oliveira & schlindwein 2009 centris analis

HORTICULTURAL ENTOMOLOGY

Searching for a Manageable Pollinator for Acerola Orchards: TheSolitary Oil-Collecting Bee Centris analis (Hymenoptera:

Apidae: Centridini)

REISLA OLIVEIRA1 AND CLEMENS SCHLINDWEIN2

J. Econ. Entomol. 102(1): 265Ð273 (2009)

ABSTRACT Acerola (Malpighia emarginata DC; Malpighiaceae) is an important fruit crop inBrazil. Among its pollinators, Centris (Heterocentris) analis (F.) stands out due to its abundanceat ßowers and prompt acceptance of trap-nests. For the Þrst time, we propose the commercial useof Centris bees as orchard pollinators. To develop protocols for rearing and management of thesebees, we analyzed trap-nest acceptance, brood-cell construction, and larval diet in Acerolaorchards. Although Centris species, in general, use numerous pollen host plants, females of C.analis showed remarkable ßower Þdelity to Acerola for pollen supply when nesting in the orchard.Such Þdelity was previously expected only for ßoral oil collection. The ease of acceptance oftrap-nests by females of C. analis, their prolonged yearly activity period, multivoltine life history,and high pollinator efÞciency characterize C. analis as an excellent potentially manageablepollinator in Acerola orchards.

KEY WORDS Centris analis, Malpighia emarginata, larval diet, crop pollination

Acerola, also called West Indian cherry (Malpighiaemarginata DC.; Malpighiaceae), is original from theAntilles, Central America, and northern South Amer-ica and has been cultivated in Brazil, Puerto Rico,Cuba, and the United States (Hawaii and Florida). InSouth America, northeastern Brazil is the main regionwhere this fruit crop is produced, holding �7,236 haof cultivated orchards, which yield more than US$6million per year (Cardoso et al. 2003).

Like other Neotropical Malpighiaceae, Acerola pro-duces ßoral oil in elaiophores, attracting bees of thetribe Centridini (Hymenoptera: Apidae) as pollina-tors (Vogel 1974, Buchmann 1987). This tribe includes�167 species of robust, fast-ßying solitary bees of thegenera Centris and Epicharis, which occur in tropicalregions of the Americas (Michener 2000, Silveira et al.2002). To complete a life cycle, these bees requirefood resources for adults (nectar) and immatures(pollen, ßoral oil, nectar, or both), nesting substrates(bare soil, nests of ants or termites or preexistingcavities) and nesting materials, such as shaved plantmaterials, ßoral oil, and sand (Vogel 1974, Alcock et al.1976, Vinson and Frankie 1977, Roubik and Michener1980, Coville et al. 1983, 1986; Pereira et al. 1999;Vinson and Frankie 1999; Jesus and Garofalo 2000,Silva et al. 2001, Gaglianone 2001, Aguiar and Gagli-

anone 2003; Aguiar and Garofalo 2004; Vinson et al.2006).

The centridine females are morphologically andbehaviorally specialized in collecting ßoral oils. Theyare the sole pollinators of hundreds of ßoral oil-pro-ducing species, mainly Malpighiaceae, Plantaginaceae(previously Scrophulariaceae) and Krameriaceae(Vogel 1974, 1990). The oil is collected with special-ized brushes on the fore and mid basitarsi and is usedto nourish the larvae or to make the walls of the broodcells impermeable (Vogel 1974, Neff and Simpson1981, Buchmann 1987).

Centridine bees, in general, are polylectic and visithundreds of plants for pollen, including buzz-pollina-tion ßowers and generalist pollen ßowers (Vogel 1974,Buchmann 1983, Aguiar 2003, Aguiar and Gaglianone2003). In Brazil, they are essential to the pollination ofnumerous plant species of Cerrado, Caatinga, Ama-zonian, and Atlantic rain forests. Bees of Centridini arealso the sole pollinators of Acerola (Raw 1979, Freitaset al. 1999, Duarte and Schlindwein 2003). In Pernam-buco, northeastern Brazil, 14 species of Centris andtwo of Epicharis were pointed out as pollinators ofAcerola in orchards. Nevertheless, fruit set in the or-chards was found to be insufÞcient (Schlindwein et al.2006, Schlindwein 2008).

All Epicharis and most of the species of Centris areground-nesting bees. Females of the subgenera Het-erocentris, Hemisiella, and Xanthemisia, however,build their nests in preestablished cavities, mostly bee-tleburrows indeadwood(Covilleet al. 1983, Jesus andGarofalo 2000, Silva et al. 2001, Aguiar and Garofalo2004). Bees of these species therefore could be reared

1 Corresponding author: Programa de Pos-Graduacao em CienciasBiologicas-Zoologia, Universidade Federal da Paraõba, Cidade Universi-taria, 58.059-900-Joao Pessoa, PB, Brazil (e-mail: [email protected]).

2 Departamento de Botanica, Universidade Federal de Pernam-buco, Avenida Prof. Moraes Rego, s/n, Cidade Universitaria, 50.670-901-Recife, PE, Brazil.

0022-0493/09/0265Ð0273$04.00/0 � 2009 Entomological Society of America

in artiÞcial nests, once their nesting behavior andspeciÞc requirements on environmental conditionsare known.

Females of Centris (Heterocentris) analis (F.) areeffective pollinators of Acerola orchards, move in-tensely between plants and touch stigmas and anthersduring each ßower visit (Schlindwein et al. 2006).Acerola blooms throughout the year and, contrary tomost other centridine bees, C. analis visits Acerolaßowers year-around. Females accept artiÞcial cavitiesas nesting sites and frequently occupy trap-nests(Aguiar and Martins 2002, Aguiar et al. 2005). Floraloils, anther fragments, and Þbers are the materialsused for nest construction and delimiting of the broodcell walls. A female builds one to three nests, contain-ing up to eight brood cells each (Jesus and Garofalo2000).

Although many solitary bee species are effectivecrop pollinators (Free 1970, Westerkamp 1991, Rou-bik 1995, Buchmann and Nabhan 1996, Cane 2002),only a few species are managed and reared for com-mercial pollination. Among these are Megachile (Eu-tricharaea) rotundata (F.) (Megachilidae) (Petersonet al. 1992, Bosch and Kemp 2005) and Nomia (Acu-nomia) melanderi Cockerell (Halictidae) (Torchio1990, 1991a) for alfalfa,Medicago sativaL. (Fabaceae),seed; and Osmia [Osmia) cornuta (Latreille)(Megachilidae)] (Bosch 1994a, Monzon et al. 2004),Osmia (Osmia) lignaria Say (Torchio 1982, 2003;Bosch et al. 2006), andOsmia cornifronsRadoszkowski(Maeta apud, Bosch and Kemp 2001) for orchard ap-ples, Malus domestica L. (Rosaceae); plums, Prunusdomestica L. (Rosaceae); and almonds, Prunus dulcis(Mill.).

For a few other bee species, their potential as man-ageable pollinators has been demonstrated:Osmia ag-laia (Cane 2005), Amegilla spp. (Hogendoorn et al.2000, 2007), Habropoda laboriosa (F.) (Apidae)(Cane 1997), and carpenter bees (Xylocopa spp.; Api-dae) (Corbet and Willmer 1980, Freitas and OliveiraFilho 2000, Buchmann 2004). Of these species, onlycarpenter bees occur in South America, and until nowno native solitary bees are being managed for polli-nation in this continent, despite the high diversity ofbees (Silveira et al. 2002).

The management of native bees for crop pollinationhas been repeatedly suggested as a means to guaranteesustainable agriculture. In the choice of the ideal pol-linator, its pollen transfer efÞciency, ßower constancy,abundance in agroecosystems, and possibility for rear-ing are essential features to consider (Roubik 1995,Williams 1996).

Here, for the Þrst time, we propose the managementof a species of Centris as an orchard pollinator. Weanalyze the potential of the solitary bee C. analis as amanageable Acerola pollinator in northeastern Braziland address nesting conditions, ßoral constancy, larvaldiet, and nesting behavior of this species in M. emar-ginata orchards.

Materials and Methods

Study Sites.The study was conducted from Novem-ber 2003 through March 2005. Trap-nests were in-stalled and monitored at the commercial orchard “Ac-erolandia”, municipality of Paudalho (07� 51�S, 35�15�W) and in Aldeia, municipality of Camaragibe (7�41�S, 34� 67�W), both in the state of Pernambuco,northeastern Brazil.

Acerolandia was the Þrst commercial Acerola or-chard in Brazil. The farm includes 6,000 Acerola treeson 4 ha and a few other crops, such as soursop (Annonamuricata L.; Annonaceae), passion fruit (Passifloraedulis Sims.; Passißoraceae), papaya (Carica papayaL.; Caricaceae), and coconut (Cocos nucifera L.;Areaceae). The surrounding vicinity is poorly urban-ized, with pasture, sugarcane monocultures, and tinyremnants of original Atlantic rain forest cover. TheAldeia site is characterized by the presence of housesand small farms with numerous ornamental plants andtropical fruit crops, surrounded by a more diverse andbetter preserved Atlantic rain forest cover than that ofthe Acerolandia site. Acerola plants were also com-mon at this site, but they occur only in small orchardsand scattered in gardens.Trap-Nests. Two types of trap-nests were used. The

Þrst model, compact trap-nests, commonly used insurveys of cavity-nesting solitary bees, consisted ofcardboard straws inserted into cavities drilled length-wise (Camillo et al. .1993, 1995; Aguiar and Martins2002; Thiele 2002, 2005). The internal diameter of thetubes ranged from 5 to 12 mm (5, 6, 7, 8, 9, 10, 11, and12 mm), with one end closed with melted parafÞnencrusted in a wad of cotton. The lengths of the holesranged from 7.5 to 8.5 cm and increased with increas-ing diameters. Each block contained 40 tubes, Þve ofeach diameter. Five of these blocks, for a total of 200cavities, were distributed in the Acerolandia orchard.

The second model of trap-nest were observationnests, as proposed by Cane (2004). These consisted of10 linear cavities of 6, 8, or 10 mm in diameter, cutlengthwise in 14- by 20- by 2-cm wooden plates. Thecavities were covered with a transparent plastic sheetÞxed the plate with an adhesive tape. This permittedvisualization of the content and monitoring of thebrood cells. A sheet of felt was glued to the bottom ofeach plate. Three plates, each containing cavities ofone of the different diameters, were joined to form aunit of 30 cavities (Fig. 1). We installed seven of theseblocks, totalling 210 cavities, in the plantation at theAcerolandia site. At the Aldeia site, only observationnests of the above cited diameters were installed (150cavities).

We counted the number of occupied nests andbrood cells and recorded the used diameters in com-pact and observation trap-nests. We compared occu-pation rates and proportion of occupied cells per nesttype and size class of cavities. The preference forcavities of different sizes was veriÞed using a chi-square test; the proportion of cells in the two nesttypes was compared with MannÐWhitney test. TheKruskalÐWallis test was used to compare the number

266 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 1

of brood-cells among straws of different size in com-pact and observation nests (Zar 1996). Data wereanalyzed with Statistica version 6 (StatSoft, Tulsa,OK) and BioEstat 4.0 (Sociedade Civil Mamiraua, Bra-sõlia, Brazil). Arithmetic means � standard errors aregiven.

The behavior of the nesting bees was studied onlyat the Acerolandia site from November 2004 to June2005. The 410 artiÞcial cavities were monitored twicea month. During this period, we recorded the insectsthat nested in the trap-nests, the time the nests wereoccupied and the used diameters. During the processof brood cell construction and provisioning, the ac-tivities of females of C. analis were described. Werecorded the time a bee left and returned to the nestand measured the duration spent inside and outsidethe nest. When a female returned from a foraging trip,we noted if she carried pollen, oil or nesting materialin the scopae. For seven females we calculated themean duration of these trips and for one female wemade continuous observations of nesting activity dur-ing three days until nest closure. In the observationnestswesometimes inspected thebroodcell under thetransparent sheet and checked the collected material.This was always performed in the absence of thefemales to avoid disturbance. Vouchers of bees aredeposited in the Entomological Collection of FederalUniversity of Pernambuco (UFPE), Recife.Pollen Analysis of Nest Provision. Larval mass pro-

visions of 18 recently closed brood cells of differentfemales ofC. analiswere removed from the trap-nestsfrom the Acerolandia and Aldeia sites to identify and

quantify the stored pollen (two in January, Þve inFebruary, nine in March, and two in April). The pollenmass of a cell was carefully transferred to an Eppen-dorf tube and dispersed in 1.5 ml of lactic acid solution.The amount of grains in 0.4 �l, the volume of thechamber, was counted under the microscope, and theaverage amount of three counts per brood cell wasextrapolated to 1.5 ml.

The pollen sources of the larval provision wereidentiÞed using light microscopy. A microscope slidewith basic fuchsin stained glycerin gelatin was pre-pared from subsamples of each cell provision (Lou-veaux et al. 1978), identifying �800 grains. Pollen wasidentiÞed using the pollen slide reference collectionof the Laboratory “Plebeia-Bee ecology and pollina-tion,” at the UFPE, Recife.

Results

Trap-Nests Occupation. Individuals of C, (Hetero-centris) analis, C. (Hemisiella) tarsata Smith, Tetrape-dia sp. (Apidae: Tetrapediini), and Dicranthidium sp.(Megachilidae: Anthidiini) occupied the providednesting blocks. Among the eight offered diameters ofcavities in compact trap-nests (5Ð12 mm), females ofC. analis used only those with 6 (39%), 7 (39%), and8 mm (22%) but showed no preferences in occupationfor any of them (�2 � 1.06492, df � 1, P� 0.5872). Inobservation trap-nests, all three offered diameters ofcavitiesÑ6 (10%), 8 (23%), and 10 mm (67%)Ñwereoccupied. The 10-mm cavities, however, were pre-

Fig. 1. Observation trap-nests. (Top) A unit with three plates and 30 holes. (Bottom) Three completed nests of C. analis;pollen content, nectar column and construction material are visible under the transparent polyvinyl chloride sheet. Larvaeare immersed in a nectar column in the apical part of each cell and not visible.

February 2009 OLIVEIRA AND SCHLINDWEIN: POLLINATOR FOR ACEROLA ORCHARDS 267

ferred to the smaller ones (�2 � 31.111, df � 1, P �0.0001).

The occupation rate in the two nest models did notdiffer: C. analis females occupied 48 cavities (22.8%)of the observation trap-nests and 17 (22.6%) of thecompact trap-nests, not considering the nonoccupiedsize classes. Females constructed up to six brood cellsper nest (Table 1), totaling 170 brood cells. Compacttrap-nests contained, on average, more brood cells(3.8) than observation nests (2.3) (U � 165.5000, P�0.001). The number of reared offspring did not differamong the cavity sizes (compact trap-nests: H � 2.758,P� 0.2518; observation nests: H: � 0.8161,P� 0.6649).A vestibular cell, an empty space between the nestplug and the last brood cell, measuring 1.3 cm onaverage, was present in all nests.

The rate of emergence was 87% in compact trap-nests and 29% in observation nests. Approximately24% of the constructed nests were reused; this meansthat many females nested in cavities previously occu-pied by other bees.Expenditure of Maternal Time in Brood-Cell Pro-visioning and Construction. To construct and provi-sion a brood cell, one female spent 5 h 28 min, from0842 to 1410 hours. This period was divided in activ-ities executed inside (135 min) and outside (193 min)the nest (Fig. 2). To collect nesting material and pro-vision a single nest cell, this female made 30 ßights,which lasted from 64 s to 36 min 40 s. Brood cellconstruction can be divided into three stages (Fig. 2).Stage 1: Construction of Cell Walls. For 26 min, the

female collected and handled construction materials,which were composed of oily substance and vegetalÞbers. At the end of this period, the bee had coated thebottom and the wall of the cell (Fig. 2). For six ob-served bees, the average duration of the trips to collectconstruction materials and ßoral oils was 4min 34s

(range, 10 s to 18 min 26 s; N � 34) and 9 min 39 s(range, 45 s to 22 min 13s; N � 10), respectively.Stage 2: Larval Provisioning and Oviposition. Col-

lection and handling of larval food took the course of294 min, amounting to �90% of the construction timeof one brood cell. Brood cell provisioning was dividedbetween a phase of pollen collection (144 min) andnectar collection with almost the same duration (143min). The female made 16 pollen collection trips. Sixobserved females performed trips of, on average, 9 min26 s (N � 55; SD � 9 min 17 s) to obtain pollen.Although the duration of the pollen collection tripsand removal of pollen loads inside the nest was similar,the females spent much more time outside the nestduring the phase of nectar collection. After pressingthe pollen mass at the bottom of the cell, the femalemade some nectar collection trips and then laid heregg, which was immersed and vertically positioned ina nectar column.Stage 3: Cell Closure. After oviposition, the female

collected a white, Þbrous plant material to close thecell and exhibited the following behavioral sequence:she ßew in front of the blocks, walked around theentrance of the nest and the block, scraped her frontlegs against one another, liberated the collected ma-terial, and returned to the interior of the nest. She thenbegan cell closure and initiated the construction of thenext brood cell.

After having Þnished closure of the last brood cellof a nest, females collected material similar to that ofthe wall of the brood cell to construct a 3-mm-thickplug at the entrance. They then deposited oil trans-ported on their hind tibia and basitarsi. To do so, thefemales remained up to 2 min at the nest entrance andremoved the oil by rubbing the mid tibia downwardsagainst the oil-Þlled hind tibia and basitarsi in rapidmovements until a droplet of transparent yellowish oilwas transferred onto the nest plug. After manipulationof the oil with the metasoma, the transparent liquidturned opaque yellow, like mayonnaise. After 2 d, theoil had solidiÞed and formed a hard crust, protectingthe nest entrance.Nest Provisions. At both study sites, the larval pro-

visions of C. analiswere a homogeneous moist yellowpollen mass and a column of nectar (Fig. 1). At the

Table 1. Number of nests and brood cells of C. analis ob-tained in two types of trap-nests installed in an Acerola orchardduring 8 mo

Type of trap-nest No. nests No. cells Mean (range)

Solid block 17 63 3.8 (1Ð6)Observation nests 48 107 2.3 (1Ð5)

NESTMATERIAL

POLLEN NM

NECTAR NM

00:0005:0010:0015:0020:0025:0030:0035:00

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55

Activities

Dur

atio

n (m

in)

Time outside of the nest Time inside of the nest

Fig. 2. Activities of a C. analis female during brood cell construction and provisioning. The bee took 5 h 28 min to shelterand feed the Þrst larva of the nest.


Acerolandia site, the brood-cells contained, on aver-age, �2 million pollen grains and at the Aldeia site,�1.7 million grains (Table 2). At both sites and in allbrood cells, pollen grains of Acerola prevailed overpollen of other plant species, and eight of the 18 broodcells contained exclusively pollen grains of the fruitcrop. Median content of Acerola pollen grains was 96%at the Acerolandia site and 94% at the Aldeia site.

The remaining pollen grains belonged to two spe-cies of Solanum (Solanaceae) at Acerolandia site.These accounted for a maximum of 7.4% of the totalpollen grains in one brood cell (Fig. 3a). In Aldeia,with exception ofM. emarginata, the females collectedpollen of Þve other plant species, but in a proportionnever higher than 14%. These plants were two speciesof Solanum, one of Malvaceae and two plant specieswhose pollen grains were not identiÞed (Fig. 3b).

Discussion

C. analis: An Effective Flower-Constant Pollinator.Despite the common polylecty of the Centris speciesin general (Vogel 1974), females of C. analis showedremarkable Þdelity to Acerola when nesting in Acer-ola orchards or in an agroforestry environment with

Acerola plants and almost exclusively used pollen ofthis fruit crop to provision their brood cells. This issurprising, because in surveys of bees and their foodplants in native environments, females of C. analiswere recorded in pollen ßowers of numerous species(Aguiar et al. 2003). Furthermore, inside and in thevicinities of the commercial orchard, at least 21 speciesof pollen plants occurred (Schlindwein et al. 2006), allof which were largely ignored by C. analis females.This indicates the strong ßoral preference for Mal-pighia pollen by this Centris species.

In orchards of M. emarginata, pollen and ßoral oilare offered in high quantities and densities. This mayoptimize foraging in relation to energy investment andtime expenditure used for resource location, com-pared with more complex environments with re-sources sparsely distributed. A better cost-beneÞt re-lation in Acerola orchards thus makes the cultivatedplants more attractive for the Centris females. In stud-ies with Bombus terrestris (L.), for example, it wasshown that the duration of the foraging ßights of theworkers were much shorter in Þelds of Phacelia tan-acetifolia Benth., which offer abundant resources,than in environments with scarce resources (West-phal et al. 2006).

Sharing of pollination services between plants ofeconomic interest and co-ßowering wild plants maydiminish the productivity of the cultivated plant (Rou-bik 1995). Because of this, in many plantations, com-peting plants are removed, which leads to an impov-erished site with respect to plants and associatedpollinators. Due to the strong preference of C. analisfemales to M. emarginata ßowers, this practice is notnecessary, especially when the bees are reared insidethe orchards.

Table 2. Number of pollen grains stored in brood-cells of C.analis in trap-nests installed in an Acerola orchard and an agro-forest site

Study areaNo. pollen grains

Mean � SD Range

Acerola orchard(n � 7)

2,046,875 � 427,397.47 1,661,250Ð2,726,250

Agroforest site(n � 9)

1,749,000 � 160,804.62 1,620,000Ð2,002,500

0

20

40

60

80

100

1 2 3 4 5 6 7 8 9 10Brood cells

Pol

len

type

(%)

Malpighia emarginata Others

0

20

40

60

80

100

1 2 3 4 5 6 7 8

Pol

len

type

(%)

a-

b-

Fig. 3. Relative amount of pollen grains ofM. emarginata and other plant species used by females of C. analis to feed larvae.The analyzed trap-nests were installed inside an Acerola orchard (a) and in an agroforest environment. Other pollen grains aretwo species of Solanum (a) and in Þve species, including a Malvaceae, Solanum, and two nonidentiÞed pollen grains types (b).


However, the Acerola ßowers offer only ßoral oil andpollen to the bees. Therefore, nectar resources for adultbeesandfor larvaeshouldbemaintainedandevenaddedin the orchard. Vinson et al. (2006) measured that onebrood cell of C. analis averaged 86.0 �l of liquid thatconsists mainly of a solution of glucose and fructose. Inthe region of the plantation, ßowers of numerous plantspecies are nectar resources for these bees such as Cae-salpinia echinata Lam., Caesalpinia ferrea Mart. ex Tul.(Caesalpiniaceae), Duranta repens L. (Verbenaceae),several species of Ipomoea L. (Convolvulaceae), Tabe-buiaaurea(Silva Manso) Benth. & Hook. F. ex S. Moore,Tabebuia impetiginosa (Mart. ex DC.) Standl., Tecomastans (L.) H. B. & K. (Bignoniaceae), and BowdichiavirgilioidesKunth (Fabaceae) (Schlindwein et al. 2006).All these plants are easily grown, have a high ornamentalvalue and may be added in the surroundings of Acerolaplantations as nectar sources for the bees.

Besides C. analis, females of other CentridiniÑC.(Centris) aeneaLepeletier,C.(Centris)flavifrons(F.),C.(Hemisiella) tarsataSmith,C.(Melacentris)obsoletaLepeletier,C. (Ptilotopus) sponsa Smith,C. (Trachina)fuscata Lepeletier, C. (Trachina) longimana F., Epi-charis (Epicharana) flava (Friese), and E. (Epicharis)bicolor Smith are ßower visitors and pollinators ofAcerola orchards in the humid part of northeasternBrazil (Schlindwein et al. 2006). However, only C.tarsata is a cavity nesting species; females of the otherspecies build nests in the soil, and their managementin artiÞcial nests is not practicable.

In this humid region and under agricultural schemesof irrigation and pruning in the dry semiarid region ofthe caatinga, Acerola blooms throughout the wholeyear, providing pollen and oil for its ßoral visitors. Themultivoltine life cycle of C. analis enables the deliverof pollination services throughout the entire ßoweringperiod of the crop. The high ßower constancy to Ac-erola ßowers when nesting inside plantations, theirhigh pollinator effectiveness and the readily accep-tance of trap-nests by females make C. analis an ex-cellent candidate for a manageable pollinator in or-chards.Efficiency and Value of Pollination Service. A

ßower of M. emarginata contains, on average, 26,000pollen grains (Schlindwein et al. 2006). To rear onebee larva, a female of C. analis must collect, on aver-age, �2 million pollen grains of Acerola. This meansthat a female would have to collect all pollen grains of�75Ð80 ßowers of M. emarginata to complete onebrood cell. Flower visits of females of C. analis, how-ever, are shortÑ3.1 s, on average (Oliveira andSchlindwein 2003)Ñand they collect only a part of thepollen amount of one ßower during a single visit.Therefore, many more ßowers are visited by femalesto provision a brood cell with pollen. Considering thatpollen-collecting trips last, on average, 9.5 min, a fe-male visits hundreds of ßowers to feed a larva withpollen.Possibilities of Management of C. analis. The oc-

cupation of trap-nests by females ofC. analis in naturalhabitats of Brazil is known since �1980, the period ofthe Þrst studies with artiÞcial nests in this country,

which were made mainly to aid bee surveys and to getÞrst information about the natural history of solitarybee species (Serrano and Garofalo 1978; Garofalo et al.1989, 1993; Camillo et al. 1995; Pereira et al. 1999;Aguiar and Martins 2002).

Observation trap-nests, to our knowledge, are usedhere for the Þrst time in Brazil and showed to beefÞcient and an excellent tool to monitor the activitiesinside the nests and of the local abundance of trap-nesting pollinators. Although females ofC. analis haveequally occupied trap-nests of the two types, we rec-ommend compact trap-nests to rear these bees inorchards. Nests in these blocks showed a larger num-ber of brood-cells and reared offspring, as well as asmaller rate of parasitism. Furthermore, they are moreappropriate to be transported among or within or-chards.

The optimal diameters of the nesting cavities shouldbe considered in the search of an optimized model oftrap-nest for C. analis. Within the range of usefuldiameters, six to eight millimeters, all were equallyused by the nesting females.

The nesting activities of C. analis follow the se-quence: collection of plant material and ßoral oil,construction of the cell walls with this material, pollenand nectar collection, oviposition, and collection ofnesting material for cell closure. Through pollen anal-ysis, it is possible to quantify and characterize theresources indispensable for larval provisioning. Thisallows monitoring of the pollen use by females that arekept in an orchard by periodically controlling theßower constancy to the crop.

To manage the few solitary bee species commer-cially used for pollination, numerous studies werenecessary to improve and optimize their rationalrearing, particularly in commercial scale (Torchio1976, 1979, 1980, 1991b; Torchio and Tepedino 1980;Torchio and Asensio 1985; Rust and Torchio 1992;Bosch 1994a,b; Bosch et al. 2000, 2006; Bosch andKemp 2000, 2001, 2004, 2005; Buckner et al. 2004;Monzon et al. 2004; Guedot et al. 2006). To makecommercial use of C. analis possible, several studiesare necessary regarding immature development,emergence control of adults, methods to controlfungi, ants, and other predators, as well as clepto-parasites, such as Mesocheira bicolor (F.) (Apidae:Ericrocidini), and species of Coelioxys (Megachili-dae: Megachilini) and of Leucospis (Leucospidae).Furthermore, the optimal number of bees/trap-nests per area must be determined to achieve highfruit set, and the procedure must be established tointroduce occupied trap-nests to a new site.

Acknowledgments

Alcindo Lacerda and Dieter Kuntze generously permit-ted us to conduct Þeldwork on personal properties. Thecurrent study was performed in the context of the Inter-national Pollinator Initiative concern over the decline ofnative pollinators and the decline of their pollination ser-vices especially for cultivated plants and is also result of astimulus of the Brazilian Ministry of Environment, which


in the last decade is searching for methodologies for man-agement and sustainable use of native pollinators. We areespecially grateful to Jim Cane for the constructive crit-icism. The manuscript was substantially improved by thecomments of three anonymous reviewers. This study wassupported by the Brazilian Ministry of Environment (Pro-jeto de Conservacao e Utilizacao Sustentavel da Diver-sidade Biologica Brasileira, Banco Internacional para Re-construcao e Desenvolvimento/Global EnvironmentalFund, Ministerio de Meio Ambiente [PROBIO, BIRD/GEF, MMA], Conselho Nacional de Desenvolvimento Ci-entõÞco e Tecnologico). We were funded by the BrazilianResearch Council (Conselho Nacional de Desenvolvi-mento CientõÞco e Tecnologico).

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Received 10 December 2007; accepted 12 August 2008.


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