Toxicity of the macerated of white and purple jurubeba flowers about bees Apismelliferas in sertao paraibano - Brazil

Allan Martins Ferreira1 Aline Carla de Medeiros2, Jussara Silva Dantas2,Rosy Carina de Araujo Ventura4 Andre Japiassu3, Edmara da Nóbrega Xavier Martins1 2 HOW TO CITE THIS PAPER and Patricio Borges Maracaja 1 M Sc.. pelo PPGSA/CCTA/UFCG – Pombal – PB - BRAZIL ALLAN MARTINS FERREIRA1 [email protected], [email protected]. ALINE CARLA DE MEDEIROS2, 2 D. Sc. Professores PPGSA/CCTA/UFCG – Pombal – PB - BRAZIL JUSSARA SILVA DANTAS2,ROSY [email protected], [email protected], [email protected] CARINA DE ARAUJO VENTURA4 3 CCTA/UFCG– Pombal – PB - BRAZIL E-mail: [email protected] ANDRE JAPIASSU3, EDMARA DA 4 PPGSA/CCTA/UFCG– Pombal – PB - BRAZIL E-mail: [email protected] 1 NÓBREGA XAVIER MARTINS AND ABSTRACT PATRICIO BORGES MARACAJA2 There are secondary components of the nectar or the pollen in some vegetal species, to can V.. 2. N. 1, 27-35. (2019) be toxics or repellentsfor their pollinators. Thus, this work had for objective to study the Toxicity of the macerated of effects from toxicity of differents concentrationsof macerated flowers of white and purple jurubeba purpleJurubebaandwhite Jurubeba, as feeding of Africanized bees in a controlled environment.Therefore, wererealizedbioassays at the Laboratory of Entomology of the flowers about bees Apismelliferas Federal University of Campina Grande, Campus ofPombal.It was used dried and crushed in sertao paraibano - Brazil flowers of the Chamber and leaddy. The powder of the flowers was weighed in three different Received: Jun 12, 2019 fractions (0,25%, 0,50% e 1,0%) and added to the candyandwater. The newly emerged Accepted: Dez 20, 2019 workers were distributed togetherof 20 insects for wood boxmeasuring 11cm in length by Published: Dez 1, 2019 Copyright 11cm in width and 7cm in height, in three replicates and control, making up 12 boxes and 240 © 2019 by authors and Scientific worker bees, were packaged in B. O. D with temperature adjusted to 32º C andhumidity of 70 Research Publishing Inc. This %. The control group received only candy and water. In view of the results obtained with the work is licensed under the research, observed that the bees of the control remained alive until the 25 days reaching a Creative Commons Attribution statistical average of 20 days and for those treated with 0,25%, 0,50% e 1,0% respectively, presented mortality in the 20th, 18th e 13th day for bees fed with paniculatum L.For International License (CC BY bees fed Dun, observed that the bees of the control remain alive up to the 4.0). 21 days reaching a statistical average of 18 days and for those treated with 0,25%, 0,50% and http://creativecommons.org/licens 1,0% respectively, presented mortality in the 17th, 13th e 12th day.The data analysis showed es/by/4.0/ Open Ac statistically significant differences between treatments and control, suggesting the toxic effect of the macerate obtained from LandSolanum albidum Dunfor Africanized bees workersApismellifera. Thus, can be concluded with the accomplishment of this work that:The bees control remained alive until the 25thand 21th dayrespectively, by treatments with Solanum paniculatum L.andSolanum albidum Dun; The treated beeswith the concentrations 0,25%, 0,50% and 1,0% of macerated flowers Solanum paniculatum L, respectively, presented mortality to the 20th, 18thand 13thday; The treated bees with the concentrations 0,25%, 0,50% and 1,0% of macerated flowers Solanum albidum Dun, respectively, presented mortality to the 17th, 13thand 12th day; Flowers of Solanum paniculatum L. andSolanum albidum Dunpresented toxicity to Apismelíferaunder controlled ambient conditions

Key Words Pollinators, Toxicity, Caatinga Flowers...

Journal of Agroindustry Sistems ISSN: 2674-7464 GVAA (2019) V.2. N.1. pp 27 - 35 Toxicity of the macerated of white and purple jurubeba flowers about bees Apismelliferas in sertao paraibano - Brazil

intermittent fevers, as well as culinary uses.It is also INTRODUCTION considered an invasive , which occupies the most varied types of soil, with the capacity for rapid colonization of open environments (including by The nectar andpollenpresentin the anthropic action) (GONÇALVES et al., 2016). flowersconstitute basically the only source of bee’s food, The purple Jurubeba belongs to the being that the nectar is an importantpower supplier, family. In Brazil, the specie is popularly known as containing sucrose, fructose and glucose,while pollen is a jurubeba, truejurubeba, jubeba, juripeba, jurupeba, rich and concentrated source of protein and minerals. juripiba, jurubebinha, jupeba, juvena, juina, Thus, in the wild, bees visit the flowers in search of food junaandjuuina. Native to Brazil, the species is found in to meet their nutritional needs (ALMEIDA et al., 2003). major proportions in the North (Para) and Northeast Northeastern flora offers several resources for regions (Alagoas, Bahia, Ceara) (BRAZIL et al., 2018). bees, such as resin, nectar and pollen, which are used as In addition to the purple, there is a specie food. These, in turn, receive transformations that generally denominatedSolanum albidumDun.,weel - originate products indispensable to the survival of these knownpopularly as white jurubeba. The two species animals (PIRES et al., 2009). belong to family Solanaceae and to the Solanum genus, According Pereira et al. (2004), the flowered play but is important to differentiate the two species in view of a very important role for the maintenance of the colonies the fact that they may have different characteristics. and the production of the bees. This production can be The white jurubeba is a native plant of the compromised due to the risk of toxic effects that some Southern Region of Brazil, occurring also in the countries may exert on them.In someregions of the country, of the Prata Basin.Common in Rio Grande doSul, bees can find plants that cause the death of the offspring especially in Central Depression.It is a perennial plant, and adult bees. These bugs can bepoisoned by pollen or reproduced by seed, its flowering occurs from the end of nectar, secretion of extrafloralnectars, and sap, of high winter until the following autumn, in a determined period, toxic content present in plants.Detzeland Wink (1993) variable from region to region. The fruits develop slowly. reports that plants that poison bees often produce little The plant occurs in clearings and edges of forests, in nectar or pollen. The big number of plants big species banks of plains and other places not flooded. Accepts contains phenolic components, alkaloids, coumarins, different types of soil, with preference for places with saponins and amino acids non-protein which are common good humidity (NETTO et al., 2016). in nectar, but may also make them toxic or repellent in the It is a shrub, erect, with up to 1,5m in face of some animals, betweenbees. height.Cylindrical stem, green on young plants and The plants, with evolution, present different greyish-green on older plants.Leaves single, isolated, strategies of self-protection and defenses, among them, the petiolate, and quite variable in shape and production of chemical substances called secondary configuration,resembling the leaves of Solanum metabolites. These substances exert an essential function variabile(NETTO et al., 2016). for the maintenance of plant life, also acting in defense of Considering the importance of bees as pollinators plants (BRANDÃO et al., 2010). of plants and for the production chain of several Once toxic, plants can cause the death of adult products,there is a need to protect them, mainly bees, interfering in the development of the colony, which Apismellifera L.in cultivation systems, so that they are not can lead these insects to extinction, causing an intoxicated by the food itself. environmental impact, because of their importance to the Thus, it is observed that some species of plants natural ecosystems.Besides involving in the productive may present themselves harmful to these beneficial process of agrosystems, many beekeepers are also harmed, insects. It is important to analyze possible plants with since these insects are responsible for the production of toxic potential, which directly contribute to the reduction honey, wax, royal jelly and propolis(WIESE, 2005). of the survival of working bee Apismellifera. In Brazil, The genderhas more than 1700 species, being research on the impact of plants such as Solanum well represented in tropical America, including Brazil.In paniculatum L. and Solanum albidum the floral and reproductive biology of species of the genus Dun.onApismellifera L. bees are scarce, making it are common characters the pollination by bees, the necessary to study the potential toxicity of these porcine dehiscence of the anthers and the predominance of organisms. alogamy.The removal of pollen from porcine anthers Against this backdrop of scarcity of information requires special behavior of the bees, the pollination of regarding the toxicity of flower maceration of these plants these flowers being called a vibration pollination to bees, this study aimed to study the effects of toxicity of (ROCHA et al., 2018). different concentrations of macerated flowers of purple Solanum paniculatum L.,commonly known as Jurubeba and white Jurubeba, as feed for workmen of purple Jurubeba, occurs throughout tropical America. It is Africanized bees in a controlled environment. attributed medicinal properties, being popularly used in the treatment of jaundice, chronic hepatitis and

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Allan Martins Ferreira, et al

MATERIALSAND METHODS and control, making up 12 boxes and 240 worker bees. Conditioned in BOD greenhouse with temperature set at The search was realized on period of 32 ° C and humidity of 70%. september2017 and september 2018 at the at the The treatments consisted of three different Laboratory of Entomology of the Federal University of fractions of flower powder (0,25%, 0,50% e 1,00%) and Campina Grande, Campus of Pombal.The flowers added to the candy(mixture of confectioners' sugar and collectsofpurple Jurubebaandwhite Jurubebawere carried honey in 5:1) and water. The insects from the control out in the caatinga area.The september month was the group received only candy and water. The extract was chosen for collect of the flowers, taking into account that placed in small plastic lids and covered with a small wire it is the season where the apex of the flowering of this mesh to prevent the insects from drowning. species occurs. The results of the samples were obtained in the It is important to note also that, in this time of the comparison of the statistical analysis between the year, the region where this study was carried out, is in treatment and control group concentrations in the unfavorable climatic conditions with respect to the experiment of macerated ingestion of flowers of purple climatic conditions.Thus, caatingavegetals species plant Jurubeba and white Jurubeba.For the analysis of the data species undergo physiological and morphological the non-parametric Log Rank Test was used in the transformations as a form of adaptation to water scarps for comparison of the survival curves. the long period of drought that had followed for several months. RESULTS AND DISCUSSION The purple and white Jurubeba flowers after being collected in the field were conducted at the Observing the results analysis, it can be verified Laboratory of Entomology of the Federal University of that there was a significant reduction in bee survival Campina Grande, Campus of Pombalfor oven drying at 40 whenfed with macerated flowers of Solanum paniculatum ° C for 48 hours and then shredded in a blender, sieved L. (Purple Jurubeba), mainly with increased diet.There is into three fine nylon meshes, resulting in a fine powder an expressive difference between the survival curves of packed in plastic tubes and properly labeled. the control in relation to the three treatments 0.25, 0.50% For the packing of the tests the insects were and 1.00%. It can be said that the survival of the bees was captured, and the workers were selected in the reduced by using the diet containing the flower extracts of honeycomb. Then distributed in a set of 20 insects per Solanum paniculatum L. (Purple Jurubeba) and that the wooden box measuring 11cm in length by 11cm in width higher mortality rates were obtained in concentrations and 7cm in height and holes in the sides closed with nylon 0.50% and 1.00% of the maceration of the flowers of this observation screen, previously lined with filter paper and plant (FIGURE 1). with glass lids. These were distributed in three replicates

FIGURE 1. Survival curves of the bees submitted to the ingestion experiment containing macerated flowers of SOLANUM PANICULATUM L. (PURPLE JURUBEBA). POMBAL, PB. 2018. Jurubeba roxa

100 Controle 0,2% 0,5% 1,0% 50

Sobrevivência (%) Sobrevivência

0 0 10 20 30 Dias

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Toxicity of the macerated of white and purple jurubeba flowers about bees Apismelliferas in sertao paraibano - Brazil

Mesquita et al (2007)reports that clinical trials Similar to the research realized by Rocha Neto et “in alive” has shown a relatively low toxicity of all parts al. (2011) with the macerated leaves of Jatropha of melon of saocaetanowhen ingested orally. However, gossypiifolia, yielding mean survival of bees of 13th, 9th toxicity and death of animals have been evidenced in and 8th day at concentrations of 0.25%, 0.50% and 1.0% laboratories when the extracts are injected intravenously, respectively.ForAzevedo et al. (2013) the bees that were as the fruit and the seed demonstrating great toxicity fed with the macerated flowers of Turnerasubulata compared to the leaves and aerial parts of the plant. presented low differences ofsurvival with respect to bees Ritter et al., (2002) Evaluating the use of fed only with candida (control bees presented 20 days of medicinal plants, reports that melon of saocaetanohas survival), specifically in concentrations of 0.25% and recognized toxicity and should be used without advice. 0.50%, presenting 20th and 17th day in survival mean, Similar results were found by Sousa et al. (2013), respectively. noting thatthe survival of workersA. melliferahad one The results of the statistical analysis of the decreasing as concentrations of the comparison between the treatment concentrations and the maceratedHeliotropiumindicumwere high,the bees fed control (witness) are in table 1, evidencing that the results only with candy remained alive on average 17 days, and were significant (P<0.0001), of the concentrations of the the bees that were submitted to the treatments of 0.25%, flower mound of Solanum paniculatum L. (Purple 0.50% and 1.0% of the flower extract of Jurubeba) applied in relation to the witness. Heliotropiumindicum, presented mean mortalities of 15th, 13th and 11th das respectively.

TABLE 1.statistical analysis of the ingestion of concentrations of Solanum paniculatum l. (purple jurubeba) and the control group in relation to the survival of workers Apis mellifera. 0,25% andcontrol 0,50% andcontrol 1% andcontrol X2 = 18,61 X2 = 181,2 X2 = 645,0

Df = 1 Df = 1 Df = 1

P<0,0001 P<0.0001 P<0.0001 Significant Significant Significant Md. Control = 20days Md. Control = 20days Md. Control = 20days Md. Trat. =20days Md. Trat. =18days Md. Trat. =13days Md. = Medium

It is observed that when the bees were fed with Catoleof Rocha, Fagundes, JacarauandAreiaand that his the maceration ofSolanum paniculatum L. fitness trait is supplying nectar. (whiteJurubeba), showed low survival in relation to bees According to the survival curves of fed only with candida (the control bees remained alive for Apismelliferathat were fed the concentrations of 25%, 25 days), specifically in the concentrations 50% and 50% and 100% of macerated flowers of Solanum albidum 100%, presenting 18 and 13 days in average survival Dunand those fed only with candi (control), it can be respectively,the bees fed 25% of the macerated Mulungu verified that the bees treated with the macerated flowers of flower showed a survival of 20 days on average. Solanum albidum Dun had their survival reduced, as the Studies of Dias et al. (2004), on reproductive concentrations were elevated,when the highest biology of Manihotsp. reported that Trigonaspinipesis concentration (100%) was applied, it was obtained the considered pollinator of the species Manihot sp. Silva lowest survival of the workers of A. melliferawith respect (2010) describes that,the M. glazioviidoes part of the bee to witness (control) and the other concentrations that were flora of Paraíba, being found in PrincesaIzabel, Cuite, 25% and 50% (Figure 2).

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Allan Martins Ferreira, et al

FIGURE 2. Survival curves of the bees submitted to the ingestion experiment containing macerated flowers of solanum albidum DUN (white jurubeba). POMBAL, PB. 2018. Jurubeba branca

1.5 controle 0,25%

1.0 0,50% 1,0%

0.5

Sobrevivencia (%) Sobrevivencia

0.0 0 5 10 15 20 25 Dias

The bees find their sources of pollen and nectar reported in the literature (38-42 days) is considered using some specific criteria related to smell and vision. normal because the bees in the cages are deprived of The smellemitted by the flowers can be detected for miles social life, access to queen and colony pheromones and away and is communicated to the other workers in the private individuals to perform their biological functions hive. As they have good vision, flower color and for which they evolved (FREE, 1987). morphology play an important role on attractiveness: they The control group bees survived until 22th day, tend to short wavelengths and prefer flowers with five the group of experimental bees treated with 0.25%, 0.50% separate petals instead of flowers with circle shaped petals and 1.0% with macerate obtained from flowers of (CRAM et al., 2017). Solanum albidum Dunpresented mean mortalities at 17th, The average survival of the workers in the 13th and 12th day respectively (TABLE 2). control group is up to 23 days, much lower than that

TABELE 2. Statistical analysis of the ingestion of concentrations of Solanum albidum DUN (white jurubeba)and the control group in relation to the survival of workers Apis mellifera. 0,25% andcontrol 0,50% andcontrol 1% andcontrol X2 =554,9 X2 = 386,8 X2 = 613,5

Df = 1 Df = 1 Df = 1

P<0.0001 P<0.0001 P<0.0001 Significant Significant Significant Md. Control = 18days Md. Control = 18days Md. Control = 18days Md. Trat. =17days Md. Trat. =13 days Md. Trat. =12days Md. = Medium

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Toxicity of the macerated of white and purple jurubeba flowers about bees Apismelliferas in sertao paraibano - Brazil

The data analysis showed statistically significant BRASIL, F. D. et al. Principais recursos florais para as differences between treatments and control, therefore, abelhas da Caatinga. Sci. Agrar. Paraná. Marechal Cândido suggesting toxic effect obtained from the maceration of the Rondon, v.17, n.2, abr./jun., p.149-156, 2018. flowers of Solanum albidum Dun to workers of Apismellifera. CASTAGNINO, G. L. B. Impacto na apicultura causado pelo pólen do barbatimão na zona da mata mineira. CONCLUSIONS Mensagem Doce. n.73, 2003. Disponível em: . Acesso em: mai. 2010. The bees control remained alive until the 25th and 21th dayrespectively,through the treatments withSolanum CHEN, P. S.; LI, J. H. 2006. Chemopreventive effect of paniculatum L. and Solanum albidum Dun; punicalagin, a novel tannin component isolated from Terminalia catappa, on H-ras-transformed NIH3T3 cells. The treated bees with the concentrations 0,25%, 0,50% and Toxicology Letters. 163 (1), 44-53. 2006. 1,0% of macerated flowers Solanum paniculatum L, respectively, presented mortality to the 20th, 18thand 13th CORREA JUNIOR, C.; MING, L. C.; SCHEFFER, M. C. day; Cultivo de plantas medicinais, condimentares e aromáticas. 2.ed., Jaboticabal, FUNEP, 1994. 162p. The treated bees with the concentrations 0,25%, 0,50% and 1,0% of macerated flowers Solanum albidum Dun, COSTA, C. T. C.; BEVILAQUA, C. M. L.; MORAIS, S. respectively, presented mortality to the 17th, 13thand 12th M.; VIEIRA, L. S. Taninos e sua utilização em pequenos day; ruminantes. Revista Brasileira de Plantas Medicinais. v.10, n.4, p.108-116, 2008.

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Journal of Agroindustry Sistems ISSN: 2674-7464 GVAA (2019) V.2. N.1. pp 27 - 35