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Concept: Llama

27

This study describes placental morphology and immunolocalization of the placental pregnancy associated glycoprotein-like family (PAGs) identified in two selected taxa of Old-World camels of the Camelidae family: Camelus dromedarius (Cd) and Camelus bactrianus (Cb). Placental tissues of Cd from days 140-293 post-coitum (dpc), term (404 dpc); and of Cb from term (440 dpc) were examined. Histological staining (hematoxylin/eosin and propidium iodine) revealed the development of the placental structure, while chorionic folding increased the feto-placental surface during the progress of pregnancy. The camelid placenta during early pregnancy is similar to the diffuse epitheliochorial type, and during later stages of pregnancy resembles the synepitheliochorial (cotyledonary) type. Placental expression of the PAGs was detected (Alexa 488 - green) within camelid trophectoderm cells (TRD - chorionic epithelium as outer layer of embryonic cells) among all placental cells with nuclei stained by propidium iodide (red). The PAGs, identified in both Camelidae taxa, were named CbPAGs and CdPAGs. Placental CbPAG and CdPAG expression is restricted to the TRD cells, which are differentially developed throughout gestation. Cross-reactivity of polyvalent anti-pPAG polyclonals with the CbPAGs and CdPAGs revealed high structural similarities of the PAG-like epitopes in pigs and camels. This is the first study identifying PAG expression in chorionic cells of the camel placenta.

Concepts: Livestock, Llama, Camel, Staining dyes, Dromedary, Camelid, Camelids, Bactrian Camel

26

Raising of alpacas as exotic livestock for wool and meat production and as companion animals is growing in importance in the United States, Europe and Australia. Furthermore the alpaca, as well as the rest of the camelids, possesses the peculiarity of producing single-chain antibodies from which nanobodies can be generated. Nanobodies, due to their structural simplicity and reduced size, are very versatile in terms of manipulation and bio-therapeutic exploitation. In fact the biotech companies involved in nanobody production and application continue to grow in number and size. Hence, the development of reagents and tools to assist in the further growth of this new scientific and entrepreneurial reality is becoming a necessity. These are needed mainly to address alpaca disease diagnosis and prophylaxis, and to develop alpaca immunization strategies for nanobody generation. For instance an immortalized alpaca cell line would be extremely valuable. In the present work the first stabilized alpaca cell line from alpaca skin stromal cells (ASSCs) was generated and characterized. This cell line was shown to be suitable for replication of viruses bovine herpesvirus-1, bovine viral diarrhea virus and caprine herpesvirus-1 and the endocellular parasite Neospora caninum. Moreover ASSCs were easy to transfect and transduce by several methods. These two latter characteristics are extremely useful when recombinant antigens need to be produced in a host homologous system. This work could be considered as a starting point for the expansion of the biotechnologies linked to alpaca farming and industry.

Concepts: Antibody, DNA, Bacteria, Biotechnology, Cell culture, Meat, Alpaca, Llama

25

The mean retention times (MRT) of solute or particles in the gastrointestinal tract and the forestomach (FS) are crucial determinants of digestive physiology in herbivores. Besides ruminants, camelids are the only herbivores that have evolved rumination as an obligatory physiological process consisting of repeated mastication of large food particles, which requires a particle sorting mechanism in the FS. Differences between camelids and ruminants have hardly been investigated so far. In this study we measured MRTs of solute and differently sized particles (2, 10, and 20 mm) and the ratio of large-to-small particle MRT, i.e. the selectivity factors (SF10/2mm, SF20/2mm, SF20/10mm), in three camelid species: alpacas (Vicugna pacos), llamas (Llama glama), and Bactrian camels (Camelus bactrianus). The camelid data were compared with literature data from ruminants and non-ruminant foregut fermenters (NRFF). Camelids and ruminants both had higher SF10/2mmFS than NRFF, suggesting convergence in the function of the FS sorting mechanism in contrast to NRFF, in which such a sorting mechanism is absent. The SF20/10mmFS did not differ between ruminants and camelids, indicating that there is a particle size threshold of about 1 cm in both suborders above which particle retention is not increased. Camelids did not differ from ruminants in MRT2mmFS, MRTsoluteFS, and the ratio MRT2mmFS/MRTsoluteFS, but they were more similar to ‘cattle-’ than to ‘moose-type’ ruminants. Camelids had higher SF10/2mmFS and higher SF20/2mmFS than ruminants, indicating a potentially slower particle sorting in camelids than in ruminants, with larger particles being retained longer in relation to small particles.

Concepts: Alpaca, Llama, Camel, Dromedary, Camelid, Guanaco, Camelids, Vicuña

5

Large-scale ungulate migrations result in changes in prey availability for top predators and, as a consequence, can alter predator behavior. Migration may include entire populations of prey species, but often prey populations exhibit partial migration with some individuals remaining resident and others migrating. Interactions of migratory prey and predators have been documented in North America and some other parts of the world, but are poorly studied in South America. We examined the response of pumas (Puma concolor) to seasonal migration of guanacos (Lama guanicoe) in La Payunia Reserve in northern Patagonia Argentina, which is the site of the longest known ungulate migration in South America. More than 15,000 guanacos migrate seasonally in this landscape, and some guanacos also are resident year-round. We hypothesized that pumas would respond to the guanaco migration by consuming more alternative prey rather than migrating with guanacos because of the territoriality of pumas and availability of alternative prey throughout the year at this site. To determine whether pumas moved seasonally with the guanacos, we conducted camera trapping in the summer and winter range of guanacos across both seasons and estimated density of pumas with spatial mark-resight (SMR) models. Also, we analyzed puma scats to assess changes in prey consumption in response to guanaco migration. Density estimates of pumas did not change significantly in the winter and summer range of guanacos when guanacos migrated to and from these areas, indicating that pumas do not follow the migration of guanacos. Pumas also did not consume more alternative native prey or livestock when guanaco availability was lower, but rather fed primarily on guanacos and some alternative prey during all seasons. Alternative prey were most common in the diet during summer when guanacos also were abundant on the summer range. The response of pumas to the migration of guanacos differs from sites in the western North America where entire prey populations migrate and pumas migrate with their prey or switch to more abundant prey when their primary prey migrates.

Concepts: Predation, Human migration, North America, South America, Argentina, Chile, Llama, Patagonia

4

In South American societies, domesticated camelids were of great cultural importance and subject to trade and translocation. South American camelids were even found on remote and hard to reach islands, emphasizing their importance to historic and pre-historic South American populations. Isla Mocha, a volcanic island 35 km offshore of Central-South Chile, is an example of such an island. When Dutch and Spanish explorers reached the island in the early 17th century, they found that domesticated camelids called “chilihueque” played a major role in the island’s society. The origin and taxonomy of these enigmatic camelids is unclear and controversial. This study aims to resolve this controversy through genetic analyses of Isla Mocha camelid remains dating from pre-Columbian to early historic times. A recent archaeological excavation of site P21-3 on Isla Mocha yielded a number of camelid remains. Three complete mitochondrial genomes were successfully recovered and analysed. Phylogenetic analyses suggest that “chilihueque” was a local term for a domesticated guanaco. Results from phylogeographic analyses are consistent with Isla Mocha camelids being sourced from Southern Chilean guanaco populations. Our data highlights the capability of ancient DNA to answer questions about extinct populations which includes species identity, potential translocation events and origins of founding individuals.

Concepts: DNA, Alpaca, Chile, Llama, Archaeology, Camelid, Guanaco, Lama

4

Methane emissions from ruminant livestock have been intensively studied in order to reduce contribution to the greenhouse effect. Ruminants were found to produce more enteric methane than other mammalian herbivores. As camelids share some features of their digestive anatomy and physiology with ruminants, it has been proposed that they produce similar amounts of methane per unit of body mass. This is of special relevance for countrywide greenhouse gas budgets of countries that harbor large populations of camelids like Australia. However, hardly any quantitative methane emission measurements have been performed in camelids. In order to fill this gap, we carried out respiration chamber measurements with three camelid species (Vicugna pacos, Lama glama, Camelus bactrianus; n = 16 in total), all kept on a diet consisting of food produced from alfalfa only. The camelids produced less methane expressed on the basis of body mass (0.32±0.11 L kg-1 d-1) when compared to literature data on domestic ruminants fed on roughage diets (0.58±0.16 L kg-1 d-1). However, there was no significant difference between the two suborders when methane emission was expressed on the basis of digestible neutral detergent fiber intake (92.7±33.9 L kg-1 in camelids vs. 86.2±12.1 L kg-1 in ruminants). This implies that the pathways of methanogenesis forming part of the microbial digestion of fiber in the foregut are similar between the groups, and that the lower methane emission of camelids can be explained by their generally lower relative food intake. Our results suggest that the methane emission of Australia’s feral camels corresponds only to 1 to 2% of the methane amount produced by the countries' domestic ruminants and that calculations of greenhouse gas budgets of countries with large camelid populations based on equations developed for ruminants are generally overestimating the actual levels.

Concepts: Alpaca, Methane, Llama, Camel, Greenhouse gas, Dromedary, Camelid, Camelids

3

Wildlife reintroduction is an increasingly used strategy to reverse anthropocene defaunation. For the purpose of ecosystem restoration, in 2007 the guanaco (Lama guanicoe) was reintroduced to the Quebrada del Condorito National Park, situated in the mountains of central Argentina. With the aim of developing management recommendations, the project included permanently monitoring the population to evaluate its dynamics and the ecological response of the individuals released into the area. Nine years later and after two releases of guanacos (113 individuals in 2007 without and 25 in 2011 with a pre-adaptation period), only 24 individuals, which conform three reproductive groups, and one group of solitary males were settled in the Park. Here I modeled a population viability analysis to evaluate extinction risk, using VORTEX software. Initial population structure, specified age distribution, mortality and reproductive rates, and mate monopolization recorded during field work were used in the model, whereas the remaining used demographic parameters, such as age of first offspring, maximum number of broods per year, mean foaling rate, and length of fecundity period, were taken from the literature. Each of the three different scenarios (without supplementation of individuals, and with a realistic and optimistic supplementation) and two possible catastrophic events (fires and food shortage) covering 100 years was repeated 1000 times. Even though the guanaco reintroduction project can be considered to have been partially successful since its start, the model predicts that the current reintroduced population could be extinct in the next few decades if no reinforcements occur, and that only a continuous supplementation can reach the probability that the population survives over the next 100 years. I conclude that, so far, the current population is at a high risk of extinction if further supplementation of individuals is discontinued.

Concepts: Ecology, Argentina, Llama, Patagonia, Camelid, Reintroduction, Guanaco, Vicuña

2

Guanacos (Lama guanicoe) are large ungulates that have been valued by human populations in South America since the Late Pleistocene. Even though they were very abundant until the end of the 19th century (before the high deforestation rate of the last decades), guanacos have nearly disappeared in the Gran Chaco ecoregion, with relicts and isolated populations surviving in some areas, such as the shrubland area near the saline depressions of Córdoba province, Argentina. In this report, we present the first data from a locally endangered guanaco wild population, through the study of skeletal remains recovered in La Providencia ranch. Our results showed that most of the elements belonged to adults aged between 36 and 96 months; sex evaluation showed similar numbers of males and females. Statistical analysis of the body size of modern samples from Córdoba demonstrated that guanacos from the Chaco had large dimensions and presented lower size variability than the modern and archaeological specimens in our database. Moreover, they exhibited dimensions similar to those of modern guanacos from Patagonia and San Juan, and to archaeological specimens from Ongamira and Cerro Colorado, although further genetic studies are needed to corroborate a possible phylogenetic relationship. Finally, we used archaeozoological techniques to provide a first characterization of a relict guanaco population from the Chaco ecoregion, demonstrating its value to the study of modern skeletal remains and species conservation biology.

Concepts: Biology, Sociology, Argentina, Chile, Llama, Patagonia, Camelid, Guanaco

2

Recent advances in paleogenomic technologies have enabled an increasingly detailed understanding of the evolutionary relationships of now-extinct mammalian taxa. However, a number of enigmatic Quaternary species have never been characterized with molecular data, often because available fossils are rare or are found in environments that are not optimal for DNA preservation. Here, we analyze paleogenomic data extracted from bones attributed to the late Pleistocene western camel, Camelops cf. hesternus, a species that was distributed across central and western North America until its extinction ~13,000 years ago. Despite a modal sequence length of only ~35 base pairs (bp), we reconstructed high-coverage complete mitochondrial genomes and low-coverage partial nuclear genomes for each specimen. We find that Camelops is sister to African and Asian bactrian and dromedary camels, to the exclusion of South American camelids (llamas, guanacos, alpacas, and vicuñas). These results contradict previous morphology-based phylogenetic models for Camelops, which suggest instead a closer relationship between Camelops and the South American camelids. The molecular data imply a Late Miocene divergence of the Camelops clade from lineages that separately gave rise to the extant camels of Eurasia. Our results demonstrate the increasing capacity of modern paleogenomic methods to resolve evolutionary relationships among distantly related lineages.

Concepts: DNA, Alpaca, North America, Llama, Camel, Dromedary, Camelid, Camelids

1

Bactrian camel (Camelus bactrianus), dromedary (Camelus dromedarius) and alpaca (Vicugna pacos) are economically important livestock. Although the Bactrian camel and dromedary are large, typically arid-desert-adapted mammals, alpacas are adapted to plateaus. Here we present high-quality genome sequences of these three species. Our analysis reveals the demographic history of these species since the Tortonian Stage of the Miocene and uncovers a striking correlation between large fluctuations in population size and geological time boundaries. Comparative genomic analysis reveals complex features related to desert adaptations, including fat and water metabolism, stress responses to heat, aridity, intense ultraviolet radiation and choking dust. Transcriptomic analysis of Bactrian camels further reveals unique osmoregulation, osmoprotection and compensatory mechanisms for water reservation underpinned by high blood glucose levels. We hypothesize that these physiological mechanisms represent kidney evolutionary adaptations to the desert environment. This study advances our understanding of camelid evolution and the adaptation of camels to arid-desert environments.

Concepts: Alpaca, Livestock, Llama, Camel, Dromedary, Camelid, Camelids, Bactrian Camel