Abomasal parasites in wild sympatric cervids, red deer, Cervus elaphus and fallow deer, Dama dama, from three localities across central and western Spain: relationship to host density and park management

A survey of abomasal parasites in cervids from Central Spain was conducted at 3 sites, Quintos de Mora (Toledo), Malué?ez de Arriba (Cáceres), and La Herguijuela (Cáceres). Commonly occurring helminths belonged to 3 polymorphic species of the Ostertagiinae: Spiculopteragia asymmetricalS. quadrispiculata, Ostertagia leptospicularis/O. kolchida, and O. drozdzi/O. ryjikovi. Trichostrongylus axei was found in very few cases. Ostertagia drozdzi/O. ryjikovi and the minor male morphotype, S. quadrispiculata, are reported for the first time in red deer from Spain. The 3 ostertagiine species are also reported for the first time in fallow deer from Spain. These 3 species of Ostertagiinae are primarily parasites of cervids, and nematode species characteristic of domestic ruminants were not present. Prevalence of infection by gastrointestinal parasites in cervids was high, ranging from 97.5 to 100%, across the 3 areas sampled. Mean intensity of infection and abundance showed a positive relationship to the population density of red deer. Helminth burdens were higher in fallow deer than in the sympatric red deer and may reflect the gregarious social structure and different foraging patterns of fallow deer.     

Emended description and redetermination of Sarwaria caballeroi n. comb. (nematoda: Ostertagiinae) with details of the synlophe and esophageal characters

Among genera of the ostertagiine nematodes, structural attributes of Spiculopteragia caballeroi are consistent with criteria that diagnose the genus Sarwaria. Specifically, the following characters are compatible with referral to this genus: (1) species characterized by monomorphic males; (2) tapering lateral synlophe in the cervical zone; (3) minuscule, thornlike cervical papillae; (4) length of Ray "4" < Ray "5"; (5) relatively thick or robust Ray "4"; (6) a substantially reduced dorsal lobe and dorsal ray that are disposed or curved ventrally relative to Rays "8"; and (7) a broad, laterally inflated dorsal lobe. Consequently, we propose Sarwaria caballeroi n. comb., and we provide further validation for the genus Sarwaria. Additionally, we propose that the ostertagiines are represented by 12 valid genera, including those characterized by a bursal formula of 2-2-1 (Cervicaprastrongylus, Hyostrongylus, Mazamastrongylus, Spiculopteragia, and Teladorsagia in addition to Sarwaria), and those in which the lateral rays describe a 2-1-2 pattern (Camelostrongylus, Longistrongylus, Marshallagia, Orloffia, Ostertagia, and Pseudomarshallagia).     

Distribution of Spiculopteragia pursglovei and S. odocoilei (Nematoda: Trichostrongyloidea) from white-tailed deer (Odocoileus virginianus) in the southeastern United States

The distribution of Spiculopteragia pursglovei (= Apteragia pursglovei) and S. odocoilei (= A. odocoilei) in 12 southeastern states was determined after examining the abomasal contents of 1,369 white-tailed deer over an 8-yr period. Spiculopteragia odocoilei was encountered with much greater frequency than S. pursglovei except in some areas along the Mississippi River drainage and the coasts of North Carolina and South Carolina. In instances where both parasites were found in a population, one usually expressed a dominance in both prevalence and intensity. These findings are in agreement with those of an earlier study conducted in the southeastern United States.     

Abomasal nematodes of the red deer Cervus elaphus in north-eastern Italy

The composition of the abomasal helminth fauna and parasite diversity were studied in 298 red deer collected during 1997-2000 from three different sectors (Bolzano, Trento and Sondrio provinces) of the Stelvio National Park, one of the main protected areas of north-eastern Italy. The association between parasite burdens and geographical areas of the hosts was assessed using the negative binomial regression. A variety of abomasal helminths, both host specific and generalist, was found in all sectors. The most commonly observed parasites were the Spiculopteragia spiculoptera morph spiculoptera and Ostertagia leptospicularis morph leptospicularis, with prevalences of 79.5% and 40.9%, respectively. The minor morphs S. spiculoptera morph mathevossiani (prevalence 31.9%) and O. leptospicularis morph kolchida (18.8%) occurred at lower prevalences. Teladorsagia circumcincta morph circumcincta, Marshallagia marshalli morph marshalli and Haemonchus contortus were rarer, at prevalences of 1, 1.3 and 1.3%, respectively. Deviance analysis of the negative binomial regression model shows that the geographical area is significantly related to parasite burdens (P = 0.001). Prevalences of hosts with parasites were greater in the Sondrio (odds ratio = 1.31; 95% confidence interval: 0.16-10.85) and smaller in the Trento (odds ratio = 0.62; 95% confidence interval: 0.20-1.96) sectors with respect to Bolzano, but these differences were not statistically significant. Possible cross-infections by more generalist parasites between wild and domestic animals were also suggested, as deer and domestic ruminants (Bovinae, Caprinae and Ovinae) used the same feeding areas of the park sectors.     

Metagenome plasticity of the bovine abomasal microbiota in immune animals in response to Ostertagia ostertagi infection

Infections in cattle by the abomasal nematode Ostertagia ostertagi result in impaired gastrointestinal function. Six partially immune animals were developed using multiple drug-attenuated infections, and these animals displayed reduced worm burdens and a slightly elevated abomasal pH upon reinfection. In this study, we characterized the abomasal microbiota in response to reinfection using metagenomic tools. Compared to uninfected controls, infection did not induce a significant change in the microbial community composition in immune animals. 16S rRNA gene-based phylogenetic analysis identified 15 phyla in the bovine abomasal microbiota with Bacteroidetes (60.5%), Firmicutes (27.1%), Proteobacteria (7.2%), Spirochates (2.9%), and Fibrobacteres (1.5%) being the most predominant. The number of prokaryotic genera and operational taxonomic units (OTU) identified in the abomasal microbial community was 70.8±19.8 (mean ± SD) and 90.3±2.9, respectively. However, the core microbiome comprised of 32 genera and 72 OTU. Infection seemingly had a minimal impact on the abomasal microbial diversity at a genus level in immune animals. Proteins predicted from whole genome shotgun (WGS) DNA sequences were assigned to 5,408 Pfam and 3,381 COG families, demonstrating dazzling arrays of functional diversity in bovine abomasal microbial communities. However, none of COG functional classes were significantly impacted by infection. Our results demonstrate that immune animals may develop abilities to maintain proper stability of their abomasal microbial ecosystem. A minimal disruption in the bovine abomasal microbiota by reinfection may contribute equally to the restoration of gastric function in immune animals.     

Hamulonema gen. nov. for Teladorsagia hamata and Ostertagia kenyensis in the ostertagiine fauna (Nematoda: Trichostrongyloidea) from African ungulates

Hamulonema gen. nov. is proposed for Teladorsagia hamata and Ostertagia kenyensis in the ostertagiine nematode fauna found in artiodactyl hosts from Africa. Monomorphic species representing this genus are characterized by a bilaterally symmetrical and parallel synlophe in males and females, a 2-2-1 bursal formula, an accessory bursal membrane that is strongly cuticularized and reduced, a strongly reduced dorsal lobe and ray, and robust spicules with a simple, weakly pointed, ventral process, and curved, hooklike dorsal process. Species referred to Hamulonema nov. gen. are immediately distinguished from those of Camelostrongylus, Longistrongylus, Marshallagia, Orloffia, Ostertagia, and Pseudomarshallagia in which the bursal formula is 2-1-2 in males. Hamulonema nov. gen. is distinguished from those genera having a 2-2-1 bursa, including Africanastrongylus, Cervicaprastrongylus, Hyostrongylus, Mazamastrongylus, Sarwaria, Spiculopteragia, and Teladorsagia by the structure of the synlophe, bursa, genital cone, "0" and "7" papillae, dorsal lobe, and spicules in specific instances. In the global fauna, 4 of 14 ostertagiine genera are endemic to Africa. African genera may represent morphologically divergent and discrete or historically isolated lineages reflecting a pattern of geographic and host colonization as a driver for diversification since the Miocene.     

L3 and adult Ostertagia (Teladorsagia) circumcincta exhibit cyanide sensitive oxygen uptake

Oxygen consumption by L3 and adult Ostertagia (Teladorsagia) circumcincta was examined in vitro to determine whether oxygen can be utilised in metabolism. The oxygen concentration in the abomasal fluid of sheep infected with O. circumcincta was also measured. Rates of consumption (in nmol O2/h/1000 worms) were 13+/-1 in sheathed L3, 34+/-6 in ex-sheathed L3, and 1944+/-495 in adult worms. Constant rates of consumption were maintained until media oxygen concentration dropped to between 10 and 20 microM. Consumption was inhibited 95% by cyanide in L3 and 74% in adults. Oxygen concentration in abomasal fluid varied between 10 and 30 microM in both infected and uninfected animals. During infection, oxygen concentration decreased slightly with increased abomasal pH, though the correlation between the two was poor (r=-0.30). In conclusion, O. circumcincta can consume oxygen and oxygen concentration at the infection site is sufficient to support at least some aerobic metabolism.     

Identical ITS-1 and ITS-2 sequences suggest Spiculopteragia asymmetrica and Spiculopteragia quadrispiculata (Nematoda: Trichostrongylidae) constitute morphologically distinct variants of a single species

Sequences of ITS-1 and ITS-2 rDNA for adult males of Spiculopteragia asymmetrica and Spiculopteragia quadrispiculata in red deer (Cervus elaphus) were determined. They were found to be identical, suggesting that S. asymmetrica and S. quadrispiculata represent a single species and do not refute the concept of dimorphic species in the Spiculopteragia.     

Identification by polymerase chain reaction (PCR) of Marshallagia marshalli and Ostertagia gruehneri from Svalbard reindeer

A polymerase chain reaction (PCR) assay to identify two common abomasal nematodes Marshallagia marshalli and Ostertagia gruehneri of Svalbard reindeer was developed. Species-specific PCR primers were designed from internal transcribed spacer (ITS)-2 sequences of rDNA and validated using morphologically identified adult male and female nematodes. Using the species-specific primers, a 110 bp fragment was amplified from M. marshalli and its minor morph Marshallagia occidentalis and a 149 bp fragment was amplified from Ostertagia gruehneri and its minor morph Ostertagia arctica. No PCR products were amplified from the third rare species, Teladorsagia circumcincta, or DNA from the reindeer host. The assay provides a useful tool to estimate species composition for both sexes in this nematode community.     

Influence of host weight, sex and reproductive status on helminth parasites of the wild rabbit, Oryctolagus cuniculus, in Navarra, Spain.

A study was carried out in Navarra (northern Spain) on the influence of the weight, sex and reproductive status (lactant, pregnant or lactant + pregnant females and testicular weight for males) of the wild rabbit (Oryctolagus cuniculus) on two cestodes species: Andrya cuniculi and Mosgovoyia ctenoides and four intestinal nematodes: Graphidium strigosum, Trichostrongylus retortaeformis, Nematodiroides zembrae and Dermatoxys hispaniensis. A significantly higher prevalence of A. cuniculi was detected in lactant + pregnant females compared with non-breeding females. Trichostrongylus retortaeformis and N. zembrae showed a significantly higher mean intensity in lactant and lactant + pregnant females than in non-reproductive females. Trichostrongylus retortaeformis presented a higher mean intensity in females than in males, and the mean intensity of the same parasite species was significantly lower in active and inactive males compared with lactant and lactant + pregnant females. There were no significant differences between sexes in the prevalence of helminth parasites. No significant correlation was detected between host weight and the intensity (of infection) of helminths studied. No significant differences in the prevalence and mean intensity of the two cestode species were observed in the three weight categories studied (kittens, juveniles and adults). The prevalence of G. strigosum and mean intensity of T. retortaeformis were significantly higher in older heavier animals than in juveniles.     

Population dynamics of Philureter trigoniopsis (Monogenea: Ancyrocephalinae) from urinary organs of Galaxias maculatus (Osmeriformes: Galaxiidae) in a cold temperate Andean Patagonian lake (Argentina)

Philureter trigoniopsis parasitizes the ureters and urinary bladder of Galaxias maculatus in Patagonian Andean lakes. To investigate factors associated with variation in the prevalence and intensity of this monogenean, fish were sampled periodically over 2 yr in Lake Gutiérrez. Prevalence and mean intensity are higher in smaller fishes than in larger ones. A seasonal pattern was observed, with peak recruitment and peak mean intensity occurring in early spring (September), followed by lows in late summer (January-February). Galaxias maculatus length classes are spatially segregated due to seasonal migrations, so the annual infection cycle is characterized by higher prevalence and intensity from late winter to early summer in the smaller fish from the deep zone of the lake.     

Skeletal evidence of probable treponemal infection in free-ranging African apes

The prevalence and patterning of inflammatory lesions of the skeleton were investigated in samples of chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) curated at the Powell-Cotton Museum, Birchington, UK. One hundred and two chimpanzees (42 adults and 60 subadults) and 126 gorillas (50 adults and 76 subadults) comprise the samples. Twenty per cent of chimpanzees and 14% of gorillas were affected with a disseminated inflammatory skeletal condition caused by infection. The lesions appear to have originated as localized patches of new bone deposition on the surface of long bones and to have progressed to infection of the bone cortex and marrow. Although female prevalence of involvement exceeds that of males in both species, the differences are not statistically significant. The age distribution of affected animals indicates that the disease began in some animals as early as 2 yr of age. Given the skeletal and demographic prevalence and patterning of the lesions as well as the ecology and behavior of these animals, the most likely diagnosis of the condition is a yaws-like treponemal infection.     

Spatio-temporal dynamics of the parasitic nematode Anguillicola crassus in Flanders, Belgium

Despite Egusa's earlier warning of the damage that the parasitic nematode Anguillicola crassus could inflict on the European eel Anguilla anguilla, its introduction in Europe was a fact in the early 1980s. Based on an elaborate dataset on Anguillicola crassus infection of 11 river catchments, this paper presents the results of a detailed study on the dispersal of the parasite in Flanders, Belgium, and the host-parasite relationship. In addition, data from 1986 and 1997 are used for comparative purposes, providing a perspective on the temporal infection pattern over 15 yr. The presence of A. crassus in Flanders was first discovered in 1985; 2 yr later a survey revealed a prevalence of 34.1% and a mean infection intensity of 5.5, based on adult nematodes only, and 10 yr later the parasite was present at all 11 sites sampled. Prevalence had increased to 62.5 % but the mean infection intensity had decreased to 3.9 adults per infected eel. Finally, in the year 2000, a third study revealed that A. crassus was present in 139 of 140 investigated sites; a further increase in prevalence to 68.7% and a decrease in mean infection intensity to 3.4 adults per infected eel was observed. When all larval stages were taken into account, mean prevalence amounted to 88.1% and mean intensity to 5.5 adults. The high infection level in Flanders is thought to be the result of restocking with glass eel and yellow eel, both of which are susceptible to A. crassus. The general infection parameters were similar in all 11 river catchments. It is possible that in Flanders both prevalence and mean infection intensity are stabilizing due to density-dependent regulation of the parasite infrapopulation. Fibrotic swimbladder walls were observed, mainly in large eels, and 20% of the total number of nematodes consisted of encapsulated larvae in the surveys of 1997 and 2000; 8 cases of swimbladder regeneration were observed.     

Abomasal and small intestinal nematodes from captive gazelles in Spain

The abomasal and small intestinal helminth fauna of three species of captive gazelles (Gazella dama mhorr, G. cuvieri and G. dorcas neglecta) kept in captivity in Almería (southeast Spain) have been studied, and the following species were identified: Nematodirus spathiger, N. filicollis, N. helvetianus, Camelostrongylus mentulatus, Trichostrongylus vitrinus, T. probolurus, T. colubriformis, Ostertagia ostertagi, O. harrisi, Teladorsagia (Ostertagia) circumcincta, and T. (Ostertagia) davtiani. Camelostrongylus mentulatus and N. spathiger were the most prevalent and abundant parasites. Ostertagia ostertagi, O. harrisi, N. helvetianus, and T. (Ostertagia) davtiani were identified for the first time in the genus Gazella. In addition, O. harrisi and Trichostrongylus probolurus are new records for Spain.     

Susceptibility of Amblyomma americanum to natural and experimental infections with Theileria cervi

One hundred fifty Amblyomma americanum were examined between March and September 1986 from Cookson Hills Wildlife Refuge in eastern Oklahoma (USA). Of these ticks, 11% (17 of 150) were infected with Theileria cervi. Field-collected nymphal ticks had an 8% (3 of 37) prevalence of infection averaging 1.0 infected acini/nymph. Female ticks had a 16% prevalence of infection averaging 1.6 infected acini/female; T. cervi was not observed in salivary glands of field-collected male ticks. When laboratory reared A. americanum nymphs were allowed to feed on experimental white-tailed deer (Odocoileus virginianus) with varying T. cervi parasitemias (less than 1, 2, 6 and greater than 20%), only ticks which fed on deer with parasitemias greater than 1% became infected. Although prevalence and intensity of infection varied in the infected ticks, there was no significant difference in prevalence of infection between males and females. However, females did acquire significantly greater intensities than males. The data from these studies confirm that T. cervi overwinters in A. americanum and suggests that the prevalence, intensity and abundance of infection of T. cervi in ticks is influenced by the parasitemia of the deer host. Furthermore, fawns may play a more important role in the epidemiology of T. cervi transmission than do adult deer because of the coordination between tick activity patterns and deer fawning.     

An exploration of diversity among the Ostertagiinae (Nematoda: Trichostrongyloidea) in ungulates from Sub-Saharan Africa with a proposal for a new genus

Abomasal nematodes (Ostertagiine: Trichostrongyloidea) representing a previously unrecognized genus and species are reported in African buffalo (Syncerus caffer caffer) from Kenya, Uganda, and South Africa. Africanastrongylus buceros gen. nov. et sp. nov. is characterized by a symmetrical tapering synlophe in the cervical region and a maximum of 60 ridges in males and females. Bursal structure is 2-2-1, with subequal Rays 4/5, massive Rays 8, and Rays 9/10, and a massive dorsal lobe that is reduced in length, laterally and dorsally inflated, and positioned ventral to externodorsal rays. Spicules are tripartite, and the gubernaculum is broadly alate in the anterior. A proconus is present. Among ostertagiines with a 2-2-1 bursa (Cervicaprastrongylus, Hyostrongylus, Mazamastrongylus, Sarwaria, Spiculopteragia, and Teladorsagia) specimens of Africanastrongylus are differentiated from respective genera based on the structure of the cervical synlophe, patterns of dorsal, externodorsal, lateral, and ventral rays, and configuration of the genital cone, gubernaculum, and spicules. Among 13 genera of the Ostertagiinae in the global fauna, 3 are entirely limited in distribution to Africa, including Africanastrongylus, Longistrongylus, and Pseudomarshallagia. Another 5 genera including Cervicaprastrongylus, Hyostrongylus, Marshallagia, Ostertagia, and Teladorsagia are represented as mosaics, with diversity centered in Eurasia or the Holarctic. Genera not represented in the African fauna include Camelostrongylus among Caprinae and some Antelopinae from Eurasia, Mazamastrongylus and Spiculopteragia in Cervidae from the Holarctic and Eurasia, respectively, Orloffia in Cervidae and Bovidae from the Holarctic, and Sarwaria among Tragulidae and Bovinae in southern Asia. The diverse nature of the ostertagiine fauna, with a disproportionate number of endemic genera relative to other regions of the northern hemisphere, may reflect the timing of episodic expansion events for artiodactyls into Africa from Eurasia during the Tertiary and Quaternary.     

Low seroprevalence of Neospora caninum infection associated with the limousin breed in cow-calf herds in Andorra, Europe

Neospora caninum seroprevalence and risk factors affecting seroprevalence in beef cattle in Andorra were investigated. Antibodies to N. caninum were evaluated by enzyme-linked immunosorbent assay performed on a yearly basis in 1,758 animals older than 6 mo, belonging to 26 herds. Mean seroprevalence of antibodies to N. caninum for the herds was 7.4 +/- 1.2% (130/1,758). Logistic regression analyses were performed on data from each animal, considering N. caninum seropositivity as the dependent variable, and herd, grazing area, year of sampling, repeat-test animal (animals sampled twice or more), sex, breed, age (animals <4 yr old or > or =5 yr old), and country of birth as possible risk factors. Based on the odds ratio, the prevalence of infection was 2.1 times higher (P < 0.01) in animals from the Ordino grazing area, 1.64 times higher in animals older than 5 yr (P < 0.01), and 6.7 times (1/0.15) lower in Limousin-mixed Limousin cattle (P < 0.002). The results suggest that the particular grazing location could promote the horizontal transmission of this parasite and that certain breeds are less susceptible to N. caninum infection than others.     

Infection patterns in white sea blue mussels Mytilus edulis of different age and size with metacercariae of Himasthla elongata (Echinostomatidae) and Cercaria parvicaudata (Renicolidae)

Infection of mussels Mytilus edulis L. by 2 trematode species was studied in a natural intertidal population in the Chupa inlet of the White Sea. The prevalence of metacercariae of Himasthla elongata (Mehlis, 1831) and Cercaria parvicaudata (Stunkard & Shaw, 1931) in mussels reached 100% in 3 to 4 yr old molluscs and remained at this level in older individuals. Infection intensity increased evenly with the age of the molluscan host, showing a tendency to decrease only in the oldest (9 yr old) mussels. These patterns of age dynamics of prevalence and infection intensity were associated with accumulation of trematode larvae in the course of the molluscs' lives. Ability of metacercariae to exist in mussels for long periods (at least 2.5 yr) was verified in the course of an experiment, during which infected molluscs were kept in a subtidal net cage. Decrease of infection intensity in the oldest individuals may reflect selective mortality of the most severely infected molluscs. Among mussels of the same age, higher infection intensity values occurred in larger individuals. This may be due to an enhanced pumping rate in large molluscs, which increases the probability of cercariae, free-living trematode larvae, infecting them via water currents.     

Epidemiology of Necator americanus hookworm infections in Xiulongkan Village, Hainan Province, China: high prevalence and intensity among middle-aged and elderly residents

Hookworm is highly endemic to Hainan Province, an island located in the South China Sea. To investigate the prevalence and intensity of infection in the area, the village of Xiulongkan was surveyed between April and July 1998. A cross-sectional study was conducted in which fecal samples of 80% of the village residents (631 individuals) were tested for the presence of helminth eggs. Hookworm was the predominant intestinal helminth in Xiulongkan, where it was determined that 60% of those tested were infected. Necator americanus was the predominant species of hookworm in this population. The prevalence of hookworm increased with age, and then leveled to a plateau for ages 41 yr and up. This observation was in contrast to infections with Ascaris lumbricoides, where the highest prevalences occurred among school-aged children. Women had a significantly higher prevalence of hookworm than men and this difference emerged in early adulthood. The intensity of hookworm infection also significantly increased with age, with the highest intensity infections occurring among middle-aged and elderly residents. Females were more likely to have moderate or heavy infections, whereas males were more likely to have light infections. The rates of hookworm transmission are particularly high among the middle-aged and elderly residents of Xiulongkan.     

Study of perkinsosis in the carpet shell clam Tapes decussatus in Galicia (NW Spain). II. Temporal pattern of disease dynamics and association with clam mortality

Temporal dynamics of the infection by Perkinsus olseni in a clam (Tapes decussatus) bed was studied over 5 yr (March 1996 to December 2000). Diagnostic techniques were compared to assess their suitability for epizootiological purposes. A technique based on incubation of 2 gill lamellae in Ray's fluid thioglycollate medium (RFTM) was more sensitive, quicker and cheaper than examination of histological sections. Incubation of the whole-clam soft tissues in RFTM allowed detection of very light infections that were not detected with incubation of only 2 gill lamellae. Nevertheless, the correlation between the infection intensity estimated by both RFTM incubations was high. Infection intensity was significantly and positively correlated with clam size/age. No infected clam smaller than 20 mm was found. There was an annual pattern of infection involving lower mean infection intensity and prevalence in winter and higher values for both variables from spring to autumn, with 2 main annual peaks in spring and late summer-early autumn. This temporal pattern was significantly associated with the seawater temperature. The annual spring peak of infection intensity occurred when seawater temperature was around 15 degrees C. Monthly mortality in the clam bed peaked in spring and summer--after peaks of P. olseni infection intensity and concurrently with high seawater temperature. A comparison of percentage mortality between clams from 2 sources (a perkinsosis-affected and a non-affected area) placed in the same clam bed revealed significantly higher mortality in the clams originating from the perkinsosis-affected area.