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Arthropod Predators of Anoles

Orange-legged wandering spider (Cupiennius coccineus) consuming house gecko (Hemidactylus frenatus) at Sirena Biological Station, Corcovado, Costa Rica

Red-legged wandering spider (Cupiennius coccineus) consuming a house gecko (Hemidactylus frenatus) at Sirena Biological Station, Corcovado, Costa Rica

When someone first asked me about the major predators of anoles, my first thought was to talk about curly-tailed lizards (Leiocephalus carinatus) in the Caribbean, vine snakes (Oxybelis spp.) in the neotropics [see my previous post on anole predation by O. aeneus at La Selva], and birds. I think that as herpetologists, we tend to fall into the trap of thinking of invertebrates as “lesser” taxa to be preyed upon by small vertebrates like lizards, and in turn for small vertebrates to be eaten by larger vertebrates.

I, too, when thinking about how selective pressures shape morphological variation in mainland and island habitats turned to fellow herps and birds as the primary predation pressure for mainland anoles. However, it wasn’t until I arrived in Costa Rica that I discovered the high prevalence of voracious arthropods, and I realized that our beloved lizards had much more to fear!

Orange wandering spider (Cupiennius getazi) with egg sac at La Selva Biological Station, Costa Rica

Orange wandering spider (Cupiennius getazi) with egg sac at La Selva Biological Station, Costa Rica

Red-legged wandering spider (Cupiennius coccineus) eating a pink katydid (Tettigoniidae: Phaneropterinae) at La Selva Biological Station, Costa Rica

Red-legged wandering spider (Cupiennius coccineus) eating a pink katydid (Tettigoniidae: Phaneropterinae) at La Selva Biological Station, Costa Rica

A large adult female mantis (Phasmomantis championi) at La Selva Biological Station, Costa Rica

A large adult female mantis (Phasmomantis championi) at La Selva Biological Station, Costa Rica

Conehead katydid (Tettigoniidae: Conocephalinae: Vestria sp.) at La Tarde, Osa Peninsula, Costa Rica

Conehead katydid (Tettigoniidae: Conocephalinae: Vestria sp.) at La Tarde, Osa Peninsula, Costa Rica

In a single night at La Selva, I could easily find dozens of large wandering spiders (Ctenidae), and if I pointed my headlamp higher in the trees I could see eyeshine from hundreds of spiders. Given the high density of large ctenids at La Selva, it is not unlikely that anoles and small tree frogs constitute a major portion of their diet. In fact, I wouldn’t be surprised if large arthropods are one of the most common predators of mainland anoles in some regions.

The same might be the case for giant mantids of the genera Macromantis and Phasmomantis, and conocephaline katydids sporting fearsome mandibles (e.g. Copiphora spp.). Since the invasive Chinese mantids (Tenodera sinensis) in North America are well documented to prey on hummingbirds almost equal in size to the mantids [see Nyffeler et al. 2017], surely larger and bulkier species in the neotropics can take lizards much smaller than themselves. Even though wandering spiders and conehead katydids are primarily nocturnal hunters, I have heard many stories of these arthropods being implicated in anole and tree frog predation. Research looking into how ctenids and nocturnal katydids forage would help determine if they can actually detect sleeping anoles or if predation events occur from the arthropods simply running in to the anoles while on the move.

If anyone here on Anole Annals has any anecdotal or photographic records, please comment below.

To throw a twist on this discussion, is it possible for a spider to prey on a lizard two and a half times its size? A new paper about a vertebrate-eating jumping spider (Salticidae) describes just that! Considering arthropods as possible major players in anole predation could shed light on behavioral and ecological studies of mainland anoles.

Figure 1 from Nyfeller et al. 2017, showing female jumping spiders (Phidippus regius) consuming Carolina anoles (Anolis carolinensis) and Cuban tree frogs (Osteopilus septentrionalis)

Figure 1 from Nyfeller et al. 2017, showing female jumping spiders (Phidippus regius) consuming Carolina anoles (Anolis carolinensis) and Cuban tree frogs (Osteopilus septentrionalis)

Here are a few more spider photos to wrap up this blog post.

Jumping spider (Salticidae: Phiale cf. guttata) eating an assassin bug (Reduviidae)

Jumping spider (Salticidae: Phiale cf. guttata) eating an assassin bug (Reduviidae)

Red-legged wandering spider (Cupiennius coccineus) consuming house gecko (Hemidactylus frenatus) at Sirena Biological Station, Corcovado, Costa Rica

Another angle of a red-legged wandering spider (Cupiennius coccineus) consuming a house gecko (Hemidactylus frenatus) at Sirena Biological Station, Corcovado, Costa Rica

Threat display of a Brazilian wandering spider (Phoneutria boliviensis) from Tárcoles, Costa Rica. A ctenid with medically significant venom.

Threat display of a Brazilian wandering spider (Phoneutria boliviensis) from Tárcoles, Costa Rica. A ctenid with medically significant venom.

Help Identify Costa Rican Anoles

I recently saw these four anoles on a trip to Costa Rica. All four were sighted in La Fortuna in the province of Alajuela. They were sighted on July 18th and 19th, all within a few meters of a forested stream. I have some ideas about their ID’s, but am not completely sure. Can anyone help me with their identification?

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This first anole was found on a tree trunk near the stream at night, while the second one was found on a pole in the morning. Both Anolis lionotus?

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This third one was found on a low shrub in the morning. Anolis limifrons?

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The fourth anole was found on a low-growing shrub at night. Anolis lemurinus?

Thank you in advance for your help.

Shades of Bumpus: Polar Vortex-Induced Natural Selection on Cold Tolerance in the Green Anole

Shane Campbell-Staton had fortuitously measured the thermal physiology of a number of populations of the green anole, Anolis carolinensis, the summer before 2014’s Polar Vortex. So, he went back and examined the survivors. And sure enough, in the most southerly populations, those most strongly affected by the cold snap, natural selection had occurred. Shane tells Scientific American all about it in this podcast. The nifty figure above comes from the University of Illinois’ press release.

 

More Information on the Knight Anole Invasion of the Turks and Caicos

We reported recently that knight anoles (Anolis equestris) have shown up in the T&C. Here’s more on the story from B Naqqi Manco, the Terrestrial Ecologist at the Department of Environment and Maritime Affairs, Turks and Caicos Islands Government:

Cuban knight anoles are currently known from two sites on Providenciales: Vicinity of Beaches Resort in The Bight and Amanyara Resort on Northwest Point. Both populations showed up after the importation of large trees for landscaping from Miami. The properties are both irrigated pretty heavily to keep the bigger trees going. The tree imports were brought in before the Department of Agriculture was fully operative, so unfortunately things got in at that time that probably shouldn’t have made it through.

I don’t have confirmation of the knight anoles breeding, but I know The Bight population has been spreading with individuals having been found on adjacent properties and in a nearby residential neighbourhood. I would be very surprised if they’re not breeding on either site. Unfortunately we don’t have the capacity to monitor them well but this is something we want to keep a closer eye on and it would make a worthwhile research project for a student or intern. 

Thus far, they have not been reported from any other island or cay. 

JMIH 2017: Anole Morphology Round-up: Comparing Gecko and Anole Toepads and Patterns of Embryonic Limb Development in Diverse Lizards

Travis in the Dominican Republic with Anolis fowleri. Photo by Luke Mahler.

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

If West Indian Weevils Colonized the Mainland 19 Million Years Ago, Were Norops Anoles Along for the Ride?

Exophthalmus scalaris. Credit: symbiota4.acis.ufl.edu/scan

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.

Book Review Rebuttal: Are Honduran Anoles Overly Split?

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.

More on the Lizard Species Whose Dewlap Differs from One Side to the Other

dewlaps

These pages have previously told the tale of Anolis lineatus, the species whose 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 authors, all of whom are headed to college this fall.

curious case

A Green Anole That’s Blue

Photo by Carissa Wickens

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. 

Local Adaptations and Signal Function in Sympatric Lizards

Figure 1 - Long-nosed (Gowidon longirostris) dragon performing a territorial.

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.

The core motor patterns refer to HB = head bob, LW = limb wave, PU = push up, TC = tail coil, and TF = tail flick (Ramos and Peters 2016). 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)

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 2 - 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)

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.

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Where Are All the Green Anoles?

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!

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.

Knight Anoles Eat Fruit and Pass Viable Seeds

knight anole

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.

Table 1. Knight anole (Anolis equestris) diet summaries (number of individuals assessed, ‘n’, are included below each study reference). Data presented in columns are the proportion of individual knight anoles with prey taxa in their stomach, P(n). For this study we also present the proportion of total stomach contents by volume, P(vol).

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).

seed dispersal in knight anole

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.

Lizards On The Loose: Middle School Students Help Track Invasive Anoles in Miami, FL

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:

How Does a Male Anolis proboscis Use Its Proboscis? Unveiling the Function of the Rostral Appendage in the Ecuadorian Horned Anole

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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).

Journal of Natural History, 2017. doi:10.1080/00222933.2017.1332790

Journal of Natural History, 2017. doi:10.1080/00222933.2017.1332790

In addition, the paper reports the first captive-born A. proboscis along with a long-awaited answer: males are born with a tiny appendage (see a previous entry or check Hepu’s footage). But most of all, in terms of use of the rostral appendage, this study confirms with several independent observations that the proboscis is actively lifted before any bite attempt and is not, under any circumstance, used as a weapon against other males— as previously discussed by Poe et al. (2012) and Losos et al. (2012). In contrast, the authors suggest that the movement of the proboscis could be performed to facilitate feeding behaviors or even other behaviors related to courtship as the proboscis was lifted when males stimulate the female’s nape (similar to what is described in other anoles).

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.

Useful References:

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.

Are There Seven Species of Anolis distichus?

distichus

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:

Abstract

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..