Species diversity of Tenebrionidae (Coleoptera) in mountaintops of extra-Andean volcanoes of Payunia (Argentina), with descriptions of two new species

Abstract

The north of Neuquén province shares with the south of Mendoza province the subprovince Payunia of the biogeographical province of Patagonic steppe, which is characterized by the presence of approximately 800 volcanoes. Although we have conducted several samplings in volcanoes of Mendoza in past years to recognize the biodiversity of tenebrionids, it is still pending which is the role that these mountains have in the biota of tenebrionids in Neuquén. In this work we reported the results of two consecutive years of prospection in two volcanoes separated by 120 km between each other, Tromen and Auca Mahuida which have 3978 and 2215 meters above sea level respectively. We found that Auca Mahuida harbours a total diversity of 10 tenebrionid species and Tromen 9, but these communities were significantly different between them. From these prospections two new endemic species of Tenebrionidae are described: Scotobius aucamahuidensis Silvestro sp. nov. (Tenebrioninae: Scotobiini) from Auca Mahuida and Psectrascelis tromensis Flores sp. nov. (Pimeliinae: Nycteliini) from Tromen. Photographs for these two new species are included, with comparisons to other known species of these genera. Based on these results we discuss the role of different factors that influence tenebrionid diversity and their implications to conserve biodiversity.

Key words
Mountains; Patagonian; monte; high-Andean; species turnover; biodiversity conservation

INTRODUCTION

Tenebrionid beetles (Coleoptera: Tenebrionidae) are one of most diverse insects inhabiting xeric environments in southern South America (Cepeda-Pizarro et al. 2005a, b, Cheli et al. 2010, Carrara et al. 2011a). Their ability to survive in these environments lies in several morphological, physiological and ethological adaptations that they present (Zachariassen 1996, Flores 1998, Cloudsley-Thompson 2001). Among these are nocturnal habits to elude extreme warm conditions, large bodies to control internal medium, interlocking of elytra and the presence of a subelytral cavity to control water conservation (Matthews et al. 2010). The presence of this sealed cavity in tenebrionids is generally accompanied by reduction or loss of wings (Matthews et al. 2010), becoming these species into flightless organisms (Carrara & Flores 2013). It has been suggested that these adaptations have positively influenced species survival (i.e. low extinction rates) and processes of speciation rates in tenebrionids (Cloudsley-Thompson 2001), which in turn can be hypothetically related as promoters of high species diversity found in arid environments. For example, it is possible hypothesize that morphological and ethological adaptations have increased tenebrionid survival because allow exploit more efficiently a great number of niches, which in turn reduce species extinction for competence (Carrara & Flores 2015). In addition, it is also possible hypothesize that the reduction or loss of wings have increased tenebrionid speciation rates by isolation because low organisms vagility reduce individuals migration between populations (Kergoat et al. 2014). Particularly, these hypotheses have been evaluated at regional scales (Carrara & Flores 2015) but remain pending understand if they have validity as determinant of tenebrionid diversity at local scales.

In the actuality, one of the most prominent local systems to conduct diversity studies is that of mountaintop environments (Lomolino 2001). This is because it is expected that species that inhabit these environments will experience an increase in their extinction risk by the effects of environmental Global Change (Payne et al. 2017). Considering the researches in this topic is possible notice that practically none of these were entirely developed in arid environments of southern South America using insect as study object. We consider that increase this type of studies is important because insect life cycles have a strong dependence on environmental conditions (Menéndez 2007), and because it was estimated that the effect of Global Change will be greater in Southern than Northern hemisphere (Urban 2015), thus probably many of insects that inhabit mountaintops can be vulnerable to extinctions. An arid area within southern South America that called the attention of biogeographers by the presence of approximately 800 volcanoes (Hernando et al. 2012) is the subprovince Payunia of the Patagonian province (i.e., center-west of Argentina; Roig-Juñent et al. 2018). Although in recent years, as a result of several prospections in these volcanoes, it has been possible to describe new insect species from the top of mountains (e.g., Roig-Juñent & Sallenave 2005, Flores & Carrara 2006, Roig-Juñent et al. 2008), but still remain elusive the understanding of which factors have influenced the diversity in these environments.

In this work we report the results of two consecutive years of prospection in high elevational environments of two extra-Andean volcanoes from Payunia, Tromen (3978 masl) and Auca Mahuida (2214 masl), separated by 120 km each other. These volcanoes are surrounded by different vegetation types (Roig 1998): i.e., Tromen presents Altoandean and Patagonian vegetations; and Auca Mahuida presents Altoandean, Patagonian and Monte vegetations. Taking in account the short distance between them and the different characteristics of vegetation we can test to what extent these factors are responsible of tenebrionid diversity in these environments. First, if more niche availability promoted more species diversity, we expect higher species richness in Auca Mahuida, which is influenced by three vegetation types than in Tromen, which is influenced by two vegetation types. Second, if a distance effect promoted different speciation processes in these volcanoes, we expect that community assemblages have significant differences between them. Additionally, if speciation processes were by a reduced migration capability of individuals between populations, we expect that community assemblage similarities are higher at generic than at specific levels.

The objectives of this work are: (1) to provide a comprehensively description of species assembly that inhabit these volcanoes mountaintops and (2) to test the influence of vegetational types and distance effect as determinant of species diversity in mountain environments. In addition, (3) as a result of our prospections we found two new microendemic species of Tenebrionidae belonging to the genera Scotobius Germar (Tenebrioninae: Scotobiini) and Psectrascelis Solier (Pimeliinae: Nycteliini) that we describe and illustrate.

The present publication of the new species is registered in the ZooBank Life Science Identifier with the following LSID code: urn:lsid:zoobank.org:pub:E5978F69-7E00-4274-B63A-2AA9C873C578.

MATERIALS AND METHODS

Study area

The study area is regionally located within the Patagonian biogeographic province (Roig-Juñent et al. 2018), specifically in the north of Neuquén province in central-western of Argentina (Figure 1). The two volcanoes prospected are considered as extra-Andean mountains, where Tromen and Auca Mahuida were located approximately at 100 km and 200 km east of the Andean mountain range, respectively. The different locations of these volcanoes give them different vegetational characteristics. For example, in Tromen prospection sites were between 2147 and 2610 m of altitude, where at the lower limit is characteristic a grassland steppe, with Stipa spp. and Poa spp. (Poaceae) being dominant (Chiapella & Ezcurra 1999) and at the higher limit are characteristic local communities belonging to high Andean vegetation (Chiapella & Ezcurra 1999), with Uncinia lechleriana (Cyperaceae) and Pratia repens (Campanulaceae) and shrub communities composed of Berberis empetrifolia (Berberidaceae), Discaria nana (Rhamnaceae), and Chiliotrichum rosmarinifolium (Asteraceae). Instead, in Auca Mahuida prospection sites were located between 1913 and 2020 m of altitude. Here, at the lower limit, the vegetation belongs to Patagonian steppe but with a strong influence of elements of Monte biogeographic province (Roig 1998), which downwards 1500 m become dominant surrounding entirely the mountain. At the higher limit, the vegetation presents some High-Andean biotic elements, such as Calceolaria sp. (Scrophulariaceae) shared with vegetation from Patagonian steppe (Roig 1998).

Figure 1
Study area: down-right box, Neuquén province within Argentina (black area) and the extension of Patagonian steppe (grey area); center, zoom to Neuquén province showing Patagonian steppe (grey area) and Monte (white area toward the right of Patagonian steppe) and spatial location of Tromen (right star) and Auca Mahuida (right star) volcanoes.

Sampling methods

Darkling beetles were sampled two consecutive years (2015-2016) between December and January. At each site we placed 32 pitfall traps for ten days, arranged in eight groups of four traps separated by 10 m from each other. Once the sampling finished, the four traps of each group were put together in an unique trap, and then considered as a sampling unit. Traps were cylindric plastic containers of 10 cm diameter, with 100 cm³ of a 30% ethylene glycol-water solution to preserve the material. Once traps had been collected, samples were washed and placed in 90% ethanol. Beetles were identified to species; voucher specimens were deposited at the entomological collection of the Instituto Argentino de Investigaciones de las Zonas Áridas (IADIZA, CCT CONICET Mendoza, Argentina).

We follow Bouchard et al. (2011) and Flores & Aballay (2015) to assign species into tribes and subfamilies. For species identification we used keys and revisions from Kulzer (1963), Peña (1985), Flores (1999, 2004), Flores & Vidal (2001), Flores & Chani-Posse (2005), Silvestro (2018), Silvestro et al. (2012, 2015) and by comparisons with the material deposited in the entomological collection of IADIZA. Terminology used in the descriptions follows recent papers dealing with genera Scotobius and Psectrascelis (Flores 2007, Silvestro et al. 2012). Type specimens of the new species are deposited in the following collections: Field Museum of Natural History, Chicago, USA (FMNH), Hungarian Natural History Museum, Budapest, Hungary (HNHM), Instituto Argentino de Investigaciones de las Zonas Áridas, Mendoza, Argentina (IADIZA), Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Buenos Aires, Argentina (MACN), Museo de Entomología Klaus Raven Büller, Universidad Nacional Agraria La Molina, Lima, Peru (MEKRB), Museo Nacional de Historia Natural, Santiago, Chile (MNNC), Museo de La Plata, La Plata, Argentina (MLPA), Natural History Museum, Basel, Switzerland (NHMB).

Statistical analyses

As first step, we assessed how complete the inventories of species obtained from our sampling design in the volcanoes were. This assessment is strongly important because species inventories can be only compared if they are complete enough (Jiménez-Valverde & Hortal 2003). To this end, we constructed for each volcano species accumulation curves that registered the increment of species according with the abundance of individuals. From these analyses were predicted the total species richness as the number of species expected when these curves reach their asymptotes (see, Jiménez-Valverde & Hortal 2003 for further explanations). Then, completeness was calculated as the ratio between the observed species richness in the area and the predicted asymptotic species richness. A completeness score higher than 70% is commonly used as a threshold that indicates a good sampling effort (Jiménez-Valverde & Hortal 2003). Species accumulation curves based on Hill numbers were used to calculate asymptotic species richness (Chao et al. 2014). We derived three diversity indexes from the first three Hill numbers: q=0 (richness), q=1 (Shannon diversity) and q=2 (Simpson diversity) (see Jost (2006) for indexes calculation formulas). Following to Colwell et al. (2012) and Chao et al. (2014), from these curves we assessed for differences in species richness, Shannon and Simpson diversity indexes between both volcanoes by testing for the non-overlapping confidence of intervals at 95% (bootstrap method based on 100 replicates; Hsieh et al. 2016).

To evaluate for differences in tenebrionid assemblages between both volcanoes, we used a non-metric multidimensional scaling (NMDS). Specifically, this method performs an ordination of the tenebrionid communities in function of their species similarity (Legendre & Legendre 2012). For this analysis we constructed a matrix of biological similarity, using the Bray-Curtis index as a measure of distance on the taxa abundances (square root transformed) (Legendre & Legendre 2012). A permutation multivariate analysis of variance (PERMANOVA) was used to test for significant differences among species groups obtained from NMDS (Anderson 2001). This test allows comparing assemblages as function of factors (in this case, Auca/Tromen volcanoes) based on distance measurements (biological matrices of similarity). Because of PERMANOVA is not based on ranges, can be applied in a randomized blocks experimental design, which is advantageous compared to other similar tests (Anderson & Walsh 2013).

Species accumulation curves and diversity analyses were performed using the iNEXT package for R (Hsieh et al. 2016) and the NMDS and PERMANOVA with the functions metaMDS and adonis of the vegan package (Oksanen et al. 2018) for R (R Core Team 2012).

RESULTS

Several pitfall traps were barefoot by the action of different vertebrates that inhabit the sampled area; thus of a total of 16 sampling units originally emplaced in each volcano (8 by year) we only considered 13 in Auca Mahuida and 15 in Tromen. Considering both volcanoes, we found a total of 639 individuals belonging to 16 species (Table I). Specifically, in Auca Mahuida we found a total of 356 individuals belonging to 10 tenebrionid species, and in Tromen 283 individuals belonging to 9 tenebrionid species. The asymptotic species richness predicted by volcano, according to species accumulation curves, was 11.99 species for Auca Mahuida, and 9 species for Tromen. These findings indicate that our species inventories were highly complete with scores of 83 % for Auca Mahuida and 100% for Tromen and allow for species comparisons between these volcanoes. In this sense, neither species richness nor diversity indexes curves (Figure 2) showed statistical differences between volcanoes because their confidence intervals at 95% were overlapped between them (Gotelli & Graves 1996).

Figure 2
Species accumulation curves used to compare species diversity corrected by different number of individuals between volcanoes: 0) showing species richness; 1) showing Shannon index and 2) showing Simpson index.

Table I
List of species with their taxonomic position and number of individuals found in each volcano.

Subfamily	Tribe	Genus	Species	Auca Mahuida	Tromen
Pimeliinae	Evaniosomini	Achanius	Achanius sp.	1	0
	Nycteliini	Epipedonota	Epipedonota cristallisata	7	0
		Epipedonota	Epipedonota nitida	34	38
		Mitragenius	Mitragenius araneiformis	93	2
		Nyctelia	Nyctelia cicatriculata	0	4
		Nyctelia	Nyctelia garciae	99	0
		Nyctelia	Nyctelia producta	0	77
		Nyctelia	Nyctelia sp.	38	0
	Epitragini	Nyctopetus	Nyctopetus argentinus	0	4
	Praociini	Patagonopraocis	Patagonopraocis sp.	2	0
		Platesthes	Platesthes sp.	0	2
		Praocis	Praocis argentina	0	61
	Nycteliini	Psectrascelis	Psectrascelis sp.	1	0
		Psectrascelis	Psectrascelis tromensis sp. nov.	0	26
Tenebrioninae	Scotobiini	Scotobius	Scotobius punctatus	13	69
		Scotobius	Scotobius aucamahuidensis sp. nov.	68	0

The NMDS results showed that tenebrionid communities of both volcanoes, at species (Figure 3a) and genus (Figure 3b) levels, had different composition. From these plots, can be visually noted that assemblages were more distant in the ordering space at species than at genus level, suggesting differences in the communities’ composition regard the taxonomic position. These differences were statistically supported by PERMANOVA analyses showing that species variation between volcanoes explained a 32.6% (pseudo-F (1, 27) = 13.051; p < 0.001) of assemblages differences, and that genus variation between volcanoes explained a 21.9% (pseudo-F (1, 27) = 7.5586; p < 0.001). These outcomes indicated that tenebrionid communities were more dissimilar at species level than at genus level.

Figure 3
Non-metric multidimensional scaling (NMDS) ordination plots: based on a) species similarity and b) genus similarity. Auca Mahuida sites from 1 to 13, Tromen sites from 14 to 29.

Finally, from these surveys two new microendemic species of Tenebrionidae were found: Scotobius aucamahuidensis Silvestro sp. nov. (Tenebrioninae: Scotobiini) from Auca Mahuida, and Psectrascelis tromensis Flores sp. nov. (Pimeliinae: Nycteliini) from Tromen.

Descriptions of new species

Scotobius aucamahuidensis Silvestro sp. nov.

ZooBank Life Science Identifier (LSID) - urn:lsid:zoobank.org:act:F0B40797-1E1C-4DC5-AC2B-C6761FD52B49

Diagnosis

Body dull, black to dark brown; clypeus and frons with strong round punctures; antennae short, surpassing midpoint of lateral margin of pronotum; pronotum wider than long, widest behind midpoint, with punctures of same size as clypeus punctures, separated by a distance smaller than one to three punctures diameter, and anterior angles produced; elytron oval, with wrinkles and punctures poorly marked, slightly smaller than pronotum punctures, not aligned in rows.

Scotobius aucamahuidensis superficially resembles S. punctatus Eschscholtz in pronotal aspect and punctures. It differs from S. punctatus which has the pronotum punctures separated by a distance smaller than one puncture diameter and elytron with nine longitudinal rows of punctures of same size or smaller than pronotum punctures; intervals carina-shape slightly raised with small disperse punctures, turning backwards into rows of tubercles and converging postero-laterally.

Description

Length 11.1 – 13.8 mm (Figure 4). Body glabrous, black to dark reddish brown, dull.

Figures 4-7
Figures 4-7. Scotobius aucamahuidensis Silvestro sp. nov.: (4) habitus in dorsal view and (5) pronotum and Psectrascelis tromensis Flores sp. nov.: (6) habitus in dorsal view and (7) pronotum.

Head. Labrum dark brown with round punctures slightly marked and disperse golden setae, anterior margin concave with thick golden setae. Clypeus and frons with strong round punctures, each with a central short seta; clypeal suture not covered by frons. Antennae short, surpassing midpoint of lateral margin of pronotum; antennomeres 2, 6 and 7 as long as wide, antennomere 3 longer than remaining, antennomeres 3 to 5 longer than wide, antennomeres 8 to 11 wider than long.

Thorax. Pronotum (Figure 5) concave, wider than long and widest behind midpoint, with punctures of same size as clypeus punctures, separated by a distance smaller than one to three punctures diameter; anterior margin concave, slightly narrower than posterior margin and anterior angles produced; lateral margin conspicuous (Figure 5), concave; posterior angles straight, not produced; posterior margin convex.

Elytron oval elongated (Figure 4), with punctures poorly marked, slightly smaller than pronotum punctures, distributed regularly; at lateral and posterior end with conical tubercles directed backward, without intervals carina-shape; pseudoepleuron occasionally with two rows of few sparse tubercles. Epipleuron conspicuous throughout, with conspicuous margin of equal width throughout.

Abdomen. Ventrites with poorly marked wrinkles and inconspicuous punctures, separated more than three times their diameter.

Legs punctate, each puncture with a short seta, metatibia straight at base, metafemoral–tibial articulation not reaching elytral apex.

Etymology

Its name is derived from the Auca Mahuida volcano (Natural Reserve, Neuquén province) in which all type specimens were collected.

Type material

Holotype, male: [Argentina, Neuquén Dto./ Añelo. Reserva Auca Mahuida/ 1913m. 2-12-XII-2016 / -37.73814, -68.90295 / G. Flores, R. Carrara, S. Roig] [Scotobius / aucamahuidensis sp. n. / HOLOTYPUS male / Det. V. Silvestro 2018] (IADIZA). Allotype, female: with the same data as holotype (IADIZA). Paratypes: 17 with data [Argentina, Neuquén Dto./ Añelo. Reserva Auca Mahuida/ -37.7393, -68.9229, 2232m./ 12-22-XII-2015, Coll. S. Roig, R. Carrara, F. Campón, S. Lagos] (three males: 2 IADIZA, 1 FMNH, six females: 2 IADIZA, 1 MEKRB, 1 FMNH, 1 MACN, 1 MLPA, and 8 IADIZA without sexing); twelve paratypes with the same data as holotype (two females: 1 MACN, 1 MNNC; five males: 2 MACN, 2 MLPA, 1 MNNC, and five without sexing: 3 IADIZA, 1 NHMB, 1 HNHM); four paratypes: [Argentina, Neuquén Dto./ Añelo. Reserva Auca Mahuida/ 2212m, 2-12-XII-2016 / -37.73928, -68.92375 / S. Roig, G. Flores, R. Carrara] (one female MNNC, one male MEKRB and two without sexing IADIZA); two paratypes: [Argentina, Neuquén Dto./ Añelo. Reserva Auca Mahuida/ -37.7346, -68.9098, 1970 m / 12-22-XII-2015, R. Carrara/ S. Roig, S. Lagos, F. Campón] without sexing (IADIZA).

Remarks

Prior to this study, the genus Scotobius included 67 species / subspecies; these species have a high variability of shapes, sizes and structures (Silvestro 2018). Within the genus, Scotobius aucamahuidensis sp. nov. presents the morphological characters of the Scotobius species of the central Andean cordillera and pre-cordillera zones such as S. punctatus Eschscholtz 1831, S. andrassyi Kaszab 1969, and S. obscurus Kulzer 1955, among others. These species are characterized by lack of teeth in profemora and elytra without marked carinae.

Psectrascelis tromensis Flores sp. nov.

ZooBank Life Science Identifier (LSID) - urn:lsid:zoobank.org:act:520CEA45-5189-4B50-9CD3-44B00AB2BF4F

Diagnosis

Pronotum with longitudinal, parallel, thick wrinkles, with anterior margin broad, lateral margins thick and raised; epicanthus without tuft of setae; elytron with two thick, flat carinae with sparse punctures and intervals with abundant, small, not arranged punctures; epipleuron conspicuous throughout.

Psectrascelis tromensis sp. nov. superficially resembles P. soniae Guerrero & Vidal in elytral configuration, especially having two thick, flat glabrous carinae or with few short setae, with sparse punctures and intervals with abundant, small, not arranged punctures and golden setae. In Psectrascelis tromensis the pronotum has lateral margins raised, concave in anterior half, parallel in posterior half, with 20 or more longitudinal wrinkles occupying all the surface (Figure 7); in P. soniae the pronotum has lateral margins not raised, concave, surface with sparse punctures, lacking longitudinal wrinkles.

Description

Length 12.0–16.0 mm (Figure 6). Body, femora, and tibiae black, antennae, maxillary palpi, and tarsi brown or body, legs, antennae, and maxillary palpi brown; dorsal surface of elytra shiny and densely setose.

Head. Clypeus and frons with abundant long umbilicate setae, punctures uniformely distributed, separated by a distance of one puncture diameter; clypeal suture not marked, genoclypeal suture marked; frons with longitudinal, parallel wrinkles, formed by the fusion of punctures. Epicanthus and genae without tuft of setae. Antennae in male reaching 3/4 of lateral margin of pronotum, in female reaching a half of lateral margin of pronotum; with golden, short setae all along the surface of all antennomeres and long setae forming a ring transverse at midlength in antennomeres 3 to 11; antennomere 3 subrectangular, 4 to 10 subquadrate, 11 ovate; male: antennomeres 3, 4 and 11 longer than wide, 5 to 10 wider than long; female: antennomeres 3 to 6 and 11 longer than wide, 7 to 10 wider than long.

Thorax. Pronotum (Figure 7) with anterior and posterior angles acute; anterior margin broad, posterior margin bisinuate; lateral margins very thick, smooth, and raised, concave in anterior half, parallel in posterior half; pronotum widest at midpoint; disc flat and depressed in posterior half, lower than lateral margins, with longitudinal, thick wrinkles, 20 or more on midlength occupying all surface: in central quarters parallel, reaching anterior and posterior margin of pronotum, in lateral quarters oblique and joining together before anterior margin (Figure 7), with very short setae on wrinkles. Proepisternum not visible dorsally, with horizontal grooves and wrinkles not reaching lateral margin of pronotum, with short, dense setae on wrinkles. Prosternum arched, higher than mesosternum.

Elytron flat, with two thick, flat carinae equidistant between suture and lateral margin, glabrous or with few short setae, with sparse punctures (Figure 6); intervals wider than carinae with abundant, small, not arranged punctures and short, golden setae; lateral margin carina-shape, rounded; pseudopleuron with abundant punctures each bearing a seta, punctures of equal size on all elytron surface. Epipleuron conspicuous throughout, with edge, anterior margin not reaching elytral humeri and posterior angle of pronotum, texture similar to that of elytron, with abundant punctures each one bearinga seta, anterior quarter three times as width as posterior half.

Abdomen. Male smooth, female with small protuberances in sagittal medial line of visible sternites 1– 4.

Legs with abundant long, golden setae. Ventral femoral surfaces densely setose; male with distal half of metatibiae arcuate and expanded, 1.5 times as wide as proximal half, with short, golden setae forming a central oval velvet-like surface; female with metatibiae not arcuate nor expanded at apex.

Etymology

Its name is derived from the Tromen volcano (Natural Reserve, Neuquén province) in which all type specimens were collected.

Type material

Holotype, male: [Argentina, Neuquén/ Dto. Chos Malal, Parque Prov./ Tromen, Guardaparque, 2150m/ -37.110397, -70.080475 / 20.XII.2015, coll: S. Roig] [Psectrascelis / tromensis sp. n. / HOLOTYPUS male / Det. G. Flores 2018] (IADIZA). Allotype, female: with the same data as holotype except date: 11.XII.2015 (IADIZA). Two paratypes males with the same data as holotype (IADIZA). One paratype female with the same data as alotype (IADIZA). Paratypes: [Argentina, Neuquén Dto. / Chos Malal, Reserva El Tromen / -37.1201, -70.072 2610m / 12-22.XII.2015, coll: S. Roig, / R. Carrara, F. Campón, S. Lagos] (one male, one female MACN); [Argentina, Neuquén Dto. / Chos Malal, Reserva El Tromen / Cº Wayle 2560m, 2-12.XII.2016 / -37.06792, -70.12266 / G. Flores, R. Carrara, S. Roig] (eight females: 1 NHMB, 1 HNHM, 1 FMNH, 2 IADIZA, 1 MLPA, 1 MNNC, 1 MEKRB and three males: 1 FMNH, 1 MNNC, 1 MEKRB).

Remarks

The genus Psectrascelis comprises 81 species prior to this study (Flores 2007, Vidal & Guerrero 2007). With the description of Psectrascelis tromensis sp. nov. the number of species of the genus is 82, being the most diverse genus of Nycteliini (Flores 1997). Psectrascelis tromensis sp. nov. shares with the central Chilean species of the genus inhabiting regions V to VIII (P. cinerea Solier 1836, P. arenaria Germain 1855, P. subcostata (Germain 1855), P. similis Kulzer 1954, P. rojasi Guerrero & Vidal 2007, P. soniae Guerrero & Vidal 2007, P. aceitunoi Guerrero & Vidal 2007, P. rossoi Vidal & Guerrero 2007, P. elguetai Guerrero & Vidal 2007) elytron with two thick carinae; instead, species of Psectrascelis inhabiting Patagonian steppe lack these carinae (P. sulcicollis Waterhouse 1841, P. hirta Kulzer 1954, P. atra Kulzer 1954, P. punctipennis Kulzer 1954, P. lucida Peña 1985, P. latithorax Peña 1985, P. neuquenensis Peña 1994). On the other hand, Psectrascelis tromensis sp. nov. shares with species of Psectrascelis inhabiting Patagonian steppe pronotum with longitudinal wrinkles occupying all the surface while the central Chilean species of the genus lack these longitudinal wrinkles on pronotum. Psectrascelis tromensis sp. nov. could be a representative of the genus of a generalized track using panbiogeographic approach that connect mesic areas in central Chile with arid Patagonian steppes in southern Argentina. This track is found in other genera of Pimeliinae and crosses the Andes between parallels 37º–41º South, where the mountain range presents low altitude (Flores & Pizarro-Araya 2006).

DISCUSSION

In this work we demonstrated that darkling beetles are successful organisms inhabiting arid environments not only in lowlands (Cheli et al. 2010, Carrara & Flores 2015) but also in mountains. Considering tenebrionid species found in both volcanoes we can notice that all of them showed several adaptations to survive to dry conditions. Following the different conditions of adaptations to aridity proposed by Sánchez-Piñero & Aalbu (2002), we can identify that 81.25 % of these species are most highly adapted because have elytra fused along the midline and abdomen, subelytral cavity, absence of defensive glands and wingless; 12.50% (Scotobius punctatus and Scotobius aucamahuidensis sp. nov.) are highly adapted because are characterized as the previous group but with the presence of defensive glands; and a 12.50% (Achanius sp. and Nyctopetus argentinus) less adapted to aridity because they are characterized by the presence of the second pair of wings and elytra not fused along the midline and abdomen, nor subelytral cavity, and loss of defensive glands. These results can be compared with those of Sánchez-Piñero & Aalbu (2002) and Carrara et al. (2011a) who suggested that the environmental water stress conditions the spatial occurrence of tenebrionid beetles, so that only species that have developed strategies against water loss can survive in these environments. An evidence that supports this affirmation is the low number of species less adapted to aridity found in these samplings because they experience a high susceptibility to water loss (Sánchez-Piñero & Aalbu 2002). But, how they survive to high altitudinal conditions of low temperature and hypoxia? This question arises because temperature, pressure of oxygen and air density diminishes as altitude increases, which generates new physiological challenges for species thermoregulation and respiration (Dillon et al. 2006). Probably, the explanation resides in the adaptations developed to survive to arid conditions: for example, it was suggested that to deal with low temperatures in thermo-regulatory processes are strongly important insect size, shape, and behavior to maximize heat transfer processes (Dillon et al. 2006). In this sense, it is widely recognized that tenebrionids can change their habits to avoid or meet different climatic conditions, as well as control internal medium according with their body size (Zachariassen 1996, Cloudsley-Thompson 2001). For other side, it was suggested that to deal with low pressure of oxygen insects may alter respiratory system or modify corporeal characteristics that ensure oxygen delivery (Dillon et al. 2006). In this sense, it has been reported that tenebrionids are able to reduce respiration and change their morphology under extreme environmental conditions (Cloudsley-Thompson 2001). Probably, the loss of flight capacity can be a morphological modification that promotes oxygen delivery, so that flight is a compromise in insect that inhabit high altitudes because is strongly dependent of high level of oxygen (Dillon et al. 2006).

Contrary to our first prediction, species richness did not differ between volcanoes, which implies that the number of biogeographic provinces does not influence tenebrionid diversity. This result contrast with that of Carrara et al. (2011a), who found that ecotonal environments of Monte and Patagonian biogeographic provinces positively influenced the coexistence of more species of tenebrionid in lowlands. Thus, our finding indicates reduced colonization capabilities of species that inhabit the Monte to higher altitudinal ecotonal environments in Auca Mahuida volcano. According with distribution patterns of collected tenebrionids in the volcanoes, it was noticed that species distributed in Monte also are distributed in Patagonian steppe (e.g. Epipedonota cristallisata (Lacordaire 1830), Mitragenius araneiformis Curtis 1845, Praocis argentina Kulzer 1962, Achanius sp., Nyctelia cicatriculata Berg 1889), and none species is distributed mainly in Monte (Flores 1999, Flores & Vidal 2001, data IADIZA collection). This can be related to the existence of hard environmental constraints that avoid to species distributed in Monte inhabit areas with lower temperature and hypoxia, to a high interspecific competition or both. Taking into account our second prediction, results showed a relatively low similarity at specific level between tenebrionid community of both volcanoes, indicating a strong distance effect influencing different communities composition. This outcome in part can be related with process of isolation that has promoted speciation by interrupting gene flow among populations (Carrara & Flores 2013). As evidence of this, Roig-Juñent et al. (2008) sustained that for carabid beetles that inhabit mountains from Payunia, speciation processes were determined by successive past climatic changes that fragmented and isolated populations at higher altitudes. Probably, some tenebrionid species experience the same processes because a 50% of genera were shared between communities. That is, an ancestor widely distributed that suffered distribution range contractions by climatic changes, isolation of populations in mountaintops and speciation by gene flow interruption caused for low vagility (Kergoat et al. 2014). Furthermore, the two new species described in this work, added to other three that are under study, whose distribution is only known from these volcanoes, also suggest the importance of these mountains in speciation processes.

Finally, our findings have strong implications to be considered in biodiversity conservation because by first time we provide an exhaustive list of species that inhabit entirely arid high mountain environments in southern South America. From this list, we were able to describe two new microendemic species, Scotobius aucamahuidensis sp. nov and Psectrascelis tromensis sp. nov which have a high extinction risk because their limited geographic distributions (Myers 2003). In addition, according to the Intergovernmental Panel on Climate Change (IPCC), climate change is expected to affect specifically narrowly-distributed species that inhabit mountain areas (Gitay et al. 2002). This is because future warming in these regions is expected to be two to three times higher than that recorded during the 20th century (Nogués-Bravo et al. 2007); thus, distributional ranges of mountain species should shift upwards and even shrink in some cases, especially for species that inhabit mountaintops, which will result in increased probability of extinction (Walther et al. 2005). So that, we strongly encourage that the species found in these volcanoes should be considered in further studies to assess how the effect of global climate change will influence their extinction risk.

ACKNOWLEDGMENTS

This research was supported by CONICET by providing continued research support to the authors, and Agencia Nacional de Promoción Científica y Técnica, Argentina (ANPCyT) additionally contributed to completing this work through the following projects: PICT#2013-3128, PICT#2013-1539, and NSF DEB-1754630 (GEF).

REFERENCES

• ANDERSON MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
• ANDERSON MJ & WALSH DC. 2013. PERMANOVA, ANOSIM, and the Mantel test in the Face of Heterogeneous Dispersions: What Null Hypothesis Are You Testing? EcolMonogr 83: 557-574.
• BOUCHARD P ET AL. 2011. Family-group names in Coleoptera (Insecta). ZooKeys 88: 1-972.
• CARRARA R, CHELI GH & FLORES GE. 2011a. Patrones biogeográficos de los tenebriónidos epigeos (Coleoptera: Tenebrionidae) del Área Natural Protegida Península Valdés, Argentina: implicaciones para su conservación. Rev Mex Biodivers 82: 1297-1310.
• CARRARA R & FLORES GE. 2013. Endemic tenebrionids (Celeoptera: Tenebrionidae) from the Patagonian steppe: a preliminary identification of areas of micro-endemism and richness hotspots. Entomol Sci 16: 100-111.
• CARRARA R & FLORES GE. 2015. Endemic epigean Tenebrionids (Coleoptera: Tenebrionidae) from the Andean Region: exploring the patagonian-diversification hypothesis. Zootaxa 4007(1): 47-62.
• CARRARA R, VÁZQUEZ DP & FLORES GE. 2011b. Habitat specificity can blur the predictions of species-energy theory: A case study of tenebrionid beetles adapted to aridity. J Arid Environ 75: 703-710.
• CEPEDA-PIZARRO J, PIZARRO-ARAYA J & VÁSQUEZ H. 2005a. Composición y abundancia de artrópodos epígeos del Parque Nacional Llanos de Challe: impactos del ENOS de 1997 y efectos del hábitat pedológico. Rev Chil HistNat 78: 635-650.
• CEPEDA-PIZARRO J, PIZARRO-ARAYA J & VÁSQUEZ H. 2005b. Variación en la abundancia de Artrópoda en un transecto latitudinal del desierto costero transicional de Chile, con énfasis en los tenebriónidos epígeos. Rev Chil Hist Nat 78: 651-663.
• CHAO A, GOTELLI NJ, HSIEH TC, SANDER E, MA KH, COLWELL RK & ELLISON AM. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84: 45-67.
• CHELI GH, CORLEY J, BRUZZONE O, DEL BRÍO M, MARTÍNEZ F, MARTÍNEZ ROMAN N & RÍOS I. 2010. The ground-dwelling arthropods community from Península Valdés (Patagonia, Argentina). J Insect Sci 10: 50.
• CHIAPELLA J & EZCURRA C. 1999. La flora del Parque Provincial Tromen, provincia de Neuquén, Argentina. Multequina 8: 51-60.
• CLOUDSLEY-THOMPSON J. 2001. Thermal and water relations of desert beetles. Naturwissenschaften 88: 447-460.
• COLWELL RK, CHAO A, GOTELLI NJ, LIN S-Y, MAO CX, CHAZDON RL & LONGINO JT. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5: 3-21.
• DILLON ME, FRAZIER MR & DUDLEY R. 2006. Into thin air: Physiology and evolution of alpine insects. Integr Comp Biol 46: 49-61.
• FLORES GE. 1997. Revisión de la tribu Nycteliini (Coleoptera: Tenebrionoidea). Rev Soc Entomol Arg 56: 1-19.
• FLORES GE. 1998. Tenebrionidae. In: Morrone JJ and Coscarón S (Eds). Biodiversidad de artrópodos argentinos: Una perspectiva biotaxonómica. La Plata: Ediciones Sur, p. 232-240.
• FLORES GE. 1999. Systematic revision and cladistic analysis of the Neotropical genera Mitragenius Solier, Auladera Solier and Patagonogenius gen. n. (Coleoptera: Tenebrionidae). Entomol Scand 30(4): 361-396.
• FLORES GE. 2004. Systematic revision and cladistic analysis of the Patagonian genus Platesthes (Coleoptera: Tenebrionidae). Eur J Entomol 101(4): 591-608.
• FLORES GE. 2007. Two new species of Psectrascelis (Coleoptera: Tenebrionidae) from Western Argentina. Rev Soc Entomol Arg 66(3-4): 91-97.
• FLORES GE & ABALLAY FH. 2015. Two Evaniosomini species (Coleoptera: Tenebrionidae) associated with decaying carcasses in Argentina, with remarks on tribal assignment of Achanius Erichson. Coleopt Bull 69: 167-179.
• FLORES GE & CARRARA R. 2006. Two new species of Nyctelia Latreille from western Argentina, with zoogeographical and ecological remarks on the high mountain habitat (Coleoptera: Tenebrionidae). Ann Zool 56(3): 487-495.
• FLORES GE & CHANI-POSSE M. 2005. Patagonopraocis, a new genus of Praocini from Patagonia (Coleoptera: Tenebrionidae). Ann Zool 55(4): 575-581.
• FLORES GE & PIZARRO-ARAYA J. 2006. The Andes mountain range uplift as a vicariant event in the Pimeliinae (Coleoptera: Tenebrionidae) in southern South America. Cahiers scientifiques (Muséum d’Histoire naturelle, Lyon) 10: 95-102.
• FLORES GE & VIDAL P. 2001. Systematic revision and redefinition of the Neotropical genus Epipedonota Solier (Coleoptera: Tenebrionidae), with descriptions of eight new species. Insect Syst Evol 32(1): 1-43.
• GITAY H ET AL. 2002. Climate change and biodiversity: IPCC Technical Paper V. Available at http://www.ipcc.ch/pdf/technical-papers/climate-changes-biodiversity-en.pdf
  » http://www.ipcc.ch/pdf/technical-papers/climate-changes-biodiversity-en.pdf
• GOTELLI NJ & GRAVES GR. 1996. Null Models in Ecology. Smithsonian Institution Press, Washingon, D.C.: Smithsonian Institution Press, 368 p.
• HERNANDO IR, LLAMBÍAS EJ, GONZÁLEZ PD & SATO K. 2012. Volcanic stratigraphy and evidence of magma mixing in the Quaternary Payún Matru volcano, andean backarc in western Argentina. Andean Geol 39(1): 158-179.
• HSIEH TC, MA KH & CHAO A. 2016. iNEXT: An R package for interpolation and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7(12): 1451-1456.
• JIMÉNEZ-VALVERDE A & HORTAL J. 2003. Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Rev Iber Aracnol 8: 151-161.
• JOST L. 2006. Entropy and diversity. Oikos 113: 363-375.
• KERGOAT GJ, BOUCHARD P, CLAMENS A-L, ABBATE JL, JOURDAN H, JABBOUR-ZAHAB R, GENSON G, SOLDATI L & CONDAMINE FL. 2014. Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family. BMC Evol Biol 14: 220-233.
• KULZER H. 1970. Eine neue Art der Gattung Hoplebaea Brenske (Col. Scarab., Melolonth., Hopliini). Entomologische Arbeiten Museum G. Frey 21: 266-267.
• LEGENDRE P & LEGENDRE L. 2012. Numerical ecology, 3rd English edition. Amsterdam: Elsevier Science, 1006 p.
• LOMOLINO MV. 2001. Elevation gradients of species diversity: Historical and prospective views. Global Ecol Biogeogr 10(1): 3-13.
• MATTHEWS EG, LAWRENCE JF, BOUCHARD P, STEINER WE & ŚLIPIŃSKI SA. 2010. Tenebrionidae Latreille, 1802. In: Leschen RAB, Beutel RG and Lawrence JF (Eds). Handbook of Zoology. Coleoptera, Beetles. Vol. 2. Morphology and systematics (Elateroidea, Bostrichiformia partim). New York: De Gruyter, Berlin, New York, p. 574-659.
• MENÉNDEZ R. 2007. How are insects responding to global warming? Tijdschrift voor EntomologieTVE 150: 355-365.
• MYERS N. 2003. Biodiversity hotspots revisited. Bioscience 53(10): 916-917.
• NOGUÉS-BRAVO D, ARAÚJO MB, ERREA MP & MARTÍNEZ-RICA JP. 2007. Exposure of global mountains system to climate warming during the 21st Century. Global Environ Chang 17: 420-428.
• OKSANEN J ET AL. 2018. vegan: Community Ecology Package. R package version 2.5-2.
• PAYNE D, SPEHN EM, SNETHLAGE M & FISCHER M. 2017. Opportunities for research on mountain biodiversity under global change. Curr Opin Env Sust 29: 40-47.
• PEÑA LE. 1985. Revisión del género Psectrascelis Solier (Coleoptera: Tenebrionidae). Rev Chil Entomol 15-51.
• R CORE TEAM. 2012. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
• ROIG FA. 1998. La vegetación de la Patagonia. In: MN Correa (Ed). Flora Patagónica. Colecc Cient INTA 8(1): 48-166.
• ROIG-JUÑENT SA, AGRAIN F, CARRARA R, RUIZ-MANZANOS E & TOGNELLI MF. 2008. Description and phylogenetic relationships of two new species of Baripus (Coleptera: Carabidae: Broscini) and considerations regarding patterns of speciation. Ann Carnegie Mus 77: 211-227.
• ROIG-JUÑENT SA ET AL. 2018. The Patagonian Steppe biogeographic province: Andean region of South American transition zone? Zool Scr 47(6): 623-629.
• ROIG-JUÑENT SA & SALLENAVE S. 2005. Una nueva especie de Trechisibus de la Argentina (Coleoptera: Carabidae). Rev Soc Entomol Arg 64(3): 87-92.
• SÁNCHEZ-PIÑERO F & AALBU RL. 2002. Tenebrionid Beetles. In: Case TJ, Cody ML and Ezcurra E (Eds). A new island biogeography of the Sea of Cortes. New York: Oxford University Press, New York, p. 129-153.
• SILVESTRO VA. 2018. Revisión sistemática y análisis filogenético de la tribu Scotobiini (Insecta: Coleoptera: Tenebrionidae). Doctoral Thesis, Universidad de Buenos Aires, Buenos Aires: Argentina, 250 p.
• SILVESTRO VA, CARRARA R & FLORES GE. 2012. Redescripción y consideraciones biogeográficas de dos especies de Scotobius (Coleoptera: Tenebrionidae) de ambientes montanos del centro de Argentina y Chile. Rev Soc Entomol Arg 71(3-4): 191-202.
• SILVESTRO VA, GIRALDO-MENDOZA AE & FLORES GE. 2015. Pumiliofossorum: A new genus of Scotobiini (Coleoptera: Tenebrionidae) with two new species from Peru, and a revised key for the genera of the tribe. Zootaxa 3986(4): 461-471.
• URBAN M. 2015. Accelerating extinction risk from climate change. Science 348(6234): 571-573.
• VIDAL P & GUERRERO M. 2007. Nuevas especies de Psectrascelis Solier, 1836 (Coleoptera: Tenebrionidae) de Chile. In: Los Tenebriónidos de Chile. Ediciones Universidad Católica de Chile. Santiago: Chile, p. 431-444.
• WALTHER G-R, BERGER S & SYKES MT. 2005. An ecological “footprint” of climate change. P Roy Soc B 272: 1427-1432.
• ZACHARIASSEN KE. 1996. The water conserving physiological compromise of desert insects. Eur J Entomol 93: 359-369.

Publication Dates

• Publication in this collection
  09 Aug 2021
• Date of issue
  2021

History

• Received
  21 Nov 2019
• Accepted
  15 June 2020