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Gastrointestinal nematode infections in roe deer (Capreolus capreolus) from 1

the NW of the Iberian Peninsula: assessment of some risk factors 2

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Pato FJ1, Vázquez L

1, Díez-Baños N

2, López C

1, Sánchez-Andrade R

1, Fernández G

1, Díez-4

Baños P1, Panadero R

1, Díaz, P

1, Morrondo P

1 5

6

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1Department of Animal Pathology (INVESAGA Group). Faculty of Veterinary Sciences. 8

University of Santiago de Compostela. 27002 Lugo, Spain. 9

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2Department of Animal Health. Faculty of Veterinary Sciences. University of León, 24071 11

León, Spain. 12

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Corresponding author: Tel.: +34 982822102; fax +34 982822001

E-mail adress: patrocinio.morrondo @usc.es. (P. Morrondo)

*ManuscriptClick here to view linked References

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Abstract 14

Intestinal contents of 218 roe deer hunted in the northwest (NW) of the Iberian 15

Peninsula during the 2008-2009 hunting seasons were examined in order to provide information 16

on the gastrointestinal (GI) nematode prevalence and intensity of infection and the possible 17

influence of some environmental and intrinsic factors such as climatic conditions, age and 18

sex. 19

All the animals studied harboured GI nematodes, and a total of 20 different species 20

belonging to ten genera were identified. Spiculopteragia spiculoptera/Spiculopteragia 21

mathevossiani, Ostertagia leptospicularis/Ostertagia kolchida and Nematodirus filicollis were 22

the most common. This is the first citation for Chabertia ovina, Cooperia pectinata, C. 23

punctata, C. oncophora, Haemonchus contortus, Nematodirus spathiger, Oesophagostomum 24

venulosum, Teladorsagia trifurcata, Trichostrongylus capricola, T. colubriformis, T. vitrinus 25

and Trichuris capreoli in roe deer from the Iberian Peninsula. Prevalence and intensity were 26

significantly higher in the abomasum, where infections with more than one GI nematode 27

species were the most common; in the other intestinal segments infections with only one GI 28

nematode species were the most prevalent. 29

When considering the influence of the different risk factors on the prevalence of GI 30

nematodes, the highest prevalence for most of the genera were observed in roe deer from 31

coastal areas, where climatic conditions are more favourable for the development and survival 32

of third stage larvae in the environment. Regarding the sex of the animals, the prevalence was, 33

in general, higher in males than in females, probably due to behavioural and physiological 34

sex-related differences. On the contrary, no differences were found in relation to the age of 35

the animals. 36

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This study reveals that roe deer from the NW of the Iberian Peninsula are widely and 37

intensely infected with gastrointestinal nematodes, which probably affect the health status of 38

these ungulates. 39

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Key words: gastrointestinal nematode species; roe deer; abomasum; intestine; risk factors; 42

Iberian Peninsula. 43

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1. Introduction 45

The distribution of the European roe deer (Capreolus capreolus, Linnaeus, 1758) 46

populations is influenced by forest structure, vegetation characteristics and human 47

disturbance. Roe deer live in woodlands or farmland providing permanent cover, although 48

they are increasingly found on open areas. They prefer humid and cold environmental 49

conditions, which may explain the lower densities recorded in Spain in relation to other 50

European areas (Centenera, 2005; Burbaitė and Csányi, 2009). However, the progressive 51

abandonment of agricultural lands in the northwest (NW) of the Iberian Peninsula has caused 52

the appearance of alternating grazing and forest areas, representing an ideal environment for 53

roe deer, and the great diversity of plant resources in this area has led to a considerable 54

increase in the census of that ungulate in the last three decades (Centenera, 2005). 55

The NW of the Iberian Peninsula has climatic conditions which favour the survival of 56

parasitic infective forms in the environment, especially gastrointestinal (GI) nematodes, thus 57

enabling the possibility for infection throughout the year (Mezo-Menéndez et al., 1995; 58

Nogareda et al., 2006). There are a number of reports of domestic ruminants (Díaz et al., 59

2005; Díez-Baños et al., 1992, 2008) and roe deer (Vázquez et al., 2009) parasitized with GI 60

nematodes in this region. The significance of GI nematode infections in roe deer has been 61

previously reported in different European countries (Jansen, 1975; Borgsteede et al., 1990; 62

Kochko, 1997; Rossi et al., 1997; Ferté et al., 1999; Rehbein et al., 2000; Balicka-Ramisz et 63

al., 2003; Pilarczyk et al., 2005; Bolukbas et al., 2012). 64

In previous studies it was also found that roe deer from the NW of the Iberian 65

Peninsula presents a high prevalence of protozoa of the genera Sarcocystis (López et al., 66

2003), Eimeria (Díaz et al., 2010), Neospora and Toxoplasma (Panadero et al., 2010), 67

bronchopulmonary nematodes (Panadero et al., 2001) and ixodid ticks (Vázquez et al., 2011). 68

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However, in relation to the prevalence of gastrointestinal nematode infection, only a few 69

studies have been conducted on roe deer from south and central Spain (Navarrete et al., 1990; 70

Reina et al., 1992; Ramajo et al. 2007). 71

The main objective of this study was to identify the species of GI nematodes affecting 72

roe deer in the NW of the Iberian Peninsula as well as to determine their prevalence and 73

intensity of infection, taking into account their location in the different parts of the digestive 74

system. This study also reports the effect of some environmental (climatic conditions) and 75

intrinsic (age, sex) factors on the GI nematode roe deer infection. 76

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2. Material and methods 78

2.1. Study area 79

The NW of the Iberian Peninsula (43º47'-41º49' N, 6º42'-9º18' W) is an important 80

livestock-rearing area with an oceanic climate characterized by mild temperature and high 81

precipitation (Díaz et al., 2007), maintaining a high level of humidity; however, the existence 82

of climatic differences allow a division into three zones, previously described by Vázquez et 83

al. (2011): a Coastal area situated from sea level to 200 m, with moderate mean annual 84

precipitation (1,300-1,500 mm) and temperature (14ºC); a Central area situated at 200-650 m 85

with lower precipitation (900-1,300 mm) and temperature (11.5ºC); and a mountainous area 86

situated at 650-2,100m), characterized by the lowest temperature (10ºC) and the highest 87

precipitation (> 1,500 mm). 88

In this region there are large areas of woodland, mainly composed of Quercus robur 89

and Castanea sativa. In winter, roe deer eat mostly shrubs (Genista tridentata, Vaccinium 90

myrtillus, Daboecia cantabrica), whereas in spring and summer months they feed on grass 91

(Poa pratensis, Lolium perenne and Festuca pratensis) and tender shoots of deciduous trees 92

(Salix alba, Betula pendula, Alnus glutinosa, Populus alba) (Ortega, 2009). 93

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2.2. Animals 95

A total of 218 roe deer killed during two consecutive hunting seasons (April-October 96

2008-2009) in the NW of the Iberian Peninsula were examined in this study. According to 97

hunting policy, only males older than two years-old should be killed; females are hunted 98

under special conditions. For that reason most roe deer were male (n=187) and only 31 were 99

females. Animals were also divided in two age-groups, young (< 3 years old; n=30) and 100

adults (≥ 3 years old; n=188), according to their teeth features. 101

Animals were eviscerated after killing and the different organs were individually 102

bagged up, identified and frozen at -20 °C until processed in the laboratory. 103

104

2.3. Parasitological procedures 105

Abomasum and small and large intestine contents were individually examined. In the 106

large intestine, the cecum was also independently considered. The different areas of the 107

intestine were identified and sealed with ligatures at the pylorus, ileocecal junction and the 108

rectum to ensure that the nematodes remained in each of the different parts of the GI tract. 109

Once the different sections were opened, the contents and washings of mucosa were rinsed 110

using a set of three sieves of meshes 1.5 mm, 400 µm and 150 µm. After the filtration of each 111

segment, the material retained on the sieves was collected and stored in 5% formaldehyde. A 112

50% aliquot was examined for worms; adult nematodes were extracted under 113

stereomicroscope at 40x, counted and classified according to their sex. For species 114

identification, males were mounted on semipermanent preparations and identified on the basis 115

of reported morphological descriptions (Skrjabin et al., 1954; Yamaguti, 1961; Gibbons and 116

Khalil, 1982; Durette-Desset, 1983, 1989; Taylor et al., 2007). Moreover, it was also taken 117

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into consideration the existence of Ostertagiinae male polymorphism that affects the 118

morphology and length of spicules and the genital cone (Dróźdź, 1995). Several approaches 119

have supported the existence of the following pairs: Teladorsagia circumcincta (minor morph 120

Teladorsagia trifurcata; Lancaster et al., 1983); Ostertagia leptospicularis (minor morph 121

Ostertagia kolchida; Dróźdź, 1995, Ortiz et al., 1996) and Spiculopteragia spiculoptera 122

(minor morph Spiculopteragia mathevossiani; Liénard et al., 2006). However, the different 123

morphotypes were considered as different species for data analysis. 124

125

2.4. Statistical analysis 126

Data were analysed using PASW Statistics (version 18.0) for Windows. The Chi-127

square test was applied to determine significant differences (p≤ 0.05) in the prevalence of GI 128

nematode species between the different digestive segments (abomasum, small intestine, large 129

intestine and cecum). For the intensity of infection (Bush et al., 1997), the arithmetic mean 130

( x ) was used as a central tendency measure and the standard deviation (SD) as a dispersion 131

measure. Non parametric Kruskal-Wallis and Mann-Whitney tests were used to compare the 132

intensity of infection between the different digestive segments. 133

Due to the low prevalence observed for some species and morphs, only GI genera 134

were included in the analysis of the extrinsic and intrinsic factors. The existence of significant 135

differences in both the prevalence and intensity of infection by GI nematode genera 136

considering the different variables studied (climatic area, sex and age) were analysed using 137

Chi-square and Kruskal-Wallis tests, respectively. Odds ratios (OR) with 95% confidence 138

intervals (95% CI) were also calculated. 139

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3. Results 141

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All the roe deer examined (100%) were infected by GI nematodes and the number of 142

worms per animal ranged from 3 to 10,072 ( x = 1,070; SD= 1,020). Moreover, 127,140 out of 143

217,786 adult nematodes recovered were females and 90,646 males, giving a female/male 144

ratio of 1.4. 145

The prevalence of infection was very high in the abomasum (100%) and small intestine 146

(91.8%) and lower in the large intestine (58.6%) and cecum (53.5%); these differences were 147

significant (p <0.001). The mean intensity in the abomasum ( x = 954; SD= 769) was higher 148

than in the small intestine ( x = 85; SD= 143), large intestine ( x = 3; SD= 2) and cecum ( x = 149

3; SD= 2); Kruskal-Wallis test showed that there were significant differences (p <0.001). 150

Mann-Whitney test also showed significant differences between the intensity of infection in 151

the abomasum and that of the rest of the GI segments (p <0.001 for all groups). 152

A total of 20 different species of GI nematodes were identified in this study, mainly in the 153

abomasum and in the small intestine. The percentage and mean intensity of infection for each 154

species, as well as its localization in the digestive system, are summarized in Table 1. 155

Ostertagia leptospicularis/O. kolchida, S. spiculoptera/S. mathevossiani and Nematodirus 156

filicollis were the dominant species. In the abomasum 12 species of GI nematodes were 157

identified. Ostertagia leptospicularis and S. spiculoptera were the species with the highest 158

prevalence and intensity of infection. In the small intestine 13 species were identified, and the 159

dominant species were N. filicollis, S. spiculoptera and O. leptospicularis. Abomasum and 160

small intestine shared nine GI species. In the large intestine and cecum Trichuris capreoli, 161

Trichuris ovis and Oesophagostomum venulosum were observed; Chabertia ovina was only 162

identified in the large intestine. 163

Infections with more than one GI nematode species were the most common in the 164

abomasum, whereas infections with one species were the most prevalent in the other segments 165

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(Figure 1 a-d). In the abomasum (Fig 1a), infections by four species were the most frequent 166

(45.1%), being O. leptospicularis/O. kolchida and S. spiculoptera/S. mathevossiani the most 167

prevalent associations. Only one GI nematode species was identified in 60% of small 168

intestines, with a predominance of N. filicollis; associations of two species (23.4%) -with a 169

predominance of N. filicollis and S. spiculoptera- were detected in less proportion (Fig 1b). 170

Infection with T. capreoli was the most frequent in the large intestine (61%), followed by the 171

association O. venulosum and T. capreoli (Fig 1c). Finally, O. venulosum was the most 172

common GI nematode species in the cecum, followed by the association O. venulosum and T. 173

capreoli (Fig. 1d). 174

When considering the influence of the different risk factors on the GI prevalence and 175

intensity of infection (Table 2), roe deer from coastal areas presented the highest values for 176

most of the genera, and significant differences were found for Oesophagostomum (p= 0.012 177

and p <0.001, respectively); differences in the prevalence for Spiculopteragia and Trichuris 178

were also significant (p= 0.030 and p= 0.042 for prevalence and intensity, respectively). 179

Moreover, odds-ratio values showed that roe deer from coastal areas have a higher risk of 180

infection by Trichostrongylus (OR= 2.0; CI 95% 1.01-3.9), Oesophagostomum (OR= 2.0; CI 181

95% 1.01-3.8) and Trichuris (OR= 2.2; CI 95% 1.1-4.4). Regarding the sex of the animals 182

(Table 2), it was observed that the prevalence and intensity of infection were generally higher 183

in males than in females, with significant differences for Oesophagostomum (p= 0.016 and p< 184

0.001, respectively) and Trichuris (p< 0.001 and p< 0.001) and only in the intensity for 185

Spiculopteragia (p= 0.012). Moreover, the percentage of roe deer infected with Nematodirus 186

were significantly higher in males (p= 0.028) and the intensity in females (p= 0.014). Odds-187

ratio values showed that males have a higher risk of infection than females for Nematodirus 188

(OR= 2.3; CI 95% 1.1-5.0), Oesophagostomum (OR= 2.7; CI 95% 1.2-6.2) and Trichuris (OR 189

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5.0; CI 95% 2.1-12.2). In contrast, no significant differences were found in relation to the age 190

of the animals (Table 2). 191

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4. Discussion 193

In the last decades, the health status of wild animals has been gradually gaining 194

importance, and in this sense it has been reported that the presence of GI nematodes has a 195

negative impact on both the nutritional status and growth of roe deer (Zaffaroni et al., 1997; 196

Segonds-Pichon et al., 2000). The current study has revealed that GI nematodes are prevalent 197

parasites in roe deer in the NW of the Iberian Peninsula, since all animals examined 198

harboured at least one nematode species. Our data correlates with several studies conducted in 199

roe deer from Central and Southern Europe (Vetýška, 1980; Kochko, 1997; Rossi et al., 1997; 200

Rehbein et al., 2000; Balicka-Ramisz et al., 2003; Togni et al., 2004; Pilarczyk et al., 2005), 201

confirming the widespread occurrence of strongylate nematodes in the European roe deer. 202

The present work is one of the largest parasitological studies carried out in roe deer in 203

Spain; the high number of animals analysed and the extent of the study area (29.574 km2) may 204

explain the high number of GI nematode genera (n= 10) and species (n= 20) identified. 205

Although all the species detected have been previously reported in roe deer from other 206

European countries (Nickel et al., 1978; Bernard et al., 1988; Kutzer et al., 1988; Rossi et al., 207

1997; Zaffaroni et al., 2000; Bolukbas et al., 2012), this is the first report of C. ovina, 208

Cooperia pectinata, Cooperia punctata, Cooperia oncophora, Haemonchus contortus, 209

Nematodirus spathiger, O. venulosum, T. trifurcata, Trichostrongylus capricola, 210

Trichostrongylus colubriformis, Trichostrongylus vitrinus and T. capreoli in roe deer from the 211

Iberian Peninsula. 212

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In addition, the dominant species found in this work (O. leptospicularis/kolchida and 213

S. spiculoptera/mathevossiani) have been frequently reported as the most common in 214

European roe deer (Borgsteede et al., 1990; Rossi et al., 1997; Rehbein et al., 2000; Zaffaroni 215

et al., 2000; Balicka-Ramisz et al., 2003; Togni et al., 2004; Bolukbas et al., 2012). Those 216

species are primarily considered pathogens of wild ruminants (Hoberg et al., 2001; Liénard et 217

al., 2006), even though they have been sporadically reported in domestic ruminants (Suarez 218

and Cabaret, 1992; Rickard et al., 1993; Stevenson et al., 1996; Silvestre et al., 2000). In 219

contrast, the presence of several species primarily parasites of livestock, such as those 220

belonging to the genera Chabertia, Cooperia, Haemonchus and Teladorsagia (Hoberg et al., 221

2001), suggests that roe deer grazed pasture previously grazed by domestic ruminants. The 222

NW of the Iberian Peninsula is an important livestock breeding area where cattle and sheep 223

are mainly reared in a semiextensive system, grazing every day and brought into the paddocks 224

at night (Pedreira et al., 2006; Díaz et al., 2007). Consequently, cross infection from livestock 225

to roe deer can occur in common grazing pastures. Previous studies have concluded that 226

infective larvae of the genera Ostertagia, Oesophagostomum, Trichostrongylus and Cooperia 227

are the most frequent in pastures from the northwest of Spain (Mezo-Menéndez et al., 1995; 228

Nogareda et al., 2006). 229

There was considerable variation in the nematode community between the different 230

segments of the GI tract. The highest prevalence and intensity were detected in the 231

abomasum, coinciding with previous reports in roe deer (Bernard et al., 1988; Rossi et al., 232

1997; Rehbein et al., 2000). Ostertagia leptospicularis/O. kolchida and S. spiculoptera/S. 233

mathevossiani were the most prevalent species in this segment, as found by several authors in 234

roe deer from other European countries (Jansen, 1975; Vetýška, 1980; Borgsteede et al., 235

1990; Dróźdź et al., 1992; Rossi et al., 1997; Ferté et al., 1999; Zaffaroni et al., 2000; Togni 236

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et al., 2004; Bolukbas et al., 2012). Ostertagia kolchida and S. mathevosiani presented lower 237

prevalence and intensity of infection than their major morphs. 238

Nematodirus spp. were the most common parasites of the small intestine, and in the 239

current study N. filicollis was the dominant nematode species. Although several investigations 240

have found the roe deer-specific N. europaeus as the most prevalent Nematodirus species in 241

the small intestine of this wild ungulate (Borgsteede et al., 1990; Dróźdź et al., 1992; Jansen, 242

1992; Rossi et al., 1997), previous studies carried out in roe deer from Spain have reported 243

only N. filicollis within this genus (Navarrete et al., 1990; Reina et al., 1992; Ramajo et al., 244

2007). In addition, our data also coincide with that observed in roe deer from other European 245

countries, such as the United Kingdom (Dunn, 1965), France (Bernard et al., 1988) and 246

Turkey (Bolukbas et al., 2012). 247

The lowest prevalence and intensity of infection were detected in the large intestine 248

and the cecum; these results are consistent with that observed by other authors (Bernard et al., 249

1988; Rossi et al., 1997; Bolukbas et al., 2012). Trichuris ovis and O. venulosum were the 250

dominant nematode species; a number of studies have reported that these two species have a 251

high prevalence in European roe deer (Borgsteede et al., 1990; Rehbein et al., 2000; Bolukbas 252

et al., 2012). Chabertia ovina was only found in the large intestine of a small number of 253

animals, confirming that this species is rare or incidental in cervids (Borgsteede et al., 1990; 254

Hoberg et al., 2001). 255

Most of the discrepancies in prevalence values reported in the literature may be as a 256

result of different climatic conditions in the areas where roe deer were captured, which can 257

influence the life cycle of several species of GI nematodes. Prevalence and intensity of 258

infection were, in general, higher in roe deer from the coastal area, where temperature and 259

humidity conditions are more favourable for the development and survival of third stage 260

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larvae of strongylate nematodes in the environment (Mezo-Menéndez et al., 1995, 1997; 261

Uriarte et al., 2003; Nogareda et al., 2006). 262

Behavioural and physiological sex-related differences may be the cause of the higher 263

prevalence and intensity observed in male roe deer. Males are more active than females, and 264

territorial bucks exhibit a pronounced territorial behaviour, aggressively expelling other males 265

(Melis et al., 2005). The expelled males are then forced to disperse, increasing the chance of 266

infection. Moreover, it has been also suggested that certain sexual hormones, such as sex 267

steroids, modulate several aspects of host immunity, so males could become more susceptible 268

than females to many infectious pathogens, including helminths (Poulin, 1996; Klein, 2000). 269

Several authors have reported that adult roe deer present lower GI nematode 270

prevalence and intensity than both fawns and old individuals (Borgsteede et al., 1990; 271

Segonds-Pichon et al., 2000; Body et al., 2011). In domestic ruminants, a general increase in 272

resistance to strongylid infection with age is observed (Kloosterman et al., 1991; Ploeger et 273

al., 1994; Bowman, 1999). Nevertheless, in the present study no significant differences on 274

both the prevalence and intensity of GI nematodes depending on the age of the animals were 275

detected, that could be related to the Spanish hunting policy, since it is only allowed to shoot 276

roe deer older than two years-old. Consequently, the group of young animals was mainly 277

composed by a low number of animals close to three years-old that have already had the 278

opportunity to get infected several times with GI nematode infective larvae and consequently, 279

may have developed a partial protective immune response. 280

In conclusion, this study reveals that roe deer from the NW of the Iberian Peninsula 281

are widely and intensely infected with GI nematodes. Significant differences were detected 282

when considering the climatic area and the sex of the animals. Infections by GI nematodes are 283

caused in this region by a high number of nematode species -12 were first cited in the Iberian 284

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Peninsula- that may affect negatively the health status of these ungulates; on the other hand, 285

roe deer may act as potential reservoirs for other domestic or wild ruminants. 286

287

Acknowledgments 288

This work was supported by the Research Projects FAU2006-00006-00-00 and 289

07MRU034261PR and by a grant for consolidating and structuring competitive research 290

groups (CN2012/326, Xunta de Galicia). 291

292

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483

23

Figure caption 484

485

Figure 1. Percentage of plurispecific and monospecific gastrointestinal nematode infections in 486

roe deer from NW Spain. a) abomasum b) small intestine c) large intestine d) cecum. 487

488

489

TOTAL Abomasum Small intestine Large intestine Cecum

Gastrointestinal nematode species % x ±SD % x ±SD

% x ±SD % x ±SD

% x ±SD

Chabertia ovina 2.3 2±1 2.3 1±1

Cooperia oncophora 1.0 9±7 1.0 9±7

Cooperia pectinata 0.5 31±31 0.5 31±31

Cooperia punctata 1.0 12±9 1.0 12±9

Haemonchus contortus 1.4 6±3 1.4 6±3

Nematodirus filicollis 65.9 199±871 2.8 200±435 65.4 191±871

Nematodirus spathiger 2.4 8±4 2.4 8±4

Oesophagostomum venulosum 50.5 4±4 35.8 2±2 36.0 3±3

Ostertagia leptospicularis 99.1 391±417 98.6 383±406 18.3 52±194

O. leptospicularis (minor morph: kolchida) 89.5 57±88 88.2 59±89 4.8 10±5

Spiculopteragia spiculoptera 96.2 485±357 96.2 483±349 21.6 33±64

S. spiculoptera (minor morph: mathevossiani) 57.5 29±49 55.9 25±32 1.9 11±7

Teladorsagia circumcincta 6.6 28±30 6.6 28±30

T. circumcincta (minor morph: trifurcata) 0.5 21±0 0.5 21±0

Trichostrongylus axei 29.6 118±217 25.6 119±219 3.4 22±16

Trichostrongylus capricola 3.4 67±117 1.4 28±40 1.9 97±154

Trichostrongylus colubriformis 3.0 30±22 0.9 13±10 2.4 26±26

Trichostrongylus vitrinus 4.9 182±369 2.4 350±474 3.4 11±7

Trichuris capreoli 53.1 2±2 40.0 2±1 28.0 2±1

Trichuris ovis 10.4 2±2 2.8 1±0 7.6 2±2

Table 1. Prevalence and intensity of infection by different gastrointestinal nematode species and its localization in the digestive system.

Table

1

GENERA OVERALL

PREVALENCE

AND INTENSITY

CLIMATIC AREA SEX AGE

COAST CENTER MOUNTAIN MALES FEMALES YOUNG ADULTS

Chabertia 2.3

(2±1)

2.3

(2±0)

3.2

(2±1)

1.4

(1±0)

2.2

(2±1)

3.4

(1±0)

3.7

(1±0)

2.2

(2±1)

Cooperia 1.9

(18±21)

2.3

(6±0)

3.2

(23±24)

0.0

-

1.7

(8±6)

3.3

(49±0)

3.6

(4±0)

1.6

(23±23)

Haemonchus 1.4

(1±0)

2.3

(1±0)

2.1

(1±0)

0.0

-

1.6

(1±0)

0.0

-

3.3

(1±0)

1.1

(1±0)

Nematodirus 66.2

(199±871)

60.0

(198±368)

58.6

(107±118)

70.3

(301±1,384)

65.8

(123±192)

45.2

(863±2,657)

56.7

(675±2,408)

63.8

(131±223)

Oesophagostomum 50.5

(6±5)

62.2

(7±5)

38.4

(6±7)

55.4

(5±4)

52.4

(6±5)

29.6

(2±0)

46.7

(4±2)

49.5

(6±5)

Ostertagia 99.1

(443±489)

100.0

(539±583)

96.0

(397±529)

89.2

(444±350)

96.3

(458±509)

93.5

(350±339)

100

(364±247)

95.2

(456±518)

Spiculopteragia 96.7

(497±367)

97.8

(507±473)

94.9

(462±318)

95.9

(542±350)

95.7

(513±368)

87.1

(391±348)

93.3

(483±326)

94.7

(500±374)

Teladorsagia 6.6

(29±33)

2.3

(8±0)

8.4

(12±10)

6.9

(62±37)

7.7

(29±33)

0.0

-

13.3

(12±12)

5.5

(36±37)

Trichostrongylus 34.5

(129±252)

44.4

(158±288)

29.3

(104±166)

28.4

(134±318)

34.2

(130±257)

19.4

(109±214)

26.7

(119±184)

33.0

(130±261)

Trichuris 55.9

(3±3)

68.9

(3±4)

46.5

(2±2)

55.4

(2±2)

59.4

(3±3)

22.6

(2±1)

46.7

(4±2)

55.3

(2±3)

2

Table 2. Prevalence (%) and intensity ( x ±SD; in brackets) by different gastrointestinal nematode genera when considering the climatic 3

area, sex and age of the animals. 4

5

Table

1

1

2

Figure