Liasis Fuscus Research Articles

Short and chubby or long and slim? Food intake, growth and body condition in free-ranging pythons

Abstract An animal's sex and body size can influence not only its rate of food consumption, but also the way in which it allocates the resultant energy among the competing demands of maintenance, growth, reproduction and storage. A 13-year mark–recapture study of pythons (Liasis fuscus) in tropical Australia provides extensive data on these topics. Rates of food intake and growth were highest in small pythons, and decreased more rapidly with body size in males than in females. Allocation to storage (as measured by the snake's mass relative to its body length) showed a more complex pattern. Body condition was high at hatching, but dropped rapidly as energy was allocated to growth rather than storage. Condition then increased through juvenile life, was at a maximum close to maturation, and was higher in females than in conspecific males. Body condition thereafter decreased with increasing body length. These allocation ‘decisions’ reflect the relative advantages of growth versus energy storage at different body sizes. Hatchling snakes grow rapidly (and hence become thin) because greater body size enables the snake to ingest larger prey items. Adult females amass larger energy reserves than males, because they need reserves to produce the clutch. Large snakes become thinner because their feeding rates are low, and they cannot compensate with increased prey size because large-bodied mammalian prey are rare in our study area.

The first record of Dracunculus mulbus (Nematoda: Dracunculidae) in the Papuan olive python Apodora papuana (Ophidia: Boidae)

Abstract A male specimen of Dracunculus (Nematoda: Dracunculidae), collected in 1973 from the lung of the Papuan olive python Apodora papuana (Peters et Doria) and now deposited in the helminthological collection of the Natural History Museum in London, is identified as Dracunculus mulbus Jones et Mulder, 2007, a species recently described from the water python Liasis fuscus Peters in northern Australia. Apodora papuana is a new host record for D. mulbus and Papua New Guinea is apparently a new geographical record.

Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet–dry tropics

In the wet-dry tropics of northern Australia, temperatures are high and stable year-round but monsoonal rainfall is highly seasonal and variable both annually and spatially. Many features of reproduction in vertebrates of this region may be adaptations to dealing with this unpredictable variation in precipitation, notably by (i) using direct proximate (rainfall-affected) cues to synchronize the timing and extent of breeding with rainfall events, (ii) placing the eggs or offspring in conditions where they will be buffered from rainfall extremes, and (iii) evolving developmental plasticity, such that the timing and trajectory of embryonic differentiation flexibly respond to local conditions. For example, organisms as diverse as snakes (Liasis fuscus, Acrochordus arafurae), crocodiles (Crocodylus porosus), birds (Anseranas semipalmata) and wallabies (Macropus agilis) show extreme annual variation in reproductive rates, linked to stochastic variation in wet season rainfall. The seasonal timing of initiation and cessation of breeding in snakes (Tropidonophis mairii) and rats (Rattus colletti) also varies among years, depending upon precipitation. An alternative adaptive route is to buffer the effects of rainfall variability on offspring by parental care (including viviparity) or by judicious selection of nest sites in oviparous taxa without parental care. A third type of adaptive response involves flexible embryonic responses (including embryonic diapause, facultative hatching and temperature-dependent sex determination) to incubation conditions, as seen in squamates, crocodilians and turtles. Such flexibility fine-tunes developmental rates and trajectories to conditions--especially, rainfall patterns--that are not predictable at the time of oviposition.

MOLECULAR CHARACTERIZATION OF THE 18S rDNA GENE OF AN AVIAN HEPATOZOON REVEALS THAT IT IS CLOSELY RELATED TO LANKESTERELLA

As a part of intensive study of blood parasite infections in a population of the passerine bird blue tit (Cyanistes caeruleus, Paridae), we detected a parasite species that, based on its morphological similarity, was tentatively identified as Hepatozoon parus, the only species of this parasite genus described from birds of this family. However, morphological measurements show that H. parus is slightly larger than the parasite detected in our population. A molecular characterization of the parasite species was conducted by amplification of the 18S rDNA gene, using primers that were reported previously to amplify in Hepatozoon sp. of water pythons. Additional primers were developed based on the new sequence obtained. The 1,484-bp fragment amplified reveals that the parasite from our bird population is more closely related to Lankesterella minima than to Hepatozoon species from other vertebrates according to analysis using the BLAST comparison method (93% identity). In addition, phylogenetic analyses using parsimony and Kimura procedures unequivocally related the parasite species detected by PCR with L. minima. The bootstrap values obtained were 97% and 100%, respectively. These results imply that this parasite is a species of a lankesterellid instead of Hepatozoon.

MHC class I variation associates with parasite resistance and longevity in tropical pythons

Using restriction fragment length polymorphism (RFLP) we identified 26 unique major histocompatibility complex (MHC) genotypes in 104 water pythons. We observed a significant independent association between reduced blood parasite load (Hepatozoon sp.) and python body length/age, presence of a specific RFLP fragment (C-fragment) and the overall number of fragments. The parasite has a negative impact on several python life-history traits such as growth, nutritional status and longevity. Thus, the C-fragment could be considered a 'good gene' (a fitness-enhancing genetic element). However, while the number of fragments affected parasite load, the association between level of parasitaemia and fragment number was not linear, and, hence, minimum parasite infection level was achieved at an intermediate number of fragments. Intermediate MHC fragment numbers were also observed among the largest/oldest pythons, suggesting that both a specific fragment and intermediate levels of MHC polymorphism enhanced python longevity. Thus, our results suggest python MHC is subject to both frequency-dependent and balancing selection.

Dracunculus mulbus n. sp. (Nematoda: Spirurida) from the water python Liasis fuscus (Serpentes: Boidae) in northern Australia

A new species of Dracunculus Reichard, 1759 (Nematoda: Spirurida) is described from the tissues surrounding organs in the body-cavity of the water python Liasis fuscus Peters in northern Australia. One to 14 worms were recovered from 22% (27/120) of pythons examined. Males were located principally around the lungs, liver and heart of the hosts, and females were recovered from peritoneal tissue surrounding the intestines and lining the body-cavity. This species differs from previously described species of Dracunculus in the position of the papillae at the posterior end in males, and in the possession of thick, narrow caudal alae. Submedian cephalic papillae are single in both sexes. Dorsal and ventral anterior cephalic papillae are absent in males. This is the first report of a species of Dracunculus from the Australian region.

Do “infectious” prey select for high levels of natural antibodies in tropical pythons?

Natural antibodies (NAbs) constitute an important component in vertebrate immune system, but, in spite of this, have often been dismissed as “non-specific background” signals. We observed a significant positive relationship between water python (Liasis fuscus) body length/age and levels of antibodies reactive with two administered antigens (tetanus and diphtheria). However, no humoral immune response to the antigens was observed. The lack of elevated immune response, and the age-associated increase in antibody titres, strongly suggest that the antibodies consisted of polyreactive NAbs, and that absence of an elevated immune response was caused by such high levels of NAbs that they were able to mask the epitopes of the antigens. In our study area pythons feed mainly on rodents that frequently, before being killed, are able to inflict numerous bites to the snakes. The bites most likely transmit pathogens such as bacteria. As NAbs have been shown to act as a first line defence against bacterial infections, the high levels of NAbs in the pythons may be an adaptation to reduce pathogenic effects of bacteria transmitted by the prey when the snakes are feeding. Thus, the results from present study suggest that NAbs may have an important immunological function by reducing deleterious effects of pathogens in wild populations.

Rain, rats and pythons: Climate‐driven population dynamics of predators and prey in tropical Australia

Abstract: All natural populations fluctuate in abundance and age structure through time; understanding why they do so is a critical step towards their effective management and conservation. However, the long‐term data sets needed for such an understanding are rarely available, especially for tropical organisms. A 17‐year capture‐mark–recapture study yielded detailed information on the demography of water pythons (Liasis fuscus) and their main prey, the dusky rat (Rattus colletti), on the Adelaide River flood plain in tropical Australia. The link between annual rainfall patterns and rat demography was highly non‐linear. Rat numbers were low during years with low and high rainfall at the end of the wet season (April). Numbers of both predators and prey fluctuated considerably among years. Annual fluctuations in rat numbers generated a corresponding variation in rates of female python reproduction, python body condition and survival. Although variation in recruitment, survival and prey abundance all had a significant impact on annual fluctuations in python numbers, our analyses suggest that recruitment constituted the main determinant in driving the population dynamics of these large tropical predators. In combination with our other studies on this system, the data show that population dynamics of the water python population is ultimately driven by annual variation in rainfall, mediated via shifts in prey availability. The water pythons and the dusky rats of the Adelaide River flood plain thus demonstrate an unusually clear and direct link between an abiotic factor (rainfall) and predator–prey population dynamics.

Dioctowittus Hughjonesi SP. N. (Nematoda: Cystoopsidae) from Liasis Fuscus (Peters, 1873)(Serpentes: Boidae) from the Northern Territory and Morelia Amethistina (Schneider, 1802) from Queensland, Australia

SummaryMulder, E. and Smales, L. R. Dioctowittus hughjonesi sp n. (Nematoda: Cystoopsidae) is described from the peritoneal cavity of Liasis fuscus (Peters, 1873) from the Adelaide River floodplain, Northern Territory and from Morelia amethistina (Schneider, 1801) from Cape York Peninsula, Queensland. Dioctowittus hughjonesi is distinguished from others members of the genus by the presence of lateral lobes at both anterior and posterior ends, size of worms, size of eggs and presence of paired ventral papillae in males. The genus Dioctowittus is found only in tropical regions with high seasonal rainfall. A possible link in the life cycle between aquatic intermediate hosts and the presence of polar filaments in the egg remains problematic, requiring further study.

Age, parasites, and condition affect humoral immune response in tropical pythons

Mounting an immune response has been suggested to be physiologically costly because of metabolic requirements of immune cells specifically and upregulation of the immune system in general. We investigated such costs in free-living water pythons (Liasis fuscus), immunized with a harmless antigen, keyhole limpet hemocyanin. In the present study, we analyze the independent effects of age, blood parasite load, and body condition on the ability to mount a humoral immune response (level of antibody production to novel antigens). Python humoral immune response decreased with increasing body length/age, decreased with increasing blood parasite load, and decreased with declining body condition. The results suggest an energetic trade-off between immunocompetence and other energetically costly processes.

Snakes don't shrink, but ‘shrinkage’ is an almost inevitable outcome of measurement error by the experimenters

The recent report of Galapagos marine iguanas showing bidirectional growth, i.e. decreasing in body size up to 20% of their initial size during periods of reduced food availability, has induced to speculate whether these ‘shrinkages’ are adaptive or not, and whether they are widespread or not in squamate reptiles living in seasonally variable environments. A first case‐test with Australian water pythons provided no evidence of ‘shrinkage’. I tested the same issue by using my mark‐recapture data of a species‐rich community of snakes (16 species) from the tropical forests of southern Nigeria, where the food availability varies seasonally (with productivity peaks during the wet months). I attributed a ‘measurability’ score to each species in relation to the easiness of their handling, taking into consideration a range of factors including the snake's body size and weight (hence the body vigour, as the large vigorous snakes are more difficult to measure correctly than small non‐vigorous species), the temperament (aggressive species are more difficult to measure correctly than placid species), and the dangerousness (highly venomous snakes are more difficult to measure correctly than non‐venomous species). Out of 6431 recapture data, 2.8% were cases of shrinkage, and 14 out of 16 species examined had at least a single case of shrinkage (the percentage of shrinkage cases was not significantly different among terrestrial, semi‐aquatic and arboreal species). The percentage of shrinkage cases varied significantly in relation to the ‘measurability’ score of the single species (producing an exponential growth curve for the relationship between the two variables). The mean SVL reduction at the second capture event compared to the first (in percent terms) was trivial compared to shrinkage data for marine iguanas, but in very good agreement with data from water pythons. Both the frequency of occurrence of shrinkage events and the percent of decrease in SVL did not differ inter‐seasonally. Hence, I conclude that shrinkage events are just apparent in snakes and are caused by measurement errors by experimenters. I also predict that future studies may observe (apparent) shrinkage events more frequently among very large and/or very dangerous species (i.e. large boas and pythons, cobras, mambas, huge vipers), and that the frequency of shrinkage cases will not be higher than 6–7% of the total recapture events.

Paternal alleles enhance female reproductive success in tropical pythons

The conventional view that female reproductive success is unlikely to benefit from multiple mating has come under strong challenge in recent years. In the present study, we demonstrate that the time wild-caught reproductive female water pythons (Liasis fuscus) spent in the laboratory prior to oviposition affected both hatching success and the number of male microsatellite alleles detected in the broods. A negative correlation between time in captivity and number of male alleles observed in the broods suggests that reduced hatching success was most likely not caused by environmental factors such as non-optimal temperatures, but rather by restricted mating opportunities. Maternal nutritional status and mean hatchling mass did not affect brood viability. However, our results revealed a positive correlation between number of male microsatellite alleles observed in the broods and hatching success, suggesting that increased paternal genetic variability enhanced female reproductive success. As microsatellite loci are unlikely to be direct targets of selection, we suggest that variability at these loci may cosegregate with other polymorphic genes directly linked to fitness.

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.

High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia.

Molecular methods were used to identify blood parasites frequently observed in blood smears of water pythons (Liasis fuscus) captured in our study area in the Northern Territory of Australia. A nested polymerase chain reaction (PCR) using primers amplifying the 18s ribosomal RNA (rRNA) nuclear gene resulted in a short PCR product (180 bp) matching this region in the genus Hepatozoon. However, because of the short sequence obtained. 2 new primers were designed based on 18s rRNA sequences of 3 Hepatozoon taxa available in GenBank. Using these primers, approximately 600 bp of the parasite's 18s rRNA gene was amplified successfully and sequenced from 2 water python samples. The new primers were used to investigate the prevalence of blood parasites in 100 pythons. In 25 of these samples we did not observe any blood parasites when examining stained slides. All the samples revealed a 600-bp PCR product, demonstrating that pythons in which we did not visually observe any parasites were infected by Hepatozoon spp. We also analyzed the nucleotide sequences of blood parasites in 4 other reptile taxa commonly encountered in our study area. The sequences obtained from water pythons and from 1 of these taxa were identical, suggesting that the parasite is capable of infecting hosts at different taxonomic levels.

Phylogenetic relationships of the Australo-Papuan Liasis pythons (Reptilia : Macrostomata), based on mitochondrial DNA

The genus Liasis comprises two groups of pythons, the olive python, Liasis olivaceus, and the water pythons L. fuscus and L. mackloti. We used partial mitochondrial control region DNA sequences to examine (a) the phylogeography of water pythons from five Indonesian Lesser Sunda islands, New Guinea, and northern Australia, (b) the relationships of the two subspecies of olive pythons, and (c) the relationship of the Papuan python, Apodora papuana, with the species of Liasis. Maximum likelihood, parsimony and distance analyses showed that A. papuana is the sister lineage to all Liasis and that Liasis fuscus/L. mackloti and L. olivaceus are separate lineages. There is also support for the reciprocal monophyly of the two olive python subspecies, L. olivaceus barroni and L. o. olivaceus, and for distinction of island populations described previously as L. mackloti dunni from Wetar and L. mackloti savuensis from Sawu. These two island populations are as equally distinct as the populations from the island cluster of Babar/Semau/Timor. There is strong support for the recognition of two lineages ('eastern' and 'western') of water pythons in Australia. We propose that the drier interior of the Plio-Pleistocene land bridge between Australia and New Guinea acted as a barrier to gene flow, influencing the genetic divergence between the 'eastern' and 'western' lineages of the semi-aquatic water pythons.

Distribution of lipids from the yolk to the tissues during development of the water python (Liasis fuscus).

Energy metabolism during embryonic development of snakes differs in several respects from the patterns displayed by other reptiles. There are, however, no previous reports describing the main energy source for development, the yolk lipids, in snake eggs. There is also no information on the distribution of yolk fatty acids to the tissues during snake development. In eggs of the water python ( Liasis fuscus), we report that triacylglycerol, phospholipid, cholesteryl ester and free cholesterol, respectively, form 70.3%, 14.1%, 5.7% and 2.1% of the total lipid. The main polyunsaturate of the yolk lipid classes is 18:2n-6. The yolk phospholipid contains 20:4n-6 and 22:6n-3 at 13.0% and 3.6% (w/w), respectively. Approximately 10% and 30% of the initial egg lipids are respectively recovered in the residual yolk and the fat body of the hatchling. A major function of yolk lipid is, therefore, to provision the neonate with large energy reserves. The proportion of 22:6n-3 in brain phospholipid of the hatchling is 11.1% (w/w): this represents only 0.24% of the amount of 22:6n-3 originally present in the egg. This also contrasts with values for free-living avian species where the proportion of DHA in neonatal brain phospholipid is 16-19%. In the liver of the newly hatched python, triacylglycerol, phospholipid and cholesteryl ester, respectively, form 68.2%, 7.7% and 14.3% of total lipid. This contrasts with embryos of birds where cholesteryl ester forms up to 80% of total liver lipid and suggests that the mechanism of lipid transfer in the water python embryo differs in some respects from the avian situation.

Epidermal differentiation during ontogeny and after hatching in the snake Liasis fuscus (Pythonidae, Serpentes, Reptilia), with emphasis on the formation of the shedding complex.

Differentiation and localization of keratin in the epidermis during embryonic development and up to 3 months posthatching in the Australian water python, Liasis fuscus, was studied by ultrastructural and immunocytochemical methods. Scales arise from dome-like folds in the skin that produce tightly imbricating scales. The dermis of these scales is completely differentiated before any epidermal differentiation begins, with a loose dermis made of mesenchymal cells beneath the differentiating outer scale surface. At this stage (33) the embryo is still unpigmented and two layers of suprabasal cells contain abundant glycogen. At Stage 34 (beginning of pigmentation) the first layers of cells beneath the bilayered periderm (presumptive clear and oberhautchen layers) have not yet formed a shedding complex, within which prehatching shedding takes place. At Stage 35 the shedding complex, consisting of the clear and oberhautchen layers, is discernible. The clear layer contains a fine fibrous network that faces the underlying oberhautchen, where the spinulae initially contain a core of fibrous material and small beta-keratin packets. Differentiation continues at Stage 36 when the beta-layer forms and beta-keratin packets are deposited both on the fibrous core of the oberhautchen and within beta-cells. Mesos cells are produced from the germinal layer but remain undifferentiated. At Stage 37, before hatching, the beta-layer is compact, the mesos layer contains mesos granules, and cells of the alpha-layer are present but are not yet keratinized. They are still only partially differentiated a few hours after hatching, when a new shedding complex is forming underneath. Using antibodies against chick scale beta-keratin resolved at high magnification with immunofluorescent or immunogold conjugates, we offer the first molecular confirmation that in snakes only the oberhautchen component of the shedding complex and the underlying beta cells contain beta-keratin. Initially, there is little immunoreactivity in the small beta-packets of the oberhautchen, but it increases after fusion with the underlying cells to produce the syncytial beta layer. The beta-keratin packets coalesce with the tonofilaments, including those attached to desmosomes, which rapidly disappear in both oberhautchen and beta-cells as differentiation progresses. The labeling is low to absent in forming mesos-cells beneath the beta-layer. This study further supports the hypothesis that the shedding complex in lepidosaurian reptiles evolved after there was a segregation between alpha-keratogenic cells from beta-keratogenic cells during epidermal renewal.

Short and chubby or long and slim? Food intake, growth and body condition in free‐ranging pythons

Abstract An animal's sex and body size can influence not only its rate of food consumption, but also the way in which it allocates the resultant energy among the competing demands of maintenance, growth, reproduction and storage. A 13‐year mark–recapture study of pythons (Liasis fuscus) in tropical Australia provides extensive data on these topics. Rates of food intake and growth were highest in small pythons, and decreased more rapidly with body size in males than in females. Allocation to storage (as measured by the snake's mass relative to its body length) showed a more complex pattern. Body condition was high at hatching, but dropped rapidly as energy was allocated to growth rather than storage. Condition then increased through juvenile life, was at a maximum close to maturation, and was higher in females than in conspecific males. Body condition thereafter decreased with increasing body length. These allocation ‘decisions’ reflect the relative advantages of growth versus energy storage at different body sizes. Hatchling snakes grow rapidly (and hence become thin) because greater body size enables the snake to ingest larger prey items. Adult females amass larger energy reserves than males, because they need reserves to produce the clutch. Large snakes become thinner because their feeding rates are low, and they cannot compensate with increased prey size because large‐bodied mammalian prey are rare in our study area.

Influence of weather conditions on activity of tropical snakes

Abstract There are many anecdotal reports of massive day‐to‐day variation in activity levels of tropical reptiles and amphibians, and intuition suggests that weather conditions may be responsible for much of that variation. Our analysis of a large data set on the activity levels of tropical snakes and frogs confirms the existence of this short‐term variation in activity levels, reveals strong synchrony between sympatric taxa in this respect, but also shows that standard weather variables (temperature, humidity, precipitation, moonlight, atmospheric pressure) are surprisingly poor at predicting the numbers of individuals and species encountered during standardized surveys. We recorded the numbers of snakes and prey taxa (frogs) encountered on 349 nights over the course of one year on a 1.3‐km transect in the Adelaide River floodplain, in the wet–dry tropics of Australia. Frogs, water pythons (Liasis fuscus), slatey‐grey snakes (Stegonotus cucullatus) and keelbacks (Tropidonophis mairii) all showed strongly seasonal patterns of activity. After adjusting for seasonal differences, encounter rates were related to climatic conditions but different taxa responded to different weather variables. Water python activity was related to amount of moonlight, keelback activity was related to temperature, and frog activity was related to relative humidity, rainfall, temperature and moonlight. However, weather variables explained relatively little of the variation in activity levels. Strong synchrony was evident among encounter rates with various taxa (independent of season and weather conditions), suggesting that activity levels may be determined by other unmeasured factors.

Responses of three sympatric snake species to tropical seasonality in northern Australia

In the Australian wet–dry tropics, temperatures are high year-round but rainfall is concentrated in a 4-mo wet season. Regular nightly surveys in the Fogg Dam Nature Reserve provided data on temporal (monthly, seasonal) variation in biological attributes of three snake species: water pythons (Liasis fuscus, Pythonidae), keelbacks (Tropidonophis mairii, Colubridae) and slatey-grey snakes (Stegonotus cucullatus, Colubridae). Adults of all three taxa were encountered more frequently during the dry season than the wet season, whereas juveniles were more commonly encountered in the wet season. The sex ratio among adult snakes also shifted seasonally, but in different ways in different species. These sex-ratio shifts probably reflect reproductive activity (mate-searching by males, oviposition migrations by females) and were accompanied by increased encounter rates. Feeding rates and body condition of keelbacks (a frog specialist) were highest during the wet season when frogs were most abundant. Rats migrated away from Fogg Dam during the wet season, and most pythons (rat specialists) left this area to follow their prey. The pythons that remained at Fogg Dam exhibited low feeding rates and poor body condition. Slatey-grey snakes (a generalist predator) showed less seasonal variation in feeding rates or body condition. Our data show that tropical seasonality induces strong fluctuations in many attributes of snake populations, and that patterns of response differ both among and within species.