RESEARCH WORK

 

 

 

Dynamics of gastrointestinal strongyle infesting larvae in grazing sheep

J. Arece1 y J.G. Rodríguez2

1Estación Experimental de Pastos y Forrajes «Indio Hatuey» . Central España Republicana CP 44280, Matanzas, Cuba

E-mail: javier.arece@indio.atenas.inf.cu

2Centro Nacional de Sanidad Agropecuria (CENSA), La Habana, Cuba

 

 

 


ABSTRACT

A study was conducted for two years, with the objective of characterizing the dynamics of the larval populations in «refuge» of gastrointestinal nematodes, as well as its interrelation with the meteorological variables in three sheep production farms in Matanzas province, Cuba (Dos Mercedes, LABIOFAM and the EEPF «Indio Hatuey»). Larvae of gastrointestinal strongyles were monthly collected from pasture and identified by means of a pasture washing technique from previously selected sentinel paddocks. The third stage larval population's dynamics in pasture showed a similar trend in the three farms; however, there were differences in the amounts of L3 , per kg DM of pasture. A significant effect of month of the year and season on larvae availability was recorded. In the rainy season (RS) a higher quantity of L3 was collected due to the favorable effects of rainfall and temperature. Haemonchus spp. was the prevailing species, followed by Trichostrongylus colubriformis and Oesophagostomum columbianum. The larval populations showed higher quantity during the RS and their dynamics was related to the environmental variables and the factors related to the production system in each unit.

Key words: Haemonchus, larvae, sheep


 

INTRODUCTION

In Cuba sheep exploitation systems base their feeding on the utilization of pastures. As a result of the grazing process there is a high risk acquiring digestive system parasites, because that is where they complete part of their biological cycle (Cuéllar, 2002).

At present, one of the main premises for the increase of the productivity and profitability of sheep exploitations is to decrease the costs associated to endoparasitosis. In this context, the search for parasite control alternatives constitutes a key element (González, 2004).

The knowledge of the seasonal fluctuations of the larval stages constitutes a main element when designing a parasite control strategy, because a pastureland contamination model can be set and thus outline the preventive and curative measures (García-Romero et al., 1995). Hence, knowing the larval population in «refuge1»is important for the maintaining the efficacy of antiparasitic drugs (Sissay et al., 2006).

The studies related to the third stage larval populations of gastrointestinal nematodes in sheep conducted in the western region of Cuba until the present are referred, mainly, to the trials on specific contamination and their development and survival in the environment (Delgado, 1983; García et al., 1994); however, few works have been conducted with the objective of characterizing the population dynamics of L3 in the pasture, as well as its interrelation with the meteorological variables under production conditions within an integral study of internal parasitism in sheep.

MATERIALS AND METHODS

Characteristics of the units

Three production units of Matanzas province were selected, which were representative of the main sheep production systems.Dos Mercedes farm

Location. Genetic Livestock Production Firm of Matanzas, located in the Manuelito Town, Pedro Betancourt municipality. It is exclusively dedicated to sheep production and it is considered a multiplying center of Pelibuey sheep, of reference in the province.

Feeding. It is based, mainly, on the use of natural pastures (Dichanthium-Bothriochloa-Paspalum -Sporobolus). As development strategy in the dry season, the animals receive approximately 5 kg/animal/day of king grass (Pennisetum purpureum), depending on the availability in the forage areas.

Animals and management. The herd is constituted by 145 sheep grouped in different categories (ewes, lambs, developing-growing animals and rams). The grazing area has 9 ha divided into large paddocks, in which the animals are taken to graze in homogeneous groups by category. The paddockos are exchanged among the existing groups, except the rams, which graze in the same area throughout the year. The lambs remain confined during the suckling period and are taken to graze once a week together with the ewes. The animals graze from seven to eight hours per day and in the nights they are transferred to the tenancy shed, where the previously-formed groups are maintained. This facility has concrete floors which allow their daily mechanical cleaning.

Dewormings. They are arbitrarily made, without the existence of a parasite control plan, and sometimes every 21 days. There is no rotation of antiparasitic drugs, for which the existing product at a given moment is used in anthelmintic treatments.

LABIOFAM

Location. It belongs to the Livestock Production Farm of the Pharmaceutical Biological Laboratories and it is located in the Yumurí Valley. It is an integral farm not only dedicated to sheep production, although the areas for each of the livestock productions in it are well limited.

Feeding. It is based on the use of natural pastures as feed source. The animals receive supplementation with king grass forage in the dry season, depending on the supplement availability. The facilities have earthen floors which are swept with certain frequency to avoid the excessive accumulation of feces.

Animals and management. The herd is constituted by 150 sheep divided into different categories (ewes, lambs, growing-fattening animals and rams). It has an area of about 20 ha without internal divisions. Grazing is free and the animals are taken to large areas with only a perimeter fence. The herd grazes under the unique herd concept, because all categories graze together. There is not an agreed breeding strategy and reproduction occurs by uncontrolled free mating, which has led to a high visible consanguinity degree in the animals.

Dewormings. They are arbitrarily made, without the existence of a parasite control plan, and the products are applied in relation to the available drugs.EEPF «Indio Hatuey»

Location. It belongs to the animal production area of the Experimental Station of Pastures and Forages «Indio Hatuey», located in the Perico municipality. It is a diversified farm which has well-limited areas and facilities dedicated to sheep production.

Feeding. It is based on the utilization of natural pastures. In the dry season different supplementary feed sources are used, such as citrus pulp and mulberry foliage, among others. The facilities have concrete floors, which allows their daily mechanical cleaning.

Animals and management. The herd is constituted by 120 animals separated in different categories (ewes, lambs, growing-fattening animals and rams), which graze in different areas (4,5 ha) depending on the category. The males are castrated and incorporated to grazing with growing ewe lambs. Reproduction is organized in campaigns (June-July/October-November), which allows the concentration of parturitions and facilitates management of
lactating animals and newly-lambed ewes. The lambs remain confined during the suckling period and graze only once a week with their mothers.

Dewormings. They are applied without a parasite control plan, as there is no criterion for their performance. Antiparasitic drugs are not rotated, but their application depends on the availability at the moment the treatment is decided.

Determination of L3 infestation rate in the pasture

The contamination rate of the pasturelands was estimated with a monthly frequency, for two years, by means of the collection and count of L3 in the pasture. For that purpose the pasture washing technique described by García-Romero et al. (2000) was modified. The modifications were made in the quantity of plant material for the analysis (100 g), the water volume (2 000 mL) and the aliquot volume (10 mL). The samplings were made from 8:00 to 9:00 a.m. The L3 were identified according to the key proposed by Valle (1978) and Gruner and Raynaud (1980). The DM content of the pasture was determined and the larvae were expressed in L3/kg DM.

Meteorological information

The meteorological information was recorded with a monthly frequency for two years (2000-2002) and it came from meteorological centers near the organizations where the study was conducted. The following variables were recorded: rainfall accumulation (mm), average relative humidity (%), mean temperature (ºC) and global solar radiation (MJ/m2), with a monthly frequency. On the other hand, the information of all the variables obtained in the last 15 years, except global solar radiation, was analyzed.

Statistical analyses and procedures

The factors considered for the analysis were unit and season (rainy season, RS, dry season, DS). The L3 quantity in the pasture was transformed [Log (X + 1)] in order to achieve homogeneity of the variances and normal data distribution, which was evaluated through Bartlett's test and the non parametric Kolmogorov-Smirnov test (P<0,05). The retransformation to obtain the geometrical mean was done as follows: geometrical mean = (10X)- 1) (Smothers et al., 1999).

The analysis was made with the statistical pack SPSSâ version 10.0.1 for Windows. The GLM procedure was used for L3 availability by means of the following mathematical model:

Yijkl = µ +Ui + Ej + Sk + Tl (Ui x Ej) + eijkl

Where:

Yijkl = Observation of L3 availability in the pasture

µ = Population mean

Ui =Effect of the ieth unit (1 =3; 1 = Dos Mercedes; 2 = LABIOFAM; 3 = EEPF)

Ej = Effect of the jeth season (j = 2; 1 = dry season; 2 = rainy season)

Sk = Effect of the keth strongyle species (K = 3; 1 = Haem. ; 2 = Trich.; 3 = Oesoph.)

Tl (Ui x Ej) = Effect of the interaction of the ieth unit with the jeth season

eijkl = Random effect of the error associated with each observation

The differences between means were established through Duncan's (1955) multiple range comparison test and any value of P<0,05 was considered significant. For the study of the
relation between meteorological variables and availability of infesting larvae in the pasture, Spearman's non lineal correlation analysis was made.

RESULTS

L3 availability in the pasture

The species recovered in the pasture were Haemonchus spp., Trichostrongylus colubriformis and Oesophagostomum columbianum. Figure 1 shows the L3 dynamics (L3 /kg DM) in the three studied units. In it the existence of similar patterns can be observed in the behavior of L3 in the three sites, in which the highest infestation peaks corresponded to the months of the RS, which values indicate an evident increase at the beginning of this period (May-June). The season (table 1) showed significant differences (P<0,001 and P<0,01) regarding the L3 quantity in Dos Mercedes and the EEPF «Indio Hatuey»; while in LABIOFAM there was a first order interaction between season and species of gastrointestinal strongyles (fig. 2). On the other hand, the highest total L3 availability was found in the RS (P<0,001) for Dos Mercedes and LABIOFAM; significant differences were also found (P<0,001 and P<0,01) in the quantity of third stage larvae of Haemonchus spp. in favor of the RS, while for T. colubriformis and O. columbianum no differences were observed.

In the particular case of LABIOFAM a first order interaction was observed between season and species of gastrointestinal strongyles. This phenomenon was the result of an increase in the L3 quantity of O. columbianum in the dry season, which exceeded the ones found in the RS.

The quantity of larvae collected in the pasture showed differences among the species (table 2), with a significant predominance (P<0,001) of Haemonchus spp. over the other infesting larvae. Significant differences (P<0,01) were also observed in the L3 quantity in the pasture in the three units (fig. 3), with the highest contamination rates at the EEPF «Indio Hatuey» and Dos Mercedes.

Relation between L3 in the pasture and the meteorological variables

Table 3 shows the correlation matrix between the meteorological variables and the total L3 quantity recovered in the pastures, in which the Haemonchus genus and the species T. colubriformis and O. columbianum are included. As can be observed, a strong relation was obtained between the L3 of Haemonchus spp. and the total L3 and rainfall (P<0,01); they were also directly related to O. columbianum in Dos Mercedes and the EEPF «Indio Hatuey».

The relative humidity was only related (P<0,05) to the Haemonchus spp. larvae and the total L3 in the Dos Mercedes farm. On the other hand, the mean temperature played an important role in the development and survival of the third stage larvae in Dos Mercedes and the EEPF «Indio Hatuey»; while solar radiation showed positive effects on the L3 of Haemonchus spp. and the total at the EEPF «Indio Hatuey».

DISCUSSION

The gastrointestinal strogyles found in the pasture washing show that the sheep herds in Matanzas province are affected by three main species: Haemonchus spp., T. colubriformis and O. columbianum, with predominance of the first one. This corroborates the results obtained by Arece and Rodríguez (2003), who consider that haemonchosis is the main parasitic problem of sheep in the region.

The average L3 values in the three units were moderate, as compared to the ones found in similar studies conducted in Guadeloupe (5 450 and 3 520 L3/kg DM for the RS and DS, respectively) by Aumont et al. (1996). This indicates that under the conditions of this research the animals were continuously exposed to considerable infestation sources throughout the year, with the highest risks in the RS.

The L3 quantity could be observed to show differences among the studied units, with the highest counts in Dos Mercedes and the EEPF «Indio Hatuey». This behavior can be ascribed to the differences in the stocking rate in the three units, which was lower in LABIOFAM. On the other hand, it is important to state that there were differences in the management of the three herds, because in this unit the animals were kept in large extensions with free grazing, while in the others paddocks were used and there was restriction of grazing. In this sense, Thamsborg et al. (1996) reported the existence of a positive relation between stocking rate and L3 quantity in the pasture, in which the highest stocking rate corresponded to the highest contamination rate of the pasture.

In this study it was interesting that the peaks of L3 in the pasture (in the three units) corresponded to the months of the RS, while in the same period the lowest quantity of eggs in the feces was found (Arece-García et al., 2007). However, in the DS the larval populations were low (at the height the animals grazed) and the animals showed the highest parasitic infestation rates. This phenomenon could be associated to the establishment of a solid immunity, due to the increase of forage availability and quality. In turn, in the DS the animals are forced to eat the pasture at lower levels, as a product of the decrease in feed availability, and in this place the larval populations are denser (Gruner et al., 1984). These results coincide with those of García-Romero et al. (1995), who obtained high FECs with low L3 densities in the pasture as a product of the possible re-infestation of the animals in certain sites of the exploitation areas, such as watering places and areas at the entrance to the paddocks.

The L3 dynamics in the pasture coincides, partly, with the one obtained by Altaif and Jacobs (1987), Aumont et al. (1996) and Fonseca et al. (2004) in Iraq, Guadeloupe, and Cuba, respectively. These authors found the highest infestation rates of pastures in the RS; such behavior was ascribed to the positive effects of rainfall, temperature and solar radiation in the development and survival process of larvae in the pasture. On the other hand, it has been proven that L3 need a small water film to move through pasture; in the DS it is minimal and depends, largely, on the humidity condensed at night (Cordero et al., 1998). These results differ from the ones obtained by Amarante and Barbosa (1995) in Brazil, who under similar climatic conditions found in the rainy season a lower quantity of infesting larvae; they consider that this behavior is due to the «washing effect» of rainfall and the «dilution effect» of the larval populations because of pasture growth, situation that was not observed in this study.

The positive relation of rainfall with the development and survival of the L3 populations in the pasture in this study coincides with the works carried out by Aumont and Gruner (1989), Rossanigo and Gruner and García-Romero et al. (1997); however not well defined relations have been reported between these two variables (Simón et al., 1996). The results proved that rainfall was the main meteorological variable that influenced the dynamics of the larval populations, under the conditions of the study.

The mean temperature influenced positively the larvae quantity recovered in dos Mercedes and the EEPF «Indio Hatuey»; yet, this behavior was not well defined in LABIOFAM. In this last farm no defined relations were found either between L3 and the global solar radiation and relative humidity. This could be explained by the characteristics of the grazing areas, which have low-size natural pastures that only reach approximately 3-8 cm of height and barely provide protection to those infesting stages; this could limit the migration of larvae, which tend to avoid high temperatures and solar radiation, when they do not find the necessary protection in the environment vegetation.

The results found in Dos Mercedes and the EEPF «Indio Hatuey» about the relation between temperatures and larval populations coincide with the ones reported by Rossanigo and Gruner (1994), who observed in a main component analysis that mean and minimum temperature, as well as water content in the feces, accounted for 54% of the total variance for the Haemonchus genus; however, they differ from the report by García-Romero et al. (1997), who found negative relations between the two analyzed variables.

The global solar radiation showed mean coefficients in the EEPF «Indio Hatuey» (r=0,45 for the larvae quantity of Haemonchus spp. and r=0,44 for total larvae), while in the other two units a defined behavior was not observed. These results differ from the ones obtained by Simón et al. (1996), who found correlation coefficients between -0,21 and -0,40 according to the species and the sampling period; this was ascribed to the pasture type and sampling hours, which was generally conducted in the morning (8:00-9:00 a.m.), moment of the day when radiations are weak and the migration of L3 towards the top layers of pasture is favored due to the positive phototropism to weak light (Cuéllar, 2002).

In an epizootiological study it is of great interest to know the origin of the increases of L3 levels in the pasture, as an element for the conception of the strategies destined to minimizing the confrontation between susceptible animals and infesting larvae populations. In the three units such increase was seasonal, which was due to the fast development of newly-expelled eggs in the pasture, because finding favorable environmental conditions in the RS they produced infesting larvae. The epizootiological implications of these peaks acquire remarkable transcendence, because Haemonchus prevails in sheep herds.

These results are very important, because the infestation rate of the pasture or the quantity of ingested larvae each day is the epizootiological variable with higher influence on the parasitic rate of grazing animals. In this sense, the knowledge of the contamination levels of pastures by the infesting larvae of strongyles is of interest for strategic parasite control plans. On the other hand, it is important to state that the current trends take into consideration not only the parasitic infestation rates of the herd, but also the larval population in the pasture, called «population in refuge» (Van Wyk, 2001) with the objective of outlining anthelmintic application strategies and thus minimizing the selection pressure of resistant individuals, for the establishment and development of control plans by effectively using antiparasitics.