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Revista Brasileira de Entomologia

Print version ISSN 0085-5626

Rev. Bras. entomol. vol.55 no.3 São Paulo July./Sept. 2011  Epub Sep 09, 2011

http://dx.doi.org/10.1590/S0085-56262011005000026 

Pollen storages in nests of bees of the genera Partamona, Scaura and Trigona (Hymenoptera, Apidae)

 

Pólen estocado nos ninhos de abelhas dos gêneros Partamona, Scaura e Trigona (Hymenoptera, Apidae)

 

 

André Rodrigo RechI; Maria Lúcia AbsyII

IPrograma de Pós-Graduação em Ecologia (PPGECO), Instituto de Biologia (IB), Universidade Estadual de Campinas (UNICAMP), Rua Monteiro Lobato 970, Caixa Postal 6190, 13083–970 Campinas–SP, Brasil. arech2003@yahoo.com.br
IICoordenação de Pesquisa em Botânica (CPBO), Instituto Nacional de Pesquisas da Amazônia (INPA), Avenida André Araújo 2936, Caixa Postal 478, 69060–001 Manaus-AM, Brasil

 

 


ABSTRACT

Bees and angiosperms established a mutualistic relationship along the evolutionary time. The aim of this study is to contribute for the understanding of this relation analyzing pollen stored by stingless bees colonies distributed along the Rio Negro. Fourteen species of Meliponini from the genera Partamona, Scaura, and Trigona were studied with regard to the content of pollen pots. The pollen material was removed from the pollen pots, homogenized, and prepared according to the usual acetolysis technique. The overlap of the trophic niche and the grouping of species by similarity of niches was calculated. The identification revealed 78 pollen types belonging to 36 families, being 37 types attractive and 16 considered as promoters of a temporary specialization event. With the results, it was possible to indicate a list of important plants for meliponiculture in the Amazon.

Keywords: Pollination, pollinic resource, stingless bee


RESUMO

Abelhas e plantas estabeleceram ao longo do tempo evolutivo uma relação mutualística. Buscando contribuir para o entendimento dessa relação, foi analisado o pólen estocado por colônias de abelhas-sem-ferrão distribuídas ao longo do rio Negro. Foram estudados potes de pólen de 14 espécies de Meliponini dos gêneros Partamona, Scaura e Trigona. O material polínico foi retirado dos potes de pólen, homogeneizado e preparado segundo técnica usual de acetólise. Foram calculados a sobreposição de nicho trófico e o agrupamento das espécies pela similaridade de nichos. Foi identificado o total de 78 tipos polínicos, pertencentes a 36 famílias, sendo 37 destes, considerados atrativos, enquanto 16 foram promotores de eventos de especialização temporária. Com os resultados obtidos foi possível indicar uma lista de plantas de importância para a meliponicultura na Amazônia.

Palavras-chave: Abelhas-sem-ferrão, polinização, recurso polínico.


 

 

The perpetuation of angiosperms occurs largely due to pollination mechanisms, especially in tropical environments, where most species of flowering plants depend on biotic pollen vectors that promote gene flow, contributing for the formation of viable seeds (Bawa et al. 1985a, b; Bawa 1990; Ennos 1994). In this context, bees stand out as the major group of potential pollinators (Simpson & Neff 1981). The relationship between bees and angiosperms is very close because pollen and nectar are vital resources for the survival and reproduction of the bees and thus require them to constantly visit flowers throughout their entire lives.

Considering the interaction networks that are established between plants and bees, the study of the identity of each species involved in the interaction may determine a pathway that adds to our understanding of the dynamics of earth's ecosystems (Biesmeijer et al. 2005; Ebeling et al. 2008). One way to access identities in a plant-pollinator interaction network is to make direct observations in the natural conditions of the floral visitors of a given group of plants (Pedro & Camargo 1991; review in Biesmeijer et al. 2005). However, given the large number of plant species and the geographical breadth of environments such as rainforests, the use of indi rect methods becomes more relevant. Pollen analysis is one such indirect method, and it has been shown to provide a fairly consistent means of identifying the plants visited by bees (Ramalho et al. 1991; Imperatriz-Fonseca et al. 1993). In spite of the usefulness and versatility of this method, only a few studies of this nature have been conducted to date in the Amazon region (Absy & Kerr 1977; Absy et al. 1980, 1984; Engel & Dingemans-Bakels 1980; Kerr et al. 1986, Marques-Souza et al. 1995, 1996, 2002, 2007; Thiele & Inouye 2007; Marques-Souza 2010).

Once the floral visitors of a given plant species are known, it becomes possible to test their effectiveness in the pollination process and thus increase fruiting or reduce the risk of extinction of endangered species (Kevan & Imperatriz-Fonseca 2002). For the bees, an understanding of their main pollen sources may allow us to establish plantations that provide them with pollen and consequently lead to the stability and productivity of colonies (Kerr et al. 1986). Furthermore, the knowledge and understanding of the local flora capable of supporting beekeeping activities decreases the need to introduce exotic species and makes beekeeping (with native bees) a practice that is both ecologically correct and potentially sustainable.

Thus, the aim of this study was to utilize the pollen analysis method to identify the plants used by fourteen species of Meliponini that occur along the Rio Negro channel in Amazonas, Brazil.

 

MATERIAL AND METHODS

The pollen material used in this study was collected and kindly provided for this study by a team (M. Mazucato and S. R. M. Pedro) led by Dr. João Maria Franco de Camargo (in memoriam) during a collection expedition held between July 15 and August 15, 1999 (rainy season). The natural nests from which the samples were obtained (pollen pots) were located along an approximately 1600 km stretch of the Rio Negro and its tributaries located between the Amazonian municipalities of Manaus and São Gabriel da Cachoeira (Fig. 1). The species studied, the locations for the collection of pollen pots, their geographical coordinates and the number of pots used for each species are listed in Table I.

Each pollen pot was considered as one sample. Pollen samples were extracted directly from storage closed pots collected in the natural nests of the bee species listed in Table I. Pollen extraction from pollen storage pots was done using 5 mm diameter sterile straws. The whole content of the pollen pots were homogenized with spatulas in Petri dishes, afterwards the samples were weighed and 0.5 g of each sample was stored in a test tube containing 3 ml Acetic Acid. After sufficient time, the samples were chemically processed via acetolysis (Erdtman 1960). Slides were prepared by mounting the samples in glycerin-gelatin and sealing them with paraffin. Three slides were prepared for each sample. For some bee species, different sample weights were taken from each pollen pot. Test results indicated no significant difference in the richness of pollen types weighing 0.5g or above. Furthermore, when new types were found in samples with heavier weights, they were characterized by an extremely low abundance of pollen. For this reason, we decided to use the sample weight of 0,5 g for each pollen pot.

Pollen types were determined by comparing them to slides from the pollen collection of the Palynology Laboratory of the Instituto Nacional de Pesquisas da Amazônia (INPA) and by consulting the specialized literature. Six hundred pollen grains were counted per sample to figure out their relative abundance. We followed Ramalho et al. (1985) in defining a minimum representation of 10% to consider a plant as attractive to a given bee species. To define the occurrence of "temporary specialization" events (concentrated collection from a specific pollen source), we established a minimum representation of 90% of a single pollen type in one sample. Data on the flowering phenophase of the species present on the pollen spectra were obtained from the information found on the labels of specimens from the INPA Herbarium.

The patterns of trophic overlap between bee species were evaluated according to the Schoener Index (1968), which is given by the following formula: S = 1 – 0.5 Σ(Pxi Pyi), where S = diet overlap; Pxi = proportion of food item i in the diet of species x; Pyi = proportion of food item i in the diet of species y. This index varies from 0 to 1. The overlap is considered to be biologically significant when S is equal to or greater than 0.6 (Zaret & Rand 1971; Wallace 1981). We also calculated the niche overlap indexes for the allopatric species. While the values we obtained do not have real biological value, they indicate the potential of such species to compete in cases of co-occurrence. The data for the abundance of pollen types were used to perform a cluster analysis for pairing based on Bray Curtis Index. The resulting graph is shown in an UPGMA format.

Voucher specimens of the bees taken from the analyzed nests were deposited in the "Camargo" Collection – RPSP of the Biology Department of the Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo. Pollen slides were deposited in the Palinoteca of the Instituto Nacional de Pesquisas da Amazonia (INPA). João M. F. Camargo identified the bee species according to the classification proposal of Camargo and Pedro (2008). The plant nomenclature follows Tropicos (Missouri Botanical Garden – MOBOT) and the classification proposal APGII.

 

RESULTS

An analysis of 104 pots of pollen led to the identification of 78 pollen types, with 47 of those being identified at species level belonging to 36 botanical families (Table II). Of the total number of recorded plants, 39.7% had a confirmed flowering phenophase during the months of June, July and August. On average, the pollen pots samples contained between one and five pollen types. The bee species with the broadest pollen spectrum were Trigona williana and Trigona cilipes (nest 22), each one with fifteen pollen types, while the narrowest pollen spectrum was recorded for Scaura sp. gr. tenuis (nest 14), with only two pollen types. The lowest average of pollen type per spectrum was recorded among Scaura species (4.4). For this genus, fewer bee species and an equally low number of pollen pots (14) were evaluated; however, when we evaluated the content of each pollen pot, we noticed the same average amount of the other species from the other two genera (Trigona and Partamona) that were studied.

The most commonly pollen type was Myrtaceae, which was present in 30.1% of the pollen samples analyzed. The species considered attractive (frequency > 10%) were the following: Alchornea sp., Aptandra liriosmoides, Astrocaryum sp., Attalea maripa, Bactris gasipaes, Bellucia imperialis, Burdachia prismatocarpa, Byrsonima sp., Cassia sp., Cecropia sp., Citharexylum macrophylum, Coco nucifera, Copaifera multijuga, Desmodium sp., Dioclea sp., Elaeis guineenses, Euterpe precatoria, Isertia hypoleuca, Laetia suaveolens, Lasiacis sp., Leopoldinia pulchra, Lindackeria paludosa, Mauritia flexuosa, Miconia sp., Piper sp., Pourouma sp., Ryania speciosa, Sapium sp., Schefflera morototoni, Scleria sp., Spondias mombin, Swartzia pendula, Tachigali hypoleuca, Trymatococcus amazonicus, Vismia sp., Vitex triflora and Zanthoxylum rhoifolium (Table III). Among these species, Alchornea, Astrocaryum, Ba. gasipaes, Byrsonima, Cassia, C. multijuga, E. guineenses, E. precatoria, L. corymbulosa, L. paludosa, M. flexuosa, Miconia, Pourouma, Scleria, T. hypoleuca and Z. rhoifolium triggered temporary specialization events (frequency > 90% in one given pot).

We registered 41 events of temporary specialization (frequency > 90%); six among 37 analyzed pots of Trigona, six among 14 pots of Scaura and 29 among 53 pollen pots of Partamona. The cluster analysis indicated that the closest associations were not based on the taxonomic proximity of the bee species (Fig. 2). None species had pollen spectra from all pots grouped together. For the overlap of the pollen niche (Table IV), only one pair of allopatric species, namely Partamona pearsoni and Partamona ferreirai (nest 12), and two nests of P. mourei (nests 6 and 9) showed a biologically significant overlap (greater than 0,6). However, one species from each pair had only one pot of pollen analyzed.

 

 

 

 

DISCUSSION

The clustering pattern of the nests did not reveal any pollen collection pattern that was characteristically inter- or intra-specific. These findings are in contrast to much of the previous literature regarding utilization of pollen resources by bees, in which the phylogeny (degree of relationship among taxa) and especially the phylogenetic/location association of nests were found to be the main determinants in the composition of the pollen spectra (Sommeijer et al. 1983; Biesmeijer & van Nieuwstadt 1997; Nagamitsu et al. 1999; Biesmeijer and Slaa 2004). In a study of three Trigona species (sensu stricto), for instance, was found a greater overlap in intra-specific pollen niches than among species of the same genus (Eltz et al. 2001).

Considering that the analysis presented here is based on naturally occurring nests, we believe that an explanation for the clustering pattern we found could be related to the fol lowing two factors: the location of the nests and the sharing of resources. Because the frequency of Meliponini nests inside the forest is usually low (Michener 1946; Hubbell & Johnson 1977; Oliveira et al. 1995), we hypothesize that some nests may be just as isolated from the others in the same sampling area as from others located in different sampling areas. In this way, the succession of massive and rapid flowering events at the various locations where the bees are present would explain the existence of pots of distinct nests being grouped in one set and pots from the same nests not being grouped (Fig. 2).

The second factor relates to nests located in such a way that there would be an overlap in the different bees' collection areas. In this case, there is the possibility of shared resources among the different species of bees, which would make it possible to find some species of plants being shared among nests in the same sampling point regardless of the bee species, while the main pollen type in the spectra of each bee species would be different (Ramalho et al. 2007). This pattern was clearly observed among the Trigona species from the Foz do Padauari sampling point (nests 19, 20, 21 and 26), among which some pollen types were shared with antagonic abundances (Table III). Another example was found at the Tapurucuara-mirim sampling point between the species P. ferreirai and Partamona vicina. P. ferreirai focused its foraging activity on Copaifera multijuga, with the pollen spectrum of all pots showing the prevalence of this plant, apart from one single pot. On the other hand, for P. vicina we observed the prevalence of the same plant, C. multijuga, in only one pot, suggesting that the both species could have succeeded in collecting this resource.

Sharing of pollen resources among different species of bee has been reported in several studies on Atlantic vegetation. However, it is rare to find the same flower as the major source of pollen for the different species of bees being compared (Ramalho et al. 2007). A vast niche overlap was reported for the pollen sources of Meliponini and Apis mellifera L. 1758 in the studies performed in the Atlantic forest. Such overlap was attributed to very productive flowering, where the chances of competition are lower (Ramalho 1990; Ramalho et al. 1991, 2007). Given the speculative nature of the explanations of fered here, we suggest that additional systematic research is needed to address the issue of the sharing of pollen resources in the natural environment of the Amazon region.

The biologically significant overlap in the pollen niches reported here have no real biological value because the bee species with overlapping niches did not occur in the same locations. However, it may be important to consider the potential characteristics of the plants involved in the overlap (in this particular case, Astrocaryum sp. and C. multijuga) for beekeeping initiatives and to fully realize the importance of these plant species for bees. It is also noteworthy that the four species whose niches overlapped belong to the genus Partamona; the nests of one pair were found in Igapó vegetation (wetland) and the other in Terra firme vegetation (land).

The data obtained here for Trigona williana confirm those from Marques-Souza et al. (1996), who, in their work with the same species, reported abundant pollen collection in species from the genera Attalea and Bellucia. Besides these two species, the authors identified 56 more pollen types collected by T. williana over a 1-yr period. They observed that the lowest total number of pollen types was collected during the rainy season. According to the authors, the competition for food intensifies during that season as the supply diminishes and, in this case, the strategy of mass collection associated with aggression may lead to an increase in the pollen spectrum. In the present study, however, the amplitude of the pollen spectrum per pot of pollen analyzed was not greater for Trigona than for any other genera analyzed.

Although the pollen grain type Myrtaceae was found in 30.1% of the pollen pots, its frequency was not sufficiently high for it to be considered attractive. We believe that this fact may be related to the onset of the flowering phenophase of some widely distributed Myrtaceae species, because pollen from plants of this family is usually intensively collected when available (Absy et al. 1984; Marques-Souza et al. 1993, 2007; Ramalho et al. 1989, 2007). Moreover, there are many reports of the pollination of Myrtaceae being attributed to the Meliponini (Gressler et al. 2006; Cortopassi-Laurino & Ramalho 1988).

Two types of pollen from Cyperaceae (Scleria and Lasiacis), collected only by T. recursa, Trigona sp. gr. recursa and Scaura tenuis, were considered attractive. This is particularly interesting because the Cyperaceae family does not have flowers that are considered attractive to bees and its pollen is light and dry, consistent with anemophily pollination (Vogel 1954; Faegri & Pijl 1979; Fenster et al. 2004). One possible explanation for this finding may be pollen shortage, a phenomenon previously described in Meliponini by others (Ducke 1902; Adams et al. 1981; Terrell & Batra 1984). Alternatively, there may be floral traits that attract visitors to the flowers; studies on pollen morphology of the species Pariana (Poaceae) and the presence of insects in the flowers suggest possible involvement of insects in its pollination mechanisms (Salgado-Labouriau et al. 1993). The authors hypothesize that the graminoids in the understory of tropical forest may require the involvement of insects for pollination when anemophily is compromised by moisture.

Along the same lines, other pollen types from anemophilous plants have been recorded (Alchornea, Cecropia, Pouroma and Piper). Just as in Cyperaceae, these plants do not possess features obviously attractive to bees (Vogel 1954; Faegri & Pijl 1979). However, all the genera mentioned produce copious amounts of pollen and this might be a very important feature for bees that continuously need pollen in large quantities to replenish brood cells (Michener 2000). Furthermore, collection of anemophilous pollen may be further intensified in periods of pollen shortage; in the Amazon, this corresponds to the rainy season when there is a reduced number of species in the flowering phenophase, which makes pollen less available as a function of the high humidity and constant rainfall (Schaik et al. 1993; Bentos et al. 2008).

The species of Arecaceae corroborate the hypothesis of attractiveness due to resource abundance. In our study, only C. nucifera, Euterpe precatoria and Leopoldinia pulchra belong to the group of palm trees primarily pollinated by bees and, secondarily, by beetles (Listabarth 1996; Henderson et al. 2000). The other genera, namely Astrocaryum, Bactris, Attalea, Mauritia and Elaeis, belong to the cantharophilic group, in which bees are secondary pollinators (Storti 1993; Henderson et al. 2000; Tandon et al. 2001). Regardless of the effectiveness of bees as pollen vectors for palm trees, the abundance and constant supply of pollen throughout the year seems to make Arecaceae an especially important resource for Meliponini (Henderson 1986; Tomlinson 1990; Storti 1993; Henderson et al. 2000). In a study of T. williana, eleven species of palm trees were recorded, with of the majority of them making pollen available for more than two months, including some species such as A. maripa and C. nucifera that were recorded in the pollen spectra for more than ten months (Marques-Souza et al. 1996).

Although not as prolific in pollen production as the previously mentioned species, C. macrophylum and Isertia hypoleuca were considered attractive for the Scaura and Trigona species, respectively. The floral morphology of cogeneric species Citharexylum myrianthum Cham. is compatible with the phalenophily syndrome. Previous studies have reported moth visits and their effectiveness in this mechanism of pollination and these studies indicated that Meliponini acted as pollen robbers (Rocca & Sazima 2006). Likewise, the morphology of I. hypoleuca is consistent with ornithophily pollination syndrome, in that visits by hummingbirds have been recorded at an appropriate frequency to make them potential pollinators (Giacomini & Webber, unpublished data).

Among the species whose morphology is consistent with melittophily syndrome, many are not effectively pollinated by the Meliponini we studied here. This is mainly due to the small size of these bees, which does not allow for legitimate visits, and also to the destructive and robber habits of some species, especially of Partamona and Trigona. Among the pollen types of melittophilous plants that are not pollinated by Meliponini are those from species with poricidal anthers such as Cassia spp., Miconia sp. and B. imperialis, which require floral visitors capable of vibrating the anthers to remove the pollen ("buzz pollination") (Buchmann 1983; Renner 1983). Because the bees we studied are non-vibrating, it appears that Trigona spp. damage the anthers with their mandibles and then rob the pollen (Renner 1983), while the remaining bees either use the hole produced by Trigona spp. to collect pollen or act as "garbage collectors" by removing the pollen remaining after the collection by vibrating bees (Wille 1963).

Another group of melittophilous plants not pollinated by the bees we studied here includes Malpighiaceae (Byrsonima and B. prismatocarpa), two species of Fabaceae (S. pendula and Dioclea sp.) and one species of Salicaceae (R. speciosa), which are only pollinated by larger solitary bees. The Malpighiaceae flowers have oil glands in their sepals and are mainly pollinated by solitary bees (Centridini, Tapinotaspidini and Tetrapediini tribes) specialized in collecting oils, that they use as larval food and nest-construction material (Teixeira & Machado 2000; Machado 2004; Rêgo et al. 2006). The Fabaceae (S. pendula and Dioclea sp.) require floral visitors larger than the Meliponini for contact to occur with the fertile parts of the flower (Lopes & Machado 1996; Pinheiro & Sazima 2007; Dutra et al. 2009), in the same way that R. speciosa is only pollinated by Euglossini bees (Martiniano, unpublished data).

C. multijuga (Freitas & Oliveira 2002), Vismia sp. (Santos & Machado 1998), S. mombin (Nadia et al. 2007), Z. rhoifolium (Bawa 1985b), L. paludosa (Flores & Webber, unpublished data), Desmodium sp. (Willmer et al. 2009) and T. hypoleuca (Venturieri 1997) are among the species visited and potentially pollinated by the Meliponini we studied here. In addition to these species, the Meliponini are thought to influence the pollination mechanisms of Vitex spp., L. suaveolens, S. morototoni and Sapium spp. because, although no specific data is available in the literature, these species have a floral morphology consistent with pollination by insects, and they are frequently found in the pollen spectra of Meliponini from the Amazon (Absy et al. 1980, 1984; Engel & Dingemans-Bakels 1980; Marques-Souza et al. 1995, 1996).

Based on the results presented in this study and the studies by Absy et al. (1984) and Rech & Absy (in press.), and considering the large number of plants identified as pollen sources for bees, it is evident that further analyses are needed to verify the real need for artificial feeding of native bees in beekeeping in the Amazon. Although not all plants have a flowering phenophase that coincides with the rainy season, we show here that with proper planning, it may possible to define and cultivate plants that allow for the existence of pollen calendars convenient to the reality of each beekeeper. The species of Copaifera, Bactris, Bellucia, Byrsonima, Astrocaryum, Euterpe, Mauritia, Pouroma and Spondias may be especially interesting given the availability of pollen for bees and the possibility that they may be utilized further by human and animal populations for their fruits, seeds and oil. Moreover, species that usually grow spontaneously and are selectively removed by farmers, such as Cecropia, Sapium, Schefflera and Vismia, may also serve as pollen sources for bees if they are not eliminated.

 

ACKNOWLEDGEMENTS

This work is dedicated to the memory of Dr. João Maria Franco Camargo, in recognition of the brilliance of his career and the significant contributions he made in advancing our understanding of the biology of stingless bees. We thank Silvia Pedro and Caroline Scherer for reading this manuscript and making valuable suggestions, and Cleonice de Moura Oliveira, Ana Paula Moraes and Mauricio Fernandez Otarola for general helping. This work was financially supported by grants from CNPq, Processes 472563/2006–8 and 472246/2008–9, a scholarship to A. Rech, the primary author, and FAPESP process 1998/11605–9 that financially supported the Rio Negro collection expedition.

 

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Received 24/8/2010; accepted 19/4/2011

 

 

Editor: Maria Cristina Gaglianone

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