The Passalidae (Coleoptera, Scarabaeoidea) from Bolivia, with the descriptions of three new species

Abstract Employing data from literature, examination of specimens in collections, and a field trip, a list of the species of Passalidae from Bolivia is elaborated. A total of 38 species is reported, including new records of Passalus inca Zang, 1905 and P. lunaris (Kaup, 1871), and three new brachypterous species: Passalus bolivianussp. nov., P. canoisp. nov., and P. gonzalezaesp. nov. Most of the species (27) belongs to the Passalini tribe, especially to the genus Passalus Fabricius, 1792 (19 species); the Proculini tribe is represented by eleven species in three genera. The number of species of Bolivia is low and reflects the lack of a systematic exploration of this country; more surveys are needed, especially in ecosystems such as montane forest and tropical rain forest.


Introduction
Passalidae is a Pantropical group of Coleoptera. With few exceptions, the species of the family live inside rotting logs, feeding on decomposing wood. In the New World the family is represented by the tribes Passalini and Proculini, and in South America the majority of the species belongs to Passalini. Zang (1905) described Veturius spinipes, constituting the first record of a Passalidae from Bolivia. After that, Gravely (1918) recorded three species and Luederwaldt (1931a) described Paxillus pleuralis from La Paz. Subsequently, other authors have cited and described additional species from Bolivia. Here we compile these records into a single annotated checklist that includes bibliographic references and general comments. Three new species from Bolivia are also described.

Materials and methods
Pedro Reyes-Castillo conducted a field trip to Santa Cruz in February 2010 and the material collected is deposited in the collection of the Instituto de Ecología in Xalapa (IEXA, Mexico). We examined the material from Bolivia deposited in this collection and also from the Museu de Zoologia, Universidade de São Paulo (MZSP, Brazil), Universidad del Valle de Guatemala (UVGC, Guatemala), The Field Museum of Natural History (FMNH, USA), the Colección Entomológica Universidad del Magdalena (CEBUMAG-ENT, Colombia) and the Colección Entomológica del Instituto de Ciencias Naturales of Universidad Nacional de Colombia (ICN, Colombia). The material was identified by us employing original descriptions, keys, and diagnoses provided in Kuwert (1898), Luederwaldt (1931a, b), Hincks (1940), Marshall (2000), Gillogly (2005), Boucher (2006), and Jiménez-Ferbans et al. (2013, 2016, and by comparison to the reliably identified material housed in IEXA and UVGC. In addition to the museum specimens, we reviewed the publications regarding the records of Passalinae from Bolivia. For every species in the list, we included the entomological collection where the specimens from Bolivia are deposited, the authors that have recorded the species, the material examined (labels cited verbatim and separated by slashes), and comments. The classification adopted and the terminology employed for the head is that proposed by Boucher (2006), for the rest of the body that of Reyes-Castillo (1970).

Results
A total of 22 species has been recorded from Bolivia in the literature; meanwhile we found 25 species in the reviewed collections, including the specimens of Passalus inca from Conchabamba, Yungas del Palmar and P. lunaris from Santa Cruz, Chiquitos, new records for Bolivia, and specimens of 3 new species described below.
Comments. originally described from Venezuela, this species is distributed in the Andes of Bolivia, Colombia, Ecuador, Peru and Venezuela (Boucher 2006). Boucher (2006) Luederwaldt (1931b) recorded it from "Campinas (Goyaz)". Fonseca and Reyes-Castillo (2004: 17) recorded it from the states of Amazonas, Pará, Goiás and Sao Paulo. Outside of Brazil, it has been recorded from Argentina by Bruch (1942) and Jiménez-Ferbans et al. (2013). This is the first record for Bolivia.
Comments. This species was described by Gravely (1918: 55) based on two specimens, one from "Santa Catharina" and the other from "Chaco", without more precision. Hincks and Dibb (1935: 43) assumed "Chaco" as Chaco, Bolivia. We believe nobody has examined specimens of this species after its description.
Comments. Dibb (1948) described this species citing the following information: "Bolivia: La Paz, received, xii.1928, H. Clemens. Type and paratype (same data) in United States National Museum Collection, Washington". Until now, nobody has cited more specimens of it.

Passalus (Passalus) coarctatus Percheron, 1835
Passalus ( Comments. Zang (1905) described this species from "Peru: Chanchamayo". This is the first record since the original description and first record from Bolivia.
Comments. Described from Cayenne, French Guiana, this species has been recorded from the Lesser Antilles, Bolivia, Brazil, and Colombia. Jiménez-Ferbans et al. (2013) considered the citation from Argentina as dubious. Similarly, we consider the record from Guatemala by Hincks and Dibb (1935) as dubious. Luederwaldt (1931b) cited an exemplar from "Bolivia, Steinbach leg., immature", remarking that it only has 29 mm total length. We doubt that this specimen belongs to P. unicornis, a species with a total length of 36-45 mm (Jiménez-Ferbans et al. 2016).

Descriptions of new species
Passalus ( Head: labrum with anterior border straight or slightly concave, covered with setae that are less dense anteriorly. Clypeus hidden under the frons, with anterior angles reduced under the mediofrontal tubercles and smaller than mediofrontal tubercles. Frons narrow, anterior frontal edge with small middle indentation, without secondary mediofrontal tubercles. Mediofrontal tubercles projected forward, larger than internal tubercles. Internal tubercles small, conical, with apex not free, joined to mediofrontal tubercles by a weak ridge, located midway between mediofrontal tubercles and central tubercle apex. Posterofrontal ridges V-shaped. Area between the frontal ridges with scarce punctures on the anterior half, divided by a longitudinal sulcus running from border of frons to the base of central tubercle. Cephalic tumescence (= mamelon sensu Jiménez-Ferbans and Reyes-Castillo 2014) divided. Mesofrontal structure of the "marginatus" type (Reyes-Castillo 1970), central tubercle wide at the base with a sulcus posteriorly, apex not free. Lateroposterior tubercles marked, conical and large, larger than central tubercle. Lateropostfrontal areas glabrous, shiny, and impunctate. Eyes reduced, canthus glabrous, covering ½ of the eye in lateral view. Postorbital pits weak. Postfrontal groove semicircular and complete, with small inverted v-shape in central part. Hypostomal process slightly separated from mentum, glabrous, extending anteriorly to the superior part of the middle zone of the mentum. Medial basal mentum protruding ventrally, laterally pubescent. Mentum with large lateral fossae that are shallow and pubescent. Antennal club trilamellate, lamellae elongate. Internal tooth of the left mandible bidentate, simple on right mandible. Dorsal tooth longitudinally straight in dorsal view but slightly sinuous in lateral view. Dorsal mandibular pubescence covering the base of mobile tooth. Mandibular fossae reaching base of mobile tooth. Maxilla with lacinia apically bidentate. Ligula tridentate, middle tooth longer than lateral teeth. Middle palpomere of the labial palp 1.3 times wider, and 1.1 times longer, than distal palpomere.
Thorax: Pronotum rounded in dorsal view, wider than elytra, with punctures restricted to areas around lateral fossae and marginal groove. Marginal groove narrow, clearly visible along anterior angles, extending along approximately 1/3 of the anterior margin of the pronotum; median longitudinal sulcus and lateral fossae well marked. Inferolateral area of pronotum with abundant pubescence. Prosternellum rhomboidal, opaque. Pre-epimeron (sensu Reyes-Castillo 1970) shiny and fully pubescent. Mesosternum with small, rounded, mesosternal scar, glabrous, lateral area opaque. Posterior corner of the mesepisternum and mesepimeron glabrous. Metasternum pubescent anteriorly and in lateral fossa; metasternal disc delimited by numerous punctures medially and posteriorly. Metasternal lateral fossa and epipleuron of similar width.
Elytron: Shiny, anterior border rounded and pubescent. Humerus and epipleuron pubescent. Rounded punctures on lateral and dorsal striae (but more strongly on lateral striae).
Leg: Femur I with ventral anterior marginal sulcus narrow and complete (reaching the apical pubescence). Tibia I with dorsal sulcus complete. Tibia II with one weak spine and tibia III unarmed.
Abdomen: Marginal groove of posterior-most sternite complete. Aedeagus: Basal piece fused with parameres in ventral view (Fig. 4). Ventral surface of median lobe almost entirely sclerotized, measured along media ventral line, length of medial lobe 0.9 times that of basal piece and parameres. Lateral projections of parameres small and apices rounded in lateral view (Fig. 3).
Etymology. Named after the country, Bolivia.
Variations. The anterior border of the labrum can be straight or slightly concave. The longitudinal sulcus on the area between frontal ridges can be weak or marked. Medial basal mentum can be fully pubescent or only laterally so.
Taxonomic discussion. Passalus (Pertinax) bolivianus sp. nov. is similar in size and habitus to Passalus nudifrons Dibb, from which it differs by having anterior border of head straight with central excision, humeri pubescent and anterior area of metasternum punctate and pubescent. Likewise, the total length of P. bolivianus sp. nov. is similar to that of P. gonzalezae sp. nov., but the former has elytral striae with rounded punctures, marked on both lateral and dorsal striae (weak punctures on striae 7-10 in P. gonzalezae) and humeri heavily pubescent. Diagnosis. Among the brachypterous species of Passalus (Pertinax), P. gonzalezae sp. nov. is recognizable by the absence of punctures on frontal area (delimited by the frontal ridges), by having anterior border of head with strong (deep) middle indentation, insinuating secondary mediofrontal tubercles, and weak punctures on elytral striae 7-10.
Head: labrum with anterior border almost straight, covered with setae uniformly. Clypeus hidden under the frons, with anterior angles reduced under the mediofrontal tubercles and smaller than mediofrontal tubercles. Frons narrow, anterior frontal edge with strong median indentation, insinuating secondary mediofrontal tubercles. Mediofrontal tubercle projected anteriorly and similar in size to internal tubercle. Internal tubercle midway between mediofrontal tubercles and apex of central tubercle, apex not free, nor joined to mediofrontal tubercles by a ridge. Posterofrontal ridges V-shaped. Area between the frontal ridges without punctures, divided by a longitudinal sulcus from the border of frons to the base of cephalic tumescence (= mamelon sensu Jimén- ez-Ferbans and Reyes-Castillo 2014). Cephalic tumescence not divided. Mesofrontal structure of the "marginatus" type (Reyes-Castillo 1970), with central tubercle wide at the base, lacking posterior sulcus, apex not free. Lateroposterior tubercle marked but small, smaller than central tubercle. Lateropostfrontal area glabrous, shiny, and impunctate. Eye reduced, canthus covering 2/3 of eye in lateral view. Left canthus with two setae, right canthus glabrous. Postorbital pit weak. Postfrontal groove semicircular, complete and with small inverted v-shape in central part. Hypostomal process slightly separated from mentum, glabrous and extending anteriorly to superior part of the middle zone of the mentum. Medial basal mentum protruding ventrally, laterally pubescent. Mentum with large lateral fossae, shallow and pubescent. Antennal club tri-lamellate, with lamellae elongate. Internal tooth of left mandible bidentate, simple on right mandible. Dorsal tooth straight in dorsal view and slightly sinuous in lateral view. Dorsal mandibular pubescence covering base of mobile tooth. Mandibular fossae reaching base of mobile tooth. Lacinia apically bidentate. Ligula tridentate, middle tooth slightly longer than lateral teeth. Middle labial palpomere same width as, and 1.1 times longer than, distal palpomere.
Thorax: Pronotum rounded in dorsal view, wider than elytra, with 34 punctures on lateral fossae areas and three punctures restricted to the area of the marginal groove. Marginal groove narrow, visible at anterior angles and extending 1/3 length of anterior margin of pronotum. Longitudinal sulcus and lateral fossa well marked. Inferolateral area of pronotum with sparse pubescence. Prosternellum rhomboidal, shiny. Preepimeron (sensu Reyes-Castillo 1970) shiny and glabrous. Mesosternum with mesosternal scar oval, glabrous, lateral area opaque. Posterior corner of the mesepisternum and mesepimere glabrous. Anterolateral part of metasternum smooth and glabrous. Metasternum glabrous anteriorly and in lateral fossa; metasternal disc smooth (without punctures), delimited by numerous punctures posteriorly. Posterior metasternal lateral fossa less wide than epipleura.
Leg: Femur I with ventral anterior marginal sulcus narrow and complete, reaching the apical pubescence. Tibia I with dorsal sulcus complete. Tibia II with one weak spine and tibia III unarmed.
Abdomen: Marginal grove of posterior-most sternite complete.
Etymology. This species is named in honor of Dr. Dolores Gonzalez from Instituto de Ecología A.C. (Mexico), who has collaborated with the authors in molecular phylogenetic studies of Passalidae.
Taxonomic discussion. Passalus gonzalezae sp. nov. is similar to P. catharinae Gravely, 1918 (31-33 mm) from which it differs by the absence of punctures on frontal area, by having anterior border of head with strong (deep) middle indentation, so strong that it produces the appearance of being flanked by secondary mediofrontal tubercles, apex of central tubercle not free (attached to the frons), the reduced wings, and weak punctures on striae 7-10. From other brachypterous species, P. gonzalezae sp. nov. is similar to P. nudifrons and P. bolivianus sp. nov. However, P. nudifrons has the head with anterior margin shallowly concave, without central excision, while in P. gonzalezae sp. nov. the anterior frontal edge has a strong median indentation, insinuating secondary mediofrontal tubercles. From P. bolivianus sp. nov., P. gonzalezae sp. nov. differs by having weak punctures on striae 7-10 (strong in P. bolivianus sp. nov.) and humeri glabrous.  Diagnosis. P. canoi sp. nov. is diagnosable by its large size (45.0-46.0 mm), strong indentation on frontal edge, internal tubercles joined to medifrontal tubercles by a weak ridge, humeri and epipleura glabrous, inferolateral area of pronotum with sparse pubescence, and metasternal disc delimited by punctures only posteriorly.
Head: labrum with anterior border concave, covered with setae that are less dense in anterior border. Clypeus hidden under the frons, anterior angles reduced under mediofrontal tubercles and smaller than mediofrontal tubercles. Frons narrow, anterior frontal edge with strong middle indentation, insinuating secondary mediofrontal tubercles. Mediofrontal tubercle projected forward, larger than internal tubercle. Internal tubercle located midway between mediofrontal tubercles and the central tubercle apex, apex not free, weakly joined to mediofrontal tubercles by a weak ridge. Posterofrontal ridges V-shaped. Area between the frontal ridges lacking punctures. Cephalic tumescence (= mamelon sensu Jiménez-Ferbans and Reyes-Castillo 2014) not divided. Mesofrontal structure of the "marginatus" type (Reyes-Castillo 1970), with central tubercle wide at the base, lacking posterior sulcus, apex not free. Lateroposterior tubercle large. Lateropostfrontal area glabrous, shiny, and impunctate. Eye reduced, canthus covering 3/4 of eye in lateral view. Canthus glabrous. Postorbital pit weak. Postfrontal groove semicircular and complete, with small inverted v-shape in central part. Hypostomal process slightly separated from mentum, glabrous and extending anteriorly to the superior part of the middle zone of the mentum. Medial basal mentum protruding ventrally, glabrous. Mentum with large lateral fossae, shallow and pubescent (the fossae is glabrous). Antennal club tri-lamellate, with lamellae elongate. Internal tooth of left mandible bidentate, simple on right mandible. Dorsal tooth straight in dorsal view and slightly concave in lateral view. Dorsal mandibular pubescence covering base of mobile tooth. Mandibular fossae reaching base of mobile tooth. Lacinia apically bidentate. Ligula tridentate, middle tooth longer than lateral teeth. Middle labial palpomere same length as, and 1.5 times wider than, distal palpomere.
Leg: Femur I with ventral anterior marginal sulcus narrow and complete (reaching the apical pubescence). Tibia I with dorsal sulcus complete. Tibia II and III with one weak spine.
Abdomen: Marginal groove of posterior-most sternite complete. Etymology. This species is named in honor of Dr. Enio Cano from Guatemala, a passionate scholar of Scarabaeoidea.
Variation. Five punctures on the anterior half (paratype), punctations restricted to the lateral fossae (11 on right and 82 on the left).
Taxonomic discussion. The size of P. canoi sp. nov. easily differentiates this species from other brachypterous Passalus (Pertinax). However, the habitus and strong indentation on frontal edge can make it similar to P. gonzalezae sp. nov., from which P. canoi sp. nov. differs by having a weak ridge joining the internal tubercles with mediofrontal tubercles; this characteristic also makes P. canoi sp. nov. different from P. nudifrons. Another difference is the medial basal mentum glabrous in P. canoi sp. nov. and laterally pubescent in P. gonzalezae sp. nov., and the frontal area divided by a longitudinal sulcus from the border of frons to the base of cephalic tumescence in P. gonzalezae sp. nov. (there is no sulcus in P. canoi sp. nov.).

Key to the Passalidae from Bolivia
Since the fauna of Passalidae from Bolivia is still poorly known, this key must be used with caution. It is probable that future surveys will yield new species and new country; for this reason, it is convenient to use this key and then confirm the determination with original description or diagnosis of the species.

Clave para las especies de Passalidae de Bolivia
Dado que la fauna de Passalidae de Bolivia aún es poco conocida, esta clave debe usarse con precaución. Es probable que estudios futuros encuentren nuevas especies y registros para el país; por ese motivo, es conveniente utilizar esta clave y luego confirmar la determinación con la descripción original o el diagnóstico de la especie.

Discussion
Bolivia has a total area of 1,098,581 km 2 and its territory includes a high variety of ecosystems. The country is divided in 12 ecoregions (Ibisch et al. 2003), of which, the Southwest Amazonia, Cerrado, Chiquitania, and Yungas seem to be suitable for Passalidae and we expected them to have high diversity of passalids. However, given its relative size, suitable climatic, ecological features, and mountainous areas, the real number of taxa occurring in the country is probably higher than the number of taxa registered to date. The number of species known from Bolivia is small in comparison with other tropical countries of the New World. For example, Mexico, Guatemala, Colombia, and Brazil have more than 80 species recorded for each country (Fonseca and Reyes-Castillo 2004;Schuster 2006;Jiménez-Ferbans et al. 2018). Similarly, the number of endemic species is low, with Veturius boliviae, Paxillus martinezi, Passalus (Pertinax) nodifrons and Passalus (Passalus) opacus being the only endemic species of Bolivia.
Without doubt, the number of species of Bolivia is underestimated due to the lack of a systematic exploration of this country. Thus, more surveys are needed, especially in ecosystems such as montane forest and tropical rain forest, which normally harbor many species. Some departments with a domain of tropical rain forest have not been sampled for Passalidae; for example, Pando department has no records of passalid beetles, and for Beni department there are records of only 5 species. The majority of the specimens examined by us came from La Paz, Cochabamba and Santa Cruz departments, especially from mid-montane range locations, corresponding with the Yungas ecoregion. Several studies have reported this pattern in Passalidae, with a high level of richness at mid-mountain ranges (MacVean and Schuster 1981, Jiménez-Ferbans et al. 2010, Chamé-Vázquez et al. 2018). However, due to the extension of these departments, the amount of known species is still considered low, pointing out the need of sampling in the mid-range montane ecosystems of Bolivia.

Reliability of the species records
From the total of 38 species listed above, we have studied material for 23 species. For the other 15 species, some authors have recorded specimens of all of them. However, three species can be discussed. The record of P. unicornis is based on a specimen recorded by Luederwaldt (1931b). However, Luedewaldt himself pointed out some differences of the Bolivian specimens regarding other specimens of P. unicornis. Likewise, the length of the specimen is too small and perhaps it corresponds to P. coarctatus, since these two species are commonly confused with each other.
Passalus morio has been recorded for Colombia, Guiana and Suriname; nonetheless, as far as we know, it is distributed mostly in the Atlantic Forest (Fonseca and Reyes-Castillo 2004;Jiménez-Ferbans et al. 2013), and its record for Bolivia must be confirmed.
Finally, the record of Passalus catharinae from Bolivia must be confirmed because no records of this species are available except for the original description. Its record for Bolivia is based on the interpretation of "Chaco" (Gravely 1918) as "Bolivia: Chaco" made by Hincks and Dibb (1935). A similar situation occurred with Veturius sinuatosulcatus Gravely. Hincks and Dibb (1935) recorded V. sinuatosulcatus from "Bolivia: Chaco". However, Boucher (2006) stating that Hincks and Dibb (1935) must have misinterpreted the type locality "Chaco" as "Chaco, Bolivia", since V. sinuatosulcatus (now synonym V. sinuatocollis sensu Boucher (2006)) does not occur in Bolivia. Then, probably the reference of "Chaco" by Gravely may not correspond to the Chao from Bolivia.