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Home , Ancylostomatidae, Ascarididae, Baylisascaris, Baylisascaris procyonis, Spectacled bear

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New records of parasites in free-ranging Andean from

Judith Figueroa1,2 and Rogers (1976), .77 of parasites (ecto and endoparasites) in wild and captive bears were 1Asociacio´n para la Investigacio´n y Conservacio´ndela reported, but no parasites were reported for Andean Biodiversidad (AICB), Av. Vicu´s 538, Lima 33, Peru; and bears ( ornatus). Estacio´n Biolo´gica Terra Natura, Grupo de Investigacio´n There is little information about parasite occur- Zoologı´a de Vertebrados, Instituto Universitario de rence in Andean bears and how parasites may affect Investigacio´n CIBIO, University of Alicante, Apdo. 99, their population dynamics. In captive Andean bears, E-03080, Alicante, Spain the most commonly reported internal parasites were ascarid (Wolff 1989) such as Toxocara Abstract: I analyzed 28 fecal samples from Andean (A.E. Bracho, Wildlife Consultant IUCN-IBA/ bears (Tremarctos ornatus) collected between 2003 BSG/ABET, unpublished data) and and 2007 from the Laquipampa Wildlife Refuge and transfuga (Schaul 2006). Coccidial organisms also Yanachaga Chemille´n National Park, Peru. I used were recorded in one individual (Wolff 1989). In free- the direct faeces test and spontaneous sedimentation ranging bears, Goldstein (1989) found nematodes tube technique to detect cysts, ova, and larvae. To belonging to the Strongyloidea superfamily in 23 of detect intestinal coccidia, I applied acid stain using 25 faeces samples collected in 3 areas of . In the Ziehl–Neelsen modified method. I detected Peru, there is a record of the trematode Paragoni- parasites in 16 scats (57.1%), identifying 3 protozoa mus kellicotti (A.E. Bracho, unpublished data). For for the first time in the Andean : Blastocystis sp., ectoparasites, Trichodectes ferrisi lice were collected in Cryptosporidium sp., and Giardia sp.; as well as 3 a free-ranging bear in Ta´chira, Venezuela (Cardozo nematodes: Strongyloides sp., an undetermined De Almeida et al. 2003). species of , and Ancylostomatidae. The Parasitic coprology, with its limitations, can pro- greatest prevalence of parasites were of the family vide reliable information on parasite fauna, although Strongyloididae (25.0%), followed by Ascarididae prevalence and sensitivity data are lower than that (21.4%), and Cryptosporidiidae (14.3%). Parasites obtained at necropsy (Torres et al. 2001). However, were found in a greater percentage of scats collected the use of noninvasive techniques allows us to assess during the dry season (87.5%) compared with the the health status of protected species’ populations. I rainy season (16.7 ). Overall, 8 species of endopar- % summarize records of parasites detected in scats of asites and 1 species of ectoparasite have been Andean bears from Peru. identified in Andean bears.

Key words: Andean bear, faeces, parasites, Peru, Study area protected natural areas, Tremarctos ornatus The study was conducted in Laquipampa Wildlife DOI: 10.2192/-D-14-00034.1 Refuge (LWR; Lambayeque department, 6u199S– Ursus 26(1):21–27 (2015) 79u269W; Fig. 1) and Yanachaga Chemille´n National Park (YCNP; Pasco department, 10u339S–75u309W; Fig. 1). The area of LWR is 113.46 km2,with elevations from 400 m to 2,600 m (Flanagan and The effect of parasitic infections on wildlife Angulo 2003). Average annual temperatures range populations is an important factor influencing the from 17u to 25uC, with average rainfall ranging from distribution and abundance of species (Ash et al. 230 mm to 1,000 mm (Proyecto Algarrobo 1993). The 2010). These infections can modulate the dynamics area of YCNP is 1,220 km2,withelevationsfrom340 of natural populations, as does the availability of m to 3,800 m. Average annual temperatures range food or predation (Scott 1988). Parasites found in ursids can be used as indicators of infection in other from 13u to 20uC, with an average rainfall ranging wild and domestic and in humans (Rogers from 1,500 mm to 2,500 mm (INRENA 2006). The and Rogers 1976). In an extensive review by Rogers dry season in LWR and YCNP is from April to October and the rainy season is from November to 2email: [email protected] March.

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Fig. 1. Locations of collected scats of Andean bears from Laquipampa Wildlife Refuge and Yanachaga Chemille´n National Park (Peru, 2003–2007). MINEDU = Ministerio de Educacio´n; MINAM = Ministerio del Ambiente.

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Methods Discussion I collected scats when encountered incidental to I documented parasites of 4 new genera in free- other studies about the diet of the Andean bear. ranging Andean bears. Including these records, .8 I collected scats in LWR during January 2003 and species of endoparasites and 1 species of ectoparasite September 2004 within the equatorial dry forest at have been identified in free-ranging Andean bears 1,050 m above sea level along Negrohuasi, Shambo, (Table 2). Some of the records I report appear rare and Sal Si Puedes creeks. I collected scats from in bears and other . For example, Blas- YCNP during January–March 2005 and August tocystis sp. has been reported in domestic and 2007 in the premontane forest of the Mascaro´n (Yoshikawa 2012) and a captive ( sector at 1,550 m and in the montane forests of San leo; Stenzel et al. 1993). I am unaware of records of Alberto, Shihua–Santa Ba´rbara and Muyumpozo, this being reported in bears or wild carnivores. between 2,200 m and 2,700 m. I preserved fresh scats Giardia sp. and Cryptosporidium sp. have been (bright appearance and distinctive color) in plastic recorded in free-ranging individuals of the families containers containing 10% formaldehyde. For each (Thompson et al. 2009), (Carver collected scat I recorded color, consistency, season of et al. 2012), and (Brent et al. 1982). deposition (dry or rainy), and presence and type of Giardia is a common water-borne protozoan through- human activity at the collection site (e.g., village, out the world; however, little is known about the crop, , and ). different species or genotypes and their role in the I performed coproparasitological tests for the maintenance of their transmission cycles (Thompson detection of cysts, ova, and larvae using the direct et al. 2009). The anthropo–zoonotic transfer suggests faeces test and the spontaneous sedimentation tube that humans can infect animals, particularly wildlife technique (Casanova and Ramos 2000). For the (Applebee et al. 2005). Within ursids, Giardia has diagnosis of intestinal coccidia, I applied acid-fast been identified in free-ranging brown bears (Ursus stain with the Ziehl–Neelsen modified method arctos) and American black bears (U. americanus; (Shoeb 2005). Parasites were fixed and then identi- Roach et al. 1993, Rodrı´guez del Rey et al. 2011). For fied to the lowest taxon possible; unavailability of Cryptosporidium, it is presumed that most infections molecular tools for genetic analysis precluded species occur through other humans or cows contaminating identification. water sources (Xiao et al. 2000). Cryptosporidium has been recorded in captive polar bears (U. maritimus), brown bears, and sun bears (Helarctos malayanus) Results and in free-ranging American black and brown bears Twenty-eight fecal samples were analyzed—6 from (Duncan et al. 1999, Rademacher et al. 1999). LWR and 22 from YCNP. Parasites were detected in One possible mechanism of transmission of 57.1% of scats; of these, 7 contained 2 parasite Blastocystis, Giardia, and Cryptosporidium between species and 1 contained 3 species. I identified humans and animals would be the ingestion of cysts 3 protozoa: Blastocystis sp. (Fig. 2A), Cryptosporid- present in water sources such as rivers and streams ium sp. (Fig. 2B), and Giardia sp. (Fig. 2C); and that were deposited by a carrier (Carver et al. 2012). 3 nematodes: Strongyloides sp. (Fig. 2D), an un- Furthermore, some species consumed by Andean determined species of Ascarididae (Baylisascaris sp. bears, including , , and (Peyton or Toxocara sp.; Fig. 2E), and an undetermined 1980), carry Cryptosporidium (Fayer 2004). species of Ancylostomatidae ( sp. or The most abundant nematodes in Andean bears sp.; Fig. 2F). In these latter 2 cases, were those of the orders and . parasites could not be distinguished because of lack Strongyloides sp. has been detected in free-ranging of detailed measurements. The highest prevalence of Canidae, Felidae, and (Vieira et al. 2008, parasites found were of the family Strongyloididae Beltra´n-Saavedra et al. 2009) and in free-ranging (25.0%), followed by Ascarididae (21.4%)and American black bears and giant pandas ( Cryptosporidiidae (14.3%; Table 1). Parasites were melanoleuca; Foster et al. 2004, Zhang et al. 2011). found in 14 of 16 (87.5%) scats collected during the Ova belonging to the Ascarididae family correspond- dry season and in 2 of 12 (16.7%) scats collected ing to Toxocara sp. or Baylisascaris sp. were detected during the rainy season. but could not be distinguished because of lack of

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Fig. 2. Parasites found in scats of Andean bears from Laquipampa Wildlife Refuge and Yanachaga Chemille´n National Park, Peru, 2003–2007. (A) Blastocystis sp. cysts. (B) Cryptosporidium sp. oocysts. (C) Giardia sp. cysts. (D) Strongyloides sp. larvae. (E) Undetermined species of Ascarididae ova. (F) Undetermined species of Ancylostomatidae ova.

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Table 1. Number of Andean bear scats (n = 28)

containing parasites, Laquipampa Wildlife Refuge A. E.

and Yanachaga Chemille´n National Park, Peru, 2003– = 2007. Laquipampa Yanachaga Wildlife Chemille´n Refuge National Park Combined Parasite (n = 6) (n = 22) % (n = 28) Protozoos Blastocystis sp. 1 1 3.6 Cryptosporidium sp. 4 4 14.3 Giardia sp. 1 1 3.6 Nematodes Strongyloides sp. 3 4 7 25.0 Ascarididae CaptiveCaptiveFree-ranging Venezuela PeruFree-ranging 4 Free-ranging PeruFree-ranging 6 Peru 5 Venezuela 6 3 4 (Baylisascaris sp. or Toxocara sp.) 6 6 21.4

Ancylostomatidae Cardozo de Almeida et al. (2003); 4 sp. Free-ranging Peru 6 sp.

(Ancylostoma sp. = sp. Free-ranging Peru 6 sp. sp. or sp. or Uncinaria sp.) 3 3 10.7 sp. Free-ranging Peru 6 Positive samples 3 13 16 57.1 sp. Free-ranging Peru 6 Toxocara transfuga or Uncinaria Blastocystis Cryptosporidium Giardia Baylisascaris Baylisascaris Strongyloides Ancylostoma Trichodectes ferrisi detailed measurements. Toxocara sp. has been recorded only in captive brown bears in Germany this study. Goldstein (1989); 3

(Rogers and Rogers 1976) and the Andean bear in = = Venezuela (A.E. Bracho, unpublished data). Bayli- sascaris has been commonly reported in all ursid species, both free-ranging and captive, except for in free-ranging Andean bears (Rogers and Rogers 1976, Foster et al. 2004, Schaul 2006, Zhang et al. 2011). Wolff (1989); 2 The transmission mechanism of ascarid parasites is Schaul (2006); 6 = by ingestion of infective ova in the soil or on the = plants on which they feed; it could also be trans- mitted by ingestion of infected animals (Page 2013). Ova corresponding to the Ancylostomatidae family (order ) were identified, but because of lack of detailed measurements, it was not possible to differentiate between Ancylostoma sp. and Uncinaria sp. Ancylostoma sp. has been recorded in all ursid species except the Andean bear (Rogers and Rogers 1976, Foster et al. 2004, Zhang et al. 2011), whereas Uncinaria sp. has been reported in free-ranging polar, American black, and brown bears (Rogers and Rogers 1976). The first records of Strongylida (superfamily Strongyloidea) were reported in 3 locations in Venezuela by Goldstein (1989), possibly indicating more widespread occurrence.

There is no evidence that parasites are a common ApicomplexaApicomplexaSarcomastigophora ZoomastigophoreaNematoda Conoidasida Conoidasida DiplomonadidaNematoda Hemaxitidae Nematoda Eucoccidiorida SecernenteaNematoda EucoccidioridaNematoda Cryptosporidiidae SecernenteaPlatyhelminthes SecernenteaArthropoda Ascaridida Secernentea Ascaridida Ascarididae Rhabditida Insecta Strongylida Ascarididae Strongylida Plagiorchiida Strongyloididae Ancylostomatidae Paragonimidae Phthiraptera Trichodectidae Captive USA 1 Free-ranging Venezuela 2 cause of mortality in ursids; however, parasites can have adverse effects on individuals, including death (Rogers and Rogers 1976, Zhang et al. 2011). For Table 2. Parasites recorded in Andean bears following:Kingdom 1 Protista Phylum HeterokontophytaAnimalia Blastocystea Nematoda Class Blastocystida Secernentea Blastocystidae Order Ascaridida Ascarididae Family Species Condition Country Source Andean bears, feces analyzed from Venezuela that Bracho, IUCN-IBA/BSG/ABET, unpublished data (2004); 5

Ursus 26(1):21–27 (2015) 26 SHORT COMMUNICATION tested positive for Strongylida nematodes showed en Santa Cruz, [A copro-parasitological study evidence of intestinal injuries (Goldstein 1989). of wild in captivity for relocation purposes in Santa Ba´rbara and other villages surrounding Santa Cruz, Bolivia]. Veterinaria y Zootecnia 3:51–60. YCNP do not have safe water supplies. Also, cattle [In Spanish]. were observed moving near rivers and streams. BRENT, L., B.S. CARLSON, AND W.N. SVEND. 1982. Cryptosporidiosis in a . Journal of the Amer- Therefore, local people and domestic and wild animals ican Veterinary Medical Association 181:1405–1406. could become infested with protozoa through con- CARDOZO DE ALMEIDA, M., P.M. LINARDI, AND J. COSTA. sumption of contaminated water. Xiao et al. (2000) 2003. The type specimens of chewing lice (Insecta, similarly suggested that deposition of American black Mallophaga) deposited in the Entomological Collection bear scat infected with Cryptosporidium oocysts in of Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil. water bodies could infest humans and livestock. Memo´rias do Instituto Oswaldo Cruz 98:233–240. Knowledge of parasites found in different species of CARVER, S., A.V. SCORZA, S.N. BEVINS, S.P.D. RILEY, K.R. wildlife is potentially important in terms of health to CROOKS,S.VANDE WOUDE, AND M.R. LAPPIN. 2012. individuals of the species as well as to possible Zoonotic parasites of around human land- infection of other species of wildlife and humans. scapes. Journal of Clinical Microbiology 50:3080–3083. CASANOVA, R.T., AND M.C. RAMOS. 2000. Te´cnicas de diagno´stico de enfermedades causadas por enteropar- Acknowledgments a´sitos [Diagnostic techniques for diseases caused by enteropara´sitos]. Diagno´stico 39:197–198. [In Spanish]. 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