Physiological Status Drives Metabolic Rate in Mediterranean Geckos Infected with Pentastomes

Negative effects of parasites on their hosts are well documented, but the proximate mechanisms by which parasites reduce their host’s fitness are poorly understood. For example, it has been suggested that parasites might be energetically demanding. However, a recent meta-analysis suggests that they have statistically insignificant effects on host resting metabolic rate (RMR). It is possible, though, that energetic costs associated with parasites are only manifested during and/or following periods of activity. Here, we measured CO₂ production (a surrogate for metabolism) in Mediterranean geckos (Hemidactylus turcicus) infected with a lung parasite, the pentastome Raillietiella indica, under two physiological conditions: rested and recently active. In rested geckos, there was a negative, but non-significant association between the number of pentastomes (i.e., infection intensity) and CO₂ production. In recently active geckos (chased for 3 minutes), we recorded CO₂ production from its maximum value until it declined to a stationary phase. We analyzed this decline as a 3 phase function (initial decline, secondary decline, stationary). Geckos that were recently active showed, in the secondary phase, a significant decrease in CO₂ production as pentastome intensity increased. Moreover, duration of the secondary phase showed a significant positive association with the number of pentastomes. These results suggest that the intensity of pentastome load exerts a weak effect on the metabolism of resting geckos, but a strong physiological effect on geckos that have recently been active; we speculate this occurs via mechanical constraints on breathing. Our results provide a potential mechanism by which pentastomes can reduce gecko fitness.     

Childhood pentastomiasis: A report of three cases with the following-up data

Pentastomiasis, a zoonotic parasitic disease, has been reported commonly in Africa and Asia. It is caused by pentastomes, which are annulated but unsegmented blood-sucking endoparasites. Fewer than 20 cases have been reported during the past two decades in China, and cases in children have been especially rare. Herein, we report three cases of pediatric patients with severe systemic symptoms, focusing on the clinical features, diagnosis, and therapy of this disease. The patients were two boys and one girl aged 3 to 13 years. They all had a history of snake or worm ingested from snake and initial symptoms of fever, abdominal pain, diarrhea, and weight loss. Eosinophilia, anemia and elevated serum IgE levels were noted. Moreover, the large numbers of nodules, or even calcification, in the liver and/or lungs were noted by ultrasound, CT or MRI scans. These pentastomes were identified as Armillifer moniliformis, Porocephalus taiwana and Armillifer agkistrodontis. Praziquantel and mebendazole deworming treatments were adopted for the patients. Hence, pentastomiasis should be considered in the differential diagnosis for patients with multiple organ or system lesions, especially abdominal signs, that develop after the ingestion of snakes. Ultrasound, CT and MRI scans and laparoscopic approaches might be helpful for the diagnosis.     

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.     

Parasites of prairie rattlesnakes (Crotalus viridis viridis) and gopher snakes (Pituophis melanoleucus sayi) from the eastern high plains of New Mexico

Three prairie rattlesnakes (Crotalus viridis viridis) and two gopher snakes (Pituophis melanoleucus sayi) from the eastern high plains of New Mexico (USA) were examined for parasites. One cestode (Oochoristica osheroffi), and two nematode (Kalicephalus inermis and Physoloptera retusa) species were recovered from two infected rattlesnakes. One female gopher snake was infected with two nematode (K. inermis and Rhabdias spp.) and one mite (Entonyssus halli) species.     

Finding of pentastomes of genus Reighardia (Pentastomida) in the Belcher's gull (Larus belcheri)

This report describes the finding of Reighardia sp. (Pentastomida) infecting the air sac of two Belcher's gulls (Larus belcheri) found dead on the beaches of Pucusana, a district in southern Lima, Peru. Three pentastomes were collected from two Belcher's gulls. Then, they were morphologically and molecular analyzed. Molecular characterization of the parasite was achieved by amplifying a fragment of the small subunit ribosomal RNA gene (SSU rRNA). Based on both morphological and molecular data the pentastomes were identified as pentastomes of the genus Reighardia. This is the first report showing that the Belcher's gull is a new natural definitive host for this pentastome.     

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.     

Prevalence and intensity of pentastomid infection in two species of snakes from northeastern Brazil.

This study aimed to evaluate the infection rates of snakes by pentastomids in the semi-arid region of Brazil. Fifteen snakes (four Micrurus ibiboboca (Merrem, 1820) and eleven Philodryas nattereri Steindachner, 1870) were collected between January and April of 2005, in the municipality of Crato (07 degrees 14' S and 39 degrees 24' W), State of Ceará, Brazil. Laboratorial analysis of the respiratory tracts of the sampled snakes indicated differences in host infection rates: four individuals of P. nattereri (36.4%) were infected by Cephalobaena tetrapoda Heymons, 1922 (mean infection intensity 1.5 +/- 0.28, 1-2) and three specimens (27.3%) by Raillietiella furcocerca (Diesing, 1863) (2.3 +/- 1.32, 1-5). Only one individual of M. ibiboboca (25%) was infected by a non-identified species of Raillietiella sp. These are the first data on pentastomid infection in snakes in Northeastern Brazil and both snake species comprise new host records for the pentastomids. The results also indicate that the generalist parasites C. tetrapoda and R. furcocerca share their definitive hosts.     

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.     

Effects of parasitic infection and radio-transmitters on condition, hematological characteristics and corticosterone concentrations in Texas ratsnakes

Parasites are a health concern of many wildlife species, although their effect on reptiles is poorly studied. Here we examine effects of hemogregarine and external parasites on Texas ratsnake Elaphe obsoleta white blood cell (WBC) concentrations, WBC differentials, heterophil/lymphocyte ratios, packed cell volume (PCV), corticosterone concentrations and body condition. We found little evidence that either ectoparasites or hemogregarines affected the health of Texas ratsnakes. We found a seasonal increase in corticosterone, consistent with glucocorticoids priming the snakes to deal with higher predation risks later in the season. We also examined whether the potential stress of carrying a surgically implanted radio-transmitter compounds any parasitic health effects. We found no effect of transmitters on most aspects of health. We did find equivocal evidence that WBC concentrations were higher in snakes with transmitters and that PCV decreased following transmitter implantation. Although our results generally support the view that data collected using radio-telemetry are unlikely to be biased due to adverse health effects of transmitters, the growing importance of telemetry for studies of snakes and other taxa argues for further research on this topic. When possible, researchers should design telemetry studies in such a way that assessing potential heath effects of transmitters is one of the objectives.     

Helminth infracommunity structure of the sympatric garter snakes Thamnophis eques and Thamnophis melanogaster from the Mesa Central of Mexico

Seventy-two Mexican garter snakes (Thamnophis eques) and 126 black-bellied garter snakes (T. melanogaster) were collected from 4 localities of the Mesa Central of Mexico between July 1996 and February 1998 and examined for helminths. Both species of garter snakes occurred sympatrically in every locality except in Lake Cuitzeo. Both species of snakes shared 9 helminth species, and in general, T. melanogaster hosted a larger number of species than T. eques. In each locality, a different helminth species showed the highest levels of prevalence and abundance (Spiroxys susanae in Ciénaga de Lerma, Telorchis corti in Lago de Pátzcuaro, Proteocephalus variabilis in Lago de Cuitzeo, and Contracaecum sp. in Lago de Chapala). Helminth communities in garter snakes of the Mesa Central are depauperate and dominated by a single parasite species. In those localities where the snakes occurred in sympatry, helminth communities were, in general, more diverse and species-rich in T. melanogaster. Differences in the ecology and physiology of these species of garter snakes may explain this pattern because black-bellied garter snakes (T. melanogaster) are more aquatic than Mexican garter snakes (T. eques) and primarily eat aquatic prey, potentially exposing themselves to a larger number of helminths transmitted by predator-prey infection. The helminth infracommunities of garter snakes in the Mesa Central of Mexico show a strong Nearctic influence because most of the species infecting these hosts have been recorded in other Nearctic colubrid snakes. However, the helminth infracommunities of these garter snakes are less species-rich and less diverse than those in colubrid snakes in more temperate latitudes. The widespread ecological perturbation of sampling sites in the Mesa Central because of human activity, and geographic differences in foraging ecology of the hosts and, thus, exposure to parasites transmitted by intermediate hosts may help to explain these patterns.     

Geography-Dependent Horizontal Gene Transfer from Vertebrate Predators to Their Prey

Horizontal transfer (HT) of genes between multicellular animals, once thought to be extremely rare, is being more commonly detected, but its global geographic trend and transfer mechanism have not been investigated. We discovered a unique HT pattern of Bovine-B (BovB) LINE retrotransposons in vertebrates, with a bizarre transfer direction from predators (snakes) to their prey (frogs). At least 54 instances of BovB HT were detected, which we estimate to have occurred across time between 85 and 1.3 Ma. Using comprehensive transcontinental sampling, our study demonstrates that BovB HT is highly prevalent in one geographical region, Madagascar, suggesting important regional differences in the occurrence of HTs. We discovered parasite vectors that may plausibly transmit BovB and found that the proportion of BovB-positive parasites is also high in Madagascar where BovB thus might be physically transported by parasites to diverse vertebrates, potentially including humans. Remarkably, in two frog lineages, BovB HT occurred after migration from a non-HT area (Africa) to the HT hotspot (Madagascar). These results provide a novel perspective on how the prevalence of parasites influences the occurrence of HT in a region, similar to pathogens and their vectors in some endemic diseases.     

Parasites in pet reptiles

Exotic reptiles originating from the wild can be carriers of many different pathogens and some of them can infect humans. Reptiles imported into Slovenia from 2000 to 2005, specimens of native species taken from the wild and captive bred species were investigated. A total of 949 reptiles (55 snakes, 331 lizards and 563 turtles), belonging to 68 different species, were examined for the presence of endoparasites and ectoparasites. Twelve different groups (Nematoda (5), Trematoda (1), Acanthocephala (1), Pentastomida (1) and Protozoa (4)) of endoparasites were determined in 26 (47.3%) of 55 examined snakes. In snakes two different species of ectoparasites were also found. Among the tested lizards eighteen different groups (Nematoda (8), Cestoda (1), Trematoda (1), Acanthocephala (1), Pentastomida (1) and Protozoa (6)) of endoparasites in 252 (76.1%) of 331 examined animals were found. One Trombiculid ectoparasite was determined. In 563 of examined turtles eight different groups (Nematoda (4), Cestoda (1), Trematoda (1) and Protozoa (2)) of endoparasites were determined in 498 (88.5%) animals. In examined turtles three different species of ectoparasites were seen. The established prevalence of various parasites in reptiles used as pet animals indicates the need for examination on specific pathogens prior to introduction to owners.     

High infection intensities,but negligible fitness costs,suggest tolerance of gastrointestinal nematodes in a tropical snake

We investigated patterns of prevalence and intensity of gastrointestinal nematode infections in a tropical natricine snake, the keelback (Tropidonophis mairii). Ninety‐eight per cent of keelbacks were infected with Tanqua anomala (Gnathostomidae), with infection intensities of up to 243 worms per snake. Infection with T. anomala caused severe inflammation of stomach mucosa and submucosa at the sites of parasite attachment and encystment. Nonetheless, we did not detect detrimental effects of nematode infection on measures of fitness among wild or captive snakes. Snakes with heavier nematode infections had higher body condition scores than less‐infected individuals. Deworming captive snakes had no measurable effect on their growth rate, body condition or locomotor performance. In combination with an earlier study on blood‐dwelling hepatozoons, our work suggests that keelbacks have a high tolerance to parasites. The ‘fast‐pace’ life history and short lifespan of these snakes may make it beneficial for them to tolerate infection, rather than expend energy on resisting parasite attack.     

Three Nematode Species Recovered from Terrestrial Snakes in Republic of Korea

The majority of parasitological studies of terrestrial snakes in Korea have focused on zoonotic parasites. However, in the present study, we describe 3 unrecorded nematode species recovered from 5 species of snakes (n=6) in Korea. The examined snakes, all confiscated from illegal hunters, were donated by the Chungnam Wild Animal Rescue Center and Korean Broadcasting System in July 2014 and February 2015. Light and scanning electron microscopies on the shapes of spicules that are either bent or straight (kalicephalids) and the presence of the intestinal cecum (ophidascarids) figured out 3 nematodes; Kalicephalus brachycephalus Maplestone, 1931, Kalicephalus sinensis Hsü, 1934, and Ophidascaris excavata Hsü and Hoeppli, 1934. These 3 species of nematode faunas are recorded for the first time in Korea.     

Blood Parasites of Some Reptiles of the Pacific Northwest

SYNOPSIS. Three hundred and fifty-seven reptiles belonging to 15 species (11 genera, 7 families) from the Pacific Northwest were examined for haematozoa. Twenty-six (7.3%) had parasites. Eleven (3.1%) were infected with haemogregarines, 6 (1.7%) with microfilariae and 9 (2.5%) with unidentified organisms. Four species of snakes and 4 of lizards were positive. Several forms of haemogregarine from the Pacific gopher snake ( Pituophis melanoleucus catenifer ) are described.     

Effects of sex, body size, temperature, and location on the antipredator tactics of free-ranging gartersnakes (Thamnophis sirtalis, Colubridae)

Gartersnakes (Thamnophis sirtalis parietalis) in southern Manitoba are subject to intense predation (primarily by crows) duringtheir spring breeding season. The huge numbers of snakes providea unique opportunity to quantify behavioral traits. We simulatedpredator attacks by "pecking" more than 500 free-ranging snakes,to explore the determinants of snake response. Snakes respondedto a human finger in the same way as they did to a more realisticstimulus (a model crow). A snake's response to attack dependedon several factors, which interacted in complex ways. The primaryinfluences on response were body temperature (warmer snakes tended to flee, whereas colder snakes remained cryptic or flattenedand/or gaped and struck) and sex (males were more likely toflee). Responses also depended on microhabitat (i.e., insidethe winter den versus in adjacent grassland) and on the snake'sprior activity (e.g., courting snakes often ignored our closeapproach). These factors interacted in significant ways; for example, snakes outside the den were smaller and warmer thanthose inside, male snakes were smaller and warmer than females,and mean body temperatures were higher in larger snakes withineach sex. Thus, a snake's body size and its location affectedits defensive response indirectly (via their influence on bodytemperature). Our results differ from those of previous studiesand suggest that antipredator responses in these animals dependin a flexible and complex way upon biotic and abiotic variables.Interactions among these variables also must be consideredbefore we can identify underlying causal processes.     

A mitogenomic study on the phylogenetic position of snakes

Phylogenetic relationships of squamates (lizards, amphisbaenians and snakes) have received considerable attention, although no consensus has been reached concerning some basal divergences. This paper focuses on the Serpentes (snakes), whose phylogenetic position within the Squamata remains uncertain despite a number of morphological and molecular studies. Some mitogenomic studies have suggested a sister-group relationship between snakes and varanid lizards, while other studies have identified snakes and lizards as sister groups. However, recent studies using nuclear data have presented a different scenario, with snakes being more closely related to anguimorph and iguanian lizards. In this mitogenomic study we have examined the above hypotheses with the inclusion of amphisbaenians, one gekkotan and one acrodont lizard, taxa not represented in previous mitogenomic studies. To this end we have also extended the representation of snakes by sequencing five additional snake genomes: two scolecophidians ( Ramphotyphlops australis and Typhlops mirus ) two henophidians ( Eunectes notaeus and Boa constrictor ) and one caenophidian ( Elaphe guttata ). The phylogenetic analysis recovered snakes and amphisbaenians as sister groups, thereby differing from previous hypotheses. In addition to a discussion on previous morphological and molecular studies in light of the results presented here, the current study also provides some details regarding features of the new snake mitochondrial genomes described.     

The fate of Hepatozoon species naturally infecting Florida black racers and watersnakes in potential mosquito and soft tick vectors, and histological evidence of pathogenicity in unnatural host species.

Haemogregarine parasites, derived from the Florida snakes Coluber constrictor and Nerodia fasciata and ingested by Aedes aegypti, completed sporogony within the hemocoeles of nearly all fed mosquitoes in 14-18 days, and produced oocysts typical of Hepatozoon. However, mortalities and morbidity were high in the Culex which had fed on the Coluber. Oocysts were not found in any Ornithodoros turicata (Argasidae) which fed upon either snake host, but many sections of fed ticks had gametocyte-like cells within the gut lumen. Most lizards, Anolis carolinensis and Anolis sagrei, infected per os with oocysts derived from both snake species developed infections. Infections in the lizards were largely confined to hepatic schizonts with few parasites found in erythrocytes. Unlike naturally infected snake hosts, Hepatozoon schizonts in livers of lizards were often either surrounded by an unidentified dark pigment or heavily infiltrated with mononuclear inflammatory cells.     

Diversity of haemogregarine parasites infecting Brazilian snakes from the Midwest and Southeast regions with a description of two new species of Hepatozoon (Apicomplexa: Adeleorina: Hepatozoidae)

Although Brazil is a hotspot for snake species, there is a lack of information on the biodiversity of haemoparasites infecting these hosts. Thus, the present study aimed to bring new insights on the diversity of species of Hepatozoon (Apicomplexa: Adeleorina: Hepatozoidae) infecting Brazilian snakes from the Midwest and Southeast regions. The snakes were captured from 2018 to 2020 from the states of Mato Grosso, Mato Grosso do Sul, Goiás, and São Paulo. Three to five blood smears were made and the remaining blood sample was stored for further molecular analysis. Moreover, histopathological slides of the organs were stained with haematoxylin-eosin. Regarding molecular diagnosis, PCR was performed targeting different regions of the 18S rRNA gene of apicomplexan parasites. From the 13 free-living snakes screened, ten (76.92%) were found infected with Hepatozoon spp. Based on morphological and morphometric tools, five different morphotypes of species of Hepatozoon gamonts were detected. Molecular data and phylogenetic analysis support the morphological data, identifying five species of Hepatozoon from snakes, of which three species belong to previously described species, Hepatozoon cevapii, Hepatozoon cuestensis, and Hepatozoon quagliattus, with a genetic similarity of 100% (based on the 18S rRNA genetic marker). The present study identifies and describes two new species of Hepatozoon, Hepatozoon annulatum sp. nov. infecting the snake Leptodeira annulata and Hepatozoon trigeminum sp. nov. infecting the snake Oxyrhopus trigeminus. Thus, based on morphological and molecular data the present study provides new insights on haemogregarine diversity infecting Brazilian snakes from the Midwest and Southeast regions.