SNFE648 Studies on Neotropical Fauna and Environment 0165-0521/02/3701-001$16.00 2002, Vol. 37, No. •, pp. ••–•• © Swets & Zeitlinger

Flower Visits of Centris (: ) in an Area of Caatinga (Bahia, Brazil)

Cândida Maria Lima Aguiar

Dept. of Biological Sciences, State University of Feira de Santana, Feira de Santana, State of Bahia, Brazil

Abstract Periodic sampling of bees visiting flowering plants resulted The Caatinga is a deciduous forest type, whose principal in the collection of 91 individuals of 10 Centris in an character is the absence of leaves during much of the year. area of Caatinga (Itatim, Bahia, Brazil). These bees visited The Caatinga comprises several different plant communities, 12 species of plants. Melochia tomentosa (Sterculiaceae), and covers about 800,000km2 in northeastern Brazil a nectar source, was the most frequently visited plant. (Andrade-Lima, 1981). Despite their presumed ecological Chamaecrista, Senna and Solanum species were visited for importance, little is known about the native species , and Stigmaphyllon auriculatum for oil. Centris bees present, and their interactions with flowering plants in the were captured from September through April. The data Caatinga. The high percentage of endemic species of bees suggest a seasonal pattern of activity, associated with the found there (32%, including two Centris species), indicates rainy season. that the Caatinga has its own bee fauna (Zanella, 2000a, b). In the Caatinga, Centris bees are the major group of oil- Keywords: Centris, Caatinga, South American dry forests, collectors, for oil-collecting bees of other genera (, bee phenology, floral resources, northeastern Brazil. Tetrapedia and Paratetrapedia) are either rare or absent (Vogel & Machado, 1991; Zanella, 2000a). According to Schlindwein (2000), the are specialized foragers 1 Introduction and key pollinators, helping to maintain plant diversity in tropical ecosystems. As they are essential to the reproductive Centris bees are fundamental components of the large-bee success of several plant species, it is important to identify guild of pollinators, and their importance in dry forests those plants which help to sustain their populations. has been noted by Frankie et al. (1976; 1983). In Brazil, The sampling of bees during floral visits, employing pollination studies in the Cerrado (Gottsberger, 1986), standardized methodology, has been undertaken at a num- on dunes (Gottsberger et al., 1988) and in the Caatinga ber Caatinga sites (Martins, 1994; Aguiar & Martins, 1997; (Vogel & Machado, 1991) have demonstrated that many Viana, 1999; Zanella, 2000a), although data concerning bee plants, such as , , as well as some phenology and the floral resources used by each species are species of Chamaecrista, Passiflora, and Turnera, are polli- rare. This work was designed to investigate species richness, nated by Centris bees. In some cases, mainly among oil as well as to identify the plants visited by Centris bees in an flowers, these bees are the only legitimate visitors (Vogel & area of Caatinga in the State of Bahia. Machado, 1991), and these plants depend on the services of Centris bees because of their specialized foraging behavior. Studies on the community of pollinators in the Brazilian Material and methods Caatinga have not yet been undertaken, although, as in other Study site Neotropical habitats with open vegetation, Centris bees would be expected to appear as important pollination agents Sampling was done in the municipal district of Itatim there. (12°42¢S, 39°46¢W), near Mount Agenor (200km from the

Received: 17 May 2000 Accepted: 26 August 2002 Correspondence: C.M.L. Aguiar, Depto. de Ciências Biologicas, Universidade Estadual de Feira de Santana, 44031-460 Feira de Santana – BA, Brazil. Fax: +55-75-224 8264; E-mail: [email protected] SNFE648 2 C.M.L. Aguiar city of Salvador) in the State of Bahia, Brazil. The vegeta- although the number of individuals was low in October 1997 tion is predominantly open shrubby Caatinga, common in the (Table 1). The highest number of bees was collected during dry areas of northeastern Brazil. Melochia tomentosa and the rainy season (November to April) while from May to Acacia bahiensis were the most abundant shrubs. Trees are September no Centris bees were recorded. However, there scarce, with Caesalpinia pyramidalis, Spondias tuberosa and was no significant correlation established between the amount Ziziphus joazeiro being the most common species (França et of rainfall and the number of individuals netted per month al., 1997). [correlation analysis: r = 0.38; p > 0.05)], nor the number of The climate is semi-arid, with an average annual tem- species collected (r = 0.29; p > 0.05). perature of 24.3°C and an average annual precipitation of 551mm, although there can be large annual variations (range: 142–1206mm). There are at least five dry months per Discussion year (Bahia, 1994). During the course of this study, the rainy Species spectrum and richness of Centris bees season started in November 1996, and ended in April 1997. The month of December 1996 was uncommonly dry, while The species richness of Centris bees found at Itatim was March and April of 1997 were the rainiest months. The dry relatively high in comparison to other areas of Caatinga, such season extended from May through September of 1997. as São João do Cariri (3 spp., Aguiar & Martins, 1997), Serra Negra do Norte (6 spp., Zanella, 2000a) and Casa Nova (8 spp., Martins, 1994), and was similar to the number of Sampling schedule species encountered in Ibiraba (11 sp., Viana, 1999) and Bees and flowering plants were collected during two Castro Alves (12 spp., Carvalho, pers. comm.). The species consecutive days each month for a fifteen-month period richness of Centris bees in areas of Caatinga is higher than (September 1996 until November 1997). Collecting was per- that observed at Boracéia, in the Atlantic Coastal Rain Forest formed between 12:00 and 06:00 p.m. on the first day and (5 spp., Wilms, pers. comm.), although slightly lower than then between 06:00 and 12:00 a.m. on the second day, for a that found in areas of Brazilian Cerrado (17 spp., Silveira & total of 180 hours of sampling time (12h/mo). Campos, 1995). Bees were captured with entomological nets at all flower- Five species (C. aenea, C. fuscata, C. tarsata, C. ing plants (48 melittophilous species) encountered while trigonoides, and C. xanthomelaena) found in Itatim have walking along a 3km transect. The transect was patrolled been sampled in several other areas of Caatinga (Martins, twice in the morning and twice in the afternoon, always start- 1994; Viana, 1999; Zanella, 2000a). Except for C. xan- ing at different points. Thus, each flowering plant was thomelaena, a species endemic to the Caatinga (Zanella, observed at different times on different days. Approximately 2000b), those species are also common in other habitats as 5min were spent at each plant to capture bees. The time of in the Cerrados (Martins, 1994; Silveira & Campos, 1995) day and the plants being visited were recorded for each and in the Atlantic Coastal Rain Forest (Wilms, pers. comm.; bee collected. Voucher specimens of bees and plants were Teixeira & Machado, 2000). On the other hand, C. caxiensis, deposited in the Herbarium and Entomological Collection of C. leprieuri, C. moerens and C. sponsa are less common the State University of Feira de Santana, at Feira de Santana, species and they have been collected in few areas of Caatinga State of Bahia, Brazil. beyond Itatim. Of these, C. moerens has not been registered in other habitats, while C. leprieuri occurs in the dune veg- etation in Northeastern Brazil (Gottsberger et al., 1988), Results C. caxiensis is present in coastal vegetation (Rêgo & Albuquerque, 1989) and in the Cerrados in the State of 2 Ninety-one individuals belonging to ten Centris species were Maranhão (Brazil) (Albuquerque & Mendonça, 1996) and obtained, 88 of them while visiting flowers. The others were C. sponsa also occurs in the Cerrados (Silveira & Campos, captured in flight. C. aenea and C. fuscata were most fre- 1995). quently captured, while other species were sampled rarely (Table. 1). Centris bees were found visiting 12 of the 48 Floral resources species of flowering plants observed along our transect (Table 2). Melochia tomentosa was the major nectar source, Flowers of Chamaecrista and Senna (Caesalpiniaceae) are being visited by the highest number of individuals from eight important pollen sources for Centris in Itatim and in other species. Caesalpiniacean species and Solanum paniculatum areas (Aguiar, unpublished). Nectar sources are more nu- (Solanaceae) were pollen sources, while Stigmaphyllon merous and are found in several plant genera, including auriculatum (Malpighiaceae) was the only source of floral oil Caesalpinia and Melochia. These were also frequented in among the plants visited by Centris bees. other areas of Caatinga (Vogel & Machado, 1991; Aguiar Centris species were captured from late September until et al., 1995; Lewis & Gibbs, 1999). 3 April. The highest number of bees was sampled between As plants offering floral oils, species of the family October and December (late dry season to early rainy season), Malpighiaceae could be expected to be of special importance SNFE648 Centris bees of the Caatinga 3 for centridine bees; however, we recorded only very few bees on only one species. This may be due to our sampling effort being limited to only one day per month, because other species of Malpighiaceae were not observed flower- ing although Barnebya harleyi, Heteropterys spp., Janusia schwannioides and Thryallis longifolia are known to occur in the vicinity of Mount Agenor (França et al., 1997).

Temporal patterns of activity Our data suggest that the activity of Centris bees was related to the rainy season in the Caatinga. At Itatim, the Centris species most frequently captured seemed to have a seasonal activity pattern like bees in other habitats, such as Costa Rican dry forests (Heithaus, 1979; Frankie et al., 1983) and Panamanian forests (Wolda & Roubik, 1986). In Costa

Rican dry forests, however, Centris species were only Aug active during the dry season (Heithaus, 1979; Frankie et al., 1983). A similar pattern was recorded in some areas in the State of Maranhão (Brazil) (Albuquerque & Rêgo, 1989; Albuquerque & Mendonça, 1996). In Panamanian tropical forests, on the other hand, these bees were active in the early rainy season, and then absent in the late rainy season, and for most of the dry season (Wolda & Roubik, 1986). However, due to the small numbers of individuals collected in most areas it may be too early to draw any conclusions about the different temporal patterns of activity of Centris species. In the Costa Rican dry forest, the seasonal patterns of activity of Centris bees seem to be related to the abundance of floral resources. The majority of plant species, including several Leguminosae, Malpighiaceae and Bignoniaceae, which are important resources for Centris bees, flower during the long dry season, and most of these employ mass flower- ing (Frankie et al., 1974). In the Caatinga, efforts have not yet been made to evaluate seasonal floral resource availabil- ity. In at least two Caesalpinia species visited by Centris,

flowering seems to be stimulated by rainfall (Lewis & Gibbs, 1996 1997 1999). Further studies on the flowering phenology of plants important to Centris bees could help in understanding the seasonal patterns observed for these bees in the Caatinga environment.

Acknowledgements bees collected per month in Itatim, State of Bahia, Brazil. The State University of Feira de Santana supported this Sep Oct Nov Dec Jan Feb Mar Apr May– Sep Oct Nov Total ––193111–1– 2––11–––––––962 –––12111––– –––––––––––––33 ––1–––––––– –––––––––––––1– 1–––5–3–––– 1–––––––––––293 –––13––3––– –––––––––2–2175 ––––––––––– 2–3–1–––––––––6 ––––––––––1 11––––––––25411––1– –––1––––1–––189 –––––––1––– –––122 ––––––––––––––1 research. I would like to thank Gilberto M. M. Santos, Janete J. Rezende and Valéria M. Monteiro for their assistance Centris during the field work, Fernando C. V. Zanella for identifying Centris species, Flávio França and Efigênia Melo for identi- fying the plants, as well as Carlos A. Garófalo and Míriam Gimenes, for their suggestions. p12–––––––––– –––––––––––––2– sp.1 Table 1.Table The number of Species 3–411366–21 61322–––12–2135 TOTAL C. (Centris) aenea C. (C.) caxiensis C. (C.) leprieuri C. (C.) C. (Hemisiella) tarsata C. (H.) trigonoides C. (Ptilotopus) moerens sponsa C. (P.) fuscata C. (Trachina) Centris xanthomelaena SNFE648 4 C.M.L. Aguiar C. moerens C. sponsa C. fuscata sp. 1 species netted at flowering plants in Itatim, State of Bahia, Brazil, between September 1996 and November 1997. September 1996 and November plants in Itatim, State of Bahia, Brazil, between species netted at flowering Centris C. aenea C. caxiensis C. leprieuri C. tarsata C. trigonoides C. xanthomelaena Centris oil 1 = P– 1 – – –P– – – – – – – – – – 2 – 3 – – P9– – – 3 – – – 1 3 N– – – 1 –N2– – 1 – – –N4– 1 – – 2 – – 2 – – N– – 1 4 – – – –O– 1 – – – – 3 – – –N– – – – – –N2– – – – – 3 – N1– 1 1 – 3 – 1 – – – 1 5 – N114 – 4 – – – – – – 1 – 1 1 – – – – – 1 3 Floral pollen and O = nectar, P nectar, belemii paniculatum heptaphylla pyramidalis scandens auriculatum cincinnata corindum tomentosa = Tecoma Tecoma procera Poeppigia Chaetocalyx Caesalpinia Chamaecrista Senna spectabilis Stigmaphyllon Passiflora foetida Passiflora Cardiospermum Melochia Solanum N Bignoniaceae Fabaceae on flowersTotal 29 6 1 12 12 1 2 6 2 17 Caesalpiniaceae Malpighiaceae Passifloraceae Sapindaceae Sterculiaceae Solanaceae Table 2.Table of The number of individuals Species of plants Resource 1 SNFE648 Centris bees of the Caatinga 5

References Viana BF (1999): A comunidade de abelhas (Hymenoptera: Apoidea) das dunas interiores do Rio São Francisco, Bahia, Aguiar CML, Martins CF (1997): Abundância relativa, diversi- Brasil. An Soc Entomol 28: 635–645. dade e fenologia de abelhas (Hymenoptera, Apoidea) na Vogel S, Machado ICS (1991): Pollination of four sympatric caatinga, São João do Cariri, Paraíba, Brasil. Iheringhia species of Angelonia (Scrophulariaceae) by oil-collecting Sér. Zool, 83: 151–163. bees in NE, Brasil. Plant Syst Evol 178: 153–178. Aguiar CML, Martins CF, Moura ACA (1995): Recursos florais Wolda H, Roubik DW (1986): Nocturnal bee abundance and utilizados por abelhas (Hymenoptera, Apoidea) em área de seasonal bee activity in a Panamanian forest. Ecology 67: caatinga (São João do Cariri, Paraíba). Rev Nordestina Biol 426–433. 10: 101–117. Zanella FCV (2000a): The bees of Caatinga (Hymenoptera, Albuquerque PMC, Mendonça JAC (1996): Anthophoridae Apoidea, Apiformes): a species list and comparative notes (Hymenoptera: Apoidea) e flora associada em uma for- regarding their distribution. Apidologie 31: 579–592. mação de cerrado no município de Barreirinhas, MA, Zanella FCV (2000b): Padrões de distribuição geográfica das Brasil. Acta Amazonica 26: 45–54. espécies de abelhas que ocorrem na Caatinga (NE do Albuquerque PMC, Rêgo MMC (1989): Fenologia das espécies Brasil). Anais do IV Encontro Sobre Abelhas, Ribeirão visitantes de murici (Byrsonima crassifolia, Malpi- Preto, Brazil, pp. 197–203. ghiaceae). Bol Mus Para Emílio Goeldi Zool 5: 163–178. Andrade-Lima D (1981): The caatingas dominium. Rev Bras Bot 4: 149–153. Bahia – Centro de Estatísticas e Informações (1994): Infor- mações Básicas sobre os Municípios Baianos. Salvador, Brazil, pp. 279–282. França F, Melo E, Santos CC (1997): Flora de inselbergs da região de Milagres, Bahia, Brasil: I – Caracterização da vegetação e lista de espécies de dois inselbergs. Sitientibus 17: 163–184. Frankie GW, Baker HG, Opler PA (1974): Comparative pheno- logical studies of trees in tropical wet and dry forest in the lowlands of Costa Rica. J Ecol 62: 881–919. Frankie GW, Haber WA, Opler PA, Bawa KS (1983): Charac- teristics and organization of the large bee pollination system in the Costa Rican dry forest. In: Jones CE, Little RJ, eds., Handbook of Experimental Pollination Biology. Van Nostrand Reinhold, New York, pp. 411–447. Frankie GW, Opler PA, Bawa KS (1976): Foraging behaviour of solitary bees: implications for outcrossing of a neotropical forest tree species. J Ecol 64: 1049–1057. Gottsberger G (1986): Some pollination strategies in Neotropi- cal savannas and forests. Plant Syst Evol 152: 29–45. Gottsberger G, Camargo JMF, Silberbauer-Gottsberger I (1988): A bee-pollinated tropical community: the beach dune veg- etation of Ilha de São Luís, Maranhão, Brazil. Bot Jahrb Syst 109: 469–500. Heithaus ER (1979): Community structure of neotropical flower visiting bees and wasps: diversity and phenology. Ecology 60: 190–202. Martins CF (1994): Comunidade de abelhas (Hym., Apoidea) da caatinga e do cerrado com elementos de campo rupestres do estado da Bahia, Brasil. Rev Nordestina Biol 9: 225– 257. Silveira FA, Campos MJO (1995): A melissofauna de Corum- bataí (SP) e Paraopeba (MG) e uma análise da biogeografia das abelhas do cerrado brasileiro. Rev Bras Entomol 39: 371–401. Teixeira IAG, Machado ICS (2000): Sistema de polinização e reprodução de Byrsonima sericea DC (Malpighiaceae). Acta Bot Bras 14: 347–357. AUTHOR QUERY FORM

Dear Author,

During the preparation of your manuscript for publication, the questions listed below have arisen. Please attend to these matters and return this form with your proof.

Many thanks for your assistance.

Query Query Remarks References

1 Au: Plaese add Schlindwein 2000 to the reference list.

2 Au: Rêgo & Albuquerque or Albuquerque & Rêgo, as in the reference list?

3 AU: Please make sure Lewis & Gibbs, 1999, is mentioned in the reference list.

SNFE648