Herpetology Notes, volume 14: 297-300 (2021) (published online on 09 February 2021)

First report of Spauligodon sp. (Oxyuroidea: Pharyngodonidae) in Pristidactylus torquatus (Squamata: Leiosauridae) from Chile

Pedro Pablo Álvarez1,*, Andrés González-Letelier2, Joseline Veloso-Frías3, Héctor Carrasco4, Mike Kinsella5, Alexandra Grandón-Ojeda6, and Daniel González-Acuña2

Reptiles are exposed to a wide range of endoparasites Skrjabinelazia Sypliaxov, 1930 in L. nigroviridis (Garín, (Jacobson, 2008; Ávila et al., 2012), including a variety 2006). of helminths (Hedley et al., 2013; Bower et al., 2019). Pristidactylus Fitzinger, 1843 (Squamata: Leiosauridae), Among nematodes, Pharyngodon Diesing, 1861, is a lizard genus endemic to South America represented Skrjabinodon Inglis, 1968, and Spauligodon Skrjabin by ten species, of which four occur in Chile (Uetz et et al., 1960 are the most commonly reported genera in al., 2020). Pristidactylus torquatus (Philippi, 1861) has reptiles (Ramallo et al., 2002; Monks et al., 2008). the widest distribution in Chile, and it is endemic to the In Chile, knowledge of endoparasitism in reptiles temperate forests in the central and southern regions of the is very limited due to the lack of specialists and, country (Demangel, 2016; Núñez and Urra, 2016; Mella, consequently, the small number of studies on the subject 2017), where it ranges from the Sierras de Bellavista (Garín and González-Acuña, 2008). The Phylum (the Libertador General Bernardo O’Higgins region) to Nematoda includes endoparasites in four genera reported Valdivia (the Los Ríos region) (Demangel, 2016; Mella, for Chile, including Spauligodon in Liolaemus tenuis 2017). Currently, no endoparasite has been reported (Duméril and Bibron, 1837), L. lemniscatus Gravenhorst, for the genus Pristidactylus, and only two studies have 1838, and L. nigroviridis Müller & Hellmich, 1932 evaluated the presence of ectoparasites in P. torquatus, (Goldberg et al., 2001; Jiménez, 2005; Garín, 2006), for which only the mite Eutrombicula araucanensis Parapharyngodon Chatterji, 1933 in L. nigroviridis Stekol’nikov & González-Acuña, 2010 (Trombiculidae) (Garín, 2006), Physaloptera Rudolphi, 1819 in L. tenuis has been recorded (Stekol’nikov and González-Acuña, and L. nigroviridis (Jiménez, 2005; Garín, 2006), and 2015; Espinoza-Carniglia, 2017). Spauligodon is a widespread nematode genus, comprising 52 species that have been reported in several families of reptiles (Pazoki and Rahimian, 2014; Bursey 1 Laboratorio de Ecología y Evolución de Enfermedades et al., 2016). In South America, four species have been Infecciosas, Instituto de Patología Animal, Facultad de described that mainly infect individuals of the genera Ciencias Veterinarias, Universidad Austral de Chile, Isla Teja Liolaemus Wiegmann, 1834 and Phyllodactylus Gray, s/n, Valdivia, Chile 1828. These include Spauligodon loboi Ramallo et al., 2 Laboratorio de Parásitos y Enfermedades de Fauna Silvestre, 2002 in Argentina; S. oxkutzcabiensis (Chitwood, 1938) Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, Vicente Méndez in Peru, Paraguay, and Brazil; S. viracochai Freitas & 595, Chillan, Chile. Ibañez, 1968 in Peru; and S. maytacapaci (Vicente & 3 Departamento de Patología y Medicina Preventiva, Ciencias Ibáñez, 1968) in Peru, Argentina, and Chile (Goldberg Veterinarias, Universidad de Concepción, Vicente Méndez et al., 2004; Garín and González-Acuña, 2008; Ávila 595, Chillán, Chile. and Silva, 2010; San Martín-Órdenes et al., 2019). In 4 DASP, Corporación Nacional Forestal, Región del Maule, this article, we report the first case of nematode infection Chile. in P. torquatus, based on field and microscopic findings. 5 Helm West Lab, 2108 Hilda Avenue, Missoula, Montana 59801, USA. On 6 March 2018, a male specimen of P. torquatus 6 School of Biological Sciences, University of Bristol, Bristol (Fig. 1) was manually captured in Altos de Lircay Life Sciences Building, 24 Tyndall Avenue, Bristol, BS8 National Reserve, Maule Region, Chile (35.6056°S, 1TQ, United Kingdom. 70.9663°W), in compliance with Servicio Agrícola y * Corresponding author. E-mail: [email protected] Ganadero Resolution (Nº 8618-2019). Its weight (141 g) © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. and morphometric measurements were recorded (26 mm 298 Pedro Pablo Álvarez et al.

Figure 1. Pristidactylus torquatus adult male captured in Altos de Lircay National Reserve, Maule region, Chile. Photo by Pedro P. Álvarez. head length, 21 mm head width, 138 mm tail length, 100 subsequently analysed using an optical microscope at mm snout–vent length, 39 mm forelimb length, 62 mm the Departamento de Patología y Medicina Preventiva, posterior limb length, and 50 mm armpit–groin length) Universidad de Concepción, Campus Chillán, Chile, and a visual review of ectoparasites was conducted. and the Helm West Lab, Missoula, Montana, USA. Following external parasitological examinations, Parasites were identified as members of the genus the individual spontaneously expelled seven live Spauligodon based on the following features: short female endoparasites (Fig. 2) from its cloaca, which and stout nematodes with a tapered tail; cuticle lined were fixed and preserved in 70% ethanol, and with concentric rings; oesophagus short, followed

Figure 2. Specimens of Spauligodon sp. leaving the cloaca at the time of manipulation. Photo by Pedro P. Álvarez. First Report of Spauligodon in Pristidactylus torquatus in Chile 299 by a round, oesophageal bulb with non-sclerotized regions, where they infect Liolaemus lemniscatus, L. valve. Ovary and uterus not extending anteriorly to nigroviridis, and L. tenuis, with all nematodes located oesophageal bulb and vulvar opening anterior to it. in the large intestine (caecum) (Goldberg et al., 2001; Tail conical, lacking spines, its end bifurcating into two Jiménez, 2005; Garín, 2006). short, pointed processes (Fig. 3). Considering that P. torquatus has the widest territorial Currently, the diagnosis of Spauligodon nematodes distribution among its congeners (Demangel, 2016; to the species level is based on an integrative approach Mella, 2017), it is likely that it would be more exposed that includes morphological traits, such as presence/ to parasitic infection. However, further studies are absence of spicule, presence/absence of spines in the tail necessary to understand the parasitic diversity in the filament (in adults), vulval position and egg shape, and species. Furthermore, more detailed microscopic molecular analysis (Chabaud and Brygoo, 1962; Bursey and molecular analyses are necessary to identify the and Goldberg, 1999; Bursey et al., 2005; Pereira et al., species of Spauligodon infecting P. torquatus, as well 2018). In this case, the morphology of the tail closely as additional studies on other potential reptile hosts that resembles S. maytacapaci, as illustrated by Ramallo could be affected by these helminths. et al. (2002), because S. maytacapaci has adornments at the tip of the tail (two terminal pointed processes) Acknowledgments. The authors thank the Corporación Nacional Forestal (CONAF) and Servicio Agrícola y Ganadero (SAG). AG-O that differentiate it from S. loboi which lacks such was funded by the National Agency for Research and Development adornments (Vicente and Ibánez, 1968; Ramallo et al., (ANID; formerly CONICYT) DOCTORADO BECAS 2002). Species determination was not possible in our CHILE/2018-72190138. DG-A was funded by FONDECYT specimens due to the presence of only females. 1170972. PPA, AG-L, JV-F, HC, MK and AG-O would like to Infections with nematodes of the genus Spauligodon express their deepest gratitude to Daniel González-Acuña, who sadly have not been reported in Pristidactylus. However, passed away before this paper was published. Thank you for the individuals of S. maytacapaci have previously been years of unconditional support, mentoring and joyful experiences. described in Chile, in the Metropolitan and Bío-Bío

Figure 3. Tail of female Spauligodon sp. retrieved from Pristidactylus torquatus. Photo by Mike Kinsella. 300 Pedro Pablo Álvarez et al.

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