The effect of supplementary feeding on the resilience and resistance of browsing Criollo kids...

The effect of supplementary feeding on the

resilience and resistance of browsing Criollo

kids against natural gastrointestinal nematode

infections during the rainy season

in tropical Mexico

J.F.J. Torres-Acostaa,*, D.E. Jacobsb, A. Aguilar-Caballeroa,C. Sandoval-Castroa, M. May-Martineza, L.A. Cob-Galeraa

aFacultad de Medicina Veterinaria y Zootecnia, Universidad Autonoma de Yucatan.

Km 15.5 carretera Merida-Xmatkuil, Merida, Yucatan, MexicobThe Royal Veterinary College, University of London, Hatfield, Herts AL9 7TA, UK

Accepted 4 July 2004

Abstract

The objective was to determine the effect of supplementary feeding on the resilience and

resistance of Criollo kids against natural gastrointestinal nematode (GIN) infections, when browsing

native vegetation during the wet season in tropical Mexico. Thirty-four 2-month old Criollo kids,

raised nematode free, were included at weaning in a 22-week trial. The kids were placed into four

groups. Two groups of 8 kids were offered 100 g/day soybean and sorghum meal (26%:74%,

respectively fresh basis) (treated/supplemented (T-S) and infected/supplemented (I-S)). Two groups

remained with no supplement for the duration of the trial (infected/non-supplemented (I-NS) (n = 10)

and treated/non-supplemented (T-NS) (n = 8)). Kids in groups T-S and T-NS were drenched with

0.2 mg of moxidectin/kg body weight orally (Cydectin, Fort Dodge) every 28 days. Groups I-S and I-

NS were naturally infected with GIN. The animals browsed native vegetation (for an average of 7 h/

day) together with a herd of 120 naturally infected adult goats. Cumulative live weight gain (CLWG),

packed cell volume (PCV), haemoglobin (Hb), total plasma protein and plasma albumin were

recorded every 14 days as measurements of resilience. Resistance parameters (faecal egg counts

www.elsevier.com/locate/vetpar

Veterinary Parasitology 124 (2004) 217–238

* Corresponding author. Tel.: +52 999 942 32 00; fax: +52 999 942 32 05.

E-mail address: [email protected] (J.F.J. Torres-Acosta).

0304-4017/$ – see front matter # 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.vetpar.2004.07.009

(FEC) and peripheral eosinophil counts (PEC)) were also measured. Bulk faecal cultures were made

for each group every 28 days. Every month a new pair of tracer kids assessed the infectivity of the

vegetation browsed by the animals. The T-S group had the highest CLWG, PCVand Hb compared to

the other three groups (P < 0.001). The I-S and T-NS group had similar mean CLWG and PCV (P >0.05), while the I-NS group had the poorest CLWG, PCV and Hb (P < 0.001). The PEC of

supplemented kids (I-S and T-S) was higher than in the I-NS and T-NS kids (P < 0.05). No effect of

supplementary feeding was found in the FEC. Tracer kids and faecal cultures showed that kids

suffered mixed infections with Haemonchus contortus, Trichostrongylus colubriformis and Oeso-

phagostomum columbianum. Supplementary feeding improved resilience of browsing Criollo kids

against natural GIN infections and was economically feasible. Improved resistance was also

suggested by the PEC but was not confirmed in the FEC.

# 2004 Elsevier B.V. All rights reserved.

Keywords: Goat; Gastrointestinal nematodes; Supplementary feeding; Resilience; Resistance

1. Introduction

Supplementation is a common practice in several ruminant production systems in the

tropics due to the reduced availability or quality of vegetation during the dry season.

During the wet season, grazing ruminants benefit from apparent improvements in forage

availability and diet quality. However, they also endure an increasing helminth challenge

that reduces production and may even cause death (Hendy and Carles, 1993). An improved

nutritional status may reduce, under some conditions, the production losses and mortality

rates associated with gastrointestinal nematode (GIN) infections (Sykes and Coop, 2001;

Walkden-Brown and Kahn, 2002). Several controlled pen trials have shown that

supplementary feeding may increase resilience and resistance of young ruminants against

GIN (Abbott et al., 1985, 1986, 1988; Bown et al., 1991; Wallace et al., 1995, 1996; Datta

et al., 1998; Knox and Steel, 1999; Kahn et al., 2000; Valderrabano et al., 2002). However,

only a small number of trials have studied the complex interactions between host nutrition

and GI parasitism in grazing animals (Bransby, 1993). Evidence from field trials with

grazing ewes has shown that dietary supplementation can overcome the peri-parturient loss

in immunity (Kahn et al., 1999). In young animals, reduction in production losses,

attributable to infection with nematodes, have been found under dry conditions when using

less degradable sources of protein (Van-Houtert et al., 1995a; 1996; Datta et al., 1999) and

energy (Van-Houtert et al., 1996). However, evidence of the use of supplementation in

grazing or browsing animals for the control of GIN during the rainy season has not been

sufficiently investigated. To date, only three studies have been reported. The first, a

simulation model, showed that the production responses of goats to supplementary feeding

during the rainy season were likely to be limited, unless helminths are also controlled

(Hendy and Carles, 1993). In the second, grazing lambs artificially and naturally infected

with H. contortus received a supplement consisting of a protein rich feed and showed an

increase in their resilience but not in their weight gain (Shaw et al., 1995). The third,

Anindo et al. (1998) claimed that molasses-urea-blocks (MUB) could be as effective as

administering anthelmintic in mitigating the effects of GIN in grazing Menz lambs. At the

present time, no experiment has addressed the effect of supplementary feeding in kids

J.F.J. Torres-Acosta et al. / Veterinary Parasitology 124 (2004) 217–238218

naturally infected with GIN and browsing during the rainy season. Data from sheep cannot

be freely extrapolated to goats due to physiological and behavioural differences between

the two species. The objective of the trial was to investigate the effect of dietary

supplementation in the resilience and resistance of browsing Criollo kids against GIN,

during the rainy season in tropical Mexico.

2. Materials and methods

The trial was conducted at the FMVZ-UADY goat farm during a wet season (August–

December, 1997). Twenty hectares of a nearby, low deciduous jungle were enclosed with

galvanized wire sheep fencing. The goats were walked each morning to browse in this

enclosure and returned to the farm buildings in the afternoon (6 km daily).

Experimental animals. Criollo goat kids (n = 34) were raised for 60 days in conditions

that minimized the possibility of infection with GIN.

Animal management. One week before the trial started, the kids and their dams were

taken to browse with the herd (settling-in period). Kids were weaned on the day the trial

started (67 days old), having been treated orally with toltrazuril (10 mg/kg body-weight;

Baycox, Bayer-Mexico) to control Eimeria spp., the day before. Baycox treatment was

performed on three occasions (weeks 0, 4 and 8 of the trial).

For the duration of the trial, the kids were kept in two pens at night, with a concrete floor

and tin roof that complied with local welfare standards. Treated groups were allocated to

one pen and untreated groups to the other. A goat keeper took all animals in the groups to

browse for an average of 7 h/day (8:00 am–3:00 pm). Time spent in the browsing enclosure

was recorded daily. The kids browsed together with the rest of the goat herd (100–110 goat

dams). The dams of the experimental kids were separated from the herd so that their

offspring had no opportunity to suckle during the browsing period. Animals were inspected

twice daily and the health status of each animal was observed.

Design of the study. The kids were randomly allocated to three groups of 8 animals and

one with 10 kids. Each group was balanced according to live weight as follows:

I-NS 10 kids infected, non-supplemented control;

I-S 8 kids infected, supplemented;

T-NS 8 kids treated, non-supplemented;

T-S 8 kids treated, supplemented

Ten kids were included to group I-NS in case any animal had to be withdrawn from the

trial for welfare reasons.

Animals in the supplemented groups (I-S and T-S) were offered 100 g/day of a feed,

consisting of 74% sorghum meal (Sorghum bicolor subglabrescens) and 26% soyabean

meal (Glycine max) fresh basis. It was assumed that the basic protein requirement for

maintenance and other nutrient requirements for maintenance and growth would be

obtained from browsing native vegetation. The composition of the native vegetation in

the study area was described by Rios and Riley (1985). The feed supplied an estimated

11.1 g of metabolizable protein (assuming a feeding level of 2.0 and associated rumen

J.F.J. Torres-Acosta et al. / Veterinary Parasitology 124 (2004) 217–238 219

outflow rate of 0.05/h; AFRC, 1993). Supplementary feed was offered to kids individually

when they returned from browsing (3:30 pm) daily. Refusals were recorded the following

morning. This routine minimized the possibility of appetite reduction during browsing.

Animals in the treated (T-S and T-NS) were treated with 0.1% moxidectin liquid

formulation (Cydectin, oral drench for sheep, Fort Dodge) administered orally at a dose of

0.2 mg/kg body weight. Treatments were given strictly according to label instructions on

weeks 0, 4, 8, 12, 16 and 20. Treated animals were observed for side effects during the hour

after treatment and at subsequent feeding times.

Live weight change. Animals were weighed at two weekly intervals for the duration of

the experiment (i.e. 12 times). Weighing took place in the mornings before the kids went

out to browse and 15 h after concentrate feed was given.

Faecal samples. Faecal samples were obtained from the rectum of kids using plastic

bags on the same days as the weighing. Faecal egg-counts (FEC) (eggs per gram (EPG))

were determined using a modified McMaster technique (Rodrıguez et al., 1994). Bulk

faecal cultures were performed for each group every 28 days. Cultures were kept at room

temperature and were harvested on day seven using the Corticelli-Lai technique

(Rodrıguez et al., 1994). The GIN L3 larvae obtained from the cultures were identified by

their morphology and size (MAFF, 1986; Bowman and Lynn, 1999). Consistency of faeces

of each kid (i.e. whether normal or loose) was recorded daily.

Blood parameters. Blood was collected on the days the kids were weighed. Packed cell

volume (PCV), haemoglobin concentration (Hb), total plasma protein (TPP) and plasma

albumin concentrations (PA) were determined using standard haematological and

biochemical procedures. Peripheral eosinophil counts (PEC) were determined following

fixation in Carpentier’s stain (Dawkins et al., 1989) and using a ‘‘Fast-Read 10’’ disposable

counting chamber (Immune Systems).

The normal ranges for the different blood parameters used in this trial were calculated

from the values obtained on the first sampling of each parameter. Normal blood ranges

were calculated as the mean � 2 S.D. when data obtained in the first sampling had a normal

distribution (Payne, 1978; Farver, 1997). Where the data did not have a normal distribution,

the normal range was considered to be within 2.5 and 97.5 percentiles (Farver, 1997).

Measuring infectivity of the browse with tracer kids. Every month a new pair of tracer

kids, that have been reared and maintained under conditions minimising the risk of

helminth infection, was taken to browse with the rest of the goat herd. The tracer kids were

left to browse for thirty days. At the end of each month, the respective pair of tracer kids

was placed in a pen with concrete floor, which limited the possibility of new infection with

GIN. Tracer kids were kept in such pen for 21 days. After that, the kids were euthanased in

compliance with local welfare standards and post-mortem worm-counts performed.

Statistical analysis. The Saphiro-Wilk test was used to test for normality in all the

parameters before analysis. Differences in CLWG, FEC, PCV, Hb, PEC, TPP and PA

between the groups were analysed by repeated measures analysis of variance (ANOVA)

using the General Linear Model procedure (Cody and Smith, 1991). FEC (EPG) and blood

PEC were transformed logarithmically by taking log10 (FEC + 1) to stabilize the variance.

The models used to analyse FEC of the strongylida order were similar to those mentioned

before, except that the first model included samplings from the moment the animals shed

detectable EPG levels (week 4). Differences in the frequency with which each animal had a


PEC superior to 1 � 109/l during the trial were analysed by the non-parametric Wilcoxon

rank-sum test. This compared different infection levels (T versus I) initially and later

supplementation levels (S versus NS). Differences in the number of individuals with PEC

superior to 1 � 109/l at least once during the trial, in each group, were compared by a

Fisher-exact test. Differences in total supplementary feed consumption were determined by

the two samples T-test (paired T-test). A multiple regression analysis was performed with a

General Linear Model procedure, to determine the effect of infection, supplementation and

their interaction on the frequency of animals with loose-faeces during the trial. Two periods

were studied, from day 0 to 105 (weeks 1–15) and from day 106–154 (weeks 16–22). Two

models were used: (I) loose faeces-days/animal = infection, supplementation, interaction.

Loose faeces were analysed as normal, logarithmic (log10(n + 1)) and squared values (n2).

(II) Loose faeces-days/animal as a proportion of the total time in the period = the same

independent variables.

Economic analysis. The cost of the intervention (treatment and/or supplementation) was

recorded and a pilot partial budget analysis was performed (Huirne and Dijkhuizen, 1997)

using a spread-sheet computer software program (Microsoft# Excel 2000) to determine

the economic significance of treatment and/or supplementation. Total production data of

the I-NS group was used as baseline performance so that results reflected kid withdrawal

(which in production terms could be considered as mortality) as well as growth rate.

3. Results

Mean browsing time recorded during the trial was 7 h, 8 min per day. One kid in the I-S

group was lost while browsing in the sixth week of the trial. Four kids from the I-NS group

were withdrawn from the trial on humanitarian grounds (two in week 19 and two in week

21). They were weak and had diarrhoea.

3.1. Parameters of resilience

Cumulative live-weight gain. Fig. 1 shows the pattern of growth found in the four

groups. Animals in the T-S group showed the highest growth rate (P = 0.0001). Animals in

groups T-NS and I-S groups showed similar growth rates between them. Kids in group I-NS

were significantly smaller than the rest of the animals (P = 0.0001). Supplementation

significantly increased CLWG (P = 0.0001), whilst, infection reduced CLWG (P = 0.0001).

The effects of infection and supplementation were more important as the trial advanced in

time (P = 0.0001). At the end of the trial there was a slight recovery in the mean CLWG in

the I-NS group as some clinically affected animals were withdrawn from the trial. Animals

of the I-S group showed a reduction in live weight gain from week 16 onwards which

resulted from the weight loss of three animals in the last month of the trial. Also from week

16, three animals in the I-NS group reduced their CLWG before they were withdrawn from

the trial.

Fig. 2 shows the mean daily live weight gain in the different groups. Supplementation

increased growth similarly in both the non-infected and infected groups (22.7 versus

20.4 g/day, respectively) when compared to the non-supplemented counterparts. The



Fig. 1. Effect of supplementation on the mean cumulative live-weight gain (CLWG), mean haemoglobin and

mean packed cell volume (PCV) concentration of infected and non-infected kids Criollo kids during the rainy

season.

reduction in growth from infection was similar in both the supplemented and the non-

supplemented groups (24.2 versus 21.91 g/day, respectively) when compared to the

respective infected groups.

Supplementary feed consumption. There was no significant effect of infection on

supplementary feed consumption during the trial but a reduction in feed consumption was

observed in both supplemented groups from weeks 4–7 and from 10 to 13. Total

supplementary feed consumption of each kid (in the 22 weeks of trial) varied from 14.1 to

15.4 kg in T-S kids and from 13.4 to 15.4 kg in I-S kids. Total supplementary feed

consumption per group was not affected by infection (mean � S.E.: 14.9 � 0.2 kg versus

14.9 � 0.2 kg for infected and treated groups, respectively).

Blood parameters. Fig. 1 shows the variation of PCV in the different groups. Average

PCV decreased as the trial advanced from weeks 0–22 (P = 0.0001) except for the T-S

group, which maintained its PCV level almost constant. Treated animals had higher mean

PCV than infected animals (P = 0.0001). Supplementary feeding also allowed higher mean

PCV values (P = 0.0006). A significant time � infection interaction showed that, as the trial

advanced in time, the effects of infection on PCV levels were more severe (P = 0.0008).

However, the time � supplementation interaction was only marginally significant (P =

0.06). The T-S group had only one animal on one occasion falling below the normal range

calculated for the trial (22–35% PCV). The T-NS group had several animals below the

normal parameter from week 12 to 22. The I-S group had three animals below the normal

value by the end of the trial. Meanwhile, most animals of group I-NS were below the


Fig. 2. Effect of supplementation on the mean daily live-weight gain (DLWG) of infected and non-infected

Criollo kids during the rainy season.

normal range from week 10. One of the kids withdrawn from the trial had a PCV less than

half the lowest normal range and the other three animals had PCV levels ranging from 15

to 17%.

Mean Hb concentrations of the different groups are presented in Fig. 1. I-NS group was

below the normal range (7.12–11.04 g/dl) from week 6 until the end of the trial. The I-S

kids also had their mean Hb concentration below the calculated normal range on weeks 8,

10, 16, 20 and 22. Non-infected groups had mean Hb concentrations within the normal

range for the duration of the trial. Infection (P = 0.0001) and lack of supplementation (P =

0.0006) reduced mean Hb concentrations. The effect of the infection on mean Hb

concentration was more severe as the trial progressed (P = 0.002) and the effect of

supplementation became less obvious (P = 0.06). The T-S group maintained its Hb level

above that of the other three groups. Hb levels of the kids withdrawn from the trial were

below the normal range.

The mean TPP and PA concentrations of the infected groups were lower than those of

the treated groups as the trial advanced in time (P < 0.03). No supplementation effect was

found.

Loose faeces. Loose faeces-days/group/week as a proportion of the total-days/group in a

given week is represented in Fig. 3. Regression analysis from weeks 1 to 15 showed no

significant effect of infection, supplementation or their interaction on the presence of

diarrhoea. However, in the following period (weeks 16–22) treated groups had less loose

faeces-days/animal (P = 0.001). Infected animals had from 8.9% to 11.4% more loose

faeces-days than treated animals at this period of the trial (last 7 weeks). Supplementary

feeding had no significant effect on diarrhoea.

3.2. Resistance parameters

Infected animals had higher PEC levels as the trial advanced in time compared to treated

animals (P = 0.001) (Fig. 4). Similarly, supplemented groups had higher PEC as the trial

advanced over time (P = 0.004). The number of individuals that had PEC above 1 � 109/l in

each group at least once during the trial was similar. However, the number of times

individual animals in each group had PEC above 1 � 109/l was higher in the supplemented

groups than in the non-supplemented (Z = 1.9, P = 0.05). Only supplemented animals

(infected and treated) had several PEC values above 2 � 109/l, reaching a maximum of 3.54

� 109/l in T-S group and 7.75 � 109/l in I-S group. Not all the kids had an overt

eosinophilia even when they had high FEC and/or clinical signs of gastro intestinal

nematodosis. For example, three of the animals withdrawn from the trial because of their

clinical condition had a PEC of zero and only the fourth kid had an overt eosinophilia (PEC

= 2 � 109/l).

Infected animals had significantly higher FEC than treated animals from week 4 (P =

0.0001) (Fig. 4). Supplementary feeding had no significant effect on the EPG output in the

infected animals for the duration of the trial. Of the four kids withdrawn from the trial, two

had FEC above 2000 EPG with the other two near 4000 EPG. Only one kid in the T-S group

shed 50 EPG once (week 16). In the I-NS group, three kids shed <200 EPG on one

occasion (week 12). Proportions of infective (L3) larvae identified from consecutive faecal

bulk cultures in the experimental groups are shown in Table 1. Small numbers of


Trichostrongylus larvae were found in the treated groups. Infected groups had large

numbers of Haemonchus larvae from the second culture. Meanwhile, the proportions of

Trichostrongylus larvae were relatively constant and Oesophagostomum larvae increased

as the trial advanced.

3.3. Meteorological data

Average maximum ambient temperatures were falling as the trial advanced and ranged

from 35.6 to 29.9 8C. Average minimum ambient temperatures showed a similar pattern


Fig. 3. Effect of supplementation on the mean on the mean peripheral eosinophil counts (PEC) and faecal egg

counts (EPG) of infected and non-infected kids Criollo kids during the rainy season.

and ranged from 22.5 to 16.8 8C (Fig. 5). A total of 500.7 mm of rainfall was concentrated

mainly in the first 12 weeks. During the trial, 69 days of rain were recorded.

3.4. Infectivity of browsing vegetation obtained from tracer kids

Fig. 5 shows the infectivity of H. contortus, T. colubriformis and O. columbianum in

tracer kids browsing together with the experimental groups. Tracer kids showed that

infection with H. contortus was important at the beginning of the trial and declined with

time. T. colubriformis infectivity increased gradually as the trial advanced from August to

December, while O. columbianum infectivity was variable.

3.5. Economic analysis

A partial budget analysis for each intervention strategy including treatment (for

maintaining animals with a non-patent infection), supplementation and treatment �supplementation is shown in Table 2. Overall, all the intervention strategies were shown to

be economically feasible when compared to no intervention. However, treatment �supplementation intervention had the highest economic return followed by treatment-only

and finally supplementation-only. The additional returns from the supplementation-only

intervention were limited to differences in growth as the I-S kids were showing signs of


Fig. 4. Effect of supplementary feeding on the proportion of loose faeces-days/group/week of infected and non-

infected Criollo kids during the rainy season.

clinical disease and therefore they were not more appealing to the consumer than the I-NS

kids at the end of the trial.

4. Discussion

4.1. Resilience

The use of supplementary feeding in Criollo kids browsing during the rainy season

improved their resilience against GIN. This was shown by increased growth rate (CLWG)

in supplemented groups compared to those not supplemented. This is the first evidence

documented under field conditions in browsing kids in tropical conditions. Similar findings

have been reported in controlled pen trials with goats (Blackburn et al., 1991; Singh et al.,

1995), as well as in field trials with grazing sheep, during dry season (Van-Houtert et al.,

1995a) and during a complete year (Anindo et al., 1998). However, Shaw et al. (1995) did

not find any effect of supplementation on CLWG during the rainy season in sheep.

Supplementation with sorghum meal + soybean meal allowed naturally infected

animals to achieve CLWG similar to those of the T-NS animals and twice as high as those


Table 1

Infective (L3) larvae recovered from consecutive bulk faecal cultures performed on the four experimental groups

of kids during the wet season

Group Genus Week Total, N/%

4, N/% 8, N/% 12, N/% 16, N/% 20, N/%

T-S Haemonchus spp. 2/4 2/1.2

Trichostrongylus spp. 12/66.67 17/34 1/2 30/17.9

Oesophagostomum spp. 0/0.0

Strongyloides papillosus 30/100 20/100 6/33.33 31/62 49/98 136/80.9

Total 30/100 20/100 18/100 50/100 50/100 168/100.0

T-NS Haemonchus spp. 0/0.0

Trichostrongylus spp. 10/22.7 2/10 30/60 8/17.8 50/23.9

Oesophagostomum spp. 0/0.0

Strongyloides papillosus 34/77.3 18/90 20/40 37/82.2 159/76.1

Total 44/100 20/40 50/100 45/100 50/100 209/100.0

I-S Haemonchus spp. 4/8.3 32/64 37/64 26/52 18/36 117/47.2

Trichostrongylus spp. 7/14.6 5/10 7/14 8/16 7/14 34/13.7

Oesophagostomum spp. 3/6 2/4 4/8 13/26 22/8.9

Strongyloides papillosus 37/77.1 10/20 4/ 8 12/24 12/24 75/30.2

Total 48/100 50/100 50/100 50/100 50/100 248/100.0

I-NS Haemonchus spp. 6/12.2 35/70 24/48 16/32 8/16 89/35.7

Trichostrongylus spp. 18/36.7 6/12 18/36 13/26 11/22 66/26.5

Oesophagostomum spp. 7/14 5/10 14/28 15/30 41/16.5

Strongyloides papillosus 25/51.1 2/4 3/6 7/14 16/32 53/21.3

Total 49/100 50/100 50/100 50/100 50/100 249/100.0

T-S: treated and supplemented; T-NS: treated and non-supplemented; I-S: infected and supplemented; I-NS:

infected and non-supplemented.


Fig. 5. Climatic variables recorded during the trial (maximum and minimum ambient temperatures, rainfall and

rain-days) in the study zone during the rainy season and worm counts of tracer kids (Haemonchus contortus,

Trichostrongylus colubriformis and Oesophagostomum columbianum).

of the I-NS kids. Conventional feedstuffs (soybean meal and sorghum meal) were used

because, at the time the trial was planned, evidence had not yet been published to indicate

that other feedstuffs such as MUB could have an effect on increasing resilience in goats

(Singh et al., 1995; Knox and Steel, 1996). Previous trials with sheep showed that the

response to supplementation was particularly effective where the protein was ‘‘protected’’

from rumen degradation (Coop and Holmes, 1996; Van-Houtert and Sykes, 1996).

However, the present trial indicates that increases of MP supply from a mixture of less

degradable protein (soybean meal) and fermentable energy (sorghum meal) can also

increase host resilience. Recent evidence in sheep showed that resilience can be improved

by supplementing energetic feeds to grazing animals (Van-Houtert et al., 1996).

However, supplementation alone could not compensate for the totality of the negative

effects of GIN in the I-S group. That group achieved just over half of the mean CLWG of

the T-S group, which was fed the same supplement. The I-S group also showed clinical

signs of infection by the end of the trial (diarrhoea, anaemia and hypoalbuminaemia). This

may suggest that a proportion of nutrients from their diet (supplement and browse

vegetation) was diverted from growth to other processes such as synthesis of plasma

protein, repair of gastrointestinal tract and mucus secretion (Steel et al., 1982; Symons,


Table 2

Partial budget analysis comparing the economic feasibility of the intervention groups (supplementation, treatment

and supplementation + treatment) vs. no intervention (infected + non-supplemented group) for the control of GIN

in kids browsing native vegetation during the rainy season

Supplementation group (I-S) vs. no intervention (I-NS)

(a) Additional returns Income from growth U.S.$3.38a

(b) Reduced costs Non-quantified

(c) Returns foregone None

(d) Extra costs Feed (including transport cost,

Storage and labour)

U.S.$1.54

(Net result of I-S compared to I-NS group

(a + b) � (c + d)

U.S.$1.84/animal

Treatment group (T-NS) vs. no intervention (I-NS)

(a) Additional returns Income from growth U.S.$3.72



(d) Extra costs Drug, dosing device

and gloves

U.S.$0.91

(Net result of T-NS compared to I-NS group

(a + b) � (c + d)

U.S.$2.81/animal

Supplementation and treatment group (T-S) vs. no intervention (I-NS)

(a) Additional returns Income from growth U.S.$6.51



(d) Extra costs Feed (including transport cost,

Storage and labour)

U.S.$1.54

Drug, dosing device and gloves U.S.$1.05

(Net result of T-S compared to I-NS

group (a + b) � (c + d)

U.S.$3.92/animal

a $ U.S. = United States Dollars ($1 U.S. = 10 mexican pesos).

1985; Bown et al., 1986; Rowe et al., 1988; Walkden-Brown and Kahn, 2002) which might

have been increased due to the presence/action of GIN. Nutrient partition of the I-S animals

(from growth towards maintenance of body protein) was different as the trial advanced in

time. In the first three-quarters of the trial, more growth was obtained. Meanwhile, a reduction

in the growth rate was observed in the last weeks of the trial, maybe as an indication that the

metabolic load induced by the GIN infection was overwhelming. Therefore, the animals

had to allocate more nutrients from the diet towards maintenance/repair function, as

this would guarantee their survival in the short term (Coop and Kyriazakis, 1999). This

confirms early evidence from a simulation model for GI nematodosis in goats (Hendy and

Carles, 1993), which concluded that responses to improvements in feeding systems and

to supplementary feeding are likely to be limited unless helminths are also controlled by

anthelmintic treatment. These findings indicate that a metabolic cost (in terms of

metabolizable protein and energy) of GIN must be considered as an additional term when

estimating the nutrient demand/allowance of young ruminants (Walkden-Brown and Kahn,

2002).

When LWG of the supplemented groups were compared with their non-supplemented

counterparts, the additional growth obtained from supplementation was similar in spite of

infection with GIN (22.65 and 20.36 g/day in the T-S and the I-S groups, respectively). This

suggests that, although the GI tract might have been locally damaged by the nematode

infection, there is little effect on the efficiency of utilization of the supplementary feed

(Coop and Holmes, 1996). At the present moment, we cannot fully elucidate the

mechanism of the observed response.

The growth pattern and the blood parameters (PCV, Hb, PA) of the I-NS animals

indicate that they were undernourished for the duration of the trial as well as infected with

GIN. In these animals, nutrient partition for growth may have been sacrificed for increased

maintenance function due to the GIT repair, as in the case of the I-S kids, but the

availability of nutrients was more restricted in the I-NS kids (Coop and Kyriazakis, 1999;

Walkden-Brown and Kahn, 2002).

At the beginning of the trial, weaning could have contributed to poor growth or weight

losses. At weaning, animals might be exposed to malnutrition because their feeding habits

have not yet developed (Shaw et al., 1995). A temporary cessation of growth after weaning

may be attributable to incomplete rumen development (Andrews and Orskov, 1970).

However, these factors would have affected all groups similarly. All animals were fed

fibrous diets before weaning and were allowed to browse for one week before the trial

started. The low growth rates at this early stage of the trial were mainly found in the I-NS

group. It is plausible therefore, that the reduced growth rates were the effect of the sudden

infection with GIN of the young, naive animals and the scarce availability of nutrients.

According to Coop and Kyriazakis (1999), parasite naive ruminants at this early stage of

growth have to put extra nutrients towards maintenance. Therefore, the ability of the I-NS

kids to maintain their growth rate may have been hindered by infection and/or malnutrition.

Faecal cultures and measurements of pasture infectivity with tracer kids indicated that,

as the trial advanced in time, the infected animals were facing a mixed infection which

included GIN of the abomasum, small and large intestines. The mixed infection was

especially evident in the last two months of the trial. During this period, the clinical signs of

infection in the infected groups were more severe. This was expected as the number and


species of worms established determines the extent of the metabolic impairment caused by

parasites (Van-Houtert and Sykes, 1996). Mixed nematode infections might have caused

endogenous losses of protein into the GI tract (Poppi et al., 1986; Rowe et al., 1988; Parkins

and Holmes, 1989). The endogenous losses might have been reabsorbed in the posterior

tract (Bown et al., 1991). However, posterior tract absorption of nitrogen (N) is largely un-

utilized by the host’s metabolic processes (Rowe et al., 1988). Furthermore, N recycling

has an energy cost, adding to the inefficiency of energy utilization in parasitized animals

(Sykes and Coop, 1976, 1977). Supplementary feeding probably compensated for part of

the extra metabolizable protein and energy that infected animals had to spend in order to

cope with GIN.

In this trial it is not possible to determine the definitive role of energy, protein and other

individual nutrients supplemented to these kids in the improvement of resilience. However,

there is a possibility that MP offered in the supplement was not fully utilized by the

browsing animals because insufficient energy is available in the total diet to fuel protein

deposition. A controlled infection trial with Criollo kids (Torres-Acosta et al., 2000)

showed that dietary protein supplementation did not improve growth rate when compared

to non-supplemented kids fed iso-energetic diets. Nitrogen balance trials showed that those

kids in the high protein diet had significantly higher excretion of urinary nitrogen, which

was evidence that the animal had a reduced supply of energy and, as a result N was not

coupled into protein and was wasted as urine-N. It is possible that the same is happening

under the rangeland conditions of the centre of Yucatan, which are known to be rich in

browsing legumes (Flores and Espejel, 1994). If this is the case, further browsing trials are

needed in order to determine whether rumen degradable energy can take advantage

of the available browsing legumes leading to positive effects on the resilience against

GIN infection in kids. Recent work showed beneficial effects of digestible energy

supplementation on resistance to GIN (Kahn et al., 2000; Valderrabano et al., 2002). A

further hypothesis needing confirmation is that supplemented kids could have induced an

increase in browsed intake. The postulated increase in intake may have resulted from two

pathways: firstly appetite stimulation as result of extra protein intake, and secondly a better

rumen environment (Van-Soest, 1994).

Appetite depression is a common feature of GI nematodosis (Coop and Holmes, 1996;

Van-Houtert and Sykes, 1996). Suppression of appetite could be responsible for substantial

negative effects in infected malnourished kids. However, it was not possible to determine if

the infected animals had a lower intake of browsed vegetation than the treated animals.

Therefore, further consideration should be given to this variable in future trials, as

attempted elsewhere (Anindo et al., 1998).

The use of moxidectin in this trial achieved a good degree of control of GIN, which

enabled the experimental design to separate the effects of nutrition from those of GIN

infection. The effect on growth of GIN control with the anthelmintic was of a similar

magnitude to that of supplementation. Extra food requirement imposed by GIN infection in

browsing animals can be estimated as 100 g/day of the supplementary feed needed for the

I-S animals to achieve similar growth to that of T-NS kids.

Treated animals during the wet season can show poor growth and anaemia. Several

animals in the T-NS group showed signs of anaemia. It is possible that, the low PCV might

have resulted from insufficient nutrients available from the seemingly abundant vegetation


during the rainy season. This is in accordance with findings of Papachristou and Nastis

(1996) that browsing goats may obtain enough nutrients for maintenance plus moderate

activity from browsing vegetation but only a fraction of the nutrients required for

production. This has not been reported before in Yucatan, but agrees with the observation

that the growth rate of the T-NS kids was 37.1% lower than that of the T-S animals. No

work has yet described the rate of growth of non-supplemented Criollo goats browsing

native vegetation during the rainy season in Yucatan. The present trial has brought doubts

on that assumption that the abundance and variety of browsing vegetation is sufficient for

the nutrition of goats at different production stages.

Loose faeces. There was a severe period of diarrhoea observed only in the infected

groups, which may have accounted for some of the observed weight-loss, anaemia and

hypo-albuminaemia. Diarrhoea was common in the infected groups by the end of the trial

when T. colubriformis infection was more abundant. Loose faeces could have caused

negative nutrient balance because of decreased digestion and absorption resulting in body

wasting (Hornbuckle and Tennant, 1997).

Blood parameters. Supplementary feeding delayed marked reductions in the PCV until

almost the end of the trial in the I-S animals. Similar findings have been reported in several

pen trials with sheep (Wallace et al., 1996; Datta et al., 1998) and goats (Blackburn et al.,

1992). For most of the trial, the effect of supplementary feeding on PCV was similar to that

of anthelmintic treatment alone. Supplementation in the I-S group produced an

improvement of resilience in these kids allowing them to maintain their PCV within

the normal range for most of the trial. However, infection rendered these kids anaemic at

the end of the trial, probably as a result of a reduction in their iron reserves (Anderson,

1982) impairing erythropoiesis (Dargie and Allonby, 1975). The Hb concentration in

several I-S kids was low from week 8. This could have resulted from low serum iron

complicated by a relative failure of globin synthesis due to persisting protein-losing

gastroenteropathy (Jennings, 1976). An unknown degree of reduction in Hb concentration

may also have been related to under-nourishment, as the Hb concentration of some animals

in the T-NS group was also low. PCVand Hb values were reduced in the I-NS group to such

a degree that four animals needed to be withdrawn from the trial on welfare grounds.

Undernourished ruminants show anaemia as a common feature when severely infected

with H. contortus (Abbott et al., 1988; Wallace et al., 1995; Blackburn et al., 1991). Under-

nutrition possibly limited the extent to which the host endured infection (Anderson, 1982).

All four severely affected animals in the I-NS group were hypo-albuminaemic when

withdrawn from the trial. Hypo-albuminaemia is a common sign of severe infection with

GIN (Abbott et al., 1988; Parkins and Holmes, 1989; Blackburn et al., 1991).

Supplementation was shown to increase resilience of I-S animals as they did not show

severe disease in spite of being anaemic and hypo-albuminaemic.

4.2. Resistance

A steady increase of PEC in all groups could have been the result of acquisition of

resistance against GI parasites rather than a reflection of the level of parasitism (Patterson

et al., 1996; Amarante et al., 1999). However, the interesting feature was that kids in the

supplemented groups showed eosinophilia (PEC above 1 � 109/l) more times during the


trial than those in the non-supplemented groups. Furthermore, some supplemented animals

(infected and treated) had several PEC values above 2 � 109/l while non-supplemented

animals did not. Supplementation therefore enabled the PEC of Criollo kids to increase as

has been reported in sheep artificially infected with T. colubriformis (Van-Houtert et al.,

1995b), H. contortus (Datta et al., 1998) and Nematodirus battus (Israf et al., 1996). A high

PEC following continuous infection may be a useful indicator of the acquisition of

resistance (Rothwell et al., 1993; Stear et al., 1995), although contradictory evidence does

exist (Woolaston et al., 1996). Thus, the results of this trial show that supplementation

seems to have improved not only resilience but also resistance of Criollo kids against GIN.

On the other hand, not all the kids with a high FEC and/or showing clinical signs of GI

nematodosis had an overt eosinophilia. Pernthaner et al. (1995) have reported this lack of

consistency in the relationship between FEC and eosinophils in sheep. The PEC of the

worst affected kids had fallen to zero by the time they were retired from the trial. This

reduction in PEC might have been the effect of depletion of body reserves used for the

formation of these cells (Bundy and Golden, 1987), a reduction in eosinopoiesis due to

depletion of bone marrow and/or a reduction in the available protein or energy for the

production of activation factors (Jones, 1993). Furthermore, these animals might have been

so stressed by the GIN infection and under-nourishment that their own corticosteroid

production increased and affected their cell mediated immunity (Halliday, 1980). The

responsiveness of Criollo kids to GIN infection has not been addressed before and further

investigation is needed. Work in African breeds of sheep has shown that the more resistant

breeds (against GIN) show higher PEC responses than non-resistant breeds (Mugambi et

al., 1996).

Supplementation of the non-treated groups had no effect on the FEC of strongylid

nematodes. Previous controlled pen trials have shown that supplementary feeding reduces

FEC only if the breed of animal studied is highly susceptible to GIN (Wallace et al., 1996).

Otherwise, the FEC of supplemented animals is not reduced when compared to non-

supplemented groups (Abbott et al., 1985; Wallace et al., 1996). This may therefore

indicate that Criollo kids have a relatively high level of innate resistance. Furthermore, two

kids in the I-S group and one in the I-NS group maintained their FEC below 1000 EPG for

the duration of the trial and did not show signs of anaemia. Natural selection of the Criollo

goats in the sub-humid tropics of Yucatan has possibly enhanced resistance. Similar results

have been obtained in other tropical breeds of sheep and goats (Waller, 1999; Baker et al.,

2003).

Oral moxidectin treatment at 28-day intervals controlled the FEC of trichostrongylid

nematodes almost completely as was expected (Torres-Acosta and Jacobs, 1999). Low FEC

values on the 28th day post-treatment were anticipated because no persistent activity was

found against T. colubriformis. Faecal cultures confirmed the presence of Trichostrongylus

spp. larvae in the treated groups. As moxidectin owes its persistent effect to its lipophilicity

(Taylor et al., 1993), it is possible that the T-NS animals in this trial might not have had

adequate amounts of fat to ensure maximum efficacy compared to the T-S group, which was

noticeably better nourished. No kids were slaughtered in either of the groups, therefore no

comparative information on their omental and subcutaneous fat is available.

Economic analysis. The partial budget analysis showed that the control of GIN by

supplementation has an economic advantage over no intervention. However, during the


rainy season, treatment to keep non-patent levels of infection and the combination of

treatment and supplementation are more advantageous. The economic analysis reflected

the biological fact that, although supplementation did increase the resilience of Criollo kids

against GIN during the rainy season, their productivity was still compromised. This

analysis also reflected the cost of the feed refused during the trial, which left

supplementation less efficient in economic terms.

The treatment scheme employed in this trial was intended to provide information on the

production of Criollo kids kept as parasite free as possible and is not intended as a

recommendation for farmers. However, under the conditions of this trial, the most

economically feasible intervention was the combination of supplementation and treatment.

Control of GIN by anthelmintic treatment alone did not achieve maximum productivity in

the kids. The treatment frequency used in this trial might accelerate the onset of

anthelmintic resistance. Thus, supplementation was more expensive than keeping the kids

free of infection (treatment) as suggested by Van-Houtert and Sykes (1996). However, the

effect of supplementation on growth rate was so important that even the use of conventional

feedstuffs, which were only intended to address a scientific question, were economically

justified. The principles of supplementation illustrated in this trial should be applied using

local feedstuffs, as suggested elsewhere (Knox and Steel, 1996; Anindo et al., 1998).

The supplementation strategy used may allow a reduced frequency of anthelmintic

treatment during the rainy season in browsing kids. Based on the information from the I-S

kids, it seems plausible that a single anthelmintic treatment in September could have been

sufficient to avoid the worst consequences of nematodosis. Thus, a single treatment might

be all that is necessary to optimize production during the wet season in the central zone of

Yucatan. Further trials would be essential to test this hypothesis.

5. Conclusion

Supplementary feeding increased the resilience of Criollo kids against natural GIN

infections during the rainy season in Yucatan, Mexico. Improved resilience was expressed

as enhanced CLWG and less severe pathophysiologial effects (reflected especially in PCV,

Hb and PA values). However, the benefits of supplementation alone were not sufficient to

control the negative effects of GIN for the totality of the trial. PEC in supplemented groups

might be a sign of increased development of resistance against GIN. This was not

confirmed in the excretion of FEC. The partial budget economic analysis showed that

supplementation was an economically feasible alternative.

Acknowledgements

This study was funded by CONACYT-Mexico (project 25019-B). We greatly

acknowledge the support of the staff at the FMVZ-UADY goat farm. We also thank

the technical assistance of MVZ Melchor Capetillo and MVZ Lesly Castillo. We greatly

appreciated the valuable advice of F. Jackson and R. Coop (Moredum Research Institute) in

the planning of this trial.


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