Research Article |
Corresponding author: Bert Kohlmann ( bkohlmann64@gmail.com ) Academic editor: Andrey Frolov
© 2019 Bert Kohlmann, Ángel Solís, Guillermo Alvarado.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kohlmann B, Solís Á, Alvarado G (2019) Description of Onthophagus humboldti and Uroxys bonplandi, two new scarab beetles (Coleoptera, Scarabaeidae, Scarabaeinae) from Costa Rica, with notes on tropical mountain brachyptery and endemicity. ZooKeys 881: 23-51. https://doi.org/10.3897/zookeys.881.38026
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Two new endemic species of scarab beetles are described from Costa Rica, Onthophagus humboldti sp. nov. and Uroxys bonplandi sp. nov. Onthophagus humboldti sp. nov. is also the tenth brachypterous Onthophagus species to be described worldwide, representing also a case of extreme brachyptery in Onthophagini. Illustrations for both new species, as well as marking differences with closely related species are included. Maps showing the distribution of the new species, as well as the distribution of brachypterous and endemic scarab-beetle species for Costa Rica are presented and discussed. The Cordillera de Talamanca represents an area where Scarabaeinae (four genera) show very high known levels of brachypterism in Mesoamerica. A reconstruction of the montane environment in the Cordillera de Talamanca during the Last Glacial Maximum (~24 ka) is analyzed, in order to try to understand a possible historical biogeography model that might promote high levels of brachypterism in scarab-beetles. The present study supports previous proposals that brachyptery is correlated with stable environments associated with deeply incised valleys. Tropical mountain ranges are also identified as having more endemics than lowland rain forests, contradicting accepted wisdom. Lastly, a mitochondrial DNA analysis supports the existence of the Onthophagus dicranius and the O. clypeatus species-groups as two well-defined and closely related branches.
Biogeography, boreotropical distribution, Cordillera de Talamanca, extreme brachyptery, refugia, Last Glacial Maximum, mitochondrial DNA, paleogeography
Notre imagination n’est frappée que par ce qui est grand; mais l’amoureux de la philosophie naturelle devrait également réfléchir aux petites choses.
Alexander von Humboldt
“Voyage aux régions équinoxiales du nouveau continent”, 1814
During the last 27 years, a concerted effort has been undertaken by the first two authors in order to study the scarab beetles (Scarabaeidae: Scarabaeinae) of Costa Rica. The detailed evaluation of the specimens of this survey has yielded many new species. Currently, Scarabaeinae in Costa Rica are represented by seven tribes and 28 genera (
The discovery of these two new species of scarab beetles, one brachypterous (Onthophagus) and both of them endemic to the country, bring to the forefront questions regarding the existence of such interesting phenomena as brachyptery and endemicity. These two mechanisms seem to be concentrated in the mountainous areas in Costa Rica. Using these new species as a model, an attempt is made to try to understand the existence of these two processes in the mountains of the tropics.
Considering the small area that Costa Rica occupies (51,100 km2), it displays a great number of brachypterous scarab-beetle species (7) from four genera (Ateuchus, Canthidium, Cryptocanthon, Onthophagus). This represents a figure of 0.014 brachypterous species / 100 km2. One can compare this number with the state of Oaxaca in Mexico, an area arguably similar to Costa Rica in extension (93,952 km2) and biogeography/ecology. This Mexican state reports four brachypterous scarabaeines from two genera (Canthidium and Onthophagus) (
Recent biogeographical studies of these scarab beetles in Costa Rica (
As mentioned previously in another paper (
Specimens studied came from the insect collection of the Museo Nacional de Costa Rica (National Museum of Costa Rica, ex INBio collection). All type material (holo- and paratypes) of both species is deposited in the same collection.
The specimens were studied using a Zeiss Stemi 2000–C stereozoom binocular microscope. Measurements were made to the nearest 0.1 mm using an ocular micrometer. Morphological nomenclature follows
The synthetic aperture radar (SAR) image of Costa Rica, which has been used as the base map in figures 5 and 6, was downloaded from the NASA website (https://www2.jpl.nasa.gov/srtm/central_america_radar_images.html). The maps were made and edited using the QGIS geographic information system software; this program is open source on the Internet for multiple platforms (https://qgis.org/en/site/forusers/download.html).
We downloaded from the Internet publicly available raster-type bathymetric maps, obtained from the General Bathymetric Chart of the Oceans (GEBCO) website (https://www.gebco.net/data_and_products/gridded_bathymetry_data/). We also obtained raster elevation maps freely available from the NASA project website and the Ministry of Economy, Trade and Industry (METI) of Japan, called the Advanced Spaceborne Thermal Emission and Reflection Radiometer (ASTER), Global Digital Elevation Model (GDEM) (https://asterweb.jpl.nasa.gov). In addition, we used the commercial program Photoshop CS3 Extended Version 10.0.1 to prepare the versions for this publication.
The mitochondrial DNA information (DNA barcoding) was obtained through the methodology described by
Costa Rica. Prov. Puntarenas. Buenos Aires, P.N. La Amistad. Tres Colinas.
Museo Nacional de Costa Rica, Santo Domingo de Heredia, Costa Rica.
Holotype male, pinned, with genitalia in a separate microvial. Original label: “Costa Rica. Provincia Puntarenas. Buenos Aires, Parque Nacional La Amistad. Tres Colinas. 2100–2200 m. 27–29 Febrero 2008. A. Solís, M. Moraga. Trampa Foso. L S 343850 565700.” “HOLOTYPE/Onthophagus humboldti Kohlmann, Solís, Alvarado [red printed label]”.
Paratypes. (8 males, 4 females). “Costa Rica. Provincia Puntarenas. Buenos Aires, Parque Nacional La Amistad. Tres Colinas. 2100–2200 m. 27–29 Febrero 2008. A. Solís, M. Moraga. Trampa Foso. L S 343850 565700.”
Elytra as long as or shorter than pronotum (Fig.
Holotype.
Male (Fig.
Pronotum (Fig.
Elytra convex, with clear margins and without a humeral callus; with eight well-marked striae, fine and clearly impressed and with crenulating punctures; intervals clearly punctured, punctures big and dense, not aligned, bearing short, stiff setae along the lateral and apical margins; microsculpture reticulate and regular. Wing brachypterous, measuring 0.75 mm (Fig.
Mesosternum with evident annular punctures bearing no setae. Metasternum shagreen and finely punctured, more coarsely laterally, basal third with a sulcus. Abdominal segments shagreen and finely punctured.
Fore femur long, slender, and punctured; meso- and metafemur short and elongate, light yellow. Fore tibia long, slender and arched (Fig.
Female, length 6.3 mm; maximum width 3.6 mm. It is similar to the male and varies in having a clypeus not forming a horn, clypeus shagreen, genae not projected as teeth, with a head frons keel, two small platelet projections at head vertex, no pronotal projection, no projected pronotal anterior angles, fore tibia short, fore femur short, last abdominal sternite broad.
Length 5.6 to 7.2 mm. Width 3.2 to 4.3 mm. Small males do not have the bifid clypeal horn, just a small erect lamella; vertex platelets forming a small projection; anterior pronotal angles not projected, pronotal projection forming a small carina. Body color varying from black to piceous red.
This species is dedicated in honor of Friedrich Wilhelm Heinrich Alexander von Humboldt, Prussian geographer, explorer, and naturalist, commemorating the 250th anniversary of his birth. He is widely recognized for fathering the work on physical and plant geography, which laid the foundation for the development of modern biogeography.
Onthophagus humboldti sp. nov. will key out to O. micropterus Zunino & Halffter, 1981, in Kohlmann and Solís´ key (
This species is so far only known from the area of Tres Colinas, near Buenos Aires, in the province of Puntarenas (Fig.
Onthophagus humboldti sp. nov. is endemic to the Cordillera de Talamanca and is the tenth known brachypterous Onthophagus species to be described worldwide. A closely related species, O. micropterus, is also distributed in the Cordillera de Talamanca (Fig.
This species belongs to the O. dicranius species group, as established by
This situation seems to be in congruence with the boreotropical distribution hypothesis (
This pattern of distribution would clarify those proposed by Halffter (
Actually, the groups of species mentioned above are congruent with the typical characteristics of the so-called boreotropical distribution. Therefore, the aforementioned distribution variant, the “Paleoamerican Tropical Pattern”, seems to be the same with the boreotropical distribution and it is proposed here to use the term boreotropical distribution from now on as it is a more complete and well-founded concept, besides being an older one. This pattern has been studied and characterized at very fine phylogenetic and biogeographic analysis levels in animal and plants (
Costa Rica. Guanacaste. Sector Santa María, path to the cone of the Santa María, part of the Rincón de la Vieja volcanic massif, 1565 m.
Museo Nacional de Costa Rica, Santo Domingo de Heredia, Costa Rica.
Holotype male, pinned, with genitalia in a separate microvial. Original label: “Costa Rica. Provincia Guanacaste. Sector Santa María, Sendero a Pico Volcán Santa María. 1565 m. 2 Diciembre 2017. Col. Sergio Salas Ríos. Biocol. 10.8039N, 85.3281W.” “HOLOTYPE/Uroxys bonplandi Kohlmann, Solís, Alvarado [red printed label]”.
Paratypes (18 males, 25 females). “Costa Rica. Provincia Guanacaste. Sector Santa María, Sendero a Pico Volcán Santa María. 1565 m. 2 Diciembre 2017. Col. Sergio Salas Ríos. Biocol. 10.8039N, 85.3281W (6 males, 10 females). “Tilarán Bosque Nuboso Santa Elena. 1600 m. 26 Noviembre – 8 Diciembre 1999. J. Rodríguez Trampa de Luz. L N 258000 45000” (1 female). “Provincia Puntarenas. Monteverde Zona Protectora Arenal-Monteverde. Parcela Brillantes. 1500–1600 m. 17–19 Junio 2009. A. Solís, J.D. Gutiérres. Trampa Foso. L N 252009 450981” (4 males, 2 females), “13–1600 m. 10°18'N, 84°48'W. Univ. California EAP 1991” (1 female). “Est. La Casona. 1520 m. Reserva Biológica Monteverde. N. Obando. Octubre 1991. L N 253250 449700” (2 males, 2 females), “Septiembre 1990 (1 male), 29 Nov – 17 Diciembre 1994, K. Martínez, L N 253200 449700” (2 males, 1 female). “Provincia Alajuela. San Ramón. Zona Protectora Arenal-Monteverde. Parcela El Valle. 1600–1700 m. 16–18 Jun 2009. A. Solís, J.D. Gutiérrez. Trampa Foso. L N 255970 452538” (3 males, 9 females).
Anterior of frons evenly convex, without carina or groove, with a dimple or transversely rugose; clypeal margin indented at junction with clypeogenal suture; dorsal ocular area twice as long as wide, distance between eyes five times eye width; pronotum evenly convex, sides angled near middle; elytral apex of the second to fourth intervals forming an oblique keel (Fig.
Holotype.
Male, length 7.4 mm; maximum width 3.8 mm. Elongate oval, shining reddish black (Fig.
Pronotum at median angulation as wide as elytra; lateral edges of pronotum produced into prominent angles (Fig.
Elytron moderately convex, clearly punctate (faintly in Uroxys dybasi Howden & Young, 1981), humeral umbone small; striae distinct but shallow, with distinct punctures evenly spaced for most of length of each stria, seventh stria extending three-fifths length of elytron; posterior tenth of first stria furrowed; intervals flat, slightly flattened and constricted, not produced, except at the apex of the second to fourth intervals forming an oblique keel (Fig.
Meso- and metasternum clearly punctate (faintly in dybasi); meso-metasternal suture medially moderately angulate anteriorly, moderately angulate laterally, three times farther from anterior margin of mesosternum than from mesocoxal cavity; metasternum swollen, with distinct median posterior depression.
Ventral abdominal segments two to five of equal length medially, each only slightly shorter medially than sixth; sixth slightly longer laterally than medially; anterior margins with small punctures (big crenulated punctures in dybasi). Pygidium strongly convex, faintly punctate, twice as wide as long; sulcus surrounding disc deep basally, shallow elsewhere; margin formed of same width apically and laterally; sulcus basally very slightly arcuate toward apex on each side of midline.
Fore tibia elongate with inner margin broadly curved (Fig.
Female, length 6.9 mm; maximum width 3.6 mm. It is similar to the male and varies in having a rugose clypeus, lateral edges of pronotum produced into less prominent angles. Elytral apex without oblique keels. Fore femur and fore tibia not as long. Middle and hind femur without a projection or swelling at apical third.
Length 5.7 to 7.6 mm. Width 3.2 to 4.1 mm. The center of the head might have a small dimple and/or also a slight transverse rugosity.
This species is dedicated in honor of Aimé Jacques Alexandre Goujaud Bonpland, French naturalist, physician, and botanist, member of the scientific expedition that accompanied Humboldt to Spanish America.
Uroxys bonplandi sp. nov. will key out to U. dybasi in
Uroxys bonplandi sp. nov. has been collected so far in the Cordillera de Guanacaste and the Cordillera de Tilarán (Fig.
Uroxys bonplandi sp. nov. coincides with U. dybasi in being distributed along the Guanacaste and Tilarán mountain ranges. (Fig.
Another related species is Uroxys tacanensis Delgado & Kohlmann, 2007, known only from its type locality, the Tacaná volcano, at the border of Mexico and Guatemala, living in cloud forest at 2000 m altitude (
As mentioned above, O. humboldti sp. nov. is a brachypterous species. There are also another two brachypterous species of Onthophagus in Costa Rica: O. inediapterus Kohlmann & Solís, 2001 (Onthophagus dicranius Bates line) and O. micropterus Zunino & Halffter, 1981 (Onthopagus dicranius Bates line) (
In relation to wing reduction,
Accepted wisdom has proposed that in Scarabaeoidea the evolution of flightlessness is related to temperate highland forests in the tropics; arid environments, such as deserts; temperate forests at low latitudes in the southern hemisphere; islands; termite nests; and cold regions (
At present, a very much accepted hypothesis that tries to explain the origin of this phenomenon is the one given by
It is clear that the distribution of brachypterous forms is not random, certain patterns are repeated. In North and Central America no brachypterous Scarabaeinae are known from the lowlands, alpine regions, or from rodent nests. They are only known from the mountains in Costa Rica, especially the Talamanca range and the Sierra Madre del Sur in Mexico. In all cases these flightless species live in humid montane forests, spanning an altitudinal distribution that goes from 1100 to 3000 m. Flightlessness in scarabaeines is confined so far in Mesoamerica to small-sized genera, like Onthophagus (9), Canthidium (4), Cryptocanthon (2), and Ateuchus (1), in descending order of known species number. On the other hand, brachyptery seems to be confined in South American Scarabaeinae to eight medium-sized species of the genus Dichotomius, out of 170 described taxa, where this condition has evolved independently, at least four times in this genus (
If it is generally accepted that the occurrence of brachyptery reflects long-term stability of habitats (
If one would plot the geographical ranges of the fore mentioned brachypterous scarab-beetles on a map, coincident occurrence of such taxa is apparent. The pattern that emerges is one in which one particular area stands out, the Cordillera de Talamanca (Fig.
Figure
Present day distribution of Onthophagus humboldti sp. nov. (blue dot) and O. micropterus (red dot) and lines indicating proposed localities (rhombi) depressed by 1500 m (14 km in straight line) generated by the last glacial maximum, ~25–23 ka, in the Cordillera de Talamanca. All mountain systems are 150 m lower than present day height and an estimated sea level descent of 120 m is depicted. Dotted black lines represent present-day sea levels.
We propose here that the Valle de El General might have acted as a refugium for the brachypterous species during the last glacial maximum (LGM). This valley would then resemble what has been called a cryptic refugium (
The Valle de El General must have been formed by the uplift of the Cordillera de Talamanca and the Fila Costeña (Costeña range), a process that began about 7 million years ago and accelerated during the last 4 million years, triggered by the arrival of the Coco submarine range (an extinct volcanic range, also known as Cocos Ridge) in the Pacific and by the compression of the microplate of Panama in the Caribbean. The Arenal depression (tectonic graben) must have originated less than 2 million years ago, although there is no better estimate. While the Valle Central (Central Valley) is of a more recent formation and its age goes back to less than half a million years (
Areas of endemism (AE) are fundamental areas in the analyses of biogeography and are defined as areas of non-random distributional congruence among taxa, whose biogeographical history probably shared common factors such as geological, ecological, or evolutionary processes (
The mapping of the AE’s (Fig.
An analysis of the cytochrome c-oxidase I (COI) for both new species was undertaken. The Bar Code Index Number (BIN) for each species is: Onthophagus humboldti, BOLD: ABA7524 and Uroxys bonplandi, BOLD: ABA3722. Results are clearly distinct, whereas the value registered for the Onthophagus pair gives an average Kimura–2–parameter [K2P] value of 6.35 % with a maximum distance of 10.6 %, the amount of DNA difference for the Uroxys pair is of only 3.3 %. Uroxys results stay in line with other similar ones calculated for a group of Caribbean-Pacific scarab-beetle sister-species pairs separated by the Cordillera de Talamanca which started its emergence around 7 million years ago; Phanaeus pyrois Bates, 1887 and P. malyi Arnaud, 2002 ([K2P]= 3.8 %) and Phanaeus beltianus Bates, 1887 and P. changdiazi
However, the value shown for the Onthophagus sister-pair looks higher ([K2P] = 6.35 %). This is interesting if we consider that this pair is formed by flightless species and the geographical nearness between them, 52 km in a straight line (Fig.
This last explanation is concordant with the previous results shown in the brachyptery section, where it is suggested that the Cordillera de Talamanca has been an area of long-term stability, thus allowing the continuous and uninterrupted presence of clades. In general, areas with a preponderance of brachypterous populations represent areas of older populations (
In a very interesting study of phylogenetics and biogeography of the genus Onthophagus inferred from mitochondrial genomes,
Among the American Onthophagini that
Onthophagus clypeatus Blanchard, 1846 and O. rhinolophus Harold, 1869, are part of the clypeatus species group and considered to be closely related to the dicranius species group (
We present in Figure
BOLD uses neighbor-joining trees which group sequences together by the number of amino acid or nucleotide differences. The arrangement of the specimens in the tree is based on sequence similarities, with the sequences that are most similar placed closer together on the tree, and with the branch length indicating the degree of similarity. The percentage of similarity between sequences can be measured against the legend (line), where the longer the branch the more disparity between the sequences. It is often expected that specimens of the same species have more similar sequences and cluster closer together than specimens from different species.
This figure is part of a more general analysis done for the genus Onthophagus in Costa Rica. All four depicted taxa are mountain species distributed in the mountains of Costa Rica and Panama. O. humboldti sp. nov. seems to be a closely related species of O. dorsipilulus Howden & Gill, 1993, a species distributed in the Cordillera de Talamanca and the Cordillera de Chiriquí in Costa Rica and Panama from 1400 to 1800 m altitude and would seem to be its ecological equivalent at a slightly lower altitudinal belt. On the other hand, O. micropterus, also distributed in the Cordillera de Talamanca, seems to be the sister species of O. quetzalis Howden & Gill, 1993, a taxon distributed in the neighboring Cordillera de Tilarán and Guanacaste. The DNA mitochondrial analysis neatly recovers the formation of this cluster belonging to the O. dicranius species-group (
Finally, Onthophagus having around 2200 valid species (
The study of mountain biology retains all of its actuality and relevance. This study on tropical mountain brachyptery and endemicity falls in line with what Humboldt had already discovered (
We would like to thank Claudia Aragón for the excellent drawings that illustrate this paper and to Sergey Tarasov and Andrey Frolov for reviewing this paper. We also thank the Alexander von Humboldt Foundation, Germany, for having donated the stereoscope used in this study, as part of a sabbatical stage by Kohlmann in 2010 at the Technical University of Dresden. We are also in debt to Ashly Salazar, librarian at EARTH University, for finding difficult references. We are also in debt to Professor Abbie Briggs of EARTH University for revising the use of English. Last but not least, we are indebted to the Museo Nacional de Costa Rica for allowing us to review its beetle collection and for its support in the preparation of this publication.