Foraging Behaviour of the Stingless Bee Melipona Orbignyi (Hymenoptera: Apidae: Meliponini) in a Dry Forest Assessed by Multivariate Analysis from Palynological Data

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Foraging behaviour of the stingless bee Melipona orbignyi (Hymenoptera: Apidae: Meliponini) in a dry forest assessed by multivariate analysis from palynological data

Favio Gerardo Vossler

To cite this article: Favio Gerardo Vossler (2019): Foraging behaviour of the stingless bee Meliponaorbignyi (Hymenoptera: Apidae: Meliponini) in a dry forest assessed by multivariate analysis from palynological data, Grana, DOI: 10.1080/00173134.2019.1615984 To link to this article: https://doi.org/10.1080/00173134.2019.1615984

Published online: 01 Jul 2019.

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Foraging behaviour of the stingless bee Melipona orbignyi (Hymenoptera: Apidae: Meliponini) in a dry forest assessed by multivariate analysis from palynological data

FAVIO GERARDO VOSSLER

Laboratorio de Actuopalinología, CICYTTP (CONICET-Prov. ER-UADER), Dr. Materi y España, Diamante, Entre Ríos, Argentina

Abstract Pollen analysis was applied to study the botanical composition of honey and pollen stored by Melipona orbignyi in its southernmost distributional range. Many studies have revealed that robust buzzing bees of this genus are associated with diverse plant families, some of which are different to those exploited by the remaining genera of Meliponini. Cluster analysis was performed to assess similarity in botanical composition between pot-pollen and pot-honey provisions from different colonies. The results indicated that each colony was capable to access to different plant species for obtaining nectar and pollen, a fact observed when discarding the contaminated honey samples. As honey samples were not clustered together with other ones but with pollen samples indicating a similar botanical composition, it could be assumed that a same plant species provided nectar and pollen to bees. Resource partitioning was not clearly observed among a subset of late spring colonies, as two families of high richness of species and abundant in this dry forest (the mimosoid clade in Fabaceae and Capparaceae) were foraged. A higher number of synchronously sampled colonies would be necessary to detect this ecological aspect. The botanical composition of samples of M. orbignyi was governed by both random factors such as local and temporary ﬂower availability plus preferences for particular plant species such as those from Solanaceae and Ximeniaceae. The Capparaceae and Ximeniaceae are here reported for the ﬁrsttimeasintensively foraged pollen resources by the genus Melipona.

Keywords: buzzing, Chaco forest, eusocial bee, meliponiculture, ‘moro moro’, pollen analysis, pot-honey, pot-pollen

Melipona Illiger is an endemic genus of the Americas, well as for home medicine since ancient times (Vellard it is distributed from Mexico to the north of Argen- 1939; Camargo & Posey 1990;Nogueira-Neto1997; tina. In Argentina it is composed of seven species, six Arenas 2003; Cortopassi-Laurino et al. 2006; of them are found in the northeast and northwest Kujawska et al. 2012;Zamudio&Hilgert2012;Roig- rainy forest (Silvestri 1902;Schwarz1932; Michener Alsina et al. 2013). 2007; Camargo & Pedro 2013; Roig-Alsina et al. In the present article, pollen analysis was used to 2013). In western dry areas of the Argentinean study the botanical origin of honey and pollen stored Chaco forest, the stingless bee Melipona (Melipona) by Melipona orbignyi. Floral resources associated orbignyi (Guérin), regionally known as ‘moro moro’, with M. orbignyi have been studied through the produces reputable honey, brown wax and pollen investigation of ﬂoral visits along the northern edge masses that are harvested from wild nests by local of the South American Chaco region (Corumbá, people (Arenas 2003). The ‘moro moro’ builds its state of Mato Grosso do Sul, Brazil; Manente- nests in well protected hollows of tree trunks (mainly Balestieri & Balestieri 2006) and in the Dry Chaco of large living trees) (Arenas 2003;Vossler2012). forest (northern Argentina; Vossler 2012). Pot-honey and pollen from Melipona species have Floral nectar and pollen resources used by the genus been reported as a culturally important for food as Melipona have been well-studied throughout its Neotro-

Correspondence: Favio Gerardo Vossler, Laboratorio de Actuopalinología, CICYTTP (CONICET-Prov. ER-UADER), Dr. Materi y España, Diamante, Entre Ríos E3105BWA, Argentina. E-mail: [email protected]

(Received 8 April 2018; accepted 16 March 2019)

© 2019 Collegium Palynologicum Scandinavicum 2 F. G. Vossler pical distribution (Absy & Kerr 1977;Absyetal.1980; Due to the importance of stingless bees in meli- Kleinert-Giovannini & Imperatriz-Fonseca 1987; poniculture, crop pollination and forest conserva- Ramalho et al. 1989, 2007;Antoninietal.2006; Oli- tion, the aim of this study was to assess the veira et al. 2009; Vossler 2013; Villanueva-Gutiérrez similarity in botanical composition of pollen and et al. 2018). These studies have revealed that these honey provisions from colonies of the ‘moro moro’ robust buzzing bees are associated with diverse plant (Melipona orbignyi) in the dry forest of the Chaco families, some of which are different to those exploited region by means of multivariate analyses. by the other genera of the Meliponini tribe (Ramalho et al. 1989, 1990). The families associated with Meli- pona fornectarandpollensourcesaremainlyMyrta- Material and methods ceae, Melastomataceae, Solanaceae and Fabaceae Pollen analysis of honey and pollen mass (mimosoid clade) followed by Anacardiaceae, Bursera- ceae, Euphorbiaceae, Guttiferae, Fabaceae (Papilionoi- In the present work, a total of eight honey and nine deae), Moraceae and Arecaceae (Ramalho et al. 1989). pollen samples (one per nest) were palynologically In the subtropical Dry Chaco forest, Myrtaceae and analysed from nine nests sampled in a xerophilous Melastomataceae families are rarely represented or not forest at two localities of the Argentinean Chaco: El present at all, while the other families commonly asso- Espinillo (25° 24ʹ S, 60° 27ʹ W) and El Sauzalito ciated with tropical Melipona species are well- (24° 24ʹ S, 61° 40ʹ W) (Figure 1, Table I). This represented. These include Fabaceae (mimosoid forest is named as ‘palosantal’ due to a dominant clade), Solanaceae, Anacardiaceae, Euphorbiaceae, zygophyllaceous tree, the ‘palo santo’ (Bulnesia sar- Fabaceae (Papilionoideae) and Arecaceae. Like all mientoi Lorentz ex Griseb.). Pot-honey and pot- Meliponini genera, Melipona bees concentrate their pollen samples were taken during winter, spring foraging on the plant families that are best represented and summer, between February 2006 and Febru- in the environment (Ramalho et al. 1990). Thus, it is ary 2009 (Table I). Per nest, one representative expected to ﬁnd plant families that have not been pre- sample of honey was kept. Honey samples were viously reported for tropical species to be associated pure in nests 1, 4, 5, 6, 7 and 11, while they were with this southernmost distributed subtropical Meli- contaminated from pot-pollen during their sampling pona species. in nests 8 and 10. The pollen of different pots of

Figure 1. Location of the Chaco region within South America, the two sites of the present study: 1, El Espinillo (25° 24ʹ S, 60° 27ʹ O); 2, El Sauzalito (24° 24ʹ S, 61° 40ʹ O) and a further site where ﬂoral resources foraged by this bee species have been previously studied: * Corumbá, Mato Grosso do Sul, Brazil (22° 14ʹ S, 53° 66ʹ W). Foraging behaviour of M. orbignyi in Chaco dry forest 3

each nest was mixed and analysed as a single sample. Honey and pollen samples were dissolved with a glass rod in 200 mL of distilled water at 80─90 ºC and then with a magnetic stirrer for 10─15 min. - 6 5 8 7 6 Five millilitres of this mixture was centrifuged at 10 14 16 472 g (Pendlenton 2006) and the sediment was

honey samples dehydrated and acetolyzed (Erdtman 1960), 24 pollen types mounted in slides using a glicerine-gelatin mixture

Number of pollen types in and identified using a Nikon Eclipse E200 light microscope at 400 and 1000 × magnification. Pollen identification was carried out by comparing pollen provision slides with the pollen reference of plants grown in the sites sampled. The counting of 500 pollen grains per slide was made for honey samples, while a total of 300–500 grains for pollen ones.

9 8 9 6 8 5 5 6 These reference plant specimens were pressed, 24 dried, identiﬁed by the author and deposited in the

pollen samples Herbaria of the Museo of La Plata (LP), the Museo 25 pollen types Argentino de Ciencias Naturales ‘Bernardino Riva-

Number of pollen types in davia’ (BA), Buenos Aires, and the Herbarium Lor-

Melipona orbignyi. entz (DTE) of Diamante, Entre Ríos, Argentina. Bees were identiﬁed by Arturo Roig-Alsina and deposited in the Entomology Collection of the Museo Argentino de Ciencias Naturales ‘Bernar- ) dino Rivadavia’, Buenos Aires, Argentina. Locality Figure 1

(for reference see Climate conditions and vegetation of the study area El Sauzalito El Sauzalito El Sauzalito El Sauzalito El Sauzalito 2 localities The climate in the study area is strongly seasonal with very hot summer (December to March) and low temperatures and frost during winter (July to Sep- tember) (Prado 1993). There is a manifest yearly variation in rainfall, with a marked dry season in winter-spring and a rainy season from October to April (Papadakis 1973). The Palosantal forest is characterised by the dominance of trees of ‘palo santo’ (Bulnesia sarmientoi, Zygophyllaceae). Other Collection date

(and time of year) elements of the ﬂora are ‘quebracho colorado santia- gueño’ (Schinopsis lorentzii [Griseb.] Engl., Anacar- diaceae), ‘quebracho blanco’ (Aspidosperma February 2006 (middle summer)December 2008 (last spring) December 2008 (last spring) December 2008 El (last Espinillo spring) December 2008 (last spring) October 2008 (early spring) February 2009 (middle summer)February 2009 (middle summer)September 2008 (last winter)4 months El and Sauzalito 3 seasons El Sauzalito El Sauzalito quebracho-blanco Schldtl., Apocynaceae), ‘mistol’ (Ziziphus mistol Griseb., Rhamnaceae), ‘molle’ or ‘guaraniná’ (Sideroxylon obtusifolium [Humb. ex Roem. et Schult.] T.D. Penn., Sapotaceae), several species of the genus Prosopis L. (‘algarrobo blanco’, ‘algarrobo negro’, ‘vinal’, ‘vinalillo’, ‘carandá’, ‘gua- chín’) (Fabaceae, mimosoid clade), ‘guayacán’ (Cae- salpinia paraguariensis [D. Parodi] Burkart, Fabaceae, Caesalpinioideae), ‘tipa colorada’ or ‘palo coca’ honey samples (Pterogyne nitens Tul., Fabaceae, Caesalpinioideae), ‘palo cruz’ (Tabebuia nodosa [Griseb.] Griseb., Bignoniaceae), ‘quebrachillo’ (Aspidosperma triterna- tum Rojas Acosta, Apocynaceae), ‘palo borracho’ or ‘yuchán’ (Ceiba chodatii [Hassl.] Ravenna, Malva- Mo 1Mo 4Mo 5Mo 6Mo P 7 + H Mo P 8 + H Mo P 9 + H Mo P 10 + H Mo P 11 + H 9 P nests + H P P + H P + H 9 pot-pollen and 8 pot- Table I. Data of the pot-provisions studied and number of pollen types found in pot-pollenNest and code pot-honey samples of Type of provision ceae), ‘palma de monte’ (Trithrinax schizophylla 4 F. G. Vossler

Drude, Arecaceae), ‘meloncillo’ (Castela coccinea coefficient (0.817) (Figure 2). The dendrogram Griseb., Simaroubaceae), ‘palo tinta’ (Achatocarpus shows a group A composed of samples Mo 9 praecox Griseb., Achatocarpaceae), ‘tala’ (Celtis spp., P summer (subgroup A), Mo 10 P summer and Mo Cannabaceae), ‘duraznillo’ (Salta triflora [Griseb.] 10 H summer (subgroup B) that diverges from the Adr. Sanchez, Polygonaceae), ‘pata’ (Ximenia amer- remaining 14 samples (group B) at low similarity icana L., Ximeniaceae), ‘molle’ (Schinus fasciculata values (0.1–0.2). Group B is made up of two sub- [Griseb.] I.M. Johnst. var. arenicola [Hauman] F.A. groups at a low similarity value (0.2). Subgroup A by Barkley, Anacardiaceae), ‘chañar’ (Geoffroea decorti- samples Mo 8 P spring, Mo 8 H spring, Mo 6 cans [Gillies ex Hook. et Arn.] Burkart, Fabaceae, H spring, Mo 7 P spring and Mo 7 H spring. One Papilionoideae), ‘sacha rosa’ (Quiabentia verticillata sample (Mo 8 P spring) is isolated at near 0.4 of [Vaupel] Vaupel ex Berger, Cactaceae), ‘sal de similarity from the remaining ones conforming two indio’ or ‘sal de monte’ (Maytenus vitis-idaea Griseb., sets with two subsets each one. One set is made up of Celastraceae), ‘paloma yuyo’(Moya spinosa Griseb., samples Mo 8 H spring and Mo 6 H spring while the Celastraceae), ‘teatín’ (Mimosa detinens Benth., other by Mo 7 H spring and Mo 7 P spring. The Fabaceae, mimosoid clade), ‘cardón’ (Stetsonia cor- larger subgroup B (nine samples) has two sets, one of yne [Salm-Dyck] Britton et Rose, Cactaceae), ‘ucle’ them is composed of samples Mo 5 H spring and Mo (Cereus forbesii hort. Bot. Berlin ex C.F. Först., Cac- 11 H winter closed at 0.5 similarity, while the other taceae), ‘escayante’ (Mimozyganthus carinatus [Gri- set by a subset having samples Mo 1 H summer and seb.] Burkart, Fabaceae, mimosoid clade), two Mo 4 P spring and another larger subset of five species of the genus Bougainvillea Comm. ex Juss. samples Mo 1 P summer, Mo 5 P spring, Mo (‘rama overa’) (Nyctaginaceae), ‘palo azul’ (Cyclolepis 4 M spring, Mo 6 P spring and Mo 11 P winter. genistoides D. Don, Asteraceae), ‘tusca’, ‘garabato’, ‘churqui’ (several species of the genera Senegalia Raf. and Vachellia Wight et Arn.) (Fabaceae, mimosoid clade), ‘atamisqui’ (Atamisquea emarginata Miers ex Hook. et Arn.), ‘sacha membrillo’ (Cappar- icordis tweediana [Eichler] Iltis et Cornejo), ‘sacha sandia’ (Sarcotoxicum salicifolium [Griseb.] Cornejo et Iltis), ‘sacha poroto’ (Cynophalla retusa [Griseb.] Cornejo et Iltis), ‘bola verde’ (Anisocapparis speciosa [Griseb.] Cornejo et Iltis) (all of them Capparaceae), and ‘cardos’ or ‘chaguares’ (several terrestrial Bro- meliaceae genera).

Multivariate analysis Cluster Analysis was the multivariate technique applied. The PAST statistic package (Hammer et al. 2008) was used. The algorithm UPGMA (Unweighted pair-group average) and Bray-Curtis distance were applied to the percentage values of the data matrix in Q-mode. The highest similarity level is 1.00 and indicates 100% of similarity among pollen composition of samples. The cophenetic correlation coefﬁcient was taken into account as a distortion mea- surement of the dendrogram (Sokal & Rohlf 1962), being values higher than 0.8 indicators of well group- ings in the dendrogram compared to the original similarity matrix (Sneath & Sokal 1973).

Results Cluster analysis Figure 2. Dendrogram showing the groups and subgroups of pot- The dendrogram of nest provisions of Melipona honey and pot-pollen samples of Melipona orbignyi in the Chaco orbignyi showed a high value of cophenetic correlation region. Foraging behaviour of M. orbignyi in Chaco dry forest 5

Samples from group A have a low number of families On the other hand, as honey samples were not (4, 5 or 7) and were dominated either by Solanaceae clustered together with other honey samples but (Mo 9 P summer) or Anacardiaceae (Mo 10 P summer with pollen ones indicating a similar botanical com- and Mo 10 H summer), and in a lesser scale composed position, it could be assumed that both nectar and of Capparaceae and Solanaceae (Mo 10 H summer) pollen were exploited from the same plant species. (Figure 2, 4, Table II). Most samples from group Similar kind of clustering is also observed on the B were composed of few to many plant families (up Chaquenian stingless bees Tetragonisca fiebrigi to 18) and dominated by Fabaceae (mimosoid clade) (Vossler 2013; Vossler et al. 2014) and Geotrigona or Capparaceae. Subgroup A is dominated by Cappar- argentina (Vossler 2013), supporting that the Dry aceae (most samples) or Ximeniaceae (Mo 8 P spring), Chaco melittophilous vegetation is dominated by while Subgroup B has two very different sets. The plants providers of both pollen and nectar, but not larger set (seven samples) has high percentages of exclusively or predominately of one of them. Fabaceae (mimosoid clade) and their two subsets are Similarity of botanical composition of pot-provisions either dominated by this family (most samples) or samples of Melipona orbignyi codominated by Solanaceae, Fabaceae (mimosoid clade) and Rhamnaceae (Mo 1 H summer) or by Like can be seen in Cluster Analysis, the association of Fabaceae (mimosoid clade), Capparaceae, Solana- some families allowed for the differentiation of groups ceae, Ximeniaceae and Anacardiaceae (Mo 4 of samples, those from the three sampled seasons P spring). The other set (two samples) characterises (dominated by Fabaceae, mimosoid clade) (a set of by the dominance of Celastraceae (Mo 5 H spring) and Subgroup B of Group B) from those typically from the codominance of this and Fabaceae (mimosoid spring (Capparaceae) (a set of Subgroup A of Group clade) (Mo 11 H winter) (Figures 2 and 4, Table II). B) or from summer (Solanaceae and Anacardiaceae) The 17 provision samples (Table II) were not (Group A and a set of Subgroup B of Group B). grouped according to the nature of the stores except It could be hypothesised that colonies concen- two honey samples dominated by Celastraceae (Mo trated on different plant families probably to avoid 5 H spring and Mo 11 H winter). From the total intraspecific competition, although this behaviour number of samples of the dendrogram (17), eight of should be assessed by comparing colonies sampled them (half) were grouped according to their season- in a same season and site. For instance, the four ality (those from group A [all from summer] and colonies of late spring 2008 (Figure 3) and those of from subgroup A of group B [all from spring]). Six mid-summer 2009 from El Sauzalito (Figure 2) out of these eight samples were grouped according were compared. Colonies Mo 4 and 7 foraged on to their similarity in botanical composition of the pollen and nectar from similar major resources, the honey and pollen from the same nest (nests 7, 8 former from Fabaceae (mimosoid clade) and the and 10). The other half of samples was not clustered latter from Capparaceae. On the other hand, colo- according to the season nor to each individual nest. nies Mo 5 and 6 foraged both kinds of provisions on different resources or in different proportion, being Celastraceae a major resource in the honey and Discussion Fabaceae (mimosoid clade) and Sapotaceae in pollen of nest Mo 5, and Capparaceae, Fabaceae Were nectar and pollen exploited from the same plant (mimosoid clade) and Celastraceae in honey and species? Fabaceae (mimosoid clade) and Capparaceae in pol- Half of samples (both types of provisions from nests len of nest Mo 6 (Figure 3). These results show that 7, 8 and 10) were grouped together or fairly closed resource partitioning was not clearly observed, as due to they were composed of similar dominant two families of high richness of species and abun- families (Group A and Subgroup A of Group B; dant in this dry forest (mimosoid clade in Fabaceae Figure 2). On the contrary, the fact that both provi- and Capparaceae) were foraged by these late spring sions of a same nest (for a total of nine samples) colonies. The comparison of the two mid-summer were located in different branches in the other half colonies from a same site (Mo 9 and 10) showed of the cluster (all non-contaminated samples: Sub- that different major families were represented in group B of Group B; Figure 2) suggests that each each one (Solanaceae in Mo 9 and Anacardiaceae colony was capable to access to different plant spe- in Mo 10) (Figure 2). A higher number of synchro- cies for obtaining nectar and pollen. Thus, when nously sampled colonies would be neccessary to test discarding the contaminated samples, this pattern intraspecific competition. for the clustering of samples of Melipona orbignyi These results would indicate that the botanical becomes clear. composition of the pot-provisions of Melipona 6 .G Vossler G. F.

Table II. Abundance (%) of plant families found in Melipona orbignyi pollen and honey samples. P = only present in pollen provisions; H = only present in honey provisions.

Pot-pollen samples Pot-honey samples

Plant families P/H Mo 1 Mo 4 Mo 5 Mo 6 Mo 7 Mo 8 Mo 9 Mo 10 Mo 11 Mo 1 Mo 4 Mo 5 Mo 6 Mo 7 Mo 8 Mo 10 Mo 11

Achatocarpaceae H 0.23 Anacardiaceae 12.95 4.33 88.75 53.89 Cactaceae H 0.45 Apocynaceae H 6.04 0.23 Arecaceae P 0.04 Bignoniaceae 0.26 0.42 0.32 0.22 0.46 Capparaceae 0.66 19.37 14.16 84.74 30.69 9.60 5.00 5.37 59.06 64.41 45.03 19.96 Celastraceae 1.32 2.69 0.84 1.89 3.45 4.03 95.01 13.87 2.19 1.62 0.60 45.57 Fabaceae, Caesalpinioideae 0.91 0.84 3.98 2.97 0.45 0.69 Fabaceae, mimosoid clade 66.45 30.50 74.48 78.76 8.77 2.64 0.62 1.56 92.45 31.03 72.48 3.05 21.48 3.38 28.41 0.40 41.77 Loranthaceae P 0.04 0.33 Nyctaginaceae 0.33 0.56 0.44 1.89 4.70 5.06 Polygonaceae H 0.22 Ranunculaceae 0.13 0.33 3.77 0.23 1.27 Rhamnaceae 0.13 0.99 13.79 6.04 1.94 1.57 0.46 0.20 6.33 Sapotaceae 2.30 2.82 23.01 0.44 0.65 0.33 3.45 2.24 2.54 Simaroubaceae P 0.09 Solanaceae 28.95 15.46 84.83 4.69 48.28 0.22 4.17 18.96 Ximeniaceae 12.99 0.42 61.72 1.34 0.22 17.78 Zygophyllaceae 0.83 5.52 0.62 25.84 2.31 5.99 Unidentiﬁed 1 P 0.13 1.33 Unidentiﬁed 2 P 0.09 0.88 Foraging behaviour of M. orbignyi in Chaco dry forest 7

Figure 3. Dendrogram of only late spring samples.

orbignyi is governed by random factors such as local (1987), Ramalho et al. (1989) and Wilms and Wie- and seasonal differences of flower availability nearby chers (1997) found that ‘mandaçaia’ (M.[Melipona] the nests. In the subtropical dry Chaco forest, the quadrifasciata quadrifasciata Lepeletier), ‘guaraipo’ southermost distributional range of the genus Meli- (M.[Eomelipona] bicolor bicolor Lepeletier), ‘man- pona, an intensive use of families not recorded in durim’ (M.[Eomelipona] marginata marginata Lepe- other areas was detected for M. orbignyi, for instance letier) concentrated on Myrtaceae, Capparaceae and Ximeniaceae. Vossler (2019) Melastomataceae, Fabaceae (mimosoid clade) and hypothesised that floral syndromes are the reason Solanaceae. In Bahia state of Brazil, Carvalho et al. for the intensive use of these resources, together (2001) and Ramalho et al. (2007) shown that with others previously known plant taxa such as ‘uruçu’ (M.[Michmelia] scutellaris Latreille) mainly Fabaceae (mimosoid clade). Similar to many sting- foraged on Myrtaceae, Fabaceae (mimosoid clade), less bee genera, bees of the genus Melipona have Fabaceae (Caesalpinioideae), Sapindaceae and Ana- been associated to different families according to cardiaceae. In Surinam (northern South America), the vegetation of the study site where samples were Engel and Dingemans-Bakels (1980) identified that taken. For instance, in the Brazilian Amazon, Absy the most important resources for ‘erica’ (M.[Meli- and Kerr (1977), Absy et al. (1980, 1984), Kerr pona] favosa [Fabricius]) were Avicenniaceae, Myr- et al. (1986), Marques-Souza et al. (1995), Mar- taceae, Melastomataceae, Polygonaceae and ques-Souza (1996) and Oliveira et al. (2009) found Solanaceae. And, in Yucatán (Mexico), Villanueva- that M. (Michmelia) seminigra merrillae Gutiérrez et al. (2018) identified that the most Cockerell, M. (Michmelia) paraensis Ducke important resources for ‘xun’an kab’ (Melipona bee- (as M. rufiventris paraensis Ducke), M. compressipes cheii) were Fabaceae (Papilionoideae and Caesalpi- manaosensis Schwarz, M. (Melikerria) fasciculata nioideae), Burseraceae, Myrtaceae, Solanaceae and Smith (as M. compressipes fasciculata Smith) and M. Cochlospermaceae. (Michmelia) fulva Lepeletier concentrated their fora- Complementary to this opportunistic foraging ging on Myrtaceae, Melastomataceae, Fabaceae behaviour here detected by multivariate methods, (mimosoid clade), Burseraceae, Fabaceae (Caesalpi- preference for particular plant families is also nioideae) and Solanaceae. In São Paulo (Brazil), observed. The dominance of Solanaceae and Kleinert-Giovannini and Imperatriz-Fonseca other plants having poricidal anthers was also 8 F. G. Vossler

Figure 4. Scanning photomicrograph of pollen grains found in pot-honey and pot-pollen samples of Melipona orbignyi. A. Cynophalla retusa (CAPPARACEAE) (a), Prosopis (FABACEAE, MIMOSOID CLADE) (b), type Senegalia praecox (FABACEAE, MIMOSOID CLADE) (c) and Sideroxylon obtusifolium (SAPOTACEAE) (d). B. Type Vachellia aroma (FABACEAE, MIMOSOID CLADE). C. Type Maytenus (CELASTRACEAE) (left) and type Schinopsis (ANACARDIACEAE) (right). D. Anisocapparis speciosa (CAPPARACEAE). Scale bars – 20 µm (A), 10 μm (B), 5 µm (C, D). recorded several times in Melipona provisions to bees. This pattern was also detected for the (Ramalho et al. 1989, 1990, 2007)andthisfact stingless bees Tetragonisca fiebrigi and Geotrigona was interpreted as floral preference and sup- argentina in this forest, supporting that the dry ported by the buzzing mechanism for pollen gath- Chaco melittophilous vegetation is dominated by ering, only found in this genus among the plants providers of both pollen and nectar, but stingless bees. not exclusively or predominately of one of them. Resource partitioning was not clearly observed among a subset of late spring colonies, as two Conclusions families of high richness of species and abundant Cluster analysis from palynological data was in this dry forest (mimosoid clade in Fabaceae applied to assess similarity in botanical composi- and Capparaceae) were foraged, hiding foraging tion between pot-pollen and pot-honey provisions tendencies. A higher number of synchronously from different colonies of the stingless bee Meli- sampled colonies are necessary for the detection pona orbignyi in a dry forest of South America. It of this ecological aspect. The botanical composi- could be observed that each colony was capable tion of samples of M. orbignyi was governed by to access to different plant species for obtaining both random factors such as local and temporary nectar and pollen, a fact observed when discard- flower availability plus preferences for particular ing the contaminated honey samples. The honey plant species such as those from Solanaceae and samples were not clustered together with other Ximeniaceae. The families Capparaceae and ones but with pollen samples indicating a similar Ximeniaceae are here reported for the first time botanical composition, it could be assumed that as intensively foraged pollen resources by the a same plant species provided nectar and pollen genus Melipona. Foraging behaviour of M. orbignyi in Chaco dry forest 9

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