doi:10.12741/ebrasilis.v8i3.519 e-ISSN 1983-0572 Publicação do Projeto Entomologistas do Brasil www.ebras.bio.br Distribuído através da Creative Commons Licence v4.0 (BY-NC-ND) Copyright © EntomoBrasilis Copyright © do(s) Autor(es)

Biodiversity of Social (: ) at Altitudes Above 1600 Meters in the Parque Estadual da Serra do Papagaio, State of Minas Gerais, Marcos Magalhães de Souza¹, Heloina Nathalliê Mariano da Silva¹, João Batista Dallo¹, Lizandra de Fátima Martins¹, Lucas Rocha Milani¹ & Mateus Aparecido Clemente²

1. Instituto Federal de Educação, Ciência e Tecnologia do Sul de Minas, Campus Inconfidentes Inconfidentes, Minas Gerais, Brazil, e-mail: [email protected], [email protected], [email protected], [email protected], [email protected]. 2. Universidade Estadual Paulista - Departamento de Zoologia - Instituto de Biociências- Rio Claro, e-mail: [email protected] (Autor para correspondência). ______

EntomoBrasilis 8 (3): 174-179 (2015)

Abstract. The Parque Estadual da Serra do Papagaio is the largest area of natural preservation in the south of Minas Gerais, with areas of Floresta Atlantica, Floresta de Araucaria and Campos de Altitude. Although this is an area of biological importance, there are many groups that have not yet been studied there: for example social wasps, which are belonging to order Hymenoptera, Vespidae, which play an important ecological role in different ecosystems. This study was carried out in the aforementioned natural preservation area at altitudes between 1600 and 2200 m in 20 days of sampling between July of 2013 and April of 2014, using active searches and attractive traps to record species. Twenty two species of social wasps were sampled, distributed in seven genera. This number is small compared to counts from other studies in this state, which is probably due to the high altitude of this area. There was a predominance of nests with protective casings in the most common species recorded, and the most populous species was fastidiosuscula Saussure, a finding that can be explained by the superior thermoregulation afforded by the nest casing. Two other common species were drewseni Saussure, and Mischocyttarus rotundicolis (Cameron), which have nests without casings; however, these species have dark coloration, as does the substrate used for nesting, and can therefore enhance retention of solar radiation; nevertheless, other biotic and abiotic factors could be involved.

Keywords: Conservation; Fields of Altitude; Independent Foundation; Nesting in Dark; Swarm-founding.

Biodiversidade de Vespas Sociais (Hymenoptera: Vespidae) em Áreas de Altitude Acima de 1600 Metros do Parque Estadual da Serra do Papagaio, Estado de Minas Gerais, Brasil

Resumo. O Parque Estadual da Serra do Papagaio é a maior Unidade de Conservação do sul de Minas Gerais, com áreas de Mata Atlântica, floresta

Ecologia de Araucária e Campos de Altitude. Apesar da importância biológica da área, muitos grupos animais não foram estudados, como as vespas sociais, insetos que pertencem à ordem Hymenoptera, família Vespidae, e que desempenham importante papel ecológico em diferentes ecossistemas. O estudo foi conduzido nessa Unidade de Conservação em altitudes entre 1600 a 2200 m, no período de julho de 2013 a abril de 2014, durante vinte dias de amostragem, utilizando busca ativa e armadilhas atrativas para registro das espécies. Foram amostradas 22 espécies de vespas sociais distribuídas em sete gêneros. Número menor em relação a outros estudos do estado, o que, provavelmente, foi ocasionado pela elevada altitude. Houve uma predominância de ninhos com invólucro protetor e a espécie mais frequente foi Polybia fastidiosuscula Saussure, o que pode ser explicado pela melhor regulação térmica obtida pelo invólucro. Outras duas espécies frequentes foram Mischocyttarus drewseni Saussure e Mischocyttarus rotundicolis (Cameron) que possuem ninhos sem invólucro, porém essas espécies possuem coloração escura, assim como o substrato utilizado para nidificação e isso poderia reter melhor a radiação solar. Contudo outros fatores bióticos e abióticos podem estar envolvidos.

Palavras-chave: Campos de altitude; Conservação; Fundação enxameante; Fundação independente; Ninhos escuros.

______here are studies describing the richness, variation and pollinators of some families (Gr a n j a & Ba r r o s 1998). abundance of different groups along elevation gradients (Ja n z e n 1973; Fe r n a n d e s & La r a 1993; He n r i q u e s - Despite their importance and the growing of the number of Ol i v e i r a & Ne s s i m i a n 2010). diversity studies in Brazil, especially in the state of Minas Gerais (So u z a & Za n u n c i o 2012), there are no data available about the The general pattern observed is the decline of species richness distribution and occurrence of social wasps in ecosystems above due to the increase in altitude. According to La w t o n et al. (1987), 1,600 m of altitude, which are located in the south of the state, the decline of species richness with increase in altitude is caused particularly in areas of altitude fields. by the increase of climate severity, the reduction of habitable areas, and the reduction of diversity of resources and primary These altitude fields are characterized by mountain tops more than productivity. Adaptive factors related to food resources for 1,500 m high which arose mainly in the Tertiary Period in Serra da life strategy are of crucial relevance (Fe r n a n d e s & Pr i c e 1991), Mantiqueira and Serra do Mar, and are associated with igneous however, data for social wasps are scarce (Ku m a r et al. 2009). and metamorphic rocks. They have very diverse herbaceous flora, including endemic species, which have remarkable similarity to These insects belong to the order Hymenoptera, family Vespidae, the vegetation of the Patagonian Andes and the southern regions and they play various ecological roles, acting as predators of pest of Brazil (Sa ffo r d 1999, 2007; Va s c o n c e lo s 2011). crops such as coffee (Coffea arabica L.) and Surinam cherry (Eugenia uniflora L.) (So u z a et al. 2013), and they are frequent Funding Agency: IFSULDEMINAS and IEF/MG visitors of various angiosperms (Cl e m e n t e et al. 2012) and www.periodico.ebras.bio.br 175 es ee itiue wt te he bis gaa psin fruit passion (guava, baits three the with distributed were sets Figure 1.Areassampled fortheregisterofsocialwasps intheParqueEstadualSerra doPapagaio,southofthestate of MinasGerais (D state the in conservation-priority considered of high climate tropical a by characterized ha, 22,917 of area total a with Gerais, Minas of south the in preservation natural of area largest the is which 44º47’11.30”W), e (22º12’18.22”S Papagaio The present study was conducted in Parque Estadual da Serra do the in Gerais Minas southeast ofBrazil. of south the with associated the ecosystems assess to and elevation, in m 1,600 above fields altitude in wasps social of diversity the assess to was study this of aim The ee cie erhn ad h ue f trcie rp (S traps attractive of use P & the and searching active were species social these survey to used methods collecting The October 2013, andJanuaryApril2014). and (July autumn and summer, spring, winter, - year park area (Figure 1), during five consecutive days per season each Sampling was conducted over 20 days, covering about 15% of the Araucaria ForestandMataAtlantic(IEF2014). vegetation, herbaceous with fields altitude of sections has It m. 2,200 and 1,600 between altitude with Alto Pouso and Itamonte The park covers the municipalities of Aiuruoca, Alagoa, Baependi, the northernpartofParqueNacionaldeItatiaia( with geographically connects it da which via Serra complex, Mantiqueira of corridor ecological the in located is It 2005). al. et opening (2 x 2 x 2 cm), using baits of guava, passion fruit and fruit (S sardines passion guava, of baits using cm), 2 x 2 x (2 opening translucent‘ two-liter the as such bottles, plastic with made were traps attractive The man-made and buildings. epiphytes in trunks, tree on leaves, bromeliad of arrangement the by formed pools in sheets, rigid of surfaces abaxial outcrops, rocky cliffs, mounds, termite in PM, 4:00 surveys to with AM 8:00 from period the in area, the of span the “ad libitum”, existing tracks in the field, without marking fixed points, recording Biodiversity ofSocialWasps(Hymenoptera:Vespidae)at… z e r o t o 06. cie erhn cnit o wlig n pre- on walking of consists searching Active 2006). o a z u in other words, all occurrences were registered over Material andehods & P & z e r o PT’ ait, ih tinua lateral triangular a with variety, ‘PET’’ t o 2006). In each collection period, five period, collection each In 2006).

IEF 2014). m u r o o a z u d n

Saussure The most frequently collected species was frequently most the also collected, beingregisteredinallcollects. was and 10), = (n species of number low collecting frequency below of 49% (Table 1). In other studies other In 1). (Table 49% of below frequency collecting low lioCmo e a. 20) Ae 0 [iy f ars, (S Barroso, of [City 04 Area 2007), al., et Elpino-Campos do Rio Doce, (S Doce, Rio do (Parque Estadual da Serra do Papagaio), Area 02 01 [Parque Area Gerais. Minas of Estadual state the in (meters) altitudes different in collected wasps social of species of comparison realized Were cinerascens rotundicollis Mischocyttarus Saussure Polybia sericea 1). (Table registered were colonies 47 and genera, seven to belonging species Twenty-two siae o boiest Jckie 1 n 0 ad species and EstimateS ( 02 and 01 used were richness Jackknife biodiversity of Estimates compared. areas both in common are which species of number the is C and area, study another is B area, study the in species of number the Gerais, the Sorensen index was used: (S) = 2C / A + B, this where A is of fauna wasp social study with the those of other studies carried out in the state of Minas of level similarity the assess To (about 5ft). ground the above metres half a and one in thevegetation of height average an fixed at days, five for field the in remained and and sardines), totalling 15 bottles (distance of 500 m) per period, of IFSULDEMINAS, Inconfidentes campus, and in the Emílio Goeldi Museum,Belém,Pará. in and campus, Inconfidentes IFSULDEMINAS, of wasps social of collection the in deposited were specimens The 2010)] (Figure1). & P & z e r o t o ,

which was found in 85% of the collections, followed by ih 65%, with 2006)] and Area 05 [City of Tiradentes, (S Tiradentes, of [City 05 Area and 2006)] C Saussure L O Results andDiscssion e w (Olivier)andMischocyttarusdrewseni o a z u L L (cole), 2013).

et al. et (Saussure) sylveirae Protonectarina with 50%, and the other species presented species other the and 50%, with Polybia 2012)], Area 03 (City of Uberlândia, of (City 03 Area 2012)], and were calculated by the program the by calculated were and (Cameron) was the with the largest the with genus the was e-ISSN 1983-0572 Polybia fastidiosuscula 55%, with Souza etal. o a z u

et al. et

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Table 1. Species of social wasps collected in different altitudes ( meters) in the state of Minas Gerais. Area 01 (Parque Estadual da Serra do Papagaio), Area 02 [Parque Estadual do Rio Doce (So u z a et al. 2012)], Area 03 [City of Uberlândia (Elp i n o -Ca m po s et al. 2007)], Area 04 [City of Barroso (So u z a & Pr e z o t o 2006)], Area 05 [City of Tiradentes (So u z a et al. 2010)]. ( - absence of species; + presence of species).

Places of Collection Area 01 Area 02 Area 03 Area 04 Area 05 Species Around of de Above 1,600 m 200-500 m 900-1,100 m 950 a 1,200 m 840 m Agelaia vicina (Saussure) + - - + - Agelaia pallipes (Olivier) - - + - - Agelaia multipicta (Saussure) + - - + + Agelaia angulata (Fabricius) - + - + - Agelaia centralis (Cameron) - + - - - Apoica pallens (Fabricius) - + + - + Apoica gelida Van der Vecht - - - + - Brachygastra augusti (Saussure) - + - + - Brachygastra lecheguana (Latreille) + + + + - Clypearia angustior Ducke - + - + - Chartergellus communis Richards - - + - - Epipona tatua (Cuvier) - + - - - Metapolybia cingulata (Fabricius) - + - - - Mischocyttarus alternatus Zikán - - - - - Mischocyttarus araujoi Zikán - - - + - Mischocyttarus atramentarius Zikán - + + + + Mischocyttarus bahiaensis Zikán - + - - - Mischocyttarus cassununga (R. von Ihering) + - + + + Mischocyttarus cerbeus styx (Richards) - - + - - Mischocyttarus confusus Zikán - - - + + Mischocyttarus drewseni Saussure + + + + + Mischocyttarus flavosculetatus Zikán, - + - - . Mischocyttarus frontalis (Fox) - + - - - Mischocyttarus fluminisensis Zikán - + - - - Mischocyttarus latior (Fox) - - + - + Mischocyttarus mirificus Zikán - - - - + Mischocyttarus punctatus (Ducke) - + - - - Mischocyttarus sp. Prox. marginatus (Fox) - - + - - Mischocyttarus rotundicolis (Cameron) + + - + + Mischocyttarus tricolor Richards - - - + - Mischocyttarus wagneri (du Buysson) - + - + + Polistes actaeon Haliday - + - + - Polistes billardieri Saussure + - + + + Polistes carnifex (Fabricius,) - + - - - Polistes cavapytiformis Richards - - - + - Polistes cinerascens Saussure + - + + + Polistes canadensis (Linnaeus) - + - - - Polistes davillae Richards - - - - + Polistes ferreri Saussure - - + + + Polistes occipitalis Ducke - + - - - Polistes pacificus Fabricius - - - + - Polistes simillimus Zikán + - + + + Polistes subsericeus Saussure - - + + + (Olivier) - + + - + Polybia bifasciata Saussure - + - + - Polybia chrysothorax (Lechtenstein) + + - + + Polybia dimidiate (Olivier) - + - - - Polybia fastitiosuscula Saussure + - - + + Polybia jurinei Saussure - + + + + Polybia ignobilis (Haliday) + + + + + Polybia minarun Ducke + - - + - Polybia occidentalis (Olivier) + + + + + Polybia paulista H. von Ihering + - + + + Polybia platycephala Richards + + + + + Polybia punctata du Buysson + - - - - Polybia rejecta (Fabricius) - + - - - Polybia ruficeps Richards - - + - - Polybia sericea (Olivier) + + + + + Polybia scutelaris (White) + - + + + Polybia striata (Fabricius) - + + - - Polybia signata Ducke - + - - - Protopolybia sedula (Saussure) + - - + + Protonectarina sylveirae (Saussure) + - - + + Parachartegus fraternus (Griboldo) - - - - + Parachartegus pseudapicalis Willinck - - + - -

Pseudopolybia vespiceps (Saussure) - - + + + 176 Synoeca cyanea (Fabricius) - + - + + Synoeca surinama (Linnaeus). - - + - - Richness of species 21 34 28 38 31

e-ISSN 1983-0572 177 The presence of presence The social waspspeciesatdifferentelevations. of groups distinct are there that conclusion the to lead to seem study, this in mentioned already was what to added data, These h ohr pce feunl cletd were collected frequently drewseni species other The of atropicalclimate. influence the under are Tiradentes and Barroso of cities the and relevant variable because the Parque Estadual Serra do Papagaio another be could weather The km. 400 around is Uberlândia the of while km, city the and 150 Doce Rio do Estadual about Parque the between Tiradentes, distance and Barroso of city the from far located is Papagaio do Serra the because areas, the of proximity geographical the to due be also may but m, 900 above These data may indicate an adaptation of both species to altitudes iá; codn t (Z to according Zikán; Francisco Joseph naturalist the of information the through out carried was comparison relevant Another above. discussion the reinforce that data common, in species eight with 0.26, of was altitude, in m 500 to 200 Doce, Rio do Estadual Parque the with and common, in species 11 having 0.43 was altitude, in m 840 Uberlândia, of city the of species the with similarity of level the while species; common 17 with Tiradentes, of city the in studies the by followed species, common 20 with 0.66, Barroso, of the city with similarity great a is there Papagaio do Serra Estadual similarity calculating the fauna and the social wasps of the Parque ee eitrd n h ct of city Barroso the (S in registered were sylveirae P. and fastidiosuscula P Table 2. Species of social wasps collected and described for the Parque Nacional de Itatiaia (MG, RJ) by the naturalist Joseph Franciscl Zikán Franciscl Joseph naturalist the by RJ) (MG, Itatiaia de Nacional Parque (R the for described and collected wasps social of Species 2. Table (S Gerais Minas in out carried C registered in the city of Barroso, 900-1,100 m in altitude (S funerulus atramentarius Mischocyttarus Zikán, Zikán confusus Mischocyttarus However, five species collected in Itatiaia (Z inItatiaia collected species five However, m. 1,600 to up altitudes at collected study present the while 1949), 2007; al. et (E high m lower elevation such as the at city of places Uberlândia, which in is about registered 800 not were they to but 950 respectively, m, and 1,200 metres 1,100 to 900 from altitudes at 2010), al. et ae y iá wr md a attds f 0-10 . (Z m. 700-1100 of altitudes at made were Zikán by made this study. This can be explained by the in fact that the observations registered were species these of Parque none the Papagaio, do with Estadual complex a forms it though even however, 2); (Table Itatiaia do Nacional Parque the in wasps social of species n ia Gerais. Minas in 1600 m could be the result of two factors: the architectural pattern the other studies analyzed (S Rio Doce, with an elevation of 200 to 500 m (S m 500 to 200 of elevation an with Doce, Rio found in the city of Tiradentes, 950 to 1,200 m (S Mischocyttarus crypticus Zikán Mischocyttarus clypeatus Zikán Mischocyttarus costalimai Mischocyttarus confusoidesZikán Mischocyttarus confususZikán Mischocyttarus confirmatus Mischocyttarus cabauna Mischocyttarus adjectusZikán Mischocyttarus araujoi Mischocyttarus alternatusRichards z e r m a Biodiversity ofSocialWasps(Hymenoptera:Vespidae)at… c i Species collectedanddescribedintheParqueNacionaldo h O P o s d r a t Zikán paraguayensis Mischocyttarus , s o

2006), including the first three which were new registers t al. et 1978)andforthecityofBarroso(MG) , M. rotundicolis rotundicolis M. P L o a z u S n i o 2007; o a z u & P & iá and Zikán -C Mischocyttarus atramentarius Polybia m a

. 2010) (Table 1). According to Sorensen’s to According 1). (Table 2010) al. et icoytrs mirificus Mischocyttarus z e r O P o S s t

o Zikán i Zikán . 2007), or the Parque Estadual do Estadual Parque the or 2007), al. et o k a z u and 2006) and the city of Tiradentes (S Itatiaia MG,RJ Zikán n á e Zikán oits simillimus Polistes

99, h ntrls dsrbd 30 described naturalist the 1949), P. cinerascens P. o 21, 02, h species the 2012), 2010, al. et Protonectarina a z u o & P a z u z e r P & o t o z e r which were found in found were which ,

2006; Zikán Zikán S at elevations above elevations at o o t Mischocyttarus , Zikán a z u o o o a z u 2006; M. sericea, P. a z u &P E

P L

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. 2012). al. et et al. k z e r n i

n á ee also were o o 1949), -C E t 2010). o o P L m a a z u 2006).(-absenceofspecies;+presencespecies). o i n i k a z u O P n á & & o P. s -

Central America (K America Central in out carried study altitudinal an in discussed was that aspect n oil ap wt lgtr ooain sc a ylo, the yellow, and as such coloration, lighter in seen as body, the along bands dark of presence with wasps social In empirical studies have described very different patterns (U patterns different very described have studies empirical however, speed; wind by influenced due are they occur but coloration, temperature to body in variations that demonstrated purpose ofregulatingbodytemperature( the with ground the to moving groups, insect other of behavior could be used by the insect, as has already been evidenced by the this and heat more retains vegetation dark with Soil effect. this solar radiation, and the presence of vegetation also accomplishes factors. Nesting in dark substrate also helps increase retention of some kinds of social wasps above 1,600 m, but also physiological which suggests temperature, that body not on only abiotic effect factors C) would 12° explain the to presence (up C) of substantial (0° to no from range may color in varying taxa different from insects for reported temperature in difference The 2013). al. et 1991; S type without protective envelopes (R gymnodomous stelocyttarous the of nests existing even m, 1800 above areas in common also were 1), (Table respectively species genera The species with foundation by swarming. 1,600, demonstrating that in above higher altitudes there is altitudes a predominance of in elevation with foundation colony the in comparison with species of independent foundation (W foundation independent of species with comparison in high are growth colony and egg-laying of rates the and queens, multiple involves more usually model of founding establishment swarm the for colonies; allows it housing; colony provides the which within protected better are queens and reduced, is foundation wasps, in which the swarming model queen mortality independent to compared foundation of type this of advantages low temperaturesandtheabsenceofsun( to adaptation physiological in help can which radiation, solar of This vegetation. absorption the increase can body insect’s herbaceous the on coloration dark dense with hillside as substrate, as such abdomen, and those who had lighter color, with yellow areas on the mesossomo altitude; however some of these specieshad dark coloration, and to be disadvantageous for the colony survival in winter at this high formation of colonies way independent foundation, which seems eaoi atvt (W activity metabolic individuals’ the and location, physical the construction, their in used materials the by also but cover, protective a of presence the by regulated only not are nests in temperatures Hymenoptera, et wih cus n fw pce o Lpdpea ih dark with (B Lepidoptera wings the of on bands species few a in occurs which heat, h cln, hc hls o anan tmeaue favorable temperature a (H survival for maintain to of helps individuals which by colony, the regulation protective thermal with better nests of allows presence envelopes The swarming. by nests of foundation the and envelope, protective a has which nest, the of Polistes bilardieri t i m Species presentinthecityofBarroso,MG h etal.2001). Mischocyttarus o i m u z r a m u

. 2010). In other social insects of order of insects social other In 2010). al. et (Fabricius), could be capable of absorbing i t r e P. cinerascens P. l

s et al. et o h n r e i 1972; and 2005). Studies with locusts have locusts with Studies 2005). 2009) is the correlation between between correlation the is 2009) + + + ------Polistes Z c i r t i m , nested in areas with dark with areas in nested , h J s d r a e n n a e e-ISSN 1983-0572 M o wt fu ad three and four with , z c i w & y a (1991) presents the 1979). R O’D 01. Another 2001). c i h to becontinued... o P. cinerascens P. s d r a Souza etal. e n n L L 1951) and 2000). m e z n e b s r e l

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Table 2. continued...

Species collected and described in the Parque Nacional do Species present in the city of Barroso, MG Itatiaia MG, RJ Mischocyttarus cryptobius Zikán - Mischocyttarus cristatus Zikán - Mischocyttarus declaratus Zikán - Mischocyttarus extinctus Zikán - Mischocyttarus flavosculetatus Zikán, - Mischocyttarus funerulus Zikán + Mischocyttarus itatiayaensis Zikán - Mischocyttarus iheringi Zikán - Mischocyttarus interjectus Zikán - Mischocyttarus infrastrigatus Zikán - Mischocyttarus mirificus Zikán + Mischocyttarus mutator Zikán - Mischocyttarus mimicus Zikán - Mischocyttarus parallelogrammus Zikán - Mischocyttarus pedunculatus Zikán - Mischocyttarus similatus Zikán - Mischocyttarus scitulus Zikán - Polistes binotatus Saussure - Polistes simillimus Zikán + Richness of species 6

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