Trop Anim Health Prod (2014) 46:641–646
DOI 10.1007/s11250-014-0543-3
REGULAR ARTICLES
Health impact evaluation of alternative management systems
in vicuña (Vicugna vicugna mensalis) populations in Peru
Veronica Risco-Castillo & Jane Collins Wheeler & Raúl Rosadio &
Francisco Javier García-Peña & Ignacio Arnaiz-Seco & Domingo Hoces &
Hugo Castillo & Álvaro Veliz & Luis Miguel Ortega-Mora
Accepted: 20 January 2014 / Published online: 5 February 2014
# Springer Science+Business Media Dordrecht 2014
Abstract To determine the impact of farming over vicuña
population in Peru, serum samples were collected from 207
vicuñas (126 captive vicuñas and 81 free-ranging vicuñas) and
614 domestic South American camelids (571 alpacas and 43
llamas), in ten Andean communities at the Salinas y Aguada
Blanca reserve, province of Arequipa, southern Peru. Samples
were tested for the presence of leptospirosis, foot and mouth
disease (FMD), bovine viral diarrhea (BVD), bovine herpes-
virus type 1 (BHV-1), brucellosis, bluetongue disease (BT),
paratuberculosis, and neosporosis. Serological results showed
that 1.9 % (4/207) of vicuñas, 18.6 % (106/571) of alpacas,
and 23.3 % (10/43) of llamas were positive to one or more
Leptospira serovars. One percent of vicuñas (2/207) and
2.4 % of domestic camelids (15/614) had Neospora caninum
antibodies tested by ELISA, but only two vicuñas and two
V. Risco-Castillo (*) : L. M. Ortega-Mora
SALUVET, Animal Health Department, Faculty of Veterinary
Sciences, Complutense University of Madrid, Ciudad Universitaria
s/n, 28040 Madrid, Spain
e-mail: vrisco@gmail.com
J. C. Wheeler
CONOPA—Instituto de Investigación y Desarrollo de Camélidos
Sudamericanos, Lima, Peru
R. Rosadio : D. Hoces : H. Castillo : Á. Veliz
Faculty of Veterinary Medicine, Universidad Nacional Mayor de San
Marcos, Avda. Circunvalación s/n San Borja, Lima, Peru
F. J. García-Peña
Laboratory of Animal Health of Algete, National Reference
Laboratory for Animal Leptospirosis, Madrid, Spain
I. Arnaiz-Seco
Laboratory of Animal Health and Production of Galicia, Lugo, Spain
Present Address:
V. Risco-Castillo
INSERM, UMR-S 945, Paris, France
alpacas were confirmed by Western blot. Epidemiological
evaluation found an association of leptospirosis to sex and
age (p<0.001), with female subjects older than 2.5 years at
higher risk of infection. Interestingly, antibodies against
Leptospira serovars were only found in captive vicuñas. This
is the first study where health status of free-ranging and
captive vicuñas has been compared. Results indicate minimal
to nil presence of FMD, BVD, BHV-1, brucellosis, BT,
paratuberculosis, and neosporosis allied to health disorders
in our sample. The detection of seropositive animals against
Leptospira, however, unveils the likely significance of lepto-
spirosis in wild and domestic South American camelids, the
impact of mixed husbandry over vicuña population and the
risk to human health.
Keywords Free-ranging . Captive . Domestic camelids .
Leptospirosis . Arequipa
Introduction
The wild South American camelids, vicuña (Vicugna vicugna)
and guanaco (Lama guanicoe), and their domestic forms, the
alpaca (Vicugna pacos) and llama (Lama glama), are native
species inhabiting the Andean plateau of South America many
millennia ago (Wheeler 2012). Today, camelids rearing in
Peru and Bolivia provide fiber, meat, and fuel to impoverished
Andean herders, who hold most of these livestock (Wheeler
and Hoces 1997).
Current vicuña distribution is limited to areas of extreme
elevation in the Andes (Wheeler 2012), and for several decades,
vicuña has been in danger due to the economic value of their
fiber (Appendix II of Convention on International Trade in
Endangered Species (CITES)), but protection laws from in-
volved countries in the last 20 years have succeeded on recov-
ering the population (Cox 2003). Several management systems
642
have been established to ease recollection of their fiber and to
avoid a likely negative ecological impact if forcing them to be
reared as domestic animals (Sahley et al. 2007). Nevertheless,
they allow their temporary or permanent captivity, placing
vicuñas in contact to domestic animals and increasing the
likelihood of disease transmission between species
(Lichtenstein et al. 2002; Vilá 2002; Wheeler and Hoces 1997).
International organizations recommend monitoring camelid
health and determination of their susceptibility to diseases affect-
ing domestic livestock (Office International des Epizooties (OIE)
2010). Although research regarding the role of domestic
camelids as reservoirs of diseases is increasing worldwide
(Kapil et al. 2009; Tibary et al. 2006), knowledge of vicuña
health status is still limited. There are few reports of infectious
diseases in wild vicuñas (Marcoppido et al. 2010), and most
results are based on detection in a limited number of individuals
(Celedon et al. 2001; Chavez-Velasquez et al. 2005). In domestic
camelids, the presence of antibodies against bovine viral diarrhea
virus (BVDV), bovine herpesvirus type 1 (BHV-1), bluetongue
virus (BTV), Mycobacterium avium subsp. paratuberculosis,
Brucella spp., and Toxoplasma gondii (Acosta et al. 1972;
Chavez-Velasquez et al. 2005; Puntel et al. 1999; Rivera et al.
1987; Rosadio et al. 1993) has been reported.
It is likely that the low reproductive profiles in alpacas and
llamas may be due to infectious agents such as BVDV
(Rosadio et al. 2003) or parasites such as T. gondii and
Neospora caninum (Chavez-Velasquez et al. 2004; Serrano-
Martinez et al. 2004, 2007). Vulnerability of vicuñas to those
diseases cannot be overruled.
In recent years, there has been an increase in reports of the
role of domestic and wild animals as reservoirs of zoonotic
agents such as Leptospira in developing countries, and hence
their potential as a source of infection in humans (Jimenez-
Coello et al. 2010; Jori et al. 2009). Some authors have
detected exposure to several Leptospira serovars (Hill and
Wyeth 1991; Santos et al. 2009) in llamas and alpacas, and
it has been suggested an association with reproductive prob-
lems as well as a potential zoonotic risk (Marin et al. 2007).
The goal of this study was to determine and compare the
health status of free-ranging and captive vicuñas and to estab-
lish the potential exposure to infectious agents from the neigh-
boring domestic camelids reared in the Salinas and Aguada
Blanca National Reserve. Our results will be a starting point in
the understanding of the effect of mixed husbandry and health
condition in both wild and captive vicuñas.
Materials studied
Area description, animals, and sample collection
We sampled ten Andean communities located at 2,800–6,050 m
above sea level, in 366.94×103 ha Salinas and Aguada Blanca
Trop Anim Health Prod (2014) 46:641–646
National Reserve (Fig. 1), in the province of Arequipa, Peru
(71°13′W, 16°5′S), between October and December of 2005.
Mean temperature ranged from 5 to 15 °C and we recorded no
precipitation (mean 0 mm3). At this season, the local population
practices the traditional chaccu during which both wild and
captive vicuñas are rounded up for shearing. We also sampled
llamas and alpacas located in areas adjacent to vicuñas (Table 1).
We used the software Win Episcope (v. 2.0) to determine the
number of samples to collect, considering a prevalence of at least
5 % for each disease under study, with a confidence interval of
99 %. Additionally, we calculated the sampling size for each
species in each community in relation to the total number of
animals in the region (2004 livestock survey, Ministry of Agri-
culture, Peru).
Trained personnel collected blood samples from either the
jugular or femoral veins and checked the animals for any sign
of disease. Sample tubes were immediately stored on ice and
transported to the laboratory for serum recovery. Ten serum
samples were also collected from alpacas born and raised at a
high-biosecurity farm in Simplon village, south Switzerland,
to be included as negative controls for all diseases tested.
Sample analysis
We performed enzyme-linked immunosorbent assays (ELISA),
following manufacturer’s recommendation for the detection of
BVD, BHV-1, foot and mouth disease (FMD), BTV,
paratuberculosis, brucellosis (Brucella abortus, Brucella ovis,
and Brucella melitensis), and neosporosis (N. caninum; Table 2).
On the other hand, diagnosis of leptospirosis was carried out by
the microscopic agglutination test (MAT) and using 17 serovars
(Leptospira borgpetersenii serovars Australis, Ballum, Bataviae,
Djasiman, Hardjo, Javanica, and Tarassovi; Leptospira
interrogans serovars Autumnalis, Bratislava, Canicola,
Copenhageni, and Pomona; Leptospira kirschneri serovars
Cynopteri and Grippotyphosa; Leptospira noguchi serovars Lou-
isiana and Panama; and Leptospira weilii serovar Sarmin).
Samples positive to brucellosis or neosporosis by ELISA
were confirmed by the rose bengal test or by Western blotting
(Chavez-Velasquez et al. 2004) with small modifications,
respectively. In the case of neosporosis test confirmation,
nitrocellulose membranes containing soluble extract of
N. caninum were incubated for 1 h at 37 °C in agitation with
the serum samples at 1:100 dilution in phosphate-buffered
saline (PBS), washed three times, and incubated for 1 h at
37 °C in agitation with a peroxidase-conjugated sheep anti-
llama antibody at 1:1,000 dilution in PBS. Finally, membranes
were developed with 4-chloro-1-naphthol.
Statistical analysis
We tabulated and analyzed the results statistically with the
SAS system software (v. 7) and the GraphPad Prism software
Trop Anim Health Prod (2014) 46:641–646 643

Fig. 1 Geographic location of

Salinas y Aguada Blanca Natural
Reserve and Andean community
samples

(v. 5), and Fisher’s exact test was applied to determine the
association between a given diagnosed disease and sex (male
or female), age (less than 2 years old, 2–5 years old, or more
than 5 years old), species and management system (free-
ranging vicuña, captive vicuña, or domestic camelids), and
location (Andean community) or geographical region within
the National Park (north, south, east, or west).
Results
The results showed that 1.9 % (4/207) of vicuñas had anti-
bodies against different serovars of Leptospira, while sero-
prevalence in the domestic camelids was of 18.9 % (116/614),
including 106 of 571 alpacas and 10 of 43 llamas. The
serovars detected were Pomona, Autumnalis, Copenhageni,
and Bratislava. The antibody titers ranged between 1:100 and
1:30,000; 93 of alpacas positive to Pomona were also positive
to Autumnalis (n=64), Bratislava (n=8), or Copenhageni (n=
20), 19 alpacas were positive to three serovars, and 4 alpacas
were positive to the four serovars, while 4 llamas were posi-
tive to two serovars (Pomona and Autumnalis). Among vi-
cuñas, two animals were positive to two serovars (Pomona
and Autumnalis or Copenhageni) and one was positive for the
four serovars. Furthermore, an association between seroposi-
tivity and species (p < 0.0001), sex (p = 0.0017), age
(p<0.001), and region of origin (p=0.069) was observed, with
the highest risk of infection found in alpacas, in female

Table 1 Location and distribu-

tion of animals sampled Location at reserve Andean community Free-ranging vicuna Captive vicuna Alpaca Lama

North Chalhuanca 27 62 4
North Chuca-Imata 14 70 1
North Colca Huallata 29 63
North Pillone 20 62 6
South Salinas Huito 2 31
East Carmen Chaclaya 21 5
East Tarucani 22 56 17
West Ampi 22 72 3
West Tambo Cañahuas 45 71
West Tocra 26 63 7

Total 81 126 571 43

644
Table 2 Serologic tests performed, methods used, and cutoff value established for the diseases studied
Disease Technique Kit
BVD Competitive ELISA ELISA BVD/MD/BD
BHV-1 Blocking ELISA HerdChek IBRgB
Paratuberculosis ELISA ID Screen
FMD Competitive ELISA CHEKIT-FMD 3ABC
Leptospirosis MAT NA
BT Competitive ELISA Ingezim BTV Compac
Brucellosis Competitive ELISA Ingezim Brucella compac
Neosporosis Competitive ELISA Chekit Neospora
BVD bovine viral diarrhea, BHV-1 bovine herpesvirus type 1, FMD foot and mouth disease, BT bluetongue disease, ELISA enzyme-linked immuno-
sorbent assay
camelids, and in animals older than 2.5 years from the eastern
area of the National Reserve. Interestingly, all positive vicuñas
came from the western region (Toccra, Ampi) and were kept
in captivity. Regarding N. caninum, 1 % of the vicuñas (2/207)
and 2.4 % of the domestic camelids (15/614) were found to
have antibodies when tested by ELISA. However, only two
vicuñas and two alpacas were confirmed by Western blotting
to have antibodies specific to N. caninum (data not shown).
No association was found with any of the variables analyzed,
and the vicuñas and alpacas came from different Andean
communities (alpacas came from the north region and vicuñas
came from the east and west of the National Park).
Regarding the serodiagnosis of Brucella sp., 2.9 % of
vicuñas (6/207), 10.5 % of alpacas (60/571), and 9.3 % of
llamas (4/43) were seropositive when tested by ELISA. Nev-
ertheless, all samples resulted negative when retested using
the reference rose bengal test. All animals were negative for
the other diseases analyzed (FMD, BVD, BHV-1, BTV, and
paratuberculosis). No clinical signs were observed in animals
sampled during the study.
Discussion
To date, the health status of South American camelids grazed
in shared pastures has been poorly investigated. This is the
first study that analyzes and compares the health status of free-
ranging and captive vicuña with that of domestic camelids
(llamas and alpacas) reared in the same area.
An association of BVD infection with respiratory disease,
abortion, ill thrift, and diarrhea has been described in llamas
and alpacas (Belknap et al. 2000; Carman et al. 2005; Foster
et al. 2007; Mattson et al. 2006), and serological findings
report up to 11 % prevalence in Peruvian alpacas (Rivera
et al. 1987). Most seropositive camelids in Peru have been
found in mixed farms (with other livestock such as sheep and
cattle) than in those where only camelids are bred (Rosadio
et al. 2003).
Trop Anim Health Prod (2014) 46:641–646
Manufacturer Sensibility Cutoff value
Pourquier BVD/MD/BD P80 ≤40 % inhibition
Idexx BHV-1 gB ≥55 % blocking
ID.Vet M. avium paratuberculosis ≥70 % S/P
Bommeli-Intervet Serotypes A, O and C According to the manufacturer
In house 17 serovars 1:100
Ingenasa 24 BTV serotypes ≤50 % inhibition
Ingenasa Multispecies (Brucella spp.) ≤60 % inhibition
Idexx N. caninum According to the manufacturer
The seronegativity in the animal population of this study
agrees, in the case of BTV, with a lack of competent vector
species in this region during the dry season (Lager 2004) and
confirms the importance of veterinary surveillance to avoid
contact and disease transmission to naïve populations from
infected livestock. This is especially true for free-ranging vicuña
since any other control measure is unacceptable in wild species.
Our results confirm for the first time the presence of the
Leptospira serovars Pomona, Autumnalis, Bratislava, and
Copenhageni among the captive vicuña populations in Peru
and the likely circulation of this pathogenic agent between
domestic and wild camelids. Similar seroprevalences have
been found in other regions (Hodgin et al. 1984; Llorente
et al. 2002), and high antibody titers have been associated to
active infection during the rainy season (Santos et al. 2009).
While Pomona and Autumnalis were the most
seroprevalent serovars among the alpaca, llama, and captive
vicuñas, there were no animals seropositive to Hardjo, which
is the more adapted to true ruminants (Gerritsen et al. 1994).
These results coincide with previous studies (Santos et al.
2009; Suárez et al. 2007) and could infer the adaptation of at
least Pomona to South American camelids, as previously
documented for cattle from swine. Precautions must be taken
regarding the risk of cross-reaction between serovars, as seen
in animals with high titers against Pomona and lower titers
against Autumnalis or Bratislava (Kingscote 1986).
Interestingly, Leptospira seroprevalences in both captive
vicuña and domestic camelids from Toccra were unex-
pectedly high, although no association between geographic
location and management system was found. Also,
Copenhageni antibodies were detected in the three species
studied regardless of their location or age. Similar results
have been observed by other authors (Rosadio et al.
2003), and while the source of transmission may come
from contaminated watercourses (Felt et al. 2011; Karesh
et al. 1998), this risk would have been reduced or nonex-
istent during our dry season study, so the detection of
high titers against Pomona and Autumnalis could indicate
Trop Anim Health Prod (2014) 46:641–646
close contact with infected livestock, rodents, or even
guinea pigs (Gressler et al. 2010). The high antibody titers
found in female subjects older than 5 years during the dry
season could also indicate a high risk of venereal trans-
mission for these serovars (Little 1986). Interestingly, we
found higher prevalence in adult female subjects than that
in adult male subjects, in contrast to what has been
observed by other authors (Santos et al. 2009).
While literature reports a rather low seroprevalence
of leptospirosis in cattle from this region (Arias et al.
2011), the role of wildlife as a source of transmission
has been described. Wild rodents such as the northern
viscacha and the colilargo or Andean pygmy mouse
(Lagidium peruanum, Oligoryzomys andinus, Thylamys
sp.) opossums (Didelphis marsupialis), weasels (Mustela
frenata), or hog-nosed skunks (Conepatus chinga) could
be implicated in Leptospira transmission to vicuñas
(Bunnell et al. 2000; Vanasco et al. 2003). Pomona
and Copenhageni have been isolated from renal tissue
of wild mice of the Akodon genus (Zamora and
Riedermann 1999), and the Andean fox (Lycalopex
culpaeus) may also play a role in the epizootiology of
Pomona and Icterohaemorrhagiae, as has been des-
cribed elsewhere for other fox species (Millan et al.
2009). Although we report low seroprevalence rates
for the southern region, our findings highlight the im-
portance of establishing proper sanitary measures to
protect both human and animal population health and
well-being (Cespedes et al. 2006).
Seroprevalence against neosporosis in the vicuñas and
domestic camelids studied was very low. Previous studies
have also detected a moderate to low seroprevalence of
neosporosis in South American camelids (Chavez-Velasquez
et al. 2004; Wolf et al. 2005), and the possible reduced
susceptibility of llamas has been suggested to propitiate their
role as intermediate hosts (More et al. 2008). This possibility
would agree with our results since we found no association
between diagnosis and location of the animals, although the
Neospora-positive vicuñas shared grazing areas with domes-
tic camelids, or a higher risk of horizontal transmission via
dogs or wild carnivores known to inhabit the region and
predate South American camelids.
The results presented here provide insights that could aid
local and governmental authorities, together with Andean
communities, to make informed decisions regarding manage-
ment strategy of wild South American camelids in the future
and to establish and make measures better adapted to
protect their health status. Although the close presence
of domestic camelids and vicuñas might not be a factor
affecting the health status of the latter, it would also be
advisable to carry out broader studies to analyze the
zoonotic risk of leptospirosis and other diseases affect-
ing South American camelids.
645
Acknowledgments We are grateful to the following people who gen-
erously helped us in this study: C. Flores and D. Arias (CONACS), A.
Cornejo and M. Avendaño (INRENA), H. Escarza (ACVIRA), and
Andean communities from Salinas y Aguada Blanca National Reserve
(Toccra, Tarucani, Chuca-Imata, Pillone, Chalhuanca, Ampi, Colca-
Huallata, Tambo Cañahuas, Salinas Huito, and Carmen Chaclaya). We
also thank J.M. Blasco (Center of Agrofood Technology and Research of
Aragon, Spain) for analyzing samples against brucellosis by MAT anal-
ysis and Dr. J. Kuonen (Alpaka-Zucht Simplon) for kindly providing
samples with negative control alpaca serum. This study was financed by a
grant for cooperation for the development from the University
Complutense of Madrid (projects for cooperation to development—
Complutense University of Madrid, ref. 14/05: health impact evaluation
of new management systems on vicuña population of Peru).
Conflict of interest All authors have given informed consent prior to their
inclusion in the study and certify that there is no conflict of interest with any
financial organization regarding the material discussed in the manuscript.
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