Gastrointestinal parasite diversity of South American camelids (Artiodactyla: Camelidae): First review throughout the native range of distribution

Abstract

In South America inhabit an endemic group of ungulates adapted to extreme environments: the South American camelids (SAC), a key component of the Andean biocultural heritage. Until today, SAC are the most important factor of Andean economies and social and ritual life. SAC include two wild species, the guanaco (Lama guanicoe) and the vicuña (Vicugna vicugna), and two domestic species, the llama (Lama glama) and the alpaca (Vicugna pacos). Endoparasitosis are one of the most common diseases in SAC, and have great economic and health relevance. Despite this, there is a lack of knowledge on this concern. The main objective of this work was to conduct the first systematic review of the diversity of gastrointestinal parasites of SAC throughout the entire native range of distribution and to identify several gaps in knowledge. The PRISMA protocol was performed and a total of 101 documents were summarized. At least 36 parasitic helminths and five Eimeria spp. were registered. This work highlights the need for a greater number of works to know with more certainty the parasitic fauna of camelids in the past and present, in order to achieve predictions that allow proper management of camelids for their future conservation. Furthermore, concerted research efforts are needed to understand the biology, epidemiology, diagnosis and distribution of the parasitosis of SAC along the entire distribution range to guide conservation decisions.

Graphical abstract

Highlights

• •Endoparasitosis are one of the most common diseases in SAC.
• •First review of parasites diversity of SAC throughout its total range of distribution.
• •At least 36 parasitic helminths and 5 Eimeria spp. were registered in camelids.
• •The registered parasites are mostly generalist parasites.
• •A better understanding of the extent and impact of parasites of SAC is needed.

1. Introduction

The South American camelids (SAC) (Artiodactyla, Camelidae) are a key component of the Andean biocultural heritage (Vilá and Arzamendia, 2020) and have occupied a central role in the development of Andean societies, both for ancient hunter-gatherers and for more recent pastoralists and farmers. SAC were the most important factor in Andean economies and social and ritual life throughout time. SAC include two wild species, the guanaco (Lama guanicoe) and the vicuña (Vicugna vicugna); and two domestic species, the llama (Lama glama) and the alpaca (Vicugna pacos) (Wheeler et al., 2006; Yacobaccio, 2021). This is an endemic group of ungulates adapted to extreme environments with a wide distributionin in arid and semiarid ecosystems from Argentina, Bolivia, Chile, Ecuador and Peru, mainly from 3000 to 5000 m.a.s.l. (Franklin, 2011). The original distribution of SAC includes the Andean high-altitude grasslands, the Altiplano and the Patagonian arid steppes (Vilá and Arzamendia, 2020). The distribution of guanacos includes a wide diversity of open habitats and temperate forest environments of Peru, Bolivia, Chile and Argentina, including Patagonian steppes. The distribution of vicuñas is limited to Northern Argentina, Chile, Peru and Bolivia, restricted to high-altitude Puna environments, above 3400 m.a.s.l. (Vilá, 2012). In pre-Hispanic times, llamas inhabit the Andean regions of Peru, Bolivia, Argentina and Chile and the alpacas were restricted to high and humid environments from the Puna of Peru, Bolivia and Chile (Yacobaccio, 2021). Under the dominion of the Incas (1470–1532), the llama distribution reached the southern Colombia and central Chile. There is no evidence of the presence of alpacas in pre-Columbian sites from Argentina (Olivera and Grant, 2009) and Ecuador (Miller and Gill, 1990) being introduced in these regions later.

Today, husbandry of SAC is an important socioeconomic activity for the Andean populations of South America. Recently, the breeding of domestic camelids also began to have great interest in other parts of the world. Numerous publications have been reported the relevance of parasites of SAC. Endoparasitosis are one of the most common diseases of SAC and have great economic and health relevance. Host-specific parasites and generalistic parasites shared with domestic ruminants such as sheep and goats are well known and have been widely described in the literature (e.g. Navone and Merino 1989; Leguia, 1991; Beldomenico et al., 2003; Aguirre and Cafrune, 2007; Arias-Pacheco et al., 2021). It is known that camelids are parasitized by gastrointestinal nematodes, trematodes and cestodes, and by coccidians, among other parasites. Many of them can cause serious diseases (Fowler, 2010) and can be transmitted to humans, including hydatidosis, fascioliasis, sarcocystosis and toxoplasmosis. The knowledgement of the diversity, spread, and evolution of parasites of SAC play a very important role in the understanding of the behavioral ecology, health, and camelids conservation. Despite this, there is a lack of knowledge about a global vision of gastrointestinal parasite diversity throughout the entire distribution range. The main objective of this work was to conduct the first systematic review of the diversity of gastrointestinal parasites of SAC throughout the native range of distribution and to identify several gaps in knowledge.

2. Materials and methods

The research was conducted using the systematic approach of the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) protocol guidelines (Shamseer et al., 2015).

2.1. Selection criteria

The literature used in this review included publications reporting on gastrointestinal parasites of SAC. The following list gives the criteria used in the selection of publications.

The inclusion criteria were:

• •Scientific peer-reviewed, scientific papers, conference proceedings and theses (PhD and MSc Thesis and Final Degree Projects) were included.
• •Literature published in English and Spanish-written in order to include research with local, regional and global impact.
• •Gastrointestinal parasite analysis of SAC in the natural range of distribution in order to conduct the first review in the subject and to identify gaps in knowledge.

The exclusion criteria were:

• •Research papers conducted in SAC from sites outside the natural range of distribution.
• •Research papers on topics other than gastrointestinal parasites of SAC.

2.2. Search strategy and data

2.2.1. Identification

The study was focused on gastrointestinal helminths and Eimeria spp., hereafter “parasites”. The literature research was carried out on internet through the Google Scholar platform (https://scholar.google.com), the PubMed platform (https://pubmed.ncbi.nlm.nih.gov), and the SciELO platform (https://scielo.org/es/). The following keywords were used for the research: “endoparasites”, “gastrointestinal”, “intestinal”, “parasites”, “helminths”, “camelids”, “South American Camelids”, “SAC”, “endoparásitos”, “parásitos”, “intestinales”, gastrointestinales”, “helmintos”, “camélidos”, “camélidos sudamericanos”, “CSA”, “guanaco”, “Lama”, “Vicugna”, “guanicoe”, “pacos”, “glama”, “llama”, “alpaca”, “vicuña”, “Eimeria”, “Coccidia”. The search rule used in English was (endoparasites OR gastrointestinal OR intestinal) AND (parasites OR helminths OR Eimeria OR coccidia) AND (camelids OR South American camelids OR SAC OR guanaco OR vicuña OR llama OR alpaca OR Lama OR Vicugna) AND (guanicoe OR glama OR vicugna OR pacos). The search rule used in Spanish was (endoparásitos OR parásitos OR helmintos OR Eimeria) AND (intestinales OR gastrointestinales) AND (camélidos OR camélidos sudamericanos OR CSA OR guanaco OR vicuña OR llama OR alpaca OR Lama OR Vicugna) AND (guanicoe OR glama OR vicugna OR pacos). The search was conducted in titles, abstracts and keywords in the above-cited databases, following the selection criteria. The snowball effect in the reference lists was used to increase the scope of the search. The initial search process generated 3960 academic papers from Google Scholar, and additional 285 papers from PubMed and 18 papers from SciELO. The publication retrieval from Google Scholar was scaled down to 237 after removing all parasite papers that did not represent the objective of this review. A flowchart of the PRISMA phases of the search is presented in Fig. 1.

Fig. 1.

PRISMA flowchart of the systematic review process.

2.2.2. Screening

After the initial search and paper retrieval, 540 academic papers were collected. After removing duplicate information, 482 publications remained. Subsequently, the generated papers were screened by applying the inclusion and exclusion criteria. A total of 98 academic papers were included for quality assessment.

2.2.3. Eligibility

The studies identified after applying the inclusion and exclusion criteria underwent further evaluation to ensure the quality of the research articles. The theses that contained only information published in scientific journals were eliminated. In total, 3 theses were excluded.

2.2.4. Included papers

A total of 95 publications were included in this review. From all reviewed documents, were extracted data regarding geographic location (country and region), number of samples evaluated, number of positive samples, taxa and prevalence of parasites reported, remarks (type of sample, animal characteristics, study remarks) and type of publication, being the data extraction performed by one author with verification by another, as the PRISMA protocol suggest (Shamseer et al., 2015).

3. Results

The present review includes documents from the period between 1963 and 2022. The information was retrieved from 95 publications and 6 more citations were added (there was no access to the original work), which makes a final number of 101 publications. A total of 74 scientific researchs, 27 theses (PhD and MSc Thesis and Final Degree Projects), four abstracts of scientific meetings and one FAO project were recopiled. The name of parasites was included exactly as reported in the retrieved publications.

The documents summarized belong to five countries (Argentina, Bolivia, Chile, Peru and Ecuador), with the alpaca being the most studied species of SAC, (49.5% of the total documents), followed by the guanaco (23.8%) and finally the llama and vicuña (both 18.8%). The geographical location of the documents summarized is shown in Fig. 2. The map was elaborated with the Google Earth platform.

Fig. 2.

Geographical location of the documents compiled in the present review (red dots). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

The reports of parasites of alpacas are summarized in Table 1. The 80% of the documents refer to alpacas from Peru, 12% from Ecuador, 4% from Chile and 4% from Bolivia. The reports of parasites of llamas are summarized in Table 2. The 47.4% of the recopiled documents belong to Argentina, 21% to Peru, 15.8% to Chile, 10.5% to Ecuador and 5.3% belong to Bolivia. The Table 3 summarized the recopiled documents of parasites of vicuñas. The 42.1% of the documents refer to vicuñas from Peru, 31.6% from Argentina and 21% from Bolivia and only one document refers to vicuñas from Ecuador (5.3%). The reports of parasites of guanacos are summarized in Table 4. Most of the recopiled documents belong to Argentina (83.33%), while documents from Chile and Peru represent both 8.33%. The data collected throught the entire native range of SAC distribution displayed that the highest species richness of gastrointestinal parasites are found in southern Peru, western Bolivia and central Patagonia. It is important to highlight that this data was elaborated from the information available to date. The parasitic richness found in SAC compiled from the information extracted is represented in Fig. 3.

Table 1.

Gastrointestinal helminths and Eimeria spp. reported in alpacas (Lama pacos) across the entire nature distribution range. (* Calculated with published data, NR: no reported).

Country	Region	No. tested samples	No. positive (%)	Reported parasites (%)	Remarks	Type of publication	Reference
Chile	Valdivia	47	NR	Nematodirus spathiger	Rectal samples	Scientific research	Valenzuela et al. (1998)
				Nematodirus filicolis
				Ostertagia sp.
				Trichostrongylus sp.
				Cooperia sp.
				Strongylida
				Trichuris sp.
				Capillaria sp.
	Arica-Parinacota	494	52 (10.53)	Fasciola hepatica	Rectal samples Only Fasciola study	Scientific meeting	Zamorano et al. (2012)
Bolivia	La Paz	22	(59.1)	Fasciola hepatica	Only abstract access	Scientific research	Ueno et al. (1975)
	La Paz	55	54 (98.0)	Eimeria punoensis (67.37)*	Fecal samples	Scientific research	Beltrán-Saavedra et al. (2014)
				Eimeria alpacae (16.36)*
				Eimeria macusaniensis (12.72)*
				Marshallagia sp. (47.27)*
				Lamanema spp. (5.45)*
				Nematodirus spp. (69.09)*
				Strongylida (52.72)*
				Capillaria sp. (25.45)*
				Trichuris sp. (36.36)*
				Moniezia expansa (5.45)*
				Moniezia benedeni (10.90)*
				Fasciola sp. (1.81)*
Peru	NR	NR	NR	Lamanema chavezi	Only abstract access	Scientific research	Becklund (1963)
				Nematodirus lamae
	Cuzco and Puno	12	NR	Eimeria lamae	Rectal samples	Scientific research	Guerrero (1967)
				Eimeria alpacae	First description
				Eimeria punoensis	Only Eimeria study
	Puno	NR	NR	Haemonchus sp.	No access to original document	Scientific research	Guerrero Diaz (1970) (in Navone and Merino, 1989)
				Ostertagia sp.
				Trichostrongylus sp.
				Cooperia sp.
				Nematodirus sp.
				Oesophagostomum sp.
				Chabertia sp.
				Trichuris sp.
				Graphinema sp.
				Lamanema sp.
				Mazamastrongylus (Spiculopteragia) sp.
				Camelostrongylus sp.
				Dictyocaulus sp.
				Fasciola sp.
				Moniezia sp.
				Eimeria sp.
	Puno	NR	NR	Eimeria lamae	Fecal samples	Scientific research	Guerrero et al. (1971)
				Eimeria alpacae	First report E. macusaniensis
				Eimeria punoensis	Only Eimeria study
				Eimeria macusaniensis
	Junín	NR	NR	Eimeria ivitaensis	Rectal samples	Scientific research	Leguía and Casas (1998)
					First description
					Only Eimeria study
	Junín	280	NR	Fasciola hepatica (7.1)	Fecal samples	Scientific research	Neyra et al. (2002)
				Trichuris sp. (40.0)
				Nematodirus sp. (34.6)
				Lamanema sp. (12.8)
				Eimeria sp. (11.8)
	Cuzco	7	NR	Eimeria lamae	Necropsy	Scientific research	Palacios et al. (2004)
				Eimeria macusaniensis	Dead animals with clinical signs of diarrhea
				Eimeria ivitaensis	Only Eimeria study
	Cuzco	48	11 (23.0)	Eimeria macusaniensis	Intestinal samples	Scientific research	Palacios et al. (2005)
				Eimeria lamae	Dead animals with diarrhea
				Eimeria punoensis	Only Eimeria study
				Eimeria alpacae
	NR	40	12	Fasciola hepatica	Fecal samples	Scientific research	Li et al. (2005)
					ELISA method
					Only Fasciola study
	Cuzco	NR	NR	Eimeria macusaniensis	Histopathological examination	Scientific research	Palacios et al. (2006)
				Eimeria ivitaensis	Only Eimeria study
	Ayacucho	10	(100)	Fasciola hepatica	Fecal and blood samples	Scientific research	Ciprián (2007)
					Necropsy
					Only Fasciola study
	Puno	NR	(3.03)	Coccidia (25.44)	Necropsy	Scientific research	Paredes et al. (2009)
				Vermes (10.52)
				Dictyocaulus sp. (0.88)
	Puno and Cuzco	108	33 (30.55)	Eimeria macusaniensis	Intestinal samples	Scientific research	Rosadio et al. (2010)
	South of Peru	316	NR	Eimeria macusaniensis (56.5)	Only Eimeria study	Scientific research	Cordero et al. (2011) (in Dubey, 2018)
	Puno	60	NR	Strongylus sp.	Rectal samples	Scientific research	Marino (2011)
				Nematodirus sp.
				Nematodirus lamae
				Lamanema chavezi
	Huancavelica	161	NR	Eimeria spp. (31.37)	Fecal samples	Scientific research	Rosadio et al. (2012)
				Eimeria macusaniensis (4.3)	Adults
	Puno	478	418 (87.5)	Eimeria lamae (60.4)	Fecal samples	Scientific research	Rodríguez et al. (2012)
				Eimeria alpacae (45.6)	Only Eimeria study
				Eimeria punoensis (30.0)
				Eimeria macusaniensis (50.4)
				Eimeria ivitaensis (6.24)
Cuzco	30	NR	Eimeria lamae	Fecal samples	Thesis	Mamani (2012)
			Eimeria alpacae
			Eimeria punoensis
			Eimeria macusaniensis
			Eimeria ivitaensis
			Nematodirus spathiger
			Nematodirus lamae
			Lamanema chavezi
			Trichuris spp.
			Capillaria spp.
			Strongylida
Huancavelica	366	(59.02)	Eimeria spp.	Rectal samples	Thesis	Auris Bellido and Santiago Cahuana (2013)
				Young animals with diarrhea
Cuzco	1001	Helminthes (68.4)	Nematodirus (54.0)	Rectal samples	Scientific research	Pérez et al. (2014)
		Eimeria spp. (61.5)	Strongylida (16.3)
			Trichuris (17.5)
			Capillaria (5.1)
			Lamanema (4.5)
			Moniezia (6.3)
			Eimeria alpacae (42.0)
			Eimeria punoensis (31.0)
			Eimeria lamae (20.0)
			Eimeria macusaniensis (7.0)
			Cooperia (40.0)
			Ostertagia (22.0)
			Trichostrongylus (20.0)
			Oesophagostomum (16.0)
			Bunostomum (2.0)
Junín, Jauja	103	(73.8)	Fasciola hepatica	Rectal samples	Scientific research	Flores et al. (2014)
				Only Fasciola study
Puno	1319	(63.9)	Nematodirus spp. (52.8)	Rectal samples	Scientific research	Contreras et al. (2014)
			Strongylida (4.9)
			Trichuris spp. (10.8)
			Capillaria spp. (1.8)
			Lamanema spp. (0.7)
			Moniezia spp. (9.6)
			Cooperia spp. (37.0)
			Oesophagostomum spp. (23.0)
			Trichostrongylus spp. (20.0)
			Ostertagia spp. (14.0)
			Bunostomum spp. (3.0)
			Haemonchus spp. (3.0)
Cajamarca	10	9 (90.0)	Nematodirus sp. (70.0)	Necropsy	Thesis	Roncal Narváez (2014)
			Bunostomum sp. (50.0)	Sacrificed alpacas from slaughterhouse
			Trichuris sp. (40.0)
			Moniezia sp. (30.0)
			Ostertagia sp. (30.0)
			Trichostrongylus sp. (20.0)
Cajamarca	151	20 (13.25)	Fasciola hepatica	Rectal samples	Thesis	López Mejía (2014)
				Only Fasciola study
Puno	369	(54.20)	Nematodirus lamae	Rectal samples	Thesis	Farfán (2014)
			Lamanema chavezi
			Trichostrongylus
			Trichuris sp.
			Moniezia benedeni
			Moniezia expansa
Puno	20	NR	Lamanema chavezi	Rectal samples and intestinal segments	Scientific research	Angulo et al. (2015)
				Redescription
				Only Lamanema study
Puno	51	14 (27.5)	Eimeria spp.	Necropsy	Abstract of Scientific meeting	Díaz et al. (2015)
				Intestinal samples
Puno	30	NR	Eimeria punoensis	Rectal samples and necropsy	Thesis	Quina Quina (2015)
			Eimeria lamae
			Eimeria macusaniensis
			Eimeria alpacae
			Eimeria ivitaensis
			Strongylus sp.
			Nematodirus spp.
			Nematodirus spathiger
			Nematodirus lamae
			Trichuris sp.
			Lamanema chavezi
			Capillaria sp.
			Moniezia benedeni
			Moniezia expansa
Puno	350	224 (64.3)	Eimeria lamae	Fecal samples from unweaned alpacas	Scientific research	Díaz et al. (2016)
			Eimeria alpacae	Only Eimeria study
			Eimeria punoensis
			Eimeria macusaniensis
			Eimeria ivitaensis
Pasco	160	NR	Strongylida (28.1)	Rectal samples	Scientific research	Masson et al. (2016)
			Eimeria ivitaensis (6.9)
			Eimeria macusaniensis (41.9)
			Nematodirus spp. (26.3)
			Trichuris sp. (20.0)
			Capillaria sp. (5.0)
			Lamanema chavezi (3.8)
			Cooperia spp.
			Oesophagostomum spp.
			Teladorsagia circumcincta
			Ostertagia ostertagi
			Trichostrongylus spp.
Pasco and Junín	60	(73.3)	Eimeria spp. (43.3)	Rectal samples and necropsy	Scientific research	Lucas et al. (2016)
			Eimeria alpacae	Dead calves with diarrhea
			Eimeria macusaniensis
			Eimeria lamae
			Nematodirus sp. (40.0)
			Strongylida (18.3)
			Trichuris sp. (1.6)
Puno	1319	(52.4)	Eimeria alpacae (31.5)	Rectal samples	Scientific research	Camareno et al. (2016)
			Eimeria lamae (2.3)	Only Eimeria study
			Eimeria punoensis (66.2)
			Eimeria macusaniensis (8.7)
			Eimeria ivitaensis (0.7)
Huancavelica	190	(81.88)	Eimeria macusaniensis	Rectal samples	Thesis	Lizana Hilario (2016)
Puno	45	NR	Eimeria spp.	Intestinal sample	Thesis	Chirinos (2017)
Arequipa, Tacna	346	(69.65)	Nematodirus spp. (46.53)	Rectal samples	Thesis	Torres Huacani (2017)
			Trichuris spp. (15.61)
			Capillaria spp. (13.01)
			Lamanema chavezi (1.45)
			Strongylida (4.34)
			Moniezia expansa (6.65)
			Eimeria spp. (45.66)
Pasco	238	51 (21.43)	Nematodirus sp.	Rectal samples	Thesis	Puicón (2018)
	178	7 (3.93)	Trichuris sp.
			Trichostrongylus colubriformis
			Teladorsagia circumcincta
			Oesophagostomum columbianum
Huancavelica	260	119 (45.8*)	Lamanema chavezi	Necropsy	Thesis	Gómez Escobar and Mallqui Saravia (2018)
Puno	92	NR	Strongylus spp.	Rectal samples	Thesis	Quispe Pino (2019)
			Nematodirus spp.
			Lamanema sp.
			Trichuris sp.
Arequipa	288	NR	Eimeria spp. (60.4)	Rectal samples	Scientific research	Frezzato et al. (2020)
			Eimeria macusaniensis (18.8)
			Trichuris spp. (5.6)
			Capillaria spp. (3.5)
			Moniezia spp. (3.5)
			Nematodirus/Marshallagia spp. (2.1)
			Strongylida (1.4)
Cuzco	78	68 (87.18)	Eimeria lamae (85.90)	Rectal samples	Scientific research	Gómez-Puerta et al. (2021)
			Eimeria punoensis (62.82)	Only Eimeria study
			Eimeria alpacae (53.85)
			Eimeria macusaniensis (41.03)
			Eimeria ivitaensis (5.13)
Ecuador	Imbabura	40	NR	Eimeria sp. (67.50)	Rectal samples	Thesis	Fierro Obregón (2010)
				Trichostrongylus sp. (35.0)
				Cooperia (32.5)
				Marshallagia sp. (5.0)
				Nematodirus sp. (12.50)
				Trichuris sp. (12.50)
	Cotopaxi and Pichincha	406	NR	Nematodirus spp. (45.5)	Rectal simples	Scientific research	Salazar et al. (2014)
				Bunostomum spp. (39.4)
				Haemonchus spp. (27.5)
				Cooperia spp. (14.5)
				Ostertagia spp. (13.7)
				Trichuris spp. (12.6)
				Marshallagia spp. (6.1)
				Strongyloides spp. (5.1)
				Moniezia benedeni (5.9)
				Moniezia expansa (4.4)
				Eimeria lamae (18.2)
				Eimeria macusaniensis (5.1)
	Pichicha	201	147 (73.0)	Haemonchus spp. (77.9)	Rectal samples	Thesis	Salazar Robayo (2015)
				Nematodirus spp. (77.6)
				Trichostrongylus spp. (77)
				Bunostomum spp. (69.9)
				Cooperia spp. (55.8)
				Ostertagia spp. (50.4)
				Oesophagostomum spp.(45.1)
				Capillaria spp. (34.5)
				Trichuris spp. (29.2)
				Marshallagia spp. (25.6)
				Lamanema spp. (22.1)
				Strongyloides spp. (18.6)
				Strongylus spp. (0.9)
				Eimeria spp. (70.7)
				Eimeria macusaniensis (29.3)
				Moniezia expansa (19.4)
				Moniezia benedeni (80.6)
	Cotopaxi	114	114 (100.0)	Marshallagia spp. (9.6)	Rectal samples	Thesis	Condor Tapia (2015)
				Nematodirus spp. (42.1)
				Strongylus spp. (14.9)
				Trichostrongylus spp. (28.9)
				Haemonchus spp. (13.2)
				Ostertagia spp. (8.8)
				Oesophagostomum spp. (9.6)
				Bunostomum spp. (0.9)
				Trichuris spp. (23.7)
				Cooperia spp. (10.5)
				Toxocara spp. (13.2)
				Capillaria spp. (7.9)
	Cotopaxi	204	(71.0)	Nematodirus spp. (89.0)	Rectal samples	Thesis	Regalado Valdivieso (2015)
				Bunostomum spp. (78.0)
				Haemonchus spp. (43.0)
				Capillaria spp. (31.0)
				Trichostrongylus spp. (31.0)
				Oesophagostomum spp. (28.0)
				Lamanema chavezi (27.0)
				Trichuris spp. (27.0)
				Ostertagia spp. (26.0)
				Cooperia spp. (20.0)
				Marshallagia spp. (20.0)
				Strongyloides spp. (10.0)
				Strongylida (2.0)
				Eimeria spp. (81.0)
				Eimeria macusaniensis (25.0)
				Moniezia benedeni (61.0)
				Moniezia expansa (41.0)
Cotopaxi	80	NR	Ostertagia sp. (29.37)	Rectal samples	Thesis	Panchi Lema (2021)
			Nematodirus sp. (24.56)
			Trichostrongylus sp. (5.79)
			Haemonchus sp. (9.06)
			Strongyloides sp. (18.89)
			Trichuris tenuis (12.99)
			Coccidia (83.75)

Table 2.

Gastrointestinal helminths and Eimeria spp. reported in llamas (Lama glama) across the entire nature distribution range. (* Calculated with published data, NR: no reported).

Country	Region	No. tested samples	No. positive (%)	Reported parasites (%)	Remarks	Type of publication	Reference
Argentina	Jujuy	15	15 (100.0)	Fasciola hepatica	Fecal samples	Scientific research	Cafrune et al. (1996a)
					Only Fasciola study
	Jujuy	37	35 (95.0)*	Trichuris tenuis	Fecal samples and Necropsy	Scientific research	Cafrune et al. (1999)
					Only Trichuris study
	Salta	2	2 (100.0)	Lamanema chavezi (100)*	Fecal samples and one Necropsy.	Scientific research	Cafrune et al. (2001)
				Trichuris tenuis (50.0)*	Farm llamas
				Trichostrongylus spp. (50.0)*
				Cooperia spp. (50.0)*
				Nematodirus spp. (50.0)*
	Jujuy	708	131 (18.5)	Lamanema chavezi (13.9)	Rectal samples	Scientific research	Cafrune et al. (2009a)
	Salta			(31.7)	Only Lamanema study
	Catamarca			(34.3)
	Jujuy	626	315 (50.3)	Eimeria ivitaensis (0.4)	Rectal samples	Scientific research	Cafrune et al. (2009b)
	Salta Catamarca			(0.0)	Only Eimeria study
				(2.0)
				Eimeria macusaniensis (48.7)
				(35.4)
				(65.0)
	Jujuy	430		Fasciola hepatica (21.6)	Fecal samples	FAO project	Marin et al. (2009)
				Lamanema chavezi (18.2)
				Trichuris sp. (70.5)
				Capillaria sp. (10.2)
				Nematodirus sp. (1.1)
				Strongyloides sp. (3.4)
				Strongylida (5.7)
				Cestoda (17.0)
				Eimeria spp. (64.8)
				Eimeria lamae
				Eimeria alpacae
				Eimeria punoensis
				Eimeria ivitaensis
				Eimeria macusaniensis
	Mendoza	2	2 (100.0)	Fasciola hepatica (100.0)	Fecal samples	Scientific research	Mera y Sierra et al. (2015)
				Nematodirus sp. (50.0)	Clinical signs of diarrhea
	Salta	NR	NR	Lamanema chavezi	Dead llama with gastrointestinal symptoms.	Scientific research	Petrigh et al. (2019)
					DNA analysis
	Catamarca	97	NR	Strongylida (1.0)	Rectal samples and necropsy	Thesis	Cardozo (2019)
		60		(18.9)	(+) indicates presence
				Trichuris sp. (15.50)
				(23.3)
				Toxocara sp. (72.30)
				(1.6)
				Lamanema chavezi (1.0)
				(18.3)
				Moniezia (+)
				Strongyloides papillosus
				(1.6)
				Nematodirus sp. (0.0)
				(11.6)
				Camelostrongylus sp. (0.0)
				(5.0)
				Eimeria lamae (4.1)
				(6.7)
				Eimeria alpacae (7.2)
				(26.7)
				Eimeria punoensis (15.5)
				(36.7)
				Eimeria macusaniensis (10.3)
				(28.3)
				Eimeria ivitaensis (3.1)
				(5.0)
				Fasciola hepatica (3.15)
				(2.6)
				Ostertagia sp. (100.0)
		+
		Trichostrongylus sp. (8.0)
		(15.0)
		Cooperia sp. (0.0)
		+
Chile	I Chile Region	150	NR	Camelostrongylus mentulatus (73.3)	Only abstract description	Scientific research	Alcaíno et al. (1991)
				Trichostrongylus axei (11.3)
				Ostertagia sp. (1.3)
				Graphinema aucheniae (1.3)
				Mazamastrongylus (Spiculopteragia) peruvianus (1.3)
				Lamanema chavezi (61.3)
				Nematodirus sp. (18.7)
				Trichuris ovis (66.7)
				Moniezia expansa (6.7)
	Araucanía, Temuco	45	NR	Strongylida	Fecal samples and field analysis	Scientific research	Müller (1998)
				Nematodirus sp.
				Ostertagia sp.
				Nematodirus spathiger
				Nematodirus filicolis
				Trichostrongylus sp.
				Cooperia sp.
	Los Ríos, Valdivia	32	(100.0)	Capillaria sp.	Rectal samples	Scientific meeting	Oyarzún-Ruiz et al. (2017)
				Eimeria sp.
				Eimeria macusaniensis
				Fasciola hepatica
				Moniezia sp.
				Trichuris sp.
				Nematodirus sp.
				Strongylida
Bolivia	Oruro, Potosí, La Paz and Cochabamba	33	NR	Lamanema chavezi (64.0)	Fecal samples and necropsy	Scientific research	Spörndly and Nissen (2008) (in Mamani, 2012)
				Nematodirus spathiger (55.0)
				Nematodirus lamae (12.0)
				Nematodirus abnormalis (15.0)
				Camelostrongylus mentulatus (33.0)
				Haemonchus contortus (15.0)
				Trichuris sp. (42.0)
				Graphinema aucheniae (12.0)
				Marshallagia occidentalis (6.0)
				Ostertagia ostertagi (12.0)
				Cooperia oncophora (9.0)
				Cooperia surnabada (3.0)
				Trichostrongylus colubriformis (6.0)
				Trichostrongylus vitrinus (3.0)
				Trichostrongylus probolurus (6.0)
				Skrjabinema sp. (3.0)
				Moniezia sp. (3.0)
				Fasciola hepatica (12.0)
				Eimeria spp. (82.0)
Peru	Cuzco	NR	NR	Eimeria lamae	Rectal samples Mother and brood	Thesis	Mamani (2012)
				Eimeria alpacae
				Eimeria punoensis
				Eimeria ivitaensis
				Eimeria macusaniensis
				Nematodirus spathiger
				Nematodirus lamae
				Lamanema chavezi
				Trichuris spp.
				Capillaria spp.
				Strongylida
	Huancavelica	155	145 (93.55)	Fasciola hepatica (9.7)	Necropsy	Thesis	Fuentes Ríos (2013)
				Haemonchus sp. (18.0)
				Trichostrongylus axei (18.7)
				Ostertagia sp. (36.8)*
				Graphinema sp. (15.5)*
				Camelostrongylus sp. (11.0)*
				Nematodirus sp. (83.22)*
				Lamanema chavezi (45.2)*
				Cooperia sp. (16.12)*
				Trichostrongylus c. (15.5)*
				Bunostomum sp. (6.45)*
				Moniezia sp. (10.32)*
				Oesophagostomum sp. (21.3)*
				Trichuris sp. (78.7)*
				Skrjabinema sp. (10.32)*
	Junín, Jauja	97	(49.5)	Fasciola hepatica	Rectal samples	Scientific research	Flores et al. (2014)
					Only Fasciola study
	Huancavelica	212	95 (44.8*)	Lamanema chavezi	Necropsy	Thesis	Gómez Escobar and Mallqui Saravia (2018)
Ecuador	Azuay, Sigsig	95	27 (28.4)	Strongylida	Fecal samples	Thesis	Zhiminaicela (2015)
				Trichuris sp.
				Bunostomum sp.
				Nematodirus sp.
				Coccidia
				Trichostrongylus sp.
	Chimborazo, Millmahuanchi	44	NR	Eimeria sp. (52.0)	Rectal samples	Thesis	Gavilanes Loja (2016)
				Strongyloides sp. (48.0)
				Nematodirus sp. (14.0)
				Trichostrongylus sp. (7.0)
				Trichuris sp. (7.0)
				Fasciola hepatica (9.0)

Table 3.

Gastrointestinal helminths and Eimeria spp. reported in vicuñas (Vicugna vicugna) across the entire distribution range. (* Calculated with published data, NR: no reported).

Country	Region	No. tested samples	No. positive (%)	Reported parasites (%)	Remarks	Type of publication	Reference
Argentina	Jujuy	187	30 (16.04)	Fasciola hepatica	Rectal samples	Scientific research	Cafrune et al., (1996b)
					Semi-captive
					Only Fasciola study
	Jujuy	69	45* (65.0)	Trichuris tenuis	Fecal samples	Scientific research	Cafrune et al. (1999)
					Semi-captive
					Only Trichuris study
	Jujuy	63	14 (22.2)	Eimeria macusaniensis	Rectal samples	Scientific research	Cafrune et al., (2009b)
	Salta	98	9 (9.2)		Semi-captive
					Only Eimeria study
	Jujuy	81 juveniles	81 (100.0)	Eimeria punoensis (100)	Rectal samples	Scientific research	Cafrune et al. (2014)
		154 adults	143 (92.8)	(89.6)	Captive
				Eimeria alpacae (85.1)	Only Eimeria study
				(66.8)
				Eimeria macusaniensis (82.7)
				(15.5)
				Eimeria lamae (48.1)
				(27.2)
				Eimeria ivitaensis (3.7)
				(1.2)
	Jujuy	150	NR	Strongylida (40.66)	Rectal samples	Scientific research	Marcoppido et al. (2016)
				Nematodirus sp. (4.66)	Wild
				Coccidia (7.33)
				Cestoda (0.66)
	Catamarca, Laguna Blanca	40	(2.5)	Capillaria sp.	Fecal samples	Thesis	Cardozo (2019)
				Haemonchus sp.
				Camelostrongylus sp.
				Eimeria spp. (7.5)
				Eimeria lamae
				Eimeria alpacae
				Eimeria punoensis
				Moniezia sp.
				Fasciola hepatica (12.5)
Bolivia	La Paz, Apolobamba	7 juveniles	7 (100.0)	Strongylida (28.6)	Rectal samples	Scientific research	Beltrán-Saavedra et al. (2011)
		25 adults	22 (88.0)	(56.0)	Wild
				Marshallagia sp.(71.4)
				(32.0)
				Lamanema spp. (42.9)
				(16.0)
				Nematodirus spp. (57.1)
				(28.0)
				Capillaria sp. (28.6)
				(0.0)
				Trichuris sp. (28.6)
				(44.0)
				Moniezia benedeni (14.3)
				(0.0)
				Eimeria punoensis (100.0)
				(80.0)
				Eimeria alpacae (100.0)
				(88.0)
				Eimeria lamae (42.9)
				(12.0)
				Eimeria macusaniensis (14.3)
				(8.0)
	La Paz, Apolobamba	54 fecal samples	(100.0)	Marshallagia sp.	Fecal and dump samples	Scientific meeting	Condori et al. (2012)
		8 dump samples		Nematodirus sp.	Wild
				Trichuris sp.
				Capillaria sp.
				Lamanema chavezi
				Moniezia benedeni
				Moniezia expansa
				Eimeria punoensis
				Eimeria alpacae
				Eimeria lamae
				Eimeria macusaniensis
				Cooperia oncophora
				Cooperia macmasteri
				Oesophagostomum columbianum
				Ostertagia circumcincta
				Trichostrongylus colubriformis
				Trichostrongylus axei
				Mazamastrongylus peruvianus
	Potosí, Tarija and Cochabamba	98	(73.5)	Trichuris spp. (32.7)*	Rectal samples	Thesis	Martela Mamani (2016)
				Lamanema chavezi (5.1)*	Semi-captive
				Marshallagia spp. (4.1)*
				Strongylida (30.61)*
				Capillaria spp. (1.02)*
				Moniezia benedeni (6.12)*
				Fasciola hepatica (1.02)*
				Eimeria punoensis (64.3)*
				Eimeria alpacae (42.9)*
				Eimeria peruviana (17.34)*
				Eimeria lamae (11.22)*
				Eimeria macusaniensis (1.02)*
	La Paz and Oruro	84	(98.6)	Marshallagia spp. (32.14)*	Rectal samples	Thesis	Ruiz Hurtado (2016)
				Lamanema spp. (1.2)*	Semi-captive
				Strongylida (38.1)*
				Nematodirus spp. (10.7)*
				Trichuris spp. (54.8)*
				Capillaria spp. (1.2)*
				Moniezia benedeni (3.6)*
				Eimeria punoensis (39.3)*
				Eimeria alpacae (40.5)*
Peru	Cuzco	NR	NR	Lamanema chavezi	First report	Scientific research	Becklund (1963)
				Nematodirus lamae	Host: llama and vicuña
					no access to original document
	Ayacucho, Pampa Galeras	39	15 (41.0)	Eimeria lamae	NR	Scientific research	Bouts et al. (2003)(in Dubey, 2018)
				Eimeria punoensis
	Tacna	120	(80.83)	Trichuris sp. (81.44)	Rectal samples	Thesis	Quispe García (2011)
				Strongylus sp. (20.62)	Semi-captive
				Nematodirus sp. (15.46)
				Capillaria sp. (11.34)
				Eimeria sp. (20.62)
	Huancavelica	80	(27.5)	Fasciola hepatica	Rectal and dump samples	Scientific research	Pizarro and Puray (2014)
					Only Fasciola study
	Junín, Paccha	143	(32.9)	Fasciola hepatica	Rectal samples	Scientific research	Samamé et al. (2016)
					Wild
					Only Fasciola study
	Cajamarca	208	NR	Strongylida (61.1)	Rectal samples	Thesis	Curay Cabanillas (2018)
				Nematodirus (39.4)	Semi-captive
				Trichuris (26.9)
				Capillaria (16.8)
				Moniezia (8.7)
				Cooperia (39.64)
				Trichostrongylus (20.76)
				Ostertagia (17.56)
				Oesophagostomum (12.88)
				Haemonchus (5.45)
				Bunostomum (3.99)
	Cuzco	147	High	Fasciola hepatica (2.0)	Rectal samples	Scientific research	Angulo-Tisoc et al. (2021)
			NR	Strongylida (42.1)	Wild and captive
				Nematodirus sp. (6.8)
				Nematodirus spathiger (26.5)
				Trichuris sp. (4.0)
				Eimeria spp. (85.0)
				Moniezia spp. (2.7)
	Cuzco	115	(84.4)	Strongylida (54.8)	Fecal samples	Scientific research	Arias-Pacheco et al. (2021)
				Nematodirus lamae (11.3)	Semi-captive
				Nematodirus spathiger (13.9)
				Trichuris spp. (9.6)
				Capillarid (2.6)
				Lamanema chavezi (13.0)
				Eimeria alpacae (23.5)
				Eimeria macusaniensis (34.8)
				Eimeria lamae (6.1)
				Eimeria punoensis (38.3)
				Trichostrongylus spp.
				Haemonchus spp.
				Cooperia spp.
				Teladorsagia spp.
				Oesophagostomum spp.
				Bunostomum phlebotomum
				Gaigeria pachyscelis
Ecuador	Bolívar, Tungurahua and Chimborazo	200	NR	Eimeria spp. (69.85)	Dump samples	Thesis	Chacaguasay Cepeda (2016)
				Helminthes (68.84)
				Larvae

Table 4.

Gastrointestinal helminths and Eimeria spp. reported in guanacos (Lama guanicoe) across the entire distribution range. (* Calculated with published data, NR: no reported).

Country	Region	No. tested samples	No. positive (%)	Parasites reported (%)	Remarks	Type of publication	Reference
Argentina	Río Negro	3	NR	Skrjabinema sp.	NR	Scientific research	Larrieu et al. (1982) (in González-Rivas et al., 2019)
				Trichuris ovis.
				Trichostrongylus sp.
				Trichostrongylus vitrinus
				Trichostrongylus axei
				Ostertagia ostertagi
				Nematodirus filicolis
				Nematodirus battus
				Nematodirus lanceolatus
				Nematodirus spathiger
				Cooperia oncophora
				Cooperia macmasteri
				Capillaria sp.
	Tierra del Fuego	58	NR	Haemonchus sp.	Fecal samples	Scientific research	Navone and Merino (1989)
				Nematodirus sp.
				Marshallagia sp.
				Ostertagia sp.
				Trichostrongylus sp.
				Oesophagostomum sp.
				Chabertia sp.
				Cooperia sp.
				Eimeria sp.
	Chubut	20	12 (60.0)*	Strongyloides sp. (5.0)*	Rectal samples	Scientific research	Karesh et al. (1998)
				Nematodirus sp. (30.0)*	Free-ranging
				Marshallagia sp. (10.0)*	Two animals in poor body conditions
				Trichostrongylus sp.(15.0)*
				Trichuris sp. (25.0)*
				Dictyocaulus sp.(5.0)*
	Chubut	12	NR	Eimeria spp. (83.3)*	Feces from necropsied animals	Scientific research	Beldoménico et al. (2003)
				Eimeria macusaniensis (75.0)*	Animals dead by starvation
				Nematodirus sp. (75.0)*	Wild
				Marshallagia sp. (66.6)*
				Trichuris sp. (8.33)*
				Dictyocaulus filaria
				Trichuris tenuis
				Moniezia expansa
	Mendoza and San Juan	35	NR	Eimeria sp.	Only access to abstract	Scientific research	Borghi et al. (2004) (in Dubey, 2018)
				Eimeria macusaniensis
	Mendoza	70	1 (1.4)	Fasciola hepatica	Fecal samples	Scientific research	Issia et al. (2007)
					First report
					Wild
					Only Fasciola study
	Neuquen, Río Negro and Chubut	NR	(84.2)	Fasciola hepatica	Rectal samples Semi-captive	Scientific research	Larroza and Olaechea (2008)
					Only Fasciola study
	Salta	4	1 (25.0)	Eimeria macusaniensis	Dung samples Semi-captive	Scientific research	Cafrune et al. (2009a)
					Only Eimeria study
	Salta	4	3 (75.0)	Lamanema chavezi	Dung samples Semi-captive	Scientific research	Cafrune et al. (2009b)
					Only Lamanema study
	Mendoza	224	(0.5)	Fasciola hepatica	Fecal samples	Scientific research	Issia et al. (2009)
					Wild
					Only Fasciola study
	Neuquén, Chubut and Río Negro	622	NR	Nematodirus spathiger	Necropsied animals	Scientific research	Olaechea et al. (2011)
				Nematodirus oriatianus	Semi-captive
				Nematodirus filicolis
				Nematodirus abnormalis
				Ostertagia ostertagi
				Ostertagia trifurcate
				Cooperia oncophora
				Trichostrongylus colubriformis
				Trichuris spp.
				Dictyocaulus spp.
				Moniezia spp.
				Eimeria macusaniensis
				Fasciola hepatica
Mendoza	75 rectal	NR	Eimeria sp.	Rectal and field samples	Scientific research	Moreno et al. (2013)
	600 field		Eimeria macusaniensis	Wild
			Nematodirus sp.
Mendoza	756	638 (84.4)*	Nematodirus spp.	Rectal samples	Scientific research	Moreno et al. (2015)
			Trichuris sp.	Wild
			Capillaria sp.
			Strongyloides sp.
			Moniezia benedeni
			Eimeria lamae
			Eimeria alpacae
			Eimeria punoensis
			Eimeria macusaniensis
			Eimeria ivitaensis
Mendoza	4	1 (25.0)*	Fasciola hepatica	Fecal samples	Scientific research	Mera y Sierra et al. (2015)
			Eimeria spp.	Semi-captive
				One dead with diarrhea
Santa Cruz	NR	NR	Nematodirus spathiger	Fecal samples	Scientific research	Petrigh and Fugassa (2014)
				Wild
				DNA analysis
				Only Nematodirus study
Santa Cruz	15	(77.0)	Nematodirus spp.(53.3)	Fecal samples	Thesis	Taglioretti (2015)
			Dictyocaulus sp.(6.7)*	Wild
			Strongylida (20.0)
Chubut	NR	NR	Lamanema chavezi	Fecal samples	Scientific research	Petrigh et al. (2019)
				Wild
				DNA analysis
				Only Lamanema study
San Juan	72	NR	Eimeria spp.	Fecal samples	Scientific research	González-Rivas et al. (2019)
			Eimeria macusaniensis	Wild
			Eimeria ivitaensis
			Nematodirus sp.
			Trichuris sp.
Santa Cruz	4	NR	Capillarid eggs	Dump samples	Scientific research	Velázquez et al. (2020)
				Wild
				Multi proxy analysis
Santa Cruz	10	10 (100.0)	Lamanema chavezi(100.0)	Necropsied animals	Scientific research	Santana et al. (2020)
			Nematodirus spp. (100.0)	Wild
			Capillaria spp. (60.0)
			Trichuris spp. (40.0)
			Coccidia (60.0)
Chile	Magallanes	NR	NR	Ostertagia sp.	NR	Scientific research	Cunazza (1982) (in Navone and Merino, 1998)
				Trichostrongylus sp.
				Nematodirus sp.
				Oesophagostomum sp.
				Trichuris sp.
				Eimeria sp.
	Magallanes	15	10 (66.7)	Eimeria macusaniensis (40.0)	Fecal samples Semi-captive	Scientific research	Correa et al. (2012)
				Nematodirus sp. (46.7)
				Strongylida (20.0)
Peru	Cuzco	NR	(72.0)	Strongylus spp. (75.0)	No access to original document	Scientific research	Hurtado et al. (1985)
				Lamanema chavezi (64.0)
				Trichuris ovis (22.0)
				Nematodirus spp. (14.0)
				Eimeria macusaniensis (28.0)
	Ayacucho	132	71 (53.8)	Strongylida (31.8)	Field samples	Scientific research	Castillo et al. (2008)
				Eimeria punoensis (21.2)	Wild
				Eimeria alpacae (13.6)
				Eimeria lamae (4.5)
				Eimeria macusaniensis (15.9)
				Trichuris sp. (8.3)
				Nematodirus sp. (1.5)
				Trichostrongylus sp.
				Cooperia sp.
				Ostertagia sp.
				Bunostomum sp.
				Mazamastrongylus peruvianus
				Graphinema aucheniae

Fig. 3.

Parasitic richness of South American camelid throught the native distribution range based on data available to date.

The gastrointestinal parasites of each of the four SAC species compiled are summarized in Table 5. At least 36 parasitic helminths were registered. Twenty two genera of the Phylum Nematoda have been reported among the four species of SAC. Seventeen genera belong to the Order Strongylida (including 28 taxa identified to the species level), one genus belong to the Order Ascaridida, one genus belong to the Order Oxyurida, one genus belong to the order Rhabditida and two genus belong to the Order Enoplida. Three genera of the Phylum Platyhelminthes were also reported. One of them belongs to Cestoda (with two identified species) and one species belong to Trematoda. Respects to Eimeria spp. (Apicomplexa), five species have been identified. The prevalence of the reported parasitic infestations in many cases was 100% (Table 1, Table 2, Table 3, Table 4). This review displays that there is no one species more prevalent than another, but rather that the prevalence varies in each of the studies.

Table 5.

Review of gastrointestinal parasites of South American Camelids.

Parasite species	Alpacas	Llamas	Vicuñas	Guanacos
NEMATODA
STRONGYLIDA/ANCYLOSTOMATIDAE
Bunostomum sp.	+	+	+	+
Bunostomum phlebotomum			+
STRONGYLIDA/MOLINEIDAE
Lamanema sp.	+	+	+	+
Lamanema chavezi	+	+	+	+
Nematodirus spp.	+	+	+	+
Nematodirus spathiger	+	+	+	+
Nematodirus filicolis	+	+		+
Nematodirus abnormalis		+		+
Nematodirus battus				+
Nematodirus lanceolatus				+
Nematodirus oriatianus				+
Nematodirus lamae	+	+	+
STRONGYLIDA/TRICHOSTRONGYLIDAE
Camelostrongylus sp.	+	+	+
Camelostrongylus mentulatus		+
Cooperia sp.	+	+	+	+
Cooperia oncophora		+	+	+
Cooperia surnabada		+
Cooperia mcmasteri			+	+
Graphinema sp.	+	+
Graphinema aucheniae		+		+
Haemonchus sp.	+	+	+	+
Haemonchus contortus		+
Marshallagia sp.	+	+	+	+
Marshallagia occidentalis		+
Mazamastrongylus (Spiculopteragia) peruvianus	+	+	+	+
Ostertagia sp.	+	+	+	+
Ostertagia ostertagi	+	+		+
Ostertagia circumcincta			+
Ostertagia trifurcate				+
Teladorsagia spp.			+
Telodorsagia circumcincta	+
Trichostrongylus sp.	+	+	+	+
Trichostrongylus colubriformis	+	+	+	+
Trichostrongylus axei		+	+	+
Trichostrongylus vitrinus		+		+
Trichostrongylus probolurus		+
STRONGYLIDA/CHABERTIDAE
Chabertia sp.	+
Oesophagostomum sp.	+	+	+	+
Oesophagostomum columbianum	+		+
STRONGYLIDA/DICTYOCAULIDAE
Dictyocaulus sp.	+			+
Dictyocaulus filaria				+
Gaigeria pachyscelis			+
STRONGYLIDA/STRONGYLIDAE
Strongylus sp.	+		+
ASCARIDIDA/ASCARIDIDAE
Toxocara spp.	+	+
OXYURIDA/OXYURIDAE
Skrjabinema sp.		+		+
RHABDITIDA/STRONGYLOIDIDAE
Strongyloides spp.	+	+		+
Strongyloides papillosus		+
ENOPLIDA/TRICHURIDAE
Capillaria sp.	+	+	+	+
Trichuris sp.	+	+	+	+
Trichuris ovis		+		+
Trichuris tenuis		+	+	+
PLATYHELMINTHES
CESTODA
Moniezia sp.	+	+	+	+
Moniezia expansa	+	+	+	+
Moniezia benedeni	+		+	+
TREMATODA
Fasciola hepatica	+	+	+	+
APICOMPLEXA
Eimeria lamae	+	+	+	+
Eimeria alpacae	+	+	+	+
Eimeria punoensis	+	+	+	+
Eimeria macusaniensis	+	+	+	+
Eimeria ivitaensis	+	+	+	+
	36	44	36	42

4. Discussion

The present work is the first scientific review that provides detailed information about gastrointestinal parasite diversity of SAC throughout the entire native distribution range, encompassing a large number of documents. The records summarized here comprise documents dating from 1963 to 2022, with an increase in the last 10 years, whenever a wide production of scientific publications and graduate and postgraduate theses were produced. This point can be explained by the growing interest in recent years for SAC conservation and, in the other hand, for the economic interest on SAC around the world. The recopilated documents are focused mainly in gastrointestinal parasites studies from fecal samples or from necropsied animals, by microscopic techniques mostly. This implies that in many occasions it is not possible to identify the species. Molecular studies on camelid parasites are scarce. Although 101 works were recopilated, results highlight that a large number of the documents summarized are not published in indexed journals and are not easily accessible to a wider audience.

The highest species richness of gastrointestinal parasites was found in southern Peru, western Bolivia and central Patagonia. This agrees with the regions with the highest population of SAC and with the regions where more studies have been carried out. The important population of Peru explain that this country produced a great number of the available knowledge. However, it is mainly focused on alpaca. Numerous studies considered that latitude is one of the main factors correlated to parasite diversity and richness. Parasite diversity is expected to decrease in high latitude areas as result of lack of intermediate hosts or high mortality rates due to harsh conditions in winter (Krasnov et al., 2004; Lindenfors et al., 2007; Bordes et al., 2010; Poulin and Leung, 2011). The data on parasitic richness of SAC summarized in this paper so far do not allow us to observe a decrease pattern in their distribution throughout their extensive distribution. However, the parasite diversity display in this review should be taken with caution as it is subject to the number and type of samples analyzed in each region. So far, all parasite genera appear to be represented throughout the distribution range.

Most wild and domestic ungulate species have few host-specific parasites, which make up less than half of the total number of nematode parasite species found in a given host; and mostly have generalist parasites (Walker and Morgan, 2014). Across vast areas, SAC coexist with domestic herbivores such as sheep, goat and cattle. Furthermore, domestic SAC coexist with human populations. This proximity facilitates the exchange of parasites between domestic and wild animals and humans. Walker and Morgan (2014) found that domestic camelids (llamas and alpacas) have a high liability index (the degree to which a host species is vulnerable to infection with generalist parasites), with a value of 0.77. This index is designed to range from −1 (entirely host-specific parasites) to 1 (entirely parasites shared with the other group). This result displays that llamas and alpacas have mostly generalist species. In the present study, 22 genera of nematodes were reported, with at least 33 species. Of all of them, only five are known as SAC-specific nematodes: Trichuris tenuis, Graphinema aucheniae, Camelostrongylus mentulatus, Nematodirus lamae, and Lamanema chavezi. Most of the registered parasites in this review are generalist parasites, and are shared with domestic ungulates and wildlife species, such as Ostertagia spp., Haemonchus contortus, Trichostrongylus spp., Cooperia spp., and Oesophagostomum. From a sanitary point of view, it would be important to know if host-specific parasites dominate the communities of their hosts and generalist parasites tend to occur at lower abundances, or vice versa (Zaffaroni et al., 2000). In this review, is clear that there is not enough data to compare the abundance of different nematode species within a host. Further studies of the contribution of shared parasite species to total parasite burden rather than only species richness would be a step toward understanding the impact that generalist parasites have on SAC. In the other hand, several studies have looked at nematodes of wild ungulates in relation to domestic species. In the present review, domestic SAC displayed to have the same genera of parasites than wild SAC.

SAC have also been described as hosts for parasites of zoonotic importance such as Fasciola hepatica. This trematode was found in wild and domestic camelids, from the north of its distribution to the north of Patagonia. It was generally assumed that entry of F. hepatica to America coincided with the first arrival of the Europeans and their associated livestock in the late 15th century. Throughout the 500 years since its introduction, the parasite gained new definitive hosts among native species. This trematode is now widespread in livestock and can be mapped across the whole South America and certain regions of North America. Nonetheless in Argentina, eggs of F. hepatica have been observed in deer and camelid coprolites dating back to 2300 years B.P., prior to the arrival of the European cattle in the 15th century (Beltrame et al., 2020; Tietze et al., 2021). This shows that the presence of Fasciola in camelids is not only due to its transmission by European cattle.

Cestodes found in SACs are ruminant-related anoplocephalid of the genus Moniezia, identified in the four camelids species in a wide variety of environments with records that go from the north of its distribution reaching as far as northern Patagonia. Parasites of Moniezia expansa were identify in all SACs species, while Moniezia benedeni were identify in vicuñas, alpacas and guanacos. In the case of llamas, findings of cestodes were scarce, and in general it was only possible to identify the genus. Recently, Moniezia eggs were also found in coprolites from the middle to late-Holocene from the Argentinian Puna, evidencing the presence of this genus in SAC prior the European cattle arrival (Tietze et al., 2021).

There are five common species of Eimeria in SAC: E. lamae, E. alpacae, E. punoensis, E. macusaniensis and E. ivitaensis (Dubey, 2018). All Eimeria spp. were recorded in wild and domestic camelids throughout its distribution range. The most prevalent Eimeria found in guanacos was E. macusaniensis, but in general the most prevalent in SAC was E. punoensis while the least prevalent was E. ivitaensis (Marin et al., 2009; Rodríguez et al., 2012; Cafrune et al., 2014; Moreno et al., 2015). Of the five Eimeria species registered in SAC, E. macusaniensis is considered the most pathogenic, clinical symptoms can develop even before oocysts are registered in the feces. The host specificity along with the characteristic morphology of its oocyst makes it an effective indicator when identifying the host in coprological studies (Dubey, 2018). The presence of E. macusaniensis is reported even in ancient samples from Argentina, Chile and Peru (Fugassa et al., 2008; Beltrame et al., 2010; Taglioretti et al., 2015; de Souza et al., 2018; Le Bailly et al., 2020; Tietze et al., 2021).

When studying the interactions between wildlife, livestock, and their parasites, it will be important to understand the historical context and patterns of contact and relatedness between the host species. A useful tool for this focus is the paleoparasitology. Paleoparasitological studies on SAC have shown the presence of diverse parasitic species in ancient times, which demonstrate the presence of some of them in prehistoric times, before the arrival of the European fauna, and others in more recent archaeological levels. Within the archaeological records were found Dictyocaulus sp., Fasciola hepatica, Lamanema chavezi, Moniezia sp., Nematodirus spathiger, Strongyloides sp., Trichuris sp. (e.g. Taglioretti et al., 2017; Petrigh et al., 2021; Tietze et al., 2021). If we are to make predictions of changes in host–parasite interactions due to, for example, climate or land use change, or to introduction of exotic species, it is necessary to have an exhaustive knowledge of the parasitic diversity of SAC throughout the time and throughout their entire distribution. Environmental changes can modify the epidemiological pattern of parasitic diseases, with impacts on the economy, public health, and/or wildlife conservation (Rhyan and Spraker, 2010). This work highlights the need for a greater number of works to know with more certainty the parasitic fauna of SAC in the past and present, in order to achieve predictions that allow proper management of camelids for their future conservation. Furthermore, concerted research efforts are needed to understand the biology, epidemiology, diagnosis and distribution of the parasitosis of SAC along the entire distribution range to guide conservation decisions.

5. Conclusions

In summary, this review presents the first compendium of studies of gastrointestinal parasites of SAC throughout the native range of distribution. This serves as a baseline for future studies focused on elucidating the role that parasites play on SAC and further epidemiological research. Clearly, a better understanding of the extent and impact of parasites on SAC, at both the individual and population levels, is needed. This shortfall in knowledge is concerning for SAC conservation.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.