Small Ruminant Research 204 (2021) 106518

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Small Ruminant Research

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Impact of different feeding systems on cost-effectiveness and Eimeria spp.

infections in Canarian goat kids
Alexandr Torres a, *, Juan Capote a, María Fresno a, Alejandra Eguiza b, Emilio Barba c,
José Manuel Molina c, Antonio Ruiz c
a
Unit of Animal Production, Pasture, and Forage in Arid and Subtropical Areas, Canary Islands Institute for Agricultural Research, 38200, La Laguna, Spain
b
College of Veterinary Medicine, National Autonomous University of Mexico, 04510, Mexico City, Mexico
c
Department of Animal Pathology, Parasitology Section, Faculty of Veterinary Medicine, University of Las Palmas de Gran Canaria, 35413, Arucas, Spain

A R T I C L E I N F O A B S T R A C T

Keywords: Rearing strategies are key factors in the overall success of goat enterprises. In order to investigate the cost-benefit
Economic performance ratio of alternative methods for rearing and the impact on the course of Eimeria infections, 36 Canarian goat kids
Eimeria infection were subjected to three different regimes under field conditions. Two groups of animals were naturally reared
Goat kid growth
with their mothers, feeding goat milk until weaning at 6 (Early weaning, EW) and 9 weeks of age (Traditional
Rearing system
weaning, TW). In the remaining group, goat kids were artificially reared with a milk replacer until 9 weeks of age
(Artificial feeding, AF). Coprological analysis were performed weekly to determine Eimeria oocyst shedding and,
with the same frequency, changes in body weights and faecal consistency were recorded. Goat kids from group
TW showed the best growth rate, while growth performance of groups EW and AF were statistical similar. Be­
sides, compared to group TW, EW and AF management practices resulted in an overall increase of about 40 %
and more than 100 % of the total number of oocysts excreted until the end of the experiment (week 15),
respectively. Although the three experimental groups were infected with the same Eimeria species, differences in
their oocysts excretion kinetics, including those of most pathogenic species, were observed throughout the
experiment, indicating that the type of rearing may affect the outcome of underlying coccidiosis in the farm.
Finally, the economic analysis determined that, mainly conditioned by the market price of goat milk, total
operating costs per goat kid from groups EW (56.37 €) and AF (48.63 €) systems were considerably lower than
those obtained in group TW (96.32 €). The selection of the former two rearing systems should be conditioned
though to the use of management strategies preventing coccidiosis outbreaks.

1. Introduction other hand, artificial rearing during the first weeks of life can result in
good daily weight gain, and is of particular interest in disease eradica­
In the Canary Islands and some Mediterranean regions, goat kids are tion and control programs (Morales-delaNuez et al., 2011). However,
traditionally reared with their dams, and later they are weaned at despite the fact that several automatic feeding systems are commercially
around 9 weeks of life. Although this practice promotes an optimal available (Bimczok et al., 2005) and milk replacer is markedly cheaper
growth and reduces weaning shock, it decreases the availability of milk than goat milk, many small and medium farmers are reluctant to its use
for cheese production, and may lead to economic losses (Lu and because, in their opinion, this type of rearing involves greater labor cost
Potchoiba, 1988; Argüello et al., 2005). Thus, it has been reported that (Argüello et al., 2005).
early weaning at 4 and 6 weeks increases the marketable quantity of Infections produced by Eimeria spp. are one of the most important
milk without causing a negative impact on the growth of goat kids, parasitic diseases in goat production systems worldwide (Chartier and
which provides important benefits to the farm (Gökdal et al., 2017; Paraud, 2012), mainly in arid and semi-arid areas (Ruiz et al., 2006;
Panzuti et al., 2018). Nevertheless, abrupt early weaning may cause Cavalcante et al., 2012). Although 100 % of the animals of a herd may be
growth retardation and weight loss, because the maturation of the infected by the parasite, clinical disease is mainly reported in young
digestive system is still incomplete (Magistrelli et al., 2013). On the animals (Ruiz et al., 2006; Keeton and Navarre, 2018), while adults are

* Corresponding author at: Canary Islands Institute for Agricultural Research, P.O. box 60, 38200, La Laguna, Tenerife, Spain.
E-mail address: [email protected] (A. Torres).

https://doi.org/10.1016/j.smallrumres.2021.106518
Received 24 July 2020; Received in revised form 30 August 2021; Accepted 31 August 2021
Available online 4 September 2021
0921-4488/© 2021 Elsevier B.V. All rights reserved.
A. Torres et al. Small Ruminant Research 204 (2021) 106518

usually asymptomatic carriers due to development of immunity (Dai 10 of the experiment. Animal procedures were conducted in strict
et al., 2006; Ruiz et al., 2013a). Clinical signs associated to coccidiosis accordance with national ethics, the current European Animal Welfare
by Eimeria spp. include dehydration, anorexia, weight loss, weakness Legislation (ART13TFEU) and by institutional review board-approved
and recumbency. Coccidiosis is also accompanied by diarrhea varying in protocols.
severity from yellowish to brownish faeces of different consistency,
sometimes watery faeces containing blood and small pieces of the in­ 2.2. Clinical and parasitological determinations
testinal mucosa (Ruiz et al., 2013a, b; Ruiz et al., 2014).
Monospecific Eimeria infections in goats are uncommon in field The amount of oocysts per gram of faeces (OPG) was determined
conditions, where the rule is that, irrespectively of the age, animals are using a modified McMaster technique (Thienpont et al., 1979). Dilutions
infected by two, three or even more different Eimeria spp. (Balick­ of the faecal suspension by 10 or 100 times were done to enable counting
a-Ramisz et al., 2012; Zhao et al., 2012). Four species are known to be when the number of oocysts was very high. The faecal consistency (FS)
highly pathogenic and most times they are the most prevalent, namely was scored immediately after individual collection according to keys
E. ninakohlyakimovae, E. arloingi, E. christenseni and E. caprina described previously (Ruiz et al., 2014). Signs of diarrhoea were judged
(Hashemnia et al., 2012; Andrews, 2013). In goat kids, coccidiosis may as evident when FS was > 0 or when faeces of lower consistency were
be a problem from the third or fourth week of life onwards and, observed down legs, including explosive, fluid and watery diarrhoea.
particularly, during weaning due to stress caused by changes on feeding Every sampling week, faecal samples from animals of each group
diets, separation from their dams, location into different pens, etc. (Ruiz were also pooled for the identification of the different Eimeria species.
et al., 2006). This leads to important economic losses, which are derived For this purpose, faecal cultures were performed in 2 % potassium di­
from deaths, delayed growth rate, treatments and veterinary assistance chromate at room temperature (20− 25 ◦ C) for at least one week in Petri
(Fthenakis and Papadopoulos, 2018; Windsor et al., 2018). culture-dishes to allow sporulation. Oocysts were then concentrated by
The aim of the present study was to assess the cost benefit associated flotation in saturated sodium chloride, washed with distilled water,
with the application of three management strategies of rearing goat kids centrifuged at 1500 x g for 10 min and preserved at 4 ◦ C until the
and to evaluate the impact on the course of Eimeria infections in field analysis was performed. The identification was carried out under a 40X
conditions. objective using a calibrated eyepiece according to keys reported previ­
ously (Levine and Ivens, 1986; Alyousif et al., 1992; Soe and Pomroy,
2. Materials and methods 1992).

2.1. Experimental animals

2.3. Economic analysis
The trial was a reference-controlled field study with parallel groups
In order to compare the costs among the three management strate­
and was carried out in the facilities of the experimental farm of the
gies, the feed efficiency ratio of goat milk (FER, intake/gain) in goat kids
Instituto Canario de Investigaciones Agrarias in Tenerife (Spain). Thirty-
of the same experimental farm was calculated at 6 and 9 weeks. Thus,
six Canarian goat kids from birth to 15 weeks of age were included in
the milk suckled by animals weaned at early stage and those reared
this study. Goat kids were divided into three balanced groups (n = 12, 6
under traditional model could be estimated, and the corresponding
males and 6 females) allocated in separated pens. Traditional weaning
outcome could be considered as marketable milk. For this purpose, 14
group (TW) included animals that were kept with their dams from birth
goat kids (7 males and 7 females) were fed three times a day (0800, 1300
until weaning at 9 weeks of age. Commercial starter concentrate (Grupo
and 1800 h) during 9 weeks by using bucket feeders fitted with nipples.
Capisa, Spain), alfalfa and water were provided as of 2 weeks of age. In
Milk consumption was recorded daily and goat kids were weighted
Early weaning group (EW), animals were kept with their dams from
weekly. The FER of goat milk obtained were 7.71 L/kg and 9.81 L/kg at
birth, as in TW group, but weaning took place at 6 weeks of age. Early-
6 and 9 weeks, respectively. In Canary Islands, the average milk price in
weaning concentrate (Cereales Archipiélago, Spain), alfalfa and water
2019, including subsidies, was 0.82 €/L (BOC, 2019; FEGA, 2020).
were also provided as of 2 weeks of age. After weaning and until 9 weeks
Prices paid for milk replacer and early-weaning concentrate were 2.60
of age, goat kids were fed with a controlled level of early-weaning
and 1.40 €/kg, respectively. Labor expenses for each rearing manage­
concentrate (500 g/d/kid) and alfalfa. In Artificial feeding group (AF),
ment were estimated according to Delgado-Pertíñez et al. (2009a) and
goat kids remained with their dams for 2 days to receive colostrum.
considered a work wage of 10.0 €/h. Other artificial feeding costs were
Thereafter, they received ad libitum milk replacer (Bacilactol®, Grupo
also taken into account, such as depreciation and maintenance for the
Capisa, Spain) reconstituted at 16 % w/w using an automated feeding
automatic feeder, water and electricity consumption. Calculations were
system until weaned (9 weeks of age). Similar to TW group, goat kids
made per goat kid from birth until 9 weeks of life.
were previously exposed to commercial starter concentrate, alfalfa and
water. From week 9 onwards, all the animals were exclusively fed with
commercial starter concentrate (1000 g/d/kid) and alfalfa. The main 2.4. Statistical analysis
composition of the feed is shown in Table 1. Body weight of each goat
kid (BW) was recorded weekly and faecal samples were weekly collected Information on the growth pattern helps to determine the efficacy of
from the rectum from 5 to 15 weeks of age. All animals were treated with feeding and breeding strategies (Lambe et al., 2006). Growth curve
2 mg/kg BW p. o. of diclazuril (Rumicox®, Esteve Veterinaria) at week parameters were estimated according to the Gompertz equation:

f(x) = Wfexp{[1− exp(-bx)]ln(Wf/W0)}

Table 1 where f(x) was BW at age x, W0 and Wf were the zero- and infinite-time
Composition of the feeds. values of BW, respectively, and b was constant (Porter et al., 2010). BW
Starter Early-weaning Milk and age were given in kilograms and weeks, respectively. Calculations
concentrate concentrate replacer were carried out with non-linear regression option. From these param­
Crude protein 17.0 17.0 23.0 eters, time of inflection (timeI), BW at inflection (BWI) and the growth
(%) rate per day at inflection (GRI.day) were calculated according to Porter
Crude fat (%) 3.4 2.5 23.0 et al. (2010).
Crude fibre (%) 6.0 4.2 0.0 Faecal oocyst counts were transformed into the logarithm of OPG
Crude ash (%) 6.1 6.0 8.2
plus one (log[OPG + 1]) to obtain normal distributions (Kolmogorov-

2
A. Torres et al. Small Ruminant Research 204 (2021) 106518

Smirnov’s Normality Test). Comparison of OPG counts among the three Table 2
management strategies was performed by One Way Repeated Measures Growth parameters in goat kids reared under three different management stra­
Analysis of Variance. For all pairwise multiple comparison procedures tegies corresponding to Gompertz equation.1
the Holm-Sidak method was used, while Krustal-Wallis test was Traditional Early Artificial SEM P-
employed for faecal score analysis. The average faecal consistency score weaning weaning feeding value
per animal and the average of log (OPG + 1) per animal were calculated Wf (kg) 29.75b 22.75a 21.94a 1.357 0.031
and then compared among the three groups by one-way ANOVA with b (wk− 1) 0.12 0.16 0.16 0.010 0.169
pairwise post-hoc comparisons by the Tukey test. timeI (wk) 6.50 5.25 5.50 0.420 0.451
BWI (kg) 10.95b 8.37a 8.08a 0.499 0.031
The Pearson correlation test was used for the analysis of the associ­
GRI.day 182.37 157.69 175.14 5.523 0.174
ation between parasitological and productive parameters (BW) at all (g/d)
sampling times (weeks 5–15). Additionally, total weight gains from R-Square 0.991 0.962 0.965
week 5 of life up to the end of the study for each kid was calculated and a–b
Means without a common superscript letter within the same row are different
Pearson correlations between this parameter and the average OPG and (P < 0.05) by using Turkey test.
FS were determined, both for each experimental group and for all three 1
W0 and Wf are the zero- and infinite-time values of BW, respectively, b is
groups together. Finally, peak OPG values of goat kids from groups TW, constant, timeI is time of inflection, BWI is BW at inflection time and GRI.day is
EW and AF were correlated with weight gain at each week following the growth rate per day at inflection time.
OPG peaks and with total weight gain between the week were peak OPG
values were found and the end of the study.
Analysis were carried out by the statistical software SigmaPlot 12.0
and the differences were considered significant at P < 0.05.

3. Results

3.1. Growth performance

Growth curves and their functional parameters according to Gom­

pertz equation are presented in Fig. 1 and Table 2, respectively. In order
to get the highest goodness of fit criteria for the Gompertz model used,
W0 was not restricted when modeling the growth data of the different
feeding and weaning treatments. The parameter that described the
mature BW (Wf) of the goat kids was significantly different, with group
TW showing a higher value than the other two groups. However, the
constant b, which determines the growth rate in the Gompertz equation
was not different among treatments (P > 0.05). As shown by Table 2, the
estimated Wf values varied between 21.94 and 29.75 kg. In addition,
significant differences for BWI among managements were observed, Fig. 2. Faecal consistency in the different experimental groups. The following
ranging between 8.08 and 10.95 kg, but there were not statistical dif­ criteria were established: 1) normal formed faeces; 2) unformed faeces of light
reduced consistency; 3) faeces of moderate reduced consistency; 4) yellowish,
ferences for GRI.day. Furthermore, all groups attained inflection at 6–7
greenish or brownish liquid faeces; 5) liquid faeces of reddish colour and/or
wk.
presence of mucosa pieces. Data are expressed as means ± SEM. a–bMeans
without a common superscript letter at the same week are different (P < 0.05)
3.2. Clinical and parasitological findings by using Holm-Sidak test.

Mean values and statistical differences of FS recorded from the ani­ animals from AF group during weeks 5 and 7 (FS > 1.8), however, this
mals of the three experimental groups are depicted in Fig. 2. The analysis value did not remain consistent and showed fluctuations. On the other
of the results shows that the highest mean FS values were observed in hand, the animals from EW group showed a reduction in faecal consis­
tency with FS values close to 1.6 in a later period (weeks 10–11), while
goat kids from TW group showed a lower mean FS value throughout the
experiment compared to the other two groups, with a slight increase at
week 11. The comparative analysis of the average faecal consistency
score per animal showed significant differences between groups, espe­
cially relevant when comparing TW and FA groups.
Mean OPG values of the three experimental groups throughout the
study has been depicted in Fig. 3. As for the faecal consistency score, the
average of log(OPG + 1) per animal were calculated and then compared
among management strategies, the results showing significant differ­
ences between the three groups, particularly when comparing EW and
AF groups. In the course of the study, TW group showed peak values at
week 7th of life and, in general, had lower mean OPG counts when
compared with the other two experimental groups. This difference was
more evident when comparisons were performed on cumulative counts
at the end of the experiment (data not shown). The kinetics of faecal
oocyst counts was different in EW and AF groups compared to TW group,
with peak values at week 9. OPG values were significantly higher in AF
group with respect groups TW and EW (P < 0.001) at this time point.
Fig. 1. Growth curves of goat kids reared under three different management
Actually, faecal counts of several animals artificially fed were extremely
strategies. The lines indicate fitted values based on the Gompertz equation.

3
A. Torres et al. Small Ruminant Research 204 (2021) 106518

The number (N) of oocysts used for Eimeria spp identification is given in bold. Other spp included: E. alijevi, E. caprina, E. caprovina, E. jolchijevi, E. hirci, E. aspheronica; W: weeks of age. Mean OPG values ± SEM (x 104) are
(12.3±4.8)
(7.5±5.1)

(0.8±0.3)
N¼98

N¼98

N¼98
49
30
10

20

60
15

30
12
42
14
9

3
W15

(8.1±2.8)

(7.2±2.0)

(5.3±3.4)
N¼101

N¼101

N¼101
48
21
19
13

10

76
10

43
17
28
13
5
W14

(12.2±3.6)
(3.3±1.1)

(6.0±2.3)
N¼100

N¼101

N¼101
74
14

16
14
48
23

18

61
14
4
8

8
W13

(0.9±0.4)

(3.8±1.7)

(0.6±0.3)
N¼100

N¼100

N¼100
61
34

14
15
41
30

65
29
3
2

4
2
Fig. 3. Fluctuation of Eimeria oocyst counts in goat kids reared under three

W12
different management strategies. The data are expressed as transformed Log
values (OPG + 1) and averages ± SEM are represented. a–cMeans without a
common superscript letter at the same week are different (P < 0.05) by using

(52.4±19.2)
(18.0±6.7)
Holm-Sidak test.

(8.9±2.2)
N¼100

N¼101

N¼101
10

56
28

27
13
37
24

20
21
26
34
6
W11
high at this week, with values reaching almost 8 million OPG, despite
these animals showed significantly lower mean OPG values at the
beginning of the study (P <0.001) compared with the other two groups.
The EW group, after reaching peak values at week 9th of life, showed

(132.6±40.4)
(40.5±11.8)

(57.3±14.5)
Eimeria spp. detected in faecal samples and mean faecal oocyst count for goats reared under three different management systems.

N¼100

N¼101

N¼101
higher mean oocyst counts than the other two experimental groups,
17

53
22

39
12
34
16

48
20
16
17
8
reaching statistical significance at weeks 11, 12 and 15 of the study (P <
W10

0.05 to P < 0.001). Interestingly, relatively high oocyst counts were

recorded after treatment with diclazuril at week 10, which was partic­
ularly evident in group EW.

(309.4±67.2)
Changes in OPG counts were positively associated to faecal score, (22.1±16.7)

(60.6±19.1)
N¼101

N¼101

N¼99
particularly in EW group (Fig. 2 and 3), while peak values for faecal
11

63
22

32
10
46
13

56
29

10
5

4
scores in group AF (highest score between weeks 7 and 8 of life) pre­
W9

ceded the increased in faecal oocyst counts (weeks 8–10). Nevertheless,

no statistical significance could be demonstrated between both param­
eters in any of the three management strategies.

(77.7±20.1)
(30.3±8.4)

(12.9±9.7)
According to higher OPG counts and transient increased values of N¼100

N¼101
N¼88

faecal scores observed in groups EW and AF, goat kids from both groups
14
46
25

21
11
48
20

60

28
3

7
6
showed decreased BWs as depicted in Fig. 1. Nevertheless, the statistical
W8

analysis revealed a lack of correlations among these parameters in both

EW (-0.027; R2 = 7.45 × 10− 4; P = 0.758) and AF (-0.008; R2 = 5.89 ×
10-5; P = 0.929) groups. Surprisingly, significant negative correlations
(64.3±21.5)

(33.0±9.6)

(32.0±8.3)
N¼100
N¼99

N¼91
between faecal oocyst counts and BW could only be demonstrated in
49
40

25
25
28
22

21
10
42
18
5
7

group TW (-0.349; R2 = 0.121; P < 0.01). Differences in weight gain

W7

were detected at the two time points after the peak of oocyst shedding
(week 9), at which points higher OPG counts were associated with lower
weight gains (P < 0.05).
(36.5±11.9)

(25.2±9.0)

(1.5±0.8)

Overall, the Eimeria species most frequently found in the three

N¼111

N¼100

N¼101
84
13

29
16
30
25

14

83

experimental groups were E. christenseni (around 40 %), followed by

5
9

E. arloingi (25–30 %) and E. ninakohlyakimovae (10–15 %); other minor

W6

species (grouped as “other species”) included E. alijevi, E. caprina, E.

caprovina, E. jolchijevi, E. hirci, E. aspheronica, which were all individu­
ally recorded in a percentage lower than 10 % (Table 3). However,
(17.6±7.6)

(16.5±6.6)

(2.9±1.3)
N¼100

N¼100

N¼100

differences in their kinetics over the course of the experiment were

44
17
34

44
17
34

33

57
5

found. Thus, the percentage of E. arloingi and E. ninakohyakimovae were

W5

high at the beginning of the sampling period (weeks 5–6 of life) in group
TW, remained relatively low up to week 13 and showed an additional
indicated in parentheses.

increase at weeks 14 and 15; while just the opposite was recorded for
Mean OPG x104 ± SEM

Mean OPG x104 ± SEM

Mean OPG x104 ± SEM

Traditional weaning

E. ninakholyakimovae

E. ninakholyakimovae

E. ninakholyakimovae

E. christenseni. Approximately the same picture was found in group EW

Oocysts counted (N)

Oocysts counted (N)

Oocysts counted (N)

Artificial feeding

but, in this case, increased frequency for E. ninakohlyakimovae was

Early weaning
E. christenseni

E. christenseni

E. christenseni

extended up to week 7 and a further increase for E. arloingi was found

Other spp

Other spp

Other spp
E. arloingi

E. arloingi

E. arloingi

between weeks 9 and 10. During this period, when the percentage of
Table 3

these two species was higher, an increase in the FS values was also
observed. The recording of data for goat kids reared under AF also

4
A. Torres et al. Small Ruminant Research 204 (2021) 106518

revealed that peak values for the most pathogenic Eimeria species gain reaches its peak at this point. However by using this formula, the
(E. ninakohlyakimovae and E. arloingi) were found between week 8 and values estimated in this study for optimal slaughter age and weight are
11, coinciding with highest values for OPG counts but, in this occasion, greater than in the real management practice, because most of the
the reduction of faecal consistency (higher FS) was observed earlier. goatkeepers in Canary Islands slaughter the male kids at a very young
After treatment with diclazuril (week 10), an increase in the per­ age: 15 days and 5–6 kg live weight (Argüello et al., 2005). Therefore, if
centages of E. arloingi and E. ninakohlyakimove was found three weeks the kids are slaughtered with higher live weights, regardless of the
later in groups TW and AF. In contrast to the previous two groups, lactation method used, there would be a significant increase in the yield
E. christenseni was the most abundant species during the whole period of the carcasses.
examined after treatment in group EW. The better growth performances exhibited by the goat kids belonging
to group TW, in comparison with the other two groups, might be
attributable not only to the intrinsic differences in nutrient composition
3.3. Economic efficiency
among goat milk, milk replacer and early-weaning concentrate but also
to the presence (long- or short-term) or absence of the dam with the
Feeding costs for the three management strategies are given in
newborn ruminant. On this way, De Paula Vieira et al. (2012) demon­
Table 4. Total operating costs per goat kid of group TW (96.32 €) were
strated that dairy calves reared with an older social companion
considerably higher than in EW (56.37 €) and AF (48.63 €) systems.
increased solid feed intake preweaning and BW gains before and after
These differences would be mainly determined by the market price of
weaning when compared with calves housed in groups of a similar age,
goat milk, early-weaning concentrate and milk replacer. Therefore,
due to the different feeding behavior as consequence of social learning.
weaning at 6 weeks of age and artificial feeding reduced feeding costs by
Thus, calves that consume little solid feed before weaning are more
around 40 % and 50 % compared to weaning at 9 weeks, respectively. In
likely to experience poor growth and prolonged hunger after weaning
addition, early-weaned goat kids do not seem to generate an important
until intake of solid feed meets their requirements for maintenance and
extra labor respect to the traditional weaning. Nevertheless, goat kids
growth (Costa et al., 2015). Furthermore, Abecia et al. (2014) reported
artificially reared using an automated feeding system required almost
differences in acetate:propionate ratio in the rumen between goat kids
twice more labor expense than those reared under natural suckling
reared with their dams and artificially reared, suggesting that the
systems.
concentrate and forage intake were lower in the animals fed on milk
replacer and isolated from adult animals, despite both groups having
4. Discussion access to the same forage and concentrate offered ad libitum.
Many authors also found a lower growth in early-weaned and/or
4.1. Growth performance artificially reared goat kids compared to those traditionally reared
(Argüello et al., 2004; Paez Lama et al., 2013; Tsiplakou et al., 2016),
The estimated Wf values obtained in the present experiment were highlighting that the severity of weaning shock may affect the growth
lower than the real Canarian goat adult weight, referenced by Castro rate immediately thereafter. However, others authors did not observe
et al. (2017) at 45 and 70 kg for females and males, respectively. It has differences in live weight at different ages between natural and artificial
been reported that Gompertz model can underestimate the asymptote rearing systems (Delgado-Pertíñez et al., 2009a, b; De Palo et al., 2015).
constant in goats, especially when the kid’s weighing age is limited to Indeed, new technology and feed additives in manufacturing milk re­
less of 4 months of life (Najari et al., 2007). Besides, it is important to placers and starter feeds for calves, lambs and goat kids have improved
emphasize that the performance of Gompertz equation or any other its palatability, stability, and digestibility. On the other hand, it should
growth models may be constrained by short-term variations that are less be noted that groups EW and AF both had a similar growth pattern
influent in long-term growth as noted by Rocha et al. (2015). Moreover, throughout the experimental period (Fig. 1). Thus, the BW of EW kids at
the literature reports a wide range for timeI and BWI for different goat 15 wk (16.18 ± 3.82 kg) was statistically similar to that of AF kids
breeds, and even for the same breed. Thus, for example, Gaddour and (17.07 ± 1.31 kg), but both were significantly lower than that of TW kids
Najari (2008) and Kume and Hajno (2010) estimated for Alpine goats a (20.42 ± 3.71 kg). In the present study, a compensatory weight gain
BWI of 6.08 and 9.04 kg at a timeI of 15.5 and 47 days, respectively. after weaning for groups EW and AF could not be found. However, other
Ghiasi et al. (2018) noted that such differences in growth parameters studies demonstrated a growth compensation in animals weaned at early
may be explained by genotype factor, data structure and management stages or artificially reared, which might be achieved by increasing
strategy. The same authors apprised that age and weight at inflection feeding supply and/or a more efficient use of food after weaning (Paez
point may be used to determine the optimal slaughter age, because BW Lama et al., 2013; Panzuti et al., 2018). Anyway, it would be interesting
for further works to determine the minimum age at which appreciable
Table 4 compensation can take place in Canarian goats reared under alternative
Feeding costs per goat kid reared under three different management strategies.1 weaning systems, because the resulting changes in growth rates may
Traditional Early Artificial only have a short-time effect.
weaning weaning feeding

Marketable milk consumed 108.40 49.72 – 4.2. Clinical and parasitological findings
(L)
Suckled milk cost (€) 88.89 40.77 – Goat kids get contact with Eimeria spp. short after kidding, probably
Early-weaning concentrate – 5.46 –
consumed (kg)
by the intake of oocysts adhered to the udders of their dams and, sub­
Early-weaning concentrate – 7.65 – sequently, by the ingestion of oocysts from the contaminated environ­
cost (€) ment (Hidalgo Argüello and Cordero del Campillo, 1999). However, the
Milk replacer consumed (kg) – – 11.54 susceptibility of goat kids to coccidian infections and the development of
Milk replacer cost (€) 30.00
– –
clinical sings seems to be higher from the 3 weeks of life onward, most
Total feed costs (€) 88.89 48.42 30.00
Labor expense (€) 7.43 7.95 14.63 likely because certain physiological changes in the gastrointestinal tract
Other artificial feeding costs – – 4.00 of the ruminant are needed to facilitate the infection and further
(€) development of the parasite, at the same time as the protection provided
Total operating costs 96.32 56.37 48.63 by the colostrum of the dam begins to be less effective (Gregory et al.,
1
From birth to the 9th week of age. Other artificial feeding costs included: 1989). This finding is in agreement with observations of vet practi­
automated feeding system depreciation, electricity and water consumption. tioners showing that clinical signs compatible with coccidiosis are rare

5
A. Torres et al. Small Ruminant Research 204 (2021) 106518

under field conditions in goat kids younger than one month; this was the This estimation, although not technically accurate, could constitute an
reason why faecal sampling was started at 5 weeks of age. Accordingly, approximation to understand the average oocyst contamination of the
Matos et al. (2018) showed that, under experimental conditions, the environment in the different experimental groups, which has unques­
prepatent period of primary infected goat kids at week 3 and 4 of life tionable epidemiological implications. For a more precise calculation of
with E. ninakohlyakimovae was slightly longer, and their corresponding cumulative counts, daily rather than weekly counts should have been
OPG peak values were delayed some days when compared to primary considered and the amount of faeces daily released by each animal
infected animals at week 5. In the same way, younger goat kids, examined (Ruiz et al., 2014).
particularly those primary infected at 3 week of age, showed milder Changes in OPG counts were associated to faecal scores, which is
clinical signs compared to animals from older groups. In agreement, consistent with other studies that reported lower faecal consistency
animals subjected either to TW or EW did not display any significant associated with multiplication of the parasite and subsequent damage to
reduced faecal consistency compatible to diarrhoea at the beginning of the intestinal mucosa (Ruiz et al., 2013a, b; Daugschies and Najdrowski,
the experiment. By contrast, goat kids reared under AF had slightly high 2015). The relation between these two parameters was more evident in
faecal score (around 2) at week 5 of age, which was most probably not group EW, while peak values for faecal scores in group AF (highest score
attributed to Eimeria infections though, as OPG counts at this time were between weeks 7 and 8 of life) preceded the increased in faecal oocyst
relatively low and significantly reduced when compared to the other two counts (weeks 8–10). This observation would indicate that damage of
experimental groups. It has been documented that goat milk contains the intestinal mucosa and development of clinical sings already occurred
bioactive components that improve nutrient absorption, reduce the before the oocyst excretion resulting from the gamogony started. Goat
incidence of intestinal infection and balance the gut microflora in case of Eimeria species developing macroschizonts during merogony I in endo­
gastrointestinal disorder (Park, 2009). Conversely, milk replacers are thelial cells of the intestinal lymph vessels (such as
mainly based on cow’s milk powder with bigger fat globules, cereals and E. ninakohlyakimovae, E. arloingi or E. christenseni) may cause severe
vegetable fats (Hernández-Castellano et al., 2015), which have digestive injury of the gut mucosa and even develop a protective immune
limitations in goat kids and may be the reason behind the diarrhoea. response during prepatency (Matos et al., 2017). Variations in the
It was unlikely that other microbial agents (bacteria or viruses, or occurrence of these Eimeria species (having different prepatent periods)
protozoa of the Cryptosporidium genus) were a major contributor to in the infected animals could explain why the negative association be­
diarrhoea throughout the experiment as there is no history of outbreaks tween these two parameters (OPG and FS) does not always coincide in
by these other pathogens in this farm and these microbial infections are time and, accordingly, no significant correlation could be demonstrated
usually associated with earlier onset of clinical symptoms that was in any of the three management strategies.
observed in this study kids (Molina et al., 1994). Giardia infections re­ In agreement to widely accepted evidence that Eimeria infections
ported in this region are usually asymptomatic (Ruiz et al., 2008). may affect growth performance (Daugschies and Najdrowski, 2005; Ruiz
In arid and semi-arid regions, clinical coccidiosis is particularly et al., 2013a; Matos et al., 2018), experimental groups that showed
evident between 6–8 weeks, sometimes coinciding with weaning, higher OPG counts throughout the study (AF and EW), had greater
although the exact period could be affected by numerous factors growth delay. However, as previously referred for FS, significant nega­
including the degree of environmental contamination, the species tive correlations between these two parameters could not be demon­
involved, and even climatic factors (Ruiz et al., 2006). Accordingly, strated synchronously over time. In contrast, the effects of high OPG
overall faecal oocyst counts found in the present study started to become levels on growth performance were observed in subsequent weeks,
significant from week 7 onwards. However, the comparative analysis although correlations could only be demonstrated in TW group.
between the three experimental groups determined some differences The high percentage of E. christenseni identified in the course of the
when comparing mean OPG values, which were particularly evident in study, which is considered of minor pathogenicity compared to
AF group in relation to TW and EW groups. Furthermore, differences in E. ninakohlyakimovae and E. arloingi (Taylor and Catchpole, 1994),
the pattern of oocyst shedding were observed between the three man­ would explain that, despite high OPG counts reported in all groups, the
agement systems with peak oocyst shedding detected two weeks earlier presence of diarrhoea was not so evident and, indeed, watery diarrohea
for the TW group compared to EW or AF. Besides, around period where or bloody diarrhoea containing pieces of intestinal mucosa (score higher
the maximum oocyst peak occurred, the highest faecal oocyst counts that 2) was barely observed. Actually, means OPG counts largely
corresponded to AF group, with significant differences being recorded exceeded the value of 105 OPG in most of the sampling times, which we
with respect to groups TW and EW. These high levels of OPG counts could considered the threshold OPG value of clinical coccidiosis in goats
(almost 8 million OPG in some cases) could be explained by accumu­ in the Canary Islands.
lation of infective oocysts in pens where goat kids artificially fed were The high prevalence of E. christenseni found in the study farm is in
reared, as discussed by Medrano-Galarza et al. (2018) for cattle in farms agreement with data recorded by our group in current field experiments
using automated milk feeders. Interestingly, the progressive contami­ on goat coccidiosis in the Canary Island, which contrasts with that
nation of the pens would have occurred despite initial counts where published by Ruiz et al. (2006), who found E. christenseni as a minor
relatively low. In contrast to AF group, animals from groups TW and EW Eimeria species in the same geographical environment. Further studies
were housed in larger pens together with their dams. OPG counts of the would be necessary to determine whether the increase in the prevalence
mothers were not determined but, we could refer to previous data from of E. christenseni in these approximately 15 years is due to the continued
the same area showing that faecal oocyst counts in dairy goats were use of anticoccidials such as diclazuril, which seem to have a greater
relatively low (Ruiz et al., 2006), so it is expected that the environmental effect on pathogenic Eimeria species, or to self-selection derived from the
coccidian contamination of these pens was not too high. The increased immune response (innate, acquired or passive immunity transmitted by
susceptibility associated with early weaning stress could explain the colostrum), which would be more effective in highly immunogenic
higher OPG counts during the last weeks of the study observed in goat pathogenic species such as E. ninakohlyakimovae (Ruiz et al., 2013a).
kids from group EW. As indicated in the results section, although the Eimeria species
Thus, based on comparative OPG analysis among the three different identified in the different experimental groups were the same, the oocyst
management practices discussed above, TW would be the strategy in shedding kinetics were different for each of the experimental group.
which the lowest oocyst counts were overall found. Differences were However, no patterns were found for drawing definitive conclusions. As
more evident when cumulative instead of week by week counts were expected, an association between the decrease in faecal consistency and
considered. Actually, when compared to TW, EW and AF resulted in an the increase in the percentages of species considered pathogenic (e. g.
increase of about 40 % and more than 100 % of the total amount of E. arloingi and E. ninakohlyakimovae) was recorded, although this tem­
oocysts released up to the end of the experiment (week 15), respectively. poral connection would have a time delay of at least 1 week.

6
A. Torres et al. Small Ruminant Research 204 (2021) 106518

The increase in the percentages of E. arloingi and E. ninakohlyakimove Aknowledgments

observed three weeks after treatment with diclazuril both in groups TW
and AF is in agreement to data showing that transient increases in This work was supported by grant CAIA2018-0002-00-00 from the
relative percentages of E. christenseni after administration of either 1 or 2 Gobierno de Canarias. All authors have no conflict of interest and
mg/kg body weight of diclazuril were soon exceeded by those of contributed to the content of this paper.
E. arloingi and E. ninakohlyakimovae from two weeks after treatment
onwards (Ruiz et al., 2012). Compared to the previous two groups,
Declaration of Competing Interest
E. christenseni was the most abundant species during the whole period
examined after treatment in group EW. Whether the different profile of
The authors report no declarations of Interest.
Eimeria species after treatment in goat kids from this group has some
relation to the management of the weaning deserves further
investigation. References
Regardless of the differences among groups, it would be interested to
Abecia, L., Ramos-Morales, E., Martínez-Fernandez, G., Arco, A., Martín-García, A.I.,
note that relatively high oocyst counts were recorded during the two Newbold, C.J., Yañez-Ruiz, D.R., 2014. Feeding management in early life influences
weeks after treatment. This is in disagreement to data published by Ruiz microbial colonisation and fermentation in the rumen of newborn goat kids. Anim.
et al. (2012), who found OPG counts close to zero until two weeks post- Prod. Sci. 54, 1449–1454. https://doi.org/10.1071/AN14337.
Alyousif, M.S., Kasim, A.A., Al-Shawa, Y.R., 1992. Coccidia of the domestic goat (Capra
treatment upon administration of diclazuril to naturally infected goat hircus) in Saudi Arabia. Int. J. Parasitol. 22, 807–811. https://doi.org/10.1016/
kids with Eimeria. The question arises of whether this finding could be an 0020-7519(92)90131-90134.
evidence of anticoccidial resistance, as the farm has a history of repeated Andrews, A.H., 2013. Some aspects of coccidiosis in sheep and goats. Small Rumin. Res.
110, 93–95. https://doi.org/10.1016/j.smallrumres.2012.11.011.
treatment with diclazuril for almost 10 years. Further research to Argüello, A., Castro, N., Capote, J., 2004. Growth of milk replacer kids fed under three
address this hypothesis need to be accomplished. different managements. J. Appl. Anim. Res. 25, 37–40. https://doi.org/10.1080/
09712119.2004.9706470.
Argüello, A., Castro, N., Capote, J., Solomon, M., 2005. Effects of diet and live weight at
4.3. Economic efficiency slaughter on kid meat quality. Meat Sci. 70, 173–179. https://doi.org/10.1016/j.
meatsci.2004.12.009.
In the Canary Islands, the demand for goat milk for cheese produc­ Balicka-Ramisz, A., Ramisz, A., Vovk, S., Snitynskyj, V., 2012. Prevalence of coccidia
infection in goats in Western Pomerania (Poland) and West Ukraine region. Ann.
tion is expected to increase in the coming years (Fresno et al., 2014), so
Parasitol. 58, 167–171.
feeding milk to kids would be expensive if the current market prices are Bimczok, D., Röhl, F.W., Ganter, M., 2005. Evaluation of lamb performance and costs in
maintained or increased. Delgado-Pertíñez et al. (2009b) and Hassan motherless rearing of German Grey Heath sheep under field conditions using
automatic feeding systems. Small Rumin. Res. 60, 255–265. https://doi.org/
et al. (2018) reported that natural rearing was around 30 % more
10.1016/j.smallrumres.2004.12.008.
expensive than artificial rearing in Payoya and Shami goats, respec­ BOC, 2019. Ayuda al productor de leche de caprino-ovino" del Programa Comunitario de
tively. However, Paez Lama et al. (2013) found that total operating costs Apoyo a las Producciones Agrarias de Canarias. http://www.gobiernodecanarias.or
of Criollo kids raised on milk replacer were significantly higher than the g/boc/2019/158/004.html (01/04/2020).
Castro, N., Argüello, A., Capote, J., 2017. The Canary Islands’ Goat Breeds (Majorera,
costs of kids raised with goat milk. This is basically due to the low price Tinerfeña, And Palmera): An Example of Adaptation to Harsh Conditions.
of the goat milk in Argentina used in their calculations (0.41 €/L). Sustainable Goat Production in Adverse Environments: Volume II. Springer, Cham,
Moreover, these same authors estimated a reduction of 22 % in the pp. 221–231.
Cavalcante, A.C., Teixeira, M., Monteiro, J.P., Lopes, C.W., 2012. Eimeria species in dairy
feeding costs whether the kids were weaned at 30 or 45 days of age. goats in Brazil. Vet. Parasitol. 183, 356–358. https://doi.org/10.1016/j.
Thus, weaning at early stages would be beneficial in terms of economic vetpar.2011.07.043.
profitability because of the highest marketable milk (Delgado-Pertíñez Chartier, C., Paraud, C., 2012. Coccidiosis due to Eimeria in sheep and goats, a review.
Small Rumin. Res. 103, 84–92. https://doi.org/10.1016/j.smallrumres.2011.10.022.
et al., 2009a). Costa, J.H.C., Meagher, R.K., Von Keyserlingk, M.A.G., Weary, D.M., 2015. Early pair
On the other hand, it should be emphasized that about 89 % of 400 housing increases solid feed intake and weight gains in dairy calves. J. Dairy Sci. 98,
cheese factories in Canary Islands are small farmhouses (Fresno et al., 6381–6386. https://doi.org/10.3168/jds.2015-9395.
Dai, Y.B., Liu, X.Y., Liu, M., Tao, J.P., 2006. Pathogenic effects of the coccidium Eimeria
2014), so is not easy to implement, from an economic perspective, an
ninakohlyakimovae in goats. Vet. Res. Commun. 30, 149–160. https://doi.org/
automated milk feeding system in the farm. Other option for the farmers 10.1007/s11259-006-3228-1.
would be the use of bucket feeders fitted with nipples, which are Daugschies, A., Najdrowski, M., 2005. Eimeriosis in cattle: current understanding. J. Vet.
Med. B 52, 417–427. https://doi.org/10.1111/j.1439-0450.2005.00894.x.
cheaper, but Bimczok et al. (2005) estimated that labor costs for bucket
De Palo, P., Maggiolino, A., Centoducati, N., Tateo, A., 2015. Effects of different milk
feeders were two to three times higher than for automated systems. replacers on carcass traits, meat quality, meat color and fatty acids profile of dairy
Hence, artificial rearing gives rise to considerable misgivings for small goat kids. Small Rumin. Res. 131, 6–11. https://doi.org/10.1016/j.
goat keepers about additional labor costs and supplies associated with smallrumres.2015.09.001.
De Paula Vieira, A., Von Keyserlingk, M.A.G., Weary, D.M., 2012. Presence of an older
this management. Notwithstanding the above, Delgado-Pertínez et al. weaned companion influences feeding behavior and improves performance of dairy
(2009a, b) explained that the situation might be very different for those calves before and after weaning from milk. J. Dairy Sci. 95, 3218–3224. https://doi.
families that produce and commercialize their own cheese through org/10.3168/jds.2011-4821.
Delgado-Pertíñez, M., Guzmán-Guerrero, J.L., Mena, Y., Castel, J.M., González-
market channels, because goat milk acquires a much higher value than Redondo, P., Caravaca, F.P., 2009a. Influence of kid rearing systems on milk yield,
that paid to the producer who sells it to the dairy industry. kid growth and cost of Florida dairy goats. Small Rumin. Res. 81, 105–111. https://
doi.org/10.1016/j.smallrumres.2008.12.007.
Delgado-Pertíñez, M., Guzmán-Guerrero, J.L., Caravaca, F.P., Castel, J.M., Ruiz, F.A.,
5. Conclusion González-Redondo, P., Alcalde, M.J., 2009b. Effect of artificial vs. natural rearing on
milk yield, kid growth and cost in Payoya autochthonous dairy goats. Small Rumin.
The application of artificial feeding system or weaning at 6 weeks in Res. 84, 108–115. https://doi.org/10.1016/j.smallrumres.2009.06.014.
FEGA, 2020. Datos de las declaraciones obligatorias del sector lácteo ovino/caprino.
goat kids could improve the profitability of dairy goat farms by an in­ Ministerio de Agricultura, Pesca y Alimentación. https://www.fega.es/sites/def
crease in marketable milk yield in Canary Islands. However, animals ault/files/Fega_Decl_Lact_OviCapr_2020_01.pdf (01/04/2020).
reared under the traditional system exhibited the best growth perfor­ Fresno, M., Álvarez, S., Diaz, E., Virto, M., de Renobales, M., 2014. Sensory profile of raw
goat milk cheeses made with artisan kid rennet pastes from commercial-weight
mance and the lowest oocyst counts overall, despite the fact that this
animals: alternative to farmhouse goat cheeses. J. Dairy Sci. 97, 6111–6115. https://
system involves much higher total feed costs. Therefore, farmers and doi.org/10.3168/jds.2014-8238.
veterinary technicians must consider the history of clinical coccidiosis Fthenakis, G.C., Papadopoulos, E., 2018. Impact of parasitism in goat production. Small
and farm characteristics (production, size, kidding interval, health sta­ Rumin. Res. 163, 21–23. https://doi.org/10.1016/j.smallrumres.2017.04.001.
Gaddour, A., Najari, S., 2008. Adjustment of the kid’s growth curve in pure goat breeds
tus, labor availability, etc.) in order to decide which rearing method best and crosses under southern Tunisian conditions. J. Appl. Anim. Res. 34, 117–120.
suits the productive, sanitary and economic needs. https://doi.org/10.1080/09712119.2008.9706954.

7
A. Torres et al. Small Ruminant Research 204 (2021) 106518

Ghiasi, H., Lupi, T.M., Mokhtari, M.S., 2018. The estimation of genetic parameters for Najari, S., Gaddoun, A., Hamouda, M.B., Djemali, M., Khaldi, G., 2007. Growth model
growth curve traits in Raeini Cashmere goat described by Gompertz model. Small adjustment of local goat population under pastoral conditions in Tunisian arid zone.
Rumin. Res. 165, 66–70. https://doi.org/10.1016/j.smallrumres.2018.06.015. J. Agron. 6, 61–67.
Gökdal, Ö., Özuğur, A.K., Atay, O., Eren, V., 2017. The effects of individual weaning Paez Lama, S., Egea, V., Grilli, D., Fucili, M., Allegretti, L., Guevara, J.C., 2013. Growth
based on birth weight on growth performance and milk yield in dairy goats. Turk. J. and economic performance of kid production under different rearing systems and
Vet. Anim. Sci. 41, 672–678. https://doi.org/10.3906/vet-1611-71. slaughter ages in arid areas of Argentina. Small Rumin. Res. 110, 9–14. https://doi.
Gregory, M.W., Catchpole, J., Nolan, A., Hebert, C.N., 1989. Ovine coccidiosis: studies on org/10.1016/j.smallrumres.2012.08.005.
the pathogenicity of Eimeria ovinoidalis and E. crandallis in conventionally-reared Panzuti, C., Mandrile, G., Duvaux-Ponter, C., Dessauge, F., 2018. Early weaning and high
lambs, including possible effects of passive immunity. Dtsch. Tierärztl. Wochenschr. feeding level in post-weaning period did not impact milk production in Alpine dairy
96, 287–292. goats. J. Dairy Res. 85, 277–280. https://doi.org/10.1017/S0022029918000377.
Hashemnia, M., Khodakaram-Tafti, A., Razavi, S.M., Nazifi, S., 2012. Experimental Park, Y.W., 2009. Bioactive components in goat milk. Bioactive Components in Milk and
caprine coccidiosis caused by Eimeria arloingi: morphopathologic and electron Dairy Products. John Wiley & Sons, p. 43.
microscopic studies. Vet. Res. Commun. 36, 47–55. https://doi.org/10.1007/ Porter, T., Kebreab, E., Darmani Kuhi, H., López, S., Strathe, A.B., France, J., 2010.
s11259-011-9511-9519. Flexible alternatives to the Gompertz equation for describing growth with age in
Hassan, T.M.M., Abdelfattah, F.A., Kamel, M.S.A., 2018. Effect of milk replacer on kid turkey hens. Poultry Sci. 89, 371–378. https://doi.org/10.3382/ps.2009-00141.
pre-weaning growth, milk production and farm profitability of Shami goat. Egypt. J. Rocha, N.S., Vieira, R.A.M., Abreu, M.L.C., Araujo, R.P., Glória, L.S., Tamy, W.P.,
Anim. Prod. 55, 43–50. Nova, C.H., Fernandes, A.M., 2015. Traditional and biphasic nonlinear models to
Hernández-Castellano, L.E., Moreno-Indias, I., Morales-delaNuez, A., Sánchez-Macías, D., describe the growth of goat kids of specialized dairy breeds. Small Rumin. Res. 123,
Torres, A., Capote, J., Argüello, A., Castro, N., 2015. The effect of milk source on 35–46. https://doi.org/10.1016/j.smallrumres.2014.11.002.
body weight and immune status of lambs. Livest. Sci. 175, 70–76. https://doi.org/ Ruiz, A., González, J.F., Rodríguez, E., Martín, S., Hernández, Y.I., Almeida, R.,
10.1016/j.livsci.2015.02.011. Molina, J.M., 2006. Influence of climatic and management factors on Eimeria
Hidalgo Argüello, M.R., Cordero del Campillo, M., 1999. Coccidiosis. In: Cordero del infections in goats from semi-arid zones. J. Vet. Med. B 53, 399–402. https://doi.
Campillo, M., Rojo Vázquez, F.A. (Eds.), Parasitología Veterinaria. McGraw-Hill- org/10.1111/j.1439-0450.2006.00985.x.
Interamericana de España, S.A.U., Madrid, Spain, pp. 195–212. Ruiz, A., Foronda, P., González, J.F., Guedes, A., Abreu-Acosta, N., Molina, J.M.,
Keeton, S.T.N., Navarre, C.B., 2018. Coccidiosis in large and small ruminants. Vet. Clin. Valladares, B., 2008. Occurrence and genotype characterization of Giardia duodenalis
North Am. Food Anim. Practic. 34, 201–208. https://doi.org/10.1016/j. in goat kids from the Canary Islands, Spain. Vet. Parasitol. 154, 137–141. https://
cvfa.2017.10.009. doi.org/10.1016/j.vetpar.2008.03.003.
Kume, K., Hajno, L., 2010. Study of growth curve variations for kids 0-6 months old of Ruiz, A., Matos, L., Muñoz, M.C., Hermosilla, C., Molina, J.M., Andrada, M.,
Alpine goat breed in Albania. Arch. Zootech. 13, 54. Rodríguez, F., Pérez, D., López, A., Guedes, A.C., Taubert, A., 2013a. Isolation of an
Lambe, N.R., Navajas, E.A., Simm, G., Bunger, L., 2006. A genetic investigation of Eimeria ninakohlyakimovae field strain (Canary Islands) and analysis of its infection
various growth models to describe growth of lambs of two contrasting breeds. characteristics in goat kids. Res. Vet. Sci. 94, 277–284. https://doi.org/10.1016/j.
J. Anim. Sci. 84, 2642–2654. https://doi.org/10.2527/jas.2006-041. rvsc.2012.08.003.
Levine, N.D., Ivens, V., 1986. The Coccidian Parasites (Protozoa, Apicomplexa) of Ruiz, A., Muñoz, M.C., Molina, J.M., Hermosilla, C., Rodríguez, F., Andrada, M.,
Artiodactyla. University of Illinois Press, Urbana, pp. 120–141. Martín, S., Guedes, A., Pérez, D., Matos, L., López, A.M., Taubert, A., 2013b. Primary
Lu, C.D., Potchoiba, M.J., 1988. Milk feeding and weaning of goat kids—a review. Small infection of goats with Eimeria ninakohlyakimovae does not provide protective
Rumin. Res. 1, 105–112. https://doi.org/10.1016/0921-4488(88)90025-90029. immunity against high challenge infections. Small Rumin. Res. 113, 258–266.
Magistrelli, D., Aufy, A.A., Pinotti, L., Rosi, F., 2013. Analysis of weaning-induced stress https://doi.org/10.1016/j.smallrumres.2013.01.006.
in Saanen goat kids. J. Anim. Physiol. Anim. Nutr. 97, 732–739. https://doi.org/ Ruiz, A., Muñoz, M.C., Molina, J.M., Hermosilla, C., Andrada, M., Lara, P., Bordón, E.,
10.1111/j.1439-0396.2012.01315.x. Pérez, D., López, A.M., Matos, L., Guedes, A.C., Falcón, S., Falcón, Y., Martín, S.,
Matos, L., Muñoz, M.C., Molina, J.M., Rodríguez, F., Pérez, D., López, A.M., Ferrer, O., Taubert, A., 2014. Immunization with Eimeria ninakohlyakimovae-live attenuated
Hermosilla, C., Taubert, A., Ruiz, A., 2017. Protective immune responses during oocysts protect goat kids from clinical coccidiosis. Vet. Parasitol. 199, 8–17. https://
prepatency in goat kids experimentally infected with Eimeria ninakohlyakimovae. Vet. doi.org/10.1016/j.vetpar.2013.09.032.
Parasitol. 242, 1–9. https://doi.org/10.1016/j.vetpar.2017.04.016. Soe, A.K., Pomroy, W.E., 1992. New species of Eimeria (Apicomplexa: Eimeriidae) from
Matos, L., Muñoz, M.C., Molina, J.M., Rodríguez, F., Pérez, D., López, A.M., the domesticated goat Capra hircus in New Zealand. Syst. Parasitol. 23, 195–202.
Hermosilla, C., Taubert, A., Ruiz, A., 2018. Age-related immune response to https://doi.org/10.1007/BF00010872.
experimental infection with Eimeria ninakohlyakimovae in goat kids. Res. Vet. Sci. Taylor, M.A., Catchpole, J., 1994. Review article: coccidiosis of domestic ruminants.
118, 155–163. https://doi.org/10.1016/j.rvsc.2018.02.004. Appl. Parasitol. 35, 73–86.
Medrano-Galarza, C., LeBlanc, S.J., Jones-Bitton, A., DeVries, T.J., Rushen, J., de Thienpont, D., Rochette, F., Van Parijs, O.F.J., 1979. Diagnosing Helminthiasis by
Passillé, A.M., Endres, M.I., Haley, D.B., 2018. Associations between management Coprological Examination. Janssen Research Foundation, Beerse, p. 187.
practices and within-pen prevalence of calf diarrhea and respiratory disease on dairy Tsiplakou, E., Papadomichelakis, G., Sparaggis, D., Sotirakoglou, K., Georgiadou, M.,
farms using automated milk feeders. J. Dairy Sci. 101, 2293–2308. https://doi.org/ Zervas, G., 2016. The effect of maternal or artificial milk, age and sex on three
10.3168/jds.2017-13733. muscles fatty acid profile of Damascus breed goat kids. Livest. Sci. 188, 142–152.
Molina, J.M., Rodríguez-Ponce, E., Ferrer, O., Gutiérrez, A.C., Hernández, S., 1994. https://doi.org/10.1016/j.livsci.2016.04.014.
Biopathological data of goat kids with cryptosporidiosis. Vet. Record. 135, 67–68. Windsor, P.A., Nampanya, S., Putthana, V., Keonam, K., Johnson, K., Bush, R.D.,
Morales-delaNuez, A., Moreno-Indias, I., Sánchez-Macías, D., Capote, J., Juste, M.C., Khounsy, S., 2018. The endoparasitism challenge in developing countries as goat
Castro, N., Hernández-Castellano, L.E., Argüello, A., 2011. Sodium dodecyl sulfate raising develops from smallholder to commercial production systems: A study from
reduces bacterial contamination in goat colostrum without negative effects on Laos. Vet. Parasitol. 251, 95–100. https://doi.org/10.1016/j.vetpar.2017.12.025.
immune passive transfer in goat kids. J. Dairy Sci. 94, 410–415. https://doi.org/ Zhao, G.H., Lei, L.H., Shang, C.C., Gao, M., Zhao, Y.Q., Chen, C.X., Chen, D.K., 2012.
10.3168/jds.2010-3624. High prevalence of Eimeria infection in dairy goats in Shaanxi province,
northwestern China. Trop. Anim. Health Prod. 44, 943–946. https://doi.org/
10.1007/s11250-011-9997-9998.