Scaptotrigona postica

Scaptotrigona postica
Scaptotrigona postica
Scientific classification
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hymenoptera
Family: Apidae
Genus: Scaptotrigona
Species: Scaptotrigona postica
Binomial name
Scaptotrigona
(Latreille, 1807)
S. postica distribution

Scaptotrigona postica (also known locally in Brazil as mandaguari) is a species of stingless bee that lives mainly in Brazil. It is a eusocial bee in the tribe Meliponini. S. postica is one of 25 species in the genus Scaptotrigona and is a critical pollinator of the tropical rain forests of Brazil. They construct their nests in hollowed sections of tree trunks, allowing for effective guarding at the nest entrance. This species shows colony structure similar to most members of the Meliponini tribe with three roles within the colony: queen, worker, and male. S. postica individuals have different forms of communication from cuticular hydrocarbons to pheromones and scent trails. Communication is especially useful during worker foraging for nectar and pollen through the Brazilian tropical rain forests. S. postica is a very important pollinator of the Brazilian tropical rain forests and is widely appreciated for its honey. Stingless bees account for approximately 30% of all pollination of the Brazilian Caatinga and Pantanal ecosystems and up to 90% of the pollination for many species of the Brazilian Atlantic Forest and the Amazon.[1]

Taxonomy and phylogeny

Scaptotrigona postica is one of the 25 species in the genus Scaptotrigona, a eusocial genus of bees. It was first described by Pierre André Latreille in 1807. In the past, it has also been called Melipona postica, Trigona postica and Trigona rustica. This bee is a member of many taxonomic sub groups including the subclass pterygota (winged insects), suborder apocrita, and subfamily Apinae (stingless bees). These groups of bees are winged, have a social hierarchy, and do not have defensive stingers. Instead they bite and try to enter in body orifices as nose and ears. This species can be very aggressive against humans that approach its nest. Other similar species in this genus include Scaptotrigona hellwegeri, Scaptotrigona mexicans and Scaptotrigona pectoralis.

Queens, workers, and males

Scaptotrigona postica are medium-sized, averaging 1.2 cm in length and cross-sectional area of 5.3 mm2. They appear dark gray with some sections of dark yellow in color, with black eyes.[2]

Queens are the largest bees in the nest, averaging 38–50 mg, and are identifiable by their swollen abdomens.[3] Also, they have more of the yellow coloring than the workers and drones.[4] There is one queen per colony, but once virgin queens are born, they are tolerated for 15 days on average until they either leave the colony or are killed. S. postica queens cannot independently colonize, instead needing a group of workers to help build a new colony. While virgin queen bees must leave the colony, a queen holds her position for several years[3]

Workers are the smallest bees in the nest, weighing between 15–22 mg and are black in color. They assume different roles in the nest based on their age.[5][6]

0 days old = produce wax
16–20 days old = provision cell broods
21–35 days old = colony cleaning
21–45 days old = nectar reception and dehydration
31–40 days old = colony defense
26–60 days old = foraging

Drones are almost identical in size as the workers, but weigh slightly more.[4] They weigh on average 17–30 mg and are black in color. The drones are the male bees hatched from unfertilized eggs. Their role is to mate with the queen to produce female bees. They do not participate in many other activities.[5]

Nest

Exterior of an S. postica nest

Scaptotrigona postica nest in partially hollow sections of trees in the tropical rain forests of Brazil. The nests range from 3–7 meters above ground with a canopy overhead, approximately 15–20 meters above the nest.[2] One of the common trees nested by S. postica is the Caryocar brasiliense, also known as the cerrado-tree.[7]

The nest consists of inner brood cells and a short entrance tube. The brood cells are sometimes compacted into combs and large wax pots for storage of honey/pollen. The cells are composed of cerumen, are vertical in shape, and open at the top of the cell. The entrance to the nest has an average cross-sectional area of 143.5 mm2 and is guarded by about 8 guards. These bees stand at attention near the entrance, occasionally flying back and forth in front of the entrance.[2]

Each nest contains one colony of S. postica. It carries between 2,000–50,000 individuals, averaging 10,000 bees per colony.

Distribution and habitat

Scaptotrigona postica is found in the southern, central-western and northern regions of Brazil as the dense tropical rain forests provide ideal nesting locations.[8] These bees maintain an average nest temperature of 32˚C,[9] which is a few degrees above the average temperature of the Brazilian rain forests (27˚C). With the addition of an insulating layer, the nest temperature can be easily maintained in this environment. S. postica have also been found in Peru but are much more common in Brazil.[9]

Colony cycle

Initiation

Worker bee swarming initiates a new colony. These bees occasionally invade the nests of nearby bee species. New nests house up to three virgin queens during initiation. The queen arrives at the new colony within 5 days of the beginning of swarming. While there can be three virgin queens to begin a nest, the workers will kill two of them to leave a single, reproductive queen for the nest.[3][10]

Growth

The growth of the colony depends on nest productivity. During colonization, productivity is low, restricting population growth. As productivity increases, colonies begin male production, increasing overall population growth until reaching an average size of 10,000 individuals. This growth is season dependent. During the rainy season, colony growth rate raises due to increased resource availability.[11]

Lifespan

The average lifespan of S. postica workers ranges from 30–40 days. They have a low mortality rate during the initial stages of life because they do not leave the nest. Death of individuals becomes significant after approximately 15 days and continues increasing until about 40 days. Unlike the worker bees, the queen bees can live for multiple years, averaging a longer lifespan.[12]

Male Production

Male production depends on the season. Production of males is restricted during food shortages, creating short periods of male production with longer periods of female production. Males are produced by unfertilized eggs laid by the workers.[13]

Communication

Scaptotrigona postica communicate to recognize nest-mates, identify the caste of any individual bee, locate food, and signal danger.

Cuticular hydrocarbons

Cuticular hydrocarbons are waxy coatings on S. postica bodies that signal the hierarchy and original colony of any bee. They are also important anti-dessicants. Workers have cuticular hydrocarbons lacking oxygens while the drones have more oxygenated compounds.[5] Hydrocarbons also provide social dominance and fertility cues that are important when determining the queen during colonization.[14]

Scent markers

Scaptotrigona postica workers leave scent paths between the nest and food sources, facilitating the successful foraging of others. The threshold distance from food to nest for the scent trail is 11–12 metres (36–39 ft), although the flight radius from the nest is larger (600 metres (2,000 ft)).[10] These marks last about 15 minutes before dissipating. Workers follow the tracks of other populations of the same species, increasing foraging success of both colonies. These scent substances are composed of two different ketones: 2-heptanone and 2-nonanone.[14]

Communication for reproduction

The specific scents that attract drones to virgin queens prior to reproduction are 2-alcohols and 2-ketones. The 2-alcohols attract the males from long distances to the virgin queen, while 2-ketones induce copulatory attempts when the male is closer to the queen.[15] These compounds have been found in the queens’ mandibular glands but are absent in those of the worker female S. postica[15]

Reproduction

Queen bees are the colony reproductive heads. While there is only one queen per colony, workers produce males without mating. However, these hemizygous individuals will always be male. So, eggs can be laid by the unfertilized females (workers) or the fertilized females (queens).

Mating

Virgin queens are most attractive to workers.[3] Males are attracted to the queens via olfactory signals composed of hexyl hexanoate.[16] These scents indicate the queen's reproductive status.[17] S. postica males respond to the pheromones of virgin queens and congregate in groups of variable size at the entrance of the nest. These groups can be from just a few individuals up to thousands of S. postica males.[18] The individuals of the group become a compact swarm as some drones sit on the backs of others. While the drones compete to mate with the virgin queen, they do not act aggressively towards each other. These individuals will quickly disperse upon any intrusion, extra commotion, or disturbance due to an alarm pheromone that spread from individual to individual.[18] Queens make one mating flight. The males lose their genitalia during mating, only inseminating one female. Flights generally occur during the afternoon, with low flight activity in the morning hours. When mating with the queen, the S. postica drones assume an upright posture, antennae stretched as far and outward as possible.[18][19] The queen will store the spermatozoa, returning to the nest to lay her eggs which she fertilizes in the laying process with remarkably few sperm per egg.[8]

Genetic relatedness

The genetic relatedness of individuals depends on the egg. The worker eggs are hemizygous, only containing genetic information from the worker. Thus, all offspring from one worker are genetically identical, also known as "full sisters".[20] The fertilized eggs of the queen contain genetic information from the queen and from one of the up to 6 mates of the female. This increases the genetic variance in the offspring. Furthermore, the drones mating with the queen are unrelated to her due to drifting of drones between colonies.[21][22] This decreases the genetic relatedness between fertilized offspring.The overall genetic relatedness within a colony for S. postica is between approximately .70 and .85, averaging around .80. This suggests that while mainly workers produce males, queens also produce male offspring, not entirely losing in the conflict between workers and queens for male production.[20]

The costs of hemizygous male production include inbreeding due to decreased genetic variance and producing nonviable or sterile males. To prevent this, drones drift between colonies.[22] However, there are few populations within the flight radius, so drone genotypic diversity is low.

Sex determination

Sex is determined through controlled fertilization of eggs. Drones are the fertilizers of the nest and will only fertilize the eggs laid by the queen of the colony. These fertilized eggs are heterozygous with complementary sex-determining loci and will always become female. Since drones do not fertilize the worker bees, the worker eggs are haploid, and they produce male offspring. However, workers are not always laying eggs.[13] Thus, male production is limited to certain periods of time (see Male Production). While the workers of S. postica produce approximately 95% of all males, the queen still produces that remaining 5% of males. The queen will release some haploid eggs among her main diploid eggs. However, after the queen has produced a certain small number of male offspring, she will revert to producing females only.[23]

Worker-queen conflict

Conflict exists between the egg-laying females in the colony. Workers can only produce males while the queen can produce females and males. Workers lay their eggs in cells after the queen has laid hers setting up a larval competition.[24] Worker eggs are larger, more rounded, and laid on the upper inside wall of cells. If the queen does not re-check the cells, the eggs of the workers will produce males. However, if other workers or the queen checks on a cell and sees the unfertilized egg, they will eat it. This shows a competition between the egg-laying females of the colony.[11][25] Furthermore, there is conflict between the larvae of both the worker and the queen. If there are two eggs in a cell, the larvae from the worker egg will develop more rapidly and devour that of the queen egg. The reciprocal has not been observed.[24]

Thermoregulation

Nest location helps regulate nest temperature. However, S. postica workers can help warm or cool the nest. At low temperatures, the bees mass incubate the brood chamber, increasing temperature. Cerumen coverings, produced by workers, insulate cold spots. During overheating, bees evacuate the nest and reduce the temperature by fanning. There is direct cooling via evaporation due to nest location. The temperature homeostasis is important because of the hot climate of the tropical Brazilian rain forests.[26]

Diet

In a study carried out in São Paulo, the main plant used by S. postica for both pollen and nectar was Eucalyptus, a popular introduced tree in the area.[27] Pollen grains containing protein from Eucalyptus could be found in the midguts of all members of the S. postica colony. These pollen grains are digested fully between 6 and 28 hours. The protein requirements for S. postica differ based on the role and age of the individual. Worker and queen bees have similar protein requirements (between 20 and 200 pollen grains).[4] Larvae ingest a significantly higher amount of pollen (between 1000 and 2300 pollen grains), as the protein is essential during development.

Predators and defense

Predation

A main predator of S. postica is the sphecid wasp Trachypus boharti. This wasp is also found in Brazil and exclusively preys on the males of S. postica. The wasps hover near the entrance of the nest in groups averaging to 11 wasps in a group. These wasps capture up to 50 S. postica drones per day close to the entrance of the nest.[28] The drones hover at the entrance of the colony waiting for emerging female queens to mate with. It captures the individual and preserves it using a secretion from the wasp's post-pharyngeal glands.[29] Fortunately for S. postica, these predation attempts are generally unsuccessful as T. boharti only captures a male drone 7% of the time. Most of these failed attempts are due to conflict with other wasps (interfering with the flight path, collisions, and competition).[28] Furthermore, if a wasp captures a different individual of the colony (mainly all female bees), it immediately releases the individual with no harm done. While the T. boharti only predate the drones of S. postica, they do not seek specifically those individuals, rather they are attracted to all S. postica and select their prey after capture.[28]

Defense Methods

The defense for S. postica nest is to have on average 8 workers guarding the front of the nest at all times. Sometimes the guards are sitting nearby and, at others, they fly back and forth across the entrance.[2] These bees are part of the tribe Meliponini, which do not have stingers. However, S. postica guard bees have been observed to bite nest intruders as they alert the other colony members through pheromone signaling.[28] These alarm pheromones contain 2-heptonal and other ketones as active substances.[14] S. postica workers also will display a specific leg posture when other members of the nest or other organisms attempt to take cerumen from the cubiculae (structures located on the hind legs functioning as pollen baskets).[30]

Human importance

Pollination

Scaptotrigona postica are pollinators for plants in the Brazilian rain forests. S. postica exploit a smaller number of the many plant species. The main flower type visited by this species on the campus of São Paulo University was that of Eucalyptus, making up over 45% of the pollen collected by the workers. Some secondary sources for pollen and honey were Mimosa daleoides, Lithraea molleoides, Leucaena leucocephala, and Piptadenia gonacantha.[27]

As pollination is vital for the plants in the Brazilian rain forests,[1] some plant species have developed pheromone mimicry to attract the drones of S. postica. Virgin S. postica queens have a mixture of 2-alkanols in the pheromones that attract the drones for mating. Many Orchidacae species common in Brazilian rain forests, such as Mormolyca ringens, have a similar mixture of alkanes/alkenes that will attract those same drones to the flower. Following the attempted "copulation" of the drone with the flower, the chemical composition of the flower’s mimicked pheromone changes so that it does not attract any more males.[31]

Pesticides

One insecticide in Brazil is Fipronil which inhibits GABA receptors of the nervous system, resulting in seizures, paralysis, and death. S. postica is in contact with Fipronil which is extremely toxic to bees. Compared to other bees, S. postica tolerate higher doses of Fipronil, but the toxicity is still high.[32] Another toxic insecticide widely used in Brazil is Imidacloprid. Similar to Fipronil, S. postica are relatively more tolerant of this insecticide. The route of intoxication is very important in determining how lethal Imidacloprid is to the S. postica bees. Imidacloprid is significantly more toxic to S. postica through topical exposure compared to consumption of the insecticide. The increase in use of pesticides could cause a decline in pollinators like S. postica hurting the environments of Brazil.[1]

Antiviral properties

Scaptotrigona postica creates propolis with plant secretions, saliva, and wax. It seals the nest but also has significant antiviral properties. The propolis from S. postica reduces production of pocornavirus 64-fold, production of influenza virus 32-fold, and production of measles virus 8-fold. It can decrease the replication of rubella virus at a rate of 103.[33]

References

  1. 1 2 3 Soares, HM; CRO Jacob; SM Carvalho; RCF Nocelli; O Malaspina (June 2015). "Toxicity of Imidacloprid to the Stingless Bee Scaptotrigona postica Latrielle, 1807 (Hymenoptera: Apidae)". Bulletin of Environmental Contamination and Toxicology. 94 (6): 675–680. doi:10.1007/s00128-015-1488-6.
  2. 1 2 3 4 Couvillon, MJ; T Wenseleers; VL Imperatrix-Fonseca; P Nogueira-Neto; FLW Ratnieks (2008). "Comparative study in stingless bees (Meliponini) demonstrates that nest entrance size predicts traffic and defensivity". Journal of Evolutionary Biology. 21: 194–201. doi:10.1111/j.1420-9101.2007.01457.x. Retrieved 23 September 2015.
  3. 1 2 3 4 Nogueira-Ferreira, FH; EV Silva-Matos; R Zucchi (16 June 2009). "Interaction and behavior of virgin and physogastric queens in three Meliponini species (Hymenoptera, Apidae)". Genetics and Molecular Research. 8 (2): 703–708. doi:10.4238/vol8-2kerr008. Retrieved 23 September 2015.
  4. 1 2 3 do Carmo Zerbo, A; RLM Silva de Moraes; MR Brochetto-Braga (May 2001). "Protein requirements in larvae and adults of Scaptotrigona postica (Hymenoptera: Apidia, Meliponinae): midgut proteolytic activity and pollen digestion". Comparative Biochemistry and Physiology B. 129 (1): 139–147. doi:10.1016/S1096-4959(01)00324-4.
  5. 1 2 3 Poiani, SB; ED Morgan; FP Drijfhout; C da Cruz-Landim (22 April 2014). "Separation of Scaptotrigona postica workers into defined task groups by chemical profile on their epicuticle wax layer". Journal of Chemical Ecology. 40 (1): 331–340. doi:10.1007/s10886-014-0423-3. Retrieved 23 September 2015.
  6. ↑ van Veen, JW; MJ Sommeijer; F Meeuwsen (November 1997). "Behaviour of drones in Melipona (Apidae, Meliponinae)". Insectes Sociaux. 44 (4): 435–447. doi:10.1007/s000400050063. Retrieved 22 September 2015.
  7. ↑ Anotnini, Y; RP Martins (July 2003). "The value of a tree species (Caryocar brasiliense) for a stingless bee Melipona quadrifasciata quadrifasciata". Journal of Insect Conservation. 7 (3): 167–174. doi:10.1023/A:1027378306119.
  8. 1 2 Engels, W (1987). "Pheromones and reproduction in Brazilian stingless bee" (PDF). International Symposium on Insects. 82 (3): 35–45. doi:10.1590/S0074-02761987000700009. Retrieved 23 September 2015.
  9. 1 2 Sung, IH; S Yamane; S Hozumi (2008). "Thermal characteristics of nests of the taiwanese stingless bee Trigona ventral is hoozana (Hymenoptera: Apidae)" (PDF). Zoological Studies. 47 (4): 417–428.
  10. 1 2 Kerr, WE; R Zucchi; JT Nakadaira; JE Butolo (December 1962). "Reproduction in the Social Bees (Hymenoptera: Apidae)". Journal of the New York Entomological Society. 70 (4): 265–276. Retrieved 21 September 2015.
  11. 1 2 Rolandi Bego, L (1990). "On social regulation in Nannotrigona (Scaptotrigona) postica Latreille, with special reference to productivity of colonies (Hymenoptera, apidae, meliponinae)". Revista brasileira de entomologia. 34 (4): 721–738. Retrieved 23 September 2015.
  12. ↑ "Division of Labor, average lifespan and life table in nannotrigona (scaptotrigona) postica Latreille". Naturalia. 16: 81–97. 1991. Retrieved 23 September 2015.
  13. 1 2 Alves, DA; VL Imperatrix-Fonseca; PS Santos-Filho (9 June 2009). "Production of workers, queens, and males in Plebeia remota colonies (Hymenoptera, Apidae, Meliponini), a stingless bee with reproductive diapause". Genetics and Molecular Research. 8 (2): 672–683. doi:10.4238/vol8-2kerr030. Retrieved 23 September 2015.
  14. 1 2 3 Kerr, WE; A Ferreira; N Simões de Mattos (June 1963). "Communication among Stingless Bees-Additional Data (Hymenoptera: Apidae)". Journal of the New York Entomological Society. 71 (2): 80–90. Retrieved 21 September 2015.
  15. 1 2 Ayasse, M; RJ Paxton; J Tengö (January 2001). "Mating behavior and chemical communication in the order hymenoptera". Annual Review of Entomology. 46: 31–78. doi:10.1146/annurev.ento.46.1.31.
  16. ↑ Verdugo-Dardon, M; L Cruz-Lopez; EA Malo; JC Rojas; M Guzman-Diaz (15 October 2010). "Olfactory attraction of Scaptotrigona mexicana drones to their virgin queen volatiles". Apidologie. 42 (1): 543–550. doi:10.1007/s13592-011-0042-8. Retrieved 23 September 2015.
  17. ↑ Engels, W (24 March 1988). "Age-Dependent Queen Attractiveness for Drones and Mating in the Stingless Bee, Scaptotrigona Postica". Journal of Apicultural Research. 27 (1): 3–8. doi:10.1080/00218839.1988.111000773. Retrieved 22 September 2015.
  18. 1 2 3 Sommeijer, MJ; KKN de Bruijn (1995). "Drone congregations apart from the nest in Melipona favosa" (PDF). Insectes Sociaux. 46 (1): 123–127.
  19. ↑ Verdugo-Dardon, M; L Cruz-Lopez; EA Malo; JC Rojas; M Guzman-Diaz (August 2011). "Olfactory attraction of Scaptotrigona mexicana drones to their virgin queen volatiles". Apidologie. 42 (4): 543–550. doi:10.1007/s13592-011-0042-8.
  20. 1 2 Tóth, E; JE Strassmann; P Nogueira-Neto; VL Imperatriz-Fonseca; DC Queller (December 2002). "Male production in stingless bees: variable outcomes of queen-worker conflict". Molecular Ecology. 11 (12): 2661–2667. doi:10.1046/j.1365-294X.2002.01625.x.
  21. ↑ Paxton, RJ (5 August 1999). "Genetic Structure of colonies and a male aggregation in the stingless bee Scaptotrigona postica, as revealed by microsatellite analysis". Insectes Sociaux. 47: 63–69. doi:10.1007/s000400050010. Retrieved 23 September 2015.
  22. 1 2 Kerr, Warwick E.; Zucchi, Ronald; Nakadaira, Julio Takeshi; Butolo, José Eduardo (1962). "Reproduction in the Social Bees (Hymenoptera: Apidae)". Journal of the New York Entomological Society. 70 (4): 265–276.
  23. ↑ Sommeijer, MJ; TX Chinh; FJAJ Meeuwsen (January 1999). "Behavioural data on the production of males by workers in the stingless bee Melipona favosa (Apidae, Meliponinae)". Insectes Sociaux. 46 (1): 92–93. doi:10.1007/s000400050118.
  24. 1 2 Tóth, E; VL Imperatriz-Fonseca; JE Strassmann (December 2002). "Genetic and behavioral conflict over male production between workers and queens in the stingless bee Paratrigona subnuda". Behavioral Ecology and Sociobiology. 53 (1): 1–8. doi:10.1007/s00265-002-0543-6.
  25. ↑ Tóth, E; DC Queller; A Dollin; JE Strassman (February 2004). "Conflict over male parentage in stingless bees". Insectes Sociaux. 51 (1): 1–11. doi:10.1007/s00040-003-0707-z. Retrieved 23 September 2015.
  26. ↑ Kerr, WE; P Rosenkranz; E Engels (1995). "Thermoregulation in the Nest of the Neotropical Stingless bee Scaptotrigona postica and a hypothesis on the evolution of temperature homeostasis in highly eusocial bees". Studies on Neotropical Fauna and Environment. 30: 193–205. doi:10.1080/01650529509360958. Retrieved 21 September 2015.
  27. 1 2 Ramalho, M (November 11, 1989). "Foraging by stingless bees of the genus, Scaptotrigona (Apidae, Meliponinae)". Journal of Apicultural Research. 29 (2): 61–67. doi:10.1080/00218839.1990.11101198. Retrieved 20 September 2015.
  28. 1 2 3 4 Koedam, D; JC Biesmeijer; P Nogueira-Neto (June 2009). "Unsuccessful attacks dominate a drone-preying wasp's hunting performance near stingless bee nests" (PDF). Genetics and Molecular Research. 8 (2): 690–702. doi:10.4238/vol8-2kerr032.
  29. ↑ Koedam, D; D Morgan; TM Nunes; EFLRA Patricio; VL Imperatriz-Fonseca (June 2011). "Selective preying of the sphecid wasp Trachypus boharti on the meliponine bee Scaptotrigona postica: potential involvement of caste-specific cuticular hydrocarbons". Physiological Entomology. 36 (2): 187–193. doi:10.1111/j.1365-3032.2010.00769.x. Retrieved 23 September 2015.
  30. ↑ Cane, JH; GC Eickwort; FR Wesley; J Spielholz (October 1983). "Foraging, Grooming and Mate-seeking behaviors of Macropis nuda (Hymenoptera, Melittadae) and use of Lysimachia ciliata (primulaceae) oils in larval provisions and cell linings". The American Midland Naturalist. 110 (2): 257–264. doi:10.2307/2425267.
  31. ↑ Flach, A; AJ Marsaioli; RB Singer; MDCE Amaral; C Menezes; WE Kerr; LG Batista-Pereira; AG Corrêa (January 2006). "Pollination by sexual mimicry in Mormolyca ringens: A floral chemistry that remarkably matches the pheromones of virgin queens of Scaptotrigona sp.". Journal of Chemical Ecology. 32 (1): 59–70. doi:10.1007/s10886-006-9351-1.
  32. ↑ Jacob, CRO; Hellen Maria Soares; Stephen Malfitano Carvalho; Roberta Cornélio Ferreira Nocelli; Osmar Malspina (2013). "Acute Toxicity of Fipronil to the Stingless Bee Scaptotrigona postica Latreille". Bulletin of Environmental Contamination and Toxicology. 90 (1): 69–72. doi:10.1007/s00128-012-0892-4. Retrieved 23 September 2015.
  33. ↑ Rabelo Coelho, G; K de Senna Villar; CA Figueiredo; JC Badari; RM Zucatelli Mendonça; MI Oliveira; S Pires Curti; PE Silva Silva; RM Do Nascimento; R Zucatelli Mendonça (10–14 November 2013). "Antviral effects of scaptotrigona postica propolis and their fractions".
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