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Gastrointestinal parasites in wild rodents in Chiloé Island-Chile

Parasitos gastrointestinais em roedores selvagens na Ilha de Chiloé-Chile

Abstract

Gastrointestinal parasites are well-documented in small mammals from north-central Chile, but little is known about endoparasites of rodents in southern Chile. A survey was conducted between January and February 2018 to evaluate gastrointestinal parasites and risk factors of wild rodents that live in rural areas in Northern Chiloé Island, Chile. A total of 174 fecal samples from rodents of six native and one introduced species were collected and examined using the Mini-FLOTAC method. Also, 41 individuals of four native wild rodent species were examined furtherly to determinate adult parasites from gastrointestinal tracts. The overall prevalence of endoparasites was 89.65% (156). Helminth egg types included: Rodentolepis spp., Capillariidae, Trichuris sp., Syphacia sp., oxyurid-type eggs, Strongyloides sp., Spirurid-type eggs, Strongilid-type eggs, Moniliformis sp., and an unidentified nematode egg and larvae. Protozoa comprised coccidia, amoeba, and unidentified cysts. From necropsies, adult parasites involved Syphacia sp. Trichuris sp., Protospirura sp. and Physaloptera sp. In Abrothrix olivacea, individuals with low-body-mass index exhibited reduced infection probability for Spirurid-type and Strongilid-type eggs. Some parasites in this study may affect human health. In rural settings where environmental conditions are changing, more research should be undertaken to understand parasitic infections in wildlife and implications for public health and conservation.

Keywords:
Small-mammals; helminth; protozoa; parasites; Chile; Austral

Resumo

Parasitos gastrointestinais são bem documentados em pequenos mamíferos do centro-norte do Chile, mas pouco conhecido sobre endoparasitos de roedores no sul do Chile. Uma pesquisa foi realizada entre janeiro e fevereiro de 2018, avaliando parasitas gastrointestinais e fatores de risco de roedores selvagens vivendo em áreas rurais no norte da Ilha de Chiloé, Chile. Um total de 174 amostras fecais de roedores de seis espécies nativas e uma introduzida foi coletado e examinado pelo método Mini-FLOTAC. Ademais, 41 indivíduos de quatro espécies nativas de roedores selvagens foram examinados para determinar parasitas adultos do trato gastrointestinal. A prevalência geral de endoparasitos foi de 89,65% (156). Os tipos de ovos de helmintos incluíram: Rodentolepis spp., Capillariidae, Trichuris sp., Syphacia sp.; dos tipos Oxyurideos, Strongyloides sp., dos tipos Spirurideos e Estrongilideos, Moniliformis sp.; e um ovo e larvas de nematoides não identificados. Os protozoários compreendiam coccídios, amebas e cistos não identificados. Nas necropsias, os parasitos adultos envolveram Syphacia sp. Trichuris sp., Protospirura sp. e Physaloptera sp. Em Abrothrix olivacea, indivíduos com baixo índice de massa corporal apresentaram probabilidade de infecção reduzida para ovos Spirurideos e Estrongilideos. Alguns parasitos, neste estudo, podem afetar a saúde humana. Em ambientes rurais, onde as condições ambientais mudam, mais pesquisas são necessárias para entender as infecções parasitárias na vida selvagem e as implicações para a saúde pública e conservação.

Palavras-chave:
Mamíferos; helmintos; protozoários; parasitas; Chile; Austral

Introduction

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Rodents are considered reservoirs and carriers for a variety of infectious diseases that can also be transmitted to humans (Han et al., 2015Han BA, Schmidt PJ, Bowden SE, Drake JM. Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci USA 2015; 112(22): 7039-7044. http://dx.doi.org/10.1073/pnas.1501598112. PMid:26038558.
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). Gastrointestinal helminths and protozoal infections can affect survival and reproduction directly by pathological effects (e.g., blood loss, tissue damage) and indirectly through reduction of host condition (e.g., malabsorption of nutrients, predator escape, energetic costs) (Lyles & Dobson, 1993Lyles AM, Dobson AP. Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J Zoo Wildl Med 1993; 24(3): 315-326.; Scantlebury et al., 2007Scantlebury M, Waterman JM, Hillegass M, Speakman JR, Bennett NC. Energetic costs of parasitism in the Cape ground squirrel Xerus inauris. Proc Biol Sci 2007; 274(1622): 2169-2177. http://dx.doi.org/10.1098/rspb.2007.0690. PMid:17613450.
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Parasitological parameters (e.g., prevalence, burden, richness) of helminths and protozoa can be influenced by host attributes, such as sex, age, and body condition, and tend to be different according to each ecological setting (Morand, 2015Morand S. (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. Int J Parasitol Parasites Wildl 2015; 4(1): 80-87. http://dx.doi.org/10.1016/j.ijppaw.2015.01.001. PMid:25830109.
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). Also, adult individuals can be more parasitized because of the cumulative exposure, whereas juveniles can be more affected given that their adaptive immunity is still under-developed (Wilson et al., 2002Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, et al. Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP, editors. The ecology of wildlife diseases. Oxford: Oxford University Press; 2002. p. 6-44.; Wells et al., 2007Wells K, Smales LR, Kalko EKV, Pfeiffer M. Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. J Trop Ecol 2007; 23(1): 35-43. http://dx.doi.org/10.1017/S0266467406003804.
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). Likewise, individuals with high body mass can harbor more parasites since a larger habitat favor parasite colonization, while individuals with low body condition can exhibit reduced immune competence related to nutrients deficiency and an increase in parasitosis (Wilson et al., 2002Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, et al. Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP, editors. The ecology of wildlife diseases. Oxford: Oxford University Press; 2002. p. 6-44.; Morand, 2015Morand S. (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. Int J Parasitol Parasites Wildl 2015; 4(1): 80-87. http://dx.doi.org/10.1016/j.ijppaw.2015.01.001. PMid:25830109.
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). In addition, environmental characteristics that influence parasitic infections include altitude, climate (e.g., temperature, humidity), habitat quality, among others (Wells et al., 2007Wells K, Smales LR, Kalko EKV, Pfeiffer M. Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. J Trop Ecol 2007; 23(1): 35-43. http://dx.doi.org/10.1017/S0266467406003804.
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In Chile, many endoparasites have been reported in native and introduced rodent species, in which parasite infection ranged from 0.5 to 88% (Alba & Jarpa, 1951Alba M, Jarpa A. Trichinosis in rats in Municipal slaughterhouse in Santiago, Chile. Bol Inf Parasit Chil 1951; 6(1): 7. PMid:14821015.; Olsen, 1966Olsen OW. Diplophallus taglei n. sp. (Cestoda: Cyclophyllidea) from the Viccacha, Lagidium peruanum Meyer, 1832 (Chinchillidae) from the Chilean Andes. Proc Helminthol Soc Wash 1966; 33(1): 49-53.; Schenone et al., 1967Schenone H, Jacob C, Rojas A, Villarroel F. Infección por Trichinella spiralis en Rattus norvegicus capturados en el matadero municipal de Santiago de Chile. Bol Chil Parasitol 1967; 22(4): 176.; Babero et al., 1975Babero BB, Cattan PE, Cabello C. Trichuris bradleyi sp. n., a Whipworm from Octodon degus in Chile. J Parasitol 1975; 61(6): 1061-1063. http://dx.doi.org/10.2307/3279376. PMid:1195067.
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). Although well-documented information is available about the taxonomy and ecological features of endoparasites in rodents mainly from Central Chile, little work has been done on gastrointestinal parasites and host determinants in rodents in southern Chile (Landaeta-Aqueveque et al., 2021Landaeta-Aqueveque C, Moreno Salas L, Henríquez A, Silva-de La Fuente MC, González-Acuña D. Parasites of native and invasive rodents in Chile: ecological and human health needs. Front Vet Sci 2021;8: 643742. https://doi.org/10.3389/fvets.2021.643742.
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). Recently, it was described the infestation of trombiculid mites in wild rodents from Chiloé Island and the presence of Orientia spp., that causes the Scrub typhus in humans (Acosta-Jamett et al., 2020Acosta-Jamett G, Martínez-Valdebenito C, Beltrami E, Silva-de La Fuente MC, Jiang J, Richards AL, et al. Identification of trombiculid mites (Acari: Trombiculidae) on rodents from Chiloé island and molecular evidence of infection with orientia species. PLoS Negl Trop Dis 2020; 14(1): e0007619. http://dx.doi.org/10.1371/journal.pntd.0007619. PMid:31971956.
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). However, information about the gastrointestinal parasitic fauna in wild rodents from rural Chiloé Island is still limited. Therefore, the aim of this study was to determine the gastrointestinal parasites in wild rodents inhabiting rural locations from Chiloé Island and assess host determinants (i.e., sex, age, and body mass) on the parasite infection probability, and thus establishing a baseline data on gastrointestinal parasites from wild rodents to better understand how habitat disturbance will impact host-parasite interactions.

Materials and Methods

Study site

A cross-sectional survey was carried out at six rural sites in the north-eastern area of Chiloe Island in Los Lagos Region, during the austral summer (January-February) in 2018. Study locations were detailed previously in Acosta-Jamett et al. (2020)Acosta-Jamett G, Martínez-Valdebenito C, Beltrami E, Silva-de La Fuente MC, Jiang J, Richards AL, et al. Identification of trombiculid mites (Acari: Trombiculidae) on rodents from Chiloé island and molecular evidence of infection with orientia species. PLoS Negl Trop Dis 2020; 14(1): e0007619. http://dx.doi.org/10.1371/journal.pntd.0007619. PMid:31971956.
http://dx.doi.org/10.1371/journal.pntd.0...
(see Figure 1). The study area comprises a highly fragmented rural mosaic of remnant old-growth and secondary forest, bogs, shrublands, exotic plantations, and artificial landscapes, which was shaped by a 200-year fire history of degradation due to logging and forest fire (Willson & Armesto, 1996Willson MF, Armesto JJ. The natural history of Chiloé: on Darwin’s trail. Rev Chil Hist Nat 1996; 69: 149-161.; Gutiérrez et al., 2009Gutiérrez A, Armesto JJ, Aravena J, Carmona M, Carrasco NV, Christie DA, et al. Structural and environmental characterization of old-growth temperate rainforest of northern Chiloé Island, Chile: regional and global relevance. For Ecol Manage 2009; 258(4): 376-388. http://dx.doi.org/10.1016/j.foreco.2009.03.011.
http://dx.doi.org/10.1016/j.foreco.2009....
). Climate is wet-temperate, with an annual mean temperature ranging from 9.1 to 10.8 C (coast: 6.9 -17.6 C; inland: 4.2 - 14.4 C) and annual rainfall of approximately 2000 mm (summer: 13-25% [January-March]) (Gutiérrez et al., 2009Gutiérrez A, Armesto JJ, Aravena J, Carmona M, Carrasco NV, Christie DA, et al. Structural and environmental characterization of old-growth temperate rainforest of northern Chiloé Island, Chile: regional and global relevance. For Ecol Manage 2009; 258(4): 376-388. http://dx.doi.org/10.1016/j.foreco.2009.03.011.
http://dx.doi.org/10.1016/j.foreco.2009....
).

Figure 1
Sampling sites and study area in rural localities of the north-eastern Chiloé Island, Los Lagos Region, Chile.

Sampling sites were selected by convenience under the availability of native forest patches and the nearest human settlements where cases of Scrub typhus had been previously reported (see Acosta-Jamett et al. 2020Acosta-Jamett G, Martínez-Valdebenito C, Beltrami E, Silva-de La Fuente MC, Jiang J, Richards AL, et al. Identification of trombiculid mites (Acari: Trombiculidae) on rodents from Chiloé island and molecular evidence of infection with orientia species. PLoS Negl Trop Dis 2020; 14(1): e0007619. http://dx.doi.org/10.1371/journal.pntd.0007619. PMid:31971956.
http://dx.doi.org/10.1371/journal.pntd.0...
for further details).

Host capture and fecal sampling

Rodents were live-trapped under the approval and supervision of the Agricultural and Livestock Service of Chile in 2017 (Nº 7034-2017) and the Scientific Ethics Committee Resolution for the Animals and Environment Care of the Pontificia Universidad Católica de Chile (Nº 160816007-2017). Animal capture and sampling followed the Standard Operating Procedures for Biosafety by the Center for Disease Control and Prevention (CDC), and for the Use of Wild Mammals in Research and Education by the American Veterinary Medicine Association and American Society of Mammologists (ASM) (CDC, 2012Centers for Disease Control and Prevention - CDC. Guidelines for Safe Work Practices in Human and Animal Medical Diagnostic Laboratories Biosafety. Morbility and Mortality Weekly Report MMWR. USA: U.S. Department of Health and Human Services; 2012.; Sikes & Animal Care and Use Committee of the American Society of Mammalogists, 2016Sikes RS, Animal Care and Use Committee of the American Society of Mammalogists. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 2016; 97(3): 663-688. http://dx.doi.org/10.1093/jmammal/gyw078. PMid:29692469.
http://dx.doi.org/10.1093/jmammal/gyw078...
).

Rodents were captured in Sherman-type live traps (n = 148-175; dimensions = 300 x 100 x 110 mm) baited with oat flakes and vanilla essence. Traps were placed under vegetal material (i.e., scrubs, fallen logs) with a distance of at least 5 meters from each other. Traps were set in the late afternoon and checked in the early morning of the next day. Trapping was conducted for 4/5 nights in each study site, ranging from 668 to 895 trap-night per site. Captured rodents were moved to a central processing tent installed at the sampling site.

After capture, each rodent was placed inside an induction chamber and anesthetized with isoflurane (1 mL isoflurane/500 mL chamber volume). Once individuals were induced (after 1-2 min), animals were classified according to species, sex, age (i.e., juvenile and adults), and reproductive status (Muñoz-Pedreros & Gill, 2009Muñoz-Pedreros A, Gill C. Order Rodentia. In: Pedreros AM, Yañez Valenzuela J, editors. Mamiferos de Chile. Santiago: CEA Ediciones; 2009. p. 93-157.). Morphometric measurements (i.e., body length, tail, and hind-foot [mm]) and weight (gr) were recorded by using a digital caliper (Uberman®, precision 0,01 mm) and a precision digital scale (Pesamatic Newton Series®, Model EJ1500; +0.1 gr SD). Fecal samples (0.05 to 2.0 g.) were opportunistically taken from the anus or collected from the previously disinfected trap base during each morning (08 am - 12 pm) to minimize the effects of temporal variation in parasitic eggs/oocyst shedding (Filipiak et al., 2009Filipiak L, Mathieu F, Moreau J. Caution on the assessment of intestinal parasitic load in studying parasite-mediated sexual selection: the case of Blackbirds coccidiosis. Int J Parasitol 2009; 39(6): 741-746. http://dx.doi.org/10.1016/j.ijpara.2008.11.005. PMid:19100267.
http://dx.doi.org/10.1016/j.ijpara.2008....
). Samples were placed in clean plastic vials with 1.5 mL ethanol (70%) and stored at 4°C. Finally, adult female rodents were marked by a haircut and released at the respective capture points. Male rodents (juveniles or adults) and juvenile females were euthanized by cervical dislocation under anesthetic plane for further chigger collection. Forty-one euthanized rodents were frozen temporally until the extraction of the gastrointestinal tract. Then, the gastrointestinal tract was preserved in ethanol 96% (approximately 70% final dilution) until parasitological examination.

Coprologic examination

A parasitological examination was carried out at the Ecology and Evolution of Infectious Diseases Lab at the Universidad Austral de Chile. Parasite infection of helminth and protozoa was assessed qualitatively and quantitatively by the Mini-FLOTAC method (Mini-FLOTAC®, University of Naples Federico II) (Cringoli et al., 2017Cringoli G, Maurelli MP, Levecke B, Bosco A, Vercruysse J, Utzinger J, et al. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat Protoc 2017; 12(9): 1723-1732. http://dx.doi.org/10.1038/nprot.2017.067. PMid:28771238.
http://dx.doi.org/10.1038/nprot.2017.067...
; Catalano et al., 2019Catalano S, Symeou A, Marsh KJ, Borlase A, Léger E, Fall CB, et al. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasit Vectors 2019; 12(1): 439. http://dx.doi.org/10.1186/s13071-019-3613-6. PMid:31522684.
http://dx.doi.org/10.1186/s13071-019-361...
). Briefly, fecal samples were weighed (Pesamatic Newton Series®, Model EJ1500; +0.1 gr SD) after ethanol removal by centrifugation (5 min at 1200 rpm), and an aliquot of feces (0.1 - 0.3 g) was poured into the Fill FLOTAC® 2 device. Zinc sulfate solution (ZnSO4*7H2O; FS7) was chosen given its previous validation in rodents (Cringoli et al., 2010Cringoli G, Rinaldi L, Maurelli MP, Utzinger J. FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 2010; 5(3): 503-515. http://dx.doi.org/10.1038/nprot.2009.235. PMid:20203667.
http://dx.doi.org/10.1038/nprot.2009.235...
; Catalano et al., 2019Catalano S, Symeou A, Marsh KJ, Borlase A, Léger E, Fall CB, et al. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasit Vectors 2019; 12(1): 439. http://dx.doi.org/10.1186/s13071-019-3613-6. PMid:31522684.
http://dx.doi.org/10.1186/s13071-019-361...
), in which the density of 1.35 was confirmed with a hydrometer (EISCO, New York 14564, US). To determine the multiplication factor, zinc sulfate solution was added in the Fill FLOTAC® until the final volume of 15 mL, as previously described (Catalano et al., 2019Catalano S, Symeou A, Marsh KJ, Borlase A, Léger E, Fall CB, et al. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasit Vectors 2019; 12(1): 439. http://dx.doi.org/10.1186/s13071-019-3613-6. PMid:31522684.
http://dx.doi.org/10.1186/s13071-019-361...
). Subsequently, the mixture was homogenized, dispensed in each of the two chambers of the Mini-FLOTAC® apparatus, and examined after 10 minutes by a microscope (Carl Zeiss 183858 Axiostar, Fisher Scientific, Schwerte DE 58239 Germany) with a digital camera (Axiocam ERc 5s, Carl Zeiss Microscopy, Göttingen 37081, Germany).

Helminth eggs and protozoa cysts/oocysts were identified to genus levels when possible, according to morphological keys (Thienpont et al., 2003Thienpont D, Rochette F, Vanparijs OFJ. Diagnosing helminthiasis by coprological examination. 3rd ed. Beerse: Janssen Animal Health; 2003.; Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.; Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.; Cordeiro et al., 2018Cordeiro HC, Melo FTV, Giese EG, Santos JND. Gongylonema parasites of rodents: A key to species and new data on Gongylonema neoplasticum. J Parasitol 2018; 104(1): 51-59. http://dx.doi.org/10.1645/17-3. PMid:29135391.
http://dx.doi.org/10.1645/17-3...
). A maximum of ten related morphotypes of eggs/oocysts in each positive sample were digitally measured and photographically recorded (length and width; µm) (Zen 3.2 Blue Edition, ZEISS Group, München 81379, Germany). Finally, related morphotypes of eggs and oocyst were counted in each of the positive samples and multiplied by the multiplication factor to obtain fecal egg/oocyst per gram of feces (EPG, OPG), as previously described (Catalano et al., 2019Catalano S, Symeou A, Marsh KJ, Borlase A, Léger E, Fall CB, et al. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasit Vectors 2019; 12(1): 439. http://dx.doi.org/10.1186/s13071-019-3613-6. PMid:31522684.
http://dx.doi.org/10.1186/s13071-019-361...
).

Post-mortem examination

Gastrointestinal tracts of euthanized individuals were examined furtherly under a stereomicroscope (Leica S6D, Leica Microsystems, Heerbrugg CH-9435, Switzerland), and each segment was studied separately (i,e., stomach, small intestine, caecum and large intestine). The presence of Nematodes were examined, and any parasitic form was cleared with lactophenol or ethanol-glycerine and identified under a microscope (Leica DM 1000, Heerbrugg CH-9435, Switzerland) following keys (Anderson et al., 2009Anderson RC, Chabaud AG, Willmott S. Keys to the Nematode Parasites of Vertebrates. Wallinford: CAB International; 2009. http://dx.doi.org/10.1079/9781845935726.0000.
http://dx.doi.org/10.1079/9781845935726....
).

Data analysis

Parasitological parameters such as prevalence, mean intensity, and mean abundance were interpreted and calculated according to Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
for both coprologic and post-mortem examination. In this regard, Prevalence (p) is the number of individuals of a host species infected with a specific parasite type divided by the number of hosts examined, and the 95% confidence interval [CI] was calculated with the Clopper-Pearson method (Clopper & Pearson, 1934Clopper CJ, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 1934; 26(4): 404-413. http://dx.doi.org/10.1093/biomet/26.4.404.
http://dx.doi.org/10.1093/biomet/26.4.40...
).

For the coprologic examination, a proxy for adult parasite intensity was calculated using the number of eggs per gram (EPG) and oocyst per gram (OPG) given that fecal samples were obtained non-invasively, as carried out elsewhere (Wells et al., 2007Wells K, Smales LR, Kalko EKV, Pfeiffer M. Impact of rain-forest logging on helminth assemblages in small mammals (Muridae, Tupaiidae) from Borneo. J Trop Ecol 2007; 23(1): 35-43. http://dx.doi.org/10.1017/S0266467406003804.
http://dx.doi.org/10.1017/S0266467406003...
; Hodder & Chapman, 2012Hodder SAM, Chapman CA. Do nematode infections of red colobus (Procolobus rufomitratus) and black-and-white colobus (Colobus guereza) on humanized forest edges differ from those on nonhumanized forest edges? Int J Primatol 2012; 33(4): 845-859. http://dx.doi.org/10.1007/s10764-012-9619-y.
http://dx.doi.org/10.1007/s10764-012-961...
; Barelli et al., 2020Barelli C, Pafčo B, Manica M, Rovero F, Rosà R, Modrý D, et al. Loss of protozoan and metazoan intestinal symbiont biodiversity in wild primates living in unprotected forests. Sci Rep 2020; 10(1): 10917. http://dx.doi.org/10.1038/s41598-020-67959-7. PMid:32616818.
http://dx.doi.org/10.1038/s41598-020-679...
). The mean intensity (MI) corresponds to the sum of eggs per gram (EPG) and oocysts per gram (OPG) in feces for each parasite type divided by the number of hosts infected with that parasite. The intensity range (RI) was the minimum and the maximum value of load (EPG, OPG) for each morphotype. The mean abundance (MA) is the total number of each isolated parasite egg or oocyst types (EPG, OPG) divided by the number of total analyzed hosts. Also, the mean helminth species richness (MHR) was calculated as the average number of simultaneously present helminth egg types (EPG) in the feces of individual hosts of each species.

For post-mortem examination, the MI corresponds to the number of helminths of a species divided by the number of infected hosts, and the MA is the number of helminths of a species divided by the number of examined hosts (Bush et al., 1997Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
). Given the sample size of host species (n >40) (Shvydka et al., 2018Shvydka S, Sarabeev V, Estruch VD, Cadarso-Suárez C. Optimum sample size to estimate mean parasite abundance in fish parasite surveys. Helminthologia 2018; 55(1): 52-59. http://dx.doi.org/10.1515/helm-2017-0054. PMid:31662627.
http://dx.doi.org/10.1515/helm-2017-0054...
), the CI for MI and MA was calculated only for A. olivacea by the bootstrapping method (2000 replications) using the Quantitative Parasitology online application, QPweb (Reiczigel et al., 2019Reiczigel J, Marozzi M, Fábián I, Rózsa L. Biostatistics for parasitologists-a primer to quantitative parasitology. Trends Parasitol 2019; 35(4): 277-281. http://dx.doi.org/10.1016/j.pt.2019.01.003. PMid:30713051.
http://dx.doi.org/10.1016/j.pt.2019.01.0...
). Additionally, for A. olivacea, the aggregation of adult parasites was assessed by parasite species with the Poulin’s Discrepancy Index using the QPweb.

To establish an approximation for body condition, the Scaled Mass Index (SMI) was calculated (Peig & Green, 2009Peig J, Green AJ. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 2009; 118(12): 1883-1891. http://dx.doi.org/10.1111/j.1600-0706.2009.17643.x.
http://dx.doi.org/10.1111/j.1600-0706.20...
), in which the individual measurements of body weight (Mi) and body length (Li) were inserted into the formula [SMI = Mi×(L0/Li )bSMA]; L0 was the arithmetic mean of body length for each rodent species (i.e., A. olivacea = 81.4; A. manni = 91.9; G. valdivianus = 90.5; I. tarsalis = 81.4; L. micropus = 112; and O. longicaudatus = 82.1), and bSMA was the slope estimate of a standardized major axis (SMA) regression of the mass-length relationship (i.e., bSMA = β OLS/r = 0.48/0.60 = 0.75). Subsequently, the SMI of individuals was categorized into three groups: Low (<40), Medium (40-60), and High (>60) (thereafter called SMI categories), as carried out elsewhere (Pannoni et al., 2022Pannoni SB, Proffitt KM, Holben WE. Non‐invasive monitoring of multiple wildlife health factors by fecal microbiome analysis. Ecol Evol 2022; 12(2): e8564. http://dx.doi.org/10.1002/ece3.8564. PMid:35154651.
http://dx.doi.org/10.1002/ece3.8564...
; Valenzuela et al., 2022Valenzuela PL, Santos-Lozano A, Barrán AT, Fernández-Navarro P, Castillo-García A, Ruilope LM, et al. Joint association of physical activity and body mass index with cardiovascular risk: A nationwide population-based cross-sectional study. Eur J Prev Cardiol 2022; 29(2): e50-e52. http://dx.doi.org/10.1093/eurjpc/zwaa151. PMid:33580798.
http://dx.doi.org/10.1093/eurjpc/zwaa151...
).

Given the sample size of each host species, parasite infection probability of most frequent parasite egg morphotypes (>5% total prevalence) were assessed in relation to host factors (sex, age, SMI, and SMI categories) only for Abrothrix olivacea, by using Generalized linear mixed models (GLMERs) (Bates et al., 2015Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using Ime4. J Stat Softw 2015; 67(1): 1-48. http://dx.doi.org/10.18637/jss.v067.i01.
http://dx.doi.org/10.18637/jss.v067.i01...
). Dependent variables comprised the presence-absence (binomial) of the most prevalent parasite types (>5% total prevalence; ie., Moniliformis sp., Capillariidae, Trichuris sp., Spirurid type eggs, Strongylid type eggs, Rodentolepis sp., coccidia, amoeba, and unidentified protozoa cysts). Fixed effects included host age (juveniles, adults), host sex (male, female), and host body condition (SMI categories [low, medium, high]). Trapping site was included as a random factor to account for the variation due to environmental conditions. The strategy for building the model consisted of an initial screening of each fixed effect (i.e., host age, host sex, and SMI) by obtaining unconditional models. Only variables associated with the outcome (p<0.05) (i.e., host sex and SMI) were eligible for inclusion in the conditional model that was built using a forward variable selection method, including potential interactions. A comparison of the goodness-of-the-fit between different models was assessed using the Akaike Information Criteria (AIC) index. Finally, confounders were evaluated based on their biological significance. Statistical significance was set at p<0.05. The “lme4” and “MASS” packages were used for calculation of models using the software R (R Foundation for Statistical Computing, Vienna, Austria) (R Development CoreTeam, 2013R Development CoreTeam. R: a language and environment for statistical computing [online]. Vienna, Austria: R Foundation for Statistical Computing; 2013. [cited 2021 Jan 8]. Available from: http://www. R-project. org/
http://www. ...
) and RStudio (RStudio Team, 2020RStudio Team. RStudio: Integrated Development for R. RStudio, PBC [online software]. Boston: Rstudio; 2020 [cited 2020 Dec 10]. Available from: http://www.rstudio.com/.
http://www.rstudio.com/...
). Odds Ratio (OR) were calculated by raising the estimates of variables to the exponent using the software R and RStudio (Sommet & Morselli, 2017Sommet N, Morselli D. Keep calm and learn multilevel logistic modeling: a simplified three-step procedure using Stata, R, Mplus, and SPSS. Int Rev Soc Psychol 2017; 30(1): 203-218. http://dx.doi.org/10.5334/irsp.90.
http://dx.doi.org/10.5334/irsp.90...
).

Results

Captured rodent community

Fecal samples were obtained from 174 captured rodents, 134 of which belonged to olive grass mouse (Abrothrix olivacea Waterhouse, 1837), 16 were Chilean climbing mouse (Irenomys tarsalis Philippi, 1900), 12 were Valdivian mole mouse (Geoxus valdivianus Philippi, 1858), five were Mann's Soft-haired Grass mice (Abrothrix manniD’Elía et al., 2015D’Elía G, Teta P, Upham NS, Pardiñas UFJ, Patterson BD. Description of a new soft-haired mouse, genus Abrothrix (Sigmodontinae), from the temperate Valdivian rainforest. J Mammal 2015; 96(4): 839-853. https://doi.org/10.1093/jmammal/gyv103
https://doi.org/10.1093/jmammal/gyv103...
), three were long-tailed colilargo (Oligoryzomys longicaudatus Bennett, 1832), two were southern pericote (Loxodontomys micropus Waterhouse, 1837), one was the brown rat (Rattus norvegicus Berkenhout, 1769), and one could not be classified to species (see Table 1). Of 174 sampled individuals, 112 (64.4%) were males (A. olivacea = 85, I. tarsalis = 12, G. valdivianus = 9, A. manni = 4, L. micropus = 1, and R. norvegicus = 1) and 62 (35.6%) were females (A. olivacea = 49, I. tarsalis = 4, G. valdivianus = 3, O. longicaudatus = 3, A. manni = 1, L. micropus = 1, and non-identified = 1). Likewise, of 174 individuals, 100 (57.5%) were adults (A. olivacea = 77, I. tarsalis = 7, G. valdivianus = 7, A. manni = 3, L. micropus = 2, O. longicaudatus = 2, and R. norvegicus = 1, and non-identified = 1) and 74 (42.5%) were juveniles (A. olivacea = 57, I. tarsalis = 9, G. valdivianus = 5, A. manni = 2, and O. longicaudatus = 1). Body weight of native rodents ranged from 8.5 to 52 g. (weight mean 23.73 ± standard error = 0.9, n = 171). Scaled body mass index of native rodents ranged from 10.5 to 95 (23.34 ± 0.7, n=170), in which 71 individuals were categorised as Low, 66 as Medium, and 33 as High.

Table 1
Captured rodents in North-eastern Chiloé Island, Chile. MSMI (SE) = Mean of scaled body mass index (standard error).

General gastrointestinal parasitism in rodent community

Of the 174 captured individuals, 156 (89.65%) were infected with any gastrointestinal parasite by coprologic and post-mortem examination. One-hundred-twelve individuals (64.4%) harbored helminths, 119 (68.4%) were infected with protozoa, and 74 (42.5%) showed mixed parasitic infection.

Coprologic findings

The overall parasite prevalence, mean intensity, intensity range, mean abundance, and mean helminth richness are shown in Table 2.

Table 2
Parasitological parameters of gastrointestinal morphotypes obtained from fecal samples of rodents collected in Chiloé Island. Prevalence (P) and 95% confidence intervals (CI), mean intensity (MI), intensity range (RI), mean abundance (MA), and mean helminth richness (MHR) are reported.

Morphotypes of helminth eggs included Rodentolepis spp. (size mean ± standard error = 42.9 ± 0.6 µm length, 27.2 ± 0.5 µm width; n =118; Fig. 2ab), Capillariidae eggs (65.3 ± 0.9 µm, 30.6 ± 0.6 µm; n = 22; Figure 2c), Trichuris sp. (65.6 ± 0.6 µm, 33.9 ± 0.6 µm; n =20; Figure 2d), Syphacia sp. (121.7 ± 7.8 µm, 39.5 ± 4.6 µm; n =10; Figure 2e), oxyurid-type 1 egg (100.5 µm, 28 µm width; n = 1; Figure 2f), oxyurid-type 2 eggs (128 ± 5.6 µm, 35.6 ± 11.1 µm; n = 3; Figure 2g), Strongyloides sp. (51.7 ± 3.2 µm, 28.3 ± 0.7 µm; n =29; Figure 2i), Spirurid-type eggs (42.8 ± 0,4 µm, 26.9 ± 0,3 µm; n =242; Figure 2j), Strongylid-type eggs (56.5 ± 0.7 µm, 32.5 ± 0.5 µm; n =184; Figure 2k), Moniliformis sp. (59.5 ± 0.5 µm, 34.4 ± 0.4 µm; n = 81; Figure 2l), and unidentified nematode egg (137.23 µm x 21.45 µm; n=1; Figure 2h) and larvae. Protozoa comprised sporulated and non-sporulated coccidia oocysts (19.1 ± 0.2 µm, 15.5 ± 0.2 µm; n =446; Figure 2m-q), amoeba cysts (38.9 ± 2.3 µm, 24.8 ± 1.4 µm; n = 22; Figure 2r), and unidentified protozoa cysts (30 ± 1.4 µm, 24.6 ± 1.3 µm; n = 65) (see Figure 2).

Figure 2
Gastrointestinal parasites in wild rodents in Chiloé Island, Chile (400x): (a-b) Rodentolepis spp. in Abrothrix olivacea and Geoxus valdivianus, (c) Capillariidae in A. olivacea, (d) Trichuris sp. in A. olivacea, (e) Syphacia sp. in A. olivacea, (f-g) oxyurid type eggs in A. olivacea, (h) Unidentified nematode egg in G. valdivianus, (i) Strongyloides sp., in A. olivacea, G. valdivianus, and Irenomys tarsais, (j) Spirurid-type egg in A. olivacea, A. manni, G. valdivianus, and I. tarsalis, (k) Strongylid-type eggs in A. olivacea, G. valdivianus, I. tarsalis, and Oligoryzomys longicaudatus, (l) Moniliformis sp. in A. olivacea, A. manni and G. valdivianus, (m-o) sporulated coccidia oocysts in A. olivacea, A. manni, G. valdivianus and Loxodontomys micropus, (p-q) unsporulated coccidia oocysts in all studied species. (r) Amoeba cyst in A. olivacea, G. valdivianus, and Rattus norvegicus. Bar 10 µm.

In A. olivacea, the most frequent helminth egg morphotypes were Spirurid-type eggs, and the most abundant was Moniliformis sp. In I. tarsalis, the most frequent helminth eggs were strongilid-type eggs, and the most abundant was Strongyloides sp. In G. valdivianus, strongilid-type eggs were the most frequent, and Moniliformis sp. eggs were the most abundant. Concerning protozoa, coccidia oocysts were the most frequent and abundant in all rodent species, with exception of R. norvegicus, in which amoeba cysts were more abundant. A. olivacea and A. manni exhibited the highest mean helminth richness (2).

Post-mortem findings

A total of 41 rodents were euthanized and examined for gastrointestinal parasites, 33 of which involved A. olivacea, six G. valdivianus, one L. micropus, and one O. longicaudatus.

Four helminth taxa were found: Protospirura sp., Physaloptera sp., Syphacia sp. and Trichuris sp. by post-mortem examination of gastrointestinal tracts (Figure 3). The estimation of the ecological parameters (p% [Confidence interval], MI, and MA is shown in Table 3. Confidence intervals for intensity and abundance and the Poulin’s discrepancy index were estimated only for A, olivacea due to sample size (n>30) (Shvydka et al., 2018Shvydka S, Sarabeev V, Estruch VD, Cadarso-Suárez C. Optimum sample size to estimate mean parasite abundance in fish parasite surveys. Helminthologia 2018; 55(1): 52-59. http://dx.doi.org/10.1515/helm-2017-0054. PMid:31662627.
http://dx.doi.org/10.1515/helm-2017-0054...
). In G. valdivianus one Physaloptera sp. and four Protospirura sp. were found in the same individual, and 12 Syphacia sp. were found in another individual. A single Syphacia sp. specimen was found in one O. longicaudatus and no worms were found in the L. micropus.

Figure 3
Gastrointestinal helminths extracted from Abrothrix olivacea in Chiloé Island, Chile: (a) Physaloptera sp. anterior end, ventral view; (b) Protospirura sp. anterior end, lateral view; (c) Trichuris sp. posterior end, lateral view; (d) Syphacia sp. anterior end, lateral view. Bar: (a) = 0.15mm; (b,c,d) = 0.3 mm.
Table 3
Parasitological descriptors of gastrointestinal adult parasites of rodents subjected to post-mortem examination in Chiloé, Chile. Sample size (N), number of positive individuals (+), percent prevalence (P) and 95% confidence intervals (CI), mean intensity (MI), mean abundance (MA), and the Poulin’s Discrepancy Index (PDI) are reported.

Host factors associated with gastrointestinal parasite infection probability of parasite egg/cyst morphotypes in Abrothrix olivacea

Prevalence of most frequent parasite eggs/cysts morphotypes (>5% total prevalence) in A. olivacea by age, sex, and scaled body mass index categories (SMI) are shown in Table 4. For GLMER unconditional models to assess the probability of infection, the presence/absence of Strongylid-type eggs were associated with age (p<0.001) and SMI category (p<0.001). Also, Spirurid-type eggs were associated with age (p<0.01) and SMI categories (p<0.05). The infection status with Capillariidae, Trichuris sp., Rodentolepis spp., Moniliformis sp., coccidia, Amoeba, and unidentified protozoa cysts were not statistically related to any host factor (i.e., sex, age, and SMI categories) (GLMER, p>0.05). The GLMER conditional models included the variables primarily associated with the infection status (i.e., host age and SMI) as fixed effects and the trapping site as random effect. After simplification of models, results exhibited statistical significance only for the SMI categories (p<0.05) for both Strongylid-type eggs and Spirurid-type eggs. No interaction or confounding effects were found to be statistically significant (e.g., SMI*AGE; SMI+AGE). Values of Odds ratio, CI 95%, and AIC index regarding the SMI categories are shown in Table 5. For Strongilid-like eggs and Spirurid-like eggs, results suggest that individuals with low Scaled Mass Index exhibited a lower risk of infection in comparison with the other SMI categories.

Table 4
Prevalence of most frequent parasite eggs/cysts morphotypes (>5% total prevalence) in Abrothrix olivacea in Chiloe Island by age, sex, and scaled body mass index categories (SMI).
Table 5
Generalized linear mixed models with binomial error showing the scaled mass index (SMI) categories as a factor for the parasitic infection with Spirurid-type eggs and Strongylid-type eggs in Abrothrix olivacea (n = 134). Random factor = trapping site.

Discussion

In the present study, it was found gastrointestinal parasites of six native (Cricetidae family: A. olivacea, I. tarsalis, G. valdivianus, A. manni, L. micropus, O. longicaudatus) and one introduced rodent species (Muridae family: R. norvegicus) in rural areas from Northern Chiloe, Chile. All native rodent species in this study were expected to be sampled according to species distribution (Muñoz-Pedreros & Gill, 2009Muñoz-Pedreros A, Gill C. Order Rodentia. In: Pedreros AM, Yañez Valenzuela J, editors. Mamiferos de Chile. Santiago: CEA Ediciones; 2009. p. 93-157.; D’Elía et al., 2015).

Helminth egg morphotypes and adult specimens found in this study have been previously recorded in rodents in Chile, with exception of Trichuris sp. in A. olivacea, Strongyloides sp. in A. olivacea, G. valdivianus, and I. tarsais, Physaloptera sp., Protospirura sp., and Rodentolepis sp. in G. valdivianus; and, Moniliformis sp. in A. manni taking into consideration that the latter rodent species was recently described (Ruiz del Río, 1939Ruiz del Río A. Contribución al estudio de las enfermedades parasitarias humanas transmitidas por las ratas en Concepción. Bol Soc Biol Concepc 1939; 13: 47-82.; Babero et al., 1975Babero BB, Cattan PE, Cabello C. Trichuris bradleyi sp. n., a Whipworm from Octodon degus in Chile. J Parasitol 1975; 61(6): 1061-1063. http://dx.doi.org/10.2307/3279376. PMid:1195067.
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; Babero et al., 1976Babero BB, Cattan PE, Cabello C. A new species of whipworm from the rodent Akodon longipilis in Chile. Trans Am Microsc Soc 1976; 95(2): 232-235. http://dx.doi.org/10.2307/3225071. PMid:1274050.
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; Babero & Murua, 1987Babero BB, Murua R. The helminth fauna of Chile. X. A new species of whipworm from a Chilean rodent. Trans Am Microsc Soc 1987; 106(2): 190-193. http://dx.doi.org/10.2307/3226320.
http://dx.doi.org/10.2307/3226320...
; Cattan et al., 1992Cattan PE, Núñez H, Yáñez J. Comunidades de parásitos en roedores: una comparación entre octodontinos y cricétidos. Bol Mus Nac Hist Nat [online]. 1992; 43: 93-103. [cited 2021 Jan 8]. Available from: https://publicaciones.mnhn.gob.cl/668/articles-64984_archivo_01.pdf
https://publicaciones.mnhn.gob.cl/668/ar...
; Landaeta-Aqueveque et al., 2007aLandaeta-Aqueveque C, Robles MDR, Cattan PE. The community of gastrointestinal helminths in the housemouse, Mus musculus, in Santiago, Chile. Parasitol Latinoam 2007a; 62(3-4): 165-169. http://dx.doi.org/10.4067/s0717-77122007000200010.
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, 2007bLandaeta-Aqueveque C, Robles MDR, Cattan PE. Helmintofauna del roedor Abrothrix olivaceus (Sigmodontinae) en áreas sub-urbanas de Santiago de Chile. Parasitol Latinoam 2007b; 62(3-4): 134-141. http://dx.doi.org/10.4067/S0717-77122007000200006.
http://dx.doi.org/10.4067/S0717-77122007...
; Landaeta-Aqueveque et al., 2014Landaeta-Aqueveque C, Notarnicola J, Correa JP, Yáñez-Meza A, Henríquez A, Cattan PE, et al. First record of Litomosoides pardinasi (Nematoda: Onchocercidae) in native and exotic rodents from Chile. Rev Mex Biodivers 2014; 85(4): 1032-1037. http://dx.doi.org/10.7550/rmb.44711.
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; Seguel et al., 2017Seguel M, Muñoz F, Paredes E, Navarrete MJ, Gottdenker NL. Pathological Findings in Wild Rats (Rattus rattus) Captured at Guafo Island, Northern Chilean Patagonia. J Comp Pathol 2017; 157(2-3): 163-173. http://dx.doi.org/10.1016/j.jcpa.2017.07.006. PMid:28942299.
http://dx.doi.org/10.1016/j.jcpa.2017.07...
; Digiani et al., 2017Digiani MC, Landaeta-Aqueveque C, Serrano PC, Notarnicola J. Pudicinae (Nematoda: Heligmonellidae) Parasitic in Endemic Chilean Rodents (Caviomorpha: Octodontidae and Abrocomidae): Description of a New Species and Emended Description of Pudica degusi (Babero and Cattan) n. comb. J Parasitol 2017; 103(6): 736-746. http://dx.doi.org/10.1645/17-81. PMid:28862918.
http://dx.doi.org/10.1645/17-81...
; Landaeta-Aqueveque et al., 2018Landaeta-Aqueveque C, Robles MDR, Henríquez A, Yáñez-Meza A, Correa JP, González-Acuña D, et al. Phylogenetic and ecological factors affecting the sharing of helminths between native and introduced rodents in Central Chile. Parasitology 2018; 145(12): 1570-1576. http://dx.doi.org/10.1017/S0031182018000446. PMid:29886859.
http://dx.doi.org/10.1017/S0031182018000...
; Yáñez-Meza et al., 2019Yáñez-Meza A, Landaeta-Aqueveque C, Quiroga N, Botto-Mahan C. Helminthic infection in three native rodent species from a semiarid Mediterranean ecosystem. Rev Bras Parasitol Vet 2019; 28(1): 119-125. http://dx.doi.org/10.1590/s1984-29612019014. PMid:30916258.
http://dx.doi.org/10.1590/s1984-29612019...
; Riquelme et al., 2021Riquelme M, Salgado R, Simonetti J, Landaeta-Aqueveque C, Fredes F, Rubio AV. Intestinal helminths in wild rodents from native forest and exotic pine plantations (Pinus radiata) in Central Chile. Animals (Basel) 2021; 11(2): 384. http://dx.doi.org/10.3390/ani11020384. PMid:33546281.
http://dx.doi.org/10.3390/ani11020384...
; D’Elía et al., 2015D’Elía G, Teta P, Upham NS, Pardiñas UFJ, Patterson BD. Description of a new soft-haired mouse, genus Abrothrix (Sigmodontinae), from the temperate Valdivian rainforest. J Mammal 2015; 96(4): 839-853. https://doi.org/10.1093/jmammal/gyv103
https://doi.org/10.1093/jmammal/gyv103...
). Overall, the prevalence of each parasite type eggs described in this study was higher than those detailed previously, with exception of Syphacia sp. in A. olivacea (i.e, 3.7% < Syphacia phyllotios = 13.6%) (Yáñez-Meza et al., 2019Yáñez-Meza A, Landaeta-Aqueveque C, Quiroga N, Botto-Mahan C. Helminthic infection in three native rodent species from a semiarid Mediterranean ecosystem. Rev Bras Parasitol Vet 2019; 28(1): 119-125. http://dx.doi.org/10.1590/s1984-29612019014. PMid:30916258.
http://dx.doi.org/10.1590/s1984-29612019...
). Variations in parasite prevalence among studies may be related to different sample size, geographical features, season sampling, and diagnosis methods (Lyles & Dobson, 1993Lyles AM, Dobson AP. Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J Zoo Wildl Med 1993; 24(3): 315-326.; Morand, 2015Morand S. (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. Int J Parasitol Parasites Wildl 2015; 4(1): 80-87. http://dx.doi.org/10.1016/j.ijppaw.2015.01.001. PMid:25830109.
http://dx.doi.org/10.1016/j.ijppaw.2015....
; Barelli et al., 2021Barelli C, Gonzalez-Astudillo V, Mundry R, Rovero F, Heistermann M, Hauffe HC, et al. Correction: altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. PLoS One 2021; 16(5): e0251617. http://dx.doi.org/10.1371/journal.pone.0251617. PMid:33956911.
http://dx.doi.org/10.1371/journal.pone.0...
). To the best author’s knowledge, this is the first time that the Mini-FLOTAC® method was used in rodents in Chile, which have shown to have increased sensitivity (i.e., 90%) in comparison to other non-invasive coprological techniques such as formol-ether concentration (60%) (Barda et al., 2013Barda BD, Rinaldi L, Ianniello D, Zepherine H, Salvo F, Sadutshang T, et al. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Negl Trop Dis 2013; 7(8): e2344. http://dx.doi.org/10.1371/journal.pntd.0002344. PMid:23936577.
http://dx.doi.org/10.1371/journal.pntd.0...
; Catalano et al., 2019Catalano S, Symeou A, Marsh KJ, Borlase A, Léger E, Fall CB, et al. Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs. Parasit Vectors 2019; 12(1): 439. http://dx.doi.org/10.1186/s13071-019-3613-6. PMid:31522684.
http://dx.doi.org/10.1186/s13071-019-361...
). However, comparisons of infection prevalence of parasite species in each host should be made with caution due to the reduced sample size per rodent species in the present study.

Spirurid-type eggs were observed in A. olivacea, A. manni, G. valdivianus, and I. tarsalis. Spirurid-type eggs were elliptical with thick shells containing well-formed larvae (Figure 2j). Regarding post-mortem analysis from 41 rodents, Spiruridae: Physaloptera sp. and Protospirura sp. were determined in A. olivacea and G. valdivianus. Physalotera sp. was identified based on the presence of two pseudolabia with a group of dentiform lobes on their middle superior margin and submedian papillae at their base (Figure 3a), and Protospirura sp. in accordance with the two large pseudolabia, each divided in three lobes (Figure 3b) and a pharynx slightly lined with chitin (Anderson et al., 2009Anderson RC, Chabaud AG, Willmott S. Keys to the Nematode Parasites of Vertebrates. Wallinford: CAB International; 2009. http://dx.doi.org/10.1079/9781845935726.0000.
http://dx.doi.org/10.1079/9781845935726....
). On previous records, Physaloptera calnuensis was identified in A. olivacea and Mus musculus in Santiago, Chile (Landaeta-Aqueveque et al., 2007aLandaeta-Aqueveque C, Robles MDR, Cattan PE. The community of gastrointestinal helminths in the housemouse, Mus musculus, in Santiago, Chile. Parasitol Latinoam 2007a; 62(3-4): 165-169. http://dx.doi.org/10.4067/s0717-77122007000200010.
http://dx.doi.org/10.4067/s0717-77122007...
, bLandaeta-Aqueveque C, Robles MDR, Cattan PE. Helmintofauna del roedor Abrothrix olivaceus (Sigmodontinae) en áreas sub-urbanas de Santiago de Chile. Parasitol Latinoam 2007b; 62(3-4): 134-141. http://dx.doi.org/10.4067/S0717-77122007000200006.
http://dx.doi.org/10.4067/S0717-77122007...
). Also, eggs of Physaloptera sp. were identified in A. longipilis, O. longicaudatus, and P. darwini in Central Chile (Riquelme et al., 2021Riquelme M, Salgado R, Simonetti J, Landaeta-Aqueveque C, Fredes F, Rubio AV. Intestinal helminths in wild rodents from native forest and exotic pine plantations (Pinus radiata) in Central Chile. Animals (Basel) 2021; 11(2): 384. http://dx.doi.org/10.3390/ani11020384. PMid:33546281.
http://dx.doi.org/10.3390/ani11020384...
). Additionally, Protospirura numidicola was reported in A. longipilis at Las Chinchillas National Reserve (Landaeta-Aqueveque et al., 2018Landaeta-Aqueveque C, Robles MDR, Henríquez A, Yáñez-Meza A, Correa JP, González-Acuña D, et al. Phylogenetic and ecological factors affecting the sharing of helminths between native and introduced rodents in Central Chile. Parasitology 2018; 145(12): 1570-1576. http://dx.doi.org/10.1017/S0031182018000446. PMid:29886859.
http://dx.doi.org/10.1017/S0031182018000...
) and Protospirura sp. in A. olivacea and A. longipilis in Lago Peñuelas, Auco and Fray Jorge National Park (Cattan et al., 1992Cattan PE, Núñez H, Yáñez J. Comunidades de parásitos en roedores: una comparación entre octodontinos y cricétidos. Bol Mus Nac Hist Nat [online]. 1992; 43: 93-103. [cited 2021 Jan 8]. Available from: https://publicaciones.mnhn.gob.cl/668/articles-64984_archivo_01.pdf
https://publicaciones.mnhn.gob.cl/668/ar...
). Other Spiruridae genera previously reported in Chile include Gongylonema neoplasticum in introduced Rattus sp. in Concepción (Landaeta-Aqueveque et al., 2021Landaeta-Aqueveque C, Moreno Salas L, Henríquez A, Silva-de La Fuente MC, González-Acuña D. Parasites of native and invasive rodents in Chile: ecological and human health needs. Front Vet Sci 2021;8: 643742. https://doi.org/10.3389/fvets.2021.643742.
https://doi.org/10.3389/fvets.2021.64374...
), as well as Gongylonema sp. in A. longipilis at the Fray Jorge National Park, and Pterygodermatites sp. in A. olivacea in Lago Peñuelas (Cattan et al., 1992Cattan PE, Núñez H, Yáñez J. Comunidades de parásitos en roedores: una comparación entre octodontinos y cricétidos. Bol Mus Nac Hist Nat [online]. 1992; 43: 93-103. [cited 2021 Jan 8]. Available from: https://publicaciones.mnhn.gob.cl/668/articles-64984_archivo_01.pdf
https://publicaciones.mnhn.gob.cl/668/ar...
). The life cycle of Spiruridae requires arthropods as intermediate hosts (e.g., coprophagous beetles or cockroaches), in which once eggs are ingested, they hatch and become infective, and rodents are infected through ingestion of the intermediate hosts (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). In addition, the acanthocephalan Moniliformis sp. was found in A. olivacea, G. valdivianus, and A. manni. Eggs were featured with elongated-oval shape with three membranes (size = 59.5 × 34.4 µm) (Figure 2l). Dimensions agree with M. clarki (50-90 × 30-50 µm) and M. spiralis (60 × 30 µm) found in Muridae rodents in Missouri-US, and Birmania, respectively (Amin & Pitts, 1966Amin OM, Pitts RM. Moniliformis clarki (Acanthocephala: Moniliformidae) from the Pocket Gopher, Geomys bursarius missouriensis, in Missouri. J Helminthol Soc Wash 1966; 63(1): 144-145.; Guerreiro Martins et al., 2017Guerreiro Martins NB, Del Rosario Robles M, Navone GT. A new species of Moniliformis from a Sigmodontinae rodent in Patagonia (Argentina). Parasitol Res 2017; 116(8): 2091-2099. http://dx.doi.org/10.1007/s00436-017-5508-9. PMid:28585077.
http://dx.doi.org/10.1007/s00436-017-550...
), and were slightly larger than M. amini, described in A. olivacea in Santa Cruz, Argentina (Guerreiro Martins et al., 2017Guerreiro Martins NB, Del Rosario Robles M, Navone GT. A new species of Moniliformis from a Sigmodontinae rodent in Patagonia (Argentina). Parasitol Res 2017; 116(8): 2091-2099. http://dx.doi.org/10.1007/s00436-017-5508-9. PMid:28585077.
http://dx.doi.org/10.1007/s00436-017-550...
). Moniliformis spp. require arthropods as intermediate hosts to develop the infective cystacanth stage that subsequently is ingested by the definitive rodent host (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Also, Rodentolepis spp. (syn. Hymenolepis) was found in A. olivacea and G. valdivianus. Eggs of Rodentolepis spp. were elliptical with a smooth clear shell wall that contain an hexacanth embryo with six hooks (Figure 1ab). The length of observed Rodentolepis spp. eggs were in accordance with dimensions for R. nana (i.e., 40-45 µm), but the width was slightly smaller (34-37 µm ≠ 27.2 µm) (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.). Also, observed Rodentolepis spp. eggs were slightly longer and thinner in comparison to that reported on R. octocoronata (37.3 um; 30.6 um) in Myocastor coypus in Argentina (Sutton, 1974Sutton CA. Contribución al conocimiento de la fauna parasitológica Argentina, Rodentolepis octocoronata (von Linstow, 1879)(Cestoda-Hymenolepididae). Neotropica 1974; 20(63): 145-148.). The R. nana can exhibit direct and indirect life cycles, in which flour beetles or fleas can serve as intermediate hosts (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Rodent species in this study may have become infected with Spiruridae, Moniliformis sp. and Rodentolepis spp., since their diet include arthropods, insect larvae, annelids, and other invertebrates (Meserve et al., 1988Meserve PL, Lang BK, Patterson BD. Trophic relationships of small mammals in a Chilean temperate rainforest. J Mammal 1988; 69(4): 721-730. http://dx.doi.org/10.2307/1381627.
http://dx.doi.org/10.2307/1381627...
; Silva, 2005Silva SI. Posiciones tróficas de pequeños mamíferos en Chile: una revisión. Rev Chil Hist Nat 2005; 78(3): 589-599. http://dx.doi.org/10.4067/S0716-078X2005000300013.
http://dx.doi.org/10.4067/S0716-078X2005...
; Muñoz-Pedreros & Gill, 2009Muñoz-Pedreros A, Gill C. Order Rodentia. In: Pedreros AM, Yañez Valenzuela J, editors. Mamiferos de Chile. Santiago: CEA Ediciones; 2009. p. 93-157.).

Trichuris sp. and Capillariidae were found only in A. olivacea. The former was identified in both coprologic and post-mortem examination. The shape and dimensions of Trichuris sp. and Capillarid-like eggs (Figure 2cd) agree with those cited in the literature, exhibiting bipolar plugs with thick shell (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.; Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Adults specimens of Trichuris sp. were identified based on a body with a thin anterior part presenting the stichosoma and a thick posterior portion presenting the reproductive and digestive organs, and a characteristic long spicula covered by a specular sheet (Figure 3c) (Anderson et al., 2009Anderson RC, Chabaud AG, Willmott S. Keys to the Nematode Parasites of Vertebrates. Wallinford: CAB International; 2009. http://dx.doi.org/10.1079/9781845935726.0000.
http://dx.doi.org/10.1079/9781845935726....
). Previously, Capillaria sp. had been reported in A. olivacea in Chile Central, and Calodium hepaticum in R. norvegicus (Landaeta-Aqueveque et al., 2021Landaeta-Aqueveque C, Moreno Salas L, Henríquez A, Silva-de La Fuente MC, González-Acuña D. Parasites of native and invasive rodents in Chile: ecological and human health needs. Front Vet Sci 2021;8: 643742. https://doi.org/10.3389/fvets.2021.643742.
https://doi.org/10.3389/fvets.2021.64374...
; Riquelme et al., 2021Riquelme M, Salgado R, Simonetti J, Landaeta-Aqueveque C, Fredes F, Rubio AV. Intestinal helminths in wild rodents from native forest and exotic pine plantations (Pinus radiata) in Central Chile. Animals (Basel) 2021; 11(2): 384. http://dx.doi.org/10.3390/ani11020384. PMid:33546281.
http://dx.doi.org/10.3390/ani11020384...
). Conversely, no reports are found about Trichuris sp. in A. olivacea in Chile, but they have been found in other native and introduced species (e.g., T. chilensis in A. longipilis, and Trichuris muris in Mus musculus) (Landaeta-Aqueveque et al., 2021Landaeta-Aqueveque C, Moreno Salas L, Henríquez A, Silva-de La Fuente MC, González-Acuña D. Parasites of native and invasive rodents in Chile: ecological and human health needs. Front Vet Sci 2021;8: 643742. https://doi.org/10.3389/fvets.2021.643742.
https://doi.org/10.3389/fvets.2021.64374...
). Trichuris spp. and some Capillaria spp. show direct life cycles, in which eggs require optimal environmental conditions to embryonate and reach the infective stage (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Rodents become infected by eating the infective stages on the ground, by cannibalism, or predation in case of C. hepaticum (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.).

Syphacia sp. was found in A. olivacea by examination of both feces and gastrointestinal tracts, and in G. valdivianus only by post-mortem analysis. Moreover, two oxyurid-type eggs (Figure 2f-g) were isolated from fecal samples of A. olivacea. Syphacia sp. eggs (Figure 2e) exhibited smooth clear shell walls with dimensions that concur with morphological keys (Syphacia = 100-142 × 30-40 µm) (Thienpont et al., 2003Thienpont D, Rochette F, Vanparijs OFJ. Diagnosing helminthiasis by coprological examination. 3rd ed. Beerse: Janssen Animal Health; 2003.; Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.), being slightly smaller than S. obvelata previously reported in Mus musculus in Chile (Landaeta-Aqueveque et al., 2007bLandaeta-Aqueveque C, Robles MDR, Cattan PE. Helmintofauna del roedor Abrothrix olivaceus (Sigmodontinae) en áreas sub-urbanas de Santiago de Chile. Parasitol Latinoam 2007b; 62(3-4): 134-141. http://dx.doi.org/10.4067/S0717-77122007000200006.
http://dx.doi.org/10.4067/S0717-77122007...
), but similar to S. obvelata previously described in A. olivacea (Landaeta-Aqueveque et al., 2007aLandaeta-Aqueveque C, Robles MDR, Cattan PE. The community of gastrointestinal helminths in the housemouse, Mus musculus, in Santiago, Chile. Parasitol Latinoam 2007a; 62(3-4): 165-169. http://dx.doi.org/10.4067/s0717-77122007000200010.
http://dx.doi.org/10.4067/s0717-77122007...
), and S. phyllotios in Phyllotis darwini (Quentin et al., 1979Quentin JC, Babero BB, Cattan PE. Helminthofaune du Chili. V. Syphacia (Syphacia) phyllotios n. sp., novel Oxyure d’un Rongeur Cricétidé au Chili. Bull Mus Natl Hist Nat, 4e Sér 1979; 1(2): 323-327.) and in A. olivacea (Yáñez-Meza et al., 2019Yáñez-Meza A, Landaeta-Aqueveque C, Quiroga N, Botto-Mahan C. Helminthic infection in three native rodent species from a semiarid Mediterranean ecosystem. Rev Bras Parasitol Vet 2019; 28(1): 119-125. http://dx.doi.org/10.1590/s1984-29612019014. PMid:30916258.
http://dx.doi.org/10.1590/s1984-29612019...
). On post-mortem examination, Syphacia sp. was identified in A. olivacea and G. valdivianus based on the presence of a muscular oesophagus ended in a oesophageal bulb, three labia on the mouth, vulva in the anterior part of the body short after the oesophageal bulb (figure 3d) and characteristic banana-shaped eggs with a subterminal operculum. The life cycle of oxyurids is direct, in which females deposit embryonated eggs on the perineal skins of hosts, and transmission occurs through ingestion of eggs in the perineum, by contaminated food, or when eggs hatch in the perineal region and migrate back via the anus (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Additionally, Strongyloides sp., was determined in I. tarsalis, A. olivacea and G. valdivianus. Eggs of Strongyloides sp. exhibited fully formed larvae with a thin shell (Figure 2i). Dimensions of observed eggs agree with reports for the species (40-60 × 32-40 µm) (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.). Strongyloides ratti has been previously recorded in Rattus sp. in Concepción (Ruiz del Río, 1939Ruiz del Río A. Contribución al estudio de las enfermedades parasitarias humanas transmitidas por las ratas en Concepción. Bol Soc Biol Concepc 1939; 13: 47-82.; Landaeta-Aqueveque et al., 2021Landaeta-Aqueveque C, Moreno Salas L, Henríquez A, Silva-de La Fuente MC, González-Acuña D. Parasites of native and invasive rodents in Chile: ecological and human health needs. Front Vet Sci 2021;8: 643742. https://doi.org/10.3389/fvets.2021.643742.
https://doi.org/10.3389/fvets.2021.64374...
). Strongyloides spp. has a direct life cycle which involves both parasitic and free-living reproductive cycles (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Eggs pass in feces and hatch in the environment where first-stage larvae are released and can develop into the infective third/stage larvae (termed homogonic development) or develop into free-living males and females. Subsequently, adults can mate and their progeny complete moults in the environment until they reach the infective larval stage (L3) (heterogonic development) (Viney, 1999Viney ME. Exploiting the Life Cycle of Strongyloides ratti. Parasitol Today 1999; 15(6): 231-235. http://dx.doi.org/10.1016/S0169-4758(99)01452-0. PMid:10366829.
http://dx.doi.org/10.1016/S0169-4758(99)...
). Hosts become infected via ingestion or penetration of the skin. Although, trans mammary infection also occurs (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.). I. tarsalis may be inhabiting locations where environmental conditions are appropriate for the development and survival of parasitic stages of Strongyloides sp., thus promoting high parasite burden in individuals. Also, strongilid morphotype eggs were isolated in G. valdivianus, I. tarsais, A. olivacea and O. longicaudatus. Observed eggs of strongilids were thin-shelled and contain morula (Figure 2k). In Chile, records of Strongylida in Cricetidae rodents are available including Inglamidium akodon (A. olivacea), Stilestrongylus manni (A. olivacea and O. longicaudatus), and Stilestrongylus valdivianus (L. micropus) (Durette-Desset et al., 1976Durette-Desset M-C, Denke MA, Murua R. Presence in a rodent of Chili of the nematode Inglamidinae (sub. fam. nov.) belonging to Amidostomatidae, a family known to be found in mammals of Australia. Ann Parasitol Hum Comp 1976; 51(4): 453-460. http://dx.doi.org/10.1051/parasite/1976514453. PMid:984673.
http://dx.doi.org/10.1051/parasite/19765...
; Denke & Murua, 1977Denke MA, Murua R. Description de Stilestrongylus manni n. sp. (Nematoda : Heligmosomidae) parasite de différents Cricétidés du Chili. Bull Mus Natl Hist Nat, 4e Sér 1977; 3: 127-131.; Durette-Desset & Murua, 1979Durette-Desset M-C, Murua R. Description de Stilestrongylus valdivianus n. sp. (Nematoda, Heligmonellidae), parasite d’un Cricétidé du Chili. Bull Mus Natl Hist Nat 4e Ser 1979; A(1): 245-249.; Landaeta-Aqueveque et al., 2021Landaeta-Aqueveque C, Moreno Salas L, Henríquez A, Silva-de La Fuente MC, González-Acuña D. Parasites of native and invasive rodents in Chile: ecological and human health needs. Front Vet Sci 2021;8: 643742. https://doi.org/10.3389/fvets.2021.643742.
https://doi.org/10.3389/fvets.2021.64374...
). Regarding life cycle of Strongylida, eggs are released in feces and develop the infective larvae (L3) in the environment that hosts have to ingest to become infected (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.).

Coccidia was common in all studied rodent species. Although most of the observed coccidia oocysts were unsporulated which made it difficult to identify to species level, some oocysts and sporocysts did show sporulation. A coccidia cyst morphotype (Figure 2m) found in A. olivacea, A. manni, G. valdivianus and L. micropus presented clear cyst wall with banana-shaped sporozoites and residual body (19.2 × 13.5 µm), which resemble Sarcocystis sp. sporocysts (Size = 7-22 × 3-15 µm) (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Also, oocysts (Figure 2n-o) found in A. olivacea contained two sporocysts with no evident stieda body, which suggest Isospora-like oocysts (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.). In Valdivia Chile, Giardia muris (36.8%), Hexamita muris (38.6%), Trichomonas muris (15.8%), and Eimeria sp. (26.3%) have been recorded in synanthropic rodents (n=57) (Franjola T. et al., 1995Franjola R, Soto G, Montefusco A. Prevalence of protozoa infections in synanthropic rodents in Valdivia City, Chile. Bol Chil Parasitol 1995; 50(3-4): 66-72. PMid:8762669.). Extraintestinal stages of Sarcocystidae have been found in Thylamys spp. opossums in northern Chile (Santodomingo et al., 2022Santodomingo AM, Thomas RS, Quintero-Galvis JF, Echeverry-Berrio DM, la Fuente MCS, Moreno-Salas L, et al. Apicomplexans in small mammals from Chile, with the first report of the Babesia microti group in South American rodents. Parasitol Res 2022; 121(3): 1009-1020. http://dx.doi.org/10.1007/s00436-022-07452-4. PMid:35102466.
http://dx.doi.org/10.1007/s00436-022-074...
). However, to the best authors’ knowledge, Sarcocystis sp. and Isospora sp. oocysts have not been reported in fecal samples of native rodents in Chile. The life cycle of Sarcocystis muris (Blanchard, 1885), for example, requires rodents as intermediate hosts and felines as definitive hosts (Powell & McCarley, 1975Powell EC, McCarley JB. A Murine Sarcocystis that causes an Isospora-Like infection in cats. J Parasitol 1975; 61(5): 928-931. http://dx.doi.org/10.2307/3279239. PMid:810560.
http://dx.doi.org/10.2307/3279239...
). Though, Sarcocystis bradyzoites can also replicate in rodents, which indicates that transmission also occurs due to cannibalism between rodents (dihomoxenous life cycle) (Koudela & Modrý, 2000Koudela B, Modrý D. Sarcocystis muris possesses both diheteroxenous and dihomoxenous characters of life cycle. J Parasitol 2000; 86(4): 877-879. http://dx.doi.org/10.1645/0022-3395(2000)086[0877:SMPBDA]2.0.CO;2. PMid:10958479.
http://dx.doi.org/10.1645/0022-3395(2000...
). It could be possible that Sarcocystis-like sporocyst in rodents in this study may be spurious findings (i.e., cyst that passed through rodents’ gastrointestinal tracts), but their life cycles involve carnivore hosts. Additionally, Isospora peromysci (Davis 1967Davis BS. Isospora peromysci n. sp., I. californica n. sp., and I. hastingsi n. sp. (Protozoa: Eimeriidae) from four sympatric species of white footed mice (Peromyscus) in Central California. J Protozool 1967; 14(4): 575-585. http://dx.doi.org/10.1111/j.1550-7408.1967.tb02044.x. PMid:5629073.
http://dx.doi.org/10.1111/j.1550-7408.19...
) (Protozoa: Eimeriidae) was reported in white-footed mice Peromyscus maniculatus (Wagner, 1845‎) in California, US (Davis, 1967Davis BS. Isospora peromysci n. sp., I. californica n. sp., and I. hastingsi n. sp. (Protozoa: Eimeriidae) from four sympatric species of white footed mice (Peromyscus) in Central California. J Protozool 1967; 14(4): 575-585. http://dx.doi.org/10.1111/j.1550-7408.1967.tb02044.x. PMid:5629073.
http://dx.doi.org/10.1111/j.1550-7408.19...
). Isospora spp. have a direct life cycle with asexual and sexual reproduction, and hosts become infected by eating infective sporulated oocysts (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Recent studies on Isospora spp. in fecal samples of bank voles (Myodes glareolus Schreber, 1780) probed that such finding was a pseudoparasite since it was phylogenetically related to birds and did not replicate in rodents by experimental infections (Trefancová et al., 2019Trefancová A, Mácová A, Kvičerová J. Isosporan oocysts in the faeces of bank voles (Myodes glareolus; Arvicolinae, Rodentia) : real parasites, or pseudoparasites? Protist 2019; 170(1): 104-120. http://dx.doi.org/10.1016/j.protis.2018.12.002. PMid:30738338.
http://dx.doi.org/10.1016/j.protis.2018....
). Thus, Isospora oocysts in the present study is likely to be also a spurious finding from bird feces, passing through rodent gastrointestinal tracts. More research should carry out to clarify the origin of these findings. Finally, amoeba cysts were found in R. norvegicus, A. olivacea and G. valdivianus. Cysts contained a varied number of nuclei (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.). Amoeba spp. can be transmitted directly by ingestion of viable cysts in contaminated food or water (Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.).

Interestingly, only Trichuris sp. and Syphacia sp. were found in both coprologic and post-mortem examination. Syphacia sp. was the most prevalent parasite in the post-mortem analysis, which contrasts with the low copro-prevalence, suggesting that the fecal examination have a low sensitivity in detecting their eggs. Maybe, the sensitivity of detection of Syphacia sp. in live rodents could be improved with the tape (Graham’s) test, which was designed to find eggs added to the anus. The other species found by both techniques was Trichuris sp., which was also found more frequently in necropsy than in coprological examination, which agrees with the recommendation of examining at least three serial stool samples per individual (Knopp et al., 2008Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, et al. at al. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis 2008; 2(11): e331. http://dx.doi.org/10.1371/journal.pntd.0000331. PMid:18982057.
http://dx.doi.org/10.1371/journal.pntd.0...
). This could also be due to the low abundances which mean low loads of eggs. Furthermore, post-mortem examination allowed to identify genera of Spiruridae: Physaloptera sp. and Protospirura sp, which were difficult only by egg morphological features. Indeed, the second most prevalent parasite obtained through the necropsy was Protospirura sp. in A. olivacea, which was in accordance with findings in fecal samples in the same species (see Table 2 and 3). Nematodes including Strongylid-type eggs, Capillariidae, and Strongyloides sp., could not be determined by post-mortem examination. It is likely that adult parasites degraded due to freezing condition during preservation of gastrointestinal tracts. Also, adult parasites in necropsies could not be identified to species level since some features are still debatable, and there may be some new records for the studied rodent species. For future assessment, molecular diagnosis should be carried out to determinate parasite species and their phylogenetic relationships.

Coprological examination is a useful noninvasive diagnosis method to study endoparasites in wild species. Though, it may have limitations in determining the actual parasite load in comparison to other methods such as necropsy (Zajac & Conboy, 2012Zajac AM, Conboy GA. Veterinary clinical parasitology. 8th ed. Iowa, USA: John Wiley & Sons, Inc.; 2012.; Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Therefore, information in the present study about parasite intensity should be evaluated with caution. Long-term surveys of rodents may be essential to assess endoparasites in eventual mortality to comply with animal welfare standards.

Contrary to what was expected, in A. olivacea, individuals classified as low body mass showed less infection probability for Spirurid-type eggs and Strongilid-type eggs. Low body mass individuals may be eating fewer arthropods and contaminated items with infective free-living larvae that might reduce the risks of parasite infection with Spiruridae and Strongylida, respectively.

Findings of the present study serve as preliminary epidemiologic information for future surveys. Several inherent factors of the study limit its explanatory power including a low sample size and the arbitrary time of the year at which the study was carried out. Due to low sample size, the scaled body mass could not be calculated in accordance with age differences (i.e., adults and juveniles). Also, environmental conditions, such as habitat type, vegetation clearance, or arthropod density, were not assessed in this study. Long-term surveys in different seasons with a higher number of sites and rodents may be required to evaluate the influence of habitat degradation on helminth infections and body condition of wild rodents inhabiting Chiloé Island.

Finally, helminths including Moniliformis sp., Rodentolepis spp., Strongyloides spp., Capillaria spp. and protozoa such as Amoeba sp. have the potential to be transmitted to humans and cause zoonotic diseases (Molavi et al., 2006Molavi GH, Massoud J, Gutierrez Y. Human Gongylonema infection in Iran. J Helminthol 2006; 80(4): 425-428. http://dx.doi.org/10.1017/JOH2006355. PMid:17125553.
http://dx.doi.org/10.1017/JOH2006355...
; Salehabadi et al., 2008Salehabadi A, Mowlavi G, Sadjjadi SM. Human infection with Moniliformis moniliformis (Bremser 1811) (Travassos 1915) in Iran: another case report after three decades. Vector Borne Zoonotic Dis 2008; 8(1): 101-103. http://dx.doi.org/10.1089/vbz.2007.0150. PMid:18237263.
http://dx.doi.org/10.1089/vbz.2007.0150...
; Taylor et al., 2016Taylor MA, Coop RL, Wall RL. Veterinary parasitology. West Sussex: John Wiley & Sons; 2016.). Therefore, further studies aiming to identify the species of these parasites should be performed to assess their zoonotic potential. Given that natural environments are continually reducing due to human-induced activities, more research should be carried out to enhance our understanding of parasitic infections in wild rodents inhabiting rural areas and the impact on public health and wildlife conservation.

Acknowledgements

Authors are grateful to all collaborators and assistants who carried out field work and collection of biological samples with special thanks to Maira Riquelme. Authors are thankful to Carolina Serrano who reviewed the Portuguese “Resumo” and to Guillermo D’Elia for his advice on the taxonomy of host species. PDCJ gratefully acknowledges ANID Agencia Nacional de Investigación y Desarrollo, Chile, for the Doctoral Fellowship N. 21200220 and the WWF Russell E. Train Fellowship. This study was funded by the Fondo Nacional de Desarrollo Científico y Tecnológico (ANID/FONDECYT grant no. 1170810).

  • How to cite: Carrera-Játiva PD, Torres C, Figueroa-Sandoval F, Beltrami E, Verdugo C, Landaeta-Aqueveque C, et al. Gastrointestinal parasites in wild rodents in Chiloé Island-Chile. Braz J Vet Parasitol 2023; 32(1): e017022. https://doi.org/10.1590/S1984-29612023002

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Publication Dates

  • Publication in this collection
    06 Jan 2023
  • Date of issue
    2023

History

  • Received
    23 Nov 2022
  • Accepted
    30 Nov 2022
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