Recent intensive samplings carried out across the mountainous regions of El Pinal (Puebla, Mexico) have provided new insights into the main environmental factors that affect the geographic distribution of the scarabaeinae beetles of the Trans-Mexican Volcanic Belt above 2500 m a.s.l. This study is part of an ongoing project investigating the diversity and biogeography of copro-necrophagous beetles (Scarabaeinae, Aphodiinae, Geotrupinae and Silphidae) in the easternmost areas of the Trans-Mexican Volcanic Belt.

Previous experience allows us to propose a series of predictions that we expect will provide possible explanations for current distribution patterns observed in Scarabaeinae and other groups of insects found in the Trans-Mexican Volcanic Belt. This mountain range has a primarily biogeographic importance, limiting the Mexican High Plateau in the South and connecting the western and eastern Sierra Madre mountain chains, which are considered the most important routes for dispersal of mountain fauna of northern origin. The taxonomic and biogeographic study of the species collected so far in El Pinal (including Onthophagus clavijeroi sp. n. and Onthophagus martinpierai sp. n. described here), along with their possible relationships with other known species, allows us to answer the preliminary assumptions proposed.

Con base en capturas intensivas realizadas en la montaña de El Pinal (estado de Puebla, México) se plantea un análisis de los factores que intervienen en la distribución geográfica de la fauna de montaña (en este caso Scarabaeinae) por encima de los 2500 m de altitud, en el Sistema Volcánico Transversal (SVT), principal cordillera dispuesta en sentido latitudinal de México y de toda América. Este artículo es parte de una serie de trabajos coordinados para estudiar los escarabajos coprófagos y necrófagos de la parte oriental del SVT.

La experiencia generada nos permite plantear una serie de premisas (Introducción) que se espera cumpla la distribución de la fauna de Scarabaeinae y de otros grupos en el SVT, cordillera de primera importancia biogeográfica, pues limita por el sur el Altiplano Mexicano (una península de Norte América) y une las dos principales cordilleras que se desarrollan N-S: las Sierras Madres Occidental y Oriental, las más importantes vías de penetración de la fauna de montaña de origen septentrional. Un análisis de las afinidades taxonómicas y biogeográficas de las colectas de Scarabaeinae en El Pinal (incluyendo dos especies nuevas de Onthophagus que se describen) nos permite dar respuesta en la Discusión a las premisas planteadas en la Introducción.

Scarabaeinae , Onthophagus , mountain fauna, Mexican Transition Zone, Trans-Mexican Volcanic Belt

Scarabaeinae , Onthophagus , fauna de montaña, Zona de Transición Mexicana, Sistema Volcánico Transversal

Mexico is a country of vast mountain ranges. In tropical areas, these environmental conditions imply a rich and peculiar biota; the particular geographic position of Mexico and the extensive Mexican Transition Zone, which occurs between the Nearctic and Neotropical regions, emphasizes the biological exclusivity of this region.

The Mexican Transition Zone (hereafter referred to as MTZ) has been proposed by Halffter for insects and other groups of animals (e.g., Halffter 1987; Halffter 2003; Halffter et al. 2008), while Rzedowski introduced the concept of Megamexico, a phytogeographic unit defined on the basis of distribution patterns observed in Mexican plants (Rzedowski 1991). The concept of the transition zone has also been utilized in general terms by Zunino and Zullini (2003: 66–68 and literature quoted therein). A biogeographical transition zone is a geographical area of biotic juxtaposition with a gradient of replacement and partial segregation between components, which are promoted by historical and ecological changes. During his travel across the Malay Peninsula between 1854 and 1862, A. R. Wallace had already realized the difficulty of delimiting clear biogeographical borders between the Oriental and Australian regions, a wide area with transitional characteristics, which is today known as Wallacea (see Ferro and Morrone 2014 for a very interesting and updated revision of biogeographic transition zones).

The transition occurs when biota of two different regions, the distribution areas of which have not been historically constrained by significant biogeographical barriers, meet and overlap within the same geographic area and time. If the transition character remains temporally, this zone may harbour species of different geographical and evolutionary origins.

The mountain ranges of the MTZ play a fundamental role as a main route for the southward dispersal of northern fauna. Among the Mexican mountain ranges, the Trans-Mexican Volcanic Belt (hereafter referred to as TMVB) is the only one in the Americas with latitudinal development, intervening as central bridge between the western and eastern Sierra Madre mountain ranges (see Map 1).

Map 1. 

Orographic systems mentioned in the text: SMOc: Sierra Madre Occidental; SMOr: Sierra Madre Oriental; AM: Mexican Plateau; SVT: Trans-Mexican Volcanic Belt; SMS: Sierra Madre del Sur; SPO: Puebla-Oaxaca Mountain System.

Recently, Luna et al. (2007) provided a description of the geology, physical environment, as well as flora and fauna of the TMVB, presenting several biogeographic studies.

The TMVB features a series of mountain ranges and volcanoes that cross Mexico transversally between the parallels 18°30’ and 21°30’ W. The orogenesis of this area is widely accepted to result from the subduction of both the Rivera Microplate and northern border of the Cocos Plate under the southern boundaries of the North American Plate. Since the Early-Mid Miocene, the TMVB became an independent geological province because of the East-West rotation of the Transvolcanic Belt, as well as the change of type and composition of the main volcanic activities: silicious and explosive in the Sierra Madre Oriental, intermediate and eruptive in the TMVB (Ferrari et al. 2012).

Four main volcanic events that occurred over the last 19 million years contributed primarily to the formation of the TMVB, with the greatest volcanic activity recorded in the Quaternary. This volcanic eruption also involved the areas and locations investigated in this study, such as the mountains Pico de Orizaba, Cofre de Perote and La Malinche (see Torres-Miranda and Luna 2007 and other chapters in Luna et al. 2007).

The TMVB stretches for approximately 1000 km in length and, despite its current unity, the geological history of the areas lying east and west of the meridian 101° does not show any degree of continuity until the end of the Pliocene and Quaternary. Along with the geomorphology of the TMVB, the main stratovolcanoes of the central and eastern regions built up in the Upper Pleistocene (see Ferrari et al. 2012) are of great importance for explaining several biogeographic patterns, as well as vicariant events that occurred along the TMVB and are commonly represented within mountain lineages of northern origin. Initially, the lineages found only either in the western or eastern halves of the TMVB can be considered to be the oldest, with different biogeographic histories, as these are related to the Sierra Madre Occidental, the Sierra Madre del Sur or the Sierra Madre Oriental, respectively. On the other hand, lineages or species that are widely distributed across the entire TMVB can be considered the most recent ones, and show a succession of very closely related taxa.

Given its East-West orientation (Map 1) and dynamic geomorphological history, the TMVB is not only an important dispersal route for northern fauna with mountain adaptations, but is also an area characterized by a large number of vicariant events reported for many organisms as well as a high beta diversity (see Luna et al. 2007).

All of the results obtained to date are included in seven articles (including the present study), (Sanchez-Huerta 2015, Arriaga et al. 2016, Moctezuma et al., Skelley and Sanchez-Huerta, Sanchez-Huerta et al. A, Sanchez Huerta et al. B), two Master’s dissertation (Moctezuma 2014, Sanchez-Huerta 2016) and a Doctoral thesis (Arriaga 2015).

The initial predictions to be tested throughout these studies are as follows:

The entomofauna (especially Scarabaeinae) of the TMVB above 2500 m a.s.l. corresponds to the Paleo-American Distribution Pattern (see Halffter 1987, Halffter 2003, Halffter et al. 2008), that are northern lineages belonging to worldwide distributed genera with old penetration in the American continent. Within this distributional pattern, the Mountain Paleo-American sub-pattern, which includes lineages limited to the mountains of the MTZ, should take over.

The dispersal of lineages of the Mountain Paleo-American distribution pattern essentially occurs horizontally (Lobo and Halffter 2000), following a given altitudinal range and presenting dispersal events only under advantageous climatic conditions, whereas isolation and vicariant events appear under adverse climatic conditions, which are also responsible for the reduction of the area of distribution. Time represents a basic difference between horizontal and vertical colonization; vertical colonization requires the adaptation of lineages to new environmental conditions while horizontal colonization only requires dispersal.

The bioclimatic zones in mountainous areas experienced major altitudinal shifts during the Quaternary and Recent periods. The complex orography of the MTZ, especially that of the TMVB, along with the catathermal climatic periods, had strong effects on the high-altitude communities, which underwent a severe displacement toward the lowlands that were interconnected to a greater extent. Under the new environmental conditions, these biological elements found a favourable situation in which to spread horizontally. However, during anathermal periods, bioclimatic zones move upward to higher elevations, with a consequent fragmentation of the distribution area of the species involved. These events are often followed by speciation processes associated with dynamic vicariance (see Zunino 2003: 161; Morrone 2009: 16).

Occasionally there are cases of vertical colonization, represented by upward dispersal from the lowlands. This dispersal event is expected to occur in species with the Paleo-American High Plateau Distribution sub-pattern (Halffter 2003). In some exceptional cases, some species of Neotropical affinity distributed on the Mexican High Plateau might penetrate the mountains, particularly at lower elevations.

Vertical movements are not expected on the southern slopes of the TMVB such as the Balsas and Tehuacán-Cuicatlán depressions, the fauna of which, adapted to warm and dry conditions, shows Neotropical affinity. The rare antiquity of the mountain El Pinal, but particularly the strong contrast in ecological conditions, has not favored the upward displacement of tropical species.

The dispersal-distribution pattern with predominantly horizontal distribution, observed in the TMVB and in Mexican mountain ranges in general, is completely different from the pattern found in the Andes (see Escobar et al. 2006, 2007) or on the Mexican mountains that are isolated within a tropical environment, such as Los Tuxtlas (Alvarado-Roberto 2014). In these cases, vertical colonization appears to be the more common distribution pattern, with the Neotropical fauna moving toward higher altitudes from the tropical lowlands.

In these tropical mountains with vertical colonization, the highest species richness occurs at intermediate elevations (at approximately 1500 to 1700 m a.s.l.), with rarefaction occurring at higher altitudes (Escobar et al. 2007). In the TMVB, which is colonized by fauna of northern origin, there is a representative number of species exclusive to high elevations that are not found at lower altitudes.

The species richness of Scarabaeinae on tropical mountains with vertical colonization is higher in wooded areas, as occurs in the surrounding lowlands (Escobar 2004, Escobar et al. 2007). As in Europe (see for example Errouissi et al. 2004, Jay-Robert et al. 2007), a higher number of Scarabaeinae species occur in opened or semi-opened areas in the TMVB, with a very low presence of species characteristic of forests and woodlands.

In this article, we describe two new Onthophagus species collected to date only in the westernmost mountains of the eastern sector of the TMVB (El Pinal). Phylogenetic and biogeographic relationships of both species are discussed, and our preliminary hypotheses on Scarabaeinae and other copro-necrophagous Scarabaeoidea of the TMVB are tested against the distribution patterns observed in these new Onthophagus and other species collected in the same sites.

Sampling was conducted on the westernmost mountains of the eastern sector of the TMVB (El Pinal, Puebla, Mexico). To date, the entomofauna of this area has been little studied compared to the tropical sector of the Mexican Transition Zone.

Copro-necrophagous beetles were collected using common pitfall traps baited with human and cow excrements, and squid. Collected specimens were processed at the Institute of Ecology (INECOL) in Xalapa.

The morphological study was carried out on multiple specimens belonging to the new species described here. In order to study the male and female genital organs, individuals were softened in hot water for approximately 20 minutes and their genitalia extracted. In males, the aedeagus was dissected for examination of the endophallic sclerotized structures of the internal sac. Genital structures of both sexes were cleared in a 10% KOH solution. Finally, the aedeagus, endophallic sclerotized pieces and vagina were either mounted on a paper-board with DMHF resin or preserved in microvials with glycerol.

Specimens collected during fieldwork were deposited in the following private and public collections (information regarding the repositories of holotypes and paratypes are provided with the species descriptions):

CNC Canadian National Collection, Ottawa, Canada

GH Gonzalo Halffter collection, Xalapa, Mexico

INECOL Instituto de Ecología A. C., Xalapa, Mexico

LD Leonardo Delgado collection, Xalapa, Mexico

MM Miguel A. Morón, collection, Xalapa, Mexico

MR Michele Rossini collection, Pesaro, Italy

MZ Mario Zunino collection, Asti, Italy

VM Victor Moctezuma collection, Xalapa, Mexico

The Scarabaeinae beetles collected during our fieldwork in El Pinal belong to the genus Onthophagus. In addition to O. clavijeroi and O. martinpierai, five more species have been found in the same localities: O. chevrolati retusus Harold, O. incensus Say, O. lecontei Harold, O. mexicanus Bates, and O. bolivari Moctezuma, Rossini & Zunino (a new species recently described in Arriaga et al. 2016).

As proposed at the beginning of this paper (prediction 1), species that occur above 2500 m belong to the Paleo-American Distribution Pattern. In the MTZ, the genus Onthophagus is a lineage of ancient penetration, showing high diversity in terms of both number of species and eco-geographic distribution. These characteristics can explain the ability of the genus to fit the Palaeo-American pattern in different ways. Only one specimen of O. incensus (a species very abundant at lower altitudes) has been collected at 2639 m. This species is distributed from Mexico to the northern regions of South America (Colombia and Venezuela) and associated with tropical conditions, although it also occurs in mountainous areas up to 2000 m a.s.l. This specimen was collected on the lowest part of El Pinal, in the same sampled area in which a large number of O. mexicanus was found, a species widely distributed on the Mexican High Plateau.

Among the lineages of Onthophagus (see Zunino and Halffter 1997) distributed across the southern High Plateau and foothills of the surrounding mountain ranges (Paleo-American Distribution on the High Plateau), two species have been found: O. lecontei (landolti group) and O. mexicanus (mexicanus group) (Zunino and Halffter 1997).

All of the remaining species, which constitute common elements of the scarabaeinae fauna of the TMVB, belong to the Mountain Paleo-American Distribution Pattern. Onthophagus chevrolati retusus is a very characteristic subspecies of the TMVB, reaching the highest elevation to date reported for Scarabaeinae in the MTZ (see Zunino and Halffter 1988). Indeed, this subspecies was found in the highest sampled locality of El Pinal (3017 m). Onthophagus c. retusus occurs in the eastern part of the TMVB, both in the Sierra Madre del Sur and in the Puebla-Oaxaca Mountain System.

Onthophagus clavijeroi and O. martinpierai, along with closely related species, occur in the central and western parts of the TMVB, a distribution pattern shared with O. bolivari (Arriaga et al. in press), the most abundant species of El Pinal, which was also collected on the mountain La Malinche.

El Pinal, a relatively recent and not particularly large mountainous formation, thus hosts representatives of the three main biogeographic patterns to which the genus Onthophagus corresponds across the MTZ. However, on older and higher mountains on the eastern side of the TMVB, the Mountain Palaeo-American distribution pattern will dominate above 2500 m.

Concerning prediction 2, it is important to emphasize that the species collected on El Pinal, as well as their close relatives, can be also found in western and eastern localities of the TMVB, including the Sierra Madre Oriental. As far as we could ascertain in this study, El Pinal appears to have been colonized from both the western and eastern sides, apart from with O. lecontei and O. mexicanus, which possibly arrived via vertical dispersion from the contiguous Mexican High Plateau. Instead, the remaining species (including O. incensus) appears to have adopted a horizontal distribution from the lower altitudes of the eastern TMVB.

The high level of endemism observed on El Pinal, quite unexpected on such a relatively small and recent mountain, may be the result of a recent vicariant event or due to the lack of intensive sampling in the central mountains of the TMVB and the nearby Puebla-Oaxaca Mountain System.

As indicated above, prediction 3 has been fully met, as has prediction 5. We could not test the fourth prediction because of the isolation of El Pinal on the northern side of the TMVB, as well as its lack of contact with the southern tropical depressions.

In accordance with the sixth preliminary hypothesis, the highest value of abundance and number of species were found at 2639 m. In contrast, sampling carried out at higher altitudes (2993 m) yielded a distinctly lower number of species and individuals: Onthophagus c. retusus and O. bolivari were the only species of the chevrolati group to be collected, with a few specimens (e.g., only one individual for O. bolivari). This altitudinal gradient firstly led us to suppose that some species and subspecies of the chevrolati group can reach the highest altitudes in the Mexican mountains. In other mountains of the TMVB, even O. hippopotamus Harold, a species of the chevrolati group associated with gopher nests, occurs at high elevations. Secondly, it is important to note that the altitudinal range between 3000–3100 m a.s.l. represents, with extreme rarefaction, the upper distributional limit of the mountain Scarabaeinae in the MTZ.

Regarding the seventh preliminary hypothesis, the Onthophagus of El Pinal are found in different types of mountain vegetation (e.g., opened and secondary forests, clearings etc.), with greatest abundance in areas dominated by plants that require high solar radiation. Furthermore, the presence and density of trees do not appear to affect the distribution of Onthophagus of El Pinal, in the way that they have been proved to be determinant in the tropical forest of the ZTM.

The authors are grateful to CONACYT for the scholarship awarded to Víctor Moctezuma (No. 281033) for his graduate studies at the Instituto de Ecología, A.C. We would like to thank the Dirección General of the Instituto de Ecología, A.C. for providing strategic funds to support the fieldwork. We express our gratitude also to Margoth Acuña Tarazona (Instituto de Ecología, A.C.), Fernando Escobar (Instituto de Ecología, A.C.) Alfonsina Arriaga (Université Paul Valéry Montpellier III) for their valuable help and assistance in the field. Alfonso Aceves Aparicio (Instituto de Ecología, A.C.) provided us with the photographs of O. clavijeroi and O. martinpierai, while Patricia Koleff (CONABIO, México) provided important tips for obtaining the book of Luna et al. (2007). The manuscript was translated into English from the original Spanish version by Bianca Delfosse, to whom we extend our gratitude.