Veterinary Parasitology 198 (2013) 244–249

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Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar

Short communication

Effect on performance of weanling alpacas following

treatments against gastro-intestinal parasites
Susan M. Thomas a,b,∗ , Eric R. Morgan a
a
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, United Kingdom
b
Pathology & Pathogen Biology (PPB) Hawkshead, The Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield,
Hertfordshire AL9 7TA, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: Nematodes and coccidia are common parasites of alpacas (Vicugna pacos), and important
Received 8 July 2013 causes of disease in this increasingly popular livestock species. Endoparasitic infestation is
Accepted 12 August 2013
thought to increase at times of natural or imposed stress, and antiparasitic treatments are
often administered, although to date there is little evidence regarding their effect. Thirty-
Keywords:
one alpaca juvenilles (cria) were divided into four groups at weaning, and received either
Alpaca
no treatment as a control (C), fenbendazole anthelmintic (FB), toltrazuril coccidiostat (T), or
Coccidiosis
Nematode both treatments (FBT). Body weights and faecal egg/oocyst counts were recorded weekly
Parasite for six weeks following treatment. Although the prophylactic treatments decreased fae-
Toltrazuril cal egg/oocyst counts of the target organisms in the short term, there was no significant
Fenbendazole difference in egg/oocyst output over the course of the trial from animals given wormer, coc-
cidiostat or both treatments. The group receiving anthelmintic only showed a significant
reduction in live weight gain (LWG), with no significant difference in LWG between the
other groups. At the conclusion of the trial, ‘wormed only’ alpacas weighed 3.3% less than
at weaning, losing an average 1.3 kg over six weeks, whereas average LWG in the control
group was 2.5 kg. Antiparasitics transiently reduced egg/oocyst output but results suggest
that further investigation is required on the action of anthelmintics administered to alpaca
cria at weaning and their effect on animal health and welfare.
© 2013 Elsevier B.V. All rights reserved.

1. Introduction (Wheeler, 1995), parasitic disease is cited as the main herd

Alpacas, members of the South American Camelid fam-
ily (SAC’s) are an increasingly popular livestock species
outside their home range, with >35,000 alpacas farmed
in the UK (British Alpaca Society (BAS) 2012, personal
communication). Published research on alpacas reared in
Europe is scarce, prompting the need for more evidence
based information for husbandry and parasite control.
In Peru, where there are more than 4 million alpacas
∗ Corresponding author at: Pathology & Pathogen Biology (PPB) Hawk-
shead, The Royal Veterinary College, Hawkshead Lane, North Mymms,
Hatfield, Hertfordshire AL9 7TA, United Kingdom. Tel.: +44 7887 511774.
E-mail address: smthomas@rvc.ac.uk (S.M. Thomas).
health problem (Palacios et al., 2006). Nematode infesta-
tions are common and are reported to have the largest
impact, particularly on alpacas aged less than one year
(Leguia, 1991). Ballweber (2009) reports that parasitism
is a major health concern in SAC’s, throughout the world,
with clinical disease causing severe economic losses. A
postal survey of camelid owners in the UK reported that
93% of owners treated their alpacas or llamas for nema-
todes, and 20% treated for coccidia (Tait et al., 2002).
Research in Germany identified that cria demonstrated
higher strongyle egg counts (average 450 eggs per gram,
epg) than adults (150 epg), and eggs of Nematodirus bat-
tus and other Nematodirus spp., Strongyloides, Trichuris,
Capillaria and Moniezia were repeatedly recovered dur-
ing a year of sampling (Rohbeck et al., 2006). A study

0304-4017/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.vetpar.2013.08.010
 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249
including faecal analysis in the UK, identified a range of
endoparasites including Ostertagia, Haemonchus, Cooperia,
Trichostrongylus sp, Nematodirus, Capillaria and Trichuris
(Tait et al., 2002). A similar range of gastrointestinal nema-
tode eggs was identified in a study in the USA (Bishop
and Rickard, 1987). The highest numbers of nematode
eggs were found in cria, possibly due to the more limited
opportunity of juveniles to develop immunity. While many
species of gastro-intestinal parasites are shared between
SAC and ruminants, the nematodes Camelostrongylus men-
tulatus and Trichuris tenuis are unique to camelids (Fowler,
1997). These species were reported in the UK following
post mortem recovery from alpaca and llama cria, respec-
tively (Welchman et al., 2008). Nematode infections reduce
alpaca productivity both in terms of fleece production and
weight gains. Infection with protozoal Eimeria species is
reported to be the main cause of mortality in young alpaca
in Peru (Palacios et al., 2006). There are six recognised coc-
cidia species specific to SAC, Eimeria alpacae, E. lamae, E.
macusaniensis, E. punoensis, E. peruviana and E. ivitaensis
(Soulsby, 1982; Leguia and Casas, 1998; Fowler and Miller,
2008). Analysis of coccidiosis presenting at post mortem in
54 UK alpaca from 1999 to 2004 concluded that coccidial
infection, particularly associated with E. macusaniensis and
E. punoensis cause disease in British alpaca over a wide age
range (Schock et al., 2007).
Signs of parasitism vary. Cria are particularly vulnerable,
possibly due to immature immune development and also
due to the reduced nourishment available from a lactating
dam if she is also parasitised (Fowler, 1998). Windsor et al.
(1992) found that parasite infection reduced weight gain
in growing alpacas, and, importantly from the commer-
cial perspective, treated male alpacas produced a greater
fleece yield. Key events (birthing, lactation and weaning)
when increased stress is linked to depressed immune sta-
tus may lead to rises in egg and oocyst counts; treatments
with anthelmintics and coccidiostats are often initiated.
Cria are weaned at approximately six months of age, having
reached 25 kg in weight. As the majority of UK cria births
are timed for summer, weaning is typically performed in
winter. Cria are removed from the dam and the protec-
tion of the herd onto relatively poor quality winter grass
at a time when the weather becomes cooler and wetter.
This can impose physiological and nutritional stress, which
may be exacerbated by parasite infection, so the benefit of
antiparasitic treatment at this time is plausible. However,
evidence for such a benefit has not been published.
The aim of this study was to examine the effects
of administering the antiparasitic drugs fenbendazole
(anthelmintic) and/or toltrazuril (coccidiostat) to cria at
weaning to assess the level of egg/oocyst shedding and the
effect on weaning performance measured by live weight
gain (LWG).
2. Materials and methods
The study was carried out over a seven week period
beginning in January 2011 on a closed alpaca farm (120
alpacas) in south-west England. A factorial, randomised
controlled trial was designed using a group of 31 sum-
mer born alpaca cria. The group satisfied weaning criteria
245
having attained an age of at least five months and a
minimum weight of 25 kg. A random number genera-
tor allocated a number to each cria which was used to
assign individuals to one of four test groups (C- control,
FB- fenbendazole anthelmintic, T- totrazuril coccidiostat
and FBT-both fenbendazole and toltrazuril). The weanling
alpacas were moved onto 5 acres of pasture where they
were co-grazed. To minimise contamination from previ-
ously shed parasite eggs the pasture had been cleared of
faecal deposits 16 months prior to the trial and had been
managed by taking a cut of hay during the summer. They
weanlings were given access to three automatically fill-
ing drinking butts of fresh water which were raised from
the ground to minimise contamination from mammalian
wildlife. Three mangers of hay were available for ad libi-
tum feeding. Commercial camelid hard feed was presented
daily in 6 m × 3 m lengths of raised guttering, as was the
practice prior to weaning, providing each cria ample space
to approach the trough with minimal competition for feed.
Faecal testing of cria prior to weaning identified the
main helminth eggs as Nematodirus battus, strongyles
(H.contortus, and Trichostrongylus spp) and Trichuris spp.
(mean total nematode egg counts of 52 epg, range 0–200).
Coccidia species identified were E. alpacae, Eimeria macu-
saniensis and Eimeria ivitaensis (mean counts 47 opg, range
0–400) Cria were weighed at the start of the trial for dosage
calculations. No antiparasitic drugs are licensed in the UK
for alpacas, so treatments were selected on the basis of
the main parasite ova present. Drugs and doses adminis-
tered were those in common current use in the camelid
industry. Recommended doses range between 2 and 4
times sheep dose for both FB anthelmintic and coccidio-
stats (Whitehead and Anderson, 2006; Whitehead, 2009).
A recent study focussing on another SAC, the llama (Lama
glama) demonstrated that dose rates of 7.5 mg/kg BW were
required to reduce egg shedding of gastrointestinal nema-
todes in contrast to a dose rate of 2.5 mg/kg to achieve
similar results in sheep (Dadak et al., 2013). It was hypo-
thesised that the three fold increase was required due to
pharmokinetic differences between species.
According to group, alpacas were given either no treat-
ment (group C, n = 8) or the allocated group treatments
of fenbendazole (15 mg per kg body weight as a single
oral dose of 1.5 ml per 10 kg body weight of Panacur 10%
suspension, MSD Animal Health, UK, i.e. triple the recom-
mended sheep dose; group FB, n = 8), toltrazuril (15 mg per
kg body weight as a single oral dose of Baycox 50 mg/ml
oral suspension, Bayer plc, corresponding to 3 ml/10 kg;
group T, n = 8) or fenbendazole followed immediately by
toltrazuril (group FBT n = 7). Drenches were administered
over the back of the tongue in the normal milk feeding
position and a swallowing reflex encouraged to avoid the
drench spit back. Each alpaca was handled in the same way,
whether they received an oral drench or no medication, to
ensure that all alpacas were exposed to the same degree of
handling and stress.
At the start of the trial (week zero), and weekly there-
after, cria were individually assessed for body condition,
weighed and observed for clinical signs of illness. Faecal
egg counts were conducted using the modified McMaster
test at a detection limit of, 50 eggs or oocysts per gram of
246 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249

Fig. 1. Faecal nematode egg counts recovered from 4 treatment groups, treated with anthelmintic (0 = untreated, 1 = treated) and coccidiostat (0 = untreated,
1 = treated) monitored from weaning week 0 to week 6. N = 8 in groups C, FB, and T, n = 7 in group FBT. Each box represents 50% of the cases with the whiskers
extending to the largest and smallest values. Horizontal lines within the box represent median values. Extreme points are represented by asterisks.

faeces (epg, opg), (Zajac and Conboy, 2006) and Sheather’s
sugar flotation solution (specific gravity 1.27). Sheather’s
was selected as flotation medium as it will float both nema-
tode eggs and the relatively large Eimeria oocysts of Eimeria
macusaniensis and E. ivitaensis.
The effect of treatment on epg and opg was evaluated.
The principal indicator of weaning performance through-
out the trial was live weight gain (LWG). To remove
the effect of variation in cria weaning weights, initial
weights were indexed to 1. As weight data were normally
distributed, they were analysed using a mixed between-
within subjects repeated measures ANOVA to determine
the effects of anthelmintic or coccidiostat treatment on
LWG, exploring any interaction effects. Statistical analy-
ses were performed using PASW v18.0 (SPSS Inc., USA)
with alpha = 0.05, except when repeated univariate com-
parisons were made, in which case Bonferroni adjustment
was applied.
3. Results
Groups FB and T showed significant reductions in
total egg/oocyst counts for the first 3 weeks of the trial
Figs. 1 and 2 and both treatments were well tolerated by
the cria.
Faecal egg and oocyst counts in treated groups returned
to untreated levels by weeks 4 and 5 such that there was no
significant difference over the entire trial period in either
epg (Kruskal–Wallis 2 (3 d.f., n = 31) = 6.59, p = 0.086) or
opg (2 (3 d.f., n = 31) = 6.85, p = 0.077). Positive weight
gains were recorded in groups C, T and FBT (Fig. 3). Group
FB, demonstrated the lowest LWG compared with other
groups (F3,27 = 5.88 p = 0.022). Neither groups T or FBT had
a statistically significant effect on LWG relative to the con-
trol group (p = 0.55 and p = 0.48 respectively). Mean LWG
over the six week trial in C was 2.5 kg, T was 1.7 kg and in
FBT was 0.7 kg, Alpacas in group FB, lost on average 1.3 kg.
4. Discussion
Anthelmintic and coccidial treatment had the expected
effect of reducing numbers of nematode eggs and coccidial
oocysts shed onto the pasture following weaning. However
the effects of treatment were transient with numbers of
ova shed returning to pre-treatment levels by week 4 and
5 of the trial. Re-infection from the pasture was unlikely
as the trial pasture had been managed and ungrazed for
>1 year prior to the trial. Survival of L3 on pasture varies
both between species and with environmental conditions,
but it is unlikely that larvae would have survived in high
numbers both a hot dry summer and adverse freezing win-
ter conditions (Kates, 1950). Given the speed of return to
pre-treatment egg counts (4–5 weeks post treatment) it is
plausible that eggs were shed by recently emerged arrested
larvae (L4) rather than re-infection from previously cleaned
and rested pasture. However, given the limited infor-
mation available on antiparasitic drug efficacy against
the various parasites found in alpacas, and the limited
 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249 247

Fig. 2. Faecal oocyst counts recovered from 4 treatment groups, treated with anthelmintic (0 = untreated, 1 = treated) and coccidiostat (0 = untreated,
1 = treated) monitored from weaning week 0 to week 6. N = 8 in groups C, FB, and T, n = 7 in group FBT. Each box represents 50% of the cases with the
whiskers extending to the largest and smallest values. Horizontal lines within the box represent median values. Extreme points are represented by
asterisks.

opportunities for specific identification of eggs and oocysts
shed in the present study, it is also possible that post-
treatment increases in epg and opg represent emergence
of species that were less affected by treatment or oth-
erwise held a competitive advantage. Whilst combined
oocyst counts in the two groups given coccidiostat were
lower than the untreated groups, numbers of oocysts shed
returned to untreated levels by week 5 following wean-
ing (although there was a temporary increase in week 3,
group T). Studies have shown continued suppression of
accurate dose based on weight. 75% of alpaca herds in the
UK comprise <20 alpacas (BAS data, 2012). Such small hold-
ings rarely own farm scales adequate to weigh an alpaca
(2012 on-line survey, unpublished data). Animal weights
are often estimated visually, which is prone to error with an
alpaca in full fleece. This could lead to sub-optimal dosing
promoting development of anthelmintic resistance.
1.10
Group mean weight Index - Weaning weight = 1.00

oocyst levels for several weeks following treatment with 1.08

toltrazuril, which destroys all intracellular stages of the
1.06
Eimerian life cycle (Mundt et al., 2007).
With no licenced antiparasitic drugs for SAC’s there 1.04
is doubt regarding optimal dose rates for treatments, 1.02
which rely on the application of approaches developed for
1.00
distantly related species, usually with no validation. Ris-
ing levels of anthelmintic resistance in ruminants must 0.98
raise concerns for alpaca herds. Anthelmintic resistance in 0.96
alpacas to macrocyclic lactone (ML) anthelmintics has been
0.94
demonstrated on an alpaca farm in Belgium (Sarre et al.,
2012) in spite of a rotational worming strategy between 0.92
ML and benzimidazole (BZ) treatments. Gillespie et al. 0.90
(2010) identified resistance to BZ (fenbendazole) and ML 0 1 2 3 4 5 6
(ivermectin and moxidectin) on alpaca and llama farms Weaning Week
in Georgia, USA. Alpacas in the UK are routinely treated C FB T FBT
against nematodes, and this can vary from twice each year
Fig. 3. % weight change (±SE) as a summary measure of 4 treatment
to six times a year (2012 on-line survey, unpublished data).
groups over 6 week trial period. Initial weights were indexed at 1 to
Reported treatment dosages vary from sheep dose rates to normalise start point weaning weights and percentage changes were cal-
up to 4x sheep dose rates. Effective treatment relies on an culated weekly.
248 S.M. Thomas, E.R. Morgan / Veterinary Parasitology 198 (2013) 244–249
LWG was affected by treatment but not in the direc-
tion anticipated. The group treated with anthelmintic alone
(FB) lost weight over the trial period while all other groups
demonstrated weight gain. This suggests that removal of
worms created an adverse environment in the gut which
had the effect of either reducing appetite or reducing effi-
ciency of nutrient absorption, utilisation, or both. The effect
appeared to be attenuated in FBT, where LWG was positive
over six weeks but at lower levels than groups C and T. Fur-
ther research is required as this unexpected outcome has
not been explained.
An alternative explanation of the weight loss is toxic-
ity of the anthelmintic. Fenbendazole has a wide safety
margin with no toxic effects in other small ruminants so
this appears unlikely. Stimulated emergence of arrested
larvae, with associated tissue damage could be consid-
ered as demonstrated in horses with cyathostomin larvae
(Matthews et al., 2004). Inflammatory effects and mucosal
damage provoked by emergence of L4 and coccidial infec-
tion concurrent with BZ worming treatment may present
a damaged mucosal surface open to secondary bacte-
rial infection. Hermans and Morgan (2003) demonstrated
that intestinal damage caused by clostridial infection in
chickens predisposed the birds to Clostridium perfrin-
gens infection followed by toxin production and necrotic
enteritis. The connection between enteritis and clostridial
infection has been described in camels (Kinne and Wernery,
1998) but requires further study in SAC’s.
It is well known that endo-parasite infestations are
rarely single species but are typically multi species occupy-
ing specific sites along the gastrointestinal tract. Removal
of nematodes from the intestinal ecology may have stimu-
lated inter/intraspecific interactions leading to the negative
effect on weight gain. Recent research has highlighted a
strong, temporary increase in Eimeria populations follow-
ing deworming in mice (Knowles et al., 2013; Pedersen and
Antonovics, 2013) however there was no clear evidence
in the present study for an increase in oocyst excretion
following treatment for nematodes.
A state of uncertainty exists amongst alpaca keepers,
endeavouring to keep internal parasite levels low, treat-
ing with unlicensed drugs, at untested dose rates, often
on alpacas of unknown weight. It is vital to make strate-
gic worming decisions in the light of the best information
from individual farms, considering stocking density and
quarantine arrangements for visiting studs, agisted alpacas
(temporarily housed on another farm) and newly pur-
chased animals. SAC’s generally defaecate in well-defined
latrines from which they do not graze. Over time these
areas enlarge, effectively reducing ‘clean’ grazing area. Reg-
ular faecal sampling with quantitative egg and oocysts
counts provide evidence of direction of change in para-
site status and should be part of a whole herd strategic
plan which incorporates individual farm knowledge of
feeding regimes, infection pressure from other species,
quarantine procedures and stresses placed on alpacas, such
as birth, lactation, weaning, travelling for shows and off
farm mating’s. Evidenced based decisions from regular
faecal sampling are preferable to blanket treatment for
infestations which may not be present, or if present may
be contributing to the build-up of natural immunity and
inflicting no harm. The current research was undertaken on
a single holding with relatively small numbers of animals,
although the unexpected outcome suggests more research
is warranted.
Acknowledgements
The authors thank Sheelagh Lloyd and Richard Wall for
valuable comments on an earlier draft.
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