G Model RBE 117 1–9 ARTICLE IN PRESS Revista Brasileira de Entomologia xxx (2016) xxx–xxx 1 REVISTA BRASILEIRA DE 2 Entomologia A Journal on Insect Diversity and Evolution www.rbentomologia.com Biology, Ecology and Diversity 3 Species richness and activity pattern of bees (Hymenoptera, Apidae) 4 in the restinga area of Lenc¸ óis Maranhenses National Park, 5 Barreirinhas, Maranhão, Brazil a b c 6 Q1 Luana Fontoura Gostinski , Gracy Chrisley Alencar Carvalho , Márcia Maria Correa Rêgo , a,c,∗ 7 Patrícia Maia Correia de Albuquerque a 8 Universidade Federal do Maranhão, Programa de Pós-Graduac¸ ão em Rede de Biodiversidade e Biotecnologia da Amazônia Legal, São Luís, MA, Brazil b 9 Universidade Federal do Maranhão, Programa de Pós-Graduac¸ ão em Biodiversidade e Conservac¸ ão, São Luís, MA, Brazil c 10 Universidade Federal do Maranhão, Departamento de Biologia, Laboratório de Estudos sobre Abelhas, São Luís, MA, Brazil 11 a b s t r a c t 12 a r t i c l e i n f o 13 14 Article history: The Apidae community structure was studied in a vegetated area of coastal dunes in Lenc¸ óis Maran- 15 Received 14 April 2016 henses National Park. Collections were performed monthly from August 2009 to July 2010. The collection 16 Accepted 26 August 2016 methods included the use of entomological nets on flowers and Moerike traps. In total, 1211 individuals 17 Available online xxx belonging to 59 species were collected. The pattern of abundance and richness was similar to those found 18 Associate Editor: Maria Cristina Gaglianone in Maranhão and other coastal areas of northeastern Brazil. The bees were present throughout the year, 19 with an increase in the number of individuals during the rainy season. Constant and dominant species 20 Keywords: included Trigona sp. gr. fulviventris, Apis mellifera, Plebeia alvarengai, Centris aenea, Xylocopa cearensis, and 21 Annual activity Centris caxiensis. 22 Apoidea © 2016 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open 23 Bee diversity access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 24 Coastal region 25 Neotropical 26 Introduction Sakagami et al. (1967) proposed the standardization of samp- 44 ling, with the collection of bees on flowers using entomological 45 27 The exuberance and uniqueness of the landscape of Lenc¸ óis nets, thus providing data on local diversity, relative abundance, 46 28 Maranhenses National Park (Parque Nacional dos Lenc¸ óis Maran- habitat preference, and associated plants. This method allows com- 47 29 henses – PNLM), represented by dune fields surrounded by lakes, parisons among various ecosystems, enabling easier to compare 48 30 beaches, mangroves, and restingas (sandy coastal plains) and the patterns in the structure of bee communities in the Neotropical 49 31 high level of local biodiversity justified the creation of the Protected region (Aguiar and Zanella, 2005). Other methods of collecting bees 50 32 Area of PNLM in 1981 (Silva and Silva Filho, 2008). To improve are scent baiting, which is typically aimed at attracting Euglossini 51 33 the understanding of this ecosystem, species inventories have been males (Nemésio and Silveira, 2007), the use of trap nests (Gazola 52 34 performed at PNLM. Among the bees, several species of Centris and and Garófalo, 2009), and more recently, sampling with coloured 53 35 Euglossa were recorded using trap nests (Ramos et al., 2006). A more trays and bowls (Gonc¸ alves and Oliveira, 2013). Without the use 54 36 complete list of 14 of species of orchid bees (Euglossa, Eulaema, of complementary methods, 20% or 8% of the bee species would 55 37 and Eufriesea) was obtained by baiting with aromatic fragrances not have been recorded in recent inventories in Santa Catarina in 56 38 (Silva et al., 2009). In a case study of murici pollinators (Byrsonima southern Brazil (Krug and Alves-dos-Santos, 2008; Kamke et al., 57 39 crassifolia (L.) Rich, Malpighiaceae), 21 species of Centridini were 2011, respectively). 58 40 identified (Rêgo et al., 2006). Although these studies yielded first As reported by Viana and Kleinert (2005), despite the variety 59 41 assessments of some species rich bee taxa, the knowledge regarding of methods, little is known regarding the bee fauna of the coastal 60 42 the bee species remained fragmentary because of the selectivity of ecosystems of Brazil. Most surveys of bees in restinga areas have 61 43 the sampling methods used. focussed on the southern region of the country, including studies 62 in Paraná (Laroca, 1974; Zanella, 1991; Schwartz-Filho and Laroca, 63 1999), Santa Catarina (Mouga, 2004; Kamke et al., 2011), and Rio 64 Grande do Sul (Alves-dos-Santos, 1999). Among the studies con- 65 ∗ ducted in the northeastern region, we can cite Viana and Kleinert 66 Corresponding author. E-mail: [email protected] (P.M. Albuquerque). (2005), Silva et al. (2015) and Moreira et al. (2016) in Bahia and 67 http://dx.doi.org/10.1016/j.rbe.2016.08.004 0085-5626/© 2016 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Gostinski, L.F., et al. Species richness and activity pattern of bees (Hymenoptera, Api- dae) in the restinga area of Lenc¸ óis Maranhenses National Park, Barreirinhas, Maranhão, Brazil. Rev. Brasil. Entomol. (2016). http://dx.doi.org/10.1016/j.rbe.2016.08.004 G Model RBE 117 1–9 ARTICLE IN PRESS 2 L.F. Gostinski et al. / Revista Brasileira de Entomologia xxx (2016) xxx–xxx 68 Madeira-da-Silva and Martins (2003) in Paraíba. Gottsberger et al. Temperature and air humidity data were obtained from the 128 69 (1988) studied pollinating bees in the dune vegetation on São Luís Geoenvironmental Centre of Maranhão State University, using the 129 70 Island (northern Brazil) and found that nine out of the 10 plant Urbano Santos station located approximately 85 km from the col- 130 71 species studied were melittophilous, and in spite of the adverse lection site. The Weather Forecasts and Climate Studies Centre in 131 72 conditions and the strong wind, 18 bee species were reported as the Northeast Region (CPTEC, 2010) provided rainfall data. 132 73 flower visitors. In addition, the studies of Albuquerque (1998) and 74 Oliveira et al. (2010) were conducted at the same location and 75 resulted in inventories of 36 and 31 bee species, respectively. Data analysis 133 76 The present study aims to evaluate, using different sampling 77 methods, the species richness, and diversity of bees in PNLM to The Shannon–Wiener index was applied to calculate the species 134 78 describe their activity pattern, and to compare the similarities with diversity, and Pielou’s index was used to calculate the area 135 79 other coastal environments of northeastern Brazil. equitability. The calculations were performed using PAST (Paleon- 136 tological Statistics 2.00) (Hammer et al., 2001). 137 For each species sampled by netting, the dominance (D) and 138 80 Material and methods constancy (C) were calculated according to Bodenheimer (1955). 139 For dominance, D = (abundance of species i/total abundance) × 100. 140 81 Study area If D > 5%, then the species was considered dominant (D); if 141 2.5% < D < 5%, then the species was considered accessory (A); and 142 82 This study was conducted in a restinga area measuring 200 ha if D < 2.4%, then the species was considered occasional (OC). 143 83 located at the edge of PNLM in the municipality of Barreirin- ◦ ◦ Constancy is the percentage of individuals present, calculated 144 84 has (2 43 22.5 S–42 49 50 W), Maranhão, Brazil. According to the as C = P × 100/N, where P is the number of samples containing the 145 85 Köppen (1948) classification, the regional climate is the Aw type, species, and N is the total number of samples. The bees collected in 146 86 which is a tropical climate with high temperatures and two well- 12 h of netting per month were considered one sample. If C > 50%, 147 87 defined seasons, dry (July–December) and rainy (January–June), then the species was considered constant (W); if 25% < C < 50%, 148 88 with approximately 1800 mm of rainfall (Maranhão, 2002). then the species was considered accessory (Y); and if C < 25%, then 149 2 2 89 The PNLM vegetation covers an area of 453.28 km , 405.16 km the species was considered accidental (Z) (Silveira-Neto et al., 150 90 (89%) of which are classified as restinga. There are also mangroves, 1976). 151 91 riparian forests, and cerrados that cover a small portion of the The Morisita index was applied to analyse the similarity with 152 92 total area (Ibama, 2003). According to studies conducted through bee communities equivalent to the restinga of PNLM, such as the 153 93 the PNLM Management Plan (Ibama, 2003), the restinga of this restinga of Cabedelo, Paraíba (Madeira-da-Silva and Martins, 2003), 154 94 region is composed of melittophilous plants that belong to the Abaeté dunes and Salvador, Bahia (Viana and Kleinert, 2005; Silva 155 95 families Lythraceae, Malpighiaceae, Turneraceae, Asteraceae, and et al., 2015), Panaquatira beach (São José de Ribamar), Maranhão 156 96 Ochnaceae. (Oliveira et al., 2010), and São Marcos beach (São Luís), Maran- 157 hão (Albuquerque, 1998), using PAST. The Morisita index was only 158 97 Sampling applied to the bee species collected with nets, the primary col- 159 lecting method used in those studies. 160 161 98 The collections were performed by two collectors at an interval To determine the representativeness of the community sam- 162 99 of 25–30 days over 12 months (August 2009–July 2010) on two pled with both methods, a species accumulation curve (collector 163 100 consecutive days: from 12:00 to 18:00 h on the first day and from curve) as well as richness estimators Chao 1 and Jackknife 1 were 164 101 6:00 to 12:00 h on the second day, for a total of 288 h of sampling.