NORTH-WESTERN JOURNAL OF ZOOLOGY 12 (2): 230-238 ©NwjZ, Oradea, Romania, 2016 Article No.: e161202 http://biozoojournals.ro/nwjz/index.html Orchid bees (Hymenoptera, Apidae) from the Brazilian savanna-like ‘Cerrado’: how to adequately survey under low population densities? André NEMÉSIO Instituto de Biologia, Universidade Federal de Uberlândia. Rua Ceará, S/N, Campus Umuarama, Uberlândia, MG. 38400-902. Brazil. E-mail: [email protected] Received: 04. January 2016 / Accepted: 25. May 2016 / Available online: 26. June 2016 / Printed: December 2016 Abstract. Orchid-bee (Hymenoptera: Apidae: Euglossina) faunas from xeric areas have been reported as presenting unusually low abundance, richness and diversity when compared with those from Neotropical forests. Traditional orchid-bee inventories are based on the use of synthetic scents to attract males once or twice a month during a whole year. This protocol presents some potential problems, such as the costs of field sampling, and the uneven distribution of these insects through the year, particularly when areas under strong precipitation seasonality are involved. Recently, a rapid sampling protocol aimed to minimize the afore- mentioned potential problems has been proposed for densely forested areas. It consists of using as many scents as possible during a 20-hour period during the season when orchid bees are most actively foraging. In the present study this rapid sampling protocol was carried out at ‘Estação Ecológica do Panga’, a patch of the savanna-like ‘Cerrado’ in Uberlândia, Central Brazil, where several samplings, using different protocols, have been conducted before, making direct comparison possible. Four hundred and thirty-one specimens belonging to 11 species were sampled. Abundance, richness, and diversity recorded through the rapid sampling protocol were the highest ever recorded for this single area. The rapid sampling protocol, originally designed to be used in forested areas, revealed to be even a stronger tool in xeric environments. Key words: bait scents, Cerrado, euglossine bees, Euglossini, gallery forest, Hexapoda, sampling method. Introduction nators in Neotropical forests, especially due to their ability of flying long distances in short times Bees present their highest diversity in warm, tem- (e.g., Janzen 1971, Dressler 1982, Roubik & Ac- perate, and xeric environments, showing a de- kerman 1987, Roubik & Hanson 2004, Pokorny et crease towards the humid tropics (Michener 1979). al. 2014), a similar role in xeric areas should also Orchid bees (Hymenoptera: Apidae), however, are be expected. Regrettably, there are only a few in- a particular group of Neotropical bees showing ventories and ecological studies of orchid-bee fau- the opposite trend, i.e., they are typical forest in- nas from xeric environments in Eastern Brazil sects reaching the highest diversity in the Amazon (Nemésio & Faria Jr. 2004, Alvarenga et al. 2007, Basin and the Evergreen forests of Central Amer- Freitas 2009, Silveira 2010, Faria & Silveira 2011, ica (Dressler 1982, Roubik & Hanson 2004, Andrade et al. 2012, Justino & Augusto 2012, Vi- Nemésio & Silveira 2007). They are conspicuous otti et al. 2013). In general, fieldwork is somewhat due to their vivid metallic colours and the re- disappointing to researchers, who spent hundreds markable behaviour of the males, which actively of hours in the field to sample only a few bees collect floral fragrances in hundreds of plant spe- (e.g., Faria & Silveira 2011), whereas a similar cies, notably orchids (Vogel 1966, Dressler 1982, sampling effort in forest areas is enough to sample Roubik & Hanson 2004, Perger 2015). Although several hundreds and even thousands of orchid most species are endemic in forested areas (e.g., bees (e.g., Roubik & Ackerman 1987, Oliveira & Morato et al. 1992, Tonhasca Jr. et al. 2002, Campos 1996, Tonhasca Jr. et al. 1992, Nemésio Nemésio & Silveira 2006b, Nemésio 2011c, 2012c, 2013a-d). Nemésio et al. 2016), a few species seem to suc- In order to adequately study diversity and dis- cessfully exploit xeric environments, but abun- tribution of species it is essential to correctly sur- dance and diversity in these xeric areas have been vey them, in such a way the samples reflect spe- usually reported as low or very low (e.g., Al- cies distributions in nature with the highest fidel- varenga et al. 2007, Faria & Silveira 2011, Andrade ity possible. Unfortunately, this is not a simple et al. 2012, Justino & Augusto 2012, Viotti et al. task, since different organisms are sampled under 2013). different protocols, and some of these protocols As orchid bees play an important role as polli- may present inadequate or biased effectiveness. Rapid sampling of orchid bees in Central Brazil 231 This is not different concerning orchid bees. The (Nemésio 2012b, Nemésio & Paula 2013), and Pe- most popular sampling protocol used in ecological ruvian Amazon (Nemésio & Rasmussen 2014). It is studies on orchid bees is based on the intensive not known, however, whether this protocol would use of synthetic scents that mimic the floral fra- be useful in more xeric environments of Eastern grances attractive to orchid-bee males (e.g. Ac- Brazil, such as the Brazilian savanna-like ‘Cer- kerman 1983, 1989, Pearson & Dressler 1985, Pow- rado’, the high altitude ‘Campos Rupestres’ (rocky ell & Powell 1987, Armbruster 1993, Milet- fields), the ‘Caatinga’, and patches of gallery for- Pinheiro & Schlindwein 2005, Nemésio & Silveira ests that happen to occur immersed in the previ- 2006a, b, 2010, Abrahamczyk et al. 2011, Nemésio ous vegetation types. & Vasconcelos 2013). Although highly effective, Thus, the main goal of this study was to com- the sole use of synthetic scents may potentially in- pare the results obtained from samplings carried troduce some artifacts, since some groups of or- out exactly at the same site through different bait- chid bees, such as the species of Euglossa (Eu- ing protocols – the traditional year-round inven- glossella) and some species of Eulaema (Eulaema), tory, with monthly samplings – with the 20-hour are poorly or not attracted to the scents commonly sampling protocol proposed by Nemésio (2010b) used in orchid-bee samplings (e.g., Moure 1996, to assess if the latter protocol can be confidently Nemésio & Silveira 2004, 2006c, Nemésio 2012a). used in more xeric areas where orchid-bee abun- Despite the potential pitfalls, the use of artifi- dance is known to be low. cial scents has gained in popularity and, in fact, most of the current information on orchid bees has been obtained through this protocol (see Nemésio Material and Methods 2012a). Nevertheless, there is a strong lack of standardization among studies, as first noticed by Site description This study was conducted at ‘Estação Ecológica do Panga’ Morato (1998). Particularly, the number of scents (EEP), a protected forest remnant with a total area of and the periodicity of collections greatly vary about 404 ha, belonging to the ‘Universidade Federal de among studies, raising questions on how compa- Uberlândia’, in the municipality of Uberlândia, state of rable results obtained from different protocols can Minas Gerais, South-Eastern Brazil (19°10’S, 48°23’W, 800 be (Morato 1998, Nemésio & Silveira 2007, Sydney m a.s.l.). The region is characterized by a subtropical cli- et al. 2010). mate with two well-defined seasons: a dry winter (May to It has been suggested that surveys of orchid- September) and a rainy summer (October to April). The mean annual temperature and precipitation are 22ºC and bee males with scent baits during a single day 1650 mm, respectively. Soils at the site are primarily red have great utility, and may reveal almost as much latosols that vary from moderately to strongly acidic about local community structure as studies lasting (Embrapa 1982). Most of EEP is covered with ‘Cerrado’ a full year (Roubik, 2004). Recently, Nemésio physiognomies – from which ‘Cerrado’ sensu stricto is the (2010a, b) proposed a 20-hour sampling protocol dominant one –, but forest physiognomies such as gallery which basically consists in actively collecting bees forests are also found, especially along the stream valleys (Ribeiro & Walter 1998, Lopes & Vasconcelos 2008, Car- with insect nets in a given site during 20 hours for doso et al. 2009). For this reason, it has been described as two to four days (consecutive or not) in any period one of the best-preserved ‘Cerrado’ sites in South-Eastern from 7am to 5pm using as many scents as possi- Brazil (Costa & de Araújo 2001, Bruna et al. 2010). ble. This protocol should be preferably used dur- Two sites at EEP were sampled: site-1 (19º10’51”S – ing the rainy summer in the Neotropics, the sea- 48º23’44”W, 800 m a.s.l.), a gallery forest patch entirely son when orchid bees are most actively foraging. surrounded by ‘Cerrado’ sensu stricto situated at the Some of the potential benefits of this method are: southern portion of EEP, and site-2 (19º10’09”S – (i) reducing the costs of fieldworks carried out in 48º23’27”W, 800 m a.s.l.), another patch of gallery forest surrounded by ‘Cerrado’ sensu stricto and pastures at the remote areas; and (ii) avoiding over-killing orchid northern portion of EEP. bees. However, the above protocol was designed taking into consideration the high abundance of Sampling orchid bees usually found in densely forested ar- Samplings were carried out during 20 hours from late eas. It was successfully used in more than twenty November, 2012 to January, 2013 in each site, when or- areas in North-Eastern Brazil (Nemésio 2010b, chid bees are usually most actively foraging in the region. Nemésio & Santos Júnior 2014), southern Bahia At site-1, samplings were carried out from 08:30h to 14:30h on the 29th and 30th of November, 2012, from 9am (Nemésio 2011a, 2013a, c, d), northern Espírito to 2pm on the 4th of December, 2012, and from 9am to Santo (Nemésio 2011b, 2013b), Minas Gerais noon on the 24th of January, 2013.