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Sharing schistosomes: the elephant schistosome Bivitellobilharzia nairi also infects the greater one- horned rhinoceros ( Rhinoceros unicornis) in Chitwan National Park, Nepal
Abstract
Because the digenetic trematode fauna of Nepal is poorly known, we began to search for schistosomes in and around Chitwan National Park (CNP) of southern Nepal. Both domestic and wild Indian elephants (Elephus maximus) are present, and we found one of two dung samples from wild elephants and 1 of 22 (4.5%) dung samples from domestic elephants to be positive for schistosome eggs. The morphology of the eggs and both cox1 and 28S sequences derived from the eggs/miracidia were consistent with Bivitellobilharzia nairi, reported here for the first time from Nepal. Also, 7 of 14 faecal samples from the Asian or greater one-horned rhinoceros (Rhinoceros unicornis) contained viable eggs indistinguishable from those of B. nairi. This identification was confirmed by comparison with both cox1 and 28S sequences from B. nairi eggs/miracidia derived from Nepalese and Sri Lankan elephants. This represents the first sequence-verified identification of a schistosome from any species of rhinoceros, and the first verified occurrence of a representative of Bivitellobilharzia (a genus of 'elephant schistosomes') in mammals other than elephants. Our work suggests that elephants and rhinos share B. nairi in CNP, even though these two members of the 'charismatic megafauna' belong to unrelated mammalian families. Their shared life style of extensive contact with freshwater habitats likely plays a role, although the snail intermediate host and mode of definitive host infection for B. nairi have yet to be documented. This report also supports Bivitellobilharzia as a monophyletic group and its status as a distinct genus within Schistosomatidae.
... Limited number of researches have been conducted on the gastrointestinal parasites of rhinoceros species. In Nepal, single study to date, documented the trematode parasites in GOHR [18]. ...
... The high prevalence rates of gastrointestinal parasites were also recorded from one-horned rhinoceros in captivity of Bangladesh [27], black rhino in the National Zoological Garden, Sri Lanka [28] and animals of order Perissodactyla in a zoological garden in Italy [29] which showed the total parasitic prevalence of 100%. Conversely, the lower infection rates of gastrointestinal parasites were reported in some of the previous studies in India and Nepal regarding the gastrointestinal parasites in GOHR [15,18] and in Javan rhinoceros from Indonesia [30,31] where the prevalence rates were 61.9%, 50% 45% and 56% respectively. The variation in the prevalence might be due to the difference in the number of samples examined, difference in the species of rhinoceros from which the samples were collected and difference in the location from where the samples were collected because the variation in topographical location can influence the rate of prevalence [32]. ...
... Not only GOHR, but there are also many threatened wildlife species including musk deer and red pandas are vulnerable to parasite/disease transmission from infected individuals including livestock due to living in the same habitat or using same resources for food [40,41]. Trematode parasites have been recorded from various species of rhinoceros both globally and in Nepal as well [18,27,28,30,31,38]. The recorded trematode parasites in the present study were Paramphistomum sp. and Fasciola sp. ...
Recently, many individuals of greater one-horned rhino (GOHR) were died with unknown reason in Chitwan National Park (CNP), Nepal. This has arisen chaos and confusion in the rhino conservation program of the country. This study was designed to determine the prevalence of gastrointestinal parasites among GOHR in the CNP. A
total of 100 dung samples were collected opportunistically by the random sampling method. Dung samples were preserved in 2.5% potassium dichromate solution and analysed in the laboratory by the direct smear and concentration method (floatation and sedimentation). Eggs and larvae of gastrointestinal parasite were found in 91% examined
samples. Altogether 13 different genera of parasites were identified with one protozoan i.e. Eimeria sp. (9%), nine nematodes i.e. Strongyloides sp. (65%), Ascaris sp. (16%), Haemonchus sp. (15%), Dromeostrongylus sp. (9%), Oxyuris sp. (8%), Bunostomum sp. (8%), Chabertia sp. (5%), Trichostrongylus sp. (4%) and Nematodirus sp. (2%), one
cestode i.e. Anoplocephala sp. (16%) and two trematodes i.e. Paramphistomum sp. (31%) and Fasciola sp. (14%). Nematode parasites were found to be most prevalent (87% of samples) followed by trematodes (45%), cestodes (16%) and protozoans (9%). The study indicates a high prevalence of gastrointestinal parasites in the GOHR of CNP and
identifies that there is need of strategic control measures to protect this endangered species from parasitic infection.
... Most reported cases of dermatitis caused by the genus Schistosoma are from parasites that infect domesticated work animals, such as cattle and buffalo, mainly in Asia. For example, in countries such as India and Nepal, the species Schistosoma turkestanicum, Schistosoma nasale, Schistosoma indicum, and Schistosoma spindale are often implicated in outbreaks of dermatitis (29)(30)(31)(32)(33)(34)(35)(36)(37)(38). This relationship may not be a surprise, as bovids are the definitive host, and the people in these areas depend upon these animals for their livelihood in farming. ...
... The genus Bivitellobilharzia is considered a schistosome of elephants, but it has also been reported from wild rhinoceroses in Nepal (38)(39)(40)(41). There are no known reports of cercarial dermatitis in humans from areas inhabited by African elephants (with the Bivitellobilharzia loxodontae schistosome), but in areas where domesticated Asian elephants are used, there have been cases of dermatitis in the mahouts, or elephant handlers, when the elephants are taken for bathing (e.g., in Sri Lanka [40]). ...
... There are no known reports of cercarial dermatitis in humans from areas inhabited by African elephants (with the Bivitellobilharzia loxodontae schistosome), but in areas where domesticated Asian elephants are used, there have been cases of dermatitis in the mahouts, or elephant handlers, when the elephants are taken for bathing (e.g., in Sri Lanka [40]). In Nepal, Bivitellobilharzia nairi has thus far been found in wild, not domesticated, elephants (38). The snail host remains unknown but is likely a pulmonate snail (42). ...
Cercarial dermatitis (swimmer's itch) is a condition caused by infective larvae (cercariae) of a species-rich group of mammalian and avian schistosomes. Over the last decade, it has been reported in areas that previously had few or no cases of dermatitis and is thus considered an emerging disease. It is obvious that avian schistosomes are responsible for the majority of reported dermatitis outbreaks around the world, and thus they are the primary focus of this review. Although they infect humans, they do not mature and usually die in the skin. Experimental infections of avian schistosomes in mice show that in previously exposed hosts, there is a strong skin immune reaction that kills the schistosome. However, penetration of larvae into naive mice can result in temporary migration from the skin. This is of particular interest because the worms are able to migrate to different organs, for example, the lungs in the case of visceral schistosomes and the central nervous system in the case of nasal schistosomes. The risk of such migration and accompanying disorders needs to be clarified for humans and animals of interest (e.g., dogs). Herein we compiled the most comprehensive review of the diversity, immunology, and epidemiology of avian schistosomes causing cercarial dermatitis.
Copyright © 2015, American Society for Microbiology. All Rights Reserved.
... Nonetheless, in spite of these difficulties, the overall picture of the diversity of nonhuman schistosomes has clarified considerably. This, in large measure, is due to the application of molecular methods that have enabled unambiguous detection of several new lineages over the past 20 years (Figure 2), detection based on objective reference sequences obtained from what might have once been an anonymous piece of an adult worm [22], or from a few schistosome eggs [23]. To further this quest, along with molecular information, Blasco-Costa et al. [24] emphasized the value of a holistic approach using what available information could be obtained from adult anatomy, life cycle stages and other sources of information. ...
... O. Both Asian and African elephants, and at least two of the five extant species of rhinos, harbor schistosomes, and although the snail hosts for them are not known [23], the fact that elephant handlers are known to experience swimmer's itch after contact with streams in which they regularly water and bathe elephants is suggestive of the possibility that cercariae of elephant schistosomes are involved. All matters related to the unknown natural intermediate hosts of these intriguing schistosomes require further investigation. ...
Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they penetrate human skin. Recent years have witnessed a dramatic increase in our understanding of schistosome diversity, now encompassing 17 genera with eight more lineages awaiting description. Collectively, schistosomes exploit 16 families of caenogastropod or heterobranch gastropod intermediate hosts. Basal lineages today are found in marine gastropods and birds, but subsequent diversification has largely taken place in freshwater, with some reversions to marine habitats. It seems increasingly likely that schistosomes have on two separate occasions colonized mammals. Swimmer’s itch is a complex zoonotic disease manifested through several different routes of transmission involving a diversity of different host species. Swimmer’s itch also exemplifies the value of adopting the One Health perspective in understanding disease transmission and abundance because the schistosomes involved have complex life cycles that interface with numerous species and abiotic components of their aquatic environments. Given the progress made in revealing their diversity and biology, and the wealth of questions posed by itch-causing schistosomes, they provide excellent models for implementation of long-term interdisciplinary studies focused on issues pertinent to disease ecology, the One Health paradigm, and the impacts of climate change, biological invasions and other environmental perturbations.
... Contemporary members of the SB clade infect a broad range of mammalian groups: Bovidae, Canidae, Elephantidae, Felidae, Hippopotamidae, Hominidae, Rhinocerotidae, Suidae, and Rodentia. Relationships among members of the SB clade have been largely resolved [41,64,78]. Schistosoma and Bivitellobilharzia have been considered to be sister genera despite conflicting phylogenies (Table 1), and all UCE datasets support the monophyly of Afro-Eurasian mammalian schistosomatids. ...
Schistosomatidae Stiles and Hassall 1898 is a medically significant family of digenetic trematodes (Trematoda: Digenea), members of which infect mammals or birds as definitive hosts and aquatic or amphibious gastropods as intermediate hosts. Currently, there are 17 named genera, for many of which evolutionary interrelationships remain unresolved. The lack of a resolved phylogeny has encumbered our understanding of schistosomatid evolution, specifically patterns of host-use and the role of host-switching in diversification. Here, we used targeted sequence capture of ultra-conserved elements (UCEs) from representatives of 13 of the 17 named genera and 11 undescribed lineages that are presumed to represent either novel genera or species to generate a phylogenomic dataset for the estimation of schistosomatid interrelationships. This study represents the largest phylogenetic effort within the Schistosomatidae in both the number of loci and breadth of taxon sampling. We present a near-comprehensive family-level phylogeny providing resolution to several clades of long-standing uncertainty within Schistosomatidae, including resolution for the placement of the North American mammalian schistosomes, implying a second separate capture of mammalian hosts. Additionally, we present evidence for the placement of Macrobilharzia at the base of the Schistosoma + Bivitellobilharzia radiation. Patterns of definitive and intermediate host use and a strong role for intermediate host-switching are discussed relative to schistosomatid diversification.
... A few surveys have been conducted to date, such as parasite prevalence in red panda (Bista et al., 2017;Lama et al., 2015), rhesus monkey (Macaca mulatta) and Assamese macaque (M. assamensis ;Jha et al., 2011;Pokheral & Maharjan, 2014;Tachibana et al., 2013), bats (Adhikari et al., 2020), indigenous pigs (Adhikari et al., 2021) and crossinfection of Schistosoma between elephant and rhinocerous (Devkota et al., 2012). However, these studies are relatively limited in scope, either targeting a particular site or a specific group of parasites. ...
Background
Disease transmission among humans, domestic animals and wildlife can have profound consequences in human health, wildlife conservation and maintenance of biodiversity. The issue of disease transmission can be particularly important for threatened wildlife species, yet such information remains scarce due to logistic constraints and government regulation on animal handlings. The red panda (Ailurus fulgens) is one of the globally threatened species challenged with habitat fragmentation and human disturbance. In Nepal, livestock grazing is recognised as one of the major threats to the red panda.
Aim
We aimed to provide the first empirical data on gastro‐intestinal parasites for sympatric livestock and red panda from two geographically isolated regions in Nepal.
Methods
In this study, we systematically sampled, and examined the faecal of livestock and red panda in two separate protected areas to provide the first empirical data on their gastro‐intestinal parasite, including the prevalence, parasite richness and load.
Results
We documented 11 parasite taxa (7 nematodes, 2 cestodes, 1 trematode and 1 coccidian), of which 8 are shared by both livestock and red panda. Furthermore, parasite prevalence, parasite load and parasite richness were generally higher in the livestock than the red panda.
Conclusion
The data provided from this systematic survey on parasites of sympatric livestock and red panda in wild raises the concern about the potential role of livestock mediating disease dynamics in the red panda. Our study suggests that cross‐transmission of parasites between livestock and red panda are likely, and the livestock may be a competent agent bringing disease to both red panda and human. Therefore, managing human‐livestock‐wildlife contact to reduce disease risk to all groups should be a key component in conservation planning of protected areas.
... Schistosomes or blood flukes are also thought to be an important yet overlooked cause of animal mortality and productivity losses in the livestock industry, with a major underestimated economic impact [69]. Certain schistosome species have also been suggested to be of concern to conservation of endangered animals such as rhinos and elephants in Asia [70] and chimpanzees in Africa [71]. In addition to liver and blood flukes, immature stomach flukes, or amphistomes, inflict damage to the intestine, leading to anorexia and diarrhea, while severe infections can be lethal [72,73]. ...
Background:
Humans impose a significant pressure on large herbivore populations, such as hippopotami, through hunting, poaching and habitat destruction. Anthropogenic pressures can also occur indirectly, such as artificial lake creation and the subsequent introduction of invasive species that alter the ecosystem. These events can lead to drastic changes in parasite diversity and transmission, but generally receive little scientific attention.
Results:
In order to document and identify trematode parasites of the common hippopotamus (Hippopotamus amphibius) in artificial water systems of Zimbabwe, we applied an integrative taxonomic approach, combining molecular diagnostics and morphometrics on archived and new samples. In doing so, we provide DNA reference sequences of the hippopotamus liver fluke Fasciola nyanzae, enabling us to construct the first complete Fasciola phylogeny. We describe parasite spillback of F. nyanzae by the invasive freshwater snail Pseudosuccinea columella, as a consequence of a cascade of biological invasions in Lake Kariba, one of the biggest artificial lakes in the world. Additionally, we report an unknown stomach fluke of the hippopotamus transmitted by the non-endemic snail Radix aff. plicatula, an Asian snail species that has not been found in Africa before, and the stomach fluke Carmyerius cruciformis transmitted by the native snail Bulinus truncatus. Finally, Biomphalaria pfeifferi and two Bulinus species were found as new snail hosts for the poorly documented hippopotamus blood fluke Schistosoma edwardiense.
Conclusions:
Our findings indicate that artificial lakes are breeding grounds for endemic and non-endemic snails that transmit trematode parasites of the common hippopotamus. This has important implications, as existing research links trematode parasite infections combined with other stressors to declining wild herbivore populations. Therefore, we argue that monitoring the anthropogenic impact on parasite transmission should become an integral part of wildlife conservation efforts.
... Schistosoma bovis, S. spindale, S. indicum, S. nasale, S. incognitum, S. mattheei, S. curassoni, S. japonicum, Bivitellobilharzia sp., Orientobilharzia sp. etc. (Chandrasekharan 1989;Modi 2001;Cherian & D'Souza2009;Devkota et al. 2014). ...
... loxodontae), India, and Sri Lanka (B. nairi); the latter species has also been found in the greater one-horned rhinoceros (Rhinoceros unicornis) from Nepal (Devkota et al. 2014). The reported prevalence in south India is about 4% (Vimalraj et al. 2012), and in Africa (Republic of Congo and Central African Republic) about 33% (Kinsella et al. 2004). ...
Trematodes of the order Diplostomida are well known as serious pathogens of man, and both farm and wild animals; members of the genus Schistosoma (Schistosomatidae) are responsible for human schistosomosis affecting more than 200 million people in tropical and subtropical countries, infections of mammals and birds by animal schistosomes are of great veterinary importance. The order Diplostomida is also rich in species parasitizing other major taxa of vertebrates. The Aporocotylidae are pathogenic in fish, Spirorchiidae in reptiles. All these flukes have two-host life cycles, with asexually reproducing larvae usually in molluscs and occasionally in annelids, and adults usually live in the blood vessels of their vertebrate hosts. Pathology is frequently associated with inflammatory reactions to eggs trapped in various tissues/organs. On the other hand, the representatives of Diplostomidae and Strigeidae have three- or four-host life cycles in which vertebrates often serve not only as definitive, but also as intermediate or paratenic hosts. Pathology is usually associated with migration of metacercariae and mesocercariae within the host tissues. The impact of these trematode infections on both farm and wild animals may be significant.
... 3 The schistosome Bivitellobilharzia nairi, previously thought to only infect elephants, has recently been found in wild greater onehorned rhino in Nepal. 6 The sampling limitations in the present study prevent specific conclusions being made about the overall prevalence of parasites in Kaziranga National Park, but provide an indication of the status of wild and orphan rhinos immediately after the monsoon season in Kaziranga. Stringer et al. 8 calculated that a minimum of nine samples was needed to accurately estimate mean parasite abundance in a host population of black rhino (Diceros bicornis). ...
Wild greater one-horned rhinos (Rhinoceros unicornis), orphaned juveniles in human care, and orphaned calves from Kaziranga National Park, Assam, India were surveyed coprologically for gastrointestinal parasites. Parasite infections were present in 100% of wild rhino samples, 96% of orphaned juvenile samples, and 27% of orphaned calf samples. In wild rhino, observed parasite ova were primarily of trematodes Paramphistomum sp. (100%), followed by those of strongyle nematodes (94%) and the cestode Anoplocephala sp. (56%). Orphaned juvenile and calf samples were positive only for strongyles. Total fecal parasite egg counts were recorded in wild rhino (mean 64 eggs per gram [epg], range 0–270), orphan juveniles (mean 43 epg, range 0–145), and orphan calves (mean 2 epg, range 0–10). Results suggest that parasite infection in rhinos in this setting is common, though more extensive sampling would provide further information on epidemiology and potential impacts on individual health and population viability.
... Evaluation of intestinal parasites in zoo animals and different geographic regions has medical and veterinary importance to prevent transmission of intestinal parasitic diseases to human and domestic animals. Many studies have been documented the intestinal parasites of the zoo animals in different populations of the world (1,2,(5)(6)(7)(8). ...
Received 18 Sep 2017
Accepted 22 Jan 2018
Abstract
Background: Intestinal parasitic infections are major causative agents of wildlife health complications among different parts of the world. This study aimed to investigate the gastro-intestinal parasites in feces of the zoo animals based on parasitological and morphometric criteria.
Material: One hundred fresh fecal samples were collected from 35 species of animal lived in Eram park zoo, Tehran, Central Iran during Oct 2015 to Jun 2015. All collected samples were examined by microscopic observation following direct wet mount preparation (normal saline and Lugol's iodine), formalin-ether concentration, and permanent staining. The morphometric aspects of the recovered eggs were surveyed with the aid of Camera Lucida (×400).
Results: 65.7% (23/35) of zoo animal species were infected with intestinal parasites. The superfamily Trichostrongyloidea (6/16) and Strongylus sp. (16/4) were the most prevalent helminthic infections, while Blastocystis sp. (6/14), Entamoeba cyst (3/14) and Eimeria sp. (3/14) were the common protozoan parasites. For the first time, Bivitellobilharzia nairi egg was identified an elephant at Iran. Intestinal parasitic infections were apparently circulating among animals of the Eram park zoo.
Conclusion: Identified parasitic infections can consider as a threatening source to visitors and workers' health that have contact with animals or their feces. Therefore, the effectual preventive strategies should be addressed to determine the risk factors, mechanisms of cross-transmission of parasite, the importance of applying the hygienic practices and well adjusting deworming programs for the animals, zoo workers and visitors.
... Bivitellobilharzia nairi, has a spine or hook at one end of the egg (Agatsuma et al., 2004;Devkota et al., 2012;Rajapakse et al., 2013). The methods for examination of parasite eggs can also be used for examining microflora ciliates from the gastrointestinal tract, and the ciliates are recognisable with iodine staining and their little tuffs of cilia (Červená, 2013;Kinsella et al., 2004). ...
Translocation of wild Asian elephants (Elephas maximus) is used extensively to mitigate human-elephant conflict (HEC) in Peninsular Malaysia since 1974. Very little is known about the fate of translocated elephants after relocation due to challenges in observing elephants in the dense rainforest. Advances in wildlife endocrinology suggest that faecal glucocorticoid metabolites (fGCM) can be used to study adrenal activity remotely, to assess the Hypothalamic-Pituitary-Adrenal (HPA) axis response towards stressors. The aim is to assess the impact of translocation on wild Asian elephants in Peninsular Malaysia using faecal endocrinology and GPS technology. The specific objectives are: (i) adapting hormone sampling methods for use under tropical field conditions, (ii) comparing fGCM concentrations between translocated and local resident elephants using enzyme immunoassay, and (iii) quantifying gastrointestinal parasite eggs and microflora ciliates in faecal samples to detect signs of immunosuppression. We found that Asian elephant’s fGCM (80 dungpiles, 685 subsamples) are stable up to eight hours in the field. From the monitoring of wild elephants at the release sites, between two months up to a year, translocated elephants (N=5) had lower fGCM concentrations in comparison to local resident elephants (N=4; Linear Mixed Models: t=-2.77, df=7.09, P=0.027). There were no differences in gastrointestinal parasite egg counts (P>0.05) or microflora ciliate counts (P>0.05) between translocated and local resident elephants. In conclusion, translocation does affect elephant physiology but this is in the opposite direction from that expected – a prolonged decrease rather than increase of adrenal activity. It is unknown if these conditions could cause immunosuppression, but it could adversely affect stress response and health of the elephant (e.g. adrenal insufficiency, chronic fatigue or Post-Traumatic Stress Disorder). When assessing HEC mitigation, conservation authorities and other stakeholders need to consider that translocation may not be the best solution for HEC, as it will have long-term consequences on elephants’ health.
... No specimens from the S. indicum group have previously been reported from Nepal, although the presence of mammalian schistosome cercariae from I. exustus has been reported (Devkota et al., 2011). The elephant schistosome Bivitellobilharzia nairi occurs in Nepal in both elephants and rhinoceros (Devkota et al., 2014a), and at least two species of avian schistosomes also occur there (Devkota et al., 2014b), but our knowledge of schistosomes present in Nepal is otherwise rudimentary. Laterally-spined schistosome eggs closely resembling the eggs of Schistosoma mansoni have been reported from human fecal samples from the Terai region of southern Nepal (Sherchand et al., 1999), but no additional reports of a schistosome with laterally-spined eggs from Nepal have since come to light. ...
From 2007-2014, 19,360 freshwater snails from the Terai and hilly regions of Nepal were screened for cercariae of mammalian schistosomes. Based on analysis of mitochondrial cytochrome oxidase I (cox1), 12S, 16S and 28S sequences (3,675 bp) of the cercariae recovered, we provide, to our knowledge, the first report of the Schistosoma indicum species group in Nepal. Five samples of Schistosoma nasale, nine of Schistosoma spindale and 17 of Schistosoma sp. were recovered, all from the snail Indoplanorbis exustus. The last-mentioned lineage failed to group in any of our analyses with S. nasale, S. spindale or S. indicum. It diverged in cox1 sequence from them by 16%, 13% and 13%, respectively, levels of difference comparable to well-studied species pairs of Schistosoma. Analysis of cox1, 16S and internal transcribed spacer 1 (ITS1) sequences (1,874 bp) for Nepalese specimens of I. exustus was also surprising in revealing the presence of four genetically distinct clades. They diverged from one another at levels comparable to those noted for species pairs in the sister genus Bulinus. There was no obvious pattern of use by Nepalese Schistosoma of the Indoplanorbis clades. We found high support for a close relationship between S. indicum and Schistosoma haematobium groups, but failed to retrieve support for a clean separation of the two, with a tendency for S. nasale to fall as the most basal representative. If this pattern holds, hypotheses for the origin of the Asian Indoplanorbis-transmitted S. indicum group from the Bulinus-transmitted S. haematobium group may require modification, including consideration of more contemporaneous origins of the two groups. The Indian subcontinent is under-studied with respect to schistosome diversity and our current knowledge of the S. indicum and I. exustus species groups is inadequate. Further study is warranted given the ability of indicum group species to cause veterinary problems and cercarial dermatitis, with a worrisome potential in the future to establish infections in humans.
... loxodontae), India, and Sri Lanka (B. nairi); the latter species has also been found in the greater one-horned rhinoceros (Rhinoceros unicornis) from Nepal (Devkota et al. 2014). The reported prevalence in south India is about 4% (Vimalraj et al. 2012), and in Africa (Republic of Congo and Central African Republic) about 33% (Kinsella et al. 2004). ...
Trematodes of the order Diplostomida are well known as serious pathogens of man, and both farm and wild animals; members of the genus Schistosoma (Schistosomatidae) are responsible for human schistosomiasis affecting more than 200 million people in tropical and subtropical countries, and infections of mammals and birds by animal schistosomes are of great veterinary importance. The order Diplostomida is also rich in species parasitizing other major taxa of vertebrates. The Aporocotylidae are pathogenic in fish and Spirorchiidae in reptiles. All these flukes have two-host life cycles, with asexually reproducing larvae usually in molluscs and occasionally in annelids, and adults usually live in the blood vessels of their vertebrate hosts. Pathology is mostly associated with inflammatory reactions to eggs trapped in various tissues/organs. On the other hand, the representatives of Diplostomidae and Strigeidae have three- or four-host life cycles in which vertebrates often serve not only as definitive, but also as intermediate or paratenic hosts. Pathology is usually associated with migration of metacercariae and mesocercariae within the host tissues. The impact of these trematode infections on both farm and wild animals may be significant.
... With this long-term goal in mind, we have undertaken a concerted search for avian schistosomes in Nepal. Although there are a few published studies of mammalian schistosomes from Nepal [3], there are no previous studies of Nepalese avian schistosomes or cercarial dermatitis. Extensive works on trematode cercariae in freshwater gastropods and schistosomes have been reported from surrounding countries like India [4], but in Nepal, studies on larval trematode infections in freshwater gastropods are very few [5]. ...
As part of a global survey of schistosomes, a total of 16,109 freshwater snails representing 14 species were collected from lakes, ponds, rivers, rice fields and swamps mostly in the Terai region of southern Nepal. Only two snails were found to harbor avian schistosome cercariae even though Nepal is well known for its rich avian diversity. One schistosome infection was from an individual of Radix luteola and on the basis of phylogenetic analyses using 28S rDNA and cox1 sequences, grouped as a distinctive and previously unknown lineage within Trichobilharzia. This genus is the most speciose within the family Schistosomatidae. It includes 40 described species worldwide, and its members mostly infect anseriform birds (ducks) and two families of freshwater snails (Lymnaeidae and Physidae). The second schistosome cercaria was recovered from an individual of Indoplanorbis exustus that was also actively emerging a Petasiger-like echinostome cercaria. Although I. exustus is commonly infected with mammalian schistosomes of the Schistosoma indicum species group on the Indian subcontinent, this is the first specifically documented avian schistosome reported in this snail. Both the cercariae reported here are among the largest of all schistosome cercariae recovered to date. The I. exustus-derived schistosome clustered most closely with Macrobilharzia macrobilharzia, although it seems to represent a distinct lineage. Specimens of Macrobilharzia have thus far not been recovered from snails, being known only as adult worms from anhingas and cormorants. This study is the first to characterize by sequence data avian schistosomes recovered from Asian freshwater habitats. This approach can help unravel the complex of cryptic species causing cercarial dermatitis here and elsewhere in the world.
... The position of Bivitellobilharzia as the sister group of Schistosoma has important implications for interpreting the geographic origin of the latter, medically important genus [28,49]. Further study of B. nairi has shown for the first time that this schistosome species can also infect the Asian One-Horned Rhinoceros (Rhinoceros unicornis) [50]. The report of B. nairi from two unrelated, large, thick-skinned mammals, Asian elephants and Asian rhinoceroses, raises the possibility that shared ecology or perhaps something associated with large body size per se that we do not fully appreciate (is it a large-host specialist?) may somehow favor acquisition of this species. ...
This review provides an update of ongoing efforts to expand our understanding of the diversity inherent within the Schistosomatidae, the parasites responsible for causing schistosomiasis and cercarial dermatitis. By revealing more of the species present, particularly among understudied avian schistosomes, we gain increased understanding of patterns of schistosome diversification, and their abilities to colonize new hosts and habitats. Schistosomes reveal a surprising ability to switch into new snail and vertebrate host species, into new intrahost habitats, and may adopt novel body forms in the process. Often these changes are not associated with deep splits or long branches in their phylogeny, suggesting some are of relatively recent origin. Several hypotheses prompted by the new observations are discussed, helping to focus thinking on processes influencing not only schistosome diversification but also their pathogenicity and abundance.
The classification of “parasites” in the medical field is a challenging notion, a group which historically has included all eukaryotes exclusive of fungi that invade and derive resources from the human host. Since antiquity, humans have been identifying and documenting parasitic infections, and this collective catalog of parasitic agents has expanded considerably with technology. As our understanding of species boundaries and the use of molecular tools has evolved, so has our concept of the taxonomy of human parasites. Consequently, new species have been recognized while others have been relegated to synonyms. On the other hand, the decline of expertise in classical parasitology and limited curricula have led to a loss of awareness of many rarely encountered species. Here, we provide a comprehensive checklist of all reported eukaryotic organisms (excluding fungi and allied taxa) parasitizing humans resulting in 274 genus-group taxa and 848 species-group taxa. For each species, or genus where indicated, a concise summary of geographic distribution, natural hosts, route of transmission and site within human host, and vectored pathogens are presented. Ubiquitous, human-adapted species as well as very rare, incidental zoonotic organisms are discussed in this annotated checklist. We also provide a list of 79 excluded genera and species that have been previously reported as human parasites but are not believed to be true human parasites or represent misidentifications or taxonomic changes.
Prevalence of endoparasites in free-ranging Greater One-horned Rhinoceros in Protected Areas of Assam, India
Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations.
Blood flukes of the family Spirorchiidae are significant pathogens of both free-ranging and captive marine turtles. Despite a significant proportion of marine turtle mortality being attributable to spirorchiid infections, details of their life cycles remain almost entirely unknown. Here we report on the molecular elucidation of the complete life cycle of a marine spirorchiid, identified as Amphiorchis sp., infecting vermetid gastropods and captive hatched neonate Caretta caretta in the Oceanogràfic Aquarium, in Valencia, Spain. Specimens of a vermetid gastropod, Thylaeodus cf. rugulosus (Monterosato, 1878), collected from the aquarium filtration system housing diseased C. caretta, were infected with sporocysts and cercariae consistent with the family Spirorchiidae. We generated rDNA sequence data [internal transcribed spacer 2 (ITS2) and partial 28S rDNA] from infections from the vermetid which were identical to sequences generated from eggs from the serosa of the intestine of neonate C. caretta, and an adult spirorchiid from the liver of a C. caretta from Florida, USA. Given the reliability of these markers in the delineation of trematode species, we consider all three stages to represent the same species and tentatively identify it as a species of Amphiorchis Price, 1934. The source of infection at the Oceanogràfic Foundation Rehabilitation Centre, Valencia, Spain, is inferred to be an adult C. caretta from the western Mediterranean being rehabilitated in the same facility. Phylogenetic analysis suggests that this Amphiorchis sp. is closely related to other spirorchiids of marine turtles (species of Carettacola Manter & Larson, 1950, Hapalotrema Looss, 1899 and Learedius Price, 1934). We discuss implications of the present findings for the control of spirorchiidiasis in captivity, for the better understanding of epidemiology in wild individuals, and the elucidation of further life cycles.
This study was carried out to determine the prevalence of gastrointestinal parasites of musk deer in Langtang National Park, Nepal. A total of 9 fecal samples were collected systematically and analyzed using standard procedures during May-June, 2014. Overall 7 species of parasites including 4 nematodes, 1 cestode, 1 trematode and 1 protozoan parasite were recorded. Prevalence of Ascaris sp. was high (88.89%) followed by Eimeria sp. (77.78%), Trichuris sp. (66.67%), Strongyloides sp. (55.56%), Moniezia sp. (44.44%), Strongyle (44.44%) and Paramphistomum sp. (44.44%). Most of the samples had heavy parasitic infestation and multiple parasites were also observed in same individual. The high parasitic prevalence might have adverse health impact on musk deer. The possibility of cross-transmission of parasites between livestock and wildlife in Langtang National Park should be studied in future.
Journal of Institute of Science and Technology
Vol. 21, No. 1, 2016, Page: 71-75</p
Fecal samples were collected from 6 African forest elephants, Loxodonta africana cyclotis, from the Nouabalé-Ndoki National Park, Republic of Congo, and the Dzangha-Sangha National Park, Central African Republic. One of the elephants was found freshly dead from natural causes, and 12 species of intestinal parasites (2 bot fly larvae, 1 trematode, and 9 nematodes) were collected during a complete necropsy. In addition, fecal samples revealed the presence of a schistosome, Bivitellobilharzia sp., a tracheal nematode, Mammomonagamus sp., and a complex of intestinal strongylids and ciliates. The nematode genera Decrusia and Equinurbia are reported for the first time from African elephants, and the ciliate genus Latteuria is reported for the first time from wild elephants. The parasite fauna of the African elephant is discussed in the light of recent genetic evidence that the forest and savannah elephants may be separate species.
One of the most poorly known of all schistosomes infecting mammals is Bivitellobilharzia loxodontae. Nearly all of our available information about this species comes from the original description of worms that were obtained from an animal park-maintained elephant in Germany, probably a forest elephant Loxodonta cyclotis, originating from the present-day Democratic Republic of Congo. We obtained schistosome eggs from faecal samples from wild forest elephants from the Central African Republic. The eggs, which were similar in size and shape to those of described B. loxodontae, were sequenced for the 28S nuclear ribosomal gene and the mitochondrial cytochrome oxidase I (cox1) gene. In a phylogenetic analysis of 28S sequences, our specimens grouped closely with B. nairi, the schistosome from the Indian elephant Elephas maximus, to the exclusion of schistosomes from other genera. However, the eggs were genetically distinct (12% distance cox1) from those of B. nairi. We conclude the specimens we recovered were of B. loxodontae and confirm this is a distinct Bivitellobilharzia species. In addition to providing the first sequence data for B. loxodontae, this report also supports Bivitellobilharzia as a monophyletic group and gives the relative phylogenetic position of the genus within the Schistosomatidae. We also provide a review of the biology of this poorly known schistosome genus.
The program MRBAYES performs Bayesian inference of
phylogeny using a variant of Markov chain Monte Carlo.
Availability: MRBAYES, including the source code, documentation,
sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
Contact: johnh{at}brahms.biology.rochester.edu
Previous analyses of relations, divergence times, and diversification patterns among extant mammalian families have relied
on supertree methods and local molecular clocks. We constructed a molecular supermatrix for mammalian families and analyzed
these data with likelihood-based methods and relaxed molecular clocks. Phylogenetic analyses resulted in a robust phylogeny
with better resolution than phylogenies from supertree methods. Relaxed clock analyses support the long-fuse model of diversification
and highlight the importance of including multiple fossil calibrations that are spread across the tree. Molecular time trees
and diversification analyses suggest important roles for the Cretaceous Terrestrial Revolution and Cretaceous-Paleogene (KPg)
mass extinction in opening up ecospace that promoted interordinal and intraordinal diversification, respectively. By contrast,
diversification analyses provide no support for the hypothesis concerning the delayed rise of present-day mammals during the
Eocene Period.
The giant panda is a global symbol of wildlife conservation that is threatened by historic and current habitat loss. Despite a great deal of research on the physiology, reproductive biology, and diet of pandas in the wild and in captivity, there is little information on wild panda mortality. Here we integrate previously unavailable data on the mortality of wild pandas. We report on three recent phases of panda mortality: deaths due to bamboo flowering in the 1970s and 1980s, surprisingly extensive poaching in the 1980s and 1990s, and a parasitic infection over the past few years. Our analyses suggest that the current most significant threat to wild panda survival is disease due to extraintestinal migration (visceral larval migrans) by an ascarid nematode. We demonstrate that the probability of death of wild pandas being caused by this disease increased significantly between 1971 and 2005 and discuss the possible factors leading to the emergence of this disease.
Larvae of the cyclophyllidean tapeworms Paradilepis scolecina (Rudolphi, 1819), Neogryporhynchus cheilancristrotus (Wedl, 1855) and Valipora campylancristrota (Wedl, 1855), are described from British freshwater fish. The morphometrics of the rostellar hooks, infection characteristics and host ranges of these parasites from fisheries in England and Wales are presented. Difficulties in the detection, handling and identification of these tapeworms are highlighted, and may in part explain the paucity of records from Britain. Tissue digestion was shown to be a useful technique for the examination of these parasites, providing clear and consistent preparations of the rostellar hooks for measurement. The pathological changes caused by P. scolecina to the liver of wild tench, Tinca tinca, are detailed for the first time. Tapeworms located in the hepatic parenchyma and pancreatic tissues caused little pathological damage and invoked only mild inflammatory responses. The small size of these tapeworms and their encapsulation within host tissues appear to limit the severity of pathology, compared with parasites that insert their rostellum during attachment.
Representative samples of Ugandan Schistosoma mansoni from Lake Albert and Lake Victoria were examined using DNA barcoding, sequence analysis of two partially overlapping regions - ASMIT (396 bp) & MORGAN (617 bp) - of the mitochondrial cytochrome oxidase subunit I (cox1). The Victorian sample exhibited greater nucleotide diversity, 1.4% vs. 1.0%, and a significant population partition appeared as barcodes did not cross-over between lakes. With one exception, Lake Albert populations were more mixed by sampled location, while those from Lake Victoria appeared more secluded. Using statistical parsimony, barcode ASMIT 1 was putatively ancestral to all others and analysis of MORGAN cox1 confirmed population diversity. All samples fell into two of five well-resolved lineages; sub-lineages therein broadly partitioning by lake. It seems that barcode ASMIT 1 (and close variants) was likely widely dispersed throughout the Nilotic environment but later diversified in situ, and in parallel, within Lake Albert and Lake Victoria. The genetic uniformity of Ugandan S. mansoni can no longer be assumed, which might better explain known epidemiological heterogeneities. While it appears plausible that locally evolved heritable traits could spread through most of the Lake Albert populations, it seems unlikely they could quickly homogenise into Lake Victoria or amongst populations therein.
MrBayes 3 performs Bayesian phylogenetic analysis combining information from different data partitions or subsets evolving under different stochastic evolutionary models. This allows the user to analyze heterogeneous data sets consisting of different data types—e.g. morphological, nucleotide, and protein—and to explore a wide variety of structured models mixing partition-unique and shared parameters. The program employs MPI to parallelize Metropolis coupling on Macintosh or UNIX clusters.
Availability: http://morphbank.ebc.uu.se/mrbayes
Contact: fredrik.ronquist@ebc.uu.se
*
To whom correspondence should be addressed.
Revealing diversity among extant blood flukes, and the patterns of relationships among them, has been hindered by the difficulty of determining if specimens described from different life cycle stages, hosts, geographic localities, and times represent the same or different species. Persistent collection of all available life cycle stages and provision of exact collection localities, host identification, reference DNA sequences for the parasite, and voucher specimens eventually will provide the framework needed to piece together individual life cycles and facilitate reconciliation with classical taxonomic descriptions, including those based on single life cycle stages. It also provides a means to document unique or rare species that might only ever be recovered from a single life cycle stage. With an emphasis on the value of new information from field collections of any available life cycle stages, here we provide data for several blood fluke cercariae from freshwater snails from Kenya, Uganda, and Australia. Similar data are provided for adult worms of Macrobilharzia macrobilharzia and miracidia of Bivitellobilharzia nairi. Some schistosome and sanguinicolid cercariae that we recovered have peculiar morphological features, and our phylogenetic analyses (18S and 28S rDNA and mtDNA CO1) suggest that 2 of the new schistosome specimens likely represent previously unknown lineages. Our results also provide new insights into 2 of the 4 remaining schistosome genera yet to be extensively characterized with respect to their position in molecular phylogenies, Macrobilharzia and Bivitellobilharzia. The accessibility of each life cycle stage is likely to vary dramatically from one parasite species to the next, and our examples validate the potential usefulness of information gleaned from even one such stage, whatever it might be.
jModelTest is a new program for the statistical selection of models of nucleotide substitution based on “Phyml” (Guindon and Gascuel 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696–704.). It
implements 5 different selection strategies, including “hierarchical and dynamical likelihood ratio tests,” the “Akaike information
criterion,” the “Bayesian information criterion,” and a “decision-theoretic performance-based” approach. This program also
calculates the relative importance and model-averaged estimates of substitution parameters, including a model-averaged estimate
of the phylogeny. jModelTest is written in Java and runs under Mac OSX, Windows, and Unix systems with a Java Runtime Environment
installed. The program, including documentation, can be freely downloaded from the software section at http://darwin.uvigo.es.
— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.
Of the fifteen valid species of mammalian blood-flukes so far known, six have been originally described from India. Montgomery (1906) described Schistosoma indicum, S. spindalis and Ornithobilharzia bomfordi (Montgomery, 1906) Price, 1929. Datta (1932) found that nasal granuloma of cattle is due to a new schistosome, which was subsequently obtained and described as Schistosoma nasalis by Rao (1933). Rao & Ayyar (1933) obtained a new schistosome from pigs and described it as S. suis . Mudaliar & Ramanujachari (1945) described S. nairi n.sp., from an elephant, which was transferred to the genus Ornithobilharzia by Bhalerao (1947). Another new species of blood-fluke has now been found in Indian buffaloes and cattle. While studying the larval trematode fauna of the local aquatic snails, large numbers of a new schistosome cercaria were obtained from nine out of three hundred specimens of Limnaea luteola examined during November 1950. When the cercariae were administered to two guinea-pigs, a buffalo-calf and a bull-calf, they developed into an interesting blood-fluke referable to the genus Ornithobilharzia Odhner, 1912. Subsequently, three out of thirteen buffaloes examined post-mortem were found to be naturally infected with the same parasite. The morphology of the adult and of its cercaria is briefly described in this paper.
This new species is described from material consisting of four males and six females said to have been recovered from the intestine of Rhinoceros bicornis in Kenya and sent to the writer through the courtesy of Mr. M. C. Round, B.Sc, of Veterinary Research Laboratory, Department of Veterinary Services, Kabete, Kenya.
Bivitellobilharzia nairi (Mudaliar and Ramanujachar, 1945) Dutt and Srivastava, 1955 was first recorded in India. A number of adult worm specimens of this schistosome species were recovered from a domestic elephant, which died in 1999 in Sri Lanka. This is the first report of this schistosome from Sri Lanka. In the present study, in order to clarify the phylogenetic relationship with other species of schistosomes, sequences from the second internal transcribed spacer (ITS2) of the ribosomal gene repeat, part of the 28S ribosomal RNA gene (28S), and part of the mitochondrial cytochrome c oxidase subunit 1 (CO1) gene from B. nairi were analyzed. Two intraspecific variations were seen within 13 individuals in the ITS2 region. In the CO1 region of the mitochondrial DNA, there were four haplotypes in the nucleotide sequences and two haplotypes in the amino acid sequences. Phylogenetic analysis using the nuclear DNA showed that B. nairi was basal to all of species of the genus Schistosoma. The 28S tree also showed that the mammalian lineage was monophyletic. However, phylogenetic analysis using the mitochondrial DNA showed that B. nairi was nested within the genus Schistosoma. The taxonomical position for this species as well as the contradiction between the results from the nuclear and mitochondrial genes were discussed.
On Bivitellobilharzia nairi (Mudaliar and Ramanujachari, 1945) Dutt and Srivastava, 1955 (Trematoda: Schistosomatidae) parasitic in Indian elephants (Elaphas maximus) with a redescription of the species
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Sundaram, R.K., Padmanabha Iyer, R., Peter, C.T. &
Alwar, V.S. (1972) On Bivitellobilharzia nairi (Mudaliar
and Ramanujachari, 1945) Dutt and Srivastava, 1955
(Trematoda: Schistosomatidae) parasitic in Indian
elephants (Elaphas maximus) with a redescription of
the species. Indian Veterinary Journal 49, 1 -10.
Schistosoma nairi n. sp. from an elephant
- Mudaliar
Mudaliar, S.V. & Ramanujachary, G. (1945) Schistosoma
nairi n. sp. from an elephant. Indian Veterinary Journal
12, 1-4.
Incidence of intestinal helminthic infection in Rhinoceros unicornis in captivity. Zoos' Print 5, 14. Fitzsimmons, W.M. (1962) Parabronema roundi n. sp. (Spiruridae: Nematoda) from Rhinoceros bicornis in Kenya
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(1990) Incidence of intestinal helminthic infection in
Rhinoceros unicornis in captivity. Zoos' Print 5, 14.
Fitzsimmons, W.M. (1962) Parabronema roundi n. sp.
(Spiruridae: Nematoda) from Rhinoceros bicornis in
Kenya. Journal of Helminthology XXXVI, 39 -44.
A survey of gastrointestinal parasitic infection in free-living rhinoceros of Kaziranga National Park
- Chakraborty
Chakraborty, A. & Islam, S. (1993) A survey of
gastrointestinal parasitic infection in free-living rhinoceros of Kaziranga National Park. Indian Journal of
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Schistosomiasis in elephants in Bombay State
- Rao
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The ecology and behavior of the great one horned rhinoceros. A dissertation submitted to the University of Cambridge for the degree of doctor of philosophy
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one horned rhinoceros. A dissertation submitted to the
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Inventory of trematode cercariae infections in freshwater snails in Chitwan and Nawalparasi Districts and trematode infections in domestic elephants of Sauraha (minor study). A thesis submitted to Central Department of Zoology
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Devkota, R. (2008) Inventory of trematode cercariae
infections in freshwater snails in Chitwan and
Nawalparasi Districts and trematode infections in
domestic elephants of Sauraha (minor study). A thesis
submitted to Central Department of Zoology, Institute
of Science and Technology, Tribhuvan University,
Kirtipur, Kathmandu, Nepal.
Parasites of the white and black rhinoceroses
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rhinoceroses. The Lammergeyer 3, 59 -70.
Parasites of African rhinos: a documentation
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- J B Walker
- J D F Boomker
- S E Knapp
- S K F Quandt
Penzhorn, B.L., Krecek, R.C., Horak, I.G., Verster, A.J.M.,
Walker, J.B., Boomker, J.D.F., Knapp, S.E. &
Quandt, S.K.F. (1994) Parasites of African rhinos: a
documentation. Proceedings of a Symposium on 'Rhinos as
Game Ranch Animals', 9 – 10 September, Onderstepoort,
Pretoria, South Africa.
Incidence of gastrointestinal helminthes in captive elephants in wildlife reserves of Nepal. Articlesbase, Free Online Articles Directory
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Karki, K. & Manandhar, P. (2008) Incidence of gastrointestinal helminthes in captive elephants in wildlife reserves of Nepal. Articlesbase, Free Online Articles Directory.
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Parasite killed elephant
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1984, Associated Press.
On the morphology and life history of a new mammalian blood fluke
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Dutt, S.C. & Srivastava, H.D. (1961) On the morphology
and life history of a new mammalian blood fluke,
Ornithobilharzia dattai n. sp. (preliminary report).
On Bivitellobilharzia nairi (Mudaliar and Ramanujachari, 1945) Dutt and Srivastava, 1955 (Trematoda: Schistosomatidae) parasitic in Indian elephants (Elaphas maximus) with a redescription of the species
- Sundaram
Helminthes parasite at feces of Sumatran Rhinoceros (Dicerorhinus sumtrensis) and Sumatran Elephant (Elephas maximus surnatranus) in Way Kambas National park Lampung (semi in situ)
- Muryani
Incidence of intestinal helminthic infection in Rhinoceros unicornis in captivity
- Dutta