Corrigendum: A revision of the trichostrongylid nematode Cooperia Ransom, 1907, from deer game: recent integrative research confirms the existence of the ancient host-specific species Cooperia ventricosa (Rudolphi, 1809).

[This corrects the article DOI: 10.3389/fvets.2024.1346417.].

A revision of the trichostrongylid nematode Cooperia Ransom, 1907, from deer game: recent integrative research confirms the existence of the ancient host-specific species Cooperia ventricosa (Rudolphi, 1809).

The trichostrongylid roundworms of the genus Cooperia, which are important in veterinary medicine, currently comprise 19 valid species that parasitize the small intestine of both free-living and domestic ruminants. Only four Cooperia spp. have been reported in Europe, namely C. oncophora, C. punctata, C. curticei and C. pectinata. In 2018-2022, 25 red deer (Cervus elaphus) and 30 sika deer (Cervus nippon) of both sexes and various ages from several remote locations in the Czech Republic were parasitologically examined. Intestinal nematodes of the genus Cooperia were found only in two northern regions. Using the globally recognized key book on trichostrongylid nematodes, they were preliminarily identified as C. pectinata. However, a molecular analysis of cox2 and ITS rDNA gene sequences revealed that Cooperia sp. parasitizing Czech deer is a separate taxon that is more closely related to C. oncophora than to C. pectinata. A subsequent morphological analysis and literature survey confirmed the independence of deer Cooperia sp., which is similar but not identical to bovid C. pectinata. Previous long-term correct identifications of bovid C. pectinata and misidentifications of deer Cooperia species were caused by a fundamental error in the key book mentioned above. Interestingly, the ancient trichostrongylid nematode Strongylus ventricosus from the type host red deer (Cervus elaphus) shot near Greifswald (Germany) was described by Rudolphi in 1809. Rudolphi's type material (one male and four females) was deposited in the Museum für Naturkunde (Berlin). Later, the ancient species S. ventricosus was taken as a synonym for various Cooperia spp. Our current re-examination of the type male indicated that there is a relatively good agreement with our new material from Czech deer regarding the most important characteristics of S. ventricosus (i.e., the shape and size of the male spicules); however, Rudolphi's type material is in rather poor condition. The suggested resurrection of the deer Cooperia sp. in this study as Cooperia ventricosa (Rudolphi, 1809) requires verification by collecting and analyzing new nematode material from the type locality near Greifswald.

An alien parasite in a changing world - Ashworthius sidemi has lost its traditional seasonal dynamics.

A non-native nematode Ashworthius sidemi has emerged in captive fallow deer in Central and Eastern Europe over the last decade. Although this parasite has been spreading in the wild outside it's native distributional range and colonising local European host species since the middle of the last century, limited information has been published on the seasonality of A. sidemi and its susceptibility to anthelmintics. To address this knowledge gap, we conducted a study to investigate seasonal dynamics of the non-native parasite in the current Central European climate conditions. We collected freshly voided faecal pellets at four-week intervals from February 2018 to February 2020 at a fallow deer reserve with a known history of A. sidemi presence. The faecal pellets obtained were pooled after each site visit (n = 25) and coprocultured to obtain the third stage larvae of trichostrongylid nematodes at monthly intervals. Total genomic DNA was extracted from the recovered larvae. Using real-time multiplex PCR, A. sidemi DNA was detected in 17 out of 25 larval samples (68% prevalence). During the monitoring period, the annual administration of ivermectin based premix (Cermix) took place in January 2018, 2019, and 2020, and additionally a mixture of rafoxanide and mebendazole (Rafendazol) was administered once in spring 2019. The probability of parasite presence was significantly influenced by the time since the drug administration (p = 0.048) and the mean temperature at the location (p = 0.013). Larval samples negative for A. sidemi were always identified shortly after the drug administration. However, rapid pasture contamination by the parasite eggs from two to three months after Cermix administration and within one month after Rafendazol administration suggest only a short-lived efficacy of both administered drugs. The abundance of A. sidemi DNA was positively affected by mean temperature (p = 0.044) and remained relatively stable throughout the monitoring period, with the highest peak in August 2018 and 2019. Pasture contamination with A. sidemi eggs occurred almost all year round, with the exception of the beginning of 2018, 2019, and 2020. These findings indicate adaptation of a non-native parasite to the current climatic conditions of the Czech Republic resulted in negligible seasonal patterns of parasite egg shedding.

Non-native Nematode Ashworthius sidemi Currently Dominates the Abomasal Parasite Community of Cervid Hosts in the Czech Republic.

Ashworthius sidemi is an abomasal nematode typical for Asiatic cervids such as sambar (Rusa unicolor) or sika deer (Cervus nippon). This non-native parasite was introduced into Europe via sika deer in the late 19th and early 20th centuries. The current dynamic spread of this parasite amongst autochthonous wild cervids occurs independently of human activities, and A. sidemi has a negative impact on the health of wild ruminants and may pose a threat to the conservation of endangered wild ungulates and to livestock. This invasive parasite has been previously detected in the Czech Republic, but more accurate information on A. sidemi is required. Only limited information is generally available on the factors influencing the spread of abomasal nematodes in wild ruminants, so more information is necessary for planning effective strategies of parasite control. We therefore conducted a survey on the abomasal nematodes in cervids in both game reserves and hunting grounds across the Czech Republic, taking into account the hosts (species, age, sex) and environmental factors (monthly average temperature). The abomasa of 104 animals belonging to five cervid species originating from various locations of the country were collected. Data on host (species, sex, and age group) and the monthly average temperature in the region were obtained for each animal. The parasitological analyses indicated that 92% of the abomasa were infected by nematodes. Ashworthius sidemi was the most prevalent (72%) and abundant (80% of the total recovered individuals) nematode species and was detected in all cervid species except white-tailed deer. The intensity of A. sidemi was highest in roe deer (Capreolus capreolus) and fallow deer (Dama dama), but A. sidemi abundance did not depend substantially on the host or environmental factors. In contrast, the abundance of nematodes from the subfamily Ostertagiinae was influenced by the host species and temperature. Parasitic load was significantly higher in roe deer and during the warmer periods of the survey. We also detected another non-native nematode species, Spiculopteragia houdemeri. The results of our study suggest that the non-native nematode A. sidemi is now widespread amongst cervid hosts in the Czech Republic, probably due to the high sensitivity of autochthonous cervids to A. sidemi infections as well as adaptation of this parasite to the current climatic conditions of this country.

Effects of excessive dietary zinc or zinc/cadmium and tapeworm infection on the biochemical parameters in rats.

The main objective of this study was to determine which biochemical blood parameters can serve as indicators of Zn or Zn/Cd burden and tapeworm infection. This study was performed on 44 Wistar male rats during a 6-week period, when rats were or were not fed a zinc/cadmium rich diet and were or were not infected with tapeworms (Hymenolepis diminuta). Total protein, albumin, urea, glucose, triacylglycerols, non-esterified fatty acids, cholesterol, alkaline phosphatase, aspartate aminotransferase, uric acid, Mg, Ca, P and Zn levels were analysed. Control rats with tapeworm infection had significantly higher (p ≤ 0.05) total protein, urea and phosphorus concentrations than did rats unaffected by any experimental factor. Rats given overdoses of zinc lactate exhibited significantly lower glucose levels than did the other rats, especially those infected with tapeworms. Low glucose level in uninfected rats indicate a Zn overdose; high doses of zinc lactate likely decrease levels of glucose via cortisol, which is released during stress. Rats fed the Zn/Cd hyperaccumulating plant Arabidopsis halleri and infected with tapeworms had significantly higher (p ≤ 0.01) cholesterol and urea levels but lower zinc, triacylglycerol, and alkaline phosphatase levels than did rats fed the same diet but free of tapeworms. The increase of alkaline phosphatase level in uninfected rats may indicate both Zn/Cd burden and rat liver damage. Overall, this study not only supports the theory that H. diminuta can serve as a promising model for helminth therapy of the host mammal but also confirmed that this tapeworm is capable to protect somehow the host organism from the harmful effects of heavy metals.

Nematode-induced pathological lesions and alterations of mucin pattern identified in abomasa of wild ruminants.

Pathological lesions as well as mucin alterations in abomasa infected by nematodes have been thoroughly studied in livestock, but such data from wild ruminants are limited or completely lacking. Pathological data for Ashworthius sidemi, an invasive nematode are particularly rare. We necropsied the abomasa of 21 wild ruminants belonging to five cervid species and detected mixed nematode infections, dominated by A. sidemi. Samples from both gross lesions and mucous membranes without macroscopically apparent pathological alterations were subjected to standard histological procedures and histochemical staining. Histological examination found chronic abomasitis, manifested by edema, and hyperemia. Various degrees of lymphoplasmacytic infiltration were observed in all samples. Initial fibrosis (8/20, 40%) was detected in samples from both gross lesions and areas without macroscopically visible changes. Tissue from hemorrhagic lesions was superficially eroded. Generalized loss of surface polysaccharides was apparent in all samples. Only residual periodic acid-Schiff and Alcian blue (pH2.5) positivity was detected in the upper abomasal pits and in mucosal neck. This study found that nematode infections, mostly by A. sidemi, caused chronic inflammation and negatively affected abomasal mucin formation in wild ruminants.

The use of high resolution melting analysis of ITS-1 for rapid differentiation of parasitic nematodes Haemonchus contortus and Ashworthius sidemi.

Among gastrointestinal nematodes, haematophagous strongylids Haemonchus contortus and Ashworthius sidemi belong to the most pathogenic parasites of both domestic and wild ruminants. Correct identification of parasitic taxa is of crucial importance in many areas of parasite research, including monitoring of occurrence, epidemiological studies, or testing of effectiveness of therapy. In this study, we identified H. contortus and A. sidemi in a broad range of ruminant hosts that occur in the Czech Republic using morphological/morphometric and molecular approaches. As an advanced molecular method, we employed qPCR followed by High Resolution Melting analysis, specifically targeting the internal transcribed spacer 1 (ITS-1) sequence to distinguish the two nematode species. We demonstrate that High Resolution Melting curves allow for taxonomic affiliation, making it a convenient, rapid, and reliable identification tool.

Effects of tapeworm infection on absorption and excretion of zinc and cadmium by experimental rats.

The main objective of this study was to determine how rat tapeworms affect the excretion of zinc and cadmium through rat feces. Male rats (Rattus norvegicus var. alba) were divided into four groups, and the experiment was conducted over a 6-week period. The control groups (00; 0T) were provided with a standard ST-1 rodent mixture and received 10.5 mg of Zn/week. Groups P0 and PT were fed a mixture supplemented with the hyperaccumulating plant Arabidopsis halleri at a dosage of 123 mg Zn/week and 2.46 mg Cd/week. Groups 0T and PT were infected with the rat tapeworm (Hymenolepis diminuta). Fecal samples were collected 24 h post exposure. Zinc and cadmium concentrations in rat feces were analyzed using inductively coupled plasma optical emission spectrometry. Tapeworm presence decreased the amount of metals excreted through the feces of the host throughout the entire experiment, with the exception of 1 week (control group). No statistically significant differences between zinc excretion rates in the control groups (00 and 0T) were detected at any time throughout the experiment. A statistically significant difference between zinc excretion rates (p < 0.05) in the exposed groups (P0 and PT) was detected in 2 of the 6 monitored weeks. Group PT excreted significantly less cadmium (p < 0.01) than group P0 did in three of the 6 weeks. Overall, our results indicate that tapeworms are able to influence the excretion of metals by their host. Tapeworms accumulate metals from intestinal contents. It is not clear whether tapeworms carry out this process before the host tissues absorb the metals from the intestines or the tapeworms accumulate metals excreted from the body of the host back to the intestines. Most likely, it is a combination of both phenomena.

How tapeworm infection and consumption of a Cd and Zn hyperaccumulating plant may affect Cu, Fe, and Mn concentrations in an animal-a plant consumer and tapeworm host.

This study evaluated the effects of a hyperaccumulator plant (Arabidopsis halleri), containing surplus of cadmium (Cd) and zinc (Zn) and being an admixture to the rat feed, on concentrations of copper (Cu), iron (Fe), and manganese (Mn) in the tissues of experimental rats infected/uninfected with the tapeworm (Hymenolepis diminuta). Male Wistar rats were divided into three groups (00, P0, and PT); the P0 and PT animals were fed a standard mixture for rats (ST-1) supplemented with the plant A. halleri at a weekly Zn and Cd dosage of 123 and 1 mg, respectively. Moreover, rats from the group PT were infected with the tapeworm. The group 00 served as control animals fed only ST-1 having no tapeworm infection. Rats were euthanized after 6 weeks, and Cu, Fe, and Mn levels were determined in rat and tapeworm tissues. The results indicated that both the consumption of hyperaccumulator plant and/or presence of tapeworms did have significant effect on Cu, Fe, and Mn concentrations in the host tissues. Concentrations of all the elements were higher in the rat liver and partially kidneys than in the tapeworms, and the concentrations of Cu, Fe, and Mn were affected by the consumption of Cd/Zn hyperaccumulator plants. Particularly, Fe concentrations in all rat tissues were significantly increased by consumption of A. halleri while decreased by the presence of tapeworms. Overall, the consumption of a Cd/Zn hyperaccumulator plant and tapeworm infection cause an imbalance in Cu, Fe, and Mn concentrations in the tissues of a consumer (experimental rats).