Exploration of aversive bioacoustics for the effective management of invasive green anoles (Anolis carolinensis)

The green anole (Anolis carolinensis) is an invasive lizard on the Ogasawara Islands, Japan. Green anoles have negatively impacted the native fauna, and thus, green anole eradication measures, such as the use of PTFE-sheet fencing to restrict their movement have been implemented. However, the effectiveness of fencing appears inadequate; therefore, new methods are needed to deter this species. In this study, we explored the use of aversive bioacoustics by testing whether green anoles froze or stayed away on being exposed to predatory sounds and heterospecific alarm calls. Green anoles showed longer freezing times on hearing bird calls than on hearing no sound or single tones. In addition, they stayed far from the audio sources playing the calls of the red-tailed hawk (Buteo jamaicensis) and alarm calls of the warbling white-eye (Zosterops japonicus). Our results suggest that green anoles avoid certain bioacoustics, especially the calls of B. jamaicensis and the alarm call of Z. japonicus. Hence, these bioacoustics can be used as an effective control method to restrict the invasion and dispersion of green anoles.     

Control of arthropod abundance by Anolis lizards on St. Eustatius (Neth. Antilles)

The two Anolis lizard species of St. Eustatius (Neth. Antilles) have large effects on the abundance of arthropods. Over a six-month period, we excluded Anolis lizards from three experimental areas and maintained three other areas with natural densities of lizards. Exclusion of anoles resulted in a two to three-fold increase in the abundance of arthropods on the forest floor (mainly Dipterans), and a twenty to thirty-fold increase in the abundance of three large web-building spiders. These abundant web-building spiders, in turn, caused approximately a 25% decrease in the abundance of insects between the forest floor and canopy. Exclusion of anoles had no observed effect on the degree of herbivory as assayed by the amount of leaf damage on two plant species.     

An Analysis of Inter-Population Divergence in Visual Display Behavior of the Green Anole Lizard (Anolis carolinensis)

Variation in habitat structure can profoundly affect the evolution of visual displays in animals. We compared the field display behavior of two populations of the green anole lizard (Anolis carolinensis) in Southern Louisiana. These two populations occupy habitats varying markedly in structure (clumped vs. continuous), ecological setting (urban vs. natural) and the degree of male competition and predation. We filmed 56 large adult male lizards during the active spring reproductive period and detected substantial divergence in display behavior between populations. We found that (1) relative dewlap areas did not differ significantly between populations, (2) Tulane anoles spent about twice as much time displaying compared with Good Hope field anoles, although the average display duration did not differ significantly between populations, and (3) the two populations differed significantly in the relative frequency of display types: lizards from the Tulane population used a higher proportion of A and B display types, whereas Good Hope Field anoles used C displays more often. Finally, we detected differences in other aspects of display behavior (use of display modifiers, volley length distributions). We suggest that these display differences may result from differences in green anole male density (three times higher at Tulane), combined with habitat differences (clumped vs. continuous).     

Genetic variation in the green anole lizard (Anolis carolinensis) reveals island refugia and a fragmented Florida during the quaternary

The green anole lizard (Anolis carolinensis) is a model organism for behavior and genomics that is native to the southeastern United States. It is currently thought that the ancestors of modern green anoles dispersed to peninsular Florida from Cuba. However, the climatic changes and geological features responsible for the early diversification of A. carolinensis in North America have remained largely unexplored. This is because previous studies (1) differ in their estimates of the divergence times of populations, (2) are based on a single genetic locus or (3) did not test specific hypotheses regarding the geologic and topographic history of Florida. Here we provide a multi-locus study of green anole genetic diversity and find that the Florida peninsula contains a larger number of genetically distinct populations that are more diverse than those on the continental mainland. As a test of the island refugia hypothesis in Pleistocene Florida, we use a coalescent approach to estimate the divergence times of modern green anole lineages. We find that all demographic events occurred during or after the Upper Pliocene and suggest that green anole diversification was driven by population divergence on interglacial island refugia in Florida during the Lower Pleistocene, while the region was often separated from continental North America. When Florida reconnected to the mainland, two separate dispersal events led to the expansion of green anole populations across the Atlantic Seaboard and Gulf Coastal Plain.     

Predation Risk Perception,Food Density and Conspecific Cues Shape Foraging Decisions in a Tropical Lizard

When foraging, animals can maximize their fitness if they are able to tailor their foraging decisions to current environmental conditions. When making foraging decisions, individuals need to assess the benefits of foraging while accounting for the potential risks of being captured by a predator. However, whether and how different factors interact to shape these decisions is not yet well understood, especially in individual foragers. Here we present a standardized set of manipulative field experiments in the form of foraging assays in the tropical lizard Anolis cristatellus in Puerto Rico. We presented male lizards with foraging opportunities to test how the presence of conspecifics, predation-risk perception, the abundance of food, and interactions among these factors determines the outcome of foraging decisions. In Experiment 1, anoles foraged faster when food was scarce and other conspecifics were present near the feeding tray, while they took longer to feed when food was abundant and when no conspecifics were present. These results suggest that foraging decisions in anoles are the result of a complex process in which individuals assess predation risk by using information from conspecific individuals while taking into account food abundance. In Experiment 2, a simulated increase in predation risk (i.e., distance to the feeding tray) confirmed the relevance of risk perception by showing that the use of available perches is strongly correlated with the latency to feed. We found Puerto Rican crested anoles integrate instantaneous ecological information about food abundance, conspecific activity and predation risk, and adjust their foraging behavior accordingly.     

Establishment of <Emphasis Type="Italic">Anolis sagrei</Emphasis> on Bermuda represents a novel ecological threat to Critically Endangered Bermuda skinks (<Emphasis Type="Italic">Plestiodon longirostris</Emphasis>)

Bermuda is an isolated, oceanic island with only one endemic terrestrial vertebrate, the Critically Endangered Bermuda skink (Plestiodon longirostris; Squamata, Scincidae). Major declines in P. longirostris populations have been caused primarily by habitat loss and mortality via invasive species (e.g., predation from birds and cats) and human waste products (e.g., trapped in discarded bottles). However, biotic interactions and interspecific competition with invasive lizards have also been identified as potentially detrimental to P. longisrostris populations. Here, we provide the first occurrence records of a highly invasive lizard, the Cuban brown anole (Anolis sagrei), on Bermuda. We assess the brown anole’s diet, habitat use, morphology, and island-wide distribution for comparison to the native skink, P. longirostris. Results of this study indicate that A. sagrei in Bermuda are highly terrestrial (>60% of all lizards observed on the ground vs. in trees) and forage primarily on terrestrial invertebrates. These data indicate substantial ecological overlap with the exclusively-terrestrial P. longirostris. This is in contrast to the other established non-native lizards on Bermuda, which are principally arboreal and have successfully coexisted with P. longirostris for >60 years. At present, the geographic distributions of A. sagrei and P. longirostris do not overlap. However, all extant skink populations are within several kilometers of brown anole populations (with the nearest being <0.5 km). The extensive overlap in ecological niche between the Bermuda skink and the invasive brown anole will likely present a serious conservation threat if contact is made. This study is exceptional in providing clear in situ ecological data which predict a conservation threat of an established invasive species to a Critically Endangered island endemic prior to coexistence. Continued monitoring of this situation as P. longirostris and A. sagrei inevitably come into contact will allow these a priori hypotheses of conservation risk via ecological overlap to be tested.     

Multi-locus phylogeographic and population genetic analysis of Anolis carolinensis: historical demography of a genomic model species

The green anole (Anolis carolinensis) has been widely used as an animal model in physiology and neurobiology but has recently emerged as an important genomic model. The recent sequencing of its genome has shed new light on the evolution of vertebrate genomes and on the process that govern species diversification. Surprisingly, the patterns of genetic diversity within natural populations of this widespread and abundant North American lizard remain relatively unknown. In the present study, we use 10 novel nuclear DNA sequence loci (N?=?62 to 152) and one mitochondrial locus (N?=?226) to delimit green anole populations and infer their historical demography. We uncovered four evolutionarily distinct and geographically restricted lineages of green anoles using phylogenetics, bayesian clustering, and genetic distance methods. Molecular dating indicates that these lineages last shared a common ancestor ～2 million years ago. Summary statistics and analysis of the frequency distributions of DNA polymorphisms strongly suggest range-wide expansions in population size. Using Bayesian Skyline Plots, we inferred the timing of population size expansions, which differ across lineages, and found evidence for a relatively recent and rapid westward expansion of green anoles across the Gulf Coastal Plain during the mid-Pleistocene. One surprising result is that the distribution of genetic diversity is not consistent with a latitudinal shift caused by climatic oscillations as is observed for many co-distributed taxa. This suggests that the most recent Pleistocene glacial cycles had a limited impact on the geographic distribution of the green anole at the northern limits of its range.     

Frequency of tail loss reflects variation in predation levels,predator efficiency,and the behaviour of three populations of brown anoles

We investigated two predictions regarding the incidence of tail regeneration in lizards for three populations of brown anoles exposed to varying predation levels from the same predator (cats). Firstly although inefficient predators are likely to increase the incidence of regenerated tails (i.e. lizards can escape through tail autotomy), highly efficient predators will kill and eat the lizard and thus leave no evidence of autotomy. At the site with no cats, only 4% of anoles demonstrated signs of tail regeneration. This value was not significantly different from the site where feral cats (i.e. ‘efficient’ predators that would capture prey to eat, as supported by behavioural observation) were present (7%). By contrast, 25% of anoles present at the site with pet cats (well‐fed domesticated cats that caught and played with anoles, i.e. were ‘inefficient’ predators) exhibited regenerated tails. Secondly, more obvious lizards are more susceptible to predation attempts. Supporting this hypothesis, our data indicate a higher incidence of regenerated tails (28%) was recorded amongst adult males (which are territorial, occupying exposed positions) compared to females and subadult males (17%) or juveniles (1%). In conclusion, the behaviour of both the predator and the lizard influences the frequency of regenerated tails in brown anoles. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 648–656.     

Escape tactics and effects of perch height and habituation on flight initiation distance in two Jamaican anoles (Squamata: polychrotidae)

Escape by Anolis lizards is influenced by microhabitats and fight initiation distance increases with predation risk. Differences in microhabitat use among ecomorphs affect escape behavior, but only two studies have reported ecomorphological differences in flight initiation distance among Greater Antillean species. I studied effects of predation risk and microhabitats on escape behavior by conducting field experiments using two species of anoles, Anolis lineatopus and A. grahami, on the campus of the University of the West Indies at Mona, Jamaica. Because ecomorphological variation of anoles has evolved independently within each island of the Greater Antilles, but relationships between ecomorphs and escape behaviors are poorly known, I characterized microhabitat use and escape tactics, and determined relationships between flight initiation distance and two risk factors, habituation to human presence and perch height, in Anolis lineatopus, a trunk-ground anole and A. grahami, a trunk-crown anole. Sample sizes for A. lineatopus and A. grahami were 214 and 93, for microhabitat use and escape destinations, 74 and 34 for human presence and 125 and 34 for perch height. The two species occurred in similar microhabitats and exhibited similar escape tactics, but exhibited key differences expected for their ecomorphs. Both species were sighted frequently on the ground and on trees, but A. lineatopus were more frequently on ground and were perched lower than A. grahami. Both species escaped from ground to trees and when on trees hid on far sides and escaped without changing climbing direction with equal frequency. The frequency of fleeing upward was greater for A. grahami than A. lineatopus. Both species exhibited habituation by having shorter flight initiation distances in areas with more frequent exposure to people. In both species flight initiation distance increased as perch height decreased because, lizards had to climb farther to be out of reach when perched lower. The relationship between flight initiation distance and perch height may apply to other anole ecomorphs that flee upward when low perched on trees.     

Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems

Understanding the evolution of complex functional traits is a challenge for evolutionary physiology. Here we investigate the evolution of subdigital toepads in lizards, which have arisen independently at least three times, although with subtle anatomical differences. Some designs (anole, gecko) appear functionally equivalent, whereas other designs (skink) are inferior. The functional equivalence of geckos and anoles highlights the creative aspect of the evolutionary process in that these two groups have arrived at the same functional endpoint along very different trajectories. However, this functional equivalence does not result in equivalence for performance at whole-organism tasks (e.g., running uphill), as the evolution of behavior (e.g., toe-furling) has enabled geckos to be superior climbers than anoles. We also show that adaptive increases in the toepad size within a closely related lizard genus (Anolis) has resulted in concomitant evolution of enhanced clinging ability and increased perch heights. A third insight is that pad-bearing geckos are capable of carrying tremendous loads (up to 250% of body weight) up smooth surfaces, and that the toepad itself does not appear limiting. This comparative and whole-organism approach to lizard toepads underscores how organisms can evolve multiple solutions to evolutionary problems.     

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards

The pattern of reproductive character displacement (RCD)—in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation—is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40 years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A. caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.     

Life cycle and postembryonic development of Oochoristica anolis (Cyclophyllidea: Linstowiidae)

Gravid proglottids of Oochoristica anolis from naturally infected anole lizards, Anolis carolinensis, were placed in covered Petri dishes with laboratory-reared beetles, Tribolium confusum and Tenebrio molitor. After maintenance at 25 C, metacestodes developed in 29 of 61 T. confusum (48%), but in none of 5 T. molitor. Beetles contained from 1 to 22 metacestodes (means = 3.3), which were fully developed by day 40 postexposure. A primary lacuna was never observed, but the possibility of its presence could not be ruled out without histological study. No cercomer was formed and metacestodes retained larval hooks throughout development. Scolices were invaginated at removal from the hemocoel, but usually evaginated quickly in Ringer's. On day 60 postexposure, metacestodes were fed by stomach tube to 5 anoles, 2 lacertid lizards (Podarcis muralis) and 2 mice. Worms developed only in anoles, 3 of which were infected upon examination. Oncospheral hooks were present in worms after 7 days development in the lizard; a median excretory pore was present at the posterior tip of all stages examined, including the terminal mature proglottid of a worm after 105 days in a lizard. Scolex growth rate was linear throughout metacestode and adult development, but growth rate in body length was diphasic, punctuated by change of hosts, associated with strobilization. Attempts to establish parenteral infections in anoles were unsuccessful. Present data constitute the most complete life history study thus far for any species of Oochoristica.     

An impact assessment of the alien lizard Plestiodon japonicus (Scincidae, Reptilia) on a threatened island population of the native lizard P. latiscutatus at an early phase of the biological invasion

On the island of Hachijojima, central Japan, a formerly abundant population of native lizard, Plestiodon latiscutatus has become endangered by predation from an alien weasel (Mustela itatsi). Recently, an alien lizard, P. japonicus, became established on the island. The impact of the alien lizard and current distribution of the native lizard were assessed by field surveys and DNA analyses. The native lizard was sparsely distributed in the western part of the island. The alien lizard occurred in the northeastern region of the island. Between these regions, several hybrid populations were identified, including some with non-F1 genotypes, suggesting that introgression is occurring. The distribution of the weasel was examined based on field observations, allowing us to estimate predator impacts on both lizard species. We found evidence that the weasel was present throughout the entire island, suggesting that the alien lizard was able to become established despite the presence of the weasel. This indicates that the alien lizard is likely to expand its habitat range and that introgression may spread. We conclude that P. latiscutatus populations will become increasingly endangered by the synergism of genetic introgression from P. japonicus and predation pressure from the weasel.     

Evidence for asymmetrical intraguild predation between native and introduced Anolis lizards

Since its introduction, Anolis sagrei (Sauria: Polychrotidae) has been replacing native A. carolinensis in Florida and native A. conspersus in Grand Cayman Island as the common anole of urban environments and other open habitats. To assess the likelihood that predation of juvenile native anoles by A. sagrei adults is an important interaction in this process, the propensities for intraguild predation and cannibalism were assessed for A. sagrei and A. carolinensis in Florida and for A. sagrei and A. conspersus in Grand Cayman. Predation experiments were conducted in cages, using freshly captured lizards, in which adult males of each species were presented with conspecific and heterospecific juveniles. Adult A. sagrei were (1) significantly more likely to eat juveniles than were adult A. carolinensis or A. conspersus, and (2) significantly more likely to eat heterospecific than conspecific juveniles, whereas adult A. carolinensis and A. conspersus were not. Thus, the propensity for intraguild predation is asymmetrical in favor of introduced A. sagrei in Florida and Grand Cayman. Further study is needed, however, to determine the importance of intraguild predation under field conditions. Received: 14 July 1999 / Accepted: 6 March 2000     

Comparative and behavioral analyses of preferred speed: Anolis lizards as a model system

I quantified the movement patterns of eight morphologically and ecologically diverse Caribbean Anolis lizard species in the field to address the following questions: (1) Do these eight species move at preferred speeds, and if so, what are these speeds? (2) What proportion of their maximum sprinting capacities do the anole species use when moving undisturbed? (3) What percentage of the time do lizards spend moving, and how far do they typically travel on a daily basis? (4) Have the preferred speeds of anoles coevolved with structural habitat use? Most of the distributions of speeds were highly skewed, with a preponderance of slow-speed locomotion (<20% of maximum capacity). Median speeds varied almost eightfold among species, from a low of 4.9 cm/s (3.0% of maximum) to a high of 38.0 cm/s (22.4% of maximum). For all eight species, at least 75% of their locomotor movements took place between 0% and 40% of maximum capacity. The eight species varied almost 15-fold in the percentage of time they spent moving, indicating that not all anole species are equally sedentary. Through usage of modern comparative methods, I showed that Anolis species that move slowly through their environments also tend to use narrow perch diameters and have large habitat breadths. These findings show how evolutionary approaches can be profitably integrated with physiological data to understand how species use their habitats.     

Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace

Caribbean Anolis lizards are often cited as a textbook example of adaptive radiation. Similar morphologies (ecomorphs) have originated in similar ecological settings on different large islands in the West Indies. However, relatively little is known about one of the morphologically most specialized and divergent ecomorphs: the twig anoles. Here, we investigate aspects of morphology, dewlap size, locomotor and bite performance, structural habitat and diet of the poorly known twig anole, Anolis sheplani from Hispaniola. Few observations have previously been made of this species in its natural habitat, and few quantitative data on its natural history are available. A. sheplani is an extreme twig anole with respect to its morphology, performance capacities, and ecological niche. Males and females of this species do not differ from each other in body dimensions, performance or habitat use, but males do have a bigger dewlap than females. We present data for 25 individuals and compare them with data for other Greater Antillean anoles. It becomes apparent that twig anoles constitute a large component of the morphological, functional, and ecological diversity of Anolis lizards. Small twig anoles such as A. sheplani appear to be pushing the boundaries of morphospace and are thus crucial in our understanding of the evolution of phenotypic diversity.     

Relationships among hormones, brain and motivated behaviors in lizards

Lizards provide a rich opportunity for investigating the mechanisms associated with arousal and the display of motivated behaviors. They exhibit diverse mating strategies and modes of conspecific communication. This review focuses on anole lizards, of which green anoles (Anolis carolinensis) have been most extensively studied. Research from other species is discussed in that context. By considering mechanisms collectively, we can begin to piece together neural and endocrine factors mediating the stimulation of sexual and aggressive behaviors in this group of vertebrates.     

Clothing color mediates lizard responses to humans in a tropical forest

Identifying how ecotourism affects wildlife can lower its environmental impact. Human presence is an inherent component of ecotourism, which can impact animal behavior because animals often perceive humans as predators and, consequently, spend more time on human-directed antipredator behaviors and less on other fitness-relevant activities. We tested whether human clothing color affects water anole (Anolis aquaticus) behavior at a popular ecotourism destination in Costa Rica, testing the hypothesis that animals are more tolerant of humans wearing their sexually selected signaling color. We examined whether clothing resembling the primary signaling color (orange) of water anoles increases number of anole sightings and ease of capture. Research teams mimicked an ecotourism group by searching for anoles wearing one of three shirt treatments: orange, green, or blue. We conducted surveys at three different sites: a primary forest, secondary forest, and abandoned pasture. Wearing orange clothing resulted in more sightings and greater capture rates compared with blue or green. A higher proportion of males were captured when wearing orange whereas sex ratios of captured anoles were more equally proportional in the surveys when observers wore green or blue. We also found that capture success was greater when more people were present during a capture attempt. We demonstrate that colors “displayed” by perceived predators (i.e., humans) alter antipredator behaviors in water anoles. Clothing choice could have unintended impacts on wildlife, and wearing colors resembling the sexually selected signaling color might enhance tolerance toward humans.     

Learning foraging thresholds for lizards: an analysis of a simple learning algorithm

This paper gives proof of convergence for a learning algorithm that describes how anoles (lizards found in the Caribbean) learn foraging threshold distance. An anole will pursue a prey if and only if it is within this threshold of the anole's perch. The learning algorithm was proposed by Roughgarden and his colleagues. They experimentally determined that this algorithm quickly converges to the foraging threshold that is predicted by optimal foraging theory. We provide analytic confirmation that the optimal foraging behavior as predicted by Roughgarden's model can be attained by a lizard that follows this simple and zoologically plausible rule of thumb. Copyright 1999 Academic Press.     

Biogeography and evolution of a widespread Central American lizard species complex: Norops humilis, (Squamata: Dactyloidae)

Background

Caribbean anole lizards (Dactyloidae) have frequently been used as models to study questions regarding biogeography and adaptive radiations, but the evolutionary history of Central American anoles (particularly those of the genus Norops) has not been well studied. Previous work has hypothesized a north-to-south dispersal pattern of Central American Norops, but no studies have examined dispersal within any Norops lineages. Here we test two major hypotheses for the dispersal of the N. humilis/quaggulus complex (defined herein, forming a subset within Savage and Guyer’s N. humilis group).

Results

Specimens of the N. humilis group were collected in Central America, from eastern Mexico to the Canal Zone of Panama. Major nodes were dated for comparison to the geologic history of Central America, and ancestral ranges were estimated for the N. humilis/quaggulus complex to test hypothesized dispersal patterns. These lineages displayed a northward dispersal pattern. We also demonstrate that the N. humilis/quaggulus complex consists of a series of highly differentiated mitochondrial lineages, with more conserved nuclear evolution. The paraphyly of the N. humilis species group is confirmed. A spatial analysis of molecular variance suggests that current populations are genetically distinct from one another, with limited mitochondrial gene flow occurring among sites.

Conclusions

The observed south-to-north colonization route within the Norops humilis/quaggulus complex represents the first evidence of a Norops lineage colonizing in a south-to-north pattern, (opposite to the previously held hypothesis for mainland Norops). One previously described taxon (N. quaggulus) was nested within N. humilis, demonstrating the paraphyly of this species; while our analyses also reject the monophyly of the Norops humilis species group (sensu Savage and Guyer), with N. tropidonotus, N. uniformis, and N. marsupialis being distantly related to/highly divergent from the N. humilis/quaggulus complex. Our work sheds light on mainland anole biogeography and past dispersal events, providing a pattern to test against other groups of mainland anoles.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-015-0391-4) contains supplementary material, which is available to authorized users.