Zoonotic Pathogens in the American Mink in Its Southernmost Distribution

Abstract

The American mink, Neovison vison, is an invasive species in Chile. Its impact on native fauna and public health has not been studied in depth in the country. In this study, we searched for gastrointestinal parasites, including helminths and zoonotic Cryptosporidium sp., the presence of Trichinella sp. in muscle, and the renal carriage of pathogenic Leptospira sp. in minks caught on Navarino Island, “Magallanes y la Antártica Chilena” Region, and Maullín and Ancud, “Los Lagos” Region, Chile. A total of 58, 15, and 21 minks from Navarino Island, Maullín, and Ancud, respectively, were examined for Trichinella sp. (artificial digestion of muscle). A total of 36, 11, and 17 minks from Navarino Island, Maullín, and Ancud, respectively, were examined for pathogenic Leptospira species (molecular detection of LipL32 gen fragment in renal tissue) infection. Finally, 45, 11, and 17 minks from Navarino Island, Maullín, and Ancud, respectively, were analyzed to detect gastrointestinal parasites (by optical inspection of the digestive tract for helminths, and by both Ziehl-Neelsen stain and molecular detection of small subunit-ribosomal DNA for Cryptosporidium species). Trichinella larvae were not observed. Pathogenic Leptospira sp. was detected in 22 samples: 15 from Navarino Island, 3 from Maullín, and 4 from Ancud. Two nematodes, belonging to Ascaridinae (subfamily) and Pterygodermatites (Paucipectines) sp., were found in samples of two minks from Navarino Island. Oocysts and DNA of Cryptosporidium sp. were detected in three fecal samples from Navarino Island. Further studies could determine the zoonotic potential of Cryptosporidium sp., as well as the potential impact of the zoonotic Leptospira sp. on the human population of the Navarino Island, Maullín, and Ancud districts. The enemy release theory could explain the low helminth species richness in the minks. In addition, we did not find evidence of parasite transmission from native fauna.

Introduction

Introduced species represent a problem in several fields. In particular, from the point of view of biological conservation, introduced invasive species are among the most important causes of biodiversity loss (Wilcove and Master 2005, Bellard et al. 2016), and their parasites also represent introduced species (Taraschewski 2006). In contrast, introduced host species can also host zoonotic pathogens, and, given that these pathogens tend to be ubiquitous, they can become a serious public health concern (Keller et al. 2011, Hulme 2014).

Although many parasitic species are lost in the process of translocation and establishment—meaning a lower number of parasite species in the colonized territory—(Torchin et al. 2003, MacLeod et al. 2010) some parasites can arrive to the new territory and be transmitted to native fauna, thereby affecting it (Lymbery et al. 2014, Morand et al. 2015). This coinvasion by parasites represents an indirect way for invasive host species to affect native fauna. Moreover, the cointroduction of zoonotic parasites (including microparasites as bacteria) is another public health concern.

Introduced hosts can also catch parasites previously present in the territory and both dilute or amplify them, leading to a spillback effect (Kelly et al. 2009, Johnson and Thieltges 2010, Mastitsky and Veres 2010). These hosts may then also become part of the human parasite reservoir, regardless of whether or not their parasites are native or previously cointroduced by other invasive host species.

The American mink, Neovison vison, is one of the most relevant invasive species in Chile, given its great colonizing ability, aggressive predation on native fauna, and the fragility of the ecosystems that it inhabits (Schüttler et al. 2009, 2010, Jiménez et al. 2014). Currently, N. vison is distributed in southern Chile, between the Araucanía and Magallanes administrative regions (Vergara and Valenzuela 2015).

There are several studies covering parasites of introduced mammals in Chile (see the literature review in Landaeta-Aqueveque et al. 2014). However, only few studies, focused on Toxoplasma gondii and Leptospira sp., have been performed in N. vison inhabiting Chile (Sepúlveda et al. 2011, Barros et al. 2014, 2018). Previous studies aiming to determine the presence of gastrointestinal and other endoparasites were not found in the current literature. In other countries, N. vison has been found to host parasites of native mammals (Dorney and Lauerman 1969, Barber and Lockard 1973, Foster et al. 2007, Sherrard-Smith et al. 2015). From this point of view, the host relationship is an important factor in the sharing of parasites between native and introduced mammals (Wells et al. 2015, Landaeta-Aqueveque et al. 2018). Thus, this suggests that the host switching of parasites to N. vison from native mustelids of Chile, such as the southern river otter, Lontra provocax, is to be expected, since its distribution overlaps with that of N. vison (Sepúlveda et al. 2015).

In other countries (for instance, Ireland, the United States, Spain, and Argentina), N. vison has also been found to host zoonotic parasites such as Cryptosporidium sp. and Trichinella sp., and Mycobacterium sp. (Miller and Harkema 1964, Gómez-Couso et al. 2007, Stuart et al. 2013, Martino et al. 2017), suggesting that the American mink has the ability to become a public health problem. Given the above, the study of parasites and zoonotic pathogens of N. vison in Chile remains an important issue to be studied. Therefore, this study aims to describe the community of gastrointestinal helminths and to determine the presence of Cryptosporidium sp., Trichinella sp., and pathogenic Leptospira sp. in the American mink in three localities in Chile.

Materials and Methods

Description of studied localities

The three localities selected for this study were (1) the Maullín district, a continental locality in Los Lagos region (41°37′0.24″S, 73°35′51.92″W, and in the surrounding areas); (2) the Ancud district, an insular locality in Northern Chiloé Island, Los Lagos Region, separated from the continent by the Chacao Channel (41°52′13.55″S, 73°49′3.58″W, and in the surrounding areas); and (3) Navarino Island, Cabo de Hornos district, Magallanes y de la Antártica Chilena Region, the southernmost population of N. vison in the world (54°56′7.44″S, 67°36′12.91″W, and in the surrounding areas) (Fig. 1). Several fur farms were established in the Magallanes and Los Lagos regions from 1934 to 1973, with some of these releasing minks to the continent or to Tierra del Fuego island after closing (Valenzuela et al. 2016).

FIG. 1.

Map of Chile with the studied localities. In the case of Navarino Island, the whole Cabo de Hornos district is marked in gray. A, Ancud; M, Maullín; N, Navarino Island.

The exact date of arrival of the minks to the Maullín district is unknown. Nonetheless, the first American mink was reported in Ancud during February 2013 and has since been found widespread throughout the island (Vergara et al. 2015). The first capture of the American mink on Navarino Island, south of Tierra del Fuego, separated from it by the Beagle Chanel, was reported in 2001 (Jaksic et al. 2002). Since that time, an increase in the population size has been reported on the island, possibly due to the lack of predators in this area. In addition, the American mink has been observed near human settlements (Rozzi and Sherriffs, 2003) and widely dispersed, even more than 800 m from water. The change in its behavior to a diurnal predator has also been observed, thus expanding its spatial and temporal niche (Crego et al. 2018).

Mink captures

American minks from Navarino Island (n = 58) were caught by a private business as part of a public tender offered by the Servicio Agrícola y Ganadero (SAG) of Chile, and were then given to the authors for this study. These minks were trapped using Conibear no. 120 traps, each trap placed 150 m apart of the other, along streams, the coast, or surrounding lakes of the north of the island between February and April 2016. Traps were checked every 5 days.

Minks of Maullín (n = 15) and Ancud (n = 21) were caught by a nongovernmental organization, the Centro de Estudios y Conservación del Patrimonio Natural (CECPAN), between January 2015 and February 2016, during an Invasive Species Control Program. These captures were performed with Tomahawk live traps placed next to streams or rivers, with a distance of 1–6 km between them. Minks caught with live traps were anesthetized with ketamine/Xylazine and euthanized with T61 solution. In both cases, corpses were kept frozen at −20°C until examination.

Laboratory analysis

After unfrozen, at least 10 g of muscle samples from each mink (mixture of diaphragm, masseter, and tongue) was examined for the presence of Trichinella larvae by muscle digestion, following Gamble et al. (2000). In some cases, the freezing of minks was not fast enough for a good conservation of the digestive tract, which was seen as a decomposed intestine. These tracts were discarded. When conservation was adequate (intestine was not decomposed), gastrointestinal tracts were fixed in ethanol 96%, and then examined directly and under a stereomicroscope for the presence of helminths.

Helminths (nematodes) were kept in 70% ethanol, cleared with lactophenol, and observed under light microscope. Identification was performed following the keys of Anderson et al. (2009). Fecal samples were obtained from the rectum of these minks and conserved in 70% ethanol. Burrows method and posterior Ziehl-Neelsen staining were used for visualizing oocysts of Cryptosporidium sp. under an optic microscope at 1000 × with immersion oil (Muñoz et al. 1984, Casemore 1991).

Not all carcasses were received with kidneys. When kidneys were present, those from Navarino Island were extracted from mink carcasses, preserved in brain–heart infusion broth and stored at −20°C until their DNA extraction. Kidneys from Maullín and Ancud were kept at −20° until DNA extraction. The number of analyzed digestive tracts (examined for Cryptosporidium sp. and helminths) and kidneys (examined for Leptospira sp.) is given in Table 1. All minks were examined for Trichinella sp.

Table 1.

Number of Analyzed and Infected Neovison vison, Prevalence (%), Confidence Interval^a (95%) of the Prevalence and Highest Possible Prevalence^b (95% CI), by Pathogen Group, in Each Studied Locality

Locality	Trichinella			Cryptosporidium				Helminths				Leptospira
Locality	Analyzed	Infected	HPP	Analyzed	Infected	Prevalence	CI/HPP	Analyzed	Infected	Prevalence	CI/HPP	Analyzed	Infected	Prevalence	CI
Navarino Island	58	0	5	45	3	6.7	0.0–14	45	2	4.4	0.0–10.5	36	15	41.7	25.6–57.8
Maullín	15	0	18.1	11	0	—	23.8	11	0	—	23.8	11	3	27.3	1–53.6
Ancud	21	0	13.3	17	0	—	16.2	17	0	—	16.2	17	4	23.5	3.4–43.7
Total	94	0	3.1	73	3	4.1	0.0–8.7	73	2	2.74	0.0–6.5	64	22	34.4	22.7–46

CIs are given only when positive individuals were identified.

HPP is given in cases wherein no positive individuals were identified.

CI, confidence interval; HPP, highest possible prevalence.

For the molecular search of Cryptosporidium sp. and pathogenic Leptospira sp., DNA extraction from feces (the same ones subjected to Burrows and Ziehl-Neelsen methods) and kidney samples was done with QIAamp DNA Stool Mini Kit (Qiagen) and DNeasy Blood and Tissue Kit (Qiagen), respectively, following the manufacturer's instructions. DNA samples were kept at −20°C until the PCR protocol was performed.

A fragment of the small subunit of the ribosomal DNA of Cryptosporidium sp. was amplified by nested PCR following Ryan et al. (2003). A fragment of the LipL32 gene that encodes the outer membrane lipoprotein of pathogenic Leptospira species was amplified by nested PCR following Jouglard et al. (2006). PCR products were separated by electrophoresis in 1.2% agarose gel and then sequenced with the same primers of the nested amplifications (Austral-Omics, Chile). Sequences were identified by means of the Basic Local Alignment Search Tool (BLAST) in GenBank.

Statistical analysis

Prevalence was calculated following Bush et al. (1997), and the confidence intervals (CIs) and highest possible prevalence (HPP; when no infected sample was observed) were calculated using the online platform Win Epi (www.winepi.net/sp/index.htm, visited on June 6, 2019).

The Ethics Committee of the Veterinary Sciences Faculty at the Universidad de Concepción approved and certified this study.

Results

Muscle samples of all caught minks were examined for the presence of Trichinella sp. However, no larvae were obtained.

A total of 73 gastrointestinal tubes and fecal samples (see details in Table 1) were examined for the presence of helminths and Cryptosporidium sp. Two helminths were observed, only in minks from Navarino Island, and identified as Pterygodermatites (Paucipectines) sp. and Ascaridinae. Three minks from Navarino Island were positive for the presence of Cryptosporidium sp. by both Burrows and Ziehl Neelsen molecular methods. The length of the PCR products was 620 bp. BLAST comparisons allowed confirmation that the DNA belonged to Cryptosporidium sp., with an identity of 99% with C. parvum and C. cuniculus.

Sixty-four minks were analyzed for pathogenic Leptospira species renal carriage: 36 from Navarino Island, 17 from Ancud, and 11 from Maullín; 22 of these were positive: 15 individuals from Navarino Island, 4 from Ancud, and 3 from Maullín. BLAST comparisons allowed confirmation that these DNA samples belonged to pathogenic Leptospira species, 100% being identical to L. interrogans serovars Copenhageni, Pomona, Bratislava, Canicola; L. kirschneri serovars Tsaratsovo, Mozdok, Altodouro; L. noguchii serovar Pomona, and L. borgpetersenii.

Discussion

The time of study was ∼1 year and the sample size was larger than that of previous studies of pathogens in N. vison (see referenced works hereunder); however, the CIs were wide for some pathogens, which suggests that the sample studied here was not large enough to provide precise estimations of the infection rates in the population (Table 1). Nevertheless, the findings of our study are of interest to the field, since in two of the three localities (Navarino Island and Ancud), this sample represents a population with a recent history of invasion. This is a trait that is not commonly observed in the populations studied in previous reports. Furthermore, these represent new localities reported to harbor minks acting as part of reservoirs of zoonotic pathogens. This provides a new direction for future studies, opening up the possibility of describing the temporal behavior of these pathogens after the arrival of a new and very invasive host.

The number of helminth species found in this study was lower than previous reports in both native and introduced ranges. For instance, Foster et al. (2007) and Zabiega (1996) found 12 helminth species in five localities of its native range, which can be explained by the parasite loss hypothesis (Torchin et al. 2003, MacLeod et al. 2010).

Conversely, Shimalov and Shimalov (2001) found 19 species of helminths colonizing N. vison in Belorussian Polesie, in its introduced European range. This difference in comparison with our results supports the hypotheses that the invasion of the American mink was recent in the three studied localities, and that there were few introduction processes and/or that there is a lower native helminth richness available for colonizing the mink than in the Belorussian helminth community. However, the hypothesis of a diluting effect [in its more restrictive definition, after Keesing et al. (2006)] on native parasites cannot be rejected because the scarce finding of parasites is in accordance with the fact that N. vison could be an inefficient host for native parasites infecting it in the studied locations. More studies on the temporal dynamics of parasites are necessary to test this hypothesis.

The lack of Trichinella larvae on Navarino Island is in accordance with the lack of reported cases of human trichinellosis in the island. However, Maullín and Ancud are in a region with a large history of human trichinellosis (Ministerio de Salud 2015). Trichinella infections have been reported previously in N. vison overseas, but always with low prevalence: 8.3% in Canada (Dick et al. 1986), 4% in Belarus (Shimalov and Shimalov 2001), and 3.3% in Poland (Hurníková et al. 2016), suggesting the need to keep a close eye on this parasite in the minks in this endemic region, considering that the HPPs (18.1% and 13.3%) in our study are higher than those mentioned.

The presence of Pterigodermatites (Paucipectines) sp. in the intestine of a mink is not necessarily evidence of parasitism by this genus, given that this genus has been previously found in Chilean rodents (Landaeta-Aqueveque et al. 2018) and in micromammals in Argentina (Gozzi et al. 2014, Fugassa 2015). This suggests that this worm could be the parasite of a prey animal rather than of the mink itself. The presence of an Ascaridinae in a mink is not the first record, given that Ascaris sp. and Baylisascaris devosi have been previously found within the native and introduced range, respectively (Miller and Harkema 1964, Shimalov and Shimalov 2001). Ascaridinae species previously reported in Chile are Toxascaris leonina, Parascaris equorum, and Ascaris suum, all mainly in domestic animals.

Given that in both cases helminths were not conserved in optimal conditions (one possibility is that the elapsed time between the capture/death and conservation was too long) and that only one female specimen per species was recovered, further identification was not possible. Considering that the HPP of helminths in this study was only 6.5% and that the observed intensities were too low, it is possible to suggest that American minks are not good reservoirs of helminths to native fauna or humans, and, rather, this lack of enemies may enhance their invasive ability.

The frequency of Cryptosporidium sp. (4.1%, CI: 0.0–8.7) was similar to that of previous studies of feral American minks elsewhere (e.g., 4.9% in wild minks of Ireland, see Stuart et al. 2013). The finding of oocysts (Burrows–Ziehl Nielsen diagnosis) in the minks is important, because it strongly suggests that the protozoa parasitized the minks rather than their prey. In other words, the amplified DNA did not belong to a protozoon that parasitized the prey of the mink, but rather it likely belonged to an oocyst resulting from mink infection. In this study, the sequences obtained did not allow the proper classification of the lineage of the isolates of Cryptosporidium that were obtained. However, the two most likely species that the samples belong to, C. parvum and C. cuniculus, are zoonotic (Puleston et al. 2014), particularly C. parvum (Lucio-Forster et al. 2010).

In Chile, previous reports identified the species C. parvum, C. hominis, C. muris, and C. meleagridis in humans, and C. parvum in calves (Díaz-Lee et al. 2011, Neira et al. 2012), although C. cuniculus was not reported. Five taxa of Cryptosporidium have been identified previously parasitizing N. vison elsewhere: C. andersoni, C. canis, C. meleagridis, and Cryptosporidium (parvum) ferret genotype and Cryptosporidium mink genotype (Gómez-Couso et al. 2007, Wang et al. 2008, Stuart et al. 2013, Zhang et al. 2016). The three species have been found in humans, but associated with a variable zoonotic potential (Lucio-Forster et al. 2010).

All of the mentioned allows us to state that there is a potential for sharing of zoonotic Cryptosporidium sp. between humans and minks of Navarino Island. Further studies considering a longer sequence and other loci may allow species identification and, considering the search for human infection in Navarino Island, this hypothesis could be tested.

Pathogenic Leptospira sp. was previously detected in the American mink in several localities in southern Chile, including Maullín (Barros et al. 2014). Overall prevalence in our study (34.4%, CI: 22.7–46) was slightly lower than that reported previously (55.6% [CI: 24.8–86.4], n = 57) and slightly higher than both studies that used molecular or immunological techniques in free-ranging American minks in France (15% [CI: 5.2–32.3], n = 33) and Argentina (13.8%, n = 87) (Moinet et al. 2010, Martino et al. 2017).

This is the first time that Leptospira sp. has been detected in minks from the Ancud district, as well as from the Magallanes Region (Navarino Island). Moreover, the finding of renal carriage of Leptospira sp. in minks from Navarino Island represents the southernmost point from where this pathogen is reported in the world. To establish future research studies, we must understand the epidemiological role of this invasive species in these areas, for instance, assessing the serovars colonizing the minks. Since Leptospira sp. has been previously reported in other species and other localities (e.g., Zamora and Riedemann 1999, Correa et al. 2017), future research must also determine the importance of other animal species that can be hosts of this zoonotic bacterium in southern Chile.

Conclusions

American mink can host zoonotic (micro)parasites in southern Chile, with a potential impact on public health and on the human population inhabiting the surrounding areas where the minks live. Considering the ecology and behavior of minks, they constitute a potential risk for water-borne diseases, especially for Cryptosporidium sp., which is highly resistant to environmental conditions. More studies are necessary to assess the importance of N. vison in the epidemiology of these pathogens. We did not find evidence of a risk of transmission of parasites from minks to native fauna, but rather a lack of parasites in this introduced species.

Footnotes

Acknowledgments

The authors thank CECPAN for providing corpses from Maullín and Ancud localities, and Miguel Gallardo and Ramón Barría, as well as SAG-Magallanes, for providing corpses from Navarino Island. We also thank Eileen Smith for editorial support. This study was funded by the Vicerrectoría de Investigación y Desarrollo of the Universidad de Concepción (grant nos. 215.152.023-1 OIN and 217.152.024-1OIN), and by the Fondo Nacional de Desarrollo Científico y Tecnológico (CONICYT/FONDECYT grant no. 11170294).

Author Disclosure Statement

No conflicting financial interests exist.

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