Sampling a biodiversity hotspot: the orchid-bee fauna (Hymenoptera: Apidae) of Tarapoto, northeastern Peru, the richest and most diverse site of the Neotropics

Nemésio, A; Rasmussen, C

doi:10.1590/1519-6984.20412

A Nemésio ^**e-mail: andre.nemesio@gmail.com

Instituto de Biologia, Universidade Federal de Uberlândia – UFU, Rua Ceará, s/n, Campus Umuarama, CEP 38.400-902, Uberlândia, MG, Brazil

C Rasmussen

Department of Boscience, Aarhus University – AU, Ny Munkegade 114, Bldg. 1540, DK-8000 Aarhus C, Denmark

*e-mail: andre.nemesio@gmail.com

Figures (3)
Tables (4)

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Figure 1.
Map of Peru showing the location of Tarapoto.

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Figure 2.
Clustering of the six areas at Tarapoto region according to their similarity.

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Figure 3.
Clustering of Peruvian areas according to their similarity. a) including our data for Tarapoto. b) including Abrahamczyk et al.'s (2011) data for Tarapoto. c) including our (TP1) and Abrahamczyk et al.'s (2011) (TP2) data for Tarapoto. NA = Nanay, TA1 = Tapiche 1, TA2 = Tapiche 2, MO = Moyobamba, CO = Contamana, PI = Pijuayal, PA = Panguana, CI = Cicra, PM = Puerto Maldonado, TB = Tambopata, IQ = Iquitos, TP = Tarapoto. Data from NA, TA1, TA2, MO, CO, PI, PA, CI, PM, and TP2 extracted from Abrahamczyk et al. (2011)ABRAHAMCZYK, S., GOTTLEUBER, P., MATAUSCHEK, C. and KESSLER, M., 2011. Diversity and community composition of euglossine bee assemblages (Hymenoptera: Apidae) in western Amazonia. Biodiversity and Conservation, vol. 20, no. 13, p. 2981-3001. http://dx.doi.org/10.1007/s10531-011-0105-1.
http://dx.doi.org/10.1007/s10531-011-010... ; TB from Pearson and Dressler (1985)PEARSON, DL. and DRESSLER, RL., 1985. Two-year study of male orchid bee (Hymenoptera: Apidae: Euglossini) attraction to chemical baits in lowland south-eastern Perú. Journal of Tropical Ecology, vol. 1, no. 01, p. 37-54. http://dx.doi.org/10.1017/S0266467400000067.
http://dx.doi.org/10.1017/S0266467400000... ; IQ from Rasmussen (2009)RASMUSSEN, C., 2009. Diversity and abundance of orchid bees (Hymenoptera: Apidae, Euglossini) in a tropical rainforest succession. Neotropical Entomology, vol. 38, no. 1, p. 812-9. http://dx.doi.org/10.1590/S1519-566X2009000100006. PMid:19347098
http://dx.doi.org/10.1590/S1519-566X2009... , TP1 (present study).

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Table 1.
Diversity, evenness, species richness and number of specimens of each orchid-bee species collected at six sampling sites near Tarapoto, Department of San Martín, northeastern Peru, after 20 hours of sampling in each site. See text for location of each site.

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Table 2.
List of orchid-bee species collected in the region of Tarapoto from April, 2002 to April, 2003.

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Table 3.
Number of specimens of each orchid-bee species collected at six sampling sites near Tarapoto, Department of San Martín, northeastern Peru, after 20 hours of sampling in each site, according to scent preference (samples from all six sites pooled). BA = benzyl acetate; TA = p-tolyl acetate; MC = methyl trans-cinnamate; CI = cineole; VA = vanillin; SK = skatole; EU = eugenol; MS = methyl salicylate; FL = flight (attracted to the area but not at any specific scent bait). NES = number of exclusive species. NES-S = number of exclusive species excluding singletons.

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Table 4.
Number of specimens of each orchid-bee species collected at six sampling sites near Tarapoto, Department of San Martín, northeastern Peru, after 20 hours of sampling in each site, according to scent preference (samples from all six sites pooled). BA = benzyl alcohol; BI = β-ionone; CA = r-carvone; CR = p-cresol acetate; DB = dimethoxibenzene; HE = heneicosane; MB = methyl benzoate; FO = on flower (Anthuriumsp.).

Sites (elevation)	Site 1 (400 m)	Site 2 (550 m)	Site 3 (800 m)	Site 4 (900 m)	Site 5 (1000 m)	Site 6 (1000 m)	Total
Species
Aglae caerulea Lepeletier and Serville, 1825	0	1	5	2	2	1	11
Eufriesea chrysopyga (Mocsáry, 1898MOCSÁRY, A., 1898. Species novae generum: Euglossa Latr. et Epicharis Klug. Természetrajzi Füzetek, vol. 21, p. 497-500.)	0	0	0	0	0	1	1
Ef. magrettii (Friese, 1899FRIESE, H., 1899. Monographie der Bienengattung Euglossa Latr. Természetrajzi Füzetek, vol. 22, p. 117-172.)	0	0	0	0	7	8	15
Ef. pulchra (Smith, 1854SMITH, F., 1854. Catalogue of the Hymenopterous insects in the collection of the British Museum. Part II, Apidæ. London: British Museum (Natural History). 267 p.)	0	1	0	0	0	0	1
Euglossa allosticta Moure, 1969MOURE, JS., 1969. The central american species of Euglossa subgenus Glossura Cockerell, 1917 (Hymenoptera, Apidae). Revista de Biologia Tropical, vol. 15, p. 227-247.	0	1	1	6	2	0	10
Eg. amazonica Dressler, 1982dDRESSLER, RL., 1982d. New species of Euglossa IV. The cordata and purpurea species groups. Revista de Biologia Tropical, vol. 30, p. 141-150.	0	3	4	5	17	5	34
Eg. analis Westwood, 1840WESTWOOD, JO., 1840. Entomology [Vol. 6]. Bees, comprehending the uses and economical management of the honey-bee of Britain and other countries, together with descriptions of the known wild species. In JARDINE, W. (Ed.). The naturalist's library. Edinburgh: W.H. Lizars. p. viii+17-301, 30 pls.	0	0	0	1	1	2	4
Eg. augaspis Dressler, 1982cDRESSLER, RL., 1982c. New species of Euglossa. III. The bursigera species group (Hymenoptera: Apidae). Revista de Biologia Tropical, vol. 30, p. 131-140.	1	2	0	4	0	0	7
Eg. bidentata Dressler, 1982bDRESSLER, RL., 1982b. New species of Euglossa. II. (Hymenoptera: Apidae). Revista de Biologia Tropical, vol. 30, p. 121-129.	0	0	0	2	3	2	7
Eg. decorata Smith, 1874SMITH, F., 1874. A revision of the genera Epicharis, Centris, Eulema and Euglossa, belonging to the family Apidae, section Scopulipedes. Annals & Magazine of Natural History, vol. 13, no. 78, p. 440-446. http://dx.doi.org/10.1080/00222937408680899. http://dx.doi.org/10.1080/00222937408680...	3	0	0	0	0	0	3
Eg. despecta Moure, 1968MOURE, JS., 1968. Espécies novas de Euglossa da América Central. Boletim da Universidade Federal do Paraná. Zoologia, vol. 3, p. 13-64.	0	1	3	3	4	0	11
Eg. dressleri Moure, 1968MOURE, JS., 1968. Espécies novas de Euglossa da América Central. Boletim da Universidade Federal do Paraná. Zoologia, vol. 3, p. 13-64.	1	0	0	0	0	0	1
Eg. hemichlora Cockerell, 1917COCKERELL, TDA., 1917. Some euglossine bees. Canadian Entomologist, vol. 49, no. 4, p. 144-146. http://dx.doi.org/10.4039/Ent49144-4. http://dx.doi.org/10.4039/Ent49144-4...	0	1	0	0	0	0	1
Eg. ignita Smith, 1874SMITH, F., 1874. A revision of the genera Epicharis, Centris, Eulema and Euglossa, belonging to the family Apidae, section Scopulipedes. Annals & Magazine of Natural History, vol. 13, no. 78, p. 440-446. http://dx.doi.org/10.1080/00222937408680899. http://dx.doi.org/10.1080/00222937408680...	7	20	1	1	12	0	41
Eg. imperialis Cockerell, 1922COCKERELL, TDA., 1922. Bees in the collection of the United States Museum. Proceedings of the United States National Museum, vol. 60, no. 18, p. 1-20.	0	5	11	26	7	25	74
Eg. intersecta Latreille, 1817LATREILLE, PA., 1817. Euglosse. In North Carolina State University (Ed.). Nouveau dictionnaire d'histoire naturelle, appliquée aux arts, à l'agriculture, à l'économie rurale et domestique, à la médecine, etc. Paris: Déterville. p. 533-535. vol. 10.	3	1	2	1	1	1	9
Eg. ioprosopa Dressler, 1982bDRESSLER, RL., 1982b. New species of Euglossa. II. (Hymenoptera: Apidae). Revista de Biologia Tropical, vol. 30, p. 121-129.	0	2	0	2	10	4	18
Eg. iopyrrha Dressler, 1982bDRESSLER, RL., 1982b. New species of Euglossa. II. (Hymenoptera: Apidae). Revista de Biologia Tropical, vol. 30, p. 121-129.	0	1	1	0	0	2	4
Eg. laurensi Bembé, 2008BEMBÉ, B., 2008. Euglossa laurensi sp. n. – Eine neue Prachtbienenart aus Bolivien (Hymenoptera, Apidae, Euglossini). Mitteilungen der Münchner Entomologischen Gesellschaft, vol. 98, p. 59-65.	0	0	0	0	1	0	1
Eg. maculilabris Moure, 1968MOURE, JS., 1968. Espécies novas de Euglossa da América Central. Boletim da Universidade Federal do Paraná. Zoologia, vol. 3, p. 13-64.	0	0	0	0	2	0	2
Eg. magnipes Dressler, 1982dDRESSLER, RL., 1982d. New species of Euglossa IV. The cordata and purpurea species groups. Revista de Biologia Tropical, vol. 30, p. 141-150.	1	2	2	4	0	0	9
Eg. mixta Friese, 1899FRIESE, H., 1899. Monographie der Bienengattung Euglossa Latr. Természetrajzi Füzetek, vol. 22, p. 117-172.	0	6	0	2	3	7	18
Eg. mourei Dressler, 1982dDRESSLER, RL., 1982d. New species of Euglossa IV. The cordata and purpurea species groups. Revista de Biologia Tropical, vol. 30, p. 141-150.	3	0	4	0	1	0	8
Eg. occidentalis Roubik, 2004bROUBIK, DW., 2004b. Sibling species among Glossura and Glossuropoda in the Amazon region (Hymenoptera: Apidae: Euglossini). Journal of the Kansas Entomological Society, vol. 77, no. 3, p. 235-253. http://dx.doi.org/10.2317/0308.20.1. http://dx.doi.org/10.2317/0308.20.1...	0	1	1	1	0	11	14
Eg. orellana Roubik, 2004bROUBIK, DW., 2004b. Sibling species among Glossura and Glossuropoda in the Amazon region (Hymenoptera: Apidae: Euglossini). Journal of the Kansas Entomological Society, vol. 77, no. 3, p. 235-253. http://dx.doi.org/10.2317/0308.20.1. http://dx.doi.org/10.2317/0308.20.1...	0	11	18	3	14	38	84
Eg. retroviridis Dressler, 1982bDRESSLER, RL., 1982b. New species of Euglossa. II. (Hymenoptera: Apidae). Revista de Biologia Tropical, vol. 30, p. 121-129.	0	0	0	0	1	0	1
Eg. rufipes Rasmussen and Skov, 2006RASMUSSEN, C. and SKOV, C., 2006. Description of a new species of Euglossa (Hymenoptera: Apidae: Euglossini) with notes on comparative biology. Zootaxa, vol. 1210, p. 53-67.	0	0	0	0	2	15	17
Eg. rugilabris Moure, 1969MOURE, JS., 1969. The central american species of Euglossa subgenus Glossura Cockerell, 1917 (Hymenoptera, Apidae). Revista de Biologia Tropical, vol. 15, p. 227-247.	0	2	2	2	0	0	6
Eg. securigera Dressler, 1982dDRESSLER, RL., 1982d. New species of Euglossa IV. The cordata and purpurea species groups. Revista de Biologia Tropical, vol. 30, p. 141-150.	2	0	0	5	5	1	13
Eg. williamsi Hinojosa-Díaz and Engel, 2011bHINOJOSA-DÍAZ, IA. and ENGEL, MS., 2011b. Euglossa williamsi, a new species of orchid bee from the Amazon Basin of Ecuador and Peru, with notes on its taxonomic association and biogeography (Hymenoptera, Apidae). ZooKeys, vol. 159, p. 49-63. http://dx.doi.org/10.3897/zookeys.159.2239. PMid:22303114 http://dx.doi.org/10.3897/zookeys.159.22...	0	0	0	0	0	1	1
Euglossa sp. 1	0	0	0	0	13	11	24
Euglossa sp. 2	0	0	0	0	0	1	1
Eulaema bombiformis (Packard, 1869PACKARD, AS., 1869. List of hymenopterous and lepidopterous insects collected by the Smithsonian expedition to South America, under Prof. James Orton. Annual Report of the Trustees of the Peabody Academy of Science, vol. 1, p. 56-69.)	0	0	1	3	1	1	6
El. marcii Nemésio, 2009NEMÉSIO, A., 2009. Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, vol. 2041, p. 1-242.	4	2	2	1	19	4	32
El. meriana (Olivier, 1789OLIVIER, GA., 1789. Abeille. In: OLIVIER, GA. (Ed.). [Encyclopédie méthodique, ou par ordre de matières; par une société de gens de lettres, de savants et d'artistes] Encyclopédie méthodique, histoire naturelle, insectes. Paris: Panckoucke, Plomteux. p. 46-84.)	3	5	4	2	10	10	34
El. mocsaryi (Friese, 1899FRIESE, H., 1899. Monographie der Bienengattung Euglossa Latr. Természetrajzi Füzetek, vol. 22, p. 117-172.)	0	1	1	0	0	0	2
El. nigrita Lepeletier, 1841	39	7	6	19	16	20	107
El. peruviana (Friese, 1903FRIESE, H., 1903. Nachtrag zur Monographie der Bienengattung Euglossa. Annales Historico-Naturales Musei Nationalis Hungarici, vol. 1, p. 574-575. [Természettudományi Múzeum évkönyve])	1	0	0	0	4	5	10
El. tenuifasciata (Friese, 1925FRIESE, H., 1925. Neue neotropischen Bienenarten, zugleich II. Nachtrag zur Bienenfauna von Costa Rica (Hym.). Stettiner Entomologische Zeitung, vol. 86, p. 1-41.)	0	0	0	0	2	1	3
Exaerete frontalis(Guérin-Méneville, 1844)	0	2	2	0	2	0	6
Ex. smaragdina(Guérin-Méneville, 1844)	7	1	0	0	0	0	8
Total	75	79	71	95	162	177	659
Richness	13	23	19	21	27	24	41
Shannon	1.78	2.62	2.52	2.48	2.89	2.6	3.02
Evenness	0.69	0.83	0.85	0.82	0.88	0.82	0.81

Species
Aglae caerulea
Eufriesea magrettii (Friese, 1899FRIESE, H., 1899. Monographie der Bienengattung Euglossa Latr. Természetrajzi Füzetek, vol. 22, p. 117-172.)
Ef. ornata (Mocsáry, 1896MOCSÁRY, A., 1896. Species Hymenopterorum magnificæ novæ in collectione musæi nationalis Hungarici. Természetrajzi Füzetek, vol. 19, p. 1-8.)
Ef. pulchra
Ef. superba (Hoffmannsegg, 1817HOFFMANNSEGG, JC., 1817. Entomologische Bemerkungen bei Gelegenheit der Abhandlungen über amerikanische Insecten, in der vierten bis sechsten Lieferung von den Recueils d'observations de Zoologie et d'Anatomie comparée, oder dem 2ten Theile der Reise, der Herren Al. v. Humboldt und A. Bonpland, nemlich: No. IX. in Livr. 4. p. 197-283 und No. XI. XII. in Livr. 5. 6. p. 294-397. Zoologisches Magazin, vol. 1, n. 1, p. 8-56.)
Ef. surinamensis (Linnaeus, 17580
Eg. analis
Eg. augaspis
Eg. bidentata
Eg. cognata Moure, 1968MOURE, JS., 1968. Espécies novas de Euglossa da América Central. Boletim da Universidade Federal do Paraná. Zoologia, vol. 3, p. 13-64.
Eg. crassipunctata Moure, 1968MOURE, JS., 1968. Espécies novas de Euglossa da América Central. Boletim da Universidade Federal do Paraná. Zoologia, vol. 3, p. 13-64.
Eg. decorata
Eg. hemichlora
Eg. ignita
Eg. imperialis
Eg. intersecta
Eg. ioprosopa
Eg. magnipes
Eg. mixta
Eg. parvula Dressler, 1982cDRESSLER, RL., 1982c. New species of Euglossa. III. The bursigera species group (Hymenoptera: Apidae). Revista de Biologia Tropical, vol. 30, p. 131-140.
Eulaema bombiformis
El. marcii
El. meriana
El. mocsaryi
El. nigrita
El. peruviana
El. polyzona (Mocsáry, 1897MOCSÁRY, A., 1897. Species septem novæ generis Euglossa Latr. in collectione musaei nationalis Hungarici. Természetrajzi Füzetek, vol. 20, p. 442-446.)
El. tenuifasciata
Exaerete frontalis

Scent	BA	TA	MC	CI	VA	SK	EU	MS	FL	Total
Species
Aglae caerulea	00	00	06	00	00	03	00	00	02	11
Eufriesea chrysopyga	00	00	00	01	00	00	00	00	00	01
Ef. magrettii	00	00	02	04	00	00	00	09	00	15
Ef. pulchra	00	00	00	00	00	00	00	01	00	01
Euglossa allosticta	00	00	00	00	00	09	01	00	00	10
Eg. amazonica	00	00	00	00	00	24	09	00	00	33
Eg. analis	00	00	00	00	00	03	01	00	00	04
Eg. augaspis	00	00	00	00	02	01	00	02	01	06
Eg. bidentata	00	00	00	00	00	07	00	00	00	07
Eg. decorata	00	00	00	00	03	00	00	00	00	03
Eg. despecta	00	00	00	02	00	07	02	00	00	11
Eg. dressleri	00	00	00	00	00	01	00	00	00	01
Eg. hemichlora	00	00	00	00	00	00	00	01	00	01
Eg. ignita	01	02	02	06	01	00	04	21	02	39
Eg. imperialis	00	02	02	62	01	00	00	07	00	74
Eg. intersecta	00	02	01	06	00	00	00	00	00	09
Eg. ioprosopa	00	00	01	01	07	08	00	00	00	17
Eg. iopyrrha	00	00	00	00	00	03	00	01	00	04
Eg. laurensi	00	00	01	00	00	00	00	00	00	01
Eg. maculilabris	00	00	00	00	00	02	00	00	00	02
Eg. magnipes	00	00	00	00	10	00	00	00	00	10
Eg. mixta	00	00	00	00	00	04	00	13	01	18
Eg. mourei	00	00	00	00	07	00	00	00	01	08
Eg. occidentalis	00	00	00	00	10	00	00	02	01	13
Eg. orellana	02	01	03	28	33	00	07	10	01	85
Eg. retroviridis	00	00	01	00	00	00	00	00	00	01
Eg. rufipes	00	01	00	16	00	00	00	00	00	17
Eg. rugilabris	00	00	00	06	00	00	00	00	00	06
Eg. securigera	00	00	02	00	00	02	09	00	01	14
Eg. williamsi	00	00	00	00	00	00	00	01	00	01
Euglossa sp. 1	00	00	22	00	00	00	02	00	00	24
Eulaema bombiformis	00	01	00	00	00	00	00	04	01	06
El. marcii	07	01	02	00	09	00	10	00	03	32
El. meriana	01	01	03	00	06	01	00	15	00	27
El. mocsaryi	00	00	00	00	00	00	00	01	01	02
El. nigrita	00	02	00	22	27	54	00	00	00	105
El. peruviana	01	05	00	00	00	00	00	00	00	06
El. tenuifasciata	00	00	00	00	00	00	00	00	01	01
Exaerete frontalis	00	00	02	02	00	00	01	01	00	06
Ex. smaragdina	00	00	01	01	06	00	00	00	00	08
Total of specimens	12	18	51	157	122	129	46	89	16	639
No. of species	05	10	15	13	13	15	10	15	12	39
NES	00	00	02	02	02	03	00	03	00*
NES-S	00	00	00	01	02	02	00	00	00

Scent	BA	BI	CA	CR	DB	MB	HE	FO	Total
Species
Euglossa amazonica	01	00	00	00	00	00	00	00	01
Eg. augaspis	00	00	00	00	01	00	00	00	01
Eg. ignita	01	00	00	00	00	00	00	01	02
Eg. intersecta	00	01	00	00	00	00	00	00	01
Eg. orellana	00	00	02	01	00	01	01	00	05
Euglossa sp. 2	00	01	00	00	00	00	00	00	01
Eulaema meriana	01	01	00	00	00	00	00	01	03
El. peruviana	01	00	00	00	00	00	00	03	04
El. tenuifasciata	00	00	00	00	00	00	00	02	02
Total	04	03	02	01	01	01	01	07	20
No. of species	04	03	01	01	01	01	01	04	09

[1] *e-mail: andre.nemesio@gmail.com

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Sampling a biodiversity hotspot: the orchid-bee fauna (Hymenoptera: Apidae) of Tarapoto, northeastern Peru, the richest and most diverse site of the Neotropics

Amostrando um ‘hotspot’ de biodiversidade: a fauna de abelhas-das-orquídeas (Hymenoptera: Apidae) de Tarapoto, nordeste do Peru, a área mais rica e diversa da região Neotropical