1Escola de Agronomia, Universidade Federal de Goiás, Goiânia, Goiás State, Brazil
2Escola de Agronomia, Universidade Federal de Goiás, Goiânia, Goiás State, Brazil and Laboratório de Acarologia (LABAC), Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Goiás State, Brazil
3Laboratório de Acarologia (LABAC), Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Goiás State, Brazil
4✉ Laboratório de Acarologia (LABAC), Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Goiás State, Brazil
2017 - Volume: 57 Issue: 2 pages: 223-232https://doi.org/10.1051/acarologia/20164151
Brazilian Savannah, referred as Cerrado, is the second largest Brazilian biome in range. However, the ecosystems that comprise the Cerrado biome have been rapidly destroyed mainly due to agriculture expansion, urbanization, industrial activities and native resource exploitation. Estimates indicate that 39 to 55 % of Cerrado original coverage has been modified into agricultural fields, such as soybeans, corn, sugarcane and pasture for livestock (Machado et al. 2004, Nepstad et al. 1997, Sano et al. 2008). According to Dobrovolski et al. (2011), the agriculture area in Cerrado biome is going to increase from 38.2 to 50.4 % in 2100. These intensive modifications have caused several negative impacts on Cerrado like habitat fragmentation, biodiversity losses, and invasion by exotic species. At least 137 animal species from Cerrado are threatened to extinction (Fundação Biodiversitas 2003, Hilton-Taylor 2004). Furthermore, important ecosystem services provided by natural vegetations to agriculture could have been reduced as a consequence of these modifications; mainly pollination (Yamamoto et al. 2012) and natural pest control (Rezende et al. 2014). Some investigations suggest Cerrado remnants as important shelters in keeping natural enemies of pests, such as predatory mites and parasitoid insects, and the benefit in conserving natural vegetation in crop-yielding areas for improving natural pest control (Demite and Feres 2008, 2007a, b, 2005, Demite et al. 2009, Giannetti et al. 2011, Harterreiten-Souza et al. 2014, Rezende et al. 2014).
Although studies on Cerrado fauna and flora have been frequent and ongoing, many arthropod species are still poorly known within this biome, such as plant mites. So far, plant mites from Cerrado remnants were evaluated by Demite et al. (2009), Demite & Feres (2008), Lofego & Moraes (2006), Lofego et al. (2005) and Flechtmann (1967) at São Paulo and Mato Grosso States, Brazil. Rezende and Lofego (2011), in turn, sampled 26 phytoseiid species on 57 Cerrado native plant species from Midwest Brazil. Yet, the importance of Cerrado remnants in keeping natural enemies was verified by Rezende et al. (2014). According to these authors, all phytoseiid mites found in soybean plants were also recorded in Cerrado remnants suggesting a possible dispersion of these mites from natural vegetation to crops. Some phytoseiid species are predators recognized as important pest biocontrol agents in several crops (Gerson et al. 2003).
Nevertheless, whether Cerrado areas conversion to agriculture persist, as estimated by Dobrovolski et al. (2011), many mite species could disappear, including unknown taxa and species with potential economic value like predator mites. Therefore, studies aiming to assess mite assemblages on native plants from Cerrado are necessary in order to reduce knowledge gap concerning these arthropods in their natural environment. Here, we sampled mites on Astronium fraxinifolium Schott (Anacardiaceae), a threatened plant species (IBAMA 1992), from Cerrado vegetation remnants associated with nickel mining areas. Furthermore, we compared mite fauna composition between more conserved vegetation remnants and remnants previously exploited for nickel mining in order to assess whether the impact of these activities alters plant mite assemblage structure. We expected that areas previously exploited for mining present distinct species composition relative to more conserved remnants.
Six Cerrado remnants belonging to the mining Enterprise Anglo-American Brazil, Niquelândia unit, Goiás State, Brazil, were sampled during May 2012 (Table 1). Among these remnants, three were more preserved (PR) and the other three experienced secondary regeneration process (SR). The SR remnants were previously explored for nickel mining in the past as opposed to the most preserved PR remnants. The nickel mines were closed for SR areas about 30 years ago. Moreover, the PR phytophysiognomy are savannah formations while the SR remnants presented more sparse trees and grassland formation with transition to savannah (Table 1). Both SR and PR remnants were located close to mining areas, at most, one kilometer away from these sites.
We selected five A. fraxinifolium individuals from each remnant, totaling 30 plants evaluated (n = 15 for PR and RS in each). For mite sampling, we extracted 10 leaves around the canopy from each selected plant using pruning shears. The extracted leaves were immediately inserted into 1 L vials (one vial separately per plant) containing about 200 mL of 70 % alcohol. Then, the vials were vigorously shaken for 30 seconds in order to wash the leaves thoroughly and, after this, they were left to rest during five minutes. Next, the leaves were carefully removed and the vials were labeled. In this way, each vial represented mite assemblage for each selected plant.
In the lab, each sample was transferred to a sedimentation glass and left to rest during 15 minutes. After this period, we discarded the superficial liquid (about 50 mL) and the sample was transferred slowly to Petri dishes to be observed under dissecting microscope. All mites found were mounted on microscope slides with Hoyers medium (Krantz and Walter 2009). The mites were identified and counted under phase contrast microscope.
Also, we applied non-metric multidimensional scaling (NMDS), using Simpson matrix, in order to compare mite fauna composition on A. fraxinifolium between PR and SR remnants. The significance of NMDS groups was tested through Analysis of Similarity (ANOSIM) adopting alpha < 0,05 (Clarke 1993).
We recorded 1,562 mites from 17 species in 12 genus and eight families on A. fraxinifolium plants from Cerrado remnants belonging to Anglo-American Enterprise. Among the mites sampled, only one species was determined up to species level, namely Agistemus brasiliensis Matioli, Ueckermann & Oliveira (Stigmaeidae), 12 up to genus level and four were unidentified species (Table 2). Tetranychidae was the most diverse family with five species, followed by Phytoseiidae and Tenuipalpidae with four and three species, respectively. Only one species was recorded in the other families. The families with highest number of individuals collected were Tenuipalpidae, Tetranychidae and Stigmaeidae (Table 2).
The most abundant species were the phytophagous mites Brevipalpus sp.1 (Tenuipalpidae), Oligonychus sp., Eotetranychus sp.1 (Tetranychidae), and the predator A. brasiliensis. Other less abundant species were predators Pronematus sp. (Iolinidae), Euseius sp., Galendromus sp., Phytoscutus sp. and Transeius sp. (Phytoseiidae), phytophages Brevipalpus sp.2 (Tenuipalpidae), Afronychus sp., and Eotetranychus sp.2 (Tetranychidae), mycophage Czenspinskia sp. (Winterschmidtiidae) and one unidentified species for each Acaridae, Tenuipalpidae, Tetranychidae and Tydeidae families (Table 2).
Regarding feeding behavior, phytophages were the most abundant and diverse on A. fraxinifolium, since they presented 1,212 individuals and eight species. For predator mites, we sampled 142 individuals and six species, while only one individual of a mycophage species (Czenspinskia sp.) was found. Three individuals from two species had unknown behavior.
Both accumulation curves (Mao Tau) determined for PR and SR remnants tend to an asymptote, indicating that enough sample efforts to assess mite assemblage on A. fraxinifolium were performed. Moreover, the estimated richness (Jackknife 1) proved to be similar to the accumulation curve, since their confidence interval bars overlap with Mao Tau mean for both PR and SR remnants (Figure 1A and B). According to ANOSIM, no differences in mite species composition between PR and SR remnants were observed (ANOSIM, r = -0.015; p = 0.64), suggesting a high overlap in fauna composition on A. fraxinifolium (Figure 2).
Despite being directly influenced by nickel mining activities, Cerrado remnants shelters substantial mite richness and abundance since we collected 17 mite species on a single host plant in a unique sample event (in March 2012). Both PR and SR remnants showed similar patterns in mite species occurrence, as suggested by NMDS and ANOSIM.
The mite genera recorded in this paper had been already sampled in Cerrado remnants from São Paulo, Goiás and Mato Grosso States by previous authors (Rezende et al. 2014, Rezende and Lofego 2011, Demite et al. 2009, Demite and Feres 2008, Lofego and Moraes 2006, Lofego et al. 2005 and Aranda 1974), except for genera Phytoscutus (Phytoseiidae) and Afronychus (Tetranychidae), which were recorded here for first time in Brazil Midwest Cerrado. Some of the genera sampled were also recorded in other Brazilian natural vegetations, such semi-deciduous forest remnants from São Paulo State, namely Agistemus, Brevipalpus, Euseius, Eotetranychus, Galendromus, Pronematus and Transeius (Demite et al. 2013, Buosi et al. 2006 and Demite and Feres 2005).
Agistemus brasiliensis was the only taxa identified up to species level and it is reported here for first time to Cerrado Biome on a Brazilian native plant. This species was only previously reported in agroecosystems, like citrus (Matioli et al. 2002) and vineyards (Johann et al. 2013) crops, in Brazil. Only Rezende et al. (2014) recorded another species from the same genus on native plants from Cerrado remnants, namely Agistemus floridanus Gonzalez.
Astronium fraxinifolium plants showed great abundance of phytophages, sheltering eight species of these mites. Among them, Tenuipalpidae and Tetranychidae were the most representative, highlighting species from Brevipalpus and Oligonychus genera. Some species of these genera presents agricultural interest since they can act as pest on crops (Moraes and Flechtmann 2008). Some Brevipalpus species can transfer viruses to their host plants. In Brazil, Brevipalpus phoenicis (Geijskes) is considered an important pest because it can infect citrus plants with leprosis viruses as well as coffee plants with ring spot viruses (Moraes and Flechtmann 2008, Reis et al. 2004). Oligonychus species can affect the photosynthesis rate on their host plant during feeding which hinders yield, depending on the species (Moraes and Flechtmann 2008). However, the phytophagous mites sampled in this work, including Brevipalpus and Oligonychus species, probably do not threaten neighboring agriculture to vegetation remnants. We provide three arguments that substantiate this hypothesis: (i) Brevipalpus species were confirmed by taxonomists and both Brevipalpus sp.1 and sp.2 are probably undescribed species (RJF Feres, pers. com.). (ii) Phytophages from Cerrado plants presumably do not disperse from natural vegetation to the crops as suggested by field experiment performed by Rezende et al. (2014). According to these authors, no phytophagous mite species from Cerrado remnants were sampled in soybean plants from Brazilian Midwest crops neighboring natural vegetation. In contrast, some predator mites collected in Cerrado remnants were also sampled in soybean crops which suggest possible dispersion of these beneficial arthropods from natural vegetation to the nearby monoculture (Rezende et al. 2014). (iii) Native plants probably cannot support pest mite development and reproduction. In a review concerning plant mite species from Brazil, Araújo and Daud (submitted) verified that some important pest mites were sampled on native plants from Cerrado and Atlantic forest remnants, such as Tetranychus urticae Koch and B. phoenicis, for example. However, these phytophagous species were always collected in low numbers on native plants, both in the Cerrado and the Atlantic forest, which suggest low suitability of native plants as food for these pests. Nevertheless, other experiments must be performed to test phytophagous mite dispersion from natural remnants to nearby crops in order to verify whether Cerrado remnants threaten or not agriculture yield.
Additionally, A. fraxinifolium plants showed considerable richness and abundance of predator mites. Agistemus brasiliensis was the most abundant predator; however, Phytoseiidae exhibited the most species richness among them. Species from Stigmaeidae and Phytoseiidae families demonstrate potential to be used as pest biocontrol agents since many previous experimental assays suggested the great capacity of these mites in preying on phytophagous mites and insects (e.g. Ferla & Moraes 2003, Gerson et al. 2003, Nomikou et al. 2001, Furtado & Moraes, 1998). Matioli and Oliveira (2007) evaluated A. brasiliensis biological cycle at different temperatures and observed acceptableness of the predator in feeding on B. phoenicis, which suggest the importance of A. brasiliensis as a natural enemy on this relevant citrus pest.
The results of accumulation (Mao Tau) and estimated richness (Jackknife 1) curves indicated enough effort to assess mite assemblage on A. fraxinifolium through sample methods applied in this study. Furthermore, the probability of sampling new mite species according to sample effort increase could be low for both SR and PR remnants. These curve patterns differ from other studies performed in natural vegetation remnants (Feres et al. 2007 and Walter and Proctor 1998) where the authors did not find asymptote for accumulation species curve, suggesting high probability of natural vegetation in harboring higher mite diversity. However, both PR and SR Cerrado remnants receive similar and frequent impact from nickel mining activities given their proximity to the mining enterprise. Therefore, it is expected that these vegetation remnants are significantly more altered and, consequently, harbor less plant mite species. As a result of these similar impacts, mite fauna composition did not show differences between PR and SR remnants.
This paper is a pioneer report of mite assemblage on A. fraxinifolium, an extinction threatened plant species from Cerrado remnants. Yet, Phytoscutus and Afronychus genera and A. brasiliensis species were recorded for Cerrado biome for the first time. At least, two species sampled here are potentially new taxa to be described in future taxonomic studies. Moreover, we observed similar impacts from mining activities on PR and SR remnants since their mite fauna did not show differences in composition species. This pattern was probably due to the proximity of both PR and SR remnants to the mining sites. Future studies comparing close and more distant areas (preferentially pristine areas) from mining enterprises must be conducted to elucidate the effect of this impact on mite occurrence and abundance. The present study highlights the importance of keeping natural vegetation in order to preserve mite diversity on native plants rendering its database useful to future conservation programs for natural ecosystems.
The authors wish to thank Leandro Maracahipes and Ana Carolina Cavalcanti (Universidade Federal de Goiás) for their help with field samples and laboratory proceedings, and to Reinaldo J.F. Feres and team (UNESP, São José do Rio Preto, Brazil) for identification assistance. This work was financially supported by Anglo American Brazil – FUNAPE agreement.
Aguiar A.V., Bortolozo F.R., Moraes M.L.T., Sá M.E. 2001 — Determinação de parâmetros genéticos em população de gonçalo-alves (Astronium fraxinifolium) através das características fisiológicas da semente — Sci. For., 60: 89-97.
Aranda B.R. 1974 — Tetranychoidea (Acari) de uma área de cerrado do Estado de São Paulo [PhD thesis] — Piracicaba: Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo. pp.47.
Baker E.W., Wharton A.E. 1952 — An introduction to Acarology — New York: The MacMillan Company.
Buosi R., Feres R.J.F., Oliveira A.R., Lofego A.C., Hernandes F.A. 2006 — Ácaros plantícolas (Acari) da "Estação Ecológica de Paulo de Faria", Estado de São Paulo, Brasil — Biota Neotrop., 6(1). Available from: ( http://www.biotaneotropica.org.br/v6n1/pt/abstract?article+bn02006012006 ). doi:10.1590/S1676-06032006000100009
Clarke K.R. 1993 — Non-parametric multivariate analyses of changes in community structure — Aust. J. Ecol., 18: 117-143. doi:10.1111/j.1442-9993.1993.tb00438.x
Colwell R.K. 2006 — EstimateS: Statistical estimation on species richness and shared species from samples — Version 7.51. User's Guide. Available from: ( http://viceroy.eeb.uconn.edu/EstimateSPages/EstSUsersGuide/EstimateSUsersGuide.htm ).
Cumming G., Fidley F., Vaux D.L. 2007 — Error bars in experimental biology — J. Cell Biol., 177: 7-11. doi:10.1083/jcb.200611141
Demite P.R., Feres R.J.F. 2008 — Influência de fragmentos de Cerrado na distribuição de ácaros em seringal — Neotrop. Entomol., 37(2): 196-204. doi:10.1590/S1519-566X2008000200015
Demite P.R., Feres R.J.F. 2007a — Ocorrência e flutuação populacional de ácaros associados a seringais vizinhos de fragmento de Cerrado — Neotrop. Entomol., 36(1): 117-127. doi:10.1590/S1519-566X2007000100015
Demite P.R., Feres R.J.F. 2007b — Influência de fragmentos de Cerrado na infecção fúngica em ácaros de seringueira — Arqu. do Inst. Biol., 74(3): 271-273.
Demite P.R., Feres R.J.F. 2005 — Influência de vegetação vizinha na distribuição de ácaros em seringal (Hevea brasiliensis Muell. Arg., Euphorbiaceae) em São José do Rio Preto, SP — Neotrop. Entomol., 34(5): 829-836. doi:10.1590/S1519-566X2005000500016
Demite P.R., Lofego A.C., Feres R.J.F. 2013 — Mite (Acari; Arachnida) diversity of two native plants in fragments of a semideciduous seaseonal forest in Brazil — Syst. Biodivers., 11(2):141-148. doi:10.1080/14772000.2013.806368
Demite P.R., Feres R.J.F, Lofego, A.C., Oliveira A.R. 2009 — Plant inhabiting mites (Acari) from the Cerrado biome of Mato Grosso State, Brazil — Zootaxa, 2061:45-60.
Dobrovolski R., Loyola R.D., De Marco P., Diniz-Filho J.A.F. 2011 — Agricutural expansion can menace Brazilian protected areas during the 21st century — Natur. & Conserv., 9(2): 208-213.
Feres R.J.F., Buosi R., Daud R.D., Demite P.R. 2007 — Padrões ecológicos da comunidade de ácaros em euforbiáceas de um fragmento de mata Estacional Semidecidual, no Estado de São Paulo — Biota Neotrop., 7(2). Available from: ( http://www.biotaneotropica.org.br/v7n2/pt/abstract?article+bn04907022007 ) doi:10.1590/S1676-06032007000200022
Ferla N.J., Moraes G.J. de. 2003 — Oviposição dos ácaros predadores Agistemus floridanus Gonzalez, Euseius concordis (Chant) e Neoseiulus anonymus (Chant & Baker) (Acari) em resposta a diferentes tipos de alimento — Rev. Bras. Zool., 20(1): 153-155. doi:10.1590/S0101-81752003000100019
Flechtmann C.H.W. 1967 — Ácaros de plantas do Cerrado — Anais E.S.A. "Luiz de Queiroz", 24: 315-316. doi:10.1590/S0071-12761967000100028
Fundação Biodiversitas. 2003 — Lista da fauna brasileira ameaçada de extinção — Belo Horizonte: Fundação Biodiversitas. Available from: http://www.biodiversitas.org.br.
Furtado I.P., Moraes G.J.de. 1998 — Biology of Euseius citrifolius, a candidate for the biological control of Mononychellus tanajoa (Acari: Phytoseiidae, Tetranychidae) — Syst. Appl. Acarol., 3(1):43-48. doi:10.11158/saa.3.1.6
Gerson U., Smiley R.L., Ochoa R. 2003— Mites (Acari) for pest control — Oxford: Blackwell Science. doi:10.1002/9780470750995
Giannetti B.F., Ogura Y., Bonilla S.H., Almeida C.M.V.B. 2011 — Emergy assessment of a coffee farm in Brazilian Cerrado considering in a broad form the environmental services, negative externalities and fair price — Agr. Syst., 104: 679-688
Harterreiten-Souza E.S., Togni P.H.B., Pires C.S.S., Sujii E.R. 2014 — The role of integrating agroforestry and vegetable planting in structuring communities of herbivorous insects and their natural enemies in the Neotropical region — Agroforest. Syst., 88(2): 205-219.
Heltshe J.F., Forrester N.E. 1983 — Estimating species richness using the jackknife procedure — Biometrics, 39: 1-11.
Hilton-Taylor, C. 2004 — IUCN red list of threatened species. Species Survival Commission (SSC), IUCN — The World Conservation Union, Cambridge, Reino Unido e Gland, Suíça. Available from: http://www.redlist.org (accessed in 13 of january of 2005).
IBAMA. 1992 — Portaria Ibama no 37-N, de 03 de abril de 1992 — Available from: ( http://licenciamento.cetesb.sp.gov.br/legislacao/federal/portarias/1992$_$Port$_$IBAMAù_ù37.pdf )
Johann L., Carvalho G.S., Majolo F., Ferla N.J. 2013 — Stigmaeid mites (Acari: Stigmaeidae) from vineyards in the state of Rio Grande do Sul, Brazil — Zootaxa, 3701(2): 238-256
Krantz G.W., Walter D.E. 2009 — A Manual of Acarology —Third ed. Texas: Texas Tech University Press, Lubbock.
Lofego A.C., Moraes, G.J. 2006 — Ácaros (Acari) Associados a mirtáceas (Myrtaceae) em áreas de Cerrado no Estado de São Paulo com análise faunística das famílias Phytoseiidae e Tarsonemidae — Neotrop. Entomol., 35(6): 731-746. doi:10.1590/S1519-566X2006000600003
Lofego A.C., Ochoa. R., Moraes, G.J. 2005 — Some tarsonemidae mites (Acari: Tarsonemidade) from the Brazilian "Cerrado" vegetation, with description of three new species — Zootaxa, 823: 1-27.
Lorenzi H. 1992 — Árvores brasileiras —Piracicaba: Plantarum.
Machado R.B., Ramos-Neto M.B., Pereira P.G.P., Caldas E.F., Gonçalves D.A., Santos N.S., Tabor K., Steininger M. 2004 — Estimativas de perda da área do Cerrado brasileiro. Brasília — Conservação Internacional.
Matioli A.L., Oliveira C.A.L. de. 2007 — Biologia de Agistemus brasiliensis Matioli, Ueckermann & Oliveira (Acari: Stigmaeidae) e sua potencialidade de predação sobre Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae) — Neotrop. Entomol., 36(7): 577-582. doi:10.1590/S1519-566X2007000400016
Matioli A.L., Ueckermann E.A., Oliveira C.A.L. 2002 — Some stigmaeid and eupalopsellid mites from citrus orchards in Brazil (Acari: Stigmaeidae and Eupalopsellidae) — Int. J. Acarol., 28(2): 99-120. doi:10.1080/01647950208684287
McMurtry J.A., Croft B.A. 1997 — Life-styles of phytoseiid mites and their roles in biological control — Ann. Rev. Entomol., 42: 291-321. doi:10.1146/annurev.ento.42.1.291
Moraes G.J., Flechtmann C.H.W. 2008 — Manual de Acarologia: Acarologia básica e ácaros de plantas cultivadas no Brasil —Ribeirão Preto: Holos Editora.
Nepstad D.C., Klink C.A., Uhl C.F., Vieira I.C., Lefebebvre P., Pedlwski M., Matricardi E., Negreiros G., Brown I.F., Amaral E., Homma A., Walker R. 1997 — Land use in Amazonia and the Cerrado of Brazil — Ciên. Cult., 49(1/2): 73-86.
Nomikou M., Janssen A., Schraag R., Sabelis N.W. 2001 — Phytoseiid predators as potential biological control agents for Bemisia tabaci — Exp. Appl. Acarol., 25: 271-291. doi:10.1023/A:1017976725685
Reis P.R., Neto M.P., Franco R.A., Teodoro A.V. 2004 — Controle de Brevipalpus phoenicis (Geijskes, 1939) e Oligonychus ilicis (Mcgregor, 1917) (Acari: Tenuipalpidae, Tetranychidae) em cafeeiro e o impacto sobre ácaros benéficos. I – Abamectin e Emamectin — Ciênc. Agrotec., 28(2): 269-281. doi:10.1590/S1413-70542004000200004
Rezende J.M.E, Lofego A.C. 2011 — Phytoseiidae (Acari: Mesostigmata) on plants of the central region of the Brazilian cerrado — Acarologia, 51(4): 449-463.
Rezende J.M., Lofego A.C., Nuvoloni F.M., Navia D. 2014 — Mites from Cerrado fragments and adjacent soybean crops: does the native vegetation help or harm the plantation — Exp. Appl. Acarol., 64(4): 501-518. doi:10.1007/s10493-014-9844-5
Sano E.E., Rosa R., Brito J.L.S., Ferreira L.G. 2008 — Mapeamento semidetalhado do uso da terra do bioma cerrado — Pesqui. Agropecu. Bras., 43(1): 153-156. doi:10.1590/S0100-204X2008000100020
Santos A.J. 2003 — Estimativa de riqueza em espécies — In: Cullen-Jr L., Rudran, R., Valladarespadua, C. (Eds.). Métodos de estudo em biologia da conservação e manejo da vida silvestre. Curitiba: Editora UFPR. pp. 19-41.
Walter E.D., Proctor, H.C. 1998 — Predatory mites in tropical Australia: Local Species Richness and complementarity — Biotropica, 30(1): 72-81.
Yamamoto M., Silva C.I., Augusto S.C., Barbosa A.A.A., Oliveira P.E. 2012 — The role of bee diversity in pollination and fruit set of yellow passion fruit (Passiflora edulis forma flavicarpa, Passifloraceae) crop in Central Brazil — Apidologie, 43(5): 515-526