The bee diversity of the Tabuleiro vegetation in the Guaribas Biological Reserve (Mamanguape, Paraíba, Brazil) 1
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1 The bees of the Tabuleiro vegetation In G. A. R. Melo & I. Alves-dos-Santos, Apoidea Neotropica: Homenagem aos 0 Anos de Jesus Santiago Moure. Editora UNESC, Criciúma, The bee diversity of the Tabuleiro vegetation in the Guaribas Biological Reserve (Mamanguape, Paraíba, Brazil) Antonio José Camillo de Aguiar Celso Feitosa Martins ABSTRACT. We conducted a study of the bee community of the Tabuleiro vegetation in the Guaribas Biological Reserve located in the northeast Paraíba state (NE, Brazil). Bees were collected once a month, during a one-year period, by using an entomological net on flowers, to study the composition and richness of bee species. A total of 0 specimens, belonging to species of bees were collected. The tribes Meliponini and Centridini presented the greatest abundance and species richness. Comparing the bee fauna with other community studies, using similar methodologies, it was observed, in terms of diversity, more similarity with communities from the open areas of the cerrado in Central Brazil, mainly due to the contribution of the tribes Centridini and Tapinotaspidini. In addition, the tribe Meliponini showed species richness and abundance more similar to areas of the Atlantic Rainforest of southeastern Brazil. The common characteristics between the bee community of Guaribas Biological Reserve and other bee communities of open formations and closed forest formations probably occurred because the Reserve represents an area of ecological tension between these vegetation types. RESUMO. Foi conduzido um estudo da comunidade de abelhas da vegetação de Tabuleiro na Reserva Biológica Guaribas, localizada no nordeste do Estado da Paraíba (NE, Brasil). As abelhas foram coletadas uma vez por mês, durante o período de um ano, com o emprego de rede entomológica quando em visita a flores, para se estudar a composição e riqueza da fauna. Foi coletado um total de 0 indivíduos, pertencentes a espécies. As tribos Meliponini e Centridini apresentaram a maior abundância e riqueza de espécies. Comparações com faunas de outras comunidades, estudadas com metodologia semelhante, revelaram uma maior similaridade, em termos de diversidade, com áreas de vegetação aberta dos cerrados do Brasil Central, principalmente pelas contribuições das tribos Centridini e Tapinotaspidini. Além disso, a tribo Meliponini apresentou uma riqueza de espécies e abundância mais semelhantes a áreas de floresta Atlântica do sudeste brasileiro. As semelhanças entre a comunidade de abelhas da Reserva Biológica Guaribas e as comunidades de formações abertas e formações florestais fechadas provavelmente ocorreram pela Reserva representar uma área de tensão ecológica entre estes tipos vegetacionais. KEYWORDS. Bees; Apidae; Tabuleiro; Paraiba; Brazil. INTRODUCTION Surveys of bee communities provide information such as composition and structure, associated flora, interactions among species for resource use, as well as allow the evaluation of the relationship between local and regional diversities (HEITHAUS ). Objective evaluations of the composition of bee communities could be the base for accurate determinations of possible changes on the local bee fauna, crop prognoses and definition of distributional occurrence patterns of bee species (BANASZAK ; WILLIAMS et al. 00). In Brazil, SAKAGAMI et al. () conducted the first study using a standardized sampling methodology for bee community in a restricted area. Following this study, several others were conducted, most of them in centralsouthern Brazil. In northeastern Brazil, the first studies on bee fauna were performed by DUCKE (0, 0, 0a, 0b). Recently, other surveys were carried out using a standardized methodology in the caatinga (MARTINS ; AGUIAR & MARTINS ) and restinga areas (VIANA et al. ; SILVA & MARTINS ). ZANELLA (000a, b) presents a preliminary list of the bee fauna in the caatinga. There are no similar studies, however, on the bee communities of the Tabuleiro areas and Atlantic Rainforest of northeastern Brazil. MOURE (000) alerts for the loss of biodiversity and proposes some important attitudes for decreasing this loss and for increasing the biological knowledge: fauna surveys, increment of collections and taxonomic revisions of the described species. The goal of the present study is to investigate the. Partial results of the M. Sc. thesis of the first author, at the Graduate program in Biological Sciences, Ecology and Systematics, Federal University of Paraíba.
2 0 Aguiar & Martins composition of the bee community and the relative abundance of its components at an area with Tabuleiro vegetation and compare this bee fauna with those of other ecosystems such as the caatinga, Atlantic rainforest and cerrado. MATERIAL AND METHODS Studied area The present study was carried out in the Guaribas Biological Reserve (Rebio Guaribas) located in the northeast of the State of Paraíba (in the municipalities of Mamanguape and Rio Tinto), between o 0' and o S, and o 0' and o W. It presents an As climate, which is, according to the Köppen system, hot and humid, with the dry season in the summer and rainy season during the autumn and winter. The average annual rainfall and temperature are mm and - C, respectively (NIMER ). The Tabuleiro vegetation seems to represent a transition or ecological tension between the open formations, caatinga and cerrado, and the Atlantic rainforest. Rebio Guaribas presents contact areas of the savanna vegetation with the seasonal rainforest forming a mosaic ecosystem, which represents an ecological gradient between these two types of vegetation (LANGGUTH ). Furthermore, Rebio Guaribas is located approximately 0 km east of the peripheral areas of the caatinga, 0 km west of the Atlantic coast and 00 km south of the northern limit of the Atlantic rainforest, near the city of Natal (POR ). The studied area has,. hectares with two rather different vegetation formations, according to the classification of phytoecologic regions (SALGADO et al. ): the semi-deciduous rainforest (Atlantic rainforest) of secondary formation and the open arboreal savanna. The semi-deciduous rainforest and the open arboreal savanna vegetation occur on red-yellow podzolic dystrophic soils and on quartz dystrophic sandy soils, respectively. The former is characterized by the presence of plant species such as Bowdichia virgilioides, Hancornia speciosa, Byrsonima crassifolia and Anacardium occidentale. The denomination Tabuleiro characterizes two different vegetation types. In southern Bahia and Espírito Santo, Tabuleiro is a dense and very species rich Atlantic forest. In northeastern Brazil, the Tabuleiro represents areas near the coastline presenting sandy, lixiviated soils as well as savanna vegetation similar to the cerrado (RIZZINI ; OLIVEIRA-FILHO & CARVALHO ). Bee sampling Four hundreds and three hours of collecting were carried out during days, from April/ to March/000, which resulted in an average of, hours per month. The methodology of SAKAGAMI et al () was used with some modifications. A transect, about,00 meters long, was established in the open areas near the border of forested areas in order to obtain samples of the contact areas between the seasonal rainforest and the open arboreal savanna. The transect line was monthly sampled during three or four consecutive days between am and pm. The blooming plants were observed at an approximate distance of fifteen meters on each side of the path, which involved a total area of about. hectares. Most bee species were collected foraging on the flowers, although some individuals on different activities were also sampled. The methodology used is in accordance with some of the recommendations suggested by WILLIAMS et al. (00). The bee specimens collected are deposited in the Coleção Entomológica do Departamento de Sistemática e Ecologia da Universidade Federal da Paraíba (DSEC); some duplicates are in the Coleção Padre Jesus S. Moure, Departamento de Zoologia da Universidade Federal do Paraná (DZUP) and in the Coleção do Laboratório de Sistemática e Ecologia de Abelhas da Universidade Federal de Minas Gerais (BHMG). Analyses The distribution of the number of individuals per species was represented using the method of PRESTON (), which plots the number of species in classes of the logarithm of the number of individuals, also named octaves. The chisquare test was performed using the Bio-Dap program (MAGURRAN ) in order to verify if the obtained curve fitted the truncated log-normal model. The species presenting a proportion of individuals higher than the total number of collected specimens divided by the number of species were considered predominant ( individuals), that is, the expected proportion if there were no domination. Therefore, bee species were considered predominant in number of individuals (Table II). The bee diversity in Rebio Guaribas was compared to that studied in different biomes (see Table IV): cerrado, from the municipalities of Paraopeba-MG and Corumbataí- SP (SILVEIRA & CAMPOS ), cerrado of Ribeirão Preto and Cajuru (PEDRO ) and Lençóis-BA (MARTINS ); caatinga, from São João do Cariri-PB (AGUIAR & MARTINS ), Casa Nova-BA (Martins ), and to preliminary lists of bee species from the caatinga (ZANELLA 000b); restinga, from Cabedelo-PB (SILVA & MARTINS ); and the Atlantic forest, from São Paulo-SP, (RAMALHO ), and Boracéia-SP (WILMS ). In order to standardize the comparisons between the studies, individuals of Apis mellifera, of the tribe Euglossini collected with attractive baits by WILMS () and RAMALHO (), and bees collected with trap-nets were not considered. Some characteristics of the studies on bee communities used for the comparisons are presented in Table I. The graphic method proposed by LAROCA et al. () was used to analyze bee diversity. This method consists of plotting the logarithm 0 of the accumulated number of
3 The bees of the Tabuleiro vegetation a),%,%,%,%,% Andrenidae Colletidae Megachilidae Halictidae Apidae 0,% individuals against the accumulated number of species. High inclination values of the obtained straight line show larger equitability in the distribution of the individuals among the species, whereas the ordinate values represent directly the species richness. The classification of bee families and tribes followed that proposed by ROIG-ALSINA & MICHENER (). RESULTS AND DISCUSSION 0,% 0,%,%,% Fig.. Proportion of number of species (a) and number of specimens (b) of each bee family collected with entomological net from April/ to May/000, at Guaribas Biological Reserve. Three thousand and twenty two specimens of bees belonging to families, genera and species were collected (Table II). The relative abundance of the number of species and individuals (in brackets) per family of bees collected in Rebio Guaribas was the following: Apidae b)).% (0.%), Halictidae.% (.%), Megachilidae.% (.%), Colletidae.% (0.%), and Andrenidae.% (0.%) (Figs. a, b). When the number of collecting hours is correlated with the number of collected species, a stabilizing tendency of the curve is observed, thereby suggesting that the studied sample of the bee community represented most of the species occurring in the area (Fig. ). The use of trap-nests as supplementary methodology allowed the detection of one more species, Mesocheira bicolor (Fabricius, 0), which was not sampled with the entomological net. Apis mellifera represents more than 0% of the specimens collected at Rebio Guaribas suggesting its possible negative effect in this bee community as a potential exotic competitor for resources. The bee fauna found at the Tabuleiro vegetation is characterized by several species with a small number of individuals (over 0% of the species with less than seven individuals) and few species with many individuals. It was observed that the distribution of the number of species in classes of abundance of individuals, i.e. octaves, did not fit the truncated log normal distribution (p>0.0) (Fig. ). Comparing the logarithm 0 of the cumulative number of individuals against the cumulative number of species from studies carried out in diverse environments, the bee diversity at the Tabuleiro vegetation was intermediate between those observed in the Atlantic rainforest and Table I. Area characteristics of the bee community studies used in the comparison with Rebio Guaribas (*: also with plant species of open vegetation from nearby highland rocky outcrops). Author AGUIAR & MARTINS () MARTINS () SILVEIRA & CAMPOS () SILVEIRA & CAMPOS () MARTINS () AGUIAR & MARTINS (this study) Location São João do Cariri (PB) Casa Nova (BA) Corumbataí (SP) Paraopeba (MG) Lençóis (BA) Mamanguape (PB) Habitat Type caatinga caatinga cerrado cerrado cerrado* Tabuleiro Latitude/ Longitude 0 o S / o 0 W 0 o S / o 0 W o S / o W o 0 S / o 0 W o S / o W o 0 S / o W Altitude (m.) Rain Fall (mm/year), 00? Sampling Period (months) Interval between Sampling (in days) SILVA & MARTINS () RAMALHO () WILMS () Cabedelo (PB) São Paulo (SP) Boracéia (SP) restinga Atlantic forest Atlantic forest º0 "S/ º0 "W o S / O W o S / o W ?
4 Aguiar & Martins number of species Collecting effort (hours) Fig.. Cumulative number of bee species by collecting effort (number of collecting hours), from April/ to May/000, at Guaribas Biological Reserve. Number of species Log abundance (octaves) Fig.. Distribution of number of bee species by classes of number of individuals, in octaves (log ), at Guaribas Biological Reserve. cerrado areas (upper curves in Fig. ) and the caatinga and the restinga areas (lower curves in Fig. ). Regarding the species richness, Meliponini, Centridini and Augochlorini stood out among the high level taxa considered by presenting, and species, respectively. Additionally, regarding the number of individuals, the most abundant tribes were Meliponini, Apini and Centridini with,%,,% and,%, respectively, of the sampled individuals (Table III). Compared with other bee communities, the number of species of the Tabuleiro vegetation was within the range of values of the caatinga and cerrado areas, and closer to the values observed in the cerrado areas. As observed in most studies carried out in the tropics, Apidae was also the most abundant family in the Tabuleiro, followed by Halictidae and Megachilidae. Surveys carried out in the south and southeast regions of Brazil show a higher number of species belonging to Halictidae (SAKAGAMI & LAROCA ; WITTMANN & HOFMANN 0; RAMALHO ; WILMS ; ALVES-DOS-SANTOS ). According to MICHENER (000), the diversity center for the tribe Augochlorini is in southern Brazil and northern Argentina. Megachilidae is more diverse in the cerrado areas of Paraopeba and Lençóis, especially due to the species of Megachilini. Regarding the number of species, although it was more abundant in the cerrado of Lençóis, restinga of Cabedelo and in the Tabuleiro vegetation of Rebio Guaribas, the tribe Anthidiini presents a small variation in the compared studies. The number of species of Colletidae and Andrenidae was larger in the southern bee communities than in the open areas of caatinga and cerrado. In number of species, both families are better represented in studies carried out in the south of Brazil. (SAKAGAMI & LAROCA ; BARBOLA & LAROCA ; WITTMANN & HOFFMANN 0). In the Atlantic rainforest and caatinga, Andrenidae was represented only by the Panurginae, while in the cerrado and the Tabuleiro, mainly by the Oxaeinae. The larger abundance, in number of specimens, of Meliponini in Rebio Guaribas has also been observed in areas studied by those works presented in Table IV. However, the tribe Meliponini presented larger species richness in the Tabuleiro vegetation than in the open areas of caatinga, cerrado and restinga, the results being closer to those found in the Atlantic rainforest. Probably, this is due to the fact that forest areas offer more nesting sites for the species of Meliponini, as well as the availability of resources such as mass flowering trees (ROUBIK ; RAMALHO ). Therefore, the greater richness and abundance of the Meliponini could be explained by the proximity between the collecting areas in Rebio Guaribas and the forest. The representation of the oil-collecting species in number of species and individuals abundance, especially the tribe Centridini, can partially explain the similarities observed between the bee species from Tabuleiro and cerrado areas. Among the species of Centridini cumulative number of species Paraopeba Cantareira Lençois Corumbatai Rebio Guaribas S.J. do Cariri Casa Nova Cabedelo Boracéia 0 log0 of cumulative numberof individuals Fig.. Relation between cumulative number of bee species and the logarithm of cumulative number of specimens in different bee communities. The regression coeficients (R ) are given for each analyzed community. Caatinga: S. J. do Cariri (R = 0,), Casa Nova (R = 0,); Restinga: Cabedelo (R = 0,); Tabuleiro: Rebio Guaribas (0,); Cerrado: Corumbataí (R = 0,), Lençóis (R = 0,), Paraopeba (R = 0,); Atlantic Forest: Cantareira (R = 0,), Boracéia (R = 0,).
5 The bees of the Tabuleiro vegetation Table II. Number of specimens for each bee species collected with entomological net, from April/ to March/000, at Rebio Guaribas (predominant species: ; bee species collected only with trap nests: TN; female: F; male: M). Taxon F M F M APIDAE Apini Apis mellifera Linnaeus, Meliponini Frieseomelitta doederleini (Friese, 00) Frieseomelitta dispar (Moure, 0) Leurotrigona muelleri (Friese, 00) Melipona scutellaris Latreille, Melipona subnitida Ducke, 0 Nannotrigona sp. Paratrigona incerta Camargo & Moure, Partamona littoralis (Pedro & Camargo, 00) Plebeia sp. Plebeia sp. Plebeia sp. Plebeia sp. Scaptotrigona. tubiba (Smith, ) Tetragonisca angustula (Latreille, ) Trigona fulviventris Guérin, Trigona aff. fuscipennis Friese, 00 Trigona spinipes (Fabricius, ) Trigonisca sp. Trigonisca sp. Euglossini Euglossa (Euglossa) cordata (Linnaeus, ) Euglossa (Glossura) ignita (Smith, ) Eulaema (Eulaema) bombiformis (Packard, ) Eulaema (Apeulaema) cingulata (Fabricius, 0) Eulaema (Eulaema) flavescens (Friese, ) Eulaema (Apeulaema) nigrita Lepeletier, Bombini Bombus (Fervidobombus) brevivillus Franklin, Centridini Centris (Centris) aenea Lepeletier, Centris (C.) caxiensis Ducke, 0 Centris (C.) flavifrons (Fabricius, ) Centris (C.) nitens Lepeletier, Centris (C.) spilopoda Moure, Centris (Heterocentris) tarsata Smith, Centris (Heterocentris) analis (Fabricius, 0) Centris hyptidis Ducke, 0 Centris (Ptilotopus) sponsa (Smith, ) Centris (Trachina) fuscata Lepeletier, Centris (Xanthemisia) ferruginea Lepeletier, Centris (X.) lutea Friese, Epicharis (Epicharoides) grandior (Friese, ) Epicharis (Epicharana) flava (Friese, 00) Epicharis (Epicharis) nigrita (Friese, 00) Epicharis (Xanthepicharis) bicolor Smith, Ericrocidini Acanthopus excellens Schrottky, 0 Mesocheira bicolor (Fabricius, 0); TN Mesonychium asteria (Smith, ) Mesoplia (Mesoplia) sp. azurea group Mesoplia (Mesoplia) sp. bifrons group Ctenioschelus goryi (Romand, 0) Osirini Parepeolus aterrimus (Friese, 0) Eucerini Florilegus (Euflorilegus) similis Urban, 0 Exomalopsini Exomalopsis (Exomalopsis) minor Schrottky, 0 Exomalopsis (E.) fulvofasciata Smith, Exomalopsis (E.) analis Spinola, Tapinotaspidini Arhysoceble huberi (Ducke, 0) Paratetrapedia (Lophopedia) sp. Paratetrapedia (Lophopedia) sp. Paratetrapedia (Paratetrapedia) sp Paratetrapedia (P.) sp. Paratetrapedia (P.) sp. Paratetrapedia (Xanthopedia) sp. Tetrapediini Tetrapedia diversipes Klug, 0 Xylocopini Xylocopa (Neoxylocopa) frontalis (Olivier, ) Xylocopa (Neoxylocopa) cearensis (Ducke, 0) Xylocopa (N.) grisescens Lepeletier, Xylocopa (N.) suspecta Moure & Camargo, Xylocopa (Schonnherria) muscaria (Fabricius, ) Ceratinini Ceratina (Ceratinula) augochloroides Ducke, 0 Ceratina (Crewella) maculifrons Smith, Ceratina sp. Ceratina sp. Ceratina (Ceratinula) sp. Ceratina (Ceratinula) sp. Ceratina (Ceratinula) sp. Ceratina (Ceratinula) manni (Cockerell, ) COLLETIDAE Colletes sp. Hyaleus sp. Hylaeus sp. Hylaeus sp. Ptiloglossa cfr. goffergei Moure, HALICTIDAE Halictini Dialictus opacus (Moure, 0) Dialictus sp. Dialictus sp. Dialictus sp. Dialictus sp. Augochorini Augochlora (Augochlora) sp. Augochlora (A.) sp. Augochlora (A.) sp. Augochlora (A.) sp. Augochlora (A.) sp. Augochlora (A.) sp. Augochlora (Oxystoglossella) thalia Smith, Augochloropsis brachycephala Moure, Augochloropsis callichroa (Cockerell, 00) Megalopta sp. Pseudaugochlora sp. Pseudaugochlora graminea (Fabricius, 0) Pseudaugochlora pandora (Smith, ) Thectochlora alaris (Vachal, 0) MEGACHILIDAE Megachilini Coelioxys (Neocoelioxys) sp Coelioxys (Acrocoelioxys) praetextata Haliday, Coelioxys sp. Coelioxys sp. Coelioxys sp. Megachile (Pseudocentron) sp. Megachile (Pseudocentron) sp. Megachile (Neochelynia) brethesi Schrottky, 0 Megachile sp. Megachile sp. Anthidiini Epanthidium tigrinum (Schrottky, 0) Hypanthidium maranhense Urban, Larocanthidium bilobatum Urban, Larocanthidium emarginatum Urban, ANDRENIDAE Callonychium brasiliense (Ducke, 0) Oxaea flavescens Klug, 0 Total F / M TOTAL 0
6 Aguiar & Martins Table III. Percentage of specimens and species number collected per tribes/sub-families from April/ to March/000, at Rebio Guaribas. Tribe/subfamily Meliponini Apini Centridini Augochlorini Tapinotaspidini Ceratinini Anthidiini Xylocopini Ericrocidini Megachilini Halictini Euglossini Eucerini Exomalopsini Bombini Oxaeinae Hylaeinae Tetrapediini Caupolicanini Calliopsini Osirini Colletinae Percentage of specimens (%),,,,,,,,,,0,0,0 0, 0, 0, 0, 0, 0, 0, 0, 0,0 0,0 Number of species 0 collected in the Tabuleiro vegetation, nine species also occurred in the cerrado of Paraopeba, eight in Corumbataí and seven in Lençóis. Five species were shared by the three areas of cerrado: Centris fuscata, C. analis, C. tarsata, C. nitens and Epicharis flava. As to abundance of individuals in these areas, species of Centridini were responsible for % of the individuals in Corumbataí,,% in Rebio Guaribas,,% in Paraopeba and,% in Lençóis. Twenty-nine species were found in common between this study and those listed by ZANELLA (000b) for the caatinga: three Augochlorini, one Andrenidae, six Centridini, one Eucerini, one Ericrocidini, one Euglossini, one Exomalopsini, seven Meliponini, one Tapinotaspidini, one Tetrapediini, one Ceratinini, and four Xylocopini. The species Callonychium brasiliense, Centris hyptidis, Arhysoceble huberi, Melipona subnitida and Paratrigona incerta, which are considered endemic to caatinga, were found in Tabuleiro, probably owing to the distance of only 0 Km of Rebio Guaribas from the closest peripheral areas of the caatinga. Some plant species from the caatinga, such as the cactuses Melocactus violaceus and Cereus jamacaru, also occur in Tabuleiro. Regarding the preliminary list of the cerrado bee species from Ribeirão Preto and Cajuru regions (PEDRO ), there were species in common with the bee fauna of Rebio Guaribas: five Augochlorini, one Apini, two Euglossini, four Meliponini, ten Centridini, three Ericrocidini, one Tetrapediini, one Ceratinini, four Xylocopini, two Megachilini, one Anthidiini, and one Andrenidae. Twenty-four bee species out of collected in the restinga of Intermares beach on the coast of Paraíba state (SILVA & MARTINS ) were also found in Tabuleiro. The distribution of the log of the number of individuals did not fit the truncated log normal distribution. This means that a higher sampling effort is necessary to collect the rare species or that the Tabuleiro bee community is not at stability or ecosystemic health in the sense of KEVAN et al. (). Comparisons among bee surveys can be a difficult task due to differences in sampling effort and subjectivity in the definition of the communities limits (HEITHAUS ) and also to the need of systematic revisions in some genera of Halictidae (e.g. Augochloropsis and Dialictus), Megachilidae (e.g. Megachile), Colletidae (e.g. Hylaeus), and Meliponini from northeastern Brazil (PEDRO & CAMARGO ; MICHENER 000). However, even considering the above difficulties, such comparisons may reveal patterns and tendencies that can be tested in the future. The number of species observed in the compared studies shows an increasing number of species from the open areas of the restinga, caatinga, and cerrados to the closed areas of the Atlantic rainforest. HEITHAUS () concludes that the physical structure of the plant community has a strong influence on bee communities. MOLDENKE (, ) suggests that neighboring plant communities with differences in physiognomy tend to present very diverse bee communities, whereas distant plant communities with similar physiognomy tend to present related bee communities. The characteristics of the bee diversity in the Tabuleiro vegetation were more similar to those of the open formations of the restinga, caatinga and cerrado than to those of the closed formations of the Atlantic rainforest. The intermediate characteristics of the Rebio Guaribas bee fauna with the open areas of the caatinga, cerrado and with closed areas of Atlantic rainforest probably reflect the local vegetation characteristics, which is an area of ecological tension with mosaic-shaped formations of seasonal semi-deciduous rainforest and of open savanna. Historical factors such as the expansions and the retractions of the open areas during the Pleistocene probably influenced the current distribution of the species by producing fragmented favorable areas, which resulted in the current sympatric or disjunct distributions of some species (SILVEIRA & CURE ; SILVEIRA & CAMPOS ; ZANELLA 000a, b). SILVA () proposes that the similarities between the bird fauna of the Atlantic rainforest of the northeast Brazil and the cerrado areas can be explained by the expansion of the cerrado vegetation on the northeastern coast during the Pleistocene. Keeping certain precautions in mind, this hypothesis may be used to
7 The bees of the Tabuleiro vegetation Table IV. Number of species and abundance (%) for each tribe, without Apis mellifera (, São João do Cariri, AGUIAR & MARTINS ;, Casa Nova, MARTINS ;, Corumbataí, SILVEIRA & CAMPOS ;, Paraopeba, SILVEIRA & CAMPOS ;, Lençóis, MARTINS ;, Mamanguape, this study;, Cabedelo, SILVA & MARTINS ;, RAMALHO, ;, WILMS ). Nr. of species/ specimens percentage caatinga cerrado Tabuleiro restinga Atlantic forest APIDAE Meliponini Euglossini Bombini Centridini Ericrocidini Osirini Eucerini Exomalopsini Tapinotaspidini Tetrapediini Xylocopini Ceratinini Emphorini Epeolini Rathymini Brachynomadini COLLETIDAE Xeromelissinae Hylaeinae Diphaglossinae Colletinae HALICTIDAE Halictini Augochlorini Rophitinae MEGACHILIDAE Megachilini Anthidiini ANDRENIDAE Oxaeinae Panurginae Total.%.% 0.% 0.%.%.%.%.% 0.% 0%.% 0.%.% %.%.%.%.% 0.% 0.% 0.%.%.% 0.% 0.% 0.% 0.%.%.%.%.% 0.% 0.% 0.%.%.% 0.%.0%.0% 0 0.0%.% 0.%.% % 0.% 0.%.%.%.%.%.% 0.%.%.0% 0.%.%.% 0.%.%.%.%.%.% 0.% 0 00.%.%.%.%.% 0.%.%.%.%.%.0%.% 0.% 0.% 0.% 0.% 0.%.%.% 0.%.%.% 0.%.%.%.%.%.0%.%.% 0.% 0.%.% 0.%.%.%.% 0.%.%.% 0.% 0.%.%.%.%.%.% 0.% 0.0% 0.0% 0.%.%.% 0.%.%.% 0.0%.0% 0.%.% 0.%.%.% 0.% 0.% 0.% 0.0%.%.%.%.%.%.% 0.% 0.% 0.% 0.%.%.% %.%.%.%.% 0.% 0.%.% 0.%.0%.%.0%.% 0.%.%.0% 0.% 0.% 0.% 0.% % 0.% 0.0%.%.%.% 0.%.%.%.0%.0%.% 0.% 0.% 0.% %.% 0.%.0% 0.% 0.% 0.0%.%.0%.% 0.%.%.% 0.% 0.0% 0.0%.% 0.%.% 0.% 0.% 0.%.%.%.%.% 0.%.%.% 0 supporting the similarities found between the bee fauna of the Tabuleiro and the core areas of the cerrado. Several authors have argued that the tropical bee fauna is composed mainly of generalist species and that seasonal activity and specialization increase towards the temperate areas (ROUBIK ; MICHENER 000). The bee fauna of Tabuleiro of Rebio Guaribas presented the expected pattern for tropical areas, with the predominance of Meliponini, Centridini and Augochlorini. Replication of this study, which is taking place in Rebio Guaribas, shall provide complementary information, but further biogeographic studies are also necessary to test the distribution patterns of the bee species. Acknowledgments. We are grateful to Pe. Jesus de Santiago Moure for his stimulus and all his work developed in the bee biodiversity knowledge that permits us to produce our studies. For help in the identification of the bee species, we thank the following colleagues: J. S. Moure, Danúncia Urban, Fernando Silveira, Fernando C. V. Zanella, Márcio Luís de Oliveira, Gabriel A. R. Melo, João Maria Franco de Camargo, Silvia Pedro, Eduardo Almeida, and Favízia Oliveira. We also thank Isabel Alves-dos-Santos, Clemens Schlindwein, Fernando C. V. Zanella and Silvio Nihei for their suggestions. This study was partially funded by CAPES. We wish to thank IBAMA for the permission to work at Rebio Guaribas. In addition, we would like to express our gratitude to the park rangers of Guaribas Biological Reserve for their logistic help, especially the administrator of the Reserve, Marcelo Marcelino. REFERENCES AGUIAR, C. M. L. & C. F. MARTINS.. Abundância relativa, diversidade e fenologia de abelhas (Hymenoptera, Apoidea) na Caatinga, São João do Cariri. Iheringia, Série Zoologia, : -. ALVES-DOS-SANTOS, I.. Abelhas e plantas melíferas da mata atlântica, restinga e dunas do litoral norte do Rio Grande do Sul, Brasil. Revista Brasileira de Entomologia (/): -. BANASZAK, J.. Ecological bases of conservation of wild bees, p. - In: A. MATHESON; S. L. BUCHMANN; C. O TOOLE; P. WESTRICH & I. H. WILLIAMS (eds.), The Conservation of Bees. London, Academic Press. xi+p. BARBOLA, I. F. & S. LAROCA.. A comunidade de Apoidea (Hymenoptera) da Reserva Passa Dois (Lapa, Paraná, Brasil): I. Diversidade, abundância relativa e atividade sazonal. Acta Biologica Paranaense (,,, ): -. DUCKE, A. 0. Contribution à la connaissance de la faune hyménoptérogique du Nord-Est du Brésil. Revue d Entomologie : -.
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