue lizards this past year it does not appear they turn the bright green you see on the other Carolina Anoles, but it would be good to observe them for a longer period of time to be certain.
Figure 1 – Long-nosed (Gowidon longirostris) dragon performing a territorial.
In the Greater Antilles, lizard radiations have produced the same suite of ecomorphs on different islands as a consequence of adaptations to similar environments. In the same way, species that use motion-based signals, and occur in sympatry, would be expected to develop similar adaptations to enhance signal efficacy as they are frequently exposed to the same environment (e.g. background noise). Additionally, sympatric species often develop mechanisms to ensure they can distinguish between conspecifics and heterospecifics, particularly if they are closely related. This means that potentially opposing selective pressures might be at work for such systems.
Agamid lizards are widespread across the Australian mainland, and species distributions regularly overlap, especially in arid and rocky habitats. We analysed the motion-based signals of two pairs of sympatric species of Australian agamids to consider how they maintain reliable communication, while at the same time they avoid misidentification during signalling interactions. We calculated the speed distributions of the motion produced by lizard signals, and also by the environment (i.e. background noise). We then compared these two sources of motion to obtain a measure of signal-noise contrast, which indicates how much the signals stand out from the background and is therefore a proxy for signal efficacy (see Ramos & Peters 2017a).
The ring-tailed dragon (Ctenophorus caudicinctus) and the long-nosed dragon (Gowidon longirostris; Figure 1) are often found in sympatry in south Northern Territory and southeast Western Australia, around gorges and rocky outcrops. We recorded territorial displays at West MacDonnell National Park, in Northern Territory. The two species differed in display complexity (example of displays by all four species) and motor pattern use, as well as overall morphology (Figure 2). Interestingly, the speeds produced during their displays (Figure 3) and their signal-noise contrast scores were strikingly similar. Not only that, but their scores indicate that the signals from both species are highly effective in the context of the plant environment. These results demonstrate similar adaptations to their shared environment, while maintaining species recognition cues through morphology and overall display appearance.
Figure 2 – Habitat, average snout-vent length and known repertoire of core motor patterns for both species pairs. The core motor patterns refer to HB = head bob, LW = limb wave, PU = push up, TC = tail coil, and TF = tail flick. Ctenophorus caudicinctus has been observed performing limb waves, but this motor pattern is not present during its territorial displays. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)
The military mallee dragon (Ctenophorus fordi) and the painted dragon (Ctenophorus pictus) are very common in arid and semiarid sandy areas of northwest Victoria, South Australia, and southwest Queensland. We recorded displays at Ngarkat Conservation Park in South Australia, where they are often found in sympatry. These two species are much closer in appearance, but their display complexity and motor pattern use were just as contrasting as in the previous pair of lizards (Figure 2). In addition, the speeds produced during their displays and their signal-noise contrast scores were considerably higher in the painted dragon (Figure 3). We suggest this difference is related to the lack of territoriality in mallee dragons. This species is not known to protect territories or perform aggressive displays, so the motivation to produce conspicuous signals is likely to be reduced compare to its territorial relatives.
Figure 3 – Comparisons of the motion speed distributions for all species. Kernel density functions for a) Ctenophorus caudicinctus (red) and Gowidon longirostris (black), and b) C. fordi (red) and C. pictus (black), averaged within species. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)
In this study we were able to show that the ring-tailed and long-nosed dragon perform displays with almost identical motion speed distributions and signal-noise contrast scores, despite utilising very different territorial displays (see Ramos & Peters 2017b for more details). In the case of the other sympatric pair, motion speed distributions and signal-noise contrast scores appeared to be much higher in the painted dragon than in the non-territorial mallee dragon. This difference in social behaviour could be key to explaining why the signals of the sympatric C. caudicinctus and G. longirostris seem equally well adapted to their local environmental noise, as evidenced by their equally high signal-noise contrast scores, but the signals produced by C. fordi and C. pictus do not. Thus, the selective pressure to generate signals with high efficacy appears to be mediated by signal function, at least in this context.
For the past eight years, my lab has conducted intensive research on green anoles (Anolis carolinensis) in Palmetto State Park in Luling, Texas, about an hour east of San Antonio. This park is beautiful – it’s centered around a swampy area dominated by dwarf palmettos (Sabal minor), and the San Marcos River flows through it. We’ve marked lizards and mapped their home ranges, watched their behavior, measured their morphology and parasite loads, and so much more. In past years, we’ve calculated that the density of green anoles in the park is approximately 0.04 lizards/m2, or about four adult lizards in every 10m x 10m area. We could regularly get sample sizes of around 150 lizards for behavioral studies in the park, but we very rarely collected animals from the park – we left them where we found them!
But this year is different. On three field trips to the park this summer, we have found very few green anoles. On our first visit this year in May, we spent 16 person-hours searching for lizards and found four green anoles. On our second visit in early June, we spent 14 person-hours searching and found eight. Last week, we spent another 12 person-hours and found only two. We see green anoles all over the city of San Antonio, and the students in my team are all skilled lizard spotters and catchers, so this isn’t due to inexperience. Also, we see other species of lizards all over the park – most commonly, Texas spiny lizards, little brown skinks, and house geckos– as well as garter snakes, copperheads, and cottonmouths. We also see tons of frogs.
Garter snake eating a tree frog, at Palmetto State Park. Other herps are thriving there!
So what happened to the anoles? We’ve considered a number of possibilities. The first thing we thought of was the possibility of feral cats – but we haven’t seen any cats in the park, and we think cats should have the same effect on the other herp species. What if the insect population had crashed? But again, that would affect the other lizards, snakes, and frogs too. This isn’t a year of particular drought or excess rain (and in previous wet and dry years, we’ve still seen lots of anoles), and the vegetation throughout the park largely looks the same as it has in the past. Perhaps an anole-specific disease has spread through this population?
In any case, the paucity of anoles in the park this year suggests that there won’t be many next year either, as there’s almost no one around laying eggs. It’s a bummer, because we’ve had such success here in the past.
Any ideas to explain this, AA readers?
Work we’ve published from our previous research in Palmetto State Park:
- Dill, A.K., T.J. Sanger, A.C. Battles and M.A. Johnson. 2013. Sexual dimorphisms in habitat-specific morphology and behavior in the green anole lizard. Journal of Zoology 290: 135-142.
- Battles, A.C., T.K. Whittle, C.M. Stehle, and M.A. Johnson. 2013. Effects of human land use on prey availability and body condition in the green anole lizard, Anolis carolinensis. Herpetological Conservation and Biology 8: 16-26.
- Bush, J.M., M.M. Quinn, E.C. Balreira, and M.A. Johnson. 2016. How do lizards determine dominance? Applying ranking algorithms to animal social behavior. Animal Behaviour 118: 65-74.
- Stehle, C.M., A.C. Battles, M.N. Sparks, and M.A. Johnson. In revision. Prey availability affects territory size, but not territorial display behavior, in green anole lizards. Acta Oecologica.
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) or en español (below).
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.