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  • Publicado pelo projeto Entomologistas do BrasilVolume 9 . Nmero 1 . Janeiro - Abril de 2016

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    v. 9, n. 1

    eISSN 1983-0572doi:10.12741

    2016

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  • Produzida no Brasil

    Periodicidade: QuadrimestralDireitos Autorais: Copyright 2008-2016, Entomologistas do BrasilIseno de Responsabilidade Legal: As opinies tcnico/cientficas e mesmo pessoais, constantes nos artigos e/ou comunicaes cientficas publicados no EntomoBrasilis so de inteira responsabilidade de seus respectivos autores.

    Projeto Grfico (Editorao): William Costa RodriguesCapa: Adulto de Horiola picta (Coquebert) no pcolo de fruto de cacaueiro Material coletado em: (192453S, 400352W ). Material: Cacau Theobroma cacao. Foto: Vera Lcia Rodrigues Machado Benassi. Artigo: Benassi, V.L.R.M., F.I. Valente, C.A.S. Souza, A.C. Benassi & A.M. Sakakibara. Biodiversidade e Sazonalidade de Cigarrinhas (Hemiptera: Membracidae) em Cacaueiros. Reviso do Portugus/Ingls/Espanhol: Corpo de ConsultoresComposio: Fonte: Georgia, variando de 7 a 26 pts., em estilo normal, itlico, negrito, sublinhado, podendo haver contorno e colorao preta ou verde (texto), azul (links)

    Site: www.periodico.ebras.bio.bre-mail: [email protected]

    Distribudo e licenciado segundo a Creative Commons Licencehttp://creativecommons.org/licenses/by-nc-sa/4.0/deed.pt_BR

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    O perodico online EntomoBrasilis fundado em 2008 pelo projeto Entomologistas do Brasil, tem como objetivo de publicar artigos originais, de forma rpida, das mais diversas reas da Entomologia Brasileira e Mundial, tais como: Bionomia; Comportamento; Ecologia; Entomologia Forense; Entomologia Geral; Fisiologia; Modelos Ecolgicos Aplicados Entomologia; Morfologia; Revises; Sade Pblica; Taxonomia e Sistemtica e demais reas afins Entomologia Brasileira e Mundial.

    The online periodical EntomoBrasilis founded in 2008 by Entomologistas do Brasil project, aims to publish original articles, quickly, from various areas of the Brazilian and World Entomology such as: Bionomics; Behavior; Ecology; Forensic entomology; General Entomology; Physiology; Applied to models Ecological Entomology; Morphology; reviews; Public health; Taxonomy and systematics and other areas related to Brazilian and World Entomology.

    Expediente

    Editor ChEfEWilliam Costa Rodrigues

    Entomologistas do Brasil / Centro Universitrio de Braslia - UniCEUB

    EditorEs AdjuntosEvaldo Martins Pires - Universidade Federal de Mato Grosso - Campus Sinop

    Jeronimo Augusto Fonseca Alencar - Instituto Oswaldo Cruz - FIOCRUZ - RJ.

    Editores Cientficos

    Ado Valmir dos Santos, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Brasil

    Alexandre Ururahy Rodrigues, Instituto Nacional de Pesquisas da Amaznia - INPA, Brasil

    Ana Tereza Araujo Rodarte, Universidade Federal do Rio de Janeiro - Museu Nacional, Brasil

    Anderson Gonalves da Silva, Universidade Federal Rural da Amaznia - UFRA, Brasil

    Arlindo Serpa Filho, Instituto Oswaldo Cruz, BrasilCleber Galvo, Instituto Oswaldo Cruz, BrasilEduardo Jos Ely Silva, Universidade Federal de Pelotas, BrasilEloy Guillermo Castelln Bermdez, INPA - Instituto Nacional

    de Pesquisas da Amaznia, BrasilHlcio Reinaldo Gil-Santana, Fundao Oswaldo Cruz, Brasil.Gisele Luziane de Almeida, Universidade Federal do Rio de

    Janeiro, Museu Nacional, BrasilHerbet Tadeu de Almeida Andrade, Universidade Federal do Rio

    Grande do Norte, BrasilMaria Christina de Almeida, Universidade Federal do Paran,

    BrasilMaria Jos do Nascimento Lopes, Instituto Nacional de Pesquisas

    da Amaznia, BrasilMarliton Rocha Barreto, Universidade Federal do Mato Grosso -

    Campus SINOP, BrasilNataly Arajo de Souza, Fundao Oswaldo Cruz, Instituto

    Oswaldo Cruz, Departamento de Entomologia, BrasilNicolas Dgallier, Institut de Recherche pour le Dveloppement,

    FranaRicardo Andreazze, Universidade Federal do Rio Grande de Norte,

    BrasilRoney Rodrigues-Guimares, Universidade Iguau / Universidade

    Estcio de S, BrasilRubens Pinto de Mello, Fundao Oswaldo Cruz, Instituto Oswaldo

    Cruz, BrasilRuberval Leone Azevedo, Casa Civil - Governo do Estado de

    Sergipe, BrasilTatiana Chrysostomo Santos, Museu Nacional - Universidade

    Federal do Rio de Janeiro, BrasilVictor Py-Daniel, Universidade de Braslia, BrasilViviane Zahner, Fundao Oswaldo Cruz, Brasil.Wedson Desidrio Fernandes, Universidade Federal da Grande

    Dourados, Brasil.Wesley Dttilo - Universidad Veracruzana, Mxico.

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    Consultores Adhoc deste Nmero

    Adelita Maria Linzmeier, Universidade Federal da Grande Dourados, Brasil

    Agno Nonato Serro Acioli, INC/UFAM, BrasilAnderson Gonalves da Silva, Universidade Federal Rural

    da Amaznia - UFRA, BrasilBruno Henrique Sardinha de Souza, FCAV/UNESP, BrasilDaniell Rodrigo Rodrigues Fernandes, FACV/UNESP,

    BrasilDanielle Anjos-Santos, Universidad Nacional de la Patagonia

    San Juan Bosco, ArgentinaDenise Lange, Universidade Federal de Uberlandia, BrasilEdilberto Giannotti, Universidade Estadual Paulista Jlio de

    Mesquita Filho, BrasilElizabeth Franklin Chilson, Instituto Nacional de Pesquisas

    da Amaznia, BrasilFbio Souto Almeida, Universidade Federal Rural do Rio de

    Janeiro, BrasilHlcio Reinaldo Gil-Santana, Fundao Oswaldo Cruz,

    BrasilHlida Ferreira da Cunha, UEG, BrasilJulianne Millo, UEPG, BrasilLuciane Gomes Batista Pereira, Universidade Federal de

    Minas Gerais, Instituto de Cincias Biolgicas, BrasilMaria Santina Morini, Universidade de Mogi das Cruzes,

    BrasilMarliton Rocha Barreto, Universidade Federal de Mato

    Grosso, BrasilPatrik Luiz Pastori, Universidade Federal do Cear, BrasilRoberth Fagundes, Universidade Federal de Ouro Preto,

    BrasilRoney Rodrigues-Guimares, Universidade Estcio de S

    - UNESA / Centro Universitrio de Barra Mansa - UBM, Brasil

    Ruberval Leone Azevedo, Casa Civil - Governo do Estado de Sergipe, Brasil

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  • iv

    Sumrio

    Frum / Review

    Magnetoreception in Social Wasps: An Update Magnetoreception in Social Wasps: An Update. Magnetorrecepo em Vespas Sociais: Uma Atualizao. Maria da Graa Cardoso Pereira-Bomfim, William Fernando Antonialli-Junior & Daniel Acosta-Avalos ................................................................................................................................................................................................ 01-05

    Bionomia e Comportamento / Bionomy and BehaviorRepertoire of Defensive Behavior in Africanized Honey Bees (Hymenoptera: Apidae): Variations in Defensive Standard and Influence of Visual Stimuli. Repertrio do Comportamento Defensivo em Apis mellifera L. africanizada (Hymenoptera: Apidae): Variaes nos Padres Defensivos e Influncia de Estmulos Visuais. Fbio de Assis Pinto, Paula Netto, Kleber de Sousa Pereira & Terezinha Maria Castro Della Lucia .............................................................................................................. 06-09

    Ecologia / EcologyInvertebrate Colonization During Leaf Decomposition of Eichhornia azurea (Swartz) Kunth (Commelinales: Pontoderiaceae) and Salvinia auriculata Aubl. (Salvinales: Salvinaceae) in a Neotropical Lentic System. Colonizao por Invertebrados Durante a Decomposio foliar de Eichhornia azurea (Swartz) Kunth (Commelinales: Pontoderiaceae) e Salvinia auriculata Aubl. (Salvinales: Salvinaceae) em um Sistema Lntico Neotropical. Lidimara Souza da Silveira, Renato Tavares Martins & Roberto da Gama Alves .................................................................................................................................................................. 10-17

    Entomologia Geral / General EntomologyDinmica Populacional de Mosca-Branca, Incidncia do Mosaico Dourado do Feijoeiro e Alternativas de Controle da Praga no Cultivo das Secas no Cerrado. Population Dynamics Whitefly, Golden Mosaic Effect of Feijoeiro and Pest Alternatives Control in Drought Cultivation in the Cerrado. Luciana Claudia Toscano, Washington Marques Aguirre, Germison Vital Tomquelski, Wilson Itamar Maruyama, Geraldo Candido Cabral Gouveia & Pamella Mingotti Dias ....................................... 18-25

    Fungos Filamentosos Associados s Espcies Atta sexdens (Linnaeus) e Atta laevigata (F. Smith) (Hymenoptera: Formicidae). Filamentous Fungi Associated With Atta sexdens (Linnaeus) and Atta laevigata (F. Smith) (Hymenoptera: Formicidae). Aline Silvestre Pereira Dornelas, Renato de Almeida Sarmento, Gil Rodrigues dos Santos, Mariela Otoni do Nascimento & Danival Jos de Souza .............................................................................................................................................. 26-30

    Tisanopterofauna Associada Plantas Ornamentais e Cultivadas no Sudoeste Baiano. Thysanopterofauna Associated with Ornamental and Crop Plants in Southwest Bahia. Andr Luiz Santos Mascarenhas, Silvia Marisa Jesien Pinent & Juvenal Cordeiro Silva Junior ........................................................................................................................................................................ 31-35

    Herbicidas e Reguladores de Crescimento de Plantas Utilizados na Cana-de-Acar e sua Ao sobre Adultos de Trichogramma galloi Zucchi (Hymenoptera: Trichogrammatidae). Herbicides and Plant Growth Regulators Used in Sugarcane and their Action on Adult Trichogramma galloi Zucchi (Hymenoptera: Trichogrammatidae) Marina de Rezende Antigo, Eduardo Mitio Shimbori, Daniele Fabiana Glaeser, Harley Nonato de Oliveira& Gerado Andrade Carvalho .......................... 36-40

    Biodiversidade e Sazonalidade de Cigarrinhas (Hemiptera: Membracidae) em Cacaueiros. Biodiversity and Sazonality of Treehoppers (Hemiptera: Membracidae) in Cocoa. Vera Lcia Rodrigues Machado Benassi, Fabrcio Iglesias Valente, Carlos Alberto Spaggiari Souza, Antonio Carlos Benassi & Albino Morimasa Sakakibara ..........................................................41-46

    Marcao de Diatraea saccharalis (Fabr.) com Diferentes Corantes em Dieta Artificial. Marking of Diatraea saccharalis (Fabr.) with Dyes in Artificial Diet. Jael Simes Santos Rando, Laila Herta Mihsfeldt, Franciele Paulette Lial de Souza & Fernanda Venancio Soares................................................................................................................................................................47-50

  • vSade Pblica / Public HealthEficcia de Ovitrampas com Diferentes Atrativos na Vigilncia e Controle de Aedes. Effectiveness of Ovitraps with Different Attractives in the Monitoring and Control of Aedes. Priscila Aparecida Claro Depoli, Joo Antonio Cyrino Zequi, Kauani Larissa Campana Nascimento & Jos Lopes .................................................................................................................................... 51-55

    Comunicao Cientfica / Scientific ComunicationFirst Record of Pseudomyrmex acanthobius Emery in Brazilian Pantanal. Primeiro Registro de Pseudomyrmex acanthobius Emery no Pantanal Brasileiro. Rodrigo Aranda, Renan Olivier & Alexandre Ferraro ..........................................................56-58

    Survey and New Distributional Records of Nocturnal Social Wasps Apoica (Hymenoptera, Vespidae, Epiponini) Along Madeira River, Rondnia, Brazil. Levantamento e Novos Registros de Vespas Sociais Noturnas Apoica (Hymenoptera, Vespidae, Epiponini) ao Longo do Rio Madeira, Rondnia, Brazil. Bruno Gomes, Caio Loureno Assuno da Silva, Marjorie da Silva & Fernando Barbosa Noll ..................................................................................................................................................................59-61

    Primeiro Registro do Gnero e Espcie Neblinagena doylei Kodada & Jch (Coleoptera: Elmidae: Larainae) no Brasil. First Record of Genus and Species Neblinagena doylei Kodada & Jch (Coleoptera: Elmidae: Larainae) in Brazil. Jaime de Liege Gama Neto & Mahedy Araujo Bastos Passos .......................................................................................................62-64

    Bulb Mites Rhizoglyphus echinopus (Fumouze and Robin) Associated with Subterranean Termite (Isoptera) in Brazil. caros do Bulbo Rhizoglyphus echinopus (Fumouze and Robin) Associados com Cupim Subterrneo (Isoptera) no Brasil. Ademar Ferreira Silva, Zeneida Teixeira Pinto, Rebecca Leal Caetano, Csar Carrio, Tayra Pereira Sato, Marinete Amorim & Gilberto Salles Gazeta ........................................................................................................................................................................65-68

    Infestao de Tetranychus ogmophallos Ferreira & Flechtmann (Acari: Tetranychidae) em Amendoim Forrageiro (Arachis pintoi Krapov. & Greg.) os Estados do Acre e Minas Gerais. Infestation of Tetranychus ogmophallos Ferreira & Flechtmann (Acari: Tetranychidae) in Plants of Forage Peanut in Acre and Minas Gerais States, Brazil. Rodrigo Souza Santos .......................................................................................................................................................................69-72

    Volume 9, nmero 1 - Jan. - Abr. 2016*************

    ISSN 1983-0572doi:10.12741/ebrasilis.v9i1

  • www.periodico.ebras.bio.br

    e-ISSN 1983-0572Publicao do Projeto Entomologistas do Brasil

    www.ebras.bio.brDistribudo atravs da Creative Commons Licence v4.0 (BY-NC-ND)

    Copyright EntomoBrasilisCopyright do(s) Autor(es)

    Magnetoreception in Social Wasps: An UpdateMaria da Graa Cardoso Pereira-Bomfim, William Fernando Antonialli-Junior & Daniel Acosta-Avalos

    1. Universidade Federal da Grande Dourados, e-mail: [email protected] (Autor para correspondncia). 2. Universidade Estadual de Mato Grosso do Sul, e-mail: [email protected]. 3. Centro Brasileiro de Pesquisas Fsicas, e-mail: [email protected].

    _____________________________________

    EntomoBrasilis 9 (1): 01-05 (2016)

    Fr

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    Abstract. Magnetoreception is a mechanism of active orientation that occurs in animals with nervous systems. Social insects such as bees, ants, wasps and termites have been studied on the influence of the magnetic field exerts on its biology. The social wasps comprise species represented in Stenogastrinae, Vespinae and Polistinae, however studies on the influence of magnetic field on wasps Vespinae address only. The areas studied include the biomineralization of magnetic material and behavioral aspects related to changes in local intensity of the geomagnetic field. The objective of this review is to integrate knowledge of social wasps magnetoreception in order to build an instructive overview of the current situation of studies, therefore, provide the conceptual framework for the development of future work on the topic.

    Keywords: Hymenoptera; Magnetic Field; Magnetosensibility; Vespidae.

    Magnetorrecepo em Vespas Sociais: Uma Atualizao

    Resumo. Magnetorrecepo um mecanismo de orientao ativa que ocorre em animais com sistema nervoso. Insetos sociais tais como abelhas, formigas, vespas e cupins so estudados sobre a influncia que o campo magntico exerce em sua biologia. As vespas sociais compreendem espcies representadas em Stenogastrinae, Vespinae e Polistinae, no entanto os estudos sobre a influncia do campo magntico em vespas abordam somente Vespinae. As reas de estudo incluem a biomineralizao do material magntico e aspectos comportamentais relacionados a mudanas na intensidade do campo geomagntico local. O objetivo desta reviso integrar o conhecimento sobre magnetorrecepo em vespas sociais, a fim de construir um panorama elucidativo da atual situao dos estudos, e assim fornecer uma estrutura conceitual para o desenvolvimento de trabalhos futuros sobre o tema.

    Palavras-Chave: Campo Magntico; Hymenoptera; Magnetossensibilidade; Vespidae.

    _____________________________________

    Wasps can be separated, according to the degree of sociability, into two groups: solitary species (Euparagiinae, Masarinae and Eumeninae) and social

    species (Stenogastrinae, Vespinae and Polistinae) (Carpenter 1982). Polistinae is the only subfamily of social wasps that occurs in Brazil, with a record of over 300 species, distributed in 22 genera in the tribes Epiponini, Mischocyttarini and Polistini (Carpenter & Marques 2001).

    The geomagnetic field is an environmental abiotic factor that interacts constantly with living beings. It is as ancient as the origin of life on Earth (Jardine 2010). The perception of the environmental abiotic factors by microorganisms and animals led to the development of different mechanisms of orientation over time, which are responsible for the survival of the species, such as navigation, contributing to the process of natural selection (skiles 1985; Gould 2008).

    Magnetoreception is a mechanism of active orientation that occurs in animals with nervous systems, and involves detecting the geomagnetic field by a sensory mechanism coupled to cellular systems, such as mechanoreceptors that transduce this signal to the brain. To explain this mechanism there are basically three hypotheses or specific models (sChiff 1991; shCherbakov & Winklhofer 1999; lohMann & Johnsen 2000).

    One hypothesis is based on Faradays law of magnetic induction, which it is assumed that the organism detects a difference in electrical potential, generated in specialized organs such as the ampolla of Lorenzini in fishes, resulting from its motion through the geomagnetic field. Another hypothesis is the light dependent magnetoreception or radical pair mechanism, which

    is based on the fact that several chemical reactions can change their kinetics in the presence of magnetic fields. Currently it is assumed that cryptochrome molecules are involved in the radical pair mechanism, because after this molecule absorb light the chemical reactions that follows vary depending on the relative orientation of the molecular axis of symmetry with the direction of the geomagnetic field (WiltsChko & WiltsChko 2006).

    The third hypothesis is the ferromagnetic hypothesis which is based on the presence of magnetic nanoparticles as magnetic field sensors. It is supported by the discovery of magnetite nanoparticles in various species of animals from insects (Gould et al. 1980; esquivel et al. 1999, WaJnberG et al. 2010) to humans (kirsChvink et al. 1992) and this hypothesis is one of the most accepted due to evidence accumulated.

    The studies of blakeMore (1975) and Bellini (2009) with aquatic bacteria demonstrated that the geomagnetic field is capable of producing effects in biological systems, verifying that magnetotactic bacteria directly respond to magnetic stimuli, swimming in the direction of the force lines of the geomagnetic field constituting the first unequivocal evidence that the magnetic field may directly influence the behavior of a living being.

    The objective of this review is to describe the state of the art in the knowledge of social wasps magnetoreception in order to get insights about the current situation of this topic and provide the conceptual structure for the development of future studies.

    Funding Agencies: CAPES; CNPq

    doi:10.12741/ebrasilis.v9i1.526

  • 2Magnetoreception in Social Wasps: An Update Pereira-Bomfim et al.

    e-ISSN 1983-0572

    SOCIAL HyMENOPTERA

    Among the social insects the bee Apis mellifera L. has been the most studied considering the sensitivity to the geomagnetic field. Despite innumerous evidences that they orient in this field, no one knows for sure what the reception mechanisms able to detect it and how the information is transmitted to the bee nervous system (aCosta-avalos et al. 2000; WaJnberG et al. 2010; vlkov & vaCh 2012).

    One of the earliest evidence of the influence of the geomagnetic field on the behavior of bees was obtained by lindauer & Martin (1968). They found that errors in the information transmitted during the execution of the waggle dance varied according to the direction and intensity of the Earths magnetic field; and also found that when a swarm leaves the original hive worker bees build new combs in the same previous magnetic direction, and that apparently the circadian rhythms of bees could be given by the variations in the intensity and direction of the geomagnetic field (toWne & Gould 1985). Magnetic fields are known to have influence on the temporal and spatial orientation of these bees (Martin & lindauer 1977; korall et al. 1988; Martin et al. 1989).

    The motility of the bees is not affected by a uniform magnetic field but when the same field is intermittently imposed (periods of 10 or 15 min) the mean activity oscillates in phase with the magnetic field oscillations (hepWorth et al. 1980).

    Martin et al. (1989) found that artificial magnetic fields can influence physiological processes in bees. They reported that in non-homogeneous static magnetic field there is a reduction in the activity of flight and an increase of more than 60% in the life span of individuals, although higher chronological age, the content of lipofuscin of brain cells was slightly reduced in these bees, in relation to bees in geomagnetic field conditions.

    Induced magnetization was measured in A. mellifera and this signal was associated to magnetic nanoparticles with diameters in the range 30-35 nm, which were assumed to be involved in the detection of magnetic fields by bees (Gould et al. 1980).

    sChiff (1991) found, in the second abdominal ganglia of these bees, electrondense material identified as magnetite particles in the range of sizes characteristic of single-domain and superparamagnetic particles. The stability of the magnetic moment in magnetic nanoparticles depends on the type of mineral, the crystalline structure and the size. Particles with magnetic moment stable in the grain structure against thermal disorientation are known as single-domain particles, and particles with magnetic moment continuously disoriented by the thermal energy are known as superparamagnetic because they react easily to external magnetic fields (bean & livinGston 1959). Superparamagnetic and single domain particles of magnetite can be used to detect the geomagnetic field parameters and their small variations and this information can be transmitted to the nervous system through secondary mechanoreceptors (Johnsen & lohMann 2005).

    sChiff & Canal (1993) found in the abdominal hairs of these bees, particles of magnetite that might be involved in the detection and amplification of the external magnetic field gradients. Other studies have also indicated the presence of iron oxides by biomineralization (Gould et al. 1978; kuterbaCh & WalCott 1986; hsu & li 1994).

    Bees can also be trained to do associations between food source and the presence and direction of local magnetic fields (Walker & bitterMan 1985; frier et al. 1996).

    In ants have been detected the influence of the magnetic field by anderson & vander der Meer (1993) who observed differences in the time to trail formation by fire ant workers (Solenopsis invicta Buren) in conditions of normal and inverted geomagnetic field.

    Recently it has been shown that this type of ant shows magnetic orientation in low light ambient, changing its orientation direction when the geomagnetic field direction changes (sandoval et al. 2012).

    For the migratory ant Pachycondyla marginata (Roger), aCosta-avalos et al. (2001) showed that the migration routes preferentially are in the geomagnetic North direction, showing the possibility of using the information of the geomagnetic field in the choice of the migration direction.

    A compass response was shown in Formica rufa L. orientation (CaMlitepe & stradlinG 1995) and Oecophylla smaragdina (Fabricius) (Jander & Jander 1998). And in the absence of sunlight cues, Atta colombica Gurin-Mneville ants respond to magnetic field reversals (banks & sryGley 2003). Distortions of the local geomagnetic field have been proposed for handling the leafcutter ant (paz et al. 2012). WaJnberG et al. (2010) presented a review of recent magnetic orientation experiments in ants. Interestingly, experiments done with ants do not show light-dependent magnetoreception up to our knowledge, perhaps because of their subterranean life that makes ants life be the most of the time in darkness or perhaps because experiments have not been planned to test specifically light-dependent magnetoreception.

    The main model used to understand magnetoreception in insects is the ferromagnetic hypothesis. It implies that there must be magnetic nanoparticles in the ant body. The usual ways to detect these nanoparticles are measurements by magnetometry techniques and extraction and observation by transmission electron microcopy. Among the magnetometry techniques two have been used in ants: ferromagnetic resonance (FMR) and SQUID magnetometry (WaJnberG et al. 2010).

    The presence of magnetic material, probably magnetite, was demonstrated by applying the FMR technique in smashed whole bodies of ants Solenopsis sp. (esquivel et al. 1999), in crushed abdomens of the migratory ant P. marginata (WaJnberG et al. 2000), in abdomens of honeybees A. mellifera (el-JaiCk et al. 2001) and in body parts of the termite Neocapritermes opacus Hagen (alves et al. 2004). SQUID magnetometry done in samples of A. mellifera bees and N. opacus termites showed hysteresis curves with parameters similar to the observed in P. marginata ants (ferreira et al. 2005)

    Magnetic materials were found in different parts of the body of social insects. Hysteresis curves at 300K, obtained with SQUID magnetometry, of ants P. marginata (WaJnberG et al. 2004) indicate that the major contribution to the saturation magnetization comes from the antenna, as well as in stingless bees, Schwarziana quadripunctata (Lepeletier) (luCano et al. 2006). In FMR results was observed greater amount of magnetic material in the heads with antennae than in abdomens with petioles of the ant Solenopsis substituta Santschi (abraado et al. 2005). These results points to the antennae as the place where the magnetoreceptor must be localized in ants and stingless bees, but until now this magnetic sensor has not been found. A study done with antenna of P. marginata ants indicates that the Johnstons organ and other antennae joints might host a magnetoreceptor sensor based in magnetic nanoparticles (oliveira et al. 2010).

    SOCIAL WASPS

    The social wasps comprise representatives in Stenogastrinae, Vespinae and Polistinae (Carpenter 1982), but studies on the influence of magnetic fields on vespids so far include only Vespinae.

    One of the first studies on social wasps was done by kisliuk & ishay (1977). In that study wasps of Vespa orientalis L. in different life stages were exposed to artificial magnetic fields, and the nest architecture construction and behavior were analyzed. Nests with 15 to 20 wasps were put inside and outside a square cross-section

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    coil, and three experimental situations were studied: one with artificial uniform horizontal magnetic field of 23.3 Oe, other with artificial uniform horizontal magnetic field of 1.3 Oe and other with an artificial nonuniform horizontal magnetic field among 0.3 and 0.6 Oe. The local geomagnetic horizontal component was 0.33 Oe. After 16 days, several observations were done. The most interesting were: adult hornets died in the incidence of an uniform magnetic field in a period of 1 to 2 days and did not construct any nest; juvenile lasted more to died and showed a period of adaptation of 4 to 5 days in places were the intensity of the magnetic field was stronger (near to the coil), constructed nest and died with 5 to 7 days; in nonuniform fields juvenile did not die and constructed nests; the architecture of the nest was similar to the normal one, but with a higher distribution of orientations in the cylindrical cells, and the pedicles inverted its normal orientation (from downward to upward).

    All these results show that wasps are sensible to magnetic fields. It is known that wasps use as reference to nest architecture the gravitational field (ishay & sadeh 1975). The influence of the magnetic field on the architecture and orientation of wasp nests show that, in some way, there is a relation among the perception of the gravitational field and the magnetic field. Also the mentioned research is not related to magnetoreception in wasps but only to magnetic sensibility.

    The hexagonal cells of immatures inside the comb in nests of V. orientalis are uniform in their architecture and orientation. stokroos et al. (2001) found that each cell contains a small crystal stuck with saliva of the wasp, which projects down from the center of its domed roof having about 100 m in diameter and composed of polydomains, and with a typical composition of the magnetic mineral ilmenite (FeTiO3). These crystals form a network that can help the wasps to assess the symmetry, the balance of the cells and the direction of gravity, while building the comb. It is not known what the wasps perceive of ilmenite, because as well as being a magnetic material it also reflects infrared light. These two properties make this material an excellent source of information for spatial orientation (ishay et al. 2008).

    These wasps possibly collect the crystals of the local environment, but it is not ruled out biomineralization, because the titanium and the iron are present in their bodies (stokroos et al. 2001).

    As mentioned above, the construction of the combs in Vespinae is always in the vertical direction, and on the roof of each cell at least a small magnetic stone is incorporated and fixed by saliva. Thus ishay et al. (2008) attempted to identify, and characterize these stones that exist in the roof and walls of the combs of V. orientalis, using bio-ferrography to isolate magnetic particles on slides. The slides, as well as the original cells were analyzed by a variety of analytical techniques in an environmental scanning electron microscope. These authors verified that both the roof and the walls of each comb cell contained minerals such as ferrites, as well as titanium and zirconium. The last two components were less abundant in the soil around the nest and are known to reflect infrared light. Infrared images showed a thermoregulatory center in the dorsal thorax of adults. However it is not known whether these insects can sense infrared light.

    Magnetic remanence has been detected in abdomens of Vespa affinis L. (hsu 2002). This suggests that magnetic materials are present in the body of these wasps. Subsequently, hsu (2004) found the deposition of intracellular iron in V. affinis using transmission electron microscopy and atomic emission spectroscopy. He shows that the deposition would begin on the 2nd day after hatching. Also noted that vesicles containing granules of iron would be randomly distributed within the cytoplasm of trophocytes below the cuticle of hornets. The iron granules are formed by aggregation of dense tiny particles, and deposited in vesicles of iron, a double membrane, which appear to derive from the endoplasmic reticulum. These granules continuously expand

    by adding dense tiny particles until the 5th day after hatching. Then, granules and vesicles merge and expand. The existence of a blurred area under the inner membrane of the vesicle plays an important role in the formation of small dense particles. The elemental composition analysis indicated that the granules were composed mainly of iron, phosphorus and minor amounts of calcium.

    Thus the deposition of intracellular iron was first demonstrated in cells of honeybees (kuterbaCh et al. 1986; hsu & li 1994), then in bumblebees (WalCott 1985) and later in wasps by hsu (2004).

    Recently pereira-boMfiM et al. (2015) showed that the social wasp Polybia paulista (Ihering) is sensible to modifications in the local geomagnetic field. The experiments were done with magnets and coils, and in both cases the foraging flight frequency increases when the geomagnetic field was modified.

    CONCLUSIONS

    There are few studies in social wasps considering magnetoreception and magnetosensibility, compared to similar studies in bees, ants and termites. More studies must be done to understand the influence of the geomagnetic field and artificial magnetic fields on the behavior of wasps.

    Studies conducted in different animals have shown that magnetoreception can depend on the existence of intracellular magnetic nanoparticles or depend on light absorbing molecules sensible to magnetic fields (light-dependent magnetoreception) (WiltsChko & WiltsChko 2006). In social insects, the most studied has been the bee A. mellifera however some studies has been inconclusive (vlkov & vaCh 2012) and there are still many studies to be done to show the type of magnetoreception (dependent or independent of light) in these insects. Ants are the second most studied group. However, in all cases is still unknown the location of the magnetorreceptor and their nature (WaJnberG et al. 2010).

    It is expected that in bees and wasps the same will happen, not in the abdomen as has been discussed. A recommendation for future studies in wasps is the search for magnetic particles on the head and antennae and the analysis of the effects of monochromatic light combined with magnetic fields.

    Special emphasis should be given to the fact that flying insects should feel magnetic fields in the same way as birds, showing both types of magnetoreception.

    ACKNOWLEDGMENTS

    The authors gratefully the CAPES for a doctoral fellowship

    awarded to the first author. WFAJ acknowledges his research

    grant from CNPq. DAA acknowledges CNPq financial support.REFERENCES

    Abraado, L.G., D.M.S. Esquivel, O.C. Alves & E. Wajnberg, 2005. Magnetic Material in Head, Thorax and Abdomen of Solenopsis substituta Ants: a Ferromagnetic Resonance (FMR) Study. Journal of Magnetic Resonance, 175: 306-316. DOI: http://dx.doi.org/10.1016/j.jmr.2005.05.006.

    Acosta-Avalos, D., D.M.S. Esquivel, E. Wajnberg, H.G.P. Lins de Barros, P.S. Oliveira & I. Leal, 2001. Seasonal patterns in the orientation system of the migratory ant Pachycondyla marginata. Naturwissenschaften, 88: 343-346. DOI: http://dx.doi.org/10.1007/s001140100245.

    Acosta-Avalos, D., E. Wajnberg, D.M.S. Esquivel & L.J. El-Jaick, 2000. Insetos sociais: um exemplo de magnetismo animal. Revista Brasileira de Ensino de Fsica, 22: 317-323.

    Alves, O.C., E. Wajnberg, J.F. Oliveira & D.M.S. Esquivel, 2004. Magnetic material arrangement in oriented

  • 4Magnetoreception in Social Wasps: An Update Pereira-Bomfim et al.

    e-ISSN 1983-0572

    termites: a magnetic resonance study. Journal of Magnetic Resonance, 168: 246-251. DOI: http://dx.doi.org/10.1016/j.jmr.2004.03.010.

    Anderson, J.B. & R.K. Vander der Meer, 1993. Magnetic orientation in fire ant, Solenopsis invicta. Naturwissenschaften, 80: 568-570. DOI: http://dx.doi.org/10.1007/BF01149274.

    Banks, A.N. & R.B. Srygley, 2003. Orientation by magnetic field in leaf-cutter ants, Atta colombica (Hymenoptera: Formicidae). Ethology, 109: 835-846. DOI: http://.doi.org/10.1046/j.0179-1613.2003.00927.x.

    Bean, C.P. & J.D. Livingston, 1959. Superparamagnetism. Journal of Applied Physics, 30: S120-S129.

    Bellini, S., 2009. On a unique behavior of freshwater bacteria. Chinese Journal of Oceanology and Limnology, 27: 3-5.

    Blackemore, R.P., 1975. Magnetotactic bacteria. Science, 19: 377-379. DOI: http://dx.doi.org/10.1126/science.170679.

    Camlitepe, Y. & D.J. Stradling, 1995. Wood ants orient to magnetic fields. Proceedings of the Royal Society of London, 261: 37-41. DOI: http://dx.doi.org/10.1098/rspb.1995.0114.

    Carpenter, J.M, 1982. The philogenetic relationships and natural classification of the Vespoidea (Hymenoptera). Systematic Entomology, 7: 11-38. DOI: http://dx.doi.org/10.1111/j.1365-3113.1982.tb00124.x.

    Carpenter, J.M. & O.M. Marques, 2001. Contribuio ao estudo dos vespdeos do Brasil (Insecta, Hymenoptera, Vespoidea, Vespidae) [CD-ROM]. Cruz das Almas BA, Brasil. Universidade Federal da Bahia, Escola de Agronomia, Departamento de Fitotecnia/ Mestrado em Cincias Agrrias. Srie Publicaes Digitais, 2.

    El-Jaick, L.J., D. Acosta-Avalos, D.M.S. Esquivel, E. Wajnberg & M.P. Linhares, 2001. Electron paramagnetic resonance study of Honeybee Apis mellifera abdomens. European Biophysics Journal, 29: 579-586. DOI: http://dx.doi.org/10.1007/s002490000115.

    Esquivel, D.M.S., D. Acosta-Avalos, L.J. El-Jaick, A.D.M. Cunha, M.G. Malheiros, E. Wajnberg & M.P. Linhares, 1999. Evidence for magnetic material in the fire ant Solenopsis sp. By Electron Paramagnetic Resonance measurements. Naturwissenschaften, 86: 30-32. DOI: http://dx.doi.org/10.1007/s001140050564.

    Ferreira, J., G. Cernicchiaro, M. Winklhofer, H. Dutra, P.S. Oliveira, D.M.S. Esquivel, E. Wajnberg, 2005. Comparative magnetic measurements on social insects. Journal of Magnetism and Magnetic Materials, 289: 442-444.

    Frier, H.J., E. Edwards, C. Smith, S. Neale & T.S. Collet, 1996. Magnetic compass cues and visual pattern learning in honeybees. Journal of Experimental Biology, 199: 1353-1361.

    Gould, J.L., 2008. Animal navigation: the evolution of magnetic orientation. Current Biology, 18: R482-R484. DOI: http://dx.doi.org/10.1016/j.cub.2008.03.052.

    Gould, J.L., J.L. Kirschvink & K.S. Deffyes, 1978. Bees have magnetic remanence. Science, 201: 1026-1028. DOI: http://dx.doi.org/10.1126/science.201.4360.1026.

    Gould, J.L., J.L. Kirschvink, K.S. Deffeyes & M.L. Brines, 1980. Orientation of Demagnetized Bees. Journal of Experimental Biology, 86: 1-8.

    Hepworth, D., R.S. Pickard & K.J. Overshott, 1980. Effects of the periodically intermittent application of a constant magnetic field on the mobility in darkness of worker honeybees. Journal of Apicultural Research, 19: 179-186.

    Hsu, C.Y. & C.W. Li, 1994. Magnetoreception in honeybees. Science, 265: 95-96. DOI: http://dx.doi.org/10.1126/science.265.5168.95.

    Hsu, C.Y., 2002. Magnetic remanence in common hornet (Vespa affnis). Journal of Minghsin Institute of Technology, 28: 181-186.

    Hsu, C.Y., 2004. The process of iron deposition in the common hornet (Vespa affinis). Biology of the Cell, 96: 529-537. DOI: http://dx.doi.org/10.1016/j.biolcel.2004.05.001.

    Ishay, J. & D. Sadeh, 1975. Direction finding by hornets under gravitational and centrifugal forces. Science, 190: 802-804.

    DOI: http://dx.doi.org/10.1126/science.1198099.Ishay, J.S., Z. Barkay, N. Eliaz, M. Plotkin, S. Volynchik & D.J.

    Bergman, 2008. Gravity orientation in social wasp comb cells (Vespinae) and the possible role of embedded minerals. Naturwissenschaften, 95: 333-342. DOI: http://dx.doi.org/10.1007/s00114-007-0334-z.

    Jander, R. & U. Jander, 1998. The light and magnetic compass of the weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae). Ethology, 104: 743-758.

    Jardine, M., 2010. Sunscreen for the young earth. Science, 327: 1206-1207.

    Johnsen, S. & K.J. Lohmann, 2005. The physics and neurobiology of magnetoreception. Nature Reviews Neuroscience 6, 703-712. DOI: http://dx.doi.org/10.1038/nrn1745.

    Kirschvink, J.L., A.K. Kirschvink & B. Woodford, 1992. Magnetite biomineralization in the human brain. Proceedings of the National Academy of Sciences USA, 26: 7683-7687.

    Kisliuk, M. & J. Ishay, 1977. Influence of an additional magnetic field on hornet nest architecture. Experientia, 33: 885-887.

    Korall, H., T. Leucht & H. Martin, 1988. Bursts of magnetic fields induce jumps of misdirection in bees by a mechanism of magnetic resonance. Journal of Comparative Physiology A, 162: 279-284.

    Kuterbach, D.A. & B. Walcott, 1986. Iron containing cells in the honeybee (Apis mellifera). I. Adult morphology and physiology. Journal of Experimental Biology, 126: 375-387.

    Lindauer, M. & H. Martin, 1968. Die Schwereoientierung der Biene unter dem Einfluss des Erdmagnetfelds. Zeitschrift fur vergleichende physiologie, 60: 219-243.

    Lohmann, K.J. & S. Johnsen, 2000. The neurobiology of magnetoreception in vertebrate animals. Tins - Trends in Neurosciences, 23: 153-159.

    Lucano, M.J., G. Cernicchiaro, E. Wajnberg & D.M.S. Esquivel, 2006. Stingless Bee Antennae: a magnetic sensory organ? BioMetals, 19: 295-300. DOI: http://dx.doi.org/10.1007/s10534-005-0520-4.

    Martin, H. & M. Lindauer, 1977. Der Einflu des Erdmagnetfeldes auf die Schwereorientierung der Honigbiene (Apis mellifica). Journal of Comparative Physiology A, 122: 145-187.

    Martin, H., H. Korall & B. Forster, 1989. Magnetic field effects on activity and ageing in honeybees. Journal of Comparative Physiology A, 164: 423-431.

    Oliveira, J.F., E. Wajnberg, D.M. Esquivel, S. Weinkauf, M. Winklhofer, M. Hanzlik, 2010. Ant antennae: are they sites for magnetoreception? Journal of the Royal Society, Interface 7: 143-152. DOI: http://dx.doi.org/10.1098/rsif.2009.0102.

    Paz, H., M.A. Vargas, O.A. Forero, J.F. Pabn, J.A. Plaza, 2012. Local distorion of the earths magnetic field as a proposal for handling the leafcutter ant species Atta spp. (Hymenoptera: Formicidae). Ingeniera e Investigacin, 32: 28-33.

    Pereira-Bomfim, M.G.C., W.F. Antonialli-Junior, D. Acosta-Avalos, 2015. Effect of magnetic field on the foraging rhythm and behavior of the swarm-founding paper wasp Polybia paulista Ihering (Hymenoptera: Vespidae). Sociobiology, 62: 99-104.

    Sandoval, E.L., E. Wajnberg, D.M.S. Esquivel, H. Lins de Barros & D. Acosta-Avalos, 2012. Magnetic orientation in Solenopsis sp. ants. Journal of Insect Behavior, 25: 612-619.

    Schiff, H. & G. Canal, 1993. The magnetic and electric fields induced by superparamagnetic magnetite in honeybees. Biological Cybernetics, 69: 7-17.

    Schiff, H., 1991. Modulation of spike frequencies by varying the ambient magnetic field and magnetite candidates in bees (Apis mellifera). Comparative Biochemistry and Physiology A, 4: 975-985. DOI: http://dx.doi.org/10.1016/0300-9629(91)90325-7.

    Shcherbakov, V.P. & M. Winklhofer, 1999. The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. European Biophysics Journal, 28: 380-392. DOI: http://dx.doi.org/10.1007/s002490050222.

  • Janeiro - Abril 2016 - www.periodico.ebras.bio.br EntomoBrasilis 9 (1)

    e-ISSN 1983-0572

    5

    Skiles, D.D., 1985. The geomagnetic field: its nature, history and biological relevance, p. 43-102. In: Kirschvink, J.L., D.S. Jones & B.J. MacFadden, (Eds.). Magnetite Biomineralization and Magnetoreception in Organisms. A new biomagnetism. New York, Plenum Press, 682p.

    Stokroos, I., L. Litinetsky, J.J.L.Van der Want & J.S. Ishay, 2001. Keystone-like crystals in cells of hornet combs. Nature, 411: 654.

    Towne, W.F. & J.L. Gould, 1985. Magnetic field sensitivity in honeybees, p. 385-406. In: Magnetite Biomineralization and Magnetoreception in Organisms. A new biomagnetism. Kirschvink, J. L., Jones, D.S. & MacFadden B.J. (Eds). Plenum Press New York and London. 704 p.

    Vlkov, T. & M. Vcha, 2012. How do honeybees use their magnetic compass? Can they see the North? Bulletin of Entomological Research, 102: 461-467. DOI: http://dx.doi.org/10.1017/S0007485311000824.

    Wajnberg, E., D. Acosta-Avalos, L.J. El-Jaick, L.G. Abraado, J.L.A. Coelho, A.F. Bakusis, P.C. Morais & D.M.S. Esquivel, 2000. Electron Paramagnetic Resonance Study of the Migratory Ant Pachycondyla marginata abdomens. Biophysical Journal, 78: 1018-1023. DOI: http://dx.doi.org/10.1016/S0006-3495(00)76660-4.

    Wajnberg, E., D. Acosta-Avalos, O.C. Alves, J.F. Oliveira, R.B. Srygley & D.M.S. Esquivel, 2010. Magnetoreception in eusocial insects: an update. Journal of the Royal Society Interface, 7: S207-S226. DOI: http://dx.doi.org/10.1098/rsif.2009.0526.focus.

    Wajnberg, E., G. Cernicchiaro & D.M.S. Esquivel, 2004. Antennae: the strongest magnetic part of the migratory ant. BioMetals, 17: 467-470. DOI: http://dx.doi.org/10.1023/B:BIOM.0000029443.93732.62.

    Walcott, B., 1985. The cellular localization of particulate iron, p. 417-438. In: Kirschvink, J.L., D.S. Jones & B.J. MacFadden (Eds.). Magnetite biomineralization and magnetoreception in organisms: A new biomagnetism. New York, Plenum Press. 682p.

    Walker, M.M. & M.E. Bitterman, 1985. Conditioned responding to magnetic field by honeybees. Journal of Comparative Physiology A, 157: 67-71. DOI: http://dx.doi.org/10.1007/BF00611096.

    Wiltschko, W. & R. Wiltschko, 2006. Magnetoreception. BioEssays, 28: 157-168.

    Received in: 03.v.2015Accept in: 10.vii.2015

    **********

    Suggested citation:

    Pereira-Bomfim, M. da G.C., W.F. Antonialli-Junior & D. Acosta-Avalos, 2016. Magnetoreception in Social Wasps: An Update. EntomoBrasilis, 9 (1): 01-05. Available in: doi:10.12741/ebrasilis.v9i1.526

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    Repertoire of Defensive Behavior in Africanized Honey Bees (Hymenoptera: Apidae): Variations in Defensive

    Standard and Influence of Visual StimuliFbio de Assis Pinto, Paula Netto, Kleber de Sousa Pereira & Terezinha Maria Castro Della Lucia

    1. Programa de Ps Graduao em Entomologia - Universidade Federal de Viosa, e-mail: [email protected] (Autor para correspondncia), [email protected], [email protected]. 2. Departamento do Biologia Animal - Universidade Federal de Viosa, e-mail: [email protected].

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    Abstract. The Africanized honey bees (AHB) are known by the high productivity and tolerance against pathogens and parasites such Varroa destructor. Besides these beneficial characteristics, the AHB are considered highly defensive and generally urges caution in management. However, little is known about the behavioral aspects of AHB in Brazilian beekeeping. In this context, our objectives were to evaluate the repertoire of defensive behavior (DB) in AHB emphasizing the relevance of environmental and visual stimuli, as well as the aggressiveness gradient among Brazilian colonies. The aspects related to defensive behavior were measured by Stort method with some adaptations. We found differences between colonies in the speed of first attack and attack intensity (p

  • 7Repertoire of Defensive Behavior in Africanized Honey Bees Pinto et al.

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    As a way to mitigate aggressiveness and emphasize positive aspects like high production, selection breeding methods are shown to be promising in modern beekeeping. In this context, we evaluated the DB in Africanized honey bees highlighting the importance of visual stimuli among other factors in the defense of the colony.

    MATERIAL AND METHODS

    The experiments were conducted at the experimental apiary of the Universidade Federal de Viosa, Minas Gerais, Brazil (-20 45 37.99, -42 51 55.50). We used in the experiments three highly populated colonies (approx. 60,000 workers) maintained in Langstroth hives with food and brood combs.

    The aggressiveness was measured by stort method (1974) with some adaptations. We utilized a 3cm diameter sphere half coated with a black fabric and the other half coated with white fabric painted with UV dye. The evaluated parameters were: (a) occurrence time of the first sting in the sphere, (b) Number of stings in each color part of sphere and (c) Total number of stings during each application test (60 seconds). During each test, the behavioral alterations were observed and recorded to construct an ethogram of defensive behavior in AHB (Table 1).

    The tests were performed three times per day (7:30h, 12h e 16h) in each colony during three consecutive days. The local temperature and relative humidity were also recorded in each test. To prevent the interference of concentration of alarm pheromone in materials, the spheres were not reused during the tests. To verify differences in defensive patterns between colonies, an analysis of variance (ANOVA) was performed, followed by Dunn test. In

    turn, the relations between environmental factors and DB were performed by Pearson Correlation Coefficient.

    RESULTS

    An ethogram of defensive behavior was generated by focal observations during the trials (Table 1). Seven events were observed and were allocated into two key-events (Identification of invader and Attack). Both evaluated aspects in defensive behavior (time for first sting and attack intensity) differed significantly between colonies (p

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    movements near the colony promoted the first attack responses. However the portion coated with white fabric painted with UV dye was also attacked posteriorly, even with a lower intensity than the black part indicating the pheromone importance in colony defense.

    The innate defensive patterns against certain textures and dark colors can be an elaborate instinctive answer due the selective pressures of mammalian predators (free 1961). Although, due to the high capacity of chemical communication, invaders without such features (dark hairs e.g.) are identified by their odors and after the first sting, alarm pheromones increase the target area (Collins & kubasek 1982; vissCher et al. 1995; kastberGer et al. 2009; roMan & Gladysz 2009).

    The visual and chemical stimuli also interact in avoiding behaviors (shorter & rueppell 2012). Typical behaviors such as intensive wing-beats and hitting the target before the sting could possibly be a warning behavior by the individual, thus avoiding the suicidal DB (tan et al. 2012). We observed these behaviors before and after the first stings. In our point-of-view this fact shows a great role in colony defense. The continuous attack of bees that have stung can enhance the visualization of the target, furthermore this behavior acts like an attempt to intimidate and expel intruders (Cunard & breed 1998; shorter & rueppell 2012).

    Genetic variability vs. DB. AHB present a great genetic variability due the hybrid character of this race originated from cross breeding between European and African bees (Collet at al. 2006). In this context, it is very possible to observe great variations in defensive behaviors between colonies in the same region (breed et al. 2004). We could observe this variation comparing the behavioral differences between colonies regardless of climatic factors and evaluation period. Similar results were also found with AHB in Mossor, Northeast of Brazil where expressive changes were observed in response speed and intensity of attacks among colonies evaluated (nasCiMento et al. 2008).

    Regardless the behavioral variability, AHB normally present faster and higher defensive pattern compared to European races. In a study using Africanized / European co-fostered colonies, 81% of the initial attacks were performed by Africanized individuals (GuzMn-novoa et al. 2004). However, even with the role of regulatory genes, the biotic and abiotic factors such as physiological condition of the colony and environmental changes are also involved in behavioral changes (alaux et al. 2009). Although we found no relationship between temperature and DB, more intensive temperature changes may affect the DB. In northeast region, AHB colonies have varied the average number of stings from 16.7 to 22.7 in accord to the daily fluctuation of temperature (nasCiMento et al. 2005).

    Assessments in different periods with different climatic conditions can gauge the importance of this character. However, the colony population change due to a longer period of time as food availability may also affect the comparisons. Apparently several biotic and abiotic factors interact in defense of the colony, which may be considered by plasticity of the DB in A. mellifera. In our study, we identified a great variation between colonies in the repertoire of defensive behavior even being kept under the same conditions. Visual stimuli including color and movement were important components in DB of AHB. However, inter /intraspecific chemical stimuli favor the identification of possible invaders and allow joint defensive actions in favor of the colony.

    ACKNOWLEDGMENTS

    We would like to thank the apicultural center of Entomology Department at the Universidade Federal de Viosa by the colonies used in this work. We are also grateful for CNPq and Capes for financial support.

    REFERENCES

    Alaux, C., S. Sinha, L. Hasadsri, G.J. Hunt, E. Guzmn-Novoa, G. DeGrandi-Hoffman & G.E. Robinson, 2009. Honey bee aggression supports a link between gene regulation and behavioral evolution. Proceedings of the National Academy of Sciences, 106: 15400-15405.

    Avargus-weber, A., T. Mota & M. Giurfa, 2012. New vistas on honey bee vision. Apidologie, 43: 244-268.

    Breed, M.D, E. Guzmn-Novoa & G.J. Hunt, 2004. Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annual Review of Entomology, 49: 271-98.

    Collet, T., K.M. Ferreira, M.C. Arias, A.E.E. Soares & M.A. Del Lama, 2006. Genetic structure of Africanized honeybee populations (Apis mellifera L.) from Brazil and Uruguay viewed through mitochondrial DNA COICOII patterns. Heredity, 97: 329-335.

    Collins, A.M. & K.J. Kubasek, 1982. Field Test of Honey Bee (Hymenoptera: Apidae) Colony Defensive Behavior. Annals of the Entomological Society of America, 75: 383-387.

    Couto, R.H.N. & L.A. Couto, 2002. Apicultura: Manejo e produtos. Jaboticabal, FUNEP, 191p.

    Cunard, S. & M. Breed, 1998. Post-stinging behavior of worker honey bees (Hymenoptera: Apidae). Annals of the Entomological Society of America, 91: 754-757.

    Free, J.B., 1961. The stimuli releasing the stinging response of honeybees. Animal Behavior, 9: 193-196.

    Gullan, P.J. & P.S. Cranston, 2010. The Insects: An Outline of Entomology 4th Edition. London, Wiley, 561p.

    Guzmn-Navoa, E., G.J. Hunt, J.L. Uribe-Rubio & D. Prieto-Merlos, 2004. Genotypic effects of honey bee (Apis mellifera) defensive behavior at the individual and colony levels: the relationship of guarding, pursuing and stinging. Apidologie, 35: 15-24.

    Guzmn-Navoa, E., G.J. Hunt, R.E. Page, J.L. Uribe-Rubio, D. Prieto-Merlos & F Becerra-Guzman, 2005. Paternal Effects on the Defensive Behavior of Honeybees. Journal of Heredity, 96: 1-5.

    Kastberger, G., R. Thenius, A. Stabentheiner & R. Hepburn, 2009. Aggressive and Docile Colony Defence Patterns in Apis mellifera. A RetreaterReleaser Concept. Journal of Insect Behavior, 22: 65-85.

    Moretto, G., L.S. Gonalves, D. De Jong & M.Z. Bichuette, 1991. The effects of climate and bee race on Varroa jacobsoni Oud. infestations in Brazil. Apidologie 22: 197-203.

    Moritz, R.F., E.E. Southwick & J.R. Harbo, 1987. Genetic analysis of defensive behaviour of honeybee colonies (Apis mellifera L.) in a field test. Apidologie, 18: 27-42.

    Nascimento, F.J., M. Gurgel & P.B. Maracaj, 2005. Avaliao da agressividade de abelhas africanizadas (Apis mellifera) associada hora do dia e a temperatura no municpio de Mossor RN. Revista de Biologia e Cincias da Terra, 5: without page.

    Nascimento, F.J., P.B. Maracaj, E.T. Diniz Filho, F.J.M. de Oliveira, R.M. Nascimento & M.G. de Sousa, 2008. Agressividade de abelhas africanizadas (Apis mellifera) associada hora do dia e a umidade em Mossor-RN. Acta Veterinaria Brasilica, 2: 80-84.

    Pinto, F.A., A. Puker, D. Message & L.M.R.C. Barreto, 2011a. Varroa destructor in Juquitiba, Vale do Ribeira, Southeastern Brazil: Seasonal Effects on the Infestation Rate of Ectoparasitic Mites in Honeybees. Sociobiology, 57: 511-518.

    Pinto, F.A., A. Puker, L.M.R.C Barreto & D. Message, 2012. The ectoparasite mite Varroa destructor Anderson and Trueman in southeastern Brazil apiaries: effects of the hygienic behavior of Africanized honey bees on infestation rates. Arquivo Brasileiro de Medicina Veterinria e Zootecnia, 64: 1194-1199.

    Pinto, F.A., G.K. Souza, M.A. Sanches & J.E. Serro, 2011b. Parasitic Effects of Varroa destructor (Acari: Varroidae)

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    e-ISSN 1983-0572

    9

    on Hypopharyngeal Glands of Africanized Apis mellifera (Hymenoptera: Apidae). Sociobiology, 58: 769-778.

    Reser, D.H., R.W. Witharanage, M.G. Rosa & A.G. Dyer, 2012. Honeybees (Apis mellifera) learn color discriminations via differential conditioning independent of long wavelength (green) photoreceptor modulation. PLoS One, 7: e48577.

    Roman, A. & Z. Gladysz, 2009. Aggressive reaction level of the honeybee (Apis mellifera L.) to smell and knock. Journal of Apicultural Science, 53: 5-16.

    Shorter, J.R. & O. Rueppell, 2012. A review on self-destructive defense behaviors in social insects. Insectes Sociaux, 59: 1-10.

    Stort, A.C., 1974. Genetical study of agressiveness of two subspecies of Apis mellifera in Brazil. Journal of Apicultural Research, 13: 33-38.

    Tan, K., J. Wang, H. Li, S. Yang, Z. Hu, G. Kastberger & B.P. Oldroyd, 2012. An I see you prey-predator signal between the Asian honeybee, Apis cerana, and the hornet, Vespa velutina. Animal Behavior, 83: 879-882.

    Visscher, P.K., R.S. Vetter & G.E. Robinson, 1995. Alarm pheromone perception in honey bees is decreased by smoke (Hymenoptera: Apidae). Journal of Insect Behavior, 8: 11-18.

    Received in: 01.vii.2014Accepted in: 14.ix.2015

    **********

    Como citar este artigo:

    Pinto, F.A, P. Netto, K. de S. Pereira & T. M. C. Della Lucia, 2016. Repertoire of Defensive Behavior in Africanized Honey Bees (Hymenoptera: Apidae): Variations in Defensive Standard and Influence of Visual Stimuli. EntomoBrasilis, 9 (1): 06-09. Acessvel em: doi:10.12741/ebrasilis.v9i1.456

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    Invertebrate Colonization During Leaf Decomposition of Eichhornia azurea (Swartz) Kunth (Commelinales:

    Pontoderiaceae) and Salvinia auriculata Aubl. (Salvinales: Salvinaceae) in a Neotropical Lentic System

    Lidimara Souza da Silveira, Renato Tavares Martins & Roberto da Gama Alves

    1. Universidade Federal de Juiz de Fora, e-mail: [email protected] (Autor para correspondncia), [email protected]. 2. Instituto Nacional de Pesquisas da Amaznia, e-mail: [email protected].

    _____________________________________

    EntomoBrasilis 9 (1): 10-17 (2016)

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    Abstract. The decomposition of macrophytes is an essential process for cycling of carbon and nutrients, and it is source of organic matter for invertebrates in lakes. We evaluated the colonization by aquatic invertebrates in decomposing leaves of two species of macrophytes in a Neotropical lentic system. The experiment was conducted from November 2007 to February 2008, with the use of 54 litter bags (Eichhornia azurea (Swartz): n = 27 and Salvinia auriculata Aubl.: n= 27), each containing 10 g of dry leaves. Three bags of each species were retrieved after 2, 4, 8, 12, 24, 36, 48, 60 and 72 days of incubation. The remaining leaf mass of the two macrophytes species tended to decrease with time, although at different rates. The decomposition of E. azurea and S. auriculata leaves were classified as rapid and intermediate, respectively. In general, during the experiment carbon: nitrogen ratio declined in E. azurea and increased in S. auriculata, and presented difference among the days of the experiment and between the macrophyte species. In E. azurea mass loss was negatively correlated with carbon: nitrogen ratio of the leaves, but the same pattern was not observed for the S. auriculata leaves. The composition and richness of invertebrates differed among days, but not between macrophytes species. We concluded that the succession process along the detritus chain was more important in structuring the invertebrate community than the variation in the nutritional quality of the leaf litter for these two species of macrophytes.

    Keywords: Aquatic insects; Carbon: nitrogen ratio; Leaf breakdown; Macrophytes; Oligochaetes.

    Colonizao por Invertebrados Durante a Decomposio foliar de Eichhornia azurea (Swartz) Kunth (Commelinales: Pontoderiaceae) e Salvinia auriculata Aubl. (Salvinales: Salvinaceae) em um

    Sistema Lntico Neotropical

    Resumo. A decomposio de macrfitas um processo essencial para ciclagem de carbono e nutrientes, e fonte de matria orgnica para invertebrados em lagos. Avaliamos a colonizao por invertebrados aquticos em folhas em decomposio de duas espcies de macrfitas em um sistema lntico Neotropical. O experimento foi conduzido entre novembro de 2007 e fevereiro de 2008, com a utilizao de 54 sacos de detrito (Eichhornia azurea (Swartz): n = 27 e Salvinia auriculata Aubl.: n = 27), cada um contendo 10 g de folhas secas. Trs sacos de cada espcie foram recuperados aps 2, 4, 8, 12, 24, 36, 48, 60 e 72 dias de incubao. A massa remanescente de folha das duas espcies de macrfitas tendeu a diminuir com o tempo, embora a velocidades diferentes. A decomposio de folhas de E. azurea e S. auriculata foram classificadas como rpida e intermdia, respectivamente. Em geral, durante o experimento a razo carbono: nitrognio diminuiu em E. azurea e aumentou em S. auriculata, e apresentou diferena entre os dias de experimento e entre as espcies de macrfitas. Em E. azurea perda de massa foi negativamente correlacionada com a razo de carbono: nitrognio das folhas, mas o mesmo padro no foi observado para as folhas de S. auriculata. A composio e riqueza de invertebrados diferiram entre os dias, mas no entre espcies de macrfitas. Conclumos que o processo de sucesso ao longo da cadeia de detritos foi mais importante na estruturao da comunidade de invertebrados do que a variao na qualidade nutricional do detrito de folha para estas duas espcies de macrfitas.

    Palavras-chave: Insetos aquticos; Decomposio foliar; Macrfitas; Oligoquetas; Razo carbono: nitrognio.

    _____________________________________acrophytes are the main source of autochthonous organic matter in the littoral zone of lakes and their decomposition is an essential process for cycling of

    carbon and nutrients (Wetzel 2001; Li et al. 2012). The use of live macrophyte leaves as food is limited due to high concentration of cellulose and carbon: nitrogen (C:N) ratios, low digestibility of some proteins and presence of allelopathic substances that cannot be degraded by invertebrates (suren & lake 1989; bruquetas de zozaya & neiff 1991). However, during the decomposition process litter of macrophyte is an important source of both food and refuge for invertebrates (MorMul et al. 2006).

    The decomposition rate of aquatic plant species is influenced by interaction of environmental variables, intrinsic properties of the leaves and activity of microorganisms and invertebrates (GiMenes et al. 2010). Leaves intrinsic properties, such as size, morphological structure and initial chemical composition

    determine different decomposition rates for each plant species (GiMenes et al. 2010). Carbon (C) is the most recalcitrant of the structural components in macrophytes, and is often found in inverse proportion to the nitrogen (N) content in plant tissue (ChiMney & pietro 2006). Generally, higher leaf decomposition rates are associated with lower C:N ratios (paGioro & thoMaz 1998; ChiMney & pietro 2006).

    Invertebrates colonization on litter is influenced by leaf chemical composition, and by physical (i.e., reduced leaf size) and chemical (i.e., increase in nitrogen concentration) modification on the substrate due to activity of microorganisms (Gessner et al. 1999; Gulis & suberkropp 2003; Capelo et al. 2004; Gonalves Jr. et al. 2012), during the degradative ecological succession

    Funding Agencies: CNPq and FAPEAM

    doi:10.12741/ebrasilis.v9i1.548

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    (Gonalves Jr. et al. 2003). Shredder invertebrates use detritus as food and increase its nutritional content by their excrement, contributing to accelerate the decomposition (Graa 2001). Despite the importance of shredders in leaf decomposition in temperate regions, the low abundance of these invertebrates in relation to microorganisms, indicates that these organisms have less influence on the decomposition of leaves in tropical streams (Mathuriau & Chauvet 2002; Moretti et al. 2007). In contrast, shredders were abundant in study in tropical Australian streams, comprising about 24% of the total macroinvertebrates biomass, not including the crayfish (Cheshire et al. 2005).

    We aimed to analyze structure and composition of invertebrates community in decomposing leaves of Eichhornia azurea (Swartz) Kunth (Commelinales: Pontederiaceae) and Salvinia auriculata Aubl. (Salviniales: Salviniaceae) in a lentic system in southeastern Brazil, to verify if the chemical composition (C:N ratio) of the substrate has an influence on invertebrate colonization. We expected that higher decomposition rate and greater richness and abundance of invertebrates in macrophytes with a smaller carbon: nitrogen ratio (E. azurea). We also expected to observe differences in the colonization by invertebrates during the decomposition process due the improvement in nutritional quality of the substrate.

    MATERIAL AND METHODS

    Study Area. The experiment was conducted in Manacs Lake (21 46 68 S, 43 22 22 W), a reservoir with a surface area of 0.02 km and a maximum depth of 5 m (azevedo et al. 2003), located in southeastern Brazil. The lakes water is turbid (Secchi disk: 0.60 0.12 m), with neutral pH (7.10 0.25) and average levels ( S.D.) of dissolved oxygen, temperature and electrical conductivity of 5.55 2.04 mgL-1, 21.35 2.25C and 28.25 12.82 S cm-1, respectively. The lakes marginal vegetation consists principally of Merostachys sp. Sprengel (Poales: Poaceae) and specimens of Tibouchina granulose Cogniaux (Myrtales: Melastomataceae). In the summer, blooms of Salvinia spp. usually occur in the lake. However, during the experiment, macrophytes were not observed (Martins et al. 2011).

    Collection and data analysis. To perform the decomposition experiment we selected E. azurea and S. auriculata, two macrophyte species that are widely distributed in the Neotropical region (barrett 1978; alves dos santos 1999; santos et al. 2004; prado 2006). Leaves of these two species were collected from a lake in the Poo DAnta Municipal Biological Reserve (2145S, 4320W). The leaves were washed to remove the adhered material (silva et al. 2011) and then were air dried in an oven at 60C (24 h) to obtain initial dry mass (raMseyer & MarChese 2009).

    The experiment was conducted from November 2007 to February 2008, with the use of 54 litter bags (E. azurea: n= 27 and S. auriculata: n=27) measuring 15x15 cm and 2 mm mesh, each filled with 10 g of dry leaves. The litter bags were immersed near the bottom of Manacs Lake, about 3 m from the shoreline and 2.40 0.41 m ( S.D.) deep. To keep the litter bags in contact with the sediment, small weights (150 g) were attached to them. Three litter bags of each species were retrieved after 2, 4, 8, 12, 24, 36, 48, 60 and 72 days of incubation.

    The remaining material in each litter bag was fixed in 4% formaldehyde and washed on a sieve (mesh: 0.21 mm). The invertebrates were sorted under a stereoscopic microscope and identified to family level, using the identification keys for insects (MCCafferty 1981; Merrit & CuMMins 1984; Carvalho & Calil 2000; fernndez & doMinGuez 2001; pes et al. 2005; Costa et al. 2006) and for oligochaetes (brinkhurst & MarChese 1989). Invertebrates were classified into functional feeding groups according to Merrit & CuMMins (1984) and sChenkov & helesiC (2006), respectively. The Chironomidae were not included in

    determination of the trophic functional groups because they have a wide variety of feeding habits and their trophic classification is still uncertain (Moretti et al. 2007).

    The remaining plant material was dried in an oven at 60 C until reaching constant mass and then utilized to calculate the decomposition coefficient (k), according to a negative exponential equation (e.g., petersen & CuMMins 1974): k = [ln (initial mass / final mass)] / duration of the experiment; mass was expressed in grams and the duration time in days. The concentration of organic carbon in the E. azurea and S. auriculata leaves was estimated as being 46.5% of the organic matter content (Wetzel & likens 1991). To calculate the organic matter content, we used subsamples of the remaining incubated leaves. This material was ashed in porcelain crucibles at 550 C in a muffle furnace for 4 h (Wetzel & likens 1991). The organic matter content was calculated by the difference in the mass before and after ashing in the muffle furnace. The concentration of total nitrogen was determined by the digestion of subsamples of the remaining dry leaves with concentrated sulfuric acid in the presence of a catalyst (allen et al. 1974).

    We used analysis of variance (ANOVA two factors) to

    verify the existence of a significant difference of the leaf mass loss,

    leaf carbon: nitrogen ratio, abundance and richness (number of

    taxa) of invertebrates between macrophyte species and among

    the days of the experiment. Moreover, we used Pearsons

    correlation coefficient to analyze the relationship between mass

    loss and leaves carbon: nitrogen ratio, and between mass loss

    and invertebrates abundance. These analyzes was performed in

    R program (r Core teaM 2013).

    The similarity of the samples (macrophyte species and days) was analyzed by cluster analysis (UPGMA; Bray-Curtis distance coefficient), based on the invertebrate abundance (log x+1), with the NTSYS-PC version 2.10 program. To verify the variation in the composition of the community of invertebrates between the groups formed in the cluster analysis, we applied the nonparametric multiple response permutation procedure (MRPP) based on the Bray-Curtis distance coefficient, with the same data matrix used in the cluster analysis. This analysis was performed using the PC-ORD 5.15 program. Analysis of similarity (ANOSIM) was carried out to verify the variation in the composition of invertebrates between the two macrophyte species, using the R program (r Core teaM 2013).

    Indicator species analysis (dufrne & leGendre 1997) was used to verify which taxa were more closely related to a determined group of days established a priori in the cluster analysis. In this analysis, an indicator value is calculated for each species in each group and these are tested for statistical significance using a randomization technique. This analysis was performed in the PC-ORD version 5.15 program.

    RESULTS

    Leaf decomposition and C:N rate of the detritus. The decomposition coefficient was higher for Eichhornia azurea (k = 0.018 d-1) than Salvinia auriculata (k = 0.008 d-1). The mass loss for S. auriculata (30.2% of initial mass) were higher than those for E. azurea (24.1% of initial mass) in the initial period (day 2), but tended to reverse with experiment time duration, remaining 26.5% leaf masses for E. azurea and 51.0% for S. auriculata (Figure 1a). The remaining dry leaf mass of litter bags differ among days of the experiment (F1, 53 = 12.53; p < 0.001), but not between species of macrophytes (F1, 53 = 46.30; p = 1.000). There was no interaction between these factors (F1, 53 = 12.53; p = 1.000).We recorded a negative correlation between mass loss and C:N ratio of the leaves only for E. azurea (r = -0.87; p = 0.001), but not for S. auriculata (r = 0.39; p = 0.270).

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    The initial concentration of nitrogen in the E. azurea and S. auriculata leaves was 1.6% Dry Mass (DM) and 2.6% DM, respectively. During the experiment there was an increase in this nutrient in E. azurea, which reached 3.1% DM on day 72 (Figure 2b). In S. auriculata, the concentration of nitrogen on the last day (2.0% DM) was lower than at the start of the experiment (Figure 2b). The concentration of carbon in E. azurea (day 0= 43.3% DM, day 72= 38.8% DM) decreased during the experiment, unlike what occurred in the S. auriculata leaves (day 0 = 41.1% DM, day 72= 41.4% DM) (Figure 2c). We recorded a significant interaction effect between days of the experiment and macrophyte species on

    C:N ratio (F1, 39 = 22.26, p = 0.001). In S. auriculata was observed increase in C:N ratio during the experiment (day 0 = 15.7%; day 72 = 20.6%), however, in E. azurea we recorded high values of C:N ratio on day 0 (27.1%) in relation to day 72 (12.4%).

    Invertebrate communities. We recorded 8,093 individuals in E. azurea and 5,970 individuals in S. auriculata. The abundance of invertebrates ranged from 125 (day 2) to 1,553 (day 36) individuals in E. azurea, and from 59 (day 2) to 1,506 (day 36) individuals in S. auriculata (Table 1). The invertebrate abundance not differed among days of experiment (F1, 53 = 3861.1; p = 0.424)

    A B

    Figure 1. A. Remaining dry mass. B. nitrogen. C. carbon (means of three replicates S.D.) of Eichhornia azurea and Salvinia auriculata leaves during the decomposition experiment in Manacs Lake (southeastern Brazil). Full line: E. azurea; dashed line: S. auriculata.

    C

    Figure 2. Cluster analysis (UPGMA, Bray-Curtis) based on the abundance of invertebrates during the decomposition experiment with Eichhornia azurea (E) and Salvinia auriculata (S) leaves in Manacs Lake (southeastern Brazil). The indicator species with their respective values (numbers between parentheses) are listed in the cluster.

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    and between species of macrophytes (F1, 53 = 3910.3; p = 0.181). Moreover, there was no interaction between these factors (F1, 53 = 3858.4, p = 0.853).There was no relationship between mass loss and invertebrate abundance for E. azurea (r = 0.00; p = 0.944) and S. auriculata (r = 0.02; p = 0.549).

    We recorded 13 taxa of invertebrates in leaf litter of E. azurea and 17 taxa in S. auriculata. The richness ranged from four (day 24 and 72) to eight (days 4 and 8) taxa in E. azurea, and from three (day 60) to ten (day 8) taxa in S. auriculata (Table 1). The invertebrate richness differed among days of the experiment (F1, 53 = 17.44, p = 0.034), but not between species of macrophytes (F1, 53 = 18.90; p = 0.629). There was no interaction between these factors (F1, 53= 16.29, p = 0.061).

    In the cluster analysis (cophenetic correlation = 0.87), the samples were separated into three groups (Figure 2) according to the decomposition stage, independent of the macrophyte species.

    The first group was composed of day 2, on which no taxon was considered to be an indicator. The second group was composed of days 4, 8, 12, 24, 36 and 48 with Chironomidae, Polycentropodidae and Copepoda as indicator taxa. The last group was composed of days 60 and 72, with Naididae and Nematoda as indicators. The composition of the invertebrates community was different among the groups of days of the experiment (T = -6.92, A = 0.25, p < 0.001), but not differed between macrophytes species (R = 0.02, p = 0.290).

    The invertebrates were distributed into two functional feeding groups (Figure 3a, b). The relative abundance of collector invertebrates ranged from 21.2% (day 12) to 100% (day 2) in E. azurea, and from 24.0% (day 24) to 93.7% (day 72) in S. auriculata. The relative abundance of predator invertebrates ranged from 0.0% (day 2) to 78.8% (day 12) in E. azurea, and from 6.3% (day 72) to 75.0% (day 2) in S. auriculata. The shredders invertebrates were absent in both macrophytes.

    A B

    Figure 3. Relative abundance of functional feeding groups of invertebrates during the decomposition experiment with Eichhornia azurea (a) and Salvinia auriculata (b) leaves in Manacs Lake (southeastern Brazil). Black: collectors; white: predators.

    Table 1. Abundance of invertebrates in Eichhornia azurea and Salvinia auriculata leaves ordered by exposure days in Manacs Lake (southeastern Brazil).

    TaxaEichhornia azurea Salvinia auriculata

    2 4 8 12 24 36 48 60 72 2 4 8 12 24 36 48 60 72

    OLIGOCHAETA

    Aelosomatidae 0 1 12 0 2 3 19 36 70 0 2 7 2 4 3 2 0 0

    Enchytraeidae 0 1 1 2 0 0 0 0 0 0 2 0 0 2 0 0 0 0

    Naididae 1 14 31 160 115 152 262 393 300 2 13 36 114 344 413 300 201 278

    COLEOPTERA

    Elmidae 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0

    DIPTERA

    Chironomidae 120 529 1048 690 448 1369 824 549 494 43 279 269 513 727 1056 516 202 302

    Ceratopogonidae 0 0 0 0 0 1 0 0 0 0 1 1 0 0 0 0 0 0

    Culicidae 0 1 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0

    Empididae 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0

    Simuliidae 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

    EPHEMEROPTERA

    Baetidae 0 0 1 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0

    HEMIPTERA

    Hebridae 0 0 0 0 0 0 0 0 0 9 2 3 7 2 1 0 0 0

    ODONATA

    Libellulidae 0 0 1 0 0 0 0 0 0 0 2 0 1 0 0 0 0 0

    TRICHOPTERA

    Ecnomidae 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0

    To be continue...

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    DISCUSSION

    Leaf decomposition and C:N rate of the detritus. Based on the classification proposed by Gonalves Jr. et al. (2014) for Brazilian aquatic environments, the decomposition rates of the E. azurea and S. auriculata leaves were classified as rapid and intermediate, respectively. The faster decomposition of E. azurea may be related to smaller C:N ratio in their detritus. There was a negative correlation between mass loss of E. azurea and detritus quality (C:N ratio). ChiMney & pietro (2006) found a negative correlation between decomposition rate and C:N ratio and a positive correlation between decomposition rate and nitrogen content of different macrophyte species Typha domingensis Pers. and T. latifolia L. (Typhaceae), E. crassipes [Mart.] Solms. (Pontederiaceae), Pistia stratiotes L. (Araceae), Najas guadalupensis [Spreng.] Magnus (Hydrocharitaceae) and Ceratophyllum demersum L. (Ceratophyllaceae). lan et al. (2006) showed that rhizomes of Zizania latifolia (Griseb.) Turcz. ex Stapf (Poaceae) with lower C:N ratio presented faster decomposition rates. These results corroborate the importance of the quality of leaf litter on decomposition rate.

    On the first two days of decomposition, there was observed rapid mass loss in both macrophyte species. This high mass loss during the initial days is due to leaching of phenols and amino acids (Gessner et al. 1999). Martins et al. (2011) attributed the high mass loss in E. azurea leaves at the start of the experiment to method of drying the leaves in an oven before immersion in the lake, because this drying promoted rupture of the cell wall, accelerating the loss of soluble components. We used the same method, so it is likely the rapid mass loss observed at the start of experiment was related to this drying procedure.

    The decrease in C:N ratio observed in E. azurea leaves was not observed in S. auriculata. Although we did not analyze the colonization by microorganisms, it is well established in the literature that these organisms immobilize nitrogen from the water to the detritus (paGioro & thoMaz 1999; padial & thoMaz 2006), which may have contributed to increase the concentration of this nutrient in the decomposing E. azurea leaves, while the decline in carbon found in this species during the study period can be attributed to carbon mineralization (reJMnkov & houdkov 2006). sCiessere et al. (2011) studied three species of macrophytes (Salvinia sp., E. azurea and Cyperus giganteus Vahl (Cyperaceae)) and found that the Salvinia sp. litter was more recalcitrant, with lower mass loss and enzyme activity than the other two species. Therefore, it is likely that the S. auriculata leaves in our study may have been less colonized by microorganisms, influencing the reduction of N during the experiment. hoWard-WilliaMs & Junk (1976) and lonGhi et al. (2008) did not observe an increase in nitrogen concentration during decomposition of S. auriculata and S. natans (L.) All. (Salviniaceae) leaves, respectively.

    Invertebrate communities. We did not observed significant differences in abundance, richness and composition of invertebrates between the two macrophytes species, probably because we did not observe significant differences in the mass

    loss and rate of carbon: nitrogen between macrophytes species. In contrast to Mathuriau & Chauvet (2002) found that in Croton gossypifolius Vahl (Euphorbiaceae) leaves, with a faster decomposition rate, colonization by fungi and the accumulation of N support faster and more highest colonization by invertebrates, while Clidemia sp. (Melastomataceae) leaves, which degrade more slowly, provide a substrate more durable to fauna and support a more diversified invertebrate community.

    We recorded a significant increase of richness along the experiment, which may be related to observation of greater uniformity of organic matter particles size these stages of the experiment. According to Capello et al. (2004), the least heterogeneity at the beginning of the experiment is due the leaves to be a new substrate to be colonized. Similarly, at the end of the experiment the action of decomposer organisms leads to greater physical homogeneity of the detritus (Capello et al. 2004). Additionally, the increase in the proportion of support material (cellulose and lignin) (beGon et al. 1995) because of the consumption of softer parts leads to reduction in the richness of invertebrates.

    The better quality of detritus at the end of experiment provides a more plentiful food supply (sMoCk & stoneburner 1980), in turn allowing greater density of fauna (Gonalves Jr. et al. 2003, 2004; Moretti et al. 2007). However, even for E. azurea in which has an increase in the concentration of nitrogen and reducing in the concentration of carbon at the end of our experiment, no correlation was observed between the abundance of invertebrates and weight loss. Mathuriau & Chauvet (2002) also observed the N increase in both leaf species studied (C. gossypifolius and Clidemia sp.), and a decrease after the peak in early colonization of leaves by invertebrates.

    The composition of invertebrates was dissimilar among the days in the cluster analysis and MRPP, probably due the fauna respond differently to physical and chemical modification on the leaf litter during the experiment as a consequence of the different survival strategies. A study in a pond in the tropical region with Typha domingensis Pers. (Typhaceae) and Nymphaea ampla (Salisb.) DC. (Nympheaceae) was observed formation of three groups, according to the stage of decomposition (initial, intermediate and advanced), in the cluster analysis and thus it can be concluded that the invertebrate community is structured mainly by degradative ecological successional (Gonalves Jr. et al. 2004).

    In our study, Chironomidae larvae have been recorded since the beginning of the experiment. Nevertheless was considered indicator, with higher abundance and frequency in intermediate days of our experiment of decomposition. This family is considered early colonizers (r-strategists), inhabiting various substrates (takeda et al. 2003), and Gonalves Jr et al. (2004), for example, show that the family Chironomidae was indicator in all stages of decomposition. Among the families of oligochaetes, Naididae occurred in greatest abundance in both macrophytes and was considered indicator of the final days of decomposition. sMoCk & stoneburner (1980) showed that species of Naididae exhibited positive responses to presumably increasing levels of food as leaf

    TaxaEichhornia azurea Salvinia auriculata

    2 4 8 12 24 36 48 60 72 2 4 8 12 24 36 48 60 72

    Polycentropodidae 1 1 7 3 2 4 2 0 0 0 0 7 1 11 19 8 0 1

    COPEPODA 2 76 103 172 0 22 11 2 0 3 41 41 85 59 12 5 0 0

    HIRUDINAE 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 0 0

    NEMATODA 0 3 0 0 0 2 6 12 10 1 0 0 0 1 0 1 2 2

    NEMATOMORPHA 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

    Total abundance 125 626 1204 1027 567 1553 1124 993 874 59 342 368 724 1150 1506 832 405 584

    Number of taxa 5 8 8 5 4 7 6 6 4 6 8 10 8 8 8 6 3 5

    Table 1. Continuation...

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    decomposition progressed, and they become abundant after the leaves visually show signs of decomposition.

    In respect to the functional feeding groups, the predators were represented mainly by Chaetogaster that feed on small invertebrates as rotifers and protozoa (Martins et al. 2011) and probably its abundance was not determined by collectors. Furthermore, we did not observe the presence of shredders. The same result was reported by rezende et al. (2010) in two other lakes in southeastern Brazil. In the absence of this functional feeding group, invertebrates such as the Tubificinae, Gastropoda and Chironomidae can assume a similar role (Chauvet et al. 1993; Capello et al. 2004; Casas et al. 2011). Nevertheless, we did not observe the presence of the first two taxa. Low abundance and richness of Tubificinae also were reported by Martins et al. (2011) in decomposing E. azurea leaves in Manacs Lake and these authors observed that this subfamily was not important to macrophyte decomposition. Although the Chironomidae were not included in the functional feeding group in this study, silveira et al. (2013) shows the importance of larvae of this family in decomposition, since the main food item observed in stomach content of the majority of genera analyzed at the start and end of the experiments was leaf detritus.

    In conclusion, we believe that decomposing E. azurea and S. auriculata leaves are important substrates for colonization by invertebrates, principally the Chironomidae and Oligochaetes, given high abundance of these groups in the two macrophytes. Changes in chemical composition and structure of the leaf litter during decomposition were more important to determine the structure of invertebrate community than quality (C:N ratio) of the two types of leaf litter.

    ACKNOWLEDGEMENTS

    We thank the Aquatic Ecology Laboratory of Juiz de Fora Federal University (LEA/UFJF) for providing the lake water data and for conducting the analysis of the carbon and nitrogen content of the leaf litter. RTM and LSS received a scholarship from CNPq and UFJF, respectively. RTM received Programa de apoio fixao de Doutores no Amazonas FIXAM/AM fellowship (FAPEAM). RGA was supported by a research fellowship (proc. 303156/2