Article

Redescriptions of Haemonchus mitchelli and Haemonchus okapiae (Nematoda: Trichostrongyloidea) and Description of a Unique Synlophe for the Haemonchinae

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Abstract

In the course of a revision of Haemonchus Cobb, 1898 (Nematoda), commonly referred to as large stomach worms, significant new morphological information was discovered that allows the recognition of 2 species believed for more than 50 yr to be synonymous. Both species, Haemonchus mitchelli Le Roux, 1929, from the eland Taurotragus oryx and other African ruminants and H. okapiae van den Berghe, 1937, from the okapi Okapia johnstoni, have a synlophe of 42 ridges, but the synlophe of H. mitchelli is longer than that of H. okapiae. The distal tip of the left spicule of H. mitchelli bears a barb that is about twice as long as the short barb and half as long as the long barb on the right spicule. In contrast, the barb on the left spicule of H. okapiae is similar in size to the short barb and about 25% as long as the long barb of the right spicule. The dorsal ray of H. mitchelli is bifurcated distally for 25-39% (32%) of its length and its stem is expanded proximally, but the dorsal ray of H. okapiae is bifurcated 37-50% (42%) and its stem is of uniform thickness.

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Introduction There is still lack of morphological and phylogenetic information on the pathogenic nematode of the camel Haemonchus longistipes . In the present study, this parasite was isolated in Saudi Arabia and described. Material and Methods The abomasa of two Arabian camels were collected from a slaughterhouse in Abha province and examined for nematode infection. Worms were described morphologically and morphometrically by electron microscopy. Multiple sequence alignment and the phylogenetic tree of the parasite were constructed from maximum likelihood analysis of its ITS-2 rDNA sequences. Results These nematodes had a slender body terminating anteriorly at a conspicuous dorsal lancet. A pair of lateral cervical papillae distant from the anterior end was observed. The buccal aperture was hexagonal and surrounded by two amphids, six externo-labial papillae, and four cephalic papillae. Males terminated posteriorly at a bursa supported by spicules and lateral and dorsal rays. Females were linguiform and knobbed morphotypes with distinct ovijectors and a dorsal rim covering the anal pore. The taxonomy was confirmed by the morphology and number of the longitudinal cuticular ridges in a 43–46 range. The sequence alignment and phylogeny revealed 92% homology with H. longistipes (AJ577461.1), and the sequence was deposited into GenBank. Conclusion The present study describes H. longistipes morphologically and molecularly which facilitates further discrimination of this species worldwide.
Article
Accurate measures of nematode fecundity can provide important information for investigating parasite life history evolution, transmission potential, and effects on host health. Understanding differences among fecundity assessment protocols and standardizing methods, where possible, will enable comparisons across different studies and host and parasite species and systems. Using the trichostrongyle nematode Cooperia fuelleborni isolated from wild African buffalo (Syncerus caffer), we compared egg recovery and enumeration between two methods for measuring the fecundity of female worms. The first method, in utero egg count, involves visual enumeration of the eggs via microscopic inspection of the uterine system. The second method, ex utero egg count, involves dissolving the same specimens from above in a sodium chloride solution to release the eggs from the female's uterus, then enumeration under an inverted microscope. On average, the ex utero method resulted in 34% more eggs than the in utero method. However, results indicate that the two methods used to quantify parasitic nematode fecundity are highly correlated. Thus, while both methods are viable options for estimating relative nematode fecundity, we recommend caution in undertaking comparative studies that utilize egg count data collected using different methods.
Chapter
History is the foundation that informs about the nuances of faunal assembly that are essential in understanding the dynamic nature of the host–parasite interface. All of our knowledge begins and ends with evolution, ecology and biogeography, as these interacting facets determine the history of biodiverse systems. These components, relating to Haemonchus, can inform about the complex history of geographical distribution, host association and the intricacies of host–parasite associations that are played out in physiological and behavioural processes that influence the potential for disease and our capacity for effective control in a rapidly changing world. Origins and evolutionary diversification among species of the genus Haemonchus and Haemonchus contortus occurred in a complex crucible defined by shifts in environmental structure emerging from cycles of climate change and ecological perturbation during the late Tertiary and through the Quaternary. A history of sequential host colonization associated with waves of dispersal bringing assemblages of ungulates from Eurasia into Africa and processes emerging from ecosystems in collision and faunal turnover defined the arena for radiation among 12 recognized species of Haemonchus. Among congeners, the host range for H. contortus is exceptionally broad, including species among artiodactyls of 40 genera representing 5 families (and within 12 tribes of Bovidae). Broad host range is dramatically reflected in the degree to which translocation, introduction and invasion with host switching, has characterized an expanding distribution over time in North America, South America, southern Eurasia, Australia and New Zealand, coincidental with agriculture, husbandry and global colonization by human populations driven particularly by European exploration after the 1500s. African origins in xeric to mesic habitats of the African savannah suggest that historical constraints linked to ecological adaptations (tolerances and developmental thresholds defined by temperature and humidity for larval stages) will be substantial determinants in the potential outcomes for widespread geographical and host colonization which are predicted to unfold over the coming century. Insights about deeper evolutionary events, ecology and biogeography are critical as understanding history informs us about the possible range of responses in complex systems under new regimes of environmental forcing, especially, in this case, ecological perturbation linked to climate change. A deeper history of perturbation is relevant in understanding contemporary systems that are now strongly structured by events of invasion and colonization. The relaxation of abiotic and biotic controls on the occurrence of H. contortus, coincidental with inception and dissemination of anthelmintic resistance may be synergistic, serving to exacerbate challenges to control parasites or to limit the socioeconomic impacts of infection that can influence food security and availability. Studies of haemonchine nematodes contribute directly to an expanding model about the nature of diversity and the evolutionary trajectories for faunal assembly among complex host–parasite systems across considerable spatial and temporal scales.
Chapter
Diagnosis is often equated with identification or detection when discussing parasitic diseases. Unfortunately, these are not necessarily mutually exclusive activities; diseases and infections are generally diagnosed and organisms are identified. Diagnosis is commonly predicated upon some clinical signs; in an effort to determine the causative agent, identification of genera and species is subsequently performed. Both identification and diagnosis play critical roles in managing an infection, and involve the interplay of direct and indirect methods of detection, particularly in light of the complex and expanding problem of drug-resistance in parasites. Accurate and authoritative identification that is cost- and time-effective, based on structural and molecular attributes of specimens, provides a foundation for defining parasite diversity and changing patterns of geographical distribution, host association and emergence of disease. Most techniques developed thus far have been grounded in assumptions based on strict host associations between Haemonchus contortus and small ruminants, that is, sheep and goats, and between Haemonchus placei and bovids. Current research and increasing empirical evidence of natural infections in the field demonstrates that this assumption misrepresents the host associations for these species of Haemonchus. Furthermore, the capacity of H. contortus to utilize a considerably broad spectrum of ungulate hosts is reflected in our understanding of the role of anthropogenic forcing, the ‘breakdown’ of ecological isolation, global introduction and host switching as determinants of distribution. Nuanced insights about distribution, host association and epidemiology have emerged over the past 30 years, coincidently with the development of increasingly robust means for parasite identification. In this review and for the sake of argument, we would like to delineate the diagnosis of haemonchosis from the identification of the specific pathogen. As a foundation for exploring host and parasite biology, we will examine the evolution of methods for distinguishing H. contortus from other common gastrointestinal nematodes of agriculturally significant and free-ranging wild ruminants using morphological, molecular and/or immunological methods for studies at the species and genus levels.
Article
Haemonchus longistipes is a gastrointestinal abomasal nematode which is one of the most prevalent and pathogenic parasites infesting the stomach of ruminants. On the basis of light and ultrastructural data, the objective of the present study was to introduce a first identification of the cameline haemonchosis caused by H. longistipes. Abomasa of 42 Egyptian camels Camelus dromedarius (Artiodactyla: Camelidae) were collected monthly from September 2013 to April 2014 from the main slaughter house of Cairo, Egypt. Adult male and female nematode worms were recovered from 26 (62 %) specimens of the examined abomasa. The parasites were of yellow color; the body was filiform (slender) tapered towards the anterior end in male and towards both ends in female. Buccal capsules absent, the buccal cavity was small with a conspicuous dorsal lancet extended from dorsal wall. The cervical papillae were prominent and spine-like. The body length of the female worm was 16.6-20.5 (18.5 ± 0.3) mm. The anterior end to the cervical papillae was 3.19-4.30 (4.12 ± 0.5) mm. The vulva of the female had a linguiform process or flap, the tail is without a spine, and the anal pore at the posterior end of the body had a simple dorsal rim. The body of male was 10.4-14.7 (13.9 ± 2.0) mm in length. The male bursa had elongated lobes supported by long, slender rays. The small dorsal lobe was asymmetrical with Y-shaped dorsal rays. The spicules were long with a length of 0.52-0.54 (0.53 ± 0.05) mm, each provided with a small barb and pore near its extremity. Synlophe was bilaterally and dorsoventrally symmetrical; it extended from cephalic expansion over anterior 50 % of prebursal or prevulvar body and consisted of a maximum of 42 ridges. The described species herein was compared with the three morphologically similar species Haemonchus mitchelli, Haemonchus okapiae, and H. longistipes with their synlophes consist of 42 ridges distributed over the anterior half of the body. These species can be separated by unique structural characteristics of their synlophes, spicules, and copulatory bursa. The most morphologically similar species to the recovered worm was H. longistipes. Also, some of the parameters with regard to morphology and morphometry of this parasite were described for the first time.
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A young male giraffe (Giraffa camelopardalis) recently acquired by the Lion Country Safari in Loxahatchee, Florida, was diagnosed and successfully treated for Haemonchus infection while in quarantine. Seven weeks after introduction into a group of resident giraffes, this giraffe presented with diarrhea. Fecal evaluation revealed an extremely high count of 16,700 eggs/g, with larval identification of the parasite as Haemonchus. A larval development assay showed resistance to the three classes of anthelmintics currently used to treat Haemonchus contortus: the benzimidazoles, imidazothiazoles, and macrocyclic lactones. The giraffe was treated with a combination of moxidectin topically and fenbendazole orally, and follow-up fecal examination 2 wk later showed a marked reduction in strongyle-type eggs. However, within 2 mo the giraffe had a packed cell volume of 22% and an eggs per gram count of 11,900. The animal was then treated with moxidectin topically and copper oxide wire particles orally and removed from the contaminated area. Because of the unusual host, molecular analysis of the parasite was employed, which confirmed the nematode as H. contortus. It is likely that the monthly rotational deworming schedule first implemented more than 5 yr earlier contributed to the development of multiple anthelmintic resistance in this H. contortus population. The proper use of anthelmintics and good pasture management are crucial to reducing the parasite burden in captive giraffe.
Article
A species of Ashworthius is reported for the first time in the Western Hemisphere, and A. patriciapilittae n. sp. is described on the basis of specimens in white-tailed deer Odocoileus virginianus from Costa Rica. Among 8 known species, A. patriciapilittae is morphologically similar to A. tuyenquangi in red muntjac Muntjacas muntjak from northern Vietnam. The synlophe in A. patriciapilittae is composed of 26 ridges in the cervical zone and is continuous to the caudal extremity in males and females. Males are characterized by a complex dorsal ray and narrow trifurcate spicules (351-356 microm long) lacking an "eyelet." with dissimilar ventral and dorsal processes; the gubernaculum is 45-48% of the spicule length. Females have a prominent linguiform flap at the vulva and large eggs (108-142 microm long). The presence of A. patriciapilittae in Costa Rica is examined in the context of competing hypotheses for cospeciation or contemporary host-switching in cervids: either A. patriciapilittae is a component of an endemic Central and South American fauna that has diversified through coevolution of Ashworthius and cervid hosts or it has been introduced. Among haemonchines in the Western Hemisphere, specimens of A. patriciapilittae may be confused with 3 species of Haemonchus, including H. contortus, H. placei, and H. similis, that occur in both domestic and wild ruminants. Discovery of A. patriciapilittae emphasizes the continued need for survey and inventory to define the structure and distribution of parasite faunas in wild and domestic ruminants from the Nearctic and Neotropical regions.
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The use of ovejector structure in the phylogeny of the Haemonchinae is hampered by differences among nematologists in the application of terminology and the recognition of homologous parts. Some workers recognize a sphincter with 2 parts, but others recognize only the proximal, rounded part of the sphincter and include the distal cylindrical part of the sphincter with the vestibule. The results of this study demonstrate that all sphincters of Haemonchinae of ruminants have 2 parts. To encourage the application of a uniform terminology to homologous parts of the ovejector, we propose the use of the terms "sphincter 1" for the rounded part and "sphincter 2" for the cylindrical part. It is hoped that clarification of the terminology for ovejectors of the Haemonchinae will provide a model useful for improving descriptions of ovejectors throughout the Trichostrongyloidea.
Article
Phylogenetic analysis of 25 morphological characters among the 12 species of Haemonchus resulted in 1 most parsimonious tree (60 steps; consistency index = 0.67, retention index = 0.80). Monophyly for Haemonchus was diagnosed by 3 unequivocal synapomorphies, including the asymmetric origin of the dorsal ray, relative size of the ventral rays, and the presence of a barb on each spicule tip. Species of Haemonchus have complex histories with respect to host and geographic associations: (1) origins in Africa with basal diversification in antelopes (H. krugeri, H. lawrencei, H. dinniki, H. horaki), (2) independent events of colonization for those species in Caprini and Bovinae (H. contortus, H. placei, H. bedfordi, H. similis), (3) colonization and development of core host associations within Camelidae (H. longistipes) and among Antilopinae, Tragelaphini, and Giraffidae (H. mitchelli, H. okapiae, H. vegliai), and (4) geographically widespread species that are represented only by those that have been translocated with domestic stock. The North American fauna is characterized by 3 introduced and exotic species, H. placei, H. contortus, H. similis, which emphasizes the importance of continued documentation of faunal diversity in the context of predictive foundations derived from phylogenetic studies. Satellite associations for species of Haemonchus, particularly among Cervidae and Camelidae in the Neotropics and Cervidae, Antilocapridae, and possibly wild Caprinae in the Nearctic, have been a consequence of introductions and exchange of parasites at historical interfaces for managed and natural ecosystems. Such distributions are emblematic of the overriding significance of anthropogenic factors as determinants of the global distributions for pathogenic parasites in domestic and wild ruminants.
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During three seasonal periods, parasitological samples were collected from six giraffes (Giraffa camelopardalis angolensis) in the Etosha National Park, Namibia. The helminths recovered included Parabronema skrjabini, Skrjabinema spp., Haemonchus mitchelli and Echinococcus sp. larvae; Cytauxzoon sp. was the only hematozoan found. The low mean abundances of all helminths which ranged from 18 to 531 may be attributed to the low rainfall of this region or because the giraffe is not a preferred host for these species of helminths.
Article
Only nine species of the genus Haemonchus are considered valid, namely, H. contortus (Rudolphi, 1803) Cobb, 1898 (type), H. bedfordi Le Roux, 1929, H. dinniki Sach, Gibbons & Lweno, 1973, H. krugeri Ortlepp, 1964, H. lawrencei Sandground, 1933, H. longistipes Railliet & Henry, 1909, H. mitchelli Le Roux, 1929, H. similis Travassos, 1914 and H. vegliai Le Roux, 1929. These are redescribed. H. bispinosus Molin, 1860, H. placei Place, 1893, H. cervinus Baylis & Daubney, 1922, H. okapiae van den Berghe, 1937 (in part), H. tartaricus Evranova, 1940, H. contortus contortus Das & Whitlock, 1960, H. contortus cayugensis Das & Whitlock, 1960, H. contortus bangalorensis Rao & Rahman, 1967, H. contortus hispanicus Martnez Gmez, 1968, H. contortus kentuckiensis Sukhapesna, 1974 and H. contortus var. uktalensis Das & Whitlock, 1960 are considered synonyms of H. contortus (Rudolphi, 1803) Cobb, 1898.The synonymy of H. lunatus Travassos, 1914, H. atectus Lebedev, 1929, H. pseudocontortus Lebedev, 1929 and H. fuhrmanni Kamensky, 1929 with H. contortus is confirmed. H. okapiae van den Berghe, 1937 (in part) is considered a synonym of H. mitchelli Le Roux, 1929 and H. bubalis Chauhan & Pande, 1968 is considered a synonym of H. similis Travassos, 1914. H. bovis Bonelli, 1941 and H. contortus var. kashmirensis Fotedar & Bambroo, 1965 are considered species inquirendae. An illustrated key to the species of the genus is provided.
Article
Established adult infections of Haemonchus contortus in sheep were found to exclude the establishment of H. placei given at dose levels of either 500 or 1500 larvae per week for at least 8 weeks. However, established infections of adult H. placei could not exclude H. contortus. At dose levels of 500 H. contortus larvae per week the existing H. placei infections in sheep were gradually replaced, during which time considerable species hybridization occurred. Dose levels of 1500 H. contortus larvae per week led to the rapid dislodgement of H. placei and much less opportunity for hybridization. A second experiment confirmed that existing H. contortus infections could exclude H. placei and that incoming H. contortus larvae could dislodge H. placei. Furthermore, the exclusion or dislodgement of H. placei was abrogated by injecting the host with dexamethasone. It is proposed that in sheep H. contortus is using a host mediated response to limit their competitor H. placei and that the resulting exclusion and dislodgement of H. placei acts as a major pre-mating barrier to species hybridization.
Article
Prominent sublateral hypodermal chords (SHC) are described in Haemonchus spp. Four large SHC are located 1 muscle cell away from the lateral chords from the level of the middle of the esophagus to midbody. The SHC are largest in midbody and merge with the lateral chords at about 65% of the body length from the anterior end. With the aid of transmission electron microscopy, a band of nerve tissue was located parallel and medial to the SHC. Haemonchus spp. and Mecistocirrus digitatus have SHC that are so large they can be identified in thick freehand midbody cross sections cut with a cataract knife. Because SHC have not been described in other Trichostrongylidae, their presence in members of the Haemonchinae may have value as a systematic character.
Article
The large stomach worms Haemonchus contortus, Haemonchus placei, and Haemonchus similis are important pathogens of cattle and sheep. This paper describes characteristics of surface cuticular ridges (synlophe), which for the first time provide morphological criteria for identifying individual adult specimens of either sex. The diagnostic patterns of the synlophe on the anterior half of specimens can be observed at 400x in temporary mounts on glass slides. The synlophe can be studied in cleared preserved specimens or in living or freshly thawed frozen specimens mounted in water. The synlophe of H. contortus has 30 ridges in the region of the posterior half of the esophagus, 4 fewer than H. placei and H. similis. The 4 extra ridges of H. placei and H. similis are consistently located bilaterally to the 3 ventralmost and the 3 dorsalmost ridges. The 4 extra ridges of H. similis extend to the end of the synlophe posterior to midbody, but in H. placei they extend posteriorly only to the end of the anterior quarter of the nematode. A key is included to the 3 species of Haemonchus parasitic in domestic sheep and cattle using characteristics of spicules, female reproductive system, female tail, and the synlophe.
Article
An easy and rapid tool for the individual identification of Haemonchus species in domestic ruminants might be very useful in the study of natural populations, especially when two (or three) species are sympatric. Techniques based on cytology, cuticular-ridge patterns, sublateral hypodermic chords, or molecular biology allow species identification but are either expensive or time-consuming. Therefore, a discriminant function combining three measures of male spicules was established from experimental infections with H. contortus in both sheep and goats and with H. placei in zebu. The discriminant function was evaluated on individual worms and on average values obtained in natural and experimental populations throughout the world. It was compared with a previously established function. The use of our function permitted better species identification for all Haemonchus species of ruminants, including H. longistipes from camels and H. similis from cattle.
Article
The trial was carried out to investigate parasite host specificity and to analyse the dynamics of infection with nematodes parasitizing sheep and cattle raised together or separately in São Paulo state, Brazil, and, also to clarify doubts about the systematics of species of the genus Haemonchus on the basis of cytological and morphological studies. Ten steers and 32 ewes were randomly assigned to three paddocks (P), as follows: P1, 5 steers; P2, 5 steers and 16 ewes; and P3, 16 ewes. The animals remained on these paddocks in continuous grazing throughout the trial (1-yr period). Faecal exams and larvae counting on pasture were performed fortnightly. Once a month two tracer lambs were placed in each paddock, while two tracer calves were also placed, but only in the eighth month of the trial. All these animals were slaughtered for worm identification and counting. At the end of the trial, one steer and one ewe from P2, which showed high faecal egg counts, were also slaughtered for the same purpose. Nematodes identified cytogenetically as H. placei presented spicule hooks longer than those identified as H. contortus. The following distribution of parasites in cattle and sheep was observed: Bunostomum phlebotomum, H. similis, Mammomonogamus laryngeus strongly adapted to cattle, H. placei and Cooperia punctata more adapted to cattle than to sheep, Trichostrongylus axei and C. spatulata apparently more adapted to cattle, T. colubriformis strongly adapted to sheep, H. contortus more adapted to sheep than to cattle and C. curticei apparently more adapted to sheep. Cross-infection was shown to occur involving some species, however, with time the animals apparently eliminate the species that are not well adapted to them. Therefore, grazing management systems using cattle and sheep appear to be promising for worm control in southeastern Brazil.
Article
The pattern of longitudinal ridges (synlophe) on the external cuticular surface of trichostrongylid nematodes has been shown to be of value for distinguishing species and determining relationships among higher taxa. In the process of studying Mecistocirrus digitatus, the large stomach worm of bovids of Asia that has been imported and established in the Americas, we observed remarkably similar synlophe patterns to those described for 3 species of Haemonchus and to those we examined in a species of Ashworthius. In all 3 genera, the synlophe is absent from the posterior part of the body. Only in Haemonchus does the synlophe extend beyond midbody. In both M. digitatus and Ashworthius sidemi, the synlophe extends posteriorly only about 1/4 of body length. In all 3 genera, the synlophe consists of about 30 ridges in the region of the esophagus with variation among species in specific areas, including additional pairs of subventral and subdorsal ridges and different lengths of sublateral ridges. This information is useful for identifying species and determining relationships among these large stomach worm parasites of cattle, sheep, goats, and farmed and wild cervids.
Article
In the course of a revision of species of Haemonchus Cobb, 1898 (Nematoda), commonly referred to as large stomach worms and significant pathogens of ruminants, a new species was discovered in the grey rhebuck Pelea capreolus, and the bontebok Damaliscus pygarthus, in South Africa. The new species, Haemonchus horaki, was previously reported as a long-spicule form of H. contortus (Rudolphi, 1803) Ransom, 1911. The new species, compared with H. contortus, can be distinguished by significantly longer spicules (555-615 microm vs. 383-475 microm); a synlophe with fewer ridges (26 vs. 30 in the region of the posterior part of the esophagus) that extend more posteriorly (within 1 mm of the copulatory bursa in males and postvulvar in females, vs. 2/3 to 3/4 of prebursal and prevulvar lengths); and an asymmetrical dorsal lobe with a long dorsal ray divided for more than half of its length, forming 2 branches of unequal length (vs. a dorsal ray divided for less than half of its length and forming 2 equal branches in H. contortus).