Ray W. Snow

Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park

Invasive species represent a significant threat to global biodiversity and a substantial economic burden. Burmese pythons, giant constricting snakes native to Asia, now are found throughout much of southern Florida, including all of Everglades National Park (ENP). Pythons have increased dramatically in both abundance and geographic range since 2000 and consume a wide variety of mammals and birds. Here we report severe apparent declines in mammal populations that coincide temporally and spatially with the proliferation of pythons in ENP. Before 2000, mammals were encountered frequently during nocturnal road surveys within ENP. In contrast, road surveys totaling 56,971 km from 2003–2011 documented a 99.3% decrease in the frequency of raccoon observations, decreases of 98.9% and 87.5% for opossum and bobcat observations, respectively, and failed to detect rabbits. Road surveys also revealed that these species are more common in areas where pythons have been discovered only recently and are most abundant outside the pythons current introduced range. These findings suggest that predation by pythons has resulted in dramatic declines in mammals within ENP and that introduced apex predators, such as giant constrictors, can exert significant top-down pressure on prey populations. Severe declines in easily observed and/or common mammals, such as raccoons and bobcats, bode poorly for species of conservation concern, which often are more difficult to sample and occur at lower densities.

BIRDS CONSUMED BY THE INVASIVE BURMESE PYTHON (PYTHON MOLURUS BIVITTATUS) IN EVERGLADES NATIONAL PARK, FLORIDA, USA

Abstract We identified 25 species of birds representing nine avian Orders from remains in digestive tracts of 85 Burmese pythons (Python molurus bivittatus) collected in Everglades National Park, Florida, USA, from 2003 to 2008. Four species of birds identified in this study are of special concern in Florida and a fifth, the Wood Stork (Mycteria americana), is listed as federally endangered. This represents the first detailed analysis of the avian component of the diet of the introduced Burmese python, now established in Everglades National Park, Florida and highlights the potential for considerable negative impact of this invasive species on native bird populations.

A field test of attractant traps for invasive Burmese pythons (Python molurus bivittatus) in southern Florida

Context. Invasive Burmese pythons (Python molurus bivittatus) are established over thousands of square kilometres of southern Florida, USA, and consume a wide range of native vertebrates. Few tools are available to control the python population, and none of the available tools have been validated in the field to assess capture success as a proportion of pythons available to be captured. Aims. Our primary aim was to conduct a trap trial for capturing invasive pythons in an area east of Everglades National Park,wheremanypythonshadbeencapturedinpreviousyears,toassesstheefficacyoftrapsforpopulationcontrol.Wealso aimed to compare results of visual surveys with trap capture rates, to determine capture rates of non-target species, and to assess capture rates as a proportion of resident pythons in the study area. Methods.Weconductedamedium-scale(6053trapnights)experimentusingtwotypesofattractanttrapsbaitedwithlive ratsintheFrogPondareaeastofEvergladesNationalPark.Wealsoconductedstandardisedandopportunisticvisualsurveys inthetrappingarea.Followingthetrap trial,theareawasdischarrowedtoexposepythonsandallowcalculationof anindex of the number of resident pythons. Key results. We captured three pythons and 69 individuals of various rodent, amphibian, and reptile species in traps. Eleven pythons were discovered during disc harrowing operations, as were large numbers of rodents. Conclusions. The trap trial captured a relatively small proportion of the pythons that appeared to be present in the study area, although previous research suggests that trap capture rates improve with additional testing of alternative trap designs. Potential negative impacts to non-target species were minimal. Low python capture rates may have been associated with extremely high local prey abundances during the trap experiment. Implications. Results of this trial illustrate many of the challenges in implementing and interpreting results from tests of control tools for large cryptic predators such as Burmese pythons.

Homing of invasive Burmese pythons in South Florida: evidence for map and compass senses in snakes

Navigational ability is a critical component of an animals spatial ecology and may influence the invasive potential of species. Burmese pythons (Python molurus bivittatus) are apex predators invasive to South Florida. We tracked the movements of 12 adult Burmese pythons in Everglades National Park, six of which were translocated 21–36 km from their capture locations. Translocated snakes oriented movement homeward relative to the capture location, and five of six snakes returned to within 5 km of the original capture location. Translocated snakes moved straighter and faster than control snakes and displayed movement path structure indicative of oriented movement. This study provides evidence that Burmese pythons have navigational map and compass senses and has implications for predictions of spatial spread and impacts as well as our understanding of reptile cognitive abilities.

Reproduction of the Burmese python (Python molurus bivittatus) in southern Florida

Kenneth L. Krysko1,5, James C. Nifong1, Ray W. Snow2, Kevin M. Enge3, Frank J. Mazzotti4 1 Florida Museum of Natural History, Division of Herpetology, University of Florida, Gainesville, Florida 32611, USA 2 Everglades National Park, 40001 State Road 9336, Homestead, Florida 33034, USA 3 Florida Fish and Wildlife Conservation Commission, 4005 South Main Street, Gainesville, Florida 32601, USA 4 Department of Wildlife Ecology and Conservation, University of Florida, Fort Lauderdale Research and Education Center, 3205 College Avenue, Davie, Florida 33314, USA 5 Corresponding author; e-mail: kenneyk@flmnh.ufl.edu

Thermoregulation by a brooding Burmese Python (Python molurus bivittatus) in Florida.

Abstract We report an observation of shivering thermogenesis and insulation by a brooding Python molurus bivittatus (Burmese Python) just outside the northern boundary of Everglades National Park, FL. Temperature data loggers were placed in and around the brooding females nest, and video was taken of the female performing shivering thermogenesis. Nest temperatures were maintained both warmer and cooler than ambient temperatures. This observation of thermoregulation through shivering thermogenesis and clutch insulation is the first documented instance of a Burmese Python exhibiting this behavior in the wild.

Parasite spillover: indirect effects of invasive Burmese pythons

Abstract Identification of the origin of parasites of nonindigenous species (NIS) can be complex. NIS may introduce parasites from their native range and acquire parasites from within their invaded range. Determination of whether parasites are non‐native or native can be complicated when parasite genera occur within both the NIS’ native range and its introduced range. We explored potential for spillover and spillback of lung parasites infecting Burmese pythons (Python bivittatus) in their invasive range (Florida). We collected 498 indigenous snakes of 26 species and 805 Burmese pythons during 2004–2016 and examined them for lung parasites. We used morphology to identify three genera of pentastome parasites, Raillietiella, a cosmopolitan form, and Porocephalus and Kiricephalus, both New World forms. We sequenced these parasites at one mitochondrial and one nuclear locus and showed that each genus is represented by a single species, R. orientalis, P. crotali, and K. coarctatus. Pythons are host to R. orientalis and P. crotali, but not K. coarctatus; native snakes are host to all three species. Sequence data show that pythons introduced R. orientalis to North America, where this parasite now infects native snakes. Additionally, our data suggest that pythons are competent hosts to P. crotali, a widespread parasite native to North and South America that was previously hypothesized to infect only viperid snakes. Our results indicate invasive Burmese pythons have affected parasite‐host dynamics of native snakes in ways that are consistent with parasite spillover and demonstrate the potential for indirect effects during invasions. Additionally, we show that pythons have acquired a parasite native to their introduced range, which is the initial condition necessary for parasite spillback.

Cytonuclear discordance in the Florida Everglades invasive Burmese python (Python bivittatus) population reveals possible hybridization with the Indian python (P. molurus)

Abstract The invasive Burmese python (Python bivittatus) has been reproducing in the Florida Everglades since the 1980s. These giant constrictor snakes have caused a precipitous decline in small mammal populations in southern Florida following escapes or releases from the commercial pet trade. To better understand the invasion pathway and genetic composition of the population, two mitochondrial (mtDNA) loci across 1,398 base pairs were sequenced on 426 snakes and 22 microsatellites were assessed on 389 snakes. Concatenated mtDNA sequences produced six haplotypes with an average nucleotide and haplotype diversity of π = 0.002 and h = 0.097, respectively. Samples collected in Florida from morphologically identified P. bivittatus snakes were similar to published cytochrome oxidase 1 and cytochrome b sequences from both P. bivittatus and Python molurus and were highly divergent (genetic distances of 5.4% and 4.3%, respectively). The average number of microsatellite alleles and expected heterozygosity were N A = 5.50 and H E = 0.60, respectively. Nuclear Bayesian assignment tests supported two genetically distinct groups and an admixed group, not geographically differentiated. The effective population size (N E = 315.1) was lower than expected for a population this large, but reflected the low genetic diversity overall. The patterns of genetic diversity between mtDNA and microsatellites were disparate, indicating nuclear introgression of separate mtDNA lineages corresponding to cytonuclear discordance. The introgression likely occurred prior to the invasion, but genetic information on the native range and commercial trade is needed for verification. Our finding that the Florida python population is comprised of distinct lineages suggests greater standing variation for adaptation and the potential for broader areas of suitable habitat in the invaded range.

Incubation Temperature and Sex Ratio of a Python bivittatus (Burmese Python) Clutch Hatched in Everglades National Park, Florida

Abstract We describe characteristics of a Python bivittatus (Burmese Python) nest from observations made from December 2008 through August 2009 in Everglades National Park, Homestead, FL. The nest hatched on 28 July with a 77% hatching success. The female lost 54% of her body weight while breeding, laying, and incubating eggs, and abandoned the nest 3 days before eggs began hatching. Egg-mass temperature was 26.29–31.41 °C (mean = 28.07 °C), and was more stable than the temperature in direct sun above the nest, which ranged from 20.81 °C to 45.70 °C (mean = 28.45 °C). Egg-mass temperature was likely buffered from extreme heat by adjacent vegetation, where the temperature ranged from 23.19 °C to 30.48 °C (mean = 27.05 °C) and from extreme cold by shivering thermogenesis. Of successful hatchlings, 9 were male and 8 were female.

A validation of 11 body-condition indices in a giant snake species that exhibits positive allometry

Body condition is a gauge of the energy stores of an animal, and though it has important implications for fitness, survival, competition, and disease, it is difficult to measure directly. Instead, body condition is frequently estimated as a body condition index (BCI) using length and mass measurements. A desirable BCI should accurately reflect true body condition and be unbiased with respect to size (i.e., mean BCI estimates should not change across different length or mass ranges), and choosing the most-appropriate BCI is not straightforward. We evaluated 11 different BCIs in 248 Burmese pythons (Python bivittatus), organisms that, like other snakes, exhibit simple body plans well characterized by length and mass. We found that the length-mass relationship in Burmese pythons is positively allometric, where mass increases rapidly with respect to length, and this allowed us to explore the effects of allometry on BCI verification. We employed three alternative measures of ‘true’ body condition: percent fat, scaled fat, and residual fat. The latter two measures mostly accommodated allometry in true body condition, but percent fat did not. Our inferences of the best-performing BCIs depended heavily on our measure of true body condition, with most BCIs falling into one of two groups. The first group contained most BCIs based on ratios, and these were associated with percent fat and body length (i.e., were biased). The second group contained the scaled mass index and most of the BCIs based on linear regressions, and these were associated with both scaled and residual fat but not body length (i.e., were unbiased). Our results show that potential differences in measures of true body condition should be explored in BCI verification studies, particularly in organisms undergoing allometric growth. Furthermore, the caveats of each BCI and similarities to other BCIs are important to consider when determining which BCI is appropriate for any particular taxon.