Stingless bees in applied pollination: practice and perspectives Ester Judith Slaa, Luis Alejandro Sánchez Chaves, Katia Sampaio Malagodi-Braga, Frouke Elisabeth Hofstede

To cite this version:

Ester Judith Slaa, Luis Alejandro Sánchez Chaves, Katia Sampaio Malagodi-Braga, Frouke Elisabeth Hofstede. Stingless bees in applied pollination: practice and perspectives. Apidologie, Springer Verlag, 2006, 37 (2), pp.293-315. ￿hal-00892203￿

HAL Id: hal-00892203 https://hal.archives-ouvertes.fr/hal-00892203 Submitted on 1 Jan 2006

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 37 (2006) 293–315 293 c INRA/DIB-AGIB/ EDP Sciences, 2006 DOI: 10.1051/apido:2006022 Review article

Stingless bees in applied pollination: practice and perspectives

Ester Judith Sa,b, Luis Alejandro S´ Cb, Katia Sampaio M-Bc, Frouke Elisabeth Hd

a Institute of Integrative and Comparative Biology and Centre for Biodiversity and Conservation, University of Leeds, LS2 9JT Leeds, UK b Centro de Investigaciones Apícolas Tropicales, Universidad Nacional, Costa Rica, Apartado postal 475-3000 Heredia, Costa Rica c Laboratório de Abelhas, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, n.321 CEP 05508-900 São Paulo, Brazil d Tropical Bee Research Unit, Behavioural Biology Department, Utrecht University, PO Box 80.086, 3508 TB Utrecht, The Netherlands

Received 17 October 2005 – revised 27 February 2006 – accepted 28 February 2006

Abstract – At present, numbers of both wild and managed bee colonies are declining rapidly, causing global concern for pollination services. Stingless bees play an important ecological role as pollinators of many wild plant species and seem good candidates for future alternatives in commercial pollination. This paper reviews the effectiveness of stingless bees as crop pollinators. Over the past six years the number of crops reported to be effectively pollinated by stingless bees has doubled, putting the total figure on 18 crops. Eleven stingless bee species across six genera have been found to forage effectively under enclosed condi- tions, indicating the potential of stingless bees as pollinators of greenhouse crops. The biological features that make stingless bees strong candidates for commercial pollination services are discussed, together with their present limitations. The effects of natural vegetation and wild bees on crop yield are reviewed, and make a strong case for habitat conservation.

agriculture / alternative pollinators / food crop / greenhouse / Meliponini

1. ECONOMIC IMPORTANCE bee species are known to be efficient and effec- OF POLLINATION tive pollinators of many crops (e.g. Freitas and IN COMMERCIALLY GROWN Paxton, 1998; Heard, 1999; Richards, 2001; CROPS Kremen et al., 2002). Nevertheless, the Euro- pean honeybee (Apis mellifera L.) is the sin- Most crop plants depend on pollination for gle most commonly used species in managed fruit and seed set. For many of these crops, pollination services, and the dependency of insects are the main pollination vector (with commercial crop yields on honeybee pollina- the main exception of grains, which are wind- tion is enormous everywhere. The economic or self-pollinated). It has been estimated that value of honeybees as agricultural pollinators about 30% of human food is derived from has been estimated for several countries (e.g. bee-pollinated crops (O’Toole, 1993 cited in ranging between $1.6 and $5.7 billion per year Kearns and Inouye, 1997). A wide variety of for the United States of America; Southwick and Southwick, 1992) and £137.8 million per year for selected crops in the United King- Corresponding author: E.J. Slaa, [email protected] dom (Carreck and Williams, 1998)), and far Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2006022 294 E.J. Slaa et al. exceeds their economic value as producers of and Inouye, 1997). When honeybees do not ef- honey, wax and other hive products (Carreck ficiently pollinate a given crop, it is probably and Williams, 1998). On a global scale, the to- economically beneficial to search for a better tal annual value of agricultural pollination has pollinator-plant match. It has been estimated been estimated at $200 billion (Kearns et al., that in the US alone, the commercial value of 1998). non-honeybee pollinators to crop yields may be as high as $6.7 billion per year (see Kearns et al., 1998). 2. COMMERCIAL POLLINATORS Over the last several decades the manage- ment of some other pollinators has been de- 2.1. Why look for new species? veloped which have proven to be much more efficient than the honeybee for certain crops. Recently, numbers of both managed and Examples include Nomia, Osmia, Megachile wild bees are declining rapidly, causing (for alfalfa), bumble bees (for crops of the global concern for pollination services (e.g. Solanaceae family, e.g. tomatoes), flies, and Watanabe, 1994; Buchmann and Nabhan, more recently, stingless bees (Torchio, 1987; 1996; Kearns and Inouye, 1997; Nabhan et al., Free, 1993; Heard, 1999). The best-known ex- 1998; Cane and Tepedino, 2001; UNEP, 2002; ample is probably the success-story of the Villanueva et al., 2005; see Ghazoul (2005a, b) commercial use of bumble bees for the pol- and Steffan-Dewenter et al. (2005) for a lination of tomatoes (see Free, 1993). In discussion on this topic). Threats include habi- tomato flowers, as a member of the Solanaceae tat destruction or alteration, overuse of pesti- family, pollen is released through vibration cides, parasites and diseases, and the introduc- (‘buzzing’) of their poricidal anthers. Bees tion of alien species (Buchmann and Nabhan, produce these vibrations by shivering the in- 1996; Kearns and Inouye, 1997; Kremen et al., direct flight muscles, and anther buzzing has 2002). Management of honeybee hives is been observed in many bee species, includ- handicapped worldwide by infectious diseases ing bumble bees and stingless bees of the and parasites such as varroa mites (Varroa genus Melipona. Not all bee genera how- destructor), American Foul Brood, (Bacillus ever seem to show this behaviour; e.g. honey- larvae), and Chalk brood (Ascosphaera apis) bees and stingless bees other than Melipona (Watanabe, 1994). In response to the world- are not buzz-pollinators (Buchmann, 1983). wide decline of pollinator populations and pol- Greenhouse tomato flowers were commonly linator diversity, the “Conference of the Par- pollinated by hand using an electrical vibra- ties to the Convention on Biological Diversity” tor, but are now almost all successfully polli- established an International Initiative for the nated by commercially bred bumble bees (see Conservation and Sustainable use of Pollina- Free, 1993). In the UK, the total value of bee tors in 2000. One of the main aims of this Ini- pollination was estimated to exceed £200 mil- tiative is to “promote the [...] sustainable use of lion per annum, of which bumble bee polli- pollinator diversity in agriculture and related nation in green houses accounted for nearly ecosystems” (UNEP, 2002). Diversification of 15% (£29.80 million) (Carreck and Williams, crop pollinators would help to achieve polli- 1998). nation services when the commonly used pol- A negative side to such a success story is the linator (specifically honeybees for most crops risk of establishment of exotic pollinators in nowadays) is not available in sufficient num- non-native areas. Both bumble bees and soli- bers. tary bees used for pollination services have In addition, honeybees are not always the been exported to different parts of the world most efficient pollinators due to various fac- to enhance crop pollination, and in many cases tors, e.g. a miss-match in body size and flower established successfully. Introduction of exotic size, low nectar production and specialized bee species causes general concern because of pollen release mechanisms in some plants, in- its potentially negative effects on both native cluding those with poridical anthers (Kearns pollinators and plants (see Goulson, 2003). Stingless bees in applied pollination 295

To avoid introduction of exotic flower visi- vidually, like bumble bees) (e.g. Roubik, 1992; tors, some researchers have tested native bum- Michener, 2000; Slaa, 2003; Slaa et al., 2003a; ble bee species for pollination services (see Biesmeijer and Slaa, 2004; Nieh, 2004). These Kaftanoglu, 2000 (Turkey); Mah et al., 2000 inter-specific differences allow for selection of (Korea)). the most appropriate stingless bee for a given Besides physical properties hindering effi- crop species and crop breeding system (green- cient pollination, honeybees may have other house, open field, etc.). drawbacks in pollination services. First, hon- Commercial pollination with stingless bees eybee colonies have seasonal cycles with has hardly been developed yet, and some ob- a long inactive period in temperate regions served potential problems include domestica- which makes them less suitable for the pol- tion, colony reproduction and mass rearing, lination of off-season products. Second, hon- which are discussed in more detail in the ‘gen- eybees have a functional sting, and although eral considerations’ section at the end of this the tendency to sting is quite low in several paper. Nevertheless, several biological fea- breeds of European honeybees, it may still tures make stingless bees strong candidates for cause problems for crop workers who are aller- commercial pollination services, as outlined gic. In addition, all honeybees present nowa- below. days in the Neotropics are Africanized (e.g. Stingless bees are true generalists, collect- Caron, 2001; Schneider et al., 2004), which re- ing nectar and pollen from a vast array of quires additional safety measures due to their plants (Heithaus, 1979a, b; Roubik, 1989; aggressive nest defense (Winston, 1992). This Ramalho et al., 1990; Biesmeijer et al., 2005). is especially a problem in enclosed areas such A single species can collect floral rewards as greenhouses, and in fields close to human or from up to 100 plant species on a yearly basis animal establishments. (Heithaus, 1979b; Cortopassi-Laurino, 1982). An economic drawback to the commercial Nevertheless, individuals tend to specialize on use of bumble bees is that colonies die after a single floral species for a certain amount of reproduction. New hives need to be bought re- time, a behavioural trait commonly referred to peatedly, making this pollinator service rather as flower constancy (Slaa, 2003; Slaa et al., expensive, especially for small-scale farmers 2003b). Flower constancy leads to assortative in developing countries. mating of the visited plants and therefore to more efficient pollination (e.g. Darwin, 1876; Thomson, 1983; Campbell and Motten, 1985). 2.2. Why stingless bees? Less pollen is wasted due to selective transfer within a species, and less non-specific pollen Good candidates for future alternatives in reaches the stigma, preventing pollen compe- commercial pollination can be found in the tition and stigma clogging (Waser, 1983). The diverse group of stingless bees (Meliponini) fact that stingless bees are generalists at the (Rindfleisch, 1980; Roubik, 1995b; Heard, colony level but specialists at the individual 1999; Sommeijer and de Ruijter, 2000). Sting- level makes them theoretically good pollina- less bees comprise a highly diverse and abun- tors. Indeed, stingless bees are considered im- dant group of eusocial bees that inhabit the portant pollinators of the native flora in tropi- tropical and subtropical parts of the world. cal and subtropical parts of the world, and they Stingless bees form perennial colonies from have been found to contribute to the pollina- which they forage year-round. Worldwide sev- tion of many crops and wild plants (see Heard, eral hundred species exist, which differ signifi- 1999 for a review). cantly in colony size (from a few dozen to tens Several species of stingless bees have of thousands of individuals), body size (from 2 been domesticated for centuries, especially to 14 mm; compare to 12 mm for honeybees), by the Maya people in Latin America (see and foraging strategy (some species recruit Weaver and Weaver, 1981; Crane, 1983, 1992; nestmates to high quality food sources, like Cortopassi-Laurino et al., 2006, this issue). honeybees, whereas others forage mainly indi- Nowadays, a number of papers on the use of 296 E.J. Slaa et al. rational hive boxes for the keeping of sting- they suffer from fewer diseases, pests and less bees is available, and hive management parasites than the honeybee (Nogueira-Neto, is fairly straightforward for certain species 1997), which simplifies colony management. (but see below). Although stingless bees nat- While not all species can be used for com- urally only occur in the tropics and subtrop- mercial pollination (e.g. obligate parasites of ics, they have also been successfully exported other stingless bees, species with restrictive and maintained indoors in colder climates, nesting habitats, extremely defensive behavior using temperature controlled rooms and/or or destructive use of flowers), several species hives (e.g. Utrecht University, The Nether- are good candidates as commercial pollinators lands; Japan (Maeta et al., 1992; Amano et al., because they can easily be kept in hives, have 2000; Amano, 2004, pers. comm.)). sufficient numbers of workers per hive and are Besides the fact that many species of stin- non-aggressive (Roubik, 1995b; Heard, 1999). gless bees can be managed in hives, several The diversity of the group indicates that they other features make this group very adequate may be of use to pollinate a wide range of for pollination services. First, colonies don’t crops and ornamental plants. die after reproducing, unlike Bombus,and colonies are naturally long-lived (Slaa, 2006). This makes it relatively easy to keep individual 3. CROPS POLLINATED hives for long periods of time (up to 60 years: BY STINGLESS BEES Murillo, 1984). Second, they lack a functional sting, which makes them especially suitable for pollination of crops that are cultivated in The first detailed review on the role of stin- inhabited areas and in enclosures such as cages gless bees in crop pollination appeared in 1999 and greenhouses. In Costa Rica, for exam- by Tim Heard. Heard (1999) reported that stin- ple, many seed producing companies grow or- gless bees are effective and important pollina- namental plants in large netted, insect proof, tors of nine crops, and that they contribute to cages. They have a high demand for pollina- pollination in ∼60 other species out of the ∼90 tors, but because all honeybees are African- crop species they were found visiting. Over ised, and hence more defensive, honeybees are the past years, several new studies on stingless hardly used for pollination in such enclosures. bee pollination appeared (Tab. I). After the re- In such cases, stingless bees might provide a view by Heard in 1999 there is a clear trend to- solution (see Slaa et al., 2000a, b; Sánchez wards a more experimental approach using en- et al., 2002). Third, many stingless bee species closures such as bags, cages and greenhouses have proven to forage well in enclosed areas (cases 13–17 Tab. I). (see Tabs. I and V), and under adequate clima- In the sections below a summary of each tological conditions they forage year-round. crop is given, using both published and unpub- This makes them especially suitable for off- lished data. Only the studies that appeared af- season production of crops in green houses. ter 1999 are included. For a review of previous Most species of stingless bees have a foraging studies see Heard (1999). range smaller than that of the honeybee, which may enhance foraging efficiency in confined spaces (Visscher and Seeley, 1982; Seeley, 3.1. Crops effectively pollinated 1985; Katayama, 1987; Kakutani et al., 1993). by stingless bees Fourth, because most stingless bees cannot survive cold winters, there is little risk of inva- sion when importing stingless bees to temper- Coffea sp., Rubiaceae ate climates. Note however that some species Coffee is one of the most economically im- do live where it occasionally freezes, and com- portant crops, but its pollination requirements bined with global warming these species might are not well understood. The two most impor- become feral when introduced outside the tant species are C. arabica and C. canephora tropics of Capricorn and Cancer. Furthermore, (Free, 1993; Roubik, 2002a). Stingless bees in applied pollination 297

Table I. Crops effectively pollinated by stingless bees. Studies 1–12 report on pollination under field con- ditions, studies 13–18 report on pollination under enclosed conditions. Studies 1–9 are reviewed in Heard (1999).

Scientific name Common name Stingless bee Reference Crops reported by Heard (1999) 1 Bixa orellana Annato Melipona melanoventer See Heard (1999) Melipona fuliginosa 2 Myrciaria dubia Camu-camu See Heard (1999) 3 Sechium edule Chayote Trigona corvina, See Heard (1999) Partamona cupira 4 Cocos nucifera Coconut See Heard (1999) 5 Averrhoa carambola Carambola Trigona thoracica See Heard (1999) 6 Macadamia intergrifolia Macadamia Trigona spp. See Heard (1999) 7 Mangifera indica Mango Trigona spp. See Heard (1999) 8 Poumora cecropiaefolia Mapati See Heard (1999) 9 Theobroma grandiflorum Cupuaçu Trigona lurida See Heard (1999)

Studies reported after 1999 10 Coffea arabica Coffee Trigona (Lepidotrigona) Klein et al. (2003a) terminata 11 Coffea canephora Coffee Trigona (Lepidotrigona) Klein et al. (2003b) terminata 12 Persea americana Avocado Trigona nigra, Can-Alonso et al. (2005) Nannotrigona perilampoides Geotrigona acapulconis, Ish-Am et al. (1999) Trigona nigerrima, Partamona bilineata, Nannotrigona perilampoides, Scaptotrigona pectoralis, Trigona nigra, Scaptotrigona mexicana, Trigona fulviventris, Plebeia frontalis, 13 Fragaria × ananassa Strawberry Plebeia tobagoensis Asiko (2004); Lalama (2001) Trigona minangkabau Kakutani et al. (1993) Nannotrigona testaceicornis Maeta et al. (1992) Tetragonisca angustula Malagodi-Braga and Kleinert (2004) 14 Nephelium lappaceum Rambutan Scaptotrigona mexicana + Rabanales et al. Tetragonisca angustula (unpubl. data) 15 Capsicum annuum Sweet pepper Melipona favosa Meeuwsen (2000) Melipona subnitida Cruz et al. (2004) Trigona carbonaria Occhiuzzi (2000) Melipona favosa Meeuwsen (2000) 16 Lycopersicon esculentum Tomato Melipona quadrifasciata Santos et al. (2004a); Sarto et al. (2005) Nannotrigona perilampoides Cauich et al. (2004) 17 Cucumis sativus Cucumber Scaptotrigona aff. depilis, Santos et al. (2004b) Nannotrigona testaceicornis 18 Salvia farinacea Nannotrigona perilampoides, Slaa et al. (2000a, b) Tetragonisca angustula 298 E.J. Slaa et al.

Coffea arabica among the species, with Trigona (Lepidotrig- C. arabica is the most common coffee ona) terminata being the most efficient sting- species and is cultivated throughout the trop- less bee pollinator (84% fruit set). As a group, ics. Coffee flowers are very attractive to a wide the less abundant solitary bees were more ef- array of insects including honeybees and stin- ficient than the more abundant social bees gless bees (Heard, 1999; Klein et al., 2003a). (Klein et al., 2003b). Although C. arabica is largely self-fertile, and Avocado, Persea americana (Lauraceae) a relatively large fruit set may be obtained Avocado originated in Central America, without any pollinators, several studies indi- ff where honeybees are not native. Two recent cate that bee pollination increases co ee pro- studies have shown that stingless bees are fre- duction (Free, 1993). Recently Roubik (2002a, quent visitors and efficient pollinators of avo- b) found that in Panama bee pollination re- cado flowers in Mexico (Ish-Am et al., 1999; sulted in a higher fruit set and heavier ma- Can-Alonso et al., 2005). Ish-Am et al. (1999) ture fruits compared to bagged branches from conducted their study mainly outside commer- which pollinators were excluded, and con- cial orchards because the application of in- cluded that bees consistently controlled over secticides highly reduced insect populations 36% of the total coffee production. Klein et al. ff in commercial orchards. Based on species (2003a) found that co ee fruit set in Indonesia abundance on the flowers, foraging behaviour, was higher in areas with a high bee diversity and number of pollen grains on the insect’s (approximately 90% fruit set) compared to ar- body zones that came in contact with the av- eas with a low diversity (approximately 60% ocado stigma, they concluded that eight to 10 fruit set), and concluded that bee diversity, not species of stingless bees were effective pol- abundance, was important for pollination suc- linators of avocado, together with the Mex- cess. Using bagging experiments, they found ican honey wasp. Can-Alonso et al. (2005), that 15 bee species, including four Trigona working in commercial orchards, found that A. species, contributed to the pollination of this ffi mellifera and Trigona nigra carried compara- shrub. However, pollination e ciency (fruit ble amounts of avocado pollen grains on their set after a single flower visit) varied among bodies, but that this number was significantly the species, with Trigona (Lepidotrigona) ter- ffi less on Nannotrigona perilampoides. They too minata being the most e cient stingless bee concluded that native stingless bees are poten- pollinator (80% fruit set). As a group, the less tially efficient pollinators of this crop. abundant solitary bees were more efficient pol- linators than the more abundant social bees Strawberry, Fragaria × ananassa (honeybees and stingless bees). (Rosaceae) Most strawberry cultivars are herma- ff Co ea canephora phrodite and self-fertile, but cultivars may vary C. canephora is an important cash crop in highly in their degree of self-compatibility many tropical countries (Willmer and Stone, due to differences in spatial segregation of 1989). Flowers are self-sterile and wind was anthers and stigmata and temporal separa- long believed to be the main pollinating vec- tion between anther maturation and stigma tor (see Free, 1993). However, several stud- receptivity (Free, 1993; Zebrowska, 1998; ies have now indicated that insects do make Malagodi-Braga, 2002). Strawberry flowers a considerable contribution to its pollination, can be pollinated by a wide range of vec- with the main visitors being bees (Willmer and tors, such as solitary bees, flies, and even wind Stone, 1989; Klein et al., 2003b, c). In Indone- (Free, 1993), although these are not (yet) used sia, fruit set increased with both abundance in commercial strawberry production. Honey- and diversity of flower visiting bees (from ap- bees are often used in greenhouses in Japan proximately 70% to 95% fruit set). Honey- and the UK, although they might not be the op- bees, solitary bees and stingless bees were all timal pollinator for strawberries under green- effective pollinators of this shrub. As with C. house conditions (Katayama, 1987; Kakutani arabica, pollination efficiency differed highly et al., 1993). McGregor (1976) reports that Stingless bees in applied pollination 299

100% 100% 90% 90% 80% 80% 70% 70% 60% SQ SQ 50% 60% 1st 1st 40% 50% 2nd 2nd 3rd 30% 3rd 40% no fruits 20% 30% 10% 20% 0% control Am control Pt 10% (n=197) (n=544) (n=360) (n=721) 0% Species Am Pt Am Pt Am Pt (n=48) (n=109) (n=141) (n=74) (n=33) (n=62)

Figure 1. Effect of bee pollination on straw- 0 1 5 berry quality. Strawberry fruits were classified into # visits/flower four quality categories (categories derived from Figure 2. Effect of controlled flower visits on straw- The Greenery International qualification for straw- berry quality. Strawberry fruits were classified into berry: SQ: super quality, perfect cone, fruit diam- four quality categories (categories derived from eter > 27 mm; 1st: light deformation, fruit diame- The Greenery International qualification for straw- ter > 22 mm; 2nd: some deformation, fruit diameter berry: SQ: super quality, perfect cone, fruit diam- > 18 mm; 3rd: Industry, deformed, fruit diameter eter > 27 mm; 1st: light deformation, fruit diame- < 17 mm). Control: no bees, Am: Apis mellifera, ter > 22 mm; 2nd: some deformation, fruit diameter Pt: Plebeia tobagoensis. After Lalama (2001). > 18 mm; 3rd: Industry, deformed, fruit diameter < 17 mm). Bees were allowed controlled visits to strawberry plants do not seem to be very 2-day old flowers that were previously bagged to attractive to honeybees, and colonies used prevent destructive behaviour to the buds. Am: A. for strawberry pollination in greenhouses in mellifera, Pt: P. tobagoensis. After Asiko, 2004. Japan decreased in population size (Kakutani et al., 1993). However, in commercial straw- aging behaviour by entering closed flower berry fields in Brazil flowers yielded a lot of buds (stigma not yet receptive) and biting the pollen and nectar and were abundantly visited anthers (which haven’t released pollen yet) by honeybees and stingless bees (Malagodi- with their mandibles (Lalama, 2001). This be- Braga, pers. obs.). Since the pollination studies haviour could have been caused by the rela- in Japan (Kakutani et al., 1993; Maeta et al., tively low numbers of flowers available, but 1992; see Heard, 1999), three more studies on more observations are needed to confirm this. strawberry pollination with stingless bees have When buds were protected from the destruc- appeared. tive behaviour through bagging before flower In The Netherlands imported Plebeia toba- opening, P. tobagoensis did have a positive goensis from Tobago, West-Indies, and hon- effect on strawberry quality (Fig. 2; Asiko, eybees were tested for their pollination effec- 2004). Five bee visits resulted in significantly tiveness and efficiency under greenhouse con- higher quality fruits than no visits for both ditions (each compartment 9 × 6 × 4m, honeybees and stingless bees (Chi-squared one colony for 100 plants; Hofstede, unpubl. test, P < 0.03, without significant differences data). When the bees were able to forage between the two species (Chi-squared test, P = freely on the strawberry plants (var. Elan), 0.7; Fig. 2). Fruit set tended to be higher after 5 honeybees had a significant positive effect on bee visits than without visitation, but this was strawberry quality (Fig. 1, Mann-Whitney test, not significant (Chi-squared test, P = 0.14 for P < 0.005), and fruit quantity was some- A. mellifera and P = 0.07 for P. tobagoensis; what higher (58% fruit set versus 48% with- Fig. 2). out bees, Student-t test, F = 1.84, P = In Sao Paulo, Brazil, the only strawberry 0.063). P. tobagoensis hadnoeffect on the study site so far where stingless bees are na- number of fruits produced (74% versus 75% tive, five stingless bee species were initially without bees, Mann-Whitney test, P = 0.8), tested for their suitability as strawberry polli- but had a negative effect on strawberry qual- nators in greenhouses (8 × 25 m): Nannotrig- ity (Fig. 1, Mann-Whitney test, P < 0.005). ona testaceicornis, Tetragonisca angustula, P. tobagoensis showed destructive pollen for- Schwarziana quadripunctata, Scaptotrigona 300 E.J. Slaa et al.

Table II. The effect of T. angustula pollination on strawberry (‘Sweet Charlie’ cultivar) production in greenhouses. Given are the mean±SD for various fruit measurements. Each greenhouse contained either one colony of T. angustula or no bee colonies (control). In the latter treatment the parcels were covered to prevent flower visitation by bees. After Malagodi-Braga, 2002.

T. angustula control T-test Fruit number 490 ± 48 519 ± 84 NS % deformed fruit 6.9 ± 2.250.1 ± 12.9t= 15.1, df = 40, P = 0.0001 Fruit weight (g) 9.6 ± 0.78.4 ± 1.2t= 3.9, df = 40, P = 0.0003 bipunctata and Trigona spinipes (Malagodi- fruits (by 86%) and yielding a significant in- Braga, 2002). Two species, S. bipunctata crease in strawberry weight (by 14%) com- and S. quadripunctata, did not forage under pared to the control (Tab. II). The relatively greenhouse conditions, and the other species high fruit production in the control was con- showed a reduction in their daily foraging sidered a result of selfing (pollen fall caused activity inside the greenhouse, despite re- by gravity and human action during the crop source availability and favourable values of handling, Malagodi-Braga, 2002). This indi- air temperature and relative humidity. Among cates that although fruit set in the ‘Sweet Char- all species T. angustula was remarkable for lie’ cultivar does not require additional pol- its relatively quick adaptation and the ability linators, out-crossing through bee pollination to keep satisfactory internal colony condi- greatly enhances fruit quality. tions (continuing cell construction and ovipo- sition, maintaining their honey pots and stor- Rambutan, Nephelium lappaceum ing pollen of strawberry flowers), even with (Sapindaceae) frequent removals and introductions in green- houses (Malagodi-Braga, 2002). T. angustula Rambutan has separate male and was tested for its pollination effectiveness hermaphrodite trees but is considered to using two different strawberry cultivars un- be functionally dioecious, with hermaphrodite der greenhouse conditions. Despite their small flowers having non-functional anthers (Free, size (about 4.5 mm in length), T. angustula 1993). This species is native to Southeast was found to be an effective pollinator of Asia, where fruit set under natural conditions both the ‘Oso Grande’ cultivar (Malagodi- was found to be 1% (Free, 1993). Heard Braga and Kleinert, 2004) and the ‘Sweet (1999) already reported that flowers in Asia Charlie’ cultivar (Malagodi-Braga, 2002). One are visited by several species of stingless bees, colony, allowed to forage freely in a green- which are potential pollinators. Rambutan house with 1350 strawberry plants of the ‘Oso is commercially grown in the Neotropics, Grande’ cultivar, resulted in nearly 100% of and Rabanales and co-workers (unpublished primary flowers developing into marketable document) studied pollination and fruit set (well-shaped) fruits, compared to 88% for in a commercial ‘female’ rambutan orchard open pollination in the field, and <20% for (7 ha, 1000 trees) in Chiapas, Mexico. They bagged flowers. Strawberry fresh weight was recorded flower visitors and compared fruit set also markedly higher after pollination by T. an- under three treatments: (1) open pollination gustula (41% increase compared to open pol- conditions, (2) bagged conditions (panicles linated plants) (Malagodi-Braga and Kleinert, bagged, all flower visitors < 1 mm excluded), 2004). and (3) ‘induced’ pollinator conditions, where In another pollination experiment using the a cage was placed over a tree. Two stingless ‘Sweet Charlie’ cultivar, a single colony of bee colonies were placed in the cage; one T. angustula was sufficient to pollinate 1 350 Scaptotrigona mexicana and one T. angustula ‘Sweet Charlie’ plants, reducing significantly colony. This last treatment resulted in obligate and drastically the percentage of misshapen geitonogamy. Stingless bees in applied pollination 301

Most flowers were hermaphrodite, but only angustula. In a greenhouse in The Nether- approximately 5% of those actually shed lands, T. angustula mainly visited the flow- pollen. Flowers were mainly visited by bees, ers for nectar, during which no contact was including several species of stingless bees, made with the stigma and therefore no pol- but were rarely visited by honeybees. The lination occurred (Kuyhor, 2001). Using the most common flower visitor was S. mexicana. same settings, Meeuwsen (2000) reports that Mature fruit set was highest under open pol- both Melipona favosa and honeybees (both lination conditions and induced pollination species one colony for 25 potted plants, each conditions (17–23%). Mature fruit set un- compartment 9 × 6 × 4 m) significantly in- der bagged conditions was only 2–3%, thus creased the number of fruits/plant compared the presence of pollinators increased fruit to the control (no bees present). However, no set by nearly 10-fold. Fruit mass was sig- numbers of flower frequency in the differ- nificantly higher under induced conditions ent compartments were given, making it dif- (geitonogamy) compared to open pollination ficult to draw conclusions on pollinator effec- where cross-pollination was possible. tiveness. In Brazil, Cruz (2003); Cruz et al. S. mexicana hives are now used to polli- (2004, 2005) studied the pollination effective- nate rambutan at this orchard, and fruit pro- ness of M. subnitida under greenhouse con- duction has increased significantly (Roubik, ditions (83 m2), using two colonies for a to- pers. comm.). tal of 153 sweet pepper plants. They had four Sweet pepper, Capsicum annuum treatments: hand pollination (auto-pollination (Solanaceae) and cross pollination), pollination by M. sub- Although many Solanaceae species have nitida, and the control (no pollinators – flow- flowers with poricidal anthers, C. annuum ers bagged for 48 h). Although fruit set did not ff does not, and does therefore not require buzz- di er among the treatments, M. subnitida sig- pollination. Flowers are pollinated through nificantly increased fruit weight (by 30%) and spontaneous selfing, although outcrossing may number of seeds per fruit (by 86%) compared occur because the stigma is often receptive be- to the control. Bee pollination did not signifi- ff fore anthers dehisce (Free, 1993). Honeybee cantly di er from hand pollination in terms of pollination can increase fruit size, seed num- fruit weight and seed set. In addition, pollina- ber, and fruit shape (Ruijter et al., 1991 cited tion with M. subnitida resulted in significantly in Free, 1993). At the time of the review by less deformed fruits compared to the control Heard (1999) various species of stingless bees (65% decrease). Interestingly, auto-pollination were known to visit the flowers, but their polli- resulted in as much deformed fruits as the nation potential had not been confirmed. Since control, whereas cross-pollination showed the then, three species of stingless bees have been same reduction in deformed fruits as bee polli- reported as effective pollinators. nation. This clearly shows the value of bees as Occhiuzzi (2000) reported that Trigona car- cross pollinators in selfing crops. bonaria effectively pollinated sweet pepper Tomato, Lycopersicon esculentum under glass greenhouse conditions in Aus- (Solanaceae) tralia. Fruit weight had increased by 11% and Tomato flowers are self-compatible but number of seeds/fruit by 34% compared to need animal or wind pollination to set fruit crops that were not pollinated by bees. On- (Free, 1993). Nectar production is generally going research by Greco confirms the effec- low, and pollen is released from poricidal an- tiveness of T. carbonaria as a pollinator of thers upon vibration. Tomato is one of the most sweet pepper, but also shows that the small widely grown vegetable crops in the world, Austroplebeia australis is not an effective pol- and is commonly produced in greenhouses linator of this plant (Greco, pers. comm.). (Benton Jones, 1998). Although commercially Roubik (1995a) already expected that smaller bred Bombus terrestris effectively pollinates bees would not be effective pollinators of greenhouse tomatoes, import of this species sweet pepper, and this has now also been con- to areas where it is not native causes gen- firmed for the small stingless bee Tetragonisca eral concern. B. terrestris already successfully 302 E.J. Slaa et al. established in Israel, New Zealand, Japan and in treatments of the non-pollinated plants (in- Tasmania, and several studies have indicated florescences bagged versus flowers tagged) is the negative impact of invasive bumble bees unknown. on the native pollinator fauna (Hingston and Cucumber, Cucumis sativus McQuillan, 1999; Goulson, 2003; Morales (Cucurbitaceaea) and Aizen, 2004). It seems logical to nar- row the search for effective tomato pollina- In Yucatán, Mexico, Partamona bilineata tors to species that can buzz-pollinate these is a frequent visitor of cucumber (Meléndez- flowers, and Melipona species seem good can- Ramirez et al., 2002). Santos et al. (2004b) reported that Scaptotrigona aff. depilis and didates. Two studies have reported on the pol- ff lination effectiveness of Melipona quadrifasci- N. testaceicornis e ectively pollinated green- ata for tomato grown in greenhouses in Brazil. house cucumber in Brazil, resulting in a higher Sarto et al. (2005) found that pollination of fruit production, higher fruit weight and a tomato (var. Rodas) by M. quadrifasciata (six higher percentage of perfect fruits compared to colonies for 700 plants in a 234 m2 plastic the control, where no pollinators were present. greenhouse, 3 m high) resulted in equal fruit Salvia farinacea and Salvia splendens quality (size and shape) compared to hand pol- (Labiatae) lination or bee plus hand pollination. How- So far, Salvia is the only ornamental plant ever, bee pollinated fruits contained 11% less for which stingless bee pollination has been seed compared to hand pollination, possibly studied. In Costa Rica, Salvia is an important due to the low temporal overlap in foraging plant for many seed companies that often grow activity and stigma receptivity. Santos et al. it in large netted cages to avoid hybridization. (2004a) compared pollination effectiveness of At such a company, T. angustula, N. perilam- M. quadrifasciata and Apis mellifera (each poides and A. mellifera were tested for polli- 2 species in a 86 m greenhouse), and found that nation efficiency and effectiveness of S. fari- tomatoes were bigger, heavier and had more nacea in netted cages (6 × 3 × 3 m). Pollina- seeds following pollination by M. quadrifasci- tion efficiency, expressed as seed set per unit of ata compared to A. mellifera. visitation rate, did not differ among the three Cauich et al. (2004) reported on the pollina- species, and all species produced good quality tion efficiency of N. perilampoides on green- seeds. Because foraging activity was highest in house tomatoes (var. Maya) in Subtropical A. mellifera, honeybee pollination yielded the México. Although this small stingless bee highest seed set compared to stingless bee pol- species is not a buzz-pollinator, it effectively lination (Slaa et al., 2000a, b). An increase in pollinated tomato plants grown in netted cages stingless bee density could potentially increase (4 × 4 × 3.5 m, one colony for 40 plants). Pol- yields, and stingless bees seem a valuable op- lination by N. perilampoides wasaseffective tion as pollinators of S. farinacea in enclo- as mechanical vibration in terms of percent- sures. S. farinacea was also commonly visited age fruit set, number of seeds per fruit and by Partamona orizabaensis and Trigona ful- fruit weight. However, of tomato flowers that viventris, but both species would be difficult to did not receive any pollination treatment more breed commercially as T. fulviventris nests in than half did set fruit. Fruits produced without the ground and P. orizabaensis is often found a pollination treatment had significantly less in termite nests and defends the nest quite ag- seeds than fruits produced after mechanical gressively. vibration or bee pollination, but fruit weight Salvia splendens has significantly larger did not significantly differ among the treat- flowers than S. farinacea, and was not ef- ments. This finding is in contrast to the study fectively pollinated by T. angustula, due to by Sarto et al. (2005), where tomato flowers its small body size in relation to flower size without vibration did not set fruit. Whether (Sánchez et al., 2002). Trigona fuscipennis and this discrepancy is due to differences in culti- N. perilampoides did not forage on these flow- vars, differences in housing conditions (plas- ers when placed in a netted cage (6×3×2.5m, tic house versus netted cage), or differences Bustamante, 1998). Flowers were visited Stingless bees in applied pollination 303 by several other species of stingless bees Table III. Relative attractiveness of various including Geotrigona sp. and Partamona sp. vegetable crops to Nannotrigona perilampoides, (Picado, 2000), but those are probably not Tetragonisca angustula, and Apis mellifera. For good candidates for commercial pollination each bee species the total number of observed vis- services because of their restrictive nesting its, the total number of plants present in the cage habits, and may be too small to be effective and the percentage relative preference (Chesson, pollinators. 1978) is given. After Fonseca and Picado, 2000. ∗ Cauliflower plants in the cage with T. angustula 3.2. Crops visited and occasionally or were attacked by Plutella xilostella, preventing vis- partially pollinated by stingless bees itation observations and seed count. N. perilampoides T. angustulaA. mellifera Calamondin, Citrus mitis (Rutaceae) # visits 523 159 1963 Citrus mitis is a miniature orange, widely # plants 65 67 59 grown as an ornamental house pot plant. The Broccoli 3 14 18 flowers are self-fertile and require no cross- Rape 2 33 9 ∗ pollination (Morton, 1987). Cervancia and Cauliflower 015 Endive 38 0 39 Manila (2000) studied the pollination of Cala- Chicory 12 3 12 mondin in the Philippines. Bagged inflores- Leek 13 49 4 cences did not set fruit (0.001% fruit set), Carrot 33 04 whereas fruit set in unbagged inflorescences was 2%. The stingless bee Trigona biro was observed to visit the flowers, along with Apis was compared in greenhouse compartments × × − cerana, A. mellifera,andXylocopa spp. The (8 6 3 5 m, 25 potted plants per com- activity of floral visitors was synchronized partment) using a colony of Tetragonisca an- with anthesis, which indicates their potential gustula, a colony of honeybees, or no bees role as pollinators. (Meeuwsen, 2000). The number of pods per plant was significantly higher in the com- Cucurbit crops (Cucurbitaceae) partments with T. angustula and honeybees Meléndez-Raminez et al. (2002) recorded compared to the control (6.6 and 9 time in- the bee visitors of pumpkin (Cucurbita crease respectively), without significant dif- moschata), cucumber (Cucumis sativus), ferences between the two bee species. How- melon (Cucumis melo) and watermelon ever, no numbers of flower frequency in the (Citrullus lanatus), on 14 sites in Yucatan, different compartments were given, making Mexico. These crops were found to be visited it difficult to draw conclusions on pollinator by 58 species of bees. Partamona bilineata effectiveness. was the second most dominant species and Nevertheless, behavioural observations in- Trigona fulviventris ranked fifth. The other dicate that although T. angustula is able to pol- stingless bee visitors were N. perilampoides, linate radish, it might not the most effective Trigona nigra, Cephalotrigona zexmeniae, agent. T. angustula only touched the stigma Melipona beecheii and occasionally Plebeia during pollen visits; nectar was extracted from frontalis and Scaptotrigona pectoralis.The the side of the flower, probably because of its authors conclude that P. bilineata is a regional small body size in relation to flower size. In pollinator of watermelon and pumpkin due addition, T. angustula visited the radish flow- to its ‘high abundance, frequent presence ers only sporadically for pollen (< 5% of all and observed contacts with female and male visits) (Thai, 2001, using the same setting and flower structures’. bee species). Radish, Raphanus sativus (Cruciferae) Although radish is mainly known for its Other vegetables succulent root, its propagation is by seed. Most At a seed production company in The cultivars are self-incompatible, and bees are Netherlands (Rijk Zwaan), N. perilampoides, the main pollinators (McGregor, 1976; Free, T. angustula and A. mellifera were introduced 1993). In the Netherlands, fruit set of radish in pollination cages (5 × 5 × 2 m) within a 304 E.J. Slaa et al.

Table IV. Average seed production (number of seeds per flower (head)) in each of the crops when no pollinators were present (control) and after pollination with N. perilampoides, T. angustula or A. mellifera. Different letters in a row indicate significant differences between treatments (Kruskall-Wallis with Multiple Comparisons Test, P < 0.05). After Fonseca and Picado, 2000. ∗ N. perilampoides was excluded from the statistical analysis for production of rape seed because original data were lost. ∗∗ Cauliflower plants in the cage with T. angustula were attacked by Plutella xilostella, preventing visitation observations and seed count.

Crops Control N. perilampoides T. angustula A. mellifera Broccoli (n = 97−155) 3.2 ± 2.7a 5.4 ± 3.6b 5.9 ± 3.5b 6.1 ± 4.4b Rape∗ (n = 112−143) 16.3 ± 9.6a 22.6 ± 8.917.4 ± 10.9a 29.9 ± 3.8b Cauliflower∗∗ (n = 250) 4.2 ± 2.6a 0.4 ± 1.1b 4.8 ± 3a Endive (n = 50) 15.2 ± 6.5a 19.4 ± 2.2b 14.2 ± 6.1a 19 ± 2.4b Chicory (n = 50) 13.6 ± 9.3a 16.1 ± 3.5a 14.6 ± 5.2a 15.2 ± 5.2a Leek (n = 150−160) 0.9 ± 1.2a 2.2 ± 1.5b 0.88 ± 1.2a 3.6 ± 1.0c Carrot1 Female line (n = 8−9) 557 ± 312a 0.4 ± 0.7b 1083 ± 561a Male line (n = 8−10) 2826 ± 1070a 52 ± 69b 3324 ± 1070a

1 In carrot, seed counts were per umbel. Plants of the female line required cross-pollination, whereas plants of the male line could be self-pollinated. large greenhouse. Each cage contained several was not significantly lower than seed set after species of vegetables in flower (see Tab. III, honeybee pollination, but significantly higher IV) and one bee colony or no colony (control). than seed set with T. angustula and the con- During a pilot experiment, the number of visits trol (Tab. IV). During limited observations, to each crop species was recorded, and seed set bees only touched the stigmas consistently in was recorded in comparison to a control area carrot, endive and leek flowers. Bees did not where no pollinators were present (Tab. IV). touch the stigmas of broccoli and rape flow- The relative attractiveness of each crop to the ers, and in only half of the visits did they bees can be expressed as the degree of prefer- touch the stigmas of chicory flowers. T. an- ence following Chesson (1983) (Tab. III): gustula visited only 4 of the 6 crops present, and preferred rape and leek flowers (> 30%). / ri ni , = However, during visits to rape and leek flow-
m i 1,...,m (Chesson 1978). rj/nj ers the stigma was never touched and those j=1 visits did not result in an increased seed set compared to the control (Tab. IV). T. angus- where m is the number of crop species, ri is the tula only touched the stigma of carrot flow- number of visits to crop i,andri is the number ers, but these flowers were hardly visited when of plants of crop i. During limited observations other crops were available (Tab. III). A. mellif- flower visitation behaviour was recorded, in- era visited all crops but preferred endive flow- cluding whether the bee’s body contacted the ers (Tab. III). Bees consistently touched the stigma (Fonseca and Picado, 2000). stigma in all crops, probably because of their Foraging behaviour differed significantly larger body size, and increased seed set sig- between the two stingless bee species, which nificantly compared to the control in 5 of the illustrates the variability in stingless bee pref- 7 crops. erence. N. perilampoides visited 6 of the 7 crops present, but preferred endive and car- Overall, A. mellifera was the most effec- rot flowers (> 30%). Visits to carrot and en- tive pollinator of the crops tested, followed dive flowers resulted in a good seed set, which by N. perilampoides. Generally T. angustula Stingless bees in applied pollination 305 was the least effective pollinator, except for put stress on the colony, often resulting in a broccoli. N. perilampoides performed best as loss of adult bees and a reduced brood pro- a pollinator of carrot and these flowers are rel- duction. Some species may be better adapted atively attractive to the bees. Although hon- to these stress factors than others, and some eybees were at least equally effective pollina- species may not forage at all under confined tors for this crop, carrot flowers were not very conditions (see Tab. V). attractive to honeybees (Tab. III), which may cause reduced visitation under field condi- tions when competing plants are nearby (Free, 4.2. Mass rearing and colony 1993). reproduction

Colonies used for pollination services need 4. GENERAL CONSIDERATIONS to be available in large numbers. Nowa- days stingless bee keeping is mainly a non- 4.1. Domestication commercial small-scale business, although a few large-scale beekeepers exist in Mex- To be able to use stingless bees for com- ico, Brazil, and Australia (Murillo, 1984; mercial pollination purposes, management of Heard and Dollin, 2000; Quezada-Euàan et al., colonies in hives is of vital importance. Al- 2001; Rosso et al., 2001; Drumond, 2004; though many different species have been kept Cortopassi et al., 2006, this issue) where it in hives (Cortopassi et al., 2006, this issue), involves the keeping of mainly Melipona, not all species may be easily transferred to T. angustula, Cephalotrigona and Scaptotrig- hives due to their specific nesting requirements ona species. In Australia, several beekeep- (e.g. Geotrigona and Trigona fulviventris nest ers sell stingless bee hives (Trigona and Aus- in the ground, Trigona corvina builds its own troplebeia species), and they are listed on exposed nest, T. fuscipennis nests in termite the Australian Native Bee Research Centre nests). In addition, although they lack a func- website (http://www.zeta.org.au/∼anbrc/buy- tional sting several species aggressively de- stingless-bees.html). Some rent out stingless fend their nest by biting or releasing a caus- bee hives for pollination practices, mainly for tic substance, which makes them less suitable pollination of macadamia (Heard and Dollin, to manage in hives and for pollination services 2000). In Brazil, many farmers use stingless (e.g. the genus Oxytrigona and several species bees as pollinators of local crops, such as uru- of the genus Trigona; see Biesmeijer and Slaa, cum, chuchu, camu-camu, carambola, coco- 2004). da-bahia and mango (Drumond, 2004). Although several species have been domes- Species that show aggressive nest defence ticated since ancient times (Cortopassi et al., also seem to exhibit intra-specific territo- 2006, this issue), management of stingless bee rial behaviour, which makes them unsuitable colonies is not as advanced as management for large-scale beekeeping where hives are of honeybee colonies (Cortopassi et al., 2006, placed close together (e.g. several Trigona this issue). In addition, stingless bee manage- species; Hubbell and Johnson, 1977; Wagner ment practices have been developed princi- and Dollin, 1983). pally for the harvest of hive products, mainly One of the main problems for cultivating honey. Using colonies for commercial polli- stingless bees at a large scale is that they nat- nation services brings along different manage- urally reproduce at a very low rate. It has ment requirements. been estimated that under natural conditions, Colonies used for pollination services are colonies of most species reproduce only once much more disturbed than colonies used for every 20–25 years (Slaa, 2006), with the no- honey production. Transportation to and from table exception of a few common species such the crop, a limited diet offered by the crop as the Neotropical T. angustula and the Asian (many crops offer no nectar), and less than op- Trigona minangkabau, that may reproduce up timal foraging conditions in greenhouses all to once a year (Inoue et al., 1993; Slaa, 2006). 306 E.J. Slaa et al.

Table V. Stingless bee species that have been reported to forage under confined conditions and those that have been reported not to forage under confined conditions.

Species Crop Foraging Greenhouse Location Reference size (l × w × h) Melipona favosa Sweet pepper Yes 9 × 6 × 4 m The Netherlands Meeuwsen (2000) M. quadrifasciata Tomato Yes 234 m2, 3 m high Brazil Santos et al. (2004a); Sarto et al. (2005) M. subnitida Sweet pepper Yes 83 m2 Brazil Cruz et al. (2004) Nannotrigona Tomato Yes 4 × 4 × 3.5 m Mexico Cauich et al. (2004) perilampoides Salvia farinacea Yes 6 × 3 × 3 m Costa Rica Slaa et al. (2000a, b) Salvia splendens No 6 × 3 × 2.5 m Costa Rica Bustamante (1998) Broccoli Yes 5 × 5 × 2 m The Netherlands Fonseca and Rape Picado (2000) Endive Chicory Leek Carrot N. testaceicornis Strawberry Yes 4.2 × 8.1 × 2.4 m Japan Maeta et al. (1992) Cucumber Yes 86.4 m2 Brazil Santos et al. (2004b) Plebeia Strawberry Yes 9 × 6 × 4 m The Netherlands Asiko (2004); tobagoensis Lalama (2001) Scaptotrigona Strawberry No 8 × 25 m Brazil Malagodi-Braga (2002) bipunctata Cucumber Yes 10 m high Japan Amano (2004) Eggplant Yes 10 m high Paprika Yes 10 m high Red pepper Yes 10 m high S.aff. depilis Cucumber Yes 86.4 m2 Brazil Santos et al. (2004b) S. mexicana Rambutan Yes 16 × 16 × 4 m Mexico Roubik pers. comm. S. quadripunctata Strawberry No 8 × 25 m Brazil Malagodi-Braga (2002) Tetragonisca S. farinacea Yes 6 × 3 × 3 m Costa Rica Slaa et al. (2000a, b); angustula Sánchez et al. (2002) Strawberry Yes 8 × 25 m Brazil Malagodi-Braga and Kleinert (2004) Rambutan Yes 16 × 16 × 4 m Mexico Roubik pers. comm. Broccoli Yes 5 × 5 × 2 m Fonseca and Picado Rape Yes The Netherlands (2000) Chicory Yes Leek Yes Radish Yes Meeuwsen (2000) Sweet pepper Yes Trigona White clover Yes 0.2 ha Japan Amano (2004) carbonaria Tomato Yes 0.2 ha Cucumber Yes 10 m high Eggplant Yes 10 m high Paprika Yes 10 m high Red pepper Yes 10 m high Sweet pepper Yes 3 × 5 × 4 m Australia Occhiuzzi (1999) T. fuscipennis S. splendens No 6 × 3 × 2.5 m Costa Rica Bustamante (1998) T. minangkabau Strawberry Yes 4.2 × 8.1 m Japan Kakutani et al. (1993) Stingless bees in applied pollination 307

Colony management has been mainly fo- 4.3. Greenhouse pollination cused on small-scale management practises (Cortopassi et al., 2006, this issue), where low Foraging under confined conditions (e.g. colony reproduction rates have not been a ma- greenhouse, netted cage) brings along its own jor issue. Colonies can be artificially repro- set of difficulties/complications. One of the duced by dividing the hive population (adult most common problems is foragers gathering bees and brood) in two parts, each part re- in the top of the enclosure, especially dur- sulting in a new colony (e.g. Roubik, 1995b; ing the first few days after introduction of the Cortopassi-Laurino et al., 2006, this issue). In hive. These bees are a loss to the colony; when the new colony lacking the mother queen, a they manage to escape from the enclosure they virgin queen has to become accepted by the do not come back, and if no escape is possi- workers and has to mate outside with one or ble they often die of exhaustion and/or over- more drones, most likely from another colony. heating (pers. obs.; Occhiuzzi, 1999; Amano, This is no problem in their natural environ- 2004). These bees are probably experienced ment, where lots of drones are available, but foragers in search of a known food source. becomes more problematic when colonies are Pilot experiments have shown that transporta- exported to areas where they are not native. tion of colonies over rough roads increases the Colonies of T. carbonaria have been split suc- incidence of orientation flights (Lukacs, pers. cessfully in Japan, using a large greenhouse comm.), and it would be interesting to see (10 m high) with multiple hives where ‘nat- whether (gentle) shaking of closed colonies ural’ mating can take place (Amano, pers. before introduction in the greenhouse could comm.). Nevertheless, records of successful reduce the problem of forager loss. However, mating or colony multiplication under en- shaking may also cause eggs, which float on closed conditions are scarce (but see Camargo, top of the larval food, to drown, leading to 1972; Cepeda Aponte, 1997; Amano, 2004). mortality of young brood (Sommeijer, pers. So far, artificial insemination has not been de- comm.). veloped for stingless bees but may be a valu- Although most stingless bee species that able alternative to natural mating. have been tried in pollination studies under confined conditions foraged effectively on the crop, some species were reported to not for- Most people assume that under favourable age on the crop under confined conditions conditions colonies can be multiplied about (Tab. V). This may suggest that some species once a year. Even for the species that have are not suitable for greenhouse pollination. been kept in hives since ancient times, the lim- However, lack of foraging may also reflect iting factors for colony growth and colony re- suboptimal foraging conditions for the given production are still mainly unknown. More re- species, such as a low attractiveness of the crop search is needed in this area before enough to the species, rather than a species-specific re- stingless bee colonies can be efficiently man- luctance to forage under confined conditions. aged for commercial pollination purposes. Clearly more studies are needed to get a bet- ter understanding of which factors attribute to successful foraging in greenhouses. No major breeding populations exist yet outside the tropics. Further research could solve the current problem of artificial colony 4.4. Pesticides multiplication in non-native areas, although it might be economically more beneficial to Application of pesticides is a common pro- restrict breeding to the tropical native areas cedure in crop production, especially in the and export existing colonies. Keeping breed- tropics where it still causes major health haz- ing programs in the tropics would also provide ards for both people and animals. Pesticide the opportunity for local people to benefit from application to crops often repels insects from their ecological resources. the flowers, can kill the pollinators and may 308 E.J. Slaa et al.

Table VI. Mismatches between crop and stingless bee species.

Crop Bee species Effective? Reference Salvia splendens T. angustula No, too small Sánchez et al. (2002) Strawberry P. tobagoensis No, pollen robbers Lalama (2001) P. tobagoensis Yes, if buds protected Asiko (2004) Tomato T. carbonaria No Amano (2004) Sweet pepper T. angustula No, does not touch stigma Kuyhor (2001) during nectar collection Radish T. angustula No, reaches nectary from outside corolla Thai (2001) kill entire colonies (e.g. Kearns and Inouye, match may result in visitation without polli- 1997; Ish-Am et al., 1999; pers. obs.). The nation, stealing or robbing pollen and/or nec- chemical effect of commonly used pesticides tar. In some instances this can be prevented on bees has been documented (see Roubik, by evaluation of floral structure and relating 1995a), although most chemicals have only the location of the stigma and anthers to bee been tested on the honeybee. Smaller-bodied body size. Literature on techniques and con- stingless bees are probably even more suscep- siderations for pollination studies can be found tible than honeybees due to their high surface in several other publications (e.g. Kearns and area-to-volume ratio. During pesticide appli- Inouye, 1993; Dafni et al., 2005). cation managed hives can be removed from The effects of prolonged enclosed condi- the site, but wild colonies may still be ex- tions and/or a restricted diet on colony health posed to the chemicals. Because colony re- are largely unknown. Regularly opening the production rate of stingless bees is very low hive to inspect the internal colony status, as of- (see above), colony mortality will have a big ten done in honeybees, is very disruptive for impact on natural stingless bee populations. stingless bees, and often causes a decline in There are several guidelines on pesticide ap- colony functioning. Monitoring colony weight plication available to minimize the impact on during pollination services can provide some pollinators, although none make pesticide use insight into colony health, but does not pro- completely safe (Kearns and Inouye, 1997). vide information on brood status. Recently, Biological control of pests, as is now offered X-ray computerized tomography has been suc- in conjunction with commercially available cessfully used to visualize internal nest struc- bumble bee pollinators (e.g. Koppert BV, The tures in a non-invasive way, and this method Netherlands), seems an ideal solution. How- would provide an excellent research tool when ever, special efforts to reduce the use of po- measuring the effect of environmental (green- tent pesticides seem necessary in the tropics, house) conditions on colony health (Greco where pesticides are easily available, generally et al., 2005). cheap, and where safety risks are commonly unknown to the farmers. 5. POLLINATION AND BIODIVERSITY CONSERVATION 4.5. Further research Although this manuscript deals mostly with From the comparative studies described the use of managed stingless bee colonies above it becomes clear that the pollination ef- for pollination services, a fair share of pol- fectiveness of a specific stingless bee species lination services can come from wild (un- depends very much on the crop species. Ta- managed) bees. For several crops it has been ble VI gives some examples of plant-pollinator shown that growing crops near intact natu- mismatches from previous studies. A mis- ral habitat (e.g. forest, woodland, chaparral) Stingless bees in applied pollination 309 increases abundance and diversity of flower- losing valuable pollinators. Wille and Orozco visiting insects, and that these crops have a (1983) report that one Costa Rican family with higher yield than crops growing away from a chayote orchard took one year to elimi- natural vegetation (Wille and Orozco, 1983; nate all Trigona nests known in their area be- Venturieri et al., 1993; Heard and Exley, 1994; cause they believed these bees ate the tendrils Kremen et al., 2002; Klein et al., 2003a, b; and young leaves. After eliminating all nests, Ricketts, 2004; Ricketts et al., 2004; Chacoff production decreased dramatically from previ- and Aizen, 2006). These findings indicate the ously high quantities of fruits to no yield at all. importance of habitat conservation for pollina- Simple management measures to increase tion purposes. Many wild bees, including stin- bee abundance and diversity include preserva- gless bees, depend on trees for nesting, and tion of natural forests and forest fragments, in- deforestation significantly reduces their num- creasing the availability of nesting sites, and bers (Slaa, 2003). Even selective logging may minimizing the use of pesticides including her- severely affect stingless bee populations, espe- bicides (Kearns and Inouye, 1997; Klein et al., cially when the larger trees that are preferred 2003b). for nesting are harvested (Eltz et al., 2002; Conservation of stingless bees may also be Samejima et al., 2004). affected by the commercial use of stingless bee In the case of coffee (C. arabica,see colonies for pollination services. Provided that above), one of the most valuable export com- colonies for such services are mainly obtained modities from developing countries, yields on from breeding programs, instead of taken from a farm in Costa Rica were 20% higher in ar- nature, commercial use of stingless bees does eas near forest than in areas away from forests. not have to have a negative impact on the The economic value of the forest in terms of feral population, and may actually contribute pollination services was estimated to be ca. to their conservation. $60 000 for one Costa Rican farm, per year. This value is of at least the same order as major competing land uses, which illustrates the eco- 6. MAIN CONCLUSIONS nomic benefit of forest conservation in agricul- AND PERSPECTIVES tural landscapes (Ricketts et al., 2004). Simi- lar results were found in Indonesia where fruit This manuscript shows that stingless bees set was negatively correlated with forest dis- are effective pollinators of a wide range of tance (Klein et al., 2003a), and in Brazil where crops. Over the past six years, stingless bees coffee plantations near forest fragments had have been confirmed as effective pollinators an increase of 15% in production that could for nine new crop species, putting the total be related to pollination services (Marco and now on 18 crops. Several species have been Coelho, 2004). Fruit set in the self-sterile low- domesticated and can be managed in hives. land coffee species C. canephora was found to The main limitation to their commercial use linearly decrease with distance from the forest as pollinators is lack of mass breeding tech- (Klein et al., 2003b). niques, which is hampered by low natural Proper information to farmers about the role colony reproduction rates. Stingless bees may of wild bees as pollinators and the pollination be especially suitable to provide pollination services of forests can play a major role in services in greenhouses, as 11 out of the 13 the conservation of wild bees and their nat- species tested and reported foraged effectively ural nesting habitat of tropical forests. Some under enclosed conditions. However, more re- species of stingless bees, especially from the search is needed to find the optimal forag- genus Trigona, have dented mandibles and are ing conditions under enclosed conditions. Al- known to damage fruits, leaves and sometimes though feral colonies are restricted to the trop- even flower buds (Wille, 1961; pers. obs.). ical and subtropical parts of the world, sting- Some farmers consider these species as pests less bees can be kept in cold climates, where and try to eliminate the easily recognizable they have to be kept indoors in heated hives. exposed nests, without knowing that they are Stingless bees have successfully pollinated 310 E.J. Slaa et al. several greenhouse crops in regions with tem- ornementale Salvia farinacea. Il a été aussi reporté perate climates, such as The Netherlands and que les abeilles sans aiguillon visitaient et étaient Japan. Pesticides may be a severe problem for des pollinisateurs potentiels de l’agrume calamon- din, des cultures de cucurbitacées comme le melon stingless bees, as they are generally smaller- d’eau et la citrouille, du radis et de plusieurs autres bodied than the commonly used honeybees légumes tels que la carotte et l’endive (Tabs. II, IV). and bumble bees, but biological control could Certaines espèces d’abeilles sans aiguillon diffèrent provide a good solution. néanmoins grandement par leur taille et l’efficacité Although this paper has indicated some pollinisatrice dépendra de l’adéquation spécifique plante-pollinisateur (voir Tab. VI pour des cas où potential problems for the use of stingless les deux partenaires sont mal assortis). bees in applied pollination, these can likely La recherche récente s’est concentrée sur l’ap- be overcome after more research. Stingless proche expérimentale à l’aide d’enceintes telles bees posses several biological characteristics que sachets, cages et serres. On a trouvé que favourable in applied pollination, and this onze espèces d’abeilles sans aiguillon représentant six genres butinaient efficacement sous enceintes paper has further strengthened their impor- (Tab. V), montrant ainsi le potentiel de ces abeilles tance as pollinators of commercially impor- comme pollinisateurs des cultures protégées. Les tant crops. This indicates that stingless bees colonies peuvent être maintenues à l’intérieur du- are strong candidates in the search for alter- rant des années et, contrairement aux bourdons, native pollinators for our crops. ne meurent pas après la période de reproduction. Ceci constitue une incitation économique pour uti- liser ces abeilles sans aiguillon comme pollinisa- teurs commerciaux. Dans les régions tempérées le ACKNOWLEDGEMENTS fait que la plupart des espèces ne survivent pas aux climats froids, ce qui rend donc l’invasion des ré- gions tempérées improbable, constitue une incita- The authors would like to thank Tim Heard tion économique. Actuellement la principale limi- and David Roubik for valuable comments on the tation à leur usage commercial pour des services manuscript. Anne Dollin, Mark Greco, Darci de de pollinisation réside dans le manque de connais- Oliveira Cruz, Manuel Rincon and David Roubik sances pour les élever en masse. Il est nécessaire kindly provided some of the information presented d’avancer dans la mise au point de la reproduction artificielle des colonies pour que les abeilles sans in this paper. aiguillon puissent être disponibles comme pollini- sateurs commerciaux. Résumé – les abeilles sans aiguillon dans la Outre l’utilisation de colonies élevées dans des pollinisation appliquée : pratiques et perspec- ruches, les abeilles sauvages de la végétation na- tives. Le nombre de colonies d’abeilles sauvages et turelle environnante peuvent fournir une bonne élevées connaît actuellement un déclin rapide, pro- contribution aux services de pollinisation. Il a été voquant une préoccupation mondiale quant aux ser- montré un accroissement de la production des vices de pollinisation. Les abeilles sans aiguillon cultures dans des plantations situées près de la fo- (Apidae, Meliponini) sont des abeilles tropicales rêt naturelle pour plusieurs cultures dont le café, eusociales qui jouent un rôle écologique important qui est partiellement pollinisé par les abeilles sans comme pollinisateurs de nombreuses espèces de aiguillon et représente l’une des cultures d’exporta- plantes sauvages. Leur rôle comme pollinisateurs tions les plus précieuses pour les pays en dévelop- des cultures est actuellement étudié et plusieurs pement. Ces résultats montrent l’importance écono- études ont été publiées ces dernières années depuis mique de la préservation des habitats dans des buts l’article de synthèse de Heard (1999). Neuf cultures de pollinisation commerciale. nouvelles ont été mentionnées comme étant effica- Apidae / Meliponini / abeille sans aiguillon / pol- cement pollinisées par les abeilles sans aiguillon, ce / / qui monte à 18 le nombre total de cultures en bénéfi- linisateur culture protégée culture alimentaire ciant (Tab. I). Cet article passe en revue les informa- tions apparues depuis 1999 et inclut aussi bien des documents publiés que des données non publiées. Zusammenfassung – Stachellose Bienen in der Les études antérieures sont référencées dans l’ar- angewandten Pollinisation: Praxis und Perspek- ticle de Heard (1999). tiven. Die Zahlen an wilden und beimkerten Bie- Au cours des six dernières années les abeilles sans nenvölkern gehen derzeit rapide zurück, was zu aiguillon ont été confirmées comme pollinisateurs einer weltweiten Bedrohung der Bestäuberdienste du caféier (deux espèces), du fraisier (Figs. 1, 2 ; führt. Die Diversifizierung der kommerziell ver- Tab. II), de l’avocatier, du rambutan, du paprika fügbaren Bestäuber kann eine der Antworten sein, doux, de la tomate, du concombre et de la plante um die Lebensmittelproduktion in der Zukunft zu Stingless bees in applied pollination 311

garantieren. Stachellose Bienen sind tropische eu- gezeigt werden, einschliesslich Kaffee, der (teilwei- soziale Bienen, die eine wichtige Rolle als Be- se) von Stachellosen Bienen bestäubt wird und der stäuber vieler Wildpflanzen spielen. Ihre Rolle als ein wertvolles Exportprodukt in Entwicklungslän- Bestäuber in der Landwirtschaft wird erst seit dern darstellt. Diese Befunde zeigen die Bedeutung kurzem untersucht, und seit dem letzten Über- der Habitatkonservierung für kommerzielle Bestäu- sichtsartikel von Heard (1999) wurden viele neue bungszwecke. Arbeiten erstellt und publiziert. Neun neue Feld- früchte konnten durch Stachellose Bienen effektiv Landwirtschaft / Bestäuberalternativen / Feld- bestäubt werden. Dies bringt ihre Gesamtzahl nun früchte / Gewächshaus / Apidae / Meliponini auf 18 (Tab. I). Die vorliegende Arbeit stellt die nach 1999 erschienenen Informationen über Sta- chellose Bienen als Bestäuber in der Landwirtschaft zusammen, und zwar sowohl aus publizierten als REFERENCES auch aus unveröffentlichten Dokumenten. Ältere Studien sind in dem Übersichtsartikel von Heard Amano K. (2004) Attempts to introduce sting- (1999) berücksichtigt. less bees for the pollination of crops un- Während der letzten sechs Jahre konnten Stachello- ff der greenhouse conditions in Japan, Food & se Bienen als Bestäuber von Ka ee, Erdberen (Abb. Fertilizer Technology Center, [online] http:// 1 und 2, Tab. II), Avocado, Rambutan, Gemüse- www.fftc.agnet.org/library/article/tb167.html (ac- paprika, Tomate, Gurke und Salvia farinacea,ei- cessed on 6 March 2006). ner Zierpflanze, etabliert werden. Ausserdem wer- den Stachellose Bienen als Besucher und potenti- Amano K., Nemoto T., Heard T.A. (2000) elle Bestäuber von Calamodin, Cucurbitaceen, wie What are stingless bees, and why and how to use them as crop pollinators? – z.B. Wassermelone und Kürbis, für Rettich und ver- a review, JARQ 34, 183–190. [online] schiedene andere Gemüse wie Karotte und Endi- http://ss.jircas.affrc.go.jp/engpage/jarq/34-3/amano/ vie beschrieben. Stachellose Bienen weisen jedoch amano.htm (accessed on 6 March 2006). erhebliche Artunterschiede hinsichtlich ihrer Kör- pergrösse auf, und die Bestäubungeseffizienz wird Asiko A.G. (2004) The effect of total visitation time davon abhängen wie gut die Bestäuber- und Pflan- and number of visits by pollinators (Plebeia zenspezies zusammenpassen (siehe Tab. VI für ei- sp. and Apis mellifera mellifera)onthestraw- nige Misserfolge). berry, M.Sc. Thesis, Utrecht University, The Neuere Untersuchungen zielen auf experimentelle Netherlands. Ansätze in geschlossenen Systemen, wie Taschen, Benton Jones J. Jr. (1998) Tomato plant culture in the Käfigen und Gewächshäusern. Elf Arten Stachel- field, greenhouse and home garden, CRC Press, loser Bienen aus sechs Gattungen erwiesen sich in Boca Raton, FL. solch geschlossenen Systemen als effektive Samm- Biesmeijer J.C., Slaa E.J. (2004) Information flow and lerinnen (Tab. V), was auf ein beachtliches Poten- organization of stingless bee foraging, Apidologie tial Stachelloser Bienen als Bestäuber in Gewächs- 35, 143–157. häusern hindeutet. Von wirtschaflicher Bedeutung Biesmeijer J.C., Slaa E.J., Siqueira de Castro M., Viana für die Nutzung Stachelloser Bienen als Bestäu- B.F., Kleinert A., Imperatriz-Fonseca V.L. 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