Elsevier

Veterinary Parasitology

Volume 278, February 2020, 109038
Veterinary Parasitology

Research paper
Integrating the control of helminths in dairy cattle: Deworming, rotational grazing and nutritional pellets with parasiticide fungi

https://doi.org/10.1016/j.vetpar.2020.109038Get rights and content

Highlights

Abstract

Thirty-two Friesian cattle under a leaders/followers four-day rotation and passing eggs of trematodes and gastrointestinal nematodes (GIN) were studied in two trials for the integrated control of these helminths over two years. In the first trial, the effect of rotational pasturing was assessed on a group of leaders (milking cows, G-L1) and followers (dried-off cows and heifers, G-F1) supplemented daily with commercial nutritional pellets. In the second trial, leaders (G-L2) and followers (G-F2) were maintained under a rotational pasturing regime; the cows received daily commercial pelleted feed and heifers pellets manufactured with a blend of parasiticide fungi (3 × 105 chlamydospores of both Mucor circinelloides and Duddingtonia flagrans/kg pellet). Deworming via closantel and albendazole was performed in cows in each trial at the beginning of their drying periods, and fourteen days later, the fecal egg-count reductions (FECR) of Calicophoron daubneyi and GIN were from 94 to 100% (average 98 %), while the percentages of reduction of cattle shedding eggs (CPCR) were from 50 to 100% (average 77 % and 82 %, respectively). The heifers were dewormed one time only, at the beginning of each trial, and the values of FECR and CPCR were 100 % against C. daubneyi and 96 % and 83 %, respectively, against GIN. Over a period of 24 months, significantly higher numbers of helminth egg-output were observed in G-L1, with the lowest numbers in G-F2. C. daubneyi egg output was reduced by 5 % (G-L1) and 42 % (G-F1) at the end of trial 1 and by 83 % (G-L2) and 100 % (G-F2) at the end of trial 2; the numbers of GIN egg-output decreased by 13 % (G-L1) and 18 % (G-F1) at the end of trial 1, and by 72 % (G-L2) and 85 % (G-F2) at the end of trial 2. No adverse effects were detected in cattle taking pellets enriched with fungal spores (G-F2). It is concluded that long-term ingestion of spores of M. circinelloides and D. flagrans provides a valuable tool to improve the effect of rotational grazing and to lessen the risk of infection by C. daubneyi and GIN in dairy cattle, and accordingly, the performance of integrated control programs.

Introduction

The numbers of grazing cattle have increased markedly, partly because this is a cost-effective regime, and partly because of the preoccupation on animal welfare in food production (Thornton, 2010). Trematodes belonging to Fasciolidae and Paramphistomidae and can frequently affect ruminants on humid habitats, where appropriate conditions are present for the development of the external phase in their life cycle (Szmidt-Adjidé et al., 2000). Gastrointestinal nematodes (GIN) are helminths that often infect grazing ruminants through the ingestion of third larvae (the infective stages) (Smith and Sherman, 2009; Craig, 2009).

Control of helminths in dairy cattle becomes especially difficult because deworming is only allowed during the dry period, which occurs consecutively on farms throughout the year. Therefore, treated and untreated cows can share the same pastures, and untreated ruminants continue to shed eggs in the feces, increasing the risk of all cows ingesting infective stages of helminths (e.g., eggs, larvae) while feeding on grass.

With the aim to diminish the presence of infective stages in the soil, rotational grazing regimes characterized by ruminants feeding on grass for a time interval (grazing period), followed by other rest periods, are advised (Undersander et al., 2002). In the last years, biological strategies for the control of helminths based on the use of certain soil saprophytic fungi have been reported. Some species (Duddingtonia flagrans, Monacrosporium thaumassium) are able to trap the infective stages of GIN (Araújo et al., 2004), and others can produce antagonistic effects on helminth eggs as trematodes, cestodes and nematodes (Pochonia chlamydosporia, Mucor circinelloides, Purpureocillium lilacinum) (Cazapal-Monteiro et al., 2015; Cortiñas et al., 2015); they can also act against the miracidia of C. daubneyi (Arroyo et al., 2017). Former studies have stated the usefulness of providing cattle chlamydospores in water solutions (Assis et al., 2013; Silva et al., 2014; Saumell et al., 2015), mass mycelia of D. flagrans or M. thaumassium in alginate pellets (Dias Luns et al., 2018), or as a blend of spores of D. flagrans and M. circinelloides in industrially manufactured pellets (Hernández et al., 2016). Recently, a commercial formulation containing chlamydospores of D. flagrans was registered (Healey et al., 2018). The efficacy and safety of combining rotation of grasslands with providing pellets enriched with chlamydospores of M. circinelloides and D. flagrans were successfully tested on horses (Hernández et al., 2018a).

In the current investigation, the helpfulness of the integrated control of helminths among dairy cattle based on anthelmintic treatment, pasture rotation and feeding on pellets manufactured with chlamydospores of M. circinelloides and D. flagrans was analyzed.

Section snippets

Area of study

The present research was carried out in Galegos (Riotorto, Lugo, NW Spain, 43° 15′ 43.9″ N - 7° 12′ 36.0″ W), an agricultural and mountainous area (250−734 m altitude) under an oceanic climate, which covers ca. 16 km2 crossed by profuse streams watering the grasslands and is mostly dedicated to dairy farming and forestry production (pine and eucalyptus).

Fungal chlamydospores

A submerged culture (COPFr) was used to obtain chlamydospores of M. circinelloides and D. flagrans simultaneously (Arias et al., 2013a). The

Helminths identified

Eggs of trematodes and gastrointestinal nematodes (GIN) were detected in the feces of all cattle at the beginning of the trial. Trematodes were identified as Calicophoron daubneyi; third stage larvae belonging to the genera Trichostrongylus, Ostertagia, Chabertia, Bunostomum, Cooperia and Oesophagostomum were recovered from the coprocultures.

Efficacy of deworming

As summarized in Table 1, during the respective drying periods, anthelmintic treatment was administered 48 times to the cows belonging to G-L1 and the same

Discussion

Infections by the ruminal fluke C. daubneyi and gastrointestinal nematodes (GIN) were detected among two groups of dairy Friesian cattle managed under a leaders/followers rotational grazing regime. Accordingly, closantel and albendazole were administered to the cows throughout the study during the corresponding drying periods, whereas the heifers were dewormed once at the beginning of each trial only. The anthelmintic treatment was successful, in concordance with data collected by administering

Conclusions

It is concluded that long-term ingestion of chlamydospores of M. circinelloides and D. flagrans provides a safe and valuable tool to improve the effect of rotational grazing to prevent helminth (by C. daubneyi and GIN) infections in grazing dairy cattle. This also constitutes a very helpful strategy to develop programs for the integrated control of helminths.

Declaration of Competing Interest

The authors declare that they have no conflict of interest.

Acknowledgements

This study was partly supported by the Research Projects AGL2012-34355 and CTM2015-65954-R (Ministerio de Economía y Competitividad, Spain; FEDER). Dr. María Sol Arias Vázquez is a recipient of a Ramón y Cajal (Spanish Ministry of Economy and Competitiveness) contract, and Dr. Cristiana F. Cazapal-Monteiro is a recipient of a postdoctoral research fellowship (Xunta de Galicia, Spain). We thank “Granxa Gayoso” (Diputación Provincial de Lugo, Spain) for their support in culturing the parasiticide

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