A scientific note on the isolation and characterization of microsatellite loci of Frieseomelitta varia (Hymenoptera, Apidae, Meliponini)

FAPESP[BIOTA 2004/15801-0]

Chemical Signals in the Stingless Bee, Frieseomelitta varia, Indicate Caste, Gender, Age, and Reproductive Status

Chemical compounds on the cuticle are a rich source of information used during interactions among social insects. Despite the multitude of studies on these substances and their function in ants, wasps, and honeybees, little is known about this subject in stingless bees (Hymenoptera: Apidae, Meliponini). We studied the chemical composition of the cuticle of the stingless bee, Frieseomelitta varia, by gas chromatography-mass spectrometry (GC-MS), to investigate potential chemical variation among castes, gender, age, and reproductive status. We found differences in the cuticular hydrocarbon composition among workers, males, and queens, recording both qualitative and quantitative differences among individuals of different ages and gender. The cuticle of physogastric queens presented a chemical profile that was distinct from all other groups in the analysis, with high relative abundances of alkenes and alkadienes with 27, 29, and 31 carbon atoms. We discuss the possibility that these compounds signal a queen`s presence to the colony, thereby initiating all vital worker-queen interactions.

Nestmate recognition in the stingless bee Frieseomelitta varia (Hymenoptera, Apidae, Meliponini): sources of chemical signals

Social insects use cuticular lipids for nestmate recognition. These lipids are chiefly hydrocarbons that can be endogenously produced or acquired from the environment. Although these compounds are already described as coming from different sources for different groups of social insects, nothing is known about the source of cuticular hydrocarbons in stingless bees. We used behavioural recognition tests and cuticle chemical investigation to elucidate the role of endogenous and environmentally based cues for nestmate recognition in the stingless bee Frieseomelitta varia. We found that although newly emerged workers present specific cuticle patterns according to their nest origin, these compounds are not used for nestmate recognition, since newly emerged workers are broadly accepted in different colonies. The cerumen used in nest construction played an important role in recognition behaviour. Twenty minutes of contact with foreign cerumen was sufficient to increase the rejection rates of nestmates and separate the groups of workers according to their chemical profile. On the other hand, tests of feeding on a common diet showed no effect on chemical cuticle pattern or recognition behaviour. (C) 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Relação entre o desenvolvimento dos ovários e atividade dos Corpora Allata de operárias de Frieseomelitta silvestri languida (Hymenoptera, Apidae)

In the absence of the queen, a few workers of F. s. languida developed their ovaries forming nevertheless, only one follicle with a single oocyte which was unable to form yolk spheres. They never showed signals of degeneration or resorption. The corpora allata were homogeneous during all the 5 months of orphanage studied. Its activity might be low but constant, able to maintain the follicle entire, but unable to promote the yolk spheres assembly.

Cell death in ovarioles causes permanent sterility in Frieseomelitta varia worker bees

Frieseomelitta varia worker bees do not lay eggs even when living in queenless colonies, a condition that favors ovary development and oviposition in the majority of highly social bees. The permanent sterility of these worker bees was initially attributed to a failure in ovary morphogenesis and differentiation. Using transmission electron microscopy we found that at the beginning of the pupal phase the ovaries of F. varia workers are formed by four ovarioles, each of them composed of 1) a terminal filament at the apex of the ovarioles, containing juxtaposed and irregularly shaped cells, 2) a germarium with clusters of cystocytes and prefollicular cells showing long cytoplasmic projections that envelop the cystocyte clusters, 3) fusiform interfollicular and basal stalk precursor cells, and 4) globular, irregularly contoured basal cells with large nuclei. However, during the pupal phase an accentuated and progressive process of cell death takes place in the ovarioles. The dying cells are characterized by large membrane bodies, electron-dense apoptotic bodies, vacuoles, vesiculation, secondary lysosomes, enlarged rough endoplasmic reticulum cisternae, swollen mitochondria, pycnotic nuclei, masses of chromatin adjacent to the convoluted nuclear envelope, and nucleoli showing signs of fragmentation. Cell death continues in ovarioles even after the emergence of the workers. Once they become nurse bees, the ovaries have become transformed into a cell mass in which structurally organized ovarioles can no longer be identified. In F. varia workers, ovariole cell death most certainly is part of the program of caste differentiation.

Regression of the lateral oviducts during the larval-adult transformation of the reproductive system of Melipona quadrifasciata and Frieseomelitta varia

Toward the end of the larval phase (pre-pupa), the reproductive systems of Melipona quadrifasciata and Frieseomelitta varia workers are anatomically similar. Scanning electron microscopy showed that during this developmental phase the right and left ovaries are fused and form a heart-shaped structure located above the midgut. Each ovary is connected to the genital chamber by a long and slender lateral oviduct. During pupal development, the lateral oviducts of workers from both species become extremely reduced due to a drastic process of cell death, as shown by transmission electron microscopy. During the lateral oviduct shortening, their simple columnar epithelial cells show some signs of apoptosis in addition to necrosis. Cell death was characterized by cytoplasmic vesiculation, peculiar accumulation of glycogen, and dilation of cytoplasmic organelles such as mitochondria and rough endoplasmic reticulum. The nuclei, at first irregularly contoured, became swollen, with chromatin flocculation and various areas of condensed chromatin next to the nuclear envelope. At the end of the pupal phase, deep recesses marked the nuclei. At emergence, worker and queen reproductive systems showed marked differences, although reduction in the lateral oviducts was an event occurring in both castes. However, in queens the ovarioles increased in length and the spermatheca was larger than that of workers. At the external anatomical level, the reproductive system of workers and queens could be distinguished in the white- and pink-eyed pupal phase. The metamorphic function of the death of lateral oviduct cells, with consequent oviduct shortening, is discussed in terms of the anatomical reorganization of the reproductive system and of the ventrolateral positioning of adult worker bee ovaries. (C) 2000 Wiley-Liss, Inc.

Gender identification of five genera of stingless bees (Apidae, Meliponini) based on wing morphology

Currently, the identification of pollinators is a critical necessity of conservation programs. After it was found that features extracted from patterns of wing venation are sufficient to discriminate among insect species, various studies have focused on this structure. We examined wing venation patterns of males and workers of five stingless bee species in order to determine if there are differences between sexes and if these differences are greater within than between species. Geometric morphometric analyses were made of the forewings of males and workers of Nannotrigona testaceicornis, Melipona quadrifasciata, Frieseomelitta varia, and Scaptotrigona aff. depilis and Plebeia remota. The patterns of males and workers from the same species were more similar than the patterns of individuals of the same sex from different species, and the patterns of both males and workers, when analyzed alone, were sufficiently different to distinguish among these five species. This demonstrates that we can use this kind of analysis for the identification of stingless bee species and that the sex of the individual does not impede identification. Computer-assisted morphometric analysis of bee wing images can be a useful tool for biodiversity studies and conservation programs.

Infestation by Pyemotes tritici (Acari, Pyemotidae) causes death of stingless bee colonies (Hymenoptera: Meliponina)

We report the infestation of stingless bee nests by the mite Pyemotes tritici, which killed four colonies of Tetragonisca angustula and one colony of Frieseomelitta varia in Brazil. The first infected colony, a colony of T. angustula, came from an area between Uberlandia and Araguari, Minas Gerais. The transfer of the mites to the other colonies occurred through the transfer of infected combs and subsequent manipulations. Other colonies in the same meliponary, which had not been manipulated, were not infected. The infestation was terminated by isolating the dead colonies from the meliponary.

Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance?

The ability to discriminate nestmates from non-nestmates is critical to the maintenance of the integrity of social insect colonies. Guard workers compare the chemical cues of an incoming individual with their internal template to determine whether the entrant belongs to their colony. In contrast to honeybees, Apis mellifera, stingless bees have singly mated queens and, therefore, are expected to have a higher chemical homogeneity in their colonies. We tested whether aggressive behaviour of Frieseomelitta varia guards towards nestmate and non-nestmate foragers reflects chemical similarities and dissimilarities, respectively, of cuticular hydrocarbon profiles. We also introduced individuals of Lestrimelitta limao, an obligatory robber species, to test the ability of guards to react effectively to intruders from other taxa. We verified that foraging nestmates were almost invariably accepted, while heterospecific and conspecific non-nestmates were rejected at relatively high rates. However, non-nestmate individuals with higher chemical profile similarity were likely to be accepted by guards. We conclude that guards compare the chemical cuticular blend of incoming individuals and make acceptance decisions according to the similarity of the compounds between the colonies. (c) 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Fenologia e produtividade do Abacate (Persea americana Mill.) na Amazônia Central1

O abacateiro (Persea americana Mill., Lauraceae) é nativo da Mesoamérica e chegou à Amazônia antes dos europeus. Acredita-se que a raça aqui introduzida foi a antilhana, similar a da maioria dos abacateiros pé-franco da Amazônia de hoje. Estudos de sua fenologia podem ajudar o planejamento de seu manejo e comercialização. A floração iniciou-se na segunda metade da estação chuvosa (março/abril) e durou até meados da estação de estiagem (agosto/setembro). As árvores produziram 25±15 mil flores em 1980 e 38±28 mil flores em 1981. A frutificação iniciou-se no final da estação chuvosa (maio/junho) e a safra ocorreu em plena estação de estiagem (agosto/outubro). As árvores produziram 634±299 frutos em 1980 e 1.054±456 frutos em 1981. O vingamento foi de 2,6±1,8%, menor que os valores na literatura. Os frutos pesaram 177,7±41,2 g na safra de 1980, com 51,1±4,5% de polpa. A produtividade, estimado em 112 kg/árvore em 1980 e 187 kg/árvore em 1981, foi abaixo da média de uma árvore bem manejada no sul do Brasil. As flores foram visitadas por oito espécies de abelhas, destacando-se Trigona branneri Ckll, Frieseomelitta sp. e Partamona pseudomusarum Camargo.

Características Morfológicas e Bioquímicas do pólen coletado por cinco espécies de Meliponíneos da Amazônia Central

Durante um ano, o pólen transportado por Melipona compressipes manaosensis, Melipona seminigra merrillae, Melipona seminigra seminigra, Frieseomelitta sp. e Scaptotrigona sp. foi coletado diretamente das corbículas das operárias. Feita a identificação dos grãos de pólen constatou-se que a abelha mais generalista foi Scaptotrigona sp., seguida de Frieseomelitta sp., as quais juntas coletaram mais tipos polínicos que as três espécies de meliponas. Duas espécies de plantas: Miconia myrianthera e Myrcia amazonica, tiveram seu pólen coletado pelas cinco espécies de meliponíneos durante o ano todo. Quanto à morfologia do pólen, não houve correlação significativa que comprovasse que as abelhas coletassem o pólen de acordo com a forma, ornamentação e o tamanho dos grãos. As cinco espécies de meliponíneos coletaram pólen de diversas formas e tamanhos. Tudo indica que as abelhas coletam o pólen de acordo com os nutrientes contidos no seu protoplasma. Análises bioquímicas de alguns tipos polínicos encontrados nas corbículas das abelhas apresentaram alto teor de açúcares solúveis totais, açúcares redutores e amido.

As abelhas eussociais (Hymenoptera, Apidae) visitantes florais em um ecossistema de dunas continentais no médio Rio São Francisco, Bahia, Brasil

Highly eusocial bees (Hymenoptera, Apidae) flower visitors in a continental sand dune ecosystem from the medium São Francisco River, Bahia, Brazil. A community of highly eusocial bees in sand dunes, covered with caatinga vegetation, in the medium São Francisco River, Bahia (10º47' 37"S and 42º49' 25"W) was studied. The local climate is semi arid and hot, with mean temperature of 25.7 ºC and annual precipitation of 653.8 mm. Censuses took place every two months, from February to December of 2000. The bees were sampled on flowers with entomological nets, from 6:00 a.m. to 5:00 p.m. A total of 2,147 individuals of eight species of Apinae were found, of which Apis mellifera Linnaeus (40.2%), Trigona spinipes (Fabricius) (28.7%) and Frieseomelitta silvestri languida Moure (14.7%) were the predominant species. The diversity was H' = 1.53 and the evenness E' = 0.73. The bees were active during the whole year, but there was a significant variation in the monthly abundance of individuals (c2= 799.55; df= 35; p<0.0001). The daily activity was greater between 6:00 a.m. and 8:00 a.m. The low bee diversity observed is a consequence of the low richness of botanical species and of the small amount of sites for the bees' nests. The community of highly eusocial bees from the dunes presents organization patterns similar to those observed in other caatinga areas, albeit with some particularities.

Notas sobre a bionomia de Trichotrigona extranea Camargo & Moure (Hymenoptera, Apidae, Meliponini)

Três ninhos de T. extranea, encontrados nas matas de igapó, na localidade de Samaúma, foz do rio Daraã (64°45'35" W, 0°27'7" S), AM, Brasil, são descritos e ilustrados. Este é o único lugar onde esta espécie é conhecida. Todos os ninhos estavam em ocos de ramos secos de "Tanimbuca" - Buchenavia suaveolens Eichler (Combretaceae). Dois deles compartilhavam o oco com ninhos de Frieseomelitta sp. e um era solitário. Um ninho continha 46 células de cria, 43 operárias adultas e uma rainha fisogástrica; o segundo, 240 células, 117 operárias, 25 machos e uma rainha fisogástrica; o terceiro, 260 células, 163 operárias, uma rainha fisogástrica e uma pupa de rainha. As células são construídas na forma de cacho, como em Friseomelitta, e as células de rainha são do mesmo tamanho e forma que as de operária. Não há potes de alimento - este é o único Meliponini que se conhece que não armazena alimento. Supostamente, esta espécie tem hábitos cleptobióticos. Rainhas e machos são também descritos.

Comunidade de abelhas (Hymenoptera, Apoidea) e plantas em uma área do Agreste pernambucano, Brasil

O Agreste é uma região de transição entre floresta tropical úmida e caatinga no nordeste brasileiro. Nessa região, grande parte da vegetação nativa foi desmatada para a implantação de pastagens. Não é sabido se áreas degradadas mantém uma apifauna e flora melitófila diversificada, ou quais são associações entre abelhas e plantas que ocorrem nessas áreas. A cobertura vegetal atual é composta por pastos, vegetação ruderal e restos da vegetação nativa. Abelhas e plantas por elas visitadas foram coletadas mensalmente entre agosto de 2001 e julho de 2002, durante dois dias consecutivos entre 5h30 e 17h30. Foram coletados 1.004 indivíduos de abelhas pertencentes a 79 espécies. Apidae foi a família mais abundante e com maior riqueza de espécies (732 indivíduos e 43 espécies), seguida por Halictidae (194 indivíduos e 20 spp.), Megachilidae (47 indivíduos e 13 spp.), Colletidae (16 indivíduos e 2 spp.) e Andrenidae (15 indivíduos e 1 sp.). Foram registradas apenas três espécies de abelhas eussocais e cinco de Euglossini, dois grupos altamente diversificados nas florestas neotropicais. A ausência de abelhas sem ferrão nativas dos gêneros Plebeia, Frieseomelitta, Partamona, Scaptotrigona e Trigonisca, assim como de outras espécies de Euglossini, deve estar relacionada à falta de sítios de nidificação e à escassez de fontes de pólen e néctar nessa área degradada. Foram registradas 87 espécies de plantas melitófilas, a maioria ervas e arbustos. Árvores nativas isoladas, assim como plantas ornamentais e frutíferas cultivadas contribuem para manter parte da diversidade da comunidade de abelhas nativas.

Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees

Competition for floral resources is a key force shaping pollinator communities, particularly among social bees. The ability of social bees to recruit nestmates for group foraging is hypothesized to be a major factor in their ability to dominate rich resources such as mass-flowering trees. We tested the role of group foraging in attaining dominance by stingless bees, eusocial tropical pollinators that exhibit high diversity in foraging strategies. We provide the first experimental evidence that meliponine group foraging strategies, large colony sizes and aggressive behavior form a suite of traits that enable colonies to improve dominance of rich resources. Using a diverse assemblage of Brazilian stingless bee species and an array of artificial ""flowers"" that provided a sucrose reward, we compared species` dominance and visitation under unrestricted foraging conditions and with experimental removal of group-foraging species. Dominance does not vary with individual body size, but rather with foraging group size. Species that recruit larger numbers of nestmates (Scaptotrigona aff. depilis, Trigona hyalinata, Trigona spinipes) dominated both numerically (high local abundance) and behaviorally (controlling feeders). Removal of group-foraging species increased feeding opportunities for solitary foragers (Frieseomelitta varia, Melipona quadrifasciata and Nannotrigona testaceicornis). Trigona hyalinata always dominated under unrestricted conditions. When this species was removed, T. spinipes or S. aff. depilis controlled feeders and limited visitation by solitary-foraging species. Because bee foraging patterns determine plant pollination success, understanding the forces that shape these patterns is crucial to ensuring pollination of both crops and natural areas in the face of current pollinator declines.