Abstract
Understanding the interactions between protected areas and the surrounding landscape has become a central issue to conservation of biodiversity. The important role of protected areas in the preservation of biodiversity in tropical hotpots is widely recognized, but the role of the landscape surrounding those hotspots is poorly understood, particularly with regard to insects. In this study, we evaluated the species richness, composition, and beta diversity of Odonata assemblages inside and in the surroundings of a protected area in the Atlantic Forest hotspot. Sampling was carried out in the Private Reserve of Natural Heritage Veracel Station and its surroundings in the southern region of Bahia. Forty sites were sampled, 22 within the reserve and 18 in the surrounding areas. We found both a greater total species richness, and a greater richness with regard to the suborder Anisoptera in the surrounding areas. In addition, the species composition differed less between the sampling sites inside the protected area. Some of the species found inside the protected area did, however, make a greater contribution of the individual species to beta diversity (SCDB). Our study suggests that the surroundings of a protected area can contribute to the maintenance of regional diversity of dragonflies, but the protected areas play a vital role in supporting critically endangered species and populations of forest specialists, e.g., phytotelmatous species.
Implications for insect conservation
Our results show that the composition of the odonate species assemblages may provide a means to assess the importance of protected areas to Odonata communities. Our study also highlights the importance of PAs to the maintenance of the regional Odonata species pool, especially to forest specialist species and to threatened species.
Similar content being viewed by others
Data availability
The data and material are available.
Code availability
Not applicable.
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Astral Ecol 26:32–42
Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83:557–574
Altermatt F, Holyoak M (2012) Spatial clustering of habitat structure effects patterns of community composition and diversity. Ecol 93(5):1125–1133. https://doi.org/10.1890/11-1190.1
Azevedo-Santos VM, Fearnside PM, Oliveira CS, Padial AA, Pelicice FM, Lima-Junior DP, Vitule JRS (2017) Removing the abyss between conservation science and policy decision in Brazil. Biodivers Conserv 26:1745–1752. https://doi.org/10.1007/s10531-017-1316-x
Basset Y, Lamarre GPA (2019) Toward a world that values insects. Conserv 364:1230–1231. https://doi.org/10.1126/science.aaw7071
Bede LC, Machado ABM, Piper W, Souza MM (2015) Odonata of the Serra de São José - Brazil’s first Wildlife Reserve aimed at the conservation of dragonflies. Not Odonatologica 8(117–155):3
Blanco J, Bellón B, Fabricius C et al (2020) Interface processes between protected and unprotected areas: A global review and ways forward. Glob Change Biol 26:1138–1154. https://doi.org/10.1111/gcb.14865
Borges LR, Barbosa MS, Carneiro MAA, Vilela DS, Santos JC (2019) Dragonflies and damselflies (Insecta: Odonata) from a Cerrado area at Triângulo Mineiro. Biota Neotrop, Minas Gerais, Brazil. https://doi.org/10.1590/1676-0611-bn-2018-0609
Calvão LB, Juen L, Oliveira-Junior JMB, Batista JD, De Marco PJ (2018) Land use modifies Odonata diversity in streams of the Brazilian Cerrado. J Insect Conserv 22:675–685. https://doi.org/10.1007/s10841-018-0093-5
Cardoso P, Parton PS, Berkhofer K, Chichorro F, Deacon C, Fartmann T, Fukushina CS, Gaigher R, Habel JC, Hallmann CA, Hell MJ, Hachkerch A, Kwak ML, Mammola S, Noruga JA, Orjinger AB, Pedraza F, Pryke JS, Vorster C, Samways MJ (2020) Scientists’ Warning to humanity on insict extinctions. Biol Conserv. https://doi.org/10.1016/j.biocon.2020.108426
Carvalho FG, Roque FO, Barbosa L, Montag LFA, Juen L (2018) Oil palm plantation is not a suitable environment for most forest specialist species of Odonata in Amazonia. Anim Conserv 21:526–533. https://doi.org/10.1111/acv.12427
Cumming GS (2016) The relevance and resilience of protected areas in the Anthropocene. Anthropocene 13:46–56. https://doi.org/10.1016/j.ancene.2016.03.003
De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90(12):3566–3574. https://doi.org/10.1890/08-1823.1
De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119(10):1674–1684
De Marco PJ, Batista JD, Cabetle HSR (2015) Community assembly of adult odonates in tropical streams: an ecophysiological hypothesis. PlosOne 4:1–17. https://doi.org/10.1371/journal.pone.0123023
DeFries R, Karanth KK, Pareeth S (2010) Interactions between protected areas and their surroundings in human-dominated tropical landscapes. Biol Conserv 143(12):2870–2880. https://doi.org/10.1016/j.biocon.2010.02.010
Fagundes CK, Vogt RC, De Marco PJ (2016) Testing the efficiency of protected areas in the Amazon for conserving freshwater turtles. Diversity Distrib 22:123–135. https://doi.org/10.1111/ddi.12396
Fernández JD, Gómez JM (2012) Advantages and drawbacks of living in protected areas: The case of the threatened Erysimum popovii (Brassicaceae) in SE Iberian Peninsula. Biodivers Conserv 21(10):2539–2554. https://doi.org/10.1007/s10531-012-0316-0
Fernández-Juricic E, Vaca R, Schroeder N (2004) Spatial and temporal responses of forest birds to human approaches in a protected area and implications for two management strategies. Biol Conserv 117(4):407–416. https://doi.org/10.1016/j.biocon.2003.02.001
Ferreira J, Aragão LEOC, Barlow J, Barreto P, Berenguer E, Bustamante M, Gardner TA, Lees AC, Lima A, Louzada J, Pardine R, Parry L, Peris CA, Pompeu PS, Tabarelli M, Zuanon J (2014) Brazil’s environmental leadership at risk. Science 346:706–707. https://doi.org/10.1126/science.1260194
Ferreira-Peruquetti PS, Marco De, PJr, (2002) Efeito da alteração Ambiental sobre comunidades de Odonata em riachos de Mata Atlântica em Minas Gerais. Brasil Revta Bras Zoo 19(2):317–327
Fonseca CR, Venticinque EM (2018) Biodiversity conservation gaps in Brazil: A role for systematic conservation planning. Perspect Ecol Conserv 16:61–67. https://doi.org/10.1016/j.pecon.2018.03.001
Frederico RG, Zuanon J, De Marco PJ (2018) Amazon protected areas and its ability to protect stream-dwelling fish fauna. Biol Conserv 219:12–19. https://doi.org/10.1016/j.biocon.2017.12.032
Furieri KS, Fraga FB, Tribull C, Colombo WD (2020) Description of two females of Leptagrion Selys (Odonata: Coenagrionidae). Zootaxa 4821(2):343–352. https://doi.org/10.11646/zootaxa.4821.2.6
Garrison RW, Ellenrieder NV, Louton JA (2006) Dragonfly genera of the New World: An illustrated and annotated key to the Anisoptera. The Johns Hopkins University Press, Baltimore
Garrison RW, Von Ellenrieder N, Louton JA (2010) Damselfly Genera of the New World: an illustrated and annotated key to the Zygoptera. Baltimore: The John Hopkins University: 490
Gotelli NJ & Ellison AM Princípios de estatística em ecologia. Porto Alegre: Artmed, 2011.
Gray CL, Hill SLL, Newbold T, Hudson LN, Börger L, Contu S, Hoskins AJ, Ferrier S, Purvis A, Scharlemann JPW (2016) Local biodiversity is higher inside than outside terrestrial protected areas worldwide. Commun, Nat. https://doi.org/10.1038/ncomms12306
ICMBio/MMA (2018) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume VII Invertebrados, 1ed. Brasília
IUCN (2014) IUCN red list categories and criteria. Version 3.1, 2nd ed.; IUCN Species Survival Commission: Gland, Switzerland; Cambridge, MA, USA
Juen L, De Marco PJ (2012) Dragonfly endemism in the Brazilian Amazon: competing hypotheses for biogeographical patterns. Biodivers Conserv 21:3507–3521. https://doi.org/10.1007/s10531-012-0377-0
Landeiro VL, Franz B, Heino J, Siqueira T, Bini LM (2018) Species-poor and low-lying sites are more ecologically unique in a hyperdiverse Amazon region: Evidence from multiple taxonomic groups. Divers Distrib. https://doi.org/10.1111/ddi.12734
Leal CJ, Lennox GD, Ferraz SFB, Ferreira J, Gardner TA, Thomson JR, Berenguer E, Lees AC, Hughes RM, MacNally R, Aragão LEOC, Brito JG, Castello L, Garrett RD, Hamada N, Juen L, Leitão RP, Louzada J, Morello TF, Moura NG, Nessimian JL, Oliveira-Junior JMB, Oliveira VHF, Oliveira VC, Parry L, Pompeu OS, Solar RRC, Zuanon J, Barlow J (2020) Integrated terrestrial-freshwater planning doubles conservation of tropical aquatic species. Science 6512:117–121. https://doi.org/10.1126/science.aba7580
Legendre P, De Ca´ceres M, (2013) Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett 16:951–963. https://doi.org/10.1111/ele.12141
Legendre P, Legendre L (1998) Numerical Ecology, 2ed. Elsevier, Amsterdam, The Netherlands
Lencion, FAA (2006) Damselflies of Brazil: an illustrated identification guide. Vol. 2. All Print Editora– São Paulo, 146 pp.
Lencioni FAA (2005) Damselflies of Brazil: An Illustrated Identification Guide – 1 – Non Coenagrionidae Families. 1ª Edição, São Paulo, All Print Editora.
Lencioni FAA (2017) Damselflies of Brazil - an illustrated identification guide - Southeast region. Vol. 1. E-Book, Brasil, 412pp.
Maestre-Andrés S, Calvet-Mir L, Van Den Bergh JCJM (2016) Sociocultural valuation of ecosystem services to improve protected area management: A multi-method approach applied to Catalonia. Spain Reg Environ Change. 16(3):717–731. https://doi.org/10.1007/s10113-015-0784-3
Mammola S, Riccardi N, Prié V, Correia R, Cardoso P, Lopes-Lima M, Sousa R (2020) Towards a taxonomically unbiasedEuropean Union biodiversity strategy for 2030. R. Soc, Proc. https://doi.org/10.1098/rspb.2020.2166
MapBiomas (2021) Relatório Anual do Desmatamento no Brasil 2020-São Paulo, Brasil, 2021–93 pp. http://alerta.mapbiomas.org
S.O.S. Mata Atlântica. (2018). Relatório anual. São Paulo - SP. Available at: <https://www.sosma.org.br/wpcontent/uploads/2019/07/RA_SOSMA_2018_DIGITAL.pdf> (accessed 08 November 2019)
Mello K, Taniwaki RH, De Paula FR, Valente RA, Randhir TO, Macedo DR, Leal CG, Rodrigues HRM (2020) Multiscale land use impacts on water quality: assessment, planning, and future perspectives in Brazil. J Environ Manage. https://doi.org/10.1016/j.jenvman.2020.110879
Ministério de Meio Ambiente (2021) Cadastro Nacional de Unidade de Conservação. Available at: <https://antigo.mma.gov.br/areas-protegidas/cadastro-nacional-de-ucs.html>. (accessed 15 December 2021).
Mittermeier RA, Fonseca GAB, Rylands AB, Brandon K (2005) Uma breve história da conservação da biodiversidade no Brasil. Megadiversidade 1(1):14–21
Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C (2011) Global Biodiversity Conservation: The Critical Role of Hotspots. In: Zachos F., Habel J. (eds) Hotspots de biodiversidade. Springer, Berlim, Heidelberg Doi: https://doi.org/10.1007/978-3-642-20992-5_1
Monteiro-Júnior CS, Couceiro SRM, Hamada N, Juen L (2013) Effect of vegetation removal for road building on richness and composition of Odonata communities in Amazonia. Brazil. Int. J. Odonatol. 16:135–144. https://doi.org/10.1080/13887890.2013.764798
Oliveira U, Soares-Filho BS, Paglia AP, Brescovit AD, Carvalho CJB, Silva DP, Rezende DP, Leite FSF, Batista JAN, Barbosa JPPP, Stehmann JR, Ascher JS, Vasconcelos MF, De Marco P, Löwenberg-Neto P, Ferro VG, Santos AJ (2017) Biodiversity conservation gaps in the Brazilian protected areas. Sci Rep 7:9141. https://doi.org/10.1038/s41598-017-08707-2
Oliveira-Junior JMB, Juen L (2019) The Zygoptera/Anisoptera Ratio (Insecta: Odonata): a New Tool for Habitat Alterations Assessment in Amazonian Streams. Neotrop Entomol 48:1–9. https://doi.org/10.1007/s13744-019-00672-x
Oliveira-Junior JMB, Shimano Y, Gardner TA, Hughes RM, De Marco PJ, Juen L (2015) Neotropical dragonflies (Insecta: Odonata) as indicators of ecological condition of small in the Eastern Amazon. Austral Ecol 40:733–744. https://doi.org/10.1038/s41598-017-08707-2
Palomo I, Montes C, Martín-López B, González JA, García-Llorente M, Alcorlo P, Mora MRG (2014) Incorporating the social- ecological approach in protected areas in the Anthropocene. Bioscience 64(3):181–191. https://doi.org/10.1093/biosci/bit033
Peralta EM, Belen AE, Buenaventura GR, Cantre FGG, Espiritu KGR et al (2019) Stream benthic macroinvertebrate assemblages reveal the importance of a recently established freshwater protected area in a tropical watershed. Pac Sci 73(3):305–320. https://doi.org/10.2984/73.3.1
Quintana C, M Girardello, AS Barfod, H Balslev (2017) Diversity patterns, environmental drivers and changes in vegetation composition in dry inter-Andean valleys. J Plant Ecol 10(3):461–475. https://doi.org/10.1093/jpe/rtw036
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PTJ, Kidd KA, MacCormack TJ, Olden JD, Ormerod SJ, Smol JP, Taylor WW, Tockner K, Vermaire JC, Dudgeon D, Cooke SJ (2018) Emerging threats and persistent conservation challenges for freshwater biodiversity Biol. Rev 94:849–873. https://doi.org/10.1111/brv.12480
Ribeiro C, Juen L, Rodrigues ME (2021a) The Zygoptera/Anisoptera ratio as a tool to assess anthropogenic changes in Atlantic Forest streams. Biodivers Conserv. https://doi.org/10.1007/s10531-021-02143-5
Ribeiro C, Santos LR, Rodrigues ME (2021b) New records of the Critically Endangered Leptagrion acutum Santos, 1961 (Odonata, Coenagrionidae) from southern Bahia. Brazil. Check List. 17(1):59–62. https://doi.org/10.15560/17.1.59
Rodrigues ME, Roque FO, Quintero JMO, Pena JCC, Sousa DC, De Marco PJ (2016) Nonlinear responses in damselfly community along a gradient of habitat loss in a savanna landscape. Biol Conserv 194:113–120. https://doi.org/10.1016/j.biocon.2015.12.001
Rodrigues ME, Roque FO, Ferreira RGN, Saito VS, Samways MJ (2018) Egg-laying traits reflect shifts in dragonfly assemblages in response to different amount of tropical forest cover. Insect Conserv. Diver. 11:01–10. https://doi.org/10.1111/icad.12319
Rodrigues ME, Moura EB, Roque FO (2019) Dragonflies as indicators of the environmental conditions of veredas in a region of central-estern Brazil. Austral Ecol 23:969–978. https://doi.org/10.4257/oeco.2019.2304.20
RPPN Estação Veracel (2016) Plano de Manejo. Veracel Celulose, Gerência de Sustentabilidade e Conservação Internacional, Bahia, Brazil, Eunápolis
Ruhı´ AT, Datry & JL Sabo, (2017) Interpreting beta-diversity components over time to conserve metacommunities in highly dynamic ecosystems. Conserv Biol 31:1459–1468. https://doi.org/10.1111/cobi.12906
Samways MJ (2017) Reconciling ethical and scientific issues for insect conservation Foottit RG, Adler PH (Eds.), Insect Biodiversity: Science and Society (second ed), 1, Wiley-Blackwell, Oxford, UK, pp 747–766. https://doi.org/10.1002/9781118945568.ch23
Samways MJ, Barton PS, Birkhofer K, Chichorro F, Deacon C, Fartmann T, Fukushim CS, Gaigher R, Habel JC, Hallmann CA, Hill MJ, Hochkirch A, Kaila L, Kwak ML, Maes D, Mammola S, Noriega JA, Orfinger AB, Pedraza F, Pryke JS, Roque FO, Settele J, Simaika JP, Storka NE, Suhling F, Vorste C, Cardoso P (2020) Solutions for humanity on how to conserve insects. Biol Conserv. https://doi.org/10.1016/j.biocon.2020.108427
Sundar S, Heino J, Roque FO et al (2020) Conservation of freshwater macroinvertebrate biodiversity in tropical regions. Aquatic Conserv Mar Freshw Ecosyst 30:1238–1250. https://doi.org/10.1002/aqc.3326
Valente-Neto F, Roque FDO, Rodrigues ME, Juen L, Swan CM (2016) Toward a practical use of Neotropical odonates as bioindicators: testing congruence across taxonomic resolution and life stages. Ecol Ind 1:952–959. https://doi.org/10.1016/j.ecolind.2015.10.052
Valente-Neto F, da Silva FH, Covich AP, de Oliveira Roque F (2020) Streams dry and ecological uniqueness rise: environmental selection drives aquatic insect patterns in a stream network prone to intermittence. Hydrobiol 847:617–628
Vilela DS, Ferreira RG, Del-Claro K (2016) The Odonata community of a Brazilian Vereda: seasonal patterns, species diversity and rarity in a palm swamp environment. Biosci J 32:486–495
Vorster C, Samways MJ, Simaika JP, Kipping J, Clausnitzer V, Suhlingf F, Dijkstra KDB (2020) Development of a new continental-scale index for freshwater assessment based on dragonfly assemblages. Ecol Indic. https://doi.org/10.1016/j.ecolind.2019.105819
Watson JEM, Dudley N, Segan DB, Hockings M (2014) The performance and potential of protected areas. Nature 515(7525):67–73. https://doi.org/10.1038/nature13947
Acknowledgements
We thank to Coordination for the Improvement of Higher Education Personnel— CAPES for the Master’s scholarship to the student CRS (Process Number 8882.460645/2019-01), who allowed us to do this work. To the post-graduate program in Tropical Aquatic Systems—PPGSAT. The RPPN Estação Veracel for allowing research in the reserve and for support in feld activities and accommodation. We also thank the Laboratory of Aquatic Organisms—LOA for supporting our research. Our colleague Lais Rorigues for making our map and Anna Lejfelt-Sahlén kindly improved the authors' English. The Universidade Estadual de Santa Cruz—UESC and to National Council for Scientifc and Technological Development—CNPQ, for funding the research project (registered number UESC/PROPP 0220.1100.1693; registered number CNPQ 423737/2018-0). We are grateful to the CNPq, Brazil (National Council for Scientifc and Technological Development) for their research productivity grants awarded to FOR.
Funding
This research has financed from Universidade Estadual de Santa Cruz—UESC, project registered for Number 0220.1100.1693. And also, by National Council for Scientific and Technological Development—CNPQ, process Number 423737/2018–0.
Author information
Authors and Affiliations
Contributions
All the authors contributed to the development of this study. CRS and MER collected the data, identified the specimens and did the analysis. The first draft of the manuscript was written by CRS. And MER, GS and FOR assisted in the writing and discussion of all parts until the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Research involved in humans and/or animals
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ribeiro, C., Rodrigues, M.E., Sahlén, G. et al. Dragonflies within and outside a protected area: a comparison revealing the role of well-preserved atlantic forests in the preservation of critically endangered, phytotelmatous species. J Insect Conserv 26, 271–282 (2022). https://doi.org/10.1007/s10841-022-00385-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10841-022-00385-4