South American Camelids in Argentina

Transcription

1 Chapter I: Origin and Evolution of South American Camelids South American Camelids in Argentina History, Use, and Animal Health

2 South American Camelids in Argentina History, Use, and Animal Health Servicio Nacional de Sanidad y Calidad Agroalimentaria Av. Paseo Colón 367, C1063ACD Ciudad Autónoma de Buenos Aires República Argentina Tel. (054) (011) The author, Dr. Daniel A. de Lamo, is member of the ad hoc Committee on Camelids Health of the World Animal Health Organization (OIE). In 1976, he obtained the Veterinarian degree, granted by the University of Buenos Aires. He attended post-graduate studies at Illinois University (Urbana-Champaign), USA. He earned his Master of Science degree in 1985 and a PhD in 1990, at said University. Since 1980, when he was admitted as a research fellow in Conicet, he began to study wild fauna species of Patagonia, especially the ecology and physiology of the guanaco (Lama guanicoe). He has published over 30 technical papers in specialized magazines and has participated as lecturer at conferences and symposiums. At present, he works as regular associate professor in General Physiology and Compared Animal Ecophysiology Chairs at the School of Natural Sciences, National University of Patagonia San Juan Bosco, at Puerto Madryn. 2

3 Chapter I: Origin and Evolution of South American Camelids South American Camelids in Argentina History, Use, and Animal Health Ciudad Autónoma de Buenos Aires January 2011

4 South American Camelids in Argentina History, Use, and Animal Health 4

5 Chapter I: Origin and Evolution of South American Camelids Table of Contents Chapter I: Origin and Evolution of South American Camelids 7 Nomenclature 7 Origin and Evolution of Camelids 8 Wild South American Camelids 10 The Guanaco (Lama guanicoe) 10 The Vicuña (Vicugna vicugna) 13 Domesticated South American Camelids 14 The Llama (Lama glama) 14 The Alpaca (Lama pacos Linnaeus, 1758; Vicugna pacos Linnaeus, 1758) 16 References 18 Chapter II: History of the Use and Preservation of South American Camelids 19 Vicuña 19 Guanaco 23 References 28 Chapter III: Animal Health in South American Camelids 30 Zoonoses 30 Infectious Diseases 30 Bacterial Diseases 30 Viral Diseases 33 Parasitic Diseases 37 Internal Parasites 37 External Parasites 41 References 42 5

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7 Chapter I: Origin and Evolution of South American Camelids Chapter I Origin and Evolution of South American Camelids Nomenclature There are currently four species of South American Camelids (SAC). Two of them are wild: the guanaco and the vicuña, while the other two are domesticated: the llama and the alpaca. SACs are classified with the Old World camels in the order Artiodactyla, suborder Tylopoda, within the Camelidae family, subdivided into the Lamini and Camelini tribes. The Camelidae have some typical distinctive features, namely: absence of horns; true canine teeth, separated from the premolars by a gap called diastema, in both the upper lower jaws; the anatomic structure of the rear limbs allows them to bend their legs beneath the body; the presence of a toenail on each phalange (instead of a hoof) on each foot and a footpad on each foot, among other features (Wheeler 1995). Like ruminants, they do not have teeth (incisors) in the upper jaw, which is covered by connective tissue (dental pad). From the viewpoint of digestive anatomy, the Tylopoda evolved independently from what are known as true ruminants of the suborder Pecora. They feature differences in the number of chambers and the disposition of pre-stomachs as against the Bovidae; however, they use similar mechanisms concerning the ability to regurgitate the cud and obtain energy from the volatile fatty acids resulting from fermentation in the rumen or main fermentation chamber. A summary of the systematic classification of the four species is shown in the Table below (after Wheeler 1995): Order: Artiodactyla owen, 1848 Suborder: Tylopoda illiger, 1811 Family: Camelidae gray, 1821 Tribe: Lamini webb,

8 South American Camelids in Argentina History, Use, and Animal Health Lama glama (Linnaeus, 1758). Common name: Llama Lama pacos (Linnaeus, 1758). Common name: Alpaca Lama guanicoe (Müller, 1776). Common name: Guanaco Vicugna vicugna (Molina, 1782). Common name: Vicuña. In addition, SACs share common features between all four species, such as the presence of metatarsal glands, a cleft lip, use of communal dung heaps, polygamous social organization, absence of pronounced sexual dimorphism, induced ovulation producing only one young per birthing or breeding season (Wheeler 1991). The chromosome analysis of the four species shows a similar value for all of them 2n = 74 (Marín et al. 2007). Origin and Evolution of Camelids Camelids appeared in the late Eocene and were amongst the first families of modern artiodactyls, followed by pigs, peccaries, and deer in the Oligocene, and by giraffes, antelopes, and cattle in the Miocene. Camels, both South American and Asian/African, first appeared in the central area of North America, where they spent 40 million years of their evolutionary history. Dispersal to other continents took place only 2-3 million years ago. The withers height of the earliest camel (Protylopus petersoni) was only 30 cm, resembling a miniature of the current guanaco, but it featured a stronger musacle structure. This species, that existed 40 million years ago (Upper Eocene) had four toes on each foot and 44 teeth with no gap between them. A desacendant from the Protylopus was the so-called ancestral camel or Poebrotherium wilsoni from Middle Oligocene (25-30 million years) which looked like a small guanaco, with the height of modern sheep, and already featured a gap between incisors and canines. Furthermore, this camel had only 2 toes on each foot and its premolars and molars had very low crowns which showed good adaptation to folivory. Ancestral camels seemed to be good runners, much more efficient in that task than modern ruminants. They already featured long legs and a long neck and had strong musacular development. In the Lower Miocene (12 25 million years), camelids split into four branches. In that epoch, there were many changes in morphology, especially in the locomotor system and food habits. There was an increase in body size (Gauthier-Pilthers and Dagg 1981) and brain matter, and footpads started showing under each limb (Webb 1972). Also in this period, upper incisors disappeared, one of them turning into a canine, and a great de- 8

9 Chapter I: Origin and Evolution of South American Camelids pression in the facial part of the maxilla developed to contain a complex musacle structure in the lips (Webb 1965), which provided those organs with greater mobility. In addition, the molars crown became higher, which shows adaptation to process abrasive plants, a morphological adaptation that goes hand in hand with a change in food habits from browser to grazer. During the Miocene, camelids featured a clear development in locomotion; movement was fast, taking long steps, a typical characteristic of long-legged species, which arises as an adaptation to wide and plain environments (Franklin 1982). From this ancestral Miocene form, the evolution in North America resulted in two large groups of much more advanced camelids. In the Late Miocene (5-10 million years), the genus Pliauchenia evolved into a form that had very similar features to the current llama. In the Late Pliocene (3 million years), camelids emigrated to Asia through the Bering land bridge. When they arrived in Europe, they SACattered rapidly throughout Eurasia, reaching the Mediterranean area to the South and China to the East, through the Gobi desert. These Old World camels split into the two currently living species of the genus Camelus, from the Miolabis, going through the Procamelus and Titanotylopus in the Late Pliocene. As early as the Pleistocene, the Paracamelus resulted in the modern camels: the two-humped or Bactrian camel (Camelus bactrianus) in the steppes and mountains of Mongolia and the Dromedary or Arabian camel (Camelus dromedarius) of Southeast Asia and the North of African deserts (Gauthier-Pilthers and Dagg 1981). Meanwhile, the Hemiauchenia (with very long legs) diversified in North America and colonized South America with the opening of the Isthmus of Panama together with other species in what was called the Great American Interchange (Marshall et al. 1982) in the early Pleistocene. In South America, camelids might have had a common ancestor in the Middle Pleistocen. The Paleolama (with short legs), now extinct, was thought to be the ancestor of the current genus Lama; nowadays, however, it is not considered to be an ancestor of the genera Lama or Vicugna (Wheeler 1995), which are the evolutionary lineage of the Hemiauchenia (López Aranguren 1930; Cabrera 1932; Webb 1972). The core of the evolutionary origin of the genus Lama would be the Andes mountain range, where short-legged animals could move around more easily and be able to maneuver in sloping and steep soils. The genus Lama SACattered rapidly throughout South America, even in places where Hemiauchenia were present, thus overlapping their distribution range. 9

10 South American Camelids in Argentina History, Use, and Animal Health Towards the end of the Policene, 10 to years ago, the great llamas of the genera Paleolama and Hemiauchenia became extinct, and the only surviving genera were the Lama and Vicugna at the end of the Pleistocene (Wheeler 1995), these being the last representatives of the two wild species of South American Camelids (SAC). Wild South American Camelids The Guanaco (Lama guanicoe) Subspecies While four geographical guanaco subspecies have been desacribed, the studies performed do not meet the required criteria to make a final classification. These subspecies were desacribed based on body measures, skin color, skull size and proportions, among other variables (González et al. 2006). In the early 20 th century, the following subspecies were identified: L. g. cacsilensis; L. g. voglii; L. g. huanacus, and L. g. guanicoe. The L. g. cacsilensis lives in the high Andes of Peru, while the L. g. huanacus can only be found in Chile, according to Molina (1782), the L. g. voglii on the eastern side of the Argentine Andes, and the L. g. guanicoe from south Peru to Tierra del Fuego. However, some molecular studies based on the cytochrome b of the mitochondrial DNA recognize only two subspecies: L. g. cacsilensis and L. g. guanicoe, while the remainder populations are grouped in a clade known as L. g. guanicoe (González et al. 2006). The most renowned and better desacribed subspecies is the 10

11 Chapter I: Origin and Evolution of South American Camelids Lama guanicoe guanicoe Müller, 1776; therefore, this will be the reference subspecies to desacribe the most relevant details of its biological cycle, social structure, and behavior. General Features The guanaco (Lama guanicoe) is the largest wild artiodactyle in South America. Its distribution is the widest of all SACs, ranging from 8 to 55 south latitude, in Tierra del Fuego. Some members of this species can be found in altitudes that go from sea level to 5,200 meters above it. Even though the presence of this species in some areas of Paraguay is a matter of debate, it can be found in the territories of Argentina, Bolivia, Chile, and Peru, which shows great adaptation to a wide range of environments and weathers. The pelage coloration of this species is quite similar among the different populations and subspecies, varying from reddish brown in the south to clay yellow tones in the north of Peru. The chest, the belly, and the insides of the legs are white, while the head features different shades of gray, with lighter areas around the eyes and the edges of the ears. As already stated, there is no pronounced sexual dimorphism, and no significant differences were observed in the growth curves of animals in captivity (De Lamo 1995). The weight of a wild adult can reach kg, although most wild guanacos sheared rarely exceed 100 kg. Some authors believe that the guanacos from North Peru feature a lower live weight, reaching up to 96 kg (Kostritsky & Vilchez 1974). Withers height varies from 100 to 120 cm, while body length from the tip of the nose to the base of the tail ranges from 167 to 210 cm (MacDonagh 1949; Raedeke 1979; Dennler de la Tour 1954). The social organization of this species has been defined in several ways: depending on the authors, it can be divided into 3 or more types of groups, although the common criterion among all of them is that of Family Groups. These groups are composed of a leading male that shares its territory with a given number of females, which may vary from 5 to 15, with their young (Puig and Videla 1995), even though this relation can vary in different years and types of environment; for instance, in the province of Chubut, the average family group showed a ratio of 4 females per each male (Garrido et al. 1980). This overt variability in the number of females that make up this type of groups in the species range of distribution is attributable to the type of resource-defense polygyny (Franklin 1983), where one male defends an area that has food, water, and 11

12 South American Camelids in Argentina History, Use, and Animal Health shelter, including esacape paths (del Valle et al. 1986). The other social groups can be further divided but, in general, they are composed of a large number of males (groups of males of different age) and can reach 200 members in high-density areas. Females reach their breeding age at 2, while males reach that age at three, although such condition does not guarantee the formation of a family group. If an adult male cannot form a family group, it generally becomes part of the so-called bachelor groups, where non-breeding females can also be found (Saba 1987). Females have copulation-induced ovulation and give birth to only one young per year, after a gestation period of around 345 days. The young stays with the mother throughout the whole year or until the birth of the next young, although weaning usually occurs during late fall, when the young has already developed its adult digestive system (De Lamo 1995). The birthing season varies according to the geographical location of the population. In Peru, the birthing season ranges from April to June (Franklin 1975), while in Argentina and Chile it starts in September and moves towards the south and the west until October and November. In the provinces of Chubut and Santa Cruz, the first birthing peak takes place between November and December (De Lamo et al. 1982), while in Tierra del Fuego it can go from December to February (Raedeke 1979). In the south of Chubut, there can be a second birthing peak from February to March; females that are born in this period and survive the first year of age reach puberty at the age of three because they fail to achieve the weight or minimum development to breed in the breeding season of 2-year-old females (De Lamo 1995). The weight of a newly-born young varies from 8 to 12 kg (Raedeke 1979; De Lamo and Saba 1993). Most births occur during the early hours of the day and the young can rapidly stand on their feet (Franklin & Johnson 1994, De Lamo and Saba 1993, Sarasqueta and De Lamo 1995). The dispersal or expulsion of the young or juvenile members from family groups by territorial males results from competition over resources, especially food, within the areas where family groups settle. From the feeding point of view, the guanaco can be classified as an intermediary or opportunistic herbivore (Hofmann 1989), since it consumes a wide variety of plants. A comprehensive summary of the feeding ecology of this species has been compiled by González et al (2006). 12

13 Chapter I: Origin and Evolution of South American Camelids The Vicuña (Vicugna vicugna) Subspecies It is the smallest wild SAC and two geographical subspecies have been desacribed: Vicugna vicugna vicugna Molina, 1872 and V.v. mensalis Thomas, The former distributes throughout the southern sector, in Peru, Bolivia and Argentina. The latter (V.v. mensalis) does so in the northern sector of its distribution area. General Features The typical pelage of the vicuña is that of the V.v. mensalis, which is cinnamon-brown in the dorsal surface and on the sides of the body, the neck and on the back of the head. The chest, the belly, the inside of the legs and the lower portion of the head are white, as well as the base and the ventral surface of the tail. This subspecies features long chest hair which can reach almost 20 cm. The coloration of the Vicugna vicugna is a little lighter and white covers a greater portion of the body, rising from the belly to the ribs and covering the anterior portion of the rear legs; it lacks the long chest hair of the other subspecies. There is no significant sexual dimorphism (same as guanacos) and the live weight of males reaches approximately 36 kg, while the weight of females amounts to 33 kg for the V.v. mensalis (Paucar et al. 1984), although some authors report weights exceeding 45 kg (Gilmore 1950). 13

14 South American Camelids in Argentina History, Use, and Animal Health The social organization of this species shows a similar pattern to that of the guanaco, that is, they are organized in family groups, small droves of males and, according to Franklin (1982; 1983), solitary male groups. The territory marked by the male has a sleeping area in the highest sector and a feeding and water supply area in a lower sector (Franklin 1983). The male controls the size of the family group according to resource availability and drives away any vicuña alien to his territory and the young (whether male or female) before the beginning of birthing in February. The gestation period ranges from 330 to 350 days, the birthing peak being in March, at least in Peru (Franklin 1982). Contrary to what happens with guanacos, the vicuña is almost exclusively a grazer. It prefers perennial grasses, selecting the most succulent. It is worthy of note that territorial and feeding stability result from the stable ecosystems where the vicuña lives. These environments rarely suffer from weather swings; that fact, coupled with the regular provision of food, derives in a sedentary life or a life in fixed territories throughout the year. Apart from getting liquid out of succulent plants, vicuñas drink water on a daily basis (Koford 1957), which distinguishes them from the guanaco, which can drink water sporadically in times of drought. Domesticated South American Camelids The Llama (Lama glama) The llama is the largest domesticated camelid and resembles in many morphological and behavioral respects its wild ancestor, the guanaco. Like the wild species, the llama has a wide 14

15 Chapter I: Origin and Evolution of South American Camelids range of geographical distribution, although it is considered to be currently narrower than the range prior to the European colonization. Nowadays, the llama spreads from Colombia, going through Ecuador, Peru, Bolivia, and Argentina, to the center of Chile (Wheeler 1991); however, since it is a domesticated animal, there are herds in Tierra del Fuego and Santa Cruz (Argentina), as well as in countries such as the United States of America, New Zeland, and some European countries. Two phenotype varieties can be found; most are Q ara or nonwoolly, with little fiber development in the body and no fibers in the face and legs. The other type, called Chaku or woolly, features more fibers in the body that cover the forehead and grow from inside the ears, but do not cover the legs (Wheeler 1991). A while ago, Cardozo (1954) proposed another classification dividing llamas into brachymorphic, with abundant fiber, and dolichomorphic, which show an elongated profile. Despite these classifications, native shepherds distinguish their animals between those producing good-quality fiber and those producing low-quality fibers; therefore, no reference to Andean types can be made in connection to llamas; although most llamas are Q ara, they have been traditionally important in economic terms as pack animals, not fiber-producers (Wheeler 1991). The pelage of the llama varies from white to black and brown, going through all shades of in-between colors, and can usually feature spots of several colors in a single animal. Size and body measurements are very similar to those of the guanaco, exceeding in many cases 130 kg of live weight, as a result of the selection of llamas as pack animals. Despite domestication, the social organization of this species resembles that of guanacos. A flock is composed of a leading breeding male with his females and young. The male marks a territory with sleeping sectors in the highest areas and feeding sectors in the lower areas; it also drives away male young before they reach one year of age. This differential feature as against the guanaco allows for the growth of domesticated animals flocks. Trophic features resemble those of the guanaco, being able to adapt to a great diversity of environments and plant types, and go through times of drought (San Martín 1987). 15

16 South American Camelids in Argentina History, Use, and Animal Health The Alpaca (Lama pacos Linnaeus, 1758; Vicugna pacos Linnaeus, 1758) It is the smallest species of domesticated camelids and shares many features with its wild ancestor, the vicuña (Marín et al. 2007). Current distribution results from domestication 6,000 years ago in the central puna territories of Peru (Wheeler 1984), covering a strip that goes from the north of Peru to the south of Bolivia, with very few members in the north of Chile and the northwest of Argentina (Wheeler 1995). There are two known phenotypes called Huacaya and Suri. The Huacaya variety is more numerous. The body is entirely covered by very thick fibers that also cover the legs, forehead and cheeks, and even form a quiff that may cover the eyes. The fiber is curly, which gives a sponge-like appearance. The Suri variety is covered by silky, straight, and longer fibers and, because of their structure, they fall from the spine down to the sides of the body. The coloration of the alpaca s pelage is much more uniform that the llama s, since the alpaca was artificially selected to produce fiber. Coloration varies from white to black, brown, and extends through many shades of in-between colors; however, pelage is generally uniform; selection has mostly been towards white, so many colors of the native Andean populations of Peru have been eliminated (Wheeler 1991). In addition, selection has led alpaca to share the thinness of its fiber with that of the vicuña. 16

17 Chapter I: Origin and Evolution of South American Camelids Despite domestication, the social aspects of the alpaca are similar to those of the vicuña. There are males and females in flocks, where the former are leaders with the same polygamous features of the other SACs. The gestation period of the alpaca varies from 342 to 345 days, contrary to the vicuña, which can reach up to 350 days. While from a trophic viewpoint, the alpaca is a selective and opportunistic herbivore, in this case, it shows preference for herbaceous plants and it only browses when in extreme need and it must drink water every day (San Martín 1991.) References Cabrera, A Sobre los camélidos fósiles y actuales de la América austral. Revista del Museo de la Plata 33: Cardozo, A Los Auquénidos. Editorial Centenario. La Paz, Bolivia. De Lamo, D.A.; Garrido, J.L. and Kovacs, Z Población y parámetros reproductivos del guanaco (Lama guanicoe, Camelidae, Mammalia). Centro Nac. Patagónico, Contribución 64:1-11. De Lamo, D Aspectos Ecofisiológicos. In: Técnicas para el manejo del guanaco. Puig, S (ed). UICN. Cap. 6: De Lamo, D.A. and Saba, S Características del parto normal en el guanaco (Lama guani coe). Vet. Arg. X(91): Del Valle, H.F.; De Lamo, D.A. & Gagliardini, D.A Environmental affinity of the guanaco (Lama guanicoe Muller, Camelidae) in two selected areas of Central Patagonia supported by ERS-1 SAR data. Earth Observation Quarterly 55: Dennler de la Tour, G The guanaco. Oryx 2: Franklin, W.L Guanacos in Peru. Oryx 13(2): Franklin, W.L Biology, ecology and relationship to man of the South American Camelids. In: Mammalian Biology in South America. Mares, M.A. & Genoways, H.H. (ed) Pymatuning Lab. of Ecology. Special Pub Nº 6: Franklin, W.L Contrasting socioecologies of South America s wild camelids: the vicuña and the guanaco. In: Advances in the study of mammalian behavior. Eisemberg, J.F. and Kleiman, D.G. (ed). Special Pub. No 7. American Soc. of Mammalogists. 753 pp. Franklin, W.L. & Johnson, W Hand capture of new-born open habitat ungulate: the South American guanaco. Wildlife Society Bulletin 22: Garrido, J.L., Amaya, J.N. and Kovacs, Z Relevamiento de una población de guanacos de la provincia de Chubut. Resultados de tres años de recuentos. CENPAT. Contribución 47:1-13. Gauthier-Pilthers, H. and Dagg, A.I The Camel: its evolution, ecology, behavior, and relationship to man. University of Chicago Press. USA. 208 PP. Gilmore, R Fauna and ethnozoology of South America. Bureau of American Ethnography Bulletin 143. Smithsonian Institution. González, B.A., Palma, R.E., Zapata, B. and Marín, J.C Taxonomic and biogeographical status of guanaco Lama guanicoe (Artiodactyla, Camelidae). Mammal Review 36(2):

18 South American Camelids in Argentina History, Use, and Animal Health Hofmann, R.R Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia, 78: Koford, C.B The Vicuña and the Puna. Ecological Monographs 27(2): Kostritsky, B & Vilchez, S Informe, proyecto Santuario Nacional del Guanaco, Calipuy. Dir. Gral. de Foresta y Caza, Ministerio de Agricultura. Lima, Perú. López Aranguren, D.J Camélidos fósiles argentinos. Anales de la Sociedad Científica Argentina. 109: MacDonagh, E.J Los guanacos de Curamalal. Notas del Museo de La Plata, Zoología 14 (129): Marín, J.C., Zapata, B., González, B.A., Bonacic, C., Wheeler, J.C., Casey, C., Bruford, M., Palma, E., Poulin, E., Alliende, M.A., and Spotorno, A.E Sistemática, taxonomía y domesticación de alpacas y llamas: nueva evidencia cromosómica y molecular. Revista Chilena de Historia Natural 80: Marshall, L.G., Webb, S.D., Sepkoski, J.J. and Raup, L Mammalian evolution and the great American interchange. Science, 215: Molina, J.I Saggio sulle storia naturale del Chile. Bologna. Paucar, A., Téllez, J., Neyra, L. and Rodríguez, J Estudio tecnológico del beneficio de vicuñas. In: F. Villiger, compilador. La Vicuña, pp Editorial Los Pinos. Puig, S. and Videla, F Comportamiento y organización social del guanaco. In: Técnicas para el manejo del guanaco. Puig, S (ed). UICN. Cap. 7: Raedeke, K.J Population dynamics and socioecology of the guanaco (Lama guanicoe) of Magallanes, Chile. An Arbor, Michigan, University Microfilms International. Saba, S.L Biología reproductiva del guanaco (Lama guanicoe M). Tesis Doctoral. Univ. Nac. De La Plata, Argentina. San Martín, F.A Comparative forage selectivity and nutrition of South American Camelids and Sheep. Ann Arbor, Univ. Microfilms International. San Martín, F.A Alimentación y Nutrición. Capítulo VII ( ). In: Fernández-Baca, S. (ed) Avances y perspectivas del conocimiento de los Camélidos Sudamericanos. FAO. Santiago, Chile. 429 pp. Sarasqueta, D. and De Lamo, D Manejo en semicautiverio. Capitulo 13. In: Técnicas para el manejo del guanaco. Puig, S (ed). UICN. Pp Webb, S.D The osteology of Camelops. Bull of Los Angeles County Museum. 1:1-54. Webb, S.D Locomotor evolution in camels. Forma et Functio. 5: Wheeler, J.C La domesticación de la alpaca (Lama pacos L.) y la llama (Lama glama L.) y el desarrollo temprano de la ganadería autóctona en los Andes Centrales. Boletín de Lima 36: Wheeler, J.C Origen, evolución y status actual. In: Fernández-Baca, S. (ed) Avances y perspectivas del conocimiento de los Camélidos Sudamericanos. FAO. Santiago, Chile. 429 pp. Wheeler, J.C Evolution and present situation of the South American Camelidae. Biological Journal of the Linnean Society, 54:

19 Chapter II: History of the Use and Preservation of South American Camelids Chapter II History of the Use and Preservation of South American Camelids Vicuña South American Camelids (SAC) have been a strategic resource for mankind in terms of supplying products such as meat, fur, wool, or as pack or transportation animals. With the arrival of man to South America 10 to 20,000 years ago, wild camelids served as a source of products with great availability for use, including forms of life that are now extinct: Paleolama and Hemiauchenia (Franklin 1982). Some archeological studies claim that pre-pottery societies, as hunter-gatherers, depended on camelids to obtain food and other resources. Probably, the social organization of the vicuña, stable throughout the year, provided these prehistoric hunters with a permanent sustenance and marked the beginning of a sedentary culture in the high Andes (Rick 1980). According to Gade (1969), nomadic pastoralism, which was common in other arid regions of the world, could never fully settle in the high Andes, and such difference would stem from the fact that camelids were not the only food source. However, seasonal herding was identified in the Puna of Junín 3,000 years B.C. (Novoa and Wheeler 1982), and Browman (1974) reported semi-nomadic pastoralism in the center of Peru between the years 2,000 and 500 before today. The most ancient camelid hunting technique consisted in herding a group of animals towards a confined site or natural enclosure, where hunters would sacrifice their prey with lances, especially vicuñas (Neira 1968); the bow and arrow were used later on, as an advanced capture or hunting means. The vicuña s domestication process might have begun 6,000-8,000 years ago at the Lake Titicaca basin, giving rise, through selection, to the domesticated species Vicugna (Lama) pacos or alpaca (Novoa and Wheeler 1982). It seems that the different races or varieties of alpacas were specially used for a given purpose to produce fine wool or meat (Wheeler 1984). Pastoralism arose with the domestication of animals; however, the hunting of wild animals remained, which was an importance source of proteins, in terms of meat as well as horns and fibers (Laker et al. 2006). With the expansion of the Inca empire, the use of the vicuña 19

20 South American Camelids in Argentina History, Use, and Animal Health became somewhat regulated, since the animals belonged to the Inca and they decided the type of capture to be implemented. One means of capture was the Chaku Real, which was guided by the Inca themselves, while the other were the chaku or qayqus guided by the native authorities of each location (Laker et al. 2006). The chaku or real hunting consisted in very large herds involving a great number of people, ranging from 4,000 to 50,000 individuals. Logically, the territory covered depended on the number of individuals involved and the number of captured animals could vary from 300/400 to 30,000/40,000 vicuñas. This tradition remained in modern times, although the number of people involved decreased. There are reports that estimate captures of around 30 and 40,000 vicuñas by the 15th century in Peru (Flores-Ochoa 1994). The situation of the vicuña started to worsen with the arrival of Spanish conquerors. Despite the fact that belief systems persisted in the native peasant communities, no cultural restriction for the killing of vicuñas to get their fur was recognized. Already in the 16th century, there are reports that show concern on the dramatic demographic decrease, reporting killings of up to 80,000 dead animals per year in Peru and the north of Chile (Chebez 1994). The empire court issued a decree in 1777 whereby it considered the killing of a vicuña an illegal act and urged for the need of control by a court. It was the first law enacted to protect the species. During the same period, an important fur exchange to new textile factories in Spain developed. From the setting of the Viceroyalty of the Rio de la Plata in 1776, an amount equivalent to the fur of 20,000 animals was exported through the port of Buenos Aires. This exchange continued through 1810 and during most of the 19th century; within a period of 190 years ( ), an amount equivalent to 1,572,000 vicuñas was exported from the port of Buenos Aires to European markets (Laker et al. 2006). Until the second decade of the 20th century, the Chaku method remained in the Argentine Northwest and likely in the other Andean countries, although not in the same gigantic proportions as in the Inca times. Around 1920, the spread of fire guns and the transformation experienced by traditional society, changed the hunting method: the collective chaku was left behind and solitary hunters or small armed groups joined by dogs arose. A Peruvian supreme decree of 1920 prohibited the exchange of vicuña products and similar measures were attempted in Argentina, where a law of 1926 prohibited the killing of animals and the trading of vicuña fiber and other products made with vicuña 20

21 Chapter II: History of the Use and Preservation of South American Camelids fiber. The measures had limited impact on hunting levels, which became a clandestine activity. In 1933, the state relaxed control and started granting export licenses in parallel to an increase in international demand for vicuña and a dramatic decrease in population. Data from an English textile company show that around the 1950s, a single buyer was responsible for the import of 1,270 kilograms in average equivalent to 5,500-6,500 individuals. Thus, the vicuña population went from 400,000 animals in the 1950s down to 10,000 animals in 1967 (Wheeler and Hoces 1997). Trading continued despite the danger posed to the species, until hunting was prohibited by international restrictions and measures introduced in the first Vicuña Convention signed between Bolivia and Peru in 1969, and later ratified by Argentina (1971), Chile (1972) and Ecuador (1979). In 1975, all vicuña populations were included in CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora) Appendix I which forbade the international trade of the vicuña fiber. This decision led to a marked recovery of populations and, in many cases, the areas where local extinctions had occurred were recolonized. Many of these measures had a high level of acceptance and observance by rural communities (Cajal et al. 1998). With the recovery of several populations in Chile and Peru, such populations became part of the CITES Appendix II, which recognizes that the species is not endangered but trade must be controlled to avoid that the species becomes once again endangered. By 1995, all populations of Peru and the north of Chile were incorporated to Appendix II. In Argentina, the vicuñas in captivity and the wild populations of Jujuy became part of such Appendix in 1997, and those from Catamarca in 2002, when all vicuña populations of Bolivia were also included. Currently, the species is regaining its distribution range and some increase in demographic density can be identified, after years of indiscriminate extraction and irrational management. The vicuña is a key species in the high-andean system and in the areas with a favorable environment for their development, its potential as a provider of special fibers under a model of sustainable use must be considered. According to some reports of the Vicuña Convention, by 2005 there was an estimate total of 285,041 vicuñas in the natural distribution range of South America. This information fails to consider the data contributed by the census carried out in Argentina in 2006/7. In Argentina, the results of the last census carried out in the 21

22 South American Camelids in Argentina History, Use, and Animal Health north of the Colorado River, shows figures that, depending on the sampling method, vary from 72,678 to 127,072 animals, the lowest estimated amount assessed being 15,234 vicuñas (Bureau of Wild Fauna [Dirección de Fauna Silvestre] 2008). The current use of this species is based on shearing animals, both wild and domesticated, under the coverage provided by Appendix II of the CITES. One of the rational use programs was implemented in Jujuy at the Experimental High-Altitude Field [Campo Experimental de Altura] of the National Institute of Agricultural Technology [INTA] in Abra Pampa. A population core or breeding ground was settled there, where many studies were performed on breeding physiology and methodologies on immobilization and shearing were implemented. The program consisted in the delivery of original vicuñas from that field to private producers. The purpose was to incorporate the species to a rational use system, giving small producers the possibility to benefit from the trading of the fiber. Since the initial investment in infrastructure was high, in most cases debt had to be undertaken (whether public or private) which was difficult to amortize. Out of the 28 breeding grounds initially registered, 13 went out of business and from the remainder very few reached the expected ecological and economic sustainability. In 2005, this pilot experience was deemed concluded and, currently, the INTA EEA Abra Pampa is working on research lines to gain more insight on the impact of handling this species to adjust protocols with methodologies and techniques to be applied in the future. However, animals are still sheared, from which nearly 85 kg of hair are obtained a year. Another experience was implemented in Jujuy with Los Pioneros producer association from Cieneguillas, where vicuñas were captured, sheared and released in private fields. Even though this experience was enriching because of its low impact on vicuñas, the impact and benefits for the general community are unknown, since the fiber has not yet been sold (Romero 2009). In the province of Catamarca (under Appendix II since 2002), wild animals continue being captured periodically in provincial Reservoirs. Animals are sheared in community called official shearing. From the herding and enclosing in the Laguna Blanca and Cerro Pabellón Reserve, nearly 50 kg of fiber a year are obtained. There are also private ventures in that province where animals are captured and sheared through different methods and they add up to a total production of nearly 400 kg a year resulting from the different use and management methods. 22

23 Chapter II: History of the Use and Preservation of South American Camelids Guanaco The domestication of the guanaco dates back to 4,200 years B.C., according to Yacobaccio (2004), and it might have derived in the domesticated form: the Llama. It is possible to state that 2,500 years B.P., in the first settlements called formative (with a productive economic basis) there is already presence of camelid fossils comparable to the current llamas (Elkin et al. 1991). As already described in the previous chapter, the distribution of the guanaco is very extensive from the geographical viewpoint and domestication led to having virtually no control over wild populations in the north of the distribution area, which resulted in the indiscriminate and virtually lethal use of the species. The native peoples of what is currently the south of Argentina and Chile depended on this species as a resource used in a more natural fashion, which avoided artificial selection and the creation of new species. Within continental Patagonia and Tierra del Fuego, the guanaco was a fundamental resource for hunter-gatherer groups that lived in those regions during most of the Holocene. Historically, the guanaco was a resource of utmost importance in the economy of Patagonian native hunters (Casamiquela 1983). For them, the guanaco was not only a meat source. Fur was used to make huts, coats, laces and straps, wool for knitting, tendons to make thread, and bones to build different kinds of instruments (Musters 1871; Moreno 1879; Mengoni 1995). For the hunter-gatherers of Patagonia, it was of the essence to have an alternative source of calories which would offset the lack of carbohydrates available; therefore, a possible strategy was the intensive exploitation of meat and animal fat sources (Claraz 1988). Apart from obtaining nutrients out of them, long bones were broken to remove the bone marrow which was mixed with mineral pigments to make paint. The splinters of some long bones (metapodial bones) were shaped and transformed into shaping tools (retocadores), which were used to make stone instruments, and awls to make holes on soft materials such as leather (Mengoni 1995). The native population of guanacos spread throughout South America and before the European conquest there were around 30 or 50 million animals, according to density figures obtained from census carried out in Patagonia (Raedeke 1979). Although these values were never confirmed scientifically, it is possible that because of the availability of forage, water and the lack of many natural predators, population densities were high and on the verge of the carrying capacity of many natural systems. 23

24 South American Camelids in Argentina History, Use, and Animal Health It is also likely that there were high mortality levels as a result of intense frost cycles and long snows as described in connection with the island of Tierra del Fuego 10 years ago (Montes et al. 2000). Likewise, the populations must have suffered strong changes because of generalized drought cycles or lack of water, where there is a reduction in the recruitment rate or a decrease in fertility caused by a lack of energy. During European colonization, populations might have decreased dramatically (Franklin and Fritz 1991). Estimates show that in the late 19 th century, the total population of guanacos was nearly 7 million animals (Cabrera and Yepes 1960; Torres 1985). Currently, the species covers only 40% of its original distribution and is divided into small and relatively isolated populations (Puig 1995; Franklin et al. 1997; Puig 1992), especially in the north of the Colorado River and in the provinces of Salta, with Catamarca, and La Rioja/San Juan with Mendoza (Bureau of Wild Fauna, 2008). Large guanaco concentrations are still found in Patagonia, especially in the provinces of Río Negro, Chubut, and Santa Cruz (Amaya et al. 2001), where nearly one million animals can be estimated, although no census has been carried out which makes it possible to obtain more precise figures and define estimation errors. From the European colonization onwards, in what is known today as Argentina, livestock was introduced, while fences, roads and other communication ways were built, which contributed to the retraction of guanaco populations. In Patagonia, basic livestock production is, since its inception, extensive and especially focused on sheep breeding (Barbería 1995). Also, the guanaco was an alternative resource for rural settlers with the capture of chulengos (local name for the young guanaco, generally used up to the first year of age, a denomination that can be extended until they reach breeding age) and the hunting of adults (De Lamo 1999). The leather of chulengos was used to make quillangos (a sewed guanaco-fur blanket, preferably made with chulengo fur, used as a cape); adult meat was used to feed shepherd dogs, while adult leather was used to make craft thongs and laces. According to the first official records, from the 1950s to the mid 1970s, guanaco-fur exports from Argentina amounted to 70,000 items per year on average (García Fernández 1993). The legal hunting of chulengos for fur export was an important economic activity. Between 1972 and 1979, 443,655 chulengo furs were legally exported, that is, an average of 63,000, with a peak of 86,000 furs exported during 1979, which were equivalent to an amount of 3.6 million dollars (Ojeda and Mares 24

25 Chapter II: History of the Use and Preservation of South American Camelids 1982). This activity continued during the following decade. In the province of Chubut, a hunting limit of over 118,000 guanacos was set between 1984 and The annual hunting limit for chulengos was usually higher than that of adults and ranged from 1,500 to 16,000 animals for the whole province depending on the season (Ribeiro and Lizurume 1995). In addition, between 1988 and 1993, interprovincial transit permits for 25,767 chulengo leathers and 10,949 guanaco leathers from Chubut were granted (Ribeiro and Lizurume 1995). The criterion followed to grant hunting permits was traditionally based on a statement of abundance made by the owners and managers of farms, who considered the guanaco to be a competitor of sheep over pastures and, therefore, used to overestimate the number of guanacos to obtain more permits (Baldi et al. 1997). As a result of the CITES recommendation in 1993, which proposed the suspension of guanaco imports from Argentina, exports were prohibited by the national Environmental Authority and the collapse of the business activity followed. Currently, Resolution No. 220/98 issued by the former Argentine Department of Natural Resources and Sustainable Development (SRNyDS) and Resolution No. 82/03 issued by the Argentine Department of the Environment and Sustainable Development (SAyDS) set management guidelines governing export activities, interprovincial transit, and trading at the federal level of guanaco products and by-products. These regulations allow the use of guanaco fiber from live animals only. On August 12, 1978, at the request of the Republic of Peru, the guanaco was included in Appendix II of the CITES Convention; therefore, the guanaco can only be used and traded under some restrictions and regulations. Even though guanaco exploitation was intense and trading was significant, Argentina ratified the CITES Treaty in Due to the export of high volumes of guanaco leather from Argentina, including chulengos, in 1992, the CITES Fauna Committee required Argentina to report the biological bases it uses to exploit such species as well as export control procedures. The CITES Administrative Authority of Argentina, after consulting with the provinces involved, failed to provide such information and, therefore, at the 29 th Meeting of the Standing Committee (March 1993), the suspension of guanaco imports from Argentina was recommended until an adequate management plan was submitted. In turn, the Standing Committee approved a study project proposal to assess the situation of the guanaco in Argentina and set a guanaco management plan for economic use, submitted by the CITES Administrative Authority of Argentina. In July, 1995 a research project was submitted which was approved by the CITES 25

26 South American Camelids in Argentina History, Use, and Animal Health in consultation with the Fauna Committee (CITES S-045). Afterwards, in the Patagonian region, different activities were carried out promoted by the Patagonian Regional Wild Fauna Advisor Council [Consejo Asesor Regional Patagónico de la Fauna Silvestre] (CARPFS), with a view to coordinating tasks and criteria to design the plan. Thus, in 1996, a Patagonian Meeting for the Management of Guanaco Populations was held in Puerto Madryn, province of Chubut. A series of agreements on the coordination of activities by provincial governments and some technical aspects to be considered in the final drafting of the Management Plan resulted from such meeting. A year later, in parallel to the Exotic Species Workshop, held in Bariloche, progress was made on agreements concerning working methods and the harmonization of legislation among provinces. When Resolution No. 220/98, issued by the former SRNyDS, entered into force, there was a recess in regional activities until 2000, when a meeting of authorities was held in Allen, Río Negro. In such meeting, agreement was reached on holding a technical forum in the context of the CARPFS to outline methodologies, marking systems, and minimum contents for management plans at breeding grounds. In November 2000, several agreements were reached and specific recommendations were made to carry out population assessments which were embodied in Annex I to Resolution No. 82/03. Meanwhile, in Chubut, a Provision (52/2000, DFyFS) was issued whereby a Registry of Evaluators was created at the provincial level. In 2002, a Workshop on Guanaco Fiber was held, followed by a Technical Meeting where information was given on the progress made in management types, and agreement was reached to draft another regulation which replaced Resolution No. 220/98. Also in 2002, the meeting continued in Buenos Aires, where the criteria to make a final draft of such regulation were agreed on. Finally, in 2004, scientific and technical experts, as well as provincial and national authorities, were called to work together on the preparation and final drafting of a Management Plan that governed the different aspects of guanaco protection, preservation, and management. In this context, two workshops were held (in Buenos Aires and Trelew) in 2004, where technical grounds were discussed and the legal aspects that the Management Plan ought to include were analyzed. A drafting Committee was selected, composed of representatives from the different sectors, which was entrusted with the preparation of a document that embodied all the conclusions reached by the working commissions during the workshops. By means of Resolution No. 477 of the Argentine Department of the Environment and Sustainable Development, the Guanaco 26

27 Chapter II: History of the Use and Preservation of South American Camelids Management Plan was approved and regulated, which was ratified by the provinces of Chubut, Mendoza, and Santa Cruz in In general terms, the plan responds to the need for regulations that turn the use of this species into a more sustainable activity; lists as some of its goals the assurance of preservation mechanisms that favor the existence of wild populations that are ecologically functional in their natural distribution range and encourages the appraisal of the guanaco from the biological, economic, and social viewpoints. In addition, it promotes the distribution of the benefits obtained from the use of the species as equitably as possible among the different social sectors. The plan states that the approval of guanaco-related ventures must include actions to mitigate the potential negative effects identified in each case. With respect to breeding in captivity, the Plan authorizes the opening of new breeding grounds provided only that their initial groups of animals are taken from livestock establishments with an adequate density of wild guanacos or from other breeding grounds. The plan includes the forms of certificates of origin and legal holding of guanaco animals and fiber. With respect to the management of wild species, the Plan calls for a population assessment before and after shearing, the drafting of periodical activity reports, highlighting the care it must be exercised when handling the animals during capture, and animal welfare throughout the entire process. In addition, the Plan also calls for the use of certificates of origin and legal holding of fiber for this type of management. Finally, the Plan intends to ground the sustainability of the species on animal welfare, taking into account unwanted effects that may result from epidemiologic interaction with other domesticated animals, especially ruminants bred in the natural distribution environment of guanacos. In 2007, in the provinces of Río Negro, Chubut, and Santa Cruz together, there were over 30 registered breeding grounds to perform live shearing of guanacos. Due to the absence of a firm market and price variability, very few continued carrying out shearing activities under that notion of production. For the 2009 shearing season, only three breeding grounds remain registered in Chubut. Total fiber production (fiber, hair, and trimmings) did not exceed 550 kilograms, which provides a picture of the lack of interest in the production of alternative fibers under a sustainable management framework. Conditions must be guaranteed for the market that will absorb such fibers to remain stable and for animal health to be monitored, in order to ensure product quality. Animal health will be discussed in the following chapter. 27

28 South American Camelids in Argentina History, Use, and Animal Health References Amaya, J. N., J. von Thüngen, and D. A. De Lamo Relevamiento y distribución de guanacos en la Patagonia. Comunicación Técnica Nº 107. Área RR NN. Fauna. INTA EEA Bariloche. INTA- GTZ-TöB.12 pp. Barbería, E. M Los dueños de la tierra en la Patagonia austral, Universidad Nacional de la Patagonia Austral. Argentina. 469 pp. Baldi, R., C. Campagna and S. Saba Abundancia y distribución del guanaco (Lama guanicoe) en el NE del Chubut, Patagonia. Argentina. Mastozool Neotrop 4:5-15. Browman, D.L Pastoral nomadism in the Andes. Current Anthropology, 15: Cabrera, A. and J. Yepes Mamíferos Sudamericanos, 2nd Edition. Ediar, Buenos Aires. 370 pp. Cajal, J.L., García Fernandez, J. and Tecchi. R (eds). La conservación de los camélidos silvestres en la puna y cordillera frontal. Bases para la conservación y manejo de la Puna y cordillera frontal FUCEMA UNESCO. Uruguay, 336 pp. Casamiquela, R.M La significación del guanaco (Lama guanicoe) en el ámbito pampeano-patagónico: Aspectos corológicos, ecológicos, etológicos y etnográficos. Mundo Ameghiniano 4: Claraz, J Diario de viaje de exploración al Chubut ( ). Marymar. Buenos Aires. Cunazza, C., S. Puig and L. Villalba Situación actual del guanaco y su ambiente. Pp In: S. Puig (ed.) Técnicas para el manejo del guanaco. UICN. Chébez, J.C Los que se van. Editorial Albatros. Buenos Aires. 604 pp. De Lamo, D.A El guanaco en Patagonia. Su relación con la producción animal y la conservación. Revista Argentina de Producción Animal 19(1): Dirección de Fauna Silvestre. Sec. de Ambiente y Desarrollo Sustentable. Argentina Primer Censo Nacional de Camélidos Silvestres al Norte del Río Colorado. 61pp. 25 mapas. Elkin, D.C., Madero, C.M., Mengoni Goñalons, G.L., Olivera, D.E. and Yacobaccio, H.D Avances en el estudio arqueológico de los camélidos del noroeste argentino. Actas de la VII Convención Internacional de Camélidos Sudamericanos. Flores-Ochoa, J Man s relationship with the camelids. Gold of the Andes: the llamas, alpacas, vicuñas and guanacos of South America. Martinez, J. (ed) pp Barcelona, Spain. Franklin, W.L Biology, ecology and relationship to man of the South American Camelids. In: Mammalian Biology in South America. Mares, M.A. & Genoways, H.H. (ed) Pymatuning Lab. of Ecology. Special Pub Nº 6: Franklin, W. L.; F. Bas, C. F.; Bonacic, C.; Cunazza, C. and Soto, N Striving to manage Patagonia guanacos for sustained use in the grazing agroecosystems of southern Chile. Wildl Soc Bull 25: Franklin, W. and M. Fritz Sustained harvesting of the Patagonian guanaco: is it possible or too late? Pp In: J. Robinson, K. Redford (eds) Neotropical Wildlife Use and Conservation. University of Chicago Press, Chicago. Gade, D.W The llama, alpaca and vicuña: fact vs. fiction. The Journal of Geography, 68: García Fernández, J Análisis del mercado de pelos finos de 28

29 Chapter II: History of the Use and Preservation of South American Camelids camélidos de la Argentina. Pp In: Taller sobre producción y comercialización de fibras especiales. INTA. EEA Bariloche. Laker, J., Baldo, J., Arzamendia, Y. and Yacobaccio, H.D La vicuña en los Andes. In: Investigación, conservación y manejo de vicuñas. Vilá, B. (ed). Cap. 4: Proyecto MACS. Universidad Nacional de Luján. Mengoni, G Importancia socio-económica del guanaco en el período pre-colombino. Pp In: S. Puig (ed) Técnicas para el Manejo del Guanaco. UICN. Montes, C., D.A. De Lamo and J. Zavatti Distribución de abundancias de guanacos (Lama guanicoe) en los distintos ambientes de Tierra del Fuego, Argentina, Mastozoología Neotropical/J. Neotrop. Mammal. 7(1): Moreno, F. P Viaje a la Patagonia Austral Buenos Aires. Musters, G. Ch.[ ] Vida entre los Patagones. Buenos Aires, Solar - Hachette. Neira, A.M Un Nuevo complejo lítico y pintura rupestre en la gruta SU-3 de Sumbay. Revista de la Facultad de letras, Universidad Nacional de San Agustín de Arequipa, 5: Novoa, C. and Wheeler, J Llamas and alpacas. In: Evolution of domesticated animals (I.L. Mason, ed). Longman, New York. Ojeda, R. A. and M. A. Mares Conservation of South American mammals: Argentina as a paradigm. Pp In: M. A. Mares and H. H. Genoways (eds.) Mammalian Biology in South America. Pymatuning Symposia in Ecology. Vol. 6. Special Publication Series. University of Pittsburgh, Pittsburgh, Pennsylvania. Puig, S Diagnóstico de situación y plan de acción para protección y manejo del guanaco en Argentina. In: H. Torres (ed.) South American Camelids. An Action Plan for their Conservation. IUCN/SSC South American Camelid Specialist Group. Puig, S. 1995b. Abundancia y distribución de las poblaciones de guanacos. Pp In: S. Puig (ed). Técnicas para el manejo del guanaco. UICN. Raedeke, K. J Population dynamics and socioecology of the guanaco (Lama guanicoe) of Magallanes, Chile. PhD thesis, University of Washington, Seattle. Rick, J.W Prehistoric hunters of the High Andes. Academic Press, New York. 362 pp. Ribeiro, G. and Lizurume, M.E Nuestra Fauna Silvestre. El Guanaco. Dirección de Fauna Silvestre. Provincia del Chubut. Publicación N 1:1-24. Romero, S.R Experiencias locales en manejo de vicuñas. In: Panorama Agropecuario de Salta y Jujuy. Ediciones INTA. 54: Torres, H Distribución y conservación del guanaco. Informe. International Union for Conservation of Nature and Natural Resources. Gland, Switzerland. 37 pp. Wheeler, J.C On the origin and early development of camelid pastoralism in the Andes. Animals and Archaeology. Grigson, C. (ed) pp BAR International Series. Wheeler, J.C. and Hoces, D Community participation, sustainable use and vicuña conservation in Perú. Mountain Research and Development 17: Yacobaccio, H.D Social dimension in camelid domestication in the southern Andes. Anthropozoologica, 39:

30 South American Camelids in Argentina. History, Use and Animal Health. Chapter III Animal Health in South American Camelids Zoonoses Infectious Diseases Parasitic Diseases Zoonoses Zoonoses are those diseases transmitted from animals to man. This transmission may occur through various channels such as air, water, biting, animal vectors, edibles of animal origin, etc. Since reported zoonoses in South American Camelids (SAC) are scarce, they will be described in each of the different categories of diseases that may affect this group of animals. Infectious Diseases Infectious diseases in SAC are important in both, domestic and wild species. In llama and alpaca because of the economic and social impact they may have on the different social strata of farmers supported by the production of fibers, meat or other by-products. In the case of guanaco and vicuña, apart from the effect that sanitary problems may have on the conservation of those species, they may harm the production profile of animals under management in semi-captive conditions or farmed as the domestic species. A large track of reports about these diseases, mainly for the domestic species in Perú and Bolivia has been published by the end of the 20 th Century (Ramírez 1991a). The information may be extrapolated for the same species in Argentina, considering the differences in the environmental conditions and the types of production. For the domestic species (llama and alpaca) several infectious diseases are associated, to the digestive tract and diagnosed as diarrheas, specially in young animals (less than one year) Bacterial Diseases Clostridioisis Diseases produced by anaerobic bacteria that in many cases are 30

31 Chapter III: Animal Health in South American Camelids part of the regular flora of the digestive tract, but under unfavorable circumstances produce the disease. Enterotoxaemia (Enteritis) is an acute infectious disease affecting the new born of llama (Venzano et al. 1997), alpaca (Ramírez 1991b) and vicuña (Ramírez 1987). The etiologic agent is Clostridium perfringens Types A and C, being Type A the most important agent under an epidemiologic point of view. C. perfringens Type D is the main pathogen in cattle and sheep, and it is described as pathogen for SAC in the USA only (Fowler 1994). In alpacas C. perfringens may show lethality when the animals are co-infected or parasitized with Eimeria sp.[see parasitism] (Londoñe et al. 2006). Tetanus is produced by Clostridium tetani being always a consequence of tissue damage (wounds), never as a spontaneous disease. Another similar disease produced by Clostridium septicum is called Malignant Edema where the original source of contamination is a bruise or tissue injury contaminated with the anaerobic bacteria; such cases were described for alpacas and llamas in the USA (Fowler 1994). The effect that bacterial diseases on newborns or young animals particularly Colibacilosis (Escherichia coli) may have, is of great importance because they may kill animals of up to two months old with a peak of infection between the second and eleventh day of life. Serotypes were classified according to their somatic antigens associated with enteropathogenic E.coli in alpacas as: O136, O78 y O8/O60/OX2B (Ramírez 1991). Infections with E. coli in adult SAC represents the most common cause of uterine (endometriosis), mammary gland (mastitis) and other infections (Fowler 1994). Records of outbreaks of diarrhea from Argentina with rates of morbidity and mortality up to 80% in captive guanacos were associated to co-infections with E. coli, Salmonella and rotavirus (Parreño et al. 2001). Serotype O26:H11 from E. coli (STEC) producer of Shiga toxin (Stx) was isolated from feces of a two months old chulengo (guanaco newborn) with severe, aqueous diarrhea. The relevance of this finding is that SAC may show susceptibility to E. coli types with zoonotic characteristics associated to hemolytic uremic syndrome in humans (Mercado et al. 2004). Pathogens of the genus Salmonella sp identified for the SAC include S. cholerasuis var kunzendorf y S. typhimurium (Parreño y Marcoppido 2006). Salmonella sp were isolated from a sample taken in an autopsy of a newborn guanaco with severe diarrhea, which later died form septicemia (Parreño et al. 2001). Acute respiratory infections are also common in the offspring 31

32 South American Camelids in Argentina. History, Use and Animal Health. of SAC, mainly those individuals who have not received colostrum. Pneumonic processes have been described with low levels of inmunoglobulin G (IgG) in young animals of less than 21 days of life (Garmendia y McGuire 1987). In baby alpacas with respiratory disease, Pasteurella multocida (Fowler 1994, Solís Hospinal 2000, Ramírez 2001) and P. heamolytica (Ramírez 1991) were isolated. In older SAC, bacteria of the genus Mycoplasma (M. mycoides and M. capricolum) could be involved in the infection (Hung et al. 1991). Staphylococcus aureus and Streptococcus sp (hemolytic) have been isolated from baby alpaca with pneumonia (Barsallo 1985). Brucellosis or infectious abortion is caused by Brucella melitensis and it is seldom found in domestic SAC (Rodriguez 1991). However, in herds of alpacas from Bolivia the disease would have caused 11.2% of the abortions (Cup et al. 2003, Parreño and Marcoppido 2006). In wild guanacos negative results were found for B. melitensis by serological tests in blood melitensis (Karesh et al. 1998) and the same happened for a sample of 86 guanacos from different farms in Argentine Patagonia for Brucella abortus, melitensis, suis, ovis y canis (Robles et al. 2006). Also, negative results were found for 35 wild guanacos in regions IV and XII of Chile for nonspecific brucellosis (Zapata et al. 2006). Brucellosis is one of the diseases transmissible to man and an actual zoonoses for field workers in contact with sick animals (Ramírez 1991a). No reports of these cases are for Argentina. There are very few reports on the occurrence of Listeriosis in Camelids. This disease mainly produced by Listeria monocytogenes has been reported to few alpacas and llamas, both young and adult (Frank et al. 1998). Leptospirosis is caused by a number of microorganisms of the genus Leptospira and it is associated with cases of epizootic abortions in llamas outside the Andes (Fowler 1994). Negative serological values were found in wild guanacos from Chubut for L. interrogans (Karesh et al. 1998). A complete study on 494 animals (llamas, guanacos and vicuñas) from different regions of Argentina, showed prevalence of Listeriosis varying between 47 and 96% in llamas; between 0 and 13% in guanacos and between 9 and 63% in vicuñas (Llorente et al. 2002). Paratuberculosis produced by the Mycobacterium paratuberculosis has not been diagnosed neither in guanacos in Patagonia or in the domestic species of SAC (Karesh et al. 1998). 32

33 Pseudo tuberculosis, caused by Corynebacterium pyogenes and C. pseudotuberculosis sometimes is wrongly diagnosed as the so-called abscesses, but involves one or more swollen lymph nodes near the mouth caused by an infection of different etiological origin. The disease was described for llamas and young alpacas (Ramírez 1991a); however, the bacteria were not isolated form lymphatic nodes of wild guanacos sampled for scientific purposes (De Lamo, pers. comm.) Tuberculosis (TB) is caused by bacteria of the genus Mycobacterium, but only M. microti, M. avium, M. tuberculosis, M. bovis and M. kansaii having been isolated for the different SAC species, particularly the domestic: llamas and alpacas (Thoen et al. 1977, Ramirez 1991). However, there are records of the disease caused by M. microti in vicuñas (Fowler 1994) and llamas (Oevermann et al. 2004) in farms outside South America. In a study, SAC were inoculated with M. bovis y M. avium and 92% of the animals showed macro and microscopic lesions compatible with TB, stressing that llamas are very susceptible to bovine TB (Blanco Viera et al. 1997). Anthrax is an acute bacterial disease caused by the Bacillus anthracis characterized by a generalized septicaemia affecting many species of mammals, and has also been recognized for SAC (Ramirez 1991a). In Argentina, the first case described by anatomic-pathology and confirmed in the laboratory was in llamas from a breeding farm, where also deaths by the same agent occurred in cattle and sheep (Blanco Viera et al. 1997). In addition, 2-3 cases were recorded in the central part of Argentina which affected llamas, sheep and goats (Parreño and Marcoppido 2006). The so-called Osteomyelitis is a chronic disease that occurs as an inflammation of the jaw or maxilla, where a bulge area is the expression of the lesions of the bones and surrounding soft structures. The main causal agent is bacteria of the genus Actinomyces, though complex and mixed infections may occur after the first injury. The start of this pathology is due to the ingestion of harsh vegetation or fibrous pastures where woody parts of the plant damage the mucosa and connective tissue allowing the entry of micro-organisms to the bone. This condition has been described in the domestic species (1948 Cuba c.f. Ramírez 1991a) and in wild guanacos (De Lamo and Garrido 1983). Viral Diseases There is not much information on clinical cases and records of this taxonomic group s own viral agents are almost zero. There 33

34 South American Camelids in Argentina. History, Use and Animal Health. is only one tumor produced by Papillomaviruses in llamas (Schulman et al. 2003) and rotavirus diarrhea in young guanacos reported (Parreño et al. 2001). Foot and Mouth Disease (FMD) is a highly contagious viral disease in cattle, sheep, pigs and goats caused by Picornavirus (aftovirus) group. Although only one case of FMD in Alpaca of Perú has been described (Guerrero, 1971), there have been no reports of clinical cases of the disease in Argentina to date (SE- NASA 2010). According to a report by the Central Laboratory of SENASA, Argentina (OIE Reference Lab) 537 sera were processed between 2005 and 2009, for determination of antibodies anti VIIA (Antigen associated with viral infection) all with negative results. Routinely tests on 212 sera for determination of viral activity of FMD were performed during the year 2007, and 17 samples during 2009; all of them with negative results using the ELISA test for determination of structural serotypes against antibodies O, A and C of this viral disease. Llamas under experimental infection with infected pigs demonstrated that there is a high resistance to FMD in these camelids, speculating that these species would not act as reservoirs of the disease (Fondevila et al. 1995). In a pilot study in Argentina, only 3 of a total of 30 llamas exposed to infected animals developed neutralizing antibodies against the Antigen associated with infection; only 2 llamas presented barely detectable signs, while the 30 animals in contact and the 40 sentinel (control) animals remained free of symptoms without evidence of infection (Blanco Viera et al. 1997). Other serological surveys made in Peru and Argentina in alpacas, llamas and wild guanacos did not detect antibodies against different serotypes of the FMD virus, which would confirm the low susceptibility of camelids to this disease (Wernery and Kaaden 2004). Surveys carried out in Argentina detected prevalence of 87.7% for Rotavirus (RV) in llamas (Puntel et al. 1999), while sampling in llamas, vicuñas and guanacos detected prevalence of more than 80% with antibodies against RV (Parreño et to the. 2003). Also, RV was the most prevalent virus in chulengos with severe diarrhea in farms raising the wild species (Parreño et al. 2001). Similarly, Parreño et al. (2004) conducted the genetic analysis of the proteins that make up the outer capsid of the virus detecting that it corresponds to P [1] G8 in Río Negro animal strain and strain P [14] G8 for animal of Chubut, both of the Patagonian region of Argentina. Similarly, antibodies against RV (100%) were detected in farmed and wild vicuñas during the years 2003 / 2004, as well as in llamas for the same period (Parreño and Marcoppido 2006). It is important to highlight that VR 34

35 Chapter III: Animal Health in South American Camelids is an agent that may be present in all populations of SAC in Argentina and that the diarrhea caused by this agent may become a serious problem when wild species are managed in captivity (Parreño and Marcoppido 2006). Blue Tongue (BT) is a disease caused by Reovirus affecting mainly sheep. It was considered exotic to Argentina until Studies in Perú have given positive serology for 21% of the sampled alpacas and 1.5% prevalence in llamas from farms in the USA, but negative in Argentina. Also, negative values for 14 samples of guanacos from Río Negro and Chubut (Argentina) were found for 2008 and 2009 (SENASA Lab 2010). Other survey in the Argentine Puna showed 0% positives in llama and vicuña (Parreño and Marcoppido 2006). Bovine Viral Diarrhea (BVDV) has been described for llamas and alpacas outside South America (Carr and Carman 2005). Surveys in South America found 10 positive llamas in cattle raising farms with loads exceeding 70% antibodies against BVD, but did not detect positive animals in areas devoted exclusively to breeding llamas in several provinces of northern Argentina. A survey carried out in Chile for four species of SAC, found antibodies against BVD in 10.8% of alpacas and 14% of llamas; but negative results were found in the wild species (Celedón et al. 2001). Another survey at a provincial reserve in the province of Catamarca (Argentina) found 15% prevalence in llamas and 30.4% vicuñas, it also found about 10% of positive sera in vicuñas in captivity in Salta and guanacos in semi-captivity in the province of Río Negro, Argentina (Leoni et al. 2000). No positive reactors were found in a study with twenty wild guanacos in a provincial reserve of the province of Chubut, Argentina (Karesh et al. 1998) either for 10 baby guanacos born in Río Negro and raised in Buenos Aires (Marcoppido et al. 2004). Positive serology for BVD was found in 14 guanacos from farms in the Río Negro and Chubut provinces by the OIE Reference Lab, Argentina (SENASA 2010). In the same study, no positive serology for BVD was found in 66 guanaco blood samples from three ranches in the south of Río Negro (Robles et al. 2006); the same results were obtained with 35 adult animals of the IV and XII region of Chile (Zapata et al. 2006). Blood sampling of vicuñas during 2004 in Argentina, showed 2.04% positive serum, while the value boosted up to 25% (2/8) positivity in llamas from Cieneguillas, Argentina during 2004 (Parreño and Marcoppido 2006). A survey carried out in Peru on the cascilensis guanaco (Lama guanicoe cascilensis), a species which is in serious risk of extinction, serology threw an incidence of 18.2% to VDB in 2005 (Rivera et al. 2006). 35

36 South American Camelids in Argentina. History, Use and Animal Health. Among diseases caused by herpes virus, bovine Herpesvirus - 1 (BHV-1) has shown a degree of positive sera in Peru, with values of antibodies anti BHV1 between 5 and 18% in alpacas (Parreño and Marcoppido 2006); also in that country, antibodies up to 16.2% were detected in llamas. These values were obtained form mixed farming (cattle/camelids) rodeos, but studies performed exclusively in domestic camelids and wild vicuñas were negative to this pathology (Rosadio et al. 1993). In Argentina, studies in llamas farmed in the provinces of Buenos Aires, Córdoba, Catamarca, Jujuy and Salta showed very low seroprevalence of 0.77% (Puntel et al. 1999). In another survey values were higher (31.4%) in llamas and 20.6% of positivite sera in vicuñas from the provinces of Salta and Catamarca, Argentina (Leoni et al. 2000). No positive guanacos sera were found in a study in Chubut (Karesh et al. 1998) or in the Río Negro province, also in Argentina (Marcoppido et al. 2004). A minimum value of 2% (1/50) prevalence was detected in wild vicuñas, and a somewhat higher value of 11.1% (1/9) for llamas of the same site (Cieneguillas, Argentina) in 2003 (Parreño and Marcoppido 2006). Equine herpesvirus 1 (EHV1) is a disease that was described for the first time in camelidsin The SAC (llamas and alpacas) caught the disease by contact of with infected zebras in a zoo (Rebhun et al. 1988). Argentina found a single positive llama for HVE1 on 278 analyzed whereas the results were negative for guanacos and vicuñas (Leoni et al. 2000). On the other hand, in Chile antibodies anti EHV1 were found in 19.4% of the alpacas analyzed; 22.7% in llamas, 24.3% in guanacos and 56% of the sampled vicuñas (Parreño and Marcoppido 2006). Most of the viral diseases associated with the respiratory system were described for cattle, among them: Bovine Parainfluenza Virus-3 (IP-3) and the Bovine Respiratory Syncytial Virus (BRSV) (Penumovirus). In alpacas studied in Peru, occurrences of 71.1% to IP-3 and 82.95% to BRSV were found associated with high mortality by pneumonia (Victorio et al. 2004). A new serological survey carried out in Peru on Lama guanicoe cascilensis, showed a 30% incidence of BRSV and 30% of IP-3 in 2003, while in 2005 results showed a reduction to 27.3% for BRSV, increasing up to 45.5% for PI-3 (Rivera et al. 2006). It is interesting to note a case of seraconversion of antibodies against IP-3 in wild guanacos bred in captivity for research purposes. Sera from animals born in Río Negro province gave negative against IP-3 at arrival to the experimental farm in the Buenos Aires province, Argentina. Monthly monitoring revealed asymptomatic infection of IP-3 when the animals were seven months old. Apparently the guanacos were infected when they took contact with calves with signs of respiratory disease 36

37 Chapter III: Animal Health in South American Camelids (Marcoppido et al. 2004). The same virus (IP-3 a paramyxovirus which causes acute pneumonia in SAC) was detected in 46.6% (34/73) of wild vicuña and about 67% (6/9) of llamas sampled in Cieneguillas, Argentina (Parreño and Marcoppido 2006). Alpaca cells cultured in vitro have shown the same susceptibility to IP-3, BRSV and BHV-1 as they do in bovine cultured cells; demonstrating that these diseases can easily spread when breeding livestock of European origin and SAC in common spaces (Sanchez et al. 2006). There are several viral diseases with low impact on SAC such as Rabies (Rhabdovirus) that has been mentioned in one isolated case of a llama bitten by a rabid fox in Perú (Ramírez 1991a) and several alpacas bitten by rabid domestic dogs; the sick alpacas may spread the virus by biting other healthy animals (Franco 1968). The same applies to Contagious Ecthyma (Parapoxvirus) which is a typical disease of sheep that was only clinical diagnosed in alpacas of Peru (Ramírez 1991b). Parasitic Diseases In the SAC parasitic diseases have an important economic impact particularly in the domestic species. The same effect is for the wild species when confined or raised in captivity. For this reason, many parasitic diseases in SAC are shared with domestic species introduced in different environments of South America, or in areas where SAC are introduced out of the Andes Internal Parasites Protozoa Coccidiosis is produced by protozoa of the genus Eimeria. Leguía (1991b) cites 6 species: E. lamae; E. alpacae; E. punoensis; E. peruviana; E. macusaniensis and E. ivitaensis. However, E. peruviana is not considered specific for the SAC anymore (Palacios et al. 2006). Almost all species of Eimeria parasitize llamas and alpacas in their natural distribution sites and in those away from South America, where SAC could be bred. Data taken in Peru show that the incidence of E. macusaniensis is high for alpacas of less than one year (77.5%), with lower incidence (17.5%) in animals older than the year of age. E. macusaniensis parasite infant guanacos in USA with a 16.7% incidence, reduced to 5.9% in older individuals. In a sample of 12 guanacos of unknown age from the south of Argentina, 75% were parasitized with E. macusaniensis (Aguirre and Cafrune 2007). Fecal analysis made in samples from farms with guanacos of Chubut and Río Negro, 37

38 South American Camelids in Argentina. History, Use and Animal Health. Argentina showed presence of Coccidia oocysts in 90% of the cases (De Lamo comm. pers.; Flores et al. 2006). A comparative study of guanaco s parasites in Chile found that Eimeria does not parasitize guanacos in the south of the country, as it does in the north (Zapata et al. 2006). Eimeria parasitize vicuñas in Catamarca, Argentina (Cafrune et to the. 2009). For instance, E. lamae parasitized 45% of the infant alpacas and 17.5% in animals older than one year in Peru. However, in the same country (Peru) E. punoensis parasitized 5% of infant alpacas and 85.5% of the older animals (Aguirre and Cafrune 2007). Sarcocystiosis is caused by protozoa of the genus Sarcocystis which require two hosts to complete its cycle. These hosts, in the SAC are Canids (dogs, foxes). The typical parasites for the domestic SAC species are S. aucheniae and S. lamacanis. Infestation by S. tilopodi and S. guanicoe-canis for guanacos of Argentina and Chile were reported; although it is not confirmed, these two separate species of parasites may correspond to a single one (Aguirre, Cafrune 2007). Due to the phylogenetic relationship of the SAC species, it is presumed that all species of Sarcocystis are potentially infective to the SAC, both wild and domestic (Leguía 1991b). In Argentina the presence of Sarcocystis sp was confirmed in llamas (Cafrune et al 2001; Pidre et al. 2002), guanacos (Beldoménico et al. 2003) and vicuñas (Kühne 1986). Sarcocystis sp macroscopic cysts in skeletal muscle and microscopic cysts in cardiac muscle were described for dead guanacos in Rio Negro, Argentina (Robles et al. 2006). Macroscopic cysts of S. tilopodi in skeletal muscle were found in a 3 year old wild guanaco in Chubut, Argentina (Dominguez 2009). There is not reliable information or certainty about Sarcocystiosis prevalence in South America. In Peru it is presumed that most of the SAC domestic species host Sarcocystis in skeletal muscles (Castro 1974). In Peru a natural transplacentary infection in an embryo of alpaca has been reported (Vélez et al. 2006); this information opens a new perspective on the transmission of these parasites in the SAC. Sarcocistiosis is a zoonoses. The consumption of raw or not sufficiently cooked infected meat causes gastroenteritis, nausea, diarrhea and cramps; these effects are caused by a toxic substance in the cysts (Leguía 1991b). Nematodes (round worms) There are few nematodes that are specific to the SAC, including Camelostrongylus mentulatus, Graphinema auchenia, Mazamastrongylus (Spiculopteragia) peruvianus, Lamanema 38

39 Chapter III: Animal Health in South American Camelids chavezi, Nematodirus lamae and Trichuris tenuis, and perhaps a kind of Capillaria [c.f. Leguía et al. 1995]: Aguirre and Cafrune 2007). Other genera of nematodes are shared with many domestic ruminants: Haemonchus Trichostrongylus, Ostertagia, Cooperia, Nematodirus, Bunostomum, Marshallagia, Chabertia, Oesophagostomum, Trichuris, Skjrabinema, Strongyloides (Aguirre and Cafrune 2007). All the specific nematode species are described for llamas (Alcaíno et al. 1991; Cafrune et al. 1999), alpacas and vicuñas (wild species). In the guanaco, only Trichuris tenuis is described as specific (Beldoménico et al. 2003). C. mentulatus was described in llamas of North America and Chile; it was also found in llamas of Argentina (Cafrune et al. 2006a) as well as Lamanema chavezi (Cafrune et al. 2006b). Trichuris tenuis was found in llamas, vicuñas (Cafrune et al. 1999) and guanacos (Beldoménico et al. 2003). In Patagonia (Argentina) adults of Cooperia sp., Ostertagia ostertagi, Trichostrongylus sp. and Nematodirus sp. were found in guanacos (Larrieu et al. 1982; Larrieu et al. 1985); all the mentioned nematodes and Haemonchus sp in llama (Larrieu et al. 1985). Adults and eggs of Capillaria sp. were described in guanaco (Larrieu et al. 1982), vicuña and llama (Cafrune et al. 2004; 2006b). Eggs of Nematodirus sp were reported for guanacos in Tierra del Fuego, Argentina (Navone and Merino 1989) and for wild guanacos in Chubut (Karesh et al. 1998; Beldoménico et al. 2003). In the study mentioned before, Larrieu et al found the following species of the genus Nematodirus: N. spathiger, N. lanceolatus, N. filicolis and N. battus, being the first report for guanacos of Patagonia (Argentina). Studies with guanacos in the south of Chile (XII Region) found the genera: Trichuris (28%), Trichostrongylus (5.5%) and Marshallagia (28%). Positive identification of the same genera with different incidence was found in the north of Chile (IV Region): Trichuris (19%), Trichostrongylus (5.5%), Eimeria (6%) and Nematodirus with 19% (Zapata et al. 2006). Flukes (flat worms) One of the most conspicuous parasites is Fasciola hepatica, which has been described both for the domestic and wild SAC, but only in the wild species when animals are restricted or raised in semi-captivity (Cafrune et al. 2004; Olaechea and Abbot 2005; Robles et al. 2006; Flores et al. 2006). The distribution of F. hepatica is very broad in the Argentinean Puna with varying prevalences (Aguirre, Cafrune 2007). For the Peruvian 39

40 South American Camelids in Argentina. History, Use and Animal Health. Altiplano, Leguía (1991b) describes a very low prevalence for alpacas and llamas (8% and 2% respectively) explaining that the low presence of flukes is due to adverse environmental conditions for the parasite and for the snail (intermediate host) that transmits the disease. The fasciolasis or distomatosis is a zoonoses of high prevalence in enzootic areas in the mountains of Peru, where consumption of vegetables of short stem in salads causes the income of the parasite by digestive tract areas (Leguía et al. 1989). The information available about the effect this zoonoses might have in Argentina is scarce. Cestodes (flat worms) These tapeworms are the same species that parasitize other domestic ruminants sharing environments or range with the different species of SAC. Moniezia expansa has been identified in dead guanacos in Chile (Alcaíno et al. 1991) and in Argentina (Beldoménico et al. 2003). In the province of Jujuy, Argentina a liver tapeworm Thysanosoma actinioides was described for llamas (Aguirre and Cafrune 2007). These cestodes have a complex cycle, with an intermediate host developing the hydatid cyst, mainly in liver and lungs. The development of cysts is the negative effect parasites may have on SAC. For instance, Echinococcus granulosus (hydatidosis) needs to complete its cycle a Canid (wild or domestic) that contaminates the pasture with feces where the herbivores forage. From an epidemiological point of view, the information is scarce for the SAC of Argentina. For alpacas in Peru, between 7 and 19% of animals with the presence of cysts and 55% of cysts fertility have been described (Leguía 1991a). In the south of Chile, from 25 wild guanacos subjected to autopsy only 3 presented cysts (2 of them fertile), which implies a 12% prevalence; the author confirms the presence of hydatid cyst in wild guanacos and estimates that the incidence may be close to 10% (Cunazza 1978). In the province of Chubut (Argentina), there is a control program of the hydatidic disease which has been successful in the epidemiological aspects with sheep. However, no records are available about the presence of cysts in guanacos. Being a (cyclic) zoonoses the control programs should consider the SAC as intermediate hosts in their protocols, since the disease can affect men in contact with dogs that have consumed viscera with infected cysts. There is not accurate information available of this disease in relationship with SAC in Argentina. In Peru rates of 9.4 per 40

41 Chapter III: Animal Health in South American Camelids inhabitants incidence was reported for the year 1988 (Leguía 1991b). Among the SAC non-specific nematodes, Dictyocaulus filaria was described in wild guanacos of Patagonia (Argentina), where an estimated prevalence of 83.3% associated with pulmonary congestion was published (Karesh et al 1998; Beldoménico et al. 2003). External Parasites Lice. Pediculosis. For the SAC, three species of lice of the genus Microthoracius are cited: M. praelongiceps; M. mazzai and M. minor; also, there is one species of the masticatory type: Bovicola breviceps. Apparently all the picks can parasitize all species of SAC, e.g. M. praelongiceps was found in four species of SAC; M. mazzai in llamas, alpacas and vicuñas and M. minor in alpacas and vicuñas (Castro and Cicchino 1998; Valencia and Infantes 2001). The incidence of this parasitosis is highly variable; a prevalence of M. praelongiceps up to 38 per cent in adult alpacas of Chile have been estimated; also about 14% incidence for yearling alpacas (Rojas et al. 1993). On the other hand, M. mazzai parasitized 40% of adult alpaca against 20% in juveniles in Peru (Cicchino et al. 1998). There are of four species of lice specific for SAC in Argentina. Three of them included in the genus Microthoracius (M. praelongiceps; M. mazzai and M. minor) and one in the genus Bovicola (B. breviceps). Mites. Scabies There are 3 types of mange in the SAC: sarcoptic, psoroptic and chorioptic. Sarcoptic produced by Sarcoptes scabiei var auchenia was described for all the SAC, particularly llamas, alpacas and vicuñas in their natural environments (Leguía 1991b) and outside South America (McKenna et al. 2005). Psoroptic scabies is produced by Psoroptes auchenia which parasitize on llamas, alpacas and vicuñas (Leguía 1991b); although, some authors consider that it is produced by a not yet defined species of Psoroptes (Aguirre and Cafrune 2007). Chorioptic scabies is probably produced in by Chorioptes bovis (Aguirre and Cafrune 2007), but has only been reported in domestic SAC raised outside the Andes. The prevalence of sarcoptic mange may exceed 40% in herds of alpacas of Peru, being the second parasitic disease in importance of that country (Leguía 1991a, b). For Argentina, there 41

42 South American Camelids in Argentina. History, Use and Animal Health. is no reliable information describing the presence of this type of scabies in guanacos raising farms in Río Negro (Larrieu et al. 1985) or in wild animals from Chubut (Karesh et al. 1998). Prevalence of scabies in wild guanacos (unspecified species) may fluctuate between 8 and 15% for the Chilean Tierra del Fuego (Raedeke 1978; Cunazza, 1978, 1982). It is considered, at least for the moment, that in the Argentinian Puna the SAC scabies would be a disease of minor importance compared to the incidence it has on the SAC in the Peruvian Highlands (Aguirre and Cafrune 2007). Mites. Ticks Only two species of ticks were described as parasites of the SAC: Amblyomma parvisatum and Otobius megnini. The first is a bloodsucker in each of its metamorphic stages (larva, nymph, adult), parasitizing a series of different hosts. Adults of A. parvisatum is specific to the SAC, although the specificity would not be strict (Estrada-Peña et al. 2005). This parasite is highly distributed in the Highlands of Peru, Chile and Argentina; the distribution comprises also both Argentine and Chilean Patagonia (Estrada-Peña et al. 2005). Otobius megnini has a single host in its cycle, being the preferred setting place the external auditory canal; this setting facilitates the occurrence of otitis (Aguirre and Cafrune 2007). Llamas are suitable host for the ordinary bovine tick (Boophilus microplus), which was experimentally verified in Argentina (Aguirre et al. 2000). References Infectious Diseases Barsallo, J Agentes bacterianos encontrados en el aparato respiratorio de alpacas aparentemente normales. Anales V Convención Internacional sobre Camélidos Sudamericanos. Cuzco, Perú. (Resumen p. 36) Blanco Viera, F.J.; Antognoli, M.C.; y Pereira, J.J Logros y futuros avances en proyectos de sanidad de camélidos sudamericanos. Aftosa, tuberculosis y brucelosis. Actas del 2º Seminario Internacional de Camélidos Sudamericanos Domésticos. Resumen: Blanco Viera, F.J.; Vena, M.M. y Carrillo, B.J Descripción de un caso de carbunclo en camélidos sudamericanos (Lama glama) en la República Argentina. Actas del 2º Seminario Internacional de Camélidos Sudamericanos Domésticos. Resumen: Carr, N. y Carman, S BDV Virus: A newly recognized serious health problem. Alpacas Magazine 4:12. 42

43 Chapter III: Animal Health in South American Camelids Celedón, M.; Sandoval, A.; Droguett, J.; Calfio, R.; Ascencio, L.; Pizarro, J. y Navarro, B Pesquisa de anticuerpos seroneutralizantes para pestivirus y herpesvirus en ovinos, caprinos y camélidos sudamericanos de Chile. Arch. Med. Vet. (33)2: Copa, S. Suxo, M. y Vino, N Incidencia de Brucelosis en alpacas en las comunidades del Cantón Ulla Ulla del Depto. de la Paz. III Congreso Mundial de Camélidos. Potosí, Bolivia. Resúmenes: Cuba, A Osteomielitis del maxilar inferior de las alpacas. Rev. Fac. Med. Veter. Lima, Perú. 4: De Lamo, D.A. y Garrido, J.L Anomalías e infecciones dentarias y su relación con la mortalidad de guanacos. Gaceta Veterinaria 45(382): Fondevila, N.A.; Marcoveccio, F. J.; Blanco Viera, J. B.; O Donnell, V.K.; Carrillo, B.J.; Schudel, A.A.; David, M.; Torres, A. y Mebus C.A Susceptibility of llamas (Lama glama) to infection with foot-and-mouth-disease virus. Zentralbl. Veterinarmed. 42(10): Fowler, M Medicine and Surgery of South American Camelids. 4th Edition. Iowa State University Press. 454 pp. Franco, E Brote de rabia en alpacas de una hacienda del Departamento de Puno. Boletín Extraord. IVITA 3: Frank, N.; Couetil, L. y Clarke, K.A Listeria monocytogenes and Escherichia coli septicemia and meningoencephalitis in a 7 day old llama. Can. Vet. J. 30(2): Garmendia, A. y McGuire, T Mechanisms and isotypes envolved in passive inmunoglobulin transfer to the newborn alpaca (Lama pacos). Am. J. Vet. Res. 48(10): Guerrero, C La alpaca: enfermedades infecciosas y parasitarias. Centro de Investigación IVITA, Univ. San Marcos, Lima, Perú. Boletín de divulgación 8:38-63 Hung, A., Alvarado, A., López, T., Perales, R., Li, O. y García, E Detection of antibodies to mycoplasmas in South American Camelids. Res. Vet. Sci. 51(3): Karesh, W.B.; Uhart, M.M.; Dierenfeld, E.S.; Braselton, W.E.; Torres, A.; House, C.; Puche, H. y Cook, R.A Health evaluation of free-ranging guanacos (Lama guanicoe). J. Zoo Wildl. Med. 29: Leoni, L.; Cheetham, S.; Lager, I.; Parreño, V.; Fondevila, N.A.; Rutter, B.; Martínez, B.; Fernández, F. y Schudel, A Prevalencia serológica de anticuerpos contra enfermedades virales del ganado en llama (Lama glama), guanaco (Lama guanicoe) y vicuña (Vicugna vicugna). Second Latin American Congress of specialist in small ruminant and South American Camelids. Mérida, México. Llorente, P.M.; Leoni, L. y Martínez Vivot, M Leptospirosis en Camélidos Sudamericanos. Estudio de prevalencia serológica en distintas regiones de la Argentina. Arch. Med. Vet. XXXIV, (1). Londoñe, P; Pérez, D.; Castillo, H.; Véliz, A.; Llanco, L.; Yaya, K.; Maturrano, L. y Rosadio, R Evidencia de coinfección de Eimeria macusaniensis y Clostridium perfringens en enterotoxemia en alpacas. IV Congreso Mundial sobre Camélidos. Resúmenes: 40. Marcoppido, G.; Parreño, V.; Romero, S.; D Amico, N.; Duro, S.; Pacienza, N.; Lager, I.; Lamas, H; Bonacic, C. y Vilá, B Seroprevalencia de anticuerpos en vicuñas (Vicugna vicugna) silvestres de la Puna Argentina. 4to Seminario Internacional de Caméli- 43

44 South American Camelids in Argentina. History, Use and Animal Health. dos Sudamericanos. Proyecto DECAMA. Córdoba, Argentina. Marcoppido, G.; D Amico, N.; Olivera, V.; Bok, K. y Parreño, V Investigación de la circulación de Rotavirus, Virus de la Diarrea Viral Bovina y Rinotraqueítis Infecciosa Bovina en chulengos criados bajo condiciones intensivas. Taller de Aprovechamiento Sustentable de Guanacos en Argentina. INTA Bariloche. Mercado, E.C., Rodríguez, S.M., Elizondo, A.M., Marcoppido, G. y Parreño, V Isolation of shiga toxin-producing Escherichia coli from a South American Camelid (Lama guanicoe) with diarrhoea. J. of Clinical Microbiology 42(10): Oevermann, A.; Pfyffer, G.E.; Zanolari, P.; Meylan, M. y Robert, N Generalized tuberculosis in llamas (Lama glama) due to Mycobacterium microti. J. of Clin. Microbiol. 42(4): Parreño, V. y Marcoppido, G Estudio de la sanidad en camélidos: Avances a partir de muestras de camélidos silvestres. En: Investigación, conservación y manejo de vicuñas. Vilá, B. (ed). Cap. 11: Proyecto MACS-Argentina. Buenos Aires. 208 pp. Parreño, V., Constantini, V., Cheetham, S., Blanco Viera, J., Saif, L., Fernández, F. Leoni, L. y Schudel, A First isolation of rotavirus associated with neonatal diarrhoea in guanacos (Lama guanicoe) in the Argentinean Patagonia region. J. Vet. Med. B Infect. Dis. Vet. Public Health 48: Parreño, V., Marcoppido, G., Constantini, V., Cheetham, S., Vagnozzi, A., Leoni, S., Schudel, A. y Fernández, F Seroprevalencia y circulación de Rotavirus en camélidos sudamericanos de la República Argentina. III Congreso Mundial de camélidos. Libro de Memorias: Puntel, M.; Fondevila, N.A.; Blanco Viera, J.B.; O Donnell, V.K.; Marcoveccio, F.J.; Carrillo, B.J.; Schudel, A.A Serological survey of viral antibodies in llamas (Lama glama) in Argentina. Zentralbl. Veterinarmed. B 46: Ramírez, A Alpaca Clostridium perfringens Type A. Enterotoxemia: purification and assays of the enterotoxin. Ph. D. Dissertation. Colorado St. University. USA. 201 pp. Ramírez, A. 1991a. Enfermedades infecciosas. Capítulo VII. En: avances y perspectivas del conocimiento de los Camélidos Sudamericanos. Fernández Baca, S. (ed). Oficina Regional FAO para América Latina y el Caribe. Santiago, Chile. Ramírez, A. 1991b. Enfermedades infecciosas en Alpacas y Llamas. Producción de Rumiantes menores: Alpacas: Rebhun, W.C; Jenkins, D.H.; Rhiis, R.C.; Dill, S.G.; Duvobi, E.J. y Torres, A An epizootic of blindness and encephalitis associated with a herpesvirus indistinguishable from equine herpesvirus 1 in a herd of alpacas and llamas. J. Am. Vet. Med. Assoc. 192(7): Rivera, H.; Castillo, H.; Véliz, A.; Manchego, A.; Hoces, D.; Rosadio, R. y Wheeler, J Evidencia serológica de circulación de agentes virales en guanacos silvestres del Perú. IV Congreso Mundial sobre Camélidos. Resúmenes: 41. Robles, C.; von Thungen, J.; Cabrera, C.; Chodilef, M.; Odeón, R. y Parreño, V Aspectos sanitarios en majadas de guanacos en semi-cautividad en la Patagonia Argentina. IV Congreso Mundial sobre Camélidos. Resúmenes: 45. Rosadio, R.H; Rivera, H. y Manchego, A Prevalence of neutralising antibodies to bovine herpesvirus-1 in Peruvian livestock. 44

45 Chapter III: Animal Health in South American Camelids Vet. Rec. 132 (24): Sánchez, M., Manchego, A., Araínga, M. y Rivera H Susceptibilidad de células de alpaca, cultivadas in vitro, a infecciones de los Virus Respiratorio Sincitial, Diarrea Viral Bovina, HerpesVirus Bovino-1 y ParaInfluenza 3 Bovina. IV Congreso Mundial sobre Camélidos. Resúmenes: 76. Schulman, F.Y.; Kraft, A.E.; Janczewski, T.; Reupert, R.; Jackson, K. y Garner M.M Camelid mucoutaneous fibropapillomas: clinocopathologic findings and association with papillomavirus. Veter. Pathol. 40(1): Thoen, C.O; Richards, W.D. y Jamagin, J.L Mycobacteria isolated from exotic animals. J. A. Vet. Med. Assoc. 170: Venzano, A.J., Passini, M.I., Blanco Viera, A.M. y Pereira, J.J Enterotoxemia en una llama lactante. Descripción de un caso de campo. Actas del 2do Seminario Internacional de Camélidos Sudamericanos Domésticos: Victorio, W.; Rivera, H.; Manchego, A.; Benito, A.; Quispe, R.; Yaya, C.; Olazábal, J. y Rosadio, R Evidencias serológicas de virus neumotrópicos en alpacas de la provincia de Canchis, Cuzco. Perú. Libro de Memorias ( ), III Congreso Mundial de Camélidos. Potosí, Bolivia. Wernery, U. y Kaaden, O.R Foot and mouth disease in camelids: a review. Vet. J. 168(2): Zapata, B.; Marín, M.P.; Mac-Niven, V.; Ríos, C.; Castro, V. y Sepúlveda, C Determinación de algunas enfermedades infecciosas y parasitarias en guanacos (Lama guanicoe) silvestres en 2 regiones de Chile. IV Congreso Mundial sobre Camélidos. Resúmenes: 75. Parasitic Diseases Alcaíno, H.; Gorman, T. y Burgos, M Helmintiasis gastrointestinal en llamas (Lama glama) de la I Región de Chile. Parasitol. al Día (Chile). 15: Aguirre, D.H.; Cafrune, M.M. and Guglielmone, A.A Experimental infestation of llamas (Lama glama) with Boophilus microplus (Acari: Ixodidae). Exp. Appl. Acarol. 24: Aguirre, D.H. y Cafrune, M.M Parásitos de los Camélidos Sudamericanos. En: Enfermedades parasitarias de los ovinos y otros rumiantes menores del Cono Sur. Suárez, V.H.; Olaechea, F.V.; Romero, J.R. y Rossanigo, C.E. (eds). INTA EEA Anguil Ediciones. Argentina. pp: Beldoménico, P.M.; Uhart, M., Bono, M.F.; Marull, C.; Baldi, R. and Peralta, J.L Internal parasites of free ranging guanacos from Patagonia. Vet. Parasitol. 118: Cafrune, M.M.; Aguirre, D.H. and Rickard, L.G Recovery of Trichuris tenuis (Chandler, 1930), from camelids (Lama glama and Vicugna vicugna) in Argentina. J. of Parasitol. 85: Cafrune, M.M.; Aguirre, D.H. and Rickard, L.G First report of Lamanema chavezi (Nematoda: Trichostrongyloidea) in llamas (Lama glama) from Argentina. Vet. Parasitol. 97: Cafrune, M.M.; Aguirre, D.H. y Freytes, I Fasciolosis en vicuñas (Vicugna vicugna) en semi-cautiverio de Molinos, Salta, Argentina, con notas de otros helmintos en este hospedador. Vet. Arg. 21:

46 South American Camelids in Argentina. History, Use and Animal Health. Cafrune, M.M.; Marín, R.E. y Aguirre, D.H. 2006a. Hallazgo de Camelostrongylus mentulatus (Nematoda: Trichostrongyloidea) en una llama (Lama glama) de Jujuy, Argentina. 4º Cong. Mundial Camélidos. Argentina. Res: Cafrune. M.M.; Marín, R.E.; Auad, G.T.; Aguirre, D. H. 2006b. Coprología parasitaria en llamas (Lama glama) de la Puna de Jujuy, Argentina. 4º Cong. Mundial Camélidos. Argentina. Res:43. Cafrune; M.M.; Marín, R.E.; Rigalt, F.A.; Romero, S.R.; Aguirre, D.H Prevalence of Eimeria macusaniensis and E. ivitaensis in South American Camelids of Northwest Argentina. Vet. Parasitol. 162(3-4): Castro, J Sarcocystis auchenia en llamas (Lama glama). Rev. Inv. Pec. IVITA (Perú) 3: Castro, D.C. y Cicchino, A.C Anoplura. En: Biodiversidad de Artrópodos Argentinos. Una perspectiva biotaxonómica. Morrone y Coscarón (Dir). Ediciones Sur. La Plata. Argentina Cicchino, A.C.; Muñoz Cobeñas, M.E.; Bulman, G.E.; Díaz, J.C.; Laos, A Identification of Microthoracius mazzai (Phtiraptera: Anoplura) as economically important parasite of alpacas. J. Med. Entomol. 35: Cunazza, C Enfermedades y parásitos del guanaco. En: Raedeke, K. El guanaco de Magallanes. Distribución y biología. CONAF, Pub. Científica Nro. 4. Apéndice 1. Cunazza, C Extracción experimental de 150 guanacos en Tierra del Fuego, Chile. CONAF. Public. Técnica 6. Domínguez, E Características y Calidad de la Carne de Guanaco. Informe Dir. Sanidad y Fiscalización Animal. Min. Ind., Agric.y Ganad. Chubut. Argentina. 11pp. Estrada-Peña, A.; Venzal, J.M., Mangold, A.J.; Cafrune, M.M.; Guglielmone, A.A The Amblyomma maculatum Koch (Acari: Ixodidae: Ambliominae) tick group: diagnostic characters, description of the larvae of A. parvisatum, Neumann, 1901, 165 rdna sequencies, distribution and hosts. Syst. Parasitol. 60: Flores, M; Martínez, R.; Rivera, S Caracterización hematológica, bioquímica y parasitaria de guanacos (Lama guanicoe) en cautiverio: datos preliminares, Chubut (Patagonia Argentina). IV Congreso Mundial sobre Camélidos. Resúmenes: 75. Karesh, W.B.; Uhart, M.M.; Dierenfeld, E.S.; Braselton, W.E.; Torres, A.; House, C.; Puche, H.; Cook, R.A Health evaluation of free ranging guanaco (Lama guanicoe). J. Wildl. Dis. 29: Kühne, G.I Parásitos diagnosticados en el decenio en la Unidad Regional de Investigación en Sanidad Animal del Noroeste Argentino. I. Helmintos y protozoarios. Rev. Inv. Agrop. (INTA) 21: Larrieu, E.J., Bigatti, R.O.; Lukovich, R.; Eddi, C.; Bonazzi, E.; Gómez, E.; Niec, R.; Oporto, N.R Contribución al estudio del parasitismo gastrointestinal en guanacos (Lama guanicoe) y llamas (Lama glama). Gaceta Veterinaria 44: Larrieu, E.J., Bigatti, R.O.; Oporto, N.R Sanidad de los Camélidos en la Argentina. En: Estado actual de las investigaciones sobre Camélidos en la República Argentina. Cajal, J. y Amaya, J. (eds). SECYT. Argentina. pp Leguía, G.; Álvarez, H.; Náquira, F. y Beltrán, M Distomatosis hepática en el Perú. An. Sem. Zoon. Enf. Transm. Alim. Ministerio de Salud. Lima, Perú. 46

47 Chapter III: Animal Health in South American Camelids Leguía, G. 1991a. The epidemiology and economic impact of llama parasites. Parsitol. Today 7: Leguía, G. 1991b. Enfermedades Parasitarias. Capítulo IX. En: avances y perspectivas del conocimiento de los camélidos sudamericanos. Fernández Baca, S. (ed). Oficina Regional FAO para América Latina y el Caribe. Santiago, Chile. Leguía, G.; Casas, E. y Wheeler, J Parasitismo en camélidos prehispánicos. Parasitología al Día (Chile). 19:435. McKenna, P.B.; Hill, F.I.; Gillet, R Sarcoptes scabiei infection on an alpaca (Lama pacos). New Zeal. Vet. J. 53:213. Navone, G.T. y Merino, M.I Contribución al conocimiento de la fauna endoparasitaria de Lama guanicoe Muller, 1776, de Península Mitre, Tierra del Fuego, Argentina. Bol. Chil. Parasitol. 44: Olaechea, F.V and Abad, M An outbreak of fascioliasis in semicaptive guanacos (Lama guanicoe) in Patagonia (Argentina). First report. Proc. 20th Int. Conf. World Assoc. Adv. Vet. Parasitol. New Zealand. 4pp. Palacios, C.A.; Perales, R.A.; Chavera, A.E.; López, M.T.; Braga, W.U.; Moro, M Eimeria macusaniensis and Eimeria ivitaensis co-infection in fatal cases of diarrhoea in young alpacas (Lama pacos) in Perú. Vet.Rec. 158: Pidre, G.A.; Eguinoa, G.; Irribarren, F.E Sarcocystosis en llamas (Lama glama) en el norte argentino. Vet. Arg. 19: Raedeke, K El guanaco de Magallanes. Distribución y biología. CONAF, Pub. Científica Nro. 4. Robles, C.; von Thungen, J.; Cabrera, C.; Chodilef, M.; Odeón, R. y Parreño, V Aspectos sanitarios en majadas de guanacos en semi-cautividad en la Patagonia Argentina. IV Congreso Mundial sobre Camélidos. Resúmenes: 77. Rojas; M.; Lobato, I.; Montalvo, M Fauna parasitaria de camélidos sudamericanos y ovinos en pequeños rebaños mixtos familiares. Rev. Inv. Pec. IVITA. Perú. 6: Valencia, N. e Infantes, C Estudio de piojos en vicuñas (Vicugna vicugna) del zoocriadero Lachocc de la región de Huancavelica. Rev. Inv. Vet. Perú (1): Vélez, V.; Torres, J.; Díaz, G.; Leyva, V Primer reporte de infección transplacentaria en un embrión de alpaca (Vicugna pacos) con un microquiste compatible a Sarcocystidae (Protozoa: Apicomplexa: Sarcocystidae). IV Congreso Mundial sobre Camélidos. Resúmenes:

48