Accepted by A. Wright: 20 Dec. 2007; published: 13 Feb. 2008
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ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN
1175-5334
(online edition)
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Ciliate protozoa of the forestomach of llamas (Lama glama) and alpacas
(Vicugna pacos) from the Bolivian Altiplano
IGNACIO DEL VALLE
1
, GABRIEL DE LA FUENTE
2
& MANUEL FONDEVILA
2,3
1
Departamento de Bioquímica y Biología Molecular, Universidad de Zaragoza, Miguel Servet 177, 50013 Zaragoza, Spain
2
Departamento de Producción Animal y Ciencia de los Alimentos, Universidad de Zaragoza, Miguel Servet 177, 50013 Zaragoza,
Spain
3
Corresponding author. E-mail: mfonde@unizar.es
Abstract
Protozoal diversity in the forestomach of South American camelids (SAC) was studied in eight llamas and six alpacas
from the Parque Natural Condoriri (3900 to 4100 m altitude, Departamento La Paz, Bolivia). Total protozoal concentra-
tions were 3.6 times higher (P < 0.001) in the stomach contents of alpacas (39.6 x 10
4
ml
-1
and 143.8 x 10
4
ml
-1
in llamas
and alpacas, respectively). Four to 11 species, all from the genus Entodinium, were observed in llamas, whereas from
eight to nine species of Entodinium and minor proportions of Diplodinium (D. anisacanthum, D. dogieli, D. rangiferi),
Eudiplodinium (E. bovis, E. maggii, E. neglectum) and Epidinium (E. ecaudatum) were observed in alpacas. The pres-
ence of Epidinium species in the alpaca is a new host record. The vestibuliferids, Dasytricha and Isotricha were absent
from the forestomach of SAC, as well as other species such as Caloscolex genus, Diplodinium cameli and Entodinium
ovumrajae, commonly found in Old World camelids.
Key words: forestomach protozoa, South American camelids
Introduction
Llamas (Lama glama) and alpacas (Vicugna pacos; Kadwell et al. 2001) are two domesticated species of
South American camelids (SAC) from the Andean Altiplano (3500 to 4500 m altitude). They have been tradi-
tionally used for labour, meat, leather and wool, accounting for up to 75% of cash income in more than half of
the Bolivian households in this area (Tichit and Genin 1997). Alpacas (50 to 70 kg live weight) are highly
adaptable grazers that preferably feed a wide range of herbage species from humid areas, whereas llamas (110
to 140 kg) are prone to consume tall and coarse bunchgrasses from the drier areas (San Martín and Bryant
1989; Tichit and Genin 1997; Castellaro et al. 2004).
Several papers have studied the digestive tract of SAC in terms of anatomy (Vallenas et al. 1971; Engel-
hart et al. 1988) and digestion processes (Sponheimer et al. 2003; Davies et al. 2007), but information about
their rumen microbial population is scarce. In their reviews, Dehority (1986) and Jouany (2000) indicated that
rumen protozoal counts of dromedaries and SAC were similar to those of ruminants. They also reported that
the protozoal population in camelids is only type B (Eadie 1962), and the family Isotrichidae was always
absent from these animals. However, neither of them presented data supporting this conclusion. A classical
reference of protozoal biodiversity of SAC is the description by Lubinsky (1964) of a guanaco (a wild SAC)
from the Winnipeg Zoo. However, these data should probably be viewed with caution since there was only
one animal and the possible cross-inoculation from individuals of another species in the zoo (Kubikova 1935).
SAC differ from dromedaries and bactrian camels in their protozoal population, because they apparently do
Zootaxa 1703 © 2008 Magnolia Press
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63
FORESTOMACH PROTOZOA OF LLAMAS AND ALPACAS
not harbour Caloscolex spp., Diplodinium cameli or Entodinium ovumrajae (Lubinsky 1964; Dehority 1986).
Further, it is unknown if the different sizes and feeding habits between llamas and alpacas would lead to dif-
ferences in their rumen protozoal population.
This paper describes the concentration and diversity of rumen protozoal populations of eight llamas and
six alpacas from the Altiplano in Bolivia.
Material and methods
Stomach contents were obtained from eight adult (about 5 years of age) male llamas, numbered 1 to 8 and six
adult (about 3 years of age) male alpacas, numbered 1 to 6, slaughtered in a commercial abattoir (Palcoco, La
Paz) in November, 2005. The animals were grazing native pasture as the only feed in the region of the Parque
Natural Condoriri (3900 to 4100 m altitude, Departamento La Paz, Bolivia). All animals were fasted for 12-15
h before being slaughtered, and sampling took place within 1 h of slaughter. The first compartment of the
stomach (C1) was eviscerated, and the contents were filtered through a double layer of gauze and 5 ml of the
filtrate was mixed 1:1 with 18 % formaldehyde for preservation (Dehority 1984).
Total and generic ciliate concentrations were determined by previously described procedures (Dehority
1984), using a Sedgewick-Rafter counting chamber. Species distribution and cellular morphology were deter-
mined on temporary preparations using methylene-blue as a nuclear stain and Lugol’s iodine as a stain for
skeletal plates (Dehority 1974). Species identification was mainly based on descriptions of Dogiel (1927),
Kofoid and MacLennan (1930, 1932), Wertheim (1935), Sláde
ček (1946), Lubinsky (1957), Dehority (1974)
and Göçmen (1999).
Data for total protozoal concentration were statistically analysed by one-way ANOVA using the Statistix
8 package (Analytical Software 2003), and differences among host species were compared by the least signif-
icant difference at a P < 0.05.
Results
Total concentration and generic distribution of ciliate protozoa in fluid contents from the first compartment of
the stomach in llamas and alpacas are shown in Table 1. Total protozoal concentrations were 3.6 times higher
(P<0.001) in the stomach contents of alpacas. No overlap in the range of concentrations was found when only
numbers of Entodinium protozoa were only considered for comparison between hosts. Concentrations were
significantly higher in alpacas (mean values of 123.4 vs. 39.6 cells x 10
4
ml
-1
; r.s.d. = 28.11).
Only Entodinium spp. were observed in llamas, whereas protozoa from the Subfamily Diplodiniinae (gen-
era Diplodinium and Eudiplodinium) and the Subfamily Ophryoscolecinae (genus Epidinium) were observed
in alpacas. However, they occurred in very low concentrations and were absent in some of the animals (Table
1).
Species occurrence and distribution of Entodinium spp. in llamas are shown in Table 2. There were 4-11
species of Entodinium present. Among them, the most common were E. dubardi (in all host llamas), E. longi-
nucleatum and E. nanellum in 7 out of eight llamas, and E. damae and E. exiguum in 6 out of eight. In con-
trast, E. rectangulatum, E. alces and E. bovis were only observed in 1 or 2 out of eight animals. Percentages of
cells from these species ranged widely within individual hosts, but E. longinucleatum, E. nanellum and E.
dubardi generally predominated.
Species distribution in alpacas is shown in Table 3, with the number of species observed ranging from 11
to 16, of which 8 to 9 were Entodinium spp. The most common Entodinium spp. were E. dubardi, E. exiguum,
E. nanellum and E. caudatum, that appeared in all animals, together with E. damae, E. longinucleatum, E.
VALLE ET AL.
64
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Zootaxa 1703 © 2008
Magnolia Press
parvum and E. simplex, that were observed in the rumen contents of 5 out of six alpacas. In this host species,
E. caudatum and E. nanellum were present in the highest percentages. Protozoa from two genera of the Sub-
family Diplodiniinae were detected in alpacas, although Diplodinium spp. were absent in two animals and
Eudiplodinium was absent in another one. Among species, none of them showed a clear prevalence in host
alpacas. The genus Epidinium was present in similar proportions in 5 out of six animals, with Ep. ecaudatum
predominant.
TABLE 1. Total concentration and generic distribution of protozoa in the stomach contents of llamas (Lama glama; n =
8) and alpacas (Vicugna pacos; n = 6) from the Bolivian Altiplano. The range is given in brackets.
r.s.d.: residual standard deviation
For mean concentration, different letters show significant differences (p < 0.05)
N.O.: not observed
1
not present in alpacas # 3 and 6
2
not present in alpaca #4
3
not present in alpaca #2
TABLE 2. Percentage distribution of Entodinium species in the rumen contents of llamas (Lama glama) .
Discussion
According to our results, protozoal concentration in alpacas would fit into the expectable range for ruminants
(Dehority 1986; Williams and Coleman 1992). Dehority (1986), studying one Peruvian alpaca, reported an
Llamas
Alpacas
r.s.d.
Mean concentration (cells x 10
4
ml
-1
)
39.64
a
(9.12–104.64)
143.79
b
(119.20–179.36)
29.326
Entodinium (%)
100
85.94 (78.93–93.83)
-
Diplodinium (%)
N.O.
3.43 (0.58–6.15)
1
-
Eudiplodinium (%)
N.O.
2.55 (1.67–8.12)
2
-
Epidinium (%)
N.O.
10.53 (3.62–14.92)
3
-
Llama no.
Species
1
2
3
4
5
6
7
8
Entodinium
alces (Dehority)
9.6
0.7
bovis (Wertheim)
1.6
4.5
caudatum (Stein) f. dubardi (Lubinsky)
5.8
4.0
63.2
damae (Sláde
ček)
3.0
10.6
19.1
0.6
2.0
3.0
dilobum (Dogiel)
0.6
0.4
1.5
dubardi (Buisson)
7.0
9.9
12.6
0.2
22.8
17.5
3.8
19.2
exiguum (Dogiel)
14.7
8.1
4.5
3.2
5.9
10.7
longinucleatum (Dogiel)
16.5
3.9
49.6
74.0
8.1
38.2
47.9
nanellum (Dogiel)
28.7
53.1
12.9
20.7
26.9
35.6
42.6
ovibos (Dehority )
10.4
3.4
26.6
parvum (Buisson)
1.4
8.3
2.8
rectangulatum (Kofoid & MacLennan)
4.2
simplex (Dogiel)
4.0
2.0
1.1
6.9
Total no. of species observed
11
10
5
5
9
5
6
4
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65
FORESTOMACH PROTOZOA OF LLAMAS AND ALPACAS
average concentration of 34.5 x 10
4
cells ml
-1
, whereas Baker and Day (1993) reported 6 to 16 x 10
4
cells ml
-1
of stomach content in three alpacas given ground or chopped hay. In New Zealand, Pinares-Patiño et al.
(2003), from a larger group of animals (n = 6), observed a total protozoal concentration in alpacas ranging
from 20.8 to 47.0 x 10
4
cells ml
-1
, depending on the given forage. However, total numbers in llamas were
lower than in alpacas and below the expected figures for ruminants. Further, even when only Entodinium pro-
tozoa were considered, alpacas still showed a significantly higher concentration. Since there were no apparent
differences between llamas and alpacas in digestibility or fermentative abilities (Sponheimer et al. 2003;
Davies et al. 2007), these differences between SAC might be explained by the trend for llamas to ingest low
quality forages, while alpacas have more selective feeding behaviour, even grazing in the same location
(Tichit and Genin 1997; Castellaro et al. 2004).
TABLE 3. Percentage distribution of protozoal species in the rumen contents of alpacas (Vicugna pacos).
In agreement with previous studies (Lubinsky 1964; Baker and Day 1993; Pinares-Patiño et al. 2003), no
vestibuliferids (Order Vestibuliferida, Isotricha and Dasytricha) protozoa were observed in any animal, as it
was also cited by Dehority (1986), Navarre et al. (1999) and Jouany (2000). Compared with other host species
of the family Camelidae (dromedaries and bactrian camels), the absence of Caloscolex spp., Buetschlia spp.,
and Diplodinium cameli (Dehority 1986; Kubesy and Dehority 2002) has also been observed. Besides, SAC
Alpaca no.
Species
1
2
3
4
5
6
Entodinium
alces (Dehority)
bovis (Wertheim)
caudatum (Stein)
f. dubardi (Lubinsky)
costatum (MacLennan)
damae (Sláde
ček)
dilobum(Dogiel)
dubardi (Buisson)
exiguum (Dogiel)
longinucleatum (Dogiel)
nanellum (Dogiel)
ovibos (Dehority)
parvum (Buisson)
simplex (Dogiel)
41.8
1.6
1.9
5.3
5.7
18.9
1.0
2.8
1.3
2.0
16.9
1.1
13.8
11.8
15.1
25.1
4.3
32.6
4.5
1.8
4.6
4.5
12.9
23.1
2.2
22.8
1.7
11.2
5.2
2.8
27.6
4.1
3.6
19.2
2.7
4.9
22.8
11.6
18.0
5.4
1.7
29.4
1.8
8.0
4.5
7.5
27.4
4.6
8.9
1.8
Diplodinium
anisacanthum (da Cunha)
f. anacanthum (Dogiel)
f. triacanthum (Dogiel)
dogieli (Kofoid & MacLennan)
rangiferi (Dogiel)
2.1
0.02
1.8
3.1
1.6
0.01
2.3
2.3
0.6
Eudiplodinium
bovis (Dogiel)
maggii (Fiorentini)
neglectum (Dogiel)
1.7
0.02
4.5
3.6
2.1
5.9
2.3
1.7
2.6
Epidinium ecaudatum
f. caudatum (Fiorentini)
f. ecaudatum (Fiorentini)
0.02
10.3
0.01
5.8
1.0
13.9
11.4
3.6
Total no. of species observed
14
12
11
12
11
11
VALLE ET AL.
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Magnolia Press
showed a much lower protozoal diversity (up to 11 protozoal species in llamas and 16 species in alpacas) than
the dromedary (31 species) (Kubesi and Dehority 2002).
TABLE 4. Average dimensions from cells (n = 20) of the protozoal species Eudiplodinium maggii and Epidinium ecau-
datum of the alpacas compared with the ranges reported by other authors. Values in brackets indicate the range of size.
To our knowledge, only Lubinsky (1964) and Baker and Day (1993) gave references of rumen protozoal
diversity in SAC. In a sample from a single guanaco from a Zoo in Winipeg (Canada), Lubinsky (1964)
observed 96% Entodinium spp., 1% Eudiplodinium maggii, and 3% Elytroplastron bubali. Baker and Day
(1993) reported that from 1.6 to 24.2% Diplodinium (Diplodinium and Eodinium, according to authors) spp.
were also observed in alpacas, as well as a minor proportion of Eudiplodinium (Eremoplastron) spp. in one
out of three animals. In a single alpaca, Dehority (unpublished results) observed a fauna of 91.8% Entodinium
and 8.2% Diplodinium anisacanthum group and Eudiplodinium maggii. In our case, the proportion of proto-
zoal species of Diplodinium and Eudiplodinium spp. in alpacas averaged 6.6% (from 2.3 to 11.6%), without
any apparently prevailing genera or species among host animals. In contrast to results from Baker and Day
(1993), we observed the important presence of Epidinium, ranging from 3.6 to 14.9 % (mean 9.2%) in 5 out of
6 rumen samples from alpacas. This represents a new host record.
It was also observed that cell sizes of the two larger protozoal species found in our alpacas (Eudiplodin-
ium maggii and Epidinium ecaudatum) were in the lower range reported in their classifications by Ogimoto
and Imai (1981), Williams and Coleman (1992) and Dehority (1993) for describing these species. Sizes of
these two species are compared to references in Table 4. The reason for this lower size is unknown, although
some differences in the rumen environment such as those recorded by Lemosquet et al. (1996) between llamas
and sheep (higher osmotic pressure, 2 º C lower rumen temperatures) might be involved.
Rumen contents of both llamas and alpacas showed the presence of the most ubiquitous Entodinium spp.,
such as E. longinucleatum, E. dubardi and E. exiguum, together with E. damae. However, the presence of E.
caudatum, E. parvum and E. simplex, which were commonly observed in alpacas, were randomly found in lla-
mas (in 3 and 4 out of eight hosts). Others, such as E. dilobum, E. alces, E. bovis and E. ovibos occurred in a
low number of individuals from each host species, whereas E. costatum was observed in two alpacas but not
in llamas and E. rectangulatum was only observed in one llama. Considering that the llamas and alpacas came
from the same geographical site and in some cases even from the same herd, thus allowing for a possible
cross-inoculation, these differences in protozoal biodiversity, either in Entodinium spp. or other ciliate spe-
cies, in the forestomach contents of SAC might be attributed to differences in feeding habits. The higher qual-
ity forages possibly ingested by the alpacas as compared with llamas would justify a larger and more diverse
protozoal community in their forestomach (Williams and Coleman 1992).
Eudiplodinium maggii
Epidinium ecaudatum
Length (µm)
Width (µm)
Length (µm)
Width (µm)
This Study
144.8
(120.5–178)
85.3
(72.3–96.4)
94.6
(79.5–108.5)
34.5
(34.1–38.5)
Ogimoto & Imai (1981)
-
(120–200)
-
(80–150)
-
(80–150)
-
(40–70)
Williams & Coleman (1992)
-
(104–198)
-
(63–125)
-
(85–140)
-
(37–54)
Dehority (1993)
151
(115–212)
100
(73–143)
124
(98–152)
48
(38–62)
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FORESTOMACH PROTOZOA OF LLAMAS AND ALPACAS
Conclusions
This paper is the first detailed description of protozoal diversity in the forestomach of South American cam-
elids involving a significant number of animals in the study. The absence of the vestibuliferids (Dasytricha
and Isotricha) has been confirmed, as well as that of some protozoal species commonly found in dromedaries
and bactrian camels such as Caloscolex spp., Diplodinium cameli, or Entodinium ovumrajae. The presence of
Epidinium species in the forestomach contents of the alpaca is a new host record. The protozoal concentration
and level of diversity in the contents of the forestomach are higher in alpacas than llamas. The alpacas har-
boured Diplodinium, Eudiplodinium and Epidinium spp. in addition to Entodinium spp.
Acknowledgements
Thanks are given to Profs. Tito Rodriguez and Freddy Lizón (Universidad Mayor de San Andrés de La Paz,
Bolivia) for his help in obtaining the samples, and to Prof. B.A. Dehority (Ohio State University, USA) for his
critical review of the manuscript
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