Can insect assemblages tell us something about the urban environment health?

Abstract

Abstract: If we consider Drosophilidae, the answer to the question above is yes. Many research groups in Brazil and abroad have been showing that assemblages of flies of this family can reflect environmental alteration levels caused by urbanization, and/or by other human disturbances. I will present here a summary of our findings in Drosophilidae assemblages reflecting different degrees of environmental perturbation. These studies were done by graduate students of two post graduate programs of UFRGS, under my supervision, along several decades. I will also present the results stemming from the effort of other Brazilian Drosophilid study groups while identifying the members of those assemblages in different Biomes. As a result of those field studies, several biological invasions were detected and many new important biological problems arose prone to be investigated by genetic, molecular biology and other related approaches.

Key words
Bioindication; Brazilian Biomes; Drosophilidae; urbanization

INTRODUCTION

The southern states of Brazil present different morphoclimatic characteristics than the other states of the country. They are influenced by a subtropical climate, with four well-defined seasons. The state of Rio Grande do Sul encompasses two biomes: Pampa and Atlantic Forest. Pampa is a biome exclusive to the state of Rio Grande do Sul, characterized by shrub and grassland ecosystems. According to the Brazilian Environment Ministry (Ministério do Meio Ambiente), “it has great biodiversity not discovered”. Despite this, it is the Brazilian biome with the lowest percentage of areas protected by conservation units. The Atlantic Forest biome, characterized by native forest formations and associated ecosystems, such as high altitude grasslands, mangroves, and open fields (“restingas)”, and is one of the most biodiverse areas in the world. These biomes are interspaced with crop fields, pastures, livestock farming, and urbanized areas.

Our group analyzed whether different levels of urban disturbance could cause changes in genetic and cytogenetic characteristics of Neotropical Drosophila populations in the urban and suburban areas of Porto Alegre, Rio Grande do Sul State (Valente et al. 1989, 1993, Santos and Valente 1990, review in Valente 1999).

Bonorino et al. (1993), Rohde and Valente (1996) and Valiati and Valente (1996) characterized the urban fauna of flies and compared assemblages of Drosophilidae in nature and in transitional environments. We detected different breeding sites being explored by distinct species, revealing the fine sensibility of those flies to changeable environments (Saavedra et al. 1995).

Later, we characterized the assemblages of Drosophilidae in the urban area of Florianopolis, in the Santa Catarina State (Gottschalk et al. 2007, 2008) and we also re-surveyed the urban area of Porto Alegre, to check if changes occurred over ten years. (Garcia et al. 2008) and (Garcia et al. 2012).

Ruszczyk (1986) compared butterfly assemblages in areas with different levels of urbanization and with woodlands in the suburbs. Lucchese et al. (2003) tested Drosophila willistoni as a bioindicator of air quality, measuring its absorption of urban pollutants, as Cd, S, and Pb. The results showed that to be true. However, not only one species should be considered a bioindicator, but the composition and stability of the assemblages.

After these studies, we perceived the presence and dominance of different species and/or composition of species in assemblages. Later, more localities were surveyed, and we detected an unexpected richness composition of the Drosophilidae assemblages in neglected biomes, such as ecosystems of Atlantic Forest, like mangroves (Schmitz et al. 2007) and “restingas” (Bizzo et al. 2010, Mendes et al. 2017).

Extending our review to studies performed in other regions and habitats, we verified the sensitivity of fly assemblages to environments, revealing the peculiarities of each of them. This corroborates other research, starting with Sene et al. 1980, which have been observing the fly associations to morphoclimatic domains in Brazil such as Cerrado (Mata et al. 2008, Ferreira and Tidon 2005, Döge et al. 2015), Amazonia (Martins 2001), xerophytic vegetations and island forest fragments and araucaria fields (Mateus et al. 2006, 2018, Cavasini et al. 2014), and other environments (Medeiros and Klaczko 2004, Torres and Madi-Ravazzi 2006).

Also, several researchers registered the occurrence and rapid expansion of invader species along the continent, such as the pest fly Zaprionus indianus, which have been registered in the state of São Paulo (Vilela 1999), in Southern Brazil (Castro and Valente 2001, Silva et al. 2005), Cerrado (Tidon et al. 2003, Leão and Tidon 2004), Amazonia (Furtado and Martins 2009, Amador et al. 2011), in the state of Rio de Janeiro (Loh and Bitner-Mathé 2005) and also in Uruguay (Goñi et al. 2001).

Recently, our group found another pest invader - Drosophila suzukii (Deprá et al. 2014) in the Rio Grande do Sul and Santa Catarina states. This species, like Z. indianus, quickly colonized a great part of the South American continent (Vilela and Mori 2014, Paula et al. 2014, Bitner-Mathé et al. 2014, Fraimount et al. 2017, Santos et al. 2017), causing significant losses to agriculture, since the females oviposit in healthy fruits (Schlesener et al. 2015).

Besides all those findings while monitoring urban fly assemblages, we detected other singular phenomena, such as hypermutability in urban populations of the cosmopolite Drosophila simulans (Loreto et al. 1998; review in Loreto et al. 2018), which paved the way to discover the effect of transposable elements and to investigate the influence of this part of the genomes. Transposable elements (review in Wicker et al. 2007) can move into the host genomes and disturb its stability in response to several types of stress, including environmental changes.

So, insects and particularly Drosophilidae could be considered as a good, cheap and informative way of monitoring the “health state” of the urban environments. They also could be “sentinels” of the invasion by other alien species, like Drosophila malerkotliana (Martins 2001), Garcia et al. 2005), besides Zaprionus indianus and Drosophila suzukii, that endanger the richness of both the native fauna and the host plants, including those of economic value. Still, the Drosophilidae family can be used to prove the importance of conservation units, as proposed by Mata et al. (2010) and verified by Oliveira et al. (2016b). In the latest study, the authors analyzed three conservation units and surrounding areas of three Northeastern Brazilian states in the Caatinga biome.

The vast Amazonian region and its progressive urban occupation should be an adequate “testing area” for such studies, as have been shown by Dr. Marlúcia Martins and her group at Emilio Goeldi Museum (review in Santa-Brígida et al. 2017).

Finally, the maturity of the Brazilian and South American Drosophilidae researchers, including zoologists, ecologists, and geneticists, allows the creation of a robust collaboration network. These researchers are capable not only of identifying the status of conservation of our natural resources but also several biological sophisticated issues, besides promoting the qualification of skilled specialists for those purposes.

REFERENCES

• AMADOR RB, MARTINS MB and FURTADO IS. 2011. Is Zaprionus indianus invading a preserved Amazon forest? Dros Inf Serv 94: 73-73.
• BITNER-MATHÉ BC, VICTORINO JS and FARIA FS. 2014. Drosophila suzukii has been found in tropical Atlantic Rainforest in southeastern Brazil. Dros Inf Serv 97: 136-137.
• BIZZO L, GOTTSCHALK MS, DE TONI DC and HOFMANN PRP 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potential as bioindicator in open environments. Ihering Sér Zool 100: 185-191.
• BONORINO CBC, CALLEGARI-JACQUES SM and VALENTE VLS. 1993. Urbanization and chromosomal polymorphism of Drosophila nebulosa. Rev Bras Gen 16(1): 59-70.
• CASTRO FL and VALENTE VLS. 2001. Zaprionus indianus is invading Drosophila communities in the Southern Brazil city of Porto Alegre. Dros Inf Serv 84: 15-17.
• CAVASINI R, BUSCHINI MLT, MACHADO LPB and MATEUS RP. 2014. Comparison of Drosophilidae (Diptera) assemblages from two highland Araucaria Forest fragments, with and without environmental conservation policies. Braz J Biol 74: 761-768.
• DEPRÁ M, POPPE JL, DE TONI DC; SCHMITZ HJ and VALENTE VLS. 2014. The first records of the invasive pest Drosophila suzukii in the South American continent. J Pest Sci 87(3): 1-5.
• DÖGE JS, OLIVEIRA HV and TIDON R. 2015. Rapid response to abiotic and biotic factors controls population growth of two invasive drosophilids (Diptera) in the Brazilian Savanna. Biol Inv 8: 2461-2474.
• FERREIRA LB and TIDON R. 2005. Colonizing potential of Drosophilidae (Insecta, Diptera) in environments with different grades of urbanization. Biodiv Conserv 14: 1809-1821.
• FRAIMOUT AD et al. 2017. Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest. Mol Biol Evol 34: msx050-996.
• FURTADO, IS and MARTINS MB. 2009. First record of Zaprionus indianus (Diptera, Drosophilidae) in the URUCU oil field station (Coari, Amazona, Brazil). Dros Inf Serv 92: 34-34.
• GARCIA ACL, GOTTSCHALK MS, AUDINO GF, ROHDE C, VALIATI VH and VALENTE VLS. 2005. First evidence of Drosophila malerkotliana in the extreme South of Brazil (Porto Alegre, Rio Grande do Sul, Brazil). Dros Inf Serv 88: 1-2.
• GARCIA ACL, VALIATI VH, GOTTSCHALK MS, ROHDE C and VALENTE VLS. 2008. Two decades of colonization of the urban environment of Porto Alegre, southern Brazil, by Drosophila paulistorum. Ihering. Sér Zool 98: 329-338.
• GARCIA CF, HOCHMÜLLER CJ, VALENTE VLS and SCHMITZ HJ. 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop Ent 41: 32-41.
• GOÑI B; FRESIA P, CALVIÑO M, VALENTE VLS and SILVA LB. 2001. First record of Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) in southern localities of Uruguay, South America. Dros Inf Serv 84: 61-65.
• GOTTSCHALK MS, DE TONI DC, VALENTE VLS and HOFMANN PRP. 2007. Changes in Brazilian Drosophila (Diptera) assemblages across an urbanization gradient. Neotrop Ent 36: 848-862.
• GOTTSCHALK MS, HOFMANN PRP and VALENTE VLS. 2008. Diptera, Drosophilidae: historical occurrence in Brazil. Check List, J Species List Distrib 4: 485-518.
• LEÃO BFD and TIDON R. 2004. Newly invading species exploiting native host-plants: the case of Zaprionus indianus in the Brazilian Cerrado. Ann Soc Ent France 40(3/4): 285-290.
• LOH R and BITNER-MATHÉ BC. 2005. Variability of wing size and shape in three populations of a recent Brazilian invader, Zaprionus indianus (Diptera: Drosophilidae), from different habitats. Genet 125: 271-281.
• LORETO EL, DEPRÁ M; DIESEL JF; PANZERA Y and VALENTE-GAIESKY VLS. 2018. Drosophila relics hobo and hobo-MITES transposons as raw material for new regulatory networks. Genet Mol Biol 41(1, Suppl1): 47-57.
• LORETO ELS, ZAHA A, NICHOLS C, POLLOCK V and VALENTE VLS. 1998. Characterization of a hypermutable strain of Drosophila simulans. Cell Mol Life Sci 54: 1283-1290.
• LUCCHESE MEP, FLORES FEV and VALENTE VLS. 2003. Drosophila as bioindicator of air pollution: Preliminary evaluation of the wild species D. willistoni. Rev Bras Biocien 1: 19-28.
• MARTINS MB. 2001. Drosophilid fruit-fly guilds in forest fragments. In: Dierregaard Jr RO et al. (Eds), Lessons from Amazonia: the ecology and conservation of a fragmented forest. Yale Univ Press, N Haven: 175-186.
• MATA RA, MCGEOCH M and TIDON R. 2008. Drosophilid assemblages as a bioindicator system of human disturbance in the Brazilian Savanna. Biodiv Conserv 17: 2899-2916.
• MATA RA, MCGEOCH M and TIDON R. 2010. Drosophilids (Insecta, Diptera) as tools for Conservation Biology. Nat Conserv 8: 60-65.
• MATEUS RP, BUSCHINI MLT and SENE FM. 2006. The Drosophila community in xerophytic vegetations of the upper Parana-Paraguay river basin. Braz J Biol 66(2): 29-41.
• MATEUS RP, MACHADO LPB and SIMÃO-SILVA DP. 2018. Drosophila (Diptera: Drosophilidae) survey in an - island of xerophytic vegetation within the Atlantic Forest biome, with emphasis on the repleta species group. St Neotrop Fauna Environ 53: 1-10.
• MEDEIROS HF and KLACZKO LB. 2004. How many species of Drosophila (Diptera, Drosophilidae) remain to be described in the forests of São Paulo, Brazil? Species lists of three forest remnants. Biot Neotrop 4(1): 01-12.
• MENDES MF, VALER FB, ALEIXO JG, BLAUTH ML and GOTTSCHALK MS. 2017. Diversity of Drosophilidae (Insecta, Diptera) in the Restinga forest of southern Brazil. Rev Bras Ent 61: 248-256.
• OLIVEIRA GF, GARCIA ACL, MONTES MA, JUCA JCL, VALENTE VLS and ROHDE C. 2016b. Are conservation units in the Caatinga biome, Brazil, efficient in the protection of biodiversity? An analysis based on the drosophilid fauna. J Natur Conserv 34: 145-150.
• OLIVEIRA GF, ROHDE C, MONTES MA and VALENTE, VLS. 2016a. Contributions of Dryland Forest (Caatinga) to Species Composition, Richness and Diversity of Drosophilidae. Neotrop Ent 45: 537-547.
• PAULA MA, LOPES PHS and TIDON R. 2014. First record of Drosophila suzukii in the Brazilian Savanna. Dros Inf Serv 97: 113-115.
• POPPE JL, SCHMITZ HJ, GRIMALDI D and VALENTE VLS. 2014. High diversity of Drosophilidae (Insecta, Diptera) in the Pampas Biome of South America, with descriptions of new Rhinoleucophenga species. Zootaxa 3779: 215-245.
• POPPE JL, SCHMITZ, HJ and VALENTE VLS. 2015. The diversity of Drosophilidae in the South American Pampas: update of the species records in an environment historically neglected. Dros Inf Serv 98: 47-51.
• POPPE JL, SCHMITZ HJ and VALENTE VLS. 2016. Changes in the structure of Drosophilidae (Diptera) assemblages associated with contrasting environments in the Pampas Biome across temporal and spatial scales. Ann Ent Soc Am 109: 567-573.
• POPPE JL, VALENTE VLS, SCHMITZ HJ. 2012. Structure od Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luiz Gonzaga, RS). Pap Av Zool 52: 185-195.
• ROHDE C and VALENTE VLS. 1996. Ecological characteristics of urban populations of Drosophila polymorpha and Drosophila cardinoides (Diptera, Drosophilidae). Rev Bras Ent 40(1): 75-79.
• RUSZCZYK A. 1986.Distribution and abundance of butterflies in the urbanization zones of Porto Alegre, Brazil. J Res Lepidop 25(3):157-178.
• SAAVEDRA CCR, CALLEGARI-JACQUES SM, NAPP M, AND VALENTE VLS. 1995. A descriptive and analytical study of four Neotropical Drosophilid communities. J Zool System Evol Res 33: 62-74.
• SANTA-BRÍGIDA R, SCHMITZ, HJ and MARTINS, MB. 2017. Drosophilidae (Insecta, Diptera) in the state of Pará (Brazil). Biot Neotrop 17(1): e20160179.
• SANTOS LA, MENDES MF, KRUGER AP, BLAUTH ML, GOTTSCHALK MS and GARCIA FRM.2017. Global potential distribution of Drosophila suzukii (Diptera, Drosophilidae). Plos One 12(3): e0174318.
• SANTOS RA and VALENTE VLS. 1990. On the occurrence of Drosophila paulistorum Dobzhansky & Pavan (Diptera, Drosophilidae) in an urban environment: ecological and cytological observations. Evol Biol IV (4): 253-268.
• SCHMITZ HJ, VALENTE VLS and HOFMANN PRP. 2007. Taxonomic survey of Drosophilidae (Diptera) from mangrove forests of Santa Catarina island, Southern Brazil. Neotrop Ent 36: 53-64.
• SCHLESENER DCH, WOLLMANN J, NUNES AM, CORDEIRO J, GOTTSCHALK MS and GARCIA FRM. 2015. Drosophila suzukii : nova praga para a fruticultura brasileira. O Biológico 77: 45-51.
• SENE FM, PEREIRA MAQ, VAL FC and VILELA CR. 1980. Preliminary data on the geographical distribution of Drosophila species within morphoclimatic domains of Brazil. Pap Av Zool 33(22): 315-326.
• SILVA NM, FANTINEL CC, VALENTE VLS and VALIATI VH. 2005. Population dynamics of the invasive species Zaprionus indianus (Gupta) (Diptera, Drosophilidae) in communities of Drosophilids of Porto Alegre city, Southern Brazil. Neotrop Ent 34(3): 363-374.
• TIDON R, LEITE DF and LEÃO BFD. 2003. Impact of the colonization of Zaprionus (Diptera, Drosophilidae) in different ecosystems of the Neotropical Region: 2 years after the invasion. Biol Conserv 112(3): 299-305.
• TORRES FR and MADI-RAVAZZI L. 2006. Seasonal variation in natural populations of Drosophila spp.(Diptera) in two woodlands in the State of São Paulo, Brazil. Ihering Sér Zool 96: 437-444.
• VALENTE VLS. 1999. Há futuro nas cidades para animais silvestres? In: Sacchet AMOF (Ed), Genética, para que te quero? 1ª ed., Porto Alegre: Ed UFRGS, p. 41-46.
• VALENTE VLS, RUSZCZYK A and SANTOS RA. 1993. Chromosomal polymorphism in urban Drosophila willistoni. Rev Bras Gen 16(2): 307-319.
• VALENTE VLS, RUSCZYK A, SANTOS RA, BONORINO CBC, BRUM BEP, REGNER L and MORALES NB. 1989. Genetic and ecological studies on urban and marginal populations of Drosophila in the South of Brazil. Evol Biol III(3): 19-35.
• VALIATI VH and VALENTE VLS. 1996. Observations on ecological parameters of urban populations of Drosophila paulistorum Dobzhansky & Pavan (Diptera, Drosophilidae). Rev Bras Ent 40: 225-231.
• VILELA CR. 1999. Is Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) currently colonizing the Neotropical Region? Dros Inf Serv 82: 37-39.
• VILELA C and MORI L. 2014. The invasive spotted-wing Drosophila (Diptera, Drosophilidae) has been found in the city of São Paulo (Brazil). Rev Bras Ent 58: 371-375.
• WICKER T, SABOT F, HUA-VAN A, BENNETZEN JL, CAPY P, CHALBOUB B, FLAVEL A, LEROY P, MORGANTE M, PANAUD O, ET AL. 2007. A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973-982.

Publication Dates

• Publication in this collection
  29 July 2019
• Date of issue
  2019

History

• Received
  15 Apr 2019
• Accepted
  12 May 2019