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Revista Peruana de Biología

versión On-line ISSN 1727-9933

Rev. peru biol. vol.26 no.2 Lima abr./jun. 2019

http://dx.doi.org/10.15381/rpb.v26i2.15586 

TRABAJOS ORIGINALES

A new species of Andinopanurgus (Hymenoptera: Andrenidae) from high elevations in southern Peru

Una especie nueva de Andinopanurgus (Hymenoptera: Andrenidae) de las grandes alturas del sur de Perú

 

Victor H. Gonzalez 1,* ORCID: 0000-0002-4146-1634 , Mabel Alvarado 2 ORCID: 0000-0001-8135-9223 , Claus Rasmussen 3 ORCID: 0000-0003-1529-6548

 

1. Division of Entomology, Natural History Museum, University of Kansas, USA.

2. Universidad Nacional Mayor de San Marcos, Museo de Historia Natural, Departamento de Entomología, Perú.

3. Department of Bioscience, Aarhus University, Denmark.


Abstract

We describe and figure a distinctive new species of the bee genus Andinopanurgus Gonzalez and Engel (Andrenidae, Protandrenini) from Apurímac and Cusco in southern Peru. Andinopanurgus vargasllosai Gonzalez and Alvarado, n. sp., occurs at elevations above 4000 m in the Central Andes and is the second species of this genus in Peru. The new species possesses terga with semi-translucent distal margins, a unique feature among Andinopanurgus, and it combines morphological features of the two species groups previously recognized in the genus. To facilitate its recognition, we provide an updated key to species of Andinopanurgus.

Keywords: Andes; Anthophila; Apoidea; pollinators.


Resumen

Describimos e ilustramos una especie nueva del género Andinopanurgus Gonzalez y Engel (Andrenidae, Protandrenini) procedentes de Apurímac y Cusco, al sur de Perú. Andinopanurgus vargasllosai Gonzalez y Alvarado, n. sp., se encuentra en alturas superiores a los 4000 m en los Andes centrales y es la segunda especie del género registrada para el Perú. La especie nueva posee tergos metasomales con las márgenes distales semi-translúcidas, una característica única dentro de Andinopanurgus, y combina características morfológicas de los dos grupos de especies hasta ahora reconocidos en el género. Con el fin de facilitar la identificación, presentamos una clave actualizada para las especies de Andinopanurgus.

Palabras clave: Andes; Anthophila; Apoidea; polinizadores.


Introduction

Andinopanurgus Gonzalez and Engel, initially described as a subgenus of Protandrena Cockerell, consists of seven species occurring at mid- and high elevations (1100 – 3400 m) in the Andes from the Venezuela to Peru. Limited information is available on the biology of Andinopanurgus. Scattered observations suggest that species nest in the ground and are polylectic, visiting a wide range of exotic, cultivated and native plants (Gonzalez & Ruz 2007, Gonzalez & Engel 2011, Gonzalez et al. 2013). Some species, such as A. bachue and A. rangeli, are common in both managed and unmanaged gardens in Bogotá, Colombia, thus showing their ability to adapt to urban environments (V.H. Gonzalez, unpublished data). At least one species, A. guarnensis, exhibits buzzing behavior on flowers of cultivated potatoes to release their pollen (Gonzalez et al. 2013).

Gonzalez and Engel (2011) recognized two species groups within Andinopanurgus based on certain male features. In the bachue species group, which contains most of the species, the first antennal flagellomere is distinctly longer than the second flagellomere, the clypeus is maculated with yellow or cream, the fifth sternum bears stout spines midapically, and the seventh tergum is medially emarginate on its distal margin. In the other species group (guarnensis group), which consists of A. guarnensis and A. femoralis, the first antennal flagellomere is about as long as the second, the clypeus is black, the fifth sternum bears normal branched setae midapically, and the distal margin of the seventh tergum is straight, not medially emarginated.

Herein, we describe a new species from Peru that exhibits morphological features of the two species groups previously recognized by Gonzalez and Engel (2011). For example, the male has a yellow clypeus and the first antennal flagellomere is longer than the second, as in the bachue species group. However, the fifth sternum lacks stout spines on its midapical margin and the apical margin of the seventh tergum is straight, as in the guarnensis species group. Thus, the new species bridges the morphological gap between these two species groups. To facilitate the recognition of the new species, we also provide an updated key to all species of the genus.

Material and methods

Morphological terminology follows that of Engel (2001) and Michener (2007). To describe and measure body features, we used an ocular micrometer on an Olympus SZX-12 stereomicroscope. We prepared photomicrographs using a Nikon D1x digital camera attached to an Infinity K-2 long-distance microscopic lens, and assembled series of images at different focal depths with the Zerene Stackertm software package. We used the abbreviations F, S, T, OD, and PW for antennal flagellomere, metasomal sternum and tergum, ocellar diameter and puncture width, respectively. Measurements of the female paratype are in parentheses. The material discussed is in the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Perú (MUSM), and the Snow Entomological Collection, Division of Entomology, University of Kansas Natural History Museum, Lawrence, Kansas, USA (SEMC).

Systematics

Tribe Protandrenini Robertson, 1904

Genus Andinopanurgus Gonzalez and Engel, 2011

Andinopanurgus vargasllosai Gonzalez and Alvarado, n. sp.

(Figs. 1, 2)

Diagnosis. Both sexes of A. vargasllosai (Fig. 1a, 2b, c) are easily separated from all other species of Andinopanurgus by their small body size (4.5–5.1 mm in body length) and T1–T4 with apical margins semi-translucent. It resembles A. femoralis in its small body size and metatibia with scopal setae whitish, but in that Peruvian species the apical margins of T1–T4 are brown, F1 is about as long as F2, and the mesoscutum and mesoscutellum are shiny, weakly imbricate between punctures (Fig. 1f). In A. vargasllosai, F1 is longer than F2 and the mesoscutum and mesoscutellum are duller, finely punctate (Fig. 1e). Furthermore, the male of A. vargasllosai can be recognized by the combination of the following features: clypeus yellow (Fig. 2a), F1 longer than F2, S5 with normal setae on midapical margin, and T7 with apical margin straight.

Description. Holotype. ♀. Total body length 4.84 mm (5.05); forewing length, as measured from apex of humeral sclerite, 3.79 mm (3.58); head width 1.28 mm. Head 1.1× wider than long; inner orbits of compound eyes slightly converging below (Fig. 1a); intertorular distance 2.4× OD, 0.8×length of torulorbital distance; torulus diameter equal to OD; ocellocular distance 2.8× OD, 2.3× greater than ocelloccipital distance; interocellar distance 2.0× OD; compound eye 1.8× longer than wide; clypeus 2.4× broader than long, projecting about 0.3× compound eye width in lateral view; gena 0.8× width of compound eye in profile; supraclypeal area gently convex in profile, slightly more elevated than clypeus; inner subantennal sulcus about 0.7× length of outer subantennal sulcus; facial fovea about 3.7× longer than broad, 0.7× length of scape; scape 3.0× longer than broad, antennal flagellum unmodified, slightly shorter than head width; pedicel 0.6× length of F1, about as long as broad, F1 1.9× longer than broad, about 2.2× longer than F2 and F3 individually, remaining flagellomeres about as long as broad, except last flagellomere longer than broad. Forewing prestigma about twice as long as broad (prestigma width measured to its margin); pterostigma 4.4× longer than broad. Mesosoma about as wide as head width; mesoscutum 1.5× wider than long, 2.4× longer than mesoscutellum, 4.2× longer than metanotum; propodeum with basal part about 0.9× mesoscutellum length in dorsal view; protibial spur with apical portion of rachis long, about as long as malus, with four elongate branches (not including apical portion of rachis); mesotibial spur straight, with coarse branches, 0.8× mesobasitarsus length; metatibial spurs about the same length, curved apically; pretarsal claws with inner ramus slightly shorter than the outer. Lateral fovea of T2 4.0× longer than broad.

Color black, except ventral surfaces of F3–F10 and outer surfaces of pro- and mesotibiae basally with yellow maculations, and apical margins of T1–T5 and S2–S5 semi-translucent (Figs. 1b–d). Tegula semi-translucent brownish; wing membranes brownish, veins and pterostigma dark brown.

Pubescence in general whitish and sparse. Head with long (2.0× OD), semierect, minutely branched setae; scape with long, scattered, minutely-branched setae, about twice as long as maximum scape diameter, pedicel with minutely-branched setae as long as its maximum diameter. Pronotum with short (0.3–0.5× OD), dense, minutelybranched setae along dorsal margin and pronotal lobe posteriorly; mesoscutum, mesoscutellum, and metanotum with sparse, long (1.1× OD), erect, minutely-branched setae arising among short (0.1–0.2× OD), denser (especially on lateral margins), simple setae; mesepisternum and lateral and posterior areas of propodeum with sparse, long (1.0× OD), erect, minutely-branched setae.

Metasomal terga with minute (≤ 0.2× OD), semierect, sparse, simple setae on discs, pre-marginally and laterally with denser, longer, minutely branched setae (~1.0× OD); T5 with setae longer, darker, and denser than on other terga; sterna with denser and longer setae than on terga, particularly on distal sterna.

Outer surface of mandible and basal area of labrum smooth and shiny, impunctate; clypeus with fine and contiguous punctures among, large, scattered setiferous punctures; supraclypeal area with fine and contiguous punctures on distal third, punctures becoming faint basally, thus integument appearing smooth and shiny at low magnifications; subantennal area and remainder of face with fine, contiguous punctures or alveoli, coarser than on clypeus; gena strongly imbricate with faint punctures. Mesoscutum, mesoscutellum, and metanotum with fine, contiguous punctures or aveoli (Fig. 1e); mesepisternum strongly imbricate with large, scattered (2–3× PW), faint setiferous punctures; metepisternum strongly imbricate with few striae near wing base. Propodeum strongly imbricate with fine and weak striae basally, lateral and posterior surfaces with faint, scattered punctures. Metasomal terga and sterna shiny, weakly imbricate with minute, scattered punctures on discs, punctures coarser and denser on apical terga and sterna; distal margins of terga weakly imbricate, impunctate.

♂. As for the female except for yellow integumental markings on clypeus, apices of femora, outer surfaces of tibiae, basitarsi (Figs. 2a–c), and the following: Total body length 4.68 mm; forewing length 3.68 mm; head width 1.50 mm. Head 1.2× wider than long (Fig. 2a); intertorular distance 2.0× OD, about as long as torulorbital distance; torulus diameter 0.8× OD; ocellocular distan-ce 2.1× greater than ocelloccipital distance; interocellar distance 1.5× OD; compound eye 2.3× longer than wide; gena about as wide as compound eye in profile; supraclypeal area, as seen in profile, on the same level with clypeus; facial fovea 5.0× longer than broad, 0.3× length of scape; scape 2.1× longer than broad; F1 1.6× longer than broad, about 1.6× longer than F2 and F3 individually. Pterostigma 3.8× longer than broad. Mesosoma narrower than head width; mesoscutum 1.4× wider than long, 3.6× longer than mesoscutellum, 6.3× longer than metanotum; protibial spur with apical portion of rachis with a row of about 10 elongate branches (not including apical portion of rachis). Lateral fovea of T2 more ovoid and shallower than that of the female, 2.5× longer than broad. T7 with distal margin straight or nearly so; S5 unmodified, without stout spines on midapical margin; S6–S8, and genital capsule as in Figs. 2d–i.

Holotype. ♀, Perú: AP [Apurímac], Mina Las Bambas, Sector Saqrapeña, 14°4’37.24"S, 72°18’33"W, 4265 m, 24.iv–03.v.2017 [24 abr–3 may 2017], L. Figueroa (MUSM).

Paratypes. One female with the same data as the holotype deposited at SEMC, and one male deposited at MUSM with the following label data: CU [Cusco], Espinar, Qbda. Chaisamayo, 14°59’46.15"S, 71°16’25.93W, 4167 m, 16–17.iii.2011 [16–17 mar 2011], Pastizal, M. Alvarado.

Etymology. This species honors the Peruvian writer, politician, journalist, and 2010 Nobel laureate Jorge Mario Pedro Vargas Llosa.

Comments. Andinopanurgus vargasllosai n. sp. occurs in Puna grasslands. Specimens of both sexes were captured in areas where Las Bambas copper mine has restoration programs for the endemic and rarely collected shrub Nototriche armeriifolia A.W. Hill (Malvaceae) (Chanco et al. 2006). Thus, it would be interesting to know if this bee is a potential visitor or pollinator of N. armeriifolia, although some species of Nototriche Turcz. appear to be pollinated by beetles and butterflies (Arroyo et al. 1982, García-Franco & Arroyo 1995).

The new species combines morphological features of the two currently recognized species groups in Andinopanurgus, the bachue and guarnensis groups. Thus, A. vargasllosai n. sp. bridges the morphological gap between these two species groups and it cannot be assigned to either one. The new species might represent an additional species group within Andinopanurgus.

Key to species of Andinopanurgus

Males

1. Clypeus without cream or yellow maculations; F1 short, about as long as F2; face and disc of mesoscutum weakly shiny; S5 without spines on midapical margin, with fringe of normal, minutelybranched setae; T7 with distal margin straight, not medially emarginate .

2

―. Clypeus with cream or yellow maculations; F1 distinctly longer than F2; face and disc of mesoscutum duller; S5 with or without distinctly stout, short spines on midapical margin; T7 with distal margin variable, straight or with V-shaped median emargination.

3

2(1). S7 with apical lobes narrow, parallel-sided, retrorse section of apex comma-shaped; gonostylus slender in profile, slightly tape-ring towards apex, basally strongly protuberant on medial margin in dorsal view (Colombia: Antioquia)

A. guarnensis (Gonzalez & Ruz)

―. S7 with apical lobes not parallel-sided, much broader apically (apex about twice as broad as base), retrorse section of apex not comma-shaped; gonostylus more robust in profile, about same width across its length, basally not protuberant on medial margin in dorsal view (Peru).

A. femoralis (Gonzalez & Engel)

3(1). T1–T4 each with semi-translucent apical margin; S5 without spines on midapical margin, with fringe of normal, minutely-branched setae; T7 with distal margin straight, not medially emarginated (Peru).

A. vargasllosai Gonzalez and Alvarado, n. sp.

―. T1–T4 with apical margins brown to black; S5 with distinctly stout, short spines on midapical margin; T7 with V-shaped median emargination on distal margin (Venezuela to Ecuador).

4

4(3). Antennal flagellum weakly or strongly crenulate on posterior surface; S5 with more than four spines on midapical margin; larger bees (body length 7.9–11.8 mm).

6

―. Antennal flagellum unmodified, not crenulate on posterior surface; S5 with a row of four spines on midapical margin; small bees (body length 5.7–6.8 mm).

5

5(4). Small bees (head width 1.6–1.7 mm; body length 5.7–6.1 mm) (Colombia: Boyacá, Cundinamarca).

A. rangeli (Gonzalez & Ruz)

―. Larger bees (head width 1.8 mm; body length 6.8 mm) (Venezuela).

A. maximina (Gonzalez & Ruz)

6(4). Antennal flagellum strongly crenulate on posterior surface, with deep concavity between flagellomeres; mandible not distinctly broad apically; posterior hypostomal carina unmodified, without a tooth; protibial spur with apex of rachis very short (less than one-third of malus length), with less than five elongate branches (not including apical portion of rachis); S3–S5 with distal margins distinctly convex; S5 with midapical row of spines medially projecting.

7

―. Antennal flagellum weakly crenulate on posterior surface, without deep concavity between flagellomeres; mandible distinctly broad apically; posterior hypostomal carina with strong tooth; protibial spur with apex long, about three-fourths of malus length, with a distinct row of 10 elongate branches (not including apical portion of rachis); S3–S4 with distal margins gently convex; S5 with midapical row of spines straight, not medially projecting (Ecuador: Napo).

A. amyae (Gonzalez & Engel)

7(6). F8 and F9 crenulate; S5 midapical row of spines of unequal sizes, distal two spines distinctly longer (Ecuador: Quito, Napo).

A. wayruronga (Gonzalez & Ruz)

―. F8 and F9 unmodified, not crenulate; S5 with midapical row of spines of about same size, without two distinctly long spines distally (Colombia: Boyacá, Cundinamarca).

A. bachue (Gonzalez & Ruz)

Females

Note that the females of A. amyae and A. wayruronga are unknown. However, given that the male of these species have crenulate antennal flagella they likely should run to A. bachue in the key.

1. Antennal flagellum unmodified, not crenulate.

2

―. Antennal flagellum modified, weakly crenulate on posterior surface of F1–F5 (Colombia: Boyacá, Cundinamarca).

A. bachue (Gonzalez & Ruz)

2(1). F1 about as long as F2; discs of mesoscutum and mesoscutellum shiny, weakly imbricate between punctures.

3

―. F1 distinctly longer than F2; discs of mesoscutum and mesoscutellum dull, finely punctate to strongly imbricate between punctures.

4

3(2). Mesofemur with posterior surface and metafemur with anterior and posterior surfaces distinctly depressed (Peru).

A. femoralis (Gonzalez & Engel)

―. Meso- and metafemora unmodified, not distinctly depressed (Colombia: Antioquia).

A. guarnensis (Gonzalez & Ruz)

4(2). T1–T4 each with semi-translucent apical margin (Figs. 1b–d); metatibia with whitish scopal setae (Peru).

A. vargasllosai Gonzalez and Alvarado, n. sp.

―. T1–T4 with apical margins brown to black; metatibia with dark brown to black scopal setae (Colombia, Venezuela).

5

5(4). Small bees (head width 1.6–1.8 mm; body length 5.6–6.3 mm) (Colombia: Boyacá, Cundinamarca).

A. rangeli (Gonzalez & Ruz)

―. Larger bees (head width 1.9–2.1 mm; body length 7.8 mm) (Venezuela).

A. maximina (Gonzalez & Ruz)

 

 

Acknowledgments:

We are grateful to Amy Comfort and two anonymous reviewers for their comments and suggestions that improved the manuscript. V.H.G. received partial support through a NSF’s REU program (DBI 1560389). This is a contribution of the Division of Entomology, University of Kansas Natural History Museum.

Competing interests:

The authors have declared that no competing interests exist.

Author contributions:

VHG: recognized novelty of the species and wrote the manuscript; MA: collected specimens, prepared photographs, and contributed in the revision and discussion of manuscript; CR: prepared photographs, and contributed in the revision and discussion of manuscript.

Funding:

V.H.G. received partial support through a National Science Foundation (NSF), Research Experiences for Undergraduates (REU) program (DBI 1560389).

Ethics and legal statement:

Material proceeded from museums and no specific permits were required.

Citación:

Gonzalez V.H., M. Alvarado, C. Rasmussen. 2019. A new species of Andinopanurgus (Hymenoptera: Andrenidae) from high elevations in southern Peru. Revista peruana de biología 26(2): 211 - 216 (Julio 2019). doi: http://dx.doi.org/10.15381/rpb.v26i2.15586

 

Literature Cited

Arroyo M.T.K., R. Primack, & J. Armesto. 1982. Community Studies in pollination ecology in the high temperate Andes of Central Chile. I. Pollination mechanisms and altitudinal variation. American Journal of Botany 69(1): 82–97. http://www.jstor.org/stable/2442833        [ Links ]

Chanco M., B. León, & I. Sánchez. 2006. Malvaceae éndemicas del Perú. Revista Peruana de Biología 13(2):413–425. DOI: https://doi.org/10.15381/rpb.v13i2.1877        [ Links ]

Engel M.S. 2001. A monograph of the Baltic amber bees and evolution of the Apoidea (Hymenoptera). Bulletin of the American Museum of Natural History 259: 1–192. URI: http://hdl.handle.net/2246/1437        [ Links ]

García-Franco J.G., & M.T.K. Arroyo. 1995. Breeding System, sex ratio and individual size of the gynodioecious Nototriche compacta (Malvaceae) in the Andes of Central Chile. Plant Species Biolology 10: 147–153. https://doi.org/10.1111/j.1442-1984.1995.tb00134.x        [ Links ]

Gonzalez V.H., & M.S. Engel. 2011. Andinopanurgus, a new Andean subgenus of Protandrena (Hymenoptera, Andrenidae). ZooKeys 126: 57–76. DOI: 10.3897/zookeys.126.1676        [ Links ]

Gonzalez V.H., & L. Ruz. 2007. New enigmatic Andean bee species of Protandrena (Hymenoptera, Andrenidae, Panurginae). Revista Brasileira de Entomologia 51(4): 397–403. http://dx.doi.org/10.1590/S0085-56262007000400001        [ Links ]

Gonzalez V.H., M. Engel, & P.A. Sepúlveda. 2013. Taxonomic and biological notes on Andinopanurgus (Hymenoptera: Andrenidae). Journal of Melittology 3:1–10. https://doi.org/10.17161/jom.v0i3.4437        [ Links ]

Michener C.D. 2007. The Bees of the World [2nd Edition]. Johns Hopkins University Press, Baltimore.         [ Links ]

Robertson C. 1904. Synopsis of Anthophila. Canadian Entomologist 36(2): 37–43. https://doi.org/10.4039/Ent3637-2        [ Links ]

 

 Correspondencia:

*Corresponding author

Victor H. Gonzalez: victorgonzab@gmail.com

Division of Entomology, Natural History Museum, 1501 Crestline Drive – Suite 140, University of -Kansas, Lawrence, Kansas 66045, USA.

Mabel Alvarado: malvaradog@unmsm.edu.pe

Universidad Nacional Mayor de San Marcos, Museo de Historia Natural, Departamento de Entomología. Av. Arenales 1256 Jesús María, Lima 14, Perú.

Claus Rasmussen: claus.rasmussen@bios.au.dk

Department of Bioscience, Aarhus University, Ole Worms Allé 1, DK-8000 Aarhus C, Denmark.

 

Otros datos de los autores / biografía:

ORCID Victor H. Gonzalez: 0000-0002-4146-1634

ORCID Mabel Alvarado: 0000-0001-8135-9223

ORCID Claus Rasmussen: 0000-0003-1529-6548

 

 

Presentado: 18/12/2018

Aceptado: 22/03/2019

Publicado online: 06/07/2019

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