Additions to the bee Brazilian fauna: first record of Anthrenoides, Callonychium and Psaenythia (Hymenoptera, Apoidea) in the state of Piauí

Abstract

The bee genera Callonychium Brèthes, Psaenythia Gerstaecker and Anthrenoides Ducke are newly recorded in Piauí State, northeastern Brazil. The species reported here are Callonychium brasilience (Ducke, 1907) and Psaenythia variabilis Ducke, 1908, and an as yet unidentified species of Anthrenoides. Images and all known distributional records of these species are also provided. The new occurrences reported herein expand the distribution range of the species to the Caatinga biome.

Key words
Calliopsini; distribution; Protandrenini; solitary bees; South America

INTRODUCTION

Piauí is the third largest State in Northeastern Brazil and exhibits mesic characteristics of relief, climate, vegetation and hydrography. It represents the transition zone among three Brazilian biomes: Caatinga, Cerrado and the Atlantic Forest. The climate is tropical hot and humid in the West and Southwest of the State and semi-arid in most of the East and Southeast (Castro 2007, CEPRO 2010). Caatinga is the predominant biome, representing 28.4% of the territory’s vegetation, followed by the Cerrado that occupies much of the southern portion of the State (Castro 2007, CEPRO 2010). Both biomes are relatively rich in endemic species but, unfortunately, they have suffered environmental degradation mainly due anthropic action leading to drastic changes of most pristine areas (Sampaio & Batista 2004, Aguiar & Monteiro 2005, MMA 2011, 2018). The accelerating losses of natural habitats in the State of Piauí are mainly driven by economic activities of the primary sector, such as agriculture (soybean, corn, cassava, cotton and sugar cane crops) and livestock (goats, cattles, pigs and chickens) (Castro 2007, CEPRO 2010).

Habitat fragmentation and loss of native vegetation may alter climate conditions on a regional scale and affects interactions between pollinators and plants (Hegland et al. 2009). Studies on the Brazilian plant communities show bees as the main pollinators of native and agricultural plant species (Kevan & Imperatriz-Fonseca 2002). Bees constitute the largest group of Aculeata, with more than 20,000 described species (Michener 2007). Despite their great importance for the maintenance of terrestrial ecosystems, the knowledge of the group’s diversity is still poorly documented. The Brazilian territory houses around 1,900 recorded species (Melo et al. 2012, Ascher & Pickering 2020) and an estimated number of 3.000 existing species for the country (Silveira et al. 2002).

The bee diversity of Piauí has remained relatively unstudied compared to that of others States in Northeastern Brazil. Studies regarding the native species are scarce and the known diversity is certainly underestimated. Published studies are basically focused on economic impacts of social bee species in commercial honey production, such as the stingless bees (Meliponini) and the exotic Apis mellifera Linnaeus, 1758 (Apini). To date, only three studies about bee species of Piauí have been published: the flora visited by the eusocial Apini and Meliponini in the Parque Nacional Serra da Capivara (Lorenzon et al. 2003), the bee fauna and the plants visited in Teresina (Lopes et al. 2010) and an inventory of Euglossini diversity in Sete Cidades National Park (Nascimento et al. 2016).

Comprehensiveness information about species diversity and distribution are essential for the conservation management of the local biodiversity and contribute to the sustainable use of environmental resources such as pollination (Pinheiro-Machado et al. 2002). Considering the meager knowledge on native bees of Piauí, the present study reports for the first time the bee genera Callonychium (Calliopsini), Anthrenoides and Psaenythia (Protandrenini) in the State and provides new distributional records for the species C. brasiliense (Ducke, 1907), Anthrenoides sp. and P. variabilis Ducke, 1908. In addition, we summarized information on the geographical distribution of these taxa in Northeastern Brazil in order to improve the knowledge and to encourage further investigations of the largely unexplored fauna of the Piauí State.

MATERIALS AND METHODS

The specimens studied were collected in Corrente and Barreiras do Piauí (Piauí State) and are deposited in the Museu de Zoologia da Universidade de São Paulo, Brazil (MZSP). Both municipalities are located in an area predominantly covered Cerrado in the south of the State, characterized by a semi-humid tropical climate, with two well-defined climatic seasons: a dry period, from May to October, and a rainy period, from November to April (CEPRO 2010, Alvares et al. 2013).

The taxonomic classification follows Melo & Gonçalves (2005) and Moure et al. (2012) in which recognizes all bees in a single family - Apidae. Labels of the specimens were exactly transcribed with apostrophe marks (‘ ’) indicating information of different labels, a backslash (\) indicating a line break. Identification of the Anthrenoides specimen was based on keys for species provided by Urban (2005, 2007, 2008) and the examination of type specimens from Northeastern Brazil described by Urban (2006), deposited in the Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Brazil (DZUP). The identification of the species of Callonychium and Psaenythia was done by comparing the specimens to images of type specimens (see Acknowledgments).

Images were taken with a Leica video camera MC190 HD attached to a Leica M205C stereomicroscope, and the series of images were processed in the software Helicon Focus 6.7.1 to produce confocal images. Illumination system employed the dome and light diffuser created using tracing paper as proposed by Kawada & Buffington (2016). Final figures were edited in commercial software for small adjustments, such as brightness and contrast.

The distribution maps were constructed using the software Quantum GIS (http://www.qgis.org). Distributional records for species were compiled from cited references in the distribution topic. Longitude and latitude coordinates were also compiled from the cited references and by consulting online SpeciesLink (http://www.splink.cria.org.br) when not provided in literature.

RESULTS AND DISCUSSION

Below we provide the first record of the andrenine bee genera Callonychium (Calliopsini), Anthrenoides and Psaenythia (Protandrenini) in Piauí State represented by, respectively, C. brasiliense, Anthrenoides sp. and P. variabilis (Figure 1). These three genera restricted to South America are very speciose, mainly occurring in xeric and temperate areas (Silveira et al. 2002, Michener 2007, Moure et al. 2012, Gonzalez & Engel 2016, Ascher & Pickering 2020).

Figure 1
Geographical distribution in the northeast of Brazil. a. Callonychium brasiliense (Ducke, 1907). b. Anthrenoides species. c. Psaenythia variabilis Ducke, 1908. Northeastern Brazilian States: Alagoas (AL), Bahia (BA), Ceará (CE), Maranhão (MA), Pernambuco (PE), Paraíba (PB), Piauí (PI), Rio Grande do Norte (RN), and Sergipe (SE). Pink stars: new records. Yellow circles: known records from literature. Gray area = Caatinga biome.

Callonychium comprises rather small (3-7 mm long), largely yellow-and-black species, mainly recognized by yellow spots on the genal area, antennal sockets usually at the lower fourth of the face, lateral parts of the clypeus strongly bent posteriorly, and sterna of males considerably modified with ridges and projections (Michener 2007). Thirteen species have been recognized in the genus with only two species reported in Brazil (Moure et al. 2012, Gonzalez & Engel 2016, Ascher & Pickering 2020). In the Brazilian Northeast, there is only one record of C. brasiliense (Figure 2), although undescribed species are also known for this region (Silveira et al. 2002, K.S.R. pers. obs.).

Figure 2
Female of Callonychium brasiliense (Ducke, 1907) from Barreiras do Piauí, Piauí, Brazil. a. Head in frontal view. b. habitus. Scale bars = 0.5 mm.

The genus Anthrenoides (Figure 3) includes 63 described species, most of which are registered in Brazil (53) especially in the Southeast and South regions of the country (Moure et al. 2012, Ascher & Pickering 2020). It is a very morphologically heterogeneous group with relatively small sized species (length 5-7 mm) that lack large yellow areas on the body (Michener 2007, Silveira et al. 2002). In this way, a generic revision of Anthrenoides became increasingly important to solve the current uncertainties in the delimitation of species based on adult morphology. Five Anthrenoides species are known to occur in Northeastern Brazil: A. caatingae Urban, 2006, A. deborae Urban, 2006, A. cearensis Urban, 2006, A. nordestinus Urban, 2006 and A. petrolinensis Urban, 2006 (Moure et al. 2012, Ascher & Pickering 2020). Species identification of the Anthrenoides specimen herein reported was not possible because a few characteristics disagree with those of other known species.

Figure 3
Male of Anthrenoides sp. from Corrente, Piauí, Brazil. a. Head in frontal view. b. habitus. Scale bars = 0.5 mm.

Psaenythia are relatively moderate-sized species (7-14 mm long), almost always exhibiting yellow markings and is the only Protandrenini group with a longitudinal ridge on the posterior side of the hind femur which bears a depressed glabrous area below (Michener 2007). There are more than seventy described species in the genus, 17 of which registered in Brazil mainly in the South and Southeast regions of the country (Silveira et al. 2002, Moure et al. 2012, Ascher & Pickering 2020). The only recorded species in the Northeast of Brazil is P. variabilis (Figure 4) (Moure et al. 2012).

Figure 4
Psaenythia variabilis Ducke, 1908 from Corrente, Piauí, Brazil. a. Female head in frontal view. b. female in lateral view. c. male head in frontal view. d. male in dorsal view. Scale bars: a and c = 0.5 mm, b and d = 1 mm.

In this work we expand the distribution range of these species by hundreds of kilometers from previous known records. This new distributional data correspond to the southwest most known occurrence of these genera in the Caatinga. All localities in Piauí State where the specimens were collected are in the semiarid region, marked by transitional areas between Cerrado and Caatinga biomes, with the predominance of species typical of the Cerrado (CEPRO 2010). However, the bee species in question seems to be primarily associated with the Caatinga biome as observed by the others known distribution records (Figure 1).

Calliopsini

Robertson, 1922

Callonychium (Callonychium) brasiliense (Ducke, 1907)

Label data of new records. Brazil, Piauí: 1 female ‘Brasil, Piauí, 15km SE de\ Barreiras do Piauí, 515m,\ 05-06.i.2012, 09°59’06”S\ 45°21’08W K. Ramos &\ V. Kanamura col. (MZSP)’ ‘Callonychium brasiliense\ (Ducke, 1907)\ K. Ramos det. 2020’; 1 female ‘Brasil: Piauí, Corrente,\ Bairro de Nova Corrente\ Área entorno do Rio Corrente,\ -10.431765°S, -45.184844°W\ 10.v.2019, Malaise, 427m\ B. Castro & H. Onody cols.’ ‘Callonychium brasiliense\ (Ducke, 1907)\ K. Ramos det. 2020’; 5 females, same data except ‘08.viii.2019’; 2 females ‘Brasil: Piauí, Corrente\ Campus UESPI, 04.vi.2019\ -10.4485°S -45.1511°W\ S. Costa & H. Onody cols\ pan trap yellow’ ‘Callonychium brasiliense\ (Ducke, 1907)\ K. Ramos det. 2020’; 1 female, same data except ‘pan trap blue’.

Distribution. Alagoas (Moura 2008), Ceará (Ducke 1910a, b), Maranhão (Ducke 1907, 1910b, Gostinski et al. 2016), Paraíba (Aguiar & Martins 1997, Aguiar & Martins 2003, Zanella & Martins 2005, Moura et al. 2018), Piauí (present study), Pernambuco (Schlindwein 2003), Rio Grande do Norte (Zanella 2003), Sergipe (Moura 2003, 2008) (Figure 1a).

Protandrenini

Robertson, 1904

Anthrenoides sp.

Label data of new records

Brazil Piauí: 1 male ‘Brasil, Piauí, Corrente\ Campus UESPI\ 04-08.iv.2019, Varredura\ Onody, H.C. col.’ ‘Anthrenoides sp.\ K. Ramos det. 2020’.

Distribution

Alagoas (Moura 2003, 2008), Bahia (Urban 2006), Ceará (Urban 2006), Paraíba (Moura et al. 2018), Piauí (present study), Pernambuco (Urban 2006), Sergipe (Moura 2008) (Figure 1b).

Psaenythia variabilis

Ducke, 1908

Label data of new records

Brazil Piauí: 1 female and 1 male ‘Brasil, Piauí, Corrente\ Campus UESPI\ 04-08.iv.2019, Varredura\ Onody, H.C. col.’ ‘Psaenythia variabilis \ (Ducke, 1908)\ K. Ramos det. 2020’.

Distribution

Alagoas (Moura 2003, 2008), Bahia (Santos et al. 2013), Ceará (Ducke 1908, 1910a, b), Paraíba (Cockerell 1912, Aguiar & Martins 1997, Schlindwein 2003, Zanella & Martins 2005, Schlindwein & Medeiros 2006, Oliveira & Santos 2016, Moura et al. 2018), Piauí (present study), Pernambuco (Schlindwein 2003, Locatelli et al. 2004), Rio Grande do Norte (Zanella 2003), Sergipe (Moura 2008) (Figure 1c).

ACKNOWLEDGMENTS

We are very grateful to Gabriel Melo (DZUP) for helping with the bee identifications and to Beatriz Coelho and Orlando Silveira (Museu Paraense Emilio Goeldi, Belém, PA, Brazil) for providing the images of the lectotype female of Psaenythia variabilis. This work was supported by a joint grant to CRFB (Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq; Process, 440574/2015-3 and Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP; Process 2016/50378-8 and 2017/07366-1). This study was also financed in part by the Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides (FAPESP Process 2008/57949-4 and 2014/50940-2, and CNPq Process 465562/2014-0). KSR also thanks PROTAX-CNPq (Process 152579/2016-8) and Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (Finance Code 001) for post-doctoral grants.

REFERENCES

• AGUIAR CML & MARTINS CF. 1997. Abundância relativa, diversidade e fenologia de abelhas (Hymenoptera, Apoidea) na caatinga, São João do Cariri, Paraíba, Brasil. Iheringia, Sér Zool 83: 151-163.
• AGUIAR CML & MARTINS CF. 2003. The bee diversity of the Tabuleiro vegetation in the Guaribas Biological Reserve (Mamanguape, Paraíba, Brazil). In: Melo GAR & Alves-dos-Santos I (Eds), Apoidea Neotropica: homenagem aos 90 anos de Jesus Santiago Moure. Criciúma, UNESC, p. 209-216.
• AGUIAR TJA & MONTEIRO MSL. 2005. Modelo agrícola e desenvolvimento sustentável: a ocupação do cerrado piauiense. Ambiente & Sociedade 8: 1-18.
• ALVARES CA, STAPE JL, SENTELHAS PC, DE MORAES G, LEONARDO J & SPAROVEK G. 2013. Köppen’s climate classification map for Brazil. Meteorol Z 22: 711-728.
• ASCHER JS & PICKERING J. 2020 Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). Available at: http://www.discoverlife.org/mp/20q?guide=Apoidea_species Access in 25/05/ 2020.
  » http://www.discoverlife.org/mp/20q?guide=Apoidea_species
• CASTRO AAJF. 2007. Unidades de Planejamento: Uma Proposta Para o Estado do Piauí com Base na Dimensão Diversidade de Ecossistemas. Publ Avulsas Conserv Ecos 18: 1-28.
• CEPRO. 2010. Piauí em Números, 8a Ed. Fundação CEPRO, 981 p.
• COCKERELL TDA. 1912. New bees from Brazil. Psyche 19: 41-61.
• DUCKE A. 1907. Contribucion a la connaissance de la faune hyménoptérologique du Nord-Est du Brésil. Rev Entomol 26: 73-96.
• DUCKE A. 1908. Contribucion a la connaissance de la faune hyménoptérologique du Nord-Est du Brésil. Rev Entomol 27: 57-87.
• DUCKE A. 1910a. Contribution a la connaissance de la faune hyménoptérologique du Nord-Est du Brésil. Rev Entomol 28: 78-96.
• DUCKE A. 1910b. Explorações botânicas e entomológicas no Estado do Ceará. Rev Trim Inst Ceará 24: 3-61.
• GONZALEZ VH & ENGEL MS. 2016. A new species of Callonychium Brèthes from Argentina (Hymenoptera: Andrenidae). Evraziat Entomol Z 1: 31-34.
• GOSTINSKI LF, CARVALHO GCA, RÊGO MMC & ALBUQUERQUE PMC. 2016. Species richness and activity pattern of bees (Hymenoptera, Apidae) in the restinga area of Lençóis Maranhenses National Park, Barreirinhas, Maranhão, Brazil. Rev Bras Entomol 60: 319-327.
• HEGLAND SJ, NIELSEN A, LÁZARO A, BJERKNES AL & TOTLAND Ø. 2009. How does climate warming affect plant-pollinator interactions? Ecol Lett 12: 184-195.
• KAWADA R & BUFFINGTON ML. 2016. A scalable and modular dome illumination system for scientific microphotography on a budget. PLoS ONE: e0153426.
• KEVAN P & IMPERATRIZ-FONSECA VL. 2002. Pollinating bees: the conservation link between Agriculture and Nature. Brasília, DF: Ministry of Environment, 313 p.
• LOCATELLI E, MACHADO ICS & MEDEIROS P. 2004. Riqueza de abelhas e a flora apícola em um fragmento da mata serrana (Brejo de Altitude) em Pernambuco, Nordeste do Brasil. In: Pôrto KC et al. (Orgs). Brejos de altitude em Pernambuco e Paraíba História Natural, Ecologia e Conservação. Ministério do Meio Ambiente. Brasília, DF, p. 153-177.
• LOPES MTR, REIS AS, SOUZA BA, PEREIRA FM, OLIVEIRA FF, NEVES LSML, PEREIRA LA, ROCHA FSB & VIEIRA NETO JM. 2010. Levantamento da fauna e plantas apícolas na Embrapa Meio-Norte, em Teresina, PI. Embrapa. Bol Pesq Desenv 91: 1-34.
• LORENZON MCA, MATRANGOLO CAR & SCHROEREDER JH. 2003. Flora visitada pelas abelhas eussociais (Hymenoptera, Apidae) na Serra da Capivara, em Caatinga do Sul do Piauí. Neotrop Entomol 32: 27-35.
• MELO GAR, AGUIAR AP & GARCETE-BARRETT BR. 2012. Hymenoptera, In: Rafael JA (Ed). Insetos do Brasil: Diversidade e Taxonomia. Ribeirão Preto, Holos, p. 553-612.
• MELO GAR & GONÇALVES RB. 2005. Higher-level bee classifications (Hymenoptera, Apoidea, Apidae sensu lato). Rev Bras Zool 22: 153-159.
• MICHENER CD. 2007. The Bees of the World, 2a Ed. John Hopkins University Press, Baltimore, 953 p.
• MMA - MINISTÉRIO DO MEIO AMBIENTE. 2011. Subsídios para a elaboração do plano de ação para a prevenção e controle do desmatamento da caatinga. MMA, Brasília, 128 p.
• MMA - MINISTÉRIO DO MEIO AMBIENTE. 2018. Desmatamento no Cerrado em 2018. Disponível em: https://www.mma.gov.br/informma/item/15309-desmatamento-no-bioma-cerrado-em-2018.html Acessado em: 30/03/2020.
  » https://www.mma.gov.br/informma/item/15309-desmatamento-no-bioma-cerrado-em-2018.html
• MOURA DC. 2003. Riqueza e abundância de abelhas em diferentes estágios de degradação da Caatinga como indicadores ambientais no entorno da Usina Hidrelétrica de Xingó. Dissertação de Mestrado. Universidade Federal de Pernambuco, Recife, 98 p. (Unpublished).
• MOURA DC. 2008. Interações entre plantas e abelhas nas matas ciliares do Rio São Francisco. Tese de Doutorado. Universidade Federal de Pernambuco, Recife, 156 p.
• MOURA DC, PEREIRA TMS, FARIAS GC & LEITE JEM. 2018. Abelhas e espécies melitófilas da mata ciliar do riacho Salgadeira, município de Alcantil, Paraíba. Revista Verde de Agroecologia e Desenvolvimento Sustentável 13: 392-398.
• MOURE JS, URBAN D & MELO GAR. 2012. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region – Online Version. Available at: http://www.moure.cria.org.br/catalogue Access in: 30/03/2020.
  » http://www.moure.cria.org.br/catalogue
• NASCIMENTO GS, SANTOS KPP, FONTENELE WM, BARROS RFM, SOUSA DC, LIMA RA & SILVA PRR. 2016. Atração de Machos de Abelhas da Tribo Euglossini (Hymenoptera, Apoidea) por Compostos Aromáticos Sintéticos no Parque Nacional de Sete Cidades, Piauí, Brasil. Rev Espacios 37: 1-9.
• OLIVEIRA GS & SANTOS CAG. 2016. Visitantes florais de Turnera subulatas m. (Passifloraceae) no município de Cuité, Paraíba. Educação Ciência e Saúde 3: 37-46.
• PINHEIRO-MACHADO C, ALVES DOS SANTOS I, IMPERATRIZ-FONSECA VL, KLEINERT AMP & SILVEIRA FA. 2002. Brazilian Bee Surveys: State of Knowledge, Conservation and Sustainable Use. In: Kevan P & Imperatriz Fonseca VL (Eds). Pollinating Bees – The Conservation Link Between Agriculture and Nature. Ministério do Meio Ambiente. Brasília.
• SAMPAIO Y & BATISTA JEM. 2004. Desenvolvimento regional e pressões antrópicas no bioma Caatinga. In: Sampaio Y & Batista JEM (Eds), Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação. Ministério do Meio Ambiente, Brasília, p. 311-324.
• SANTOS GMM, CARVALHO CA, AGUIAR CML, MACÊDO LSSR & MELLO MAR. 2013. Overlap in trophic and temporal niches in the flower-visiting bee guild (Hymenoptera, Apoidea) of a tropical dry forest. Apidologie 44: 64-74.
• SCHLINDWEIN C. 2003. Panurginae (Hymenoptera, Andrenidae) in Northeastern Brazil. In: Melo GAR & Alves dos Santos I. (Eds). Apoidea Neotropica: Homenagem aos 90 Anos de Jesus Santiago Moure. Criciúma: UNESC, p. 217-222.
• SCHLINDWEIN C & MEDEIROS PCR. 2006. Pollination in Turnera subulata (Turneraceae): Unilateral reproductive dependence of the narrowly oligolectic bee Protomeliturga turnerae (Hymenoptera, Andrenidae). Flora 201: 178-188.
• SILVEIRA FA, MELO GAR & ALMEIDA EAB. 2002. Abelhas Brasileiras: Sistemática e Identificação. Editado por F.A. Silveira, Belo Horizonte, 253 p.
• URBAN D. 2005. Espécies novas de Anthrenoides Ducke (Hymenoptera, Andrenidae) do Brasil. Rev Bras Entomol 49: 36-62.
• URBAN D. 2006. Espécies novas de Anthrenoides Ducke (Hymenoptera, Andrenidae) do nordeste do Brasil. Acta Biol Paraná 34: 73-87.
• URBAN D. 2007. Espécies novas de Anthrenoides Ducke (Hymenoptera, Andreninae) do Sudeste do Brasil. Rev Bras Entomol 51: 23-34.
• URBAN D. 2008. Espécies novas de Anthrenoides Ducke (Hymenoptera, Apidae, Andreninae) do Rio Grande do Sul e notas descritivas. Rev Bras Entomol 52: 575-587.
• ZANELLA FCV. 2003. Abelhas da Estação Ecológica do Seridó (Serra Negra do Norte, RN): aportes ao conhecimento da diversidade, abundância e distribuição espacial das espécies na caatinga. In: Melo GAR & Alves-dos-Santos I (Eds.) Apoidea Neotropica: homenagem aos 90 anos de Jesus Santiago Moure. Criciúma: UNESC, p. 231-240.
• ZANELLA FCV & MARTINS CF. 2005. Abelhas (Hymenoptera, Apoidea, Apiformes) da área do Curimataú, Paraíba. In: Araújo FS et al. (Org). Análise das variações da biodiversidade do bioma Caatinga: suporte a estratégias regionais de conservação. Brasília, DF: Ministério do Meio Ambiente, p. 379-371.

Publication Dates

• Publication in this collection
  10 May 2021
• Date of issue
  2021

History

• Received
  24 Apr 2020
• Accepted
  29 June 2020