Original article
Reassessment of the taxonomic status of Amblyomma cajennense (Fabricius, 1787) with the description of three new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp. and Amblyomma patinoi n. sp., and reinstatement of Amblyomma mixtum Koch, 1844, and Amblyomma sculptum Berlese, 1888 (Ixodida: Ixodidae)

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Abstract

A reassessment of the taxonomic status of Amblyomma cajennense based on the morphological analyses of ticks from the whole distribution area of the species resulted in the redescription of A. cajennense, the validation of 2 species which had been reduced to synonymy in the past, Amblyomma mixtum and Amblyomma sculptum, and the description and definition of 3 new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp., and Amblyomma patinoi n. sp. This study provides descriptions and redescriptions, scanning electron microscopic and stereomicroscopic images, updated synonymies, information on geographical distributions, and host associations for each of the 6 species. Amblyomma cajennense s.s. is found in the Amazonian region of South America, A. interandinum is reported from the northern part of the Inter-Andean valley of Peru, A. mixtum is present from Texas (U.S.A.) to western Ecuador, A. patinoi occurs in the Eastern Cordillera of Colombia, A. tonelliae is associated with the dry areas of the Chaco region which spans from central-northern Argentina to Bolivia and Paraguay, whereas A. sculptum is distributed from the humid areas of northern Argentina, to the contiguous regions of Bolivia and Paraguay and the coastal and central-western states of Brazil.

Introduction

Amblyomma cajennense (Fabricius, 1787) is a widely distributed tick taxon, which feeds on a variety of vertebrate hosts, mostly mammals. Its distribution spans from southern Texas (U.S.A.) to northern Argentina (Estrada-Peña et al., 2004). This tick is an important pest of domestic animals and humans in the Neotropical region (Guglielmone et al., 2003, Guglielmone et al., 2006). It is also one of the main vectors of Rickettsia rickettsii, the agent of Rocky Mountain spotted fever, in some areas of Central and South America (Labruna, 2009). In addition, different arboviruses have been isolated from, or associated with, A. cajennense (Belle et al., 1980, Linthicum et al., 1991). In the past, the taxonomic status of this tick was the object of much debate. Aragão and Fonseca (1953), and later Kohls (1958), concluded that a number of species described or revalidated by Koch (1844) and Tonelli-Rondelli (1937) should be returned to synonymy. The proposals of Aragão and Fonseca (1953) and Kohls (1958) were never challenged. The conclusions of these authors were further corroborated by an analysis of the cuticular hydrocarbons of A. cajennense from distinct geographical origins, which did not reveal any significant difference (Estrada-Peña et al., 1993).

Nevertheless, the tick is found in environments as diverse as the dry grasslands of the Chaco region of Argentina and Paraguay, the highlands of the Peruvian Andes, and the tropical forest of Guiana (Estrada-Peña et al., 2004). Despite its nearly ubiquitous geographic distribution in the Neotropical region, A. cajennense ticks from different areas are found infected with different rickettsial genospecies. A. cajennense infected with R. rickettsii have been collected in localized foci in Mexico, Panama, Colombia, Brazil, and Argentina (Patiño-Camargo, 1941, Bustamante and Varela, 1946, Rodaniche, 1953, Guedes et al., 2005, Paddock et al., 2008). Rickettsia amblyommii is very prevalent in some A. cajennense populations from Panama, northern Brazil (Labruna et al., 2004, Bermúdez et al., 2009), and Ecuador (Beati, unpublished data), but has not been detected in any of the thousands of specimens examined from southern Brazil (Sangioni et al., 2005, Pacheco et al., 2009).

Cross-mating experiments with A. cajennense ticks from geographically distant areas of Brazil (Labruna et al., 2011) and Argentina (Mastropaolo et al., 2011) suggested that this taxon is probably represented by a complex of different species. Afterwards, a molecular analysis of the genetic diversity within A. cajennense based on the comparison of multiple gene sequences in ticks collected from the entire distributional range of this tick species (Beati et al., 2013) showed strong genetic structure and delimited 6 geographically mutually exclusive clades compatible with cryptic speciation. In the study of Beati et al. (2013), all clades corresponded to allo- and parapatric localities characterized by different ecological features: One clade occurred in the Interandean valley of Peru, the second clade was associated with the dry part of the Chaco region of Argentina and Paraguay, the third clade with humid forested areas of northern Argentina and coastal southern Brazil, the fourth clade with the Amazonian region, the fifth clade with mountainous area of the Eastern cordillera of Colombia, and the sixth clade spanned the Pacific coast of Ecuador, through Central America, to Texas. Therefore, in this work, the morphology of representative specimens of each clade was examined and compared, in order to verify whether or not the observed genetic subdivision could be associated with distinctive phenotypic features. The taxonomic status of A. cajennense and of the synonymized related species was reassessed in light of these new findings, by expanding the morphological comparison to type material and specimens from different museum collections.

Section snippets

Materials and methods

The morphological comparison included adult specimens from the following tick collections: the Instituto Nacional de Tecnología Agropecuaria, Estación Experimental Agropecuaria in Rafaela, Argentina (INTA), the Coleçao Nacional de Carrapatos da Faculdade de Medicina Veterinaria e Zootecnia, Universidade de São Paulo, Brazil (CNC), and the U.S. National Tick Collection, Georgia Southern University, Statesboro, Georgia, U.S.A. (USNTC, RML accession numbers). We obtained type specimens also from

Synonyms:

Acarus cajennensis Fabricius J.C. 1787, p. 372

Ixodes cajennensis Fabricius J.C. 1805, p. 427

Amblyomma finitimum Tonelli-Rondelli M. 1937, pp. 293–294, Figs. 15 and 16

Amblyomma tapiri Tonelli-Rondelli M. 1937, pp. 295–296, Figs. 17 and 18

Material examined: Neotype ♂ (RML 124079). Material deposited at the USNTC, the CNC, and the MSNS: BRAZIL – State of Pará: Marabá (05°21′S 49°07′W) 1♂ 1♀ ex Cuniculus paca (CNC 599), 4♂♂ 3♀♀ ex Tapirus terrestris (CNC 502); Parauapebas (06°04′S 49°54′W) 1♂ 5♀♀

Description of Amblyomma tonelliae n. sp. Nava, Beati and Labruna

Etymology: This species is named for Maria Tonelli Rondelli, in recognition of her contribution to the taxonomic studies of Neotropical ticks.

Type locality: ARGENTINA, Pampa de los Guanacos (26°08′S 61°48′W), Santiago del Estero Province.

Material examined: Holotype ♂ and allotype ♀, paratype 5♂♂ and 4♀♀, collected December 2008 by A.J. Mangold, M. Mastropaolo, and S. Nava on vegetation, deposited at the USNTC (RML 124455); paratypes 20♂♂ 20♀♀ ex vegetation, Pampa de los Guanacos (26°08′S

Description of Amblyomma interandinum n. sp. Beati, Nava and Cáceres

Etymology: This species is named for the inter-Andean valley of Peru, where the type specimens were collected.

Type locality: PERU, Bellavista (5°41′S 78°42′W), Cajamarca Province.

Material examined: Holotype ♂ collected in January 2004 by Antero González Perez on “deer”, deposited at the USNTC (RML 124077), allotype ♀ collected January 2004 by Antero González Perez on “deer” in Bellavista (5°41′S 78°42′W), deposited at the USNTC (RML 124075); paratypes 100♂♂ and 30♀♀, Bellavista (5°41′S

Description of Amblyomma patinoi n. sp. Labruna, Nava and Beati

Etymology: This species is named for Dr. Luis Patiño Camargo, in recognition of his pioneering contribution to the study of tick-borne rickettsioses in Cundinamarca, Colombia.

Type locality: COLOMBIA, Villeta (05°01′N 74°28′W), Department of Cundinamarca.

Material examined: Holotype ♂ and allotype ♀, collected July, 2005 by M.B. Labruna, E. Benavides, and G. Valbuena on cattle, deposited at the CNC (CNC 1584); paratypes 8♂♂ and 3♀♀, collected July 2005 by M.B. Labruna, E. Benavides, and G.

Redescription of Amblyomma mixtum Koch, 1844

Synonym:

Amblyomma versicolor Nuttall G.H.F. and Warburton M.A. 1908, pp. 407–408, Figs. 27–29.

Material examined: A female lectotype from Mexico was selected within Koch's type series (ZMB 1061). Material deposited at the USNTC: COSTA RICA – Province of Guanacaste: Guanacaste (10°37′N 85°22′W) 1♀ host unknown (RML 23247), Parque Nacional Palo Verde (10°19′N 85°16′W) 1♀ ex H. sapiens (RML 123174). CUBA – Isla de la Juventud (21°39′N 82°48′W) 1♀ ex mule (RML 57540). ECUADOR – Province of El Oro:

Redescription of Amblyomma sculptum Berlese, 1888

Material examined: Neotype ♂ collected on Bubalus bubalis in BRAZIL, Corumbá, Alegría Farm (19°08′S 56°46′W), Mato Grosso do Sul (RML 122966). Material deposited at INTA, the CNC, and the USNTC: ARGENTINA – Province of Formosa: Reserva el Bagual (26°10′S 58°56′W) 1♂ ex vegetation (INTA 2148); San Hilario (26°03′S 58°38′W) 1♂ 1♀ ex H. hydrochaeris (INTA 41). Province of Jujuy: Ingenio Ledesma (23°50′S 64°47′W) 25♂♂ 5♀♀ ex E. caballus (INTA 1458); Palma Sola (23°53′S 64°21′W) 1♂ ex vegetation

Morphological comparisons

The morphological characters shared by the members of A. cajennense s.l. are in both genders extensive ornamentation of the scutum corresponding to the patterns outlined in Fig. 19, Fig. 20, conspicuous punctation, complete marginal groove delimiting all festoons and reaching level of the eyes, flat eyes, elongated palps with a small and blunt posteriorly projecting ventral spur on article I, hypostome spatulate, hypostomal dention 3:3, absence of spurs on trochanter I and on metatarsi II–IV,

Conclusions

This study shows that morphology is congruent with the results of the molecular and biological analyses (Labruna et al., 2011, Mastropaolo et al., 2011, Beati et al., 2013) which indicated that A. cajennense is a complex of 6 species: A. cajennense s.s., A. interandinum, A. mixtum, A. patinoi, A. sculptum, and A. tonelliae. Three of them, A. interandinum, A. patinoi, and A. tonelliae, represent new species, whereas A. mixtum and A. sculptum are resurrected. Morphological determination of these

Acknowledgements

We acknowledge the financial support of INTA, Asociación Cooperadora EEA-INTA Rafaela, CONICET, and PICT1298 to SN, AJM, and AAG. We wish to thank Jonathan Coddington (Smithonian Institution) for letting us use his BK Plus Digital Lab System and for teaching us how to use it, David Furth (Smithsonian Institution) for providing technical help and logistical support, and Patricia Sarmiento (Servicio de Microscopía Electrónica, Museo de La Plata, Argentina) for preparing the scanning electron

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