Animal performance and endoparasitosis
When it comes to small ruminant production, the host-parasite-environment triad (Charlier et al., 2020) is a dynamic and complex system, as it undergoes several changes according to the intrinsic and extrinsic conditions of each component and their interactions. Nutrition is a tool that can contribute to ameliorate the pathophysiological effects and improve the host response to infections caused by NGIs.
However, since the eggs are laid on the pasture, the knowledge of the macro and microclimate, and its effect on the development of the free life stages of these parasites are essential to try to reduce or control the L3 potentials that are present in the system, and will give continuity of its cycle, by parasitizing its hosts.
The replacement of the true protein source (eg soybean meal) by a non-protein nitrogen source (NPN, eg EU) in the diet of beef lambs finished on Brachiaria spp. up to the level of 18 g 100 kg− 1 LW of EU, maintained the animal weight gain, even when all groups had EPG counts greater than 1200 eggs/g, with no apparent impairment of metabolic status or welfare, all the levels tested maintained the estimated slaughter weight (28–35 kg).
The used level of 24 g 100 kg− 1 LW of EU resulted in lower animal live weight and higher infections, with EPG counts above 1600 eggs/gram. It is known that ruminants are very sensitive to the use of urea, given its rapid hydrolysis in the rumen to ammonia, often exceeding the rate of carbohydrate fermentation in the rumen. The asynchrony between ammonia production and the availability of fermentable energy in the rumen negatively affects the efficiency of microbial protein synthesis.
This condition decreases the amount of microbial protein output from the rumen, which can reduce the availability of metabolizable protein needed to meet ruminant maintenance and production needs (Salami et al., 2021). Thus, animal performance can be compromised and even cause ammonia intoxication (Xu et al., 2019). In addition, the greater number of gastrointestinal nematode infections cause a metabolic imbalance between protein and energy, influencing weight gain.
With this, it can be observed that the EU can be an alternative NPN source to SF, since it provided similar performance up to the level of 18 g 100 kg− 1 LW, aid in the resilience of the hosts and did not cause ammonia intoxication or any other disturbance. visible.
Among the genera observed in coprocultures, Haemonchus and Trichostrongylus were the most frequent, corroborating several studies (Roberto et al., 2020; Gurgel et al., 2020; Roberto et al., 2018; Hoste et al., 2016). These two genera are the main gastrointestinal parasites of sheep, a cosmopolitan habit, due to the biological peculiarities of each one (including feeding method and reproduction rate); its epidemiological characteristics; their pathophysiological effects and the development of anthelmintic resistance (Hoste et al., 2016), which makes them a global concern for veterinary parasitology and ruminant production in pasture.
The third genus observed and present among all evaluated groups was Cooperia, this nematode is located in the first segments of the small intestine, where the infection can cause villous atrophy, mucosal thickening, mucus hypersecretion (Charlier et al., 2020), This feature can be evidenced in hosts resistant to infections by Haemonchus spp. This being the last clinical sign observed in the feces of some animals that received 12 g 100 kg− 1 LW of EU.
It was also observed that, in the wettest month (February) with 255.2 mm of precipitation, there was an increase in the EPG count, with a predominance of Haemonchus spp. (76%) and Trichostrongylus spp. (24%) and an increase in the percentage of parasite load and, consequently, animals with diarrhea (14 lambs), among the groups that received the different levels of EU. Diarrhea, in addition to impairing animal performance, is a source of attraction for blowflies and causes health problems such as myiasis (Jacobson et al., 2020).
Among the phenotypic characteristics evaluated, the animals had moderate EPG (between 1000 and 2000 eggs/g) and an acceptable FAMACHA© degree (FAM1 and FAM2), which demonstrates resilience and reinforces the idea that the EU levels provided adequate nutritional conditions for the animals. animals tolerated NGI infection well, gaining an average weight of 110.8 ± 23.4 g day− 1.
Mhomga et al., (2012) observed that there is a positive correlation between protein supplementation, weight gain and BCS in goats. In animals with moderate-heavy and undernourished infections, the higher the EPG, the greater the competition for nutrients, and in susceptible animals, the despoiling effect will result in evident clinical signs (Waruiru, Ngotho and Mutune, 2004), which will be reflected in a decrease in the good -being and expression of genetic, nutritional competence and, consequently, animal performance, whether for meat, milk and wool production (Charlier et al., 2020).
Due to the high proportion (> 78%) of Haemonchus spp. of the lambs, associated with the moderate degree of infection of the animals, one of the most evident clinical signs were from FAM3 to FAM5 by these parasites in the host. Therefore, it is essential to evaluate the mucosal staining using the FAMACHA© method, showing that the groups that consumed the supplements with EU levels of 12 g and 18 g 100 kg− 1 LW of EU were the ones that suffered from the effect of parasitism and were detected by the FAMACHA© method with scores 4 and 5, while the animals of the other treatments had more animals distributed in scores between 3 and 5, in which, the score 3 is already considered a warning sign and indicated interventions with antiparasitics (Van Wyk and Bath, 2002).
The NGIs through despoiling action and as a result the occurrence of hemorrhages, causes a decline in hemato-biochemical parameters. With protein supplementation, there may be an increase in nutrient support, which gives a better condition to control worms and suffer less from the deleterious effects, such as anemia (Atiba, Zewei and Qingzhen, 2020), all of which are used to achieve homeostasis. in the body, and maintain serum levels for survival.
Protein supplementation can improve apparent digestibility, nutrient utilization and efficiency of parasitized ruminants (Atiba, Zewei and Qingzhen, 2020; Crawford et al., 2020; Hoste et al., 2016). Extruded urea levels provided similar performance results and phenotypic characteristics as FAMACHA© up to 18 g 100 kg− 1 LW when compared to true protein source, which suggests that this NPN can be implemented in the diet of beef lambs, in addition to to be a lower cost nitrogen source.
Deposition in pasture
From the propagation of the eggs of the NGIs in the environment, the macro and microclimatic conditions are the main determining factors for the survival, development and larval migration. In the pasture of the paddocks grazed by the lambs naturally infected with NGIs and supplemented with increasing levels of EU, larvae of NGIs in different free-living stages and in different proportions were recovered. However, even with pastures with higher (0, 12, 24 and 18 g 100 kg− 1 LW) and lower (6 g 100 kg− 1 LW) concentrations of larvae, the parasitic infection was similar, due to the host factor.
The larvae observed in the forage were of the genera Haemonchus and Trichostrongylus, which demonstrates adaptability to the micro and macroclimatic conditions of the studied region, mainly of Haemonchus spp. Many specimens of L1/L2 were recovered in all paddocks evaluated (263.2 ± 177.1), this is due to the fact that this larval stage is more protected either by feces, dead material from the pasture and even by physical and physiological mechanisms (Heckler and Borges, 2016).
This greater dispersion of L1/L2 in the pasture can be explained by two reasons, (1) samples were collected, close to the ground and without stratification, and then all larvae present in the aerial part of the plant were recovered. Since the L1/L2 are concentrated at the bottom of the clumps to protect themselves from adverse environmental conditions and continue their development (Roberto et al., 2020; Tontini et al., 2019; Pegoraro et al., 2018; Tontini et al., 2015), these were accounted for; (2) the survey was carried out during the region's rainy season, with frequent and torrential rainfall, which may have contributed to dispersing these larvae among the different canopy extracts, and about 90% of the larvae are transported by splashes (Heckler and Borges, 2016). Molento, Buzzatti and Sprenger (2016) report that the impact of rain droplets can provide greater larval dispersion, reaching the point of releasing L3 at a distance of up to 90 cm from the fecal mass, suggesting that the same occurs with L1/L2.
The fact of identifying the genus Haemonchus spp. in all components evaluated (animal-pasture-soil), with greater or lesser frequency, reinforces the idea of prevalence, pathogenicity and biotic potential (Knox and Steel, 1999; Wallace et al., 1998). Females of this genus have characteristics such as laying between 5 and 10 thousand eggs day− 1 (Molento, Buzatti and Sprenger, 2016; Romero and Boero, 2001) and being less susceptible to ultraviolet (UV) radiation.
The presence of Cooperia spp. and Oesophagostomum spp. was observed in coproculture. However, it was not possible to recover larvae of these genera in the samples of environmental components. This can be explained by the fact that there is a low percentage of these genera infecting the animals and, therefore, the distribution of eggs in the faeces and the development of eggs to larvae is reduced, when compared to the others.
Still, it may be related to the fact that each genus presents morphological distinctions, even if minimal, reactions and behaviors that increase or reduce the friction on the plant surface, and consequently, the migratory rate. An example of this is Oesophagostomum spp., which, in addition to being more robust than other NGIs of veterinary importance, has undulations in the cuticle that make movement difficult (Romero and Boero, 2001), especially in forage plants with trichomes and twisted surfaces (Molento, Buzatti and Sprenger, 2016; Rocha et al., 2008). As a compensatory means of survival, the highest concentration of these nematodes is present in the animals' gastrointestinal tract.
When considering the cultivars that composed the pastures, the type of morphological structure may have influenced and provided a favorable microclimate for the survival and development of the free life stages of the NGIs. The cultivar Marandu presents erect growth with initial prostrations, whereas the cultivar Basilisk presents decumbent growth, which gives greater shading at the base of the clumps. However, L3 recovery was considered low when compared to other studies, even though this is the period of greatest larval recovery in the region (Heckler and Borges, 2016).
However, neither the greater height nor the habit of spending less time on grazing were able to reduce or increase the proportion of larvae in the pasture and reduce the EPG of the lambs, respectively. This last point can be explained by the grazing habit, since lambs graze longer at the coldest times (at sunrise and sunset; De Paula et al., 2010), concomitantly with a higher frequency of larval migration to the canopy apex.
Deposition in soil
The soil component is considered one of the reservoirs of NGI larvae at different stages of development, as well as pasture. L1/L2 and L3 larvae can survive for several months in this component, if the meso-variations (macroclimatic variations) and the pasture microclimate prove to be favorable (Heckler and Borges, 2016). In addition to climatic conditions, the type of soil and its respective physical characteristics may or may not influence the survival and migration of NGI larvae, and consequently, their recovery rates (Knapp-Lawitzke et al., 2014). Few specimens of NGIs were recovered in soil samples from areas grazed by naturally infected lambs. In 125 soil samples collected throughout the experimental period, eighteen specimens of L1/L2 and six of L3H were recovered.
This was due to the soil of the studied region being classified as Dystrophic Red Latosol (Teixeira et al., 2017), which has microporosity and impermeability, which results in less aeration and greater water saturation. These characteristics reduce positive and horizontal geotropic vertical migration, reducing the survival and development of free life forms of ruminant gastrointestinal parasites in the soil. In addition, it was observed that, on average, after two days without rainfall, the soil became very dry and with high mechanical resistance to penetration, conditions that made it difficult to collect samples manually and, consequently, the viability of larvae in this component. .
The mobility of larvae is influenced by the degree of soil moisture and oxygen concentration, as water-saturated soils reduce the migration speed, since this migration is potentiated in the presence of particles surrounded by a thin film of water (Bruns, 1937). It is also worth mentioning that the size of the sand grains and the width of the pores provide more favorable conditions for migration, in which, the migration in coarse sand soils, the L3 migrate at an average speed of 1.5 cm h− 1, since in fine sand 1 cm h− 1 and in clayey soils 0.5 cm h− 1.
The type of soil and the microclimate existing in it can influence the larval recovery rate, migration capacity, migration speed and direction (vertical and horizontal). The experimental period was carried out in the rainy season, with the presence of torrential rains that may have eliminated a large number of larvae, due to the rupture of the cybals and exposure of the eggs. Or even, result in soil with excessive moisture, preventing adequate aeration of the fecal layer and soil surface, which negatively influences the development and migration of larvae in the pastoral environment (Heckler and Borges, 2016). The rain may have carried the larvae to points on the paddocks where sampling was not carried out (Molento, Buzatti and Sprenger, 2016).
Among the genera observed in coproculture (Haemonchus, Trichostrongylus, Cooperia and Oesophagostomum) and in pasture (Haemonchus, Trichostrongylus), in soil samples only the presence of larvae of Haemonchus spp. considered the most prevalent and pathogenic, it is also adapted to the adversities of the tropical climate.
In view of this, it is assumed that faecal formations, forage and dead material become the main reservoirs of NGIs. Once the soil becomes “impermeable” to the larvae and does not show a favorable microclimate for their survival and development.
There are few reports in the literature about the influence of dead material bedding, its representativeness as a reservoir of NGIs and the microclimate existing in this litter. Therefore, it is important that this component also be evaluated in subsequent research, due to the physiology of each forage cultivar, as the production and disposal of senescent material in the pastoral environment is different.
The increasing levels of extruded urea replacing soybean meal did not influence the EPG count. The 0 to 18 g 100 kg-1 LW level of EU maintains animal performance and BCS and FAMACHA© phenotypic characteristics. There is less dispersal of NGI larvae in pasture and soil as EU levels increase. The Dystrophic Red Latosol is not a good reservoir for NGI larvae, in the edaphoclimatic conditions of the rainy tropical savanna.