Old pythons stay fit; effects of haematozoan infections on life history traits of a large tropical predator

We document the impact of blood parasite infections caused by Hepatozoon sp. on water python (Liasis fuscus) life history traits such as growth rates, condition, reproductive output and survival. Individual snakes maintained similar among-year parasite loads. Hepatozoon infections affected python growth rate, i.e. snakes suffering from high infection levels exhibited significantly slower growth compared to individuals with low parasite loads. Our results suggest that the parasites also affected the pythons nutritional status (condition), as snakes with low condition scores suffered from higher parasite infection levels than snakes with high scores. Furthermore, our data suggest that parasitaemia may affect female reproductive output, as reproductive female pythons harboured lower parasite loads compared to non-reproductive adult females. High levels of parasite infections also affected juvenile python survival, as recaptured snakes harboured significantly lower parasite loads compared to non-recaptured yearling pythons. In our study area, water python have very few natural predators and, hence, experience low mortality rates and commonly reach an age of >15 years. In contrast to results obtained in other studies, parasite loads in larger/older pythons were lower compared to younger snakes, suggesting that only snakes harbouring lower levels of parasitaemia were able to survive to old age. We suggest that a possible cause for the opposing results regarding parasite prevalence and host age may be due to different levels of extrinsic mortality rates and longevity. Long-lived organisms, such as water pythons, may invest relatively more into crucial self-maintenance functions such as parasite defence, compared to short-lived organisms.     

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

Navigational ability is a critical component of an animal''s 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.     

Reptilian endothermy: a field study of thermoregulation by brooding diamond pythons

Miniature temperature-sensitive radiotransmitters were surgically implanted into free-ranging adult diamond pythons ( Morelia s. spilota ), which are medium-sized boid snakes of south-eastern Australia. Four female pythons oviposited during the study, and constructed incubation mounds. These apparently provided excellent insulation, and the snakes maintained high (approx. 31 C) and relatively constant body temperatures throughout the two-month incubation period. They apparently maintained these temperatures primarily by endogenous heat production (shivering thermogenesis), but also basked briefly on most mornings.
Brooding females maintained a body temperature differential above ambient of about 9C, occasionally up to 13C; their temperatures were significantly higher amd less variable than those of non-brooding females or males. The energetic cost of brooding must be high, but these costs may be outweighed by the benefits of rapid embryonic development and high embryonic survivorship.     

Chronic upper respiratory tract disease of free-ranging desert tortoises (Xerobates agassizii)

Seventeen desert tortoises, Xerobates agassizii, with upper respiratory tract disease were examined; thirteen were euthanatized for necropsy. Four normal control desert tortoises from a clinically healthy population were similarly evaluated. Hemoglobin and phosphorus values were significantly (P less than or equal to 0.05) lower and serum sodium, urea, SGOT, and cholesterol values were significantly higher in ill tortoises compared to controls. No significant differences in concentrations of serum or liver vitamins A and E were found between the two groups. While no significant differences were found for concentrations of lead, copper, cadmium, and selenium, the livers of ill tortoises had higher concentrations of mercury and iron. Lesions were found consistently in the upper respiratory tract (URT) of ill tortoises. In all ill tortoises dense infiltrates of lymphocytes and histiocytes obscured the mucosal epithelium and underlying glands. The mucosal epithelium was variably dysplastic, hyperplastic, and occasionally ulcerated. Electron microscopic studies revealed small (350 to 900 nm), pleomorphic organisms resembling Mycoplasma sp., in close association with the surface epithelium of the URT of ill tortoises. Pasteurella testudinis was cultured from the nasal cavity of all ill tortoises and one of four control tortoises. A Mycoplasma sp. was cultured from the nasal passageways of four ill tortoises and was ultrastructurally similar to the pleomorphic organism present on the mucosa in tissue section.     

Harvest Effects on Blood Pythons in North Sumatra

Wildlife populations exposed to intense harvesting often exhibit shifts in attributes of the commercial offtake (e.g., numbers, body sizes, body condition, sex ratios, size at maturation, reproductive frequency). To look for such changes, we examined >2,500 specimens of field-collected blood pythons (Python brongersmai) brought to 2 processing facilities in North Sumatra over 2 survey periods (1996–1997 and 2014–2015). Over the 18 years between our surveys, approximately 900,000 blood pythons were taken from Indonesia for the commercial trade; North Sumatra accounted for about 35% of that trade volume. Between survey periods, numbers of snakes brought to 1 processing facility decreased and mean body size increased, whereas at the second facility numbers and sizes of snakes remained the same. Overall, the pythons collected in 2015–2016 were thinner-bodied than in 1996–1997, with fewer immature animals and a reduced size at maturation and reproductive frequency among females. Clutch size relative to maternal size decreased also. These temporal shifts in python demographics likely reflect a response to harvesting, although ecosystem changes may have played a role. Compared to other squamate reptiles, blood pythons may be more vulnerable to over-harvesting because most snakes are intensively collected from discrete habitat patches (oil palm plantations), and the species can be targeted by specific hunting methods. To ensure sustainability of the harvest, we recommend minimum and maximum size limits for skins used in the commercial trade, and more intensive monitoring at processing facilities. © 2019 The Wildlife Society.     

Spatial ecology of a threatened python (Morelia spilota imbricata) and the effects of anthropogenic habitat change

Abstract Large predators play important ecological roles, but often are sensitive to habitat changes and thus are early casualties of habitat perturbation. Pythons are among the largest predators in many Australian environments, and hence warrant conservation‐orientated research. Carpet pythons (Morelia spilota imbricata) have declined across much of south‐western Australia presumably because of habitat clearance and degradation. Information on habitat use, home range sizes and movements is needed to plan for the conservation of this important predator. We studied pythons at two study sites (Garden Island and Dryandra Woodland) with markedly different climates, habitat types and disturbance histories. We surgically implanted radio‐transmitters in 91 pythons and tracked them for periods of 1 month to 4 years. Dryandra pythons remained inactive inside tree hollows during cooler months (May–September), whereas some (especially small) pythons on Garden Island continued to move and feed. Overall weekly displacements (mean = 100–150 m) were similar at the two study sites and among sex/age classes, except that reproductive females were sedentary during summer while they were incubating eggs. Home ranges averaged 15–20 ha. Adult male pythons had larger home ranges than adult females at Dryandra, but not at Garden Island. Radio‐tracked snakes at Dryandra exhibited high site fidelity, returning to previously occupied logs after long absences and reusing tree hollows for winter shelter. Many of the logs used by snakes had been felled during plantation establishment >70 years ago, with little subsequent regeneration of source trees. In contrast, Garden Island snakes usually sheltered under dense shrubs. Habitat usage was similar among different sex/age classes of snakes at each site, except that juvenile pythons were more arboreal than adults. Although carpet pythons demonstrate great flexibility in habitat use, certain habitat elements appear critical for the persistence of viable populations. Fire plays a central role in this process, albeit in complex ways. For example, low‐intensity fires reduce the availability of hollow logs on the ground at Dryandra and fail to regenerate shrub thickets required by prey species. Paradoxically, high‐intensity fires stimulate shrub thickets and fell trees creating new logs – but might also threaten overwinter trees. Thus, the impact of disturbances (such as wildfires) on the viability of python populations will be mediated in complex ways by alteration to important microhabitats such as vegetation cover or log availability. At Dryandra, landscape management should include occasional fire events to generate new logs as well as shrub thickets used by prey. Strategic burning may also be required at Garden Island to regenerate some vegetation communities.     

Pythons metabolize prey to fuel the response to feeding

We investigated the energy source fuelling the post-feeding metabolic upregulation (specific dynamic action, SDA) in pythons (Python regius). Our goal was to distinguish between two alternatives: (i) snakes fuel SDA by metabolizing energy depots from their tissues; or (ii) snakes fuel SDA by metabolizing their prey. To characterize the postprandial response of pythons we used transcutaneous ultrasonography to measure organ-size changes and respirometry to record oxygen consumption. To discriminate unequivocally between the two hypotheses, we enriched mice (= prey) with the stable isotope of carbon (13C). For two weeks after feeding we quantified the CO2 exhaled by pythons and determined its isotopic 13C/12C signature. Ultrasonography and respirometry showed typical postprandial responses in pythons. After feeding, the isotope ratio of the exhaled breath changed rapidly to values that characterized enriched mouse tissue, followed by a very slow change towards less enriched values over a period of two weeks after feeding. We conclude that pythons metabolize their prey to fuel SDA. The slowly declining delta13C values indicate that less enriched tissues (bone, cartilage and collagen) from the mouse become available after several days of digestion.     

Antipredator behaviour of invasive geckos in response to chemical cues from snakes

Antipredator behaviours and the ability to appropriately assess predation risk contribute to increased fitness. Predator avoidance can be costly; however, so we expect prey to most strongly avoid predators that pose the greatest risk (i.e., prey should show threat sensitivity). For invasive species, effectively assessing the relative risk posed by predators in the new environment may help them establish in new environments. We examined the antipredator behaviour of introduced Asian house geckos, Hemidactylus frenatus (Schlegel), by determining if they avoided shelters scented with the chemical cues of native predatory snakes (spotted pythons, Antaresia maculosa [Peters]; brown tree snakes, Boiga irregularis [Merrem]; common tree snakes, Dendrelaphis punctulata [Grey]; and carpet pythons, Morelia spilota [Lacépède]). We also tested if Asian house geckos collected from vegetation vs. anthropogenic substrates (buildings) responded differently to the chemical cues of predatory snakes. Asian house geckos did not show a generalised antipredator response, that is, they did not respond to the chemical cues of all snakes in the same way. Asian house geckos avoided the chemical cues of carpet pythons more strongly than those of other snake species, providing some support for the threat‐sensitivity hypothesis. There was no difference in the antipredator behaviour of Asian house geckos collected from buildings vs. natural vegetation, suggesting that individuals that have invaded natural habitats have not changed their antipredator behaviour compared to urban individuals. Overall, we found some evidence indicating Asian house geckos are threat‐sensitive to some Australian predacious snakes.     

Parasite spillover: indirect effects of invasive Burmese pythons

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.     

Genetic diversity of Cryptosporidium spp. in captive reptiles

The genetic diversity of Cryptosporidium in reptiles was analyzed by PCR-restriction fragment length polymorphism and sequence analysis of the small subunit rRNA gene. A total of 123 samples were analyzed, of which 48 snake samples, 24 lizard samples, and 3 tortoise samples were positive for Cryptosporidium: Nine different types of Cryptosporidium were found, including Cryptosporidium serpentis, Cryptosporidium desert monitor genotype, Cryptosporidium muris, Cryptosporidium parvum bovine and mouse genotypes, one C. serpentis-like parasite in a lizard, two new Cryptosporidium spp. in snakes, and one new Cryptosporidium sp. in tortoises. C. serpentis and the desert monitor genotype were the most common parasites and were found in both snakes and lizards, whereas the C. muris and C. parvum parasites detected were probably the result of ingestion of infected rodents. Sequence and biologic characterizations indicated that the desert monitor genotype was Cryptosporidium saurophilum. Two host-adapted C. serpentis genotypes were found in snakes and lizards.     

Does body size influence thermal biology and diet of a python (Morelia spilota imbricata)?

Current theory predicts that larger‐bodied snakes not only consume larger prey (compared with smaller individuals), but may also have a different range of prey available to them due to their thermal biology. It has been argued that smaller individuals, with lower thermal inertia (i.e. faster cooling rates at nightfall when air temperature falls and basking opportunities are limited), may be thermally restricted to foraging and hunting during the day on diurnally active prey, and have reduced capacity to hunt crepuscular and nocturnal prey species. This predictive theory was investigated by way of dietary analysis, assessment of thermal biology and thermoregulation behaviour in an ambush forager, the south‐west carpet python (Morelia spilota imbricata, Pythonidae). Eighty‐seven scats were collected from 34 individual pythons over a 3‐year radiotelemetry monitoring study. As predicted by gape size limitation, larger pythons took larger prey; however, 65% of prey items of small pythons were represented by nocturnally active, small mammals, a larger proportion than present in larger snakes. Several measures of thermal biology (absolute body temperature, thermal differential of body temperature to air temperature, maximum hourly heating and cooling rates) were not strongly affected by python body mass. Additionally, body temperature was only influenced by the behavioural choice of microhabitat selection and was not affected by python body size or position, suggesting that these behavioural choices do not allow smaller pythons to vastly increase their temporal foraging window. By coupling dietary analysis, measures of body temperature and behavioural observations of free‐ranging animals, we conclude that, contrary to theoretical predictions, a small body size does not thermally restrict the temporal window for ambush foraging in M. s. imbricata. An ontogenetic or size‐determined switch from ambush feeding to actively foraging on slower prey would account for the differences in prey taken by these animals. The concept of altered foraging behaviour warrants further investigation in this species.     

Experimentally derived salinity tolerance of hatchling Burmese pythons (Python molurus bivittatus) from the Everglades,Florida (USA)

In a laboratory setting, we tested the ability of 24 non-native, wild-caught hatchling Burmese pythons (Python molurus bivittatus) collected in the Florida Everglades to survive when given water containing salt to drink. After a one-month acclimation period in the laboratory, we grouped snakes into three treatments, giving them access to water that was fresh (salinity of 0, control), brackish (salinity of 10), or full-strength sea water (salinity of 35). Hatchlings survived about one month at the highest marine salinity and about five months at the brackish-water salinity; no control animals perished during the experiment. These results are indicative of a “worst-case scenario”, as in the laboratory we denied access to alternate fresh-water sources that may be accessible in the wild (e.g., through rainfall). Therefore, our results may underestimate the potential of hatchling pythons to persist in saline habitats in the wild. Because of the effect of different salinity regimes on survival, predictions of ultimate geographic expansion by non-native Burmese pythons that consider salt water as barriers to dispersal for pythons may warrant re-evaluation, especially under global climate change and associated sea-level-rise scenarios.     

Can invasive Burmese pythons inhabit temperate regions of the southeastern United States?

Understanding potential for range expansion is critical when evaluating the risk posed by invasive species. Burmese pythons (Python molurus bivittatus) are established in southern Florida and pose a significant threat to native ecosystems. Recent studies indicate that climate suitable for the species P. molurus exists throughout much of the southern United States. We examined survivorship, thermal biology, and behavior of Burmese pythons from South Florida in a semi-natural enclosure in South Carolina, where winters are appreciably cooler than in Florida, but within the predicted region of suitable climate. All pythons acclimated to the enclosure, but most died after failing to seek appropriate refugia during sub-freezing weather. The remaining snakes used refugia but died during an unusually cold period in January 2010. Although all snakes died during the study, most survived extended periods at temperatures below those typical of southern Florida and none exhibited obvious signs of disease. Our study represents a first step in evaluating the results of climate matching models and we address factors that may affect range expansion in this invasive species.     

ZW,XY, and yet ZW: Sex chromosome evolution in snakes even more complicated

Snakes are historically important in the formulation of several central concepts on the evolution of sex chromosomes. For over 50 years, it was believed that all snakes shared the same ZZ/ZW sex chromosomes, which are homomorphic and poorly differentiated in “basal” snakes such as pythons and boas, while heteromorphic and well differentiated in “advanced” (caenophidian) snakes. Recent molecular studies revealed that differentiated sex chromosomes are indeed shared among all families of caenophidian snakes, but that boas and pythons evolved likely independently male heterogamety (XX/XY sex chromosomes). The historical report of heteromorphic ZZ/ZW sex chromosomes in a boid snake was previously regarded as ambiguous. In the current study, we document heteromorphic ZZ/ZW sex chromosomes in a boid snake. A comparative approach suggests that these heteromorphic sex chromosomes evolved very recently and that they are poorly differentiated at the sequence level. Interestingly, two snake lineages with confirmed male heterogamety possess homomorphic sex chromosomes, but heteromorphic sex chromosomes are present in both snake lineages with female heterogamety. We point out that this phenomenon is more common across squamates. The presence of female heterogamety in non‐caenophidian snakes indicates that the evolution of sex chromosomes in this lineage is much more complex than previously thought, making snakes an even better model system for the evolution of sex chromosomes.     

Effects of feeding on luminal pH and morphology of the gastroesophageal junction of snakes

At the gastroesophageal junction, most vertebrates possess a functional lower esophageal sphincter (LES) which may serve to regulate the passage of liquids and food into the stomach and prevent the reflux of gastric contents into the esophagus. Snakes seemingly lack an LES and consume meals large enough to extend anteriorly from the stomach into the esophagus thereby providing the opportunity for the reflux of gastric juices. To explore whether snakes experience or can prevent gastric reflux, we examined post-feeding changes of luminal pH of the distal esophagus and stomach, the fine scale luminal pH profile at the gastroesophageal junction, and the morphology of the gastroesophageal junction for the Burmese python (Python molurus), the African brown house snake (Lamprophis fuliginosus), and the diamondback water snake (Nerodia rhombifer). For each species fasted, there was no distension of the gastroesophageal junction and only modest changes in luminal pH from the distal esophagus into the stomach. Feeding resulted in marked distension and changes in tissue morphology of the gastroesophageal junction. Simultaneously, there was a significant decrease in luminal pH of the distal esophagus for pythons and house snakes, and for all three species a steep gradient in luminal pH decreasing across a 3-cm span from the distal edge of the esophagus into the proximal edge of the stomach. The moderate acidification of the distalmost portion of the esophagus for pythons and house snakes suggests that there is some anterior movement of gastric juices across the gastroesophageal junction. Given that this modest reflux of gastric fluid is localized to the most distal region of the esophagus, snakes are apparently able to prevent and protect against acid reflux in the absence of a functional LES.     

First identification of a ranavirus from green pythons (Chondropython viridis)

Ten juvenile green pythons (Chondropython viridis) died or were euthanized shortly after having been illegally imported into Australia from Indonesia in 1998. Histologic examination of two of the three snakes that died revealed moderately severe chronic ulceration of the nasal mucosa and focal or periacinar degeneration and necrosis of the liver. In addition there was severe necrotizing inflammation of the pharyngeal submucosa accompanied by numerous macrophages, heterophils, and edema. An iridovirus was isolated in culture from several tissues and characterized by immunohistochemistry, electron microscopy, enzyme-linked immunosorbent Assay, polyacrylamide gel electrophoresis, polymerase chain reaction and sequence analysis, restriction endonuclease digestion, and DNA hybridization. This is the first report of a systemic ranavirus infection in any species of snake and is a new member of the genus, Ranavirus.     

<Emphasis Type="Italic">Armillifer</Emphasis>-Infected Snakes Sold at Congolese Bushmeat Markets Represent an Emerging Zoonotic Threat

African pythons (Pythonidae) and large vipers (Bitis spp.) act as definitive hosts for Armillifer armillatus and Armillifer grandis parasites (Crustacea: Pentastomida) in the Congo Basin. Since the proportion of snakes in bushmeat gradually increases, human pentastomiasis is an emerging zoonotic disease. To substantiate the significance of this threat, we surveyed snakes offered for human consumption at bushmeat markets in the Kole district, Democratic Republic of the Congo, for the presence of adult pentastomids. In Bitis vipers (n = 40), Armillifer spp. infestations exhibited an 87.5% prevalence and 6.0 median intensity. Parasite abundance covaried positively with viper length, but not with body mass. In pythons (n = 13), Armillifer spp. exhibited a 92.3% prevalence and 3.5 median intensity. The positive correlations between parasite abundance and python length or mass were statistically nonsignificant. Ninety-one percent of A. grandis were discovered in vipers and 97% of infected vipers hosted A. grandis, whereas 81% of A. armillatus specimens were found in pythons and 63% of infected pythons hosted A. armillatus. Thus, challenging the widespread notion of strict host specificity, we found ‘reversed’ infections and even a case of coinfection. In this study, we also gathered information about the snake consumption habits of different tribal cultures in the area. Infective parasite ova likely transmit to humans directly by consumption of uncooked meat, or indirectly through contaminated hands, kitchen tools or washing water.     

Molecular and morphological description of a Hepatozoon species in reptiles and their ticks in the Northern Territory, Australia

Ticks, representing 3 species of Amblyomma, were collected from the water python (Liasis fuscus) and 3 additional reptile species in the Northern Territory, Australia, and tested for the presence of Hepatozoon sp., the most common blood parasites of snakes. In addition, blood smears were collected from 5 reptiles, including the water python, and examined for the presence of the parasite. Hepatozoon sp. DNA was detected in all tick and reptile species, with 57.7% of tick samples (n = 187) and 35.6% of blood smears (n=35) showing evidence of infection. Phylogenetic analysis of the 18S rRNA gene demonstrated that half of the sequences obtained from positive tick samples matched closest with a Hepatozoon species previously identified in the water python population. The remaining sequences were found to be more closely related to mammalian and amphibian Hepatozoon species. This study confirms that species of Amblyomma harbor DNA of the same Hepatozoon species detected in the water pythons. The detection of an additional genotype suggests the ticks may be exposed to 2 Hepatozoon species, providing further opportunity to study multiple host-vector-parasite relationships.     

Amblyomma marmoreum on tortoises of southern province, Zambia

Reptiles from Southern Province, Zambia were captured and inspected for ticks. Seven of 18 tortoises (Geochelone pardalis) were infested by small numbers of adults and nymphs of Amblyomma marmoreum. Under such circumstances, the tick had little apparent effect on the host. None of the 13 specimens representing four species of snakes examined were infested with ticks.     

Patterns of interspecific variation in the heart rates of embryonic reptiles

New non-invasive technologies allow direct measurement of heart rates (and thus, developmental rates) of embryos. We applied these methods to a diverse array of oviparous reptiles (24 species of lizards, 18 snakes, 11 turtles, 1 crocodilian), to identify general influences on cardiac rates during embryogenesis. Heart rates increased with ambient temperature in all lineages, but (at the same temperature) were faster in lizards and turtles than in snakes and crocodilians. We analysed these data within a phylogenetic framework. Embryonic heart rates were faster in species with smaller adult sizes, smaller egg sizes, and shorter incubation periods. Phylogenetic changes in heart rates were negatively correlated with concurrent changes in adult body mass and residual incubation period among the lizards, snakes (especially within pythons) and crocodilians. The total number of embryonic heart beats between oviposition and hatching was lower in squamates than in turtles or the crocodilian. Within squamates, embryonic iguanians and gekkonids required more heartbeats to complete development than did embryos of the other squamate families that we tested. These differences plausibly reflect phylogenetic divergence in the proportion of embryogenesis completed before versus after laying.