Helminth-fauna of Patagonian armadillos: comparative analysis of parasites geographical variation

Abstract

The similarity between parasites communities’ decay with distance and its analysis may explain important ecological process such host dispersion. Patagonia is inhabited by two armadillo species, Chaetophractus villosus and Zaedyus pichiy. In this study we describe and analyze the variation on helminth fauna of these armadillos in Patagonia compared with northern localities described in previous studies. A total of 49 armadillos were collected in Patagonia. Quantitative descriptors of parasite ecology were calculated and community structure of helminths was analyzed following the central-satellite species hypothesis. The parasite richness in Patagonia decreases almost 50% in both armadillos. Zaedyus pichiy present the same central species in Patagonia as in northern localities. For C. villosus central-satellite species analysis could not be applied. The loss of some helminths in Z. pichiy could be the result of lower temperatures or the absence of intermediate arthropods hosts. But in C. villosus the absence of some helminths with Patagonian distribution could be explained by its recent dispersion in Patagonia. Trichohelix tuberculata still being the only helminth in C. villosus introduced population of Tierra del Fuego.

Key words
endoparasites; Xenarthra; Patagonia; geographical variation; Zaedyus pichiy; Chaetophractus villosus

INTRODUCTION

Parasite diversity in vertebrates depends mainly on host exposure to parasites, which is strongly related to morphological traits, habits and environmental factors (Krasnov et al. 2004, Ezenwa et al. 2006, Luque & Poulin 2008). However, parasite richness is also the result of parasite life-history, host ecology and host defenses (Bush et al. 1997). In this context, numerous studies considered that latitude is one of the main factors correlated to parasite diversity and richness (Poulin 1995, Krasnov et al. 2004, Nunn et al. 2005, Lindenfors et al. 2007, Poulin & Leung 2011). 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 (Bordes et al. 2010). Geographical patterns of host are also extremely associated to parasite community. The similarity between parasites communities’ decay with distance (Poulin & Krasnov 2010). The difference or similarity in parasite species composition between localities may explain important ecological process such host dispersion (Poulin & Krasnov 2010). Thus, natural dispersion or introduction of hosts into new areas results in loss, transference or acquisition of their parasites (Lafferty et al. 2010). In this context, Lymbery et al. (2014) proposed using the terminology of co-introduced for those parasites which have been introduced and established in a new area outside of their native range with an alien host, and co-invader for those parasites which have been co-introduced and then switched from alien to native hosts.

Chaetophractus villosus and Zaedyus pichiy are the only two armadillo species present in Patagonia (Abba et al. 2014). These armadillos are among to the 9 genera and 14 species of armadillos present in Argentina (Teta et al. 2018). The large hairy armadillo, C. villosus, is present in the Gran Chaco of Bolivia, Paraguay, and Argentina as far south as Tierra del Fuego - Argentina and Chile (Gardner 2005, Gallo et al. 2020). This armadillo inhabits a wide variety of habitats including grasslands, forest, steppe, and areas degraded by agricultural use (Abba et al. 2015, 2016, Gallo J.A. et al., unpublished data). The pichi, Z. pichiy, is endemic from Argentina and Chile and frequent in the Patagonian steppe (Superina & Abba 2018), and the main distribution area occurs in Argentina from La Rioja to Santa Cruz provinces (Superina et al. 2019). The diet of both armadillos is similar and includes invertebrates, plant material and small vertebrates (Gallo et al. 2019, Superina et al. 2019).

The colonization process of southern Patagonia is different for each species. Abba et al. (2014) suggest that Z. pichiy is a frequent species in northern and central Patagonia since the Holocene. But the presence of C. villosus in central and southern Patagonia is recent. This armadillo dispersed from the Pampas region, considered as the original area of the species (Poljak et al. 2010), through the south of Chubut river in the last century, with an estimated expansion rate of 13 km/year (Abba et al. 2014). The expansion in the continental area of Patagonia seemed facilitated by human structures and activities such as roads, bridges and the increase of agricultural production (Abba et al. 2014). In the Isla Grande of Tierra del Fuego (TDF), the large hairy armadillo was introduced in 1980 decade (Poljak et al. 2007). Since then, this armadillo has increased its distribution at an expansion rate of 10.9 km/year and now is frequently seen in the northern part of the island (Gallo et al. 2020). In this context, the presence of C. villosus in continental and insular Patagonia (Isla Grande of Tierra del Fuego) is relatively recent.

The parasite fauna of these armadillos in the center-northern of Argentina is well documented (Navone 1988, 1990, Ribicich et al. 2010, Ezquiaga et al. 2012, Ezquiaga 2013, Ezquiaga & Navone 2014, Ríos T.A., unpublished data), but only a few studies describe the helminths fauna of C. villosus and Z. pichiy in Patagonia (Ezquiaga et al. 2009, 2016, 2017). Ezquiaga (2013) described 11 helminths species in C. villosus for localities northern at the Chubut province. The last and only study for large hairy armadillo in southern Patagonia was conducted by Ezquiaga et al. (2016) in the Isla Grande of Tierra del Fuego analyzing samples collected between 2005 and 2006 (after 23 years since introduction, see Poljak et al. 2007). The authors described a dramatically decline of parasite richness in Tierra del Fuego population compared with those of Pampas region (1 versus 11). The only helminth species was Trichohelix tuberculata (Parona & Stossich 1902) (Trichostrongylina: Molineidae).

Twelve helminths species were described for northern distribution of Z. pichiy. In the Patagonian steppe of Mendoza province, Ezquiaga et al. (2009) described 5 helminths using coproparasitological technics. Then, Ezquiaga el al. (2013) analyzed the digestive tracts of hosts and found 11 helminths species, including those described for Mendoza province (see Ezquiaga et al. 2009), except for Trichuris sp.

In this context some questions have arisen: (1) is the helminth diversity of armadillos of southern Patagonia comparable to that analyzed in the northern localities (Ezquiaga 2013)? (2) If variation exists, are parasites indicators of the recent colonization of C. villosus in central-southern Patagonia? (3) Helminth fauna of the C. villosus introduced population of Tierra del Fuego have changed in the last 5 years? The objective of this study is to answer these questions by describing and analyzing the variation on helminth fauna of both armadillo species of central and southern Patagonia.

MATERIALS AND METHODS

During summer season of 2017-2019 principal and secondary roads of Chubut, Santa Cruz and Tierra del Fuego were tracked. A total of 49 armadillos were collected, 23 road-killed C. villosus and 14 road-killed Z. pichiy from Chubut and Santa Cruz (Fig. 1). In Tierra del Fuego, 12 C. villosus of the introduced invasive population were euthanized in accordance with the guidelines of the American Society of Mammologists for the use of wild mammals in research (Sikes et al. 2016) and the Resolución S.A.D.SyC.C.064/2014 of Tierra del Fuego, Antártida e Islas del Atlántico Sur province). Digestive systems were extracted and fixed in formaldehyde 10% solution until their dissection in the laboratory. Nematodes were stored in alcohol 70%, cleared with Amman’s lactophenol and mounted on a temporary slide under a coverslip. Cestodes were stored in alcohol 70%, stained with hydrochloric carmine, dehydrated in a series of ethanol solutions of increasing concentration, cleared with eugenol and mounted in Canada balsam on a slide under a coverslip. Helminths were examined using an Olympus BX51 compound microscope (Olympus Corporation, Tokyo, Japan). CellSens v1.11 (Olympus Corporation) image analyzer software was used to take corresponding morphometric measurements (X40–X600). Parasites were identified using specifics keys (Anderson 2000, Anderson et al. 2009) and descriptions of Navone (1987) and Ezquiaga et al. (2017). For the relevant comparisons on helminths diversity, different areas of host populations were defined. For Z. pichiy: a Northern population (Ezquiaga et al. 2009, Ezquiaga 2013) and a Southern population (this study). For C. villosus three populations were distinguished: a Core population (Pampas region, Ezquiaga 2013); a Southern Patagonian population (Chubut and Santa Cruz provinces, this study) and the exotic population of Isla Grande of Tierra del Fuego TDF, which includes samples of C. villosus of two periods of time that allowed a temporal comparison: 2005-2006 analyzed by Ezquiaga et al. (2016) and 2017-2018 (this study).

Figure 1
Sites of sample collection in Patagonia and helminthes species found in Chaetophractus villosus (a) and Zaedyus pichiy (b). Illustrations modified from Díaz & Barquez (2002), and Parera & Erize (2002).

We calculated prevalence (P), mean abundance (MA), mean intensity (MI), richness (S) and Shannon’s Diversity Index (H) for each host population (Bush et al. 1997). We analyzed the structure of the helminth community of the Patagonian populations following central-satellite species hypothesis (Hanski 1982, Bush & Holmes 1987, Holmes 1987). Two statistical assumptions must be considered to classify helminths community in central-satellite species: 1) significant correlation between prevalence and mean intensity and 2) bimodal or trimodal distribution of prevalence frequencies. The results were contrasted with those found by Ezquiaga (2013) following the next comparisons between host populations: Z. pichiy Northern population vs. Z. pichiy Southern population; C. villosus core population vs. C. villosus Southern Patagonia population and C. villosus TDF population 2005-2006 vs. C. villosus TDF population 2017-2018.

Differences in prevalence values of helminths shared by both hosts were tested with a Chi square test (α = 0.05). Helminths eggs described by Ezquiaga et al. (2009) were excluded.

RESULTS

In this study the total prevalence of helminths was 100% for C. villosus (n = 35) and 92.8% for Z. pichiy (n = 14; 95 % C. I. = 86% – 97%). Eight helminths taxa were found, 7 were nematodes and 1 cestode. The richness was the same for both hosts (S=6). The Shannon diversity index (H’) was 0.954 for C. villosus and 0.755 for Z. pichiy. Aspidodera fasciata (Schneider, 1866) (Ascaridida: Aspidoderidae), A. scoleciformis (Diesing 1851) (Ascaridida: Aspidoderidae), Pterygodermatites argentinensis (Ezquiaga, Rios, Abba and Navone 2017) (Spirurida: Rictulariidae) and Physalopteridae (Larvae) (Railliet, 1893) (Spirurida: Physalopteridae), were present in both hosts with low-moderate prevalence (<50%; Table I). The cestode Mathevotaenia sp. and the nematode Cruzia sp. (larvae) were found only in Z. pichiy while the nematodes Strongyloides sp. and Trichohelix tuberculata were present only in C. villosus. The highest values of mean intensity and mean abundance were for the helminth T. tuberculata, A. fasciata and A. scoleciformis in C. villosus and both Aspidodera species in Z. pichiy. There was significant difference in prevalence of A. scoleciformis (X² = 18.2; p= <0.001; d.f.=1) and P. argentinensis (X² = 16.1; p= <0.005; d.f.= 1) for both hosts.

Table I
Prevalence (P), mean intensity (MI) and mean abundance (MA) estimated for the helminths found in armadillos from Patagonia. (Larvae stages are indicated with L.).

Parasite	Chaetophractus villosus								Zaedyus pichiy
	Southern Patagonia				TDF				Southern Patagonia
	P(%)	IM	AM		P(%)	IM	AM		P(%)	IM	AM
Aspidodera fasciata	39.1	138.7	54.3		-	-	-		50.0	163.1	96.6
Aspidodera scoleciformis	17.4	117.8	20.5		-	-	-		42.9	80.8	34.6
Cruzia sp. (L)	-	-	-		-	-	-		14.3	11.0	1.6
Mathevotaenia sp.	-	-	-		-	-	-		14.3	6.5	0.9
Physalopteridae (L)	8.7	23.5	2.0		-	-	-		7.1	1.0	0.1
P. argentinensis	26.1	8.0	1.4		-	-	-		50.0	5.0	2.5
Strongyloides sp.	4.3	83.0	3.6		-	-	-		-	-	-
Trichohelix tuberculata	95.7	102.7	102.7		100	116.08	116.08		-	-	-

Analysis of community structure of Chaetophractus villosus and Zaedyus pichiy in Patagonia

The correlation between the prevalence and mean intensity was not significant (r = 0.52; p > 0.05) for the large hairy armadillo and therefore the central-satellite species analysis could not be applied to describe the helminth community structure of this species.

In the case of Z. pichiy, the assumptions required by the central-satellite species hypothesis were met. The helminths community of the southern population of this armadillo showed a bimodal distribution of frequencies of prevalence and a positive significant correlation between prevalence vs. mean intensity (r = 0.73; p < 0.05). Then, three central species were identified: A. fasciata, A. scoleciformis and P. argentinensis (Fig. 2).

Figure 2
Community structure of helminthes of Zaedyus pichiy in Patagonia. Illustration modified from Díaz & Barquez (2002).

Comparison of Zaedyus pichiy helminth fauna

Northern population vs. Southern population: The species richness reported in the northern population (Ezquiaga et al. 2009, Ezquiaga 2013) and found in the Southern Patagonia population (this study) was S = 11 and S = 6 respectively. Only three species of helminths are shared by both populations: two nematodes, A. fasciata and A. scoleciformis, and one cestode, Mathevotaenia sp. (Table II). Significant differences in prevalence of both populations were found for both species of Aspidodera genus, A. fasciata (X² = 16.1; p < 0.001; d.f. = 1) and A. scoleciformis (X ² = 7.8; p < 0.005; d.f. = 1).

Table II
Helminths prevalence in Zaedyus pichiy northern and southern Patagonian population. H’= Shannon’s Diversity Index.

Parasite	Northern population (Ezquiaga, 2013) H’= 1.08	Southern population (This study) H’= 0.75
Ancylostoma caninum	18	-
Aspidodera fasciata	100	50
Aspidodera scoleciformis	73	42.9
Cyclobulura superinae	27	-
Cruzia sp. (L)	-	14.3
Delicata ransomi	23	-
Mathevotaenia sp.	23	14.3
Orihelia anticlava	4	-
Pterygodermatites chaetophracti	23	-
Pterygodermatites argentinensis	-	50
Physalopteridae (L)	-	7.1
Strongyloides sp.	9	-
Travassosia sp.	5	-
Trichohelix tuberculata	23	-

Comparison of Chaetophractus villosus helminth fauna

Core population vs. Southern Patagonia population

The species richness reported for the core population (Ezquiaga 2013) and found in the Southern Patagonia population (this study) was S=11 and S=6 respectively. Only four helminths species are shared in both populations (Table III). Significant differences in prevalence were found for A. fasciata (X² = 40.6; p < 0.001; d.f. = 1); A. scoleciformis (X² = 66.6; p < 0.001; d.f. = 1) and Strongyloides sp. (X² = 14.8; p < 0.001; d.f. = 1).

Table III
Helminthes prevalence (%) in Chaetophractus villosus core population and southern Patagonia population. H’= Shannon’s Diversity Index.

Parasite	Core population (Ezquiaga, 2013) H’= 1.10	Southern Patagonia Population (this study) H’=0.95
Ancylostoma caninum	56	-
Aspidodera fasciata	96	39.1
Aspidodera scoleciformis	96	17.4
Delicata ransomi	26	-
Mazzia bialata	22	-
Moenningia sp.	9	-
Mathevotaenia sp.	26	-
Orihelia anticlava	17	-
Pterygodermatites cheatophracti	9	-
Pterygodermatites argentinensis	-	26.1
Physalopteridae (L)	-	8.7
Strongyloides sp.	22	4.3
Trichohelix tuberculata	96	95.7

TDF population 2005-2006 vs. TDF population 2017-2018

In the last study on C. villosus exotic population, Ezquiaga et al. (2016) found one helminth species, the nematode T. tuberculata, with prevalence of 89%. In this study we recorded the same species with a prevalence of 100%. Prevalence of T. tuberculata did not change significantly between periods (X ² = 0.640; p = 0.423; d.f. = 1).

DISCUSSION

The community of Patagonian helminths of C. villosus and Z. pichiy was analyzed, and with this work, we contribute to the general description of helminths of both Patagonian armadillos.

The similarity between two parasites communities of different localities decreases with distance (Soininen et al. 2007, Poulin & Krasnov 2010), and latitude is determinant of parasite richness (Nunn et al. 2005, Preisser 2019). The richness found for both hosts in this study decrease considerably compared to northern populations (Ezquiaga 2013). Some parasites such Mathevotaenia sp. and T. tuberculata were exclusive of Z. pichiy and C. villosus respectively.

The presence of two larvae of nematodes of Physalopteridae family and the genus Cruzia recovered in both armadillo’s hosts was accidental infection due to consumption of arthropods intermediate hosts. These helminths are parasites of carnivorous mammals, marsupials, birds and, amphibians, reptiles and fish (Anderson 2000, Adnet et al. 2009, Vieira et al. 2020). The nematode Pterygodermatites argentinensis has been already described in Patagonia by Ezquiaga et al. (2017) in Z. pichiy but not in C. villosus, which means a new host-parasite association found in this study.

Variation in helminths of northern and southern populations of Zaedyus pichiy

In the southern population the specific richness and the parasite diversity was a 50% of the ones reported for the northern population (Ezquiaga 2013). Decrease in parasite richness and significant difference in prevalence of both Z. pichiy populations could be result of lower temperatures of Patagonia, which surely affect normal development of infective stages of some parasites, such Cyclobulura superinae and Travassosia sp. acanthocephalans. But also these results could be a consequence of the low diversity or the absence of intermediate arthropods hosts in Patagonia (Nunn et al. 2005, Poulin & Leung 2011, Preisser 2019) such Orihelia anticlava, which use mites as vectors. According to Ezquiaga et al. 2021, armadillos ectoparasites show a north-south reduction on prevalence.

Variations in helminths of Patagonian populations of Chaetophractus villosus

The richness of helminths decreases almost to a 54.5% in C. villosus Patagonian populations in relation to central Argentina populations (Ezquiaga 2013). The most prevalent parasite was T. tuberculata (95.7%), which is also the only helminth found in Tierra del Fuego by Ezquiaga et al. (2016) and in the present work.

The presence of C. villosus in Patagonia is relatively recent. As result of anthropogenic causes, this armadillo spread from the core region (Pampas region) to Patagonia, approx. 100 years ago (Abba et al. 2014). The parasites species least prevalent in the core region (prevalence lower than 50%, Ezquiaga 2013) are those absent in individuals from Patagonia. The individuals of C. villosus that dispersed in Patagonia derived from a small subset of core population and it is possible that only few hosts were parasitized. Also, the loss of these helminths species could be the result of the absence of intermediate arthropod host and the harsh climatic conditions of Patagonia could affect the life cycles of many parasites. Many authors suggest that these causes of helminths loss are frequent at highest latitudes (Nunn et al. 2005, Poulin & Leung 2011, Preisser 2019). Mathevotaenia sp. is one of the lost helminths in Patagonian population of C. villosus. This cestode is frequent in armadillos using Lepidoptera and Coleoptera larvae as intermediate hosts (Bienek & Klikoff 1974). Those arthropods are frequent in diet of both Patagonian armadillos (Gallo et al. 2019) and Mathevotaenia sp. is also present in Z. pichiy. In this case, the absence of this parasite in C. villosus could be the result of the recent spread of this armadillo through Patagonia, while the loss of other helminths with heteroxenous life cycles (Cyclobulura superinae, Orihelia anticlava, Travassosia sp.–Acanthocephala–) could be the result of the absence of intermediate hosts in Patagonia.

Trichohelix tuberculata is the only parasite species present in the exotic population of C. villosus in the Isla Grande of Tierra del Fuego as it was recorded by Ezquiaga et al. (2016). Torchin et al. (2003) suggested that parasites with highest prevalence are those presents in invader host population. The prevalence of T. tuberculata increased since the last study made on Tierra del Fuego exotic population by Ezquiaga et al. (2016). This nematode is frequent in the Tribe Euphractini of armadillos and the infective free-living larvae stage (L2) retain the moult of the previous stage (L2) as protection cover against harsh climatic conditions (Anderson 2000), which allow them to survive to the extreme climate of Tierra del Fuego as proposed by Ezquiaga et al. (2016).

Helminths community structure of Zaedyus pichiy and Chaetophractus villosus

The southern and northern populations of Z. pichiy present the same central species of helminths, A. scoleciformis and A. fasciata and the prevalence of both parasites species is lower in the southern population. This difference could be related to the limited encounters between potential hosts and infective forms of parasites.

In C. villosus core population, Ezquiaga (2013) found three central species (T. tuberculata, A. fasciata and A. scoleciformis). In Patagonia the structure of helminths community of C. villosus did not show a significant correlation between prevalence and mean intensity. Holmes (1987) suggested that this may be the way that the parasites respond to host quality. Considering that both Aspidodera species and T. tuberculata are frequent in armadillos and occurs along their distribution (Navone 1990, Ezquiaga et al. 2019), this result could respond to the recent dispersion of a small subset of C. villosus in Patagonia, carrying a small subset of helminths that were co-introduced with the host. Also, the prevalence of both Aspidodera species decreases in Patagonia and some helminths with Patagonian distribution as Mathevotaenia sp. are absent in C. villosus southern Patagonian population.

Contributions to knowledge of the Patagonian helminths range

In view of the results of this study, the geographical range of some helminth parasite species was extended. Both Aspidodera species occur from southern U.S.A to central Argentina (Jiménez Ruiz & Gardner 2003). Pterygodermatites argentinensis, descripted by Ezquiaga et al. (2017) occurs as far as Chubut province in Argentina. The southern limit of Strongyloides sp. and Mathevotaenia sp. were Buenos Aires and Rio Negro province respectively (Ezquiaga, 2013). With the results of this study, the species named above increased their geographical range through Patagonia a far as Santa Cruz province (Argentina).

Future prospective

In this context, Patagonian populations of C. villosus (Southern Patagonia and TDF) present extreme variations in helminths community as results of the recently presence of this armadillo losing almost 50% of parasites compared to core population. In the next years is possible that exotic population of Tierra del Fuego does not show any changes or develop an event of host-parasite co-invasion, and T. tuberculata could infect other hosts in Tierra del Fuego.

ACKNOWLEDGMENTS

We would like to thank to M. L. Carranza and E. Curto from Dirección General de Áreas Protegidas y Biodiversidad of Tierra del Fuego; M. L. Marcías; To Dirección de Flora y Fauna de la provincial del Chubut; E. Villanova and J. Barría from Estancia Sara; M. R. Couto from Estancia El Rincón; V. M. Durán Bodelón; N.A. Cossa and M. Malerba for assistance during fieldwork. To G. Martin and D. Udrizar-Sauthier for provide part of samples and help during fieldwork. J. S. Verón and B. J. S. for supporting us. To the Centro Austral de Investigaciones Científicas (CADIC-CONICET), to Laboratorio de Parasitología (CRUB-UNComa) and to CENAC (PNNH) for providing the infrastructure to analyze the samples. This work was supported by Neotropical Grassland Conservancy-NGC and Programa Patagonia/Aves Argentinas (AOP).

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Publication Dates

• Publication in this collection
  22 Oct 2021
• Date of issue
  2021

History

• Received
  20 Apr 2021
• Accepted
  27 July 2021