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Phthiraptera (Amblycera and Anoplura) Parasites of the Family Octodontidae, Ctenomyidae and Abrocomidae (Mammalia: Rodentia) from Chile

Phthiraptera (Amblycera and Anoplura) Parasites of the Family Octodontidae, Ctenomyidae and Abrocomidae (Mammalia: Rodentia) from Chile

Rudolstädter nat.hist. Schr. 13, 115-118Rudolstädter nat.hist. Schr. 13 (2005) Dezember 2005115

Phthiraptera (Amblycera and Anoplura) parasites of the Family , Ctenomyidae and Abrocomidae (Mammalia: Rodentia) from Chile

LUCILA MORENO SALAS1, DOLORES DEL C. CASTRO2, JUAN C. TORRES-MURA3 and DANIEL GONZÁLEZ-ACUÑA1

Resumen Phthiraptera (Amblycera y Anoplura) parasitos de la Familia Octodontidae, Ctenomyidae y Abrocomidae (Mammalia, Rodentia) de Chile Ocho especies de piojos (Insecta: Amblycera & Anoplura) son reportados en nueve especies de roedores pertenecientes a las familas Octodontidae, Ctenomyidae y Abrocomidae. Ellos son Gyropus distinctus (Amblycera, Gyropidae) y Ferrisella chilensis (Anoplura, Hoplopleuridae) colectados desde degus; G. distinctus colectado de Octodon lunatus; Gyropus elongatus colectado de fuscus; Ferrisella disgrega colectado de Octodontomys gliroides; Phtheiropoios pearsoni (Amblycera, Gyropidae) colectado de Abrocoma bennetti; Phtheiropoios pollicaris colectado de Ctenomys magellanicus; Phtheiropoios nematophallus colectado de Ctenomys opimus y Gyropus parvus colectado de Ctenomys maulinus. Los piojos chupadores Ferrisella disgrega, Phtheiropoios pearsoni y Phtheiropoios nematophallus son reportados en Chile por primera vez. Reportamos Octodontomys degus como nuevo hospeador para Ferrisella chilensis, Abrocoma benetti para Phtheiropoios pearsoni, Ctenomys maulinus para Gyropus parvus, y Abrocoma bennetti para Phtheiropoios pearsoni.

Zusammenfassung Phthiraptera (Amblycera und Anoplura) aus den Nagerfamilien Octodontidae, Ctenomyidae und Abrocomidae (Mammalia, Rodentia) von Chile Acht Arten von Tierläusen (Amblycera und Anoplura) wurden auf neun Nagetier-Arten der Familien Octodontidae, Ctenomyidae und Abrocomidae nachgewiesen. Dies sind: Gyropus distinctus (Amblycera, Gyropidae) und Ferrisella chilensis (Anoplura, Hoplopleuridae) ex Octodon degus; Gyropus distinctus ex Octodon lunatus; Gyropus elongatus ex Aconaemys fuscus; Ferrisella disgrega ex Octodontomys gliroides, Phtheiropoios pearsoni ex Abrocoma bennetti, Phtheiropoios pollicaris ex Ctenomys magellanicus, Phtheiropoios nematophallus ex Ctenomys opimus und Gyropus parvus ex Ctenomys maulinus. Ferrisella disgrega, Phtheiropoios pearsoni und Phtheiropoios nematophallus wur- den zum ersten Mal in Chile festgestellt. Vier bisher unbekannte Wirt-Parasit-Beziehungen sind nachgewiesen wor- den, und zwar Octodontomys degus als neuer Wirt von Ferrisella chilensis, das gleiche Abrocoma benetti von P. pearsoni, Ctenomys maulinus von Gyropus parvus und Abrocoma bennetti von Phtheiropoios pearsoni.

Summary Eight of lice (Insecta: Phthiraptera) are reported from nine species of belonging to the families Octodontidae, Ctenomyidae and Abrocomidae. They are Gyropus distinctus (Amblycera, Gyropidae) and Ferrisella chilensis (Anoplura, Hoplopleuridae) off Octodon degus; Gyropus distinctus off Octodon lunatus; Gyropus elongatus collected from Aconaemys fuscus; Ferrisella disgrega collected from Octodontomys gliroides; Phtheiropoios pearsoni (Amblycera, Gyropidae) collected from Abrocoma bennetti; Phtheiropoios pollicaris collected from Ctenomys magellanicus; Phtheiropoios nematophallus collected from Ctenomys opimus and Gyropus parvus collected from Ctenomys maulinus. The lice Ferrisella disgrega, Phtheiropoios pearsoni and Phtheiropoios nematophallus are reported from Chile for the first time. We report Octodontomys degus as a new host for Ferrisella chilensis, Abrocoma benetti for Phtheiropoios pearsoni, Ctenomys maulinus for Gyropus parvus, and Abrocoma bennetti for Phtheiropoios pearsoni.

Keywords: Phthiraptera, sucking lice, chewing lice, new records, Rodents, Octodontidae, Ctenomyidae, Abrocomidae, Chile.

1 L. Moreno Salas and Dr. D. González-Acuña, Facultad de Medicina Veterinaria, Universidad de Concepción, Casilla 537, Chillán, Chile. 2 Dr. D. del C. Castro, Facultad de Ciencias Naturales y Museo de la Plata, Paseo del Bosque s/n, 1900, La Plata, Buenos Aires, . 3 Dr. J. C. Torres-Mura, Museo Nacional de Historia Natural, Casilla 787, Santiago, Chile. 116 L Moreno Salas et al.: Phthiraptera parasites of rodents from Chile

Introduction (28° 28’ S; 71° 13’ W) to Santiago (33º 27’ S; 70º 38’ W), three Octodon lunatus from National Park Fray The South American mammalian fauna contains Jorge (30° 39’ S; 71° 40’ W) and Peñuelas National an ancient (Oligocene) and diverse lineage of Reserve (33° 09’ S; 71° 32’ W), 19 Aconaemys fuscus Caviomorph rodents. They have distinctive cha- distributed from Baños del Flaco (35° 57’ S; 70° 26’ W) racters such as their dental formula (1/1, 0/0, 1/1, to Vilches National Reserve, nine Aconaemys sagei from 3/3), small litter size, long gestation period, and Malleco Lagoon (38° 12’ S; 71° 50’ W) and Paso Reigolil precociality; they are also herbivores and live (39º 07’S; 71º 25’ W), 15 Octodontomys gliroides mainly in burrows (WOODS 1982, REDFORD & distributed from Zapahuira (18° 20’ S; 69° 36’ W) and EISENBERG 1992). The family Octodontidae ranges Chuzmiza (19° 41’ S; 69° 11’ W). For the family in weight from 100 to 300 g, has a simplified Ctenomyidae, there were five Ctenomys maulinus from occlusal pattern in the shape of an 8, and is Maule Lake (36° 04’ S; 70° 30’ W), four Ctenomys distributed from southwestern to southern magellanicus from Tierra del Fuego (54° 04’ S; 68° 57’ Chile and Argentina. It includes desert adapted W), and three Ctenomys opimus from Japu Bajo (18° rodents and also fossorial and semifossorial spe- 24’ S; 69° 16’ W). For the family Abrocomidae, 13 cies (CONTRERAS et al. 1987). The Abrocomidae specimens of Abrocoma bennetti distributed from Huasco is a monotypic family ( Abrocoma) whose to Itata River (36° 50’ S; 72° 24’ W) were examined. species range from 200 to 300 g, and is found The recovered Phthiraptera were stored in alcohol, and from Peru to central Chile and Argentina. These for better identification they were later mounted species have soft fur, short limbs, and large ears according to PALMA (1978). The lice are deposited in and tails (REDFORD & EISENBERG 1992; SPOTORNO the collection of the Laboratory of Zoology, Faculty of & WALKER 2000). The diverse family Cteno- Veterinary Medicine, University of Concepción, Chillán, myidae includes the single genus Ctenomys, Chile. The material was collected by LUCILA MORENO adapted for a fossorial life, with a very short tail, SALAS and DANIEL GONZÁLEZ-ACUÑA. small eyes and ears, and very long front claws. Ctenomys is distributed from southern Peru and Brazil to Tierra del Fuego (CONTRERAS et al. 1987, REDFORD & EISENBERG 1992). Results Parasites from the Phthiraptera are poorly studied in Chile. For the Octodontidae there are Suborder Amblycera reports of Gyropus parvus WERNECK, 1936 in Family Gyropidae Octodon degus MOLINA, 1782 (WERNECK 1951); Genus Gyropus NITZSCH, 1818 G. elongatus CASTRO, CICCHINO & TORRES-MURA, 1987 in Aconaemys fuscus WATERHOUSE, 1842 Gyropus elongatus CASTRO, CICCHINO & TORRES (CASTRO et al. 1987), and G. distinctus CASTRO & MURA, 1987 CICCHINO, 2002 in O. degus and O. lunatus OS- GOOD, 1943 (CASTRO & CICCHINO 2002). For the Type host: Aconaemys fuscus WATERHOUSE, 1842 family Ctenomyidae, WERNECK (1948) reported Other host: Aconaemys sagei PEARSON, 1984 Phtheiropoios pollicaris EWING, 1924 in Cteno- (CASTRO et al. 1987) mys magellanicus BENNET, 1836 and CASTRO et al. Examined: 19 Aconaemys fuscus, positive to lice (1987) reported G. p. parvus in C. magellanicus. six, from El Flaco Hot Springs, Las Cabras (34º For the family Abrocomidae, WERNECK (1948) 38’ S; 70º 41’ W) and Vilches National Reserve. reported Gyropus longus NEUMANN, 1912 in Nine Aconaemys sagei, positive to lice three, from Abrocoma bennetti WATERHOUSE, 1837 and PRICE Malleco Lagoon and Paso Reigolil. & TIMM (2000) reported Abrocomophaga Material examined: three males, three females, chilensis EMERSON & PRICE, 1976 for the same three larvae (nymphs). host. Gyropus distinctus CASTRO & CICCHINO, 2002

Materials and methods Type host: Octodon degus (MOLINA, 1782) Other hosts: Octodon lunatus OSGOOD, 1943 All specimens analyzed were from the collections (CASTRO & CICCHINO 2002) of the National Museum of Natural History in Santiago, Examined: 51 O. degus, positive to lice Chile. The lice were collected from the following species: 13, from Los Dominicos (33º 27’ S; 70º 38’ W), 51 specimens of Octodon degus, distributed from Huasco Coquimbo (29º 57’ S; 71º 22’ W), National Park Rudolstädter nat.hist. Schr. 13 (2005) 117

Fray Jorge (30º 39’ S; 71º 40’ W), Lagunillas (30º Suborder Anoplura 06’ S; 71º 21’ W), Peñuelas National Reserve (33° Family Hoplopleuridae 09’ S; 71° 32’ W). Three O. lunatus, positive to Genus Ferrisella EWING, 1929 lice one from Peñuelas National Reserve. Material examined: seven males, 12 females. Ferrisella chilensis (WERNECK, 1937) Syn.: Hoplopleura chilensis WERNECK, 1937 Gyropus parvus EWING, 1924 Type host: Octodon degus (MOLINA, 1782) Type host: Ctenomys magellanicus BENNET, 1836 Examined: 51 O. degus, positive to lice one from Other hosts: Ctemomys mendocinus PHILIPPI, Santiago. 1869; C. t. talarum THOMAS, 1898; C. porteuosi Material examined: one female. THOMAS, 1916; C. australis RUSCONI, 1934; C. sericeus ALLEN, 1903; C. opimus WAGNER, 1848; Ferrisella disgrega (FERRIS, 1921) C. colburni ALLEN, 1903; C. haigi THOMAS, 1919; Syn.: Hoplopleura disgrega Ferris, 1921 C. chasquensis CONTRERAS, MANCEÑIDO & RIPAS ALSINA, 1970; C. azarae THOMAS, 1903; C. Type host: Octodontomys gliroides (GERVAIS & saltarius THOMAS, 1912 (WERNECK 1951; CASTRO D’ORBIGNYI, 1844) et al. 1987). Other hosts: O. degus (CASTRO & GONZÁLEZ 1997) Examined: five C. maulinus PHILIPPI, 1872, one Examined: 15 O. gliroides, six positive to lice from positive to lice from Maule Lake (36° 04’ S 70° 30’ Zapahuira and Chuzmiza. W). Material examined: one male, four females, three Material examined: two males, three females. nymphs.

Genus Phtheiropoios EICHLER, 1940 Discussion

Phtheiropoios pearsoni WERNECK, 1948 Eight species of lice belonging to the genera Gy- ropus, Ferrisella, and Phtheiropoios are reported Type host: Abrocoma cinerea THOMAS, 1919 from nine hosts of the Caviomorph families Octo- Examined: 13 Abrocoma bennetti, five positive dontidae, Abrocomidae, and Ctenomyidae. The to lice from Fray Jorge National Park. genus Ferrisella EWING, 1929 was considered part Material examined: one male, four females. of Hoplopleura but was confirmed as a genus by CASTRO & VERZI (2002). It has five species Phtheiropoios pollicaris (EWING, 1924) parasitizing the family Octodontidae, and is re- Syn.: Gyropus pollicaris EWING, 1924 stricted to Bolivia, Argentina, and Chile. In the present study we report two additional species Type host: Ctenomys magellanicus osgoodi Ferrisella disgrega and Ferrisiella chilensis. (ALLEN, 1905) Gyropus parvus is found on at least eleven Other host: C. magellanicus fueguinus BENETT, species of Ctenomys, but future collections will 1836 (WERNECK 1948) probably augment this number considerably. Examined: four C. magallenicus fueguinus, one Gyropus parvus is very uniform in size and positive to lice from Tierra del Fuego. morphology, even within different Caviomorph Material examined: five females. species/populations that serve as its host. Both Gyropus elongatus and G. distinctus have long Phtheiropoios nematophallus (WERNECK, 1935) bodies in both sexes and a greater number of Syn.: Gyropus nematophallus WERNECK, 1835 setae, both characters that differentiate these two species from G. parvus. These characters pos- Type host: Ctenomys luteolus THOMAS, 1900 sibly reflect a different niche from the one Other host: Ctenomys opimus WAGNER, 1848 occupied by G. parvus. This is also supported (WERNECK 1948) by their different host families, Ctenomys vs. Examined: three C. opimus, two positive to lice Aconaemys and Octodon (CASTRO & CICCHINO from Japu Bajo (18° 24’ S; 69° 16’ W). 2002). The differences in parasite morphology Material examined: four females, three nymphs could be a consequence of one of two scenarios. (larvae). The first would presume a common phylogenetic 118 L Moreno Salas et al.: Phthiraptera parasites of rodents from Chile origin for Aconaemys and Octodon on the one of the C. mendocinus group. Suggestively, Gyro- hand and for Ctenomys on the other. The second pus parvus is absent in some species of the could be the result of a secondary colonization, eastern subgroup of the Ctenomys mendocinus contemporary or extemporaneous, of members group, which is parasitized primarily by C. rione- of the taxon that finally led to Aconaemys and grensis. Octodon from a Ctenomyidae lineage. Both Gyro- pus elongatus and G. distinctus would not be sister species but rather species derived from a common Literature trunk that share a convergent body shape. Indeed the hosts known for both species are CASTRO, D. C. & A. CICCHINO (2002): Las especies de los allopatric. The two known hosts for Gyropus géneros Gyropus NITZSCH, 1818 (Phthiraptera: distinctus, Octodon degus, and O. lunatus, are Gyroponidae) parásitas de Octodontidae (Mammalia: partially sympatric in the central region of Chile Rodentia). - Rev. Chil. Hist. Nat. 75 (2), 293-298. - , - & J. C. TORRES-MURA (1987): Estudio descriptivo (REDFORD & EISENBERG 1992), but they do not y comparativo de Gyropus parvus (Mallophaga), have similar habits. Octodon lunatus apparently parásito de roedores Octodontoideos. - Anales del is less fossorial and inhabits areas that are more Museo de Historia Natural de Valparaíso (Chile) 18, humid and densely shrubbed than O. degus, 41-45. therefore water availability might be an important - & A. GONZÁLEZ (1997): Las especies del genero factor in the distribution of both species (CON- Hoplopleura ENDERLEIN, 1904 (Phthiraptera, Insecta) TRERAS et al. 1987). Nevertheless, the environ- parasitas de roedores de la Región Neotropical. - mental and behavioral separation seems not to Papeis Avulsos Zool. 40 (13), 203-215. have influenced the differentiation of both popu- - & D. VERZI (2002): A new species of Ferrisella lations of Gyropus, which are morphologically (Phthiraptera, Anoplura, Hoplopleuridae) parasitic indistinguishable, and therefore considered the on the desert-adapted rodent barre- same species. The only known host for Gyropus rae (Rodentia, Octodontidae). - Rudolstädter nat.hist. elongatus, Aconaemys fuscus, exhibits a great Schr. 9, 113-123. environmental tolerance, and is found from CONTRERAS, L. C., J. C. TORRES-MURA & J. YÁÑEZ (1987): steppes and subxeric grasslands to forests of Biogeography of octodontid rodents: an eco-evolu- Nothofagus and Araucaria of the central tionary hypothesis. - Fieldiana Zoology, n. ser., 39, 401-411. of Chile and Argentina (REDFORD & EISENBERG FERRIS, G. F. (1951): The sucking lice. - Mem. Pac. 1992). It is semifossorial (CONTRERAS et al. 1987) Coast Entomol. Soc. (San Francisco) 1; 320 pp. and allopatric with respect to both species of PALMA, R. (1978): Slide-mounting of lice: a detailed Octodon. This allopatry also would have contri- description of the Canada balsam technique. - New buted to the genetic isolation of this species of Zealand Entomologist 6 (4), 432-436. Gyropus in comparison to G. distinctus, and it PRICE, R. D. & R. TIMM (2000): Review of the chewing only lives on Abrothrix longipilis and Notiomys louse genus Abrocomophaga (Phthiraptera: Am- valdivianus (REDFORD & EISENBERG 1992). Both blycera), with description of two new species. - Proc. these sigmodontine rodents are hosts only for Biol. Soc. Washington 113 (1), 210-217. species of Hoplopleura ENDERLEIN, 1904 (Ano- REDFORD, K. H. & J. F. EISENBERG (1992): of plura: Hoplopleuridae). Gyropus parvus (EWING, the Neotropics. Volume 2: The Southern Cone. Chile, 1924) is closely associated with the C. mendo- Argentina, Uruguay and Paraguay. - Chicago (Uni- cinus group and the Patagonian species. This versity of Chicago Press); 430 pp. suggests that Gyropus parvus is part of an an- SPORTORNO, A. & L. WALKER (2000): Origen y evolución cestral lineage that derived exclusively from the de los mamíferos chilenos. Pp. 217-227. - In: Ma- western offspring of Ctenomys. Its presence in nual de Mamíferos de Chile. CEA Ediciones, Valdivia, populations of the Ctenomys mendocinus- 464 pp. WERNECK, F. L. (1948): Os Mallóphagos de mammíferos. Patagonian species is consistent with the inferred Parte I: Amblycera e Ischnocera (Philopteridae e parte evolutionary history of this genus. In turn its de Trichodectidae). - Río de Janeiro (Revista Brasi- presence in Ctenomys talarum might be due to leira de Biologia); 243 pp. secondary infestations at the expense of species - (1951): Notas sôbre malófagos (Gyropidae). - Revista of the C. mendocinus group that are partially Brasileira de Biologia 11 (3), 303-313. sympatric with it. Alternatively, it might be a nor- WOODS, C. A. (1982): The history and classification of mal component of Ctenomys talarum, given the South American hystricognath rodents: reflections taxonomic proximity of C. talarum with species on the far away and long ago. - Special Publication Series, University of Pittsburgh 6, 377-392.