DOI: 10.13102/sociobiology.v67i1.4478Sociobiology 67(1): 112-120 (March, 2020) Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology ISSN: 0361-6525 Introduction The Neotropical region has a rich fauna of social insects, as well as a great diversity of social wasps (Vespidae, Polistinae) (Richards, 1978; Carpenter & Marques, 2001; Noll, 2013). Polistinae wasps are represented by around 940 species (Noll, 2013; Somavilla et al., 2014a) and the Brazilian social wasps fauna (Polistinae) is the richest in the world, with more than 300 species, 104 of them endemic from Brazil (Somavilla et al., 2014b). This subfamily is divided into four tribes: Mischocyttarini (with one genus, Mischocyttarus), Polistini (with one genus, Polistes), Epiponini (19 genera) and Ropalidiini, with no representatives in Brazil (Noll, 2013). Abstract A survey of social wasps (Vespidae, Polistinae), common insects of Neotropical fauna, which perform a great variety of ecosystemic services, was conducted for the first time in areas of the Amazon forest in Rondônia state. The state is part of the Western Amazon, a region harboring high biodiversity, which is under threat due to constant deforestation. Three areas were sampled, and the wasps were actively collected, and an attractive liquid was sprayed onto the vegetation to bait the wasps. Two thousand nine hundred and sixty-one wasps were sampled in all three areas, distributed in 72 species of 15 genera. Thirty- nine species were recorded for the first time in the state and three others (Agelaia melanopyga Cooper, Brachygastra cooperi Andena and Carpenter and Polybia diguetana du Buysson) represents the first record for Brazil. Agelaia Lepeletier was the most abundant genus in all areas and the greatest species richness was found for Polybia Lepeletier. The highest number of species was recorded in Floresta Nacional do Jamari (51), followed by Estação Ecológica de Cuniã (46) and forest fragment of Universidade Federal de Rondônia (39). The latter also presented the highest number of different genera. The great diversity, mainly for Epiponini, which represented 64 of the 72 species, can be attributed to location of the areas and methodology. Sociobiology An international journal on social insects B Gomes1, CS Lima2, M Silva3, FB Noll3 Article History Edited by Evandro Nascimento Silva, UEFS, Brazil Received 19 April 2019 Initial acceptance 27 September 2019 Final acceptance 06 January 2020 Publication date 18 April 2020 Keywords Epiponini, new records, rainforest, social insects, swarm-founding wasps. Corresponding author Marjorie da Silva Depto. Zoologia e Botânica Instituto de Biociências, Letras e Ciências Exatas, IBILCE/UNESP Rua Cristóvão Colombo nº 2265 Jardim Nazareth, CEP: 15054-000 São José do Rio Preto-SP, Brasil. E-Mail: marjoriebio@gmail.com Social wasps perform important and priceless ecosystemic services. As predators of other insects, they are important in the maintenance of food chains and in biological control, since they feed on larvae that are crop pests such as tomato, coffee, corn, eucalyptus, citrus fruits and vegetables (Carpenter & Marques, 2001; Souza et al., 2008, 2010a; Brügger et al., 2019; Prezoto et al., 2019). These wasps also act as pollinators (Hunt et al., 1991; Hermes & Köler, 2006; Santos et al., 2006; Nadia et al., 2007) and are well known for symbiosis with ants (Espelie & Herman, 1988), honey insects (Letourneau & Choe, 1987) and birds (Joyce, 1993). Some species are still useful as indicators of environmental quality (Souza et al., 2010b; Urbini et al., 2010). 1 - Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo (USP), Ribeirão Preto-SP, Brazil 2 - Universidade Federal de Rondônia (UNIR), Campus José Ribeiro Filho, Porto Velho-RO, Brazil 3 - Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), São José do Rio Preto-SP, Brazil RESEARCH ARTICLE - WASPS High Number of Species of Social Wasps (Hymenoptera, Vespidae, Polistinae) Corroborates the Great Biodiversity of Western Amazon: a Survey from Rondônia, Brazil Sociobiology 67(1): 112-120 (March, 2020) 113 The Brazilian Amazon harbor the great diversity of Polistinae wasps (Silveira, 2002; Silva & Silveira, 2009), where 20 genera and about 200 species were recorded, representing 70% of the Brazilian social wasps fauna (Silveira, 2002). Although this number seems very expressive, they are probably underestimated, given the extent of the Amazon and the low number of surveys for social wasps in this biome: Ilha de Maracá – Roraima (Raw, 1998), Caxiuanã – Pará (Silveira, 2002; Silveira & Silva, 2009), Serra do Divisor – Acre (Morato et al., 2008), Porto Acre, Senador Guiomard and Rio Branco – Acre (Gomes et al., 2018), dos Lagos Region – Amapá (Silveira et al., 2008), Mamirauá and Alvarães – Amazonas (Silveira et al., 2008), Reserva Ducke and Jaú National Park - Amazonas (Somavilla et al., 2014b; 2015) and Gurupi Biological Reserve – Maranhão (Somavilla et al., 2014a). There is also a bias in sampling, with most of the inventories (and consequently, the highest number of recorded species) concentrated in the Amazonas state (Barbosa et al., 2016). Thus, further investigations should lead to an increase in recorded species. Located in the Northwestern of Brazil, the state of Rondônia is part of the Western Brazilian Amazon (Martins et al., 2014), which includes Bolivia, Colombia, Ecuador, Peru, and Western Brazil (Finer et al., 2015). This region is one of the world’s last high-biodiversity wilderness areas (Finer et al., 2015), characterized by large tracts of relatively intact humid tropical forest, which harbor an extraordinary species richness (Bass et al., 2010; Pointekowski et al., 2019). However, the Western Amazon has been suffering from constant deforestation (Rosa et al., 2012; Mayes et al., 2019). Rondônia presents the third highest rate of deforestation and forest degradation of this biome, totaling 21% of the deforested areas of Amazon from August 2014 to January 2016 (Fonseca et al., 2016; Pointekowski et al., 2019). The high index of deforestation in the state is a reflection of the expansion of the agriculture frontier towards northern Brazil during the recent decades (Souza Jr. et al., 2013). The destruction of natural areas in the Amazon, especially habitat fragmentation is the direct cause of the reduction of diversity due to severe abiotic and biotic changes (Magnago et al., 2014; Rocha et al., 2018). The only previous information regarding the social wasps of Rondônia are the works of Richards (1978), which is still the largest source of information on the distribution of Epiponini and other Neotropical Polistinae, and Raw (1988). In a current context of global climate change and accelerated species loss, the knowledge of biodiversity and the consequences of its destruction has become a major concern and challenge for the 21st century, since, as species disappear, we lose both known and unknown benefits they provide (Gascon et al., 2015; Troudet et al., 2017). Despite the high abundance and richness in Amazonian areas, knowledge about the diversity and biology of social wasps in the region is still underestimated. Here, we presented the first survey of social wasps (Polistinae) of Rondônia state. Material and Methods Three areas of Amazon rainforest located in the northern state of Rondônia, Brazil were studied (Fig 1): I – Estação Ecológica de Cuniã (ESEC) with approximately 186.743,26 ha (ICMBio, 2019a) is located between the cities of Porto Velho - RO and Humaita - AM (8º 05’ 24’’ S 63º 26’ 07’’ W); II – Floresta Nacional do Jamari (FLONA) with 222.114,24 ha (ICMBio, 2019b) the region covers the districts of Candeias do Jamari, Itapuã do Oeste and Cujubim - RO (09º 00’ 00’’ S 62º 44’ 05’’ W); III – Forest Fragment of Universidade Federal de Rondônia (UNIR) in the capital Porto Velho (08º 49’ 53’’ S 63º 56’ 26’’ W), with approximately 50 ha (Miranda, 2005). In the three areas, the vegetation is composed of dense ombrophilous forest and open ombrophilous forest. The climate is tropical humid, with an average temperature of 25 ºC, very rainy summer and winter a little drier. The relief is a little rough, and the average altitude is 240 meters (Schlindwein et al., 2012; SEDAM, 2012). Samples were performed from April 2010 to November 2011 in ESEC and, from December 2011 to December 2012 in FLONA and UNIR. Wasps were collected actively (with the aid of an entomological net), follow the protocol developed by Noll and Gomes (2009), on trails or roads previously available in the forest. The protocol is based on the use of an attractive solution (50g of salt and 200g of sugar per liter of water), which was sprayed on the vegetation in five points equidistant 20 m. The points were observed individually for ten minutes and the liquid was reapplied every three hours of collection. Fourteen collections of 12 hours (6:00 am to 06:00 pm) were made in each area, totaling 168 hours of work and 504 hours considering all areas. The collected specimens were stored in micro-tubes containing ethanol absolute. After identified, part of the collected material was deposited in the zoological collection of the Museu Paraense Emílio Goeldi, in Belém, Pará state, Brazil (Mischocyttarus) and in the Hymenoptera collection of Universidade Estadual Paulista “Júlio de Mesquita Filho”, in São José do Rio Preto, São Paulo state, Brazil. Sampling adequacy was evaluated by the construction of a rarefaction curve for each area using the Mao Tau method (Colwell et al., 2004). The non-parametric estimator Jackknife 1 was used to compare the sample with the estimated richness since the species richness observed is often an additive estimator in relation to the real species richness (Campos et al., 2013). Both analyses were performed using PAST 3.24 (Hammer et al., 2001). Results A total of 72 species of 15 genera of social wasps were collected (Table 1), most of them (17) sampled in the three areas, totalizing 2961 specimens. FLONA was the area with the highest number of species, 51, followed by ESEC, with 46 species and UNIR with 39 species. Considering the number of B Gomes, CS Lima, M Silva, FB Noll – High number of species of social wasps in Western Amazon114 Agelaia Lepeletier, representing almost half (47.8%) of the total wasps sampled. The same occurred when each area was analyzed individually, with Agelaia representing 46.8% of specimens sampled in FLONA, 58,7% in ESEC and 36% in UNIR. From the 72 species, 39 of them are new records for the state. Other three species – Agelaia melanopyga Cooper 2000, Brachygastra cooperi (Richards, 1978), and Polybia diguetana du Buysson 1905 – were sampled for the first time in Brazil. Despite the high number of species sampled, Jackknife values indicate that there were still species to be collected. However, the rarefaction curve (Fig 2) tended to stabilize, indicating that the sampling effort was sufficient for a significant species registration. Fig 2. Rarefaction curve for species of social wasps (Polistinae) collected in Floresta Nacional do Jamari (FLONA), Estação Ecológica de Cuniã (ESEC) and in the forest fragment of Universidade Federal de Rondônia (UNIR). The x-axis represents the number of collections (1 to 14) and the y-axis represents the number of species sampled. The isolated symbols represent the richness estimated by the Jackknife1 index, indicating that there were still species to be sampled for all areas. Fig 1. Satellite image of the areas sampled. A. Floresta Nacional do Jamari (FLONA); B. Estação Ecológica de Cuniã (ESEC); C. forest fragment of Universidade Federal de Rondônia (UNIR). Scale bar: 10Km. Source: GoogleEarth. genera, 14 different genera were sampled in UNIR, followed by ESEC and FLONA, both with ten genera. Four of the 15 genera sampled – Apoica Lepeletier, Chartergellus Bequaert, Chartergus Lepeletier, and Pseudopolybia von Dalla Torre – were only found in UNIR. FLONA was also the area with the largest number of exclusive species (12), followed by UNIR (11) and ESEC (6). Four of the six species of Mischocyttarus de Saussure were found only in ESEC. Seventeen species were collected in all areas. Polybia Lepeletier and Agelaia Lepeletier were the most diverse genera, with 23 (one-third of species) and 13 species collected respectively. The greatest species richness for each area was also found for Polybia, with 19 species in FLONA, 16 in UNIR and 14 in ESEC. Despite the highest number of species of Polybia, for all three areas, the most abundant genus was Discussion From the surveys of social wasps carried out for the Amazon biome, this survey sampled the highest number of Epiponini species (64) and was the second in the number of Polistinae species, 72 in total (the first was Silveira, 2002 with 79 species sampled). Three species were recorded for the first time in Brazil. Prior to this survey, the only distributional record for B. cooperi was the data of the holotype, in Colombia (Andena & Carpenter, 2012). P. diguetana has already been recorded in Bolivia, a country bordering Rondônia. This species presents a broad distribution in other eastern Amazon countries (Peru, Ecuador, and Colômbia), Venezuela, Central America, México and Southwestern of U.S.A. The presence of A. melanopyga in Rondônia extends its distribution southernmost since the previous records are from Central America, Colombia and Ecuador (Richards, 1978; Natural History Laboratory IUNH). Sociobiology 67(1): 112-120 (March, 2020) 115 Species FLONA ESEC UNIR Total Epiponini Agelaia angulata (Fabricius, 1804) 25 49 - 74 Agelaia cajennensis (Fabricius, 1798)1 13 21 21 55 Agelaia centralis (Cameron, 1907)1 15 53 - 68 Agelaia fulvofasciata (Degeer, 1773) 278 165 142 585 Agelaia hamiltoni (Richards, 1978) 117 223 7 347 Agelaia lobipleura (Richards, 1978)1 1 - - 1 Agelaia melanopyga Cooper, 20002 1 - - 1 Agelaia myrmecophila (Ducke, 1905)1 11 33 37 81 Agelaia ornata (Ducke, 1905)1 16 18 - 34 Agelaia pallipes (Olivier, 1791) 20 - 3 23 Agelaia pallidiventris (Richards, 1978)1 1 - - 1 Agelaia testacea (Fabricius, 1804) 61 1 84 146 Agelaia timida Cooper, 20001 1 - - 1 Angiopolybia paraensis (Spinola, 1851) 54 35 31 120 Angiopolybia zischkai Richards, 19781 85 190 198 473 Apoica gelida Van der Vecht, 1973 - - 1 1 Brachygastra albula Richards, 1978 3 - - 3 Brachygastra augusti (de Saussure, 1854)1 2 1 - 3 Brachygastra bilineolata Spinola, 1841 8 2 - 10 Brachygastra cooperi (Richards, 1978)2 1 - - 1 Brachygastra lecheguana (Latreille, 1824) 5 - - 5 Brachygastra scutellaris (Fabricius, 1804) 5 1 1 7 Chartergellus amazonicus (Fabricius, 1804)1 - - 30 30 Chartergellus communis Richards, 19781 - - 1 1 Chartergellus zonatus (Spinola, 1851)1 - - 1 1 Charterginus fulvus Fox, 18981 - 1 1 2 Chartergus globiventris de Saussure, 18541 - - 2 2 Leipomeles dorsata Fabricius,1804 1 5 8 7 20 Parachartergus flavofasciatus (Cameron, 1906)1 4 4 15 23 Parachartergus fraternus (Gribodo, 1892)1 3 - 1 4 Parachartergus lenkoi Richards, 19781 - 1 2 3 Parachartergus pseudoapicalis Willink, 19591 1 - 1 2 Parachartergus smithii (de Saussure, 1854)1 - 1 1 2 Polybia bifasciata de Saussure, 18541 5 - - 5 Polybia bistriata (Fabricius, 1804) 2 - 6 8 Polybia catillifex Moebius, 18561 4 - 9 13 Polybia depressa (Ducke, 1905)1 - 4 - 4 Polybia diguetana Buysson, 19052 1 - - 1 Polybia dimidiata (Olivier, 1791) 3 5 2 10 Polybia eberhardae Cooper, 19931 4 - 20 24 Polybia emaciata Lucas,1879 - 19 23 42 Polybia gorytoides gorytoides Fox, 18991 13 3 17 33 Polybia jurinei de Saussure, 1854 39 1 5 45 Polybia liliacea (Fabricius, 1804) 42 4 2 48 Polybia micans Ducke, 19041 24 10 48 82 Table 1. List of species and number of specimens of social wasps (Vespidae, Polistinae) collected in three areas of Rondônia state, Brazil. Floresta Nacional do Jamari (FLONA); Estação Ecológica de Cuniã (ESEC); forest fragment of Universidade Federal de Rondônia (UNIR). B Gomes, CS Lima, M Silva, FB Noll – High number of species of social wasps in Western Amazon116 Although many of the species found are common in other areas of the Amazon, we also found species, such as Agelaia pallidiventris (Richards, 1978), with a single previous record for Brazil in Amazonas state. This species seems to be endemic to the Western Amazon, occurring also in Colombia, Ecuador and Peru (Richards, 1978; Natural History Laboratory IUNH). For other species, the presence in Rondonia helps to fill a gap in geographical distribution, as observed for Chartergellus zonatus (Spinola, 1851) and Protopolybia rotundata Ducke, 1910. Geographic records for the former were from Peru and Pará state, in the north of Brazil. The later, also represents the first record in northern Brazil, since previous occurrence data were from French Guiana and Mato Grosso state, in middle-west of Brazil (Richards, 1978; Natural History Laboratory IUNH). The first occurrence in northern Brazil was also found for Parachartergus pseudoapicalis Willink, 1959, previously recorded for the Northeast, Middle- west, South and Southeastern regions of the country (Richards, 1978; Natural History Laboratory IUNH). Agelaia was more abundant not only in this work but also in other regions of Amazon Forest (Raw, 1988; Silveira, 2002; Silveira et al., 2008; Morato et al., 2008; Silva & Silveira, 2009), probably by the habits of this genus that presents generalist and opportunistic species in relation to Polybia parvulina Richards, 19701 3 - 3 6 Polybia platycephala Richards, 1951 7 2 8 17 Polybia procellosa dubitata Ducke, 19101 - 1 - 1 Polybia quadricincta Saussure, 1854 3 - - 3 Polybia rejecta (Fabricius, 1798) 79 58 59 196 Polybia rufitarsis Ducke, 19041 4 2 - 6 Polybia scrobalis Richards, 1970 1 - 5 6 Polybia sericea (Olivier, 1791) - - 1 1 Polybia singularis Ducke, 1909 7 1 - 8 Polybia striata (Fabricius, 1787) 59 4 1 64 Polybia tinctipennis tinctipennis Fox, 18981 24 1 1 26 Protopolybia acutiscutis Cameron, 1907 1 - - 1 Protopolybia chartergoides Gribodo, 1891 - - 1 1 Protopolybiarotundata Ducke, 19101 - - 1 1 Pseudopolybia compressa de Saussure, 18641 - - 1 1 Pseudopolybia vespiceps de Saussure, 1864 - - 1 1 Synoeca chalibea de Saussure, 18521 14 - 1 15 Synoeca surinama (Linnaeus,1767) 8 3 - 11 Synoeca virginea (Fabricius, 1804) 96 18 1 115 Mischocyttarini Mischocyttarus flavicans flavicans (Fabricius, 1804)1 - - 1 1 Mischocyttarus gomesi Silveira, 2013 - 1 - 1 Mischocyttarus interruptus Richards, 19781 - 2 - 2 Mischocyttarus labiatus (Fabricius, 1804)1 13 2 3 18 Mischocyttarus lecointei (Ducke, 1904)1 2 - 1 3 Mischocyttarus tomentosus Zikan, 1935 - 6 - 6 Polistini Polistes canadensis Linnaeus, 17581 - 4 - 4 Polistes occipitalis Ducke, 19041 1 - - 1 Species richness 51 46 39 Species abundance 1195 958 808 2961 1 New records for Rondonia; 2 New records for Brazil. Table 1. List of species and number of specimens of social wasps (Vespidae, Polistinae) collected in three areas of Rondônia state, Brazil. Floresta Nacional do Jamari (FLONA); Estação Ecológica de Cuniã (ESEC); forest fragment of Universidade Federal de Rondônia (UNIR). (Continuation) Species FLONA ESEC UNIR Total Epiponini Sociobiology 67(1): 112-120 (March, 2020) 117 the food and resources choice (Oliveira et al., 2010). Polybia was the richest genus in number of species, and also had been collected more frequently in other studies conducted in Amazonia (Silveira, 2002; Silveira et al., 2008; Morato et al., 2008; Somavilla et al., 2014a; 2014b; 2015; Gomes et al., 2018). Once it is the genus of Epiponini that presents the greatest number of species, with 58 already described (Carpenter & Kojima, 2002), this could be considered a predictable result. A sampling of a large diversity of Polistinae can be attributed to more than one factor. One of them is the location of the collection areas in the Western Amazon, known for harboring great biodiversity (Brown, 1991; Hoorn et al., 2010; Gomes et al., 2018). Another factor is the methodology used. Although the employment of only one type of capture method seems not to be able to conduct a comprehensive species inventory, due to the great diversity of ecological niches occupied by wasps (Santos et al., 2007), the use of an attractive demonstrated to be a successful methodology, allowing the collection of more wasps than in previous surveys (Raw, 1988; Silveira, 2002; Silveiraet al., 2008; Moratoet al., 2008; Silva & Silveira, 2009). Raw (1988) studying the activity of social wasps visiting various crops in two indigenous tribes in eastern Rondonia, collected 13 species of which only five Agelaia fulvofasciata (Degeer, 1773), Polybia bistriata (Fabricius, 1804), P. jurinei de Saussure, 1854, P. striata (Fabricius, 1787) and Synoeca surinama (Linnaeus, 1767) were also sampled in this study. The author also collected Epipona tatua, a species belonging to a genus not sampled in this survey, even with a much longer period of sampling and almost six times more species collected than Raw. This fact is in line with data on the rarefaction curve and the richness index, suggesting that all the diversity of social wasps of the state was not accessed, reinforcing the need for further studies not only for Rondônia but for Amazonia and the entire Neotropical region. An interesting result was the greater diversity in terms of the genera found in UNIR, with the presence of Apoica, Chartergellus, Chartergus, and Pseudopolybia registered only in this area. UNIR is the smallest area (around three and four times smaller than ESEC and FLONA, respectively) and the one with the greatest anthropogenic interference, with nearby buildings and constant flow of people and vehicles. Studies conducted in areas with different levels of environmental preservation in the semideciduous Atlantic forest, showed a great diversity of social wasps also in small fragments and degraded areas (Noll & Gomes, 2009; Tanaka Jr. & Noll, 2011). The generalist characteristic of many species of social wasps in the choice of food and resources on foraging activities (Raveret-Richter, 2000; Oliveira et al., 2010), and the flexibility in building nests according to the variety of ecological and climatic conditions (Rodrigues, 1968; Santos et al., 2007) allows some species to be well adapted to areas with anthropic interference (Gomes & Noll, 2009). Nevertheless, consideration should also be given to the fact that anthropogenic environments provide resources, such as water, which may make it advantageous for wasps to nest near them. Moreover, a smaller area is easier to be sampled more significantly than the larger ones. Conclusion This is the first survey of social wasps carried out for the state of Rondônia. Among the 72 species collected, there were three new records for Brazil. Three areas were sampled and even in UNIR, the smallest one and under the anthropic influence, diversity was high, with some genera found only there, showing the importance of conservation of small forest fragments. Moreover, most of the species were recorded for the first time in the state helping to fill in gaps in geographic distribution. Nevertheless, large holes still remain in the geographic distribution for many species of social wasps in Brazil, mainly in the Amazon Region, but also throughout the Neotropical region. The absence of taxonomic and biogeographic data generates insufficient information to attribute any condition (such as “rare” or “threatened”) to the wasp species of the sampled areas. In a region of great diversity but also high indexes of deforestation, as Western Amazon, further studies become necessary and urgent. Acknowledgments The authors thank John W. Wenzel, James M. Carpenter, Orlando T. Silveira, Sidnei Mateus, Rogério B. Lopes, Raduan A. Soleman, Sérgio R. Andena and Luis F. F. Gelin, for the support in the identification of the species. We also thank Caio L. Assunção, Tony H. Katsuragawa, Moreno S. Rodrigues and Tainá Kobs for the assistance in the collections. The specimens were collected under permits (SISBio nº 23197-1, 31901-1 and 31904-1). References Andena, S.R. & Carpenter, J.M. (2012). A phylogenetic analysis of the social wasp genus Brachygastra Perty, 1833, and description of a new species (Hymenoptera: Vespidae: Epiponini). American Museum Novitates, 3753: 1-38. doi: 10.1206/3753.2. Barbosa, B.C., Detoni, M., Maciel, T.T. & Prezoto, F. (2016). Studies of social wasp diversity in Brazil: Over 30 years of research, advancements, and priorities. Sociobiology, 63: 858-880. doi: 10.13102/sociobiology.v63i3.1031. Bass, M.S., Finer, M., Jenkins, C.N., Kreft, H., Cisneros- Heredia, D.F., McCracken, S.F., et al.(2010). Global conservation significance of Ecuador’s Yasuní National Park. PLoS One, 5: e8767. doi: 10.1371/journal.pone.0008767. Brown K.S. Jr. (1991). Conservation of Neotropical environments: insects as indicators. In: N.M. Collins & J.A. B Gomes, CS Lima, M Silva, FB Noll – High number of species of social wasps in Western Amazon118 Tomas (Eds.), The conservation of insects and their habitats (pp. 349-404). London: Academic Press. Brügger, B.P.; Alcántara-de la Cruz, R.; de Carvalho, A.G.; Soares, M.A.; Prezoto, F. & Zanuncio, J.C. (2019). Polybia fasticiosuscula (Hymenoptera: Vespidae) foraging activity patterns. Florida Entomologist, 102: 264-265. doi: https10.1653/024.102.0150. Campos, V.A., Oda, F.H., Juen, L., Barth, A. & Dartora, A. (2013). Composition and species richness of anuran amphibians in three different habitats in an agrosystem in Central Brazilian Cerrado. Biota Neotropica, 13, 124-132. Retrieved from: http://www.biotaneotropica.org.br/v13n1/en/abstract?i nventory+bn03213012013. Carpenter, J.M. & Kojima, J. (2002). A new species of paper wasp from Costa Rica (Hymenoptera: Vespidae; Polistinae, Epiponini). Journal of New York Entomology Society, 110: 212-223. Retrieved from: http://www.jstor.org/ stable/25010418. Carpenter, J.M. & Marques, O.M. (2001). Contribuição ao estudo de vespídeos do Brasil (Insecta, Hymenoptera, Vespoidea, Vespidae). Série Publicações digitais. v.2. Cruz das Almas: Universidade Federal da Bahia., versão 1.0. 1 CDROM. Colwell, R.K., Mao, C.X. & Chang, J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology, 85: 2717-2727. doi: 10.1890/03-0557. Espelie, K.E. & Hermann, H.R. (1998). Congruent cuticular hydrocarbons: biochemical convergence of a social wasp, an ant, and a host plant. Biochemical Systematics and Ecology, 16: 505-508. doi: 10.1016/0305-1978(88)90053-1. Finer, M., Babbitt, B., Novoa, S., Ferrarese, F., Pappalardo, S.E., De Marchi, M., et al. (2015). Future of oil and gas development in the western Amazon. Environment Research Letters, 10: 2-6. doi: 10.1088/1748-9326/10/2/024003. Fonseca, A., Souza, C. Jr. & Veríssimo, A. (2016). Deforestation report for the Brazilian Amazon. SAD. Imazon. Retrieved from: https://imazon.org.br/publicacoes/boletim-do-desmatamento- da- amazonia-legal-setembro-de-2016-sad/. Gascon, C., Brooks, T.M., Contreras-MacBeath, T., Heard, N., Konstant, W., Lamoreux, J., et al. (2015). The importance and benefits of species. Current Biology, 25: R431–R438. doi: 10.1016/j.cub.2015.03.041 Gomes, B. & Noll, F.B. (2009). Diversity of social wasps (Hymenoptera, Vespidae, Polistinae) in three fragments of semideciduous seasonal forest in the northwest of the São Paulo State, Brazil. Revista Brasileira de Entomologia, 53: 428-431. doi: 10.1590/S0085-56262009000300018. Gomes, B., Knidel, S.V.L., Moraes, H.S. & da Silva, M. (2018). Survey of social wasps (Hymenoptera, Vespidae, Polistinae) in Amazon rainforest fragments in Acre, Brazil. Acta Amazonica, 48: 109-116. doi: 10.1590/1809- 4392201700913. Hammer, Ø., Harper, D.A.T., & Ryan, P.D. (2001). PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1-9. Retrieved from: http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Hermes, M.G. & Köhler, A. (2006). The flower-visiting social wasps (Hymenoptera, Vespidae, Polistinae) in two areas of Rio Grande do Sul state, southern Brazil. Revista Brasileira de Entomologia, 50: 268-274. doi: 10.1590/S0085- 56262006000200008. Hoorn, C., Wesselingh, F.P., ter Steege, H., Bermudez, M.A., Mora A., Sevink, J., et al. (2010). Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330: 927-931. doi: 10.1126/ science.1194585. Hunt, J.H., Brown, P.A., Sago, K.M. & Kerker, J.A.(1991). Vespid wasps eat pollen (Hymenoptera: Vespidae). Journal of the Kansas Entomological Society, 64: 127-130. Retrieved from: http://www.umsl.edu/~huntj/Number%2046.pdf. ICMBio - O Instituto Chico Mendes de Conservação da Biodiversidade. (2019a). Estação Ecológica de Cuniã. http://www.icmbio.gov.br/portal/unidadesdeconservacao/ biomas-brasileiros/amazonia/unidades-de-conservacao- amazonia/1911-esec-de-cunia (accessed date: 2 April, 2019). ICMBio - O Instituto Chico Mendes de Conservação da Biodiversidade. (2019b). Floresta Nacional do Jamari. http://www.icmbio.gov.br/portal/unidadesdeconservacao/ biomas-brasileiros/amazonia/unidades-de-conservacao- amazonia/1959-flona-do-jamari (accessed date: 2 April, 2019). Joyce, F. (1993). Nest success of rufous-naped wrens (Camplyorhynchus rufuncha) is greater near wasp nests. Behavioral Ecology and Sociobiology, 32: 71-77. doi: 10.1007/BF00164038. Letourneau, D.K. & Choe, J. (1987). Homopteran attendance by wasps and ants: the stochastic nature of interactions. Psyche. 1987: 94, 81-91. doi: 10.1155/1987/12726. Magnago, L.F.S., Edwards, D.P., Edwards, F.A., Magrach, A., Martins, S.V. & Laurance, W.F. (2014). Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. Journal of Ecology,102: 475-485. http://dx.doi.org/10.1111/1365-2745.12206. Martins, T.F., Venzal, J.M., Terassini, F.A., Costa, F.B., Marcili, A., Camargo, L.M.A. et al. (2014). New tick records from the state of Rondônia, western Amazon, Brazil. Experimental and Applied Acarology, 62: 121-128. doi: 10.1007/s10493-013-9724-4. Mayes, D.M., Bhatta, C.P., Shi, D., Brown, J.C. & Smith, D.R. (2019). Body size influences stingless bee (Hymenoptera: Apidae) communities across a range of deforestation levels in Sociobiology 67(1): 112-120 (March, 2020) 119 Rondônia, Brazil. Journal of Insect Science, 19: 23; 1-7 doi: 10.1093/jisesa/iez032. Miranda, A. (2005). A geoestatística e a criação de modelo digital de elevação do Campus José Filho, UNIR. Monografia. UNIR, Porto Velho-RO. 57 p. Morato, E.F., Amarante S.T. & Silveira, O.T. (2008). Avaliação ecológica rápida da fauna de vespas (Hymenoptera: Aculeata) do Parque Nacional da Serra do Divisor, Acre, Brasil. Acta Amazonica, 38: 789-797. doi: 10.1590/S0044- 59672008000400025. Nadia, T. de L., Machado, I.C. & Lopes, A.V. (2007). Polinização de Spondias tuberosa Arruda (Anacardiaceae) e análise da partilha de polinizadores com Ziziphus joazeiro Mart. (Rhamnaceae), espécies frutíferas e endêmicas da caatinga. Revista Brasileira de Botânica, 30: 89-100. doi: 10.1590/S0100-84042007000100009. Natural History Laboratory/IUNH (Ibaraki University). Tentative Checklist of the Polistine Tribe Epiponini, Carpenter, J.M. http://iunh2.sci.ibaraki.ac.jp/wasp/Epiponini/ epiponini.htm (accessed date: 28 March, 2019). Noll, F.B. & Gomes, B. (2009). An improved bait method for collecting Hymenoptera, especially social wasps (Vespidae: Polistinae). Neotropical Entomology, 38: 477-481. doi: 10.15 90/S1519-566X2009000400006. Noll, F.B. (2013). “Marimbondos”: a review on the neotropical swarm-founding polistines. Sociobiology, 60: 347-354. doi: 10.13102/sociobiology.v60i4.347-354. Oliveira, O.A.L., Noll, F.B & Wenzel, J.W. (2010). Foraging behavior and colony cycle of Agelaia vicina (Hymenoptera: Vespidae; Epiponini). Journal of Hymenoptera Research, 19: 4-11. doi: biostor.org/reference/111460. Prezoto, F., Maciel, T.T., Detoni, M., Mayorquin, A.Z. & Barbosa, B.C. (2019). Pest control potential of social wasps in small farms and urban gardens. Insects, 10: 1-10. doi: 10.3390/insects10070192. Piontekowski V.J, Ribeiro F.P., Matricardi E.A.T., Lustosa Jr. I.M., Bussinguer A.P. & Gatto A. (2019). Modeling deforestation in the state of Rondônia. Floresta e Ambiente, 26: e20180441. doi: 10.1590/2179-8087.044118. Raveret-Richter, M. (2000). Social wasp (Hymenoptera: Vespidae) foraging behavior. Annual Review of Entomology, 45: 121-150. doi: 10.1146/annurev.ento.45.1.121. Raw, A. (1988). Social wasps (Hymenoptera: Vespidae) and insect pests of crops of the Suruí and Cinta Larga Indians in Rondônia, Brasil. The Entomologist, 107: 104-109. Retrieved from: https://www.researchgate.net/publication/236684476_ Social_wasps_Hymenoptera_Vespidae_and_insect_pests_ of_crops_of_the_Surui_and_Cinta_Larga_indians_in_ Rondonia_Brazil. Raw, A. (1998). Social wasps (Hymenoptera, Vespidae) of Ilha de Maracá. In: J.A. Ratter & W. Milliken (Eds.), The biodiversity and environment of an Amazonian rainforest (pp. 307-321). Edinburgh: Royal Botanic. Richards, O.W. (1978). The social wasps of the Americas, excluding the Vespinae. London: British Museum (Natural History), 580 p. Rodrigues, V.M. (1968). Estudo sobre as vespas sociais do Brasil (Hymenoptera-Vespidae); estudo sobre populações de vespas sociais dos generos Polistes e Polybia (Vespidae- Polistinae e Polybiinae). Tese de Doutorado. Universidade Estadual de Campinas, 112p. Retireved from: http://www. repositorio.unicamp.br/handle/REPOSIP/315696. Rocha, R., Ovaskainen, O., López-Baucells, A., Farneda, F., Sampaio, E.M., Bobrowiec, P.E.D. et al. (2018). Secondary forest regeneration benefits old-growth specialist bats in a fragmented tropical landscape. Scientific Reports,8: 3819. http://dx.doi.org/10.1038/s41598-018-21999- 2. PMid:29491428. Rosa, I.M.D., Souza Jr, C. & Ewers, R.M. (2012). Changes in size of deforested patches in the Brazilian Amazon. Conservation Biology, 26: 932-937. doi: 10.1111/J.1523-1739.2012.01901.x. Reeve, H.K. & Nonacs, P. (1992). Social contracts in wasp societies. Nature, 359: 823-825. Retrieved from: sci-hub.tw/ 10.1038/359823a0. Santos, G.M. de M., Bichara-Filho, C.C., Resende, J.J., Cruz, J.D. & Marques, O.M. (2007). Diversity and community structure of social wasps (Hymenoptera: Vespidae) in three ecosystems in Itaparica Island, Bahia state, Brazil. Neotropical Entomology, 36: 180-185. doi: 10.1590/S1519-566X2007000200002. Santos, G.M. de M., Aguiar, C.M.L., Gobbi, N. (2006). Characterization of the social wasp guild (Hymenoptera, Vespidae) visiting flowers in the caatinga (Itatim, Bahia, Brazil). Sociobiology, 47: 483-494. Retrieved from: http:// www2.uefs.br/lent/professores/profa_candida/Arquivos/ PDF12_Santos_etal_2006.pdf. Schlindwein, J.A., Marcolan, A.L., Fioreli-Perira, E.C., Pequeno, P.L. de L. & Militão, J.S.T.L. (2012). Solos de Rondônia: usos e perspectivas. Revista Brasileira de Ciências da Amazônia, 1: 213-231. Retrieved from: http://www.periodicos.unir.br/index. php/rolimdemoura/article/view/612/660. SEDAM, Secretaria de Estado do Desenvolvimento Ambiental. (2012). Boletim Climatológico de Rondônia - Ano 2010, v.2. Porto Velho: COGEO - SEDAM. Retrieved from: https://docplayer.com.br/52866255-Boletim-climatologico- de-rondonia-2010.html. Silva, S.S. & Silveira, O.T. (2009). Vespas sociais (Hymenoptera, Vespidae, Polistinae) de floresta pluvial amazônica de terra firme em Caxiuanã, Melgaço, Pará. Iheringia, Série Zoologia, 99: 317-323. doi: 10.1590/S0073-47212009000300015. B Gomes, CS Lima, M Silva, FB Noll – High number of species of social wasps in Western Amazon120 Silveira, O.T. (2002). Surveying Neotropical social wasps. An evaluation of methods in the “Ferreira Penna” Research Station (ECFPn), in Caxiuanã, PA, Brazil (Hymenoptera, Vespidae, Polistinae). Papéis Avulsos de Zoologia, 42: 299- 323. doi: 10.1590/S0031-10492002001200001. Silveira, O.T., Costa Neto, S.V. & Silveira, O.F.M. (2008). Social wasps of two wetland ecosystems in Brazilian Amazonia (Hymenoptera, Vespidae, Polistinae). Acta Amazonica, 38: 333-344. doi: 10.1590/S0044-59672008000200018. Somavilla, A., Marques, D.W.A., Barbosa, E.A.S., Pinto Junior, J.S. & Oliveira, M.L. (2014a). Vespas sociais (Vespidae: Polistinae) de uma área de Floresta Ombrófla Densa Amazônica no Estado do Maranhão, Brasil. EntomoBrasilis, 7: 183-187. doi: 10.12741/ebrasilis.v7i3.404. Somavilla, A., Oliveira, M.L. & Silveira, O.T. (2014b). Diversity and aspects of the ecology of social wasps (Vespidae, Polistinae) in Central Amazonian” terra frme” forest. Revista Brasileira de Entomologia, 58: 349-355. doi: 10.1590/s0085- 56262014005000007. Somavilla, A., Andena, S.R. & Oliveira, M.L. (2015). Social wasps (Hymenoptera: Vespidae: Polistinae) of Jaú National Park, Amazonas, Brazil. EntomoBrasilis, 8: 45-50. doi: 10.12 741/ebrasilis.v8i1.447. Souza, M.M., Silva, M.J., Silva, M.A. & Assis, N.R.G. (2008). A capital dos marimbondos; Vespas sociais (Hymenoptera, Vespidae) do município de Barroso, Minas Gerais. MG Biota, 1: 24-38. Retrieved from: http://www.ief.mg.gov.br/images/ stories/MGBIOTA/mgbiota03_082008.pdf. Souza, M.M.,Ladeira, T.M, Assis, N.R.G, Elpino-Campos, A., Carvalho, P. & Louzada, J.N.C. (2010a). Ecologia de vespas sociais (Hymenoptera, Vespidae) no campo rupestre na Área de Proteção Ambiental, APA, São José, Tiradentes, MG. MG Biota, 3: 15-30. Retrieved from: https://www.researchgate. net/publication/267775255_Ecologia_de_vespas_sociais_ Hymenoptera_Vespidae_no_Campo_Rupestre_na_Area_de_ Protecao_Ambiental_APA_Sao_Jose_Tiradentes_MG. Souza, M.M., Louzada, J., Serrão, J.E. & Zanuncio, J.C. (2010b). Social wasps (Hymenoptera: Vespidae) as indicators of conservation degree of Riparian forests in southeast Brazil. Sociobiology, 56: 387-396. Retrieved from: https://www. researchgate.net/publication/261833422_Social_Wasps_ Hymenoptera_Vespidae_as_Indicators_of_Conservation_ Degree_of_Riparian_Forests_in_Southeast_Brazil. Souza Jr., C.M., Siqueira, J.V., Sales, M.H., Fonseca, A.V., Ribeiro, J.G., Numata, I. et al. (2013). Ten-year Landsat classification of deforestation and forest degradation in Brazilian Amazon. Remote Sensing, 5: 5493-5513. doi: 10.33 90rs5115493. Tanaka Jr., G.M. & Noll, F.B. (2011). Diversity of social wasps on semideciduous seasonal forest fragments with different surrounding matrix in Brazil. Psyche, 2011: 1-8. doi: 10.1155/2011/861747. Troudet, J., Grandcolas, P., Blin, A., Vignes-Lebbel & Legendre, F. (2017). Taxonomic bias in biodiversity data and societal preferences. Scientific Reports, 7:1-14. doi: 10.1038/s41598- 017-09084-6. Urbini, A., Sparvoli, E. & Turillazzi, S. (2010). Social paper wasps as bioindicators: a preliminar research with Polistes dominulus (Hymenoptera, Vespidae) as a trace metal accumulator. Chemosphere, 64: 697-703. doi: 10.1016/j. chemosphere. 2005.11.009.