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Nematodes of the genus Dictyocaulus Railliet et Henry, 1907 are found in the bronchial branches of the respiratory system of wild and domestic ruminants, they have a direct life cycle and are considered as important agents of respiratory disease. Dictyocaulus eckerti Skrjabin, 1931 (Strongylida: Dictyocaulidae) is a lungworm that parasitizes wild and farmed deers mainly from Europe and Oceania (Gibbons & Khalil, 1988; Panuska, 2006). For some time D. eckerti was considered a synonym of Dictyocaulus viviparus (Bloch, 1782) Railliet et Henry, 1907, the cattle lungworm. At present, with the aid of molecular tools, both nematodes are classified as separate species (Divina et al., 2002; Epe et al., 1995; Höglund et al., 2003; Johnson et al., 2001). The southern pudu Pudu puda Molina, 1782 (Artiodactyla: Cervidae) is the most austral deer in South America, being restricted to the southern temperate rainforest of Argentina and Chile (Jiménez, 2010). According to Silva-Rodríguez et al. (2016)P. puda is cataloged as Near Threatened with its populations decreasing. Meanwhile in Argentina and Chile it is considered as a Vulnerable species (Jiménez, 2010). Wild mammals such as the Southern pudu are threatened by anthropogenic factors, i.e., destruction of habitat, road kills, hunting activities by local residents and predation by domestic and feral dogs (Jiménez, 2010; Silva-Rodríguez et al., 2009). On the other hand, the surveillance of pathogens such as viruses, bacterias and parasites is necessary to understand the distribution of those agents and assess the potential impact on these mammal species (Pedersen et al., 2007). There are few reports with regard to the helminth fauna of P. puda. Some species recorded are gastrointestinal nematodes as Nematodirus sp. (Nematoda: Molineidae), Oesophagostomum venulosum Rudolphi, 1809 (Nematoda: Chabertiidae), Cooperia sp., Ostertagia sp., Ostertagia ostertagi Stiles, 1892, Spiculopteragia asymmetrica Ware, 1925, Trichostrongylus axei Cobbold, 1879 (Nematoda: Trichostrongylidae) and parasites of the liver as Fasciola hepatica Linnaeus, 1758 (Platyhelminthes: Fasciolidae). Furthermore, some larval metazoan were also mentioned, i.e. as hydatid cyst of Echinococcus granulosus Batsch, 1786, Cysticercus tenuicollis of Taenia hydatigena Pallas, 1766 (Platyhelminthes: Taeniidae), nymphs of Linguatula serrata Frohlich, 1789 (Arthropoda: Linguatulidae) and muscle cysts of the protozoan Sarcocystis sp. (Apicomplexa: Sarcocystidae) (Díaz et al., 1977; Duval et al., 1990; Fernández & Villalba, 1986; Fugasa, 2015; González-Acuña, 2002; Ríoseco et al., 1976, 1979).
A pool of nematodes kept in the Helminthological Collection of the Laboratory of Veterinary Parasitology of the Universidad Austral de Chile (1163Parasitol. UACh) was used for the present study. The nematodes were isolated from the bronchi of a Southern pudu from an unspecified locality of Los Ríos Region, Southern Chile (40°13’51” S; 72°19’52” O). The lungworms were mounted in Amann’s lactophenol solution for 7 days in order to achieve diaphanization. Then, they were measured with the software ScopeImage v9.0 associated with a light microscope SudeLab. All measurements were expressed in µm, unless otherwise stated, and subsequently compared with published data, i.e. Bienioschek et al. (1996), Divina et al. (2000), Durette-Desset et al. (1988), Gibbons and Khalil (1988), Jansen and Borgsteede (1990) and Panayotova-Pencheva (2012).
All the nematodes were identified as ovigerous females (n = 3) and adult males (n = 4) of Dictyocaulus eckerti Skrjabin, 1931 (Nematoda: Dictyocaulidae) (Fig. 1-4, Table 1). The morphology and morphometric characters were coincident with those given by previous authors. However, according to Bienioschek et al. (1996), Divina et al. (2000), Durette-Desset et al. (1988), Gibbons and Khalil (1988), and Jansen and Borgsteede (1990) the buccal capsule is the most important character to distinguish D. eckerti from the other species of Dictyocaulus, being kidney- or bean-shaped and with a thick wall, as was evident in the present specimens (Fig. 1). Indeed, such morphological characters has been verified with molecular tools (Divina et al., 2000). Regarding this genus, there are previous reports of an unidentified Dictyocaulus in P. puda from Southern Chile (Díaz et al., 1977; Ríoseco et al., 1979). However, this is the first report of D. eckerti in this cervid. Another lungworm isolated from Southern pudu was Muellerius sp. (Nematoda: Protostrongylidae) (Duval et al., 1990), which commonly parasites small ruminants such as sheep and goats (Panuska, 2006). Dictyocaulus eckerti have been found in various species of Cervidae (i.e., Alces alces, Cervus elaphus, Dama dama, Capreolus capreolus, Rangifer tarandus Linnaeus, 1758) mainly from Europe (Ács et al., 2016; Carreno et al., 2009; Divina et al., 2000, 2002; Höglund et al., 2003; Hugonnet & Cabaret, 1987; Panadero et al., 2001; Rahko et al., 1992; Rehbein et al., 2014), New Zealand (Johnson et al., 2001, 2003) and North America (Fruetel & Lankester, 1989; Kutz et al., 2012).
Figures 1-4 Dictyocaulus eckerti from Pudu puda. 1. A, anterior end with a wide buccal capsule. Scale bar = 200 µm; B, buccal capsule with thick kidney-shaped wall. Scale bar = 50 µm. 2. A, uterus full of embryonated eggs. Scale bar = 200 µm; B, larvae coiled inside eggs, typical of lungworms. Scale bar = 50 µm. 3. A, posterior end of a male specimen, note the small copulatory bursa with short spicules. Scale bar = 200 µm; B, close-up of spicules and gubernaculum immediately below it. Scale bar = 50 µm. 4. Finger-shaped posterior end of female. Scale bar = 200 µm.
Table 1 Comparison of morphometric characters of Dictyocaulus eckerti isolated from different hosts, including Pudu puda. Measurements expressed in µm as a range, unless otherwise stated.
| Reference | Skrjabin, Shihobalova & Shultz (1954)** | Durette-Desset et al. (1988) | Gibbons & Khalil (1988) | Divina et al. (2000) | Panayotova-Pencheva (2012) | Present study | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Hosts | Rangifer tarandus | Capreolus capreolus | Axis porcinus, Cervus elaphus, Cervus nippon, Dama dama | Capreolus capreolus | Cervus elaphus | Pudu puda | |||||||
| Country | Russia | France | England | Sweden | Bulgaria | Chile | |||||||
| ♂ | ♀ | ♂ | ♀ | ♂ | ♀ | ♂ | ♀ | ♂ | ♀ | ♂ | ♀ | ||
| TBL* | 18.9-40.5 | 31.8-65.0 | 25.0-51.0 | 36.8-63.9 | 12.0-44.0 | 20.0-59.0 | 28.0-62.0 | 33.0-81.0 | 10.9-40.0 | 29.0-59.0 | 30.0-38.5 | 58.0-59.0 | |
| OL* | 0.9-1.2 | 0.9-1.2 | 0.9-1.2 | 0.9-1.3 | 0.6-1.3 | 0.8-1.5 | - | - | 1.0-1.4 | 1.0-1.4 | 1.1-1.2 | 1.0-1.2 | |
| OW | 120.0-192.0 | 152.0-176.0 | - | - | - | - | - | - | 111.4-200.0 | 115.2-169.0 | 107.8-137.4 | 150.6 | |
| BCWM | - | Kidney-shaped | Kidney-shaped | Kidney-shaped | Kidney-shaped | Kidney-shaped | |||||||
| BCWT | - | - | 9.0-10.0 | - | - | 8.0-12.6 | 8.2.-14.9 | - | - | 9.8-12.6 | 9.1 | ||
| BCWL | - | - | 12.0-14.0 | - | - | 13.2-23.8 | 14.5-23.4 | - | - | 21.5-22.3 | 21.0 | ||
| CVL | - | - | - | - | 134.0-218.0 | 149.0-216.0 | - | - | - | - | - | - | |
| BWDE | 248.0-432.0 | 248.0-432.0 | - | - | - | - | - | - | 184.3-420.0 | 172.8-288.0 | 272.5-328.6 | 329.1 | |
| BWV | - | 352.0-640.0 | - | - | - | 294.0-526.0 | - | - | - | 299.5-540.0 | - | 519.7-624.8 | |
| DAN | - | - | 325.0 | 225.0-400.0 | - | - | - | - | - | - | - | - | |
| DAE | - | - | 250.0-570.0 | 240.0-520.0 | 351.0-602.0 | 294.0-611.0 | - | - | - | - | 405.6-527.1 | 375.0 | |
| DAC | - | - | 540.0 | 530.0 | 356.0-630.0 | 408.0-642.0 | - | - | - | - | 431.8-527.1 | 375.0 | |
| DAV* | - | 14.4-29.9 | - | 15.4-36.3 | - | 10.4-33.0 | - | - | - | 20.0-28.0 | - | 28.0-29.0 | |
| SL | 190.0-360.0 | - | 230.0-260.0 | - | 180.0-245.0 | - | 127.1-293.7 | - | 219.1-292.3 | - | 237.1-269.9 | - | |
| GL | 40.0-52.0 | - | 55.00-65.0 | - | 31.0-67.0 | - | - | - | 40.8-70.0 | - | 53.3-55.4 | - | |
| TL | - | 300.0-400.0 | - | 350.0-460.0 | - | - | - | - | - | 257.3-400.0 | - | 445.1-520.9 | |
| EL | - | 68.0-92.0 | - | 75.0-100.0 | - | 74.0-113.0 | - | - | - | 84.0-99.9 | - | 70.1-88.0 | |
| EW | - | 44.0-50.0 | - | 40.0-60.0 | - | 37.0-55.0 | - | - | - | 40.1-51.0 | - | 44.6-53.4 | |
| OL/TBL | 0.030-0.048 | 0.018-0.028 | 0.024-0.036 | 0.020-0.026 | 0.030-0.050 | 0.025-0.040 | - | - | 0.035-0.092 | 0.024-0.034 | 0.032-0.043 | 0.021 | |
| DAV/ | |||||||||||||
| TBL | - | 0.453-0.460 | - | 0.418-0.568 | - | 0.520-0.559 | - | - | - | 0.475-0.690 | - | 0.475-0.500 | |
| SL/TBL | 0.009-0.010 | - | 0.005-0.009 | - | 0.006-0.015 | - | 0.005 | - | 0.007-0.020 | - | 0.006-0.009 | - | |
| GL/SL | 0.144-0.211 | - | 0.239-0.250 | - | 0.172-0.273 | - | - | - | 0.186-0.239 | - | 0.205-0.225 | - | |
TBL = yotal body length; OL = oesophagus length; OW = oesophagus width; BCWM = buccal capsule wall morphology; BCWT = buccal capsule wall thickness; BCWL = buccal capsule wall length; CVL = cephalic vesicle length; BWDE = body width at distal end oesophagus; BWNR = body width at nerve ring; BWV = body width at vulva; DAN = distance between anterior end-nerve ring; DAE = distance between anterior end-excretory pore; DAC = distance between anterior end-cervical papillae; DAV = distance between anterior end-vulva; SL = spicules length; GL = gubernaculum length; TL = tail length; EL = eggs length; EW = eggs width; OL/TBL = ratio oesophagus length/body length; DAV/TBL = ratio distance between anterior end-vulva/body length; SL/TBL = ratio spicule length/Body length; GL/SL = ratio gubernaculum length/ spicule length; *measurements expressed in millimeters (mm); **cited in Panayotova-Pencheva (2012).
Some of the parasites recorded for the Southern pudu could have a domestic origin, with dogs acting as definitive hosts, e.g. hydatid cyst, C. tenuicollis, L. serrata and Sarcocystis sp. or could be acquired from wild canids such as foxes (Fugassa, 2015; Kutz et al., 2012). In the same way, other helminths are shared with livestock and free-ranging exotic ruminants, e.g. O. ostertagi and S. asymetrica (Jiménez, 2010). Cervus elaphus and D. dama recorded as host for D. eckerti were introduced in Chile years ago for commercial and hunting activities. At present, also wild populations are established in national territory (Díaz et al., 1977; Jaksic et al., 2002). Dictyocaulus eckerti seems to have a wide host range (Divina et al., 2002), thus P. puda could not be an accidental host. In consequence, the interaction of exotic species with Southern pudu through sharing grazing areas could promote the transmission of parasites.
On the other hand, the detection of Toxoplasma gondii Nicolle & Manceaux, 1908 and Neospora caninum Dubey, Carpenter, Speer, Topper & Uggla, 1988 (Apicomplexa: Sarcocystidae) should be of interest because they can infect deers with the risk of causing abortions and neonatal mortality (De Craeye et al., 2011; Dubey et al., 2008; Kutz et al., 2012), thus being of importance for species with conservancy issues. Finally, the finding of this lungworm, as well as previous records of adult and larval parasites, highlight the additional impact of non-native mammals over this threatened deer (Díaz et al., 1977; Ríoseco et al., 1979).
We are grateful of Dr. Enrique Paredes who donated to us the specimens isolated from a Southern pudu. Also to the Drs. Anna Pyziel, Marion Johnson, Steffen Rehbein and Sinasi Umur for helping us with the literature, and to the anonymous reviewers for their valuable comments.
