New natural history note: “Nocturnal foraging and activity by diurnal lizards: Six species of day gecko (Phelsuma spp.) using the night‐light niche”.
A set of observations, recently published in Austral Ecology, noted six different species of day gecko (Phelsuma spp.) using artificial light at night (ALAN) to engage in nocturnal activity (e.g., foraging, courtship, and agonistic behavior). Lizards of this genus are widely believed to be primarily diurnal, however, their propensity to colonize both urban and highly-modified habitats, as well as establish invasive populations within novel landscapes, suggests they are a taxon that is quite flexible and adaptable.
A blue‐tailed day gecko, Phelsuma cepediana, foraging for insects under a fluorescent light in Mauritius. Photo credit J. L. Riley.
Remind you of any other small- to medium-sized adaptable and diverse group of lizards?
Keen readers of the Anole Annals will recall several posts about the effect ALAN can have on anoles, including its impact on physiological stress, metabolism, invasive potential, and reproductive output. With many accounts noting the costs and benefits of shifting diel cycles and daily activity period, but also the general impact light pollution may have. No doubt, there remains a lot of research potential to examine similar questions for the many Phelsuma species across their native and invasive ranges.
Reunion ornate day geckos, Phelsuma inexpectata, engaging in nocturnal activity under a fluorescent light inside a bathroom in Manapany-Les-Bains, Reunion (A,B), including courtship behavior (C). Photos credits C. Baider and F.B.V. Florens.
It is always worth keeping your eyes peeled in the field.
The observations that led to this note came from nine researchers working in various sites, locations, and projects across a number of archipelagos spanning the Indian Ocean and over several years. As with many natural history observations, most of these accounts began with a researcher – who was no doubt occupied with an entirely different task – seeing something out of the ordinary, snapping a picture and jotting down some quick details, and carrying on with their work. A great reminder to never leave home without your trusty notebook; digital or otherwise. Then later on, sometimes much later, this information regarding “something weird you saw” is shared between colleagues, sometimes met with an “oh ya, I saw that too, different species, different location, but the same thing,” and from there, patterns emerge and collaborations bear fruit.
Over the years, Anoles Annals has featured a number of posts related to day geckos, with some keener anolologists expressing the feeling that these colorful, charismatic, and adaptable geckos could be seen as “honorary anoles.” A compliment, surely, the geckos would appreciate and reciprocate toward anoles, if given the chance. Despite their stunning appearance, long history of public awareness, and ability to sell car insurance, there remains a lot of information we do not know about day gecko behavior, biology, and ecology. We hope this natural history note will prompt further research interest into this enigmatic group of lizards.
Chelsea Connor presenting her research at SICB 2020
Invasive species can often compete for resources with native species, which can have a negative impact on the community. This is an especially common occurrence when it comes to the diet of these competing species. It is important to investigate the diet of both the invader and the native species in order to determine whether this competition is present and if it will cause negative effects in the future.
Chelsea Connor grew up on the island of Dominica. She is currently an undergraduate student at Midwestern State University in Wichita Falls, Texas in the lab of Dr. Charles M. Watson. Her research addresses the dietary niche overlap of native and invasive species on her home island of Dominica. For this research, Chelsea and another undergraduate student, Destiny Zinn captured and collected feces from Anolis oculatus (a native species) and Anolis cristatellus (an invasive species) on Dominica. They successfully extracted and amplified a region of the cytochrome oxidase I gene from 44 samples. Then they ligated the PCR products and transformed them into E. coli to grow on a plate. After this, they sequenced the resulting clones and placed them into Molecular Taxonomic Operational Units, which were matched using the databases BOLD and GenBank with the help of Daniella Biffi and Dr. Dean Williams at Texas Christian University. They calculated the similarity of diets using the Sørenson coefficient.
Chelsea and her collaborators found a shockingly low degree of dietary overlap, discovering that these two species of anoles on Dominica consume different arthropod prey. They identified 40 prey species in this experiment, and only 4 species were contained in the diet of both the native and invasive anoles. Chelsea emphasizes that there may be dietary niche partitioning, which could explain how the two species are able to coexist across the island and avoid competition.
Brown anoles are invasive throughout the southeastern United States and are often transported via the nursery trade.
As invasive species expand across landscapes, they may engage in new interactions including with native competitors and prey as well as encountering novel environmental conditions such as different temperatures or patterns of rainfall. It is often difficult to observe the process of how invasive species which are dispersing across landscapes are affected by these novel conditions, because it may be difficult to find edge populations of invaders, and those extralimital populations which do not survive may have disappeared before scientists can observe them.
In southern Florida, many anole species have been introduced and are expanding their ranges, perhaps none more prolifically so than the brown anole (Anolis sagrei). In the past 75 years or so, brown anoles have occupied all of peninsular Florida, the eastern seaboard of Georgia, and Gulf Coast habitats through Louisiana. Many of these expansions are thought to occur via hitchhikers on cars or via the nursery trade, in which potted plants with adults or eggs are transported to new areas. These introductions may fail for many reasons (e.g., inhospitable environments, low numbers of colonizers, intentional extirpation by humans), but these processes of dispersal, establishment, and extirpation are difficult to study. Dan Warner, a professor at Auburn University, took advantage of a known extralimital population of brown anoles in a greenhouse in central Alabama to study the survival of a population created through this type of dispersal.
This population of anoles existed well north of its continuous invasive range in the United States and was exposed to much colder winter conditions than other studied populations. It was present at the greenhouse from at least 2006, and so survived for at least 10 generations, long enough for adaptation to these novel thermal conditions to potentially occur. Working with a team of undergraduates, graduate students, and post-docs, Dan assessed the thermal conditions in the greenhouse environment, conducted mark-recapture studies of the population, and measured thermal tolerances of lizards.
Dr. Amélie Fargevieille and Jenna Pruett representing the Warner Lab at SICB 2019.
At SICB 2019, Dr. Amélie Fargevieille and Jenna Pruett presented results from the study, showing that the greenhouse population included all life stages of lizards and reached a total size of >1000 individuals. While one might expect that these northern lizards would have altered critical thermal limits, the Warner lab showed that both the upper and lower thermal limits of these lizards (the temperatures at which their movements became uncoordinated), were the same as those found in lizards from warmer, southern populations. These results indicate that existence in a colder northern climate for >10 years did not lead to adaptive changes in thermal limits, perhaps due to the population occupying a thermally-buffered habitat, i.e., the greenhouse.
While hurricanes have facilitated several fascinating studies of anole adaptation (e.g., Schoener et al., 2017, Donihue et al., 2018), they may also take these opportunities away. In the case of this population, Hurricane Irma blew off the greenhouse roof in 2017 (which remained unrepaired), exposing this population to the rigors of a central Alabama winter. Multiple surveys in 2018 confirmed that there were no survivors of this previously robust population. Dataloggers confirmed that, even in the most sheltered microhabitats that remained, temperatures dropped below the critical thermal minima of brown anoles, presumably extirpating the entire population.
Recent Extinction of a Viable Tropical Lizard Population from a Temperate AreaWARNER, DA*; HALL, JM; HULBERT, A; TIATRAGUL, S; PRUETT, J; MITCHELL, TS; Auburn University.
Figure 1. Native and non-native ranges of Anolis sagrei. Map from Kolbe et al. (2017).In this study, Kolbe and collaborators (2017) surveyed A. sagrei populations across Cayman Brac. First, they looked for red-dewlapped lizards to determine whether invasive A. sagrei from Grand Cayman have invaded Cayman Brac. Second, they collected brown anole lizards on Grand Cayman and Little Cayman to determine the source of red-dewlapped A. sagrei. For all lizards captured, they quantified dewlap phenotypes (i.e., reflectance spectra) using spectrophotometric methods, measured structural habitat use (i.e., perch height and diameter) and body size (i.e., snout-vent length (SVL) and mass), and genotyped ten nuclear microsatellite loci. For lizards with intermediate multilocus genotypes or with a genotype that did not match their island, they sequenced mitochondrial DNA (mtDNA) haplotypes (ND2) to test for nuclear-mitochondrial mismatches. Genomic data was combined with previously published microsatellite genotypes (Kolbe et al. 2008) and mtDNA (ND2) sequences for the Cayman Islands (Kolbe et al. 2004, 2007). With these data, they evaluated whether invasive A. sagrei from Grand Cayman have been introduced to native populations on Cayman Brac, and if so, whether invasive lizards have interbred with native lizards.
Under current trends of globalization, human activities impact the distribution of species by facilitating dispersal of propagules. Human-mediated dispersal prevents geographic distance from being a barrier to the introduction and movement of many species. These long-distance colonization events can gather evolutionary distinct lineages that might have been separated for millions of years (e.g., Kolbe et al. 2004). Moreover, dispersal events can potentially reintroduce individuals from an invasive population back into their native range; either back into their original source population or to any part of their native range. This previously undocumented dimension of biological invasion was termed cryptic back-introduction by Guo (2005).
Anolis sagrei is an excellent colonist, judging by its geographical distribution. This species has reached many islands and mainland areas in the Caribbean by overwater dispersal (Williams 1969). About 2.5 million years ago, A. sagrei naturally colonized Cayman Brac and Little Cayman. These populations subsequently differentiated into the yellow-dewlapped endemic subspecies A. sagrei luteosignifer on Cayman Brac and the red-dewlapped A. s. sagrei on Little Cayman (Schwartz and Henderson 1991); the dewlap (i.e., an extendible flap of skin attached to the throat) is used for mate attraction, male-male and interspecific competition, and predator deterrence (Losos 2009). However, this species failed to naturally colonize the third of the Cayman Islands, Grand Cayman. In the early 1980s, through human-mediated dispersal, a red-dewlapped form of A. sagrei established on Grand Cayman. These populations resulted from the introduction of genetically admixed lizards from non-native populations in south Florida (Minton and Minton 1984; Kolbe et al. 2004, 2008; Figure 1). Since then, inter-island supply shipments by air and sea within the Caymans could have transported invasive and native brown anole lizards among the three islands. Kolbe et al. (2017) explored whether cryptic back-introduction is occurring in brown anole (A. sagrei) lizards and the implications of this type of invasion for native populations.
Figure 2. Results of PCA for dewlap reflectance (Kolbe et al. 2017).
Kolbe et al. (2017) found no differences among islands in structural habitat use. They conducted a principal component analysis (PCA) for dewlap reflectance data using the average wavelength of each lizard. PCA results show that there is strong differentiation in dewlap reflectance between yellow-dewlapped lizards on Cayman Brac and the red-dewlapped lizards on Little Cayman and Grand Cayman (Figure 2), which supports their field observations of red-dewlapped lizards occurring on Cayman Brac (Figure 3B). This suggests the introduction of brown anole lizards to Cayman Brac from either of the two other Cayman Islands.
Figure 3. Examples of Anolis sagrei dewlaps from the Cayman Islands (Kolbe et al. 2017).
Furthermore, this study reports strong population-genetic structure among the three Cayman Islands and evidence for non-equilibrium. They identified intermediate multilocus genotypes between Grand Cayman and Cayman Brac (Figure 4). Also, the authors found an intermediate microsatellite genotype in one individual from Cayman Brac. This lizard had a red dewlap and a mtDNA haplotype from Grand Cayman. This mismatch among genetic and phenotypic data suggests that A. sagrei lizards (with different colored dewlaps) from Grand Cayman and Cayman Brac are interbreeding.
Figure 4. Results of a PCoA using multilocus genotypes from ten microsatellite loci (Kolbe et al. 2017).
This study reports the first evidence of cryptic back-introduction; however the frequency with which this phenomenon occurs is still unknown. By studying cryptic back-introductions we can eventually understand how lineages change though a brief period of isolation from its native range and determine if these are incompatible when brought together again. Likewise, future studies should address how phenotypic variation affects ecological interactions with native species and its consequences.
Guo, Q. 2005. Possible cryptic invasion through “back introduction”?
Kolbe, J. J., R. E. Glor, L. R. Schettino, A. C. Lara, A. Larson, and J. B. Losos. 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181.
Kolbe, J. J., A. Larson, and J. B. Losos. 2007. Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Molecular Ecology 16:1579–1591.
Kolbe, J. J., A. Larson, J. B. Losos, and K. de Queiroz. 2008. Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biology letters 4:434–437.
Losos, J. B. 2009. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of anoles. University of California Press.
Schwartz A, Henderson RW (1991) Amphibians and reptiles of the West Indies: descriptions, distributions, and natural history. University of Florida Press, Gainesville
Williams, E. E. 1969. The ecology of colonization as seen in the zoogeography of anoline lizards on small islands.
In one of the few anole talks here at the annual Ecology meeting in Ft. Lauderdale, Florida, James Stroud presented on a project he conducted with the Fairchild Tropical Botanical Garden, Jason Kolbe, and others. Together, they organized a large citizen science project engaging middle-school aged students to collect distribution and abundance data about anoles in the Southern Miami region in a program they call “Lizards on the Loose.”
In this outreach project, James and colleagues had 101 schools participate in collecting data. Armed with a handy anole ID guide created by Jason Kolbe and a video by James explaining anole biology and species differences, students and teachers set out to conduct 15 minute visual surveys. On these surveys, they recorded how many animals they encountered, the species ID, and the approximate body size using a provided standardized collection protocol and entering data into a Google forms site.
The results were overwhelming: more than 1,000 students conducted a total of 1,356 surveys resulting in 12,000+ lizard observations! This project produced massive amounts of data on very short time frames. In general, distribution patterns fell as they were expected to, although some records certainly hint at some mis-identification (e.g. some A. cristatellus locations). Unsurprisingly, the least abundant lizards were those that were hardest to detect: the species typically found high in trees.
While the resulting dataset is impressively large, James admits that there are data quality issues with collecting data in this manner and asked for input on how to improve data collection. Specifically, he suggested that in the future they would like to incorporate photographic and smartphone GPS information, perhaps via an app. Does anyone have any suggestions for James on implementing such an app or otherwise improving the design?
James emphasized that providing meaningful natural experiences with wildlife for kids is good for conservation, fosters an appreciation for nature and helps inspire the next generation of scientists. Many of our readers may find inspiration from the success of this program and we would love to hear about it if you implement similar types of citizen science projects with anoles!
The brown anole (Anolis sagrei) was discovered in Santzepu, Chiayi County, southwestern Taiwan, in mid 2000, and except for a few academics, most people didn’t seem to notice the existence of this exotic invasive species. That all changed when red fire ants (Solenopsis invicta) were discovered in northern parts of the island in 2003. Suddenly, invasive species became a very hot topic, and the authorities launched various projects to assess and study invasive species in Taiwan. Soon, as could be expected, A. sagrei was also in the news.
